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Comprehensive Review on the Effect of Stem Cells in Cancer Progression

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Abstract

Purpose of Review

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Adult stem cells play a pivotal role in the regeneration and revival of tissues that have been affected by aging or injury. Emerging studies have provided strong evidence to support the idea that cells with properties resembling stem cells play a crucial role in the development and progression of various types of human cancers (Wang and Dick, Trends Cell Biol 15:494–501, 2005; Reya et al., Nature 414:105–11, 2001). This review will specifically focus on the interplay between cancer stem cells and various forms of cancer.

Recent Findings

The notion of cancer stem cells (CSCs) was initially explored in depth within the context of acute myelogenous leukemia (AML) and has since garnered significant interest in the field of cancer research (Nguyen et al., Nat Rev Cancer 12:133–43, 2012). Cancer stem cells share many similarities with stem cells in various aspects. CSCs are a subset of cells found within tumors that possess the ability to self-renew, differentiate, and induce tumor formation when introduced into an animal model. A specific group of cell surface markers, such as CD133, CD44, CD166, EpCAM, CD34, CD90, and CD24, are frequently employed in the identification and enrichment of CSCs (Zhou et al., Biochem Pharmacol 209:115441, 2023; Levin et al., Gastroenterology 139:2072–2082.e5, 2010; Shaikh et al., Cancer Biomarkers 16:301–7, 2016; Gao et al., Stem Cell Rev Rep 2023).

Summary

There is substantial evidence indicating that CSCs exhibit resistance to various standard treatments as well as playing an essential part in tumor recurrence along with the initiation of cancer metastasis. CSCs are also engaged in intercellular communication with various constituents within the tumor microenvironment (TME), thereby promoting the advancement of the tumor. The recent progress in the field of CSCs has generated hope regarding the potential for enhanced efficacy in future cancer treatments.

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References

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  1. Dewey MJ, Martin DW, Martin GR, Mintz B. Mosaic mice with teratocarcinoma-derived mutant cells deficient in hypoxanthine phosphoribosyltransferase. Proc Nat Acad Sci. 1977;74:5564–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981;292:154–6.

    Article  CAS  PubMed  Google Scholar 

  3. Martin GR. Teratocarcinomas as a model system for the study of embryogenesis and neoplasia. Cell. 1975;5:229–43.

    Article  CAS  PubMed  Google Scholar 

  4. Yu Z, Pestell TG, Lisanti MP, Pestell RG. Cancer stem cells. Int J Biochem Cell Biol. 2012;44:2144–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Yu Z, Pestell TG, Lisanti MP, Pestell RG. Cancer stem cells. Int J Biochem Cell Biol. 2012;44:2144–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Zhou H, Tan L, Liu B, Guan X-Y. Cancer stem cells: recent insights and therapies. Biochem Pharmacol. 2023;209:115441. Excellent review highlighting the role of CSCs and their potential for therapeutic applications.

    Article  CAS  PubMed  Google Scholar 

  7. Gao Q, Zhan Y, Sun L, Zhu W. Cancer stem cells and the tumor microenvironment in tumor drug resistance. Stem Cell Rev Rep. 2023;19:2141–54. https://doi.org/10.1007/s12015-023-10593-3. Excellent overview on the crosstalk between cancer stem cells and tumor microenvironment.

  8. Al-Hajj M, Clarke MF. Self-renewal and solid tumor stem cells. Oncogene. 2004;23:7274–82.

    Article  CAS  PubMed  Google Scholar 

  9. Yang L, Shi P, Zhao G, Xu J, Peng W, Zhang J, et al. Targeting cancer stem cell pathways for cancer therapy. Signal Transduct Target Ther. 2020;5:8. Excellent review provides a concise overview of the characterization and identification of cancer stem cells (CSCs).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Rosen JM, Jordan CT. The increasing complexity of the cancer stem cell paradigm. Science. 1979;2009(324):1670–3.

    Google Scholar 

  11. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105–11.

    Article  CAS  PubMed  Google Scholar 

  12. Al-Hajj M, Becker MW, Wicha M, Weissman I, Clarke MF. Therapeutic implications of cancer stem cells. Curr Opin Genet Dev. 2004;14:43–7.

    Article  CAS  PubMed  Google Scholar 

  13. Fialkow PJ, Gartler SM, Yoshida A. Clonal origin of chronic myelocytic leukemia in man. Proc Nat Acad Sci. 1967;58:1468–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Hamburger AW, Salmon SE. Primary bioassay of human tumor stem cells. Science. 1979;1977(197):461–3.

    Google Scholar 

  15. Jordan CT, Guzman ML, Noble M. Cancer stem cells. New Engl J Med. 2006;355:1253–61.

    Article  CAS  PubMed  Google Scholar 

  16. Li Y, Laterra J. Cancer stem cells: distinct entities or dynamically regulated phenotypes? Cancer Res. 2012;72:576–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Li Y, Li A, Glas M, Lal B, Ying M, Sang Y, et al. c-Met signaling induces a reprogramming network and supports the glioblastoma stem-like phenotype. Proc Nat Acad Sci. 2011;108:9951–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Jamieson CHM, Ailles LE, Dylla SJ, Muijtjens M, Jones C, Zehnder JL, et al. Granulocyte–macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. New Engl J Med. 2004;351:657–67.

    Article  CAS  PubMed  Google Scholar 

  19. Cozzio A, Passegué E, Ayton PM, Karsunky H, Cleary ML, Weissman IL. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev. 2003;17:3029–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Huntly BJP, Shigematsu H, Deguchi K, Lee BH, Mizuno S, Duclos N, et al. MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell. 2004;6:587–96.

    Article  CAS  PubMed  Google Scholar 

  21. Krivtsov AV, Twomey D, Feng Z, Stubbs MC, Wang Y, Faber J, et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL–AF9. Nature. 2006;442:818–22.

    Article  CAS  PubMed  Google Scholar 

  22. Yin W, Wang J, Jiang L, James KY. Cancer and stem cells. Exp Biol Med. 2021;246:1791–801.

    Article  CAS  Google Scholar 

  23. Li Y, Welm B, Podsypanina K, Huang S, Chamorro M, Zhang X, et al. Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammary cancers from progenitor cells. Proc Nat Acad Sci. 2003;100:15853–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Riggi N, Cironi L, Provero P, Suvà M-L, Kaloulis K, Garcia-Echeverria C, et al. Development of Ewing’s sarcoma from primary bone marrow–derived mesenchymal progenitor cells. Cancer Res. 2005;65:11459–68.

    Article  CAS  PubMed  Google Scholar 

  25. Guo W, Lasky JL, Wu H. Cancer stem cells. Pediatr Res. 2006;59:59R–64R.

    Article  PubMed  Google Scholar 

  26. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367:645–8.

    Article  CAS  PubMed  Google Scholar 

  27. Identification of a cancer stem cell in human brain tumors [Internet]. Cancer Res. 2003. http://aacrjournals.org/cancerres/article-pdf/63/18/5821/2506915/ch1803005821.pdf?casa_token=5Kp5K84136kAAAAA:rZMVNfj6AsKBQ6PC7b87lgZljCxeS4swKtDc1FwHfvDe5CeHZghAIPDTdxvv748Mw_EwxuxX3g

  28. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Nat Acad Sci. 2003;100:3983–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Kelly PN, Dakic A, Adams JM, Nutt SL, Strasser A. Tumor growth need not be driven by rare cancer stem cells. Science. 1979;2007(317):337–7.

    Google Scholar 

  30. Borovski T, De Sousa E, Melo F, Vermeulen L, Medema JP. Cancer stem cell niche: the place to be. Cancer Res. 2011;71:634–9.

    Article  CAS  PubMed  Google Scholar 

  31. Medema JP, Vermeulen L. Microenvironmental regulation of stem cells in intestinal homeostasis and cancer. Nature. 2011;474:318–26.

    Article  CAS  PubMed  Google Scholar 

  32. Ricci-Vitiani L, Pallini R, Biffoni M, Todaro M, Invernici G, Cenci T, et al. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature. 2010;468:824–8.

    Article  CAS  PubMed  Google Scholar 

  33. Wang R, Chadalavada K, Wilshire J, Kowalik U, Hovinga KE, Geber A, et al. Glioblastoma stem-like cells give rise to tumour endothelium. Nature. 2010;468:829–33.

    Article  CAS  PubMed  Google Scholar 

  34. Liu S, Ginestier C, Ou SJ, Clouthier SG, Patel SH, Monville F, et al. Breast cancer stem cells are regulated by mesenchymal stem cells through cytokine networks. Cancer Res. 2011;71:614–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Vermeulen L, De Sousa E, Melo F, van der Heijden M, Cameron K, de Jong JH, Borovski T, et al. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol. 2010;12:468–76.

    Article  CAS  PubMed  Google Scholar 

  36. Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, et al. A perivascular niche for brain tumor stem cells. Cancer Cell. 2007;11:69–82.

    Article  CAS  PubMed  Google Scholar 

  37. Spradling A, Drummond-Barbosa D, Kai T. Stem cells find their niche. Nature. 2001;414:98–104.

    Article  CAS  PubMed  Google Scholar 

  38. Le NH, Franken P, Fodde R. Tumour–stroma interactions in colorectal cancer: converging on β-catenin activation and cancer stemness. Br J Cancer. 2008;98:1886–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Mani SA, Guo W, Liao M-J, Eaton ENG, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133:704–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Ansieau S, Bastid J, Doreau A, Morel A-P, Bouchet BP, Thomas C, et al. Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell. 2008;14:79–89.

    Article  CAS  PubMed  Google Scholar 

  41. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004;117:927–39.

    Article  CAS  PubMed  Google Scholar 

  42. Morel A-P, Lièvre M, Thomas C, Hinkal G, Ansieau S, Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One. 2008;3:e2888.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Scheel C, Eaton EN, Li SH-J, Chaffer CL, Reinhardt F, Kah K-J, et al. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell. 2011;145:926–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Migrating cancer stem cells — an integrated concept of malignant tumour progression. Nat Rev Cancer. 2005;5:744–9.

    Article  CAS  PubMed  Google Scholar 

  45. Medema JP. Cancer stem cells: the challenges ahead. Nat Cell Biol. 2013;15:338–44.

    Article  CAS  PubMed  Google Scholar 

  46. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell. 2008;14:818–29.

    Article  CAS  PubMed  Google Scholar 

  47. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell. 2007;1:555–67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Yu Z, Pestell RG. MicroRNAs and cancer stem cells. In: MicroRNAs in cancer translational research. Dordrecht: Springer Netherlands; 2011. p. 373–88.

    Chapter  Google Scholar 

  49. Döhner H, Weisdorf DJ, Bloomfield CD. Acute myeloid leukemia. New Engl J Med. 2015;373:1136–52.

    Article  PubMed  Google Scholar 

  50. Döhner H, Estey EH, Amadori S, Appelbaum FR, Büchner T, Burnett AK, et al. Diagnosis and management of acute myeloid leukemia in adults: recommendations from an international expert panel, on behalf of the European LeukemiaNet. Blood. 2010;115:453–74.

    Article  PubMed  Google Scholar 

  51. Ries LAG, Harkins D, Krapcho M, Mariotto A, Miller BA, Feuer EJ, et al. SEER cancer statistics review, 1975-2003. 2006;

    Google Scholar 

  52. Tan BT, Park CY, Ailles LE, Weissman IL. The cancer stem cell hypothesis: a work in progress. Lab Investig. 2006;86:1203–7.

    Article  CAS  PubMed  Google Scholar 

  53. Spangrude GJ, Heimfeld S, Weissman IL. Purification and characterization of mouse hematopoietic stem cells. Science. 1979;1988(241):58–62.

    Google Scholar 

  54. Dick JE. Acute myeloid leukemia stem cells. Ann N Y Acad Sci. 2005;1044:1–5.

    Article  PubMed  Google Scholar 

  55. Jordan C. Unique molecular and cellular features of acute myelogenous leukemia stem cells. Leukemia. 2002;16:559–62.

    Article  CAS  PubMed  Google Scholar 

  56. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997;3:730–7.

    Article  CAS  PubMed  Google Scholar 

  57. Blair A, Hogge DE, Ailles LE, Lansdorp PM, Sutherland HJ. Lack of expression of Thy-1 (CD90) on acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo. Blood. 1997;89:3104–12.

    Article  CAS  PubMed  Google Scholar 

  58. Blair A, Sutherland HJ. Primitive acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo lack surface expression of c-kit (CD117). Exp Hematol. 2000;28:660–71.

    Article  CAS  PubMed  Google Scholar 

  59. Wang JCY, Dick JE. Cancer stem cells: lessons from leukemia. Trends Cell Biol. 2005;15:494–501.

    Article  CAS  PubMed  Google Scholar 

  60. Miyamoto T, Weissman IL, Akashi K. AML1/ETO-expressing nonleukemic stem cells in acute myelogenous leukemia with 8;21 chromosomal translocation. Proc Nat Acad Sci. 2000;97:7521–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Jemal A, Thun MJ, Ries LAG, Howe HL, Weir HK, Center MM, et al. Annual report to the nation on the status of cancer, 1975–2005, featuring trends in lung cancer, tobacco use, and tobacco control. JNCI: J Nat Cancer Instit. 2008;100:1672–94.

    Article  Google Scholar 

  62. Dubey S, Powell CA. Update in lung cancer 2008. Am J Respir Crit Care Med. 2009;179:860–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Eramo A, Haas TL, De Maria R. Lung cancer stem cells: tools and targets to fight lung cancer. Oncogene. 2010;29:4625–35.

    Article  CAS  PubMed  Google Scholar 

  64. Collins LG, Haines C, Perkel R, Enck RE. Lung cancer: diagnosis and management. Am Fam Physician. 2007;75:56–63.

    PubMed  Google Scholar 

  65. Zheng Y, Wang L, Yin L, Yao Z, Tong R, Xue J, et al. Lung cancer stem cell markers as therapeutic targets: an update on signaling pathways and therapies. Front Oncol. 2022;12:873994. https://doi.org/10.3389/fonc.2022.873994. Review highlighting a comprehensive and current analysis of lung cancer stem cell markers.

  66. Adini A, Adini I, Ghosh K, Benny O, Pravda E, Hu R, et al. The stem cell marker prominin-1/CD133 interacts with vascular endothelial growth factor and potentiates its action. Angiogenesis. 2013;16:405–16.

    Article  CAS  PubMed  Google Scholar 

  67. Aghajani M, Mansoori B, Mohammadi A, Asadzadeh Z, Baradaran B. New emerging roles of CD133 in cancer stem cell: signaling pathway and miRNA regulation. J Cell Physiol. 2019;234:21642–61. This study investigates the novel and emerging roles of CD133 in cancer stem cells.

    Article  CAS  PubMed  Google Scholar 

  68. Jang J-W, Song Y, Kim S-H, Kim J, Seo HR. Potential mechanisms of CD133 in cancer stem cells. Life Sci. 2017;184:25–9.

    Article  CAS  PubMed  Google Scholar 

  69. Kumari R, Chouhan S, Singh S, Chhipa RR, Ajay AK, Bhat MK. Constitutively activated ERK sensitizes cancer cells to doxorubicin: involvement of p53-EGFR-ERK pathway. J Biosci. 2017;42:31–41.

    Article  CAS  PubMed  Google Scholar 

  70. Prabavathy D, Swarnalatha Y, Ramadoss N. Lung cancer stem cells—origin, characteristics and therapy. Stem Cell Investig. 2018;5:6–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Reynolds SD, Malkinson AM. Clara cell: progenitor for the bronchiolar epithelium. Int J Biochem Cell Biol. 2010;42:1–4.

    Article  CAS  PubMed  Google Scholar 

  72. Griffiths MJ, Bonnet D, Janes SM. Stem cells of the alveolar epithelium. The Lancet. 2005;366:249–60.

    Article  Google Scholar 

  73. Jackson S-R, Lee J, Reddy R, Williams GN, Kikuchi A, Freiberg Y, et al. Partial pneumonectomy of telomerase null mice carrying shortened telomeres initiates cell growth arrest resulting in a limited compensatory growth response. Am J Physiol Lung Cellul Mole Physiol. 2011;300:L898–909.

    Article  CAS  Google Scholar 

  74. Kim CF. Paving the road for lung stem cell biology: bronchioalveolar stem cells and other putative distal lung stem cells. Am J Physiol Lung Cellul Mole Physiol. 2007;293:L1092–8.

    Article  CAS  Google Scholar 

  75. Berns A. Stem cells for lung cancer? Cell. 2005;121:811–3.

    Article  CAS  PubMed  Google Scholar 

  76. Kratz JR, Yagui-Beltrán A, Jablons DM. Cancer stem cells in lung tumorigenesis. Ann Thorac Surg. 2010;89:S2090–5.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Rawlins EL, Okubo T, Xue Y, Brass DM, Auten RL, Hasegawa H, et al. The role of Scgb1a1+ Clara cells in the long-term maintenance and repair of lung airway, but not alveolar, epithelium. Cell Stem Cell. 2009;4:525–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Kim CFB, Jackson EL, Woolfenden AE, Lawrence S, Babar I, Vogel S, et al. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell. 2005;121:823–35.

    Article  CAS  PubMed  Google Scholar 

  79. Peacock CD, Watkins DN. Cancer stem cells and the ontogeny of lung cancer. J Clin Oncol. 2008;26:2883–9.

    Article  CAS  PubMed  Google Scholar 

  80. Sutherland KD, Berns A. Cell of origin of lung cancer. Mol Oncol. 2010;4:397–403.

    Article  PubMed  PubMed Central  Google Scholar 

  81. Das B, Tsuchida R, Malkin D, Koren G, Baruchel S, Yeger H. Hypoxia enhances tumor stemness by increasing the invasive and tumorigenic side population fraction. Stem Cells. 2008;26:1818–30.

    Article  PubMed  Google Scholar 

  82. Salcido CD, Larochelle A, Taylor BJ, Dunbar CE, Varticovski L. Molecular characterisation of side population cells with cancer stem cell-like characteristics in small-cell lung cancer. Br J Cancer. 2010;102:1636–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Shi Y, Fu X, Hua Y, Han Y, Lu Y, Wang J. The side population in human lung cancer cell line NCI-H460 is enriched in stem-like cancer cells. PLoS One. 2012;7:e33358.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Lundin A, Driscoll B. Lung cancer stem cells: progress and prospects. Cancer Lett. 2013;338:89–93.

    Article  CAS  PubMed  Google Scholar 

  85. Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, Gobel U, et al. A distinct “side population” of cells with high drug efflux capacity in human tumor cells. Proc Nat Acad Sci. 2004;101:14228–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Sullivan JP, Minna JD, Shay JW. Evidence for self-renewing lung cancer stem cells and their implications in tumor initiation, progression, and targeted therapy. Cancer Metastasis Rev. 2010;29:61–72.

    Article  PubMed  PubMed Central  Google Scholar 

  87. Dong J, Kislinger T, Jurisica I, Wigle DA. Lung cancer: developmental networks gone awry? Cancer Biol Ther. 2009;8:312–8.

    Article  CAS  PubMed  Google Scholar 

  88. Gomperts B, Spira A, Massion P, Walser T, Wistuba I, Minna J, et al. Evolving concepts in lung carcinogenesis. Semin Respir Crit Care Med. 2011;32:032–43.

    Article  Google Scholar 

  89. Alison MR, Le Brenne AC, Islam S. Stem cells and lung cancer: future therapeutic targets? Expert Opin Biol Ther. 2009;9:1127–41.

    Article  CAS  PubMed  Google Scholar 

  90. Chen Y-C, Hsu H-S, Chen Y-W, Tsai T-H, How C-K, Wang C-Y, et al. Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells. PLoS One. 2008;3:e2637.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Adcock IM, Caramori G, Barnes PJ. Chronic obstructive pulmonary disease and lung cancer: new molecular insights. Respiration. 2011;81:265–84.

    Article  CAS  PubMed  Google Scholar 

  92. Chiou S-H, Wang M-L, Chou Y-T, Chen C-J, Hong C-F, Hsieh W-J, et al. Coexpression of Oct4 and Nanog enhances malignancy in lung adenocarcinoma by inducing cancer stem cell–like properties and epithelial–mesenchymal transdifferentiation. Cancer Res. 2010;70:10433–44.

    Article  CAS  PubMed  Google Scholar 

  93. Yan X, Luo H, Zhou X, Zhu B, Wang Y, Bian X. Identification of CD90 as a marker for lung cancer stem cells in A549 and H446 cell lines. Oncol Rep. 2013;30:2733–40.

    Article  CAS  PubMed  Google Scholar 

  94. Sauzay C, Voutetakis K, Chatziioannou A, Chevet E, Avril T. CD90/Thy-1, a cancer-associated cell surface signaling molecule. Front Cell. Dev Biol. 2019:7:66. https://doi.org/10.3389/fcell.2019.00066.

  95. Jiang F, Qiu Q, Khanna A, Todd NW, Deepak J, Xing L, et al. Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Res. 2009;7:330–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Sholl LM, Long KB, Hornick JL. Sox2 expression in pulmonary non-small cell and neuroendocrine carcinomas. Appl Immunohistochem Mole Morphol. 2010;18:55–61.

    Article  CAS  Google Scholar 

  97. Leung EL-H, Fiscus RR, Tung JW, Tin VP-C, Cheng LC, Sihoe AD-L, et al. Non-small cell lung cancer cells expressing CD44 are enriched for stem cell-like properties. PLoS One. 2010;5:e14062.

    Article  PubMed  PubMed Central  Google Scholar 

  98. Li F, Zeng H, Ying K. The combination of stem cell markers CD133 and ABCG2 predicts relapse in stage I non-small cell lung carcinomas. Med Oncol. 2011;28:1458–62.

    Article  CAS  PubMed  Google Scholar 

  99. Ghoncheh M, Mohammadian M, Mohammadian-Hafshejani A, Salehiniya H. The incidence and mortality of colorectal cancer and its relationship with the human development index in Asia. Ann Glob Health. 2017;82:726.

    Article  Google Scholar 

  100. Haggar F, Boushey R. Colorectal cancer epidemiology: incidence, mortality, survival, and risk factors. Clin Colon Rectal Surg. 2009;22:191–7.

    Article  PubMed  PubMed Central  Google Scholar 

  101. Fleming M, Ravula S, Tatishchev SF, Wang HL. Colorectal carcinoma: pathologic aspects. J Gastrointest Oncol. 2012;3:153–73.

    PubMed  PubMed Central  Google Scholar 

  102. Neo JH, Ager EI, Angus PW, Zhu J, Herath CB, Christophi C. Changes in the renin angiotensin system during the development of colorectal cancer liver metastases. BMC Cancer. 2010;10:134.

    Article  PubMed  PubMed Central  Google Scholar 

  103. Lampropoulos P, Zizi-Sermpetzoglou A, Rizos S, Kostakis A, Nikiteas N, Papavassiliou AG. TGF-beta signalling in colon carcinogenesis. Cancer Lett. 2012;314:1–7.

    Article  CAS  PubMed  Google Scholar 

  104. Markowitz SD, Bertagnolli MM. Molecular basis of colorectal cancer. New Engl J Med. 2009;361:2449–60.

    Article  CAS  PubMed  Google Scholar 

  105. Vries RGJ, Huch M, Clevers H. Stem cells and cancer of the stomach and intestine. Mol Oncol. 2010;4:373–84.

    Article  PubMed  PubMed Central  Google Scholar 

  106. Vaiopoulos AG, Kostakis ID, Koutsilieris M, Papavassiliou AG. Concise review: colorectal cancer stem cells. Stem Cells. 2012;30(3):363–71. https://doi.org/10.1002/stem.1031.

    Article  CAS  PubMed  Google Scholar 

  107. Ricci-Vitiani L, Fabrizi E, Palio E, De Maria R. Colon cancer stem cells. J Mol Med. 2009;87:1097–104.

    Article  PubMed  Google Scholar 

  108. Das PK, Islam F, Lam AK. The roles of cancer stem cells and therapy resistance in colorectal carcinoma. Cells. 2020;9:1392. Excellent review exploring the roles of cancer stem cells in colorectal cancers.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Singh S, Mayengbam SS, Chouhan S, Deshmukh B, Ramteke P, Athavale D, et al. Role of TNFα and leptin signaling in colon cancer incidence and tumor growth under obese phenotype. Biochimica et Biophysica Acta (BBA) – Mole Basis Dis. 2020;1866:165660.

    Article  CAS  Google Scholar 

  110. Wang EL, Qian ZR, Nakasono M, Tanahashi T, Yoshimoto K, Bando Y, et al. High expression of Toll-like receptor 4/myeloid differentiation factor 88 signals correlates with poor prognosis in colorectal cancer. Br J Cancer. 2010;102:908–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Singh S, Chouhan S, Mohammad N, Bhat MK. Resistin causes G1 arrest in colon cancer cells through upregulation of <scp>SOCS</scp> 3. FEBS Lett. 2017;591:1371–82.

    Article  CAS  PubMed  Google Scholar 

  112. Zhou Y, Xia L, Wang H, Oyang L, Su M, Liu Q, et al. Cancer stem cells in progression of colorectal cancer. Oncotarget. 2018;9:33403–15.

    Article  PubMed  Google Scholar 

  113. Basu S, Haase G, Ben-Ze’ev A. Wnt signaling in cancer stem cells and colon cancer metastasis. F1000Res. 2016;5:699.

    Article  Google Scholar 

  114. Cleophas M, Joosten L, Stamp L, Dalbeth N, Woodward O, Merriman T. ABCG2 polymorphisms in gout: insights into disease susceptibility and treatment approaches. Pharmgenomics Pers Med. 2017;10:129–42.

    CAS  PubMed  PubMed Central  Google Scholar 

  115. Gao W, Chen L, Ma Z, Du Z, Zhao Z, Hu Z, et al. Isolation and phenotypic characterization of colorectal cancer stem cells with organ-specific metastatic potential. Gastroenterology. 2013;145:636–646.e5.

    Article  CAS  PubMed  Google Scholar 

  116. Dalerba P, Dylla SJ, Park I-K, Liu R, Wang X, Cho RW, et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Nat Acad Sci. 2007;104:10158–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Wang JY, Chang CC, Chiang CC, Chen WM, Hung SC. Silibinin suppresses the maintenance of colorectal cancer stem-like cells by inhibiting PP2A/AKT/mTOR pathways. J Cell Biochem. 2012;113(5):1733–43. https://doi.org/10.1002/jcb.24043.

    Article  CAS  PubMed  Google Scholar 

  118. López-Arribillaga E, Rodilla V, Pellegrinet L, Guiu J, Iglesias M, Roman AC, et al. Bmi1 regulates murine intestinal stem cell proliferation and self-renewal downstream of Notch. Development. 2015;142:41–50.

    Article  PubMed  Google Scholar 

  119. Zhang F, Sun H, Zhang S, Yang X, Zhang G, Su T. Overexpression of PER3 inhibits self-renewal capability and chemoresistance of colorectal cancer stem-like cells via inhibition of Notch and β-catenin signaling. Oncol Res Feat Preclin Clin Cancer Therap. 2017;25:709–19.

    Google Scholar 

  120. Rodda DJ, Chew J-L, Lim L-H, Loh Y-H, Wang B, Ng H-H, et al. Transcriptional regulation of Nanog by OCT4 and SOX2. J Biol Chem. 2005;280:24731–7.

    Article  CAS  PubMed  Google Scholar 

  121. Wang J, Zhang B, Wu H, Cai J, Sui X, Wang Y, et al. CD51 correlates with the TGF-beta pathway and is a functional marker for colorectal cancer stem cells. Oncogene. 2017;36:1351–63.

    Article  PubMed  Google Scholar 

  122. Weichert W, Denkert C, Burkhardt M, Gansukh T, Bellach J, Altevogt P, et al. Cytoplasmic CD24 expression in colorectal cancer independently correlates with shortened patient survival. Clin Cancer Res. 2005;11:6574–81.

    Article  CAS  PubMed  Google Scholar 

  123. Pang R, Law WL, Chu ACY, Poon JT, Lam CSC, Chow AKM, et al. A subpopulation of CD26+ cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell. 2010;6:603–15.

    Article  CAS  PubMed  Google Scholar 

  124. Fujimoto K, Beauchamp RD, Whitehead RH. Identification and isolation of candidate human colonic clonogenic cells based on cell surface integrin expression. Gastroenterology. 2002;123:1941–8.

    Article  CAS  PubMed  Google Scholar 

  125. Munro MJ, Wickremesekera SK, Peng L, Tan ST, Itinteang T. Cancer stem cells in colorectal cancer: a review. J Clin Pathol. 2018;71:110–6.

    Article  CAS  PubMed  Google Scholar 

  126. Wang X, Xia B, Liang Y, Peng L, Wang Z, Zhuo J, et al. Membranous ABCG2 expression in colorectal cancer independently correlates with shortened patient survival. Cancer Biomarkers. 2013;13:81–8.

    Article  CAS  PubMed  Google Scholar 

  127. Hadjimichael C. Common stemness regulators of embryonic and cancer stem cells. World J Stem Cells. 2015;7:1150.

    Article  PubMed  PubMed Central  Google Scholar 

  128. Beumer J, Clevers H. Regulation and plasticity of intestinal stem cells during homeostasis and regeneration. Development. 2016;143:3639–49.

    Article  CAS  PubMed  Google Scholar 

  129. He S, Zhou H, Zhu X, Hu S, Fei M, Wan D, et al. Expression of Lgr5, a marker of intestinal stem cells, in colorectal cancer and its clinicopathological significance. Biomed Pharmacother. 2014;68:507–13.

    Article  CAS  PubMed  Google Scholar 

  130. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 2007;449:1003–7.

    Article  CAS  PubMed  Google Scholar 

  131. Schepers AG, Snippert HJ, Stange DE, van den Born M, van Es JH, van de Wetering M, et al. Lineage tracing reveals Lgr5 + stem cell activity in mouse intestinal adenomas. Science. 1979;2012(337):730–5.

    Google Scholar 

  132. Shimokawa M, Ohta Y, Nishikori S, Matano M, Takano A, Fujii M, et al. Visualization and targeting of LGR5+ human colon cancer stem cells. Nature. 2017;545:187–92.

    Article  CAS  PubMed  Google Scholar 

  133. Merlos-Suárez A, Barriga FM, Jung P, Iglesias M, Céspedes MV, Rossell D, et al. The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell. 2011;8:511–24.

    Article  PubMed  Google Scholar 

  134. Deng S, Yang X, Lassus H, Liang S, Kaur S, Ye Q, et al. Distinct expression levels and patterns of stem cell marker, aldehyde dehydrogenase isoform 1 (ALDH1), in human epithelial cancers. PLoS One. 2010;5:e10277.

    Article  PubMed  PubMed Central  Google Scholar 

  135. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, Appelman H, et al. Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res. 2009;69:3382–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Trzpis M, McLaughlin PMJ, de Leij LMFH, Harmsen MC. Epithelial cell adhesion molecule. Am J Pathol. 2007;171:386–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Maetzel D, Denzel S, Mack B, Canis M, Went P, Benk M, et al. Nuclear signalling by tumour-associated antigen EpCAM. Nat Cell Biol. 2009;11:162–71.

    Article  CAS  PubMed  Google Scholar 

  138. Mani SKK, Zhang H, Diab A, Pascuzzi PE, Lefrançois L, Fares N, et al. EpCAM-regulated intramembrane proteolysis induces a cancer stem cell-like gene signature in hepatitis B virus-infected hepatocytes. J Hepatol. 2016;65:888–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Katoh M, Katoh M. WNT signaling pathway and stem cell signaling network. Clin Cancer Res. 2007;13:4042–5.

    Article  CAS  PubMed  Google Scholar 

  140. Lamb R, Bonuccelli G, Ozsvári B, Peiris-Pagès M, Fiorillo M, Smith DL, et al. Mitochondrial mass, a new metabolic biomarker for stem-like cancer cells: Understanding WNT/FGF-driven anabolic signaling. Oncotarget. 2015;6:30453–71.

    Article  PubMed  PubMed Central  Google Scholar 

  141. Katoh M, Nakagama H. FGF receptors: cancer biology and therapeutics. Med Res Rev. 2014;34:280–300.

    Article  CAS  PubMed  Google Scholar 

  142. Spring FA, Dalchau R, Daniels GL, Mallinson G, Judson PA, Parsons SF, et al. The Ina and Inb blood group antigens are located on a glycoprotein of 80,000 MW (the CDw44 glycoprotein) whose expression is influenced by the In(Lu) gene. Immunology. 1988;64:37–43.

    CAS  PubMed  PubMed Central  Google Scholar 

  143. Lee SY, Kim KA, Kim CH, Kim YJ, Lee J-H, Kim HR. CD44-shRNA recombinant adenovirus inhibits cell proliferation, invasion, and migration, and promotes apoptosis in HCT116 colon cancer cells. Int J Oncol. 2017;50:329–36.

    Article  CAS  PubMed  Google Scholar 

  144. Li Y, Xiao B, Tu S, Wang Y, Zhang X. Cultivation and identification of colon cancer stem cell-derived spheres from the Colo205 cell line. Brazil J Med Biol Res. 2012;45:197–204.

    Article  CAS  Google Scholar 

  145. Kazama S, Kishikawa J, Kiyomatsu T, Kawai K, Nozawa H, Ishihara S, et al. Expression of the stem cell marker CD133 is related to tumor development in colorectal carcinogenesis. Asian J Surg. 2018;41:274–8.

    Article  PubMed  Google Scholar 

  146. Li Z. CD133: a stem cell biomarker and beyond. Exp Hematol Oncol. 2013;2:17.

    Article  PubMed  PubMed Central  Google Scholar 

  147. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, et al. Identification and expansion of human colon-cancer-initiating cells. Nature. 2007;445:111–5.

    Article  CAS  PubMed  Google Scholar 

  148. Todaro M, Alea MP, Di Stefano AB, Cammareri P, Vermeulen L, Iovino F, et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell. 2007;1:389–402.

    Article  CAS  PubMed  Google Scholar 

  149. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science. 1979;2007(318):1917–20.

    Google Scholar 

  150. Hao L, Zhao Y, Wang Z, Yin H, Zhang X, He T, et al. Expression and clinical significance of SALL4 and β-catenin in colorectal cancer. J Mol Histol. 2016;47:117–28.

    Article  CAS  PubMed  Google Scholar 

  151. Amini S, Fathi F, Mobalegi J, Sofimajidpour H, Ghadimi T. The expressions of stem cell markers: Oct4, Nanog, Sox2, nucleostemin, Bmi, Zfx, Tcl1, Tbx3, Dppa4, and Esrrb in bladder, colon, and prostate cancer, and certain cancer cell lines. Anat Cell Biol. 2014;47:1.

    Article  PubMed  PubMed Central  Google Scholar 

  152. Shi G, Jin Y. Role of Oct4 in maintaining and regaining stem cell pluripotency. Stem Cell Res Ther. 2010;1:39.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Pan G, Thomson JA. Nanog and transcriptional networks in embryonic stem cell pluripotency. Cell Res. 2007;17:42–9.

    Article  CAS  PubMed  Google Scholar 

  154. Dai X, Ge J, Wang X, Qian X, Zhang C, Li X. OCT4 regulates epithelial-mesenchymal transition and its knockdown inhibits colorectal cancer cell migration and invasion. Oncol Rep. 2013;29:155–60.

    Article  CAS  PubMed  Google Scholar 

  155. Zhang S. Sox2, a key factor in the regulation of pluripotency and neural differentiation. World J Stem Cells. 2014;6:305.

    Article  PubMed  PubMed Central  Google Scholar 

  156. Talebi A, Kianersi K, Beiraghdar M. Comparison of gene expression of SOX2 and OCT4 in normal tissue, polyps, and colon adenocarcinoma using immunohistochemical staining. Adv Biomed Res. 2015;4:234.

    Article  PubMed  PubMed Central  Google Scholar 

  157. Neumann J, Bahr F, Horst D, Kriegl L, Engel J, Mejías-Luque R, et al. SOX2 expression correlates with lymph-node metastases and distant spread in right-sided colon cancer. BMC Cancer. 2011;11:518.

    Article  PubMed  PubMed Central  Google Scholar 

  158. Verma P, Shukla N, Kumari S, Ansari MS, Gautam NK, Patel GK. Cancer stem cell in prostate cancer progression, metastasis and therapy resistance. Biochimica et Biophysica Acta (BBA) – Rev Cancer. 2023;1878:188887. This review offers a thorough analysis of the role played by prostate cancer stem cells.

    Article  CAS  Google Scholar 

  159. Abramovic I, Ulamec M, Katusic Bojanac A, Bulic-Jakus F, Jezek D, Sincic N. miRNA in prostate cancer: challenges toward translation. Epigenomics. 2020;12:543–58.

    Article  CAS  PubMed  Google Scholar 

  160. Doghish AS, Ismail A, El-Mahdy HA, Elkady MA, Elrebehy MA, Sallam A-AM. A review of the biological role of miRNAs in prostate cancer suppression and progression. Int J Biol Macromol. 2022;197:141–56.

    Article  CAS  PubMed  Google Scholar 

  161. Gupta S, Coronado GD, Argenbright K, Brenner AT, Castañeda SF, Dominitz JA, et al. Mailed fecal immunochemical test outreach for colorectal cancer screening: summary of a Centers for Disease Control and Prevention–sponsored Summit. CA Cancer J Clin. 2020;70:283–98.

    Article  PubMed  PubMed Central  Google Scholar 

  162. Nguyen T, Sridaran D, Chouhan S, Weimholt C, Wilson A, Luo J, et al. Histone H2A Lys130 acetylation epigenetically regulates androgen production in prostate cancer. Nat Commun. 2023;14:3357.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Sridaran D, Chouhan S, Mahajan K, Renganathan A, Weimholt C, Bhagwat S, et al. Inhibiting ACK1-mediated phosphorylation of C-terminal Src kinase counteracts prostate cancer immune checkpoint blockade resistance. Nat Commun. 2022;13:6929.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Chouhan S, Sawant M, Weimholt C, Luo J, Sprung RW, Terrado M, et al. TNK2/ACK1-mediated phosphorylation of ATP5F1A (ATP synthase F1 subunit alpha) selectively augments survival of prostate cancer while engendering mitochondrial vulnerability. Autophagy. 2023;19:1000–25.

    Article  CAS  PubMed  Google Scholar 

  165. Jaworska D, Król W, Szliszka E. Prostate cancer stem cells: research advances. Int J Mol Sci. 2015;16:27433–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Nagle RB, Ahmann FR, McDaniel KM, Paquin ML, Clark VA, Celniker A. Cytokeratin characterization of human prostatic carcinoma and its derived cell lines. Cancer Res. 1987;47:281–6.

    CAS  PubMed  Google Scholar 

  167. Signoretti S, Waltregny D, Dilks J, Isaac B, Lin D, Garraway L, et al. p63 is a prostate basal cell marker and is required for prostate development. Am J Pathol. 2000;157:1769–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. De Marzo AM, Meeker AK, Epstein JI, Coffey DS. Prostate stem cell compartments. Am J Pathol. 1998;153:911–9.

    Article  PubMed  PubMed Central  Google Scholar 

  169. Van Leenders GJLH, Schalken JA. Stem cell differentiation within the human prostate epithelium: implications for prostate carcinogenesis. BJU Int. 2001;88:35–42.

    Article  PubMed  Google Scholar 

  170. Wang ZA, Toivanen R, Bergren SK, Chambon P, Shen MM. Luminal cells are favored as the cell of origin for prostate cancer. Cell Rep. 2014;8:1339–46.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 2005;65:10946–51.

    Article  CAS  PubMed  Google Scholar 

  172. Signoretti S, Loda M. Prostate stem cells: from development to cancer. Semin Cancer Biol. 2007;17:219–24.

    Article  CAS  PubMed  Google Scholar 

  173. Hurt EM, Kawasaki BT, Klarmann GJ, Thomas SB, Farrar WL. CD44+CD24− prostate cells are early cancer progenitor/stem cells that provide a model for patients with poor prognosis. Br J Cancer. 2008;98:756–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, Tang S, et al. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene. 2006;25:1696–708.

    Article  CAS  PubMed  Google Scholar 

  175. Collins AT, Maitland NJ. Prostate cancer stem cells. Eur J Cancer. 2006;42:1213–8.

    Article  CAS  PubMed  Google Scholar 

  176. Baccelli I, Trumpp A. The evolving concept of cancer and metastasis stem cells. J Cell Biol. 2012;198:281–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Gu G, Yuan J, Wills M, Kasper S. Prostate cancer cells with stem cell characteristics reconstitute the original human tumor in vivo. Cancer Res. 2007;67:4807–15.

    Article  CAS  PubMed  Google Scholar 

  178. Maitland NJ, Collins AT. Prostate cancer stem cells: a new target for therapy. J Clin Oncol. 2008;26:2862–70.

    Article  PubMed  Google Scholar 

  179. Liu T, Xu F, Du X, Lai D, Liu T, Zhao Y, et al. Establishment and characterization of multi-drug resistant, prostate carcinoma-initiating stem-like cells from human prostate cancer cell lines 22RV1. Mol Cell Biochem. 2010;340:265–73.

    Article  CAS  PubMed  Google Scholar 

  180. Mimeault M, Johansson SL, Vankatraman G, Moore E, Henichart J-P, Depreux P, et al. Combined targeting of epidermal growth factor receptor and hedgehog signaling by gefitinib and cyclopamine cooperatively improves the cytotoxic effects of docetaxel on metastatic prostate cancer cells. Mol Cancer Ther. 2007;6:967–78.

    Article  CAS  PubMed  Google Scholar 

  181. Mimeault M, Johansson SL, Henichart J-P, Depreux P, Batra SK. Cytotoxic effects induced by docetaxel, gefitinib, and cyclopamine on side population and nonside population cell fractions from human invasive prostate cancer cells. Mol Cancer Ther. 2010;9:617–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Wang X, Julio MK, Economides KD, Walker D, Yu H, Halili MV, et al. A luminal epithelial stem cell that is a cell of origin for prostate cancer. Nature. 2009;461:495–500.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Korsten H, Ziel-van der Made A, Ma X, van der Kwast T, Trapman J. Accumulating progenitor cells in the luminal epithelial cell layer are candidate tumor initiating cells in a Pten knockout mouse prostate cancer model. PLoS One. 2009;4:e5662.

    Article  PubMed  PubMed Central  Google Scholar 

  184. Mateo F, Meca-Cortés Ó, Celià-Terrassa T, Fernández Y, Abasolo I, Sánchez-Cid L, et al. SPARC mediates metastatic cooperation between CSC and non-CSC prostate cancer cell subpopulations. Mol Cancer. 2014;13:237.

    Article  PubMed  PubMed Central  Google Scholar 

  185. Mathieu J, Zhang Z, Zhou W, Wang AJ, Heddleston JM, Pinna CMA, et al. HIF induces human embryonic stem cell markers in cancer cells. Cancer Res. 2011;71:4640–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Ravenna L, Principessa L, Verdina A, Salvatori L, Russo MA, Petrangeli E. Distinct phenotypes of human prostate cancer cells associate with different adaptation to hypoxia and pro-inflammatory gene expression. PLoS One. 2014;9:e96250.

    Article  PubMed  PubMed Central  Google Scholar 

  187. Dai Y, Bae K, Siemann DW. Impact of hypoxia on the metastatic potential of human prostate cancer cells. Int J Rad Oncol Biol Phys. 2011;81:521–8.

    Article  Google Scholar 

  188. Luo J, Ok Lee S, Liang L, Huang C-K, Li L, Wen S, et al. Infiltrating bone marrow mesenchymal stem cells increase prostate cancer stem cell population and metastatic ability via secreting cytokines to suppress androgen receptor signaling. Oncogene. 2014;33:2768–78.

    Article  CAS  PubMed  Google Scholar 

  189. Richardson GD, Robson CN, Lang SH, Neal DE, Maitland NJ, Collins AT. CD133, a novel marker for human prostatic epithelial stem cells. J Cell Sci. 2004;117:3539–45.

    Article  CAS  PubMed  Google Scholar 

  190. Rentala S, Yalavarthy PD, Mangamoori LN. α1 and β1 integrins enhance the homing and differentiation of cultured prostate cancer stem cells. Asian J Androl. 2010;12:548–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Klarmann GJ, Hurt EM, Mathews LA, Zhang X, Duhagon MA, Mistree T, et al. Invasive prostate cancer cells are tumor initiating cells that have a stem cell-like genomic signature. Clin Exp Metastasis. 2009;26:433–46.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Rybak AP, He L, Kapoor A, Cutz J-C, Tang D. Characterization of sphere-propagating cells with stem-like properties from DU145 prostate cancer cells. Biochimica et Biophysica Acta (BBA) - Molecular. Cell Res. 2011;1813:683–94.

    CAS  Google Scholar 

  193. Jiao J, Hindoyan A, Wang S, Tran LM, Goldstein AS, Lawson D, et al. Identification of CD166 as a surface marker for enriching prostate stem/progenitor and cancer initiating cells. PLoS One. 2012;7:e42564.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  194. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun X-W, et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science. 1979;2005(310):644–8.

    Google Scholar 

  195. Demichelis F, Rubin MA. TMPRSS2-ETS fusion prostate cancer: biological and clinical implications. J Clin Pathol. 2007;60:1185–6.

    Article  PubMed  PubMed Central  Google Scholar 

  196. Birnie R, Bryce SD, Roome C, Dussupt V, Droop A, Lang SH, et al. Gene expression profiling of human prostate cancer stem cells reveals a pro-inflammatory phenotype and the importance of extracellular matrix interactions. Genome Biol. 2008;9:R83.

    Article  PubMed  PubMed Central  Google Scholar 

  197. Mehra R, Tomlins SA, Yu J, Cao X, Wang L, Menon A, et al. Characterization of TMPRSS2 -ETS gene aberrations in androgen-independent metastatic prostate cancer. Cancer Res. 2008;68:3584–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  198. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71:209–49.

    Article  PubMed  Google Scholar 

  199. Soerjomataram I, Bray F. Planning for tomorrow: global cancer incidence and the role of prevention 2020–2070. Nat Rev Clin Oncol. 2021;18:663–72.

    Article  PubMed  Google Scholar 

  200. Crabtree J, Miele L. Breast cancer stem cells. Biomedicines. 2018;6:77.

    Article  PubMed  PubMed Central  Google Scholar 

  201. Lombardo Y, de Giorgio A, Coombes CR, Stebbing J, Castellano L. Mammosphere formation assay from human breast cancer tissues and cell lines. J Visual Exp. 2015;(97):52671. https://doi.org/10.3791/52671.

  202. Dontu G, Jackson KW, McNicholas E, Kawamura MJ, Abdallah WM, Wicha MS. Role of Notch signaling in cell-fate determination of human mammary stem/progenitor cells. Breast Cancer Res. 2004;6:R605.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  203. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 2003;17:1253–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  204. Grimshaw MJ, Cooper L, Papazisis K, Coleman JA, Bohnenkamp HR, Chiapero-Stanke L, et al. Mammosphere culture of metastatic breast cancer cells enriches for tumorigenic breast cancer cells. Breast Cancer Res. 2008;10:R52.

    Article  PubMed  PubMed Central  Google Scholar 

  205. Iliopoulos D, Hirsch HA, Wang G, Struhl K. Inducible formation of breast cancer stem cells and their dynamic equilibrium with non-stem cancer cells via IL6 secretion. Proc Nat Acad Sci. 2011;108:1397–402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  206. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 2005;65:5506–11.

    Article  CAS  PubMed  Google Scholar 

  207. Rios AC, Fu NY, Lindeman GJ, Visvader JE. In situ identification of bipotent stem cells in the mammary gland. Nature. 2014;506:322–7.

    Article  CAS  PubMed  Google Scholar 

  208. Van Keymeulen A, Rocha AS, Ousset M, Beck B, Bouvencourt G, Rock J, et al. Distinct stem cells contribute to mammary gland development and maintenance. Nature. 2011;479:189–93.

    Article  PubMed  Google Scholar 

  209. Visvader JE, Stingl J. Mammary stem cells and the differentiation hierarchy: current status and perspectives. Genes Dev. 2014;28:1143–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  210. Liu S, Cong Y, Wang D, Sun Y, Deng L, Liu Y, et al. Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Reports. 2014;2:78–91.

    Article  CAS  PubMed  Google Scholar 

  211. Koren S, Bentires-Alj M. Mouse models of PIK3CA mutations: one mutation initiates heterogeneous mammary tumors. FEBS J. 2013;280:2758–65.

    Article  CAS  PubMed  Google Scholar 

  212. Meyer DS, Brinkhaus H, Müller U, Müller M, Cardiff RD, Bentires-Alj M. Luminal expression of PIK3CA mutant H1047R in the mammary gland induces heterogeneous tumors. Cancer Res. 2011;71:4344–51.

    Article  CAS  PubMed  Google Scholar 

  213. Liu P, Cheng H, Santiago S, Raeder M, Zhang F, Isabella A, et al. Oncogenic PIK3CA-driven mammary tumors frequently recur via PI3K pathway–dependent and PI3K pathway–independent mechanisms. Nat Med. 2011;17:1116–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  214. Koren S, Reavie L, Couto JP, De Silva D, Stadler MB, Roloff T, et al. PIK3CAH1047R induces multipotency and multi-lineage mammary tumours. Nature. 2015;525:114–8.

    Article  CAS  PubMed  Google Scholar 

  215. Chaffer CL, Marjanovic ND, Lee T, Bell G, Kleer CG, Reinhardt F, et al. Poised chromatin at the ZEB1 promoter enables breast cancer cell plasticity and enhances tumorigenicity. Cell. 2013;154:61–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  216. Lagadec C, Vlashi E, Della Donna L, Dekmezian C, Pajonk F. Radiation-induced reprogramming of breast cancer cells. Stem Cells. 2012;30:833–44.

    Article  CAS  PubMed  Google Scholar 

  217. Poli V, Fagnocchi L, Fasciani A, Cherubini A, Mazzoleni S, Ferrillo S, et al. MYC-driven epigenetic reprogramming favors the onset of tumorigenesis by inducing a stem cell-like state. Nat Commun. 2018;9:1024.

    Article  PubMed  PubMed Central  Google Scholar 

  218. Conley SJ, Gheordunescu E, Kakarala P, Newman B, Korkaya H, Heath AN, et al. Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proc Nat Acad Sci. 2012;109:2784–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  219. Ginestier C, Liu S, Diebel ME, Korkaya H, Luo M, Brown M, et al. CXCR1 blockade selectively targets human breast cancer stem cells in vitro and in xenografts. J Clin Investig. 2010;120:485–97.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  220. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, et al. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res. 2009;69:1302–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  221. Ordaz-Ramos A, Tellez-Jimenez O, Vazquez-Santillan K. Signaling pathways governing the maintenance of breast cancer stem cells and their therapeutic implications. Front Cell. Dev Biol. 2023:11:1221175. https://doi.org/10.3389/fcell.2023.1221175.

  222. Conde I, Ribeiro AS, Paredes J. Breast cancer stem cell membrane biomarkers: therapy targeting and clinical implications. Cells. 2022;11:934. This review discusses the importance of breast cancer stem cell membrane biomarkers as potential targets for prognosis and therapy.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  223. Liu TJ, Sun BC, Zhao XL, Zhao XM, Sun T, Gu Q, et al. CD133+ cells with cancer stem cell characteristics associates with vasculogenic mimicry in triple-negative breast cancer. Oncogene. 2013;32:544–53.

    Article  CAS  PubMed  Google Scholar 

  224. Wright MH, Calcagno AM, Salcido CD, Carlson MD, Ambudkar SV, Varticovski L. Brca1 breast tumors contain distinct CD44+/CD24- and CD133+cells with cancer stem cell characteristics. Breast Cancer Res. 2008;10:R10.

    Article  PubMed  PubMed Central  Google Scholar 

  225. Brugnoli F, Grassilli S, Piazzi M, Palomba M, Nika E, Bavelloni A, et al. In triple negative breast tumor cells, PLC-β2 promotes the conversion of CD133high to CD133low phenotype and reduces the CD133-related invasiveness. Mol Cancer. 2013;12:165.

    Article  PubMed  PubMed Central  Google Scholar 

  226. Friedrichs K, Ruiz P, Franke F, Gille I, Terpe H-J, Imhof BA. High expression level of α6 integrin in human breast carcinoma is correlated with reduced survival. Cancer Res. 1995;55:901–6.

    CAS  PubMed  Google Scholar 

  227. Pham PV, Phan NL, Nguyen NT, Truong NH, Duong TT, Le DV, et al. Differentiation of breast cancer stem cells by knockdown of CD44: promising differentiation therapy. J Transl Med. 2011;9:209.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  228. Goodarzi N, Ghahremani MH, Amini M, Atyabi F, Ostad SN, Shabani Ravari N, et al. CD44-targeted docetaxel conjugate for cancer cells and cancer stem-like cells: a novel hyaluronic acid-based drug delivery system. Chem Biol Drug Des. 2014;83:741–52.

    Article  CAS  PubMed  Google Scholar 

  229. Muntimadugu E, Kumar R, Saladi S, Rafeeqi TA, Khan W. CD44 targeted chemotherapy for co-eradication of breast cancer stem cells and cancer cells using polymeric nanoparticles of salinomycin and paclitaxel. Colloids Surf B Biointerfaces. 2016;143:532–46.

    Article  CAS  PubMed  Google Scholar 

  230. Phillips TM, McBride WH, Pajonk F. The response of CD24 −/low /CD44 + breast cancer–initiating cells to radiation. JNCI: J Nat Cancer Instit. 2006;98:1777–85.

    Article  Google Scholar 

  231. Bensimon J, Altmeyer-Morel S, Benjelloun H, Chevillard S, Lebeau J. CD24−/low stem-like breast cancer marker defines the radiation-resistant cells involved in memorization and transmission of radiation-induced genomic instability. Oncogene. 2013;32:251–8.

    Article  CAS  PubMed  Google Scholar 

  232. Marcato P, Dean CA, Giacomantonio CA, Lee PWK. Aldehyde dehydrogenase: its role as a cancer stem cell marker comes down to the specific isoform. Cell Cycle. 2011;10:1378–84.

    Article  CAS  PubMed  Google Scholar 

  233. Yang F, Cao L, Sun Z, Jin J, Fang H, Zhang W, et al. Evaluation of breast cancer stem cells and intratumor stemness heterogeneity in triple-negative breast cancer as prognostic factors. Int J Biol Sci. 2016;12:1568–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  234. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.

    Article  PubMed  Google Scholar 

  235. Simard EP, Ward EM, Siegel R, Jemal A. Cancers with increasing incidence trends in the United States: 1999 through 2008. CA Cancer J Clin. 2012;62:118–28.

    Article  PubMed  Google Scholar 

  236. Ferlay J, Shin H-R, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2010;127:2893–917.

    Article  CAS  PubMed  Google Scholar 

  237. Chouhan S, Singh S, Athavale D, Ramteke P, Vanuopadath M, Nair BG, et al. Sensitization of hepatocellular carcinoma cells towards doxorubicin and sorafenib is facilitated by glucose dependent alterations in reactive oxygen species, P-glycoprotein and DKK4. J Biosci. 2020;45:97.

  238. Athavale D, Chouhan S, Pandey V, Mayengbam SS, Singh S, Bhat MK. Hepatocellular carcinoma-associated hypercholesterolemia: involvement of proprotein-convertase-subtilisin-kexin type-9 (PCSK9). Cancer Metab. 2018;6:16.

    Article  PubMed  PubMed Central  Google Scholar 

  239. Nio K, Yamashita T, Kaneko S. The evolving concept of liver cancer stem cells. Mol Cancer. 2017;16:4.

    Article  PubMed  PubMed Central  Google Scholar 

  240. Ma S, Chan K, Hu L, Lee TK, Wo JY, Ng IO, et al. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology. 2007;132:2542–56.

    Article  CAS  PubMed  Google Scholar 

  241. Yang ZF, Ho DW, Ng MN, Lau CK, Yu WC, Ngai P, et al. Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell. 2008;13:153–66.

    Article  CAS  PubMed  Google Scholar 

  242. Yang ZF, Ngai P, Ho DW, Yu WC, Ng MNP, Lau CK, et al. Identification of local and circulating cancer stem cells in human liver cancer. Hepatology. 2008;47:919–28.

    Article  CAS  PubMed  Google Scholar 

  243. Yang W, Yan H-X, Chen L, Liu Q, He Y-Q, Yu L-X, et al. Wnt/β-catenin signaling contributes to activation of normal and tumorigenic liver progenitor cells. Cancer Res. 2008;68:4287–95.

    Article  CAS  PubMed  Google Scholar 

  244. Yamashita T, Ji J, Budhu A, Forgues M, Yang W, Wang H, et al. EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology. 2009;136:1012–1024.e4.

    Article  CAS  PubMed  Google Scholar 

  245. Haraguchi N, Ishii H, Mimori K, Tanaka F, Ohkuma M, Kim HM, et al. CD13 is a therapeutic target in human liver cancer stem cells. J Clin Investig. 2010;120:3326–39.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  246. Lee TKW, Castilho A, Cheung VCH, Tang KH, Ma S, Ng IOL. CD24+ liver tumor-initiating cells drive self-renewal and tumor initiation through STAT3-mediated NANOG regulation. Cell Stem Cell. 2011;9:50–63.

    Article  CAS  PubMed  Google Scholar 

  247. Xu X, Liu R-F, Zhang X, Huang L-Y, Chen F, Fei Q-L, et al. DLK1 as a potential target against cancer stem/progenitor cells of hepatocellular carcinoma. Mol Cancer Ther. 2012;11:629–38.

    Article  CAS  PubMed  Google Scholar 

  248. Zhao W, Wang L, Han H, Jin K, Lin N, Guo T, et al. 1B50-1, a mAb raised against recurrent tumor cells, targets liver tumor-initiating cells by binding to the calcium channel α2δ1 subunit. Cancer Cell. 2013;23:541–56.

    Article  CAS  PubMed  Google Scholar 

  249. Liu S, Li N, Yu X, Xiao X, Cheng K, Hu J, et al. Expression of intercellular adhesion molecule 1 by hepatocellular carcinoma stem cells and circulating tumor cells. Gastroenterology. 2013;144:1031–1041.e10.

    Article  PubMed  Google Scholar 

  250. Lee TK-W, Cheung VC-H, Lu P, Lau EYT, Ma S, Tang KH, et al. Blockade of CD47-mediated cathepsin S/protease-activated receptor 2 signaling provides a therapeutic target for hepatocellular carcinoma. Hepatology. 2014;60:179–91.

    Article  CAS  PubMed  Google Scholar 

  251. Lei Z-J, Wang J, Xiao H-L, Guo Y, Wang T, Li Q, et al. Lysine-specific demethylase 1 promotes the stemness and chemoresistance of Lgr5+ liver cancer initiating cells by suppressing negative regulators of β-catenin signaling. Oncogene. 2015;34:3188–98.

    Article  CAS  PubMed  Google Scholar 

  252. Yamashita T, Wang XW. Cancer stem cells in the development of liver cancer. J Clin Investig. 2013;123:1911–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  253. He G, Dhar D, Nakagawa H, Font-Burgada J, Ogata H, Jiang Y, et al. Identification of liver cancer progenitors whose malignant progression depends on autocrine IL-6 signaling. Cell. 2013;155:384–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  254. Wu K, Ding J, Chen C, Sun W, Ning B-F, Wen W, et al. Hepatic transforming growth factor beta gives rise to tumor-initiating cells and promotes liver cancer development. Hepatology. 2012;56:2255–67.

    Article  CAS  PubMed  Google Scholar 

  255. Tang Y, Kitisin K, Jogunoori W, Li C, Deng C-X, Mueller SC, et al. Progenitor/stem cells give rise to liver cancer due to aberrant TGF-β and IL-6 signaling. Proc Nat Acad Sci. 2008;105:2445–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  256. Holczbauer Á, Factor VM, Andersen JB, Marquardt JU, Kleiner DE, Raggi C, et al. Modeling pathogenesis of primary liver cancer in lineage-specific mouse cell types. Gastroenterology. 2013;145:221–31.

    Article  CAS  PubMed  Google Scholar 

  257. Zhang X, Bai Y, Huang L, Liu S, Mo Y, Cheng W, et al. CHD1L augments autophagy-mediated migration of hepatocellular carcinoma through targeting ZKSCAN3. Cell Death Dis. 2021;12:950. This study reveals the involvement of CHD1L in tumor migration regulation through ZKSCAN3-mediated autophagy in hepatocellular carcinoma (HCC).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  258. Lee TKW, Castilho A, Ma S, Ng IOL. Liver cancer stem cells: implications for a new therapeutic target. Liver Int. 2009;29:955–65.

    Article  CAS  PubMed  Google Scholar 

  259. Williams GM, Gebhardt R, Sirma H, Stenbäck F. Non-linearity of neoplastic conversion induced in rat liver by low exposures to diethylnitrosamine. Carcinogenesis. 1993;14:2149–56.

    Article  CAS  PubMed  Google Scholar 

  260. Tatematsu M, Nagamine Y, Farber E. Redifferentiation as a basis for remodeling of carcinogen-induced hepatocyte nodules to normal appearing liver1. Cancer Res. 1983;43:5049–58.

    CAS  PubMed  Google Scholar 

  261. Marrero JA. Hepatocellular carcinoma. Curr Opin Gastroenterol. 2005;21:308–12.

    Article  PubMed  Google Scholar 

  262. Libbrecht L, De Vos R, Cassiman D, Desmet V, Aerts R, Roskams T. Hepatic progenitor cells in hepatocellular adenomas. Am J Surg Pathol. 2001;25:1388–96.

    Article  CAS  PubMed  Google Scholar 

  263. Kim H, Park C, Han K-H, Choi J, Kim YB, Kim JK, et al. Primary liver carcinoma of intermediate (hepatocyte–cholangiocyte) phenotype. J Hepatol. 2004;40:298–304.

    Article  CAS  PubMed  Google Scholar 

  264. Robrechts C, Vos R, Heuvel M, Cutsem E, Damme B, Desmet V, et al. Primary liver tumour of intermediate (hepatocyte-bile duct cell) phenotype: a progenitor cell tumour? Liver. 2008;18:288–93.

    Article  Google Scholar 

  265. Dumble ML, Croager EJ, Yeoh GCT, Quail EA. Generation and characterization of p53 null transformed hepatic progenitor cells: oval cells give rise to hepatocellular carcinoma. Carcinogenesis. 2002;23:435–45.

    Article  CAS  PubMed  Google Scholar 

  266. Wicha MS, Liu S, Dontu G. Cancer stem cells: an old idea—a paradigm shift. Cancer Res. 2006;66:1883–90.

    Article  CAS  PubMed  Google Scholar 

  267. Chouhan S, Singh S, Athavale D, Ramteke P, Pandey V, Joseph J, et al. Glucose induced activation of canonical Wnt signaling pathway in hepatocellular carcinoma is regulated by DKK4. Sci Rep. 2016;6:27558.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  268. Li B, Chen Y, Wang F, Guo J, Fu W, Li M, et al. Bmi1 drives hepatocarcinogenesis by repressing the TGFβ2/SMAD signalling axis. Oncogene. 2020;39:1063–79.

    Article  CAS  PubMed  Google Scholar 

  269. Taniguchi H, Chiba T. Stem cells and cancer in the liver. Dis Markers. 2008;24:223–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  270. Hoey T, Yen W-C, Axelrod F, Basi J, Donigian L, Dylla S, et al. DLL4 blockade inhibits tumor growth and reduces tumor-initiating cell frequency. Cell Stem Cell. 2009;5:168–77.

    Article  CAS  PubMed  Google Scholar 

  271. Diehn M, Clarke MF. Cancer stem cells and radiotherapy: new insights into tumor radioresistance. JNCI: J Nat Cancer Instit. 2006;98:1755–7.

    Article  Google Scholar 

  272. Nguyen LV, Vanner R, Dirks P, Eaves CJ. Cancer stem cells: an evolving concept. Nat Rev Cancer. 2012;12:133–43.

    Article  CAS  PubMed  Google Scholar 

  273. Levin TG, Powell AE, Davies PS, Silk AD, Dismuke AD, Anderson EC, et al. Characterization of the intestinal cancer stem cell marker CD166 in the human and mouse gastrointestinal tract. Gastroenterology. 2010;139:2072–2082.e5.

    Article  CAS  PubMed  Google Scholar 

  274. Shaikh MV, Kala M, Nivsarkar M. CD90 a potential cancer stem cell marker and a therapeutic target. Cancer Biomarkers. 2016;16:301–7.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to acknowledge the Department of Biochemistry, Purdue University, USA. Figures 1 and 2 were created with BioRender (www.biorender.com). We are extremely grateful to the reviewers for their constructive criticisms, suggestions, and comments, which certainly enriched this article.

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  1. Department of Biochemistry, Purdue University, 175 S. University Street, West Lafayette, IN, 47907-2063, USA

    Subhadeep Das

  2. Department of Pathology and Immunology, Washington University in St. Louis, 660. S Euclid Ave, St. Louis, MO, 63110, USA

    Tabish H. Khan

  3. Department Developmental Neurobiology, St. Jude Children’s Research Hospital, 262 Danny Thomas Place, Memphis, TN, 38105, USA

    Debasish Sarkar

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Conception and design: SD, DS. Writing, review, and revision of the manuscript: SD, THK, DS. Study supervision: SD, DS

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Correspondence to Debasish Sarkar.

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Das, S., Khan, T.H. & Sarkar, D. Comprehensive Review on the Effect of Stem Cells in Cancer Progression. Curr. Tissue Microenviron. Rep. 5, 39–59 (2024). https://doi.org/10.1007/s43152-024-00053-6

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