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. 2011 May 12;473(7346):234-8.
doi: 10.1038/nature09917. Epub 2011 Apr 17.

Acetylation-dependent regulation of endothelial Notch signalling by the SIRT1 deacetylase

Affiliations

Acetylation-dependent regulation of endothelial Notch signalling by the SIRT1 deacetylase

Virginia Guarani et al. Nature. .

Abstract

Notch signalling is a key intercellular communication mechanism that is essential for cell specification and tissue patterning, and which coordinates critical steps of blood vessel growth. Although subtle alterations in Notch activity suffice to elicit profound differences in endothelial behaviour and blood vessel formation, little is known about the regulation and adaptation of endothelial Notch responses. Here we report that the NAD(+)-dependent deacetylase SIRT1 acts as an intrinsic negative modulator of Notch signalling in endothelial cells. We show that acetylation of the Notch1 intracellular domain (NICD) on conserved lysines controls the amplitude and duration of Notch responses by altering NICD protein turnover. SIRT1 associates with NICD and functions as a NICD deacetylase, which opposes the acetylation-induced NICD stabilization. Consequently, endothelial cells lacking SIRT1 activity are sensitized to Notch signalling, resulting in impaired growth, sprout elongation and enhanced Notch target gene expression in response to DLL4 stimulation, thereby promoting a non-sprouting, stalk-cell-like phenotype. In vivo, inactivation of Sirt1 in zebrafish and mice causes reduced vascular branching and density as a consequence of enhanced Notch signalling. Our findings identify reversible acetylation of the NICD as a molecular mechanism to adapt the dynamics of Notch signalling, and indicate that SIRT1 acts as rheostat to fine-tune endothelial Notch responses.

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Conflict of interest statement

The authors declare no competing financial interests.

Figures

Figure 1
Figure 1. SIRT1 limits endothelial DLL4/Notch signalling and targets NICD for deacetylation
a, b, TP1- (a), 4×CBF1- or CBF1 mutant- (mt) luciferase activity (b) in control (scrambled) or SIRT1-siRNA-transfected endothelial cells. c, NRARP and HEY2 mRNA levels in SCR or SIRT1 siRNA-transfected endothelial cells. d, e, TP1-luciferase activity (d) and NRARP and HEY2 mRNA levels (e) in endothelial cells stimulated with SRT2183. f, TP1-luciferase activity in control and SIRT1-deficient endothelial cells co-transfected with NICD. g, TP1-luciferase activity in endothelial cells transfected with combinations of NICD, SIRT1 and SIRT1 H363Y. h, i, Co-immunoprecipitations from SIRT1–Flag and NICD–V5 or NICD(ΔC)–Myc co-transfected 293 cells. IP, immunoprecipitation; WB, western blot. j, Co-immunoprecipitation of NICD and SIRT1 in endothelial cells treated with or without MG132. k, Acetylation of NICD–V5 in 293 cells treated with NAM, TSA, or combinations thereof. l, Acetylation of NICD in endothelial cells treated with NAM. m, Acetylation of NICD–V5 in SIRT1-siRNA-transfected 293 cells. n, Deacetylation assay with NICD(ΔC)–Myc, recombinant wild-type or H363Y SIRT1. Relative quantifications of NICD acetylation are shown on the right of the panel in l, m. DLL4 was used to stimulate Notch signalling in endothelial cells in a–e, j and l. All experiments n ≥ 3; error bars, mean ± s.d. *, P < 0.05; **, P < 0.01; ***, P < 0.001; NS, not significant.
Figure 2
Figure 2. Destabilization of NICD by SIRT1
a, HCD (higher energy collisionally activated dissociation) MS/MS spectrum showing acetylation of NICD lysine residue 2154. b, Overview of acetylated lysines in the NICD. RAM, RBPj-associated molecule; ANK, ankyrin repeats; PEST, proline (P), glutamic acid (E), serine (S) and threonine (T) enriched sequence. c, Acetylation of NICD–V5 wild type or 14KR in transfected 293 cells treated with NAM. d, TP1-luciferase activity in scrambled and SIRT1-siRNA-transfected endothelial cells co-transfected with wild-type or NICD(14KR). e, NICD protein levels in 293 cells expressing NICD–V5 and SIRT1–Flag. f, NICD–V5 protein levels in 293 cells transfected with scrambled or SIRT1 siRNA and NICD–V5 wild type or 14KR. g, h, NICD protein expression in endothelial cells treated with NAM and/or TSA (g) or transfected with SIRT1 siRNA (h). Relative quantifications of NICD protein levels are shown on the right of the panel. i, NICD protein levels in endothelial cells pre-treated with or without MG132 and/or SRT2183. j, Endothelial cells were pre-treated with CHX and NAM or SRT2183 and NICD protein levels analysed at the indicated time points. DLL4 was used to stimulate Notch signalling in endothelial cells in g–j. NICD protein levels in g–i were assessed after 6 h of DLL4 stimulation. All experiments n ≥ 3; error bars, mean ± s.d. *, P < 0.05; **, P < 0.01; ***, P < 0.001; NS, not significant.
Figure 3
Figure 3. Inactivation of SIRT1 enhances endothelial Notch responses in mice
a, Sirt1 localization (red) in the retinal endothelium (isolectin B4, green). b, Higher magnification of inset in a is shown. Asterisks indicate Sirt1 expression in stalk endothelial cells; arrowheads indicate tip cells with weak or absent Sirt1 expression. c–e, Images of P5 Sirt1 control and mutant retinas stained with isoB4. Blue and green boxes indicate the vascular front and capillary plexus, respectively. A, arteries; V, veins. f–h, IsoB4 (red) and BrdU (green) labelling in P5 retinas of the respective genotypes. i, j, Statistical summary of the number of vessel branch points and the number of BrdU/IsoB4-positive cells of the respective genotypes. k, qPCR of Hey2, Nrarp and Lfng mRNA expression in Dll4-stimulated endothelial cells derived from the respective genotypes. l, Statistical summary of the percentage of IsoB4-positive vessel coverage in vehicle and DAPT-treated retinas of control and Sirt1 mutant mice. All experiments n ≥ 4; error bars, mean ± s.d. *, P < 0.05; **, P < 0.01; ***, P < 0.001; NS, not significant.
Figure 4
Figure 4. Inactivation of SIRT1 leads to a cell-autonomous increase in Notch signalling and defective endothelial cell sprouting
a–d, Lateral trunk views of 48 h post fertilization Tg(fli1a:EGFP)y71 zebrafish embryos. Control embryos or sirt1 morphants were treated with DAPT and DMSO. e, Endothelial cell nuclei counts in the intersomitic vessels (ISVs) of transgenic Tg(fli1a:nEGFP)y7 embryos at 28 h post fertilization (h. p. f.) treated with or without DAPT, or injected with dll4-specific morpholinos. f–h, Overview of vascular sprouts from EBs of DsRed (WT) (f), Sirt1Δe4/Δe4 (g) ES cells and 1:1 chimaeras (h). i, Quantification of total pixel intensity of the NICD immunostaining per nucleus in DsRed and Sirt1 mutant endothelial cells. j, Quantification of tip-cell contribution of each ES cell genotype in vascular sprouts. k–m, NICD immunostaining (green) of individual sprouts of EBs from the respective genotypes. DsRed cells (red), Sirt1 mutant cells (non-labelled), DAPI (blue), PECAM1 (grey). All experiments n ≥ 4. Error bars, mean ± s.d. **, P < 0.01; ***, P < 0.001.

Comment in

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