The effect that different regions of the Alu consensus sequence have upon the stability and accumulation of its RNA polymerase III (Pol III) directed transcripts was determined by transiently overexpressing Alu deletion and chimeric constructs in human 293 cells. Transcripts of the left Alu monomer are more stable than those of the full-length consensus sequence and any additional 3' sequence beyond the left monomer destabilizes the resulting transcript. Neither the middle A-rich region nor the 3' A-rich tail specifically affect the stability of Alu transcripts. However, the right monomer is inherently less stable than corresponding left monomer transcripts. Alu's dimeric structure and sequences peculiar to the right monomer each limit the stability and steady state accumulation of its transcripts. A host requirement to rapidly metabolize Alu RNA or restrict its abundance may have selected for these two features of the Alu consensus sequence.