RNAi screen for telomerase reverse transcriptase transcriptional regulators identifies HIF1α as critical for telomerase function in murine embryonic stem cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 31, 2010, Pages 13842-13847

  Coussens, Matthew ^a   Davy, Philip ^a   Brown, Lancer ^b   Foster, Christopher ^b   Andrews, William H ^b   Nagata, Melissa ^a   Allsopp, Richard ^a  

^a UNIVERSITY OF HAWAII   (United States)

^b Sierra Sciences   (United States)

Author keywords

Embryo; Telomere

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; SHORT HAIRPIN RNA; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; HIF1A PROTEIN, MOUSE; TERT PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL GROWTH; CELL STRUCTURE; CELL SURVIVAL; EMBRYONIC STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA INTERFERENCE; TELOMERE; ANIMAL; C57BL MOUSE; CELL HYPOXIA; CELL LINE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HOMEOSTASIS; METABOLISM; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE;

MURINAE;

ANIMALS; BASE SEQUENCE; CELL HYPOXIA; CELL LINE; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION; HOMEOSTASIS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; RNA INTERFERENCE; TELOMERASE; TRANSCRIPTION, GENETIC;

EID: 77956387858     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0913834107     Document Type: Article

References (48)

1. Hayflick L, Moorhead PS (1961) The serial cultivation of human diploid cell strains. Exp Cell Res 25:585-621.
2. Thomson JA, et al. (1998) Embryonic stem cell lines derived from human blastocysts. Science 282:1145-1147.
3. Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154-156.
4. Harrison DE, Astle CM (1982) Loss of stem cell repopulating ability upon transplantation. Effects of donor age, cell number, and transplantation procedure. J Exp Med 156:1767-1779.
5. Allsopp RC, Cheshier S, Weissman IL (2001) Telomere shortening accompanies increased cell cycle activity during serial transplantation of hematopoietic stem cells. J Exp Med 193:917-924.
6. Chan SR, Blackburn EH (2004) Telomeres and telomerase. Philos Trans R Soc Lond B Biol Sci 359:109-121.
7. Harley CB, Futcher AB, Greider CW (1990) Telomeres shorten during ageing of human fibroblasts. Nature 345:458-460.
8. Hastie ND, et al. (1990) Telomere reduction in human colorectal carcinoma and with ageing. Nature 346:866-868.
9. Hemann MT, Strong MA, Hao LY, Greider CW (2001) The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 107:67-77.
10. Nakamura TM, et al. (1997) Telomerase catalytic subunit homologs from fission yeast and human. Science 277:955-959.
11. Bodnar AG, et al. (1998) Extension of life-span by introduction of telomerase into normal human cells. Science 279:349-352.
12. Kolquist KA, et al. (1998) Expression of TERT in early premalignant lesions and a subset of cells in normal tissues. Nat Genet 19:182-186.
13. Lee HW, et al. (1998) Essential role of mouse telomerase in highly proliferative organs. Nature 392:569-574.
14. Allsopp RC, Morin GB, DePinho R, Harley CB, Weissman IL (2003) Telomerase is required to slow telomere shortening and extend replicative lifespan of HSCs during serial transplantation. Blood 102:517-520.
15. Greenwood MJ, Lansdorp PM (2003) Telomeres, telomerase, and hematopoietic stem cell biology. Arch Med Res 34:489-495.
16. Siegl-Cachedenier I, Flores I, Klatt P, Blasco MA (2007) Telomerase reverses epidermal hair follicle stem cell defects and loss of long-term survival associated with critically short telomeres. J Cell Biol 179:277-290.
17. Wang J, Xie LY, Allan S, Beach D, Hannon GJ (1998) Myc activates telomerase. Genes Dev 12:1769-1774.
18. Takakura M, Kyo S, Inoue M, Wright WE, Shay JW (2005) Function of AP-1 in transcription of the telomerase reverse transcriptase gene (TERT) in human and mouse cells. Mol Cell Biol 25:8037-8043.
19. Paddison PJ, et al. (2004) A resource for large-scale RNA-interference-based screens in mammals. Nature 428:427-431.
20. Carmell MA, Zhang L, Conklin DS, Hannon GJ, Rosenquist TA (2003) Germline transmission of RNAi in mice. Nat Struct Biol 10:91-92.
21. Holt SE, Wright WE, Shay JW (1996) Regulation of telomerase activity in immortal cell lines. Mol Cell Biol 16:2932-2939.
22. Buchkovich KJ, Greider CW (1996) Telomerase regulation during entry into the cell cycle in normal human T cells. Mol Biol Cell 7:1443-1454.
23. O'Rourke JF, et al. (1997) Hypoxia response elements. Oncol Res 9:327-332.
24. Nozawa K, Maehara K, Isobe K (2001) Mechanism for the reduction of telomerase expression during muscle cell differentiation. J Biol Chem 276:22016-22023.
25. Seimiya H, et al. (1999) Hypoxia up-regulates telomerase activity via mitogen-activated protein kinase signaling in human solid tumor cells. Biochem Biophys Res Commun 260:365-370.
26. Nishi H, et al. (2004) Hypoxia-inducible factor 1 mediates upregulation of telomerase (hTERT). Mol Cell Biol 24:6076-6083.
27. Yatabe N, et al. (2004) HIF-1-mediated activation of telomerase in cervical cancer cells. Oncogene 23:3708-3715.
28. Yu RM, et al. (2006) Hypoxia induces telomerase reverse transcriptase (TERT) gene expression in non-tumor fish tissues in vivo: The marine medaka (Oryzias melastigma) model. BMC Mol Biol 7:27-34.
29. Forsythe JA, et al. (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16:4604-4613.
30. Ulrich HD (2007) SUMO teams up with ubiquitin to manage hypoxia. Cell 131:446-447.
31. Anderson CJ, Hoare SF, Ashcroft M, Bilsland AE, Keith WN (2006) Hypoxic regulation of telomerase gene expression by transcriptional and post-transcriptional mechanisms. Oncogene 25:61-69.
32. Lou F, et al. (2007) The opposing effect of hypoxia-inducible factor-2alpha on expression of telomerase reverse transcriptase. Mol Cancer Res 5:793-800.
33. d'Adda di Fagagna F, et al. (2003) A DNA damage checkpoint response in telomere-initiated senescence. Nature 426:194-198.
34. Iyer NV, et al. (1998) Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 12:149-162.
35. Wright DL, et al. (2001) Characterization of telomerase activity in the human oocyte and preimplantation embryo. Mol Hum Reprod 7:947-955.
36. Xu J, Yang X (2000) Telomerase activity in early bovine embryos derived from parthenogenetic activation and nuclear transfer. Biol Reprod 63:1124-1128.
37. Schaetzlein S, et al. (2004) Telomere length is reset during early mammalian embryogenesis. Proc Natl Acad Sci USA 101:8034-8038.
38. Xu J, Yang X (2001) Telomerase activity in early bovine embryos derived from parthenogenetic activation and nuclear transfer. Biol Reprod 64:770-774.
39. Cheng J, Kang X, Zhang S, Yeh ETH (2007) SUMO-specific protease 1 is essential for stabilization of HIF1alpha during hypoxia. Cell 131:584-595.
40. Koshiji M, et al. (2004) HIF-1alpha induces cell cycle arrest by functionally counteracting Myc. EMBO J 23:1949-1956.
41. Ramírez-Bergeron DL, Runge A, Adelman DM, Gohil M, Simon MC (2006) HIF-dependent hematopoietic factors regulate the development of the embryonic vasculature. Dev Cell 11:81-92.
42. Rodesch F, Simon P, Donner C, Jauniaux E (1992) Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol 80:283-285.
43. Allsopp R, Shimoda J, Easa D, Ward K (2007) Long telomeres in the mature human placenta. Placenta 28:324-327.
44. Parmar K, Mauch P, Vergilio JA, Sackstein R, Down JD (2007) Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci USA 104:5431-5436.
45. Vaziri H, et al. (1993) Loss of telomeric DNA during aging of normal and trisomy 21 human lymphocytes. Am J Hum Genet 52:661-667.
46. Vaziri H, et al. (1994) Evidence for a mitotic clock in human hematopoietic stem cells: Loss of telomeric DNA with age. Proc Natl Acad Sci USA 91:9857-9860.
47. Coussens M, et al. (2006) Regulation and effects of modulation of telomerase reverse transcriptase expression in primordial germ cells during development. Biol Reprod 75:785-791.
48. Allsopp RC, Harley CB (1995) Evidence for a critical telomere length in senescent human fibroblasts. Exp Cell Res 219:130-136.