Alternative lengthening of telomeres in cancer stem cells in vivo

Oncogene

Volumn 34, Issue 5, 2015, Pages 611-620

  Bojovic, B ^a   Booth, R E ^a   Jin, Y ^a   Zhou, X ^a   Crowe, D L ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

basal cells; DNA damage; keratin 15; metastasis; squamous cell carcinoma

Indexed keywords

RNA; TELOMERASE; TELOMERASE RNA;

ANIMAL; APOPTOSIS; CANCER STEM CELL; CELL LINE; CHROMOSOME; DNA DAMAGE; GENETIC RECOMBINATION; GENETICS; HUMAN; MOUSE; NEOPLASM; PATHOLOGY; TELOMERE; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING;

ANIMALS; APOPTOSIS; CELL LINE; CHROMOSOMES; DNA DAMAGE; HUMANS; MICE; NEOPLASMS; NEOPLASTIC STEM CELLS; RECOMBINATION, GENETIC; RNA; TELOMERASE; TELOMERE; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING;

EID: 84893737474     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.603     Document Type: Article

References (42)

1. Palm W, de Lange T. How shelterin protects mammalian telomeres. Ann Rev Genet 2008; 42: 301-334.
2. Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H et al. Mammalian telomeres end in a large duplex loop. Cell 1999; 97: 503-514.
3. Hemann MT, Greider CW. G strand overhangs on telomeres in telomerase deficient mouse cells. Nuc Acids Res 1999; 27: 3964-3969.
4. Martinez P, Blasco MA. Role of shelterin in cancer and aging. Aging Cell 2010; 9: 653-666.
5. Counter CM, Avilion AA, LeFeuvre CE, Stewart NG, Greider CW, Harley CB et al. Telomere shortening associate with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J 1992; 11: 1921-1929.
6. Blasco MA, Lee HW, Hande MP, Samper E, Lansdorp PM, DePinho RA et al. Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 1997; 91: 25-34.
7. Rajaraman S, Choi J, Cheung P, Beaudry V, Moore H, Artandi SE. Telomere uncapping in progenitor cells with critical telomere shortening is coupled to S phase progression in vivo. Proc Natl Acad Sci USA 2007; 104: 17747-17752.
8. Belair CD, Yeager TR, Lopez PM, Reznikoff CA. Telomerase activity: a biomarker of cell proliferation, not malignant transformation. Proc Natl Acad Sci USA 1997; 94: 13677-13682.
9. Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP, Morin GB et al. Extension of lifespan by introduction of telomerase into normal human cells. Science 1998; 279: 349-352.
10. Counter CM, Hahn WC, Wei W, Caddle SD, Beijersbergen RL, Lansdorp PM et al. Dissociation among in vitro telomerase activity, telomere maintenance, and cellular immortalization. Proc Natl Acad Sci USA 1998; 95: 14723-14728.
11. Harrington L, Zhou W, McPhail T, Oulton R, Yeung DS, Mar V et al. Human telomerase contains evolutionarily conserved catalytic and structural subunits. Genes Dev 1997; 11: 3109-3115.
12. Meyerson M, Counter CM, Eaton EN, Ellisen LW, Steiner P, Caddle SD et al. hEST2, the putative human telomerase catalytic subunit gene, is upregulated in tumor cells and during immortalization. Cell 1997; 90: 785-795.
13. Ramakrishnan S, Eppendberger U, Mueller H, Shinkai Y, Narayanan R. Expression profile of the putative catalytic subunit of the telomerase gene. Cancer Res 1998; 58: 622-625.
14. Henderson S, Allsopp R, Spector D, Wang SS, Harley C. In situ analysis of changes in telomere size during replicative aging and cell transformation. J Cell Biol 1996; 134: 1-12.
15. Wu G, Jiang X, Lee WH, Chen PL. Assembly of functional ALT associated promyelocytic leukemia bodies requires Nijmegen Breakage Syndrome 1. Cancer Res 2003; 63: 2589-2595.
16. Nabetani A, Ishikawa F. Unusual telomeric DNAs in human telomerase negative immortalized cells. Mol Cell Biol 2009; 29: 703-713.
17. Rossi DJ, Jamieson CHM, Weissman IL. Stem cells and the pathways to aging and cancer. Cell 2008; 132: 681-696.
18. Fuchs E. The tortoise and the hair: slow cycling cells in the stem cell race. Cell 2009; 137: 811-819.
19. Flores I, Canela A, Vera E, Tejera A, Cotsarelis G, Blasco MA. The longest telomeres: a general signature of adult stem cell compartments. Genes Dev 2008; 22: 654-667.
20. Morris RJ, Liu Y, Marles L, Yang Z, Trempus C, Li S et al. Capturing and profiling adult hair follicle stem cells. Nat Biotechnol 2004; 22: 411-417.
21. Fuchs E. Scratching the surface of skin development. Nature 2007; 445: 834-842.
22. Liu Y, Lyle S, Yang Z, Cotsarelis G. Keratin 15 promoter targets putative epithelial stem cells in the hair follicle bulge. J Invest Dermatol 2003; 121: 963-968.
23. Cotsarelis G. Epithelial stem cells: a folliculocentric view. J Invest Dermatol 2006; 126: 1459-1468.
24. Fuchs E. Skin stem cells: rising to the surface. J Cell Biol 2008; 180: 273-284.
25. Flores I, Cayuela ML, Blasco MA. Effects of telomerase and telomere length on epidermal stem cell behavior. Science 2005; 309: 1253-1256.
26. Sarin KY, Cheung P, Gilison D, Lee E, Tennen RI, Wang E et al. Conditional telomerase induction causes proliferation of hair follicle stem cells. Nature 2005; 436: 1048-1052.
27. Siegl-Cachedenier I, Flores I, Klatt P, Blasco MA. Telomerase reverses epidermal hair follicle stem cell defects and loss of long term survival associated with critically short telomeres. J Cell Biol 2007; 179: 277-290.
28. Harle-Bachor C, Boukamp P. Telomerase activity in the regenerative basal layer of the epidermis in human skin and in immortal and carcinoma derived skin keratinocytes. Proc Natl Acad Sci USA 1996; 93: 6476-6481.
29. Gonzalez-Suarez E, Samper E, Ramirez A, Flores JM, Martin-Caballero J, Jorcano JL et al. Increased epidermal tumors and increased skin wound healing in transgenic mice overexpressing the catalytic subunit of telomerase mTERT in basal keratinocytes. EMBO J 2001; 20: 2619-2630.
30. Crowe DL, Nguyen DC, Tsang KJ, Kyo S. E2F-1 represses transcription of the human telomerase reverse transcriptase gene. Nuc Acids Res 2001; 29: 2789-2794.
31. Kang MK, Guo W, Park NH. Replicative senescence of normal human oral keratinocytes is associated with the loss of telomerase activity without shortening of telomeres. Cell Growth Diff 1998; 9: 85-95.
32. Kang MK, Kameta A, Shin KH, Baluda MA, Park NH. Senescence occurs with hTERT repression and limited telomere shortening in human oral keratinocytes cultured with feeder cells. J Cell Physiol 2004; 199: 364-370.
33. Grobelny JV, Kulp-McEliece M, Broccoli D. Effects of reconstitution of telomerase activity on telomere maintenance by the alternative lengthening of telomeres (ALT) pathway. Hum Mol Genet 2001; 10: 1953-1961.
34. Ford LP, Zou Y, Pongracz K, Gryaznov SM, Shay JW, Wright WE. Telomerase can inhibit the recombination based pathway of telomere maintenance in human cells. J Biol Chem 2001; 276: 32198-32203.
35. Henson JD, Reddel RR. Assaying and investigating alternative lengthening of telomeres activity in human cells and cancers. FEBS Lett 2010; 584: 3800-3811.
36. Heaphy CM, Subhawong AP, Hong SM, Goggins MG, Montgomery EA, Gabrielson E et al. Prevalence of the alternative lengthening of telomeres telomere maintenance mechanism in human cancer subtypes. Am J Pathol 2011; 179: 1608-1615.
37. Wu Y, Zacal NJ, Rainbow AJ, Zhu XD. XPF with mutations in its conserved nuclease domain is defective in DNA repair but functions in TRF2 mediated telomere shortening. DNA Repair 2007; 6: 157-166.
38. van Steensel B, Smogorzewska A, de Lange T. TRF2 protects human telomeres from end to end fusions. Cell 1998; 92: 401-413.
39. Malanchi I, Peinado H, Kassen D, Hussenet T, Metzger D, Chambon P et al. Cutaneous cancer stem cell maintenance is dependent on b-catenin signaling. Nature 2008; 452: 650-653.
40. Callicott RJ, Womack JE. Real time PCR assay for measurement of mouse telomeres. Comp Med 2006; 56: 17-22.
41. Henson JD, Cao Y, Huschtscha LI, Chang AC, Au AYM, Pickett HA et al. DNA C circles are specific and quantifiable markers of alternative lengthening of telomeres activity. Nat Biotechnol 2009; 27: 1181-1186.
42. Celli GB, Lazzerini Denchi E, de Lange T. Ku70 stimulates fusion of dysfunctional telomeres yet protects chromosome ends from homologous recombination. Nat Cell Biol 2006; 8: 885-890.