Regulation of the Human Telomerase Gene TERT by Telomere Position Effect—Over Long Distances (TPE-OLD): Implications for Aging and Cancer

PLoS Biology

Volumn 14, Issue 12, 2016, Pages

  Kim, Wanil ^a   Ludlow, Andrew T ^a   Min, Jaewon ^a   Robin, Jerome D ^b   Stadler, Guido ^c   Mender, Ilgen ^a   Lai, Tsung Po ^a   Zhang, Ning ^a   Wright, Woodring E ^a   Shay, Jerry W ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c Berkeley Lights Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TELOMERASE REVERSE TRANSCRIPTASE; TELOMERIC REPEAT BINDING FACTOR 2; TELOMERASE; TERT PROTEIN, HUMAN;

AGING; ARTICLE; CELL DIVISION; CHROMATIN STRUCTURE; CHROMOSOME 5P; CONTROLLED STUDY; DNA DAMAGE; DNA METHYLATION; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; GENE STRUCTURE; GENETIC DISTANCE; GENETIC SUSCEPTIBILITY; HUMAN; LIMIT OF QUANTITATION; MALIGNANT NEOPLASM; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING; TERT GENE; ANIMAL; CHROMOSOME 5; GENE EXPRESSION REGULATION; GENETICS; NEOPLASM; PRIMATE; TELOMERE;

AGING; ANIMALS; CHROMOSOMES, HUMAN, PAIR 5; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; NEOPLASMS; PRIMATES; TELOMERASE; TELOMERE;

EID: 85009090862     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.2000016     Document Type: Article

References (51)

1. de Lange T, Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 2005;19(18):2100–10. Epub 2005/09/17. doi: 10.1101/gad.134600516166375
2. Giraud-Panis MJ, Teixeira MT, Geli V, Gilson E, CST meets shelterin to keep telomeres in check. Mol Cell. 2010;39(5):665–76. doi: 10.1016/j.molcel.2010.08.02420832719
3. Armanios M, Telomeres and age-related disease: how telomere biology informs clinical paradigms. The Journal of clinical investigation. 2013;123(3):996–1002. PubMed Central PMCID: PMC3673231. doi: 10.1172/JCI6637023454763
4. Ozturk S, Telomerase activity and telomere length in male germ cells. Biol Reprod. 2015;92(2):53. doi: 10.1095/biolreprod.114.12400825568305
5. Alder JK, Barkauskas CE, Limjunyawong N, Stanley SE, Kembou F, Tuder RM, et al. Telomere dysfunction causes alveolar stem cell failure. Proc Natl Acad Sci U S A. 2015;112(16):5099–104. PubMed Central PMCID: PMC4413294. doi: 10.1073/pnas.150478011225840590
6. Cong YS, Wright WE, Shay JW, Human telomerase and its regulation. Microbiology and molecular biology reviews: MMBR. 2002;66(3):407–25, table of contents. PubMed Central PMCID: PMC120798. doi: 10.1128/MMBR.66.3.407-425.200212208997
7. Hiyama E, Hiyama K, Telomere and telomerase in stem cells. Br J Cancer. 2007;96(7):1020–4. PubMed Central PMCID: PMC2360127. doi: 10.1038/sj.bjc.660367117353922
8. Wright WE, Piatyszek MA, Rainey WE, Byrd W, Shay JW, Telomerase activity in human germline and embryonic tissues and cells. Dev Genet. 1996;18(2):173–9. doi: 10.1002/(SICI)1520-6408(1996)18:2<173::AID-DVG10>3.0.CO;2-38934879
9. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, et al. Specific association of human telomerase activity with immortal cells and cancer. Science. 1994;266(5193):2011–5. Epub 1994/12/23. 7605428
10. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science. 2009;326(5950):289–93. PubMed Central PMCID: PMC2858594. doi: 10.1126/science.118136919815776
11. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature. 2012;485(7398):376–80. PubMed Central PMCID: PMC3356448. doi: 10.1038/nature1108222495300
12. Robin JD, Ludlow AT, Batten K, Magdinier F, Stadler G, Wagner KR, et al. Telomere position effect: regulation of gene expression with progressive telomere shortening over long distances. Genes Dev. 2014;28(22):2464–76. PubMed Central PMCID: PMC4233240. doi: 10.1101/gad.251041.11425403178
13. Robin JD, Ludlow AT, Batten K, Gaillard MC, Stadler G, Magdinier F, et al. SORBS2 transcription is activated by telomere position effect-over long distance upon telomere shortening in muscle cells from patients with facioscapulohumeral dystrophy. Genome Res. 2015.
14. Lou Z, Wei J, Riethman H, Baur JA, Voglauer R, Shay JW, et al. Telomere length regulates ISG15 expression in human cells. Aging (Albany NY). 2009;1(7):608–21. Epub 2010/02/17.
15. Baur JA, Zou Y, Shay JW, Wright WE, Telomere position effect in human cells. Science. 2001;292(5524):2075–7. doi: 10.1126/science.106232911408657
16. James MA, Wen W, Wang Y, Byers LA, Heymach JV, Coombes KR, et al. Functional characterization of CLPTM1L as a lung cancer risk candidate gene in the 5p15.33 locus. PLoS ONE. 2012;7(6):e36116. PubMed Central PMCID: PMCPMC3366984. doi: 10.1371/journal.pone.003611622675468
17. Hrdlickova R, Nehyba J, Bose HR, Jr.Alternatively spliced telomerase reverse transcriptase variants lacking telomerase activity stimulate cell proliferation. Mol Cell Biol. 2012;32(21):4283–96. PubMed Central PMCID: PMC3486134. doi: 10.1128/MCB.00550-1222907755
18. Arnoult N, Van Beneden A, Decottignies A, Telomere length regulates TERRA levels through increased trimethylation of telomeric H3K9 and HP1alpha. Nat Struct Mol Biol. 2012;19(9):948–56. doi: 10.1038/nsmb.236422922742
19. Balk B, Maicher A, Dees M, Klermund J, Luke-Glaser S, Bender K, et al. Telomeric RNA-DNA hybrids affect telomere-length dynamics and senescence. Nat Struct Mol Biol. 2013;20(10):1199–205. doi: 10.1038/nsmb.266224013207
20. Mathon NF, Malcolm DS, Harrisingh MC, Cheng L, Lloyd AC, Lack of replicative senescence in normal rodent glia. Science. 2001;291(5505):872–5. doi: 10.1126/science.105678211157166
21. Horikawa I, Chiang YJ, Patterson T, Feigenbaum L, Leem SH, Michishita E, et al. Differential cis-regulation of human versus mouse TERT gene expression in vivo: identification of a human-specific repressive element. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(51):18437–42. PubMed Central PMCID: PMC1317953. doi: 10.1073/pnas.050896410216344462
22. Wong MS, Chen L, Foster C, Kainthla R, Shay JW, Wright WE, Regulation of telomerase alternative splicing: a target for chemotherapy. Cell Rep. 2013;3(4):1028–35. PubMed Central PMCID: PMC3640656. doi: 10.1016/j.celrep.2013.03.01123562158
23. Wong MS, Shay JW, Wright WE, Regulation of human telomerase splicing by RNA:RNA pairing. Nature communications. 2014;5:3306. PubMed Central PMCID: PMC3948165. doi: 10.1038/ncomms430624577044
24. Wong MS, Wright WE, Shay JW, Alternative splicing regulation of telomerase: a new paradigm?Trends Genet. 2014;30(10):430–8. doi: 10.1016/j.tig.2014.07.00625172021
25. Bell RJ, Rube HT, Kreig A, Mancini A, Fouse SF, Nagarajan RP, et al. The transcription factor GABP selectively binds and activates the mutant TERT promoter in cancer. Science. 2015.
26. Walker EJ, Zhang C, Castelo-Branco P, Hawkins C, Wilson W, Zhukova N, et al. Monoallelic expression determines oncogenic progression and outcome in benign and malignant brain tumors. Cancer Res. 2012;72(3):636–44. doi: 10.1158/0008-5472.CAN-11-226622144470
27. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E, A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337(6096):816–21. doi: 10.1126/science.122582922745249
28. Srivastava M, Nambiar M, Sharma S, Karki SS, Goldsmith G, Hegde M, et al. An inhibitor of nonhomologous end-joining abrogates double-strand break repair and impedes cancer progression. Cell. 2012;151(7):1474–87. doi: 10.1016/j.cell.2012.11.05423260137
29. Stadler G, Rahimov F, King OD, Chen JC, Robin JD, Wagner KR, et al. Telomere position effect regulates DUX4 in human facioscapulohumeral muscular dystrophy. Nat Struct Mol Biol. 2013;20(6):671–8. PubMed Central PMCID: PMC3711615. doi: 10.1038/nsmb.257123644600
30. Cong YS, Wen J, Bacchetti S, The human telomerase catalytic subunit hTERT: organization of the gene and characterization of the promoter. Hum Mol Genet. 1999;8(1):137–42. 9887342
31. Bechter OE, Eisterer W, Dlaska M, Kuhr T, Thaler J, CpG island methylation of the hTERT promoter is associated with lower telomerase activity in B-cell lymphocytic leukemia. Exp Hematol. 2002;30(1):26–33. 11823034
32. Guilleret I, Yan P, Grange F, Braunschweig R, Bosman FT, Benhattar J, Hypermethylation of the human telomerase catalytic subunit (hTERT) gene correlates with telomerase activity. Int J Cancer. 2002;101(4):335–41. doi: 10.1002/ijc.1059312209957
33. Zinn RL, Pruitt K, Eguchi S, Baylin SB, Herman JG, hTERT is expressed in cancer cell lines despite promoter DNA methylation by preservation of unmethylated DNA and active chromatin around the transcription start site. Cancer Res. 2007;67(1):194–201. doi: 10.1158/0008-5472.CAN-06-339617210699
34. Renaud S, Bosman FT, Benhattar J, Implication of the exon region in the regulation of the human telomerase reverse transcriptase gene promoter. Biochem Biophys Res Commun. 2003;300(1):47–54. 12480519
35. Renaud S, Loukinov D, Alberti L, Vostrov A, Kwon YW, Bosman FT, et al. BORIS/CTCFL-mediated transcriptional regulation of the hTERT telomerase gene in testicular and ovarian tumor cells. Nucleic Acids Res. 2011;39(3):862–73. PubMed Central PMCID: PMC3035453. doi: 10.1093/nar/gkq82720876690
36. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature. 2007;448(7153):553–60. PubMed Central PMCID: PMCPMC2921165. doi: 10.1038/nature0600817603471
37. Shats I, Milyavsky M, Tang X, Stambolsky P, Erez N, Brosh R, et al. p53-dependent down-regulation of telomerase is mediated by p21waf1. J Biol Chem. 2004;279(49):50976–85. doi: 10.1074/jbc.M40250220015371422
38. Withers JB, Ashvetiya T, Beemon KL, Exclusion of exon 2 is a common mRNA splice variant of primate telomerase reverse transcriptases. PLoS ONE. 2012;7(10):e48016. PubMed Central PMCID: PMCPMC3480478. doi: 10.1371/journal.pone.004801623110161
39. Wood AM, Rendtlew Danielsen JM, Lucas CA, Rice EL, Scalzo D, Shimi T, et al. TRF2 and lamin A/C interact to facilitate the functional organization of chromosome ends. Nature communications. 2014;5:5467. PubMed Central PMCID: PMC4235626. doi: 10.1038/ncomms646725399868
40. Simonet T, Zaragosi LE, Philippe C, Lebrigand K, Schouteden C, Augereau A, et al. The human TTAGGG repeat factors 1 and 2 bind to a subset of interstitial telomeric sequences and satellite repeats. Cell Res. 2011;21(7):1028–38. PubMed Central PMCID: PMCPMC3193489. doi: 10.1038/cr.2011.4021423270
41. Ye J, Renault VM, Jamet K, Gilson E, Transcriptional outcome of telomere signalling. Nat Rev Genet. 2014;15(7):491–503. doi: 10.1038/nrg374324913665
42. Deng W, Lee J, Wang H, Miller J, Reik A, Gregory PD, et al. Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor. Cell. 2012;149(6):1233–44. PubMed Central PMCID: PMCPMC3372860. doi: 10.1016/j.cell.2012.03.05122682246
43. Zhang H, Niu B, Hu JF, Ge S, Wang H, Li T, et al. Interruption of intrachromosomal looping by CCCTC binding factor decoy proteins abrogates genomic imprinting of human insulin-like growth factor II. J Cell Biol. 2011;193(3):475–87. PubMed Central PMCID: PMCPMC3087012. doi: 10.1083/jcb.20110102121536749
44. Hastie ND, Dempster M, Dunlop MG, Thompson AM, Green DK, Allshire RC, Telomere reduction in human colorectal carcinoma and with ageing. Nature. 1990;346(6287):866–8. doi: 10.1038/346866a02392154
45. Jia W, Wang S, Horner JW, Wang N, Wang H, Gunther EJ, et al. A BAC transgenic reporter recapitulates in vivo regulation of human telomerase reverse transcriptase in development and tumorigenesis. FASEB J. 2011;25(3):979–89. PubMed Central PMCID: PMC3042838. doi: 10.1096/fj.10-17398921135040
46. Zhu J, Zhao Y, Wang S, Chromatin and epigenetic regulation of the telomerase reverse transcriptase gene. Protein Cell. 2010;1(1):22–32. PubMed Central PMCID: PMCPMC3683535. doi: 10.1007/s13238-010-0014-121203995
47. Zhao Y, Wang S, Popova EY, Grigoryev SA, Zhu J, Rearrangement of upstream sequences of the hTERT gene during cellular immortalization. Genes Chromosomes Cancer. 2009;48(11):963–74. PubMed Central PMCID: PMC2889911. doi: 10.1002/gcc.2069819672873
48. Peifer M, Hertwig F, Roels F, Dreidax D, Gartlgruber M, Menon R, et al. Telomerase activation by genomic rearrangements in high-risk neuroblastoma. Nature. 2015;526(7575):700–4. doi: 10.1038/nature1498026466568
49. Ludlow AT, Robin JD, Sayed M, Litterst CM, Shelton DN, Shay JW, et al. Quantitative telomerase enzyme activity determination using droplet digital PCR with single cell resolution. Nucleic Acids Res. 2014;42(13):e104. PubMed Central PMCID: PMC4117742. doi: 10.1093/nar/gku43924861623
50. Zhao Y, Sfeir AJ, Zou Y, Buseman CM, Chow TT, Shay JW, et al. Telomere extension occurs at most chromosome ends and is uncoupled from fill-in in human cancer cells. Cell. 2009;138(3):463–75. PubMed Central PMCID: PMCPMC2726829. doi: 10.1016/j.cell.2009.05.02619665970
51. Lai TP, Wright WE, Shay JW, Generation of digoxigenin-incorporated probes to enhance DNA detection sensitivity. Biotechniques. 2016;60(6):306–9. doi: 10.2144/00011442727286808