Postnatal telomere dysfunction induces cardiomyocyte cell-cycle arrest through p21 activation

Journal of Cell Biology

Volumn 213, Issue 5, 2016, Pages 571-583

  Aix, Esther ^a   Gutiérrez Gutiérrez, Óscar ^a   Sánchez Ferrer, Carlota ^a   Aguado, Tania ^a   Flores, Ignacio ^a  

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P21; TELOMERASE; CYCLIN DEPENDENT KINASE INHIBITOR 1A;

ANAPHASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARDIAC MUSCLE CELL; CELL CYCLE ARREST; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; ENZYME ACTIVITY; HEART INJURY; INTRACELLULAR SIGNALING; MAMMAL; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; TELOMERE; UPREGULATION; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; CELL CYCLE CHECKPOINT; CYTOLOGY; DNA DAMAGE; DNA REPAIR; METABOLISM; TELOMERE HOMEOSTASIS;

ANAPHASE; ANIMALS; ANIMALS, NEWBORN; CELL CYCLE CHECKPOINTS; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA DAMAGE; DNA REPAIR; MICE, INBRED C57BL; MODELS, BIOLOGICAL; MYOCYTES, CARDIAC; TELOMERASE; TELOMERE; TELOMERE HOMEOSTASIS;

EID: 84975217547     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201510091     Document Type: Article

References (76)

1. Artandi, S.E., and L.D. Attardi. 2005. Pathways connecting telomeres and p53 in senescence, apoptosis, and cancer. Biochem. Biophys. Res. Commun. 331:881-890. http://dx.doi.org/10.1016/j.bbrc.2005.03.211
2. Baker, D.J., R.L. Weaver, and J.M. van Deursen. 2013. p21 both attenuates and drives senescence and aging in BubR1 progeroid mice. Cell Reports. 3:1164-1174. http://dx.doi.org/10.1016/j.celrep.2013.03.028
3. Bär, C., B. Bernardes de Jesus, R. Serrano, A. Tejera, E. Ayuso, V. Jimenez, I. Formentini, M. Bobadilla, J. Mizrahi, A. de Martino, et al. 2014. Telomerase expression confers cardioprotection in the adult mouse heart after acute myocardial infarction. Nat. Commun. 5:5863. http://dx.doi.org/10.1038/ncomms6863
4. Basel-Vanagaite, L., I. Dokal, H. Tamary, A. Avigdor, B.Z. Garty, A. Volkov, and T. Vulliamy. 2008. Expanding the clinical phenotype of autosomal dominant dyskeratosis congenita caused by TERT mutations. Haematologica. 93:943-944. http://dx.doi.org/10.3324/haematol.12317
5. Bednarek, D., J.M. González-Rosa, G. Guzmán-Martínez, Ó. Gutiérrez-Gutiérrez, T. Aguado, C. Sánchez-Ferrer, I.J. Marques, M. Galardi-Castilla, I. de Diego, M.J. Gómez, et al. 2015. Telomerase is essential for Zebrafish heart regeneration. Cell Reports. 12:1691-1703. http://dx.doi.org/10.1016/j.celrep.2015.07.064
6. Begus-Nahrmann, Y., A. Lechel, A.C. Obenauf, K. Nalapareddy, E. Peit, E. Hoffmann, F. Schlaudraff, B. Liss, P. Schirmacher, H. Kestler, et al. 2009. p53 deletion impairs clearance of chromosomal-instable stem cells in aging telomere-dysfunctional mice. Nat. Genet. 41:1138-1143. http://dx.doi.org/10.1038/ng.426
7. Bergmann, O., R.D. Bhardwaj, S. Bernard, S. Zdunek, F. Barnabé-Heider, S. Walsh, J. Zupicich, K. Alkass, B.A. Buchholz, H. Druid, et al. 2009. Evidence for cardiomyocyte renewal in humans. Science. 324:98-102. http://dx.doi.org/10.1126/science.1164680
8. Bergmann, O., S. Zdunek, A. Felker, M. Salehpour, K. Alkass, S. Bernard, S.L. Sjostrom, M. Szewczykowska, T. Jackowska, C. Dos Remedios, et al. 2015. Dynamics of cell generation and turnover in the human heart. Cell. 161:1566-1575. http://dx.doi.org/10.1016/j.cell.2015.05.026
9. Blasco, M.A., H.W. Lee, M.P. Hande, E. Samper, P.M. Lansdorp, R.A. DePinho, and C.W. Greider. 1997. Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell. 91:25-34. http://dx.doi.org/10.1016/S0092-8674(01)80006-4
10. Boon, R.A., K. Iekushi, S. Lechner, T. Seeger, A. Fischer, S. Heydt, D. Kaluza, K. Tréguer, G. Carmona, A. Bonauer, et al. 2013. MicroRNA-34a regulates cardiac ageing and function. Nature. 495:107-110. http://dx.doi.org/10.1038/nature11919
11. Borges, A., and C.C. Liew. 1997. Telomerase activity during cardiac development. J. Mol. Cell. Cardiol. 29:2717-2724. http://dx.doi.org/10.1006/jmcc.1997.0503
12. Brugarolas, J., C. Chandrasekaran, J.I. Gordon, D. Beach, T. Jacks, and G.J. Hannon. 1995. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature. 377:552-557. http://dx.doi.org/10.1038/377552a0
13. Chan, S.W., and E.H. Blackburn. 2002. New ways not to make ends meet: telomerase, DNA damage proteins and heterochromatin. Oncogene. 21:553-563. http://dx.doi.org/10.1038/sj.onc.1205082
14. Choudhury, A.R., Z. Ju, M.W. Djojosubroto, A. Schienke, A. Lechel, S. Schaetzlein, H. Jiang, A. Stepczynska, C. Wang, J. Buer, et al. 2007. Cdkn1a deletion improves stem cell function and lifespan of mice with dysfunctional telomeres without accelerating cancer formation. Nat. Genet. 39:99-105. http://dx.doi.org/10.1038/ng1937
15. d'Adda di Fagagna, F., P.M. Reaper, L. Clay-Farrace, H. Fiegler, P. Carr, T. Von Zglinicki, G. Saretzki, N.P. Carter, and S.P. Jackson. 2003. A DNA damage checkpoint response in telomere-initiated senescence. Nature. 426:194-198. http://dx.doi.org/10.1038/nature02118
16. Daniali, L., A. Benetos, E. Susser, J.D. Kark, C. Labat, M. Kimura, K. Desai, M. Granick, and A. Aviv. 2013. Telomeres shorten at equivalent rates in somatic tissues of adults. Nat. Commun. 4:1597. http://dx.doi.org/10.1038/ncomms2602
17. Davoli, T., and T. de Lange. 2011. The causes and consequences of polyploidy in normal development and cancer. Annu. Rev. Cell Dev. Biol. 27:585-610. http://dx.doi.org/10.1146/annurev-cellbio-092910-154234
18. de Lange, T. 2002. Protection of mammalian telomeres. Oncogene. 21:532-540. http://dx.doi.org/10.1038/sj.onc.1205080
19. de Lange, T. 2005. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19:2100-2110. http://dx.doi.org/10.1101/gad.1346005
20. Ding, H., F. Yan, L.L. Zhou, X.H. Ji, X.N. Gu, Z.W. Tang, and R.H. Chen. 2014. Association between previously identified loci affecting telomere length and coronary heart disease (CHD) in Han Chinese population. Clin. Interv. Aging. 9:857-861. http://dx.doi.org/10.2147/CIA.S60760
21. Drenckhahn, J.D., Q.P. Schwarz, S. Gray, A. Laskowski, H. Kiriazis, Z. Ming, R.P. Harvey, X.J. Du, D.R. Thorburn, and T.C. Cox. 2008. Compensatory growth of healthy cardiac cells in the presence of diseased cells restores tissue homeostasis during heart development. Dev. Cell. 15:521-533. http://dx.doi.org/10.1016/j.devcel.2008.09.005
22. Engel, F.B., M. Schebesta, and M.T. Keating. 2006. Anillin localization defect in cardiomyocyte binucleation. J. Mol. Cell. Cardiol. 41:601-612. http://dx.doi.org/10.1016/j.yjmcc.2006.06.012
23. Flores, I., A. Canela, E. Vera, A. Tejera, G. Cotsarelis, and M.A. Blasco. 2008. The longest telomeres: a general signature of adult stem cell compartments. Genes Dev. 22:654-667. http://dx.doi.org/10.1101/gad.451008
24. Goffart, S., J.C. von Kleist-Retzow, and R.J. Wiesner. 2004. Regulation of mitochondrial proliferation in the heart: power-plant failure contributes to cardiac failure in hypertrophy. Cardiovasc. Res. 64:198-207. http://dx.doi.org/10.1016/j.cardiores.2004.06.030
25. González-Suárez, E., E. Samper, J.M. Flores, and M.A. Blasco. 2000. Telomerase-deficient mice with short telomeres are resistant to skin tumorigenesis. Nat. Genet. 26:114-117. http://dx.doi.org/10.1038/79089
26. Greider, C.W., and E.H. Blackburn. 1985. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell. 43:405-413. http://dx.doi.org/10.1016/0092-8674(85)90170-9
27. Greider, C.W., and E.H. Blackburn. 1987. The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity. Cell. 51:887-898. http://dx.doi.org/10.1016/0092-8674(87)90576-9
28. Greider, C.W., and E.H. Blackburn. 1989. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature. 337:331-337. http://dx.doi.org/10.1038/337331a0
29. Harley, C.B. 1991. Telomere loss: mitotic clock or genetic time bomb? Mutat. Res. 256:271-282. http://dx.doi.org/10.1016/0921-8734(91)90018-7
30. Harrington, L. 2004. Does the reservoir for self-renewal stem from the ends? Oncogene. 23:7283-7289. http://dx.doi.org/10.1038/sj.onc.1207948
31. Haubner, B.J., J. Schneider, U. Schweigmann, T. Schuetz, W. Dichtl, C. Velik-Salchner, J.-I. Stein, and J.M. Penninger. 2016. Functional recovery of a human neonatal heart after severe myocardial infarction. Circ. Res. 118:216-221. http://dx.doi.org/10.1161/CIR CRE SAHA.115.307017
32. Herbert, B.S., A.E. Hochreiter, W.E. Wright, and J.W. Shay. 2006. Nonradioactive detection of telomerase activity using the telomeric repeat amplification protocol. Nat. Protoc. 1:1583-1590. http://dx.doi.org/10.1038/nprot.2006.239
33. Herrera, E., E. Samper, J. Martín-Caballero, J.M. Flores, H.W. Lee, and M.A. Blasco. 1999. Disease states associated with telomerase deficiency appear earlier in mice with short telomeres. EMBO J. 18:2950-2960. http://dx.doi.org/10.1093/emboj/18.11.2950
34. Hoffelder, D.R., L. Luo, N.A. Burke, S.C. Watkins, S.M. Gollin, and W.S. Saunders. 2004. Resolution of anaphase bridges in cancer cells. Chromosoma. 112:389-397. http://dx.doi.org/10.1007/s00412-004-0284-6
35. Ikenishi, A., H. Okayama, N. Iwamoto, S. Yoshitome, S. Tane, K. Nakamura, T. Obayashi, T. Hayashi, and T. Takeuchi. 2012. Cell cycle regulation in mouse heart during embryonic and postnatal stages. Dev. Growth Differ. 54:731-738. http://dx.doi.org/10.1111/j.1440-169X.2012.01373.x
36. Ju, Z., A.R. Choudhury, and K.L. Rudolph. 2007. A dual role of p21 in stem cell aging. Ann. N. Y. Acad. Sci. 1100:333-344. http://dx.doi.org/10.1196/annals.1395.036
37. Kikuchi, K., and K.D. Poss. 2012. Cardiac regenerative capacity and mechanisms. Annu. Rev. Cell Dev. Biol. 28:719-741. http://dx.doi.org/10.1146/annurev-cellbio-101011-155739
38. Lansdorp, P.M. 2005. Role of telomerase in hematopoietic stem cells. Ann. N. Y. Acad. Sci. 1044:220-227. http://dx.doi.org/10.1196/annals.1349.027
39. Lansdorp, P.M., N.P. Verwoerd, F.M. van de Rijke, V. Dragowska, M.T. Little, R.W. Dirks, A.K. Raap, and H.J. Tanke. 1996. Heterogeneity in telomere length of human chromosomes. Hum. Mol. Genet. 5:685-691. http://dx.doi.org/10.1093/hmg/5.5.685
40. Leri, A., L. Barlucchi, F. Limana, A. Deptala, Z. Darzynkiewicz, T.H. Hintze, J. Kajstura, B. Nadal-Ginard, and P. Anversa. 2001. Telomerase expression and activity are coupled with myocyte proliferation and preservation of telomeric length in the failing heart. Proc. Natl. Acad. Sci. USA. 98:8626-8631. http://dx.doi.org/10.1073/pnas.151013298
41. Leri, A., S. Franco, A. Zacheo, L. Barlucchi, S. Chimenti, F. Limana, B. Nadal-Ginard, J. Kajstura, P. Anversa, and M.A. Blasco. 2003. Ablation of telomerase and telomere loss leads to cardiac dilatation and heart failure associated with p53 upregulation. EMBO J. 22:131-139. http://dx.doi.org/10.1093/emboj/cdg013
42. Liu, D., M.S. O'Connor, J. Qin, and Z. Songyang. 2004. Telosome, a mammalian telomere-associated complex formed by multiple telomeric proteins. J. Biol. Chem. 279:51338-51342. http://dx.doi.org/10.1074/jbc.M409293200
43. Margolis, R.L., O.D. Lohez, and P.R. Andreassen. 2003. G1 tetraploidy checkpoint and the suppression of tumorigenesis. J. Cell. Biochem. 88:673-683. http://dx.doi.org/10.1002/jcb.10411
44. Martin, M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal. 17:10-12. http://dx.doi.org/10.14806/ej.17.1.200
45. Maubaret, C.G., K.D. Salpea, C.E. Romanoski, L. Folkersen, J.A. Cooper, C. Stephanou, K.W. Li, J. Palmen, A. Hamsten, A. Neil, et al. EAR SII consortium. 2013. Association of TERC and OBFC1 haplotypes with mean leukocyte telomere length and risk for coronary heart disease. PLoS One. 8:e83122. http://dx.doi.org/10.1371/journal.pone.0083122
46. McClintock, B. 1939. The behavior in successive nuclear divisions of a chromosome broken at meiosis. Proc. Natl. Acad. Sci. USA. 25:405-416. http://dx.doi.org/10.1073/pnas.25.8.405
47. McClintock, B. 1941. The stability of broken ends of chromosomes in Zea mays. Genetics. 26:234-282.
48. Mollova, M., K. Bersell, S. Walsh, J. Savla, L.T. Das, S.Y. Park, L.E. Silberstein, C.G. Dos Remedios, D. Graham, S. Colan, and B. Kühn. 2013. Cardiomyocyte proliferation contributes to heart growth in young humans. Proc. Natl. Acad. Sci. USA. 110:1446-1451. http://dx.doi.org/10.1073/pnas.1214608110
49. Muller, H.J. 1938. The remaking of chromosomes. Collecting Net. 13:181-198.
50. Muralidhar, S.A., A.I. Mahmoud, D. Canseco, F. Xiao, and H.A. Sadek. 2013. Harnessing the power of dividing cardiomyocytes. Glob. Cardiol. Sci. Pract. 2013:212-221. http://dx.doi.org/10.5339/gcsp.2013.29
51. Murnane, J.P. 2012. Telomere dysfunction and chromosome instability. Mutat. Res. 730:28-36. http://dx.doi.org/10.1016/j.mrfmmm.2011.04.008
52. Oh, H., G.E. Taffet, K.A. Youker, M.L. Entman, P.A. Overbeek, L.H. Michael, and M.D. Schneider. 2001. Telomerase reverse transcriptase promotes cardiac muscle cell proliferation, hypertrophy, and survival. Proc. Natl. Acad. Sci. USA. 98:10308-10313. http://dx.doi.org/10.1073/pnas.191169098
53. Olovnikov, A.M. 1973. A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J. Theor. Biol. 41:181-190. http://dx.doi.org/10.1016/0022-5193(73)90198-7
54. Pampalona, J., C. Frías, A. Genescà, and L. Tusell. 2012. Progressive telomere dysfunction causes cytokinesis failure and leads to the accumulation of polyploid cells. PLoS Genet. 8:e1002679. http://dx.doi.org/10.1371/journal.pgen.1002679
55. Porrello, E.R., and E.N. Olson. 2014. A neonatal blueprint for cardiac regeneration. Stem Cell Res. (Amst.). 13:556-570. http://dx.doi.org/10.1016/j.scr.2014.06.003
56. Porrello, E.R., A.I. Mahmoud, E. Simpson, J.A. Hill, J.A. Richardson, E.N. Olson, and H.A. Sadek. 2011. Transient regenerative potential of the neonatal mouse heart. Science. 331:1078-1080. http://dx.doi.org/10.1126/science.1200708
57. Porrello, E.R., A.I. Mahmoud, E. Simpson, B.A. Johnson, D. Grinsfelder, D. Canseco, P.P. Mammen, B.A. Rothermel, E.N. Olson, and H.A. Sadek. 2013. Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family. Proc. Natl. Acad. Sci. USA. 110:187-192. http://dx.doi.org/10.1073/pnas.1208863110
58. Puente, B.N., W. Kimura, S.A. Muralidhar, J. Moon, J.F. Amatruda, K.L. Phelps, D. Grinsfelder, B.A. Rothermel, R. Chen, J.A. Garcia, et al. 2014. The oxygen-rich postnatal environment induces cardiomyocyte cell-cycle arrest through DNA damage response. Cell. 157:565-579. http://dx.doi.org/10.1016/j.cell.2014.03.032
59. Quaife-Ryan, G.A., C.B. Sim, E.R. Porrello, and J.E. Hudson. 2016. Resetting the epigenome for heart regeneration. Semin. Cell Dev. Biol. http://dx.doi.org/10.1016/j.semcdb.2015.12.021
60. Rabinowitz, M., and R. Zak. 1975. Mitochondria and cardiac hypertrophy. Circ. Res. 36:367-376. http://dx.doi.org/10.1161/01.RES.36.3.367
61. Ramirez, R.D., W.E. Wright, J.W. Shay, and R.S. Taylor. 1997. Telomerase activity concentrates in the mitotically active segments of human hair follicles. J. Invest. Dermatol. 108:113-117. http://dx.doi.org/10.1111/1523-1747.ep12285654
62. Richardson, G.D., D. Breault, G. Horrocks, S. Cormack, N. Hole, and W.A. Owens. 2012. Telomerase expression in the mammalian heart. FAS EB J. 26:4832-4840. http://dx.doi.org/10.1096/fj.12-208843
63. Robinson, M.D., D.J. McCarthy, and G.K. Smyth. 2010. edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 26:139-140. http://dx.doi.org/10.1093/bioinformatics/btp616
64. Saretzki, G., and T. Von Zglinicki. 2002. Replicative aging, telomeres, and oxidative stress. Ann. N. Y. Acad. Sci. 959:24-29. http://dx.doi.org/10.1111/j.1749-6632.2002.tb02079.x
65. Senyo, S.E., R.T. Lee, and B. Kühn. 2014. Cardiac regeneration based on mechanisms of cardiomyocyte proliferation and differentiation. Stem Cell Res. (Amst.). 13:532-541. http://dx.doi.org/10.1016/j.scr.2014.09.003
66. Shimizu, N., K. Shingaki, Y. Kaneko-Sasaguri, T. Hashizume, and T. Kanda. 2005. When, where and how the bridge breaks: anaphase bridge breakage plays a crucial role in gene amplification and HSR generation. Exp. Cell Res. 302:233-243. http://dx.doi.org/10.1016/j.yexcr.2004.09.001
67. Soonpaa, M.H., G.Y. Koh, M.G. Klug, and L.J. Field. 1994. Formation of nascent intercalated disks between grafted fetal cardiomyocytes and host myocardium. Science. 264:98-101. http://dx.doi.org/10.1126/science.8140423
68. Soonpaa, M.H., K.K. Kim, L. Pajak, M. Franklin, and L.J. Field. 1996. Cardiomyocyte DNA synthesis and binucleation during murine development. Am. J. Physiol. 271:H2183-H2189.
69. Takeuchi, T. 2014. Regulation of cardiomyocyte proliferation during development and regeneration. Dev. Growth Differ. 56:402-409. http://dx.doi.org/10.1111/dgd.12134
70. Tane, S., A. Ikenishi, H. Okayama, N. Iwamoto, K.I. Nakayama, and T. Takeuchi. 2014. CDK inhibitors, p21(Cip1) and p27(Kip1), participate in cell cycle exit of mammalian cardiomyocytes. Biochem. Biophys. Res. Commun. 443:1105-1109. http://dx.doi.org/10.1016/j.bbrc.2013.12.109
71. von Zglinicki, T. 2002. Oxidative stress shortens telomeres. Trends Biochem. Sci. 27:339-344. http://dx.doi.org/10.1016/S0968-0004(02)02110-2
72. Vousden, K.H., and C. Prives. 2009. Blinded by the light: The growing complexity of p53. Cell. 137:413-431. http://dx.doi.org/10.1016/j.cell.2009.04.037
73. Vulliamy, T., A. Marrone, R. Szydlo, A. Walne, P.J. Mason, and I. Dokal. 2004. Disease anticipation is associated with progressive telomere shortening in families with dyskeratosis congenita due to mutations in TERC. Nat. Genet. 36:447-449. http://dx.doi.org/10.1038/ng1346
74. Watson, J.D. 1972. Origin of concatemeric T7 DNA. Nat. New Biol. 239:197-201. http://dx.doi.org/10.1038/newbio239197a0
75. Wright, W.E., M.A. Piatyszek, W.E. Rainey, W. Byrd, and J.W. Shay. 1996. Telomerase activity in human germline and embryonic tissues and cells. Dev. Genet. 18:173-179. http://dx.doi.org/10.1002/(SICI)1520-6408(1996)18 :2<173::AID-DVG10>3.0.CO;2-3
76. Zijlmans, J.M., U.M. Martens, S.S. Poon, A.K. Raap, H.J. Tanke, R.K. Ward, and P.M. Lansdorp. 1997. Telomeres in the mouse have large interchromosomal variations in the number of T2AG3 repeats. Proc. Natl. Acad. Sci. USA. 94:7423-7428. http://dx.doi.org/10.1073/pnas.94.14.7423