Telomere homeostasis is compromised in spermatocytes from patients with idiopathic infertility

Fertility and Sterility

Volumn 102, Issue 3, 2014, Pages

  Reig Viader, Rita ^a   Capilla, Laia ^a   Vila Cejudo, Marta ^a   Garcia, Ferrán ^b   Anguita, Begoña ^b   Garcia Caldés, Montserrat ^a   Ruiz Herrera, Aurora ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b Fecunmed   (Spain)

Author keywords

infertility; meiosis; recombination; spermatocytes; telomerase; telomeres; TERRA

Indexed keywords

PROTEIN; RNA; TELOMERASE; TELOMERIC REPEAT CONTAINING RNA; UNCLASSIFIED DRUG;

ARTICLE; CHROMOSOME SIZE; CHROMOSOME STRUCTURE; CLINICAL ARTICLE; CONTROLLED STUDY; FLUORESCENCE IN SITU HYBRIDIZATION; GERM CELL; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IDIOPATHIC DISEASE; IMMUNOFLUORESCENCE MICROSCOPY; MALE; MALE INFERTILITY; MEIOTIC RECOMBINATION; PRIORITY JOURNAL; SPERMATOCYTE; TELOMERE; TELOMERE HOMEOSTASIS; TESTIS BIOPSY; TESTIS CELL;

INFERTILITY; MEIOSIS; RECOMBINATION; SPERMATOCYTES; TELOMERASE; TELOMERES; TERRA;

CASE-CONTROL STUDIES; CELL NUCLEUS; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; INFERTILITY, MALE; MALE; RECOMBINATION, GENETIC; SPERMATOCYTES; TELOMERASE; TELOMERE; TELOMERE HOMEOSTASIS; TRANSCRIPTION FACTORS;

EID: 84906940691     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2014.06.005     Document Type: Article

References (89)

1. M.A. Handel, and J.C. Schimenti Genetics of mammalian meiosis: regulation, dynamics and impact on fertility Nat Rev Genet 11 2010 124 136
2. S.Z. Jan, G. Hamer, S. Repping, D.G. de Rooij, A.M. van Pelt, and T.L. Vormer Molecular control of rodent spermatogenesis Biochim Biophys Acta 1822 2012 1838 1850
3. F. Sánchez, and J. Smitz Molecular control of oogenesis Biochim Biophys Acta 1822 2012 1896 1912
4. A. Waclawska, and M. Kurpisz Key functional genes of spermatogenesis identified by microarray analysis Syst Biol Reprod Med 58 2012 229 235
5. R. Li, and D.F. Albertini The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte Nat Rev Mol Cell Biol 14 2013 141 152
6. A.J. Wilcox, C.R. Weinberg, and D.D. Baird Timing of sexual intercourse in relation to ovulation. Effects on the probability of conception, survival of the pregnancy, and sex of the baby N Engl J Med 333 1995 1517 1521
7. A. Jungwirth, T. Diemer, G.R. Dohle, A. Giwercman, Z. Kopa, and H. Torunaye et al. Guidelines on male infertility Male Infertility - European Association of Urology 2013 Available at: http://www.uroweb.org/. Last accessed June 26, 2014
8. B. Lunenfeld, and A. van Steirteghem Bertarelli Foundation. Infertility in the third millennium: implications for the individual, family and society: condensed meeting report from the Bertarelli Foundation's second global conference Hum Reprod Update 10 2004 317 326
9. M.N. Mascarenhas, S.R. Flaxman, T. Boerma, S. Vanderpoel, and G.A. Stevens National, regional, and global trends in infertility prevalence since 1990: a systematic analysis of 277 health surveys PLoS Med 9 2012 e1001356
10. S.J. Silber, and N. Barbey Scientific molecular basis for treatment of reproductive failure in the human: an insight into the future Biochim Biophys Acta 2012 1822 1981 1996
11. M.A. Morelli, and P.E. Cohen Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis Reproduction 130 2005 761 781
12. W. Edelmann, P.E. Cohen, M. Kane, K. Lau, B. Morrow, and S. Bennett et al. Meiotic pachytene arrest in MLH1-deficient mice Cell 85 1996 1125 1134
13. L.M. Woods, C.A. Hodges, E. Baart, S.M. Baker, M. Liskay, and P.A. Hunt Chromosomal influence on meiotic spindle assembly: abnormal meiosis I in female Mlh1 mutant mice J Cell Biol 145 1999 1395 1406
14. L. Yuan, J.G. Liu, J. Zhao, E. Brundell, B. Daneholt, and C. Höög The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility Mol Cell 5 2000 73 83
15. A. Celeste, S. Petersen, P.J. Romanienko, O. Fernandez-Capetillo, H.T. Chen, and O.A. Sedelnikova et al. Genomic instability in mice lacking histone H2AX Science 296 2002 922 927
16. L. Yuan, J.G. Liu, M.R. Hoja, J. Wilbertz, K. Nordqvist, and C. Höög Female germ cell aneuploidy and embryo death in mice lacking the meiosis-specific protein SCP3 Science 296 2002 1115 1118
17. P.A. Hunt, and T.J. Hassold Human female meiosis: what makes a good egg go bad? Trends Genet 24 2008 86 93
18. S.I. Nagaoka, T.J. Hassold, and P.A. Hunt Human aneuploidy: mechanisms and new insights into an age-old problem Nat Rev Genet 13 2012 493 504
19. J. Gonsalves, F. Sun, P.N. Schlegel, P.J. Turek, C.V. Hopps, and C. Greene et al. Defective recombination in infertile men Hum Mol Genet 13 2004 2875 2883
20. M. Codina-Pascual, M. Oliver-Bonet, J. Navarro, M. Campillo, F. García, and S. Egozcue et al. Synapsis and meiotic recombination analyses: MLH1 focus in the XY pair as an indicator Hum Reprod 20 2005 2133 2139
21. I. Roig, P. Robles, R. Garcia, I. Martinez-Flores, L. Cabero, and J. Egozcue et al. Chromosome 18 pairing behavior in human trisomic oocytes. Presence of an extra chromosome extends bouquet stage Reproduction 129 2005 565 575
22. F. Sun, C. Greene, P.J. Turek, E. Ko, A. Rademaker, and R.H. Martin Immunofluorescent synaptonemal complex analysis in azoospermic men Cytogenet Genome Res 111 2005 366 370
23. F. Sun, P. Turek, C. Greene, E. Ko, A. Rademaker, and R.H. Martin Abnormal progression through meiosis in men with nonobstructive azoospermia Fertil Steril 87 2007 565 571
24. K.A. Ferguson, E.C. Wong, V. Chow, M. Nigro, and S. Ma Abnormal meiotic recombination in infertile men and its association with sperm aneuploidy Hum Mol Genet 16 2007 2870 2879
25. M.A. Brieno-Enriquez, R. Reig-Viader, L. Cabero, N. Toran, F. Martinez, and I. Roig et al. Gene expression is altered after bisphenol A exposure in human fetal oocytes in vitro Mol Hum Reprod 18 2012 171 183
26. H. Scherthan Telomere attachment and clustering during meiosis Cel Mol Life Sci 64 2007 117 124
27. D.L. Keefe, K. Marquard, and L. Liu The telomere theory of reproductive senescence in women Curr Opin Obstet Gynecol 18 2006 280 285
28. C.W. Hanna, K.L. Bretherick, J.L. Gair, M.R. Fluker, M.D. Stephenson, and W.P. Robinson Telomere length and reproductive aging Hum Reprod 24 2009 1206 1211
29. J. Thilagavathi, S. Venkatesh, and R. Dada Telomere length in reproduction Andrologia 45 2013 289 304
30. L. Liu, M.A. Blasco, and D.L. Keefe Requirement of functional telomeres for metaphase chromosome alignments and integrity of meiotic spindles EMBO Rep 3 2002 230 234
31. L. Liu, M. Blasco, J. Trimarchi, and D. Keefe An essential role for functional telomeres in mouse germ cells during fertilization and early development Dev Biol 249 2002 74 84
32. L. Liu, S. Franco, B. Spyropoulos, P.B. Moens, M.A. Blasco, and D.L. Keefe Irregular telomeres impair meiotic synapsis and recombination in mice Proc Natl Acad Sci USA 101 2004 6496 6501
33. N.R. Treff, J. Su, D. Taylor, and R.T. Scott Telomere DNA deficiency is associated with development of human embryonic aneuploidy PLoS Genet 7 2011 e1002161
34. S. Rodríguez, V. Goyanes, E. Segrelles, M. Blasco, J. Gosálvez, and J.L. Fernández Critically short telomeres are associated with sperm DNA fragmentation Fertil Steril 84 2005 843 845
35. S.I. Moskovtsev, J. Willis, J. White, and J.B. Mullen Disruption of telomere-telomere interactions associated with DNA damage in human spermatozoa Syst Biol Reprod Med 56 2010 407 412
36. R. Santiso, M. Tamayo, J. Gosálvez, M. Meseguer, N. Garrido, and J.L. Fernández Swim-up procedure selects spermatozoa with longer telomere length Mutat Res 688 2010 88 90
37. J.O. O'Sullivan, and J. Karlseeder Telomeres: protecting chromosomes against genome instability Nat Rev Mol Cell Biol 11 2010 171 181
38. S. Feuerhahn, N. Iglesias, A. Panza, A. Porro, and J. Lingner TERRA biogenesis, turnover and implications for function FEBS Lett 584 2010 3812 3818
39. C.M. Azzalin, P. Reichenbach, L. Khoriauli, E. Giulotto, and J. Lingner Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends Science 318 2007 798 801
40. S. Schoeftner, and M.A. Blasco Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II Nature 10 2008 228 236
41. Z. Deng, J. Norseen, A. Wiedmer, H. Riethman, and P.M. Lieberman TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres Mol Cell 35 2009 403 413
42. B.O. Farnung, C.M. Brun, R. Arora, L.E. Lorenzi, and C.M. Azzalin Telomerase efficiently elongates highly transcribing telomeres in human cancer cells PLoS One 7 2012 e35714
43. R. Reig-Viader, M.A. Brieño-Enríquez, L. Khouriauli, N. Toran, L. Cabero, and E. Giulotto et al. Telomeric repeat-containing RNA and telomerase in human fetal oocytes Hum Reprod 28 2013 414 422
44. R. Reig-Viader, M. Vila-Cejudo, V. Vitelli, M. Sabaté, E. Giulotto, and M.G. Caldés et al. Telomeric repeat-containing RNA (TERRA) and telomerase are components of telomeres during mammalian gametogenesis Biol Reprod 90 2014 103
45. I. López de Silanes, M. Stagno d'Alcontres, and M.A. Blasco TERRA transcripts are bound by a complex array of RNA-binding proteins Nat Commun 1 2010 33
46. Z. Deng, Z. Wang, N. Stong, R. Plasschaert, A. Moczan, and H.S. Chen et al. A role for CTCF and cohesin in subtelomere chromatin organization, TERRA transcription, and telomere end protection EMBO J 31 2012 4165 4178
47. S. Redon, P. Reichenbach, and J. Lingner The non-coding RNA TERRA is a natural ligand and direct inhibitor of human telomerase Nucleic Acids Res 38 2010 5797 5806
48. N. Arnoult, A. van Beneden, and A. Decottignies Telomere length regulates TERRA levels through increased trimethylation of telomeric H3K9 and HP1α Nat Struct Mol Biol 20 2012 244
49. S. Redon, I. Zemp, and J. Lingner A three-state model for the regulation of telomerase by TERRA and hnRNPA1 Nucleic Acids Res 41 2013 9117 9128
50. J. Zhu, H. Wang, J.M. Bishop, and E.H. Blackburn Telomerase extends the lifespan of virus-transformed human cells without net telomere lengthening Proc Natl Acad Sci U S A 96 1999 3723 3728
51. G.G. Sharma, A. Gupta, H. Wang, H. Scherthan, S. Dhar, and V. Gandhi et al. hTERT associates with human telomeres and enhances genomic stability and DNA repair Oncogene 22 2003 131 146
52. M. Kim, L. Xu, and E.H. Blackburn Catalytically active human telomerase mutants with allele-specific biological properties Exp Cell Res 288 2003 277 287
53. K. Masutomi, R. Possemato, J.M. Wong, J.L. Currier, Z. Tothova, and J.B. Manola et al. The telomerase reverse transcriptase regulates chromatin state and DNA damage responses PNAS 102 2005 8223 8227
54. S. Mukherjee, E.J. Firpo, Y. Wang, and J.M. Roberts Separation of telomerase functions by reverse genetics PNAS 108 2011 1363 1371
55. A. Canela, E. Vera, P. Klatt, and M.A. Blasco High-throughput telomere length quantification by FISH and its application to human population studies Proc Natl Acad Sci USA 104 2007 5300 5305
56. M. Garcia, A.J. Dietrich, L. Freixa, A.C. Vink, M. Ponsà, and J. Egozcue Development of the first meiotic prophase stages in human fetal oocytes observed by light electron microscopy Hum Genet 77 1987 223 232
57. E. Ko, and R.H. Martin Immunofluorescence analysis of human spermatocytes Methods Mol Biol 558 2009 401 418
58. J. Segura, L. Ferretti, S. Ramos-Onsins, L. Capilla, M. Farré, and F. Reis et al. Evolution of recombination in eutherian mammals: insights into mechanisms that affect recombination rates and crossover interference Proc Biol Sci 280 2013 20131945
59. S.S. Poon, and P.M. Lansdorp Measurements of telomere length on individual chromosomes by image cytometry Z. Darzynkiewicz, H.A. Crissman, J.P. Robinson, Methods in cell biology: flow cytometry 2001 Academic Press San Diego 69 96
60. R. Arora, C.M. Brun, and C.M. Azzalin Transcription regulates telomere dynamics in human cancer cells RNA 18 2012 684 693
61. W.E. Wright, M.A. Piatyszek, W.E. Rainey, W. Byrd, and J.W. Shay Telomerase activity in human germline and embryonic tissues and cells Dev Genet 18 1996 173 179
62. M. Fujisawa, H. Tanaka, N. Tatsumi, H. Okada, S. Arakawa, and S. Kamidono Telomerase activity in the testis of infertile patients with selected causes Hum Reprod 13 1998 1476 1479
63. K. Yashima, A. Maitra, B.B. Rogers, C.F. Timmons, A. Rathi, and H. Pinar et al. Expression of the RNA component of telomerase during human development and differentiation Cell Growth Differ 9 1998 805 813
64. M. Schrader, M. Müller, R. Heicappell, H. Krause, W. Schulze, and K. Miller Telomerase activity and expression of telomerase subunits in the testicular tissue of infertile patients Fertil Steril 73 2000 706 711
65. S. Yehezkel, Y. Segev, E. Viegas-Péquignot, K. Skorecki, and S. Selig Hypomethylation of subtelomeric regions in ICF syndrome is associated with abnormally short telomeres and enhanced transcription from telomeric regions Hum Mol Genet 17 2008 2776 2789
66. S. Yehezkel, A. Rebibo-Sabbah, Y. Segev, M. Tzukerman, R. Shaked, and I. Huber et al. Reprogramming of telomeric regions during the generation of human induced pluripotent stem cells and subsequent differentiation into fibroblast-like derivatives Epigenetics 6 2011 63 75
67. A. Smirnova, R. Gamba, L. Khoriauli, V. Vitelli, S.G. Nergadze, and E. Giulotto TERRA expression levels do not correlate with telomere length and radiation sensitivity in human cancer cell lines Fron Oncol 3 2013 115
68. V. Vitelli, P. Falvo, L. Khoriauli, A. Smirnova, R. Gamba, and M. Santagostino et al. More on the lack of Correlation between Terra Expression and Telomere Length Front Oncol 3 2013 245
69. M.T. Hemann, K.L. Rudolph, M.A. Strong, R.A. DePinho, L. Chin, and C.W. Greider Telomere dysfunction triggers developmentally regulated germ cell apoptosis Mol Biol Cell 12 2001 2023 2030
70. S. Turner, and G.M. Hartshorne Telomere lengths in human pronuclei, oocytes and spermatozoa Mol Hum Reprod 19 2013 510 518
71. J. Thilagavathi, M. Kumar, S.S. Mishra, S. Venkatesh, R. Kumar, and R. Dada Analysis of sperm telomere length in men with idiopathic infertility Arch Gynecol Obstet 287 2013 803 807
72. J. Thilagavathi, S.S. Mishra, M. Kumar, K. Vemprala, D. Deka, and V. Dhadwal et al. Analysis of telomere length in couples experiencing idiopathic recurrent pregnancy loss J Assist Reprod Genet 30 2013 793 798
73. A. Ferlin, E. Rampazzo, M.S. Rocca, S. Keppel, A.C. Frigo, and A. de Rossi et al. In young men sperm telomere length is related to sperm number and parental age Hum Reprod 28 2013 3370 3376
74. D.M. Baird, B. Britt-Compton, J. Rowson, N.N. Amso, L. Gregory, and D. Kipling Telomere instability in the male germline Hum Mol Genet 15 2006 45 51
75. P.B. Jørgensen, J. Fedder, S. Koelvraa, and J. Graakjaer Age-dependence of relative telomere length profiles during spermatogenesis in man Maturitas 75 2013 380 385
76. T. De Lange, L. Shiue, R.M. Myers, D.R. Cox, S.L. Naylor, and A.M. Killery et al. Structure and variability of human chromosome ends Mol Cell Biol 10 1990 518 527
77. R.C. Allsopp, H. Vaziri, C. Patterson, S. Goldstein, E.V. Younglai, and A.B. Futcher et al. Telomere length predicts replicative capacity of human fibroblasts Proc Natl Acad Sci USA 89 1992 10114 10118
78. A. Hamada, S.C. Esteves, M. Nizza, and A. Agarwal Unexplained male infertility: diagnosis and management Int Braz J Urol 38 2012 576 594
79. F. Sun, M. Mikhaail-Philips, M. Oliver-Bonet, E. Ko, A. Rademaker, and P. Turek et al. Reduced meiotic recombination on the XY bivalent is correlated with an increased incidence of sex chromosome aneuploidy in men with non-obstructive azoospermia Mol Hum Reprod 14 2008 399 404
80. M. De Vries, L. Ramos, and P. de Boer Immunofluorescent characterization of meiotic recombination in human males with variable spermatogenesis Andrology 1 2013 262 273
81. Z. Deng, Z. Wang, C. Xiang, A. Molczan, V. Baubet, and J. Conejo-Garcia et al. Formation of telomeric repeat-containing RNA (TERRA) foci in highly proliferating mouse cerebellar neuronal progenitors and medulloblastoma J Cell Sci 125 2012 4383 4394
82. N. Ravindranath, R. Dalal, B. Solomon, D. Djakiew, and M. Dym Loss of telomerase activity during male germ cell differentiation Endocrinology 138 1997 4026 4029
83. Y. Yamamoto, N. Sofikitis, K. Ono, T. Kaki, T. Isoyama, and N. Suzuki et al. Postmeiotic modifications of spermatogenic cells are accompanied by inhibition of telomerase activity Urol Res 27 1999 336 345
84. M.V. Achi, N. Ravindranath, and M. Dym Telomere length in male germ cells is inversely correlated with telomerase activity Biol Reprod 63 2000 591 598
85. L. Riou, H. Bastos, B. Lassalle, M. Coureuil, J. Testart, and F.D. Boussin et al. The telomerase activity of adult mouse testis resides in the spermatogonial alpha6-integrin-positive side population enriched in germinal stem cells Endocrinology 146 2005 3926 3932
86. K. Tanemura, A. Ogura, C. Cheong, H. Gotoh, K. Matsumoto, and E. Sato et al. Dynamic rearrangement of telomeres during spermatogenesis in mice Dev Biol 281 2005 196 207
87. P.M. Lansdorp, N.P. Verwoerd, F.M. van de Rijke, V. Dragowska, M.T. Little, and R.W. Dirks et al. Heterogeneity in telomere length of human chromosomes Hum Mol Genet 5 1996 685 691
88. D.M. Baird, J. Rowson, D. Wynford-Thomas, and D. Kipling Extensive allelic variation and ultrashort telomeres in senescent human cells Nat Genet 33 2003 203 207
89. G.S. Roeder, and J.M. Bailis The pachytene checkpoint Trends Genet 16 2000 395 403