Telomerase activity and telomere length in male germ cells

Biology of Reproduction

Volumn 92, Issue 2, 2015, Pages

  Ozturk, Saffet ^a  

^a AKDENIZ UNIVERSITY   (Turkey)

Author keywords

Infertility; Male germ cell; Spermatogenesis; Telomerase activity; Telomeres

Indexed keywords

TELOMERASE;

ANIMAL CELL; ENZYME ACTIVITY; ENZYME REGULATION; GERM CELL; HUMAN; HUMAN CELL; MALE; MALE INFERTILITY; NONHUMAN; PATERNAL AGE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; SHORT SURVEY; SPERMATOGENESIS; TELOMERE; TELOMERE SHORTENING; TESTIS; ANIMAL; METABOLISM; PHYSIOLOGY;

EUKARYOTA; MAMMALIA;

ANIMALS; GERM CELLS; HUMANS; MALE; SPERMATOGENESIS; TELOMERASE; TELOMERE;

EID: 84929578198     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.114.124008     Document Type: Short Survey

References (128)

1. Blackburn EH. Structure and function of telomeres. Nature 1991; 350:569-573.
2. Wellinger RJ, Sen D. The DNA structures at the ends of eukaryotic chromosomes. Eur J Cancer 1997; 33:735-749.
3. Kalmbach KH, Fontes Antunes DM, Dracxler RC, Knier TW, Seth-Smith ML, Wang F, Liu L, Keefe DL. Telomeres and human reproduction. Fertil Steril 2013; 99:23-29.
4. Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 2007; 318:798-801.
5. Reig-Viader R, Brieno-Enriquez MA, Khouriauli L, Toran N, Cabero L, Giulotto E, Garcia-Caldes M, Ruiz-Herrera A. Telomeric repeatcontaining RNA and telomerase in human fetal oocytes. Hum Reprod 2013; 28:414-422.
6. O'Sullivan RJ, Karlseder J. Telomeres: protecting chromosomes against genome instability. Nat Rev Mol Cell Biol 2010; 11:171-181.
7. Palm W, de Lange T. How shelterin protects mammalian telomeres. Annu Rev Genet 2008; 42:301-334.
8. Kim MK, Kang MR, Nam HW, Bae YS, Kim YS, Chung IK. Regulation of telomeric repeat binding factor 1 binding to telomeres by casein kinase 2-mediated phosphorylation. J Biol Chem 2008; 283:14144-14152.
9. van Steensel B, de Lange T. Control of telomere length by the human telomeric protein TRF1. Nature 1997; 385:740-743.
10. Smogorzewska A, van Steensel B, Bianchi A, Oelmann S, Schaefer MR, Schnapp G, de Lange T. Control of human telomere length by TRF1 and TRF2. Mol Cell Biol 2000; 20:1659-1668.
11. Matsutani N, Yokozaki H, Tahara E, Tahara H, Kuniyasu H, Haruma K, Chayama K, Yasui W. Expression of telomeric repeat binding factor 1 and 2 and TRF1-interacting nuclear protein 2 in human gastric carcinomas. Int J Oncol 2001; 19:507-512.
12. De Boeck G, Forsyth RG, Praet M, Hogendoorn PC. Telomereassociated proteins: cross-talk between telomere maintenance and telomere-lengthening mechanisms. J Pathol 2009; 217:327-344.
13. Counter CM. The roles of telomeres and telomerase in cell life span. Mutat Res 1996; 366:45-63.
14. Scherthan H. Telomere attachment and clustering during meiosis. Cell Mol Life Sci 2007; 64:117-124.
15. Nandakumar J, Cech TR. Finding the end: recruitment of telomerase to telomeres. Nat Rev Mol Cell Biol 2013; 14:69-82.
16. Ozturk S, Sozen B, Demir N. Telomere length and telomerase activity during oocyte maturation and early embryo development in mammalian species. Mol Hum Reprod 2014; 20:15-30.
17. Olovnikov AM. Telomeres, telomerase, and aging: origin of the theory. Exp Gerontol 1996; 31:443-448.
18. Olovnikov AM. A theory of marginotomy: the incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J Theor Biol 1973; 41:181-190.
19. Levy MZ, Allsopp RC, Futcher AB, Greider CW, Harley CB. Telomere end-replication problem and cell aging. J Mol Biol 1992; 225:951-960.
20. Martens UM, Chavez EA, Poon SS, Schmoor C, Lansdorp PM. Accumulation of short telomeres in human fibroblasts prior to replicative senescence. Exp Cell Res 2000; 256:291-299.
21. Liu L, Trimarchi JR, Smith PJ, Keefe DL. Mitochondrial dysfunction leads to telomere attrition and genomic instability. Aging Cell 2002; 1:40-46.
22. Cattan V, Mercier N, Gardner JP, Regnault V, Labat C, Maki-Jouppila J, Nzietchueng R, Benetos A, Kimura M, Aviv A, Lacolley P. Chronic oxidative stress induces a tissue-specific reduction in telomere length in CAST/Ei mice. Free Radic Biol Med 2008; 44:1592-1598.
23. Thilagavathi J, Venkatesh S, Dada R. Telomere length in reproduction. Andrologia 2013; 45:289-304.
24. Desai N, Sabanegh E Jr, Kim T, Agarwal A. Free radical theory of aging: implications in male infertility. Urology 2010; 75:14-19.
25. Cohen SB, Graham ME, Lovrecz GO, Bache N, Robinson PJ, Reddel RR. Protein composition of catalytically active human telomerase from immortal cells. Science 2007; 315:1850-1853.
26. Morin GB. The human telomere terminal transferase enzyme is a ribonucleoprotein that synthesizes TTAGGG repeats. Cell 1989; 59:521-529.
27. Venteicher AS, Abreu EB, Meng Z, McCann KE, Terns RM, Veenstra TD, Terns MP, Artandi SE. A human telomerase holoenzyme protein required for Cajal body localization and telomere synthesis. Science 2009; 323:644-648.
28. Blasco MA, Gasser SM, Lingner J. Telomeres and telomerase. Genes Dev 1999; 13:2353-2359.
29. Greider CW. Telomere length regulation. Annu Rev Biochem 1996; 65:337-365.
30. Martin-Rivera L, Herrera E, Albar JP, Blasco MA. Expression of mouse telomerase catalytic subunit in embryos and adult tissues. Proc Natl Acad Sci U S A 1998; 95:10471-10476.
31. Yi X, Tesmer VM, Savre-Train I, Shay JW, Wright WE. Both transcriptional and posttranscriptional mechanisms regulate human telomerase template RNA levels. Mol Cell Biol 1999; 19:3989-3997.
32. Blasco MA, Funk W, Villeponteau B, Greider CW. Functional characterization and developmental regulation of mouse telomerase RNA. Science 1995; 269:1267-1270.
33. Counter CM, Gupta J, Harley CB, Leber B, Bacchetti S. Telomerase activity in normal leukocytes and in hematologic malignancies. Blood 1995; 85:2315-2320.
34. Liu JP, Li H. Telomerase in the ovary. Reproduction 2010; 140:215-222.
35. Kolquist KA, Ellisen LW, Counter CM, Meyerson M, Tan LK, Weinberg RA, Haber DA, Gerald WL. Expression of TERT in early premalignant lesions and a subset of cells in normal tissues. Nat Genet 1998; 19:182-186.
36. Choudhary B, Karande AA, Raghavan SC. Telomere and telomerase in stem cells: relevance in ageing and disease. Front Biosci (Schol Ed) 2012; 4:16-30.
37. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, Coviello GM, Wright WE, Weinrich SL, Shay JW. Specific association of human telomerase activity with immortal cells and cancer. Science 1994; 266:2011-2015.
38. Yasumoto S, Kunimura C, Kikuchi K, Tahara H, Ohji H, Yamamoto H, Ide T, Utakoji T. Telomerase activity in normal human epithelial cells. Oncogene 1996; 13:433-439.
39. Wright WE, Piatyszek MA, Rainey WE, Byrd W, Shay JW. Telomerase activity in human germline and embryonic tissues and cells. Dev Genet 1996; 18:173-179.
40. Kipling D. Telomere structure and telomerase expression during mouse development and tumorigenesis. Eur J Cancer 1997; 33:792-800.
41. Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP, Morin GB, Harley CB, Shay JW, Lichtsteiner S, Wright WE. Extension of life-span by introduction of telomerase into normal human cells. Science 1998; 279:349-352.
42. Cong YS, Wright WE, Shay JW. Human telomerase and its regulation. Microbiol Mol Biol Rev 2002; 66:407-425.
43. Liu L, Bailey SM, Okuka M, Munoz P, Li C, Zhou L, Wu C, Czerwiec E, Sandler L, Seyfang A, Blasco MA, Keefe DL. Telomere lengthening early in development. Nat Cell Biol 2007; 9:1436-1441.
44. Cesare AJ, Reddel RR. Alternative lengthening of telomeres: models, mechanisms and implications. Nat Rev Genet 2013; 11:319-330.
45. Neumann AA, Watson CM, Noble JR, Pickett HA, Tam PP, Reddel RR. Alternative lengthening of telomeres in normal mammalian somatic cells. Genes Dev 2013; 27:18-23.
46. Conomos D, Pickett HA, Reddel RR. Alternative lengthening of telomeres: remodeling the telomere architecture. Front Oncol 2013; 3:27.
47. Herrera E, Martinez AC, Blasco MA. Impaired germinal center reaction in mice with short telomeres. EMBO J 2000; 19:472-481.
48. Bailey SM, Brenneman MA, Goodwin EH. Frequent recombination in telomeric DNA may extend the proliferative life of telomerase-negative cells. Nucleic Acids Res 2004; 32:3743-3751.
49. Leblond CP, Clermont Y. Spermiogenesis of rat, mouse, hamster and guinea pig as revealed by the periodic acid-fuchsin sulfurous acid technique. Am J Anat 1952; 90:167-215.
50. Vergouwen RP, Huiskamp R, Bas RJ, Roepers-Gajadien HL, Davids JA, de Rooij DG. Postnatal development of testicular cell populations in mice. J Reprod Fertil 1993; 99:479-485.
51. Olsen AK, Lindeman B, Wiger R, Duale N, Brunborg G. How do male germ cells handle DNA damage? Toxicol Appl Pharmacol 2005; 207:521-531.
52. Kimmins S, Kotaja N, Davidson I, Sassone-Corsi P. Testis-specific transcription mechanisms promoting male germ-cell differentiation. Reproduction 2004; 128:5-12.
53. Dym M. Spermatogonial stem cells of the testis. Proc Natl Acad Sci U S A 1994; 91:11287-11289.
54. Russell LD, Ettlin RA, Sinha Hikim AP, Clegg ED. Histological and Histopathological Evaluation of the Testis. Clearwater, FL: Cache River Press; 1990:62-193.
55. n arrays. Mol Reprod Dev 1998; 51:98-104.
56. Allsopp RC, Vaziri H, Patterson C, Goldstein S, Younglai EV, Futcher AB, Greider CW, Harley CB. Telomere length predicts replicative capacity of human fibroblasts. Proc Natl Acad Sci U S A 1992; 89:10114-10118.
57. Greenberg RA, Allsopp RC, Chin L, Morin GB, DePinho RA. Expression of mouse telomerase reverse transcriptase during development, differentiation and proliferation. Oncogene 1998; 16:1723-1730.
58. Prowse KR, Greider CW. Developmental and tissue-specific regulation of mouse telomerase and telomere length. Proc Natl Acad Sci U S A 1995; 92:4818-4822.
59. Yamamoto Y, Sofikitis N, Ono K, Kaki T, Isoyama T, Suzuki N, Miyagawa I. Postmeiotic modifications of spermatogenic cells are accompanied by inhibition of telomerase activity. Urol Res 1999; 27:336-345.
60. Weise JM, Gunes C. Differential regulation of human and mouse telomerase reverse transcriptase (TERT) promoter activity during testis development. Mol Reprod Dev 2009; 76:309-317.
61. Tanemura K, Ogura A, Cheong C, Gotoh H, Matsumoto K, Sato E, Hayashi Y, Lee HW, Kondo T. Dynamic rearrangement of telomeres during spermatogenesis in mice. Dev Biol 2005; 281:196-207.
62. Forand A, Messiaen S, Habert R, Bernardino-Sgherri J. Exposure of the mouse perinatal testis to radiation leads to hypospermia at sexual maturity. Reproduction 2009; 137:487-495.
63. Ozturk S, Guzeloglu-Kayisli O, Demir N, Sozen B, Ilbay O, Lalioti MD, Seli E. Epab and Pabpc1 are differentially expressed during male germ cell development. Reprod Sci 2012; 19:911-922.
64. Bellve AR. Purification, culture, and fractionation of spermatogenic cells. Methods Enzymol 1993; 225:84-113.
65. Jia W, Wang S, Horner JW, Wang N, Wang H, Gunther EJ, DePinho RA, Zhu J. A BAC transgenic reporter recapitulates in vivo regulation of human telomerase reverse transcriptase in development and tumorigenesis. FASEB J 2011; 25:979-989.
66. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. Distinctive chromatin in human sperm packages genes for embryo development. Nature 2009; 460:473-478.
67. Churikov D, Siino J, Svetlova M, Zhang K, Gineitis A, Morton Bradbury E, Zalensky A. Novel human testis-specific histone H2B encoded by the interrupted gene on the X chromosome. Genomics 2004; 84:745-756.
68. Ravindranath N, Dalal R, Solomon B, Djakiew D, Dym M. Loss of telomerase activity during male germ cell differentiation. Endocrinology 1997; 138:4026-4029.
69. Yashima K, Maitra A, Rogers BB, Timmons CF, Rathi A, Pinar H, Wright WE, Shay JW, Gazdar AF. Expression of the RNA component of telomerase during human development and differentiation. Cell Growth Differ 1998; 9:805-813.
70. Izadyar F, Wong J, Maki C, Pacchiarotti J, Ramos T, Howerton K, Yuen C, Greilach S, Zhao HH, Chow M, Chow YC, Rao J, et al. Identification and characterization of repopulating spermatogonial stem cells from the adult human testis. Hum Reprod 2011; 26:1296-1306.
71. Achi MV, Ravindranath N, Dym M. Telomere length in male germ cells is inversely correlated with telomerase activity. Biol Reprod 2000; 63:591-598.
72. Clermont Y, Perey B. Quantitative study of the cell population of the seminiferous tubules in immature rats. Am J Anat 1957; 100:241-267.
73. Bellve AR, Cavicchia JC, Millette CF, O'Brien DA, Bhatnagar YM, Dym M. Spermatogenic cells of the prepubertal mouse: isolation and morphological characterization. J Cell Biol 1977; 74:68-85.
74. Eisenhauer KM, Gerstein RM, Chiu CP, Conti M, Hsueh AJ. Telomerase activity in female and male rat germ cells undergoing meiosis and in early embryos. Biol Reprod 1997; 56:1120-1125.
75. Reig-Viader R, Vila-Cejudo M, Vitelli V, Busca R, Sabate M, Giulotto E, Caldes MG, Ruiz-Herrera A. Telomeric repeat-containing RNA (TERRA) and telomerase are components of telomeres during mammalian gametogenesis. Biol Reprod 2014; 90:103.
76. Masutomi K, Yu EY, Khurts S, Ben-Porath I, Currier JL, Metz GB, Brooks MW, Kaneko S, Murakami S, DeCaprio JA, Weinberg RA, Stewart SA, et al. Telomerase maintains telomere structure in normal human cells. Cell 2003; 114:241-253.
77. Tomlinson RL, Ziegler TD, Supakorndej T, Terns RM, Terns MP. Cell cycle-regulated trafficking of human telomerase to telomeres. Mol Biol Cell 2006; 17:955-965.
78. Kierszenbaum AL, Tres LL. RNA transcription and chromatin structure during meiotic and postmeiotic stages of spermatogenesis. Fed Proc 1978; 37:2512-2516.
79. Steger K. Transcriptional and translational regulation of gene expression in haploid spermatids. Anat Embryol (Berl) 1999; 199:471-487.
80. Fradiani PA, Ascenzioni F, Lavitrano M, Donini P. Telomeres and telomerase activity in pig tissues. Biochimie 2004; 86:7-12.
81. Pickett HA, Henson JD, Au AY, Neumann AA, Reddel RR. Normal mammalian cells negatively regulate telomere length by telomere trimming. Hum Mol Genet 2011; 20:4684-4692.
82. Baird DM, Britt-Compton B, Rowson J, Amso NN, Gregory L, Kipling D. Telomere instability in the male germline. Hum Mol Genet 2006; 15:45-51.
83. Kimura M, Cherkas LF, Kato BS, Demissie S, Hjelmborg JB, Brimacombe M, Cupples A, Hunkin JL, Gardner JP, Lu X, Cao X, Sastrasinh M, et al. Offspring's leukocyte telomere length, paternal age, and telomere elongation in sperm. PLOS Genet 2008; 4:e37.
84. Turner S, Hartshorne GM. Telomere lengths in human pronuclei, oocytes and spermatozoa. Mol Hum Reprod 2013; 19:510-518.
85. Hultdin M, Gronlund E, Norrback K, Eriksson-Lindstrom E, Just T, Roos G. Telomere analysis by fluorescence in situ hybridization and flow cytometry. Nucleic Acids Res 1998; 26:3651-3656.
86. Oexle K. Telomere length distribution and Southern blot analysis. J Theor Biol 1998; 190:369-377.
87. Santiso R, Tamayo M, Gosalvez J, Meseguer M, Garrido N, Fernandez JL. Swim-up procedure selects spermatozoa with longer telomere length. Mutat Res 2010; 688:88-90.
88. Jørgensen PB, Fedder J, Koelvraa S, Graakjaer J. Age-dependence of relative telomere length profiles during spermatogenesis in man. Maturitas 2013; 75:380-385.
89. Moskovtsev SI, Willis J, White J, Mullen JB. Disruption of telomeretelomere interactions associated with DNA damage in human spermatozoa. Syst Biol Reprod Med 2010; 56:407-412.
90. Ishii A, Nakamura K, Kishimoto H, Honma N, Aida J, Sawabe M, Arai T, Fujiwara M, Takeuchi F, Kato M, Oshimura M, Izumiyama N, et al. Telomere shortening with aging in the human pancreas. Exp Gerontol 2006; 41:882-886.
91. Keefe DL, Liu L. Telomeres and reproductive aging. Reprod Fertil Dev 2009; 21:10-14.
92. Ferlin A, Rampazzo E, Rocca MS, Keppel S, Frigo AC, De Rossi A, Foresta C. In young men sperm telomere length is related to sperm number and parental age. Hum Reprod 2013; 28:3370-3376.
93. De Meyer T, Rietzschel ER, De Buyzere ML, De Bacquer D, Van Criekinge W, De Backer GG, Gillebert TC, Van Oostveldt P, Bekaert S. Paternal age at birth is an important determinant of offspring telomere length. Hum Mol Genet 2007; 16:3097-3102.
94. Eisenberg DT, Hayes MG, Kuzawa CW. Delayed paternal age of reproduction in humans is associated with longer telomeres across two generations of descendants. Proc Natl Acad Sci U S A 2012; 109:10251-10256.
95. Unryn BM, Cook LS, Riabowol KT. Paternal age is positively linked to telomere length of children. Aging Cell 2005; 4:97-101.
96. Forsyth NR, Evans AP, Shay JW, Wright WE. Developmental differences in the immortalization of lung fibroblasts by telomerase. Aging Cell 2003; 2:235-243.
97. Franco S, Alsheimer M, Herrera E, Benavente R, Blasco MA. Mammalian meiotic telomeres: composition and ultrastructure in telomerase-deficient mice. Eur J Cell Biol 2002; 81:335-340.
98. Scherthan H, Weich S, Schwegler H, Heyting C, Harle M, Cremer T. Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J Cell Biol 1996; 134:1109-1125.
99. Meyer-Ficca M, Muller-Navia J, Scherthan H. Clustering of pericentromeres initiates in step 9 of spermiogenesis of the rat (Rattus norvegicus) and contributes to a well defined genome architecture in the sperm nucleus. J Cell Sci 1998; 111(Pt 10):1363-1370.
100. Ritz JM, Kuhle O, Riethdorf S, Sipos B, Deppert W, Englert C, Gunes C. A novel transgenic mouse model reveals humanlike regulation of an 8-kbp human TERT gene promoter fragment in normal and tumor tissues. Cancer Res 2005; 65:1187-1196.
101. Gunes C, Lichtsteiner S, Vasserot AP, Englert C. Expression of the hTERT gene is regulated at the level of transcriptional initiation and repressed by Mad1. Cancer Res 2000; 60:2116-2121.
102. Oh S, Song YH, Yim J, Kim TK. Identification of Mad as a repressor of the human telomerase (hTERT) gene. Oncogene 2000; 19:1485-1490.
103. Misiti S, Nanni S, Fontemaggi G, Cong YS, Wen J, Hirte HW, Piaggio G, Sacchi A, Pontecorvi A, Bacchetti S, Farsetti A. Induction of hTERT expression and telomerase activity by estrogens in human ovary epithelium cells. Mol Cell Biol 2000; 20:3764-3771.
104. Kyo S, Takakura M, Kanaya T, Zhuo W, Fujimoto K, Nishio Y, Orimo A, Inoue M. Estrogen activates telomerase. Cancer Res 1999; 59:5917-5921.
105. Fujisawa M, Tanaka H, Tatsumi N, Okada H, Arakawa S, Kamidono S. Telomerase activity in the testis of infertile patients with selected causes. Hum Reprod 1998; 13:1476-1479.
106. Bayne S, Jones ME, Li H, Pinto AR, Simpson ER, Liu JP. Estrogen deficiency leads to telomerase inhibition, telomere shortening and reduced cell proliferation in the adrenal gland of mice. Cell Res 2008; 18:1141-1150.
107. Pines A. Telomere length and telomerase activity in the context of menopause. Climacteric 2013; 16:629-631.
108. Dolci S, Levati L, Pellegrini M, Faraoni I, Graziani G, Di Carlo A, Geremia R. Stem cell factor activates telomerase in mouse mitotic spermatogonia and in primordial germ cells. J Cell Sci 2002; 115:1643-1649.
109. Blume-Jensen P, Jiang G, Hyman R, Lee KF, O'Gorman S, Hunter T. Kit/stem cell factor receptor-induced activation of phosphatidylinositol 30-kinase is essential for male fertility. Nat Genet 2000; 24:157-162.
110. Kissel H, Timokhina I, Hardy MP, Rothschild G, Tajima Y, Soares V, Angeles M, Whitlow SR, Manova K, Besmer P. Point mutation in Kit receptor tyrosine kinase reveals essential roles for Kit signaling in spermatogenesis and oogenesis without affecting other Kit responses. EMBO J 2000; 19:1312-1326.
111. Kang SS, Kwon T, Kwon DY, Do SI. Akt protein kinase enhances human telomerase activity through phosphorylation of telomerase reverse transcriptase subunit. J Biol Chem 1999; 274:13085-13090.
112. Liu L, Blasco M, Trimarchi J, Keefe D. An essential role for functional telomeres in mouse germ cells during fertilization and early development. Dev Biol 2002; 249:74-84.
113. Thilagavathi J, Kumar M, Mishra SS, Venkatesh S, Kumar R, Dada R. Analysis of sperm telomere length in men with idiopathic infertility. Arch Gynecol Obstet 2013; 287:803-807.
114. Lee HW, Blasco MA, Gottlieb GJ, Horner JW II, Greider CW, DePinho RA. Essential role of mouse telomerase in highly proliferative organs. Nature 1998; 392:569-574.
115. Hemann MT, Strong MA, Hao LY, Greider CW. The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 2001; 107:67-77.
116. Allan DJ, Harmon BV, Kerr JFR. Telomere length in male germ cells is inversely correlated with telomerase activity. In: Potten CS (ed.), Perspectives on Mammalian Cell Death. London: Oxford University Press; 1987:229-258.
117. Weikert S, Christoph F, Schulze W, Krause H, Kempkensteffen C, Schostak M, Miller K, Schrader M. Testicular expression of survivin and human telomerase reverse transcriptase (hTERT) associated with spermatogenic function in infertile patients. Asian J Androl 2006; 8:95-100.
118. Schrader M, Muller M, Heicappell R, Krause H, Schulze W, Miller K. Telomerase activity and expression of telomerase subunits in the testicular tissue of infertile patients. Fertil Steril 2000; 73:706-711.
119. Schrader M, Muller M, Heicappell R, Straub B, Miller K. Quantification of human telomerase RNA (hTR) and human telomerase reverse transcriptase (hTERT) mRNA in testicular tissue of infertile patients. Asian J Androl 2001; 3:263-270.
120. Schrader M, Muller M, Schulze W, Heicappell R, Krause H, Straub B, Miller K. Quantification of telomerase activity, porphobilinogen deaminase and human telomerase reverse transcriptase mRNA in testicular tissue-new parameters for a molecular diagnostic classification of spermatogenesis disorders. Int J Androl 2002; 25:34-44.
121. Giannakis D, Baltogiannis D, Tsoukanelis K, Loutradis D, Miyagawa I, Makrydimas G, Kanakas N, Sofikitis N. Role of testicular tissue telomerase assay for the prediction of the presence of testicular spermatozoa in azoospermic men with varicoceles, pre- and postvaricocelectomy. Andrologia 2004; 36:111-122.
122. Yamamoto Y, Sofikitis N, Mio Y, Miyagawa I. Highly sensitive quantitative telomerase assay of diagnostic testicular biopsy material predicts the presence of haploid spermatogenic cells in therapeutic testicular biopsy in men with Sertoli cell-only syndrome. Hum Reprod 1999; 14:3041-3047.
123. Schaetzlein S, Lucas-Hahn A, Lemme E, Kues WA, Dorsch M, Manns MP, Niemann H, Rudolph KL. Telomere length is reset during early mammalian embryogenesis. Proc Natl Acad Sci U S A 2004; 101:8034-8038.
124. Thilagavathi J, Mishra SS, Kumar M, Vemprala K, Deka D, Dhadwal V, Dada R. Analysis of telomere length in couples experiencing idiopathic recurrent pregnancy loss. J Assist Reprod Genet 2013; 30:793-798.
125. Reig-Viader R, Capilla L, Vila-Cejudo M, Garcia F, Anguita B, Garcia-Caldes M, Ruiz-Herrera A. Telomere homeostasis is compromised in spermatocytes from patients with idiopathic infertility. Fertil Steril 2014; 102:728-738.e1.
126. Keefe DL. In every end there is a beginning-telomeres in male reproduction. Fertil Steril 2014; 102:690-691.
127. Yan L, Wu S, Zhang S, Ji G, Gu A. Genetic variants in telomerase reverse transcriptase (TERT) and telomerase-associated protein 1 (TEP1) and the risk of male infertility. Gene 2014; 534:139-143.
128. Salahshourifar I, Karimi H, Tavakolzadeh T, Beheshti Z, Maeda T, Aviv H, Gourabi H. Constitutional telomeric dysfunction in an azoospermic male with extensive telomeric association. Am J Med Genet A 2010; 152A:2413-2416.