Deletion of genes implicated in protecting the integrity of male germ cells has differential effects on the incidence of DNA breaks and germ cell loss

PLoS ONE

Volumn 2, Issue 10, 2007, Pages

  Paul, Catriona ^a   Povey, Joanne E ^b   Lawrence, Nicola J ^b   Selfridge, Jim ^b   Melton, David W ^b   Saunders, Philippa T K ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; DNA; EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; PROTEIN MSH2; PROTEIN P53; DNA BINDING PROTEIN; ENDONUCLEASE; ERCC1 PROTEIN, MOUSE; MSH2 PROTEIN, MOUSE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL FUNCTION; CELL LOSS; CELL PROTECTION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA STRAND BREAKAGE; EPIDIDYMIS; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GERM CELL; MALE; MALE INFERTILITY; MOUSE; NONHUMAN; PACHYTENE; PHENOTYPIC VARIATION; SERTOLI CELL; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOZOON COUNT; TESTIS; ANIMAL; CHROMATIN; CYTOLOGY; DISEASE MODEL; DNA DAMAGE; DNA REPAIR; GENETICS; METABOLISM;

MUS;

ANIMALS; CHROMATIN; DISEASE MODELS, ANIMAL; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; ENDONUCLEASES; GENE DELETION; GERM CELLS; INFERTILITY, MALE; MALE; MICE; MUTS HOMOLOG 2 PROTEIN; SPERMATOCYTES; TESTIS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 39449094163     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0000989     Document Type: Article

References (85)

1. Dunson DB, Baird DD, Colombo B (2004) Increased infertility with age in men and women. Obstet Gynecol 103: 51-56.
2. Campbell AJ, Irvine DS (2000) Male infertility and intracytoplasmic sperm injection (ICSI). Br Med Bull 56: 616-629.
3. Twigg JP, Irvine DS, Aitken RJ (1998) Oxidative damage to DNA in human spermatozoa does not preclude pronucleus formation at intracytoplasmic sperm injection. Hum Reprod 13: 1864-1871.
4. Zenzes MT, Puy LA, Bielecki R, Reed TE (1999) Detection of benzo[a]pyrene diol epoxide-DNA adducts in embryos from smoking couples: evidence for transmission by spermatozoa. Mol Hum Reprod 5: 125-131.
5. Zenzes MT (2000) Smoking and reproduction: gene damage to human gametes ar d embryos. Hum Reprod Update 6: 122-131.
6. Ji BT, Shu XO, Liner MS, Zheng W, Wacholder S, et al. (1997) Paternal cigarette smoking and the risk of childhood cancer among offspring of nonsmoking mothers. J Natl Cancer Inst 89: 238-244.
7. Sorahan T, Prior P, Lancashire RJ, Faux SP, Hulten MA, et al. (1997) Childhood cancer and parental use of tobacco: deaths from 1971 to 1976. Br J Cancer 76: 1525-1531.
8. Cooke HJ, Saunders PT (2002) Mouse models of male infertility. Nat Rev Genet 3: 790-801.
9. Baarends WM, van der Laan R, Grootegoed JA (2001) DNA repair mechanisms and gametogenesis. Reproduction 121: 31-39.
10. Baudat F, Manova K, Yuen JP, Jasin M, Keeney S (2000) Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spol1. Mol Cell 6: 989-998.
11. Romanienko PJ, Camerini-Otero RD (2000) The mouse Spol1 gene is required for meiotic chromosome synapsis. Mol Cell 6: 975-987.
12. Marcon E, Moens PB (2005) The evolution of meiosis: recruitment and modification of somatic DNA-repair proteins. Bioessays 27: 795-808.
13. Cohen PE, Pollard JW (2001) Regulation of meiotic recombination and prophase I progression in mammals. Bioessays, 23: 996-1009.
14. Jaroudi S, SenGupta S (2007) DNA repair in mammalian embryos. Mutat Res 635: 53-77.
15. Sedelnikova OA, Rogakou EP, Panyutin IG, Bonner WM (2002) Quantitative detection of (125)IdU-induced DNA double-strand breaks with gamma-H2AX antibody. Radiat Res 158: 486-492.
16. Celeste A, Petersen S, Romanienko PJ, Fernandez-Capetillo O, Chen HT, et al. (2002) Genomic Instability in Mice Lacking Historic H2AX. Science 296: 922-927.
17. Downs JA, Lowndes NF, Jackson SP (2000) A role for Saccharomyces cerevisiae historic H2A in DNA repair. Nature 408: 1001-1004.
18. Bassing CH, Chua KF, Sekiguchi J, Suh H, Whitlow SR, et al. (2002) Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc Natl Acad Sci U S A 99: 8173-8178.
19. Rogakou EP, Boon C, Redon C, Bonner WM (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146: 905-916.
20. Stojic L, Brun R, Jiricny J (2004) Mismatch repair and DNA damage signalling. DNA Repair (Amst) 3: 1091-1101.
21. Kunkel TA, Erie DA (2005) DNA mismatch repair. Annu Rev Biochem 74: 681-710.
22. Richardson LL, Pedigo C, Handel MA (2000) Expression of deoxyribonucleic acid repair enzymes during spermatogenesis in mice. Biology of Reproduction 62: 789-796.
23. Meira LB, Cheo DL, Reis AM, Claij N, Burns DK, et al. (2002) Mice defective in the mismatch repair gene Msh2 show increased predisposition, to UVB radiation-induced skin cancer. DNA Repair (Amst) 1: 929-934.
24. Yoshino M, Nakatsu Y, te Riele H, Hirota S, Kitamura Y, et al. (2002) Additive roles of XPA and MSH2 genes in UVB-induced skin tumorigenesis in mice. DNA Repair (Amst) 1: 935-940.
25. Wood RD (1996) DNA repair in eukaryotes, Annu Rev Biochem 65: 135-167.
26. Haja KT, Millar MR, King S, Selfridge J, Redhead NJ, et al. (2003) DNA repair gene Ercc1 is essential for normal spermatogenesis and oogenesis and for functional integrity of germ cell DNA in the mouse. Development 130: 369-378.
27. Schiestl RH, Prakash S (1990) RAD10, an excision repair gene of Saccharomyces cerevisiae, is involved in the RAD1 pathway of mitotic recombination. Mol Cell Biol 10: 2485-2491.
28. Davies AA, Friedberg EC, Tomkinson AE, Wood RD, West SC (1995) Role of the Rad1 and Rad10 proteins in nucleotide excision repair and recombination. J Biol Chem 270: 24638-24641.
29. McWhir J, Selfridge J, Harrison DJ, Squires S, Melton DW (1993) Mice with DNA repair gene (ERCC-1) deficiency have elevated levels of p53. liver nuclear abnormalities and die before weaning. Nat Genet 5: 217-224.
30. Selfridge J, Hsia KT, Redhead M, Melton DW (2001) Correction of liver dysfunction in DNA repair-deficient mice widi an ERCC1 transgene. Nucleic Acids Res 29: 4541-4550.
31. Odorisio T, Rodriguez TA, Evans EP, Clarke AR, Burgoyne PS (1998) The meiotic checkpoint monitoring synapsis eliminates spermatocytes via p53-independent apoptosis. Nat Genet 18: 257-261.
32. Schwartz D, Goldfinger N, Rotter V (1993) Expression of p53 protein in spermatogenesis is confined to the tetraploid pachytene primary spermatocytes. Oncogenc 8: 1487-1494.
33. Sjoblom T, Lahdetie J (1996) Expression of p53 in normal and gammairradiated rat testis suggests a role for p53 in meiotic recombination and repair. Oncogene 12: 2499-2505.
34. Bakalkin G, Yakovleva T, Terenius L (1993) NF-kappa B-like factors in the murine brain. Dcvelopmentally-regulated and tissue-specific expression. Brain Res Mol Brain Res 20: 137-146.
35. Linke SP, Sengupta S, Khabie N, Jeffries BA, Buchhop S, et al. (2003) p53 interacts with hRAD51 and hRAD54, and directly modulates homologous recombination. Cancer Res 63: 2596-2605.
36. Tang W, Willers H, Powell SN (1999) p53 directly enhances rejoining of DNA double-strand br?aks with cohesive ends in gamma-irradiated mouse fibroblasts. Cancer Res 59: 2562-2565.
37. Schwartz D, Goldfinger N, Kam Z, Rotter V (1999) p53 controls low DNA damage-dependent premeiotic checkpoint and facilitates DNA repair during spermatogenesis. Cell Growth Differ 10: 665-675.
38. Yin Y, Stahl BC, DeWolf WC, Morgentaler A (1998) p53-mediated germ cell quality control in spermatogenesis. Dev Biol 204: 165-171.
39. de Wind N, Dekker M, Berns A, Radman M, te Riele H (1995) Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell 82: 321-330.
40. Clarke AR, Purdie CA, Harrison DJ, Morris RG, Bird CC, et al. (1993) Thymocyte apoptosis induced by p53-dependent and independent pathways. Nature 362: 849-852.
41. Saunders PT, Sharpe RM, Williams K, Macpherson S, Urquart H, et al. (2001) Differential expression of oestrogen receptor alpha and beta proteins in the testes and male reproductive system of human and non-human primates. Moll Hum Reprod 7: 227-236.
42. Biggers J, Whitten W, Whittingham D, eds (1971) The culture of mouse embryos in vitro. San Fransisco: Freeman Press. pp, 86-94.
43. Gorczyca W, Traganos F, Jesionowska H, Darzynkiewicz Z (1993) Presence of DNA strand breaks and increased sensitivity of DNA in situ to denaturation in abnormal human sperm cells: analogy to apoptosis of somatic cells. Exp Cell Res 207: 202-205.
44. Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Experimental Cell Research 175: 184-191.
45. Chohan KR, Griffin JT, Carrell DT (2004) Evaluation of chromatin integrity in human sperm using acridine orange staining with different fixatives and after cryopreservation. Andrologia 36: 321-326.
46. Barlow AL, Benson FE, West SC, Hulton MA (1997) Distribution of the Rad51 recombinase in human and mouse spermatocytes: Embo J 16: 5207-5215.
47. Lammers JH, Offenberg HH, van Aalderen M, Vink AC, Dietrich AJ, et al. (1994) The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes. Mol Cell Biol 14: 1137-1146.
48. Hamer G, Roepers-Gajadien HL, van Duyn-Goedhart A, Gademan IS, Kal HB, et al. (2003) DNA double-strand breaks and gamma-H2AX signaling in the testis. Biol Reprod 68: 628-634.
49. Clermont Y (1963) The cycle of the seminiferous epithelium in man. American Journal of Anatomy 112: 35-51.
50. Edelmann W, Cohen PE, Kane M, Lau K, Morrow B, et al. (1996) Meiotic pachytene arrest in MLH1-deficient mice. Cell 85: 1125-1134.
51. Griswold MD (1995) Interactions between germ cells and Sertoli cells in the testis. Biology of Reproduction 52: 211-216.
52. Matzuk MM, Kumar TR, Bradley A (1995) Different phenotypes for mice deficient in either activins or activin receptor type II. Nature 374: 356-360.
53. Xu Y, Ashley T, Brainerd EE, Bronson RT, Meyn MS, et al. (1996) Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev 10: 2411-2422.
54. Yuan L, Liu JG, Zhao J, Brundell E, Daneholt B, et al. (2000) The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Mol Cell 5: 73-83.
55. Zimmermann KC, Bonzon C, Green DR (2001) The machinery of programmed cell death. Pharmacol Ther 92: 57-70.
56. Kolodner R (1996) Biochemistry and genetics of eukaryotic mismatch repair. Genes Dev 10: 1433-1442.
57. Modrich P (1997) Strand-specific mismatch repair in mammalian cells. J Biol Chem 272: 24727-24730.
58. Kirkpatrick DT (1999) Roles of the DNA mismatch repair and nucleotide excision repair proteins during meiosis. Cell Mol Life Sci 55: 437-449.
59. Edelmann W, Cohen PE, Kneitz B, Winand N, Lia M, et al. (1999) Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nature Genetics 21: 123-127.
60. Kneitz B, Cohen PE, Avdievich E, Zhu L, Kane MF, et al. (2000) MutS homolog 4 localization to meiotic chromosomes is required for chomosome pairing during meiosis in male and female mice. Genes and Development 14: 1085-1097.
61. Svetlanov A, Cohen PE (2004) Mismatch repair proteins, meiosis, and mice: understanding the complexities of mammalian meiosis. Exp Cell Res 296: 71-79.
62. Moens PB, Kolas NK, Tarsounas M. Marcon E, Cohen PE, et al. (2002) The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. J Cell Sci 115: 1611-1622.
63. Baker SM, Plug AW, Prolla TA, Bronner CE, Harris AC, et al. (1996) Involvement ofmouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet 13: 336-342.
64. Kolas, NK, Svetlanov A, Lenzi ML, Macaluso FP, Lipkin SM, et al. (2005) Localization of MMR proteins on meiotic chromosomes in mice indicates distinct functions during prophase I. J Cell Biol 171: 447-458.
65. Rotter V, Schwartz D, Almon E, Goldfinger N, Kapon A, et al. (1993) Mice with reduced levels of p53 protein exhibit the testicular giant-cell degenerative syndrome. Proc Natl Acad Sci U S A 90: 9075-9079. 66 Embree-Ku M, Boekelheide K (2002) Absence of p53 and FasL has sexually dimorphic effects on both development and reproduction. Exp Biol Med (Maywood), 227: 545-553.
66. Marty MS, Singh NP, Holsapple MP, Gollapudi BB (1999) Influence of p53 zygosity on select sperm parameters of the mouse. Mutat Res 427: 39-45.
67. Seo YR, Jung HJ (2004) The potential roles of p53 tumor suppressor in nucleotide excision repair (NER) and base excision repair (BER). Exp Mol Med 36: 505-509.
68. Rogakou EP, Pilch DR, Orr AH, Ivanova. VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868.
69. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, et al. (2000) A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 10: 886-895.
70. Shannon M, Lamerdin JE, Richardson L, McCutchen-Maloney SL, Hwang MR, et al. (19909) Characterization of the mouse Xpf DNA repair gene and differential expression during spermatogenesis. Genomics, 62: 427-435.
71. Weeda G, Ma L, van Ham RC, Bootsma D, van der Eb AJ, et al. (1991) Characterization of the mouse homolog of the XPBC/ERCC-3 gene implicated in xeroderma pigmentosum and Cockayne's syndrome. Carcinogenesis 12: 2361-2368.
72. Li L, Peterson C, Legerski R (1996) Sequence of the mouse XPC cDNA and genomic structure of the human XPC gene. Nucleic Acids Res 24: 1026-1028.
73. Sugasawa K, Ng JM, Masutani C, Iwai S, van der Spek PJ, et al. (1998) Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol Cell 2: 223-232.
74. Jansen HT, West C, Lehman MN,. Padmanabhan V (2001) Ovarian estrogen receptor-beta (ERbeta) regulation: I. Changes in ERbeta messenger RNA expression prior to ovulation in the ewe. Biol Reprod 65: 866-872.
75. Xu G, Spivak G, Mitchell DL, Mori T, McCarrey JR, et al. (2005) Nucleotide excision repair activity varies among murine spermatogenic cell types. Biol Reprod 73: 123-130.
76. de Vries A, van Costrom CT, Hofhuis FM, Dortant PM, Berg RJ, et al. (1995) Increased susceptibility to ultraviolet-B and carcinogens of mice lacking the DNA excision repair gene XPA. Nature 377: 169-173.
77. Nakane H, Takeuchi S, Yuba S, Saijo M, Nakatsu Y, et al. (1995) High incidence of ultraviolet-B-or chemical-carcinogen-induced skin tumours in mice lacking the xeroderma pigmentosum group A gene. Nature 377: 165-168.
78. Ng JM, Vrieling H, Sugasawa K, Ooms MP, Grootegoed JA, et al. (2002) Developmental defects and male sterility in mice lacking the ubiquitin-like DNA repair gene mHR23B. Mol Cell Biol 22: 1233-1245.
79. Waldbieser GC, Chrisman CL (1986) X-Y Chromosome Univalency in the Testes of Hyperthermic Mice: I. Concomitant Formation of Multinucleated Giant Cells. Gamete Research 15: 153-160.
80. van Zelst SJ, Zupp JL, Hayman DL, Setchell BP (1995) X-Y chromosome dissociation in mice and rats exposed to increased testicular or environmental temperatures. Reprod Fertil Dev 7: 1117-1121.
81. Krzanowska H (1989) X-Y chromosome dissociation in mouse strains differing in efficiency of spermatogenesis: elevated frequency of univalents in pubertal males. Gamete Res 23: 357-365.
82. Polanski Z (2000) Sex-dependent frequency and type of autosomal univalency at the first meiotic metaphase in mouse germ cells. J Reprod Fertil 119: 165-171.
83. Yin Y, Stahl BC, DeWolf WC, Morgentaler A (2002) P53 and Fas are sequential mechanisms of testicular germ cell apoptosis. J Androl 23: 64-70.
84. Nagata S, Golstein P (1995) The Fas death factor. Science 267: 1449-1456.
85. Erster S, Mihara M, Kim RH, Petrenko O, Moll UM (2004) In vivo mitochondrial p53 translocation triggers a rapid first wave of cell death in response to DNA damage that can precede p53 target gene activation. Mol Cell Biol 24: 6728-6741.