Morphogenetic investigation of metaphase-specific cell death in meiotic spermatocytes in mice

Anatomical Science International

Volumn 80, Issue 3, 2005, Pages 141-152

  Kon, Yasuhiro ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Apoptosis; Exonuclease 1; Meiosis; MRL MpJ mice; Spermatogenesis

Indexed keywords

APOPTOSIS; ARTHRITIS; AUTOIMMUNITY; CELL DEATH; CELL STRUCTURE; COLLAGEN DISEASE; GENETIC ANALYSIS; GLOMERULONEPHRITIS; HEAT STRESS; MEIOSIS; METAPHASE; MORPHOGENESIS; MUTANT; NONHUMAN; OOCYTE; PRIORITY JOURNAL; REVIEW; SIALOADENITIS; SPERMATOCYTE; STRAIN DIFFERENCE; SYSTEMIC VASCULITIS; TESTIS; ANIMAL; C57BL MOUSE; CHROMOSOME MAP; CYTOLOGY; ENZYMOLOGY; GENETICS; HEAT SHOCK RESPONSE; MALE; METABOLISM; MOUSE; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; MUTATION; NICK END LABELING; PHYSIOLOGY; SEMINIFEROUS TUBULE; SPECIES DIFFERENCE; ULTRASTRUCTURE;

EXODEOXYRIBONUCLEASE; EXODEOXYRIBONUCLEASE I;

ANIMALS; APOPTOSIS; CHROMOSOME MAPPING; EXODEOXYRIBONUCLEASES; HEAT-SHOCK RESPONSE; IN SITU NICK-END LABELING; MALE; MEIOSIS; METAPHASE; MICE; MICE, INBRED C57BL; MICE, INBRED MRL LPR; MUTATION; SEMINIFEROUS TUBULES; SPECIES SPECIFICITY; SPERMATOCYTES;

EID: 25144462138     PISSN: 14476959     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1447-073x.2005.00117.x     Document Type: Review

References (78)

1. Allan DJ, Harmon BV, Kerr JFR (1987) Cell death in spermatogenesis. In: Perspectives on Mammalian Cell Death (Rotten CS, ed.). Oxford University Press, Oxford, 229-58.
2. Allan DJ, Harmon BV, Roberts SA (1992) Spermatogonial apoptosis has three morphologically recognizable phases and shows no circadian rhythm during normal spermatogenesis in the rat. Cell Prolif 25, 241-50.
3. Animal Care Committee in Graduate School of Veterinary Medicine, Hokkaido University (2003) Guide for the Care and Use of Laboratory Animals. Hokkaido University, Graduate School of Veterinary Medicine, Sapporo.
4. Bertuch AA, Lundblad V (2004) EXO1 contributes to telomere maintenance in both telomerase-proficient and telomerase-deficient Saccharomyces cerevisiae. Genetics 166, 1651-9.
5. Billing H, Furuta I, Rivier C, Tapanainen J, Parvinen M, Hsueh AJW (1995) Apoptosis in testis germ cells: Developmental changes in gonadotropin dependence and localization to selective tubule stages. Endocrinology 136, 5-12.
6. Blanco-Rodriguez J, Martinez-Garcia C (1996) Spontaneous germ cell death in the testis of the adult rat takes the form of apoptosis: Re-evaluation of cell types that exhibit the ability to die during spermatogenesis. Cell Prolif 29, 13-31.
7. Breathnach R, Chambon P (1981) Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem 50, 349-83.
8. Brick JE, Walker SE, Wise KS (1988) Hormone control of autoantibodies to calf thymus nuclear extract (CTE) and DNA in MRL-lpr and MRL-+/+ mice. Clin Immunol lmmunopathol 46, 68-81.
9. Brinkworth MH, Weibauer GF, Schlatt S, Nieschlag E (1995) Identification of male germ cells undergoing apoptosis in adult rats. J Reprod Fertil 105, 25-33.
10. Buja LM, Eigenbrodt ML, Eigenbrodt EH (1993) Apoptosis and necrosis. Basic types and mechanisms of cell death. Arch Pathol Lab Med 117, 1208-14.
11. Clark AM, Maguir SM, Griswold MD (1997) Accumulation of clusterin/sulfated glycoprotein-2 in degenerating pachytene spermatocytes of adult rats treated with methoxyacetic acid. Biol Reprod 57, 837-46.
12. Collins JA, Schandl CA, Young KK, Vesely J, Willingham MC (1997) Major DNA fragmentation is a late event in apoptosis. J Histochem Cytochem 45, 923-34.
13. de Kretser DM, Kerr JB (1994) The cytology of the testis. In: The Physiology of Reproduction, 2nd edn. (Knobil E, Neill JP, eds). Raven Press, New York, 1177-290.
14. + thymocytes and activated mature lymphocytes in normal mice but not in the lupus-prone strain, MRL lpr/lpr. Proc Natl Acad Sci USA 90, 10 340-4.
15. Elledge SJ (1996) Cell cycle checkpoints: Preventing an identity crisis. Science 274, 1664-72.
16. Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119, 493-501.
17. Gerschenson LE, Rotello RJ (1992) Apoptosis: A different type of cell death. FASEB J 6, 2450-5.
18. Gorbsky GJ, Ricketts WA (1993) Differential expression of a phosphoepitope at the kinetochores of moving chromosomes. J Cell Biol 122, 1311-21.
19. Gosh S, Bartke A, Grasso P, Reichert LE, Russell LD (1992) Structural manifestations of the rat Sertoli cell to hypophysectomy: A correlative morphometric and endocrine study. Endocrinology 131, 485-97.
20. Greider CW (1996) Telomere length regulation. Annu Rev Biochem 65, 337-65.
21. Hartwell LH, Weinert TA (1989) Checkpoints: Controls that ensure the order of cell cycle events. Science 246, 629-34.
22. Hasegawa M, Wilson G, Russell LD, Meistrich ML (1997) Radiation-induced cell death in the mouse testis: Relationship to apoptosis. Radiat Res 147, 457-67.
23. Hermeking H, Lengauer C, Polyak K et al. (1997) 14-3-3σ is a p53-regulated inhibitor of G2/M progression. Mol Cell 1, 3-11.
24. Hoyt MA, Totis L, Roberts BT (1991) S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 66, 519-31.
25. Jacks T, Weinberg RA (1996) Cell cycle control and its watchman. Nature 381, 643-4.
26. Johnson L, Nguyen HB, Petty C, Neaves WB (1987) Quantification of human spermatogenesis: Germ cell degeneration during spermatocytogenesis and meiosis in testes from younger and older adult men. Biol Reprod 37, 739-47.
27. Kazusa K, Namiki Y, Asano A, Kon Y, Endoh D, Agui T (2004) Differences in spermatogenesis in cryptorchid testes among various strains of mice. Comp Med 54, 179-84.
28. Kodaira K, Takahashi R, Hirabayashi M, Suzuki T, Obinata M, Ueda M (1996) Overexpression of c-myc induces apoptosis at the prophase of meiosis of rat primary spermatocytes. Mol Reprod Dev 45, 403-10.
29. Kon Y, Endoh D (2000) Morphological study of metaphase-specific apoptosis in MRL mouse testis. Anat Histol Embryol 29, 313-19.
30. Kon Y, Endoh D (2001) Heat-shock resistance in experimental cryptorchid testis of mice. Mol Reprod Dev 58, 216-22.
31. Kon Y, Horikoshi H, Endoh D (1999) Metaphase-specific cell death in meiotic spermatocytes in mice. Cell Tissue Res 296, 359-69.
32. Krämer A (1996) The structure and function of proteins involved mammalian pre-mRNA splicing. Annu Rev Biochem 65, 367-409.
33. Lee BI, Wilson III DM (1999) The RAD2 domain of human exonuclease I exhibits 5′ to 3′ exonuclease and flap structure-specific endonuclease activities. J Biol Chem 274, 37 763-9.
34. Lee BI, Shannon M, Stubbs L, Wilson III DM (1999) Expression specificity of the mouse exonuclease 1 (mExo1) gene. Nucleic Acids Res 27, 4114-20.
35. Lee J, Richburg JH, Younkin SC, Boekelheide K (1997) The fas system is a key regulator of germ cell apoptosis in the testis. Endocrinology 136, 2081-8.
36. Lee K, Wolgemuth DJ (1998) The role of transcriptional control during spermatogenesis. J Androl 19, 639-49.
37. Leferovich JM, Bedelbaeva K, Samulewicz S et al. (2001) Heart regeneration in adult MRL mice. Proc Natl Acad Sci USA 98, 9830-5.
38. Loveland KL, Schlatt S (1997) Stem cell factor and c-kit in the mammalian testis: Lessons originating from Mother Nature's gene knockouts. J Endocrinol 153, 337-44.
39. Maringele L, Lyndall D (2004) EXO1 plays a role in generating type I and type II survivors in budding yeast. Genetics 166, 1641-9.
40. Masinde G, Li X, Gu W, Davidson H, Mohan S, Baylink DJ (2001) Identification of wound healing/regeneration quantitative trait loci (QTL) at multiple time points that explain seventy percent of variance in (MRL/MpJ and SJL/J) mice F2 population. Genome Res 11, 2027-33.
41. McBreaty BA, Clark LD, Zhang XM, Blankenhorn EP, Heber-Katz E (1998) Genetic analysis of a mammalian wound-healing trait. Proc Natl Acad Sci USA 95, 11 792-7.
42. Mori C, Nakamura N, Dix DJ et al. (1997) Morphological analysis of germ cell apoptosis during postnatal testis development in normal and Hsp70-2 knockout mice. Dev Dyn 208, 125-36.
43. Murphy ED (1981) Lymphoproliferation (lpr) and other single-locus models for murine lupus. In: Immunologic Defects in Laboratory Animals (Gershwin ME, Merchant B, eds). Plenum Press, New York, 143-73.
44. Murray AW (1995) The genetics of cell cycle checkpoints. Curr Opin Genet Dev 5, 5-11.
45. Murray AW, Kirschner MW (1989) Cyclin synthesis drives the early embryonic cell cycle. Nature 339, 275-80.
46. Namiki Y, Endoh D, Kon Y (2003) Genetic mutation associated with meiotic metaphase-specific apoptosis in MRL/MpJ mice. Mol Reprod Dev 64, 179-88.
47. Namiki Y, Kon Y, Sasaki N, Agui T, Endoh D (2004) Exon skipping of exonuclease 1 in MRL/MpJ mice is caused by a nucleotide substitution of the branchpoint sequence in intron eight. Jpn J Vet Res 52, 125-34.
48. Namiki Y, Kon Y, Kazusa K, Asano A, Sasaki N, Agui T (2005) Quantitative trait loci analysis of heat stress resistance of spermatocytes in the MRL/MpJ mouse. Mamm Genome 16, 96-102.
49. Nantel F, Monaco L, Foulkes NS et al. (1996) Spermiogenesis deficiency and germ-cell apoptosis in CREM-mutant mice. Nature 380, 159-62.
50. Nicklas RB, Ward SC, Gorbshy GJ (1995) Kinetochore chemistry is sensitive to tension and may link mitotic forces to a cell cycle checkpoint. J Cell Biol 130, 929-39.
51. Nose M, Terada M, Nishihara M et al. (2000) Genome analysis of collagen disease in MRL/lpr mice: Polygenic inheritance resulting in the complex pathological manifestations. Int J Cardiol 75, S53-S61.
52. Ohta Y, Nishikawa A, Fukazawa Y et al. (1996) Apoptosis in adult mouse testis induced by experimental cryptorchidism. Acta Anat 157, 195-204.
53. Paulovich AG, Toczyski DP, Hartwell LH (1997) When checkpoints fail. Cell 88, 315-21.
54. Peng CY, Graves PR, Thoma RS, Wu Z, Shaw AS, Piwnica-Worms H (1997) Mitotic and G2 checkpoint control: Regulation of 14-3-3 protein binding by phosphorylation of cdc25c on serine-216. Science 277, 1501-5.
55. Qiu J, Guan MX, Balis AM, Shen B (1998) Saccharomyces cerevisiae exonuclease-1 play s a role in UV resistance that is distinct from nucleotide excision repair. Nucleic Acids Res 26, 3077-83.
56. Qiu J, Qian Y, Chen V, Guan MX, Shen B (1999) Human exonuclease 1 functionally complements its yeast homologues in DNA recombination, RNA primer removal, and mutation avoidance. J Biol Chem 274, 17 893-900.
57. Rieder CL, Cole RW, Khodjakov A, Sluder G (1995) The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores. J Cell Biol 130, 941-8.
58. Russell LD, Clermont Y (1977) Degeneration of germ cells in normal, hypophysectomized and hormone treated hypophysectomized rats. Anat Rec 187, 347-66.
59. Russell LD, Alger BV, Nequin LG (1987) Hormonal control of pubertal spermatogenesis. Endocrinology 120, 1615-32.
60. Russell LD, Etllin RA, Sinha-Hikim AP, Clegg ED (1990a) Histological and Histopathological Evaluation of the Testis. Cache River Press, Clearwater.
61. Russell LD, Ren HP, Hikim IS, Schulze W, Hikim APS (1990b) A comparative study in twelve mammalian species of volume densities, volumes, and numerical densities of selected testis components, emphasizing those related to the sertoli cell. Am J Anat 188, 21-30.
62. Russell LD, Corbin TJ, Ren HP, Amador A, Bartke A, Gosh S (1992) Structural changes in rat Leydig cells posthypophysectomy: A morphometric and endocrine study. Endocrinology 131, 498-508.
63. Sanchez Y, Wong C, Thoma RS et al. (1997) Conservation of the Chk1 checkpoint pathway in mammals: Linkage of DNA damage to cdk regulation through cdc25. Science 277, 1497-501.
64. Searle J, Kerr JFR, Bishop CJ (1982) Necrosis and apoptosis: Distinct models of cell death with fundamentally different significance. Pathol Annu 17, 229-59.
65. Steger K (1999) Transcriptional and translational regulation of gene expression in haploid spermatids. Anat Embryol 199, 471-87.
66. Szankasi P, Smith GR (1995) A role for exonuclease 1 from S. pombe in mutation avoidance and mismatch correction. Science 267, 1166-9.
67. Tapanainen JS, Tilly JL, Vihko KK, Hsueh AJW (1993) Hormonal control of apoptotic cell death in the testis: Gonadotropins and androgens as testicular cell survival factors. Mol Endocrinol 7, 643-50.
68. Tishkoff DX, Boerger AL, Bertrand P et al. (1997) Identification and characterization of Saccharomyces cerevisiae EXO1, a gene encoding an exonuclease that interacts with Msh2. Proc Natl Acad Sci USA 94, 7487-92.
69. Tran RT, Erdeniz N, Symington LS, Liskay RM (2004) EXO1-A multi-tasking eukaryotic nuclease. DNA Repairs, 1549-59.
70. Vasen HFA, Watson P, Mecklin JP, Lynch HT, International Collaborative Group-Hereditary Nonpolyposis Colorectal Cancer (1999) New clinical criteria for hereditary nonpolyposis colorectal cancer (HNPCC, Lynch syndrome) proposed by the International Colaborative Group on HNPCC. Gastroenterology 116, 1453-6.
71. Wei K, Clark A, Wong E et al. (2003) Inactivation of exonuclease 1 in mice results in DNA mismatch repair defects, increased cancer susceptibility, and male and female sterility. Genes Dev 17, 603-14.
72. Weinberg RA (1995) The retinoblastoma protein and cell cycle control. Cell 81, 323-30.
73. Weiss E, Winey M (1996) The Saccharomyces cerevisiae spindle pole body duplication gene MPS1 is part of a mitotic checkpoint. J Cell Biol 132, 111-23.
74. Wellinger RJ, Wolf AJ, Zakian VA (1993) Saccharomyces telomeres acquire single-strand TGI-3 tails in S phase. Cell 72, 51-60.
75. Wing T-Y, Christensen AK (1982) Morphometric studies on rat seminiferous tubules. Am J Anat 165, 13-25.
76. Wu Y, Berends MJW, Post JG et al. (2001) Germline mutations of EXO1 gene in patients with hereditary nonpolyposis colorectal cancer (HNPCC) and atypical HNPCC forms. Gastroenterology 120, 1580-7.
77. Yan H, Papadopoulos N, Merra G et al. (2000) Conversion of dipoidy to haploidy. Nature 403, 723-4.
78. Yin Y, Hawkins KL, Dewolf WC, Morgentaler A (1997) Heat stress causes testicular germ cell apoptosis in adult mice. J Androl 18, 159-65.