Induction of Apoptosis Involving Multiple Pathways Is a Primary Response to Cyclin A1-Deficiency in Male Meiosis

Developmental Dynamics

Volumn 234, Issue 1, 2005, Pages 114-123

  Salazar, Glicella ^a   Joshi, Ayesha ^a   Liu, Dong ^a   Wei, Hongquan ^a   Persson, Jenny Liao ^a   Wolgemuth, Debra J ^a  

^a College of Physicians and Surgeons ^*  (United States)

Author keywords

Apoptosis; Cell cycle; Cyclin A1; Gene knockout; Germ cells; Male sterility; Meiosis

Indexed keywords

CASPASE 3; CYCLIN A; CYCLIN A1; PROTEIN BAX; PROTEIN P53; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE G2 PHASE; CELL DEATH; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVATION; GERM CELL; MALE; MALE STERILITY; MEIOSIS; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SEMINIFEROUS TUBULE; SPERMATOCYTE; SPERMATOGENESIS; TESTIS;

ANIMALS; APOPTOSIS; CASPASE 3; DNA FRAGMENTATION; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; MALE; MEIOSIS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SPERMATOCYTES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 23944503265     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/dvdy.20533     Document Type: Article

References (59)

1. Ahuja HS, Zhu Y, Zakeri Z. 1997. Association of cyclin-dependent kinase 5 and its activator p35 with apoptotic cell death. Dev Genet 21:258-267.
2. Almon E, Goldfinger N, Kapon A, Schwartz D, Levine AJ, Rotter V. 1993. Testicular tissue-specific expression of the p53 suppressor gene. Dev Biol 156:107-116.
3. An S, Park MJ, Park IC, Hong SI, Knox K. 2003. Procaspase-3 and its active large subunit localized in both cytoplasm and nucleus are activated following application of apoptotic stimulus in Ramos-Burkitt lymphoma B cells. Int J Mol Med 12:311-317.
4. Antonsson B, Montessuit S, Sanchez B, Martinou JC. 2001. Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J Biol Chem 276:11615-11623 Epub 2001 Jan 2.
5. Barlow C, Brown KD, Deng CX, Tagle DA, Wynshaw-Boris A. 1997. Atm selectively regulates distinct p53-dependent cell-cycle checkpoint and apoptotic pathways. Nat Genet 17:453-456.
6. Baudat F, Manova K, Yuen JP, Jasin M, Keeney S. 2000. Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking spo11. Mol Cell 6:989-998.
7. Beumer TL, Roepers-Gajadien HL, Gademan IS, van Buul PP, Gil-Gomez G, Rutgers DH, de Rooij DG. 1998. The role of the tumor suppressor p53 in spermatogenesis. Cell Death Differ 5:669-677.
8. Beumer TL, Roepers-Gajadien HL, Gademan IS, Lock TM, Kal HB, De Rooij DG. 2000. Apoptosis regulation in the testis: involvement of Bcl-2 family members. Mol Reprod Dev 56:353-359.
9. Burns TF, El-Deiry WS. 1999. The p53 pathway and apoptosis. J Cell Physiol 181:231-239.
10. Carambula SF, Matikainen T, Lynch MP, Flavell RA, Goncalves PB, Tilly JL, Rueda BR. 2002. Caspase-3 is a pivotal mediator of apoptosis during regression of the ovarian corpus luteum. Endocrinology 143:1495-1501.
11. Chang HY, Yang X. 2000. Proteases for cell suicide: functions and regulation of caspases. Microbiol Mol Biol Rev 64:821-846.
12. Cory S, Adams JM. 2002. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2:647-656.
13. Dix DJ, Allen JW, Collins BW, Poorman-Allen P, Mori C, Blizard DR, Brown PR, Goulding EH, Strong BD, Eddy EM. 1997. HSP70-2 is required for desynapsis of synaptonemal complexes during meiotic prophase in juvenile and adult mouse spermatocytes. Development 124:4595-4603.
14. Edelmann W, Cohen PE, Kane M, Lau K, Morrow B, Bennett S, Umar A, Kunkel T, Cattoretti G, Chaganti R, Pollard JW, Kolodner RD, Kucherlapati R. 1996. Meiotic pachytene arrest in MLH1-deficient mice. Cell 85:1125-1134.
15. Furuchi T, Masuko K, Nishimune Y, Obinata M, Matsui Y, 1996. Inhibition of testicular germ cell apoptosis and differentiation in mice misexpressing Bcl-2 in spermatogonia. Development 122:1703-1709.
16. Handel MA, Cobb J, Eaker S. 1999. What are the spermatocyte's requirements for successful meiotic division? J Exp Zool 285:243-250.
17. Haupt S, Berger M, Goldberg Z, Haupt Y. 2003. Apoptosis - the p53 network. J Cell Sci 116:4077-4085.
18. Hsu YT, Youle RJ. 1998. Bax in murine thymus is a soluble monomeric protein that displays differential detergent-induced conformations. J Biol Chem 273:10777-10783.
19. Jahnukainen K, Chrysis D, Hou M, Parvinen M, Eksborg S, Soder O. 2004. Increased apoptosis occurring during the first wave of spermatogenesis is stage-specific and primarily affects mid-pachytene spermatocytes in the rat testis. Biol Reprod 70:290-296 Epub 2003 Oct 1.
20. Jordan SA, Speed RM, Bernex F, Jackson IJ. 1999. Deficiency of Trp53 rescues the male fertility defects of Kit(W-v) mice but has no effect on the survival of melanocytes and mast cells. Dev Biol 215:78-90.
21. Kannan K, Krishnamurthy J, Feng J, Nakajima T, Tsuchida N, Shanmugam G. 2000. Mutation profile of the p53, fhit, p16INK4a/p19ARF and H-ras genes in Indian breast carcinomas. Int J Oncol 17:1031-1035.
22. Kirn JM, Luo L, Zirkin BR. 2000. Caspase-3 activation is required for Leydig cell apoptosis induced by ethane dimethanesulfonate. Endocrinology 141:1846-1853.
23. Kim JM, Ghosh SR, Weil AC, Zirkin BR. 2001. Caspase-3 and caspase-activated deoxyribonuclease are associated with testicular germ cell apoptosis resulting from reduced intratesticular testosterone. Endocrinology 142:3809-3816.
24. Knudson CM, Tung KS, Tourtellotte WG, Brown GA, Korsmeyer SJ. 1995. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270:96-99.
25. Koji T. 2001. Male germ cell death in mouse testes: possible involvement of Fas and Fas ligand. Med Electron Microsc 34:213-222.
26. Kojima S, Hatano M, Okada S, Fukuda T, Toyama Y, Yuasa S, Ito H, Tokuhisa T. 2001. Testicular germ cell apoptosis in Bcl6-deficient mice. Development 128:57-65.
27. Kuida K, Zheng TS, Na S, Kuan C, Yang D, Karasuyama H, Rakic P, Flavell RA. 1996. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384:368-372.
28. Lee J, Richburg JH, Younkin SC, Boekelheide K. 1997. The Fas system is a key regulator of germ cell apoptosis in the testis. Endocrinology 138:2081-2088.
29. Liu D, Matzuk MM, Sung WK, Guo Q, Wang P, Wolgemuth DJ. 1998. Cyclin A1 is required for meiosis in the male mouse. Nat Genet 20:377-380.
30. Ludwig T, Chapman DL, Papaioannou VE, Efstratiadis A, 1997. Targeted mutations of breast cancer susceptibility gene homologs in mice; lethal phenotypes of Brca1, Brca2, Brca1/Brca2, Brca1/p53, and Brca2/p53 nullizygous embryos. Genes Dev 11:1226-1241.
31. Mandal M, Adam L, Mendelsohn J, Kumar R. 1998. Nuclear targeting of Bax during apoptosis in human colorectal cancer cells. Oncogene 17:999-1007.
32. Matsui Y, Nagano R, Obinata M. 2000. Apoptosis of fetal testicular cells is regulated by both p53-dependent and independent mechanisms. Mol Reprod Dev 55:399-405.
33. Meehan T, Loveland KL, de Kretser D, Cory S, Print CG. 2001. Developmental regulation of the bcl-2 family during spermatogenesis: insights into the sterility of bcl-w-/- male mice. Cell Death Differ 8:225-233.
34. Moroni MC, Hickman ES, Denchi EL, Caprara G, Colli E, Cecconi F, Muller H, Helin K. 2001. Apaf-1 is a transcriptional target for E2F and p53. Nat Cell Biol 3:552-558.
35. Nakano K, Vousden KH. 2001. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 7:683-694.
36. Nechushtan A, Smith CL, Hsu YT, Youle RJ. 1999. Conformation of the Bax C-terminus regulates subcellular location and cell death. EMBO J 18:2330-2341.
37. Nechushtan A, Smith CL, Lamensdorf I, Yoon SH, Youle RJ. 2001. Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J Cell Biol 153:1265-1276.
38. Oda E, Ohki R, Murasawa H, Nemoto J, Shibue T, Yamashita T, Tokino T, Taniguchi T, Tanaka N. 2000. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 288:1053-1058.
39. Orrenius S, Zhivotovsky B, Nicotera P. 2003. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 4:552-565.
40. Print CG, Loveland KL. 2000. Germ cell suicide: new insights into apoptosis during spermatogenesis. Bioessays 22:423-430.
41. Ramuz O, Isnardon D, Devilard E, Charafe-Jauffret E, Hassoun J, Birg F, Xerri L. 2003. Constitutive nuclear localization and initial cytoplasmic apoptotic activation of endogenous caspase-3 evidenced by confocal microscopy. Int J Exp Pathol 84:75-81.
42. Rubles AI, Bemmels NA, Foraker AB, Harris CC. 2001. APAF-1 is a transcriptional target of p53 in DNA damage-induced apoptosis. Cancer Res 61:6660-6664.
43. Rodriguez I, Ody C, Araki K, Garcia I, Vassalli P. 1997. An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO J 16:2262-2270.
44. Romanienko PJ, Camerini-Otero RD. 2000. The mouse spoil gene is required for meiotic chromosome synapsis. Mol Cell 6:975-987.
45. Salazar G, Liu D, Liao C, Batkiewicz L, Arbing R, Chung SS, Lele K, Wolgemuth DJ. 2003. Apoptosis in male germ cells in response to cyclin A1-deficiency and cell cycle arrest. Biochem Pharmacol 66:1571-1579.
46. Shi SR, Key ME, Kalra KL. 1991. Antigen retrieval in formalin-fixed, paraffin-embedded tissues: an enhancement method for immunohistochemical staining based on microwave oven heating of tissue sections. J Histochem Cytochem 39:741-748.
47. Sugiyama N, Obinata M, Matsui Y. 2001. Bcl-2 inhibits apoptosis of spermatogonia and growth of spermatogonial stem cells in a cell-intrinsic manner. Mol Reprod Dev 58:30-38.
48. Sweeney C, Murphy M, Kubelka M, Ravnik SE, Hawkins CF, Wolgemuth DJ, Carrington M. 1996. A distinct cyclin A is expressed in germ cells in the mouse. Development 122:53-64.
49. Thornborrow EC, Patel S, Mastropietro AE, Schwartzfarb EM, Manfredi JJ. 2002. A conserved intronic response element mediates direct p53-dependent transcriptional activation of both the human and murine bax genes. Oncogene 21:990-999.
50. Toscani A, Mettus RV, Coupland R, Simpkins H, Litvin J, Orth J, Hatton KS, Reddy EP. 1997. Arrest of spermatogenesis and defective breast development in mice lacking A-myb. Nature 386:713-717.
51. Vera Y, Diaz-Romero M, Rodriguez S, Lue Y, Wang C, Swerdloff RS, Sinha Hikim AP. 2004. Mitochondria-dependent pathway is involved in heat-induced male germ cell death: lessons from mutant mice. Biol Reprod 70:1534-1540.
52. Wolgemuth DJ. 2003. Insights into regulation of the mammalian cell cycle from studies on spermatogenesis using genetic approaches in animal models. Cytogenet Genome Res 103:256-266.
53. Wolgemuth DJ, Rhee K, Wu S, Ravnik SE. 1995. Genetic control of mitosis, meiosis and cellular differentiation during mammalian spermatogenesis. Reprod Fertil Dev 7:669-683.
54. Woolveridge I, de Boer-Brouwer M, Taylor MF, Teerds KJ, Wu FC, Morris ID. 1999. Apoptosis in the rat spermatogenic epithelium following androgen withdrawal: changes in apoptosis-related genes. Biol Reprod 60:461-470.
55. Xu Y, Ashley T, Brainerd EE, Bronson RT, Meyn MS, Baltimore D. 1996. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev 10:2411-2422.
56. Yamamoto CM, Sinha Hikim AP, Huynh PN, Shapiro B, Lue Y, Salameh WA, Wang C, Swerdloff RS. 2000. Redistribution of Bax is an early step in an apoptotic pathway leading to germ cell death in rats, triggered by mild testicular hyperthermia. Biol Reprod 63:1683-1690.
57. Yan W, Samson M, Jegou B, Toppari J. 2000. Bcl-w forms complexes with Bax and Bak, and elevated ratios of Bax/ Bcl-w and Bak/Bcl-w correspond to spermatogonial and spermatocyte apoptosis in the testis. Mol Endocrinol 14:682-699.
58. Yin Y, DeWolf WC, Morgentaler A. 1998. Experimental cryptorchidism induces testicular germ cell apoptosis by p53-dependent and -independent pathways in mice. Biol Reprod 58:492-496.
59. Yu Q, Brain J, Laneuville P, Osmond DG. 2001. Suppressed apoptosis of pre-B cells in bone marrow of pre-leukemic p190bcr/ abl transgenic mice. Leukemia 15:819-827.