Absence of p53 and FasL has sexually dimorphic effects on both development and reproduction

Experimental Biology and Medicine

Volumn 227, Issue 7, 2002, Pages 545-553

  Embree Ku, Michelle ^a   Boekelheide, Kim ^a,b  

^a BROWN UNIVERSITY   (United States)

^b BROWN UNIVERSITY   (United States)

Author keywords

Apoptosis; Development; FasL; p53; Reproduction

Indexed keywords

FAS LIGAND; PROTEIN P53;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CHILDBIRTH; CONGENITAL MALFORMATION; CONTROLLED STUDY; CORPUS LUTEUM; DYSTOCIA; ESTRUS CYCLE; FEMALE; GENOTYPE; MALE; MALE FERTILITY; MOUSE; MOUSE STRAIN; NEURAL TUBE DEFECT; NEWBORN; NONHUMAN; PHENOTYPE; REPRODUCTION; SEX DIFFERENCE; SEXUAL DEVELOPMENT; SPERMATOGENESIS; SPERMATOZOON COUNT;

ANIMALIA;

EID: 0036655710     PISSN: 00379727     EISSN: None     Source Type: Journal    
DOI: 10.1177/153537020222700720     Document Type: Article

References (47)

1. Knudson CM, Tung KSK, Tourtellotte WG, Brown GAJ, Korsmeyer SJ. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270:96-98, 1995.
2. Perez GI, Robles R, Knudson CM, Flaws JA, Korsmeyer SJ, Tilly JL. Prolongation of ovarian lifespan into advanced chronological age by Bax-deficiency. Nat Genet 21:200-203, 1999.
3. Ratts VS, Flaws JA, Kolp R, Sorenson CM, Tilly JL. Ablation of bcl-2 gene expression decreases the numbers of oocytes and primordial follicles established in the post-natal female mouse gonad. Endocrinology 136:3665-3668, 1995.
4. Rodriguez I, Ody C, Araki K, Garcia I, Vassalli P. An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO J 16:2262-2270, 1997.
5. Furuchi T, Masuko K, Nishimune Y, Obinata M, Matsui Y. Inhibition of testicular germ cell apoptosis and differentiation in mice misexpressing bcl-2 in spermatogonia. Development 122:1703-1709, 1996.
6. Flaws JA, Hirshfield AN, Hewitt JA, Babus JK, Furth PA. Effect of bcl-2 on the primordial follicle endowment in the mouse ovary. Biol Reprod 64:1153-1159, 2001.
7. Hsu SY, Lai RJ, Finegold M, Hsueh AJ. Targeted over-expression of Bcl-2 in ovaries of transgenic mice leads to decreased follicle apoptosis, enhanced folliculogenesis, and increased germ cell tumorigenesis. Endocrinology 137:4837-4843, 1996.
8. Rodriguez I, Araki K, Khatib K, Martinou JC, Vassalli P. Mouse vaginal opening is an apoptosis-dependent process which can be prevented by the over expression of Bcl-2. Dev Biol 184:115-121, 1997.
9. Cohen PL, Eisenberg RA. Lpr and gld: single gene models of systemic autoimmunity and lymphoproliferative disease. Annu Rev Immunol 9:243-269, 1991.
10. Agarwal ML, Taylor WR, Chernov MV, Chernova OB, Stark GR. The p53 network. J Biol Chem 273:1-4, 1998.
11. Bellamy CO. p53 and apoptosis. Br Med Bull 53:522-538, 1997.
12. Makrigiannakis A, Amin K, Coukos G, Tilly JL, Coutifaris C. Regulated expression and potential roles of p53 and Wilms' tumor suppressor gene (WT1) during follicular development in the human ovary. J Clin Endocrinol Metab 85:449-459, 2000.
13. Tilly KI, Banerjee S, Banerjee PP, Tilly JL. Expression of the p53 and Wilms' tumor suppressor genes in the rat ovary: gonadotropin repression in vivo immunohistochemical localization of nuclear p53 protein to apoptotic granulosa cells of atretic follicles. Endocrinology 136:1394-1402, 1995.
14. Keren-Tal I, Suh BS, Dantes A, Lindner S, Oren M, Amsterdam A. Involvement of p53 expression in c2AMP-mediated apoptosis in immortalized granulosa cells. Exp Cell Res 218:283-295, 1995.
15. Kim JM, Yoon YD, Tsang BK. Involvement of the Fas/Fas ligand system in p53-mediated granulosa cell apoptosis during follicular development and atresia. Endocrinology 140:2307-2317, 1999.
16. Matsubara H, Ikuta K, Ozaki Y, Suzuki Y, Suzuki N, Sato T, Suzumori K. Gonadotropins and cytokines affect luteal function through control of apoptosis in human luteinized cells. J Clin Endocrinol Metab 85:1620-1626, 2000.
17. Hakuno N, Koji T, Yano T, Kobayashi N, Tsutsumi O, Taketani Y, Nakane PK. Fas/APO-1/CD95 system as a mediator of granulosa cell apoptosis in ovarian follicle atresia. Endocrinology 137:1938-1948, 1996.
18. Quirk SM, Cowan RG, Joshi SG, Henrikson KP. Fas antigen-mediated apoptosis in human granulosa/luteal cells. Biol Reprod 52:279-287, 1995.
19. Jose de los Santos M, Anderson DJ, Racowsky C, Hill JA. Presence of Fas-Fas ligand system and bcl-2 gene products in cells and fluids from gonadotropin-stimulated human ovaries. Biol Reprod 63:1811-1816, 2000.
20. Lee J, Richburg JH, Younkin SC, Boekelheide K. The Fas system is a key regulator of germ cell apoptosis in the testis. Endocrinology 138:2081-2088, 1997.
21. Xu JP, Li X, Mori E, Guo MW, Matsuda I, Takaichi H, Amano T, Mori T. Expression of Fas-Fas ligand in murine testis Am J Reprod Immunol 42:381-388, 1999.
22. Rotter V, Schwartz D, Almon E, Goldfinger N, Kapon A, Meshorer A, Donehower LA, Levine AJ. Mice with reduced levels of p53 protein exhibit the testicular giant-cell degenerative syndrome. Proc Natl Acad Sci U S A 90:9075, 1993.
23. Sjoblom T, Lahdetie J. Expression of p53 in normal and gamma-irradiated rat testis suggests a role for p53 in meiotic recombination and repair. Oncogene 12:2499-2505, 1996.
24. Beumer TL, Roepers-Gajadien HL, Gademan IS, van Buul PP, Gil-Gomez G, Rutgers DH, de Rooij DG. The role of the tumor suppressor p53 in spermatogenesis. Cell Death Differ 5:669-677, 1998.
25. Koji T, Hishikawa Y, Ando H, Nakanishi Y, Kobayashi N. Expression of Fas and Fas ligand in normal and ischemia-reperfusion testes: involvement of the Fas system in the induction of germ cell apoptosis in the damaged mouse testis. Biol Reprod 64:946-954, 2001.
26. Wang R-A, Nakane PK, Koji T. Autonomous cell death of mouse male germ cells during fetal and postnatal period. Biol Reprod 58:1250-1256, 1998.
27. Hunt JS, Vassmer D, Ferguson TA, Miller L. Fas ligand is positioned in mouse uterus and placenta to prevent trafficking of activated leukocytes between mother and the conceptus. J Immunol 158:4122-4128, 1997.
28. Chaouat G, Clark DA. FAS/FAS ligand interaction at the placental interface is not required for the success of allogeneic pregnancy in anti-paternal MHC pre-immunized mice. Am J Reprod Immunol 45:108-115, 2001.
29. Yin Y, Stahl BC, DeWolf WC, Morgentaler A. p53-mediated germ cell quality control in spermatogenesis. Dev Biol 204:165-171, 1998.
30. Richburg JH, Nanez A, Williams LR, Embree ME, Boekelheide K. Sensitivity of testicular germ cells to toxicant-induced apoptosis in gld mice that express a nonfunctional form of Fas ligand. Endocrinology 141:787-793, 2000.
31. Sah VP, Attardi LD, Mulligan GJ, Williams BO, Bronson RT, Jacks T. A subset of p53-deficient embryos exhibits exencephaly. Nat Genet 10:175-180, 1995.
32. Armstrong JF, Kaufman MH, Harrison DJ, Clarke AR. High-frequency developmental abnormalities in p53-deficient mice. Curr Biol 5:931-936, 1995.
33. Copp AJ. Genetic models of mammalian neural tube defects. CIBA Found Syrup 181:118-143, 1994.
34. Jacks T, Remington L, Williams BO. Tumor spectrum analysis in p53-mutant mice. Curr Biol 4:1-4, 1994.
35. Takahashi T, Tanaka M, Brannan CI, Jenkins NA, Copeland NG, Suda T, Nagata S. Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell 76:969-976, 1994.
36. Schneider P, Bodmer J-L, Holler N, Mattmann C, Scuderi P, Terskikh A, Peitsch MC, Tscopp J. Characterization of Fas (Apo-1, CD95)-Fas ligand interaction. J Biol Chem 272:18827-18833, 1997.
37. Cheng LE-C, Chan FK-M, Cado D, Winoto A. Functional redundancy of the Nur77 and Nor-1 orphan steroid receptors in T-cell apoptosis. EMBO J 16:1865-1875, 1997.
38. Blazak WF, Treinen KA, Juniewicz PE. Application of testicular sperm head counts in the assessment of male reproductive toxicity. In: Chapin RE, Heindel J, Eds. Methods in Toxicology. New York: Academic Press, Vol 3A:pp86-105, 1993.
39. Kalter H. Sporadic congenital malformations of newborn inbred mice. Teratology 1:193-200, 1968.
40. Dagg CP. Teratogenesis. In: Green EL, Ed. Biology of the Laboratory Mouse. New York: McGraw-Hill, pp309-328, 1966.
41. Robinson ML, Holmgren A, Dewey MJ. Genetic control of ocular morphogenesis: defective lens development associated with ocular anomalies in C57BL/6 mice. Exp Eye Res 56:7-16, 1993.
42. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA Jr., Butel JS, Bradley A. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356:215-221, 1992.
43. Tilly KI, Banerjee S, Banerjee PP, Tilly JL. Expression of the p53 and Wilms' tumor suppressor genes in the rat ovary: gonadotropin repression in vivo and immunohistochemical localization of nuclear p53 protein to apoptotic granulosa cells of atretic follicles. Endocrinology 136:1394-1402, 1995.
44. Yu CL, Driggers P, Barrera-Hernandez G, Nunez SB, Segars JH, Cheng S. The tumor suppressor p53 is a negative regulator of estrogen receptor signaling. Biochem Biophys Res Commun 239:617-620, 1997.
45. Seller MJ. Neural tube defects and sex ratios. Am J Med Genet 26:699-707, 1987.
46. Seller MJ, Perkins-Cole KJ. Sex difference in mouse embryonic development at neurulation. J Reprod Fertil 79:159-161, 1987.
47. Yin Y, Stahl BC, DeWolf WC, Morgentaler A. P53 and Fas are sequential mechanisms of testicular germ cell apoptosis. J Androl 23:64-70, 2002.