- Revue
- Apoptose
- Published:
Mort programmée des cellules germinales testiculaires: causes et mécanismes mis en jeu
Apoptotic process in testicular germ cells: causes and mechanisms
Andrologie volume 15, pages 263–277 (2005)
Résumé
La spermatogenèse résulte d'un équilibre entre prolifération et apoptose. Si cet équilibre est rompu il peut conduire à certaines pathologies testiculaires: cancers testiculaires, infertilités. L'apoptose semble être particulièrement importante lors de la spermatogenèse puisque 60 à 75% des cellules germinales formées n'atteignent pas le stade spermatozoïde.
Dans les cellules germinales de rongeurs ou bien humaines, les différentes molécules de l'apoptose ont été détectées: caspases effectrices qui sont au cœur du processus et en amont les protéines de la voie des récepteurs de mort ou de la voie mitochondriale. Selon le type d'apoptose des cellules germinales (apoptose physiologique, induite par un retrait hormonal, par des lésions chimiques ou physiques), une ou les différentes voies entrent en jeu.
Enfin, dans différentes pathologies testiculaires humaines, les voies de l'apoptose et particulièrement les caspases semblent être impliquées.
Abstract
Spermatogenesis results from a balance between proliferation and apoptosis. An alteration in this balance could lead to testicular diseases such as testicular tumour or infertility. Apoptosis seem to be important in regulating the processes of spermatogenesis since 60 to 75% of germ cells do not reach the spermatozoa stage. The various molecules of the apoptotic cascade have been detected in rodent or human germ cells, such as effector caspases and upstream proteins from cell death receptor or mitochondrial pathways. One or several different pathways may be involved in the germ cell apoptotic process triggered physiologically, by hormonal deprivation, or by chemical or physical inducers. Finally, caspases appear to play a role in various testicular diseases (particularly infertility).
References
ADAMS J.M., CORY S.: The Bcl-2 protein family: arbiters of cell survival. Science, 1998, 281: 1322–1326.
ALLAN D.J., HARMON B.V., ROBERTS S.A.: Spermatogonial apoptosis has three morphologically recognizable phases and shows no circadian rhythm during normal spermatogenesis in the rat. Cell Prolif., 1992, 25: 241–250.
ANTICH M., FABIAN E., SARQUELLA J. et al.: Effect of testicular damage induced by cryptorchidism on insulin-like growth factor I receptors in rat Sertoli cells. J. Reprod. Fertil., 1995, 104: 267–275.
BARQAWI A., CARUSO A., MEACHAM R.B.: Experimental varicocele induces testicular germ cell apoptosis in the rat. J. Urol., 2004, 171: 501–503.
BARQAWI A., TRUMMER H., MEACHAM R.: Effect of prolonged cryptorchidism on germ cell apoptosis and testicular sperm count. Asian J. Androl., 2004, 6: 47–51.
BARTKE A.: Apoptosis of male germ cells, a generalized or a cell type-specific phenomenon? Endocrinology, 1995, 136: 3–4.
BEUMER T.L., ROEPERS-GAJADIEN H.L., GADEMAN I.S. et al.: The role of the tumor suppressor p53 in spermatogenesis. Cell Death Differ., 1998, 5: 669–677.
BILLIG H., FURUTA I., RIVIER C. et al.: Apoptosis in testis germ cells: developmental changes in gonadotropin dependence and localization to selective tubule stages. Endocrinology, 1995, 136: 5–12.
BLANCO-RODRIGUEZ J., MARTINEZ-GARCIA C.: Apoptosis is physiologically restricted to a specialized cytoplasmic compartment in rat spermatids. Biol. Reprod., 1999, 61: 1541–1547.
BOEKELHEIDE K., FLEMING S.L., JOHNSON K.J. et al.: Role of Sertoli cells in injury-associated testicular germ cell apoptosis. Proc. Soc. Exp. Biol. Med., 2000, 225: 105–115.
BOZEC A., CHUZEL F., CHATER S. et al.: The mitochondrial-dependent pathway is chronically affected in testicular germ cell death in adult rats exposed in utero to anti-androgens. J. Endocrinol., 2004, 183: 79–90.
BUDNIK L.T., JAHNER D., MUKHOPADHYAY A.K.: Inhibitory effects of TNF alpha on mouse tumor Leydig cells: possible role of ceramide in the mechanism of action. Mol. Cell. Endocrinol., 1999, 150: 39–46.
BUJAN L., MIEUSSET R.: Contraception masculine par la chaleur. Contracept. Fertil. Sex., 1995, 23: 611–614.
CHAUDHARY P.M., EBY M., JASMIN A. et al.: Death receptor 5, a new member of the TNFR family, and DR4 induce FADD-dependent apoptosis and activate the NF-kappaB pathway. Immunity, 1997, 7: 821–830.
CONWAY E.M., POLLEFEYT S., CORNELISSEN J. et al.: Three differentially expressed survivin cDNA variants encode proteins with distinct antiapoptotic functions. Blood, 2000, 95: 1435–1442.
CORDELLI E., FRESEGNA A.M., LETER G. et al.: Evaluation of DNA damage in different stages of mouse spermatogenesis after testicular X irradiation. Radiat. Res., 2003, 160: 443–451.
CROMTON M.: Bax, Bid and the permeabilization of the mitochondrial outer membrane in apoptosis. Curr. Opin. Cell. Biol., 2000, 12: 414–419.
DATTA R., OKI E., ENDO K. et al.: XIAP regulates DNA damage-induced apoptosis downstream of caspase-9 cleavage. J. Biol. Chem., 2000, 275: 31733–31738.
DE FRANCA L.R., GHOSH S., YE S.J. et al.: Surface and surface-to-volume relationships of the Sertoli cell during the cycle of the seminiferous epithelium in the rat. Biol. Reprod., 1993, 49: 1215–1228.
DE S.K., CHEN H.L., PACE J.L. et al.: Expression of tumor necrosis factor-alpha in mouse spermatogenic cells. Endocrinology, 1993, 133: 389–396.
DEVERAUX Q.L., REED J.C.: IAP family proteins—suppressors of apoptosis. Genes Dev., 1999, 13: 239–252.
DIERICH A., SAIRAM M.R., MONACO L. et al.: Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc. Natl Acad. Sci. USA, 1998, 95: 13612–136177.
DUNDAR M., KOCAK I., CULHACI N.: A new experimental model for cryptorchidism: inguinoscrotal approach. Urol. Res., 2001, 29: 178–181.
EVAN G., LITTLEWOOD T.: A matter of life and cell death. Science, 1998, 281: 1317–1322.
FAROOQUI S.M., AL-BAGDADI F., HOUSLAY M.D. et al.: Surgically induced cryptorchidism-related degenerative changes in spermatogonia are associated with loss of cyclic adenosine monophosphate-dependent phosphodiesterases type 4 in abdominal testes of rats. Biol. Reprod., 2001, 64: 1583–1589.
FELDAMN M., TAYLOR P., PALEOLOG E. et al.: Anti-TNF alpha therapy is useful in rheumatoid arthritis and Crohn's disease: analysis of the mechanism of action predicts utility in other diseases. Transplant Proc., 1998, 30: 4126–4127.
FISHER J.S.: Environmental anti-androgens and male reproductive health: focus on phthalates and testicular dysgenesis syndrome. Reproduction, 2004, 127: 305–315.
FRANCAVILLA S., D'ABRIZIO P., RUCCI N. et al.: Fas and Fas ligand expression in fetal and adult human testis with normal or deranged spermatogenesis. J. Clin. Endocrinol. Metab., 2000, 85: 2692–2700.
FUJISAWA M., HIRAMINE C., TANAKA H. et al.: Decrease in apoptosis of germ cells in the testes of infertile men with varicocele. World J. Urol., 1999, 17: 296–300.
FURUCHI T., MASUKO K., NISHIMUNE Y. et al.: Inhibition of testicular germ cell apoptosis and differentiation in mice misexpressing Bcl-2 in spermatogonia. Development, 1996, 122: 1703–1709.
GANDINI L., LOMBARDO F., PAOLI D. et al.: Study of apoptotic DNA fragmentation in human spermatozoa. Hum. Reprod., 2000, 15: 830–839.
GODDARD I., FLORIN A., MAUDUIT C. et al.: Alteration of lactate production and transport in the adult rat testis exposed in utero to flutamide. Mol. Cell. Endocrinol., 2003, 206: 137–146.
GRATAROLI R., VINDRIEUX D., GOUGEON A. et al.: Expression of tumor necrosis factor-alpha-related apoptosis-inducing ligand and its receptors in rat testis during development. Biol. Reprod., 2002, 66: 1707–1715.
GRAY L.E. Jr., OSTBY J., FURR J. et al.: Perinatal exposure to the phthalates DEHP, BBP, and DINP, but not DEP, DMP, or DOTP, alters sexual differentiation of the male rat. Toxicol. Sci., 2000, 58: 350–365.
GRAY L.E. Jr., OSTBY J.S., KELCE W.R.: Developmental effects of an environmental antiandrogen: the fungicide vinclozolin alters sex differentiation of the male rat. Toxicol. Appl. Pharmacol., 1994, 129: 46–52.
GRAY L.E. Jr., WOLF C., LAMBRIGHT C. et al.: Administration of potentially antiandrogenic pesticides (procymidone, linuron, iprodione, chlozolinate, p,p′-DDE, and ketoconazole) and toxic substances (dibutyl- and diethylhexyl phthalate, PCB 169, and ethane dimethane sulphonate) during sexual differentiation produces diverse profiles of reproductive malformations in the male rat. Toxicol. Ind. Health, 1999, 15: 94–118.
GUPTA S., RADHA V., FURUKAWA Y. et al.: Direct transcriptional activation of human caspase-1 by tumor suppressor p53. J. Biol. Chem., 2001, 276: 10585–10588.
HANEJI T., MAEKAWA M., NISHIMUNE Y.: Vitamin A and follicle-stimulating hormone synergistically induce differentiation of type A spermatogonia in adult mouse cryptorchid testes in vitro. Endocrinology, 1984, 114: 801–805.
HENRIKSEN K., HAKOVIRTA H., PARVINEN M.: Testosterone inhibits and induces apoptosis in rat seminiferous tubules in a stage-specific manner: in situ quantification in squash preparations after administration of ethane dimethane sulfonate. Endocrinology, 1995, 136: 3285–3291.
HIKIM A.P., LUE Y., YAMAMOTO C.M. et al.: Key apoptotic pathways for heat-induced programmed germ cell death in the testis. Endocrinology, 2003, 144: 3167–3175.
HOCKENBERY D.M., ZUTTER M., HICKEY W. et al.: BCL2 protein is topographically restricted in tissues characterized by apoptotic cell death. Proc. Natl Acad. Sci. USA, 1991, 88: 6961–6965.
HUCKINS C.: The morphology and kinetics of spermatogonial degeneration in normal adult rats: an analysis using a simplified classification of the germinal epithelium. Anat. Rec., 1978, 190: 905–926.
HULEIHEL M., LUNENFELD E.: Regulation of spermatogenesis by paracrine/autocrine testicular factors. Asian J. Androl., 2004, 6: 259–268.
IMPERATO-McGINLEY J., SANCHEZ R.S., SPENCER J.R. et al.: Comparison of the effects of the 5 alpha-reductase inhibitor finasteride and the antiandrogen flutamide on prostate and genital differentiation: dose-response studies. Endocrinology, 1992, 131: 1149–1156.
ITO K., TANEMURA K., GOTOH H. et al.: Apoptosis-like cell death in experimentally-induced cryptorchidism in adult mice. J. Vet. Med. Sci., 1997, 59: 353–359.
JEYAKUMAR M., SURESH R., KRISHNAMURTHY H.N. et al.: Changes in testicular function following specific deprivation of LH in the adult male rabbit. J. Endocrinol., 1995, 147: 111–120.
JOSHI D.S., YICK J., MURRAY D. et al.: Stage-dependent variation in the radiosensitivity of DNA in developing male germ cells. Radiat. Res., 1990, 121: 274–281.
KASOF G.M., GOMES B.C.: Livin, a novel inhibitor of apoptosis protein family member. J. Biol. Chem., 2001, 276: 3238–3246.
KAYAGAKI N., KAWASAKI A., EBATA T. et al.: Metalloproteinase-mediated release of human Fas ligand. J. Exp. Med., 1995, 182: 1777–1783.
KEENEY D.S., MENDIS-HANDAGAMA S.M., ZiRKIN B.R. et al.: Effect of long term deprivation of luteinizing hormone on Leydig cell volume, Leydig cell number, and steroidogenic capacity of the rat testis. Endocrinology, 1988, 123: 2906–2915.
KEENEY D.S., SPRANDO R.L., ROBAIRE B. et al.: Reversal of long-term LH deprivation on testosterone secretion and Leydig cell volume, number and proliferation in adult rats. J. Endocrinol., 1990, 127: 47–58.
KERR J.F., WYLLIE A.H., CURRIE A.R.: Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer, 1972, 26: 239–257.
KILINC F., GUVEL S., KAYASELCUK F. et al.: p53 Expression and apoptosis in varicocele int the rat testis. J. Urol., 2004, 172: 2475–2478.
KIM J.M., GHOSH S.R., WEIL A.C. et al.: Caspase-3 and caspase-activated deoxyribonuclease are associated with testicular germ cell apoptosis resulting from reduced intratesticular testosterone. Endocrinology, 2001, 142: 3809–3816.
KITAYAMA T.: [Study on testicular temperature in men]. Hinyokika Kiyo, 1965, 11: 435–465.
KNUDSON C.M., TUNG K.S., TOURTELLOTTE W.G. et al.: Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science, 1995, 270: 96–99.
KOCAK I., DUNDAR M., HEKIMGIL M. et al.: Assessment of germ cell apoptosis in cryptorchid rats. Asian J. Androl., 2002, 4: 183–186.
KOJIMA S., HATANO M., OKADA S. et al.: Testicular germ cell apoptosis in Bcl6-deficient mice. Development, 2001, 128: 57–65.
KRAJEWSKI S., BODRUG S., KRAJEWSKA M. et al.: Immunohistochemical analysis of Mcl-1 protein in human tissues. Differential regulation of Mcl-1 and Bcl-2 protein production suggests a unique role for Mcl-1 in control of programmed cell death in vivo. Am. J. Pathol., 1995, 146: 1309–1319.
KRISHNAMURTHY P.K., MAYS J.L., BIJUR G.N. et al.: Transient oxidative stress in SH-SY5Y human neuroblastoma cells results in caspase dependent and independent cell death and tau proteolysis. J. Neurosci. Res., 2000, 61: 515–523.
LEE J., RICHBURG J.H., SHIPP E.B. et al.: The Fas system, a regulator of testicular germ cell apoptosis, is differentially upregulated in Sertoli cell versus germ cell injury of the testis. Endocrinology, 1999, 140: 852–858.
LEE J., RICHBURG J.H., YOUNKIN S.C. et al.: The Fas system is a key regulator of germ cell apoptosis in the testis. Endocrinology, 1997, 138: 2081–2088.
LIU Z.M., ZHENG X.M., LI S.W. et al.: Germ cell apoptosis and expression of Bcl-2 and Bax following testicular torsion/detorsion in rats. Zhonghua Nan Ke Xue, 2003, 9: 40–42.
LIU Z.P., LI W.Y., LIN B. et al.: Influence of FasL overexpression in transgenic mice on the immune regulative function of Sertoli cell. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi, 2004, 20: 456–460.
LUE Y.H., HIKIM A.P., SWERDLOFF R.S. et al.: Single exposure to heat induces stage-specific germ cell apoptosis in rats: role of intratesticular testosterone on stage specificity. Endocrinology, 1999, 140: 1709–1717.
LUE Y.H., LASLEY B.L., LAUGHLIN L.S. et al.: Mild testicular hyperthermia induces profound transitional spermatogenic suppression through increased germ cell apoptosis in adult cynomolgus monkeys (Macaca fascicularis). J. Androl., 2002, 23: 799–805.
MAUDUIT C., BESSET V., CAUSSANEL V. et al.: Tumor necrosis factor alpha receptor p55 is under hormonal (folliclestimulating hormone) control in testicular Sertoli cells. Biochem. Biophys. Res. Commun., 1996, 224: 631–637.
MAUDUIT C., HARTMANN D.J., CHAUVIN M.A. et al.: Tumor necrosis factor alpha inhibits gonadotropin action in cultured porcine Leydig cells: site(s) of action. Endocrinology, 1991, 129: 2933–2940.
MIEUSSET R., BUJAN L.: Testicular heating and its possible contributions to male infertility: a review. Int. J. Androl., 1995, 18: 169–184.
MIGNON A., GUIDOTTI J.E., MITCHELL C. et al.: Selective repopulation of normal mouse liver by Fas/CD95-resistant hepatocytes. Nat. Med., 1998, 4: 1185–1188.
MOORE C., HUTSON J.C.: Physiological relevance of tumor necrosis factor in mediating macrophage-Leydig cell interactions. Endocrinology, 1994, 134: 63–69.
MORENO S.G., DUTRILLAUX B., COFFIGNY H.: Status of p53, p21, mdm2, pRb proteins, and DNA methylation in gonocytes of control and gamma-irradiated rats during testicular development. Biol. Reprod., 2001, 64: 1422–1431.
MYLCHREEST E., CATTLEY R.C., FOSTER P.M.: Male reproductive tract malformations in rats following gestational and lactational exposure to Di(n-butyl) phthalate: an antiandrogenic mechanism? Toxicol. Sci., 1998, 43: 47–60.
NAGATA S., GOLSTEIN P.: The Fas death factor. Science, 1995, 267: 1449–1456.
NANDI S., BANERJEE P.P., ZIRKIN B.R.: Germ cell apoptosis in the testes of Sprague Dawley rats following testosterone withdrawal by ethane 1,2-dimethanesulfonate administration: relationship to Fas? Biol. Reprod., 1999, 61: 70–75.
OGI S., TANJI N., YOKOYAMA M. et al.: Involvement of Fas in the apoptosis of mouse germ cells induced by experimental cryptorchidism. Urol. Res., 1998, 26: 17–21.
OLDEREID N.B., ANGELIS P.D., WIGER R. et al.: Expression of Bcl-2 family proteins and spontaneous apoptosis in normal human testis. Mol. Hum. Reprod., 2001, 7: 403–408.
OMEZZINE A., CHATER S., MAUDUIT C. et al.: Long-term apoptotic cell death process with increased expression and activation of caspase-3 and-6 in adult rat germ cells exposed in utero to flutamide. Endocrinology, 2003, 144: 648–661.
ORTH J.M.: Cell Biology of testicular development in fetus and neonate. In: Desjardins C., Ewing L.L. eds. Cell and molecular biology of testis. New York, Oxford University Press, 1993: 3–4.
PAREDES ESTEBAN R.M., RAMIREZ CHAMOND R., CARRACEDE ANON J. et al.: [Valoration of the FAS in the contralateral testis after unilateral testicular torsion. Experimental study in rats]. Cir. Pediatr., 2003, 16: 4–7.
PENTIKAINEN V., ERKKILA K., DUNKEL L.: Fas regulates germ cell apoptosis in the human testis in vitro. Am. J. Physiol., 1999, 276: E310-E316.
PENTIKAINEN V., SUOMALAINEN L., ERKKILA K. et al.: Nuclear factor-kappa B activation in human testicular apoptosis. Am. J. Pathol., 2002, 160: 205–218.
PEREZ G.I., ROBLES R., KNUDSON C.M. et al.: Prolongation of ovarian lifespan into advanced chronological age by Baxdeficiency. Nat. Genet., 1999, 21: 200–203.
PETER A.T., LINDE-FORSBERG C.: Efficacy of the anticaspase agent zVAD-fmk on post-thaw viability of canine spermatozoa. Theriogenology, 2003, 59: 1525–1532.
PRINT C.G., LOVELAND K.L.: Germ cell suicide: new insights into apoptosis during spermatogenesis. Bioessays, 2000, 22: 423–430.
PRINT C.G., LOVELAND K.L., GIBSON L. et al.: Apoptosis regulator bcl-w is essential for spermatogenesis but appears otherwise redundant. Proc. Natl Acad. Sci. USA, 1998, 95: 12424–12431.
RICHBURG J.H.: The relevance of spontaneous-and chemically-induced alterations in testicular germ cell apoptosis to toxicology. Toxicol. Lett., 2000, 112–113: 79–86.
RICHTER B.W., MIR S.S., EIBEN L.J. et al.: Molecular cloning of ILP-2, a novel member of the inhibitor of apoptosis protein family. Mol. Cell. Biol., 2001, 21: 4292–4301.
RODRIGUEZ I., ODY C., ARAKI K. et al.: An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. Embo. J., 1997, 16: 2262–2270.
ROSSI P., DOLCI S., ALBANESI C. et al.: Follicle-stimulating hormone induction of steel factor (SLF) mRNA in mouse Sertoli cells and stimulation of DNA synthesis in spermatogonia by soluble SLF. Dev. Biol., 1993, 155: 68–74.
ROY N., DEVERAUX Q.L., TAKAHASHI R. et al.: The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases. Embo. J., 1997, 16: 6914–6925.
RUCKER E.B. 3rd, DIERISSEAU P., WAGNER K.U. et al.: Bcl-x and Bax regulate mouse primordial germ cell survival and apoptosis during embryogenesis. Mol. Endocrinol., 2000, 14: 1038–1052.
RUSSELL L.D., CHIARINI-GARCIA H., KORSMEYER S.J. et al.: Bax-dependent spermatogonia apoptosis is required for testicular development and spermatogenesis. Biol. Reprod., 2002, 66: 950–958.
SAID T.M., PAASCH U., GLANDER H.J. et al.: Role of caspases in male infertility. Hum. Reprod. Update, 2004, 10: 39–51.
SAKKAS D., MOFFATT O., MANICARDI G.C. et al.: Nature of DNA damage in ejaculated human spermatozoa and the possible involvement of apoptosis. Biol. Reprod., 2002, 66: 1061–1067.
SCHENDEL S.L., MONTAL M., REED J.C.: Bcl-2 family proteins as ion-channels. Cell. Death Differ., 1998, 5: 372–380.
SHARPE R.M., KERR J.B., McKINNELL C. et al.: Temporal relationship between androgen-dependent changes in the volume of seminiferous tubule fluid, lumen size and seminiferous tubule protein secretion in rats. J. Reprod. Fertil., 1994, 101: 193–198.
SHIKONE T., BILLIG H., HSUEH A.J.: Experimentally induced cryptorchidism increases apoptosis in rat testis. Biol. Reprod., 1994, 51: 865–872.
SHIRAISHI K., NAITO K., YOSHIDA K.: Inhibition of calpain but not caspase protects the testis against injury after experimental testicular torsion of rat. Biol. Reprod., 2000, 63: 1538–1548.
SHUTTLESWORTH G.A., DE ROOIJ D.G., HUHTANIEMI I. et al.: Enhancement of A spermatogonial proliferation and differentiation in irradiated rats by gonadotropin-releasing hormone antagonist administration. Endocrinology, 2000, 141: 37–49.
SIMSEK F., TURKERI L., CEVIK I. et al.: Role of apoptosis in testicular tissue damage caused by varicocele. Arch. Esp. Urol., 1998, 51: 947–950.
SINHA HIKIM A.P., RAJAVASHISTH T.B., SINHA HIKIM I. et al.: Significance of apoptosis in the temporal and stage-specific loss of germ cells in the adult rat after gonadotropin deprivation. Biol. Reprod., 1997, 57: 1193–1201.
SINHA HIKIM A.P., SWERDLOFF R.S.: Hormonal and genetic control of germ cell apoptosis in the testis. Rev. Reprod., 1999, 4: 38–47.
SINHA HIKIM A.P., SWERDLOFF R.S.: Temporal and stagespecific changes in spermatogenesis of rat after gonadotropin deprivation by a potent gonadotropin-releasing hormone antagonist treatment. Endocrinology, 1993, 133: 2161–2170.
SKAKKEBAEK N.E., RAJPERT-DE MEYTS E., MAIN K.M.: Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum. Reprod., 2001, 16: 972–978.
SOLARY E., EYMIN B., DROIN N. et al.: Proteases, proteolysis, and apoptosis. Cell. Biol. Toxicol., 1998, 14: 121–132.
SRIRAMAN V., SAIRAM M.R., JAGANNADHA RAO A.: Evaluation of relative role of LH and FSH in restoration of spermatogenesis using ethanedimethylsulphonate-treated adult rats. Reprod. Biomed. Online, 2004, 8: 167–174.
SUGIHARA A., SAIKI S., TSUJI M. et al.: Expression of Fas and Fas ligand in the testes and testicular germ cell tumors: an immunohistochemical study. Anticancer Res., 1997, 17: 3861–3865.
SYLVESTER S.R., GRISWOLD M.D.: The testicular iron shuttle: a “nurse” function of the Sertoll cells. J. Androl., 1994, 15: 381–385.
SZUMIEL I.: Ionizing radiation-induced cell death. Int. J. Radiat. Biol., 1994, 66: 329–341.
TANAKA H., FUJISAWA M., OKADA H. et al.: Apoptosis-related proteins in the testes of infertile men with varicocele. Brit. J. Urol. Int., 2002, 89: 905–909.
TANAKA M., SUDA T., TAKAHASHI T. et al.: Expression of the functional soluble form of human fas ligand in activated lymphocytes. Embo. J., 1995, 14: 1129–1135.
TESARIK J., MARTINEZ F., RIENZI L. et al.: In-vitro effects of FSH and testosterone withdrawal on caspase activation and DNA fragmentation in different cell types of human seminiferous epithelium. Hum. Reprod., 2002, 17: 1811–1819.
THONNEAU P., BUJAN L., MULTIGNER L., MIEUSSET R.: Occupational heat exposure and male fertility: a review. Hum. Reprod., 1998, 13: 2122–2125.
THORNBERRY N.A., LAZEBNIK Y.: Caspases: enemies within. Science, 1998, 281: 1312–1316.
TILLY J.L., TILLY K.I., KENTON M.L. et al.: Expression of members of the bcl-2 gene family in the immature rat ovary: equine chorionic gonadotropin-mediated inhibition of granulosa cell apoptosis is associated with decreased bax and constitutive bcl-2 and bcl-xlong messenger ribonucleic acid levels. Endocrinology, 1995, 136: 232–241.
TURNER T.T.: Acute experimental testicular torsion. No effect on the contralateral testis. J. Androl., 1985, 6: 65–72.
TURNER T.T., BROWN K.J.: Spermatic cord torsion: loss of spermatogenesis despite return of blood flow. Biol. Reprod., 1993, 49: 401–407.
TURNER T.T., TUNG K.S., TOMOMASA H. et al.: Acute testicular ischemia results in germ cell-specific apoptosis in the rat. Biol. Reprod., 1997, 57: 1267–1274.
VAISHNAV M., MOUDGAL N.R.: Role of FSH in regulating testicular germ cell transformations in the rat: a study using DNA flow cytometry. Andrologia, 1994, 26: 111–117.
VARFOLOMEEV E.E., SCHUCHMANN M., LURIA V. et al.: Targeted disruption of the mouse Caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity, 1998, 9: 267–276.
VERGOUVEN R.P., HUISKAMP R., BAS R.J. et al.: Radiosensitivity of testicular cells in the fetal mouse. Radiat. Res., 1995, 141: 66–73.
VIGODNER M., LEWIN L.M., SHOCHAT L. et al.: Evaluation of damage to the testicular cells of golden hamsters caused by experimental cryptorchidism using flow cytometry and confocal microscopy. Int. J. Androl., 2003, 26: 84–90.
WANG R.A., NAKANE P.K., KOJI T.: Autonomous cell death of mouse male germ cells during fetal and postnatal period. Biol. Reprod., 1998, 58: 1250–1256.
WANG Z.Q., TODANI T., WATANABE Y. et al.: Germ-cell degeneration in experimental unilateral cryptorchidism: role of apoptosis. Pediatr. Surg. Int., 1998, 14: 9–13.
WATANABE M.: Characteristics of TNF alpha- and TNF beta-induced fever in the rabbit. Jpn. J. Physiol., 1992, 42: 101–116.
WATTS L.M., HASTHORPE S., FARMER P.J. et al.: Apoptotic cell death and fertility in three unilateral cryptorchid rat models. Urol. Res., 2000, 28: 332–337.
WEI Y.H., LEE H.C.: Oxidative stress, mitochondrial DNA mutation, and impairment of antioxidant enzymes in aging. Exp. Biol. Med. (Maywood), 2002, 227: 671–682.
WENG S.L., TAYLOR S.L., MORSHEDI M. et al.: Caspase activity and apoptotic markers in ejaculated human sperm. Mol. Hum. Reprod., 2002, 8: 984–991.
WEST A., LAHDETIE J.: X-irradiation—induced changes in the progression of type B spermatogonia and preleptotene spermatocytes. Mol. Reprod. Dev., 2001, 58: 78–87.
WILLIAMS G.T., SMITH C.A.: Molecular regulation of apoptosis: genetic controls on cell death. Cell, 1993, 74: 777–779.
WOOLVERIDGE I., BRYDEN A.A., TAYLOR M.F. et al.: Apoptosis and expression of apoptotic regulators in the human testis following short- and long-term anti-androgen treatment. Mol. Hum. Reprod., 1998, 4: 701–707.
WOOLVERIDGE I., DE BOER-BROUWER M., TAYLOR M.F. et al.: Apoptosis in the rat spermatogenic epithelium following androgen withdrawal: changes in apoptosis-related genes. Biol. Reprod., 1999, 60: 461–470.
XIA Q., ZHANG X.B., ZHANG J.: The apoptosis in damaged testicular tissue caused by varicocele. Zhonghua Nan Ke Xue, 2002, 8: 414–415.
XU J., XU Z., JIANG Y. et al.: Cryptorchidism induces mouse testicular germ cell apoptosis and changes in bcl-2 and bax protein expression. J. Environ. Pathol. Toxicol. Oncol., 2000, 19: 25–33.
YAMAMOTO C.M., SINHA HIKIM A.P., HUYNH P.N. et al.: 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., 2000, 63: 1683–1690.
YAN W., HUANG J.X., LAX A.S. et al.: Overexpression of Bcl-W in the testis disrupts spermatogenesis: revelation of a role of BCL-W in male germ cell cycle control. Mol. Endocrinol., 2003, 17: 1868–1879.
YAN W., SAMSON M., JEGOU B. et al.: 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., 2000, 14: 682–699.
YAN W., SUOMINEN J., SAMSON M. et al.: Involvement of Bcl-2 family proteins in germ cell apoptosis during testicular development in the rat and pro-survival effect of stem cell factor on germ cells in vitro. Mol. Cell. Endocrinol., 2000, 165: 115–129.
ZAMZAMI N., BRENNER C., MARZO I. et al.: Subcellular and submitochondrial mode of action of Bcl-2-like oncoproteins. Oncogene, 1998, 16: 2265–2282.
ZHANG Z.H., HU Z.Y., SONG X.X. et al.: Disrupted expression of intermediate filaments in the testis of rhesus monkey after experimental cryptorchidism. Int. J. Androl., 2004, 27: 234–239.
ZHANG Z.H., JIN X., ZHANG X.S. et al.: Bcl-2 and Bax are involved in experimental cryptorchidism-induced testicular germ cell apoptosis in rhesus monkey. Contraception, 2003, 68: 297–301.
ZHENG S. TURNER T.T., LYZIAK J.J.: Role of Caspase-2 in Germ Apoptosis During the First Phase of Spermatogenesis. Departement of Urology and Cell Biology, University of Virginia Heath Science System, Charlottesville, VA, 2005, Abstract.
ZINI A., ABITBOL J., SCHULSINGER D. et al.: Restoration of spermatogenesis after scrotal replacement of experimentally cryptorchid rat testis: assessment of germ cell apoptosis and eNOS expression. Urology, 1999, 53: 223–227.
ZOU H., LI Y., LIU X. et al.: An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem., 1999, 274: 11549–11556.
Author information
Authors and Affiliations
Corresponding author
Additional information
Bourse SALF 2004 de Recherche en Andrologie.
Rights and permissions
About this article
Cite this article
Amara, S., Bozec, A., Benahmed, M. et al. Mort programmée des cellules germinales testiculaires: causes et mécanismes mis en jeu. Androl. 15, 263–277 (2005). https://doi.org/10.1007/BF03034773
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF03034773