Male sterility in mice lacking retinoic acid receptor α involves specific abnormalities in spermiogenesis

Differentiation

Volumn 73, Issue 4, 2005, Pages 188-198

  Chung, Sanny S W ^a   Wang, Xiangyuan ^a   Wolgemuth, Debra J ^a  

^a NewYork Presbyterian Hospital   (United States)

Author keywords

Acrosome; Apoptosis; Caspase 3; Ectoplasmic specializations; RAR ; Retinoid signaling; Spermiogenesis

Indexed keywords

CASPASE 3; RETINOIC ACID RECEPTOR ALPHA; CASP3 PROTEIN, MOUSE; CASPASE; RETINOIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; IMMUNOHISTOCHEMISTRY; MALE; MALE STERILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SERTOLI CELL; SPERMATID; SPERMATOGENESIS; SPERMATOGONIUM; ANIMAL; APOPTOSIS; CELL NUCLEUS; CONGENITAL MALFORMATION; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE INFERTILITY; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; SPERMATOZOON; TESTIS;

ANIMALIA;

ANIMALS; APOPTOSIS; CASPASE 3; CASPASES; CELL NUCLEUS; INFERTILITY, MALE; MALE; MICE; MICE, MUTANT STRAINS; RECEPTORS, RETINOIC ACID; SERTOLI CELLS; SPERMATOGENESIS; SPERMATOZOA; TESTIS;

EID: 23844489864     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1111/j.1432-0436.2005.00018.x     Document Type: Article

References (58)

1. Akmal, K.M., Dufour, J.M. and Kim, K.H. (1997) Retinoic acid receptor alpha gene expression in the rat testis: potential role during the prophase of meiosis and in the transition from round to elongating spermatids. Biol Reprod 56:549-556.
2. Akmal, K.M., Dufour, J.M., Vo, M., Higginson, S. and Kim, K.H. (1998) Ligand-dependent regulation of retinoic acid receptor alpha in rat testis: in vivo response to depletion and repletion of vitamin A. Endocrinology 139:1239-1248.
3. Alnemri, E.S., Livingston, D.J., Nicholson, D.W., Salvesen, G., Thornberry, N.A., Wong, W.W. and Yuan, J. (1996) Human ICE/CED-3 protease nomenclature. Cell 87:171.
4. Beumer, T.L., Roepers-Gajadien, H.L., Gademan, L.S., Rutgers, D.H. and de Rooij, D.G. (1997) P21(Cip1/WAF1) expression in the mouse testis before and after X irradiation. Mol Reprod Dev 47:240-247.
5. Billig, H., Furuta, I., Rivier, C., Tapanainen, J., Parvinen, M. and Hsueh, A.J. (1995) Apoptosis in testis germ cells: developmental changes in gonadotropin dependence and localization to selective tubule stages. Endocrinology 136:5-12.
6. Callard, G.V., Jorgensen, J.C. and Redding, J.M. (1995) Biochemical analysis of programmed cell death during premeiotic stages of spermatogenesis in vivo and in vitro. Dev Genet 16:140-147.
7. Chung, S.S., Sung, W., Wang, X. and Wolgemuth, D.J. (2004) Retinoic acid receptor alpha is required for synchronization of spermatogenic cycles and its absence results in progressive breakdown of the spermatogenic process. Dev Dyn 230:754-766.
8. Chung, S.S. and Wolgemuth, D.J. (2004) Role of retinoid signaling in the regulation of spermatogenesis. Cytogenet Genome Res 105:189-202.
9. Cregan, S.P., Dawson, V.L. and Slack, R.S. (2004) Role of AIF in caspase-dependent and caspase-independent cell death. Oncogene 23:2785-2796.
10. de Rooij, D.G. and de Boer, P. (2003) Specific arrests of spermatogenesis in genetically modified and mutant mice. Cytogenet Genome Res 103:267-276.
11. de Rooij, D.G., van Pelt, A.M.M., Van de Kant, H.J.G., van der Saag, P.T., Peters, A.H.F.M., Heyting, C. and de Boer, P. (1994) Role of retinoids in spermatogonial proliferation and differentiation and the meiotic prophase. In: Bartke, A. (ed). Function of somatic cells in the testis. Springer, Berlin, p. 345.
12. Earnshaw, W.C., Martins, L.M. and Kaufmann, S.H. (1999) Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68:383-424.
13. Eskild, W. and Hansson, V. (1994) Vitamin A functions in the reproductive organs. In: Blomhoff, R. (ed). Vitamin A in health and disease. Dekker, New York, pp. 531-559.
14. Eskild, W., Ree, A.H., Levy, F.O., Jahnsen, T. and Hansson, V. (1991) Cellular localization of mRNAs for retinoic acid receptor-alpha, cellular retinol-binding protein, and cellular retinoic acid-binding protein in rat testis: evidence for germ cell-specific mRNAs. Biol Reprod 44:53-61.
15. Gambhir, K.K. and Ahluwalia, B.S. (1975) Vitamin A in bovine sperm acrosomes. J Reprod Fertil 43:129-132.
16. Henriksen, K., Hakovirta, H. and Parvinen, M. (1995) In-situ quantification of stage-specific apoptosis in the rat seminiferous epithelium: effects of short-term experimental cryptorchidism. Int J Androl 18:256-262.
17. Hikim, A.P., Wang, C., Leung, A. and Swerdloff, R.S. (1995) Involvement of apoptosis in the induction of germ cell degeneration in adult rats after gonadotropin-releasing hormone antagonist treatment. Endocrinology 136:2770-2775.
18. Huang, H.F. and Marshall, G.R. (1983) Failure of spermatid release under various vitamin A states-an indication of delayed spermiation. Biol Reprod 28:1163-1172.
19. Huang, H.F., Yang, C.S., Meyenhofer, M., Gould, S. and Boccabella, A.V. (1988) Disruption of sustentacular (Sertoli) cell tight junctions and regression of spermatogenesis in vitamin-A-deficient rats. Acta Anat (Basel) 133:10-15.
20. Ismail, N., Morales, C. and Clermont, Y. (1990) Role of spermatogonia in the stage-synchronization of the seminiferous epithelium in vitamin-A-deficient rats. Am J Anat 188:57-63.
21. Jahnukainen, K., Chrysis, D., Hou, M., Parvinen, M., Eksborg, S. and Soder, O. (2004) Increased apoptosis occurring during the first wave of spermatogenesis is stage-specific and primarily affects midpachytene spermatocytes in the rat testis. Biol Reprod 70:290-296.
22. Kastner, P., Mark, M. and Chambon, P. (1995) Nonsteroid nuclear receptors: what are genetic studies telling us about their role in real life? Cell 83:859-869.
23. Kastner, P., Mark, M., Leid, M., Gansmuller, A., Chin, W., Grondona, J.M., Decimo, D., Krezel, W., Dierich, A. and Chambon, P. (1996) Abnormal spermatogenesis in RXR beta mutant mice. Genes Dev 10:80-92.
24. Kim, J.M., Ghosh, S.R., Weil, A.C. and Zirkin, B.R. (2001) Caspase-3 and caspase-activated deoxyribonuclease are associated with testicular germ cell apoptosis resulting from reduced intra-testicular testosterone. Endocrinology 142:3809-3816.
25. Kim, K.H. and Griswold, M.D. (1990) The regulation of retinoic acid receptor mRNA levels during spermatogenesis. Mol Endocrinol 4:1679-1688.
26. Kim, K.H. and Wang, Z.Q. (1993) Action of vitamin A on testis: role of the Sertoli cell. In: Griswold, M.D. and Rusell, L.D. (eds.). The sertoli cell. Cache River Press, Clearwater, FL, pp. 514-535.
27. Liu, D., Matzuk, M.M., Sung, W.K., Guo, Q., Wang, P. and Wolgemuth, D.J. (1998) Cyclin A1 is required for meiosis in the male mouse. Nat Genet 20:377-380.
28. Lorenzo, H.K. and Susin, S.A. (2004) Mitochondrial effectors in caspase-independent cell death. FEBS Lett 557:14-20.
29. Lufkin, T., Lohnes, D., Mark, M., Dierich, A., Gorry, P., Gaub, M.P., LeMeur, M. and Chambon, P. (1993) High postnatal lethality and testis degeneration in retinoic acid receptor alpha mutant mice. Proc Natl Acad Sci USA 90:7225-7229.
30. Mangelsdorf, D.J. and Evans, R.M. (1995) The RXR heterodimers and orphan receptors. Cell 83:841-850.
31. Mangelsdorf, D.J., Thummel, C., Beato, M., Herrlich, P., Schutz, G., Umesono, K., Blumberg, B., Kastner, P., Mark, M. and Chambon, P., Evans, R.M., et al. (1995) The nuclear receptor superfamily: the second decade. Cell 83:835-839.
32. Morales, C.R. and Griswold, M.D. (1991) Variations in the level of transferrin and SGP-2 mRNAs in Sertoli cells of vitamin A-deficient rats. Cell Tissue Res 263:125-130.
33. Mutter, G.L., Grills, G.S. and Wolgemuth, D.J. (1988) Evidence for the involvement of the proto-oncogene c-mos in mammalian meiotic maturation and possibly very early embryogenesis. EMBO J 7:683-689.
34. Nicholson, D.W. and Thornberry, N.A. (1997) Caspases: killer proteases. Trends Biochem Sci 22:299-306.
35. Nicholson, D.W. and Thornberry, N.A. (2003) Apoptosis. Life and death decisions. Science 299:214-215.
36. Oakberg, E.F. (1956) A description of spermiogenesis in the mouse and its use in an analysis of the cycle of the seminiferous epithelium and germ cell renewal. Am J Anat 99:391-414.
37. Omezzine, A., Chater, S., Mauduit, C., Florin, A., Tabone, E., Chuzel, F., Bars, R. and Benahmed, M. (2003) 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 144:648-661.
38. Packer, A.I. and Wolgemuth, D.J. (1999) Genetic and molecular approaches to understanding the role of retinoids in mammalian spermatogenesis. In: Nau, H. and Blaner, W.S. (eds.). Retinoids: the biochemical and molecular basis of vitamin A and retinoid action. Springer-Verlag, Berlin, pp. 347-368.
39. Rajguru, S.U., Kang, Y.H. and Ahluwalia, B.S. (1982) Localization of retinol (vitamin A) in rat testes. J Nutr 112:1881-1891.
40. Rodriguez, I., Ody, C., Araki, K., Garcia, I. and 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.
41. Ross, M.H. (1976) The Sertoli cell junctional specialization during spermiogenesis and at spermiation. Anat Rec 186:79-104.
42. Russell, L. (1977a) Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am J Anat 148:313-328.
43. Russell, L. (1977b) Observations on rat Sertoli ectoplasmic ('junctional') specializations in their association with germ cells of the rat testis. Tissue Cell 9:475-498.
44. Russell, L.D. (1993) Role in spermiation. In: Griswold, M.D. and Russell, L.D. (eds.). The sertoli cell. Cache River Press, Clearwater, FL, pp. 269-303.
45. Russell, L.D., Ettlin, R.A., SinhaHikim, A.P. and Clegg, E.D. (1990) Histological and histopathological evaluation of the testis. Cache River Press, Clearwater, FL.
46. Russell, L.D., Lee, I.P., Ettlin, R. and Malone, J.P. (1983a) Morphological pattern of response after administration of procarbazine: alteration of specific cell associations during the cycle of the seminiferous epithelium of the rat. Tissue Cell 15:391-404.
47. Russell, L.D., Lee, I.P., Ettlin, R. and Peterson, R.N. (1983b) Development of the acrosome and alignment, elongation and entrenchment of spermatids in procarbazine-treated rats. Tissue Cell 15:615-626.
48. Said, T.M., Paasch, U., Glander, H.J. and Agarwal, A. (2004) Role of caspases in male infertility. Hum Reprod Update 10:39-51.
49. Shetty, J., Marathe, G.K. and Dighe, R.R. (1996) Specific immunoneutralization of FSH leads to apoptotic cell death of the pachytene spermatocytes and spermatogonial cells in the rat. Endocrinology 137:2179-2182.
50. Shi, S.R., Key, M.E. and Kalra, K.L. (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.
51. Sjoblom, T., West, A. and Lahdetie, J. (1998) Apoptotic response of spermatogenic cells to the germ cell mutagens etoposide, adriamycin, and diepoxybutane. Environ Mol Mutagen 31:133-148.
52. van Pelt, A.M. and de Rooij, D.G. (1990) Synchronization of the seminiferous epithelium after vitamin A replacement in vitamin A-deficient mice. Biol Reprod 43:363-367.
53. van Pelt, A.M., van den Brink, C.E., de Rooij, D.G. and van der Saag, P.T. (1992) Changes in retinoic acid receptor messenger ribonucleic acid levels in the vitamin A-deficient rat testis after administration of retinoids. Endocrinology 131:344-350.
54. Velazquez, A., Rosado, A. Jr. and Rosado, A. (1975) Participation of vitamin A in the maturation of rabbit spermatozoa. Int J Fertil 20:151-151.
55. Vogl, A.W., Pfeiffer, D.C., Mulholland, D., Kimel, G. and Guttman, J. (2000) Unique and multifunctional adhesion junctions in the testis: ectoplasmic specializations. Arch Histol Cytol 63:1-15.
56. Wang, X., Yang, C., Chai, J., Shi, Y. and Xue, D. (2002) Mechanisms of AIF-mediated apoptotic DNA degradation in Caenorhabditis elegans. Science 298:1587-1592.
57. Weil, M., Jacobson, M.D. and Raff, M.C. (1998) Are caspases involved in the death of cells with a transcriptionally inactive nucleus?. Sperm and chicken erythrocytes. J Cell Sci 111:2707-2715.
58. Yan, W., Suominen, J., Samson, M., Jegou, B. and Toppari, J. (2000) 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 165:115-129.