New aspects of spermatogenesis. Expression of mitochondrial marker proteins during spermatogenesis

Human Reproduction Update

Volumn 5, Issue 2, 1999, Pages 108-119

  Meinhardt, Andreas ^a   Wilhelm, Beate ^a   Seitz, Jürgen ^a,b  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b Inst F Anatomic und Zellbiologie   (Germany)

Author keywords

Chaperones; Lon protease; Mitochondria; Spermatogenesis; Sulphydryl oxidase

Indexed keywords

BIOLOGICAL MARKER; CYTOCHROME C1; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 70; POLYPEPTIDE; PROTEIN; PROTEINASE; THIOL OXIDASE; ADENOSINE TRIPHOSPHATE DEPENDENT PROTEINASE; CHAPERONIN; CYTOCHROME C; HEAT SHOCK PROTEIN; OXIDOREDUCTASE; SERINE PROTEINASE;

CELL DIFFERENTIATION; CELL STRUCTURE; GENE ACTIVATION; GERM CELL; HUMAN; IMMUNOHISTOCHEMISTRY; MALE; MITOCHONDRION; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REVIEW; SEMINIFEROUS TUBULE EPITHELIUM; SPERMATOGENESIS; TESTIS; ANIMAL; GENE EXPRESSION REGULATION; GENETIC MARKER; GENETICS; HAMSTER; PRIMATE; SPERMATOZOON;

ANIMALS; ATP-DEPENDENT PROTEASES; CHAPERONIN 60; CRICETINAE; CYTOCHROME C GROUP; GENE EXPRESSION REGULATION; GENETIC MARKERS; HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; MALE; MITOCHONDRIA; OXIDOREDUCTASES; PRIMATES; RATS; SERINE ENDOPEPTIDASES; SPERMATOGENESIS; SPERMATOZOA;

EID: 0033088466     PISSN: 13554786     EISSN: None     Source Type: Journal    
DOI: 10.1093/humupd/5.2.108     Document Type: Review

References (115)

1. Ackland, J.F., Schwartz, N.B., Mayo, K.E. et al. (1992) Nonsteroidal signals originating in the gonads. Physiol. Rev., 72, 731-787.
2. Allen, R.L., O'Brien, D.A. and Eddy, E.M. (1988) A novel hsp70-like protein (P70) is present in mouse spermatogenetic cells. Mol. Cell. Biol., 8, 828-832.
3. André, J. (1962) Contribution à la connaissance du chondriome. Etude de ses modifications ultrastructurales pendent la spermatogénèse. J. Ultrastruct. Res., 6, (Suppl. 3), 1-185.
4. Arlt, H., Tauer, R., Feldmann, H. Neupert, W. et al. (1996) The YTA10-12 complex, a AAA protease with chaperone-like activity in the inner membrane of mitochondria. Cell, 85, 875-885.
5. Aumüller, G., Bergmann, M. and Seitz, J. (1991) Immunohistochemical distribution of sulfhydryl oxidase in the human testis. Cell Tissue Res., 266, 23-28.
6. Attardi, G. (1986) The elucidation of the mitochondrial genome: a historical perspective. BioEssays, 5, 34-39.
7. Azem, A., Oppliger, W., Lustig, A. et al. (1997) The mitochondrial hsp70 chaperone system. Effect of adenine nucleotides, peptide substrate, and mGrpE on the oligomeric state of mhsp70. J. Biol. Chem., 272, 20901-20906.
8. Bereiter-Hahn, J. (1990) Behavior of mitochondria in the living cell. Int. Rev. Cytol., 122, 1-63.
9. Bereiter-Hahn, J. and Vöth, M. (1983) Metabolic control of shape and structure of mitochondria. Biol. Cell, 47, 309-322.
10. Bereiter-Hahn, J. and Vöth, M. (1994) Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc. Res. Tech., 27, 198-219.
11. Bergmann, M., Kumari, M., Aumüller, G. et al. (1990) Distribution pattern of testicular sulfhydryl oxidase (SOx) immunoreactivity in the Djungarian hamster (Phodopus sungorus) during photoperiodically induced involution and recrudescence. Int. J. Androl., 13, 488-499.
12. Bergmann, M., Oehmen, F., Kumari, M. et al. (1991) Immunohistochemical localization of testicular sulfhydryl oxidase (SOx) during sexual maturation of the Djungarian hamster (Phodopus sungorus). J. Reprod. Fertil., 91, 259-265.
13. Bergmann, M., Aumüller, G., Seitz, J. et al. (1992) Sulfhydryl oxidase immunoreactivity in seminiferous tubules of infertile men. Cell Tissue Res., 267, 209-214.
14. Bomer, U., Meijer, M., Maarse, A.C. et al. (1997) Multiple interactions of components mediating preprotein translocation across the inner mitochondrial membrane. EMBO J., 16, 2205-2216.
15. Chloupkova, M. and Luciakova K. (1995) In vitro association of mitochondrial ATP-dependent protease with mitochondrial heat-shock proteins. Neoplasma, 42, 325-329.
16. Cuezwa, J.N., Flores, A.I., Liras, A. et al. (1993) Molecular chaperones and the biogenesis of mitochondria and peroxisomes. Biol. Cell, 77, 47-62
17. Cummins, J.M., Jequier, A.M. and Kan, R. (1994) Molecular biology of human infertility: links with aging, mitochondrial genetics, and oxidative stress? Mol. Reprod. Dev., 37, 345-362.
18. Dahlmann, B., Kuehn, L. and Reinauer, H. (1995) Studies on the activation by ATP of the 26 S proteasome complex from rat skeletal muscle. Biochem. J., 309, 195-202.
19. Dekker, P.J. and Pfanner, N. (1997) Role of mitochondrial GrpE and phosphate in the ATPase cycle of matrix hsp70. J. Mol. Biol., 270, 321-327.
20. De Martino C., A. Stefanini, M., et al. (1974) Morphological and functional modifications of mitochondrion in the rat germ cells. J. Submicrosc. Cytol., 6, 115-116.
21. De Martino, C., Floridi, M.L., Marcante. P., et al. (1979) Morphological, histochemical and biochemical studies on germ cell mitochondria of normal rats. Cell Tissue Res., 196, 1-22.
22. Desautels, M. and Goldberg, A.L. (1982a) Demonstration of an ATP-dependent, vanadate-sensitive endoprotease in the matrix of rat liver mitochondria. J. Biol. Chem., 257, 11673-11679.
23. Desautels, M. and Goldberg, A.L. (1982b) Liver mitochondria contain a ATP-dependent, vanadate-sensitive pathway for the degradation of proteins. Proc. Natl. Acad. Sci. USA, 79, 1869-1873.
24. de Winter, J.P., Hoogerbrugge, J.W., Klaij, I.A. et al. (1992) Activin receptor mRNA expression in the rat testicular cell types. Mol. Cell. Endocrinol., 83, R1-R8.
25. de Winter, J.P., Vanderstichele, H.M.J., Timmerman, M.A. et al. (1993) Activin is produced by rat Sertoli cells in vitro and can act as an autocrine regulator of Sertoli cell function. Endocrinology, 123, 975-982.
26. Dix, D.J., Allen, J.W., Collins, B.W. et al. (1996) Targeted gene disruption of Hsp70-2 results in failed meiosis, germ cell apoptosis, and male infertility. Proc. Natl. Acad. Sci. USA, 93, 3264-3268.
27. Ellis, R.J. and van der Vries, S.M. (1991) Molecular chaperones. Annu. Rev. Biochem., 60, 321-347.
28. Fawcett, D. W. (1970) A comparative view of sperm ultrastructure. Biol. Reprod., 2 (Suppl.), 90-127.
29. Fawcett, D.W., Eddy, E.M. and Philipps, D.M. (1970) Observation on the fine structure and relationships of the chromatoid body in mammalian spermatogenesis. Biol. Reprod., 2, 129-153.
30. Folgero, T., Bertheussen, K., Lindal, S. et al. (1993) Mitochondrial disease and reduced sperm motility. Hum. Reprod., 8, 1863-1868.
31. Fu, G.K., Smith, M.J. and Markovitz, D.M. (1997) Bacterial protease Lon is a site-specific DNA-binding protein. J. Biol. Chem., 272, 534-538.
32. Georgopoulos, C. and Welch, W.J. (1993) Role of the major heat shock proteins as molecular chaperones. Annu. Rev. Cell Biol., 9, 601-634.
33. Gething, M.J. and Sambrook, J. (1992) Protein folding in the cell. Nature, 355, 33-45.
34. Glick, B., Beasley, E.M. and Schatz, G. (1992) Protein sorting in mitochondria. Trends Biochem. Sci., 17, 453-459.
35. Goldberg, E., Sberna, D., Wheat, T., et al. (1977) Cytochrome c: Immunofluorescence localization of the testis-specific form. Science, 196, 1010-1012.
36. Grootegoed, J.A., Jansen, R. and Van der Molen, H.J. (1984) The role of glucose, pyruvate and lactate in ATP production by rat spermatocytes and spermatids. Biochim. Biophys. Acta, 767, 248-256.
37. Guzelin, E., Rep, M. and Grivell, L.A. (1996) Afg3p, a mitochondrial ATP-dependent metalloprotease, is involved in degradation of mitochondrially-encoded Cox1, Cox3, Cob, Su6, Su8 and Su9 subunits of the inner membrane complexes III, IV and V. FEBS Lett., 381, 42-46.
38. Gyllensten, U., Wharton, D., Josefsson, A. et al. (1991) Paternal inheritance of mitochondrial DNA in mice. Nature, 352, 255-257.
39. Hachiya, N., Komiya, T., Alam, R. et al. (1994) MSF, a novel cytoplasmic chaperone which functions in precursor targeting to mitochondria. EMBO J., 13, 5146-5164.
40. Hackenbrock, C.R. (1966) Ultrastructural bases for metabolically linked mechanical activity in mitochondria. I. Reversible ultrastructural changes with change in metabolic steady state in isolated liver mitochondria. J. Cell Biol., 30, 269-297.
41. Hackenbrock, C.R. (1968) Ultrastructural bases for metabolically linked mechanical activity in mitochondria. II. Electron transport-linked ultrastructural transformations in mitochondria. J. Cell Biol., 37, 345-369.
42. Hackenbrock, C.R., Rehn, T.G., Weinbach, E.C. et al. (1971) Oxidative phosphorylation and ultrastructural transformation in mitochondria in the intact ascites tumor cell. J. Cell Biol., 51, 123-137.
43. Hartl, F.-U. and Martin, J. (1995) Molecular chaperones in cellular protein folding. Curr. Opin. Struct. Biol., 5, 92-102.
44. Hartl, F.-U., Hlodan, R. and Langer, T. (1994) Molecular chaperones in protein folding: the art of avoiding sticky situations. Trends Biochem. Sci., 19, 20-25.
45. Haugaard, N. (1968) Cellular mechanism of oxygen toxicity. Physiol. Rev., 48, 311-373.
46. Hecht, W. (1992) Mitochondrien-genetische Aspekte und Besonderheiten im Fortpflanzungsgeschehen. Fertilität, 8, 16-20.
47. Hecht, N.B. (1995) The making of a spermatozoon: a molecular perspective. Dev. Genet., 16, 95-103.
48. Hendrick, J.P. and Hartl, F.U. (1993) Molecular chaperone function of heat-shock proteins. Annu. Rev. Biochem., 62, 349-384.
49. Herrmann, J.M., Stuart, R.A., Craig, E.A. et al. (1994) Mitochondrial heat shock protein 70, a molecular chaperone for proteins encoded by mitochondrial DNA. J. Cell Biol., 127, 893-902.
50. Hess, R.A., Miller, L.A., Kirby, J.D. et al. (1993) Immunoelectron microscopic localization of testicular and somatic cytochromes c in the seminiferous epithelium of the rat. Biol. Reprod., 48, 1299-1308.
51. Horst, M., Oppliger, W., Rospert, S. et al. (1997a) Sequential action of two hsp70 complexes during protein import into mitochondria. EMBO J., 16, 1842-1849.
52. Horst, M., Azem, A., Schatz, G. et al. (1997b) What is the driving force for protein import into mitochondria? Biochim. Biophys. Acta, 1318, 71-78.
53. Kaipia, A., Parvinen, M. and Toppari, J. (1993) Localisation of activin receptor (actR-IIb) mRNA in the rat seminiferous epithelium. Endocrinology, 132, 477-479
54. Kao, S.H., Chao, H.T. and Wie, Y.H. (1998) Multiple deletions of mitochondrial DNA are associated with the decline of motility and fertility of human spermatozoa. Mol. Hum. Reprod., 4, 657-666.
55. Kaya, M. and Harrison, R.G. (1976) The ultrastructural relationships between Sertoli cells and spermatogenic cells in the rat. J. Anat., 121, 279-290.
56. Komiya, T., Rospert, S., Schatz, G. et al. (1997) Binding of mitochondrial precursor proteins to the cytoplasmic domains of the import receptors Tom70 and Tom20 is determined by cytoplasmic chaperones. EMBO J., 16, 4267-4275.
57. Krawcyk, Z., Mali, P. and Parvinen, M. (1988) Expression of a testis-specific hsp70 gene-related RNA in defined stages of rat seminiferous epithelium. J. Cell Biol., 107, 1317-1323.
58. Krummen, L.A., Moore, A., Woodruff, T.K. et al. (1994) Localisation of inhibin and activin binding sites in the testis during development by in situ ligand binding. Biol. Reprod., 50, 734-744.
59. Kumari, M., Aumüller, G., Bergmann, M. et al. (1990) Stage-dependent appearance of sulfhydryl oxidase during spermatogenesis in the testis of rat and hamster. An immunohistochemical study. Histochemistry, 94, 365-371.
60. Langer, T. and Neupert, W. (1996) Regulated protein degradation in mitochondria. Experientia, 52, 1069-1076.
61. Lestienne, P., Reynier, P., Chrétien, M.-F. et al. (1997) Oligoasthenospermia associated with multiple mitochondrial DNA rearrangements. Mol. Hum. Reprod., 3, 811-814.
62. Lindquist, S. and Craig, E.A. (1988) The heat shock proteins. Annu. Rev. Genet., 22, 631-677.
63. Machado de Domenech, E., Domenech, C. E., Aoki, A. et al. (1972) Association of the testicular lactate dehydrogenase isozyme with a special type of mitochondria. Biol. Reprod., 6, 136-147.
64. Manella, C.A., Marko, M., Penczek, P. et al. (1994) The internal compartmentation of rat-liver mitochondria: tomographic study using the high-voltage transmission electron microscope. Microsc. Res. Tech., 27, 278-283.
65. Margulis, L. (1970) Origin of Eucaryotic Cells. Yale University Press, New Haven, pp. 294-297.
66. Martin, J. (1997) Molecular chaperones and mitochondrial protein folding. J. Bioenerg. Biomembr., 29, 35-43.
67. Mathews, L.S. (1994) Activin receptors and cellular signaling by the receptor serine kinase family. Endocrine Rev., 15, 310-325.
68. Meinhardt, A., Parvinen, M., Bacher, M. et al. (1995) Expression of the mitochondrial chaperonin hsp60 in distinct cell types and defined stages of rat seminiferous epithelium. Biol. Reprod., 52, 798-807.
69. Meinhardt, A., Seitz, J., McFarlane, J.R. et al. (1996) Activin A maintains the differentiated state of meiotic germ cell mitochondria in vitro. Proc. 10th Int Congress of Endocrinology, San Francisco, Abstracts of The Endocrine Society, (abstr. OR30-4).
70. Meinhardt, A., Renneberg, H., Dersch, A. et al. (1997) The immortalized germ cell lines GC-1spg and GC-2spd as a model for mitochondrial differentiation during spermatogenesis. Adv. Exp. Med. Biol., 424, 61-63.
71. Meinhardt, A., Seitz, J., Aumüller, G. et al. (1998a) Germ cell- and stage specific expression of heat shock protein 60 (hsp60) in the testis of macaque monkeys (Macaca mulatta and M. fascicularis). Int. J. Androl., 21, 301-307.
72. Meinhardt, A., O'Bryan, M.K., McFarlane, J.R. et al. (1998b) Localization of follistatin in the rat testis. J. Reprod. Fertil., 112, 33-241.
73. Mihara, K. and Omura, T. (1996) Cytosolic factors in mitochondrial protein import. Experientia, 52, 1063-1068.
74. Möbius, J., Groos, S., Meinhardt, A. et al. (1997) Differential distribution of the mitochondrial heat shock protein 60 in rat gastrointestinal tract. Cell Tissue Res., 287, 343-350.
75. Morales, C.R., Hake, L.E. and Hecht, N.B. (1993) Cellular localization of the mRNAs of the somatic and testis-specific cytochromes c during spermatogenesis in the rat. Mol. Reprod. Dev., 34, 196-205.
76. Morimito, R.I., Tissières, A. and Georgopoulos, C. (eds) (1994) Progress and perspectives on the biology of heat shock proteins and molecular chaperones. In The Biology of Heat Shock Proteins and Molecular Chaperones. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, pp. 1-30.
77. Moussa, F., Oko, R. and Hermo, L. (1994) The immunolocalization of small nuclear ribonucleoprotein particles in testicular cells during the cycle of the seminiferous epithelium in the adult rat. Cell Tissue Res., 278, 363-378.
78. Mundy, A.J., Ryder, T.A. and Edmonds, D.K. (1995) Asthenozoospermia and the human sperm mid-piece. Hum. Reprod., 10, 116-119.
79. Nakamura, T., Takio, K., Eto, Y. et al. (1990) Activin-binding protein from rat ovary is follistatin. Science, 247, 836-838.
80. Oehmen, F., Aumüller, G., Bergmann, M. et al. (1991) Distribution of sulfhydryloxidase (SOx) immunoreactivity in the testis of the axolotl (Ambystoma mexicanum) (Amphibia, Urodela). Tissue Cell, 23, 377-384.
81. Paniagua, R., Codesal, J., Nistal, M. et al. (1987) Quantification of cell types throughout the cycle of the human seminiferous epithelium and their DNA content. A new approach to the spermatogonial stem cell in man. Anat. Embryol., 176, 225-230.
82. Paranko, J., Seitz, J., and Meinhardt, A. (1996) Developmental expression of heat shock protein 60 (HSP60) in the rat testis and ovary. Differentiation, 60, 159-167.
83. Parsell, D.A. and Lindquist, S. (1993) The function of heat shock proteins in stress tolerance: reactivation of damaged proteins. Annu. Rev. Genet., 27, 437-496.
84. Rassow, J., Maarse, A.C., Krainer, E. et al. (1994) Mitochondrial protein import: biochemical and genetic evidence for interaction of matrix hsp70 and the inner membrane protein MIM44. J. Cell Biol., 127, 1547-1556.
85. Rep, M., van Dijl, J.M., Suda, K. et al. (1996) Promotion of mitochondrial membrane complex assembly by a proteolytically inactive yeast Lon. Science, 274, 103-106.
86. Rosario, M.O., Perkins, S.L., O'Brien, D.A. et al. (1992) Identification of the gene for the developmentally expressed 70 kDa heat-shock protein (P70) of mouse spermatogenic cells. Dev. Biol., 150, 1-11.
87. Rowley, N., Prip-Buus, C., Westermann, B. et al. (1994) Mdj1p, a novel chaperone of the DnaJ family, is involved in mitochondrial biogenesis and protein folding. Cell, 77, 249-259.
88. Robertson, D.M., Klein, R., de Vos, F.L. et al. (1987) The isolation of polypeptides with FSH suppressing activity from bovine follicular fluid which are structurally different to inhibin. Biochem. Biophys. Res. Commun., 149, 744-749.
89. Russel, L. and Frank, B. (1978) Ultrastructural characterization of nuage in spermatocytes of the rat testis. Anat. Rec., 190, 79-97.
90. Sarge, K.D. and Cullen, K.E. (1997) Regulation of hsp expression during rodent spermatogenesis. Cell. Mol. Life Sci., 53, 191-197.
91. Schlatt, S., Meinhardt, A. and Nieschlag, E. (1997) Paracrine regulation of cellular interactions in the testis: factors in search of a function. Eur. J. Endocrinol., 137, 107-117.
92. Schneider, A., Oppliger, W. and Jeno, P. (1994) Purified inner membrane protease I of yeast mitochondria is a heterodimer. J. Biol. Chem., 269, 8635-8638.
93. Schneyer, A.l., Rzucildo, D.A., Sluss, P.M. et al. (1994) Characterization of unique binding kinetics of follistatin and activin or inhibin in serum. Endocrinology, 135, 667-674.
94. Seitz, J., Kumari, M. and Aumuller, G. (1990) Sulfhydryl oxidase - an immunohistochemical marker for postnatal differentiation of rat testis. Anat. Rec., 226, 91A.
95. Seitz, J., Möbius, J., Bergmann, M. et al. (1995) Mitochondrial differentiation during meiosis of germ cells. Int. J. Androl., 18 (Suppl. 2), 7-11.
96. Seitz, J., Keppler, C., Spangenberg, O. et al. (1988) Thiol oxidase-a new mitochondrial enzyme: characterization and immunohistochemical localization. Eur. J. Cell Biol., 46 (Suppl. 22), 69 (abstr.).
97. Shimasaki, S., Kaga, M., Esch, F. et al. (1988) Porcine follistatin gene structure supports two forms of mature follistatin produced by alternative splicing. Biochem. Biophys. Res. Commun., 152, 717-723.
98. Sitte, N., Drung, I. and Dubiel, W. (1995) Identification of a novel ATP-dependent proteolytic activity in mitochondrial intermembrane space. Biochem. Mol. Biol. Int., 36, 871-881.
99. Söderström, K-O. and Parvinen, M. (1976) Incorporation of [3H]uridine by the chromatoid body during rat spermatogenesis. J. Cell Biol., 70, 239-246.
100. Sonezaki, S., Okita, K., Oba, T. et al. (1995) Protein substrates and heat shock reduce the DNA-binding ability of Escherichia coli Lon protease. Appl. Microbiol. Biotechnol., 44, 484-488.
101. Stuart, R.A., Cyr, D.M., Craig, E.A. et al. (1994) Mitochondrial molecular chaperones: their role in protein translocation. Trends Biochem. Sci., 19, 87-92.
102. Sugino, K., Kurosawa, N., Nakamura, T. et al. (1993) Molecular heterogeneity of follistatin, an activin-binding protein. J. Biol. Chem., 268, 15579-15587.
103. Teichmann, U., van Dyck, L., Guiard, B. et al. (1996) Substitution of PIM1 protease in mitochondria by Escherichia coli Lon protease. J. Biol. Chem., 271, 10137-10142.
104. Ueno, N., Ling, N., Ying, S. et al. (1987) Isolation and partial characterisation of follistatin: a single chain Mr 35 000 monomeric protein that inhibits the release of follicle stimulating hormone. Proc. Natl. Acad. Sci. USA, 84, 8282-8286.
105. Van Dyk, L., Pearce, D.A. and Sherman, F. (1994) PIM1 encodes a mitochondrial ATP-dependent protease that is required for mitochondrial function in the yeast Saccharomyces cerevisiae. J. Biol. Chem., 269, 238-242.
106. Viitanen, P.V., Lorimer, G.H., Seetharam, R. et al. (1992) Mammalian mitochondrial chaperonin 60 functions as a single toroid ring. J. Biol. Chem., 26, 695-698.
107. Wagner, I., Arlt, H., van Dyck, L. et al. (1994) Molecular chaperones cooperate with PIM1 protease in the degradation of misfolded proteins in mitochondria. EMBO. J., 1, 5135-5145.
108. Wallace, D.C. (1989) Mitochondrial DNA mutations and neuromuscular disease. Trends Genet., 5, 9-13.
109. Wang, N., Gottesman, S., Willingham, M.C. et al. (1993) A human mitochondrial ATP-dependent protease that is highly homologous to bacterial Lon protease. Proc. Natl. Acad. Sci. USA, 90, 11247-11251.
110. Wang, N., Maurizi, M.R., Emmertbuck, L. et al. (1994) Synthesis, processing, and localization of human Lon protease. J. Biol. Chem., 269, 29308-29313.
111. Watabe, S. and Kimura, T. (1985) Adrenal cortex mitochondrial enzyme with ATP-dependent protease and protein-dependent ATPase activities. J. Biol. Chem., 260, 14498-14504.
112. Werner, A., Meinhardt, A., Seitz, J. et al. (1997) Distribution of heat-shock protein 60 immunoreactivity in testes of infertile men. Cell Tissue Res., 288, 539-544.
113. Zakeri, Z.F. and Wolgemuth, D.J. (1987) Developmental-stage-specific expression of the hsp70 gene family during differentiation of the mammalian germ line. Mol. Cell. Biol., 7, 1791-1796.
114. Zeviani, M. and Antozzi, C. (1997) Mitochondrial disorders. Mol. Hum. Reprod., 3, 133-148.
115. Zhu, D., Dix, D.J. and Eddy, E.M. (1997) HSP70-2 is required for CDC2 kinase activity in meiosis I of mouse spermatocytes. Development, 124, 3007-3014.