Stem cell factor/c-kit system in spermatogenesis

Human Reproduction Update

Volumn 5, Issue 5, 1999, Pages 535-545

  Mauduit, Claire ^a   Hamamah, Samir ^b   Benahmed, Mohamed ^a  

^a INSERM   (France)

^b HÔPITAL ANTOINE BÉCLÈRE   (France)

Author keywords

c kit; Germ cells; Stem cell factor; Testicular development; Testis

Indexed keywords

STEM CELL FACTOR; STEM CELL FACTOR RECEPTOR;

ALTERNATIVE RNA SPLICING; APOPTOSIS; CELL MIGRATION; CELL PROLIFERATION; GENE DELETION; GENE EXPRESSION; HUMAN; MALE; MALE INFERTILITY; POINT MUTATION; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; REVIEW; SEMINOMA; SPERMATOGENESIS; SPERMATOGONIUM; TESTIS DEVELOPMENT;

ANIMALS; APOPTOSIS; CELL DIVISION; CELL MOVEMENT; GENE EXPRESSION REGULATION; HUMANS; INFERTILITY, MALE; MALE; MICE; MICE, MUTANT STRAINS; PROTO-ONCOGENE PROTEINS C-KIT; RATS; SIGNAL TRANSDUCTION; SPERMATOGENESIS; STEM CELL FACTOR; TESTIS; YOLK SAC;

EID: 0032756373     PISSN: 13554786     EISSN: None     Source Type: Journal    
DOI: 10.1093/humupd/5.5.535     Document Type: Review

References (93)

1. Albanesi, C., Geremia, R., Giorgio, M. et al. (1996) A cell- and developmental stage-specific promoter drives the expression of a truncated c-kit protein during mouse spermatid elongation. Development, 122, 1291-1302.
2. Allard, E.K., Blanchard, K.T. and Boekelheide, K. (1996) Exogenous stem cell factor (SCF) compensates for altered endogenous SCF expression in 2,5-hexanedione-induced testicular atrophy in rats. Biol. Reprod., 55, 185-193.
3. Anderson, D.M., Lyman, S.D., Baird, A. et al. (1990) Molecular cloning of mast cell growth factor, a hematopoietin that is active in both membrane bound and soluble forms. Cell, 63, 235-243.
4. Ashby, J., Houthoff, E., Kennedy, S.J. et al. (1997) The challenge posed by endocrine-disrupting chemicals. Environ. Health Perspect., 105, 164-169.
5. Bedell, M.A., Brannan, C.I., Evans, E.P. et al. (1995) DNA rearrangements located over 100 kb 5' of the Steel (Sl)-coding region in Steel-panda and Steel-contrasted mice deregulate Sl expression and cause female sterility by disrupting ovarian follicle development. Genes Dev., 9, 455-470.
6. Bellvé, A.R., Cavicchia, J.C., Millette, C.F. et al. (1977) Spermatogenic cells of the prepubertal mouse. Isolation and morphological characterization. J. Cell Biol., 74, 68-85.
7. Benahmed, M. (1996) Growth factors and cytokines in the testis. In Comhaire, F (ed.), Male Infertility: Clinical Investigation, Cause, Evaluation and Treatment, Chapman & Hall, London, pp. 55-96.
8. Blanchard, K.T., Lee, J. and Boekelheide, K. (1998) Leuprolide, a gonadotropin-releasing hormone agonist, reestablishes spermatogenesis after 2,5-hexanedione-induced irreversible testicular injury in the rat, resulting in normalized stem cell factor expression. Endocrinology, 139, 236-244.
9. Blume, J.P., Claesson, W.L., Siegbahn, A. et al. (1991) Activation of the human c-kit product by ligand-induced dimerization mediates circular actin reorganization and chemotaxis. EMBO J., 10, 4121-4128.
10. Bokemeyer, C., Kuczyk, M.A., Dunn, T. et al. (1996) Expression of stem-cell factor and its receptor c-kit protein in normal testicular tissue and malignant germ-cell tumors. J. Cancer Res. Clin. Oncol., 122, 301-306.
11. Brannan, C.I., Lyman, S.D., Williams, D.E. et al. (1991) Steel-Dickie mutation encodes a c-kit ligand lacking transmembrane and cytoplasmic domains. Proc. Natl Acad. Sci. USA, 88, 4671-4674.
12. Brannan, C.I., Bedell, M.A., Resnick, J.L. et al. (1992) Developmental abnormalities in Steel 17H mice result from a splicing defect in the steel factor cytoplasmic tail. Genes Dev., 6, 1832-1842.
13. Breyer, P.R., Rothrock, J.K., Beaudry, N. et al. (1996) A novel peptide from the growth hormone releasing hormone gene stimulates Sertoli cell activity. Endocrinology, 137, 2159-2162.
14. Boussouar, F., Grataroli, R., Ji, J. and Benahmed, M. (1999) Tumor necrosis factor a stimulates lactate dehydrogenase A expression in porcine cultured Sertoli cells: mechanisms of action. Endocrinology, 140, 3054-3062.
15. Carson, W.E., Haldar, S., Baiocchi, R.A. et al. (1994) The c-kit ligand suppresses apoptosis of human natural killer cells through the upregulation of bcl-2. Proc. Natl Acad. Sci. USA, 91, 7553-7557.
16. Chabot, B., Stephenson, D.A., Chapman, V.M. et al. (1988) The proto-oncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus. Nature, 335, 88-89.
17. Cheek, A.O. and McLachlan, J.A. (1998) Environmental hormones and the male reproductive system. J. Androl., 19, 5-10.
18. Cooper, R.L. and Kavlock, R.J. (1997) Endocrine disruptors and reproductive development: a weight-of-evidence overview. J. Endocrinol., 152, 159-166.
19. Copeland, N.G., Gilbert, D.J., Cho, B.C. et al. (1990) Mast cell growth factor maps near the Steel locus on mouse chromosome 10 and is deleted in a number of Steel alleles. Cell, 63, 175-183.
20. DeRooj, D. and Grootegoed, J.A. (1998) Spermatogonial stem cells. Curr. Opin. Cell Biol., 10, 694-701.
21. Dolci, S., Williams, D.E., Ernst, M.K. et al. (1991) Requirement for mast cell growth factor for primordial germ cell survival in culture. Nature, 352, 809-811.
22. Dym, M., Jia, M.C., Dirami, G. et al. (1995) Expression of c-kit receptor and its autophosphorylation in immature rat type A spermatogonia. Biol. Reprod., 52, 8-19.
23. Eddy, E.M., Clark, J.M., Gong, D. et al. (1981) Origin and migration of primordial germinal cells in mammals. Gamete Res., 4, 333-362.
24. Feng, H., Sandlow, J.I. and Sandra, A. (1997) Expression and function of the c-kit proto-oncogene protein in mouse sperm. Biol. Reprod., 57, 194-203. Feng, H.L., Sandlow J.I., Sparks, A.E.T. et al. (1999) Decreased expression of the c-kit receptor is associated with increased apoptosis in subfertile human testes. Fertil. Steril., 71, 85-89.
25. Feng, H., Sandlow, J.I. and Sandra, A. (1997) Expression and function of the c-kit proto-oncogene protein in mouse sperm. Biol. Reprod., 57, 194-203. Feng, H.L., Sandlow J.I., Sparks, A.E.T. et al. (1999) Decreased expression of the c-kit receptor is associated with increased apoptosis in subfertile human testes. Fertil. Steril., 71, 85-89.
26. Flanagan, J.G., Chan, D. and Leder, P. (1991) Transmembrane form of the c-kit ligand growth factor is determined by alternative splicing and is missing in the SId mutation. Cell, 64, 1025-1035.
27. Fritz, I.B., Tung, P.S. and Ailenberg, M. (1993) Proteases and antiproteases in the seminiferous tubule. In Russell, L.D. and Griswold, M.D. (eds), The Sertoli Cell. Cache River Press, Clearwater, pp. 217-235.
28. Fusigawa, M., Kanzaki, M., Okuda, Y. et al. (1998) Stem Cell Factor in human seminal plasma as a marker of spermatogenesis. Urology, 3, 460-463.
29. Geissler, E.N., McFarland, E.C. and Russell, E.S. (1981) Analysis of pleiotropism at the dominant white-spotting (W) locus of the house mouse: a description of ten new W alleles. Genetics, 97, 337-361.
30. Geissler, E.N., Ryan, M.A. and Housman, D.E. (1988) The dominant-white spotting (W) locus of the mouse encodes the c-kit proto-oncogene. Cell, 55, 185-192.
31. Giebel, L.B. and Spritz, R.A. (1991) Mutation of the KIT (mast/stem cell growth factor receptor) protooncogene in human piebaldism. Proc. Natl Acad. Sci. USA, 88, 8696-8699.
32. Giebel, L.B., Strunk, K.M., Holmes, S.A. et al. (1992) Organization and nucleotide sequence of the human KIT (mast/stem cell growth factor receptor) proto-oncogene. Oncogene, 7, 2207-2217.
33. Gilbert, S.F. (1994) The saga of germ cells. In Developmental Biology. Sinauer Associates Inc. Publishers, Sunderland, Massachusetts, pp. 788-792.
34. Gnessi, L., Fabbri, A. and Spera, G. (1997) Gonadal peptides as mediators of development and functional control of the testis: an integrated system with hormones and local environment. Endocr. Rev., 18, 541-609.
35. Godin, I., Deed, R., Cooke, J. et al. (1991) Effects of the steel gene product on mouse primordial germ cells in culture. Nature, 352, 807-809.
36. Hakovirta, H., Yan, W., Kaleva, M. et al. (1999) Function of stem cell factor as a survival factor of spermatogonia and localization of messenger ribonucleic acid in the rat seminiferous epithelium. Endocrinology, 140, 1492-1498.
37. Huang, E.J., Nocka, K.H., Buck, J. et al. (1992) Differential expression and processing of two cell associated forms of the kit-ligand: KL-1 and KL-2. Mol. Biol. Cell, 3, 349-362.
38. Izquierdo, M.A., Van der Valk, P., Van Ark-Otte, J.. et al. (1995) Differential expression of the c-kit proto-oncogene in germ cell tumours. J. Pathol., 177, 253-258.
39. Jiang, C., Hall, S.J. and Boekelheide, K. (1997) Cloning and characterization of the 5' flanking region of the stem cell factor gene in rat Sertoli cells. Gene, 185, 285-290.
40. Kierszenbaum, A.L. (1994) Mammalian spermatogenesis in vivo and in vitro: a partnership of spermatogenic and somatic cell lineages. Endocr. Rev., 15, 116-134.
41. Lamb, D.J. (1999) Debate: Is ICSI a genetic time bomb? Yes. J. Androl., 20, 23-33.
42. Lev, S., Yarden, Y. and Givol, D. (1992) Dimerization and activation of the kit receptor by monovalent and bivalent binding of the stem cell factor. J. Biol. Chem., 267, 15970-15977.
43. Longley, B.J., Tyrrell, L., Ma, Y. et al. (1997) Chymase cleavage of stem cell factor yields a bioactive, soluble product. Proc. Natl Acad. Sci. USA, 94, 9017-9021.
44. Loveland, K.L. and Schlatt, S. (1997) Stem cell factor and c-kit in the mammalian testis: lessons originating from Mother Nature's gene knockouts. J. Endocrinol., 153, 337-344.
45. Lyon, M.F., Glenister, P.H., Loutit, J.F. et al. (1984) A presumed deletion covering the W and Ph loci of the mouse. Genet. Res., 44, 161-168.
46. Majumdar, M.K., Feng, L., Medlock, E. et al. (1994) Identification and mutation of primary and secondary proteolytic cleavage sites in murine stem cell factor cDNA yields biologically active, cell-associated protein. J. Biol. Chem., 269, 1237-1242.
47. Manova, K. and Bachvarova, R.F. (1991) Expression of c-kit encoded at the W locus of mice in developing embryonic germ cells and presumptive melanoblasts. Dev. Biol., 146, 312-324.
48. Manova, K., Nocka, K., Besmer, P. et al. (1990) Expression of c-kit encoded at the W locus mice in developing embryonic germ cells and presumptive melanoblasts. Development, 110, 1057-1069.
49. Manova, K., Huang, E.J., Angeles, M. et al. (1993) The expression pattern of the c-kit ligand in gonads of mice supports a role for the c-kit receptor in oocyte growth and in proliferation of spermatogonia. Dev. Biol., 157, 85-99.
50. Martin, F.H., Suggs, S.V., Langley, K.E. et al. (1990) Primary structure and functional expression of rat and human stem cell factor DNAs. Cell, 63, 203-211.
51. Marziali, G., Lazzaro, D. and Sorrentino, V. (1993) Binding of germ cells to mutant Sld Sertoli cells is defective and is rescued by expression of the transmembrane form of the c-kit ligand. Dev. Biol., 157, 182-190.
52. Matsui, Y., Zsebo, K.M. and Hogan, B.L.M. (1990) Embryonic expression of a haematopoietic growth factor encoded by the Sl locus and the ligand for c-kit. Nature, 347, 667-669.
53. Matsui, Y., Toksoz, D., Nishikawa, S. et al. (1991) Effect of Steel factor and leukaemia inhibitory factor on murine primordial germ cells in culture. Nature, 353, 750-752.
54. Mauduit, C., Hamamah, S. and Benahmed, M. (1999) Growth factors in testis development and function: an update. In Hamamah, S., Frydman, R., Mieusset, R. and Olivennes, F. (eds), Male Sterility for Motility Disorders: Etiological Factors and Treatment. Springer-Verlag, Berlin, 173-188.
55. Mauduit, C., Chatelain, G., Magre, S. et al. (1999) Regulation by pH of the alternative splicing of the stem cell factor pre-mRNA in the testis. J. Biol. Chem., 274, 770-775.
56. McCoshen, J.A. and McCallion, D.J. (1975) A study of the primordial germ cells during their migratory phase in Steel mutant mice. Experientia, 31, 589-590.
57. Meyts, E.R., Jorgensen, N., Muller, J. et al. (1996) Prolonged expression of the c-kit receptor in germ cells of intersex fetal testes. J. Pathol., 178, 166-169.
58. Mintz, B. and Russell, E.S. (1957) Gene-induced embryological modifications of primordial germ cells in the mouse. J. Exp. Zool., 134, 207-237.
59. Monk, M. and McLaren, A. (1981) X-chromosome activity in foetal germ cells of the mouse. J. Embryol. Exp. Morphol., 63, 75-84.
60. Morrison, G.K. and Takahashi, Y. (1993) Steel factor and c-kit receptor: from mutants to a growth factor system. BioEssays, 15, 77-83.
61. Morrison, S.J., Shah, N.M. and Anderson, D.J. (1997) Regulatory mechanisms in stem cell biology. Cell, 88, 287-298.
62. Motro, B., Van der Kooy, D., Rossant, J. et al. (1991) Contiguous patterns of c-kit and steel expression: analysis of mutations at the W and Sl loci. Development, 102, 1207-1221.
63. Nehar, D., Mauduit, C., Boussouar, F. and Benahmed, M. (1997) TNFα-stimulated lactate production is linked to lactate dehydrogenase A expression and activity increase in porcine cultured Sertoli cells. Endocrinology, 138, 1964-1971.
64. Nocka, K., Tan, J.C., Chiu, E. et al. (1990) Molecular bases of dominant negative and loss of function mutations at the murine c-kit/white spotting locus: W37, Wv, W41 and W. EMBO J., 9, 1805-1813.
65. Ogawa, M., Matsuzaki, Y., Nishikawa, S. et al. (1991) Expression and function of c-kit in hemopoietic progenitor cells. J. Exp. Med., 174, 63-71.
66. Okabe, M., Ikawa, M. and Ashkenas, J. (1998) Gametogenesis '98: male infertility and the genetics of spermatogenesis. Am. J. Hum. Genet., 62, 1274-1281.
67. Orth, J.M., Jester, W.F. and Qiu, J. (1996) Gonocytes in testes of neonatal rats express the c-kit gene. Mol. Reprod. Dev., 45, 123-131.
68. Pandiella, A., Bosenberg, M.W., Huang, E.J. et al. (1992) Cleavage of membrane-anchored growth factors involves distinct protease activities regulated through common mechanisms. J. Biol. Chem., 267, 24028-24033.
69. Rajpert-De Meyts, M.E. and Skakkebaek, N.E. (1994) Expression of the c-kit protein product in carcinoma-in-situ and invasive testicular germ cell tumours. Int. J. Androl., 17, 85-92.
70. Reith, A.D., Rottapel, R., Giddens, E. et al. (1990) W mutant mice with mild or severe developmental defects contain distinct point mutations in the kinase domain of the c-kit receptor. Genes Dev., 4, 390-400.
71. Reith, A.D., Ellis, C., Lyman, S.D. et al. (1991) Signal transduction by normal isoforms and W mutant variants of the Kit receptor tyrosine kinase. EMBO J., 10, 2451-2459.
72. Robertson, D.M., Risbridger, G.P., Hedger, M. and McLachlan, R.I. (1993) Growth factors in the control of testicular function. In de Kretser, D. (ed.), Molecular Biology of the Male Reproductive System. Academic Press, San Diego, pp. 411-438.
73. Roosen-Runge, E.C. (1952) Kinetic of spermatogenesis in mammals. Ann. N.Y. Acad. Sci., 55, 574-584.
74. Rossi, P., Albanesi, C., Grimaldi, P. et al. (1991) Expression of the mRNA for the ligand of c-kit in mouse Sertoli cells. Biochem. Biophys. Res. Commun., 176, 910-914.
75. Rossi, P., Dolci, S., Albanesi, C. et al. (1993) 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., 155, 68-74.
76. Sandlow, J.I., Feng, H.-L., Cohen, M.B. et al. (1996) Expression of c-kit and its ligand, stem cell factor, in normal and subfertile human testicular tissue. J. Androl., 17, 403-408.
77. Sarvella, P.A. and Russell, L.B. (1956) Stell, a new dominant gene in the house mouse. J. Hered., 47, 123-128.
78. Schlegel, P.N. (1999) Debate: Is ICSI a genetic time bomb? No: ICSI is safe and effective. J. Androl., 20, 18-23.
79. Strohmeyer, T., Reese, D., Press, M. et al. (1995) Expression of the c-kit proto-oncogene and its ligand stem cell factor (SCF) in normal and malignant human testicular tissue. J. Urol., 153, 511-515.
80. Tajima, Y., Onoue, H., Kitamura, Y. et al. (1991) Biologically active c-kit ligand growth factor is produced by mouse Sertoli cells and is defective in Sl/d mutant mice. Development, 113, 1031-1035.
81. Tam, P.P.L. and Snow, M.H.L. (1981) Proliferation and migration of primordial germinal cells during compensatory growth in mouse embryos. J. Embryol. Exp. Morphol., 64, 133-147.
82. Tan, J.C., Nocka, K., Ray, P. et al. (1990) The dominant W42 spotting phenotype results from a missense mutation in the c-kit receptor kinase. Science, 247, 209-212.
83. Tesarik, J., Greco, E., Cohen-Bacrie, P. et al. (1998) Germ cell apoptosis in men with complete and incomplete spermiogenesis failure. Mol. Hum. Reprod., 4, 757-762.
84. Toksoz, D., Zsebo, K.M., Smith, K.A. et al. (1992) Support of human hematopoiesis in long-term bone marrow cultures by murine stromal cells selectively expressing the membrane-bound and secreted forms of the human homolog of the steel gene product, stem cell factor. Proc. Natl Acad. Sci. USA, 89, 7350-7354.
85. Vandenbark, G.R., de Castro, C.M., Taylor, H. et al. (1992) Cloning and structural analysis of the human c-kit gene. Oncogene, 7, 1259-1266.
86. Verhoeven, G. and Cailleau, J. (1991) Rat tumor Leydig cells as a test system for the study of Sertoli cell factors that stimulate steroidogenesis. J. Androl., 12, 9-17.
87. Vincent, S., Segretain, D., Nishikawa, S. et al. (1998) Stage-specific expression of the kit receptor and its ligand (KL) during male gametogenesis in the mouse: a kit-KL interaction critical for meiosis. Development, 125, 4585-1593.
88. Wang, R.A., Nakane, P.K. and Koji, T. (1998) Autonomous cell death of mouse male germ cells during fetal and postnatal period. Biol. Reprod., 58, 1250-1256.
89. Wassarman, P.M. (1996) Oogenesis. In Adashi, E.Y., Rock, J.A. and Rosenwaks, Z. (eds) Reproductive Endocrinology, Surgery and Technology. Lippincott-Raven, Philadelphia, pp. 341-358.
90. Yan, W., Linderborg, J., Suominen, J. et al., (1999) Stage specific regulation of stem cell factor gene expression in the rat seminiferous epithelium. Endocrinology, 140, 1499-1504.
91. Yarden, Y., Kuang, W.-J., Yang-Feng et al. (1987) Human proto-oncogene c-kit: a new cell surface receptor tyrosine kinase for an unidentified ligand. EMBO J., 6, 3341-3351.
92. Yee, N.S., Paek, I. and Besmer, P. (1994) Role of kit-ligand in proliferation and suppression of apoptosis in mast cells: basis for radiosensitivity of white spotting and steel mutant mice. J. Exp. Med., 179, 1777-1787.
93. Yoshinaga, K., Nishikawa, S., Ogawa, M. et al. (1991) Role of c-kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c-kit expression and function. Development, 113, 689-699.