Point mutation in Kit receptor tyrosine kinase reveals essential roles for Kit signaling in spermatogenesis and oogenesis without affecting other Kit responses

EMBO Journal

Volumn 19, Issue 6, 2000, Pages 1312-1326

  Kissel, Holger ^a   Timokhina, Inna ^a,b   Hardy, Matthew P ^c   Rothschild, Gerson ^a,b   Tajima, Youichi ^a,d   Soares, Vera ^a,e   Angeles, Michael ^a   Whitlow, Scott R ^a   Manova, Katia ^a   Besmer, Peter ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Weill Cornell Medical Center   (United States)

^c POPULATION COUNCIL   (United States)

^d TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^e UNIVERSITY OF IOWA   (United States)

Author keywords

Kit receptor tyrosine kinase; Leydig cells; Oogenesis; PI 3 kinase; Spermatogenesis

Indexed keywords

MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL HYPERPLASIA; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; INFERTILITY; LEYDIG CELL; MALE; MAST CELL; MOUSE; MOUSE MUTANT; NONHUMAN; OOCYTE DEVELOPMENT; OVARY FOLLICLE DEVELOPMENT; POINT MUTATION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPERMATOGENESIS;

ANIMALIA;

EID: 0034654307     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.6.1312     Document Type: Article

References (86)

1. Alai, M., Mui, A.L., Cutler, R.L., Bustelo, X.R., Barbacid, M. and Krystal, G. (1992) Steel factor stimulates the tyrosine phosphorylation of the proto-oncogene product, p95vav, in human hemopoietic cells. J. Biol. Chem., 267, 18021-18025.
2. Bachvarova, R.F., Manova, K. and Besmer, P. (1993) Role in gametogenesis of c-kit encoded at the W locus of mice. In Bernfield, M. (ed.), Molecular Basis of Morphogenesis. Wiley-Liss, New York, NY.
3. Bennett, D. (1956) Developmental analysis of a mutation with pleiotropic effects in the mouse. J. Morphol., 98, 199-229.
4. Besmer, P. (1997) Kit-ligand-stem cell factor. In Garland, J.M., Quesenberry, P.J. and Hilton, D.J. (eds), Colony-Stimulating Factors: Molecular and Cellular Biology. Marcel Dekker, New York, NY.
5. Besmer, P., Manova, K., Duttlinger, R., Huang, E.J., Packer, A., Gyssler, C. and Bachvarova, R.F. (1993) The kit-ligand (steel factor) and its receptor c-kit/W: pleiotropic roles in gametogenesis and melanogenesis. Dev. Suppl., 125-137.
6. Blume-Jensen, P., Ronnstrand, L., Gout, I., Waterfield, M.D. and Heldin, C.H. (1994) Modulation of Kit/stem cell factor receptor-induced signaling by protein kinase C. J. Biol. Chem., 269, 21793-21802.
7. Brannan, C.I. et al. (1992) Developmental abnormalities in Steel17H mice result from a splicing defect in the steel factor cytoplasmic tail. Genes Dev., 6, 1832-1842.
8. Brunet, A. et al. (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor: Cell, 96, 857-868.
9. Buehr, M., McLaren, A., Bartley, A. and Darling, S. (1993) Proliferation and migration of primordial germ cells in We/We mouse embryos. Dev. Dyn., 198, 182-189.
10. Carpenter, C.L. and Cantley, L.C. (1996) Phosphoinositide kinases. Curr. Opin. Cell Biol., 8, 153-158.
11. Chabot, B., Stephenson, D.A., Chapman, V.M., Besmer, P. and Bernstein, A. (1988) The proto-oncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus. Nature, 335, 88-89.
12. Chandrashekar V., Bartke, A. and Wagner, T.E. (1988) Endogenous human growth hormone (GH) modulates the effect of gonadotropin-releasing hormone on pituitary function and the gonadotropin response to the negative feedback effect of testosterone in adult male transgenic mice bearing human GH gene. Endocrinology, 123, 2717-2722.
13. Cochran, R.C., Ewing, L.L. and Niswender, G.D. (1981) Serum levels of follicle stimulating hormone, luteinizing hormone, prolactin, testosterone, 5 α-dihydrotestosterone, 5 α-androstane-3 α, 17 β-diol, 5 α-androstane-3 β, 17 β-diol, and 17 β-estradiol from male beagles with spontaneous or induced benign prostatic hyperplasia. Invest. Urol., 19, 142-147.
14. Copeland, N.G., Gilbert, D.J., Cho, B.C., Donovan, P.J., Jenkins, N.A., Cosman, D., Anderson, D., Lyman, S.D. and Williams, D.E. (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.
15. Cutler, R.L., Liu, L., Damen, J.E. and Krystal, G. (1993) Multiple cytokines induce the tyrosine phosphorylation of Shc and its association with Grb2 in hemopoietic cells. J. Biol. Chem., 268, 21463-21465.
16. Datta, S.R., Dudek, H., Tao, X., Masters, S., Fu, H., Gotoh, Y. and Greenberg, M.E. (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell, 91, 231-241.
17. Datta, S.R., Brunet, A. and Greenberg, M.E. (1999) Cellular survival: a play in three Akts. Genes Dev., 13, 2905-2927.
18. Domin, J. and Waterfield, M.D. (1997) Using structure to define the function of phosphoinositide 3-kinase family members. FEBS Lett., 410, 91-95.
19. Dong, J., Albertini, D.F., Nishimori, K., Kumar, T.R., Lu, N. and Matzuk, M.M. (1996) Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature, 383, 531-535.
20. Dube, J.L., Wang, R., Elvin, J., Lyons, K.M., Celeste, A.J. and Matzuk, M.M. (1998) The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol. Endocrinol., 12, 1809-1817.
21. Duronio, V., Welham, M.J., Abraham, S., Dryden, P. and Schrader, J.W. (1992) p21ras activation via hemopoietin receptors and c-kit requires tyrosine kinase activity but not tyrosine phosphorylation of p21ras GTPase-activating protein. Proc. Natl. Acad. Sci. USA, 89, 1587-1591.
22. Eppig, J.J., Chesnel, F., Hirao, Y., O'Brien, M.J., Pendola, F.L., Watanabe, S. and Wigglesworth, K. (1997) Oocyte control of granulosa cell development: how and why. Hum. Reprod., 12, 127-132.
23. Franke, T.F., Yang, S.I., Chan, T.O., Datta, K., Kazlauskas, A., Morrison, D.K., Kaplan, D.R. and Tsichlis, P.N. (1995) The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell, 81, 727-736.
24. Fruman, D.A., Rameh, L.E. and Cantley, L.C. (1999a) Phosphoinositide binding domains: embracing 3-phosphate. Cell, 97, 817-820.
25. Fruman, D.A., Snapper, S.B., Yballe, C.M., Davidson, L., Yu, J.Y. Alt, F.W. and Cantley, L.C. (1999b) Impaired B cell development and proliferation in absence of phosphoinositide 3-kinase p85α. Science, 283, 393-397.
26. Galli, S.J., Zsebo, K.M. and Geissler, E.N. (1994) The kit ligand, stem cell factor. Adv. Immunol., 55, 1-96.
27. Gavrieli, Y., Sherman, Y. and Ben-Sasson, S.A. (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol., 119, 493-501.
28. Ge, R.S., Shan, L.X. and Hardy, M.P. (1996) Pubertal development of Leydig cells. In Payne, A.H., Hardy, M.P. and Russell, L.D. (eds), The Leydig Cell. Cache River Press, Vienna, IL, pp. 159-173.
29. 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.
30. Gokkel, E., Grossman, Z., Ramot, B., Yarden, Y. Rechavi, G. and Givol, D. (1992) Structural organization of the murine c-kit proto-oncogene. Oncogene, 7, 1423-1429.
31. Gougeon, A. (1996) Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr. Rev., 17, 121-155.
32. Herbst, R., Shearman, M.S., Jallal, B., Schlessinger, J. and Ullrich, A. (1995) Formation of signal transfer complexes between stem cell and platelet-derived growth factor receptors and SH2 domain proteins in vitro. Biochemistry, 34, 5971-5979.
33. Horie, K., Takakura, K., Taii, S., Narimoto, K., Noda, Y. Nishikawa, S., Nakayama, H., Fujita, J. and Mori, T. (1991) The expression of c-kit protein during oogenesis and early embryonic development. Biol. Reprod., 45, 547-552.
34. Huang, E.J., Nocka, K., Beier, D.R., Chu, T.Y. Buck, J., Lahm, H.W., Wellner, D., Leder, P. and Besmer, P. (1990) The hematopoietic growth factor KL is encoded by the SI locus and is the ligand of the c-kit receptor, the gene product of the W locus. Cell, 63, 225-233.
35. Huang, E.J., Manova, K., Packer, A.I., Sanchez, S., Bachvarova, R.F. and Besmer, P. (1993) The murine steel panda mutation affects kit ligand expression and growth of early ovarian follicles. Dev. Biol., 157, 100-109.
36. Kitamura, Y., Go, S. and Hatanaka, K. (1978) Decrease of mast cells in W/Wv mice and their increase by bone marrow transplantation. Blood, 52, 447-452.
37. Koshimizu, U., Sawada, K., Tajima, Y., Watanabe, D. and Nishimune, Y. (1991) White-spotting mutations affect the regenerative differentiation of testicular germ cells: demonstration by experimental cryptorchidism and its surgical reversal. Biol. Reprod., 45, 642-648.
38. Kuroda, H., Terada, N., Nakayama, H., Matsumoto, K. and Kitamura, Y. (1988) Infertility due to growth arrest of ovarian follicles in SI/SIt mice. Dev. Biol., 126, 71-79.
39. Lakso, M., Pichel, J.G., Gorman, J.R., Sauer, B., Okamoto, Y., Lee, E., Alt, F.W. and Westphal, H. (1996) Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl Acad. Sci. USA, 93, 5860-5865.
40. Lau, M.M. Stewart, C.E., Liu, Z., Bhatt, H., Rotwein, P. and Stewart, C.L. (1994) Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev., 8, 2953-2963.
41. Lee, M.M., Seah, S.C., Masiakos, P.T., Sottas, C.M., Preffer, F.I., Donahoe, P.K., Maclaughlin, D.T. and Hardy, M.P. (1999) Mullerian-inhibiting substance type II receptor expression and function in purified rat Leydig cells. Endocrinology, 140, 2819-2827.
42. 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.
43. Manova, K., Nocka, K., Besmer, P. and Bachvarova, R.F. (1990) Gonadal expression of c-kit encoded at the W locus of the mouse. Development, 110, 1057-1069.
44. Manova, K., Huang, E.J., Angeles, M., De Leon, V., Sanchez, S., Pronovost, S.M., Besmer, P. and Bachvarova, R.F. (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.
45. Manova, K. et al. (1998) Apoptosis in mouse embryos: elevated levels in pregastrulae and in the distal anterior region of gastrulae of normal and mutant mice. Dev. Dyn., 213, 293-308.
46. McDevitt, M.A., Shivdasani, R.A., Fujiwara, Y., Yang, H. and Orkin, S.H. (1997) A 'knockdown' mutation created by cis-element gene targeting reveals the dependence of erythroid cell maturation on the level of transcription factor GATA-1. Proc. Natl Acad. Sci. USA, 94, 6781-6785.
47. McGrath, S.A., Esquela, A.F. and Lee, S.J. (1995) Oocyte-specific expression of growth/differentiation factor-9. Mol. Endocrinol., 9, 131-136.
48. McLaren, A. and Southee, D. (1997) Entry of mouse embryonic germ cells into meiosis. Dev. Biol., 187, 107-113.
49. Mishina, Y., Rey, R., Finegold, M.J., Matzuk, M.M., Josso, N., Cate, R.L. and Behringer, R.R. (1996) Genetic analysis of the Mullerian-inhibiting substance signal transduction pathway in mammalian sexual differentiation. Genes Dev., 10, 2577-2587.
50. Motro, B. and Bernstein, A. (1993) Dynamic changes in ovarian c-kit and Steel expression during the estrous reproductive cycle. Dev. Dyn., 197, 69-79.
51. Motro, B., van der Kooy, D., Rossant, J., Reith, A. and Bernstein, A. (1991) Contiguous patterns of c-kit and steel expression: analysis of mutations at the W and SI loci. Development, 113, 1207-1221.
52. Murphy, E.D. (1972) Hyperplastic and early neoplastic changes in the ovaries of mice after genic deletion of germ cells. J. Natl Cancer Inst., 48, 1283-1295.
53. Murphy, E.D. and Beamer, W.G. (1973) Plasma gonadotropin levels during early stages of ovarian tumorigenesis in mice of the Wx-Wu genotype. Cancer Res., 33, 721-723.
54. Nakayama, H., Kuroda, H., Onoue, H., Fujita, J., Nishimune, Y., Matsumoto, K., Nagano, T., Suzuki, F. and Kitamura, Y. (1988) Studies of SI/SId in equilibrium with +/+ mouse aggregation chimaeras. II. Effect of the steel locus on spermatogenesis. Development, 102, 117-126.
55. Nishimune, Y. Haneji, T. and Kitamura, Y. (1980) The effects of steel mutation on testicular germ cell differentiation. J. Cell Physiol., 105, 137-141.
56. Orth, J.M., Qiu, J., Jester, W.F., Jr and Pilder, S. (1997) Expression of the c-kit gene is critical for migration of neonatal rat gonocytes in vitro. Biol. Reprod., 57, 676-683.
57. Packer, A.I., Besmer, P. and Bachvarova, R.F. (1995) Kit ligand mediates survival of type A spermatogonia and dividing spermatocytes in postnatal mouse testes. Mol. Reprod. Dev., 42, 303-310.
58. Peters, H. and Pedersen, T. (1967) Origin of follicle cells in the infant mouse ovary. Fertil. Steril., 18, 309-313.
59. Racine, C., Rey, R., Forest, M.G., Louis, F., Ferre, A., Huhtaniemi, I., Josso, N. and di Clemente, N. (1998) Receptors for anti-mullerian hormone on Leydig cells are responsible for its effects on steroidogenesis and cell differentiation. Proc. Natl Acad. Sci. USA, 95, 594-599.
60. Rameh, L.E. and Cantley, L.C. (1999) The role of phosphoinositide 3-kinase lipid products in cell function. J. Biol. Chem., 274, 8347-8350.
61. Reith, A.D., Ellis, C., Lyman, S.D., Anderson, D.M., Williams, D.E., Bernstein, A. and Pawson, T. (1991) Signal transduction by normal isoforms and W mutant variants of the Kit receptor tyrosine kinase. EMBO J., 10, 2451-2459.
62. Risma, K.A., Clay, C.M., Nett, T.M., Wagner, T., Yun, J. and Nilson, J.H. (1995) Targeted overexpression of luteinizing hormone in transgenic mice leads to infertility, polycystic ovaries, and ovarian tumors. Proc. Natl Acad. Sci. USA, 92, 1322-1326.
63. Rottapel, R., Reedijk, M., Williams, D.E., Lyman, S.D., Anderson, D.M., Pawson, T. and Bernstein, A. (1991) The Steel/W transduction pathway: kit autophosphorylation and its association with a unique subset of cytoplasmic signaling proteins is induced by the Steel factor. Mol. Cell. Biol., 11, 3043-3051.
64. Russell, E.S. (1979) Hereditary anemias of the mouse: a review for geneticists. Adv. Genet., 20, 357-459.
65. Schluter, C., Duchrow, M., Wohlenberg, C., Becker, M.H., Key, G., Flad, H.D. and Gerdes, J. (1993) The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining proteins. J. Cell Biol., 123, 513-522.
66. Serve, H., Hsu, Y.C. and Besmer, P. (1994) Tyrosine residue 719 of the c-kit receptor is essential for binding of the P85 subunit of phosphatidylinositol (PI) 3-kinase and for c-kit-associated PI 3-kinase activity in COS-1 cells. J. Biol. Chem., 269, 6026-6030.
67. Serve, H., Yee, N.S., Stella, G., Sepp-Lorenzino, L., Tan, J.C. and Besmer, P. (1995) Differential roles of PI3-kinase and Kit tyrosine 821 in Kit receptor-mediated proliferation, survival and cell adhesion in mast cells. EMBO J., 14, 473-483.
68. Silvers, W.K. (1979) The Coal Colors of Mice. Springer Verlag, New York, NY.
69. Suzuki, H., Terauchi, Y., Fujiwara, M., Aizawa, S., Yazaki, Y., Kadowaki, T. and Koyasu, S. (1999) Xid-like immunodeficiency in mice with disruption of the p85α subunit of phosphoinositide 3-kinase. Science, 283, 390-392.
70. Swiatek, P.J. and Gridley, T. (1993) Perinatal lethality and defects in hindbrain development in mice homozygous for a targeted mutation of the zinc finger gene Krox20. Genes Dev., 7, 2071-2084.
71. Tajima, Y., Huang, E.J., Vosseller, K., Ono, M., Moore, M.A. and Besmer, P. (1998a) Role of dimerization of the membrane-associated growth factor kit ligand in juxtacrine signaling: the SI17H mutation affects dimerization and stability-phenotypes in hematopoiesis. 7. Exp. Med., 187, 1451-1461.
72. Tajima, Y., Moore, M.A.S., Soares, V., Ono, M., Kissel, H. and Besmer, P. (1998b) Consequences of exclusive expression in vivo of kit-ligand lacking the major proteolytic cleavage site. Proc. Natl Acad. Sci. USA, 95, 11903-11908.
73. Tan, J.C., Nocka, K., Ray, P., Traktman, P. and Besmer, P. (1990) The dominant W42 spotting phenotype results from a missense mutation in the c-kit receptor kinase. Science, 247, 209-212.
74. Timokhina, I., Kissel, H., Stella, G. and Besmer, P. (1998) Kit signaling through PI 3-kinase and Src kinase pathways: an essential role for Rac1 and JNK activation in mast cell proliferation. EMBO J., 17, 6250-6262.
75. Toker, A. and Cantley, L.C. (1997) Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature, 387, 673-676.
76. Tomihara-Newberger, C., Haub, O., Lee, H.G., Soares, V., Manova, K. and Lacy, E. (1998) The amn gene product is required in extraembryonic tissues for the generation of middle primitive streak derivatives. Dev. Biol., 204, 34-54.
77. Vanderhyden, B.C. and Macdonald, E.A. (1998) Mouse oocytes regulate granulosa cell steroidogenesis throughout follicular development. Biol. Reprod., 59, 1296-1301.
78. Vanderhyden, B.C. and Tonary, A.M. (1995) Differential regulation of progesterone and estradiol production by mouse cumulus and mural granulosa cells by A factor(s) secreted by the oocyte. Biol. Reprod., 53, 1243-1250.
79. Verheij, M. et al. (1996) Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature, 380, 75-79.
80. Vincent, S., Segretain, D., Nishikawa, S., Nishikawa, S.I., Sage, J., Cuzin, F. and Rassoulzadegan, M. (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, 4585-4593.
81. Vosseller, K., Stella, G., Yee, N.S. and Besmer, P. (1997) c-kit receptor signaling through its phosphatidylinositide-3′-kinase-binding site and protein kinase C: role in mast cell enhancement of degranulation, adhesion, and membrane ruffling. Mol Biol. Cell, 8, 909-912.
82. 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.
83. Yi, T. and Ihle, J.N. (1993) Association of hematopoietic cell phosphatase with c-Kit after stimulation with c-Kit ligand. Mol. Cell. Biol., 13, 3350-3358.
84. Yoshida, H., Takakura, N., Kataoka, H., Kunisada, T., Okamura, H. and Nishikawa, S.I. (1997) Stepwise requirement of c-kit tyrosine kinase in mouse ovarian follicle development. Dev. Biol. 184, 122-137.
85. Yoshinaga, K., Nishikawa, S., Ogawa, M., Hayashi, S., Kunisada, T. and Fujimoto, T. (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.
86. Zsebo, K.M. et al. (1990) Stem cell factor is encoded at the SI locus of the mouse and is the ligand for the c-kit tyrosine kinase receptor Cell, 63, 213-224.