Deficiency of Trp53 rescues the male fertility defects of Kit(W-v) mice but has no effect on the survival of melanocytes and mast cells

Developmental Biology

Volumn 215, Issue 1, 1999, Pages 78-90

  Jordan, Siobhán A ^a   Speed, Robert M ^a   Bernex, Florence ^b   Jackson, Ian J ^a  

^a WESTERN GENERAL HOSPITAL   (United Kingdom)

^b ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

Author keywords

Germ cells; Kit(W v); Mast cells; Melanocytes; Mgf; Mice; Trp53

Indexed keywords

INTERLEUKIN 3; PROTEIN P53; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FEMALE; GERM CELL; MALE; MALE FERTILITY; MAST CELL; MELANOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALIA; MAMMALIA;

EID: 0033230194     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1999.9440     Document Type: Article

References (75)

1. Abrahamson J. L., Lee J. M., Bernstein A. Regulation of p53-mediated apoptosis and cell cycle arrest by Steel factor. Mol. Cell. Biol. 15:1995;6953-6960.
2. Bachvarova R. F., Manova K., Besmer P. Role in gametogenesis of c-kit encoded at the W locus of mice. Bernfield M. Molecular Basis of Morphogenesis. 1993;1-18 Wiley-Liss, New York.
3. Bedell M. A., Brannan C. I., Evans E. P., Copeland N. G., Jenkins N. A., Donovan P. J. 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. 9:1995;455-470.
4. lacZ mouse embryos. Development. 122:1996;3023-3033.
5. Blume-Jensen P., Siegbahn A., Stabel S., Heldin C. H., Ronnstrand L. Increased Kit/SCF receptor induced mitogenicity but abolished cell motility after inhibition of protein kinase C. EMBO J. 12:1993;4199-4209.
6. Blume-Jensen P., Ronnstrand L., Gout I., Waterfield M. D., Heldin C. H. Modulation of Kit/stem cell factor receptor-induced signaling by protein kinase C. J. Biol. Chem. 269:1994;21793-21802.
7. Blume-Jensen P., Janknecht R., Hunter T. The kit receptor promotes cell survival via activation of PI 3-kinase and subsequent Akt-mediated phosphorylation of Bad on Ser136. Curr. Biol. 8:1998;779-782.
8. Brandt J. E., Bhalla K., Hoffman R. Effects of interleukin-3 and c-kit ligand on the survival of various classes of human hematopoietic progenitor cells. Blood. 83:1994;1507-1514.
9. Buehr M., Pearce-Kelly A., McLaren A. Failure of primordial germ cells to proliferate on fibroblasts from Steel mutant mice in vitro. Biol. Res. 26:1993;411-415.
10. Cable J., Jackson I. J., Steel K. P. Mutations at the W locus affect survival of neural crest-derived melanocytes in the mouse. Mech. Dev. 50:1995;139-150.
11. Canman C. E., Gilmer T. M., Coutts S. B., Kastan M. B. Growth factor modulation of p53-mediated growth arrest versus apoptosis. Genes Dev. 9:1995;600-611.
12. Clarke A. R., Purdie C. A., Harrison D. J., Morris R. G., Bird C. C., Hooper M. L., Wyllie A. H. Thymocyte apoptosis induced by p53-dependent and independent pathways. Nature. 362:1993;849-852.
13. Coulombre J. L., Russell E. S. Analysis of the pleiotropism at the W-locus in the mouse. J. Exp. Zool. 126:1954;277-295.
14. Copeland N. G., Gilbert D. J., Cho B. C., Donovan P. J., Jenkins N. A., Cosman D., Anderson D., Lyman S. D., Williams D. E. Mast cell growth factor maps near the steel locus on mouse chromosome 10 and is deleted in a number of steel alleles. Cell. 63:1990;175-183.
15. Digiuseppe J. A., Kastan M. B., Weng L. J., Gore S. D. Cytoprotective effects of hematopoietic growth factors on primary human acute myeloid leukemias are not mediated through changes in BCL-2, BAX, or p21WAF1/CIP1. In Vivo. 13:1999;1-6.
16. Dolci S., Williams D. E., Ernst M. K., Resnick J. L., Brannan C. I., Lock L. F., Lyman S. D., Boswell H. S., Donehower L. A., Harvey M., Slagle B. L., McArthur M. J., Montgomery C. A. J., Butel J. S., Bradley A. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature. 356:1992;215-221.
17. Donovan P. J. Requirement for mast cell growth factor for primordial germ cell survival in culture. Nature. 352:1991;809-811.
18. Fujita J., Nakayama H., Onoue H., Kanakura Y., Nakano T., Asai H., Takeda S., Honjo T., Kitamura Y. Fibroblast-dependent growth of mouse mast cells in vitro: Duplication of mast cell depletion in mutant mice of W/Wv genotype. J. Cell. Physiol. 134:1988;78-84.
19. Geissler E. N., McFarland E. C., Russell E. S. Analysis of pleiotropism at the dominant white-spotting (W) locus of the house mouse: A description of ten new W alleles. Genetics. 97:1981;337-361.
20. Godin I., Deed R., Cooke J., Zsebo K., Dexter M., Wylie C. C. Effects of the steel gene product on mouse primordial germ cells in culture. Nature. 352:1991;807-809.
21. Gottlieb E., Oren M. p53 facilitates pRb cleavage in IL-3-deprived cells: Novel pro-apoptotic activity of p53. EMBO J. 17:1998;3587-3596.
22. Hemesath T. J., Price E. R., Takemoto C., Badalian T., Fisher D. E. MAP kinase links the transcription factor Microphthalmia to c-Kit signalling in melanocytes. Nature. 391:1998;298-301.
23. Horie K., Takakura K., Taii S., Narimoto K., Noda Y., Nishikawa S., Nakayama H., Fujita J., Mori T. The expression of c-kit protein during oogenesis and early embryonic development. Biol. Reprod. 45:1991;547-552.
24. Huang E. J., Manova K., Packer A. I., Sanchez S., Bachvarova R. F., Besmer P. The murine steel panda mutation affects kit ligand expression and growth of early ovarian follicles. Dev. Biol. 157:1993;100-109.
25. Ikuta K., Weissman I. L. Evidence that hematopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation. Proc. Natl. Acad. Sci. USA. 89:1992;1502-1506.
26. Johnson P., Chung S., Benchimol S. Growth suppression of Friend virus-transformed erythroleukemia cells by p53 protein is accompanied by hemoglobin production and is sensitive to erythropoietin. Mol. Cell. Biol. 13:1993;1456-1463.
27. The Atlas of Mouse Development. 1992;Academic Press, London.
28. t mice. Dev. Biol. 126:1988;71-79.
29. Lahav R., Lecoin L., Ziller C., Nataf V., Carnahan J. F., Martin F. H., Le Douarin N. M. Effect of the Steel gene product on melanogenesis in avian neural crest cell cultures. Differentiation. 58:1994;133-139.
30. Li M., Hu J., Heermeier K., Hennighausen L., Furth P. A. Apoptosis and remodeling of mammary gland tissue during involution proceeds through p53-independent pathways. Cell Growth Differ. 7:1996;13-20.
31. Lotem J., Sachs L. Hematopoietic cells from mice deficient in wild-type p53 are more resistant to induction of apoptosis by some agents. Blood. 82:1993;1092-1096.
32. Lowe S. W., Schmitt E. M., Smith S. W., Osborne B. A., Jacks T. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature. 362:1993;847-849.
33. MacKenzie M. A., Jordan S. A., Budd P. S., Jackson I. J. Activation of the receptor tyrosine kinase Kit is required for the proliferation of melanoblasts in the mouse embryo. Dev. Biol. 192:1997;99-107.
34. Macleod K. F., Hu Y., Jacks T. Loss of Rb activates both p53-dependent and independent cell death pathways in the developing mouse nervous system. EMBO J. 15:1996;6178-6188.
35. Manova K., Nocka K., Besmer P., Bachvarova R. F. Gonadal expression of c-kit encoded at the W locus of the mouse. Development. 110:1990;1057-1069.
36. Manova K., Bachvarova R. F. Expression of c-kit encoded at the W locus of mice in developing embryonic germ cells and presumptive melanoblasts. Dev. Biol. 146:1991;312-324.
37. Manova K., Huang E. J., Angeles M., De L. V., Sanchez S., Pronovost S. M., Besmer P., Bachvarova R. F. 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. 157:1993;85-99.
38. Malcomson R. D., Clarke A. R., Peter A., Coutts S. B., Howie S. E., Harrison D. J. Apoptosis induced by gamma-irradiation, but not CD4 ligation, of peripheral T lymphocytes in vivo is p53-dependent. J. Pathol. 181:1997;166-171.
39. Matsui Y., Toksoz D., Nishikawa S., Williams D., Zsebo K., Hogan B. L. Effect of Steel factor and leukaemia inhibitory factor on murine primordial germ cells in culture. Nature. 353:1991;750-752.
40. McCoshen J. A., McCallion D. J. A study of the primordial germ cells during their migratory phase in Steel mutant mice. Experientia. 31:1975;589-590.
41. McLaren A. Oocytes in the testis. Nature. 283:1980;688-689.
42. Mintz B., Russell E. S. Gene-induced embryological modifications of primordial germ cells in the mouse. J. Exp. Zool. 134:1957;207-237.
43. Morrison-Graham K., Weston J. A. Transient steel factor dependence by neural crest-derived melanocyte precursors. Dev. Biol. 159:1993;346-352.
44. Motro B., Bernstein A. Dynamic changes in ovarian c-kit and Steel expression during the estrous reproductive cycle. Dev. Dyn. 197:1993;69-79.
45. Murphy M., Reid K., Williams D. E., Lyman S. D., Bartlett P. F. Steel factor is required for maintenance, but not differentiation, of melanocyte precursors in the neural crest. Dev. Biol. 153:1992;396-401.
46. Nishikawa S., Kusakabe M., Yoshinaga K., Ogawa M., Hayashi S., Kunisada T., Era T., Sakakura T. In utero manipulation of coat color formation by a monoclonal anti-c-kit antibody: Two distinct waves of c-kit-dependency during melanocyte development. EMBO J. 10:1991;2111-2118.
47. 41 and W. EMBO J. 9:1990;1805-1813.
48. Ogawa M., Matsuzaki Y., Nishikawa S., Hayashi S., Kunisada T., Sudo T., Kina T., Nakauchi H. Expression and function of c-kit in hemopoietic progenitor cells. J. Exp. Med. 174:1991;63-71.
49. Ogawa M., Nishikawa S., Yoshinaga K., Hayashi S., Kunisada T., Nakao J., Kina T., Sudo T., Kodama H. Expression and function of c-Kit in fetal hemopoietic progenitor cells: Transition from the early c-Kit-independent to the late c-Kit-dependent wave of hemopoiesis in the murine embryo. Development. 117:1993;1089-1098.
50. Packer A. I., Hsu Y. C., Besmer P., Bachvarova R. F. The ligand of the c-kit receptor promotes oocyte growth. Dev. Biol. 161:1994;194-205.
51. Paulson R. F., Vesely S., Siminovitch K. A., Bernstein A. Signalling by the W/Kit receptor tyrosine kinase is negatively regulated in vivo by the protein tyrosine phosphatase Shp1. Nat. Genet. 13:1996;309-315.
52. Pesce M., Di Carlo A., De Felici M. The c-kit receptor is involved in the adhesion of mouse primordial germ cells to somatic cells in culture. Mech. Dev. 68:1997;37-44.
53. Peters H. The development of the mouse ovary from birth to maturity. Acta Endocrinol. (Copenhagen). 62:1969;98-116.
54. Philo J. S., Wen J., Wypych J., Schwartz M. G., Mendiaz E. A., Langley K. E. Human stem cell factor dimer forms a complex with two molecules of the extracellular domain of its receptor, Kit. J. Biol. Chem. 271:1996;6895-6902.
55. Reith A. D., Rottapel R., Giddens E., Brady C., Forrester L., Bernstein A. W mutant mice with mild or severe developmental defects contain distinct point mutations in the kinase domain of the c-kit receptor. Genes Dev. 4:1990;390-400.
56. Rossi P., Dolci S., Albanesi C., Grimaldi P., Ricca R., Geremia R. 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. 155:1993;68-74.
57. Rotter V., Schwartz D., Almon E., Goldfinger N., Kapon A., Meshorer A., Donehower L. A., Levine A. J. Mice with reduced levels of p53 protein exhibit the testicular giant-cell degenerative syndrome. Proc. Natl. Acad. Sci. USA. 90:1993;9075-9079.
58. Sandlow J. I., Feng H. L., Sandra A. Localization and expression of the c-kit receptor protein in human and rodent testis and sperm. Urology. 49:1997;494-500.
59. Searle A. G., Beechey C. V. Sperm-count, egg-fertilization and dominant lethality after X-irradiation of mice. Mutat. Res. 22:1974;63-72.
60. Serve H., Yee N. S., Stella G., Sepp-Lorenzino L., Tan J. C., Besmer P. Differential roles of PI3-kinase and Kit tyrosine 821 in Kit receptor-mediated proliferation, survival and cell adhesion in mast cells. EMBO J. 14:1995;473-483.
61. Shibata M. A., Maroulakou I. G., Jorcyk C. L., Gold L. G., Ward J. M., Green J. E. p53-independent apoptosis during mammary tumor progression in C3(1)/SV40 large T antigen transgenic mice: Suppression of apoptosis during the transition from preneoplasia to carcinoma. Cancer Res. 56:1996;2998-3003.
62. Silva A., Wyllie A., Collins M. K. p53 is not required for regulation of apoptosis or radioprotection by interleukin-3. Blood. 89:1997;2717-2722.
63. Simpson E. M., Linder C. C., Sargent E. E., Davisson M. T., Mobraaten L. E., Sharp J. J. Genetic variation among 129 substrains and its importance for targeted mutagenesis in mice. Nat. Genet. 16:1997;19-27.
64. Sorrentino V., Giorgi M., Geremia R., Besmer P., Rossi P. Expression of the c-kit proto-oncogene in the murine male germ cells. Oncogene. 6:1991;149-151.
65. Steel K. P., Davidson D. R., Jackson I. J. TRP-2/DT, a new early melanoblast marker, shows that steel growth factor (c-kit ligand) is a survival factor. Development. 115:1992;1111-1119.
66. Threadgill D. W., Yee D., Matin A., Nadeau J. H., Magnuson T. Genealogy of the 129 inbred strains: 129/SvJ is a contaminated inbred strain. Mamm. Genome. 8:1997;390-393.
67. Timokhina I., Kissel H., Stella G., Besmer P. Kit signaling through PI 3-kinase and Src kinase pathways: An essential role for Rac1 and JNK activation in mast cell proliferation. EMBO J. 17:1998;6250-6262.
68. Wehrle-Haller B., Weston J. A. Soluble and cell-bound forms of steel factor activity play distinct roles in melanocyte precursor dispersal and survival on the lateral neural crest migration pathway. Development. 121:1995;731-742.
69. Yee N. S., Paek I., Besmer P. 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. 179:1994;1777-1787.
70. Yin Y., Stahl B. C., DeWolf W. C., Morgentaler A. p53-mediated germ cell quality control in spermatogenesis. Dev. Biol. 204:1998;165-171.
71. Yonish-Rouach E., Resnitzky D., Lotem J., Sachs L., Kimchi A., Oren M. Wild-type p53 induces apoptosis of myeloid leukaemic cells that is inhibited by interleukin-6. Nature. 352:1991;345-347.
72. Yonish-Rouach E., Grunwald D., Wilder S., Kimchi A., May E., Lawrence J. J., May P., Oren M. p53-mediated cell death: Relationship to cell cycle control. Mol. Cell. Biol. 13:1993;1415-1423.
73. Yoshida H., Takakura N., Kataoka H., Kunisada T., Okamura H., Nishikawa S. I. Stepwise requirement of c-kit tyrosine kinase in mouse ovarian follicle development. Dev. Biol. 184:1997;122-137.
74. Yoshinaga K., Nishikawa S., Ogawa M., Hayashi S., Kunisada T., Fujimoto T. Role of c-kit in mouse spermatogenesis: Identification of spermatogonia as a specific site of c-kit expression and function. Development. 113:1991;689-699.
75. Zha J., Harada H., Yang E., Jockel J., Korsmeyer S. J. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell. 87:1996;619-628.