Parthenogenetic activation of mouse eggs by microinjection of a truncated c-kit tyrosine kinase present in spermatozoa

Development

Volumn 124, Issue 11, 1997, Pages 2267-2274

  Sette, Claudio ^a   Bevilacqua, Arturo ^b   Bianchini, Andrea ^a   Mangia, Franco ^b   Geremia, Raffaele ^a   Rossi, Pellegrino ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

c kit; Calcium; Egg activation; MAP kinase; Metaphase II arrest; Phospholipase C; Spermatozoa; Truncated receptor; Tyrosine kinase

Indexed keywords

CYTOPLASM PROTEIN; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; ONCOPROTEIN; PHOSPHOLIPASE C INHIBITOR; PROTEIN TYROSINE KINASE; RECEPTOR PROTEIN; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; EGG; ENZYME ACTIVITY; ENZYME LOCALIZATION; EXOCYTOSIS; FEMALE; FERTILIZATION; FLAGELLUM; MALE; MEIOSIS; MOUSE; NONHUMAN; ONCOGENE C KIT; OOCYTE; OOCYTE CLEAVAGE; OOCYTE DEVELOPMENT; PARTHENOGENESIS; PRIORITY JOURNAL; PRONUCLEUS; SPERMATOZOON;

ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CHELATING AGENTS; COS CELLS; CYTOPLASM; EGTAZIC ACID; ENZYME INHIBITORS; EXOCYTOSIS; FEMALE; ISOENZYMES; MALE; MEIOSIS; MICE; MICROINJECTIONS; OOCYTES; OVUM; PARTHENOGENESIS; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA; PROTO-ONCOGENE PROTEINS C-KIT; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; SEQUENCE DELETION; SPERM-OVUM INTERACTIONS; SPERMATOZOA;

ANIMALIA;

EID: 0030739524     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (46)

1. Albanesi, C., Geremia, R., Giorgio, M., Dolci, S., Sette, C. and Rossi, P. (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. Besmer, P. (1991). The kit ligand encoded at the murine steel locus: a pleiotropic growth and differentiation factor. Curr. Opin. Cell Biol. 3, 939-946.
3. Chantry, A. (1995). The kinase domain and membrane localization determine intracellular interactions between epidermal growth factor receptors. J. Biol. Chem. 270, 3068-3073.
4. Clarke, H. J., Rossant, J. and Masui, Y. (1988). Suppression of chromosome condensation during meiotic maturation induces parthenogenetic development of mouse oocytes. Development 104, 97-103.
5. Colledge, W. H., Carlton, M. B. L., Udy, G. B. and Evans, M. J (1994). Disruption of c-mos causes parthenogenetic development of unfertilized mouse eggs. Nature 370, 65-68.
6. Dale, B., De Felice, L. J. and Ehrenstein, G. (1985). Injection of a soluble sperm fraction into sea-urchin eggs triggers the cortical reaction. Experientia 41, 1068-1070.
7. Dolci, S., Williams, D. E., Ernst, M. K., Resnick, J. L., Brannan, C. I., Lock, L. F., Lyman, S. D., Boswell, H. S. and Donovan, P. J. (1991). Requirement for mast cell growth factor for primordial germ cell survival in culture. Nature 352, 809-811.
8. Dozortsev, D., Rybouchkin, A., De Sutter, P., Qian, C. and Dhont, M. (1995). Human oocyte activation following intracytoplasmic injection: the role of the sperm cell. Hum. Reprod. 10, 403-407.
9. Ducibella, T., Anderson, E., Albertini, D. F., Aalberg, J. and Rangarajan, S. (1988). Quantitative studies of changes in cortical granule number and distribution in the mouse oocyte during meiotic maturation. Dev. Biol. 130, 184-197.
10. 2+ spiking. Biochem J. 316, 53-591.
11. Haccard, O., Sarcevic, B., Lewellyn, A., Hartley, R., Roy, L., Izumi, T., Erikson, E. and Mailer, J. L. (1993). Induction of metaphase arrest in cleaving Xenopus embryos by MAP kinase. Science 262, 1262-1265.
12. Hashimoto, N., Watanabe, N., Furuta, Y., Tamemoto, H., Sagata, N., Yokoyama, M., Okazaki, K., Nagayoshi, M., Takeda, N., Ikawa, Y. and Aizawa, S. (1994). Parthenogenetic activation of oocytes in c-mos-deficient mice. Nature 370, 68-71
13. 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
14. Hernandez-Sotomayor, S. M. and Carpenter, G. (1993). Non-catalytic activation of phospholipase C-gamma1 in vitro by epidermal growth factor receptor. Biochem. J. 293, 507-511.
15. Hogan, B., Beddington, R., Costantini, F. and Lacy, E. (1994). In Manipulating the Mouse Embryo. Cold Spring Harbor. NY: Cold Spring Harbor Laboratory Press.
16. Homa, S. T., Carroll, J. and Swann, K. (1993). The role of calcium in mammalian oocyte maturation and egg activation. Hum. Reprod. 8, 1274-1281.
17. Horie, K., Takakura, K., Taii, S., Narimoto, K., Noda, Y., Nishikawa, S., Nakayama, H., Fujita, J. and Mori., T. (1991). The expression of the c-kit protein during oogenesis and early embryonic development. Biol. Reprod. 45, 547-552.
18. Ismail, R. S., Okawara, Y., Fryer, J. N. and Vanderheyden, B. C. (1996). Hormonal regulation of the ligand of c-kit in the rat ovary and its effects on spontaneous oocyte meiotic maturation. Mol. Reprod. Dev. 43, 458-469.
19. Kimura, Y. and Yanagimachi, R. (1995). Mouse oocytes injected with testicular spermatozoa or round spermatids can develop into normal offspring. Development 121, 2397-2405.
20. Kline, D. and Kline, J. T. (1992). Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Dev. Biol. 149, 80-89.
21. Kubiak, J. Z., Weber, M., de Pennart, H., Winston, N. J. and Maro, B. (1993). The metaphase II arrest in mouse oocytes is controlled through microtubule-dependent destruction of cyclin B in the presence of CSF. EMBO J. 12, 3773-3778.
22. Lorca, T., Cruzalegui, F. H., Fesquet, D., Cavadore, J. C., Mery, J., Means, A. and Doree, M. (1993). Calmodulin-dependent protein kinase II mediates inactivation of MPF and CSF upon fertilization of Xenopus eggs. Nature, 366, 270-273.
23. 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.
24. Melton, D. A., Krieg, P. A., Rebagliati, M. R., Maniatis, T., Zinn, K. and Green, M. R. (1984). Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids. Res. 12, 7035-7056.
25. Minshull, J., Sun, H., Tonks, N. K. and Murray, A. W. (1994). A MAP kinase-dependent spindle assembly checkpoint in Xenopus egg extracts. Cell 79, 475-486.
26. 2+ oscillations at fertilization of mammalian eggs. Dev. Biol. 158, 62-78.
27. Moos, J., Visconti, P. E., Moore, G. D., Schultz, R. M. and Kopf, G. S. (1995). Potential role of mitogen-activated protein kinase in pronuclear envelope assembly and disassembly following fertilization of mouse eggs. Biol. Reprod. 53, 692-699.
28. Moos, J., Xu, Z., Schultz, R. M. and Kopf, G. S. (1996) Regulation of nuclear envelope assembly/disassembly by MAP kinase. Dev. Biol 175, 358-361.
29. Packer, A. I., Hsu, Y. C., Besmer, P. and Bachvarova, R. F. (1994). The ligand of the c-kit receptor promotes oocyte growth. Dev. Biol. 161, 194-205.
30. Parrington, J., Swann, K., Shevchenko, V. I., Sesay, A. K. and Lai, F. A.(1996). Calcium oscillations in mammalian eggs triggered by a soluble sperm protein. Nature 379, 364-368.
31. Qiu, F., Ray, P., Barker, P. E., Jhanwar, S., Ruddle, F. H. and Besmer, P. (1988). Primary structure of c-kit: relationship with the CSF-1/PDGF receptor kinase family - oncogene activation of v-kit involves deletion of extracellular domain and C terminus. EMBO J. 7, 1003-1011.
32. Rossi, P., Marziali, G., Albanesi, C., Charlesworth, A., Geremia, R. and Sorrentino, V. (1992). A novel c-kit transcript, potentially encoding a truncated receptor, originates within a kit gene intron in mouse spermatids. Dev. Biol. 152, 203-207.
33. Rossi, P., Dolci, S., Albanesi, C., Grimaldi, P., Ricca, R. and Geremia, R. (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.
34. Sagata, N., Watanabe, N., Vande Woude, G. F. and Ikawa, Y. (1989). The c-mos proto-oncogene product is a cytostatic factor responsible for meiotic arrest in vertebrate eggs. Nature 342, 512-518.
35. 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.
36. Sorrentino, V., Giorgi, M., Geremia, R., Besmer, P. and Rossi P. (1991). Expression of the c-kit proto-oncogene in the murine male germ cells. Oncogene 6, 149-151.
37. Stice, S. L. and Robl, J. M. (1990). Activation of mammalian oocytes by a factor obtained from rabbit sperm. Mol. Reprod. Dev. 25, 272-280.
38. Swann, K. (1990). A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development 110, 1295-1302.
39. Tauchi, T., Feng, G. S., Marshall, M. S., Shen, R., Mantel, C., Pawson, T. and Broxmeyer, H. E. (1994). The ubiquitously expressed Syp phosphatase interacts with c-kit and Grb2 in hematopoietic cells. J. Biol. Chem. 269, 25206-25211.
40. Vande Woude, G. F. (1994) On the loss of Mos. Nature 370, 20-21.
41. Verlhac, M.-H., de Pennart, H., Maro, B., Cobb, M. H. and Clarke, H. J. (1993). MAP kinase becomes stably activated at metaphase and is associated with microtubule-organizing centers during meiotic maturation of mouse oocytes. Dev. Biol. 158, 330-340.
42. Verlhac, M.-H., Kubiak, J. Z., Clarke, H. J. and Maro, B. (1994) Microtubule and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development 120, 1017-1025.
43. Verlhac, M.-H., Kubiak, J. Z., Weber, M., Geraud, G., Colledge, W. H., Evans, M. J. and Maro, B. (1996). Mos is required for MAP kinase activation and is involved in microtubule organization during meiotic maturation in the mouse. Development 122, 815-822.
44. Whitaker, M. and Swann, K. (1993). Lighting the fuse at fertilization. Development 117, 1-12.
45. Yanagimachi, R. (1994). Mammalian fertilization. In The Physiology of Reproduction (ed. E. Knobil and J.D. Neill), pp. 189-317. Raven Press, Ltd, New York.
46. Yoshinaga, K., Nishikawa, S., Ogawa, M., Hayashi, S., Kunisada, T., Fujimoto, T. and Nishikawa, S.-I. (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.