A novel Rap1/B-Raf/14-3-3 θ protein complex is formed in vivo during the morphogenetic differentiation of postmeiotic male germ cells

Experimental Cell Research

Volumn 257, Issue 1, 2000, Pages 172-179

  Berruti, Giovanna ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

143 3 ; B Raf; Protein interaction; Rap1; Spermiogenesis

Indexed keywords

HYBRID PROTEIN; PROTEIN; RAF PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; ENZYME ACTIVITY; GERM CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MALE; MEIOSIS; MORPHOGENESIS; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION;

ANIMALIA; MAMMALIA;

EID: 0034713343     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.2000.4877     Document Type: Article

References (35)

1. Morrison D. K., Cutler R. E. Jr. The complexity of Raf-1 regulation. Curr. Opin. Cell Biol. 9:1997;174-179.
2. Daum G., Eisenmann-Tappe I., Fries H. W., Troppmair J., Rapp U. R. The ins and outs of Raf kinases. Trends Biochem. Sci. 19:1994;474-480.
3. Kitayama H., Sugimoto Y., Matsuzaki T., Ikawa Y., Noda M. A ras-related gene with transformation suppressor activity. Cell. 56:1989;77-84.
4. Barnier J. V., Papin C., Eychène A., Lecoq O., Calothy G. The mouse B-Raf gene encodes multiple protein isoforms with tissue-specific expression. J. Biol. Chem. 270:1995;23381-23389.
5. Vossler M. R., Yao H., York R. D., Pan M.-G., Rim C. S., Stork P. J. S. cAMP activates MAP kinase and Elk-1 through a B-Raf- and Rap1-dependent pathway. Cell. 89:1997;73-82.
6. York R. D., Yao H., Dillon T., Ellig C. L., Eckert S. P., McCleskey E. W., Stork P. J. S. Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature. 392:1998;622-626.
7. Asha H., de Ruiter N. D., Wang M.-G., Hariharan I. K. The Rap1 GTPase functions as a regulator of morphogenesis in vivo. EMBO J. 18:1999;605-615.
8. Hoog C. Expression of a large number of novel testis-specific genes during spermatogenesis coincides with the functional reorganization of the male germ cell. Int. J. Dev. Biol. 39:1995;719-726.
9. Loveland K. L., Schlatt S. Stem cell factor and c-kit in the mammalian testis: Lessons originating from mother nature's gene knockouts. J. Endocrinol. 153:1997;337-344.
10. Perego L., Berruti G. Molecular cloning and tissue-specific expression of the mouse homologue of the rat brain 14-3-3 θ protein: Characterization of its cellular and developmental pattern of expression in the male germ line. Mol. Reprod. Dev. 47:1997;370-379.
11. Aitken A. 14-3-3 and its possible role in coordinating multiple signalling pathways. Trends Cell Biol. 6:1996;341-347.
12. Fantl W. J., Muslin A. J., Kikuchi A., Martin J. A., MacNicol A. M., Gross R. W., Williams L. T. Activation of Raf-1 by 14-3-3 proteins. Nature. 371:1994;612-614.
13. Bonnefoy-Bérard N., Liu Y.-C., von Willebrand M., Sung A., Elly C., Mustelin T., Yoshida H., Ishizaka K., Altman A. Inhibition of phosphatidylinositol 3-kinase activity by association with 14-3-3 proteins in T cells. Proc. Natl. Acad. Sci. USA. 92:1995;10142-10146.
14. Fanger G. R., Widmann C., Porter A. C., Sather S., Johnson G. L., Vaillancourt R. R. 14-3-3 proteins interact with specific MEK kinases. J. Biol. Chem. 273:1998;3476-3483.
15. Tzivion G., Luo Z., Avruch J. A dimeric 14-3-3 protein is an essential cofactor for Raf kinase activity. Nature. 394:1998;88-92.
16. Bellvé A. R. Purification, culture, and fractionation of spermatogenic cells. Methods Enzymol. 225:1993;84-113.
17. Xiao B., Smerdon S. J., Jones D. H., Dodson G. G., Soneji Y., Aitken A., Gamblin S. J. Structure of a 14-3-3 protein and implications for coordination of multiple signalling pathways. Nature. 376:1995;188-191.
18. Wadewitz A. G., Winer M. A., Wolgemuth D. J. Developmental and cell lineage specificity of raf family gene expression in mouse testis. Oncogene. 8:1993;1055-1062.
19. Sithanandam G., Kolch W., Duh F.-M., Rapp U. R. Complete coding sequence of a human B-Raf cDNA and detection of B-Raf protein kinase with isozyme specific antibodies. Oncogene. 5:1990;1775-1780.
20. Eychène A., Barnier J. V., Dézélée P., Marx M., Laugier D., Calogeraki I., Calothy G. Quail neuroretina c-Rmil(B-Raf) proto-oncogene cDNAs encode two proteins of 93.5 and 95 kDa resulting from alternative splicing. Oncogene. 7:1992;1315-1323.
21. Bos J. L., Franke B., M'Rabet L., Reedquist K., Zwartkruis F. In search of a function for the Ras-like GTPase Rap1. FEBS Lett. 410:1997;59-62.
22. Oakberg E. F. A description of spermiogenesis in the mouse and its use in analysis of the cycle of the seminiferous epithelium and germ cell renewal. Am. J. Anat. 99:1952;391-413.
23. Béranger F., Goud B., Tavitian A., De Gunzburg J. Association of the Ras-antagonistic Rap1/Krev-1 proteins with the Golgi complex. Proc. Natl. Acad. Sci. USA. 88:1991;1606-1610.
24. Bartles J. R. The spermatid plasma membrane comes of age. Trends Cell Biol. 5:1995;400-404.
25. Reuter C. W. M., Catling A. D., Jelinek T., Weber M. J. Biochemical analysis of MEK activation in NIH3t3 fibroblasts: Identification of B-Raf and other activators. J. Biol. Chem. 270:1995;7644-7655.
26. Papin C., Denouel A., Calothy G., Eychène A. Identification of signalling proteins interacting with B-Raf in the yeast two-hybrid system. Oncogene. 12:1996;2213-2221.
27. Bos J. L. All in the family? New insights and questions regarding interconnectivity of Ras, Rap1 and Ra1. EMBO J. 17:1998;6776-6782.
28. Hecht N. B. The making of a spermatozoon: A molecular perspective. Dev. Gen. 16:1995;95-103.
29. Barinaga M. New clues to how proteins link up to run the cell. Science. 283:1999;1247-1249.
30. Berruti G. Signaling events during male germ cell differentiation: Bases and perspectives. Front. Biosci. 3:1998;d1097-1108.
31. Sassone-Corsi P. Transcriptional checkpoints determining the fate of male germ cells. Cell. 88:1997;163-166.
32. Kawasaki H., Springett G. M., Mochizuki N., toki S., Nakaya M., Matsuda M., Housman D. E., Graybiel A. M. A family of cAMP-binding proteins that directly activate Rap1. Science. 282:1998;2275-2279.
33. de Rooij J., Zwartkruis F. J. T., Verheijen M. H. G., Cool R. H., Nijman S. M. B., Wittinghofer A., Bos J. L. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature. 396:1998;474-477.
34. Marshall C. J. Taking the Rap. Nature. 392:1998;553-554.
35. de Rooij J., Grootegoed J. A. Spermatogonial stem cells. Curr. Opin. Cell Biol. 10:1998;694-701.