Activation of a UBC4-dependent pathway of ubiquitin conjugation during postnatal development of the rat testis

Developmental Biology

Volumn 212, Issue 1, 1999, Pages 217-228

  Rajapurohitam, Venkatesh ^a   Morales, Carlos R ^a   El Alfy, Mohamed ^a   Lefrançois, Stephane ^a   Bedard, Nathalie ^a   Wing, Simon S ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Spermatogenesis; Spermiogenesis; Testis; Ubiquitin; Ubiquitin conjugating enzymes

Indexed keywords

MESSENGER RNA; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME;

ADOLESCENT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONJUGATION; CONTROLLED STUDY; ENZYME ACTIVATION; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; MALE; MEIOSIS; MITOSIS; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; RAT; SPERMATID; SPERMATOGENESIS; SPERMATOZOON; TESTIS DEVELOPMENT;

EID: 0033178830     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1999.9342     Document Type: Article

References (54)

1. Agell N., Mezquita C. Cellular content of ubiquitin and formation of ubiquitin conjugates during chicken spermatogenesis. Biochem. J. 250:1988;883-889.
2. Argiles J. M., Lopezsoriano F. J. The ubiquitin-dependent proteolytic pathway in skeletal muscle - Its role in pathological states. Trends Pharm. Sci. 17:1996;223-226.
3. Ausabel, F. M, Brent, R, Kingston, D. D, Moore, D. D, Seidman, J. G, Smith, J. A, and, Struhl, K. 1993, Current protocols in molecular biology, Wiley, New York.
4. Bellvé A. The molecular biology of mammalian spermatogenesis. Finn C. A. Oxford Reviews of Reproductive Biology. 1979;159-164 Oxford Univ. Press, Oxford.
5. Bond U., Schlesinger M. J. The chicken ubiquitin gene contains a heat shock promoter and expresses an unstable mRNA in heat-shocked cells. Mol. Cell. Biol. 6:1986;4602-4610.
6. Ciechanover A., Heller H., Elias S., Haas A. L., Hershko A. ATP-dependent conjugation of reticulocyte proteins with the polypeptide required for protein degradation. Proc. Natl. Acad. Sci. USA. 87:1980;1365-1368.
7. Clermont Y., Oko R., Hermo L. Cell biology of mammalian spermiogenesis. Desjardins C. Cell and Molecular Biology of the Testis. 1993;Oxford Univ. Press, New York.
8. Clermont Y., Rambourg A. Evolution of the endoplasmic reticulum during rat spermiogenesis. Am. J. Anat. 151:1978;191-212.
9. Finley D., Ozkaynak E., Varshavsky A. The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses. Cell. 48:1987;1035-1046.
10. Fort P., Marty L., Piechaczyk M., El Sabrouty S., Dani C., Jeanteur P., Blanchard J. M. Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family. Nucleic Acids Res. 13:1985;1431-1442.
11. Fujimoro M., Sawada H., Yokosawa H. Production and characterization of monoclonal antibodies specific to multi-ubiquitin chains of polyubiquitinated proteins. FEBS Lett. 349:1994;173-180.
12. Haas A. L., Baboshina O., Williams B., Schwartz L. M. Coordinated induction of the ubiquitin conjugation pathway accompanies the developmentally programmed death of insect skeletal muscle. J. Biol. Chem. 270:1995;9407-9412.
13. Haas A. L., Bright P. M. The resolution and characterization of putative ubiquitin carrier protein isozymes from rabbit reticulocytes. J. Biol. Chem. 263:1988;13258-13267.
14. Haas A. L., Bright P. M., Jackson V. E. Functional diversity among putative E2 isozymes in the mechanism of ubiquitin-histone ligation. J. Biol. Chem. 263:1988;13268-13275.
15. Haas A. L., Warms J. V. B., Hershko A., Rose I. A. Ubiquitin-activating enzyme: Mechanism and role in protein-ubiquitin conjugation. J. Biol. Chem. 257:1982;2543-2548.
16. Hershko A., Heller H., Elias S., Ciechanover A. Components of ubiquitin-protein ligase system. J. Biol. Chem. 258:1983;8206-8214.
17. Hershko A., Leshinsky E., Ganoth D., Heller H. ATP-dependent degradation of ubiquitin-protein conjugates. Proc. Natl. Acad. Sci. USA. 81:1984;1619-1623.
18. Hochstrasser M. Ubiquitin-dependent protein degradation. Annu. Rev. Genet. 30:1996;405-439.
19. Jensen J. P., Bates P. W., Yang M., Vierstra R. D., Weissman A. M. Identification of a family of closely related human ubiquitin conjugating enzymes. J. Biol. Chem. 270:1995;30408-30414.
20. Jentsch S., McGrath J. P., Varshavsky A. The yeast DNA repair gene RAD6 encodes a ubiquitin-conjugating enzyme. Nature. 329:1987;131-134.
21. Kay G. F., Ashworth A., Penny G. D., Dunlop M., Swift S., Brockdorff N., Rastan S. A candidate spermatogenesis gene on the mouse Y chromosome is homologous to ubiquitin-activating enzyme E1. Nature. 354:1991;486-489.
22. King R. W., Deshaies R. J., Peters J.-M., Kirschner M. W. How proteolysis drives the cell cycle. Science. 274:1996;1652-1659.
23. Koken M. H. M., Hoogerbrugge J. W., Jaspers-Dekker I., de Wit J., Willemsen R., Roest H. P., Grootegoed J. A., Hoeijmakers J. H. J. Expression of the ubiquitin-conjugating DNA repair enzymes HHR6A and B suggests a role in spermatogenesis and chromatin modification. Dev. Biol. 173:1996;119-132.
24. Lahav-Baratz S., Sudakin V., Ruderman J. V., Hershko A. Reversible phosphorylation controls the activity of cyclosome-associated cyclin-ubiquitin ligase. Proc. Natl. Acad. Sci. USA. 92:1995;9303-9307.
25. 2+-activated, and ATP-ubiquitin-dependent proteolytic pathways in skeletal muscle from head trauma patients. Proc. Natl. Acad. Sci. USA. 93:1996;2714-2718.
26. Mitch W. E., Goldberg A. L. Mechanisms of muscle wasting: The role of the ubiquitin-proteasome pathway. N. Engl. J. Med. 335:1996;1897-1905.
27. Mitchell M. J., Woods D. R., Tucker P. K., Opp J. S., Bishop C. E. Homology of a candidate spermatogenic gene from the mouse Y chromosome to the ubiquitin-activating enzyme E1. Nature. 354:1991;483-489.
28. Morales C., Clermont Y., Hermo L. Nature and function of endocytosis in Sertoli cells of the rat. Am. J. Anat. 173:1985;203-217.
29. Morales C. R., Kwon Y. K., Hecht N. B. Cytoplasmic localization during storage and translation of the mRNAs of transition protein 1 and protamine 1, two translationally regulated transcript of the mammalian testis. J. Cell Sci. 100:1991;119-131.
30. Moussa F., Oko R., Hermo L. The immunolocalization of small nuclear ribonucleoprotein particles in testicular cells during the cycle of the seminiferous epithelium of the adult rat. Cell Tissue Res. 278:1994;363-378.
31. Muller D., Rehbein M., Baumeister H., Richter D. Molecular characterization of a novel rat protein structurally related to poly(A) binding proteins and the 70K protein of the U1 small nuclear ribonucleoprotein particle (snRNP). Nucleic Acids Res. 20:1992;1471-1475.
32. Newsholme E. A., Start C. Regulation in Metabolism. 1973;Wiley, London.
33. Oko R. Comparative analysis of proteins from the fibrous sheath and outer dense fiber protein of rat spermatozoa. Biol. Reprod. 39:1998;169-172.
34. Oko R., Clermont Y. Biogenesis of specialized cytoskeletal elements of rat spermatozoa. Ann. N. Y. Acad. Sci. 637:1991;203-223.
35. Oughtred R., Bédard N., Vrielink A., Wing S. S. Identification of amino acid residues in a class I ubiquitin conjugating enzyme involved in determining specificity of conjugation of ubiquitin to proteins. J. Biol. Chem. 273:1998;18435-18442.
36. Palombella V. J., Rando O. J., Goldberg A. L., Maniatis T. The ubiquitin-proteasome pathway is required for processing the NF-κB1 precursor protein and the activation of NF-κB. Cell. 78:1994;773-785.
37. Petrie R. G., Morales C. R. Receptor-mediated endocytosis of testicular transferrin by germinal cells of the rat testis. Cell Tissue Res. 267:1992;45-55.
38. Pickart C. M., Rose I. A. Functional heterogeneity of ubiquitin carrier proteins. J. Biol. Chem. 260:1985;1573-1581.
39. Pickart C. M., Vella A. T. Levels of active ubiquitin carrier proteins decline during erythroid maturation. J. Biol. Chem. 263:1988;12028-12035.
40. Reiss Y., Heller H., Hershko A. Binding sites of ubiquitin-protein ligase. Binding of ubiquitin-protein conjugates and of ubiquitin-carrier protein. J. Biol. Chem. 264:1989;10378-10383.
41. Roest H. P., van Klaveren J., de Wit J., van Gurp C. G., Koken M. H. M., Vermey M., van Roijen J. H., Hoogerbrugge J. W., Vreeburg J. T. M., Baarends W. M., Bootsma D., Grootegoed J. A., Hoeijmakers J. H. J. Inactivation of the HR6B ubiquitin-conjugating DNA repair enzyme in mice causes male sterility associated with chromatin modification. Cell. 86:1996;799-810.
42. Russell L. D. Spermatid-Sertoli cell tubulobulbar complexes as devices for the elimination of cytoplasm from the head region of late spermatids fo the rat. Anat. Rec. 194:1979;233-246.
43. Scheffner M., Nuber U., Huibregtse J. M. Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thiolester cascade. Nature. 373:1995;81-83.
44. Schlesinger M. J., Bond U. Ubiquitin genes. Oxford Surv. Eukaryot. Genes. 4:1987;77-91.
45. Seufert W., Jentsch S. Ubiquitin-conjugating enzymes UBC4 and UBC5 mediate selective degradation of short-lived and abnormal proteins. EMBO J. 9:1990;543-550.
46. 2+-activated and ATP-ubiquitin-dependent proteinases in the unweighted rat soleus muscle. Biochem. J. 316:1996;65-72.
47. Temparis S., Asensi M., Taillandier D., Aurousseau E., Larbaud D., Obled A., Bechet D., Ferrara M., Estrela J. M., Attaix D. Increased ATP-ubiquitin-dependent proteolysis in skeletal muscles of tumor-bearing rats. Cancer Res. 54:1994;5568-5573.
48. Tipler C. P., Hutchon S. P., Hendil K., Tanaka K., Fishel S., Mayer R. J. Purification and characterization of 26S proteasomes from human and mouse spermatozoa. Mol. Hum. Reprod. 3:1997;1053-1060.
49. Ward W. S., Coffey D. S. DNA packaging and organization in mammalian spermatozoa: Comparison with somatic cells. Biol. Reprod. 44:1991;569-574.
50. Wefes I., Mastrandrea L. D., Haldeman M., Koury S. T., Tamburlin J., Pickart C. M., Finley D. Induction of ubiquitin-conjugating enzymes during terminal erythroid differentiation. Proc. Natl. Acad. Sci. USA. 92:1995;4982-4986.
51. Wing S., Jain P. Molecular cloning, expression, and characterization of a ubiquitin conjugation enzyme (E2 17KB) highly expressed in rat testis. Biochem. J. 305:1995;125-132.
52. Wing S. S., Banville D. 14-kDa ubiquitin-conjugating enzyme: Structure of the rat gene and regulation upon fasting and by insulin. Am. J. Physiol. 267:1994;E39-E48.
53. Wing S. S., Bedard N., Morales C., Hingamp P., Trasler J. A novel rat homologue of the S. cerevisiae ubiquitin conjugating enzyme UBC4 with distinct biochemical features is induced during spermatogenesis. Mol. Cell. Biol. 16:1996;4064-4072.
54. Wing S. S., Goldberg A. L. Glucocorticoids activate the ATP-ubiquitin-dependent proteolytic system in skeletal muscle during fasting. Am. J. Physiol. 264:1993;E668-E676.