Nature and role of proteasomes in maturation of fish oocytes

International Review of Cytology

Volumn 186, Issue , 1998, Pages 261-294

  Tokumoto, Toshinobu ^a  

^a SHIZUOKA UNIVERSITY   (Japan)

Author keywords

Cyclin B degradation; Fertilization; Maturation promoting factor; Oocyte maturation; Proteasomes

Indexed keywords

CELL PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR; CYCLINE; PROTEASOME; UBIQUITIN;

ANIMAL CELL; BIOCHEMISTRY; CELL CYCLE; EUKARYOTIC CELL; FISH; MEIOSIS; NONHUMAN; OOCYTE MATURATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW;

ANIMALIA; EUKARYOTA;

EID: 0031755478     PISSN: 00747696     EISSN: None     Source Type: Book Series    
DOI: 10.1016/s0074-7696(08)61056-6     Document Type: Article

References (110)

1. Aristarkhov, A., Eytan, M. W., Moghe, A., Admon, A., Hershko, A., and Ruderman, J. V. (1996). E2-C, a cyclin-selective ubiquitin carrier protein required for the destruction of mitotic cyclins. Proc. Nail. Acad. Sci. USA 93, 4294-4299.
2. Armon, T., Gonoth, D., and Hershko, A. (1990). Assembly of the 26S complex that degrades proteins ligated to ubiquitin is accompanied by formation of ATPase activity. J. Biol. Chem. 265, 20726-20726.
3. Azuma, Y., Tokumoto, T., and Ishikawa, K. (1991). High molecular weight-multicatalytic proteinases in premature and mature oocytes of Rana pipiens. Mol.Cell. Biochem. 100, 171-181.
4. Castano, J. G., Mahillo, E., Arizti, P., and Arribas, J. (1996). Phosphorylation of C8 and C9 subunits of the multicatalytic proteinase by casein kinase II and identification of the C8 phosphorylation sites by direct mutagenesis. Biochemistry 35, 3782-3789.
5. Chiba, K., Sato, E., and Hoshi, M. (1997). Detection of in vivo proteasome activity in a starfish oocyte using membrane-impermeant substrate. J. Biochem. 122, 286-293.
6. Ciechanover, A., Finley, D., and Varshavsky, A. (1984). The ubiquitin-mediated proteolytic pathway and mechanisms of energy-dependent intracellular protein degradation. J. Cell. Biochem. 24, 27-53.
7. Coux, O., Tanaka, K., and Goldberg, A. L. (1996). Structure and functions of the 20S and 26S proteasomes. Annii. Rev. Biochem. 65, 801-847.
8. Dahlmann, B., Rutschmann, M., Kuehn, L., and Reinauer, H. (1985). Activation of the multicatalytic proteinase from rat skeletal muscle by fatty acids or sodium dodecyl sulfate. Biochem. J. 228, 171-177.
9. Dick, L. R., Moomaw, C. R., DeMartino, G. N., and Slaughter, C. A. (1991). Degradation of oxidized insulin B chain by the multiproteinase complex macropain (proteasome). Biochemistry 30, 2725-2734.
10. Djaballah, H., Harness, J. A., Savory, P. J., and Rivett, J. (1992). Use of serine-protease inhibitors as probes for the different proteolytic activities of the rat liver multicatalytic proteinase complex. Enr. J. Biochem. 209, 629-634.
11. Driscoll, J., and Goldberg, A. L. (1990). The proteasome (multicatalytic protease) is a component of the 1500-kDa proteolytic complex which degrades ubiquitin-conjugated proteins. J. Biol. Chem. 265, 4789-4792.
12. Driscoll, J., Fryman, J., and Goldberg, A. L. (1992). An ATP-stabilized inhibitor of the proteasome is a component of the 1500-kDa ubiquitin conjugated-degrading complex. Proc. N all. Acad. Sei. USA 89, 4986-4990.
13. Etlinger, J. D., and Goldberg, A. L. (1977). A soluble ATP-dependent proteolytic system responsible for the degradation of abnormal proteins in reticulocytes. Proc. Natl. Acad. Sei. USA 74, 54-58.
14. Figueiredo-Pereira, M. E., Berg, K. A., and Wilk, S. (1994). A new inhibitor of the chymotrypsin-like activity of the multicatalytic proteinase complex (20S proteasome) induces accumulation of ubiquitin-protein conjugates in a neuronal cell. J. Neurochem. 63, 1578-1581.
15. Funabiki, H., Kumada, K., and Yanagida, M. (1996a). Fission yeast Cutl and Cut2 are essential for sister chromatid separation, concentrate along the metaphase spindle and form large complexes. EMBO J. 15, 6617-6628.
16. Funabiki, H., Yamano, H., Kumada, K., Nagao, K., Hunt, T., and Yanagida, M. (1996b). Cut2 proteolysis required for sister-chromatid separation in fission yeast. Nature (London) 381, 438-441.
17. Gautier, J., Pal, J. K., Grossi, de S. A., Beetshen, J. C, and Scherrer, K. (1988). Differential cytolocalization of prosomes in axolotol during oogenesis and meiotic maturation. J. Cell Sei. 90, 543-553.
18. Gavilanes, J. G., Gonzalez, B. G., Perez-Castells, R., and Rodringuez, R. (1982). Isolation, characterization, and amino acid sequence of a ubiquitin-like protein from insect eggs. J. Biol. Chem. 257, 10267-10270.
19. Ghislain, M., Udvardy, A., and Mann, C. (1993). 5. cerevisiae 26S protease mutants arrest cell division in G2/metaphase. Nature (London) 366, 358-362.
20. Glotzer, M., Murray, A. W., and Kirshner, M. W. (1991). Cyclin is degraded by the ubiquitin pathway. Nature (London) 349, 132-138.
21. Goldstein, G. (1975). Molecular conservation of 74 amino acid sequence of ubiquitin between cattle and man. Nature (London) 255, 423-424.
22. Gordon, C, McGurk, G., Dillon, P., Rosen, G, and Hastie, N. D. (1993). Defective mitosis due to a mutation in the gene for a fission yeast 26S protease subunit. Nature (London) 366, 355-357.
23. Guerrier, P., Moreau, M., and Doree, M. (1977). Inhibition de la reinitiation de la meiose des ovocytes de Xenopus laevis partrois antiproteases naturelleas, l'antipain, la chymostatine et la leupeptine. C R Acad. Sei. Paris 284, 317-319.
24. Haas, A., Reback, P. M., Pratt, G., and Rechsteiner, M. (1990). Ubiquitin-mediated degradation of histone H3 does not require the substrate-binding ubiquitin protein ligase, E3, or attachment of polyubiquitin chains. J. Biol. Chem. 265, 21664-21669.
25. Haas, A. L., and Wilkinson K. D. (1985). The large scale purification of ubiquitin from human erythrocytes. Prep. Biochem. 15, 49-60.
26. Haas, G, and Kloetzel, P. M. (1989). The Drosophila proteasome undergoes changes in its subunit pattern during development. Exp. Cell Res. 180, 243-252.
27. Habibi, H., and Lessman, G A. (1986). Effect of demecolcine (Colcemid) on goldfish oocyte meiosis in vitro. Gamete Res. 13, 103-114.
28. Hershko, A., Ciechanover, A., Heller, H., Haas, A. L., and Rose, I. A. (1980). Proposed role of ATP in protein breakdown: Conjugation of proteins with multiple chains of the polypeptide of ATP-dependent proteolysis. Proc. Nail Acad. Sei. USA 77, 1783-1786.
29. Hershko, A., and Ciechanover, A. (1982). Mechanisms of intracellular protein breakdown. Annu. Rev. Biochem. 51, 335-364.
30. Hershko, A., Ganoth, D., Pehrson, J., Palazzo, R. E., and Cohen, L. H. (1991). Methylated ubiquitin inhibits cyclin degradation in clam embryo extracts. J. Biol. Chem. 266, 16376-16379.
31. Hershko, A., Leshinsky, E., Ganoth, D., and Heller, H. (1984). ATP-dependent degradation of ubiquitin-protein conjugates. Proc. Natl. Acad. Sei. USA 81, 1619-1623.
32. Hirai, T., Yamashita, M., Yoshikuni, M., Lou, Y. H., and Nagahama, Y. (1992). Cyclin B in fish oocytes: Its cDNA and amino acid sequences, appearance during maturation, and induction of p34cdc2 activation. Mol. Reprod. Dev. 33, 131-140.
33. Huffman, L., Pratt, G., and Rechsteiner, M. (1992). Multiple forms of the 20S multicatalytic and the 26S ubiquitin/ATP-dependent proteases from rabbit reticulocyte lysate. J. Biol. Chem. 267, 22362-22368.
34. Hough, R., Pratt, G., and Rechsteiner, M. (1987). Purification of two high molecular weight proteases from rabbit reticulocyte lysate. J. Biol. Chem. 262, 8303-8313.
35. Ishikawa, K., Schuetz, A. W., and San Fransisco, S. K. (1989). Induction and inhibition of amphibian (Rana pipiens) oocyte maturation by protease inhibitor (TPCK). Gamete Res. 22, 339-354.
36. Jensen, T. J., Loo, M. A., Find, S., Williams, D. B., Goldberg, A. L., and Riordan, J. R. (1995). Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell 83, 129-135.
37. Kagawa, H., Young, G., Adachi, S., and Nagahama, Y. (1985). Estrogen synthesis in the teleost ovarian follicle: The two-cell type model in salmonids. In Salmonid Reproduction (R. N. Iwamoto and S. Sower, Eds.), pp 20-25. Washington Sea Grant Program, University of Washington, Seattle.
38. Kajiura, H., Yamashita, M., Katsu, Y., and Nagahama, Y. (1993). Isolation and characterization of goldfish cdc2, a catalytic component of maturation-promoting factor. Dev. Growth Differ. 35, 647-654.
39. Kanayama, H., Tamura, T., Ugai, S., Kagawa, S., Takahashi, N., Yoshiura, T., Tanaka, K., and Ichihara, A. (1992). Demonstration that a human 26S proteolytic complex consists of a proteasome and multiple associated protein components and hedrolyzes ATP and ubiquitinligated proteins by closely linked machanisms. Eur. J. Biochem. 2056, 567-578.
40. Katsu, Y., Yamashita, M., Kajiura, H., and Nagahama, Y. (1993). Behavior of the components of maturation-promoting factor, cdc2 kinase and cyclin B, during oocyte maturation of goldfish. Dev. Biol. 160, 99-107.
41. Katsu, Y., Yamashita, M., and Nagahama, Y. (1997). Isolation and characterization of goldfish Y box protein, a germ-cell-specific RNA-binding protein. Eur. J. Biochem. 249, 854-861.
42. Kawahara, H., and Yokosawa, H. (1992). Cell cycle-dependent changes of proteasome distribu-tion during embryonic development of the ascidian Halocynthia roretzi. Dev. Biol. 151, 27-33.
43. King, R. W., Glotzer, M., and Kirshner, M. W. (1996). Mutagenic analysis of the destruction signal of mitotic cyclins and structural characterization of ubiquitinated intermediates. Mol. Bio!. Cell 7, 1343-1357.
44. King, R. W., Peter, J., Tugendreich, S., Rolfe, M., Hinter, P., and Kirshner, M. W. (1995). A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cycliln B. Cell 81, 279-288.
45. Kishimoto.T. (1988). Regulation of metaphase by a maturation-promoting factor. Dev. Growth Diff. 30, 105-115.
46. Kishimoto, T., Clark, T. G., Kondo, H. K., Shirai, H., and Kanatani, H. (1982). Inhibition of a starfish oocyte maturation by some inhibitors of proteolytic enzymes. Gamete Res. 5,11-18.
47. Klotzbücher, A., Stewart, E., Harrison, D., and Hunt, T. (1996). The 'destruction box' of cyclin A allows B-type cyclins to be ubiquitinated, but not efficiently destroyed. EMBO J. 15, 3053-3064.
48. cdk2 protein kinase subunits. Mol. Biol. Cell. 3, 1279-1294.
49. Kobayashi, M., Kato, Y., Yoshiura, Y., and Aida K. (1997). Molecular cloning of cDNAs encoding two types of pituitary gonadotropin a subunit from the goldfish, Carassius auratiis. Gen. Comp. Endocrinol. 105, 372-378.
50. Lessman, C. L., and Kavumpurath, S. (1984). Cytological analysis of nuclear migration and dissolution during steroid-induced meiotic maturation in vitro of follicle-enclosed oocytes of the goldfish (Carassius auratiis). Gamete Res. 10, 21-29.
51. Lorca, T., Cruzalegui, F. H., Fesquet, D., Cavadore, J., Méry, J., Means, A., and Dorée, M. (1993). Calmodulin-dependent protein kinase II mediates inactivation of MPF and CSF upon fertilization of Xenopus eggs. Nature (London) 366, 270-273.
52. Lorca, T., Fesquet, D., Zindy, F., Bouffant, F., Cerrui, M., Brechot, C, Devauchelle, G., and Dorée, M. (1991). An okadaic acid-sensitive phosphatase negatively controls the cyclin degradation pathway in amphibian eggs. Mol. Cell. Biol. 11, 1171-1175.
53. Luca, F. C, Shibuya, E. K., Dahlmann, C. E., and Ruderman, J. V. (1991). Both cyclin A A60 and B A97 are stable and arrest cells in M-phase, but only cyclin B A97 turns on cyclin destruction. EMBO J. 10, 4311-4320.
54. Ludemann, R., Lerea, K. M., and Etlinger, J. D. (1993). Copurification of casein kinase II with 20S proteasomes and phosphorylation of a 30-kDa proteasome subunit. J. Biol. Cliem. 268,17413-17417.
55. Mailer, J. L. (1991). Mitotic control. GOT. Opin. Cell Biol. 3, 269-275.
56. Matthews, W., Tanaka, K., Driscoll, J., Ichihara, A., and Goldberg, A. L. (1989). Involvement of the proteasome in various degradative processes in mammalian cells. Proc. Nail. Acad. Sei. USA 86, 2597-2601.
57. Murakami, Y., Matsufuji, S., Kameji, T., Hayashi, S., Igarashi, K., Tamura, T., Tanaka, K., and Ichihara, A. (1992). Ornithine decarboxylase is degraded by the 26S proteasome without ubiquitination. Nature (London) 360, 597-599.
58. Murray, A.W. (1995). Cyclin ubiquitination: The destructive end of mitosis. Cell 81,149-152.
59. Murray, A. W., Solomon, M. J., and Kirshner, M. W. (1989). The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature (London) 339, 280-286.
60. Mykles, D. (1989). Purification and characterization of a multicatalytic proteinase from crustacean muscle: Comparison of latent and heat-activated forms. Arch. Biochem. Biophys. 274, 216-228.
61. Nagahama, Y. (1987a). Endocrine control of oocyte maturation. In "Hormones and Reproduction in Fishes, Amphibians, and Reptiles" (D. O. Norris and R. E. Jones, Eds.), pp. 171-202. Plenum Press, New York.
62. Nagahama, Y. (1987b). Gonadotropin action on gametogenesis and steroidogenesis in teleost gonads. Zool Sei. 4, 209-222.
63. Nagahama, Y., and Adachi, S. (1985). Identification of maturation-inducing steroid in a teleost, the amago salmon (Oncorhynclms rhodurus). Dev. Biol. 109, 428-435.
64. Nagahama, Y., Yoshikuni, M., Yamashita, M., Tokumoto, T., and Katsu, Y. (1995). Regulation of oocyte growth and maturation in fish. In "Current Topics in Developmental Biology" (R. A. Pederson and G. P. Schatten, Eds.), Vol. 30, pp. 103-145. Academic Press, San Diego.
65. Oba, Y., Yoshikuni, M., Tanaka, M., Mita, M., and Nagahama, Y. (1997). Inhibitory guaninenucleotide-binding-regulatory protein a subunits in medaka (Oryzias lalipes) oocytes. Eur. J. Biochem. 249, 846-853.
66. cdc2-cyclin B complex at meiosis reinitiation in starfish oocytes. EMBO J. 11, 1763-1772.
67. Orlowsky, M. (1990). The multicatalytic proteinase complex, a major extralysosomal proteolytic system. Biochemistry 29, 10289-10297.
68. Ozaki, M., Fujinami, K., Tanaka, K., Amemiya, Y., Sato, T., Ogura, N., and Nakagawa, H. (1992). Purification and initial characterization of the proteasome from the higher plant Spinacia oleracea. J. Biol. Chem. 267, 21678-21684.
69. Ozkaynak, E., Finley, D., and Varshavsky, A. (1984). The yeast ubiquitin gene: Head-to-tail repeats encoding a poly-ubiquitin precursor protein. Nature (London) 312, 663-666.
70. Pereria, M. E., and Wilk, S. (1990). Phosphorylation of the multicatalytic proteinase complex from bovine pituitaries by a copurifying cAMP-dependent protein kinase. Arch. Biochem. Biophys. 283, 68-74.
71. Peters, J.-M., King, R. W., Höög, C, and Kirschner, M.W. (1996). Identification of DIME as a subunit of the anaphase-promoting complex. Science 274,1199-1201.
72. Pines, J., and Hunter, T. (1991). Human cyclins A and Bl are differentially located in the cell and undergo cell cycle-dependent nuclear transport. J. Cell Biol. 115, 1-17.
73. Reits, E. A. J., Benham, A. M., Plougastel, B., Neefjes, J., and Trowsdale, J. (1997). Dynamics of proteasome distribution in living cells. EMBO J. 16, 6087-6094.
74. Rivett, A. J. (1985). Purification of a liver alkaline protease which degrades oxidatively modified glutamine synthetase. J. Biol. Chem. 260, 12600-12606.
75. Rock, K. L., Gramm, C, Rothstein, L., Clark, K., Stein, R., Dick, L., Hwang, D., and Goldberg, A. L. (1994). Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78, 761-771.
76. SIC1 controls the Gl to S transition in S. cerevisiae. Cell 79, 233-244.
77. Seufert, W., Futcher, B., and Jentsch, S. (1995). Role of a ubiquitin-conjugating enzyme in degradation of S- and M-phase cyclins. Nature (London) 373, 78-81.
78. cdc2. EMBO J. 13, 584-594.
79. Sudakin, V., Ganoth, D., Dahan, A., Heller, H., Hershko, J., Luca, F. C, Ruderman, J. V., and Hershko, A. (1995). The cyclosome, a large complex containing cyclin-selective ubiquitin ligase activity, targets cyclins for destruction at the end of mitosis. Mol. Biol. Cell 6,185-198.
80. Takagi-Sawada, M., Kyozuka, K., Morinaga, C, Izumi, K., and Sawada, H. (1997). The proteasome is an essential mediator of the activation of pre-MPF during starfish oocyte maturation. Biochem. Biophys. Res. Commun. 236, 40-43.
81. Takagi-Sawada, M., Someno, T., Hoshi, M., and Sawada, H. (1989). Inhibition of starfish oocyte maturation by leupeptin analogs, potent trypsin inhibitors. Dev. Biol. 133, 609-612.
82. Takagi-Sawada, M., Someno, T., Hoshi, M., and Sawada, H. (1992). Participation of 650-kDa protease (20S proteasome) in starfish oocyte maturation. Dev. Biol. 150, 414-418.
83. Takahashi, M., Tokumoto, T., and Ishikawa, K. (1994). DFP-sensitive multicatalytic protease complexes (proteasomes) in the control of oocyte maturation in the toad, Bufo japonicus. Mol. Reprod. Dev. 38, 310-317.
84. Takahashi, T., Tokumoto, T., Ishikawa, K., and Takahashi, K. (1993). Cleavage specificity and inhibition profile of proteasome isolated from the cytosol oiXenopiis oocyte. J. Biochem. 113, 225-228.
85. Tamura, T., Tanaka, K., Tanahashi, N., and Ichihara, A. (1991). Improved method for preparation of ubiquitin-ligated lysozyme as substrate of ATP-dependent proteolysis. FEBS Lett. 292, 154-158.
86. Tanaka, K., li, K., Ichihara, A., Waxman, L., and Goldberg, A. L. (19S6). A high molecular weight protease in the cytosol of rat liver. J. Biol. Chem. 261, 15197-15203.
87. Tanaka, K., Tamura, T., Kumatori, A., Kwak, T. H., Chung, C. H., and Ichihara, A. (1989). Separation of yeast proteasome subunits; immunoreactivity with antibodies against ATP-dependent protease Ti from Escliericlria coli. Biochem. Biophys. Res. Commun. 164,1253- 1261.
88. Tanaka, K., Tamura, T., Yoshimura, T., and Ichihara, A. (1992). Direct evidence for nuclear and cytoplasmic colocalization of proteasomes (multiprotease complexes) in liver. J. Cell Physiol. 139, 34-41.
89. Tanaka, K., Waxman, L., and Goldberg, A. L. (1983). ATP serves two distinct roles in protein degradation in reticulocytes, one requiring and one independent of ubiquitin. J. Cell Biol. 96,1580-1585.
90. Tanaka, K., Yoshimura, T., Kumatori, A., Ichihara, A., Ikai, A., Nishigai, M., Kameyama, K., and Takagi, T. (1988). Proteasomes (multi-protease complexes) as 20S ring-shaped particles in a variety of eukaryotic cells. J. Biol. Chem. 263, 16209-16217.
91. Tokumoto, M., Horiguchi, R., Yamashita, M., Nagahama, Y., and Tokumoto, T. (1997a). Involvement of 26S proteasome in oocyte maturation of goldfish Carassiiis auratus. ZooJ. Sei. 14, 347-351.
92. Tokumoto, T., and Ishikawa, K. (1993). A novel "active" form of proteasomes from Xenopus laevis ovary cytosol. Biochem. Biophys. Res. Commun. 192, 1106-1114.
93. Tokumoto, T., and Ishikawa, K. (1995). Characterization of active proteasome (26S proteasome) from Xenopus oocytes. Biomed. Res. 16, 295-302.
94. Tokumoto, T., Kajiura, H., Yoshikuni, M., Yamashita, M., and Nagahama, Y. (1993a). Purification of ubiquitin from goldfish oocytes. Biomed. Res. 14, 309-311.
95. Tokumoto, T., Yamashita, M., Tokumoto, M., Katsu, Y., Horiguchi, R., Kajiura, H., and Nagahama, Y. (1997b). Initiation of cyclin B degradation by the 26S proteasome upon egg activation. J. Cell Biol. 138,1313-1322.
96. Tokumoto, T., Yamashita, M., Yoshikuni, M., Kajiura, H., and Nagahama, Y. (1995a). Purification of latent proteasome (20S proteasome) and demonstration of active proteasome in goldfish (Carassiiis auratus) oocyte cytosol. Biomed. Res. 16, 173-186.
97. Tokumoto, T., Yamashita, M, Yoshikuni, M., and Nagahama, Y. (1993b). Changes in the activity and protein levels of proteasomes during oocyte maturation in goldfish (Carassius mirants). Biomed. Res. 14, 305-308.
98. Tokumoto, T., Yoshikuni, M., Yamashita, M., Kajiura, H., and Nagahama, Y. (1995b). Purification and characterization of active proteasome (26S proteasome) from goldfish ovaries. Biomed. Res. 16, 207-218.
99. Tsukahara, T., Ishiura, S., and Sugita, H. (19S8). An ATP-dependent protease and ingensine, the multicatalytic proteinase, in K562 cells. Eur. J. Biocliem. 177, 261-265.
100. Velden, H. M. W., and Lohka, M. J. (1993). Mitotic arrest caused by the amino terminus of Xenopits cyclin B. Mol. Cell Biol. 13, 1480-1488.
101. Watson, D. C., Levy, W. B., and Dixon, G. H. (1978). Free ubiquitin is a nonhistone protein of trout testis chromatin. Nature (London) 276,196-198.
102. Wilk, S., and Orlowski, M. (1980). Cation-sensitive neural endopeptidases: Isolation and specificity of the bovine pituitary enzyme. J. Neurochem. 35, 1172-1182.
103. Wöjcik, C, Scheroeter, D., Stoehr, M., Wilk, S., and Paweletz, N. (1996). An inhibitor of the chymotrypsin-like activity of the multicatalytic proteinase complex (20S proteasome) induces arrest in G2-phase and metaphase in HeLa cells. Eur. J. Cell Biol. 70, 172-178.
104. Yamashita, M., Fukada, S., Yoshikuni, M., Bulet, P., Hirai, T., Yamaguchi, A., Lou, Y. H., Zhao, Z., Nagahama, Y. (1992a). Purification and characterization of maturation-promoting factor in fish. Dev. Biol. 148, 8-15.
105. Yamashita, M., Fukada, S., Yoshikuni, M., Bulet, P., Hirai, T., Yamaguchi, A., Yasuda, H., Ohba, Y., and Nagahama, Y. (1992b). M-phase-specific histone HI kinase in fish oocytes: Its purification, components and biochemical properties. Eur. J. Biochem. 205, 537-543.
106. Yamashita, M., Kajiura, H., Tanaka, M., Onoe, S., and Nagahama, Y. (1995). Molecular mechanisms of the activation of maturation-promoting factor during goldfish oocyte maturation. Dev. Biol. 168, 62-75.
107. Yoshikuni, M., and Nagahama, Y. (1994). Involvement of an inhibitory G-protein in the signal transduction pathway of maturation-inducing hormone (17α,20β-dihydroxy-4-prognen-3-one) action in rainbow trout (Oncorhynchus mykiss) oocytes. Dev. Biol. 166, 615-622.
108. 3H] 17α,20β-dihydroxy-4-prognen-3-one to oocyte cortices of rainbow trout (Oncorhynchus mykiss). Fish Physiol. Biochem. 11, 15-24.
109. Yoshiura, Y., Kobayashi, M., Kalo, Y., and Aida, K. (1997). Molecular cloning of the cDNAs encoding two gonadotropin β subunits (GTH-Iβ and -IIβ) from the goldfish, Carassius auratus. Gen. Comp. Endocriiwl. 105, 379-389.
110. Zachariae, W., Shin, T. H., Galova, M., Obermaier, B., and Nasmyth, K. (1996). Identification of subunits of the anaphase-promoting complex of Saccharomyces cerevisiae. Science 274, 1201-1204.