Cdna sequence analysis of proteins involved in reproduction and cell cycle of the zebra mussel, dreissena polymorpha

Invertebrate Reproduction and Development

Volumn 41, Issue 1-3, 2002, Pages 41-52

  Lamers, Anne E ^a   Heiney, Jake P ^a   Ram, Jeffrey L ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Actin; Cell cycle proteins; Cyclins; Dna sequences; Dreissena polymorpha; Protein phosphatase; Reproduction

Indexed keywords

ACTIN; AMINO ACID; CYCLIN A; CYCLIN B; LYSINE; MESSENGER RNA; PHOSPHOPROTEIN PHOSPHATASE; TUBULIN;

AMINO ACID SEQUENCE; BIVALVE; CELL CYCLE; CELL MATURATION; DNA LIBRARY; DNA SEQUENCE; GENETIC REGULATION; MEIOSIS; MITOSIS; POLYMERASE CHAIN REACTION; RNA STRUCTURE; SEQUENCE HOMOLOGY;

DREISSENA POLYMORPHA;

EID: 0036710765     PISSN: 07924259     EISSN: None     Source Type: Journal    
DOI: 10.1080/07924259.2002.9652734     Document Type: Article

References (87)

1. Aboussekhra, A., Chanet, R., Adjiri, A., and Fabre, F., 1992. Semidominant suppressors of Srs2 helicase mutations of Saccharomyces cerevisiae map in the RAD51 gene. whose sequence predicts a protein with similiarities to procaryotic RecA proteins. Mol. Cell. Biol., 122:3224–3234.
2. Basile, G., Aker, M., and Mortimer, R. K., 1992. Nucleotide sequence and transcriptional regulation of the yeast recombinational repair gene RAD51. Mol. Cell. Biol., 12:3235–3246.
3. Bates, S., Bonetta, L., MacAllan, D., Parry, D., Holder, A., Dickson, C., and Peters, G., 1994. CDK6 (PLSTIRE) and CDK4 (PSK-J3) are a distinct subset of the cyclin-dependent kinases that associate with cyclin Dl. Oncogene, 9:71–79.
4. Bernier, L., and Wang, E., 1996. A prospective view on phos-phatases and replicative senescence. Exp. Gerontol., 31:13–19.
5. Bishop, D., Park, K. D., Xu, L., and Kleckner, N., 1992. Dmcl:a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation. and cell cycle progression. Cell, 69:439–456.
6. Bishop, D. K., 1994. RecA homologs Dmcl and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell, 79:1081–1092.
7. Borcherding, J., 1991. The annual reproductive cycle of the freshwater mussel Dreissena polymorpha Pallas in lakes. Oecologia, 87:208–218.
8. Boulikas, T., 1995. Phosphorylation of transcription factors and control of the cell cycle. Crit. Rev. Eukaryotic Expression, 5:1–77.
9. Cohen, P., 1989. The structure and regulation of protein phos-phatases. Ann. Rev. Biochem., 58:453–508.
10. Dermott, R., and Kerec, D., 1997. Changes to the deep-water benthos of eastern Lake Erie since the invasion of Dreissena. 1979-1993. Can. J. Fisheries Aquatic Sci., 54:922–930.
11. DesGroseillers, L., Auclair, D., Wickham, L., and Mallouf, M., 1994. A novel actin cDNA is expressed in the neurons of Aplysia californica. Biochim. Biophys. Acta, 1217:322–324.
12. Durkacz, B., Carr, A., and Nurse, P., 1986. Transcription of the cdc2 cell cycle control gene of the fission yeast Schizosaccharomyces pombe. EMBO J., 5:369–373.
13. Evans, D. R., and Hemmings, B. A., 2000a. Mutation of the C-terminal leucine of PP2Ac inhibits PR55/B subunit binding and confers supersensitivity to microtubule destabilization in Saccharomyces cerevisiae. Mol. Gene Genetics, 264:425–432.
14. Evans, D. R., and Hemmings, B. A., 2000b. Important role for phylogenetically invariant PP2Acalpha active site and C-terminal residues revealed by mutational analysis in Saccharomyces cerevisiae. Genetics, 156:21–29.
15. Evans, D. R., and Stark, M. J., 2000. Mutations in the Saccharomyces cerevisiae type 2A protein phosphatase catalytic subunit reveal roles in cell wall integrity, actin cytoskeleton organization. and mitosis. Genetics, 145:227–241.
16. Fong, P. P., Hardege, J. D., and Ram, J. L., 1994a. Long-lasting, sex-specific inhibition of serotonin-induced spawning by methiothepin in the zebra mussel, Dreissena polymorpha (Pallas). J. Exp. Zool., 270:314–320.
17. Fong, P. P., Kyozuka, K., Abdelghani, H., Hardege, J. D., and Ram, J. L., 1994b. In vivo in vitro induction of germinal vesicle breakdown in a freshwater bivalve. the zebra mussel. J. Exp. Zool., 269:467–474.
18. Funabiki, H., Yamano, H., Nagao, K., Tanaka, H., Yasuda, H., Hunt, T., and Yanagida, M., 1997. Fission yeast Cut2 required for anaphase has two destruction boxes. EMBO J., 16:5977–5987.
19. Furnari, B. A., Russel, P., and Leatherwood, J., 1997. pchl+, a second essential C-type cyclin gene in Schizosaccharomyces pombe. J. Biol. Chem., 272:12100–12106.
20. Gallant, P., and Nigg, E. A., 1992. Cyclin B2 undergoes cell cycle-dependent nuclear translocation and, when expressed as a non-destructible mutant. causes mitotic arrent in HeLa cells. J. Cell. Biol., 117:213–224.
21. Glotzer, M., Murray, A. W., and Kirschner, M. W., 1991. Cyclin is degraded by the ubiquitin pathway. Nature, 349:132–138.
22. Gould, K., and Nurse, P., 1989. Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis. Nature, 342:39–45.
23. Gromoll, J., Wessels, J., Rosiepen, G., Brinkworth, M. H., and Weinbauer, G. F., 1997. Expression of mitotic cyclin Bl is not confined to proliferating cells in the rat testis. Biol. Reprod., 57:1312–1319.
24. Healy, A. M., Zolnierowicz, S., Stapleton, A. E., Goebl, M., DePaoli-Roach, A. A., and Pringle, J. R., 1991. Cdc55, a Saccharomyces cerevisiae gene involved in cellular morphogenesis:identification, characterization. and homology to the B subunit of mammalian type 2A protein phosphatase. Mol. Cell. Biol., 11:5767–5780.
25. Hebert, P. D.N., Muncaster, B. W., and Mackie, G. L., 1989. Ecological and genetic studies on Dreissena polymorpha (Pallas):A new mollusc in the Great Lakes. Can. J. Fish. Aqua. Sci., 46:1587–1591.
26. Hecht, N. B., Distel, R. J., Yelick, P. C., Tanhauser, S. M., Driscoll, C. E., Goldberg, E., and Tung, K. S.K., 1988. Localization of a highly divergent mammalian testicular alpha tubulin that is not detectable in brain. Mol. Cell. Biol., 8:996–1000.
27. Hunter, P., and Pines, J., 1994. Cyclins and cancer II:cyclin D and cdk inhibitors come of age. Cell, 79:573–582.
28. Ivanov, E. L., and Haber, J. E., 1997. DNA repair:rad alert. Curr. Biol., 7 R492-R495
29. Karatayev, A. Y., Burlakova, L. E., and Padilla, D. K., 1997. The effects of Dreissena polymorpha (Pallas) invasion on aquatic communities in Eastern Europe. J. Shellfish Res., 16:187–203.
30. Kinoshita, N., Ohkura, H., and Yanagida, M., 1990. Distinct. essential roles of type 1 and 2A protein phosphatases in the control of the fission yeast cell division cycle. Cell, 63:405–415.
31. Kondo, T., Kotani, T., and Yamashita, M., 2001. Dispersion of cyclin B mRNA aggregation is coupled with translational activation of the mRNA during zebrafish ooctye maturation, [journal?. 229:421–431. ]
32. Krek, W., and Nigg, E. A., 1989. Structure and developmental expression of the chicken Cdc2 kinase. EMBO J., 8:3071–3078.
33. Labbé, J. C., Capony, J. P., Caput, D., Cavadore, J. C., Derancourt, J., Kaghad, M., Lelias, J. M., Picard, A., and Dorée, M., 1989. MPF from starfish oocytes at first meiotic metaphase is a heterodimer containing one molecule of cdc2 and one molecule of cyclin B. EMBO J., 8:3053–3058.
34. Lamers, A. E., Heiney, J. P., and Ram, J. L., 1998. Isolation and characterization of a cDNA encoding an actin protein from the zebra mussel, Dreissena polymorpha. J. Shellfish Res., 17:1215–1217.
35. Lamers, A. E., Heiney, J. P., and Ram, J. L., 1999. Cloning and sequence analysis of two cDNAs encoding cyclin A and cyclin B in the zebra mussel Dreissena polymorpha. Biochim. Biophys. Acta, 1448:519–524.
36. Leclerc, V., Tassan, J., O'Farrell, P. H., Nigg, E. a., and Léopold, P., 1996. Drosophila Cdk8. a kinase partner of cyclin C that interacts with the large subunit of RNA polymerase II. Mol. Biol. Cell, 7:505–513.
37. Lee, M. G., Norbury, C. J., Spurr, N. K., and Nurse, P., 1988. Regulated expression and phosphorylation of a possible mammalian cell-cycle control protein. Nature, 333:676–679.
38. Lee, T. H., Solomon, M. J., Mumby, M. C., and Kirschner, M. W., 1991. INH, a negative regulator of MPF. is a form of protein phosphatase 2A. Cell, 64:415–423.
39. Lehner, C. F., and O'Farrell, P. H., 1990. Drosophila cdc2 homologs:a functional homolog is coexpressed with a cognate variant. EMBO J., 9:3573–3581.
40. Léopold, P., and O'Farrell, P. H., 1991. An evolutionarily conserved cyclin homolog from Drosophila rescues yeast deficient in Gl cyclins. Cell, 66:1207–1216.
41. Lew, D. J., Dulic, V., and Reed, S. I., 1991. Isolation of three novel human cyclins by rescue of Gl cyclin (Cln) function in yeast. Cell, 66:1197–1206.
42. Lewis, S. A., Lee, M. G., and Cowan, N. J., 1985. Five mouse tubulin isotypes and their regulated expression during development. J. Cell. Biol, 101:852–861.
43. Li, H., Lahti, J. M., and Kidd, V. J., 1996. Alternatively spliced cyclin C mRNA is widely expressed, cell cycle regulated. and encodes a truncated cyclin box. Oncogene, 13:705–712.
44. Matsushime, H, Ewen, M. E., Strom, D. K., Kato, J. Y., Hanks, S. K., Roussel, M. F., and Sherr, C. J., 1992. Identification and properties of an atypical catalytic subunit (p34PSKJ3/cdk4) for mammalian D type Gl cyclins. Cell, 71:323–334.
45. Matsushime, H., Roussel, M. F, Ashmun, R. A., and Sherr, C. J., 1991. Colony-stimulating factor 1 regulates novel cyclins during the Gl phase of the cell cycle. Cell, 65:701–713.
46. Mayer-Jaekel, R. E., Ohkura, H., Gomes, R., Sunkel, C. E., Baumgartner, S., Hemmings, B. A., and Glover, D. M., 1993. The 55 kd regulatory subunit of Drosophila protein phosphatase 2A is required for anaphase. Cell, 72:621–633.
47. Meyerson, M., and Harlow, E., 1994. Identification of Gl kinase activity for cdk6. a novel cyclin D partner. Mol. Cell. Biol, 14:2077–2086.
48. Miller, R. L, Mojares, J. J., and Ram, J. L., 1994. Species specific sperm attraction in the zebra mussels Dreissena polymorpha D. bugensis. Can. J. Zool, 72:1764–1770.
49. Minshull, J., Golsteyn, R., Hill, C. S., and Hunt, T., 1990. The A-and B-type cyclin associated cdc2 kinases in Xenopus turn on and off at different times in the cell cycle. EMBO J., 9:2865–2875.
50. Misamore, M. J., and Lynn, J. W., 2000. Role of the cytoskeleton in sperm entry during fertilization in the freshwater bivalve Dreissena polymorpha. Biol. Bull, 199:144–156.
51. Mitchell, E. J., Zimmerman, S., and Zimmerman, A. M., 1985. Actin and tubulin in Tetrahymena. Can. J. Biochem. Cell Biol, 63:389–396.
52. Molloy, D. P, Powell, J., and Ambrose, P., 1994. Short-term reduction of adult zebra mussels (Dreissena polymorpha) in the Hudson River near Catskill, New York:an effect of juvenile blue crab (Callinectes sapidus) predation. J. Shellfish Res, 13:367–371.
53. Monteiro, M. J., and Cleveland, D. W., 1988. Sequence of chicken c beta 7 tubulin. Analysis of a complete set of vertebrate beta-tubulin isotypes. J. Mol. Biol, 199:439–446.
54. Morita, T., Yoshimura, Y., Yamamoto, A., Murata, K., Mori, M., Yamamoto, H., and Matsushiro, A., 1993. A mouse homolog of the Escherichia coli recA and Sacccharomyces cerevisiae RAD51 genes. Proc. Natl. Acad. Sci. USA, 90:6577–6580.
55. Murray, A. W., and Kirschner, M. W., 1989. Cyclin synthesis drives the early embryonic cell cycle. Nature, 339:275–280.
56. Murray, A. W., Soloman, M. J., and Kirschner, M. W., 1989. The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature, 339:280–286.
57. Namsaraev, E., and Berg, P., 1997. Characterization of strand exchange activity of yeast rad51 protein. Mol. Cell. Biol, 17:5359–5368.
58. Nishida, H., Morokuma, J., and Nishikata, T., 1999. Maternal cytoplasmic factors for generation of unique cleavage patterns in animal embryos. Curr. Topics Develop. Biol, 46:1–37.
59. Nurse, P., 1990. Universal control mechanism regulating onset of M-phase. Nature, 344:503–508.
60. Nurse, P., and Bissett, Y., 1981. Gene required in Gl for commitment to cell cycle and in G2 for control of mitosis in fission yeast. Nature, 292:558–560.
61. Ogawa, T. A.S., and Ikeya, T., 1995. A species-specific interaction of rad51 and rad52 proteins in eukaryotes. Adv. Biophys, 31:93–100.
62. Orgad, S., Brewis, N. D., Alphey, L., Axton, J. M., Dudai, Y., and Cohen, P. T., 1990. The structure of protein phosphatase 2A is as highly conserved as that of protein phosphatase 1. FEBS Lett, 275:44–48.
63. Pagano, M., Pepperkok, R., Verde, F., Ansorge, W., and Draetta, G., 1992. Cyclin A is required at two points in the human cell cycle. EMBO J., 11:961–971.
64. Parsons, R., 1998. Phosphatases and tumorigenesis. Curr. Opinion Oncol, 10:88–91.
65. Patwary, M. U., Reith, M., and Kenchington, E. L., 1996. Isolation and characterization of cDNA encoding an actin gene from sea scallop (Placopecten magellanicus). J. Shellfish Res, 15:265–270.
66. cdc2. Cell, 58:833–846.
67. Ram, J. L., Crawford, G. W., Walker, J. U., Mojares, J. J., Patel, N., Fong, P. P., and Kyozuka, K., 1993. Spawning in the zebra mussel (Dreissena polymorpha):Activation by internal or external application of serotonin. J. Exper. Zool, 265:587–598.
68. Ram, J. L., Fong, P. P., and Garton, D. W., 1996. Physiological aspects of zebra mussel reproduction:Maturation. spawning and fertilization. Amer. Zool., 36:326–338.
69. Reed, B. H., 1995. Drosophila development pulls the strings of the cell cycle. BioEssays, 17:553–556.
70. Schloesser, D. W., and Nalepa, T. F., 1994. Dramatic decline of unionid bivalves in offshore waters of Western Lake Erie after infestation by the zebra mussel, Dreissena polymorpha. Can. J. Fisheries Aquatic Sci., 51:2234–2242.
71. Schroeder, T. E., 1975. Molecules and Cell Movement Edited by:Inoue, S., and Stephens, R. E., 305–334. New York:Raven Press.
72. Shaw, G., and Kamen, R., 1986. A conserved AU sequence from the 3′-untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell, 46:659–667.
73. Sherr, C. J., 1993. Mammalian Gl cyclins. Cell, 73:1059–1065.
74. Sherr, C. J., 1994. Gl phase progression:cycling on cue. Cell, 79:551–555.
75. Shinohara, A., Ogawa, E. L., and Ogawa, T., 1992. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell, 69:457–470.
76. Simanis, V., and Nurse, P., 1986. The cell cycle control gene cdc2+ of fission yeast encodes a protein kinase potentially regulated by phosphorylation. Cell, 45:261–268.
77. Sprung, M., 1989. Field and laboratory observations of Dreissena polymorpha larvae:A bundance growth. mortality and food demands. Arch. Hydrobiol., 115:537–561.
78. Stanczykowska, A., and Lewandowski, K., 1993. “ Thirty years of studies of Dreissena polymorpha ecology in Mazurian Lakes of Northeastern Poland ”. In Zebra Mussels:Biology, Impacts and Control Edited by:Nalepa, T. F., and Schloesser, D. W., 3–37. Boca Raton, FL:Lewis.
79. Stassen, N. Y., Logsden, J. M., Jr., Vora, G. J., Offenberg, H. H., Palmer, J. D., and Zolan, M. E., 1997. Isolation and characterization of rad51 orthologs from Coprinus cinereus Lycopersicon esculentum. and phylogenetic analysis of eukaryotic recA homologs. Curr. Gen., 31:144–157.
80. Suganuma, M., Fujiki, H., Suguri, H., Yoshizawa, H., Hirota, S., Nakayasu, M., Ojika, M., Wakamatsu, M., Yamada, K., and Suganuma, T., 1988. Okadaic acid:an additional non- phorbol-12- tetradecanoate-13- acetatetype tumour promoter. Proc. Natl. Acad. Sci. USA, 85:1768–1771.
81. Sullivan, K. F., 1988. Structure and utilization of tubulin isotypes. Ann. Rev. Cell Biol., 4:687–716.
82. Sung, P., 1994. Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast rad51 protein. Science, 265:1241–1243.
83. Villasante, A., Wang, D., Dobner, P. D. P., Lewis, S. A., and Cowan, N. J., 1986. Six mouse alpha-tubulin mRNAs encode five distinct isotypes:testis-specific expression of two sister genes. Mol. Cell. Biol., 6:2409–2419.
84. Waller, D. L., Rach, J. J., Cope, W. G., Marking, L. L., Fisher, S. W., and Dabrowska, H., 1993. Toxicity of candidate molluscicides to zebra mussel (Dreissena polymorpha) and selected nontarget organisms. J. Great Lakes Res., 19:695–702.
85. Xiong, Y., Menninger, J., Beach, D., and Ward, D. C., 1992. Molecular cloning and chromosomal mapping of CCND genes encoding human D-type cyclins. Genomics, 13:575–584.
86. Yoshimura, Y., Morita, T., Yamamoto, A., and Matsushiro, A., 1993. Cloning and sequence of the human RecA-like gene cDNA. Nucleic Acids Res., 21:1665
87. Zimmerman, A. M., and Forer, A., eds. 1981. Mitosis and Cytokinesis New York:Academic Press.