Expression characteristics of the SUMOylation genes SUMO-1 and Ubc9 in the developing testis and ovary of Chinese mitten crab, Eriocheir sinensis

Gene

Volumn 501, Issue 2, 2012, Pages 135-143

  Wang, Qun ^a   Wang, Ying ^a   Chen, Lili ^a   He, Lin ^a   Li, Weiwei ^a   Jiang, Hui ^a  

^a EAST CHINA NORMAL UNIVERSITY   (China)

Author keywords

EsSUMO 1; EsUbc9; In situ hybridization; Oogenesis; Quantitative real time PCR; Spermatogenesis

Indexed keywords

MESSENGER RNA; PROTEIN UBC9; SUMO 1 PROTEIN;

ANIMAL TISSUE; ARTICLE; CRAB; CRUSTACEA; ERIOCHEIR SINENSIS; FEMALE; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; IN SITU HYBRIDIZATION; MALE; NONHUMAN; OOCYTE DEVELOPMENT; OVARY DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SPERMATOGENESIS; SUMOYLATION; TESTIS DEVELOPMENT;

AMINO ACID SEQUENCE; ANIMALS; ANOMURA; BASE SEQUENCE; FEMALE; GAMETOGENESIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MOLECULAR SEQUENCE DATA; OOCYTES; OVARY; PHYLOGENY; SEQUENCE ALIGNMENT; SPERMATIDS; SUMO-1 PROTEIN; SUMOYLATION; TESTIS; UBIQUITIN-CONJUGATING ENZYMES;

CRUSTACEA; ERIOCHEIR SINENSIS; EUKARYOTA; VERTEBRATA;

EID: 84860710966     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2012.04.016     Document Type: Article

References (63)

1. Artus J., Babinet C., Cohen- Tannoudji M. The cell cycle of early mammalian embryos lessons from genetic mouse models. Cell Cycle 2006, 5:499-502.
2. Bayer P., et al. Structure determination of the small ubiquitin-related modifier SUMO-1. J. Mol. Biol. 1998, 280:275-286.
3. Bernier-Villamor V., Sampson D.A., Matunis M.J., Lima C.D. Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP. Cell 2002, 108:345-356.
4. Chang Y., Liang L., Ma H., He J., Sun X. Microsatellite analysis of genetic diversity and population structure of Chinese mitten crab (Eriocheir sinensis). J. Genet. Genomics 2008, 35:171-176.
5. Desterro J.M.P., Thomson J., Hay R.T. Ubc9 conjugates SUMO but not ubiquitin. FEBS Lett. 1997, 417:297-300.
6. Du N.S., Lai W., Xue L.Z. Studies on the sperm of Chinese mitten-hand crab, Eriocheir sinensis (Crustacea, Decapoda): I. The morphology and ultrastructure of mature sperm. Oceanol. Limnol. Sin. 1987, 18:119-125.
7. Du N.S., Lai W., Nan C.R., Jiang H.W. The morphology and ultrastructure of the mature egg of Eriocheir sinensis (Crustacean, Decapoda). Acta Zool. Sin. 1995, 41:229-234.
8. Geiss-Friedlander R., Melchior F. Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 2007, 8:947-956.
9. Gill G. SUMO and ubiquitin in the nucleus: different functions, similar mechanisms?. Genet. Dev. 2004, 18:2046-2059.
10. Gong L., Kamitani T., Fujise K., Caskey L.S., Yeh E.T. Preferential interaction of sentrin with a ubiquitin-conjugating enzyme, Ubc9. J. Biol. Chem. 1997, 272:28198-28201.
11. Grewal S.I.S., Rice J.C. Regulation of heterochromatin by histone methylation and small RNAs. Curr. Opin. Cell Biol. 2004, 16:230-238.
12. Hannich J.T., et al. Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J. Biol. Chem. 2005, 280:4102-4110.
13. Hashiyama K., Shigenobu S., Kobayashi S. Expression of genes involved in sumoylation in the Drosophila germline. Gene Expr. Patterns 2009, 9:50-53.
14. Hay R. SUMO-specific proteases: a twist in the tail. Trends Cell Biol. 2007, 17:370-376.
15. Herrmann J., Lerman L.O., Lerman A. Ubiquitin and ubiquitin-like proteins in protein regulation. Circ. Res. 2007, 100:1276-1291.
16. Hochstrasser M. Ubiquitin and intracellular protein degradation. Curr. Opin. Cell Biol. 1992, 4:1024-1031.
17. Howe K., et al. The ubiquitin-homology gene PIC1: characterization of mouse (Pic1) and human (UBL1) genes and pseudogenes. Genomics 1998, 47:92-100.
18. Jentsch S. The ubiquitin-conjugation system. Annu. Rev. Genet. 1992, 26:179-207.
19. Jiang H., et al. Functional annotation and analysis of expressed sequence tags from the hepatopancreas of mitten crab (Eriocheir sinensis). Mar. Biotechnol. 2008, 11:317-326.
20. Johnson E.S. Protein modification by SUMO. Annu. Rev. Biochem. 2004, 73:355-382.
21. Johnson E.S., Blobel G. Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p. J. Biol. Chem. 1997, 272:26799-26802.
22. Johnson E.S., Schwienhorst I., Dohmen R.J., Blobel G. The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. EMBO J. 1997, 16:5509-5519.
23. Knipscheer P., et al. Ubc9 sumoylation regulates SUMO target discrimination. Mol. Cell 2008, 31:371-382.
24. La Salle S., Sun F., Zhang X.D., Matunis M.J., Handel M.A. Developmental control of sumoylation pathway proteins in mouse male germ cells. Dev. Biol. 2008, 321:227-237.
25. Laoong-U-Thai Y., Zhao B.P., Phongdara A., Ako H., Yang J.Z. Identifications of SUMO-1 cDNA and its expression patterns in Pacific White shrimp Litopeanaeus vannamei. Int. J. Biol. Sci. 2009, 5:205-214.
26. Leelatanawit R., et al. Identification, characterization and expression of sex-related genes in testes of the giant tiger shrimp Penaeus monodon. Comp. Biochem. Phys. A 2009, 152:66-76.
27. Li Y.F., Kang X.J., Zhao X.Y., Wen X.R., Han L.Q. Intrinsic factors of precocity in mitten-handed crab Eriocheir sinensis. Fish. Sci. 2005, 24:34-36.
28. Li K., et al. The site of vitellogenin synthesis in Chinese mitten-handed crab Eriocheir sinensis. Comp. Biochem. Phys. B 2006, 143:453-458.
29. Lin D., et al. Identification of a substrate recognition site on Ubc9. J. Biol. Chem. 2002, 277:21740-21748.
30. Livak K.J., Schmittgen T.D. Analysis of temporal gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) method. Methods 2001, 25:402-408.
31. Mahajan R., Delphin C., Guan T., Gerace T., Melchior F. A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 1997, 88:97-107.
32. Matunis M.J., Coutavas E., Blobel G. A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J. Cell Biol. 1996, 135:1457-1470.
33. Mukhopadhyay D., Dasso M. Modification in reverse: the SUMO proteases. Trends Biochem. Sci. 2007, 32:286-295.
34. Mukhopadhyay D., Dasso M. The SUMO pathway in mitosis. SUMO Regulation of Cellular 2009, 153-170. V.G. Wilson (Ed.).
35. Nottke A.C., Colaiácovo M.P. Wrestling with chromosomes: the roles of SUMO during meiosis. SUMO Regulation of Cellular 2009, 171-186. V.G. Wilson (Ed.).
36. Novatchkova M., Budhiraja R., Coupland G., Eisenhaber F., Bachmair A. SUMO conjugation in plants. Planta 2004, 220:1-8.
37. Pickart C.M. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 2001, 70:503-533.
38. Qiu G.F., Liu P. On the role of Cdc2 kinase during meiotic maturation of oocyte in the Chinese mitten crab, Eriocheir sinensis. Comp. Biochem. Phys. B 2009, 152:243-248.
39. Rogers R.S., Inselman A., Handel M.A., Matunis M.J. SUMO modified proteins localize to the XY body of pachytene spermatocytes. Chromosoma 2004, 113:233-243.
40. Rose T.M., Schultz E.R., Henikoff J.G., Pietrokovski S., McCallum C.M., Henikoff S. Consensus-degenerate hybrid oligonucleotide primers for amplification of distantly related sequences. Nucleic Acids Res. 1998, 26(7):1628-1635.
41. Rudnick D., et al. A life history model for the San Francisco Estuary population of Chinese mitten crab, Eriocheir sinensis (Decapoda: Grapsoidea). Biol. Invas. 2005, 7:333-350.
42. Sakaguchi K., Koshiyama A., Iwabata K. Meiosis and small ubiquitin-related modifier (SUMO)-conjugating enzyme, Ubc9. FEBS J. 2007, 274:3519-3531.
43. Seufert W., Futcher B., Jentsch S. Role of a ubiquitin-conjugating enzyme in degradation of S- and M-phase cyclins. Nature 1995, 373:78-81.
44. Shen Z., Pardington-Purtymun P.E., Comeaux J.C., Moyzis R.K., Chen D.J. UBL1, a human ubiquitin-like protein associating with human RAD51/RAD52 proteins. Genomics 1996, 36:271-279.
45. Shen B., et al. Differential expression of ubiquitin-conjugating enzyme E2r in the developing ovary and testis of penaeid shrimp Marsupenaeus japonicus. Mol. Biol. Rep. 2008, 36:1149-1157.
46. Snedecor G., Cochran W. Statistical Methods 1971, The Iowas State University Press, Ames, Iowa.
47. Spiro R.G. Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 2002, 12:43-56.
48. Trifonov S., et al. In situ hybridization study of the distribution of choline acetyltransferase mRNA and its splice variants in the mouse brain and spinal cord. Neuroscience 2009, 159:344-357.
49. Vertegaal A.C. Small ubiquitin-related modifiers in chains. Biochem. Soc. Trans. 2007, 35:1422-1423.
50. Vigodner M., Morris P. Testicular expression of small ubiquitin-related modifier-1 (SUMO-1) supports multiple roles in spermatogenesis: silencing of sex chromosomes in spermatocytes, spermatid microtubule nucleation, and nuclear reshaping. Dev. Biol. 2005, 282:480-492.
51. Vigodner M., Ishikawa T., Schlegel P.N., Morris P.L. SUMO-1, human male germ cell development, and the androgen receptor in the testis of men with normal and abnormal spermatogenesis. Am. J. Physiol. Endocrinol. Metab. 2006, 290:E1022-E1033.
52. Waby J.S., Bingle C.D., Corfe B.M. Post-translational control of sp-family transcription factors. Curr. Genomics 2008, 9:301-311.
53. Walsh C.T., Garneau-Tsodikova S., Gatto G.J. Protein posttranslational modifications: the chemistry of proteome diversifications. Angew. Chem. Int. Ed. 2005, 44:7342-7372.
54. Wang D.H., Yang W.X. Molecular cloning and characterization of KIFC1-like kinesin gene (es-KIFC1) in the testis of the Chinese mitten crab Eriocheir sinensis. Comp. Biochem. Phys. A 2010, 157:123-131.
55. Watts F.Z. The role of SUMO in chromosome segregation. Chromosoma 2007, 116:15-20.
56. Wen X.B., Chen L.Q., Zhou Z.L., Ai C.X., Deng G.Y. Reproduction response of Chinese mitten-handed crab (Eriocheir sinensis) fed different sources of dietary lipid. Comp. Biochem. Phys. A 2002, 131:675-681.
57. Xue L.Z., Du N., Lai W. Histology of female reproductive system in Chinese mitten-handed crab, Eriocheir sinensis (Crustacean, Dacapoda). J. East China Norm. Univ. Nat. Sci. Ed. 1987, 3:88-97.
58. Yang M., Hsu C.T., Ting C.Y., Liu L.F., Wang J.H. Assembly of a polymeric chain of SUMO-1 on human topoisomerase I in vitro. J. Biol. Chem. 2006, 281:8264-8274.
59. Yeh E.T.H., Gong L., Kamitani T. Ubiquitin-like proteins: new wines in new bottles. Gene 2000, 248:1-14.
60. Zhang Z., et al. Ribosomal protein L24 is differentially expressed in ovary and testis of the marine shrimp Marsupenaeus japonicus. Comp. Biochem. Phys. B 2007, 147:466-474.
61. Zhang X.D., et al. SUMO-2/3 modification and binding regulate the association of CENP-E with kinetochores and progression through mitosis. Mol. Cell 2008, 29:729-741.
62. Zhang F., et al. cDNA cloning and expression of Ubc9 in the developing embryo and ovary of oriental river prawn, Macrobrachium nipponense. Comp. Biochem. Phys. B 2010, 155:288-293.
63. Zhou W., Ryan J.J., Zhou H. Global analyses of sumoylated proteins in Saccharomyces cerevisiae. Induction of protein sumoylation by cellular stresses. J. Biol. Chem. 2004, 279:32262-32268.