Purification and antimicrobial function of ubiquitin isolated from the gill of Pacific oyster, Crassostrea gigas

Molecular Immunology

Volumn 53, Issue 1-2, 2013, Pages 88-98

  Seo, Jung Kil ^a   Lee, Min Jeong ^a   Go, Hye Jin ^a   Kim, Gun Do ^a   Jeong, Hyun Do ^a   Nam, Bo Hye ^b   Park, Nam Gyu ^a  

^a Pukyong National University   (South Korea)

^b National Fisheries Research and Development Institute (NFRDI)   (South Korea)

Author keywords

Antimicrobial activity; Innate immunity; MRNA expression; Pacific oyster (Crassostrea gigas); Ubiquitin

Indexed keywords

AMINO ACID; ARGININE; CARBOXYPEPTIDASE B; COMPLEMENTARY DNA; GLYCINE; MESSENGER RNA; RIBOSOME PROTEIN; UBIQUITIN;

AEROMONAS HYDROPHILA; ALPHA HELIX; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ANTIBACTERIAL ACTIVITY; ANTIFUNGAL ACTIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BACILLUS SUBTILIS; BACTERICIDAL ACTIVITY; BACTERIOSTASIS; CANDIDA ALBICANS; CARBOXY TERMINAL SEQUENCE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CRASSOSTREA GIGAS; CYTOTOXICITY; DNA LIBRARY; ESCHERICHIA COLI; EXPRESSED SEQUENCE TAG; HEMOLYSIS; HUMAN; HUMAN CELL; INNATE IMMUNITY; MEMBRANE PERMEABILITY; MOLECULAR WEIGHT; NONHUMAN; OYSTER; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN MOTIF; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PSEUDOMONAS AERUGINOSA; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SEQUENCE HOMOLOGY; SHIGELLA FLEXNERI; SHIGELLA SONNEI; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS INIAE; UPREGULATION; VIBRIO PARAHAEMOLYTICUS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CRASSOSTREA; HUMANS; IMMUNITY, INNATE; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; UBIQUITIN;

CRASSOSTREA GIGAS; OSTREIDAE; POSIBACTERIA; STREPTOCOCCUS INIAE; VIBRIO PARAHAEMOLYTICUS; VIBRIO SP.;

EID: 84864415104     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2012.07.003     Document Type: Article

References (57)

1. Alonso S., Pethe K., Russell D.G., Purdy G.E. Lysosomal killing of Mycobacterium mediated by ubiquitin-derived peptides is enhanced by autophagy. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:6031-6036.
2. Audhya T., Goldstein G. Thymopoietin and ubiquitin. Methods in Enzymology 1985, 116:279-291.
3. Baker R.T., Board P.G. The human ubiquitin-52 amino acid fusion protein gene shares several structural features with mammalian ribosomal protein genes. Nucleic Acids Research 1991, 19:1035-1040.
4. Busch H. Ubiquitination of proteins. Methods in Enzymology 1984, 106:238-262.
5. Catic A., Ploegh H.L. Ubiquitin-conserved protein or selfish gene?. Trends in Biochemical Sciences 2005, 30:600-604.
6. Charlet M., Chernysh S., Philippe H., Hetru C., Hoffmann J.A., Bulet P. Innate immunity: isolation of several cysteine-rich antimicrobial peptides from the blood of a mollusk, Mytilus edulis. Journal of Biological Chemistry 1996, 271:21808-21813.
7. Destoumieux D., Bulet P., Loew D., VanDorsselaer A., Rodriguez J., Bachere E. Penaeidins, a new family of antimicrobial peptides isolated from the shrimp Penaeus vannamei. Journal of Biological Chemistry 1997, 272:28398-28406.
8. Ecker D.J., Butt T.R., Marsh J., Sternberg E.J., Margolis N., Monia B.P., Jonnalagadda S., Khan M.I., Weber P.L., Mueller L., Crooke S.T. Gene synthesis, expression, structures, and functional activities of site-specific mutants of ubiquitin. Journal of Biological Chemistry 1987, 262:14213-14221.
9. Goldstein G., Scheid M.S., Hammerling V., Boyse E.A., Schlesinger D.H., Niall H.D. Isolation of a polypeptide that has lymphocyte-differentiating properties and is probably represented universally in living cells. Proceedings of the National Academy of Sciences of the United States of America 1975, 72:11-15.
10. Gueguen Y., Bernard R., Julie F., Paulina S., Delphine D.G., Franck V., Philippe B., Evelyne B. Oyster hemocytes express a proline-rich peptide displaying synergistic antimicrobial activity with a defensin. Molecular Immunology 2009, 46:516-522.
11. Gueguen Y., Herpin A., Aumelas A., Garnier J., Fievet J., Escoubas J.M., Bulet P., Gonzalez M., Lelong C., Favrel P., Bachère E. Characterization of a defensin from the oyster Crassostrea gigas. Recombinant production, folding, solution structure, antimicrobial activities, and gene expression. Journal of Biological Chemistry 2006, 281:313-323.
12. Hegde A.N. Ubiquitin-proteasome-mediated local protein degradation and synaptic plasticity. Progress in Neurobiology 2004, 73:311-357.
13. Herbinière J., Braqart-Varnier C., Grève P., Strub J-M., Frère J., Van Dorsselaer A., Martin G. Armadillidin: a novel glycine-rich antibacterial peptide directed against gram-positive bacteria in the woodlouse Armadillium vulgare (Terrestrial Isopod, Crustacean). Developmental and Comparative Immunology 2005, 29:489-499.
14. Hicke L. Protein regulation by monoubiquitin. Nature Reviews Molecular Cell Biology 2001, 2:195-201.
15. Howell S.J., Wilk D., Yadav S.P., Bevins C.L. Antimicrobial polypeptides of the human colonic epithelium. Peptides 2003, 24:1763-1770.
16. Hubert F., Noel T., Roch P. A member of the arthopod defensin family from edible Mediterranean mussels (Mtyilus galloprovincials). European Journal of Biochemistry 1996, 240:302-306.
17. Iijima R., Kisugi J., Yamazaki M. A novel antimicrobial peptide from the sea hare Dolabella auricularia. Developmental and Comparative Immunology 2003, 27:305-311.
18. Jang W.S., Kim K.N., Lee Y.S., Nam M.H., Lee I.H. Halocidin: a new antimicrobial peptide from hemocytes of the solitary tunicate, Halocynthia aurantium. FEBS Letters 2002, 521:81-86.
19. Khoo L., Robinette D.W., Noga E.J. Callinectin, an antibacterial peptide from blue crab, Callinectes sapidus, hemocytes. Marine Biotechnology 1999, 1:44-51.
20. Kieffer A.E., Goumon Y., Ruh O., Chasserot-Golaz S., Nullans G., Gasnier C., Aunis D., Metz-Boutigue M.H. The N- and C-terminal fragments of ubiquitin are important for the antimicrobial activities. FASEB Journal 2003, 17:776-778.
21. Kim J.Y., Lee S.Y., Park S.C., Shin S.Y., Choi S.J., Park Y., Hahm K.S. Purification and antimicrobial activity studies of the N-terminal fragment of ubiquitin from human amniotic fluid. Biochimica et Biophysica Acta 2007, 1774:1221-1226.
22. Komander D., Clague M.J., Urbé S. Breaking the chains: structure and function of the deubiquitinases. Nature Reviews Molecular Cell Biology 2009, 10:550-563.
23. Koo Y.S., Kim J.M., Park I.Y., Yu B.J., Jang S.A., Kim K.S., Park C.B., Cho J.H., Kim S.C. Structure-activity relations of parasin I, a histone H2A-related antimicrobial peptide. Peptides 2008, 29:1102-1108.
24. Lee I.H., Lee Y.S., Kim C.H., Kim C.R., Hong T., Menzel L., Boo L.M., Pohl J., Sherman M.A., Waring A., Lehrer R.I. Dicynthaurin: an antimicrobial peptide from hemocytes of the solitary tunicate, Halocynthia aurantium. Biochimica et Biophysica Acta 2001, 1527:141-148.
25. Lee M., Taylor G.T., Bricelj V.M., Ford S.E., Zahn S. Evaluation of Vibrio spp. and microplankton blooms as causative agents of juvenile oyster disease in Crassostrea virginica (Gmelin). The Journal of Shellfish Research 1996, 15:319-329.
26. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using realtime quantitative PCR and the 2-ΔΔCt method. Methods 2001, 25:402-408.
27. Loir M., Caraty A., Lanneau M., Menezo Y., Muh J.P., Sautiere P. Purification and characterization of ubiquitin from mammalian testis. FEBS Letters 1984, 169:199-204.
28. Metz-Boutigue M.H., Kieffer A.E., Goumon Y., Aunis D. Innate immunity: involvement of new neuropeptides. Trends in Microbiology 2003, 11:585-592.
29. Mitta G., Vandenbulcke F., Hubert F., Roch P. Mussel defensins are synthesized and processed in granulocytes then released into the plasma after bacterial challenge. Journal of Cell Science 1999, 112:4233-4242.
30. Nabika T., Terashima M., Momose I., Hosokawa Y., Nagasue N., Tanigawa Y. Synergistic effect of ubiquitin on lipopolysaccharide induced TNF-alpha production in murine macrophage cell line RAW264.7 cells. Biochimica et Biophysica Acta 1999, 1450:25-34.
31. Nakamura T., Furunake H., Myyata T., Tokunaga F., Muta T., Iwanaga S. Tachyplesin, a class of antimicrobial peptides from the hemocytes of the horseshoe crab (Tachypleus tridentatus). Journal of Biological Chemistry 1988, 263:16709-16713.
32. Nenoi M., Ichimura S., Mita K. Interspecific comparison in the frequency of concerted evolution at the polyubiquitin gene locus. Journal of Molecular Evolution 2000, 51:161-165.
33. Park E.M., Kim Y.O., Nam B.H., Kong H.J., Kim W.J., Lee S.J., Kong I.S., Choi T.J. Cloning, characterization and expression analysis of the gene for a putative lipopolysaccharide-induced TNF-α factor of the Pacific oyster, Crassostrea gigas. Fish and Shellfish Immunology 2008, 24:11-17.
34. Park N.G., Silphaduang U., Moon H.S., Seo J.-K., Corrales J., Noga E.J. Structure-activity relationships of piscidin 4, a piscine antimicrobial peptide. Biochemistry 2011, 50:3288-3299.
35. Patrzykat A., Gallant J.W., Seo J.K., Pytyck J., Douglas S.E. Novel antimicrobial peptides related from flatfish genes. Antimicrobial Agents and Chemotherapy 2003, 47:2464-2470.
36. Phadke S.M., Lazarevic V., Bahr C.C., Islam K., Stolz D.B., et al. Lentivirus lytic peptide-1 perturbs both outer and inner membranes of Serratia marcescens. Antimicrobial Agents and Chemotherapy 2002, 46:2041-2045.
37. Relf J.M., Chisholm J.R.S., Kemp G.D., Smith V.J. Purification and characterization of a cysteine-rich 11.5-kDa antibacterial protein from the granular haemocytes of the shore crab. Carcinus maenas. European Journal of Biochemistry 1999, 264:350-357.
38. Rosa R.D., Santini A., Fievet J., Bulet P., Destoumieux-Garzón D., Bachère E. Big defensins, a diverse family of antimicrobial peptides that follows different patterns of expression in hemocytes of the oyster Crassostrea gigas. PLoS ONE 2011, 6(9):e25594.
39. Scheid M.S., Goldstein G., Hammerling U., Boyse E.A. Ir genes and antigen recognition. Annals of the New York Academy of Sciences 1975, 249:541-547.
40. Schlesinger D.H., Goldstein G. Molecular conservation of 74 amino acid sequence of ubiquitin between cattle and man. Nature 1975, 255:423-424.
41. Schlesinger D.H., Goldstein G., Niall H.D. Complete amino acid sequence of ubiquitin, an adenylate cyclase stimulating polypeptide probably universal in living cells. Biochemistry 1975, 14:2214-2218.
42. Schnapp D., Kemp G.D., Smith V.J. Purification and characterization of a proline-rich antibacterial peptides, with sequence similarity to bactenecin-7, from the haemocytes of the shore crab, Carcinus maenas. European Journal of Biochemistry 1996, 240:532-539.
43. Seo J.-K., Crawford J.M., Stone K.L., Noga E.J. Purification of a novel arthropod defensin from the American oyster, Crassostrea virginica. Biochemical and Biophysical Research Communications 2005, 338:1998-2004.
44. Seo J.-K., Crawford J.M., Stone K.L., Noga E.J. American oyster, Crassostrea virginica, expresses a potent antibacterial histone H2B protein. Marine Biotechnology 2010, 12:543-551.
45. Seo J.-K., Stephenson J., Crawford J.M., Noga E.J. Multiple antibacterial histone H2B proteins are expressed in tissues of American oyster. Comparative Biochemistry and Physiology. B: Comparative Biochemistry 2011, 158:223-229.
46. Sharp P.M., Li W.H. Ubiquitin genes as a paradigm of concerted evolution of tandem repeats. Journal of Molecular Evolution 1987, 25:58-64.
47. Shigenaga T., Muta T., Toh Y., Tokunaga F., Iwanaga S. Antimicrobial tachyplesin peptide precursor. Journal of Biological Chemistry 1990, 265:21350-21354.
48. Siegelman M., Bond M.W., Gallatin W.M., St John T., Smith H.T., Fried V.A., Weissman I.L. Cell surface molecule associated with lymphocyte homing is a ubiquitinated branched-chain glycoprotein. Science 1986, 231:823-829.
49. Silphaduang U., Noga E.J. Peptide antibiotics in mast cells of fish. Nature 2001, 414:268-269.
50. Skerlavaj B., Romeo D., Gennaro R. Rapid membrane permeabilization and inhibition of vital functions of Gram-negative bacteria by bactenecins. Infection and Immunity 1990, 58:3724-3730.
51. Svensson I., Calles K., Lindskog E., Henriksson H., Eriksson U., Häggström L. Antimicrobial activity of conditioned medium fractions from Spodoptera frugiperda Sf9 and Trichoplusia in Hi5 insect cells. Applied Microbiology and Biotechnology 2005, 69:92-98.
52. Tincu J.A., Taylor S.W. Antimicrobial peptides from marine invertebrates. Antimicrobial Agents and Chemotherapy 2004, 48:3645-3654.
53. Vijay-Kumar S., Bugg C.E., Wilkinson K.D., Cook W.J. Three-dimensional structure of ubiquitin at 2.8Å resolution. Proceedings of the National Academy of Sciences of the United States of America 1985, 82:3582-3585.
54. Wang B., Harwig S.S., Lehrer R.I. Rat bladder ubiquitin-like molecule: isolation, purification and N-terminal sequencing. Hua Xi Yi Ke Da Xue Xue Bao 1993, 24:127-130.
55. Wang Y., Griffiths W.J., Jörnvall H., Agerberth B., Johansson J. Antibacterial peptides in stimulated human granulocytes: characterization of ubiquitinated histone H1A. European Journal of Biochemistry 2002, 269:512-518.
56. Watson D.C., Levy W.B., Dixon G.H. Free ubiquitin is a non-histone protein of trout testis chromatin. Nature 1978, 276:196-198.
57. Wilkinson K.D., Audhya T.K. Stimulation of ATP-dependent proteolysis requires ubiquitin with the COOH-terminal sequence Arg-Gly-Gly. Journal of Biological Chemistry 1981, 256:9235-9241.