Cation metals specific hemocyanin exhibits differential antibacterial property in mud crab, Scylla serrata

References

Adachi K., Hirata T., Nagai K. & Sakaguchi M. 2008. Hemocyanin a most likely inducer of black spots in kuruma prawn Penaeus japonicus during storage. J. Food Sci. 66: 1130–1136.10.1111/j.1365-2621.2001.tb16093.xSearch in Google Scholar

Allison J. & Cole W. 1940. The nitrogen, copper and hemocyanin content of the sera of several arthropods. J. Biol. Chem. 135: 259–265.10.1016/S0021-9258(18)73182-7Search in Google Scholar

Ansorge W. 1985. Fast and sensitive detection of protein and DNA bands by treatment with potassium permanganate. J. Biochem. Biophys. Methods 11: 13–20.10.1016/0165-022X(85)90037-5Search in Google Scholar

Arumugam M. & Ravindranath M.H. 1986. Significance of the variation in haemolymph copper-free-and-bound proteins during ageing and time of day in the crab Scylla serrata (Forskal). Arch. Int. Physiol. Biochem. 94: 11–17.10.3109/13813458609069101Search in Google Scholar

Bachére E., Destoumieux D. & Bulet P. 2000. Penaeidins, antimicrobial peptides of shrimp: a comparison with other effectors of innate immunity. Aquaculture 191: 71–88.10.1016/S0044-8486(00)00419-1Search in Google Scholar

Battison A.L., Summerfield R. & Patrzykat A. 2008. Isolation and characterisation of two antimicrobial peptides from haemocytes of the American lobster Homarus americanus. Fish Shellfish Immunol. 25: 181–187.10.1016/j.fsi.2008.04.005Search in Google Scholar

Brenowitz M., Bonaventura C., Bonaventura J. & Gianazza E. 1981. Subunit composition of a high molecular weight oligomer: Limulus polyphemus hemocyanin. Arch. Biochem. Biophys. 210: 748–761.10.1016/0003-9861(81)90242-3Search in Google Scholar

Bruyninckx W.J., Gutteridge S. & Mason H.S. 1978. Detection of copper on polyacrylamide gels. Anal. Biochem. 89: 174–7.10.1016/0003-2697(78)90738-8Search in Google Scholar

Chattopadhyay I. & Chatterjee B.P. 1993. A low-molecular weight lectin from the edible crab Scylla serrata hemolymph: purification and partial characterization. Biochem. Arch. 9: 65–72.Search in Google Scholar

Cornick J.W. & Stewart J.E. 1968. Interaction of the pathogen Gaffkya homari with natural defense mechanisms of Homarus americanus. J. Fish. Res. Board Canada 25: 695–709.10.1139/f68-064Search in Google Scholar

Decker H. & Jaenicke E. 2004. Recent findings on phenoloxidase activity and antimicrobial activity of hemocyanins. Dev. Comp. Immunol. 28: 673–87.10.1016/j.dci.2003.11.007Search in Google Scholar PubMed

Destoumieux D., Bulet P., Loew D., Van Dorsselaer A., Rodriguez J. & Bachère E. 1997. Penaeidins, a new family of antimicrobial peptides isolated from the shrimp Penaeus vannamei (Decapoda). J. Biol. Chem. 272: 28398–28406.10.1074/jbc.272.45.28398Search in Google Scholar

Dolashka P., Dolashki A., Voelter W., Van Beeumen J. & Stevanovic S. 2015. Antimicrobial activity of peptides from the hemolymph of Helix lucorum snails. Int. J. Curr. Microbiol. Appl. Sci. 4: 1061–1071.Search in Google Scholar

Dolashka P., Dolashki A., Van Beeumen J., Floetenmeyerd M., Velkova L., Stevanovic S. & Voelter W. 2016. Antimicrobial activity of molluscan hemocyanins from helix and rapana snails. Curr. Pharm. Biotechnol. 17: 263–270.10.2174/1389201016666150907113435Search in Google Scholar

Dolashka P., Zal F., Dolashki A., Molin L., Traldi P. & Salvato B. 2012. ESI-MS and MALLS analysis of quaternary structure of molluscan hemocyanins. J. Mass Spectrom. 47: 940–947.10.1002/jms.2967Search in Google Scholar

Dolashka P., Moshtanska V., Borisova V., Dolashki A., Stevanovic S., Dimanov T. & Voelter W. 2011. Antimicrobial proline-rich peptides from the hemolymph of marine snail Rapana venosa.Peptides 32: 1477–1483.10.1016/j.peptides.2011.05.001Search in Google Scholar

Dolashka-Angelova P., Dolashki A., Savvides S.N., Hristova R., Van Beeumen J., Voelter W., Devreese B., Weser U., Di Muro P., Salvato B. & Stevanovic S. 2005a. Structure of hemocyanin subunit CaeSS2 of the crustacean Mediterranean crab Carcinus aestuarii.J. Biochem. 138: 303–312.10.1093/jb/mvi130Search in Google Scholar

Dolashka-Angelova P., Dolashki A., Stevanovic S., Hristova R., Atanasov B., Nikolov P. & Voelter W. 2005b. Structure and stability of arthropodan hemocyanin Limulus polyphemus. Spectrochim. Acta –Part A Mol. Biomol. Spectrosc. 61: 1207–1217.10.1016/j.saa.2004.06.043Search in Google Scholar

Dolashki A., Radkova M., Todorovska E., Ivanov M., Stevanovic S., Molin L., Traldi P., Voelter W. & Dolashka P. 2015. Structure and characterization of Eriphia verrucosa hemocyanin. Mar. Biotechnol. 17: 743–752.10.1007/s10126-015-9653-9Search in Google Scholar

Figueroa-Soto C.G., de la Barca A.M.C., Vazquez-Moreno L., Higuera-Ciapara I. & Yepiz-Plascencia G. 1997. Purification of hemocyanin from white shrimp (Penaeus vannamei Boone) by immobilized metal affinity chromatography. Comp. Biochem. Physiol. Part B Biochem Mol. Biol. 117: 203–208.10.1016/S0305-0491(96)00321-5Search in Google Scholar

Freimoser F.M., Jakob C.A., Aebi M. & Tuor U. 1999. The MTT [3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide] assay is a fast and reliable method for colorimetric determination of fungal cell densities. Appl. Environ. Microbiol. 65: 3727–3729.10.1128/AEM.65.8.3727-3729.1999Search in Google Scholar PubMed PubMed Central

García-Carreño F.L., Cota K. & Del Toro M.A.N. 2008. Phenoloxidase activity of hemocyanin in whiteleg shrimp Penaeus vannamei: conversion, characterization of catalytic properties, and role in postmortem melanosis. J. Agric. Food Chem. 56: 6454–6459.10.1021/jf800839xSearch in Google Scholar PubMed

Herbinière J., Braquart-Varnier C., Grève P., Strub J.M., Frère J., Van Dorsselaer A. & Martin G. 2005. Armadillidin: a novel glycine-rich antibacterial peptide directed against gram-positive bacteria in the woodlouse Armadillidium vulgare (Terrestrial Isopod, Crustacean). Dev. Comp. Immunol. 29: 489–499.10.1016/j.dci.2004.11.001Search in Google Scholar

Hoq M.I., Seraj M.U. & Chowdhury S. 2003. Isolation and characterization of antibacterial peptides from the mud-crab, Scylla serrata. Pakistan J. Biol. Sci. 6: 1345–1353.10.3923/pjbs.2003.1345.1353Search in Google Scholar

Horn E.C. & Kerr M.S. 1969. The hemolymph proteins of the blue crab, callinectes sapidus –I. Hemocyanins and certain other major protein constituents. Comp. Biochem. Physiol. 29: 493–508.10.1016/0010-406X(69)91602-8Search in Google Scholar

Huang W.S., Wang K.J., Yang M., Cai J.J., Li S.J. & Wang G.Z. 2006. Purification and part characterization of a novel antibacterial protein scygonadin, isolated from the seminal plasma of mud crab, Scylla serrata (Forskal, 1775). J. Exp. Mar. Biol. Ecol. 339:37–42.10.1016/j.jembe.2006.06.029Search in Google Scholar

Jayasankar V. & Subramoniam T. 1999. Antibacterial activity of seminal plasma of the mud crab Scylla serrata (Forskal). J. Exp. Mar. Biol. Ecol. 236: 253–259.10.1016/S0022-0981(98)00203-2Search in Google Scholar

Jayasree S. 2001. Biological properties of a natural agglutinin in the hemolymph of Indian white prawn, Penaeus indicus H. Milne Edwards. Aquaculture 194: 245–252.10.1016/S0044-8486(00)00528-7Search in Google Scholar

Jiravanichpaisal P., Lee S.Y., Kim Y.A., Andrén T. & Söderhäll I. 2007. Antibacterial peptides in hemocytes and hematopoietic tissue from freshwater crayfish Pacifastacus leniusculus:characterization and expression pattern. Dev. Comp. Immunol. 31: 441–455.10.1016/j.dci.2006.08.002Search in Google Scholar

Kawabata S.I., Tokunaga F., Kugi Y., Motoyama S., Miura Y., Hirata M. & Iwanaga S. 1996. Limulus factor D, a 43-kDa protein isolated from horseshoe crab hemocytes, is a serine protease homologue with antimicrobial activity. FEBS Lett. 398: 146–150.10.1016/S0014-5793(96)01224-0Search in Google Scholar

Kawabata T., Yasuhara Y., Ochiai M., Matsuura S. & Ashida M. 1995. Molecular cloning of insect pro-phenol oxidase: a copper-containing protein homologous to arthropod hemocyanin. Proc. Natl. Acad. Sci. USA 92:7774–7778.10.1073/pnas.92.17.7774Search in Google Scholar PubMed PubMed Central

Khoo L., Robinette D. & Noga E. 1999. Callinectin, an antibacterial peptide from blue crab, Callinectes sapidus, hemocytes. Mar. Biotechnol. 1: 44–51.10.1007/PL00011750Search in Google Scholar PubMed

Kingston H. & Jessie L. 1989. Introduction to microwave sample preparation: theory and practice. Anal. Chem. 61: 330A–330A.10.1021/ac00180a709Search in Google Scholar

Laemmli U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685.10.1038/227680a0Search in Google Scholar

Lamy J., Lamy J., Sizaret P.Y., Billiald P., Jolles P., Jolles J., Feldmann R.J. & Bonaventura J. 1983. Quaternary structure of Limulus polyphemus hemocyanin. Biochemistry 22:5573–5583.10.1021/bi00293a019Search in Google Scholar

Lee S.Y., Lee B.L. & Söderhäll K. 2003. Processing of an antibacterial peptide from hemocyanin of the freshwater crayfish Pacifastacus leniusculus. J. Biol. Chem. 278: 7927–7933.10.1074/jbc.M209239200Search in Google Scholar

Majumder M., Chattopadhyay T., Guha A.K. & Chatterjee B.P. 1997. Inhibition of bacterial respiration by a low-molecular weight lectin, scyllin, from Scylla serrata crab hemolymph. Indian J. Biochem. Biophys. 34: 87–89.Search in Google Scholar

Mangum C.P. & Greaves J. 1996. Hemocyanins of the genus Uca: structural polymorphisms and native oligomers. J. Exp. Mar. Biol. Ecol. 199: 1–15.10.1016/0022-0981(95)00154-9Search in Google Scholar

Markl J. & Decker H. 1992. Molecular structure of the arthropod hemocyanins. Adv. Comp. Environ. Physiol. 13: 325–376.10.1007/978-3-642-76418-9_12Search in Google Scholar

Martin J.L.M. 1975. Recherches sur le métabolisme des métaux chez les Crustacés décapodes marins?: leurs rapports avec la mue et la reproduction. Thèse doctorat: Sciences naturelles, Université d’Aix-Marseille 2.Search in Google Scholar

Maurer H.R. 1971. Disc Electrophoresis and Related Techniques of Polyacrylamide Gel Electrophoresis. Walter de Gruyter, Berlin, 222 pp.Search in Google Scholar

Meiyalagan V. & Arumugam M. 2015. Detection and preliminary characterization of antibacterial protein(s) in the serum of mud crab, Scylla serrata. Invertebrate Survival Journal 12: 287–295.Search in Google Scholar

Nagai T. & Kawabata S.I. 2000. A link between blood coagulation and prophenol oxidase activation in arthropod host defense. J. Biol. Chem. 275: 29264–29267.10.1074/jbc.M002556200Search in Google Scholar

Pan J.Y., Zhang Y.L., Wang S.Y. & Peng X.X. 2008. Dodecamer is required for agglutination of Litopenaeus vannamei hemocyanin with bacterial cells and red blood cells. Mar. Biotechnol. 10:645–652.10.1007/s10126-008-9115-8Search in Google Scholar

Paul R. & Pirow R. 1998. The physiological significance of respiratory proteins in invertebrates. Zool. (Jena) 100: 298–306.Search in Google Scholar

Pisuttharachai D., Yasuike M., Aono H., Yano Y., Murakami K., Kondo H., Aoki T. & Hirono I. 2009. Characterization of two isoforms of Japanese spiny lobster Panulirus japonicus defensin cDNA. Dev. Comp. Immunol. 33: 434–438.10.1016/j.dci.2008.11.007Search in Google Scholar

Redfield A.C., Coolidge T. & Mary AS. 1928. The respiratory proteins of the blood. I. The copper content and the minimal molecular weight of the hemocyanin of Limulus polyphemus. J. Biol. Chem. 76: 185–195.10.1016/S0021-9258(18)84119-9Search in Google Scholar

Rolland J.L., Abdelouahab M., Dupont J., Lefevre F., Bachère E. & Romestand B. 2010. Stylicins, a new family of antimicrobial peptides from the Pacific blue shrimp Litopenaeus stylirostris.Mol.Immunol. 47:1269–1277.10.1016/j.molimm.2009.12.007Search in Google Scholar

Schnapp D., Kemp G.D. & Smith V.J. 1996. Purification and characterization of a proline-rich antibacterial peptide, with sequence similarity to bactenecin-7, from the haemocytes of the shore crab, Carcinus maenas.Eur. J. Biochem. 240:532–539.10.1111/j.1432-1033.1996.0532h.xSearch in Google Scholar

Sheena N., Ajith T.A., Mathew A.T. & Janardhanan K.K. 2003. Antibacterial activity of three macrofungi, Ganoderma lucidum, Navesporus floccosa and Phellinus rimosus occurring in South India. Pharm. Biol. 41:564–567.10.1080/13880200390501226Search in Google Scholar

Smith V.J. & Chisholm J.R. 1992. Non-cellular immunity in crustaceans. Fish Shellfish Immunol. 2:1–31.10.1016/S1050-4648(06)80024-0Search in Google Scholar

Smith V.J. & Chisholm J.R. 2001. Antimicrobial proteins in crustaceans. Adv. Exp. Med. Biol. 484:95–112.10.1007/978-1-4615-1291-2_10Search in Google Scholar PubMed

Smith V.J., Fernandes J.M.O., Kemp G.D. & Hauton C. 2008. Crustins: enigmatic WAP domain-containing antibacterial proteins from crustaceans. Dev. Comp. Immunol. 32:758–772.10.1016/j.dci.2007.12.002Search in Google Scholar PubMed

Sperstad S.V., Haug T., Vasskog T. & Stensvåg K. 2009. Hyastatin, a glycine-rich multi-domain antimicrobial peptide isolated from the spider crab (Hyas araneus) hemocytes. Mol. Immunol. 46:2604–2612.10.1016/j.molimm.2009.05.002Search in Google Scholar PubMed

Stensvåg K., Haug T., Sperstad S.V., Rekdal Ø., Indrevoll B. & Styrvold O.B. 2008. Arasin 1, a proline-arginine-rich antimicrobial peptide isolated from the spider crab, Hyas araneus. Dev. Comp. Immunol. 32:275–285.10.1016/j.dci.2007.06.002Search in Google Scholar PubMed

Takagi T. & Nemoto T. 1980. Tachypleus tridentatus hemocyanin. Separation and characterization of monomer subunits and studies on sulfhydryl groups. J. Biochem. 87:1785–1793.10.1093/oxfordjournals.jbchem.a132923Search in Google Scholar PubMed

Tamura K., Stecher G., Peterson D., Filipski A. & Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30:2725–2729.10.1093/molbev/mst197Search in Google Scholar PubMed PubMed Central

Yan F., Zhang Y., Jiang R., Zhong M., Hu Z., Du H., Lun J., Chen J. & Li Y. 2011. Identification and agglutination properties of hemocyanin from the mud crab (Scylla serrata). Fish Shellfish Immunol. 30:354–360.10.1016/j.fsi.2010.11.004Search in Google Scholar PubMed

Yedery R.D. & Reddy K.V.R. 2009. Purification and characterization of antibacterial proteins from granular hemocytes of Indian mud crab, Scylla serrata. Acta Biochim. Pol. 56:71–82.10.18388/abp.2009_2518Search in Google Scholar

Zahri S., Nouri-Ganbalani G. & Agahi S. 2010. Hemocyanin subunits composition as a molecular marker for identification of intra-specific variations of Gammarus. J. Cell Mol. Res.2:56–60.Search in Google Scholar

Zhang Y., Yan F., Hu Z., Zhao X., Min S., Du Z., Zhao S., Ye X. & Li Y. 2009. Hemocyanin from shrimp Litopenaeus vannamei shows hemolytic activity. Fish Shellfish Immunol. 27:330–335.10.1016/j.fsi.2009.05.017Search in Google Scholar PubMed