Enzyme characterisation and gene expression profiling of Atlantic salmon chicken- and goose-type lysozymes

Developmental and Comparative Immunology

Volumn 40, Issue 1, 2013, Pages 11-19

  Myrnes, Bjørnar ^a   Seppola, Marit ^a   Johansen, Audny ^a   Øverbø, Kersti ^a   Callewaert, Lien ^b   Vanderkelen, Lise ^b   Michiels, Chris W ^b   Nilsen, Inge W ^a  

^a NOFIMA   (Norway)

^b LEUVEN FOOD SCIENCE AND NUTRITION RESEARCH CENTRE LFORCE   (Belgium)

Author keywords

Activity; Gene expression; Ivy; Lysozyme; PliG; Purification

Indexed keywords

CHICKEN TYPE LYSOZYME; DIVALENT CATION; GOOSE TYPE LYSOZYME; LIPOPOLYSACCHARIDE; LYSOZYME; MONOVALENT CATION; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; ATLANTIC SALMON; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; IN VITRO STUDY; MACROPHAGE; NONHUMAN; ORGAN DISTRIBUTION; PRIORITY JOURNAL; TEMPERATURE DEPENDENCE;

ANSER; BACTERIA (MICROORGANISMS); HEDERA; SALMO SALAR;

EID: 84875607536     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2013.01.010     Document Type: Article

References (44)

1. Bakkemo K.R., Mikkelsen H., Bordevik M., Torgersen J., Winther-Larsen H.C., Vanberg C., Olsen R., Johansen L.H., Seppola M. Intracellular localisation and innate immune responses following Francisella noatunensis infection of Atlantic cod (Gadus morhua) macrophages. Fish Shellfish Immunol. 2011, 31:993-1004.
2. Boland J.S., Davidson P.M., Bruce B., Weiss J. Cations reduce antimicrobial efficacy of lysozyme-chelator combinations. J. Food Prot. 2004, 67:285-294.
3. Callewaert L., Masschalck B., Deckers D., Nakimbugwe D., Atanassova M., Aertsen A., Michiels C.W. Purification of Ivy, a lysozyme inhibitor from Escherichia coli, and characterisation of its specificity for various lysozymes. Enzyme Microb. Technol. 2005, 37:205-211.
4. Callewaert L., Aertsen A., Deckers D., Vanoirbeek K.G.A., Vanderkelen L., Van Herreweghe J.M., Masschalck B., Nakimbugwe D., Robben J., Michiels C.W. A new family of lysozyme inhibitors contributing to lysozyme tolerance in Gram-negative bacteria. PLoS Pathog 2008, 4(3):e1000019. 10.1371/journal.ppat.1000019.
5. Callewaert L., Michiels C.W. Lysozymes in the animal kingdom. J. Biosci. 2010, 35:127-160.
6. Canfield R.E., McMurry S. Purification and characterization of a lysozyme from goose egg white. Biochem. Biophys. Res. Commun. 1967, 26:38-42.
7. Fernández-Trujilloa M.A., Portaam J., Manchadob M., Borregoc J.J., Alvareza M.C., Béjara J. C-Lysozyme from Senegalese sole (Solea senegalensis): cDNA cloning and expression pattern. Fish Shellfish Immunol. 2008, 25:697-700.
8. Fleming A. On a remarkable bacteriolytic element found in tissues and secretions. Proc. R. Soc. Lond. 1922, B39:306-317.
9. Gokam Y.R., Fesinmeyer R.M., Saluja A., Razinkov V., Chase S.F., Laue T.M., Brems D.N. Effective charge measurements reveal selective and preferential accumulation of anions, but not cations, at the protein surface in dilute salt solutions. Protein Sci. 2011, 20:580-587.
10. Hikima J., Hirono I., Aoki T. Characterization and expression of c-type lysozyme cDNA from Japanese flounder (Paralichthys olivaceus). Mol. Mar. Biol. Biotechnol. 1997, 6:339-344.
11. Hikima J., Minagawa S., Hirono I., Aoki T. Molecular cloning, expression and evolution of the Japanese flounder goose-type lysozyme gene, and the lytic activity of its recombinant protein. Biochim. Biophys. Acta 2001, 1520:35-44.
12. Ibrahim H.R. Insights into the structure-function relationship of ovalbumin, ovotransferrin and lysozyme. Hen Eggs: Their Basic and Applied Science 1997, 37-56. CRC Press Inc., New York, NY. T. Yamamoto, I.R. Juneja, H. Hatta, M. Kim (Eds.).
13. Jiménez-Cantizano R.M., Infante C., Martin-Antonio B., Ponce M., Hachero I., Navas J.I., Manchado M. Molecular characterization, phylogeny, and expression of c-type and g-type lysozymes in brill (Scophthalmus rhombus). Fish Shellfish Immunol. 2008, 25:57-65.
14. Jollès P. Lysozymes: Model Enzymes in Biochemistry and Biology 1996, Birkhäuser, Basel.
15. Jollès J., Jollès P. The lysozyme from Asterias rubens. Eur. J. Biochem. 1975, 54:19-23.
16. Julin K., Johansen L.H., Sommer A.I. Reference genes evaluated for use in infectious pancreatic necrosis virus real-time RT-qPCR assay applied during different stages of an infection. J. Virol. Methods. 2009, 162:30-39.
17. Kawamura S., Ohkuma M., Chijiiwa Y., Kohno D., Nakagawa H., Hirakawa H., Kuhara S., Torikata T. Role of disulfide bonds in goose-type lysozyme. FEBS J. 2008, 275:2818-2830.
18. Kyomuhendo P., Myrnes B., Nilsen I.W. A cold-active salmon goose-type lysozyme with high heat tolerance. Cell. Mol. Life Sci. 2007, 64:2841-2847.
19. Kyomuhendo P., Myrnes B., Brandsdal B.-O., Smalås A., Nilsen I.W., Helland R. Thermodynamics and structure of a salmon cold-active goose-type lysozyme. Comp. Biochem. Physiol. Part B. 2010, 156:254-263.
20. Kyomuhendo P., Nilsen I.W., Brandsdal B.O., Smalås A.O. Structural evidence for lack of inhibition of fish goose-type lysozymes by a bacterial inhibitor of lysozyme. J. Mol. Model. 2008, 14:777-788.
21. Larsen A.N., Solstad T., Svineng G., Seppola M., Jørgensen T.Ø. Molecular characterisation of a goose-type lysozyme gene in Atlantic cod (Gadus morhua L.). Fish Shellfish Immunol. 2008, 26:122-132.
22. Lie Ø., Evensen Ø., Sørensen A., Frøysadal E. Study on lysozyme activity in some fish species. Dis. Aquat. Org. 1989, 6:1-5.
23. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Methods 2001, 25:402-408.
24. Magnadóttir B. Innate immunity of fish. Fish Shellfish Immunol. 2006, 20:137-151.
25. Monchois V., Abergel C., Sturgis J., Jeudy S., Claverie J.M. Escherichia coli ykfE ORFan gene encodes a potent inhibitor of C-type lysozyme. J. Biol. Chem. 2001, 276:18437-18441.
26. Myrnes B., Johansen A. Recovery of lysozyme from scallop waste. Prep. Biochem. 1994, 24:69-80.
27. Nakimbugwe D., Masschalck B., Deckers D., Callewaert L., Aertsen A., Michiels C.W. Cell wall substrate specificity of six different lysozymes and lysozyme inhibitory activity of bacterial extracts. FEMS Microbiol. Lett. 2006, 259:41-46.
28. Nilsen I.W., Øverbø K., Sandsdalen E., Sandaker E., Sletten K., Myrnes B. Protein purification and gene isolation of chlamysin, a cold-active lysozyme-like enzyme with antibacterial activity. FEBS Lett. 1999, 464:153-158.
29. Nilsen I.W., Myrnes B., Edvardsen R., Chourrot D. Urochordates carry multiple genes for goose-type lysozyme and no genes for chicken- or invertebrate-type lysozymes. Cell. Mol. Life Sci. 2003, 60:2210-2218.
30. Paulsen S.M., Robertsen B., Engstad E. In vivo effects of β-glucan and LPS on lysozyme activity and mRNA expression in Atlantic salmon (Salmo salar L.). Fish Shellfish Immunol. 2003, 14:39-54.
31. Posse E., De Arcuri B.F., Morero R.D. Lysozyme interactions with phospholipid vesicles: relationships with fusion and release of aqueous content. Biochim. Biophys. Acta Biomembr. 1994, 1193:101-106.
32. Saurabh S., Sahoo P.K. Lysozyme: an important defence molecule of fish innate immune system. Aquaculture Res. 2008, 39:223-239.
33. Schnaitman C.A. Effect of ethylenediaminetetraacetic acid, Triton X-100, and lysozyme on the morphology and chemical composition of isolate cell walls of Escherichia coli. J. Bacteriol. 1971, 108:553-563.
34. Seppola M., Stenvik J., Steiro K., Solstad T., Robertsen B., Jensen I. Sequence and expression analysis of an interferon stimulated gene (ISG15) from Atlantic cod (Gadus morhua L.). Dev. Comp. Immunol. 2007, 31:156-171.
35. Sveinbjørnsson B., Olsen R., Paulsen S. Immunocytochemical localization of lysozyme in intestinal eosinophilic granule cells (EGCs) of Atlantic salmon, Salmo salar L. J. Fish Disease. 1996, 19:349-355.
36. Vanderkelen L., Van Herreweghe J.M., Vanoirbeek K.G.A., Baggerman G., Myrnes B., Declerck P.J., Nilsen I.W., Michiels C.W., Callewaert L. Identification of a bacterial inhibitor against g-type lysozyme. Cell. Mol. Life Sci. 2011, 68:1053-1064.
37. Van Herreweghe J.M., Vanderkelen L., Callewaert L., Aertsen A., Compernolle G., Declerck P.J., Michiels C.W. Lysozyme inhibitor conferring bacterial tolerance to invertebrate type lysozyme. Cell. Mol. Life Sci. 2010, 67:1177-1188.
38. Whang I., Lee Y., Lee S., Oh M.-J., Jung S.-J., Cho C.Y., Lee W.S., Kim H.S., Kim S.-J., Lee J. Characterization and expression analysis of a goose-type lysozyme from the rock bream Oplegnathus fasciatus, and antimicrobial activity of its recombinant protein. Fish Shellfish Immunol. 2011, 30:532-542.
39. Ye X., Zhang L., Tian Y., Tan A., Bai J., Li S. Identification and expression analysis of the g-type and c-type lysozymes in grass carp Ctenopharyngodon idellus. Dev. Comp. Immunol. 2010, 34:501-509.
40. Yin Z.X., He J.G., Deng W.X., Chan S.M. Molecular cloning, expression of orange-spotted grouper goose-type lysozyme cDNA, and lytic activity of its recombinant protein. Dis. Aquat. Org. 2003, 55:117-123.
41. Zhao L., Sun J.-s., Sun L. The g-type lysozyme of Scophthalmus maximus has a broad substrate spectrum and is involved in the immune response against bacterial infection. Fish Shellfish Immunol. 2011, 30:630-637.
42. Zheng W., Tian C., Chen X. Molecular characterization of goose-type lysozyme homologue of large yellow croaker and its involvement in immune response induced by trivalent bacterial vaccine as an acute-phase protein. Immunol. Lett. 2007, 113:107-116.
43. Zou H., Song L., Xu W., Yang G. Molecular cloning and characterization analysis of cDNA encoding g-type lysozyme from scallop (Argopecten irradians). High Tech. Lett. 2005, 15:101-106.
44. Zschörnig O., Paasche G., Thieme C., Korb N., Arnold K. Modulation of lysozyme charge influences interaction with phospholipid vesicles. Colloids Surf. B 2005, 42:69-78.