Abstract
Lysozymes are antibacterial enzymes widely distributed among organisms. Within the animal kingdom, mainly three major lysozyme types occur. Chicken (c)-type lysozyme and goose (g)-type lysozyme are predominantly, but not exclusively, found in vertebrate animals, while the invertebrate (i)-type lysozyme is typical for invertebrate organisms, and hence its name. Since their discovery in 1975, numerous research articles report on the identification of i-type lysozymes in a variety of invertebrate phyla. This review describes the current knowledge on i-type lysozymes, outlining their distribution, molecular mechanism and in vivo function taking the representative from Venerupis philippinarum (formerly Tapes japonica) (Vp-ilys) as a model. In addition, invertebrate g-type and ch-type (chalaropsis) lysozymes, which have been described in molluscs and nematodes, respectively, are also briefly discussed.
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Notes
Isopeptide bond: amide linkage between a carboxyl or carboxamide group of one amino acid and an amino group of another amino acid in which at least one of these groups is not on the amino acid α-carbon.
Imd pathway: Immune pathway primarly involved in defence against Gram-negative bacteria in Drosophila melanogaster.
Fat body: organ in insects similar in function to the vertebrate liver
Malphighian tubules: excretory and osmoregulatory organ of insects that opens near the junction of the midgut and hindgut.
Mesohyl: Gelatinous matrix within a sponge filling the space between the external pinacoderm (epidermis) and the internal choanoderm (cell layer that lines the inner central cavity of sponges).
References
Abergel C, Monchois V, Byrne D, Chenivesse S, Lembo F, Lazzaroni JC and Claverie JM 2007 Structure and evolution of the Ivy protein family, unexpected lysozyme inhibitors in Gram-negative bacteria. Proc. Natl. Acad. Sci. USA 104 6394–6399
Allam B and Paillard C 1998 Defense factors in clam extrapallial fluids. Dis. Aquat. Organ. 33 123–128
Allam B, Paillard C and Auffret M 2000 Alterations in hemolymph and extrapallial fluid parameters in the Manila clam, Ruditapes philippinarum, challenged with the pathogen Vibrio tapetis. J. Invertebr. Pathol. 76 63–69
Araujo CAC, Waniek PJ, Stock P, Mayer C, Jansen AM and Schaub GA 2006 Sequence characterization and expression patterns of defensin and lysozyme encoding genes from the gut of the reduviid bug Triatoma brasiliensis. Insect Biochem. Mol. Biol. 36 547–560
Bachali S, Jager M, Hassanin A, Schoentgen F, Jolles P, Fiala-Medioni A and Deutsch JS 2002 Phylogenetic analysis of invertebrate lysozymes and the evolution of lysozyme function. J. Mol. Evol. 54 652–664
Bailey K and Worboys B 1960 The lamellibranch crystalline style. Biochem. J. 76 487–491
Barnes RD 1982 Invertebrate zoology (Philadelphia: Saunders College)
Bedoya RJU, Mitzey AM, Obraztsova M and Lowenberger C 2005 Molecular cloning and transcriptional activation of lysozyme-encoding cDNAs in the mosquito Aedes aegypti. Insect Mol. Biol. 14 89–94
Bendtsen JD, Nielsen H, von Heijne G and Brunak S 2004 Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340 783–795
Bera A, Herbert S, Jakob A, Vollmer W and Götz F 2005 Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Mol. Microbiol. 55 778–787
Berman H, Henrick K and Nakamura H 2003 Announcing the worldwide Protein Data Bank. Nat. Struct. Biol. 10 980
Boehm M and Bonifacino JS 2001 Adaptins - The final recount. Mol. Biol. Cell 12 2907–2920
Boehnisch C, Wong D, Habig M, Isermann K, Michiels NK, Roeder T, May RC, Schulenburg H 2011 Protist-Type Lysozymes of the Nematode Caenorhabditis elegans Contribute to Resistance against Pathogenic Bacillus thuringiensis. PLoS One 6
Brown KL and Hancock REW 2006 Cationic host defense (antimicrobial) peptides. Curr. Opin. Immunol. 18 24–30
Callewaert L and Michiels CW 2010 Lysozymes in the animal kingdom. J. Biosci. 35 127–160
Callewaert L, Aertsen A, Deckers D, Vanoirbeek KG, Vanderkelen L, Van Herreweghe JM, Masschalck B, Nakimbugwe D, Robben J and Michiels CW 2008 A new family of lysozyme inhibitors contributing to lysozyme tolerance in gram-negative bacteria. PLoS Pathog. 4
Cancado FC, Effio PC, Terra WR and Marana SR 2008 Cloning, purification and comparative characterization of two digestive lysozymes from Musca domestica larvae. Braz. J. Med. Biol. Res. 41 969–977
Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V and Henrissat B 2009 The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 37 D233–238
Carballala MJ, Lópeza C, Azevedob C and Villalbaa A 1997 Enzymes involved in defense functions of hemocytes of mussel Mytilus galloprovincialis. J. Invertebr. Pathol. 70 96–105
Cong L, Yang X, Wang X, Tada M, Lu M, Liu H and Zhu B 2009 Characterization of an i-type lysozyme gene from the sea cucumber Stichopus japonicus, and enzymatic and nonenzymatic antimicrobial activities of its recombinant protein. J. Biosci. Bioeng. 107 583–588
Coyette J and van der Ende A 2008 Peptidoglycan: the bacterial Achilles heel. FEMS Microbiol. Rev. 32 147–148
Crooks G, Hon G, Chandonia J and Brenner S 2004 WebLogo: a sequence logo generator.. Genome Res. 14 1188–1190
Deckers D, Masschalck B, Aertsen A, Callewaert L, Van Tiggelen CGM, Atanassova M and Michiels CW 2004 Periplasmic lysozyme inhibitor contributes to lysozyme resistance in Escherichia coli. Cell. Mol. Life Sci. 61 1229–1237
Deckers D, Vanlint D, Callewaert L, Aertsen A and Michiels CW 2008 Role of the lysozyme inhibitor Ivy in growth or survival of Escherichia coli and Pseudomonas aeruginosa bacteria in hen egg white and in human saliva and breast milk. Appl. Environ. Microbiol. 74 4434–4439
Demain AL and Vaishnav P 2009 Production of recombinant proteins by microbes and higher organisms. Biotechnol. Adv. 27 297–306
DeMaio J, Pumpuni CB, Kent M and Beier JC 1996 The midgut bacterial flora of wild Aedes triseriatus, Culex pipiens, and Psorophora columbiae mosquitoes. Am. J. Trop. Med. Hyg. 54 219–223
Ding J, Li J, Bao Y, Li L, Wu F and Zhang G 2011 Molecular characterization of a mollusk chicken-type lysozyme gene from Haliotis discus hannai Ino, and the antimicrobial activity of its recombinant protein. Fish Shellfish Immunol. 30 163–172
Du Pasquier L 2006 Germline and somatic diversification of immune recognition elements in Metazoa. Immunol. Lett. 104 2–17
Dunn PE and Dai W 1990 Bacterial peptidoglycan: A signal for initiation of the bacteria regulated synthesis and secretion of lysozyme in Manduca sexta. Defense Molecules 121 33–46
Dunn C, Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, et al. 2008 Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452 745–749
Dziarski R and Gupta D 2006 The peptidoglycan recognition proteins (PGRPs). Genome Biol. 7 232–245
Felsenstein J 1985 Confidence-limits on phylogenies- and approach using the bootstrap. Evolution 39 783–791
Fouche PB and Hash JH 1978 The N,O-diacetylmuramidase of Chalaropsis species. Identificaiton of aspartyl and glutamyl residues in the active site. J. Biol. Chem. 253 6787–6793
Fradkov A, Berezhnoy S, Barsova E, Zavalova L, Lukyanov S, Baskova I and Sverdlov E 1996 Enzyme from the medicinal leech (Hirudo medicinalis) that specifically splits endo-epsilon(−gamma-Glu)-Lys isopeptide bonds: cDNA cloning and protein primary structure. FEBS Lett. 390 145–148
Fujimoto S, Toshimori-Tsuda I, Kishimoto K, Yamano Y and Morishima I 2001 Protein purification, cDNA cloning and gene expression of lysozyme from eri-silkworm, Samia cynthia ricini. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 128 709–718
Fujita A, Minamoto T, Shimizu I and Abe T 2002 Molecular cloning of lysozyme-encoding cDNAs expressed in the salivary gland of a wood-feeding termite, Reticulitermes speratus. Insect Biochem. Mol. Biol. 32 1615–1624
Gao Y and Fallon AM 2000 Immune activation upregulates lysozyme gene expression in Aedes aegypti mosquito cell culture. Insect Mol. Biol. 9 553–558
Goto T, Abe Y, Kakuta Y, Takeshita K, Imoto T and Ueda T 2007 Crystal structure of Tapes japonica lysozyme with substrate analogue - Structural basis of the catalytic mechanism and manifestation of its chitinase activity accompanied by quaternary structural change. J. Biol. Chem. 282 27459–27467
Grunclova L, Fouquier H, Hypsa V and Kopacek P 2003 Lysozyme from the gut of the soft tick Ornithodoros moubata: the sequence, phylogeny and post-feeding regulation. Dev. Comp. Immunol. 27 651–660
Hikima S, Hikima J, Rojtinnakorn J, Hirono I and Aoki T 2003 Characterization and function of kuruma shrimp lysozyme possessing lytic activity against Vibrio species. Gene 316 187–195
Horiuchi S and Lane CE 1965 Digestive enzymes of crystalline style of Strombus gigas linné. I. Cellulase and some other carbohydrases. Biol. Bull. 129 273–281
Hultmark D 1996 Insect lysozymes; in Lysozymes: model enzymes in biochemistry and biology (ed) P Jollès (Basel: Birkhäuser Verlag) pp 87–102
Ito Y, Yoshikawa A, Hotani T, Fukuda S, Sugimura K and Imoto T 1999 Amino acid sequences of lysozymes newly purified from invertebrates imply wide distribution of a novel class in the lysozyme family. Eur. J. Biochem. 259 456–461
Itoh N and Takahashi K 2007 cDNA cloning and in situ hybridization of a novel lysozyme in the Pacific oyster, Crassostrea gigas.. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 148 160–166
Itoh N and Takahashi KG 2009 A novel peptidoglycan recognition protein containing a goose-type lysozyme domain from the Pacific oyster, Crassostrea gigas. Mol. Immunol. 46 1768–1774
Itoh N, Okada Y, Takahashi K and Osada M 2010 Presence and characterization of multiple mantle lysozymes in the Pacific oyster, Crassostrea gigas. Fish Shellfish Immunol. 29 126–135
Jollès J and Jollès P 1975 The lysozyme from Asterias rubens. Eur. J. Biochem. 54 19–23
Jolles J, Schoentgen F, Croizier G, Croizier L and Jolles P 1979 Insect lysozymes from 3 species of lepidoptera: Their structural relatedness to the c-(chicken)-type lysozyme. J. Mol. Evol. 14 267–271
Josková R, Silerová M, Procházková P and Bilej M 2009 Identification and cloning of an invertebrate-type lysozyme from Eisenia andrei. Dev. Comp. Immunol. 33 932–938
Kang DW, Romans P and Lee JY 1996 Analysis of a lysozyme gene from the malaria vector mosquito, Anopheles gambiae. Gene 174 239–244
Kikuchi Y and Graf J 2007 Spatial and temporal population dynamics of a naturally occurring two-species microbial community inside the digestive tract of the medicinal leech. Appl. Environ. Microbiol. 73 1984–1991
Kirby AJ 2001 The lysozyme mechanism sorted - after 50 years. Nat. Struct. Biol. 8 737–739
Kollien AH, Fechner S, Waniek PJ and Schaub GA 2003 Isolation and characterization of a cDNA encoding for a lysozyme from the gut of the reduviid bug Triatoma infestans. Arch. Insect Biochem. Physiol. 53 134–145
Kyomuhendo P, Myrnes B and Nilsen I 2007 A cold-active salmon goose-type lysozyme with high heat tolerance. Cell. Mol. Life Sci. 64 2841–2847
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, et al. 2007 Clustal W and Clustal X version 2.0. Bioinformatics 23 2947–2948
Lee WJ and Brey PT 1995 Isolation and characterization of the lysozyme encoding gene from the silkworm Bombyx mori. Gene 161 199–203
Leippe M 1999 Antimicrobial and cytolytic polypeptides of amoeboid protozoa-effector molecules of primitive phagocytes. Dev. Comp. Immunol. 23 267–279
Leysen S, Van Herreweghe JM, Callewaert L, Heirbaut M, Buntinx P, Michiels CW and Strelkov SV 2011 Molecular Basis of bacterial defense against host lysozymes: x-ray structures of periplasmic lysozyme inhibitors PliI and PliC. J. Mol. Biol. 405 1233–1245
Li B, Calvo E, Marinotti O, James AA and Paskewitz SM 2005 Characterization of the c-type lysozyme gene family in Anopheles gambiae. Gene 360 131–139
Mallo GV, Kurz CL, Couillault C, Pujol N, Granjeaud S, Kohara Y and Ewbank JJ 2002 Inducible antibacterial defense system in C. elegans. Curr. Biol. 12 1209–1214
Marsh EK, van den Berg MCW and May RC 2011 A Two-Gene Balance Regulates Salmonella Typhimurium Tolerance in the Nematode Caenorhabditis elegans. PLoS One 6 7
Matsumoto T, Nakamura AM and Takahashi KG 2006 Cloning of cDNAs and hybridization analysis of lysozymes from two oyster species, Crassostrea gigas and Ostrea edulis. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 145 325–330
McHenery J and Birkbeck T 1982 Characterization of the lysozyme of Mytilus edulis (L). Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 71 583–589
McHenery JG, Birkbeck TH and Allen JA 1979 Occurrence of lysozyme in marine bivalves. Comp. Biochem. Physiol. B, Biochem. Mol. Biol.63 25–28
Miyauchi K, Matsumiya M and Mochizuki A 2006 Purification and characterization of lysozyme from purple washington clam Saxidomus purpurata. Fish. Sci. 72 1300–1305
Monchois V, Abergel C, Sturgis J, Jeudy S and Claverie J 2001 Escherichia coli ykfE ORFan gene encodes a potent inhibitor of C-type lysozyme.. J. Biol. Chem. 276 18437–18441
Moreira-Ferro CK, Daffre S, James AA and Marinotti O 1998 A lysozyme in the salivary glands of the malaria vector Anopheles darlingi. Insect Mol. Biol. 7 257–264
Morton B. 1983. Feeding and digestion in Bivalvia; in The mollusca vol 5 part 2 (eds) ASM Saleuddin and KM Wilbur (New York: Academic Press)
Moynihan P and Clarke A 2010 O-acetylation of peptidoglycan in gram-negative bacteria: identification and characterization of peptidoglycan O-acetyltransferase in Neisseria gonorrhoeae. J. Biol. Chem. 285 13264–13273
Mulnix AB and Dunn PE 1994 Structure and induction of a lysozyme gene from the tobacco hornworm, Manduca sexta. Insect Biochem. Mol. Biol. 24 271–281
Nandakumar M and Tan M-W 2008 Gamma-linolenic and stearidonic acids are required for basal immunity in caenorhabditis elegans through their effects on p38 MAP kinase activity. PLoS Genet. 4 e1000273
Nilsen I, Overbø K, Sandsdalen E, Sandaker E, Sletten K and Myrnes B 1999 Protein purification and gene isolation of chlamysin, a cold-active lysozyme-like enzyme with antibacterial activity. FEBS Lett. 464 153–158
Olsen OM, Nilsen IW, Sletten K and Myrnes B 2003 Multiple invertebrate lysozymes in blue mussel (Mytilus edulis). Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 136 107–115
O'Rourke D, Baban D, Demidova M, Mott R and Hodgkin J 2006 Genomic clusters, putative pathogen recognition molecules, and antimicrobial genes are induced by infection of C. elegans with M. nematophilum. Genome Res. 16 1005–1016
Paskewitz SM, Li B and Kajla MK 2008 Cloning and molecular characterization of two invertebrate-type lysozymes from Anopheles gambiae. Insect Mol. Biol. 17 217–225
Phillips DC 1966 Crystallographic studies of enzyme properties of lysozyme. Acta Crystallogr. S 21 A163
Prager EM 1996 Adaptive evolution of lysozyme: changes in amino acid sequence, regulation of expression and gene number; in Lysozymes: model enzymes in biochemistry and biology (ed) P Jollès (Basel: Birkhäuser Verlag) pp 323–334
Rau A, Hogg T, Marquardt R and Hilgenfeld R 2001 A new lysozyme fold. Crystal structure of the muramidase from Streptomyces coelicolor at 1.65 A resolution. J. Biol. Chem. 276 31994–31999
Ren Q, Zhao XF and Wang JX 2009 Molecular characterization and expression analysis of a chicken-type lysozyme gene from housefly (Musca domestica). J. Genet. Genomics. 36 7–16
Russell VW and Dunn PE 1991 Lysozyme in the midgut of Manduca sexta during metamorphosis. Arch. Insect Biochem. Physiol. 17 67–80
Saitou N and Nei M 1987 The neighbor joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4 406–425
Schulenburg H and Boehnisch C 2008 Diversification and adaptive sequence evolution of Caenorhabditis lysozymes (Nematoda: Rhabditidae). BMC Evol. Biol. 8 114 doi: 10.1186/1471–2148–1188–1114
Schulenburg H, Boehnisch C and Michiels NK 2007 How do invertebrates generate a highly specific innate immune response? Mol. Immunol. 44 3338–3344
Schulenburg H, Hoeppner MP, Weiner J and Bornberg-Bauer E 2008 Specificity of the innate immune system and diversity of C-type lectin domain (CTLD) proteins in the nematode Caenorhabditis elegans. Immunobiology 213 237–250
Simonsen KT, Moller-Jensen J, Kristensen AR, Andersen JS, Riddle DL and Kallipolitis BH 2011 Quantitative proteomics identifies ferritin in the innate immune response of C. elegans. Virulence 2 120–130
Strynadka NC and James MN 1996 Lysozyme: a model enzyme in protein crystallography; in Lysozymes: model enzymes in biochemistry and biology (ed) P Jollès (Basel: Birkhäuser Verlag) pp 185–222
Sun SC, Asling B and Faye I 1991 Organization and expression of the immunoresponsive lysozyme gene in the giant silk moth, Hyalophora cecropia. J. Biol. Chem. 266 6644–6649
Supungul P, Rimphanitchayakit V, Aoki T, Hirono I and Tassanakajon A 2010 Molecular characterization and expression analysis of a c-type and two novel muramidase-deficient i-type lysozymes from Penaeus monodon. Fish Shellfish Immunol. 28 490–498
Takeshita K, Hashimoto Y, Ueda T and Imoto T 2003 A small chimerically bifunctional monomeric protein: Tapes japonica lysozyme. Cell. Mol. Life Sci. 60 1944–1951
Takeshita K, Hashimoto Y, Thujihata Y, So T, Ueda T and Iomoto T 2004 Determination of the complete cDNA sequence, construction of expression systems, and elucidation of fibrinolytic activity for Tapes japonica lysozyme. Protein Expr. Purif. 36 254–262
Talley K and Alexov E 2010 On the pH-optimum of activity and stability of proteins. Proteins. 78 2699–2706
Tamura K, Dudley J, Nei M and Kumar S 2007 MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24 1596–1599
Thakur NL, Perovic-Ottstadt S, Batel R, Korzhev M, Diehl-Seifert B, Muller IM and Muller WEG 2005 Innate immune defense of the sponge Suberites domuncula against gram-positive bacteria: induction of lysozyme and AdaPTin. Mar. Biol. 146 271–282
Van Herreweghe JM, Vanderkelen L, Callewaert L, Aertsen A, Compernolle G, Declerck PJ and Michiels CW 2010 Lysozyme inhibitor conferring bacterial tolerance to invertebrate type lysozyme. Cell. Mol. Life Sci. 67 1177–1188
Vanderkelen L, Van Herreweghe JM, Vanoirbeek KG, Baggerman G, Myrnes B, Declerck PJ, Nilsen IW, Michiels CW and Callewaert L 2010 Identification of a bacterial inhibitor against g-type lysozyme. Cell. Mol. Life Sci. 68 1053–1064
Vocadlo DJ, Davies GJ, Laine R and Withers SG 2001 Catalysis by hen egg-white lysozyme proceeds via a covalent intermediate. Nature 412 835–838
Voet A, Callewaert L, Ulens T, Vanderkelen L, Vanherreweghe JM, Michiels CW and De Maeyer M 2011 Structure based discovery of small molecule suppressors targeting bacterial lysozyme inhibitors. Biochem. Biophys. Res. Commun. 405 527–532
Waniek PJ, Mendonca-Lima L, Menezes GB, Jansen AM and Araujo CAC 2009 Recombinant expression and characterization of a lysozyme from the midgut of Triatoma brasiliensis (Hemiptera, Reduviidae) in comparison with intestinal muramidase activity. Physiol. Entomol. 34 309–317
Wohlkönig A, Huet J, Looze Y and Wintjens R 2010 Structural relationships in the lysozyme superfamily: significant evidence for glycoside hydrolase signature motifs.. PLoS ONE 5 e15388
Worm Sequencing Consortium 1998 Genome sequence of the nematode C. elegans: A platform for investigating biology. Science 282 2012–2018
Xue QG, Schey KL, Volety AK, Chu FL E and La Peyre JF 2004 Purification and characterization of lysozyme from plasma of the eastern oyster (Crassostrea virginica). Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 139 11–25
Xue Q, Itoh N, Schey K, Li Y, Cooper R and La Peyre J 2007 A new lysozyme from the eastern oyster (Crassostrea virginica) indicates adaptive evolution of i-type lysozymes.. Cell. Mol. Life Sci. 64 82–95
Xue Q, Hellberg M, Schey K, Itoh N, Eytan R, Cooper R and La Peyre J 2010 A new lysozyme from the eastern oyster, Crassostrea virginica, and a possible evolutionary pathway for i-type lysozymes in bivalves from host defense to digestion. BMC Evol. Biol. 10 213
Yum S, Kim MJ, Xu Y, Jin XL, Yoo HY, Park JW, Gong JH, Choe KM, Lee BL and Ha NC 2009 Structural basis for the recognition of lysozyme by MliC, a periplasmic lysozyme inhibitor in Gram-negative bacteria. Biochem. Biophys. Res. Commun. 378 244–248
Zavalova L, Lukyanov S, Baskova I, Snezhkov E, Akopov S, Berezhnoy S, Bogdanova E, Barsova E, Sverdlov ED 1996 Genes from the medicinal leech (Hirudo medicinalis) coding for unusual enzymes that specifically cleave endo-epsilon(gamma-Glu)-Lys isopeptide bonds and help to dissolve blood clots. Mol. Gen. Genet. 253 20–25
Zavalova LL, Baskova IP, Lukyanov SA, Sass AV, Snezhkov EV, Akopov SB, Artamonova II, Archipova VS, et al. 2000 Destabilase from the medicinal leech is a representative of a novel family of lysozymes. Biochim. Biophys. Acta 1478 69–77
Zhang Y, Huang JH, Zhou B, Zhang CL, Liu WB, Miao XX and Huang YP 2009 Upregulation of lysozyme gene expression during metamorphosis and immune challenge of the cotton bollworm, Helicover armigera. Arch. Insect Biochem. Physiol. 70 18–29
Zhang H, Sun C, Sun S, Zhao X and Wang J 2010 Functional analysis of two invertebrate-type lysozymes from red swamp crayfish, Procambarus clarkii. Fish Shellfish Immunol. 29 1066–1072
Zhao J, Song L, Li C, Zou H, Ni D, Wang W and Xu W 2007 Molecular cloning of an invertebrate goose-type lysozyme gene from Chlamys farreri, and lytic activity of the recombinant protein. Mol. Immunol. 44 1198–1208
Zhao JM, Qiu LH, Ning XX, Chen AQ, Wu HF and Li CH 2010 Cloning and characterization of an invertebrate type lysozyme from Venerupis philippinarum. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 156 56–60
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[Van Herreweghe JM and Michiels CW 2012 Invertebrate lysozymes: Diversity and distribution, molecular mechanism and in vivo function. J. Biosci. 37 1–22] DOI 10.1007/s12038-012-9201-y
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Van Herreweghe, J.M., Michiels, C.W. Invertebrate lysozymes: Diversity and distribution, molecular mechanism and in vivo function. J Biosci 37, 327–348 (2012). https://doi.org/10.1007/s12038-012-9201-y
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DOI: https://doi.org/10.1007/s12038-012-9201-y