BMC Evolutionary Biology | |
Evolution of the vertebrate goose-type lysozyme gene family | |
David M Irwin1  | |
[1] Department of Laboratory Medicine and Pathobiology, Faculty of Medicine, University of Toronto, 1 King’s College Circle, Toronto M5S 1A8, Ontario, Canada | |
关键词: Phylogeny; Genome evolution; Gene duplication; Vertebrates; Lysozyme g; | |
Others : 1117977 DOI : 10.1186/s12862-014-0188-x |
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received in 2014-04-20, accepted in 2014-08-12, 发布年份 2014 | |
【 摘 要 】
Background
Lysozyme g is an antibacterial enzyme that was first found in the eggs of some birds, but recently has been found in additional species, including non-vertebrates. Some previously characterized lysozyme g sequences are suggested to have altered secretion potential and enzymatic activity, however the distribution of these altered sequences is unknown. Duplicated copies of the lysozyme g gene exist in some species; however, the origins of the duplicates and their roles in altered function are unclear.
Results
We identified 234 lysozyme g sequences from 118 vertebrate species, including 181 sequences that are full or near full length representing all vertebrate classes except cartilaginous fish. Phylogenetic analysis shows that most lysozyme g gene duplicates are recent or lineage specific events, however three amplification events are more ancient, those in an early amniote, an early mammal, and an early teleost. The older gene duplications are associated with changes in function, including changes in secretion potential and muramidase antibacterial enzymatic activity.
Conclusions
Lysozyme g is an essential muramidase enzyme that is widespread in vertebrates. Duplication of the lysozyme g gene, and the retention of non-secreted isozymes that have lost enzymatic activity indicate that lysozyme g has an activity other than the muramidase activity associated with being an antibacterial enzyme.
【 授权许可】
2014 Irwin; licensee BioMed Central Ltd
【 预 览 】
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20150206014351679.pdf | 627KB | download | |
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Figure 2. | 87KB | Image | download |
Figure 1. | 80KB | Image | download |
【 图 表 】
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【 参考文献 】
- [1]Karplus M, Post CB: Simulations of Lysozyme: Internal Motions and the Reaction Mechanism. In Lysozymes: Model Enzymes in Biochemistry Andmolecular Biology. Edited by Jollès P. Birkhäuser Verlag, Basel; 1996:111-141.
- [2]Fukamizo T: Chitinolytic enzymes: catalysis, substrate binding, and their application. Curr Protein Pept Sci 2000, 1:105-124.
- [3]Strynadka NC, James MN: Lysozyme: A Model Enzyme in Protein Crystallography. In Lysozymes: Model Enzymes in Biochemistry and Molecular Biology. Edited by Jollès P. Birkhäuser Verlag, Basel; 1996:185-222.
- [4]Matagne A, Dobson CM: The folding process of hen lysozyme: a perspective from the ‘new view’. Cell Mol Life Sci 1998, 54:363-371.
- [5]Merlini G, Bellotti V: Lysozyme: a paradigmatic molecule for the investigation of protein structure, function and misfolding. Clin Chim Acta 2005, 357:168-172.
- [6]Bonifer C, Huber MC, Faust N, Sippel AE: Regulation of the chicken lysozyme locus in transgenic mice. Crit Rev Eukaryot Gene Expr 1996, 6:285-297.
- [7]Bonifer C, Jägle U, Huber MC: The chicken lysozyme locus as a paradigm for the complex developmental regulation of eukaryotic gene loci. J Biol Chem 1997, 272:26075-26080.
- [8]McKenzie HA, White FH Jr: Lysozyme and alpha-lactalbumin: structure, function, and interrelationships. Adv Protein Chem 1991, 41:173-315.
- [9]Prager EM, Jollès P: Animal Lysozymes c and g: An Overview. In Lysozymes: Model Enzymes in Biochemistry and Molecular Biology. Edited by Jollès P. Birkhäuser Verlag, Basel; 1996:9-31.
- [10]Qasba PK, Kumar S: Molecular divergence of lysozymes and alpha-lactalbumin. Crit Rev Biochem Mol Biol 1997, 32:255-306.
- [11]Callewaert L, Michiels CW: Lysozymes in the animal kingdom. J Biosci 2010, 35:127-160.
- [12]Irwin DM, Biegel JM, Stewart CB: Evolution of the mammalian lysozyme gene family. BMC Evol Biol 2011, 11:166. BioMed Central Full Text
- [13]Jollès P, Jollès J: What’s new in lysozyme research? Always a model system, today as yesterday. Mol Cell Biochem 1984, 63:165-189.
- [14]Weaver LH, Grütter MG, Remington SJ, Gray TM, Isaacs NW, Matthews BW: Comparison of goose-type, chicken-type, and phage-type lysozymes illustrates the changes that occur in both amino acid sequence and three-dimensional structure during evolution. J Mol Evol 1984–1985, 21:97-111.
- [15]Van Herreweghe JM, Michiels CW: Invertebrate lysozymes: diversity and distribution, molecular mechanism and in vivo function. J Biosci 2012, 37:327-348.
- [16]Beintema JJ, Terwisscha Van Scheltinga AC: Plant Lysozymes. In Lysozymes: Model Enzymes in Biochemistry and Molecular Biology. Edited by Jollès P. Birkhäuser Verlag, Basel; 1996:75-86.
- [17]Höltje JV: Bacterial Lysozymes. In Lysozymes: Model Enzymes in Biochemistry and Molecular Biology. Edited by Jollès P. Birkhäuser Verlag, Basel; 1996:65-74.
- [18]Fischetti VA: Bacteriophage lytic enzymes: novel anti-infectives. Trends Microbiol 2005, 13:491-496.
- [19]Grütter MG, Weaver LH, Matthews BW: Goose lysozyme structure: an evolutionary link between hen and bacteriophage lysozymes? Nature 1983, 303:828-831.
- [20]Monzingo AF, Marcotte EM, Hart PJ, Robertus JD: Chitinases, chitosanases, and lysozymes can be divided into procaryotic and eucaryotic families sharing a conserved core. Nat Struct Biol 1996, 3:133-140.
- [21]Canfield RE, McMurry S: Purification and characterization of a lysozyme from goose egg white. Biochem Biophys Res Commun 1967, 26:38-42.
- [22]Prager EM, Wilson AC, Arnheim N: Widespread distribution of lysozyme g in egg white of birds. J Biol Chem 1974, 249:7295-7297.
- [23]Hindenburg A, Spitznagel J, Arnheim N: Isozymes of lysozyme in leukocytes and egg white: evidence for the species-specific control of egg-white lysozyme synthesis. Proc Natl Acad Sci U S A 1974, 71:1653-1657.
- [24]Nakano T, Graf T: Goose-type lysozyme gene of the chicken: sequence, genomic organization and expression reveals major differences to chicken-type lysozyme gene. Biochim Biophys Acta 1991, 1090:273-276.
- [25]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.
- [26]Yin ZX, He JG, Deng WX, Chan SM: Molecular cloning, expression of orange-spotted grouper goose-type lysozyme cDNA, and lytic activity of its recombinant protein. Dis Aquat Organ 2003, 55:117-123.
- [27]Sakai M, Kono T, Savan R: Identification of expressed genes in carp (Cyprinus carpio) head kidney cells after in vitro treatment with immunostimulants. Dev Biol (Basel) 2005, 121:45-51.
- [28]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.
- [29]Irwin DM, Gong Z: Molecular evolution of vertebrate goose-type lysozyme genes. J Mol Evol 2003, 56:234-242.
- [30]Kyomuhendo P, Myrnes B, Nilsen IW: A cold-active salmon goose-type lysozyme with high heat tolerance. Cell Mol Life Sci 2007, 64:2841-2847.
- [31]Nile CJ, Townes CL, Michailidis G, Hirst BH, Hall J: Identification of chicken lysozyme g2 and its expression in the intestine. Cell Mol Life Sci 2004, 61:2760-2766.
- [32]Nilsen IW, Myrnes B, Edvardsen RB, Chourrout 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.
- [33]Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
- [34][http://www.ensembl.org/index.html] webcite ᅟ: Ensembl Genome Browser. ᅟ []
- [35][http://pre.ensembl.org/index.html] webcite ᅟ: Ensembl Pre-release Genome Browser. ᅟ []
- [36][http://www.ncbi.nlm.nih.gov/] webcite ᅟ: National Center for Biotechnology Information. ᅟ []
- [37]Bailey JA, Eichler EE: Primate segmental duplications: crucibles of evolution, diversity and disease. Nat Rev Genet 2006, 7:552-564.
- [38]Meyer A, Wilson AC: Origin of tetrapods inferred from their mitochondrial DNA affiliation to lungfish. J Mol Evol 1990, 31:359-364.
- [39]Gorr T, Kleinschmidt T, Fricke H: Close tetrapod relationships of the coelacanth Latimeria indicated by haemoglobin sequences. Nature 1991, 351:394-397.
- [40]Venkatesh B, Lee AP, Ravi V, Maurya AK, Lian MM, Swann JB, Ohta Y, Flajnik MF, Sutoh Y, Kasahara M, Hoon S, Gangu V, Roy SW, Irimia M, Korzh V, Kondrychyn I, Lim ZW, Tay BH, Tohari S, Kong KW, Ho S, Lorente-Galdos B, Quilez J, Marques-Bonet T, Raney BJ, Ingham PW, Tay A, Hillier LW, Minx P, Boehm T, et al.: Elephant shark genome provides unique insights into gnathostome evolution. Nature 2014, 505:174-179.
- [41][http://www.ncbi.nlm.nih.gov/unigene] webcite ᅟ: NCBI UniGene Database. ᅟ []
- [42]Katoh K, Misawa K, Kuma K, Miyata T: MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002, 30:3059-3066.
- [43]Penn O, Privman E, Ashkenazy H, Landan G, Graur D, Pupko T: GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Res 2010, 38:W23-W28.
- [44]Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP: Bayesian inference of phylogeny and its impact on evolutionary biology. Science 2001, 294:2310-2314.
- [45]Felsenstein J: Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981, 17:368-376.
- [46]Cameron CB, Garey JR, Swalla BJ: Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla. Proc Natl Acad Sci U S A 2000, 97:4469-4474.
- [47]Meyer A, Van de Peer Y: From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 2005, 27:937-945.
- [48]Thammasirirak S, Pukcothanung Y, Preecharram S, Daduang S, Patramanon R, Fukamizo T, Araki T: Antimicrobial peptides derived from goose egg white lysozyme. Comp Biochem Physiol 2010, 151C:84-91.
- [49]Petersen TN, Brunak S, Von Heijne G, Nielsen H: SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011, 8:785-786.
- [50]Nickel W: Pathways of unconventional protein secretion. Curr Opin Biotechnol 2010, 21:621-626.
- [51]Bendtsen JD, Jensen LJ, Blom N, Von Heijne G, Brunak S: Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng Des Sel 2004, 17:349-356.
- [52]Mandal A, Klotz KL, Shetty J, Jayes FL, Wolkowicz MJ, Bolling LC, Coonrod SA, Black MB, Diekman AB, Haystead TA, Flickinger CJ, Herr JC: SLLP1, a unique, intra-acrosomal, non-bacteriolytic, c lysozyme-like protein of human spermatozoa. Biol Reprod 2003, 68:1525-1537.
- [53]Zhang K, Gao R, Zhang H, Cai X, Shen C, Wu C, Zhao S, Yu L: Molecular cloning and characterization of three novel lysozyme-like genes, predominantly expressed in the male reproductive system of humans, belonging to the c-type lysozyme/alpha-lactalbumin family. Biol Reprod 2005, 73:1064-1071.
- [54]Kawamura S, Ohno K, Ohkuma M, Chijiiwa Y, Torikata T: Experimental verification of the crucial roles of Glu73 in the catalytic activity and structural stability of goose type lysozyme. J Biochem 2006, 140:75-85.
- [55]Hirakawa H, Ochi A, Kawahara Y, Kawamura S, Torikata T, Kuhara S: Catalytic reaction mechanism of goose egg-white lysozyme by molecular modelling of enzyme-substrate complex. J Biochem 2008, 144:753-761.
- [56]Helland R, Larsen RL, Finstad S, Kyomuhendo P, Larsen AN: Crystal structures of g-type lysozyme from Atlantic cod shed new light on substrate binding and the catalytic mechanism. Cell Mol Life Sci 2009, 66:2585-2598.
- [57]Castoe TA, De Koning AP, Hall KT, Card DC, Schield DR, Fujita MK, Ruggiero RP, Degner JF, Daza JM, Gu W, Reyes-Velasco J, Shaney KJ, Castoe JM, Fox SE, Poole AW, Polanco D, Dobry J, Vandewege MW, Li Q, Schott RK, Kapusta A, Minx P, Feschotte C, Uetz P, Ray DA, Hoffmann FG, Bogden R, Smith EN, Chang BS, Vonk FJ, et al.: The Burmese python genome reveals the molecular basis for extreme adaptation in snakes. Proc Natl Acad Sci U S A 2013, 110:20645-20650.
- [58][http://pipmaker.bx.psu.edu/pipmaker/] webcite ᅟ: PipMaker and MultiPipMaker. ᅟ []
- [59]Schwartz S, Zhang Z, Frazer KA, Smit A, Riemer C, Bouck J, Gibbs R, Hardison R, Miller W: PipMaker–a web server for aligning two genomic DNA sequences. Genome Res 2000, 10:577-586.
- [60]Schwartz S, Elnitski L, Li M, Weirauch M, Riemer C, Smit A, Green ED, Hardison RC, Miller W: MultiPipMaker and supporting tools: alignments and analysis of multiple genomic DNA sequences. Nucleic Acids Res 2003, 31:3518-3524.
- [61]Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP: MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 2012, 61:539-542.
- [62]Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010, 59:307-321.
- [63]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
- [64]Posada D, Crandall KA: Selecting the best-fit model of nucleotide substitution. Syst Biol 2001, 50:580-601.
- [65][http://www.hiv.lanl.gov/content/sequence/findmodel/findmodel.html] webcite ᅟ: Find Model Server. ᅟ []
- [66][http://tree.bio.ed.ac.uk/software/tracer/] webcite Rambaut A, Drummond AJ: MCMC Trace Analysis Package, Version 1.5. ᅟ []
- [67][http://www.atgc-montpellier.fr/phyml/] webcite ᅟ: PhyML 3.0: new Algorithms, Methods and Utilities. ᅟ []
- [68]Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680.
- [69]Irwin DM: Data from: evolution of the vertebrate goose-type lysozyme gene family.Dryad Reposit ᅟ, ᅟ:ᅟ [doi:10.5061/dryad.681sn]