1887

Abstract

Bacterial chitinases (EC 3.2.1.14) and chitin-binding proteins (CBPs) play a fundamental role in the degradation of the ubiquitous biopolymer chitin, and the degradation products serve as an important nutrient source for marine- and soil-dwelling bacteria. However, it has recently become clear that representatives of both Gram-positive and Gram-negative bacterial pathogens encode chitinases and CBPs that support infection of non-chitinous mammalian hosts. This review addresses this biological role of bacterial chitinases and CBPs in terms of substrate specificities, regulation, secretion and involvement in cellular and animal infection.

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2013-05-01
2020-05-26
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References

  1. Aachmann F. L., Sørlie M., Skjåk-Bræk G., Eijsink V. G., Vaaje-Kolstad G..( 2012;). NMR structure of a lytic polysaccharide monooxygenase provides insight into copper binding, protein dynamics, and substrate interactions. Proc Natl Acad Sci U S A109:18779–18784 [CrossRef][PubMed]
    [Google Scholar]
  2. Beintema J. J., Terwisscha van Scheltinga A. C..( 1996;). Plant lysozymes. EXS75:75–86[PubMed]
    [Google Scholar]
  3. Bhowmick R., Ghosal A., Das B., Koley H., Saha D. R., Ganguly S., Nandy R. K., Bhadra R. K., Chatterjee N. S..( 2008;). Intestinal adherence of Vibrio cholerae involves a coordinated interaction between colonization factor GbpA and mucin. Infect Immun76:4968–4977 [CrossRef][PubMed]
    [Google Scholar]
  4. Bøhle L. A., Mathiesen G., Vaaje-Kolstad G., Eijsink V. G. H..( 2011;). An endo-β-N-acetylglucosaminidase from Enterococcus faecalis V583 responsible for the hydrolysis of high-mannose and hybrid-type N-linked glycans. FEMS Microbiol Lett325:123–129 [CrossRef][PubMed]
    [Google Scholar]
  5. Boot R. G., van Achterberg T. A. E., van Aken B. E., Renkema G. H., Jacobs M. J. H. M., Aerts J. M. F. G., de Vries C. J. M..( 1999;). Strong induction of members of the chitinase family of proteins in atherosclerosis. Chitotriosidase and human cartilage gb-39 expressed in lesion macrophages. Arterioscler Thromb Vasc Biol19:687–694 [CrossRef]
    [Google Scholar]
  6. Bork P., Doolittle R. F..( 1992;). Proposed acquisition of an animal protein domain by bacteria. Proc Natl Acad Sci U S A89:8990–8994 [CrossRef][PubMed]
    [Google Scholar]
  7. Brinkman J., Wijburg F. A., Hollak C. E., Groener J. E., Verhoek M., Scheij S., Aten J., Boot R. G., Aerts J. M..( 2005;). Plasma chitotriosidase and CCL18: early biochemical surrogate markers in type B Niemann-Pick disease. J Inherit Metab Dis28:13–20 [CrossRef][PubMed]
    [Google Scholar]
  8. Bussink A. P., van Eijk M., Renkema G. H., Aerts J. M., Boot R. G..( 2006;). The biology of the Gaucher cell: the cradle of human chitinases. Int Rev Cytol252:71–128 [CrossRef][PubMed]
    [Google Scholar]
  9. Bussink A. P., Speijer D., Aerts J. M., Boot R. G..( 2007;). Evolution of mammalian chitinase(-like) members of family 18 glycosyl hydrolases. Genetics177:959–970 [CrossRef][PubMed]
    [Google Scholar]
  10. Canard B., Garnier T., Saint-Joanis B., Cole S. T..( 1994;). Molecular genetic analysis of the nagH gene encoding a hyaluronidase of Clostridium perfringens. Mol Gen Genet243:215–224[PubMed]
    [Google Scholar]
  11. Cantarel B. L., Coutinho P. M., Rancurel C., Bernard T., Lombard V., Henrissat B..( 2009;). The Carbohydrate-Active enZYmes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res37:Database issueD233–D238 [CrossRef][PubMed]
    [Google Scholar]
  12. Chatterjee S. S., Hossain H., Otten S., Kuenne C., Kuchmina K., Machata S., Domann E., Chakraborty T., Hain T..( 2006;). Intracellular gene expression profile of Listeria monocytogenes. Infect Immun74:1323–1338 [CrossRef][PubMed]
    [Google Scholar]
  13. Chaudhuri S., Bruno J. C., Alonzo F. III, Xayarath B., Cianciotto N. P., Freitag N. E..( 2010;). Contribution of chitinases to Listeria monocytogenes pathogenesis. Appl Environ Microbiol76:7302–7305 [CrossRef][PubMed]
    [Google Scholar]
  14. Chugani S., Greenberg E. P..( 2007;). The influence of human respiratory epithelia on Pseudomonas aeruginosa gene expression. Microb Pathog42:29–35 [CrossRef][PubMed]
    [Google Scholar]
  15. Collin M., Fischetti V. A..( 2004;). A novel secreted endoglycosidase from Enterococcus faecalis with activity on human immunoglobulin G and ribonuclease B. J Biol Chem279:22558–22570 [CrossRef][PubMed]
    [Google Scholar]
  16. Collin M., Olsén A..( 2001;). EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. EMBO J20:3046–3055 [CrossRef][PubMed]
    [Google Scholar]
  17. DebRoy S., Dao J., Söderberg M., Rossier O., Cianciotto N. P..( 2006;). Legionella pneumophila type II secretome reveals unique exoproteins and a chitinase that promotes bacterial persistence in the lung. Proc Natl Acad Sci U S A103:19146–19151 [CrossRef][PubMed]
    [Google Scholar]
  18. Desvaux M., Hébraud M..( 2006;). The protein secretion systems in Listeria: inside out bacterial virulence. FEMS Microbiol Rev30:774–805 [CrossRef][PubMed]
    [Google Scholar]
  19. Di Rosa M., Dell’Ombra N., Zambito A. M., Malaguarnera M., Nicoletti F., Malaguarnera L..( 2006;). Chitotriosidase and inflammatory mediator levels in Alzheimer’s disease and cerebrovascular dementia. Eur J Neurosci23:2648–2656 [CrossRef][PubMed]
    [Google Scholar]
  20. Dubos R. J..( 1945;). The Bacterial Cell in its Relation to Problems of Virulence, Immunity and Chemotherapy Cambridge, Massachusetts: Harvard University Press;
    [Google Scholar]
  21. Eriksson S., Lucchini S., Thompson A., Rhen M., Hinton J. C..( 2003;). Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol47:103–118 [CrossRef][PubMed]
    [Google Scholar]
  22. Faucher S. P., Porwollik S., Dozois C. M., McClelland M., Daigle F..( 2006;). Transcriptome of Salmonella enterica serovar Typhi within macrophages revealed through the selective capture of transcribed sequences. Proc Natl Acad Sci U S A103:1906–1911 [CrossRef][PubMed]
    [Google Scholar]
  23. Ficko-Blean E., Boraston A. B..( 2012;). Insights into the recognition of the human glycome by microbial carbohydrate-binding modules. Curr Opin Struct Biol22:570–577 [CrossRef][PubMed]
    [Google Scholar]
  24. Folders J., Tommassen J., van Loon L. C., Bitter W..( 2000;). Identification of a chitin-binding protein secreted by Pseudomonas aeruginosa. J Bacteriol182:1257–1263 [CrossRef][PubMed]
    [Google Scholar]
  25. Folders J., Algra J., Roelofs M. S., van Loon L. C., Tommassen J., Bitter W..( 2001;). Characterization of Pseudomonas aeruginosa chitinase, a gradually secreted protein. J Bacteriol183:7044–7052 [CrossRef][PubMed]
    [Google Scholar]
  26. Forsberg Z., Vaaje-Kolstad G., Westereng B., Bunæs A. C., Stenstrøm Y., MacKenzie A., Sørlie M., Horn S. J., Eijsink V. G..( 2011;). Cleavage of cellulose by a CBM33 protein. Protein Sci20:1479–1483 [CrossRef][PubMed]
    [Google Scholar]
  27. Francetic O., Badaut C., Rimsky S., Pugsley A. P..( 2000a;). The ChiA (YheB) protein of Escherichia coli K-12 is an endochitinase whose gene is negatively controlled by the nucleoid-structuring protein H-NS. Mol Microbiol35:1506–1517 [CrossRef][PubMed]
    [Google Scholar]
  28. Francetic O., Belin D., Badaut C., Pugsley A. P..( 2000b;). Expression of the endogenous type II secretion pathway in Escherichia coli leads to chitinase secretion. EMBO J19:6697–6703 [CrossRef][PubMed]
    [Google Scholar]
  29. Fung C., Naughton S., Turnbull L., Tingpej P., Rose B., Arthur J., Hu H., Harmer C., Harbour C. et al.( 2010;). Gene expression of Pseudomonas aeruginosa in a mucin-containing synthetic growth medium mimicking cystic fibrosis lung sputum. J Med Microbiol59:1089–1100 [CrossRef][PubMed]
    [Google Scholar]
  30. Funkhouser J. D., Aronson N. N. Jr.( 2007;). Chitinase family GH18: evolutionary insights from the genomic history of a diverse protein family. BMC Evol Biol7:96 [CrossRef][PubMed]
    [Google Scholar]
  31. Galka F., Wai S. N., Kusch H., Engelmann S., Hecker M., Schmeck B., Hippenstiel S., Uhlin B. E., Steinert M..( 2008;). Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles. Infect Immun76:1825–1836 [CrossRef][PubMed]
    [Google Scholar]
  32. Garbe J., Collin M..( 2012;). Bacterial hydrolysis of host glycoproteins – powerful protein modification and efficient nutrient acquisition. J Innate Immun4:121–131 [CrossRef][PubMed]
    [Google Scholar]
  33. Ghasemi S., Ahmadian G., Sadeghi M., Zeigler D. R., Rahimian H., Ghandili S., Naghibzadeh N., Dehestani A..( 2011;). First report of a bifunctional chitinase/lysozyme produced by Bacillus pumilus SG2. Enzyme Microb Technol48:225–231 [CrossRef][PubMed]
    [Google Scholar]
  34. Gooday G. W..( 1990;). The ecology of chitin degradation. Adv Microb Ecol11:387–430 [CrossRef]
    [Google Scholar]
  35. Gooday G. W..( 1999;). Aggressive and defensive roles for chitinases. EXS87:157–169[PubMed]
    [Google Scholar]
  36. Guillén D., Sánchez S., Rodríguez-Sanoja R..( 2010;). Carbohydrate-binding domains: multiplicity of biological roles. Appl Microbiol Biotechnol85:1241–1249 [CrossRef][PubMed]
    [Google Scholar]
  37. Harvey P. C., Watson M., Hulme S., Jones M. A., Lovell M., Berchieri A. J. Jr, Young J., Bumstead N., Barrow P..( 2011;). Salmonella enterica serovar Typhimurium colonizing the lumen of the chicken intestine grows slowly and upregulates a unique set of virulence and metabolism genes. Infect Immun79:4105–4121 [CrossRef][PubMed]
    [Google Scholar]
  38. Hashimoto M., Ikegami T., Seino S., Ohuchi N., Fukada H., Sugiyama J., Shirakawa M., Watanabe T..( 2000;). Expression and characterization of the chitin-binding domain of chitinase A1 from Bacillus circulans WL-12. J Bacteriol182:3045–3054 [CrossRef][PubMed]
    [Google Scholar]
  39. Hautefort I., Thompson A., Eriksson-Ygberg S., Parker M. L., Lucchini S., Danino V., Bongaerts R. J., Ahmad N., Rhen M., Hinton J. C..( 2008;). During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell Microbiol10:958–984 [CrossRef][PubMed]
    [Google Scholar]
  40. Henrissat B..( 1999;). Classification of chitinase modules. Chitin and Chitinases137–156 Jollès P., Muzzarelli R. A. A.. Berlin: Birkhäuser Verlag; [CrossRef]
    [Google Scholar]
  41. Hoenerhoff M. J., Starost M. F., Ward J. M..( 2006;). Eosinophilic crystalline pneumonia as a major cause of death in 129S4/SvJae mice. Vet Pathol43:682–688 [CrossRef][PubMed]
    [Google Scholar]
  42. Holm L., Sander C..( 1994;). Structural similarity of plant chitinase and lysozymes from animals and phage: an evolutionary connection. FEBS Lett340:129–132 [CrossRef][PubMed]
    [Google Scholar]
  43. Horn S. J., Sørbotten A., Synstad B., Sikorski P., Sørlie M., Vårum K. M., Eijsink V. G..( 2006;). Endo/exo mechanism and processivity of family 18 chitinases produced by Serratia marcescens. FEBS J273:491–503 [CrossRef][PubMed]
    [Google Scholar]
  44. Jee J. G., Ikegami T., Hashimoto M., Kawabata T., Ikeguchi M., Watanabe T., Shirakawa M..( 2002;). Solution structure of the fibronectin type III domain from Bacillus circulans WL-12 chitinase A1. J Biol Chem277:1388–1397 [CrossRef][PubMed]
    [Google Scholar]
  45. Johansen J. S., Krabbe K. S., Møller K., Pedersen B. K..( 2005;). Circulating YKL-40 levels during human endotoxaemia. Clin Exp Immunol140:343–348 [CrossRef][PubMed]
    [Google Scholar]
  46. Joshi M. B., Rogers M. E., Shakarian A. M., Yamage M., Al-Harthi S. A., Bates P. A., Dwyer D. M..( 2005;). Molecular characterization, expression, and in vivo analysis of LmexCht1: the chitinase of the human pathogen, Leishmania mexicana. J Biol Chem280:3847–3861 [CrossRef][PubMed]
    [Google Scholar]
  47. Jude B. A., Martinez R. M., Skorupski K., Taylor R. K..( 2009;). Levels of the secreted Vibrio cholerae attachment factor GbpA are modulated by quorum-sensing-induced proteolysis. J Bacteriol191:6911–6917 [CrossRef][PubMed]
    [Google Scholar]
  48. Kadzhaev K., Zingmark C., Golovliov I., Bolanowski M., Shen H., Conlan W., Sjöstedt A..( 2009;). Identification of genes contributing to the virulence of Francisella tularensis SCHU S4 in a mouse intradermal infection model. PLoS ONE4:e5463 [CrossRef][PubMed]
    [Google Scholar]
  49. Karlsson M., Stenlid J..( 2009;). Evolution of family 18 glycoside hydrolases: diversity, domain structures and phylogenetic relationships. J Mol Microbiol Biotechnol16:208–223 [CrossRef][PubMed]
    [Google Scholar]
  50. Kawada M., Chen C. C., Arihiro A., Nagatani K., Watanabe T., Mizoguchi E..( 2008;). Chitinase 3-like-1 enhances bacterial adhesion to colonic epithelial cells through the interaction with bacterial chitin-binding protein. Lab Invest88:883–895 [CrossRef][PubMed]
    [Google Scholar]
  51. Kawase T., Yokokawa S., Saito A., Fujii T., Nikaidou N., Miyashita K., Watanabe T..( 2006;). Comparison of enzymatic and antifungal properties between family 18 and 19 chitinases from S. coelicolor A3(2). Biosci Biotechnol Biochem70:988–998 [CrossRef][PubMed]
    [Google Scholar]
  52. Kay E., Humair B., Dénervaud V., Riedel K., Spahr S., Eberl L., Valverde C., Haas D..( 2006;). Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. J Bacteriol188:6026–6033 [CrossRef][PubMed]
    [Google Scholar]
  53. Kazmierczak M. J., Mithoe S. C., Boor K. J., Wiedmann M..( 2003;). Listeria monocytogenes σB regulates stress response and virulence functions. J Bacteriol185:5722–5734 [CrossRef][PubMed]
    [Google Scholar]
  54. Keyhani N. O., Roseman S..( 1999;). Physiological aspects of chitin catabolism in marine bacteria. Biochim Biophys Acta1473:108–122 [CrossRef][PubMed]
    [Google Scholar]
  55. Kim Y. G., Kim J. H., Kim K. J..( 2009;). Crystal structure of the Salmonella enterica serovar typhimurium virulence factor SrfJ, a glycoside hydrolase family enzyme. J Bacteriol191:6550–6554 [CrossRef][PubMed]
    [Google Scholar]
  56. Kirn T. J., Jude B. A., Taylor R. K..( 2005;). A colonization factor links Vibrio cholerae environmental survival and human infection. Nature438:863–866 [CrossRef][PubMed]
    [Google Scholar]
  57. Konkel M. E., Larson C. L., Flanagan R. C..( 2010;). Campylobacter jejuni FlpA binds fibronectin and is required for maximal host cell adherence. J Bacteriol192:68–76 [CrossRef][PubMed]
    [Google Scholar]
  58. Larsen M. H., Leisner J. J., Ingmer H..( 2010;). The chitinolytic activity of Listeria monocytogenes EGD is regulated by carbohydrates but also by the virulence regulator PrfA. Appl Environ Microbiol76:6470–6476 [CrossRef][PubMed]
    [Google Scholar]
  59. Larsen T., Petersen B. O., Storgaard B. G., Duus J. O., Palcic M. M., Leisner J. J..( 2011;). Characterization of a novel Salmonella Typhimurium chitinase which hydrolyzes chitin, chitooligosaccharides and an N-acetyllactosamine conjugate. Glycobiology21:426–436 [CrossRef][PubMed]
    [Google Scholar]
  60. Lautner R., Mattsson N., Schöll M., Augutis K., Blennow K., Olsson B., Zetterberg H..( 2011;). Biomarkers for microglial activation in Alzheimer’s disease. Int J Alzheimers Dis2011:939426[PubMed]
    [Google Scholar]
  61. Lee C. G., Da Silva C. A., Lee J. Y., Hartl D., Elias J. A..( 2008;). Chitin regulation of immune responses: an old molecule with new roles. Curr Opin Immunol20:684–689 [CrossRef][PubMed]
    [Google Scholar]
  62. Lee C. G., Da Silva C. A., Dela Cruz C. S., Ahangari F., Ma B., Kang M. J., He C. H., Takyar S., Elias J. A..( 2011;). Role of chitin and chitinase/chitinase-like proteins in inflammation, tissue remodeling, and injury. Annu Rev Physiol73:479–501 [CrossRef][PubMed]
    [Google Scholar]
  63. Lee C. G., Herzog E. L., Ahangari F., Zhou Y., Gulati M., Lee C.-M., Peng X., Feghali-Bostwick C., Jimenez S. A. et al.( 2012;). Chitinase 1 is a biomarker for and therapeutic target in scleroderma-associated interstitial lung disease that augments TGF-β1 signaling. J Immunol189:2635–2644 [CrossRef][PubMed]
    [Google Scholar]
  64. Leisner J. J., Larsen M. H., Ingmer H., Petersen B. O., Duus J. O., Palcic M. M..( 2009;). Cloning and comparison of phylogenetically related chitinases from Listeria monocytogenes EGD and Enterococcus faecalis V583. J Appl Microbiol107:2080–2087 [CrossRef][PubMed]
    [Google Scholar]
  65. Lenz L. L., Mohammadi S., Geissler A., Portnoy D. A..( 2003;). SecA2-dependent secretion of autolytic enzymes promotes Listeria monocytogenes pathogenesis. Proc Natl Acad Sci U S A100:12432–12437 [CrossRef][PubMed]
    [Google Scholar]
  66. Lesic B., Lépine F., Déziel E., Zhang J., Zhang Q., Padfield K., Castonguay M. H., Milot S., Stachel S. et al.( 2007;). Inhibitors of pathogen intercellular signals as selective anti-infective compounds. PLoS Pathog3:e126 [CrossRef][PubMed]
    [Google Scholar]
  67. Little E., Bork P., Doolittle R. F..( 1994;). Tracing the spread of fibronectin type III domains in bacterial glycohydrolases. J Mol Evol39:631–643 [CrossRef][PubMed]
    [Google Scholar]
  68. Liu Q., Cheng L. I., Yi L., Zhu N., Wood A., Changpriroa C. M., Ward J. M., Jackson S. H..( 2009;). p47phox deficiency induces macrophage dysfunction resulting in progressive crystalline macrophage pneumonia. Am J Pathol174:153–163 [CrossRef][PubMed]
    [Google Scholar]
  69. Martens E. C., Chiang H. C., Gordon J. I..( 2008;). Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe4:447–457 [CrossRef][PubMed]
    [Google Scholar]
  70. Marth J. D., Grewal P. K..( 2008;). Mammalian glycosylation in immunity. Nat Rev Immunol8:874–887 [CrossRef][PubMed]
    [Google Scholar]
  71. Martinez-Fleites C., Korczynska J. E., Davies G. J., Cope M. J., Turkenburg J. P., Taylor E. J..( 2009;). The crystal structure of a family GH25 lysozyme from Bacillus anthracis implies a neighboring-group catalytic mechanism with retention of anomeric configuration. Carbohydr Res344:1753–1757 [CrossRef][PubMed]
    [Google Scholar]
  72. Mattsson N., Tabatabaei S., Johansson P., Hansson O., Andreasson U., Månsson J. E., Johansson J.-O., Olsson B., Wallin A. et al.( 2011;). Cerebrospinal fluid microglial markers in Alzheimer’s disease: elevated chitotriosidase activity but lack of diagnostic utility. Neuromolecular Med13:151–159 [CrossRef][PubMed]
    [Google Scholar]
  73. Morimoto K., Karita S., Kimura T., Sakka K., Ohmiya K..( 1997;). Cloning, sequencing, and expression of the gene encoding Clostridium paraputrificum chitinase ChiB and analysis of the functions of novel cadherin-like domains and a chitin-binding domain. J Bacteriol179:7306–7314[PubMed]
    [Google Scholar]
  74. Mortensen B. L., Fuller J. R., Taft-Benz S., Kijek T. M., Miller C. N., Huang M. T., Kawula T. H..( 2010;). Effects of the putative transcriptional regulator IclR on Francisella tularensis pathogenesis. Infect Immun78:5022–5032 [CrossRef][PubMed]
    [Google Scholar]
  75. Mraheil M. A., Billion A., Mohamed W., Rawool D., Hain T., Chakraborty T..( 2011;). Adaptation of Listeria monocytogenes to oxidative and nitrosative stress in IFN-γ-activated macrophages. Int J Med Microbiol301:547–555 [CrossRef][PubMed]
    [Google Scholar]
  76. Murata T., Amarume S., Hattori T., Tokuyama S., Tokuyasu K., Kawagishi H., Usui T..( 2005;). Purification and characterization of a chitinase from Amycolatopsis orientalis with N-acetyllactosamine-repeating unit releasing activity. Biochem Biophys Res Commun336:514–520 [CrossRef][PubMed]
    [Google Scholar]
  77. Nakamura T., Mine S., Hagihara Y., Ishikawa K., Ikegami T., Uegaki K..( 2008;). Tertiary structure and carbohydrate recognition by the chitin-binding domain of a hyperthermophilic chitinase from Pyrococcus furiosus. J Mol Biol381:670–680 [CrossRef][PubMed]
    [Google Scholar]
  78. Orikoshi H., Nakayama S., Hanato C., Miyamoto K., Tsujibo H..( 2005;). Role of the N-terminal polycystic kidney disease domain in chitin degradation by chitinase A from a marine bacterium, Alteromonas sp. strain O-7. J Appl Microbiol99:551–557 [CrossRef][PubMed]
    [Google Scholar]
  79. Pankov R., Yamada K. M..( 2002;). Fibronectin at a glance. J Cell Sci115:3861–3863 [CrossRef][PubMed]
    [Google Scholar]
  80. Paulsen I. T., Banerjei L., Myers G. S., Nelson K. E., Seshadri R., Read T. D., Fouts D. E., Eisen J. A., Gill S. R. et al.( 2003;). Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science299:2071–2074 [CrossRef][PubMed]
    [Google Scholar]
  81. Potts J. R., Campbell I. D..( 1996;). Structure and function of fibronectin modules. Matrix Biol15:313–320, discussion 321 [CrossRef][PubMed]
    [Google Scholar]
  82. Punta M., Coggill P. C., Eberhardt R. Y., Mistry J., Tate J., Boursnell C., Pang N., Forslund K., Ceric G. et al.( 2012;). The Pfam protein family database. Nucleic Acids Res40:D290–D301 [CrossRef][PubMed]
    [Google Scholar]
  83. Renzi F., Manfredi P., Mally M., Moes S., Jenö P., Cornelis G. R..( 2011;). The N-glycan glycoprotein deglycosylation complex (Gpd) from Capnocytophaga canimorsus deglycosylates human IgG. PLoS Pathog7:e1002118 [CrossRef][PubMed]
    [Google Scholar]
  84. Salunkhe P., Smart C. H., Morgan J. A., Panagea S., Walshaw M. J., Hart C. A., Geffers R., Tümmler B., Winstanley C..( 2005;). A cystic fibrosis epidemic strain of Pseudomonas aeruginosa displays enhanced virulence and antimicrobial resistance. J Bacteriol187:4908–4920 [CrossRef][PubMed]
    [Google Scholar]
  85. Sánchez B., González-Tejedo C., Ruas-Madiedo P., Urdaci M. C., Margolles A..( 2011;). Lactobacillus plantarum extracellular chitin-binding protein and its role in the interaction between chitin, Caco-2 cells, and mucin. Appl Environ Microbiol77:1123–1126 [CrossRef][PubMed]
    [Google Scholar]
  86. Sanders N. N., Eijsink V. G., van den Pangaart P. S., Joost van Neerven R. J., Simons P. J., De Smedt S. C., Demeester J..( 2007;). Mucolytic activity of bacterial and human chitinases. Biochim Biophys Acta1770:839–846 [CrossRef][PubMed]
    [Google Scholar]
  87. Shih N. R., McDonald K. A., Jackman A. P., Girbes T., Iglesias R..( 1997;). Bifunctional plant defence enzymes with chitinase and ribosome inactivating activities from Trichosanthes kirilowii cell cultures. Plant Sci130:145–150 [CrossRef]
    [Google Scholar]
  88. Shoda S., Misawa Y., Nishijima Y., Tawata Y., Kotake T., Noguchi M., Kobayashi A., Watanabe T..( 2006;). Chemo-enzymatic synthesis of novel oligo-N-acetyllactosamine derivatives having a β(1-4)–β(1-6) repeating unit by using transition state analogue substrate. Cellulose13:477–484 [CrossRef]
    [Google Scholar]
  89. Sikora A. E., Zielke R. A., Lawrence D. A., Andrews P. C., Sandkvist M..( 2011;). Proteomic analysis of the Vibrio cholerae type II secretome reveals new proteins, including three related serine proteases. J Biol Chem286:16555–16566 [CrossRef][PubMed]
    [Google Scholar]
  90. Sjögren J., Okumura C. Y., Collin M., Nizet V., Hollands A..( 2011;). Study of the IgG endoglycosidase EndoS in group A streptococcal phagocyte resistance and virulence. BMC Microbiol11:120 [CrossRef][PubMed]
    [Google Scholar]
  91. Sotgiu S., Musumeci S., Marconi S., Bonetti B..( 2008;). Microglia and chitotriosidase in multiple sclerosis. Eur Neurolog Rev3:90–93
    [Google Scholar]
  92. Sriramulu D. D., Nimtz M., Romling U..( 2005;). Proteome analysis reveals adaptation of Pseudomonas aeruginosa to the cystic fibrosis lung environment. Proteomics5:3712–3721 [CrossRef][PubMed]
    [Google Scholar]
  93. Stauff D. L., Bassler B. L..( 2011;). Quorum sensing in Chromobacterium violaceum: DNA recognition and gene regulation by the CviR receptor. J Bacteriol193:3871–3878 [CrossRef][PubMed]
    [Google Scholar]
  94. Suzuki K., Taiyoji M., Sugawara N., Nikaidou N., Henrissat B., Watanabe T..( 1999;). The third chitinase gene (chiC) of Serratia marcescens 2170 and the relationship of its product to other bacterial chitinases. Biochem J343:587–596 [CrossRef][PubMed]
    [Google Scholar]
  95. Svitil A. L., Kirchman D. L..( 1998;). A chitin-binding domain in a marine bacterial chitinase and other microbial chitinases: implications for the ecology and evolution of 1,4-β-glycanases. Microbiology144:1299–1308 [CrossRef][PubMed]
    [Google Scholar]
  96. Toledo-Arana A., Dussurget O., Nikitas G., Sesto N., Guet-Revillet H., Balestrino D., Loh E., Gripenland J., Tiensuu T. et al.( 2009;). The Listeria transcriptional landscape from saprophytism to virulence. Nature459:950–956 [CrossRef][PubMed]
    [Google Scholar]
  97. Tran H. T., Barnich N., Mizoguchi E..( 2011;). Potential role of chitinases and chitin-binding proteins in host-microbial interactions during the development of intestinal inflammation. Histol Histopathol26:1453–1464[PubMed]
    [Google Scholar]
  98. Twine S. M., Mykytczuk N. C., Petit M. D., Shen H., Sjöstedt A., Wayne Conlan J., Kelly J. F..( 2006;). In vivo proteomic analysis of the intracellular bacterial pathogen, Francisella tularensis, isolated from mouse spleen. Biochem Biophys Res Commun345:1621–1633 [CrossRef][PubMed]
    [Google Scholar]
  99. Vaaje-Kolstad G., Houston D. R., Rao F. V., Peter M. G., Synstad B., van Aalten D. M., Eijsink V. G..( 2004;). Structure of the D142N mutant of the family 18 chitinase ChiB from Serratia marcescens and its complex with allosamidin. Biochim Biophys Acta1696:103–111 [CrossRef][PubMed]
    [Google Scholar]
  100. Vaaje-Kolstad G., Westereng B., Horn S. J., Liu Z. L., Zhai H., Sørlie M., Eijsink V. G. H..( 2010;). An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science330:219–222 [CrossRef][PubMed]
    [Google Scholar]
  101. Vaaje-Kolstad G., Bøhle L. A., Gåseidnes S., Dalhus B., Bjørås M., Mathiesen G., Eijsink V. G. H..( 2012;). Characterization of the chitinolytic machinery of Enterococcus faecalis V583 and high-resolution structure of its oxidative CBM33 enzyme. J Mol Biol416:239–254 [CrossRef][PubMed]
    [Google Scholar]
  102. van Bueren A. L., Higgins M., Wang D., Burke R. D., Boraston A. B..( 2007;). Identification and structural basis of binding to host lung glycogen by streptococcal virulence factors. Nat Struct Mol Biol14:76–84 [CrossRef][PubMed]
    [Google Scholar]
  103. Van den Eijnden D. H., Neeleman A. P., Van der Knaap W. P., Bakker H., Agterberg M., Van Die I..( 1995;). Novel glycosylation routes for glycoproteins: the lacdiNAc pathway. Biochem Soc Trans23:175–179[PubMed]
    [Google Scholar]
  104. van der Veen S., Hain T., Wouters J. A., Hossain H., de Vos W. M., Abee T., Chakraborty T., Wells-Bennik M. H..( 2007;). The heat-shock response of Listeria monocytogenes comprises genes involved in heat shock, cell division, cell wall synthesis, and the SOS response. Microbiology153:3593–3607 [CrossRef][PubMed]
    [Google Scholar]
  105. Varki A., Cummings R. D., Esko J. D., Freeze H. H., Stanley P., Bertozzi C. R., Hart G. W., Etzler M. E..( 2009;). Essentials of Glycobiology, 2nd edn. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press;
    [Google Scholar]
  106. Vebø H. C., Snipen L., Nes I. F., Brede D. A..( 2009;). The transcriptome of the nosocomial pathogen Enterococcus faecalis V583 reveals adaptive responses to growth in blood. PLoS ONE4:e7660 [CrossRef][PubMed]
    [Google Scholar]
  107. Vebø H. C., Solheim M., Snipen L., Nes I. F., Brede D. A..( 2010;). Comparative genomic analysis of pathogenic and probiotic Enterococcus faecalis isolates, and their transcriptional responses to growth in human urine. PLoS ONE5:e12489 [CrossRef][PubMed]
    [Google Scholar]
  108. Verbeek M. M., Notting E. A., Faas B., Claessens-Linskens R., Jongen P. J. H..( 2010;). Increased cerebrospinal fluid chitotriosidase index in patients with multiple sclerosis. Acta Neurol Scand121:309–314 [CrossRef][PubMed]
    [Google Scholar]
  109. Wang S. L., Chang W. T..( 1997;). Purification and characterization of two bifunctional chitinases/lysozymes extracellularly produced by Pseudomonas aeruginosa K-187 in a shrimp and crab shell powder medium. Appl Environ Microbiol63:380–386[PubMed]
    [Google Scholar]
  110. Watanabe T., Kobori K., Miyashita K., Fujii T., Sakai H., Uchida M., Tanaka H..( 1993;). Identification of glutamic acid 204 and aspartic acid 200 in chitinase A1 of Bacillus circulans WL-12 as essential residues for chitinase activity. J Biol Chem268:18567–18572[PubMed]
    [Google Scholar]
  111. Watanabe T., Ito Y., Yamada T., Hashimoto M., Sekine S., Tanaka H..( 1994;). The roles of the C-terminal domain and type III domains of chitinase A1 from Bacillus circulans WL-12 in chitin degradation. J Bacteriol176:4465–4472[PubMed]
    [Google Scholar]
  112. Winson M. K., Camara M., Latifi A., Foglino M., Chhabra S. R., Daykin M., Bally M., Chapon V., Salmond G. P., Bycroft B. W..( 1995;). Multiple N-acyl-l-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A92:9427–9431 [CrossRef][PubMed]
    [Google Scholar]
  113. Wohlkönig A., Huet J., Looze Y., Wintjens R..( 2010;). Structural relationships in the lysozyme superfamily: significant evidence for glycoside hydrolase signature motifs. PLoS ONE5:e15388 [CrossRef][PubMed]
    [Google Scholar]
  114. Wong E., Vaaje-Kolstad G., Ghosh A., Hurtado-Guerrero R., Konarev P. V., Ibrahim A. F., Svergun D. I., Eijsink V. G., Chatterjee N. S., van Aalten D. M..( 2012;). The Vibrio cholerae colonization factor GbpA possesses a modular structure that governs binding to different host surfaces. PLoS Pathog8:e1002373 [CrossRef][PubMed]
    [Google Scholar]
  115. Wright J. A., Tötemeyer S. S., Hautefort I., Appia-Ayme C., Alston M., Danino V., Paterson G. K., Mastroeni P., Ménager N. et al.( 2009;). Multiple redundant stress resistance mechanisms are induced in Salmonella enterica serovar Typhimurium in response to alteration of the intracellular environment via TLR4 signalling. Microbiology155:2919–2929 [CrossRef][PubMed]
    [Google Scholar]
  116. Xu L., Wang Y., Wang L., Gao Y., An C..( 2008;). TYchi, a novel chitinase with RNA N-glycosidase and anti-tumor activities. Front Biosci13:3127–3135 [CrossRef][PubMed]
    [Google Scholar]
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