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
2019-10-14
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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 A 109:, 18779–18784. [CrossRef][PubMed]
    [Google Scholar]
  2. Beintema J. J., Terwisscha van Scheltinga A. C.. ( 1996;). Plant lysozymes. . EXS 75:, 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 Immun 76:, 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 Lett 325:, 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 Biol 19:, 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 A 89:, 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 Dis 28:, 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 Cytol 252:, 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. . Genetics 177:, 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 Genet 243:, 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 Res 37: (Database issue), D233–D238. [CrossRef][PubMed]
    [Google Scholar]
  12. CAZy (2013). Carbohydrate-Active enZYmes, Université d’Aix-Marseille. http://www.cazy.org/
  13. 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 Immun 74:, 1323–1338. [CrossRef][PubMed]
    [Google Scholar]
  14. 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 Microbiol 76:, 7302–7305. [CrossRef][PubMed]
    [Google Scholar]
  15. Chugani S., Greenberg E. P.. ( 2007;). The influence of human respiratory epithelia on Pseudomonas aeruginosa gene expression. . Microb Pathog 42:, 29–35. [CrossRef][PubMed]
    [Google Scholar]
  16. Collin M., Fischetti V. A.. ( 2004;). A novel secreted endoglycosidase from Enterococcus faecalis with activity on human immunoglobulin G and ribonuclease B. . J Biol Chem 279:, 22558–22570. [CrossRef][PubMed]
    [Google Scholar]
  17. Collin M., Olsén A.. ( 2001;). EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. . EMBO J 20:, 3046–3055. [CrossRef][PubMed]
    [Google Scholar]
  18. 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 A 103:, 19146–19151. [CrossRef][PubMed]
    [Google Scholar]
  19. Desvaux M., Hébraud M.. ( 2006;). The protein secretion systems in Listeria: inside out bacterial virulence. . FEMS Microbiol Rev 30:, 774–805. [CrossRef][PubMed]
    [Google Scholar]
  20. 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 Neurosci 23:, 2648–2656. [CrossRef][PubMed]
    [Google Scholar]
  21. Dubos R. J.. ( 1945;). The Bacterial Cell in its Relation to Problems of Virulence, Immunity and Chemotherapy. Cambridge, Massachusetts:: Harvard University Press;.
    [Google Scholar]
  22. 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 Microbiol 47:, 103–118. [CrossRef][PubMed]
    [Google Scholar]
  23. 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 A 103:, 1906–1911. [CrossRef][PubMed]
    [Google Scholar]
  24. Ficko-Blean E., Boraston A. B.. ( 2012;). Insights into the recognition of the human glycome by microbial carbohydrate-binding modules. . Curr Opin Struct Biol 22:, 570–577. [CrossRef][PubMed]
    [Google Scholar]
  25. Folders J., Tommassen J., van Loon L. C., Bitter W.. ( 2000;). Identification of a chitin-binding protein secreted by Pseudomonas aeruginosa. . J Bacteriol 182:, 1257–1263. [CrossRef][PubMed]
    [Google Scholar]
  26. 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 Bacteriol 183:, 7044–7052. [CrossRef][PubMed]
    [Google Scholar]
  27. 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 Sci 20:, 1479–1483. [CrossRef][PubMed]
    [Google Scholar]
  28. 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 Microbiol 35:, 1506–1517. [CrossRef][PubMed]
    [Google Scholar]
  29. 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 J 19:, 6697–6703. [CrossRef][PubMed]
    [Google Scholar]
  30. 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 Microbiol 59:, 1089–1100. [CrossRef][PubMed]
    [Google Scholar]
  31. Funkhouser J. D., Aronson N. N. Jr. ( 2007;). Chitinase family GH18: evolutionary insights from the genomic history of a diverse protein family. . BMC Evol Biol 7:, 96. [CrossRef][PubMed]
    [Google Scholar]
  32. 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 Immun 76:, 1825–1836. [CrossRef][PubMed]
    [Google Scholar]
  33. Garbe J., Collin M.. ( 2012;). Bacterial hydrolysis of host glycoproteins – powerful protein modification and efficient nutrient acquisition. . J Innate Immun 4:, 121–131. [CrossRef][PubMed]
    [Google Scholar]
  34. 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 Technol 48:, 225–231. [CrossRef][PubMed]
    [Google Scholar]
  35. Gooday G. W.. ( 1990;). The ecology of chitin degradation. . Adv Microb Ecol 11:, 387–430. [CrossRef]
    [Google Scholar]
  36. Gooday G. W.. ( 1999;). Aggressive and defensive roles for chitinases. . EXS 87:, 157–169.[PubMed]
    [Google Scholar]
  37. Guillén D., Sánchez S., Rodríguez-Sanoja R.. ( 2010;). Carbohydrate-binding domains: multiplicity of biological roles. . Appl Microbiol Biotechnol 85:, 1241–1249. [CrossRef][PubMed]
    [Google Scholar]
  38. 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 Immun 79:, 4105–4121. [CrossRef][PubMed]
    [Google Scholar]
  39. 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 Bacteriol 182:, 3045–3054. [CrossRef][PubMed]
    [Google Scholar]
  40. 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 Microbiol 10:, 958–984. [CrossRef][PubMed]
    [Google Scholar]
  41. Henrissat B.. ( 1999;). Classification of chitinase modules. . In Chitin and Chitinases, pp. 137–156. Edited by Jollès P., Muzzarelli R. A. A... Berlin:: Birkhäuser Verlag;. [CrossRef]
    [Google Scholar]
  42. Hoenerhoff M. J., Starost M. F., Ward J. M.. ( 2006;). Eosinophilic crystalline pneumonia as a major cause of death in 129S4/SvJae mice. . Vet Pathol 43:, 682–688. [CrossRef][PubMed]
    [Google Scholar]
  43. Holm L., Sander C.. ( 1994;). Structural similarity of plant chitinase and lysozymes from animals and phage: an evolutionary connection. . FEBS Lett 340:, 129–132. [CrossRef][PubMed]
    [Google Scholar]
  44. 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 J 273:, 491–503. [CrossRef][PubMed]
    [Google Scholar]
  45. 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 Chem 277:, 1388–1397. [CrossRef][PubMed]
    [Google Scholar]
  46. Johansen J. S., Krabbe K. S., Møller K., Pedersen B. K.. ( 2005;). Circulating YKL-40 levels during human endotoxaemia. . Clin Exp Immunol 140:, 343–348. [CrossRef][PubMed]
    [Google Scholar]
  47. 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 Chem 280:, 3847–3861. [CrossRef][PubMed]
    [Google Scholar]
  48. 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 Bacteriol 191:, 6911–6917. [CrossRef][PubMed]
    [Google Scholar]
  49. 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 ONE 4:, e5463. [CrossRef][PubMed]
    [Google Scholar]
  50. Karlsson M., Stenlid J.. ( 2009;). Evolution of family 18 glycoside hydrolases: diversity, domain structures and phylogenetic relationships. . J Mol Microbiol Biotechnol 16:, 208–223. [CrossRef][PubMed]
    [Google Scholar]
  51. 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 Invest 88:, 883–895. [CrossRef][PubMed]
    [Google Scholar]
  52. 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 Biochem 70:, 988–998. [CrossRef][PubMed]
    [Google Scholar]
  53. 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 Bacteriol 188:, 6026–6033. [CrossRef][PubMed]
    [Google Scholar]
  54. Kazmierczak M. J., Mithoe S. C., Boor K. J., Wiedmann M.. ( 2003;). Listeria monocytogenes σB regulates stress response and virulence functions. . J Bacteriol 185:, 5722–5734. [CrossRef][PubMed]
    [Google Scholar]
  55. Keyhani N. O., Roseman S.. ( 1999;). Physiological aspects of chitin catabolism in marine bacteria. . Biochim Biophys Acta 1473:, 108–122. [CrossRef][PubMed]
    [Google Scholar]
  56. 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 Bacteriol 191:, 6550–6554. [CrossRef][PubMed]
    [Google Scholar]
  57. Kirn T. J., Jude B. A., Taylor R. K.. ( 2005;). A colonization factor links Vibrio cholerae environmental survival and human infection. . Nature 438:, 863–866. [CrossRef][PubMed]
    [Google Scholar]
  58. Konkel M. E., Larson C. L., Flanagan R. C.. ( 2010;). Campylobacter jejuni FlpA binds fibronectin and is required for maximal host cell adherence. . J Bacteriol 192:, 68–76. [CrossRef][PubMed]
    [Google Scholar]
  59. 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 Microbiol 76:, 6470–6476. [CrossRef][PubMed]
    [Google Scholar]
  60. 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. . Glycobiology 21:, 426–436. [CrossRef][PubMed]
    [Google Scholar]
  61. 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 Dis 2011:, 939426.[PubMed]
    [Google Scholar]
  62. 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 Immunol 20:, 684–689. [CrossRef][PubMed]
    [Google Scholar]
  63. 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 Physiol 73:, 479–501. [CrossRef][PubMed]
    [Google Scholar]
  64. 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 Immunol 189:, 2635–2644. [CrossRef][PubMed]
    [Google Scholar]
  65. 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 Microbiol 107:, 2080–2087. [CrossRef][PubMed]
    [Google Scholar]
  66. 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 A 100:, 12432–12437. [CrossRef][PubMed]
    [Google Scholar]
  67. 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 Pathog 3:, e126. [CrossRef][PubMed]
    [Google Scholar]
  68. Little E., Bork P., Doolittle R. F.. ( 1994;). Tracing the spread of fibronectin type III domains in bacterial glycohydrolases. . J Mol Evol 39:, 631–643. [CrossRef][PubMed]
    [Google Scholar]
  69. 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 Pathol 174:, 153–163. [CrossRef][PubMed]
    [Google Scholar]
  70. 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 Microbe 4:, 447–457. [CrossRef][PubMed]
    [Google Scholar]
  71. Marth J. D., Grewal P. K.. ( 2008;). Mammalian glycosylation in immunity. . Nat Rev Immunol 8:, 874–887. [CrossRef][PubMed]
    [Google Scholar]
  72. 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 Res 344:, 1753–1757. [CrossRef][PubMed]
    [Google Scholar]
  73. 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 Med 13:, 151–159. [CrossRef][PubMed]
    [Google Scholar]
  74. 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 Bacteriol 179:, 7306–7314.[PubMed]
    [Google Scholar]
  75. 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 Immun 78:, 5022–5032. [CrossRef][PubMed]
    [Google Scholar]
  76. 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 Microbiol 301:, 547–555. [CrossRef][PubMed]
    [Google Scholar]
  77. 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 Commun 336:, 514–520. [CrossRef][PubMed]
    [Google Scholar]
  78. 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 Biol 381:, 670–680. [CrossRef][PubMed]
    [Google Scholar]
  79. 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 Microbiol 99:, 551–557. [CrossRef][PubMed]
    [Google Scholar]
  80. Pankov R., Yamada K. M.. ( 2002;). Fibronectin at a glance. . J Cell Sci 115:, 3861–3863. [CrossRef][PubMed]
    [Google Scholar]
  81. 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. . Science 299:, 2071–2074. [CrossRef][PubMed]
    [Google Scholar]
  82. Potts J. R., Campbell I. D.. ( 1996;). Structure and function of fibronectin modules. . Matrix Biol 15:, 313–320, discussion 321. [CrossRef][PubMed]
    [Google Scholar]
  83. 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 Res 40:, D290–D301. [CrossRef][PubMed]
    [Google Scholar]
  84. 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 Pathog 7:, e1002118. [CrossRef][PubMed]
    [Google Scholar]
  85. 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 Bacteriol 187:, 4908–4920. [CrossRef][PubMed]
    [Google Scholar]
  86. 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 Microbiol 77:, 1123–1126. [CrossRef][PubMed]
    [Google Scholar]
  87. 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 Acta 1770:, 839–846. [CrossRef][PubMed]
    [Google Scholar]
  88. 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 Sci 130:, 145–150. [CrossRef]
    [Google Scholar]
  89. 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. . Cellulose 13:, 477–484. [CrossRef]
    [Google Scholar]
  90. 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 Chem 286:, 16555–16566. [CrossRef][PubMed]
    [Google Scholar]
  91. 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 Microbiol 11:, 120. [CrossRef][PubMed]
    [Google Scholar]
  92. Sotgiu S., Musumeci S., Marconi S., Bonetti B.. ( 2008;). Microglia and chitotriosidase in multiple sclerosis. . Eur Neurolog Rev 3:, 90–93.
    [Google Scholar]
  93. Sriramulu D. D., Nimtz M., Romling U.. ( 2005;). Proteome analysis reveals adaptation of Pseudomonas aeruginosa to the cystic fibrosis lung environment. . Proteomics 5:, 3712–3721. [CrossRef][PubMed]
    [Google Scholar]
  94. Stauff D. L., Bassler B. L.. ( 2011;). Quorum sensing in Chromobacterium violaceum: DNA recognition and gene regulation by the CviR receptor. . J Bacteriol 193:, 3871–3878. [CrossRef][PubMed]
    [Google Scholar]
  95. 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 J 343:, 587–596. [CrossRef][PubMed]
    [Google Scholar]
  96. 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. . Microbiology 144:, 1299–1308. [CrossRef][PubMed]
    [Google Scholar]
  97. 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. . Nature 459:, 950–956. [CrossRef][PubMed]
    [Google Scholar]
  98. 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 Histopathol 26:, 1453–1464.[PubMed]
    [Google Scholar]
  99. 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 Commun 345:, 1621–1633. [CrossRef][PubMed]
    [Google Scholar]
  100. 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 Acta 1696:, 103–111. [CrossRef][PubMed]
    [Google Scholar]
  101. 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. . Science 330:, 219–222. [CrossRef][PubMed]
    [Google Scholar]
  102. 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 Biol 416:, 239–254. [CrossRef][PubMed]
    [Google Scholar]
  103. 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 Biol 14:, 76–84. [CrossRef][PubMed]
    [Google Scholar]
  104. 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 Trans 23:, 175–179.[PubMed]
    [Google Scholar]
  105. 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. . Microbiology 153:, 3593–3607. [CrossRef][PubMed]
    [Google Scholar]
  106. 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]
  107. 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 ONE 4:, e7660. [CrossRef][PubMed]
    [Google Scholar]
  108. 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 ONE 5:, e12489. [CrossRef][PubMed]
    [Google Scholar]
  109. 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 Scand 121:, 309–314. [CrossRef][PubMed]
    [Google Scholar]
  110. 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 Microbiol 63:, 380–386.[PubMed]
    [Google Scholar]
  111. 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 Chem 268:, 18567–18572.[PubMed]
    [Google Scholar]
  112. 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 Bacteriol 176:, 4465–4472.[PubMed]
    [Google Scholar]
  113. 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 A 92:, 9427–9431. [CrossRef][PubMed]
    [Google Scholar]
  114. Wohlkönig A., Huet J., Looze Y., Wintjens R.. ( 2010;). Structural relationships in the lysozyme superfamily: significant evidence for glycoside hydrolase signature motifs. . PLoS ONE 5:, e15388. [CrossRef][PubMed]
    [Google Scholar]
  115. 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 Pathog 8:, e1002373. [CrossRef][PubMed]
    [Google Scholar]
  116. 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. . Microbiology 155:, 2919–2929. [CrossRef][PubMed]
    [Google Scholar]
  117. Xu L., Wang Y., Wang L., Gao Y., An C.. ( 2008;). TYchi, a novel chitinase with RNA N-glycosidase and anti-tumor activities. . Front Biosci 13:, 3127–3135. [CrossRef][PubMed]
    [Google Scholar]
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