The Listeria monocytogenes ChiA chitinase enhances virulence through suppression of host innate immunity

mBio

Volumn 4, Issue 2, 2013, Pages

  Chaudhuri, Swarnava ^a   Gantner, Benjamin N ^a   Ye, Richard D ^a   Cianciotto, Nicholas P ^b   Freitag, Nancy E ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHIA PROTEIN; CHITIN; CHITINASE; INDUCIBLE NITRIC OXIDE SYNTHASE; UNCLASSIFIED DRUG; NOS2 PROTEIN, MOUSE; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COUNT; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM MUTANT; BACTERIUM REPLICATION; CONTROLLED STUDY; ENZYME RELEASE; HOST; HYDROLYSIS; IMMUNE RESPONSE; IMMUNOMODULATION; IN VIVO STUDY; INNATE IMMUNITY; LISTERIA MONOCYTOGENES; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE; ANIMAL; BIOSYNTHESIS; DISEASE MODEL; DOWN REGULATION; DRUG EFFECT; GENE DELETION; GENETIC COMPLEMENTATION; GENETICS; IMMUNE EVASION; IMMUNOLOGY; LISTERIOSIS; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; PATHOGENICITY;

ANIMALS; CHITINASE; DISEASE MODELS, ANIMAL; DOWN-REGULATION; GENE DELETION; GENETIC COMPLEMENTATION TEST; IMMUNE EVASION; IMMUNITY, INNATE; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICE; MICROBIAL VIABILITY; NITRIC OXIDE SYNTHASE TYPE II; VIRULENCE FACTORS;

EID: 84880078857     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00617-12     Document Type: Article

References (59)

1. Czuprynski CJ. 2005. Listeria monocytogenes: silage, sandwiches and science. Anim. Health Res. Rev. 6:211-217.
2. Xayarath B, Freitag NE. 2012. Optimizing the balance between host and environmental survival skills: lessions learned from Listeria monocytogenes. Future Microbiol. 7:839-852.
3. CDC. 2003. Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food-selected sites, United States. MMWR Morb. Mortal. Wkly. Rep. 53:338-343.
4. CDC. 2009. Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food-10 states. MMWR Morb. Mortal. Wkly. Rep. 58:333-337.
5. CDC. 2011. Multistate outbreak of listeriosis associated with Jensen farms cantaloupe-United States, August-September 2011. MMWR Morb. Mortal. Wkly. Rep. 60:1357-1358.
6. Cossart P, Toledo-Arana A. 2008. Listeria monocytogenes, a unique model in infection biology: an overview. Microbes Infect. 10:1041-1050.
7. Cossart P. 2011. Illuminating the landscape of host-pathogen interactions with the bacterium Listeria monocytogenes. Proc. Natl. Acad. Sci. U. S. A. 108:19484-19491.
8. Bhowmick R, Ghosal A, Das B, Koley H, Saha DR, Ganguly S, Nandy RK, Bhadra RK, Chatterjee NS. 2008. Intestinal adherence of Vibrio cholerae involves a coordinated interaction between colonization factor GbpA and mucin. Infect. Immun. 76:4968-4977.
9. Chaudhuri S, Bruno JC, Alonzo F, III, Xayarath B, Cianciotto NP, Freitag NE. 2010. Contribution of chitinases to Listeria monocytogenes pathogenesis. Appl. Environ. Microbiol. 76:7302-7305.
10. DebRoy S, Dao J, Söderberg M, Rossier O, Cianciotto NP. 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.
11. Jude BA, Martinez RM, Skorupski K, Taylor RK. 2009. Levels of the secreted Vibrio cholerae attachment factor GbpA are modulated by quorum-sensing-induced proteolysis. J. Bacteriol. 191:6911-6917.
12. Kawada M, Chen CC, 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.
13. Kirn TJ, Jude BA, Taylor RK. 2005. A colonization factor links Vibrio cholerae environmental survival and human infection. Nature 438: 863-866.
14. Cohen-Kupiec R, Chet I. 1998. The molecular biology of chitin digestion. Curr. Opin. Biotechnol. 9:270-277.
15. Dahiya N, Tewari R, Hoondal GS. 2006. Biotechnological aspects of chitinolytic enzymes: a review. Appl. Microbiol. Biotechnol. 71:773-782.
16. Bhattacharya D, Nagpure A, Gupta RK. 2007. Bacterial chitinases: properties and potential. Crit. Rev. Biotechnol. 27:21-28.
17. Leisner JJ, Larsen MH, Ingmer H, Petersen BO, Duus JO, Palcic MM. 2009. Cloning and comparison of phylogenetically related chitinases from Listeria monocytogenes EGD and Enterococcus faecalis V583. J. Appl. Microbiol. 107:2080-2087.
18. Leisner JJ, Larsen MH, Jorgensen RL, Brondsted L, Thomsen LE, Ingmer H. 2008. Chitin hydrolysis by Listeria spp., including L. monocytogenes. Appl. Environ. Microbiol. 74:3823-3830.
19. Chatterjee SS, 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.
20. Larsen MH, Leisner JJ, 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.
21. de las Heras A, Cain RJ, Bielecka MK, Vázquez-Boland JA. 2011. Regulation of Listeria virulence: PrfA master and commander. Curr. Opin. Microbiol. 14:118-127.
22. Eurich K, Segawa M, Toei-Shimizu S, Mizoguchi E. 2009. Potential role of chitinase 3-like-1 in inflammation-associated carcinogenic changes of epithelial cells. World J. Gastroenterol. 15:5249-5259.
23. Kawada M, Hachiya Y, Arihiro A, Mizoguchi E. 2007. Role of mammalian chitinases in inflammatory conditions. Keio J. Med. 56:21-27.
24. Ober C, Chupp GL. 2009. The chitinase and chitinase-like proteins: a review of genetic and functional studies in asthma and immune-mediated diseases. Curr. Opin. Allergy Clin. Immunol. 9:401-408.
25. Lee CG, Da Silva CA, Dela Cruz CS, Ahangari F, Ma B, Kang MJ, He CH, Takyar S, Elias JA. 2011. Role of chitin and chitnase/chitinase-like proteins in inflammation, tissue remodeling, and injury. Annu. Rev. Physiol. 73:479-501.
26. Lecuit M. 2005. Understanding how Listeria monocytogenes targets and crosses host barriers. Clin. Microbiol. Infect. 11:430-436.
27. Lecuit M. 2007. Human listeriosis and animal models. Microbes Infect. 9:1216-1225.
28. Lecuit M, Vandormael-Pournin S, Lefort J, Huerre M, Gounon P, Dupuy C, Babinet C, Cossart P. 2001. A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science 292:1722-1725.
29. Wollert T, Pasche B, Rochon M, Deppenmeier S, van den Heuvel J, Gruber AD, Heinz DW, Lengeling A, Schubert WD. 2007. Extending the host range of Listeria monocytogenes by rational protein design. Cell 129: 891-902.
30. Auerbuch V, Lenz LL, Portnoy DA. 2001. Development of a competitive index assay to evaluate the virulence of Listeria monocytogenes actA mutants during primary and secondary infection of mice. Infect. Immun. 69:5953-5957.
31. Songsiriritthigul C, Pantoom S, Aguda AH, Robinson RC, Suginta W. 2008. Crystal structures of Vibrio harveyi chitinase A complexed with chitooligosaccharides: implications for the catalytic mechanism. J. Struct. Biol. 162:491-499.
32. Svitil AL, Kirchman DL. 1998. A chitin-binding domain in a marine bacterial chitinase and other microbial chitinases: implications for the ecology and evolution of 1,4-beta-glycanases. Microbiology 144: 1299-1308.
33. Lauer P, Chow MY, Loessner MJ, Portnoy DA, Calendar R. 2002. Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. J. Bacteriol. 184:4177-4186.
34. Endres R, Luz A, Schulze H, Neubauer H, Fütterer A, Holland SM, Wagner H, Pfeffer K. 1997. Listeriosis in p47(phox-/-) and TRp55-/- mice: protection despite absence of ROI and susceptibility despite presence of RNI. Immunity 7:419-432.
35. Myers JT, Tsang AW, Swanson JA. 2003. Localized reactive oxygen and nitrogen intermediates inhibit escape of Listeria monocytogenes from vacuoles in activated macrophages. J. Immunol. 171:5447-5453.
36. Shiloh MU, MacMicking JD, Nicholson S, Brause JE, Potter S, Marino M, Fang F, Dinauer M, Nathan C. 1999. Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity 10:29-38.
37. Bassler BL, Yu C, Lee YC, Roseman S. 1991. Chitin utilization by marine bacteria: degradation and catabolism of chitin oligosaccharides by Vibrio furnissii. J. Biol. Chem. 266:24276-24286.
38. Inbar J, Chet I. 1991. Evidence that chitinase produced by Aeromonas caviae is involved in biological control of soil borne plant pathogens by this bacterium. Soil Biol. Biochem. 23:973-978.
39. Wang S, Shih I, Liang T, Wang C. 2002. Purification and characterization of two antifungal chitinases extracellularly produced by Bacillus amyloliquefaciens V656 in a SCSP medium. J. Agric. Food Chem. 50: 2241-2248.
40. Björk S, Breimer ME, Hansson GC, Karlsson KA, Leffler H. 1987. Structures of blood group glycosphingolipids of human small intestine. A relation between the expression of fucolipids of epithelial cells and the ABO, Le and Se phenotype of the donor. J. Biol. Chem. 262:6758-6765.
41. Liu Z, Masuko S, Solakyildirim K, Pu D, Linhardt RJ, Zhang F. 2010. Glycosaminoglycans of the porcine central nervous system. Biochemistry 49:9839-9845.
42. Semino CE, Specht CA, Raimondi A, Robbins PW. 1996. Homologs of the Xenopus developmental gene DG42 are present in zebrafish and mouse and are involved in the synthesis of Nod-like chitin oligosaccharides during early embryogenesis. Proc. Natl. Acad. Sci. U. S. A. 93: 4548-4553.
43. Mortier A, Van Damme J, Proost P. 2008. Regulation of chemokine activity by posttranslational modification. Pharmacol. Ther. 120:197-217.
44. Recny MA, Luther MA, Knoppers MH, Neidhardt EA, Khandekar SS, Concino MF, Schimke PA, Francis MA, Moebius U, Reinhold BB, Reinhold VN, Reinherz EL. 1992. N-glycosylation is required for human CD2 immunoadhesion functions. J. Biol. Chem. 267:22428-22434.
45. Rudd PM, Wormald MR, Stanfield RL, Huang M, Mattsson N, Speir JA, DiGennaro JA, Fetrow JS, Dwek RA, Wilson IA. 1999. Roles for glycosylation of cell surface receptors involved in cellular immune recognition. J. Mol. Biol. 293:351-366.
46. Boockvar KS, Granger DL, Poston RM, Maybodi M, Washington MK, Hibbs JB, Kurlander RL. 1994. Nitric oxide produced during murine listeriosis is protective. Infect. Immun. 62:1089-1100.
47. Nathan CF, Hibbs JB, Jr. 1991. Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol. 3:65-70.
48. Cole C, Thomas S, Filak H, Henson PM, Lenz LL. 2012. Nitric oxide increases susceptibility of Toll-like receptor-activated macrophages to spreading Listeria monocytogenes. Immunity 36:807-820.
49. MacMicking J, Xie QW, Nathan C. 1997. Nitric oxide and macrophage function. Annu. Rev. Immunol. 15:323-350.
50. Fang FC. 1997. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J. Clin. Invest. 99: 2818-2825.
51. Fang FC. 2004. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat. Rev. Microbiol. 2:820-832.
52. Fang FC, Vazquez-Torres A. 2002. Nitric oxide production by human macrophages: there's NO doubt about it. Am. J. Physiol. Lung Cell. Mol. Physiol. 282:L941-L943.
53. Serbina NV, Jia T, Hohl TM, Pamer EG. 2008. Monocyte-mediated defense against microbial pathogens. Annu. Rev. Immunol. 26:421-452.
54. Shi C, Pamer EG. 2011. Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 11:762-774.
55. Lee CG. 2009. Chitin, chitinases and chitinase-like proteins in allergic inflammation and tissue remodeling. Yonsei Med. J. 50:22-30.
56. Greenwell-Wild T, Moutsopoulos NM, Gliozzi M, Kapsogeorgou E, Rangel Z, Munson PJ, Moutsopoulos HM, Wahl SM. 2011. Chitinases in the salivary glands and circulation of patients with Sjögren's syndrome: macrophage harbingers of disease severity. Arthritis Rheum. 63: 3103-3115.
57. Watabe-Rudolph M, Song Z, Lausser L, Schnack C, Begus-Nahrmann Y, Scheithauer MO, Rettinger G, Otto M, Tumani H, Thal DR, Attems J, Jellinger KA, Kestler HA, von Arnim CA, Rudolph KL. 2012. Chitinase enzyme activity in CSF is a powerful biomarker of Alzheimer disease. Neurology 78:569-577.
58. Alonzo F, III, Port GC, Cao M, Freitag NE. 2009. The posttranslocation chaperone PrsA2 contributes to multiple facets of Listeria monocytogenes pathogenesis. Infect. Immun. 77:2612-2623.
59. Bruno JC, Jr, Freitag NE. 2010. Constitutive activation of PrfA tilts the balance of Listeria monocytogenes fitness towards life within the host versus environmental survival. PLoS One 5:e15138. http://dx.doi.org/10.1371/journal.pone.0015138.