Peptidoglycan deacetylation in Helicobacter pylori contributes to bacterial survival by mitigating host immune responses

Infection and Immunity

Volumn 78, Issue 11, 2010, Pages 4660-4666

  Wang, Ge ^a   Maier, Susan E ^a   Lo, Leja F ^a   Maier, George ^a   Dosi, Shruti ^a   Maier, Robert J ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; LYSOZYME; MACROPHAGE INFLAMMATORY PROTEIN 2; PEPTIDOGLYCAN; PEPTIDOGLYCAN DEACETYLASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CELL; BACTERIAL COLONIZATION; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM MUTANT; BLOOD SAMPLING; CONTROLLED STUDY; DEACETYLATION; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HOST; HOST CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VIVO STUDY; INOCULATION; MACROPHAGE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSITIVITY ANALYSIS; WILD TYPE;

AMIDOHYDROLASES; ANIMALS; CHEMOKINE CXCL2; COLONY COUNT, MICROBIAL; CYTOKINES; DISEASE MODELS, ANIMAL; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HL-60 CELLS; HUMANS; MICE; MUTATION; PEPTIDOGLYCAN; STOMACH;

EID: 78049430106     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00307-10     Document Type: Article

References (40)

1. Akada, J. K., K. Ogura, D. Dailidiene, G. Dailide, J. M. Cheverud, and D. E. Berg. 2003. Helicobacter pylori tissue tropism: mouse-colonizing strains can target different gastric niches. Microbiology 149:1901-1909.
2. Algood, H. M., and T. L. Cover. 2006. Helicobacter pylori persistence: an overview of interactions between H. pylori and host immune defenses. Clin. Microbiol. Rev. 19:597-613.
3. Aspholm, M., F. O. Olfat, J. Norden, B. Sonden, C. Lundberg, R. Sjostrom, S. Altraja, S. Odenbreit, R. Haas, T. Wadstrom, L. Engstrand, C. Semino- Mora, H. Liu, A. Dubois, S. Teneberg, A. Arnqvist, and T. Boren. 2006. SabA is the H. pylori hemagglutinin and is polymorphic in binding to sialylated glycans. PLoS Pathog. 2:e110.
4. Atherton, J. C. 2006. The pathogenesis of Helicobacter pylori-induced gastro- duodenal diseases. Annu. Rev. Pathol. 1:63-96.
5. Boneca, I. G., O. Dussurget, D. Cabanes, M. A. Nahori, S. Sousa, M. Lecuit, E. Psylinakis, V. Bouriotis, J. P. Hugot, M. Giovannini, A. Coyle, J. Bertin, A. Namane, J. C. Rousselle, N. Cayet, M. C. Prevost, V. Balloy, M. Chignard, D. J. Philpott, P. Cossart, and S. E. Girardin. 2007. A critical role for peptidoglycan N-deacetylation in Listeria evasion from the host innate immune system. Proc. Natl. Acad. Sci. U. S. A. 104:997-1002.
6. Crabtree, J. E., A. Covacci, S. M. Farmery, Z. Xiang, D. S. Tompkins, S. Perry, I. J. Lindley, and R. Rappuoli. 1995. Helicobacter pylori induced interleukin-8 expression in gastric epithelial cells is associated with CagA positive phenotype. J. Clin. Pathol. 48:41-45.
7. Crabtree, J. E., R. L. Ferrero, and J. G. Kusters. 2002. The mouse colonizing Helicobacter pylori strain SS1 may lack a functional cag pathogenicity island. Helicobacter 7:139-140.
8. Crabtree, J. E., P. Peichl, J. I. Wyatt, U. Stachl, and I. J. Lindley. 1993. Gastric interleukin-8 and IgA IL-8 autoantibodies in Helicobacter pylori infection. Scand. J. Immunol. 37:65-70.
9. Dunn, B. E., H. Cohen, and M. J. Blaser. 1997. Helicobacter pylori. Clin. Microbiol. Rev. 10:720-741.
10. Ferrero, R. L., P. Ave, D. Ndiaye, J.-C. Bambou, M. R. Huerre, D. J. Philpott, and S. Memet. 2008. NF-kappaB activation during acute Helicobacter pylori infection in mice. Infect. Immun. 76:551-561.
11. Fittipaldi, N., T. Sekizaki, D. Takamatsu, L. Dominguez-Punaro Mde, J. Harel, N. K. Bui, W. Vollmer, and M. Gottschalk. 2008. Significant contribution of the pgdA gene to the virulence of Streptococcus suis. Mol. Microbiol. 70:1120-1135.
12. Fox, J. G., and T. C. Wang. 2007. Inflammation, atrophy, and gastric cancer. J. Clin. Invest. 117:60-69.
13. Garcia-Gonzalez, M. A., M. A. Aisa, M. Strunk, R. Benito, E. Piazuelo, P. Jimenez, F. Sopena, and A. Lanas. 2009. Relevance of IL-1 and TNF gene polymorphisms on interleukin-1beta and tumor necrosis factor-alpha gastric mucosal production. Hum. Immunol. 70:935-945.
14. Girardin, S. E., I. G. Boneca, L. A. Carneiro, A. Antignac, M. Jehanno, J. Viala, K. Tedin, M. K. Taha, A. Labigne, U. Zahringer, A. J. Coyle, P. S. DiStefano, J. Bertin, P. J. Sansonetti, and D. J. Philpott. 2003. Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 300:1584-1587.
15. Girardin, S. E., L. H. Travassos, M. Herve, D. Blanot, I. G. Boneca, D. J. Philpott, P. J. Sansonetti, and D. Mengin-Lecreulx. 2003. Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J. Biol. Chem. 278:41702-41708.
16. Israel, D. A., N. Salama, C. N. Arnold, S. F. Moss, T. Ando, H. P. Wirth, K. T. Tham, M. Camorlinga, M. J. Blaser, S. Falkow, and R. M. Peek, Jr. 2001. Helicobacter pylori strain-specific differences in genetic content, identified by microarray, influence host inflammatory responses. J. Clin. Invest. 107: 611-620.
17. Kaparakis, M., L. Turnbull, L. Carneiro, S. Firth, H. A. Coleman, H. C. Parkington, L. Le Bourhis, A. Karrar, J. Viala, J. Mak, M. L. Hutton, J. K. Davies, P. J. Crack, P. J. Hertzog, D. J. Philpott, S. E. Girardin, C. B. Whitchurch, and R. L. Ferrero. 2010. Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells. Cell. Microbiol. 12:372-385.
18. Le Bourhis, L., S. Benko, and S. E. Girardin. 2007. Nod1 and Nod2 in innate immunity and human inflammatory disorders. Biochem. Soc. Trans. 35: 1479-1484.
19. Meylan, E., J. Tschopp, and M. Karin. 2006. Intracellular pattern recognition receptors in the host response. Nature 442:39-44. (Pubitemid 44064203)
20. Mitchell, P., C. Germain, P. L. Fiori, W. Khamri, G. R. Foster, S. Ghosh, R. I. Lechler, K. B. Bamford, and G. Lombardi. 2007. Chronic exposure to Helicobacter pylori impairs dendritic cell function and inhibits Th1 development. Infect. Immun. 75:810-819.
21. Necchi, V., M. E. Candusso, F. Tava, O. Luinetti, U. Ventura, R. Fiocca, V. Ricci, and E. Solcia. 2007. Intracellular, intercellular, and stromal invasion of gastric mucosa, preneoplastic lesions, and cancer by Helicobacter pylori. Gastroenterology 132:1009-1023. (Pubitemid 46440875)
22. Noach, L. A., N. B. Bosma, J. Jansen, F. J. Hoek, S. J. van Deventer, and G. N. Tytgat. 1994. Mucosal tumor necrosis factor-alpha, interleukin-1 beta, and interleukin-8 production in patients with Helicobacter pylori infection. Scand. J. Gastroenterol. 29:425-429.
23. Ohtsuka, Y., J. Lee, D. S. Stamm, and I. R. Sanderson. 2001. MIP-2 secreted by epithelial cells increases neutrophil and lymphocyte recruitment in the mouse intestine. Gut 49:526-533.
24. Philpott, D. J., D. Belaid, P. Troubadour, J. M. Thiberge, J. Tankovic, A. Labigne, and R. L. Ferrero. 2002. Reduced activation of inflammatory responses in host cells by mouse-adapted Helicobacter pylori isolates. Cell. Microbiol. 4:285-296.
25. Ramarao, N., S. D. Gray-Owen, and T. F. Meyer. 2000. Helicobacter pylori induces but survives the extracellular release of oxygen radicals from professional phagocytes using its catalase activity. Mol. Microbiol. 38:103-113.
26. Remick, D. G., L. B. Green, D. E. Newcomb, S. J. Garg, G. L. Bolgos, and D. R. Call. 2001. CXC chemokine redundancy ensures local neutrophil recruitment during acute inflammation. Am. J. Pathol. 159:1149-1157.
27. Sartor, R. B. 1994. Cytokines in intestinal inflammation: pathophysiological and clinical considerations. Gastroenterology 106:533-539. (Pubitemid 24041233)
28. Seyler, R. W., Jr., J. W. Olson, and R. J. Maier. 2001. Superoxide dismutase-deficient mutants of Helicobacter pylori are hypersensitive to oxidative stress and defective in host colonization. Infect. Immun. 69:4034-4040.
29. Strober, W., P. J. Murray, A. Kitani, and T. Watanabe. 2006. Signalling pathways and molecular interactions of NOD1 and NOD2. Nat. Rev. Immunol. 6:9-20.
30. Suerbaum, S., and P. Michetti. 2002. Helicobacter pylori infection. N. Engl. J. Med. 347:1175-1186.
31. Viala, J., C. Chaput, I. G. Boneca, A. Cardona, S. E. Girardin, A. P. Moran, R. Athman, S. Memet, M. R. Huerre, A. J. Coyle, P. S. DiStefano, P. J. Sansonetti, A. Labigne, J. Bertin, D. J. Philpott, and R. L. Ferrero. 2004. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat. Immunol. 5:1166-1174.
32. Vollmer, W., and A. Tomasz. 2002. Peptidoglycan N-acetylglucosamine deacetylase, a putative virulence factor in Streptococcus pneumoniae. Infect. Immun. 70:7176-7178.
33. Wang, G., P. Alamuri, and R. J. Maier. 2006. The diverse antioxidant systems of Helicobacter pylori. Mol. Microbiol. 61:847-860.
34. Wang, G., Y. Hong, A. Olczak, S. E. Maier, and R. J. Maier. 2006. Dual roles of Helicobacter pylori NapA in inducing and combating oxidative stress. Infect. Immun. 74:6839-6846.
35. Wang, G., and R. J. Maier. 2009. A RecB-like helicase in Helicobacter pylori is important for DNA repair and host colonization. Infect. Immun. 77:286-291.
36. Wang, G., A. Olczak, L. S. Forsberg, and R. J. Maier. 2009. Oxidative stress-induced peptidoglycan deacetylase in Helicobacter pylori. J. Biol. Chem. 284:6790-6800.
37. Wang, G., A. A. Olczak, J. P. Walton, and R. J. Maier. 2005. Contribution of the Helicobacter pylori thiol peroxidase bacterioferritin comigratory protein to oxidative stress resistance and host colonization. Infect. Immun. 73:378-384.
38. Wilson, K. T., and J. E. Crabtree. 2007. Immunology of Helicobacter pylori: insights into the failure of the immune response and perspectives on vaccine studies. Gastroenterology 133:288-308.
39. Wilson, K. T., K. S. Ramanujam, H. L. Mobley, R. F. Musselman, S. P. James, and S. J. Meltzer. 1996. Helicobacter pylori stimulates inducible nitric oxide synthase expression and activity in a murine macrophage line. Gastroenterology 111:1524-1533.
40. Yamaoka, Y., M. Kita, T. Kodama, N. Sawai, K. Kashima, and J. Imanishi. 1997. Induction of various cytokines and development of severe mucosal inflammation by cagA gene positive Helicobacter pylori strains. Gut 41:442-451.