Coxiella burnetii acid phosphatase inhibits the release of reactive oxygen intermediates in polymorphonuclear leukocytes

Infection and Immunity

Volumn 79, Issue 1, 2011, Pages 414-420

  Hill, J ^a   Samuel, J E ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ARTICLE; COXIELLA BURNETII; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INFECTION CONTROL; LEUKOCYTE; NONHUMAN; OPEN READING FRAME; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ACID PHOSPHATASE; AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; COXIELLA BURNETII; GENE EXPRESSION REGULATION; HUMANS; HYDROGEN-ION CONCENTRATION; MICE; MOLECULAR SEQUENCE DATA; NADPH OXIDASE; NEUTROPHILS; NITRIC OXIDE SYNTHASE TYPE II; REACTIVE OXYGEN SPECIES;

EID: 78650907944     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01011-10     Document Type: Article

References (47)

1. Akporiaye, E., D. Stefanovich, V. Tsosie, and G. Baca. 1990. Coxiella burnetii fails to stimulate human neutrophil superoxide anion production. Acta Virol. 34:64-70.
2. Andoh, M., T. Naganawa, A. Hotta, T. Yamaguchi, H. Fukushi, T. Masegi, and K. Hirai. 2003. SCID mouse model for lethal Q fever. Infect. Immun. 71:4717-4723.
3. Angelakis, E., and D. Raoult. 2010. Q fever. Vet. Microbiol. 140:297-309.
4. Baca, O., M. Roman, R. Glew, R. Christner, J. Buhler, and A. Aragon. 1993. Acid phosphatase activity in Coxiella burnetii: a possible virulence factor. Infect. Immun. 61:4232-4239.
5. Barquero-Calvo, E., E. Chaves-Olarte, D. S. Weiss, C. Guzmán-Verri, C. Chacón-Díaz, A. Rucavado, I. Moriyón, and E. Moreno. 2007. Brucella abortus uses a stealthy strategy to avoid activation of the innate immune system during the onset of infection. PLoS One 2:e631.
6. Beare, P. A., J. E. Samuel, D. Howe, K. Virtaneva, S. F. Porcella, and R. A. Heinzen. 2006. Genetic diversity of the Q fever agent, Coxiella burnetii, assessed by microarray-based whole-genome comparisons. J. Bacteriol. 188: 2309-2324.
7. Brennan, R., K. Russell, G. Zhang, and J. Samuel. 2004. Both inducible nitric oxide synthase and NADPH oxidase contribute to the control of virulent phase I Coxiella burnetii infections. Infect. Immun. 72:6666-6675.
8. Carlyon, J., D. Abdel-Latif, M. Pypaert, P. Lacy, and E. Fikrig. 2004. Anaplasma phagocytophilum utilizes multiple host evasion mechanisms to thwart NADPH oxidase-mediated killing during neutrophil infection. Infect. Immun. 72:4772-4783.
9. Cassatella, M. A. 2003. The neutrophil: an emerging regulator of inflammatory and immuune response. Karger Publishers, Basel, Switzerland.
10. Clark, R. A. 1999. Activation of the neutrophil respiratory burst oxidase. J. Infect. Dis. 179(Suppl. 2):S309-S317.
11. DeLeo, F. R. A. 1999. NADPH oxidase activation and assembly during phagocytosis. J. Immunol. 163:6732-6740.
12. El-Benna, J., P. M. Dang, M. A. Gougerot-Pocidalo, J. C. Marie, and F. Braut-Boucher. 2009. p47phox, the phagocyte NADPH oxidase/NOX2 organizer: structure, phosphorylation and implication in diseases. Exp. Mol. Med. 41:217-225.
13. Elgert, K. D. 2009. Immunology, second ed. Wiley-Blackwell, Hoboken, NJ.
14. Ferencik, M., S. Schramek, J. Kazar, and J. Stefanovic. 1984. Effect of Coxiella burnetii on the stimulation of hexose monophosphate shunt and on superoxide anion production in human polymorphonuclear leukocytes. Acta Virol. 28:246-250.
15. Fumarulo, R., D. Giordano, A. Mosca, R. Monno, and G. Miragliotta. 1989. Different priming on human neutrophil respiratory burst by lipopolysaccha-rides from phase I and phase II Coxiella burnetii. Microbiologica 12:55-60.
16. Gueirard, P., A. Laplante, C. Rondeau, G. Milon, and M. Desjardins. 2008. Trafficking of Leishmania donovani promastigotes in non-lytic compartments in neutrophils enables the subsequent transfer of parasites to macro-phages. Cell. Microbiol. 10:100-111.
17. Hackstadt, T. 1986. Antigenic variation in the phase I lipopolysaccharide of Coxiella burnetii isolates. Infect. Immun. 52:337-340.
18. Hackstadt, T., M. G. Peacock, P. J. Hitchcock, and R. L. Cole. 1985. Lipo-polysaccharide variation in Coxiella burnetii: intrastrain heterogeneity in structure and antigenicity. Infect. Immun. 48:359-365.
19. Heinzen, R. A., M. E. Frazier, and L. P. Mallavia. 1992. Coxiella burnetii superoxide dismutase gene: cloning, sequencing, and expression in Esche-richia coli. Infect. Immun. 60:3814-3823.
20. Hitchcock, P. J., and T. M. Brown. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained poly-acrylamide gels. J. Bacteriol. 154:269-277.
21. Hotta, A., M. Kawamura, H. To, M. Andoh, T. Yamaguchi, H. Fukushi, and K. Hirai. 2002. Phase variation analysis of Coxiella burnetii during serial passage in cell culture by use of monoclonal antibodies. Infect. Immun. 70:4747-4749.
22. Kazar, J., E. Skultetyova, and R. Brezina. 1975. Phagocytosis of Coxiella burneti[sic] by macrophages. Acta Virol. 19:426-431.
23. Klebanoff, S. J. 2005. Myeloperoxidase: friend and foe. J. Leukoc. Biol. 77:598-625.
24. Laskay, T., G. van Zandbergen, and W. Solbach. 2008. Neutrophil granulocytes as host cells and transport vehicles for intracellular pathogens: apop-tosis as infection-promoting factor. Immunobiology 213:183-191.
25. Li, Y., G. Curley, M. Lopez, M. Chavez, R. Glew, A. Aragon, H. Kumar, and O. Baca. 1996. Protein-tyrosine phosphatase activity of Coxiella burnetii that inhibits human neutrophils. Acta Virol. 40:263-272.
26. Little, J. S., R. A. Kishimoto, and P. G. Canonico. 1983. Intracellular fate of phase I Coxiella burnetii in guinea pig peritoneal macrophages. J. Reticu-loendothel. Soc. 33:331-341.
27. Maurin, M., A. Benoliel, P. Bongrand, and D. Raoult. 1992. Phagolysosomes of Coxiella burnetii-infected cell lines maintain an acidic pH during persistent infection. Infect. Immun. 60:5013-5016.
28. Mohapatra, N. P., S. Soni, T. J. Reilly, J. Liu, K. E. Klose, and J. S. Gunn. 2008. Combined deletion of four Francisella novicida acid phosphatases attenuates virulence and macrophage vacuolar escape. Infect. Immun. 76: 3690-3699.
29. Mott, J., and Y. Rikihisa. 2000. Human granulocytic ehrlichiosis agent inhibits superoxide anion generation by human neutrophils. Infect. Immun. 68:6697-6703. (Pubitemid 32463373)
30. Murphy, K. P., P. Travers, C. Janeway, and M. Walport. 2008. Janeway's immunobiology, seventh ed. Garland Science, New York, NY.
31. Nieto-Sandoval, J. M., L. Almela, J. A. Fernández-López, and J. A. Muñoz. 2000. Effect of electron beam irradiation on color and microbial bioburden of red paprika. J. Food Prot. 63:633-637.
32. O'Bryan, C. A., P. G. Crandall, S. C. Ricke, and D. G. Olson. 2008. Impact of irradiation on the safety and quality of poultry and meat products: a review. Crit. Rev. Food Sci. Nutr. 48:442-457.
33. Omsland, A., D. C. Cockrell, D. Howe, E. R. Fischer, K. Virtaneva, D. E. Sturdevant, S. F. Porcella, and R. A. Heinzen. 2009. Host cell-free growth of the Q fever bacterium Coxiella burnetii. Proc. Natl. Acad. Sci. U.S.A. 106:4430-4434.
34. Parker, N. R., J. H. Barralet, and A. M. Bell. 2006. Q fever. Lancet 367: 679-688.
35. Raoult, D., T. Marrie, and J. Mege. 2005. Natural history and pathophysi-ology of Q fever. Lancet Infect. Dis. 5:219-226.
36. Reilly, T. J., G. S. Baron, F. E. Nano, and M. S. Kuhlenschmidt. 1996. Characterization and sequencing of a respiratory burst-inhibiting acid phos-phatase from Francisella tularensis. J. Biol. Chem. 271:10973-10983.
37. Robinson, J. M. 2009. Phagocytic leukocytes and reactive oxygen species. Histochem. Cell Biol. 131:465-469.
38. Segal, A. W. W. 1999. Components and organization of the NADPH oxidase of phagocytic cells, p. 441-483. In S. Gordon (ed.), Phagocytosis: the host. JAI Press, Greenwich, CT.
39. Segal, A. W. 2005. How neutrophils kill microbes. Annu. Rev. Immunol. 23:197-223.
40. Seshadri, R., I. T. Paulsen, J. A. Eisen, T. D. Read, K. E. Nelson, W. C. Nelson, N. L. Ward, H. Tettelin, T. M. Davidsen, M. J. Beanan, R. T. Deboy, S. C. Daugherty, L. M. Brinkac, R. Madupu, R. J. Dodson, H. M. Khouri, K. H. Lee, H. A. Carty, D. Scanlan, R. A. Heinzen, H. A. Thompson, J. E. Samuel, C. M. Fraser, and J. F. Heidelberg. 2003. Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc. Natl. Acad. Sci. U.S.A. 100:5455-5460.
41. Sheppard, F. R., M. R. Kelher, E. E. Moore, N. J. D. McLaughlin, A. Banerjee, and C. C. Silliman. 2005. Structural organization of the neutrophil NADPH oxidase: phosphorylation and translocation during priming and activation. J. Leukoc. Biol. 78:1025-1042.
42. Siemsen, D. W., L. N. Kirpotina, M. A. Jutila, and M. T. Quinn. 2009. Inhibition of the human neutrophil NADPH oxidase by Coxiella burnetii. Microbes Infect. 11:671-679.
43. Tissot Dupont, H., D. Raoult, P. Brouqui, F. Janbon, D. Peyramond, P. J. Weiller, C. Chicheportiche, M. Nezri, and R. Poirier. 1992. Epidemiologic features and clinical presentation of acute Q fever in hospitalized patients: 323 French cases. Am. J. Med. 93:427-434.
44. Wang, T., S. Malawista, U. Pal, M. Grey, J. Meek, M. Akkoyunlu, V. Thomas, and E. Fikrig. 2002. Superoxide anion production during Anaplasma phago-cytophila infection. J. Infect. Dis. 186:274-280.
45. Wang, X., F. Meng, and H. Zhou. 2004. Unfolding and inactivation during thermal denaturation of an enzyme that exhibits phytase and acid phos-phatase activities. Int. J. Biochem. Cell Biol. 36:447-459.
46. Zamboni, D. S., and M. Rabinovitch. 2003. Nitric oxide partially controls Coxiella burnetii phase II infection in mouse primary macrophages. Infect. Immun. 71:1225-1233.
47. Zhang, Y. X., Y. Zhu, and H. M. Zhou. 2000. Conformational changes and inactivation of calf intestinal alkaline phosphatase in trifluoroethanol solutions. Int. J. Biochem. Cell Biol. 32:887-894.