Reactive oxygen species produced by the NADPH oxidase 2 complex in monocytes protect mice from bacterial infections

Journal of Immunology

Volumn 188, Issue 10, 2012, Pages 5003-5011

  Pizzolla, Angela ^a   Hultqvist, Malin ^b,i   Nilson, Bo ^c   Grimm, Melissa J ^d   Eneljung, Tove ^e   Jonsson, Ing Marie ^e   Verdrengh, Margareta ^e   Kelkka, Tiina ^a,f,g   Gjertsson, Inger ^e   Segal, Brahm H ^d,h   Holmdahl, Rikard ^a,b,g  

^a KAROLINSKA INSTITUTE   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c LUND UNIVERSITY   (Sweden)

^d ROSWELL PARK CANCER INSTITUTE   (United States)

^e UNIVERSITY OF GOTHENBURG   (Sweden)

^f UNIVERSITY OF TURKU   (Finland)

^g Medicity   (Finland)

^h UNIVERSITY AT BUFFALO   (United States)

ⁱ Redoxis AB   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CD68 ANTIGEN; NCF1 PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL GENETICS; ANIMAL MODEL; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL INFECTION; BURKHOLDERIA CEPACIA; CHRONIC GRANULOMATOUS DISEASE; CONTROLLED STUDY; DISEASE COURSE; DISEASE PREDISPOSITION; DISEASE RESISTANCE; ENZYME ACTIVITY; ENZYME STRUCTURE; GENE; INFECTION PREVENTION; MACROPHAGE; MOLECULAR MECHANICS; MONOCYTE; MOUSE; NCF1 GENE; NEUTROPHIL; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SPONTANEOUS MUTATION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS XYLOSUS;

ANIMALS; ANTI-BACTERIAL AGENTS; BURKHOLDERIA CEPACIA; BURKHOLDERIA INFECTIONS; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, KNOCKOUT; MICE, TRANSGENIC; MONOCYTES; NADPH OXIDASE; REACTIVE OXYGEN SPECIES; STAPHYLOCOCCAL INFECTIONS;

EID: 84861164816     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103430     Document Type: Article

References (52)

1. Bridges, R. A., H. Berendes, and R. A. Good. 1959. A fatal granulomatous disease of childhood; the clinical, pathological, and laboratory features of a new syndrome. AMA J. Dis. Child. 97: 387-408.
2. Grimm, M. J., R. R. Vethanayagam, N. G. Almyroudis, D. Lewandowski, N. Rall, T. S. Blackwell, and B. H. Segal. 2011. Role of NADPH oxidase in host defense against aspergillosis. Med. Mycol. 49(Suppl. 1): S144-S149.
3. Holland, S. M. 2010. Chronic granulomatous disease. Clin. Rev. Allergy Immunol. 38: 3-10.
4. van den Berg, J. M., E. van Koppen, A. Ahlin, B. H. Belohradsky, E. Bernatowska, L. Corbeel, T. Español, A. Fischer, M. Kurenko-Deptuch, R. Mouy, et al. 2009. Chronic granulomatous disease: the European experience. PLoS ONE 4: e5234.
5. Segal, A. W., O. T. Jones, D. Webster, and A. C. Allison. 1978. Absence of a newly described cytochrome b from neutrophils of patients with chronic granulomatous disease. Lancet 2: 446-449. (Pubitemid 9033263)
6. Segal, B. H., T. L. Leto, J. I. Gallin, H. L. Malech, and S. M. Holland. 2000. Genetic, biochemical, and clinical features of chronic granulomatous disease. Medicine (Baltimore) 79: 170-200. (Pubitemid 30327531)
7. Matute, J. D., A. A. Arias, N. A. Wright, I. Wrobel, C. C. Waterhouse, X. J. Li, C. C. Marchal, N. D. Stull, D. B. Lewis, M. Steele, et al. 2009. A new genetic subgroup of chronic granulomatous disease with autosomal recessive mutations in p40 phox and selective defects in neutrophil NADPH oxidase activity. Blood 114: 3309-3315.
8. Pollock, J. D., D. A. Williams, M. A. Gifford, L. L. Li, X. Du, J. Fisherman, S. H. Orkin, C. M. Doerschuk, and M. C. Dinauer. 1995. Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat. Genet. 9: 202-209.
9. Ju, J. Y., C. Polhamus, K. A. Marr, S. M. Holland, and J. E. Bennett. 2002. Efficacies of fluconazole, caspofungin, and amphotericin B in Candida glabrata-infected p47phox-/- knockout mice. Antimicrob. Agents Chemother. 46: 1240-1245. (Pubitemid 34415297)
10. Mardiney, M., III, S. H. Jackson, S. K. Spratt, F. Li, S. M. Holland, and H. L. Malech. 1997. Enhanced host defense after gene transfer in the murine p47phox-deficient model of chronic granulomatous disease. Blood 89: 2268-2275. (Pubitemid 27143271)
11. Jackson, S. H., J. I. Gallin, and S. M. Holland. 1995. The p47phox mouse knockout model of chronic granulomatous disease. J. Exp. Med. 182: 751-758.
12. Hultqvist, M., P. Olofsson, J. Holmberg, B. T. Bäckström, J. Tordsson, and R. Holmdahl. 2004. Enhanced autoimmunity, arthritis, and encephalomyelitis in mice with a reduced oxidative burst due to a mutation in the Ncf1 gene. Proc. Natl. Acad. Sci. USA 101: 12646-12651. (Pubitemid 39122077)
13. Quie, P. G., J. G. White, B. Holmes, and R. A. Good. 1967. In vitro bactericidal capacity of human polymorphonuclear leukocytes: diminished activity in chronic granulomatous disease of childhood. J. Clin. Invest. 46: 668-679.
14. Huang, C. K., L. Zhan, M. O. Hannigan, Y. Ai, and T. L. Leto. 2000. P47(phox)- deficient NADPH oxidase defect in neutrophils of diabetic mouse strains, C57BL/6J-m db/db and db/+. J. Leukoc. Biol. 67: 210-215.
15. Pizzolla, A., K. A. Gelderman, M. Hultqvist, M. Vestberg, K. Gustafsson, R. Mattsson, and R. Holmdahl. 2011. CD68-expressing cells can prime T cells and initiate autoimmune arthritis in the absence of reactive oxygen species. Eur. J. Immunol. 41: 403-412.
16. Svensson, L., J. Jirholt, R. Holmdahl, and L. Jansson. 1998. B cell-deficient mice do not develop type II collagen-induced arthritis (CIA). Clin. Exp. Immunol. 111: 521-526. (Pubitemid 28160894)
17. Geng, H., S. Carlsen, K. S. Nandakumar, R. Holmdahl, A. Aspberg, A. Oldberg, and R. Mattsson. 2008. Cartilage oligomeric matrix protein deficiency promotes early onset and the chronic development of collagen-induced arthritis. Arthritis Res. Ther. 10: R134.
18. Gelderman, K. A., M. Hultqvist, A. Pizzolla, M. Zhao, K. S. Nandakumar, R. Mattsson, and R. Holmdahl. 2007. Macrophages suppress T cell responses and arthritis development in mice by producing reactive oxygen species. J. Clin. Invest. 117: 3020-3028. (Pubitemid 47529631)
19. Goldenberger, D., T. Schmidheini, and M. Altwegg. 1997. Detection of Bartonella henselae and Bartonella quintana by a simple and rapid procedure using broad-range PCR amplification and direct single-strand sequencing of part of the 16S rRNA gene. Clin. Microbiol. Infect. 3: 240-245. (Pubitemid 27202316)
20. Fredricks, D. N., and D. A. Relman. 1998. Improved amplification of microbial DNA from blood cultures by removal of the PCR inhibitor sodium poly-anetholesulfonate. J. Clin. Microbiol. 36: 2810-2816. (Pubitemid 28429396)
21. Bannerman, T. L. 2003. Staphylococcus, Micrococcus, and other catalase-positive cocci that grow aerobically. In Manual of Clinical Microbiology, 8th Ed. P. R. Murray, E. J. Baron, J. H. Jorgensen, M. A. Pfaller, and R. H. Yolken, eds. ASM Press, Washington, DC, p. 719-728.
22. Segal, B. H., L. Ding, and S. M. Holland. 2003. Phagocyte NADPH oxidase, but not inducible nitric oxide synthase, is essential for early control of Burkholderia cepacia and Chromobacterium violaceum infection in mice. Infect. Immun. 71:205-210. (Pubitemid 36026021)
23. Hultqvist, M., P. Olofsson, K. A. Gelderman, J. Holmberg, and R. Holmdahl. 2006. A new arthritis therapy with oxidative burst inducers. PLoS Med. 3: e348.
24. Kielland, A., T. Blom, K. S. Nandakumar, R. Holmdahl, R. Blomhoff, and H. Carlsen. 2009. In vivo imaging of reactive oxygen and nitrogen species in inflammation using the luminescent probe L-012. Free Radic. Biol. Med. 47:760-766.
25. Bremell, T., A. Abdelnour, and A. Tarkowski. 1992. Histopathological and serological progression of experimental Staphylococcus aureus arthritis. Infect. Immun. 60: 2976-2985.
26. Daley, J. M., A. A. Thomay, M. D. Connolly, J. S. Reichner, and J. E. Albina. 2008. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J. Leukoc. Biol. 83: 64-70.
27. Rothe, G., A. Oser, and G. Valet. 1988. Dihydrorhodamine 123: a new flow cytometric indicator for respiratory burst activity in neutrophil granulocytes. Naturwissenschaften 75: 354-355.
28. Daiber, A., M. August, S. Baldus, M. Wendt, M. Oelze, K. Sydow, A. L. Kleschyov, and T. Munzel. 2004. Measurement of NAD(P)H oxidase-derived superoxide with the luminol analogue L-012. Free Radic. Biol. Med. 36: 101-111. (Pubitemid 38068295)
29. Winkelstein, J. A., M. C. Marino, R. B. Johnston, Jr., J. Boyle, J. Curnutte, J. I. Gallin, H. L. Malech, S. M. Holland, H. Ochs, P. Quie, et al. 2000. Chronic granulomatous disease. Report on a national registry of 368 patients. Medicine (Baltimore) 79: 155-169. (Pubitemid 30327530)
30. Sieber, O. F., Jr., and V. A. Fulginiti. 1976. Pseudomonas cepacia pneumonia in a child with chronic granulomatous disease and selective IgA deficiency. Acta Paediatr. Scand. 65: 519-520.
31. Speert, D. P., M. Bond, R. C. Woodman, and J. T. Curnutte. 1994. Infection with Pseudomonas cepacia in chronic granulomatous disease: role of nonoxidative killing by neutrophils in host defense. J. Infect. Dis. 170: 1524-1531. (Pubitemid 24369913)
32. Segal, B. H., N. Sakamoto, M. Patel, K. Maemura, A. S. Klein, S. M. Holland, and G. B. Bulkley. 2000. Xanthine oxidase contributes to host defense against Burkholderia cepacia in the p47(phox2/2) mouse model of chronic granulomatous disease. Infect. Immun. 68: 2374-2378. (Pubitemid 30164882)
33. Bustamante, J., A. A. Arias, G. Vogt, C. Picard, L. B. Galicia, C. Prando, A. V. Grant, C. C. Marchal, M. Hubeau, A. Chapgier, et al. 2011. Germline CYBB mutations that selectively affect macrophages in kindreds with X-linked predisposition to tuberculous mycobacterial disease. Nat. Immunol. 12: 213-221.
34. Gough, P. J., S. Gordon, and D. R. Greaves. 2001. The use of human CD68 transcriptional regulatory sequences to direct high-level expression of class A scavenger receptor in macrophages in vitro and in vivo. Immunology 103: 351-361. (Pubitemid 32626183)
35. Lang, R., R. L. Rutschman, D. R. Greaves, and P. J. Murray. 2002. Autocrine deactivation of macrophages in transgenic mice constitutively overexpressing IL-10 under control of the human CD68 promoter. J. Immunol. 168: 3402-3411. (Pubitemid 34250404)
36. Lykens, J. E., C. E. Terrell, E. E. Zoller, S. Divanovic, A. Trompette, C. L. Karp, J. Aliberti, M. J. Flick, and M. B. Jordan. 2010. Mice with a selective impairment of IFN-gamma signaling in macrophage lineage cells demonstrate the critical role of IFN-gamma-activated macrophages for the control of protozoan parasitic infections in vivo. J. Immunol. 184: 877-885.
37. Savina, A., C. Jancic, S. Hugues, P. Guermonprez, P. Vargas, I. C. Moura, A. M. Lennon-Duménil, M. C. Seabra, G. Raposo, and S. Amigorena. 2006. NOX2 controls phagosomal pH to regulate antigen processing during cross-presentation by dendritic cells. Cell 126: 205-218. (Pubitemid 44026552)
38. Kuhns, D. B., W. G. Alvord, T. Heller, J. J. Feld, K. M. Pike, B. E. Marciano, G. Uzel, S. S. DeRavin, D. A. Priel, B. P. Soule, et al. 2010. Residual NADPH oxidase and survival in chronic granulomatous disease. N. Engl. J. Med. 363: 2600-2610.
39. Ohno, Y., and J. I. Gallin. 1985. Diffusion of extracellular hydrogen peroxide into intracellular compartments of human neutrophils. Studies utilizing the inactivation of myeloperoxidase by hydrogen peroxide and azide. J. Biol. Chem. 260: 8438-8446. (Pubitemid 15011814)
40. Rex, J. H., J. E. Bennett, J. I. Gallin, H. L. Malech, and D. A. Melnick. 1990. Normal and deficient neutrophils can cooperate to damage Aspergillus fumigatus hyphae. J. Infect. Dis. 162: 523-528. (Pubitemid 20239974)
41. Roos, D., M. de Boer, F. Kuribayashi, C. Meischl, R. S. Weening, A. W. Segal, A. Ahlin, K. Nemet, J. P. Hossle, E. Bernatowska-Matuszkiewicz, and H. Middleton-Price. 1996. Mutations in the X-linked and autosomal recessive forms of chronic granulomatous disease. Blood 87: 1663-1681. (Pubitemid 26068882)
42. Björgvinsdó ttir, H., C. Ding, N. Pech, M. A. Gifford, L. L. Li, and M. C. Dinauer. 1997. Retroviral-mediated gene transfer of gp91phox into bone marrow cells rescues defect in host defense against Aspergillus fumigatus in murine X-linked chronic granulomatous disease. Blood 89: 41-48.
43. Sareila, O., T. Kelkka, A. Pizzolla, M. Hultqvist, and R. Holmdahl. 2011. NOX2 complex-derived ROS as immune regulators. Antioxid. Redox Signal. 15: 2197-2208.
44. West, A. P., I. E. Brodsky, C. Rahner, D. K. Woo, H. Erdjument-Bromage, P. Tempst, M. C. Walsh, Y. Choi, G. S. Shadel, and S. Ghosh. 2011. TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 472: 476-480.
45. Lee, K., H. Y. Won, M. A. Bae, J. H. Hong, and E. S. Hwang. 2011. Spontaneous and aging-dependent development of arthritis in NADPH oxidase 2 deficiency through altered differentiation of CD11b+ and Th/Treg cells. Proc. Natl. Acad. Sci. USA 108: 9548-9553.
46. Foster, T. J. 2005. Immune evasion by staphylococci. Nat. Rev. Microbiol. 3: 948-958. (Pubitemid 43078158)
47. Sanmun, D., E. Witasp, S. Jitkaew, Y. Y. Tyurina, V. E. Kagan, A. Ahlin, J. Palmblad, and B. Fadeel. 2009. Involvement of a functional NADPH oxidase in neutrophils and macrophages during programmed cell clearance: implications for chronic granulomatous disease. Am. J. Physiol. Cell Physiol. 297: C621-C631.
48. Hampton, M. B., M. C. Vissers, J. I. Keenan, and C. C. Winterbourn. 2002. Oxidant-mediated phosphatidylserine exposure and macrophage uptake of activated neutrophils: possible impairment in chronic granulomatous disease. J. Leukoc. Biol. 71: 775-781.
49. Fernandez-Boyanapalli, R. F., S. C. Frasch, K. McPhillips, R. W. Vandivier, B. L. Harry, D. W. Riches, P. M. Henson, and D. L. Bratton. 2009. Impaired apoptotic cell clearance in CGD due to altered macrophage programming is reversed by phosphatidylserine-dependent production of IL-4. Blood 113: 2047-2055.
50. Segal, B. H., W. Han, J. J. Bushey, M. Joo, Z. Bhatti, J. Feminella, C. G. Dennis, R. R. Vethanayagam, F. E. Yull, M. Capitano, et al. 2010. NADPH oxidase limits innate immune responses in the lungs in mice. PLoS ONE 5: e9631.
51. Mantegazza, A. R., A. Savina, M. Vermeulen, L. Pérez, J. Geffner, O. Hermine, S. D. Rosenzweig, F. Faure, and S. Amigorena. 2008. NADPH oxidase controls phagosomal pH and antigen cross-presentation in human dendritic cells. Blood 112: 4712-4722.
52. Romani, L., F. Fallarino, A. De Luca, C. Montagnoli, C. D'Angelo, T. Zelante, C. Vacca, F. Bistoni, M. C. Fioretti, U. Grohmann, et al. 2008. Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 451: 211-215.