NOX2 protects against prolonged inflammation, lung injury, and mortality following systemic insults

Journal of Innate Immunity

Volumn 5, Issue 6, 2013, Pages 565-580

  Whitmore, Laura C ^a,b,c   Hilkin, Brieanna M ^a,b   Goss, Kelli L ^a,b   Wahle, Erin M ^d   Colaizy, Tarah T ^a   Boggiatto, Paola M ^a   Varga, Steven M ^a   Miller, Francis J ^d   Moreland, Jessica G ^a,b,c  

^a UNIVERSITY OF IOWA   (United States)

^b Inflammation Program   (United States)

^c Molecular and Cellular Biology Program   (United States)

^d Department of Internal Medicine ^*  (United States)

Author keywords

Chronic granulomatous disease; Gp91phox; Inflammation; NOX2; Systemic inflammatory response syndrome

Indexed keywords

CHEMOKINE RECEPTOR CXCR2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; ZYMOSAN;

ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; BONE MARROW; CD4+ T LYMPHOCYTE; COMPARATIVE STUDY; CONTROLLED STUDY; DOSE RESPONSE; GENOTYPE; HYPOTENSION; HYPOTHERMIA; LEUKOPENIA; LUNG ALVEOLUS; LUNG HEMORRHAGE; LUNG INJURY; MALE; MORTALITY; MOUSE; NEUTROPHIL; NONHUMAN; PERITONEUM; PHENOTYPE; PRIORITY JOURNAL; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; UPREGULATION; ANIMAL EXPERIMENT; ANTIINFLAMMATORY ACTIVITY; CHRONIC GRANULOMATOUS DISEASE; CYTOKINE PRODUCTION;

ANIMALS; APOPTOSIS; CYTOKINES; FLOW CYTOMETRY; INFLAMMATION; KAPLAN-MEIER ESTIMATE; LUNG; LUNG INJURY; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; NADPH OXIDASE; NEUTROPHIL INFILTRATION; PERITONEUM; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; T-LYMPHOCYTES;

EID: 84888307493     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000347212     Document Type: Article

References (39)

1. Robertson CM, Coopersmith CM: The systemic inflammatory response syndrome. Microbes Infect 2006; 8: 1382-1389.
2. Adib-Conquy M, Cavaillon JM: Compensatory anti-inflammatory response syndrome. Thromb Haemost 2009; 101: 36-47.
3. Galley HF, Howdle PD, Walker BE, Webster NR: The effects of intravenous antioxidants in patients with septic shock. Free Radic Biol Med 1997; 23: 768-774.
4. Spies CD, Reinhart K, Witt I, Meier-Hellmann A, Hannemann L, Bredle DL, Schaffartzik W: Influence of N-acetylcysteine on indirect indicators of tissue oxygenation in septic shock patients: results from a prospective, randomized, double-blind study. Crit Care Med 1994; 22: 1738-1746.
5. Peake SL, Moran JL, Leppard PI: N-acetyl-Lcysteine depresses cardiac performance in patients with septic shock. Crit Care Med 1996; 24: 1302-1310.
6. Holland SM: Chronic granulomatous disease. Clin Rev Allergy Immunol 2010; 38: 3-10.
7. Winkelstein JA, Marino MC, Johnston RB Jr, Boyle J, Curnutte J, Gallin JI, Malech HL, Holland SM, Ochs H, Quie P, Buckley RH, Foster CB, Chanock SJ, Dickler H: Chronic granulomatous disease. Report on a national registry of 368 patients. Medicine (Baltimore) 2000; 79: 155-169.
8. Rieber N, Hector A, Kuijpers T, Roos D, Hartl D: Current concepts of hyperinflammation in chronic granulomatous disease. Clin Dev Immunol 2012; 2012: 252460.
9. Schappi MG, Jaquet V, Belli DC, Krause KH: Hyperinflammation in chronic granulomatous disease and anti-inflammatory role of the phagocyte NADPH oxidase. Semin Immunopathol 2008; 30: 255-271.
10. Moreland JG, Davis AP, Matsuda JJ, Hook JS, Bailey G, Nauseef WM, Lamb FS: Endotoxin priming of neutrophils requires NADPH oxidase-generated oxidants and is regulated by the anion transporter ClC-3. J Biol Chem 2007; 282: 33958-33967.
11. Pollock JD, Williams DA, Gifford MA, Li LL, Du X, Fisherman J, Orkin SH, Doerschuk CM, Dinauer MC: Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat Genet 1995; 9: 202-209.
12. Mastroeni P, Vazquez-Torres A, Fang FC, Xu Y, Khan S, Hormaeche CE, Dougan G: Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. II. Effects on microbial proliferation and host survival in vivo. J Exp Med 2000; 192: 237-248.
13. Aratani Y, Kura F, Watanabe H, Akagawa H, Takano Y, Suzuki K, Dinauer MC, Maeda N, Koyama H: Critical role of myeloperoxidase and nicotinamide adenine dinucleotide phosphate-oxidase in high-burden systemic infection of mice with Candida albicans. J Infect Dis 2002; 185: 1833-1837.
14. Zhang WJ, Wei H, Frei B: Genetic deficiency of NADPH oxidase does not diminish, but rather enhances, LPS-induced acute inflammatory responses in vivo. Free Radic Biol Med 2009; 46: 791-798.
15. Zhang WJ, Wei H, Tien YT, Frei B: Genetic ablation of phagocytic NADPH oxidase in mice limits TNFα-induced inflammation in the lungs but not other tissues. Free Radic Biol Med 2011; 50: 1517-1525.
16. Segal BH, Han W, Bushey JJ, Joo M, Bhatti Z, Feminella J, Dennis CG, Vethanayagam RR, Yull FE, Capitano M, Wallace PK, Minderman H, Christman JW, Sporn MB, Chan J, Vinh DC, Holland SM, Romani LR, Gaffen SL, Freeman ML, Blackwell TS: NADPH oxidase limits innate immune responses in the lungs in mice. PLoS One 2010; 5:e9631.
17. van de Loo FA, Bennink MB, Arntz OJ, Smeets RL, Lubberts E, Joosten LA, van Lent PL, Coenen-de Roo CJ, Cuzzocrea S, Segal BH, Holland SM, van den Berg WB: Deficiency of NADPH oxidase components p47phox and gp91phox caused granulomatous synovitis and increased connective tissue destruction in experimental arthritis models. Am J Pathol 2003; 163: 1525-1537.
18. Volman TJ, Hendriks T, Goris RJ: Zymosaninduced generalized inflammation: experimental studies into mechanisms leading to multiple organ dysfunction syndrome. Shock 2005; 23: 291-297.
19. Lee K, Won HY, Bae MA, Hong JH, Hwang ES: 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 2011; 108: 9548-9553.
20. Horvath R, Rozkova D, Lastovicka J, Polouckova A, Sedlacek P, Sediva A, Spisek R: Expansion of T helper type 17 lymphocytes in patients with chronic granulomatous disease. Clin Exp Immunol 2011; 166: 26-33.
21. Martin B, Hirota K, Cua DJ, Stockinger B, Veldhoen M: Interleukin-17-producing γδ T cells selectively expand in response to pathogen products and environmental signals. Immunity 2009; 31: 321-330.
22. Matsushima A, Ogura H, Fujita K, Koh T, Tanaka H, Sumi Y, Yoshiya K, Hosotsubo H, Kuwagata Y, Shimazu T, Sugimoto H: Early activation of γδ T lymphocytes in patients with severe systemic inflammatory response syndrome. Shock 2004; 22: 11-15.
23. Luo HR, Loison F: Constitutive neutrophil apoptosis: mechanisms and regulation. Am J Hematol 2008; 83: 288-295.
24. Crimi E, Sica V, Williams-Ignarro S, Zhang H, Slutsky AS, Ignarro LJ, Napoli C: The role of oxidative stress in adult critical care. Free Radic Biol Med 2006; 40: 398-406.
25. Impellizzeri D, Mazzon E, Di Paola R, Paterniti I, Bramanti P, Cuzzocrea S: Effect of NADPH-oxidase inhibitors in the experimental model of zymosan-induced shock in mice. Free Radic Res 2011; 45: 820-834.
26. Cuzzocrea S, Costantino G, Mazzon E, Caputi AP: Protective effect of N-acetylcysteine on multiple organ failure induced by zymosan in the rat. Crit Care Med 1999; 27: 1524-1532.
27. Leaver SK, Evans TW: Acute respiratory distress syndrome. BMJ 2007; 335: 389-394.
28. Bianchi ME: DAMPS, PAMPS and alarmins: all we need to know about danger. J Leukoc Biol 2007; 81: 1-5.
29. Hsieh CH, Frink M, Hsieh YC, Kan WH, Hsu JT, Schwacha MG, Choudhry MA, Chaudry IH: The role of MIP-1 alpha in the development of systemic inflammatory response and organ injury following trauma hemorrhage. J Immunol 2008; 181: 2806-2812.
30. Iwakura Y, Ishigame H, Saijo S, Nakae S: Functional specialization of interleukin-17 family members. Immunity 2011; 34: 149-162.
31. Romani L, Fallarino F, De Luca A, Montagnoli C, D'Angelo C, Zelante T, Vacca C, Bistoni F, Fioretti MC, Grohmann U, Segal BH, Puccetti P: Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 2008; 451: 211-215.
32. Reynolds JM, Pappu BP, Peng J, Martinez GJ, Zhang Y, Chung Y, Ma L, Yang XO, Nurieva RI, Tian Q, Dong C: Toll-like receptor 2 signaling in CD4(+) T lymphocytes promotes T helper 17 responses and regulates the pathogenesis of autoimmune disease. Immunity 2010; 32: 692-702.
33. Duffin R, Leitch AE, Fox S, Haslett C, Rossi AG: Targeting granulocyte apoptosis: mechanisms, models, and therapies. Immunol Rev 2010; 236: 28-40.
34. Rieber N, Hector A, Kuijpers T, Roos D, Hartl D: Current concepts of hyperinflammation in chronic granulomatous disease. Clin Dev Immunol 2012; 2012: 252460.
35. Sica A, Mantovani A: Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 2012; 122: 787-795.
36. Bystrom J, Evans I, Newson J, Stables M, Toor I, van Rooijen N, Crawford M, Colville-Nash P, Farrow S, Gilroy DW: Resolution-phase macrophages possess a unique inflammatory phenotype that is controlled by cAMP. Blood 2008; 112: 4117-4127.
37. Menten P, Wuyts A, Van Damme J: Macrophage inflammatory protein-1. Cytokine Growth Factor Rev 2002; 13: 455-481.
38. Balamayooran G, Batra S, Balamayooran T, Cai S, Jeyaseelan S: Monocyte chemoattractant protein 1 regulates pulmonary host defense via neutrophil recruitment during Escherichia coli infection. Infect Immun 2011; 79: 2567-2577.
39. Fernandez-Boyanapalli RF, Frasch SC, McPhillips K, Vandivier RW, Harry BL, Riches DW, Henson PM, Bratton DL: Impaired apoptotic cell clearance in CGD due to altered macrophage programming is reversed by phosphatidylserine- dependent production of IL-4. Blood 2009; 113: 2047-2055.