Augmented inducible nitric oxide synthase expression and increased NO production reduce sepsis-induced lung injury and mortality in myeloperoxidase-null mice

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 295, Issue 1, 2008, Pages

  Brovkovych, Viktor ^a   Gao, Xiao Pei ^a   Ong, Evan ^a   Brovkovych, Svitlana ^a   Brennan, Marie Luise ^b   Su, Xiao ^a   Hazen, Stanley L ^b   Malik, Asrar B ^a   Skidgel, Randal A ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Endotoxin shock; Host defense; Inflammation; Rodent

Indexed keywords

3 NITROTYROSINE; INDUCIBLE NITRIC OXIDE SYNTHASE; MYELOPEROXIDASE; 3-NITROTYROSINE; DRUG DERIVATIVE; NITRIC OXIDE; NOS2 PROTEIN, MOUSE; OXIDIZING AGENT; PEROXIDASE; TYROSINE;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL COLONIZATION; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ESCHERICHIA COLI; LUNG EDEMA; LUNG INJURY; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEPSIS; SURVIVAL RATE; ANIMAL; BIOSYNTHESIS; ENTEROBACTER INFECTION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; INJURY; LUNG; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; NEUTROPHIL; PATHOLOGY;

ANIMALS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; LUNG; MICE; MICE, KNOCKOUT; NEUTROPHILS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; OXIDANTS; PEROXIDASE; PULMONARY EDEMA; SEPSIS; TYROSINE;

EID: 49049100515     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00450.2007     Document Type: Article

References (43)

1. Abu-Soud HM, Hazen SL. Nitric oxide is a physiological substrate for mammalian peroxidases. J Biol Chem 275: 37524-37532, 2000.
2. Abu-Soud HM, Hazen SL. Nitric oxide modulates the catalytic activity of myeloperoxidase. J Biol Chem 275: 5425-5430, 2000.
3. Anderson HD, Rahmutula D, Gardner DG. Tumor necrosis factor-alpha inhibits endothelial nitric-oxide synthase gene promoter activity in bovine aortic endothelial cells. J Biol Chem 279: 963-969, 2004.
4. Bogdan C. Of microbes, macrophages and nitric oxide. Behring Inst Mitt: 58-72, 1997.
5. Brennan ML, Anderson MM, Shih DM, Qu XD, Wang X, Mehta AC, Lim LL, Shi W, Hazen SL, Jacob JS, Crowley JR, Heinecke JW, Lusis AJ. Increased atherosclerosis in myeloperoxidase-deficient mice. J Clin Invest 107: 419-430, 2001.
6. Brovkovych V, Stolarczyk E, Oman J, Tomboulian P, Malinski T. Direct electrochemical measurement of nitric oxide in vascular endothelium. J Pharm Biomed Anal 19: 135-143, 1999.
7. Cirino G, Fiorucci S, Sessa WC. Endothelial nitric oxide synthase: the Cinderella of inflammation? Trends Pharmacol Sci 24: 91-95, 2003.
8. Closs EI, Scheld JS, Sharafi M, Forstermann U. Substrate supply for nitric-oxide synthase in macrophages and endothelial cells: role of cationic amino acid transporters. Mol Pharmacol 57: 68-74, 2000.
9. Cuzzocrea S, Mazzon E, Dugo L, Barbera A, Centorrino T, Ciccolo A, Fonti MT, Caputi AP. Inducible nitric oxide synthase knockout mice exhibit resistance to the multiple organ failure induced by zymosan. Shock 16: 51-58, 2001.
10. Dikshit M, Sharma P. Nitric oxide mediated modulation of free radical generation response in the rat polymorphonuclear leukocytes: a flowcytometric study. Methods Cell Sci 24: 69-76, 2002.
11. Eiserich JP, Baldus S, Brennan ML, Ma W, Zhang C, Tousson A, Castro L, Lusis AJ, Nauseef WM, White CR, Freeman BA. Myeloperoxidase, a leukocyte-derived vascular NO oxidase. Science 296: 2391-2394, 2002.
12. Eiserich JP, Hristova M, Cross CE, Jones AD, Freeman BA, Halliwell B, van der Vliet A. Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature 391: 393-397, 1998.
13. Galijasevic S, Saed GM, Diamond MP, Abu-Soud HM. Myeloperoxidase up-regulates the catalytic activity of inducible nitric oxide synthase by preventing nitric oxide feedback inhibition. Proc Natl Acad Sci USA 100: 14766-14771, 2003.
14. Gao XP, Zhu X, Fu J, Liu Q, Frey RS, Malik AB. Blockade of class IA phosphoinositide 3-kinase in neutrophils prevents NADPH oxidase activation-and adhesion-dependent inflammation. J Biol Chem 282: 6116-6125, 2007.
15. Hampton MB, Kettle AJ, Winterbourn CC. Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 92: 3007-3017, 1998.
16. Hampton MB, Kettle AJ, Winterbourn CC. Involvement of superoxide and myeloperoxidase in oxygen-dependent killing of Staphylococcus aureus by neutrophils. Infect Immun 64: 3512-3517, 1996.
17. Hazen SL, Zhang R, Shen Z, Wu W, Podrez EA, MacPherson JC, Schmitt D, Mitra SN, Mukhopadhyay C, Chen Y, Cohen PA, Hoff HF, Abu-Soud HM. Formation of nitric oxide-derived oxidants by myeloperoxidase in monocytes: pathways for monocyte-mediated protein nitration and lipid peroxidation in vivo. Circ Res 85: 950-958, 1999.
18. Hickman-Davis JM, Lindsey JR, Matalon S. Cyclophosphamide decreases nitrotyrosine formation and inhibits nitric oxide production by alveolar macrophages in mycoplasmosis. Infect Immun 69: 6401-6410, 2001.
19. Hickman-Davis JM, McNicholas-Bevensee C, Davis IC, Ma HP, Davis GC, Bosworth CA, Matalon S. Reactive species mediate inhibition of alveolar type II sodium transport during mycoplasma infection. Am J Respir Crit Care Med 173: 334-344, 2006.
20. Hogg N, Kalyanaraman B. Nitric oxide and lipid peroxidation. Biochim Biophys Acta 1411: 378-384, 1999.
21. Kaku Y, Nanri H, Sakimura T, Ejima K, Kuroiwa A, Ikeda M. Differential induction of constitutive and inducible nitric oxide synthases by distinct inflammatory stimuli in bovine aortic endothelial cells. Biochim Biophys Acta 1356: 43-52, 1997.
22. Klebanoff SJ. Myeloperoxidase: friend and foe. J Leukoc Biol 77: 598-625, 2005.
23. Kristof AS, Goldberg P, Laubach V, Hussain SN. Role of inducible nitric oxide synthase in endotoxin-induced acute lung injury. Am J Respir Crit Care Med 158: 1883-1889, 1998.
24. Kumar AP, Ryan C, Cordy V, Reynolds WF. Inducible nitric oxide synthase expression is inhibited by myeloperoxidase. Nitric Oxide 13: 42-53, 2005.
25. Lai PF, Mohamed F, Monge JC, Stewart DJ. Downregulation of eNOS mRNA expression by TNFalpha: identification and functional characterization of RNA-protein interactions in the 3′UTR. Cardiovasc Res 59: 160-168, 2003.
26. Lanza F. Clinical manifestation of myeloperoxidase deficiency. J Mol Med 76: 676-681, 1998.
27. Lowell C, Fumagalli L, Berton G. Deficiency of Src family kinases p59/61hck and p58c-fgr results in defective adhesion-dependent neutrophil functions. J Cell Biol 133: 895-910, 1996.
28. Ong ES, Gao XP, Xu N, Predescu D, Rahman A, Broman MT, Jho DH, Malik AB. E. coli pneumonia induces CD18-independent airway neutrophil migration in the absence of increased lung vascular permeability. Am J Physiol Lung Cell Mol Physiol 285: L879-L888, 2003.
29. Pacelli R, Wink DA, Cook JA, Krishna MC, DeGraff W, Friedman N, Tsokos M, Samuni A, Mitchell JB. Nitric oxide potentiates hydrogen peroxide-induced killing of Escherichia coli. J Exp Med 182: 1469-1479, 1995.
30. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87: 315-424, 2007.
31. Quinn MT, Gauss KA. Structure and regulation of the neutrophil respiratory burst oxidase: comparison with nonphagocyte oxidases. J Leukoc Biol 76: 760-781, 2004.
32. Schmekel B, Venge P. The distribution of myeloperoxidase, eosinophil cationic protein, albumin and urea in sequential bronchoalveolar lavage. Eur Respir J 4: 517-523, 1991.
33. Segal BH, Leto TL, Gallin JI, Malech HL, Holland SM. Genetic, biochemical, and clinical features of chronic granulomatous disease. Medicine 79: 170-200, 2000.
34. Sethi S, Sharma P, Dikshit M. Nitric oxide- and oxygen-derived free radical generation from control and lipopolysaccharide-treated rat polymorphonuclear leukocyte. Nitric Oxide 5: 482-493, 2001.
35. Shepherd VL. The role of the respiratory burst of phagocytes in host defense. Semin Respir Infect 1: 99-106, 1986.
36. Skidgel RA, Gao XP, Brovkovych V, Rahman A, Jho D, Predescu S, Standiford TJ, Malik AB. Nitric oxide stimulates macrophage inflammatory protein-2 expression in sepsis. J Immunol 169: 2093-2101, 2002.
37. Su X, Lee JW, Matthay ZA, Mednick G, Uchida T, Fang X, Gupta N, Matthay MA. Activation of the alpha7 nAChR reduces acid-induced acute lung injury in mice and rats. Am J Respir Cell Mol Biol 37: 186-192, 2007.
38. Tiruppathi C, Naqvi T, Wu Y, Vogel SM, Minshall RD, Malik AB. Albumin mediates the transcytosis of myeloperoxidase by means of caveolae in endothelial cells. Proc Natl Acad Sci USA 101: 7699-7704, 2004.
39. Tsan MF, Turkall RM. Degradation and oxidation of methionine enkephalin by human neutrophils. J Reticuloendothel Soc 31: 353-360, 1982.
40. Virta M, Karp M, Vuorinen P. Nitric oxide donor-mediated killing of bioluminescent Escherichia coli. Antimicrob Agents Chemother 38: 2775-2779, 1994.
41. Wahl SM, McCartney-Francis N, Chan J, Dionne R, Ta L, Orenstein JM. Nitric oxide in experimental joint inflammation. Benefit or detriment? Cells Tissues Organs 174: 26-33, 2003.
42. Whiteman M, Chu SH, Siau JL, Rose P, Sabapathy K, Schantz JT, Cheung NS, Spencer JP, Armstrong JS. The pro-inflammatory oxidant hypochlorous acid induces Bax-dependent mitochondrial permeabilisation and cell death through AIF-/EndoG-dependent pathways. Cell Signal 19: 705-714, 2007.
43. Zhang R, Brennan ML, Shen Z, MacPherson JC, Schmitt D, Molenda CE, Hazen SL. Myeloperoxidase functions as a major enzymatic catalyst for initiation of lipid peroxidation at sites of inflammation. J Biol Chem 277: 46116-46122, 2002.