Chlorine gas exposure causes systemic endothelial dysfunction by inhibiting endothelial nitric oxide synthase-dependent signaling

American Journal of Respiratory Cell and Molecular Biology

Volumn 45, Issue 2, 2011, Pages 419-425

  Honavar, Jaideep ^a   Samal, Andrey A ^a   Bradley, Kelley M ^a   Brandon, Angela ^a   Balanay, Joann ^b   Squadrito, Giuseppe L ^b   MohanKumar, Krishnan ^c,d   Maheshwari, Akhil ^c,d   Postlethwait, Edward M ^b   Matalon, Sadis ^b   Patel, Rakesh P ^a,b  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d University of Alabama at Birmingham   (United States)

Author keywords

Endothelium; Inflammation; Inhaled reactive oxidants; Nitric oxide

Indexed keywords

ACETYLCHOLINE; CHLORINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; NITRIC OXIDE; PHENYLEPHRINE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ARTERIAL PRESSURE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVITY; LEUKOCYTE; MALE; NONHUMAN; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; UPREGULATION; VASCULARIZATION; VASOCONSTRICTION; VASODILATATION;

ACUTE LUNG INJURY; ANIMALS; AORTA; BLOOD PRESSURE; BLOTTING, WESTERN; CHEMICAL WARFARE AGENTS; CHLORINE; CYTOKINES; ENDOTHELIUM, VASCULAR; FLUORESCENT ANTIBODY TECHNIQUE; INHALATION EXPOSURE; MALE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; VASODILATION;

ANIMALIA; RATTUS;

EID: 80051640222     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2010-0151OC     Document Type: Article

References (55)

1. Evans RB. Chlorine: state of the art. Lung 2005;183:151-167. (Pubitemid 41187517)
2. Van Sickle D, Wenck MA, Belflower A, Drociuk D, Ferdinands J, Holguin F, Svendsen E, Bretous L, Jankelevich S, Gibson JJ, et al. Acute health effects after exposure to chlorine gas released after a train derailment. Am J Emerg Med 2009;27:1-7.
3. Wenck MA, Van Sickle D, Drociuk D, Belflower A, Youngblood C, Whisnant MD, Taylor R, Rudnick V, Gibson JJ. Rapid assessment of exposure to chlorine released from a train derailment and resulting health impact. Public Health Rep 2007;122:784-792.
4. Almagro Nievas D, Acuna Castillo R, Hernandez Jerez A, Robles Montes A. Investigation of an outbreak of acute respiratory illness due to exposure to chlorine gas in a public swimming pool [in Spanish]. Gac Sanit 2008;22:287-290.
5. Cevik Y, Onay M, Akmaz I, Sezigen S. Mass casualties from acute inhalation of chlorine gas. South Med J 2009;102:1209-1213.
6. Szinicz L. History of chemical and biological warfare agents. Toxicology 2005;214:167-181. (Pubitemid 41406257)
7. Matalon S, Maull EA. Understanding and treating chlorine-induced lung injury. Proc Am Thorac Soc 2010;7:253.
8. Crouch EC, Hirche TO, Shao B, Boxio R, Wartelle J, Benabid R, McDonald B, Heinecke J, Matalon S, Belaaouaj A. Myeloperoxidase-dependent inactivation of surfactant protein d in vitro and in vivo. J Biol Chem 2010;285:16757-16770.
9. Leustik M, Doran S, Bracher A, Williams S, Squadrito GL, Schoeb TR, Postlethwait E, Matalon S. Mitigation of chlorine-induced lung injury by low-molecular-weight antioxidants. Am J Physiol Lung Cell Mol Physiol 2008;295:L733-L743.
10. Song W, Wei S, Zhou Y, Lazrak A, Liu G, Londino JD, Squadrito GL, Matalon S. Inhibition of lung fluid clearance and epithelial Na+ channels by chlorine, hypochlorous acid, and chloramines. J Biol Chem 2010;285:9716-9728.
11. Donnelly SC, FitzGerald MX. Reactive airways dysfunction syndrome (RADS) due to chlorine gas exposure. Ir J Med Sci 1990;159:275-276, discussion 276-277.
12. Gunnarsson M, Walther SM, Seidal T, Bloom GD, Lennquist S. Exposure to chlorine gas: effects on pulmonary function and morphology in anaesthetised and mechanically ventilated pigs. J Appl Toxicol 1998;18:249-255. (Pubitemid 28360803)
13. Martin JG, Campbell HR, Iijima H, Gautrin D, Malo JL, Eidelman DH, Hamid Q, Maghni K. Chlorine-induced injury to the airways in mice. Am J Respir Crit Care Med 2003;168:568-574. (Pubitemid 37088600)
14. Tian X, Tao H, Brisolara J, Chen J, Rando RJ, Hoyle GW. Acute lung injury induced by chlorine inhalation in c57bl/6 and fvb/n mice. Inhal Toxicol 2008;20:783-793. (Pubitemid 352032210)
15. Tuck SA, Ramos-Barbon D, Campbell H, McGovern T, Karmouty-Quintana H, Martin JG. Time course of airway remodelling after an acute chlorine gas exposure in mice. Respir Res 2008;9:61.
16. Uyan ZS, Carraro S, Piacentini G, Baraldi E. Swimming pool, respiratory health, and childhood asthma: should we change our beliefs? Pediatr Pulmonol 2009;44:31-37.
17. Song W, Wei S, Liu G, Yu Z, Estell K, Yadav A, Schwiebert L, Matalon S. Post exposure administration of a b2-agonist decreased chlorine induced airway hyperreactivity in mice. Am J Respir Cell Mol Biol (In press)
18. Chuang GC, Yang Z, Westbrook DG, Pompilius M, Ballinger CA, White CR, Krzywanski DM, Postlethwait EM, Ballinger SW. Pulmonary ozone exposure induces vascular dysfunction, mitochondrial damage, and atherogenesis. Am J Physiol Lung Cell Mol Physiol 2009;297:L209-L216.
19. Guo X, Oldham MJ, Kleinman MT, Phalen RF, Kassab GS. Effect of cigarette smoking on nitric oxide, structural, and mechanical properties of mouse arteries. Am J Physiol Heart Circ Physiol 2006;291:H2354-H2361.
20. Knuckles TL, Lund AK, Lucas SN, Campen MJ. Diesel exhaust exposure enhances venoconstriction via uncoupling of enos. Toxicol Appl Pharmacol 2008;230:346-351.
21. Mills NL, Donaldson K, Hadoke PW, Boon NA, MacNee W, Cassee FR, Sandstrom T, Blomberg A, Newby DE. Adverse cardiovascular effects of air pollution. Nat Clin Pract Cardiovasc Med 2009;6:36-44.
22. Moncada S. Nitric oxide: discovery and impact on clinical medicine. J R Soc Med 1999;92:164-169. (Pubitemid 29213859)
23. Napoli C, Ignarro LJ. Nitric oxide and pathogenic mechanisms involved in the development of vascular diseases. Arch Pharm Res 2009;32:1103-1108.
24. Al-Qaisi M, Kharbanda RK, Mittal TK, Donald AE. Measurement of endothelial function and its clinical utility for cardiovascular risk. Vasc Health Risk Manag 2008;4:647-652. (Pubitemid 352037922)
25. Widlansky ME, Gokce N, Keaney JF Jr, Vita JA. The clinical implications of endothelial dysfunction. J Am Coll Cardiol 2003;42:1149-1160. (Pubitemid 37188333)
26. Squadrito GL, Postlethwait EM, Matalon S. Elucidating mechanisms of chlorine toxicity: reaction kinetics, thermodynamics, and physiological implications. Am J Physiol Lung Cell Mol Physiol 2010;299:L289-L300.
27. Bergt C, Pennathur S, Fu X, Byun J, O'Brien K, McDonald TO, Singh P, Anantharamaiah GM, Chait A, Brunzell J, et al. The myeloperoxidase product hypochlorous acid oxidizes hdl in the human artery wall and impairs abca1-dependent cholesterol transport. Proc Natl Acad Sci USA 2004;101:13032-13037. (Pubitemid 39167578)
28. Marsche G, Heller R, Fauler G, Kovacevic A, Nuszkowski A, Graier W, Sattler W, Malle E. 2-chlorohexadecanal derived from hypochlorite-modified high-density lipoprotein-associated plasmalogen is a natural inhibitor of endothelial nitric oxide biosynthesis. Arterioscler Thromb Vasc Biol 2004;24:2302-2306. (Pubitemid 39658033)
29. Marsche G, Semlitsch M, Hammer A, Frank S, Weigle B, Demling N, Schmidt K, Windischhofer W, Waeg G, Sattler W, et al. Hypochlorite-modified albumin colocalizes with RAGE in the artery wall and promotes MCP-1 expression via the RAGE-Erk1/2 MAP-kinase pathway. FASEB J 2007;21:1145-1152. (Pubitemid 46495704)
30. McCall MR, Carr AC, Forte TM, Frei B. LDL modified by hypochlorous acid is a potent inhibitor of lecithin-cholesterol acyltransferase activity. Arterioscler Thromb Vasc Biol 2001;21:1040-1045. (Pubitemid 34168666)
31. McMillen TS, Heinecke JW, LeBoeuf RC. Expression of human myeloperoxidase by macrophages promotes atherosclerosis in mice. Circulation 2005;111:2798-2804. (Pubitemid 40791552)
32. Stocker R, Huang A, Jeranian E, Hou JY, Wu TT, Thomas SR, Keaney JF Jr. Hypochlorous acid impairs endothelium-derived nitric oxide bioactivity through a superoxide-dependent mechanism. Arterioscler Thromb Vasc Biol 2004;24:2028-2033. (Pubitemid 39482425)
33. Xu J, Xie Z, Reece R, Pimental D, Zou MH. Uncoupling of endothelial nitric oxidase synthase by hypochlorous acid: role of NAD(P)H oxidase-derived superoxide and peroxynitrite. Arterioscler Thromb Vasc Biol 2006;26:2688-2695.
34. Yang J, Cheng Y, Ji R, Zhang C. Novel model of inflammatory neointima formation reveals a potential role of myeloperoxidase in neointimal hyperplasia. Am J Physiol Heart Circ Physiol 2006;291:H3087-H3093. (Pubitemid 44904111)
35. Zhang C, Patel R, Eiserich JP, Zhou F, Kelpke S, Ma W, Parks DA, Darley-Usmar V, White CR. Endothelial dysfunction is induced by proinflammatory oxidant hypochlorous acid. Am J Physiol Heart Circ Physiol 2001;281:H1469-H1475.
36. Zhang C, Reiter C, Eiserich JP, Boersma B, Parks DA, Beckman JS, Barnes S, Kirk M, Baldus S, Darley-Usmar VM, et al. L-arginine chlorination products inhibit endothelial nitric oxide production. J Biol Chem 2001;276:27159-27165.
37. Zheng L, Nukuna B, Brennan ML, Sun M, Goormastic M, Settle M, Schmitt D, Fu X, Thomson L, Fox PL, et al. Apolipoprotein A-I is a selective target for myeloperoxidase-catalyzed oxidation and functional impairment in subjects with cardiovascular disease. J Clin Invest 2004;114:529-541. (Pubitemid 39572103)
38. Zheng L, Settle M, Brubaker G, Schmitt D, Hazen SL, Smith JD, Kinter M. Localization of nitration and chlorination sites on apolipoprotein A-I catalyzed by myeloperoxidase in human atheroma and associated oxidative impairment in ABCA1-dependent cholesterol efflux from macrophages. J Biol Chem 2005;280:38-47. (Pubitemid 40164962)
39. Bell DP. Management of acute respiratory distress syndrome (ARDS) following chlorine exposure [abstract]. Am J Respir Crit Care Med 2008;176:A314.
40. Svendsen ER, Whittle NC, Sanders L, McKeown RE, Sprayberry K, Heim M, Caldwell R, Gibson JJ, Vena JE. Grace: public health recovery methods following an environmental disaster. Arch Environ Occup Health 2010;65:77-85.
41. Yadav AK, Bracher A, Doran SF, Leustik M, Squadrito GL, Postlethwait EM, Matalon S. Mechanisms and modification of chlorine-induced lung injury in animals. Proc Am Thorac Soc 2010;7:278-283.
42. Vitturi DA, Teng X, Toledo JC, Matalon S, Lancaster JR Jr, Patel RP. Regulation of nitrite transport in red blood cells by hemoglobin oxygen fractional saturation. Am J Physiol Heart Circ Physiol 2009;296:H1398-H1407.
43. Shaik SS, Soltau TD, Chaturvedi G, Totapally B, Hagood JS, Andrews WW, Athar M, Voitenok NN, Killingsworth CR, Patel RP, et al. Low intensity shear stress increases endothelial elr+ cxc chemokine production via a focal adhesion kinase-p38{beta} MAPK-NF-{kappa}B pathway. J Biol Chem 2009;284:5945-5955.
44. O'Donnell VB, Freeman BA. Interactions between nitric oxide and lipid oxidation pathways: implications for vascular disease. Circ Res 2001;88:12-21. (Pubitemid 32064077)
45. Patel RP, McAndrew J, Sellak H, White CR, Jo H, Freeman BA, Darley-Usmar VM. Biological aspects of reactive nitrogen species. Biochim Biophys Acta 1999;1411:385-400. (Pubitemid 29221963)
46. White CR, Darley-Usmar V, Berrington WR, McAdams M, Gore JZ, Thompson JA, Parks DA, Tarpey MM, Freeman BA. Circulating plasma xanthine oxidase contributes to vascular dysfunction in hypercholesterolemic rabbits. Proc Natl Acad Sci USA 1996;93:8745-8749. (Pubitemid 26269631)
47. 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 2004;279:963-969. (Pubitemid 38082617)
48. Demnati R, Fraser R, Martin JG, Plaa G, Malo JL. Effects of dexamethasone on functional and pathological changes in rat bronchi caused by high acute exposure to chlorine. Toxicol Sci 1998;45:242-246. (Pubitemid 28516665)
49. Kim SF, Huri DA, Snyder SH. Inducible nitric oxide synthase binds, S-nitrosylates, and activates cyclooxygenase-2. Science 2005;310:1966-1970. (Pubitemid 43005992)
50. Beach FX, Jones ES, Scarrow GD. Respiratory effects of chlorine gas. Br J Ind Med 1969;26:231-236.
51. Kleinbongard P, Dejam A, Lauer T, Rassaf T, Schindler A, Picker O, Scheeren T, Godecke A, Schrader J, Schulz R, et al. Plasma nitrite reflects constitutive nitric oxide synthase activity in mammals. Free Radic Biol Med 2003;35:790-796. (Pubitemid 37329482)
52. Gao X, Xu X, Belmadani S, Park Y, Tang Z, Feldman AM, Chilian WM, Zhang C. TNF-alpha contributes to endothelial dysfunction by upregulating arginase in ischemia/reperfusion injury. Arterioscler Thromb Vasc Biol 2007;27:1269-1275. (Pubitemid 46809414)
53. Thukkani AK, McHowat J, Hsu FF, Brennan ML, Hazen SL, Ford DA. Identification of alpha-chloro fatty aldehydes and unsaturated lysophosphatidylcholine molecular species in human atherosclerotic lesions. Circulation 2003;108:3128-3133. (Pubitemid 38031803)
54. Soro-Paavonen A, Zhang WZ, Venardos K, Coughlan MT, Harris E, Tong DC, Brasacchio D, Paavonen K, Chin-Dusting J, Cooper ME, et al. Advanced glycation end-products induce vascular dysfunction via resistance to nitric oxide and suppression of endothelial nitric oxide synthase. J Hypertens 2010;28:780-788.
55. Chang PC, Chen TH, Chang CJ, Hou CC, Chan P, Lee HM. Advanced glycosylation end products induce inducible nitric oxide synthase (INOS) expression via a p38 MAPK-dependent pathway. Kidney Int 2004;65:1664-1675. (Pubitemid 38591014)