Chronic fine particulate matter exposure induces systemic vascular dysfunction via NADPH oxidase and TLR4 pathways

Circulation Research

Volumn 108, Issue 6, 2011, Pages 716-726

  Kampfrath, Thomas ^a   Maiseyeu, Andrei ^a   Ying, Zhekang ^a   Shah, Zubair ^a   Deiuliis, Jeffrey A ^a   Xu, Xiaohua ^b   Kherada, Nisharahmed ^a   Brook, Robert D ^c   Reddy, Kongara M ^d   Padture, Nitin P ^d   Parthasarathy, Sampath ^a   Chen, Lung Chi ^e   Moffatt Bruce, Susan ^a   Sun, Qinghua ^a,b   Morawietz, Henning ^f   Rajagopalan, Sanjay ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d Ohio State University   (United States)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

monocyte; oxidized phospholipids; particulate matter; superoxide; Toll like receptor 4

Indexed keywords

1 PALMITOYL 2 ARACHIDONYL SN GLYCERO 3 PHOSPHORYLCHOLINE; CYTOKINE; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; PHOSPHOLIPID DERIVATIVE; PROTEIN P47; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

AIRBORNE PARTICLE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL HOMING; CYTOKINE RELEASE; ENZYME ACTIVATION; GENE EXPRESSION; LONG TERM EXPOSURE; LUNG LAVAGE; MACROPHAGE; MALE; MONOCYTE; MOUSE; NONHUMAN; PARTICULATE MATTER; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SYSTEMIC VASCULAR DYSFUNCTION; VASCULAR DISEASE;

ADMINISTRATION, INHALATION; AIR POLLUTANTS; ANIMALS; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVATION; INFLAMMATION; LUNG; MALE; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MICE, TRANSGENIC; NADPH OXIDASE; OXIDATION-REDUCTION; PARTICLE SIZE; PARTICULATE MATTER; PHOSPHOLIPIDS; TIME FACTORS; TOLL-LIKE RECEPTOR 4; VASCULAR DISEASES;

EID: 79953058038     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.110.237560     Document Type: Article

References (50)

1. Peters A, von Klot S, Heier M, Trentinaglia I, Hormann A, Wichmann HE, Lowel H. Exposure to traffic and the onset of myocardial infarction. N Engl J Med. 2004;351:1721-1730. (Pubitemid 39383207)
2. Peters A, Pope CA III. Cardiopulmonary mortality and air pollution. Lancet. 2002;360:1184-1185. (Pubitemid 35232712)
3. Pope CA III, Burnett RT, Krewski D, Jerrett M, Shi Y, Calle EE, Thun MJ. Cardiovascular mortality and exposure to airborne fine particulate matter and cigarette smoke: shape of the exposure-response relationship. Circulation. 2009;120:941-948.
4. Pope CA III, Ezzati M, Dockery DW. Fine-particulate air pollution and life expectancy in the United States. N Engl J Med. 2009;360: 376-386.
5. Brook RDRS, Pope III CA, Brook JR, Bhatnagar A, Diez-Roux A, Holguin F, Hong Y, Luepker R, Mittleman M, Peters A, Siscovick D, Smith SC, Whitsel L, Kaufman JD. Particulate matter air pollution and cardiovascular disease. Circulation. 2010;121:2331-2378.
6. Miller KA, Siscovick DS, Sheppard L, Shepherd K, Sullivan JH, Anderson GL, Kaufman JD. Long-term exposure to air pollution and incidence of cardiovascular events in women. N Engl J Med. 2007;356: 447-458. (Pubitemid 46193072)
7. Puett RC, Schwartz J, Hart JE, Yanosky JD, Speizer FE, Suh H, Paciorek CJ, Neas LM, Laden F. Chronic particulate exposure, mortality, and coronary heart disease in the nurses' health study. Am J Epidemiol. 2008;168:1161-1168.
8. Mills NL, Tornqvist H, Gonzalez MC, Vink E, Robinson SD, Soderberg S, Boon NA, Donaldson K, Sandstrom T, Blomberg A, Newby DE. Ischemic and thrombotic effects of dilute diesel-exhaust inhalation in men with coronary heart disease. N Engl J Med. 2007;357:1075-1082. (Pubitemid 47443212)
9. Sun Q, Wang A, Jin X, Natanzon A, Duquaine D, Brook RD, Aguinaldo JG, Fayad ZA, Fuster V, Lippmann M, Chen LC, Rajagopalan S. Long-term air pollution exposure and acceleration of atherosclerosis and vascular inflammation in an animal model. JAMA. 2005;294: 3003-3010. (Pubitemid 41817662)
10. Seaton A, Soutar A, Crawford V, Elton R, McNerlan S, Cherrie J, Watt M, Agius R, Stout R. Particulate air pollution and the blood. Thorax. 1999;54:1027-1032. (Pubitemid 29495399)
11. van Eeden SF, Tan WC, Suwa T, Mukae H, Terashima T, Fujii T, Qui D, Vincent R, Hogg JC. Cytokines involved in the systemic inflammatory response induced by exposure to particulate matter air pollutants PM(10). Am J Respir Crit Care Med. 2001;164:826-830. (Pubitemid 32881920)
12. Mutlu GM, Green D, Bellmeyer A, Baker CM, Burgess Z, Rajamannan N, Christman JW, Foiles N, Kamp DW, Ghio AJ, Chandel NS, Dean DA, Sznadjar JI, Budinger GR. Ambient particulate matter accelerates coagulation via an IL-6-dependent pathway. J Clin Invest. 2007;117: 2952-2961. (Pubitemid 47529625)
13. Dostert C, Petrilli V, Van Bruggen R, Steele C, Mossman BT, Tschopp J. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science. 2008;320:674-677. (Pubitemid 351928351)
14. Imai Y, Kuba K, Neely GG, Yaghubian-Malhami R, Perkmann T, van Loo G, Ermolaeva M, Veldhuizen R, Leung YH, Wang H, Liu H, Sun Y, Pasparakis M, Kopf M, Mech C, Bavari S, Peiris JS, Slutsky AS, Akira S, Hultqvist M, Hohmdahl R, Nicholls J, Jiang C, Binder CJ, Peninger JM. Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell. 2008;133: 235-249. (Pubitemid 351512299)
15. Kawai T, Akira S. TLR signaling. Semin Immunol. 2007;19:24-32. (Pubitemid 46498752)
16. Takeda K, Akira S. Toll-like receptors. Curr Protoc Immunol. 2007; Chapter 14:Unit 14 12.
17. Chen LC, Zhong M, Narciso S, Kleinman M, Nadziejko C, Lippmann M. Methods for Exposing Rodents and Cells to Concentrated Ambient PM using a VACES. In American Association for Aerosol Research-Particulate Matter Conference. 2003; Pittsburgh, PA.
18. Maciejczyk P, Zhong M, Li Q, Xiong J, Nadziejko C, Chen LC. Effects of subchronic exposures to concentrated ambient particles (CAPs) in mice. II. The design of a CAPs exposure system for biometric telemetry monitoring. Inhal Toxicol. 2005;17:189-197. (Pubitemid 40516017)
19. Kampfrath T, Deiuliis JA, Moffatt-Bruce SD, Anderson J, Sun Q, Wood K, Ostrowski MC, Rajagopalan S. A mouse model of yellow fluorescent protein (YFP) expression in hematopoietic cells to assess leukocyte-en-dothelial interactions in the microcirculation. Microvasc Res. 2009;78: 294-300.
20. US Environmental Protection Agency. Air Quality Criteria for Par-ticulate Matter. Washington DC: 2006. Available at http://www.epa.gov/ ttn/naaqs/pm/pm25-index.html.
21. Chen BT, Yordanov AT, Johnson GA. Ventilation-synchronous magnetic resonance microscopy of pulmonary structure and ventilation in mice. Magn Reson Med. 2005;53:69-75. (Pubitemid 40110478)
22. Chatterjee TK, Stoll LL, Denning GM, Harrelson A, Blomkalns AL, Idelman G, Rothenberg FG, Neltner B, Romig-Martin SA, Dickson EW, Ruch S, Weintraub EL. Proinflammatory phenotype of perivascular adipocytes: influence of high-fat feeding. Circ Res. 2009; 104:541-549.
23. Pacquelet S, Johnson JL, Ellis BA, Brzezinska AA, Lane WS, Munafo DB, Catz SD. Cross-talk between IRAK-4 and the NADPH oxidase. Biochem J. 2007;403:451-461. (Pubitemid 46706973)
24. Park HS, Jung HY, Park EY, Kim J, Lee WJ, Bae YS. Cutting edge: direct interaction of TLR4 with NAD(P)H oxidase 4 isozyme is essential for lipopolysaccharide-induced production of reactive oxygen species and activation of NF-kappa B. J Immunol. 2004;173: 3589-3593. (Pubitemid 39280716)
25. Laroux FS, Romero X, Wetzler Engel P, Terhorst C. Cutting edge: MyD88 controls phagocyte NADPH oxidase function and killing of gram-negative bacteria. J Immunol. 2005;175:5596-5600. (Pubitemid 41508037)
26. Li XY, Gilmour PS, Donaldson K, MacNee W. Free radical activity and pro-inflammatory effects of particulate air pollution (PM10) in vivo and in vitro. Thorax. 1996;51:1216-1222. (Pubitemid 26413140)
27. Crowther JE, Kutala VK, Kuppusamy P, Ferguson JS, Beharka AA, Zweier JL, McCormack FX, Schlesinger LS. Pulmonary surfactant protein a inhibits macrophage reactive oxygen intermediate production in response to stimuli by reducing NADPH oxidase activity. J Immunol. 2004;172:6866-6874. (Pubitemid 38669125)
28. Henning LN, Azad AK, Parsa KV, Crowther JE, Tridandapani S, Schlesinger LS. Pulmonary surfactant protein A regulates TLR expression and activity in human macrophages. J Immunol. 2008;180: 7847-7858.
29. Seaton A, MacNee W, Donaldson K, Godden D. Particulate air pollution and acute health effects [see comments]. Lancet. 1995;345: 176-178.
30. Peretz A, Peck EC, Bammler TK, Beyer RP, Sullivan JH, Trenga CA, Srinouanprachnah S, Farin FM, Kaufman JD. Diesel exhaust inhalation and assessment of peripheral blood mononuclear cell gene transcription effects: an exploratory study of healthy human volunteers. Inhal Toxicol. 2007;19:1107-1119. (Pubitemid 350072473)
31. Tan WC, Qiu D, Liam BL, Ng TP, Lee SH, van Eeden SF, D'Yachkova Y, Hogg JC. The human bone marrow response to acute air pollution caused by forest fires. Am J Respir Crit Care Med. 2000;161: 1213-1217. (Pubitemid 30243832)
32. van Eeden SF, Yeung A, Quinlam K, Hogg JC. Systemic response to ambient particulate matter: relevance to chronic obstructive pulmonary disease. Proc Am Thorac Soc. 2005;2:61-67. (Pubitemid 40562964)
33. Ghio AJ, Hall A, Bassett MA, Cascio WE, Devlin RB. Exposure to concentrated ambient air particles alters hematologic indices in humans. Inhal Toxicol. 2003;15:1465-1478. (Pubitemid 38009661)
34. Brook RD, Urch B, Dvonch JT, Bard RL, Speck M, Keeler G, Morishita M, Marsik FJ, Kamal AS, Kaciroti N, Harkema J, Corey P, Silverman F, Gold DR, Wellenius G, Mittleman MA, Rajagopalan S, Brook JR. Insights into the mechanisms and mediators of the effects of air pollution exposure on blood pressure and vascular function in healthy humans. Hypertension. 2009;54:659-667.
35. Tacke F, Alvarez D, Kaplan TJ, Jakubzick C, Spanbroek R, Llodra J, Garin A, Liu J, Mack van Rooijen N, Lira SA, Habenicht AJ, Randolph GJ. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest. 2007;117: 185-194. (Pubitemid 46048465)
36. Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, Figueiredo JL, Kohler RH, Chudnovskiy A, Waterman P, Aikawa E, Mempel TR, Libby P, Weissleder R, Pittet MJ. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science. 2009;325:612-616.
37. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity. 2003;19: 71-82. (Pubitemid 36859902)
38. Tacke F, Randolph GJ. Migratory fate and differentiation of blood monocyte subsets. Immunobiology. 2006;211:609-618.
39. Weisberg S, Hunter D, Huber R, Lemieux J, Slaymaker S, Vaddi K, Charo I, Leibel RL, and Ferrante AW Jr. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J Clin Invest. 2006;116: 115-124. (Pubitemid 43121796)
40. Tsou CL, Peters W, Si Y, Slaymaker S, Aslanian AM, Weisberg SP, Mack M, Charo IF. Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest. 2007;117:902-909. (Pubitemid 46556746)
41. Kirk EA, Sagawa ZK, McDonald TO, O'Brien KD, Heinecke JW. Monocyte chemoattractant protein deficiency fails to restrain macro-phage infiltration into adipose tissue [corrected]. Diabetes. 2008;57: 1254-1261.
42. Lassegue B, Griendling KK. NADPH oxidases: functions and pathologies in the vasculature. Arterioscler Thromb Vasc Biol. 2010; 30:653-661.
43. Rajagopalan S, Kurz S, Munzel T, Tarpey M, Freeman BA, Griendling KK, Harrison DG. Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation. Contribution to alterations of vasomotor tone. J Clin Invest. 1996;97:1916-1923.
44. Lassegue B, Griendling KK. Reactive oxygen species in hypertension; An update. Am J Hypertens. 2004;17:852-860. (Pubitemid 39201104)
45. Guzik TJ, Hoch NE, Brown KA, McCann LA, Rahman A, Dikalov S, Goronzy J, Weyand C, Harrison DG. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med. 2007;204:2449-2460. (Pubitemid 47529329)
46. Haurani MJ, Pagano PJ. Adventitial fibroblast reactive oxygen species as autacrine and paracrine mediators of remodeling: bellwether for vascular disease? Cardiovasc Res. 2007;75:679-689. (Pubitemid 47238744)
47. Siow RC, Churchman AT. Adventitial growth factor signalling and vascular remodelling: potential of perivascular gene transfer from the outside-in. Cardiovasc Res. 2007;75:659-668. (Pubitemid 47238743)
48. Lemmers B, Salmena L, Bidere N, Su H, Matysiak-Zablocki E, Murakami K, Ohashi PS, Jurisicova A, Lenardo M, Hakem R, Hakem A. Essential role for caspase-8 in Toll-like receptors and NFkappaB signaling. J Biol Chem. 2007;282:7416-7423. (Pubitemid 47093691)
49. Li X, Wang H, Qiu P, Luo H. Proteomic profiling of proteins associated with methamphetamine-induced neurotoxicity in different regions of rat brain. Neurochem Int. 2008;52:256-264. (Pubitemid 350235699)
50. Pope CA III, Dockery DW. Health effects of fine particulate air pollution: lines that connect. J Air Waste Manag Assoc. 2006;56:709-742.50. (Pubitemid 43954090)