β2-Adrenergic agonists augment air pollution-induced IL-6 release and thrombosis

Journal of Clinical Investigation

Volumn 124, Issue 7, 2014, Pages 2935-2946

  Chiarella, Sergio E ^a   Soberanes, Saul ^a   Urich, Daniela ^a   Morales Nebreda, Luisa ^a   Nigdelioglu, Recep ^a   Green, David ^a   Young, James B ^a   Gonzalez, Angel ^a   Rosario, Carmen ^a   Misharin, Alexander V ^a   Ghio, Andrew J ^b   Wunderink, Richard G ^a   Donnelly, Helen K ^a   Radigan, Kathryn A ^a   Perlman, Harris ^a   Chandel, Navdeep S ^a   Budinger, G R Scott ^a   Mutlu, Gökhan M ^a,c  

^a NORTHWESTERN UNIVERSITY   (United States)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; BETA 2 ADRENERGIC RECEPTOR; CATECHOLAMINE; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; FORMOTEROL; FORSKOLIN; INTERLEUKIN 6; PROPRANOLOL; REACTIVE OXYGEN METABOLITE; SALBUTAMOL;

ADRENERGIC SYSTEM; AIR POLLUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY THROMBOSIS; ARTICLE; AUGMENTATION INDEX; CYTOKINE RELEASE; DRUG MECHANISM; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LUNG ALVEOLUS MACROPHAGE; MITOCHONDRION; MOUSE; NONHUMAN; PARTICULATE MATTER; PHARMACOLOGICAL PARAMETERS; PNEUMONIA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION;

ADENYLATE CYCLASE; ADRENERGIC BETA-2 RECEPTOR AGONISTS; ANIMALS; ANTITHROMBIN III; BRONCHOALVEOLAR LAVAGE FLUID; CATECHOLAMINES; COLFORSIN; HUMANS; INTERLEUKIN-6; MACROPHAGES, ALVEOLAR; MALE; MICE; MICE, KNOCKOUT; PARTICULATE MATTER; PEPTIDE HYDROLASES; PROPRANOLOL; REACTIVE OXYGEN SPECIES; RECEPTORS, ADRENERGIC, BETA; RECEPTORS, ADRENERGIC, BETA-1; THROMBOSIS;

EID: 84903780974     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI75157     Document Type: Article

References (75)

1. Pope CA 3rd, Ezzati M, Dockery DW. Fine-particulate air pollution and life expectancy in the United States. N Engl J Med. 2009;360(4):376-386.
2. UN Environment Program World Health Organization. Air Pollution In The World's Megacities: A Report From The UN Environment Programme And Who Environment. New York, New York, USA: United Nations; 1994;35-37.
3. Brook RD, et al. Particulate matter air pollution and cardiovascular disease: An update to the scientific statement from the American Heart Association. Circulation. 2010;121(21):2331-2378
4. Mutlu GM, et al. Ambient particulate matter accelerates coagulation via an IL-6-dependent pathway. J Clin Invest. 2007;117(10):2952-2961. (Pubitemid 47529625)
5. Baccarelli A, et al. Effects of exposure to air pollution on blood coagulation. J Thromb Haemost. 2007;5(2):252-260. (Pubitemid 46139447)
6. Baccarelli A, et al. Exposure to particulate air pollution and risk of deep vein thrombosis. Arch Intern Med. 2008;168(9):920-927. (Pubitemid 351679631)
7. Ghio AJ, Kim C, Devlin RB. Concentrated ambient air particles induce mild pulmonary inflammation in healthy human volunteers. Am J Respir Crit Care Med. 2000;162(3 pt 1):981-988.
8. Riediker M, et al. Particulate matter exposure in cars is associated with cardiovascular effects in healthy young men. Am J Respir Crit Care Med. 2004;169(8):934-940. (Pubitemid 38457320)
9. Mills NL, et al. Ischemic and thrombotic effects of dilute diesel-exhaust inhalation in men with coronary heart disease. N Engl J Med. 2007;357(11):1075-1082. (Pubitemid 47443212)
10. Budinger GR, et al. Particulate matter-induced lung inflammation increases systemic levels of PAI-1 and activates coagulation through distinct mechanisms. PLoS One. 2011;6(4):e18525.
11. Gold DR, et al. Ambient pollution and heart rate variability. Circulation. 2000;101(11):1267-1273. (Pubitemid 30158614)
12. Pope CA 3rd, et al. Heart rate variability associated with particulate air pollution. Am Heart J. 1999;138(5 pt 1):890-899.
13. Watkinson WP, Campen MJ, Costa DL. Cardiac arrhythmia induction after exposure to residual oil fly ash particles in a rodent model of pulmonary hypertension. Toxicol Sci. 1998;41(2):209-216.
14. Bartoli CR, et al. Mechanisms of inhaled fine particulate air pollution-induced arterial blood pressure changes. Environ Health Perspect. 2009;117(3):361-366.
15. Niwa Y, Hiura Y, Sawamura H, Iwai N. Inhalation exposure to carbon black induces inflammatory response in rats. Circ J. 2008;72(1):144-149. (Pubitemid 351413343)
16. 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(4-5):189-197.
17. Erickson JD, Schafer MK, Bonner TI, Eiden LE, Weihe E. Distinct pharmacological properties and distribution in neurons and endocrine cells of two isoforms of the human vesicular monoamine transporter. Proc Natl Acad Sci U S A. 1996;93(10):5166-5171. (Pubitemid 26162890)
18. Mutlu GM, et al. Upregulation of alveolar epithelial active Na+ transport is dependent on β2-adrenergic receptor signaling. Circ Res. 2004;94(8):1091-1100. (Pubitemid 38579704)
19. Mutlu GM, Koch WJ, Factor P. Alveolar epithelial β2-adrenergic receptors: their role in regulation of alveolar active sodium transport. Am J Respir Crit Care Med. 2004;170(12):1270-1275. (Pubitemid 39657189)
20. Mutlu GM, Factor P. Alveolar epithelial β2-adrenergic receptors. Am J Respir Cell Mol Biol. 2008;38(2):127-134.
21. Stiles GL, Caron MG, Lefkowitz RJ. β-Adrenergicreceptors: biochemical mechanisms of physiological regulation. Physiol Rev. 1984;64(2):661-743. (Pubitemid 14139089)
22. Bosmann M, et al. Anti-inflammatory effects of β2 adrenergic receptor agonists in experimental acute lung injury. FASEB J. 2012;26(5):2137-2144.
23. Konstantinides S, Schafer K, Thinnes T, Loskutoff DJ. Plasminogen activator inhibitor-1 and its cofactor vitronectin stabilize arterial thrombi after vascular injury in mice. Circulation. 2001;103(4):576-583. (Pubitemid 32116244)
24. Krief S, et al. Tissue distribution of β3-adrenergic receptor mRNA in man. J Clin Invest. 1993;91(1):344-349. (Pubitemid 23037290)
25. Hjemdahl P, Larsson K, Johansson MC, Zetterlund A, Eklund A. β-Adrenoceptors in human alveolar macrophages isolated by elutriation. Br J Clin Pharmacol. 1990;30(5):673-682. (Pubitemid 20377595)
26. Broug-Holub E, Persoons JH, Schornagel K, Mastbergen SC, Kraal G. Effects of stress on alveolar macrophages: a role for the sympathetic nervous system. Am J Respir Cell Mol Biol. 1998;19(5):842-848. (Pubitemid 128353685)
27. Liggett SB. Identification and characterization of a homogeneous population of β2-adrenergic receptors on human alveolar macrophages. Am Rev Respir Dis. 1989;139(2):552-555. (Pubitemid 19057440)
28. Delghandi MP, Johannessen M, Moens U. The cAMP signalling pathway activates CREB through PKA, p38 and MSK1 in NIH 3T3 cells. Cell Signal. 2005;17(11):1343-1351. (Pubitemid 41206644)
29. Soberanes S, et al. Mitochondrial complex III-generated oxidants activate ASK1 and JNK to induce alveolar epithelial cell death following exposure to particulate matter air pollution. J Biol Chem. 2009; 284(4):2176-2186
30. Kerr R, Stirling D, Ludlam CA. Interleukin 6 and haemostasis. Br J Haematol. 2001;115(1):3-12. (Pubitemid 32995086)
31. Rich DQ, et al. Association between changes in air pollution levels during the Beijing Olympics and biomarkers of inflammation and thrombosis in healthy young adults. JAMA. 2012;307(19):2068-2078
32. Kramer JM. Balancing the benefits and risks of inhaled long-acting β-agonists-the influence of values. N Engl J Med. 2009;360(16):1592-1595.
33. Drazen JM, O'Byrne PM. Risks of long-acting β-agonists in achieving asthma control. N Engl J Med. 2009;360(16):1671-1672
34. Martinez FD. Safety of long-acting β-agonists-an urgent need to clear the air. N Engl J Med. 2005;353(25):2637-2639. (Pubitemid 41817711)
35. FDA. Long-Acting Beta-Agonists (LABAs): New Safe Use Requirements. FDA Web site. http://www. fda.gov/Safety/MedWatch/SafetyInformation/ SafetyAlertsforHumanMedicalProducts/ ucm201003.htm. Updated April 15, 2011. Accessed April 23, 2014.
36. Salpeter SR, Buckley NS, Salpeter EE. Meta-analysis: anticholinergics, but not β-agonists, reduce severe exacerbations and respiratory mortality in COPD. J Gen Intern Med. 2006;21(10):1011-1019. (Pubitemid 44337728)
37. Chowdhury BA, Dal Pan G. The FDA and safe use of long-acting β-agonists in the treatment of asthma. N Engl J Med. 2010;362(13):1169- 1171.
38. Spitzer WO, et al. The use of β-agonists and the risk of death and near death from asthma. N Engl J Med. 1992;326(8):501-506.
39. Rutten FH, Zuithoff NP, Hak E, Grobbee DE, Hoes AW. Beta-blockers may reduce mortality and risk of exacerbations in patients with chronic obstructive pulmonary disease. Arch Intern Med. 2010;170(10):880-887.
40. Sin DD, Man SF. A curious case of beta-blockers in chronic obstructive pulmonary disease. Arch Intern Med. 2010;170(10):849-850.
41. Dransfield MT, Rowe SM, Johnson JE, Bailey WC, Gerald LB. Use of beta blockers and the risk of death in hospitalised patients with acute exacerbations of COPD. Thorax. 2008;63(4):301-305. (Pubitemid 351497940)
42. Au DH, et al. Beta-blockers as single-agent therapy for hypertension and the risk of mortality among patients with chronic obstructive pulmonary disease. Am J Med. 2004;117(12):925-931. (Pubitemid 40075560)
43. National Heart, Lung, Blood Institute Acute Respiratory Distress Syndrome (ARDS) Clinical Trials Network, et al. Randomized, placebo-controlled clinical trial of an aerosolized β2-agonist for treatment of acute lung injury. Am J Respir Crit Care Med. 2011;184(5):561-568.
44. Gao Smith F, et al. Effect of intravenous β-2 agonist treatment on clinical outcomes in acute respiratory distress syndrome (BALTI-2): a multicentre, randomised controlled trial. Lancet. 2012;379(9812):229-235
45. Budinger GR, Mutlu GM. β2-agonists and acute respiratory distress syndrome. Am J Respir Crit Care Med. 2014;189(6):624-625.
46. Imai Y, et al. Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell. 2008;133(2):235-249. (Pubitemid 351512299)
47. Hume DA. Applications of myeloid-specific promoters in transgenic mice support in vivo imaging and functional genomics but do not support the concept of distinct macrophage and dendritic cell lineages or roles in immunity. J Leukoc Biol. 2011;89(4):525-538.
48. Nemmar A, Hoet PH, Dinsdale D, Vermylen J, Hoylaerts MF, Nemery B. Diesel exhaust particles in lung acutely enhance experimental peripheral thrombosis. Circulation. 2003;107(8):1202-1208. (Pubitemid 36297215)
49. Wilson DW, et al. Exposure of mice to concentrated ambient particulate matter results in platelet and systemic cytokine activation. Inhal Toxicol. 2010;22(4):267-276.
50. Nunn B. Some characteristics of mouse platelet aggregation and a comparison of the activity of a range of compounds in mouse and human plateletrich plasma in vitro. Thromb Haemost. 1981;45(1):1-5. (Pubitemid 11155220)
51. Pozgajova M, Sachs UJ, Hein L, Nieswandt B. Reduced 2Aadrenergic receptor.?thrombus stability in mice lacking the Blood. 2006;108(2):510-514.
52. Lanza F, Cazenave JP. Studies of 2-adrenergic receptors of intact and functional washed human platelets by? binding of 3H-dihydroergocryptine and 3H-yohimbine-correlation of 3H-yohimbine binding with the potentiation by adrenaline of ADP-induced aggregation. Thromb Haemost. 1985;54(2):402-408. (Pubitemid 16252458)
53. Nieswandt B, et al. Evidence for cross-talk between glycoprotein VI and Gi-coupled receptors during collagen-induced platelet aggregation. Blood. 2001;97(12):3829-3835.
54. Larson MK, et al. Identification of P2Y12-dependent and-independent mechanisms of glycoprotein VI-mediated Rap1 activation in platelets. Blood. 2003;101(4):1409-1415. (Pubitemid 36182513)
55. Woulfe D, Jiang H, Mortensen R, Yang J, Brass LF. Activation of Rap1B by G(i) family members in platelets. J Biol Chem. 2002;277(26):23382-23390.
56. Kjeldsen SE, Weder AB, Egan B, Neubig R, Zweifler AJ, Julius S. Effect of circulating epinephrine on platelet function and hematocrit. Hypertension. 1995;25(5):1096-1105.
57. Clapham DE. TRP channels as cellular sensors. Nature. 2003;426(6966):517-524. (Pubitemid 37522633)
58. Minke B, Cook B. TRP channel proteins and signal transduction. Physiol Rev. 2002;82(2):429-472. (Pubitemid 34654458)
59. Deering-Rice CE, et al. Transient receptor potential vanilloid-1 (TRPV1) is a mediator of lung toxicity for coal fly ash particulate material. Mol Pharmacol. 2012;81(3):411-419.
60. Deering-Rice CE, et al. Electrophilic components of diesel exhaust particles (DEP) activate transient receptor potential ankyrin-1 (TRPA1): a probable mechanism of acute pulmonary toxicity for DEP. Chem Res Toxicol. 2011;24(6):950-959.
61. Hinoi E, et al. The sympathetic tone mediates leptin's inhibition of insulin secretion by modulating osteocalcin bioactivity. J Cell Biol. 2008;183(7):1235-1242.
62. Kajimura D, et al. Genetic determination of the cellular basis of the sympathetic regulation of bone mass accrual. J Exp Med. 2011;208(4):841-851.
63. Sioutas C, Koutrakis P, Burton RM. A technique to expose animals to concentrated fine ambient aerosols. Environ Health Perspect. 1995;103(2):172-177.
64. Maciejczyk P, Chen LC. Effects of subchronic exposures to concentrated ambient particles (CAPs) in mice. VIII. Source-related daily variations in in vitro responses to CAPs. Inhal Toxicol. 2005;17(4-5):243-253.
65. Sioutas C, Seongheon K, Chang M. Development and evaluation of a prototype ultrafine particle concentrator. J Aerosol Sci. 1999;30(8):1001-1017. (Pubitemid 29332709)
66. State of Illinois Environmental Protection Agency. Illinois Annual Air Quality Report 2012. State of Illinois Web site. http://www.epa.state.il.us/air/ air-quality-report/2012/air-quality-report-2012. pdf. Accessed April 23, 2014.
67. Binaku K, O'Brien T, Schmeling M, Fosco T. Statistical analysis of aerosol species, trace gasses, and meteorology in Chicago. Environ Monit Assess. 2013;185(9):7295-7308.
68. EPA. Our Nation's Air: Status and Trends through 2008. EPA Web site. http://www.epa.gov/airtrends/2010/ report/fullreport.pdf. Accessed April 23, 2014.
69. Babich P, Davey M, Allen G, Koutrakis P. Method comparisons for particulate nitrate, elemental carbon, and PM2.5 mass in seven U.S. cities. J Air Waste Manag Assoc. 2000;50(7):1095-1105.
70. Currie LA, et al. A critical evaluation of interlaboratory data on total, elemental, and isotopic carbon in the carbonaceous particle reference material, NIST SRM 1649a. J Res NIST. 2002;107(3):279-298. (Pubitemid 34963666)
71. National Institute of Standards and Technology. SRM 1649a: Urban Dust/Organics. US Department of Commerce Web site. https://www-s.nist. gov/srmors/view-detail.cfm?srm=1649A. Updated August 28, 2013. Accessed April 23, 2014.
72. Mutlu GM, et al. Airborne particulate matter inhibits alveolar fluid reabsorption in mice via oxidant generation. Am J Respir Cell Mol Biol. 2006;34(6):670-676. (Pubitemid 43825331)
73. Williams M, Young JB, Rosa RM, Gunn S, Epstein FH, Landsberg L. Effect of protein ingestion on urinary dopamine excretion. Evidence for the functional importance of renal decarboxylation of circulating 3,4-dihydroxyphenylalanine in man. J Clin Invest. 1986;78(6):1687-1693. (Pubitemid 17219534)
74. Adir Y, et al. Augmentation of endogenous dopamine production increases lung liquid clearance. Am J Respir Crit Care Med. 2004;169(6):757-763. (Pubitemid 38344113)
75. Misharin AV, Morales-Nebreda L, Mutlu GM, Budinger GR, Perlman H. Flow cytometric analysis of macrophages and dendritic cell subsets in the mouse lung. Am J Respir Cell Mol Biol. 2013;49(4):503-510.