Resolvins attenuate inflammation and promote resolution in cigarette smokeexposed human macrophages

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 309, Issue 8, 2015, Pages L888-L901

  Croasdell, Amanda ^a   Thatcher, Thomas H ^a   Kottmann, R Matthew ^a   Colas, Romain A ^b   Dalli, Jesmond ^b   Serhan, Charles N ^b   Sime, Patricia J ^a   Phipps, Richard P ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Chronic obstructive pulmonary disease; Cigarette smoke; Macrophage; Resolvin; Specialized proresolving mediators

Indexed keywords

12 HYDROXYICOSATETRAENOIC ACID; 14 HYDROXYDOCOSAHEXAENOIC ACID; 15 HYDROXYICOSATETRAENOIC ACID; 17 HYDROXYDOCOSAHEXAENOIC ACID; 5 HYDROXYICOSATETRAENOIC ACID; ANTIINFLAMMATORY AGENT; ARACHIDONIC ACID DERIVATIVE; B7 ANTIGEN; CIGARETTE SMOKE; CYCLOOXYGENASE 2; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 32; HEXANOIC ACID DERIVATIVE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 6; INTERLEUKIN 8; LYMPHOTOXIN; POLYUNSATURATED FATTY ACID; PROSTAGLANDIN E2; PROTEIN P100; REACTIVE OXYGEN METABOLITE; RESOLVIN D1; RESOLVIN D2; SYNAPTOTAGMIN I; TRANSCRIPTION FACTOR RELB; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; AUTACOID; CYTOKINE; DOCOSAHEXAENOIC ACID; SMOKE;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL DIFFERENTIATION; CELL VIABILITY; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; DRUG EFFECT; ENZYME PHOSPHORYLATION; ENZYME REPRESSION; FATTY ACID ANALYSIS; FATTY ACID BLOOD LEVEL; FEMALE; HUMAN; HUMAN CELL; INFLAMMATION; LIPIDOMICS; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; MACROPHAGE FUNCTION; MALE; MODULATION; MONOCYTE; NEUTROPHIL; OXIDATIVE STRESS; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CARBONYLATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; ADVERSE EFFECTS; BIOSYNTHESIS; CELL CULTURE; DRUG EFFECTS; LIPID METABOLISM; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SMOKE; SMOKING;

CELLS, CULTURED; CYTOKINES; DOCOSAHEXAENOIC ACIDS; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; LIPID METABOLISM; MACROPHAGES, ALVEOLAR; OXIDATIVE STRESS; PHAGOCYTOSIS; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; SIGNAL TRANSDUCTION; SMOKE; SMOKING;

EID: 84944447664     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00125.2015     Document Type: Article

References (79)

1. Anonymous. Surgeon General’s Report. How Tobacco Smoke Causes Disease: The Biology and Behavioral Basis for Smoking-Attributable Disease. Atlanta, GA: Centers for Disease Control, 2010.
2. Arita M, Bianchini F, Aliberti J, Sher A, Chiang N, Hong S, Yang R, Petasis NA, Serhan CN. Stereochemical assignment, antiinflammatory properties, and receptor for the -3 lipid mediator resolvin E1. J Exp Med 201: 713-722, 2005.
3. Arita M, Ohira T, Sun YP, Elangovan S, Chiang N, Serhan CN. Resolvin E1 selectively interacts with leukotriene B4 receptor BLT1 and ChemR23 to regulate inflammation. J Immunol 178: 3912-3917, 2007.
4. Back M, Powell WS, Dahlen SE, Drazen JM, Evans JF, Serhan CN, Shimizu T, Yokomizo T, Rovati GE. Update on leukotriene, lipoxin and oxoeicosanoid receptors: IUPHAR Review 7. Br J Pharmacol 171: 3551-3574, 2014.
5. Baglole CJ, Maggirwar SB, Gasiewicz TA, Thatcher TH, Phipps RP, Sime PJ. The aryl hydrocarbon receptor attenuates tobacco smokeinduced cyclooxygenase-2 and prostaglandin production in lung fibroblasts through regulation of the NF-B family member RelB. J Biol Chem 283: 28944-28957, 2008.
6. Bagole CJ, Bushinsky SM, Garcia TM, Kode A, Rahman I, Sime PJ, Phipps RP. Differential induction of apoptosis by cigarette smoke extract in primary human lung fibroblast strains: implications for emphysema. Am J Physiol Lung Cell Mol Physiol 291: L19-L29, 2006.
7. Buckley CD, Gilroy DW, Serhan CN. Proresolving lipid mediators and mechanisms in the resolution of acute inflammation. Immunity 40: 315-327, 2014.
8. Cassetta L, Cassol E, Poli G. Macrophage polarization in health and disease. Sci World J 11: 2391-2402, 2011.
9. Chen F, Fan XH, Wu YP, Zhu JL, Wang F, Bo LL, Li JB, Bao R, Deng XM. Resolvin D1 improves survival in experimental sepsis through reducing bacterial load and preventing excessive activation of inflammatory response. Eur J Clin Microbiol Infect Dis 33: 457-464, 2014.
10. Chen J, Shetty S, Zhang P, Gao R, Hu Y, Wang S, Li Z, Fu J. Aspirin-triggered resolvin D1 down-regulates inflammatory responses and protects against endotoxin-induced acute kidney injury. Toxicol Appl Pharmacol 277: 118-123, 2014.
11. Chiang N, Arita M, Serhan CN. Anti-inflammatory circuitry: lipoxin, aspirin-triggered lipoxins and their receptor ALX. Prostaglandins Leukot Essent Fatty Acids 73: 163-177, 2005.
12. Chiang N, Fredman G, Backhed F, Oh SF, Vickery T, Schmidt BA, Serhan CN. Infection regulates pro-resolving mediators that lower antibiotic requirements. Nature 484: 524-528, 2012.
13. Chiang N, Serhan CN, Dahlen SE, Drazen JM, Hay DW, Rovati GE, Shimizu T, Yokomizo T, Brink C. The lipoxin receptor ALX: potent ligand-specific and stereoselective actions in vivo. Pharmacol Rev 58: 463-487, 2006.
14. Cipollina C, Di Vincenzo S, Gerbino S, Siena L, Gjomarkaj M, Pace E. Dual anti-oxidant and anti-inflammatory actions of the electrophilic cyclooxygenase-2-derived 17-oxo-DHA in lipopolysaccharide- and cigarette smoke-induced inflammation. Biochim Biophys Acta 1840: 2299-2309, 2014.
15. Colas RA, Shinohara M, Dalli J, Chiang N, Serhan CN. Identification and signature profiles for pro-resolving and inflammatory lipid mediators in human tissue. Am J Physiol Cell Physiol 307: C39-C54, 2014.
16. Dalli J, Zhu M, Vlasenko NA, Deng B, Haeggstrom JZ, Petasis NA, Serhan CN. The novel 13S,14S-epoxy-maresin is converted by human macrophages to maresin1 (MaR1), inhibits leukotriene A4 hydrolase (LTA4H), and shifts macrophage phenotype. FASEB J 27: 2573-2583, 2013.
17. de Batlle J, Sauleda J, Balcells E, Gomez FP, Mendez M, Rodriguez E, Barreiro E, Ferrer JJ, Romieu I, Gea J, Anto J, Garcia-Aymerich J. Association between -3 and -6 fatty acid intakes and serum inflammatory markers in COPD. J Nutr Biochem 23: 817-821, 2012.
18. DiDonato JA, Mercurio F, Karin M. NF-B and the link between inflammation and cancer. Immunol Rev 246: 379-400, 2012.
19. Domej W, Oettl K, Renner W. Oxidative stress and free radicals in COPD-implications and relevance for treatment. Int J Chron Obstruct Pulm Dis 9: 1207-1224, 2014.
20. Drannik AG, Pouladi MA, Robbins CS, Goncharova SI, Kianpour S, Stampfli MR. Impact of cigarette smoke on clearance and inflammation after Pseudomonas aeruginosa infection. Am J Respir Crit Care Med 170: 1164-1171, 2004.
21. Drozdovszky O, Barta I, Antus B. Sputum eicosanoid profiling in exacerbations of chronic obstructive pulmonary disease. Respir Int Rev Thorac Dis 87: 408-415, 2014.
22. Fiore S, Ryeom SW, Weller PF, Serhan CN. Lipoxin recognition sites. Specific binding of labeled lipoxin A4 with human neutrophils. J Biol Chem 267: 16168-16176, 1992.
23. Fredman G, Oh SF, Ayilavarapu S, Hasturk H, Serhan CN, Van Dyke TE. Impaired phagocytosis in localized aggressive periodontitis: rescue by resolvin E1. PLos One 6: 2011.
24. Fritscher LG, Post M, Rodrigues MT, Silverman F, Balter M, Chapman KR, Zamel N. Profile of eicosanoids in breath condensate in asthma and COPD. J Breath Res 6: 026001, 2012.
25. Giles H, Leff P. The biology and pharmacology of PGD2. Prostaglandins 35: 277-300, 1988.
26. Gilroy DW, Colville-Nash PR, McMaster S, Sawatzky DA, Willoughby DA, Lawrence T. Inducible cyclooxygenase-derived 15-deoxy-12,14-PGJ2 brings about acute inflammatory resolution in rat pleurisy by inducing neutrophil and macrophage apoptosis. FASEB J 17: 2269-2271, 2003.
27. Gilroy DW, Colville-Nash PR, Willis D, Chivers J, Paul-Clark MJ, Willoughby DA. Inducible cyclooxygenase may have anti-inflammatory properties. Nat Med 5: 698-701, 1999.
28. Gosset P, Bureau F, Angeli V, Pichavant M, Faveeuw C, Tonnel AB, Trottein F. Prostaglandin D2 affects the maturation of human monocytederived dendritic cells: consequence on the polarization of naive Th cells. J Immunol 170: 4943-4952, 2003.
29. Harizi H, Corcuff JB, Gualde N. Arachidonic-acid-derived eicosanoids: roles in biology and immunopathology. Trends Mol Med 14: 461-469, 2008.
30. Hsiao HM, Sapinoro RE, Thatcher TH, Croasdell A, Levy EP, Fulton RA, Olsen KC, Pollock SJ, Serhan CN, Phipps RP, Sime PJ. A novel anti-inflammatory and pro-resolving role for resolvin D1 in acute cigarette smoke-induced lung inflammation. PLos One 8: e58258, 2013.
31. Hsiao HM, Thatcher TH, Levy EP, Fulton RA, Owens KM, Phipps RP, Sime PJ. Resolvin D1 attenuates polyinosinic-polycytidylic acidinduced inflammatory signaling in human airway epithelial cells via TAK1. J Immunol 193: 4980-4987, 2014.
32. Kalinski P. Regulation of immune responses by prostaglandin E2. J Immunol 188: 21-28, 2012.
33. Kirkham PA, Spooner G, Rahman I, Rossi AG. Macrophage phagocytosis of apoptotic neutrophils is compromised by matrix proteins modified by cigarette smoke and lipid peroxidation products. Biochem Biophys Res Commun 318: 32-37, 2004.
34. Krishnamoorthy S, Recchiuti A, Chiang N, Yacoubian S, Lee CH, Yang R, Petasis NA, Serhan CN. Resolvin D1 binds human phagocytes with evidence for proresolving receptors. Proc Natl Acad Sci USA 107: 1660-1665, 2010.
35. Kure I, Nishiumi S, Nishitani Y, Tanoue T, Ishida T, Mizuno M, Fujita T, Kutsumi H, Arita M, Azuma T, Yoshida M. Lipoxin A4 reduces lipopolysaccharide-induced inflammation in macrophages and intestinal epithelial cells through inhibition of nuclear factor-B activation. J Pharmacol Exp Ther 332: 541-548, 2010.
36. Maddox JF, Hachicha M, Takano T, Petasis NA, Fokin VV, Serhan CN. Lipoxin A4 stable analogs are potent mimetics that stimulate human monocytes and THP-1 cells via a G-protein-linked lipoxin A4 receptor. J Biol Chem 272: 6972-6978, 1997.
37. Martey CA, Pollock SJ, Turner CK, O’Reilly KM, Baglole CJ, Phipps RP, Sime PJ. Cigarette smoke induces cyclooxygenase-2 and microsomal prostaglandin E2 synthase in human lung fibroblasts: implications for lung inflammation and cancer. Am J Physiol Lung Cell Mol Physiol 287: L981-L991, 2004.
38. Marti-Lliteras P, Regueiro V, Morey P, Hood DW, Saus C, Sauleda J, Agusti AG, Bengoechea JA, Garmendia J. Nontypeable Haemophilus influenzae clearance by alveolar macrophages is impaired by exposure to cigarette smoke. Infect Immun 77: 4232-4242, 2009.
39. Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 27: 451-483, 2009.
40. McMillan DH, Baglole CJ, Thatcher TH, Maggirwar S, Sime PJ, Phipps RP. Lung-targeted overexpression of the NF-B member RelB inhibits cigarette smoke-induced inflammation. Am J Pathol 179: 125-133, 2011.
41. Mobley A, Tanizawa H, Iwanaga T, Tai CL, Tai HH. Selective inhibition of 5-lipoxygenase pathway in rat pulmonary alveolar macrophages by cigarette smoking. Biochim Biophys Acta 918: 115-119, 1987.
42. Moghaddam SJ, Ochoa CE, Sethi S, Dickey BF. Nontypeable Haemophilus influenzae in chronic obstructive pulmonary disease and lung cancer. Int J Chron Obstruct Pulm Dis 6: 113-123, 2011.
43. Monick MM, Powers LS, Walters K, Lovan N, Zhang M, Gerke A, Hansdottir S, Hunninghake GW. Identification of an autophagy defect in smokers’ alveolar macrophages. J Immunol 185: 5425-5435, 2010.
44. Nakahata N. Thromboxane A2: physiology/pathophysiology, cellular signal transduction and pharmacology. Pharmacol Ther 118: 18-35, 2008.
45. Norling LV, Dalli J, Flower RJ, Serhan CN, Perretti M. Resolvin D1 limits polymorphonuclear leukocyte recruitment to inflammatory loci: receptor-dependent actions. Arterioscler Thromb Vasc Biol 32: 1970-1978, 2012.
46. O’Banion MK, Winn VD, Young DA. cDNA cloning and functional activity of a glucocorticoid-regulated inflammatory cyclooxygenase. Proc Natl Acad Sci USA 89: 4888-4892, 1992.
47. Phipps JC, Aronoff DM, Curtis JL, Goel RD, O’Brien E, Mancuso P. Cigarette smoke exposure impairs pulmonary bacterial clearance and alveolar macrophage complement-mediated phagocytosis of Streptococcus pneumoniae. Infect Immun 78: 1214-1220, 2010.
48. Pietras T, Szemraj J, Panek M, Witusik A, Banasiak M, Antczak A, Gorski P. Functional polymorphism of cyclooxygenase-2 gene (G-765C) in chronic obstructive pulmonary disease patients. Mol Biol Rep 39: 2163-2167, 2012.
49. Prescott D, McKay DM. Aspirin-triggered lipoxin enhances macrophage phagocytosis of bacteria while inhibiting inflammatory cytokine production. Am J Physiol Gastrointest Liver Physiol 301: G487-G497, 2011.
50. Prieto P, Cuenca J, Traves PG, Fernandez-Velasco M, Martin-Sanz P, Bosca L. Lipoxin A4 impairment of apoptotic signaling in macrophages: implication of the PI3K/Akt and the ERK/Nrf-2 defense pathways. Cell Death Differ 17: 1179-1188, 2010.
51. Profita M, Sala A, Bonanno A, Riccobono L, Ferraro M, La Grutta S, Albano GD, Montalbano AM, Gjomarkaj M. Chronic obstructive pulmonary disease and neutrophil infiltration: role of cigarette smoke and cyclooxygenase products. Am J Physiol Lung Cell Mol Physiol 298: L261-L269, 2010.
52. Psychogios N, Hau DD, Peng J, Guo AC, Mandal R, Bouatra S, Sinelnikov I, Krishnamurthy R, Eisner R, Gautam B, Young N, Xia J, Knox C, Dong E, Huang P, Hollander Z, Pedersen TL, Smith SR, Bamforth F, Greiner R, McManus B, Newman JW, Goodfriend T, Wishart DS. The human serum metabolome. PLos One 6: e16957, 2011.
53. Quehenberger O, Armando AM, Brown AH, Milne SB, Myers DS, Merrill AH, Bandyopadhyay S, Jones KN, Kelly S, Shaner RL, Sullards CM, Wang E, Murphy RC, Barkley RM, Leiker TJ, Raetz CR, Guan Z, Laird GM, Six DA, Russell DW, McDonald JG, Subramaniam S, Fahy E, Dennis EA. Lipidomics reveals a remarkable diversity of lipids in human plasma. J Lipid Res 51: 3299-3305, 2010.
54. Rahman I, Morrison D, Donaldson K, MacNee W. Systemic oxidative stress in asthma, COPD, and smokers. Am J Respir Crit Care Med 154: 1055-1060, 1996.
55. Ramon S, Bancos S, Serhan CN, Phipps RP. Lipoxin A modulates adaptive immunity by decreasing memory B-cell responses via an ALX/FPR2-dependent mechanism. Eur J Immunol 44: 357-369, 2014.
56. Ramon S, Gao F, Serhan CN, Phipps RP. Specialized proresolving mediators enhance human B cell differentiation to antibody-secreting cells. J Immunol 189: 1036-1042, 2012.
57. Rogerio AP, Haworth O, Croze R, Oh SF, Uddin M, Carlo T, Pfeffer MA, Priluck R, Serhan CN, Levy BD. Resolvin D1 and aspirin-triggered resolvin D1 promote resolution of allergic airways responses. J Immunol 189: 1983-1991, 2012.
58. Rossi A, Kapahi P, Natoli G, Takahashi T, Chen Y, Karin M, Santoro MG. Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IB kinase. Nature 403: 103-108, 2000.
59. Sandig H, Pease JE, Sabroe I. Contrary prostaglandins: the opposing roles of PGD2 and its metabolites in leukocyte function. J Leukoc Biol 81: 372-382, 2007.
60. Sarir H, Henricks PA, van Houwelingen AH, Nijkamp FP, Folkerts G. Cells, mediators and Toll-like receptors in COPD. Eur J Pharmacol 585: 346-353, 2008.
61. Sasaki A, Fukuda H, Shiida N, Tanaka N, Furugen A, Ogura J, Shuto S, Mano N, Yamaguchi H. Determination of -6 and -3 PUFA metabolites in human urine samples using UPLC/MS/MS. Anal Bioanal Chem 407: 1625-1639, 2015.
62. Scannell M, Maderna P. Lipoxins and annexin-1: resolution of inflammation and regulation of phagocytosis of apoptotic cells. Sci World J 6: 1555-1573, 2006.
63. Serhan CN, Chiang N, Van Dyke TE. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol 8: 349-361, 2008.
64. Sethi S. Inhibition of leukocyte-endothelial interactions by oxidized -3 fatty acids: a novel mechanism for the anti-inflammatory effects of -3 fatty acids in fish oil. Redox Rep Commun Free Radic Res 7: 369-378, 2002.
65. Shang S, Ordway D, Henao-Tamayo M, Bai X, Oberley-Deegan R, Shanley C, Orme IM, Case S, Minor M, Ackart D, Hascall-Dove L, Ovrutsky AR, Kandasamy P, Voelker DR, Lambert C, Freed BM, Iseman MD, Basaraba RJ, Chan ED. Cigarette smoke increases susceptibility to tuberculosis-evidence from in vivo and in vitro models. J Infect Dis 203: 1240-1248, 2011.
66. Spite M, Norling LV, Summers L, Yang R, Cooper D, Petasis NA, Flower RJ, Perretti M, Serhan CN. Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis. Nature 461: 1287-1291, 2009.
67. Stenfeldt AL, Karlsson J, Wenneras C, Bylund J, Fu H, Dahlgren C. Cyclosporin H, Boc-MLF and Boc-FLFLF are antagonists that preferentially inhibit activity triggered through the formyl peptide receptor. Inflammation 30: 224-229, 2007.
68. Sun SC. The noncanonical NF-B pathway. Immunol Rev 246: 125-140, 2012.
69. Telenga ED, Hoffmann RF, Ruben TK, Hoonhorst SJ, Willemse BW, van Oosterhout AJ, Heijink IH, van den Berge M, Jorge L, Sandra P, Postma DS, Sandra K, ten Hacken NH. Untargeted lipidomic analysis in chronic obstructive pulmonary disease Uncovering sphingolipids. Am J Respir Crit Care Med 190: 155-164, 2014.
70. Thatcher TH, Maggirwar SB, Baglole CJ, Lakatos HF, Gasiewicz TA, Phipps RP, Sime PJ. Aryl hydrocarbon receptor-deficient mice develop heightened inflammatory responses to cigarette smoke and endotoxin associated with rapid loss of the nuclear factor-B component RelB. Am J Pathol 170: 855-864, 2007.
71. Titos E, Rius B, Gonzalez-Periz A, Lopez-Vicario C, Moran-Salvador E, Martinez-Clemente M, Arroyo V, Claria J. Resolvin D1 and its precursor docosahexaenoic acid promote resolution of adipose tissue inflammation by eliciting macrophage polarization toward an M2-like phenotype. J Immunol 187: 5408-5418, 2011.
72. Tuder RM, Petrache I. Pathogenesis of chronic obstructive pulmonary disease. J Clin Invest 122: 2749-2755, 2012.
73. Wang YP, Wu Y, Li LY, Zheng J, Liu RG, Zhou JP, Yuan SY, Shang Y, Shang-Long Y. Aspirin-triggered lipoxin A4 attenuates LPS-induced pro-inflammatory responses by inhibiting activation of NF-B and MAPKs in BV-2 microglial cells. J Neuroinflamm 8: 95, 2011.
74. Wang Z, Cheng Q, Tang K, Sun Y, Zhang K, Zhang Y, Luo S, Zhang H, Ye D, Huang B. Lipid mediator lipoxin A4 inhibits tumor growth by targeting IL-10-producing regulatory B (Breg) cells. Cancer Lett 364: 118-124, 2015.
75. Wang ZF, Li Q, Liu SB, Mi WL, Hu S, Zhao J, Tian Y, Mao-Ying QL, Jiang JW, Ma HJ, Wang YQ, Wu GC. Aspirin-triggered lipoxin A4 attenuates mechanical allodynia in association with inhibiting spinal JAK2/STAT3 signaling in neuropathic pain in rats. Neuroscience 273: 65-78, 2014.
76. Wu D, Zheng S, Li W, Yang L, Liu Y, Zheng X, Yang Y, Yang L, Wang Q, Smith FG, Jin S. Novel biphasic role of resolvin D1 on expression of cyclooxygenase-2 in lipopolysaccharide-stimulated lung fibroblasts is partly through PI3K/AKT and ERK2 pathways. Mediators Inflamm 2013: 964012, 2013.
77. Yin H, Brooks JD, Gao L, Porter NA, Morrow JD. Identification of novel autoxidation products of the -3 fatty acid eicosapentaenoic acid in vitro and in vivo. J Biol Chem 282: 29890-29901, 2007.
78. Zago M, Rico de Souza A, Hecht E, Rousseau S, Hamid Q, Eidelman DH, Baglole CJ. The NF-B family member RelB regulates microRNA miR-146a to suppress cigarette smoke-induced COX-2 protein expression in lung fibroblasts. Toxicol Lett 226: 107-116, 2014.
79. Zaslona Z, Okunishi K, Bourdonnay E, Domingo-Gonzalez R, Moore BB, Lukacs NW, Aronoff DM, Peters-Golden M. Prostaglandin E2 suppresses allergic sensitization and lung inflammation by targeting the E prostanoid 2 receptor on T cells. J Allergy Clin Immunol 133: 379-387, 2014.