Modulatory role for retinoid-related orphan receptor α in allergen-induced lung inflammation

American Journal of Respiratory and Critical Care Medicine

Volumn 174, Issue 12, 2006, Pages 1299-1309

  Jaradat, Maisa ^b   Stapleton, Cliona ^b   Tilley, Stephen L ^b   Dixon, Darlene ^b   Erikson, Christopher J ^b   McCaskill, Joshua G ^b   Hong, Soon Kang ^b   Angers, Martin ^b   Liao, Grace ^b   Collins, Jennifer ^b   Grissom, Sherry ^b   Jetten, Anton M ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b NONE

Author keywords

Asthma; Inflammation; Lung; Nuclear receptor

Indexed keywords

ALLERGEN; CHEMOKINE; CHLORIDE CHANNEL; CYTOKINE; EOTAXIN; IMMUNOGLOBULIN E; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MUCIN 5B; OVALBUMIN; PROTEIN CLCA3; PROTEIN RORALPHA; PROTEIN S 100; RNA; SERUM AMYLOID A; SOMATOMEDIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DISEASE PREDISPOSITION; EOSINOPHILIA; GENE EXPRESSION; HYPERPLASIA; IMMUNE RESPONSE; MICROARRAY ANALYSIS; MOUSE; MUCOUS CELL; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCORING SYSTEM; TH2 CELL;

ALLERGENS; ANIMALS; ASTHMA; CHEMOKINES, CC; CHLORIDE CHANNELS; EOSINOPHILIA; INFLAMMATION; INSULIN-LIKE GROWTH FACTOR I; LUNG; MACROPHAGE INFLAMMATORY PROTEIN-1; MICE; MICE, MUTANT STRAINS; MUCINS; MUCOPROTEINS; OVALBUMIN; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SERUM AMYLOID A PROTEIN; TRANS-ACTIVATORS;

EID: 33845483452     PISSN: 1073449X     EISSN: 1073449X     Source Type: Journal    
DOI: 10.1164/rccm.200510-1672OC     Document Type: Article

References (66)

1. Bousquet J, Jeffery P, Busse WW, Johnson M, Vignola AM. Asthma. From bronchoconstriction to airways inflammation and remodeling. Am J Respir Crit Care Med 2000;161:1720-1745.
2. Blumenthal MN. The role of genetics in the development of asthma and atopy. Curr Opin Allergy Clin Immunol 2005;5:141-145.
3. Fireman P. Understanding asthma pathophysiology. Allergy Asthma Proc 2003;24:79-83.
4. Ryu JH, Myers JL, Swensen SJ. Bronchiolar disorders. Am J Respir Crit Care Med 2003;168:1277-1292.
5. Wills-Karp M. Interleukin-13 in asthma pathogenesis. Immunol Rev 2004;202:175-190.
6. Ngoc LP, Gold DR, Tzianabos AO, Weiss ST, Celedon JC. Cytokines, allergy, and asthma. Curr Opin Allergy Clin Immunol 2005;5:161-166.
7. Bisset LR, Schmid-Grendelmeier P. Chemokines and their receptors in the pathogenesis of allergic asthma: progress and perspective. Curr Opin Pulm Med 2005;11:35-42.
8. McDonald DM. Angiogenesis and remodeling of airway vasculature in chronic inflammation. Am J Respir Crit Care Med 2001;164:S39-S45.
9. Willy PJ, Mangelsdorf DJ. Nuclear orphan receptors: the search for novel ligands and signaling pathways. In: O'Malley BW, editor. Hormones and signaling. San Diego, CA: Academic Press; 1998. pp. 308-358.
10. Benayoun L, Letuve S, Druilhe A, Boczkowski J, Dombret MC, Mechighel P, Megret J, Leseche G, Aubier M, Pretolani M. Regulation of peroxisome proliferator-activated receptor gamma expression in human asthmatic airways: relationship with proliferation, apoptosis, and airway remodeling. Am J Respir Crit Care Med 2001;164:1487-1494.
11. Trifilieff A, Bench A, Hanley M, Bayley D, Campbell E, Whittaker P. PPAR-alpha and -gamma but not -delta agonists inhibit airway inflammation in a murine model of asthma: in vitro evidence for an NF-kappaB-independent effect. Br J Pharmacol 2003;139:163-171.
12. Serhan CN, Devchand PR. Novel antiinflammatory targets for asthma: a role for PPARγ? Am J Respir Cell Mol Biol 2001;24:658-661.
13. Pelaia G, Vatrella A, Cuda G, Maselli R, Marsico SA. Molecular mechanisms of corticosteroid actions in chronic inflammatory airway diseases. Life Sci 2003;72:1549-1561.
14. Wittke A, Weaver V, Mahon BD, August A, Cantorna MT. Vitamin D receptor-deficient mice fail to develop experimental allergic asthma. J Immunol 2004;173:3432-3436.
15. Poon AH, Laprise C, Lemire M, Montpetit A, Sinnett D, Schurr E, Hudson TJ. Association of vitamin D receptor genetic variants with susceptibility to asthma and atopy. Am J Respir Crit Care Med 2004;170:967-973.
16. Raby BA, Lazarus R, Silverman EK, Lake S, Lange C, Wjst M, Weiss ST. Association of vitamin D receptor gene polymorphisms with childhood and adult asthma. Am J Respir Crit Care Med 2004;170:1057-1065.
17. Usmani OS, Ito K, Maneechotesuwan K, Ito M, Johnson M, Barnes PJ, Adcock IM. Glucocorticoid receptor nuclear translocation in airway cells after inhaled combination therapy. Am J Respir Crit Care Med 2005;172:704-712.
18. Adcock IM. Glucocorticoids: new mechanisms and future agents. Curr Allergy Asthma Rep 2003;3:249-257.
19. ten Brinke A, Zwinderman AH, Sterk PJ, Rabe KF, Bel EH. "Refractory" eosinophilic airway inflammation in severe asthma: effect of parenteral corticosteroids. Am J Respir Crit Care Med 2004;170:601-605.
20. Goleva E, Li LB, Eves PT, Strand MJ, Martin RJ, Leung DY. Increased glucocorticoid receptor β alters steroid response in glucocorticoid- insensitive asthma. Am J Respir Crit Care Med 2006;173:607-616.
21. Jetten AM, Kurebayashi S, Ueda E. The ROR nuclear orphan receptor subfamily: critical regulators of multiple biological processes. Prog Nucleic Acid Res Mol Biol 2001;69:205-247.
22. Jetten AM. Recent advances in the mechanisms of action and physiological functions of the retinoid-related orphan receptors (RORs). Curr Drug Targets Inflamm Allergy 2004;3:395-412.
23. Giguere V, Tini M, Flock G, Ong E, Evans RM, Otulakowski G. Isoform-specific amino-terminal domains dictate DNA-binding properties of RORα, a novel family of orphan hormone nuclear receptors. Genes Dev 1994;8:538-553.
24. Jarvis CI, Staels B, Brugg B, Lemaigre-Dubreuil Y, Tedgui A, Mariani J. Age-related phenotypes in the staggerer mouse expand the RORalpha nuclear receptor's role beyond the cerebellum. Mol Cell Endocrinol 2002;186:1-5.
25. Trenker E, Hoffmann M. Defective development of the thymus and immunological abnormalities in the neurological mouse mutation "staggerer." J Neurosci 1986;6:1733-1737.
26. Delerive P, Monte D, Dubois G, Trottein F, Fruchart-Najib J, Mariani J, Fruchart JC, Staels B. The orphan nuclear receptor ROR alpha is a negative regulator of the inflammatory response. EMBO Rep 2001;2:42-48.
27. Kopmels B, Mariani J, Delhaye-Bouchaud N, Audibert F, Fradelizi D, Wollman EE. Evidence for a hyperexcitability state of staggerer mutant mice macrophages. J Neurochem 1992;58:192-199.
28. Dzhagalov I, Giguere V, He YW. Lymphocyte development and function in the absence of retinoic acid-related orphan receptor alpha. J Immunol 2004;173:2952-2959.
29. Steinmayr M, André E, Conquet F, Rondi-Reig L, Delhaye-Bouchaud N, Auclair N, Daniel H, Crépel F, Mariani J, Sotelo C, et al. Staggerer phenotype in retinoid-related orphan receptor a-deficient mice. Proc Natl Acad Sci USA 1998;95:3960-3965.
30. Stapleton CM, Jaradat M, Dixon D, Kang HS, Kim SC, Liao G, Carey MA, Cristiano J, Moorman MP, Jetten AM. Enhanced susceptibility of Staggerer (RORαsg/sg) mice to lipopolysaccharide-induced lung inflammation. Am J Physiol Lung Cell Mol Physiol 2005;289:L144-L152.
31. Sidman RL, Lane PW, Dickie MN. Staggerer, a new mutation in the mouse affecting the cerebellum. Science 1962;137:610-612.
32. Lambrecht BN, Salomon B, Klatzmann D, Pauwels RA. Dendritic cells are required for the development of chronic eosinophilic airway inflammation in response to inhaled antigen in sensitized mice. J Immunol 1998;160:4090-4097.
33. Mueller C, August A. Attenuation of immunological symptoms of allergic asthma in mice lacking the tyrosine kinase ITK. J Immunol 2003;170:5056-5063.
34. Holtzman M, Morton J, Shornick L, Tyner J, O'Sullivan M, Antao A, Castro M, Walter M. Immunity, inflammation, and remodeling in the airway epithelial barrier:epithelial-viral-allergicparadigm. Physiol Rev 2002;82:19-46.
35. Ying S, Durham S, Corrigan C, Hamid Q, Kay A. Phenotype of cells expressing mRNA for TH2-type (interleukin 4 and interleukin 5) and TH1-type (interleukin 2 and interferon gamma) cytokines in bronchoalveolar lavage and bronchial biopsies from atopic asthmatic and normal control subjects. Am J Respir Cell Mol Biol 1995;12:477-487.
36. Nakanishi A, Morita S, Iwashita H, Sagiya Y, Ashida Y, Shirafuji H, Fujisawa Y, Nishimura O, Fujino M. Role of gob-5 in mucus overproduction and airway hyperresponsiveness in asthma. Proc Natl Acad Sci USA 2001;98:5175-5180.
37. Jousilahti P, Salomaa V, Hakala K, Rasi V, Vahtera E, Palosuo T. The association of sensitive systemic inflammation markers with bronchial asthma. Ann Allergy Asthma Immunol 2002;89:381-385.
38. Zhou Y, Dong Q, Louahed J, Dragwa C, Savio D, Huang M, Weiss C, Tomer Y, McLane MP, Nicolaides NC, et al. Characterization of a calcium-activated chloride channel as a shared target of Th2 cytokine pathways and its potential involvement in asthma. Am J Respir Cell Mol Biol 2001;25:486-491.
39. Fahy JV, Corry DB, Boushey HA. Airway inflammation and remodeling in asthma. Curr Opin Pulm Med 2000;6:15-20.
40. Leigh R, Ellis R, Wattie JN, Hirota JA, Matthaei KI, Foster PS, O'Byrne PM, Inman MD. Type 2 cytokines in the pathogenesis of sustained airway dysfunction and airway remodeling in mice. Am J Respir Crit Care Med 2004;169:860-867.
41. Zhang W, Zhang X, Qiu D, Sandford A, Tan WC. IL-4 receptor genetic polymorphisms and asthma in Asian populations. Respir Med [online ahead of print] June 6, 2006; DOI: 10.1016/j.rmed.2006.04.004. Most recent version available from: http://dx.doi.org/10.1016/j.rmed.2006.04.004
42. Pope SM, Fulkerson PC, Blanchard C, Akei HS, Nikolaidis NM, Zimmermann N, Molkentin JD, Rothenberg ME. Identification of a cooperative mechanism involving interleukin-13 and eotaxin-2 in experimental allergic lung inflammation. J Biol Chem 2005;280:13952-13961.
43. Berin MC, Eckmann L, Broide DH, Kagnoff MF. Regulated production of the T helper 2-type T-cell chemoattractant TARC by human bronchial epithelial cells in vitro and in human lung xenografts. Am J Respir Cell Mol Biol 2001;24:382-389.
44. Conroy DM, Williams TJ. Eotaxin and the attraction of eosinophils to the asthmatic lung. Respir Res 2001;2:150-156.
45. Miyazaki E, Nureki S, Fukami T, Shigenaga T, Ando M, Ito K, Ando H, Sugisaki K, Kumamoto T, Tsuda T. Elevated levels of thymus- and activation-regulated chemokine in bronchoalveolar lavage fluid from patients with eosinophilic pneumonia. Am J Respir Crit Care Med 2002;165:1125-1131.
46. Wilder JA, Collie DD, Wilson BS, Bice DE, Lyons CR, Lipscomb MF. Dissociation of airway hyperresponsiveness from immunoglobulin E and airway eosinophilia in a murine model of allergic asthma. Am J Respir Cell Mol Biol 1999;20:1326-1334.
47. Birrell MA, Battram CH, Woodman P, McCluskie K, Belvisi MG. Dissociation by steroids of eosinophilic inflammation from airway hyperresponsiveness in murine airways. Respir Res 2003;4:3.
48. Eum SY, Maghni K, Tolloczko B, Eidelman DH, Martin JG. IL-13 may mediate allergen-induced hyperresponsiveness independently of IL-5 or eotaxin by effects on airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 2005;288:L576-L584.
49. Yang G, Volk A, Petley T, Emmell E, Giles-Komar J, Shang X, Li J, Das AM, Shealy D, Griswold DE, et al. Anti-IL-13 monoclonal antibody inhibits airway hyperresponsiveness, inflammation and airway remodeling. Cytokine 2004;28:224-232.
50. Barnes PJ, Chowdhury B, Kharitonov SA, Magnussen H, Page CP, Postma D, Saetta M. Pulmonary biomarkers in COPD. Am J Respir Crit Care Med 2006;174:6-14.
51. Malerba G, Pignatti PF. A review of asthma genetics: gene expression studies and recent candidates. J Appl Genet 2005;46:93-104.
52. Thorn CF, Whitehead AS. Differential transcription of the mouse acute phase serum amyloid A genes in response to pro-inflammatory cytokines. Amyloid 2002;9:229-236.
53. Kelly EA, Jarjour NN. Role of matrix metalloproteinases in asthma. Curr Opin Pulm Med 2003;9:28-33.
54. Ramos CD, Canetti C, Souto JT, Silva JS, Hogaboam CM, Ferreira SH, Cunha FQ. MIP-1α [CCL3] acting on the CCR1 receptor mediates neutrophil migration in immune inflammation via sequential release of TNF-α and LTB4. J Leukoc Biol 2005;78:167-177.
55. Grenningloh R, Gho A, di Lucia P, Klaus M, Bollag W, Ho IC, Sinigaglia F, Panina-Bordignon P. Cutting edge: inhibition of the retinoid X receptor (RXR) blocks T helper 2 differentiation and prevents allergic lung inflammation. J Immunol 2006;176:5161-5166.
56. Desmet C, Gosset P, Pajak B, Cataldo D, Bentires-Alj M, Lekeux P, Bureau F. Selective blockade of NF-kappa B activity in airway immune cells inhibits the effector phase of experimental asthma. J Immunol 2004;173:5766-5775.
57. Kim SR, Lee KS, Park HS, Park SJ, Min KH, Jin SM, Lee YC. Involvement of IL-10 in peroxisome proliferator-activated receptor gamma-mediated anti-inflammatory response in asthma. Mol Pharmacol 2005;68:1568-1575.
58. Wu C, Yang G, Bermudez-Humaran LG, Pang Q, Zeng Y, Wang J, Gao X. Immunomodulatory effects of IL-12 secreted by Lactococcus lactis on Th1/Th2 balance in ovalbumin (OVA)-induced asthma model mice. Int Immunopharmacol 2006;6:610-615.
59. Kanehiro A, Lahn M, Makela MJ, Dakhama A, Fujita M, Joetham A, Mason RJ, Born W, Gelfand EW. Tumor necrosis factor-α negatively regulates airway hyperresponsiveness through γ-δ T cells. Am J Respir Crit Care Med 2001;164:2229-2238.
60. Ek A, Larsson K, Siljerud S, Palmberg L. Fluticasone and budesonide inhibit cytokine release in human lung epithelial cells and alveolar macrophages. Allergy 1999;54:691-699.
61. McKay LI, Cidlowski JA. Cross-talk between nuclear factor-kappa B and the steroid hormone receptors: mechanisms of mutual antagonism. Mol Endocrinol 1998;12:45-56.
62. O'Leary EC, Marder P, Zuckerman SH. Glucocorticoid effects in an endotoxin-induced rat pulmonary inflammation model: differential effects on neutrophil influx, integrin expression, and inflammatory mediators. Am J Respir Cell Mol Biol 1996;15:97-106.
63. Simonin MA, Bordji K, Boyault S, Bianchi A, Gouze E, Becuwe P, Dauca M, Netter P, Terlain B. PPAR-gamma ligands modulate effects of LPS in stimulated rat synovial fibroblasts. Am J Physiol Cell Physiol 2002;282:C125-C133.
64. Chinetti G, Fruchart JC, Staels B. Peroxisome proliferator-activated receptors and inflammation: from basic science to clinical applications. Int J Obes Relat Metab Disord 2003;27:S41-S45.
65. Kallen JA, Schlaeppi J-M, Bitsch F, Delhon I, Fournier B. Crystal structure of the human RORa ligand binding domain in complex with cholesterol sulfate at 2.2Å. J Biol Chem 2004;279:14033-14038.
66. Al-Shawwa B, Al-Huniti N, Titus G, Abu-Hasan M. Hypercholesterolemia is a potential risk factor for asthma. J Asthma 2006;43:231-233.