Th2 cytokine-induced upregulation of 11β-hydroxysteroid dehydrogenase-1 facilitates glucocorticoid suppression of proasthmatic airway smooth muscle function

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 296, Issue 5, 2009, Pages

  Hu, Aihua ^a   Fatma, Sumbul ^a   Cao, Jing ^a   Grunstein, Judith S ^a   Nino, Gustavo ^a   Grumbach, Yael ^a   Grunstein, Michael M ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

Activator protein 1; Asthma; Glucocorticoid receptor transactivation; Mitogen activated protein kinase activation; T helper type 2 cytokines

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 1; CORTISONE; DEXAMETHASONE; HYDROCORTISONE; INTERLEUKIN 13; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OXIDOREDUCTASE; TRANSCRIPTION FACTOR AP 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREATHING MUSCLE; CONTROLLED STUDY; DRUG BIOAVAILABILITY; DRUG EFFECT; ENZYME ACTIVITY; GENE AMPLIFICATION; HUMAN; HUMAN CELL; MUSCLE FUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; SMOOTH MUSCLE FIBER; TH2 CELL; TRANSCRIPTION INITIATION; UPREGULATION;

11-BETA-HYDROXYSTEROID DEHYDROGENASES; ANIMALS; ASTHMA; CORTISONE; CYTOKINES; CYTOPROTECTION; ENZYME ACTIVATION; GLUCOCORTICOIDS; HUMANS; INTERLEUKIN-13; INTERLEUKIN-4; LUNG; MITOGEN-ACTIVATED PROTEIN KINASES; MUSCLE CONTRACTION; MUSCLE RELAXATION; MUSCLE, SMOOTH; MYOCYTES, SMOOTH MUSCLE; RABBITS; RESPONSE ELEMENTS; TH2 CELLS; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 66149183019     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.90572.2008     Document Type: Article

References (57)

1. Bai TR. Abnormalities in airway smooth muscle in fatal asthma. Am Rev Respir Dis 141: 552-557, 1990. (Pubitemid 20109136)
2. Bai TR, Mak JC, Barnes PJ. A comparison of beta-adrenergic receptors and in vitro relaxant responses to isoproterenol in asthmatic airway smooth muscle. Am J Respir Cell Mol Biol 6: 647-651, 1992.
3. Barnes PJ. Anti-inflammatory actions of glucocorticoids: molecular mechanisms. Clin Sci 94: 557-572, 1998. (Pubitemid 28269054)
4. Best R, Nelson SM, Walker BR. Dexamethasone and 11-dehydrodexamethasone as tools to investigate the isozymes of 11 beta-hydroxysteroid dehydrogenase in vitro and in vivo. J Endocrinol 153: 41-48, 1997. (Pubitemid 27146256)
5. Blum A, Maser E. Enzymology and molecular biology of glucocorticoid metabolism in humans. Prog Nucleic Acid Res Mol Biol 75: 173-216, 2003. (Pubitemid 137639558)
6. Blumenthal MN, Mclean JA, Mathews KP, Sheldon JM, Mich AA. Adrenal-pituitary function in bronchial asthma. Arch Intern Med 117: 34-38, 1996.
7. Cai TQ, Wong B, Mundt SS, Thieringer R, Wright SD, Hermanowski-Vosatka A. Induction of 11beta-hydroxysteroid dehydrogenase type 1 but not -2 in human aortic smooth muscle cells by inflammatory stimuli. J Steroid Biochem Mol Biol 77: 117-122, 2001. (Pubitemid 32476819)
8. Cano E, Mahadevan LC. Parallel signal processing among mammalian MAPKs. Trends Biochem Sci 20: 117-122, 1995.
9. Chapman KE, Coutinho A, Gray M, Gilmour JS, Savill JS, Seckl JR. Local amplification of glucocorticoids by 11beta-hydroxysteroid dehydrogenase type 1 and its role in the inflammatory response. Ann NY Acad Sci 1088: 265-273, 2006. (Pubitemid 47092051)
10. Chapoval SP, Al-Garawi A, Lora JM, Strickland I, Ma B, Lee PJ, Homer RJ, Ghosh S, Coyle AJ, Elias JA. Inhibition of NF-kappaB activation reduces the tissue effects of transgenic IL-13. J Immunol 179: 7030-7041, 2007.
11. Cooper MS, Bujalska I, Rabbitt E, Walker EA, Bland R, Sheppard MC, Hewison M, Stewart PM. Modulation of 11beta-hydroxysteroid dehydrogenase isozymes by proinflammatory cytokines in osteoblasts: an autocrine switch from glucocorticoid inactivation to activation. J Bone Miner Res 16: 1037-1044, 2001. (Pubitemid 32467147)
12. Damo M, Rabier M, Loubatiere J, Blotman F, Crastes de Paulet A. Glucocorticoid receptors in fibroblasts from synovial tissue. Changes during the inflammatory process. Preliminary results. Agents Actions 17: 478-483, 1986. (Pubitemid 16111308)
13. De Bie JJ, Hessel EM, Van Ark I, Van Esch B, Hofman G, Nijkamp FP, Van Oosterhout AJ. Effect of dexamethasone and endogenous corticosterone on airway hyperresponsiveness and eosinophilia in the mouse. Br J Pharmacol 119: 1484-1490, 1996. (Pubitemid 26402028)
14. Freeman L, Hewison M, Hughes SV, Evans KN, Hardie D, Means TK, Chakraverty R. Expression of 11beta-hydroxysteroid dehydrogenase type 1 permits regulation of glucocorticoid bioavailability by human dendritic cells. Blood 106: 2042-2049, 2005. (Pubitemid 41291718)
15. Fujitaka M, Nomura S, Sakura N, Ueda K, Matuura R, Yumiba C. Morning and afternoon serum levels of cortisone and cortisol in asthmatic patients. Clin Chim Acta 299: 101-108, 2000. (Pubitemid 30438793)
16. Georen S, Ahnblad P, Stjarne P, Wikstrom AC, Stierna P. Significance of endogenous glucocorticoid sensitivity for airway eosinophilia in a murine model of allergy. Acta Otolaryngol (Stockh) 125: 378-385, 2005. (Pubitemid 40525000)
17. Gladman DD, Urowitz MB, Doris F, Lewandowski K, Anhorn K. Glucocorticoid receptors in systemic lupus erythematosus. J Rheumatol 18: 681-684, 1991.
18. Goldie RG, Spina D, Henry PJ, Lulich KM, Paterson JW. In vitro responsiveness of human asthmatic bronchus to carbachol, histamine, β-adrenoceptor agonists and theophylline. Br J Clin Pharmacol 22: 669-676, 1986. (Pubitemid 17199006)
19. Goldsmith AM, Hershenson MB, Wolbert MP, Bentley JK. Regulation of airway smooth muscle alpha-actin expression by glucocorticoids. Am J Physiol Lung Cell Mol Physiol 292: L99-L106, 2007. (Pubitemid 46103435)
20. Goto K, Chiba Y, Sakai H, Misawa M. Glucocorticoids inhibited airway hyperresponsiveness through downregulation of CPI-17 in bronchial smooth muscle. Eur J Pharmacol 591: 231-236, 2008.
21. Grunig G, Warnock M, Wakil AE, Venkayya R, Brombacher F, Rennic DM, Sheppard D, Mohrs M, Donaldson DD, Locksley RM, Corry DB. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 282: 2261-2263, 1998. (Pubitemid 29004075)
22. Grunstein MM, Hakonarson H, Leiter J, Chen M, Whelan R, Grunstein JS, Chuang S. IL-13-dependent autocrine signaling mediates altered responsiveness of IgE-sensitized airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 282: L520-L528, 2002. (Pubitemid 34654657)
23. Hakonarson H, Grunstein MM. Autocrine regulation of airway smooth muscle responsiveness. Respir Physiol Neurobiol 137: 263-276, 2003. (Pubitemid 37153287)
24. Hakonarson H, Halapi E, Whelan R, Gulcher J, Stefansson K, Grunstein MM. Association between IL-1β/TNF-α-induced glucocorticoid-sensitive changes in multiple gene expression and altered responsiveness in airway smooth muscle. Am J Respir Cell Mol Biol 25: 761-771, 2001. (Pubitemid 33124694)
25. Hakonarson H, Herrick DJ, Grunstein MM. Mechanism of impaired β-adrenoceptor responsiveness in atopic sensitized airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 269: L645-L652, 1995.
26. Hardy R, Rabbitt EH, Filer A, Emery P, Hewison M, Stewart PM, Gittoes NJ, Buckley CD, Raza K, Cooper MS. Local and systemic glucocorticoid metabolism in inflammatory arthritis. Ann Rheum Dis 67: 1204-1210, 2008.
27. Hirst SJ, Lee TH. Airway smooth muscle as a target of glucocorticoid action in the treatment of asthma. Am J Respir Crit Care Med 158: S201-S206, 1998. (Pubitemid 28536591)
28. 2-adrenoceptor desensitization promotes proasthmatic airway smooth muscle function via PKA/ERK1/2-mediated phosphodiesterase-4 induction. Am J Physiol Lung Cell Mol Physiol 294: L1055-L1067, 2008.
29. Irusen E, Matthews JG, Takahashi A, Barnes PJ, Chung KF, Adcock IM. p38 Mitogen-activated protein kinase-induced glucocorticoid receptor phosphorylation reduces its activity: role in steroid-insensitive asthma. J Allergy Clin Immunol 109: 649-657, 2002. (Pubitemid 34327193)
30. Kam JC, Szefler SJ, Surs W, Sher ER, Leung DY. Combination IL-2 and IL-4 reduces glucocorticoid receptor-binding affinity and T cell response to glucocorticoids. J Immunol 151: 3460-3466, 1993. (Pubitemid 23282658)
31. Kang BN, Jude JA, Panettieri RA Jr, Walseth TF, Kannan MS. Glucocorticoid regulation of CD38 expression in human airway smooth muscle cells: role of dual specificity phosphatase 1. Am J Physiol Lung Cell Mol Physiol 295: L186-L193, 2008.
32. Karin M, Liu Z, Zandi E. AP-1 function and regulation. Curr Opin Cell Biol 9: 240-246, 1997. (Pubitemid 27135992)
33. Laporte JC, Moore PE, Baraldo S, Jouvin MH, Church TL, Swartzman IN, Panettieri RA Jr, Kinet JP, Shore SA. Direct effects of interleukin-13 on signaling pathways for physiological responses in cultured human airway smooth muscle cells. Am J Respir Crit Care Med 164: 141-148, 2001. (Pubitemid 33151311)
34. Maser E, Volker B, Friebertshauser J. 11 Beta-hydroxysteroid dehydrogenase type 1 from human liver: dimerization and enzyme cooperativity support its postulated role as glucocorticoid reductase. Biochemistry 41: 2459-2465, 2002. (Pubitemid 34160910)
35. Muller C, Cluzeaud F, Pinon GM, Rafestin-Oblin ME, Morfin R. Dehydroepiandrosterone and its 7-hydroxylated metabolites do not interfere with the transactivation and cellular trafficking of the glucocorticoid receptor. J Steroid Biochem Mol Biol 92: 469-476, 2004. (Pubitemid 40187164)
36. Nagai H, Tsuji F, Goto S, Koda A. Pharmacological study of bacterial lipopolysaccharide-induced airway hyperresponsiveness in guinea-pigs. Arch Int Pharmacodyn Ther 313: 161-175, 1991.
37. Ozols J. Lumenal orientation and post-translational modifications of the liver microsomal 11 beta-hydroxysteroid dehydrogenase. J Biol Chem 270: 2305-2312, 1995.
38. Panettieri RA Jr. Effects of corticosteroids on structural cells in asthma, and chronic obstructive pulmonary disease. Proc Am Thorac Soc 1: 231-234, 2004.
39. Peebles RS Jr, Togias A, Bickel CA, Diemer FB, Hubbard WC, Schleimer RP. Endogenous glucocorticoids and antigen-induced acute and late phase pulmonary responses. Clin Exp Allergy 30: 1257-1265, 2000.
40. Sasaki H, Yanai M, Shimura S, Okayama H, Aikawa T, Sasaki T, Takishima T. Late asthmatic response to Ascaris antigen challenge in dogs treated with metyrapone. Am Rev Respir Dis 136: 1459-1465, 1987. (Pubitemid 18030283)
41. Schottelius A, Wedel S, Weltrich R, Rohde W, Buttgereit F, Schreiber S, Lochs H. Higher expression of glucocorticoid receptor in peripheral mononuclear cells in inflammatory bowel disease. Am J Gastroenterol 95: 1994-1999, 2000.
42. Shan X, Hu A, Veler H, Fatma S, Grunstein JS, Chuang S, Grunstein MM. Regulation of Toll-like receptor 4-induced proasthmatic changes in airway smooth muscle function by opposing actions of ERK1/2 and p38 MAPK signaling. Am J Physiol Lung Cell Mol Physiol 291: L324-L333, 2006. (Pubitemid 44343706)
43. Sher ER, Leung DY, Surs W, Kam JC, Zieg G, Kamada AK, Szefler SJ. Steroid-resistant asthma. Cellular mechanisms contributing to inadequate response to glucocorticoid therapy. J Clin Invest 93: 33-39, 1994. (Pubitemid 24030817)
44. Shore SA, Moore PE. Regulation of β-adrenergic responses in airway smooth muscle. Respir Physiol Neurobiol 137: 179-195, 2003. (Pubitemid 37158008)
45. Silverman ES, Breault DT, Vallone J, Subramanian S, Yilmaz AD, Mathew S, Subramaniam V, Tantisira K, Pacak K, Weiss ST, Majzoub JA. Corticotropin- releasing hormone deficiency increases allergen-induced airway inflammation in a mouse model of asthma. J Allergy Clin Immunol 114: 747-754, 2004. (Pubitemid 39330242)
46. Singh RP, Dhawan P, Golden C, Kapoor GS, Mehta KD. One-way cross-talk between p38(MAPK) and p42/44(MAPK). Inhibition of p38(MAPK) induces low density lipoprotein receptor expression through activation of the p42/44(MAPK) cascade. J Biol Chem 274: 19593-19600, 1999. (Pubitemid 129519400)
47. Spahn JD, Szefler SJ, Surs W, Doherty DE, Nimmagadda SR, Leung DY. A novel action of IL-13: induction of diminished monocyte glucocorticoid receptor-binding affinity. J Immunol 157: 2654-2659, 1996. (Pubitemid 126450482)
48. Thieringer R, Le Grand CB, Carbin L, Cai TQ, Wong B, Wright SD S, Hermanowski-Vosatka A. 11 Beta-hydroxysteroid dehydrogenase type 1 is induced in human monocytes upon differentiation to macrophages. J Immunol 167: 30-35, 2001. (Pubitemid 32567757)
49. Tomlinson JW, Walker EA, Bujalska IJ, Draper N, Lavery GG, Cooper MS, Hewison M, Stewart PM. 11Beta-hydroxysteroid dehydrogenase type 1: a tissue-specific regulator of glucocorticoid response. Endocr Rev 25: 831-866, 2004. (Pubitemid 39366049)
50. Vacchio MS, Papadopoulos V, Ashwell JD. Steroid production in the thymus: implications for thymocyte selection. J Exp Med 179: 1835-1846, 1994. (Pubitemid 24155664)
51. + T lymphocytes elicits reciprocal proasthmatic changes in airway function. J Immunol 178: 3627-3636, 2007.
52. Verheggen MM, van Hal PT, Adriaansen-Soeting PW, Goense BJ, Hoogsteden HC, Brinkmann AO, Versnel MA. Modulation of glucocorticoid receptor expression in human bronchial epithelial cell lines by IL-1 beta, TNF-alpha and LPS. Eur Respir J 9: 2036-2043, 1996. (Pubitemid 26333541)
53. Webster JC, Cidlowski JA. Mechanisms of glucocorticoid-receptor-mediated repression of gene expression. Trends Endocrinol Metab 10: 396-402, 1999.
54. Williams LJ, Lyons V, MacLeod I, Rajan V, Darlington GJ, Poli V, Seckl JR, Chapman KE. C/EBP regulates hepatic transcription of 11beta-hydroxysteroid dehydrogenase type 1. A novel mechanism for crosstalk between the C/EBP and glucocorticoid signaling pathways. J Biol Chem 275: 30232-30239, 2000.
55. Wills-Karp M, Luyimbazi J, Xu X, Schofield B, Neben TY, Karp CL, Donaldson DD. Interleukin-13: central mediator of allergic asthma. Science 282: 2258-2260, 1998. (Pubitemid 29004074)
56. Zhang H, Shi X, Hampong M, Blanis L, Pelech S. Stress-induced inhibition of ERK1 and ERK2 by direct interaction with p38 MAP kinase. J Biol Chem 276: 6905-6908, 2001. (Pubitemid 37391982)
57. Zhang TY, Ding X, Daynes RA. The expression of 11 beta-hydroxysteroid dehydrogenase type I by lymphocytes provides a novel means for intracrine regulation of glucocorticoid activities. J Immunol 174: 879-889, 2005. (Pubitemid 40094283)