11β-hydroxysteroid dehydrogenases are regulated during the pulmonary granulomatous response to the mycobacterial glycolipid trehalose-6,6′- dimycolate

NeuroImmunoModulation

Volumn 16, Issue 3, 2009, Pages 147-154

  Abbott, A N ^a,b   Guidry, T V ^b   Welsh, K J ^a   Thomas, A M ^b   Kling, M A ^c   Hunter, R L ^a,b   Actor, J K ^a,b  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c PFIZER INC   (United States)

Author keywords

11 Hydroxysteroid dehydrogenases; Granuloma; Inflammation; Lung; Trehalose 6,6 dimycolate; Tuberculosis

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE; 11BETA HYDROXYSTEROID DEHYDROGENASE 1; 11BETA HYDROXYSTEROID DEHYDROGENASE 2; CORD FACTOR; CORTICOSTERONE; DEHYDROCORTICOSTERONE; GLYCOLIPID; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; 11-DEHYDROCORTICOSTERONE; CYTOKINE; DRUG DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CELL WALL; CONTROLLED STUDY; FEMALE; HORMONAL REGULATION; IMMUNOPATHOLOGY; INFLAMMATION; LUNG GRANULOMATOSIS; LUNG TUBERCULOSIS; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; BAGG ALBINO MOUSE; DISEASE MODEL; DOWN REGULATION; ENZYMOLOGY; GENETICS; IMMUNOLOGICAL TOLERANCE; LUNG; LUNG GRANULOMA; METABOLISM; MICROBIOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; UPREGULATION;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 1; 11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 2; ANIMALS; CORD FACTORS; CORTICOSTERONE; CYTOKINES; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FEMALE; GRANULOMA, RESPIRATORY TRACT; IMMUNE TOLERANCE; LUNG; MICE; MICE, INBRED BALB C; MYCOBACTERIUM TUBERCULOSIS; RNA, MESSENGER; TUBERCULOSIS, PULMONARY; UP-REGULATION;

EID: 60749088602     PISSN: 10217401     EISSN: None     Source Type: Journal    
DOI: 10.1159/000204227     Document Type: Article

References (47)

1. Balow JE, Hurley DL, Fauci AS: Immunosuppressive effects of glucocorticosteroids: differential effects of acute vs chronic administration on cell-mediated immunity. J Immunol 1975;114:1072-1076.
2. Rook GA, Hernandez-Pando R: Immunological and endocrinological characteristics of tuberculosis that provide opportunities for immunotherapeutic intervention. Novartis Found Symp 1998;217:73-87, discussion 87-98.
3. Bottasso O, Bay ML, Besedovsky H, del Rey A: The immuno-endocrine component in the pathogenesis of tuberculosis. Scand J Immunol 2007;66:166-175.
4. Perez RL, Roman J, Staton GW Jr, Hunter RL: Extravascular coagulation and fibrinolysis in murine lung inflammation induced by the mycobacterial cord factor trehalose-6,6′-dimycolate. Am J Respir Crit Care Med 1994;149:510-518.
5. Behling CA, Perez RL, Kidd MR, Staton GW Jr, Hunter RL: Induction of pulmonary granulomas, macrophage procoagulant activity, and tumor necrosis factor-alpha by trehalose glycolipids. Ann Clin Lab Sci 1993;23:256-266.
6. Geisel RE, Sakamoto K, Russell DG, Rhoades ER: In vivo activity of released cell wall lipids of Mycobacterium bovis bacillus Calmette-Guerin is due principally to trehalose mycolates. J Immunol 2005;174:5007-5015.
7. Hunter RL, Olsen MR, Jagannath C, Actor JK: Multiple roles of cord factor in the pathogenesis of primary, secondary, and cavitary tuberculosis, including a revised description of the pathology of secondary disease. Ann Clin Lab Sci 2006;36:371-386.
8. Rao V, Gao F, Chen B, Jacobs WR Jr, Glickman MS: Trans -cyclopropanation of mycolic acids on trehalose dimycolate suppresses Mycobacterium tuberculosis-induced inflammation and virulence. J Clin Invest 2006;116:1660-1667.
9. Wang Z, Schwab U, Rhoades E, Chess PR, Russell DG, Notter RH: Peripheral cell wall lipids of Mycobacterium tuberculosis are inhibitory to surfactant function. Tuberculosis (Edinb) 2008;88:178-186.
10. Actor JK, Leonard CD, Watson VE, Wells A, Jagannath C, Hunter RL Jr, Dasgupta A: Cytokine mRNA expression and serum cortisol evaluation during murine lung inflammation induced by Mycobacterium tuberculosis. Comb Chem High Throughput Screen 2000;3:343-351.
11. Perez RL, Roman J, Roser S, Little C, Olsen M, Indrigo J, Hunter RL, Actor JK: Cytokine message and protein expression during lung granuloma formation and resolution induced by the mycobacterial cord factor trehalose-6,6′-dimycolate. J Interferon Cytokine Res 2000;20:795-804.
12. Welsh KJ, Abbott AN, Hwang SA, Indrigo J, Armitige LY, Blackburn MR, Hunter RL Jr, Actor JK: A role for tumour necrosis factor-alpha, complement C5 and interleukin-6 in the initiation and development of the mycobacterial cord factor trehalose 6,6′-dimycolate induced granulomatous response. Microbiology 2008;154:1813-1824.
13. McEwen BS, Biron CA, Brunson KW, Bulloch K, Chambers WH, Dhabhar FS, Goldfarb RH, Kitson RP, Miller AH, Spencer RL, Weiss JM: The role of adrenocorticoids as modulators of immune function in health and disease: neural, endocrine and immune interactions. Brain Res Brain Res Rev 1997;23:79-133.
14. Elenkov IJ, Chrousos GP: Stress hormones, proinflammatory and antiinflammatory cytokines, and autoimmunity. Ann NY Acad Sci 2002;966:290-303.
15. Elenkov IJ, Chrousos GP: Stress system - organization, physiology and immunoregulation. Neuroimmunomodulation 2006;13:257-267.
16. Seckl JR, Walker BR: 11beta-hydroxysteroid dehydrogenase type 1 as a modulator of glucocorticoid action: from metabolism to memory. Trends Endocrinol Metab 2004;15:418-424.
17. Holmes MC, Yau JL, Kotelevtsev Y, Mullins JJ, Seckl JR: 11 Beta-hydroxysteroid dehydrogenases in the brain: two enzymes two roles. Ann NY Acad Sci 2003;1007:357-366.
18. Seckl JR, Walker BR: Minireview: 11beta-hydroxysteroid dehydrogenase type 1 - a tissue-specific amplifier of glucocorticoid action. Endocrinology 2001;142:1371-1376.
19. Guidry TV, Hunter RL Jr, Actor JK: Mycobacterial glycolipid trehalose 6,6′-dimycolate-induced hypersensitive granulomas: contribution of CD4+ lymphocytes. Microbiology 2007;153:3360-3369.
20. Guidry TV, Olsen M, Kil KS, Hunter RL Jr, Geng YJ, Actor JK: Failure of CD1D-/- mice to elicit hypersensitive granulomas to mycobacterial cord factor trehalose 6,6′-dimycolate. J Interferon Cytokine Res 2004;24:362-371.
21. Collins FM, Congdon CC, Morrison NE: Growth of Mycobacterium bovis (BCG) in T lymphocyte-depleted mice. Infect Immun 1975;11:57-64.
22. Guidry TV, Hunter RL Jr, Actor JK: CD3+ cells transfer the hypersensitive granulomatous response to mycobacterial glycolipid trehalose 6,6′-dimycolate in mice. Microbiology 2006;152:3765-3775.
23. Bustin SA: Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol 2000;25:169-193.
24. Heid CA, Stevens J, Livak KJ, Williams PM: Real time quantitative PCR. Genome Res 1996;6:986-994.
25. -ΔΔCT method. Methods 2001;25:402-408.
26. Yamagami H, Matsumoto T, Fujiwara N, Arakawa T, Kaneda K, Yano I, Kobayashi K: Trehalose 6,6′-dimycolate (cord factor) of Mycobacterium tuberculosis induces foreign-body- and hypersensitivity-type granulomas in mice. Infect Immun 2001;69:810-815.
27. Pelletier M, Forget A, Bourassa D, Gros P, Skamene E: Immunopathology of BCG infection in genetically resistant and susceptible mouse strains. J Immunol 1982;129:2179-2185.
28. Stewart PM, Krozowski ZS: 11 beta-Hydroxysteroid dehydrogenase. Vitam Horm 1999;57:249-324.
29. Rook GA, Hernandez-Pando R: Pathogenetic role, in human and murine tuberculosis, of changes in the peripheral metabolism of glucocorticoids and antiglucocorticoids. Psychoneuroendocrinology 1997;22(suppl 1):S109-S113.
30. Baker RW, Walker BR, Shaw RJ, Honour JW, Jessop DS, Lightman SL, Zumla A, Rook GA: Increased cortisol:cortisone ratio in acute pulmonary tuberculosis. Am J Respir Crit Care Med 2000;162:1641-1647.
31. Algood HM, Lin PL, Yankura D, Jones A, Chan J, Flynn JL: TNF influences chemokine expression of macrophages in vitro and that of CD11b+ cells in vivo during Mycobacterium tuberculosis infection. J Immunol 2004;172:6846-6857.
32. Chensue SW, Warmington KS, Ruth JH, Lincoln P, Kunkel SL: Cytokine function during mycobacterial and schistosomal antigen-induced pulmonary granuloma formation. Local and regional participation of IFN-gamma, IL-10, and TNF. J Immunol 1995;154:5969-5976.
33. Chrousos GP: The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation. N Engl J Med 1995;332:1351-1362.
34. Morand EF, Leech M: Glucocorticoid regulation of inflammation: the plot thickens. Inflamm Res 1999;48:557-560.
35. Davies E, MacKenzie SM: Extra-adrenal production of corticosteroids. Clin Exp Pharmacol Physiol 2003;30:437-445.
36. Brown DH, Sheridan J, Pearl D, Zwilling BS: Regulation of mycobacterial growth by the hypothalamus-pituitary-adrenal axis: differential responses of Mycobacterium bovis BCG-resistant and -susceptible mice. Infect Immun 1993;61:4793-4800.
37. Brown DH, Zwilling BS: Activation of the hypothalamic-pituitary-adrenal axis differentially affects the anti-mycobacterial activity of macrophages from BCG-resistant and susceptible mice. J Neuroimmunol 1994;53:181-187.
38. Rees RJ, Hart PD: Analysis of the host-parasite equilibrium in chronic murine tuberculosis by total and viable bacillary counts. Br J Exp Pathol 1961;42:83-88.
39. Actor JK, Olsen M, Jagannath C, Hunter RL: Relationship of survival, organism containment, and granuloma formation in acute murine tuberculosis. J Interferon Cytokine Res 1999;19:1183-1193.
40. Gilmour JS, Coutinho AE, Cailhier JF, Man TY, Clay M, Thomas G, Harris HJ, Mullins JJ, Seckl JR, Savill JS, Chapman KE: Local amplification of glucocorticoids by 11 beta-hydroxysteroid dehydrogenase type 1 promotes macrophage phagocytosis of apoptotic leukocytes. J Immunol 2006;176:7605-7611.
41. Lim HY, Muller N, Herold MJ, van den Brandt J, Reichardt HM: Glucocorticoids exert opposing effects on macrophage function dependent on their concentration. Immunology 2007;122:47-53.
42. Sheridan JF, Dobbs C, Brown D, Zwilling B: Psychoneuroimmunology: stress effects on pathogenesis and immunity during infection. Clin Microbiol Rev 1994;7:200-212.
43. Rey AD, Mahuad CV, Bozza VV, Bogue C, Farroni MA, Bay ML, Bottasso OA, Besedovsky HO: Endocrine and cytokine responses in humans with pulmonary tuberculosis. Brain Behav Immun 2007;21:171-179.
44. Seckl JR, Morton NM, Chapman KE, Walker BR: Glucocorticoids and 11beta-hydroxysteroid dehydrogenase in adipose tissue. Recent Prog Horm Res 2004;59:359-393.
45. Hunter RL, Jagannath C, Actor JK: Pathology of postprimary tuberculosis in humans and mice: contradiction of long-held beliefs. Tuberculosis (Edinb) 2007;87:267-278.
46. Webster JI, Sternberg EM: Role of the hypothalamic-pituitary-adrenal axis, glucocorticoids and glucocorticoid receptors in toxic sequelae of exposure to bacterial and viral products. J Endocrinol 2004;181:207-221.
47. Abbott A, Guidry T, Welsh K, Hunter R, Actor J: Involvement of 11β-hydroxysteroid dehydrogenase type 2 during the pulmonary granulomatous response to mycobacterial glycolipid trehalose-6,6′-dimycolate. Conference abstracts, American Society for Microbiology 107th General Meeting, Toronto, 2007.