Transforming growth factor-β1 suppression of endotoxin-induced heme oxygenase-1 in macrophages involves activation of Smad2 and downregulation of Ets-2

Journal of Cellular Physiology

Volumn 227, Issue 1, 2012, Pages 351-360

  Chung, Su Wol ^a,b   Kwon, Min Young ^b   Kang, Young Ho ^b   Chung, Hun Taeg ^b   Lee, Seon Jin ^a   Kim, Hong Pyo ^b   Perrella, Mark A ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b University of Ulsan   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; ESCHERICHIA COLI ENDOTOXIN; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; HEME OXYGENASE 1; MESSENGER RNA; RECOMBINANT TRANSFORMING GROWTH FACTOR BETA1; SMAD2 PROTEIN; TRANSCRIPTION FACTOR ETS 2;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BINDING SITE; CONTROLLED STUDY; DOWN REGULATION; INFLAMMATION; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION SITE; UPREGULATION;

ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; DOWN-REGULATION; ENDOTOXINS; ENZYME ACTIVATION; GENE SILENCING; HEME OXYGENASE-1; INFLAMMATION; MACROPHAGES; MICE; PROTO-ONCOGENE PROTEIN C-ETS-2; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA1;

BACTERIA (MICROORGANISMS);

EID: 80054919933     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22741     Document Type: Article

References (57)

1. Abraham NG, Kappas A. 2005. Heme oxygenase and the cardiovascular-renal system. Free Radic Biol Med 39:1-25.
2. Abraham E, Singer M. 2007. Mechanisms of sepsis-induced organ dysfunction. Crit Care Med 35:2408-2416.
3. Alam J, Cook JL. 2003. Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr Pharm Des 9:2499-2511.
4. Alam J, Cook JL. 2007. How many transcription factors does it take to turn on the heme oxygenase-1 gene? Am J Respir Cell Mol Biol 36:166-174.
5. Alam J, Cai J, Smith A. 1994. Isolation and characterization of the mouse heme oxygenase-1 gene. Distal 5' sequences are required for induction by heme or heavy metals. J Biol Chem 269:1001-1009.
6. Alam J, Camhi S, Choi AMK. 1995. Identification of a second region upstream of the mouse heme oxygenase-1 gene that functions as a basal level and inducer-dependent transcriptional enhancer. J Biol Chem 270:11977-11984.
7. Anderson KL, Perkin H, Surh CD, Venturini S, Maki RA, Torbett BE. 2000. Transcription factor PU.1 is necessary for development of thymic and myeloid progenitor-derived dendritic cells J Immunol 164:1855-1861.
8. Bone RC, Grodzin CJ, Balk RA. 1997. Sepsis: A new hypothesis for pathogenesis of the disease process. Chest 112:235-243.
9. Camhi SL, Alam J, Otterbein L, Sylvester SL, Choi AMK. 1995. Induction of heme oxygenase-1 gene expression by lipopolysaccharide is mediated by AP-1 activation. Am J Respir Cell Mol Biol 13:387-398.
10. Chen Y-H, Layne MD, Watanabe M, Yet S-F, Perrella MA. 2001. Upstream stimulatory factors regulate aortic preferentially expressed gene-1 expression in vascular smooth muscle cells. J Biol Chem 276:47658-47663.
11. Choi AMK, Alam J. 1996. Heme oxygenase-1: Function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Respir Cell Mol Biol 15:9-19.
12. Chung SW, Chen Y-H, Perrella MA. 2005. Role of Ets-2 in the regulation of heme oxygenase-1 by endotoxin. J Biol Chem 280:4578-4584.
13. Chung SW, Chen Y-H, Yet S-F, Layne MD, Perrella MA. 2006. Endotoxin-induced down-regulation of Elk-3 facilitates heme oxygenase-1 induction in macrophages. J Immunol 176:2414-2420.
14. Chung SW, Liu X, Macias AA, Baron RM, Perrella MA. 2008. Heme oxygenase-1-derived carbon monoxide enhances the host defense response to microbial sepsis in mice. J Clin Invest 118:239-247.
15. Deramaudt BM, Remy P, Abraham NG. 1999. Upregulation of human heme oxygenase gene expression by Ets-family proteins. J Cell Biochem 72:311-321.
16. Dhulipala PD, Datta PK, Reddy ES, Lianos EA. 2005. Differential regulation of the rat heme oxygenase-1 expression by Ets oncoproteins in glomerular mesangial cells. J Lab Clin Med 146:326-332.
17. Dittmer J, Nordheim A. 1998. Ets transcription factors and human disease. Biochim Biophys Acta 1377:F1-F11.
18. Ejima K, Layne MD, Carvajal IM, Nanri H, Ith B, Yet S-F, Perrella MA. 2002. Modulation of the thioredoxin system during inflammatory responses and its effect on heme oxygenase-1 expression. Antioxid Redox Signal 4:569-576.
19. Ejima K, Layne MD, Carvajal IM, Kritek PA, Baron RM, Chen Y-H, vom Saal J, Levy BD, Yet S-F, Perrella MA. 2003. Cyclooxygenase-2 deficient mice are resistant to endotoxin-induced inflammation and death. FASEB J 10:1325-1327.
20. Feng X-H, Derynck R. 2005. Specificity and versatility in TGF-b signaling through Smads. Annu Rev Cell Dev Biol 21:659-693.
21. Fowles LF, Martin ML, Lelsen L, Stacey KJ, Redd D, Clark YM, Nagamine Y, McMahon M, Hume DA, Ostrowski MC. 1998. Persistent activation of mitogen-activated protein kinases p42 and p44 and ets-2 phosphorylation in response to colony-stimulating factor 1/c-fms signaling. Mol Cell Biol 18:5148-5156.
22. Fujiwara N, Kobayashi K. 2005. Macrophages in inflammation. Curr Drug Targets Inflamm Allergy 4:281-286.
23. Hayashi H, Abdollah S, Qiu Y, Cai J, Xu YY, Grinnell BW, Richardson MA, Topper JN, Gimbrone MA, Jr., Wrana JL, Falb D. 1997. The MAD-related protein Smad7 associates with the TGFbeta receptor and functions as an antagonist of TGFbeta signaling. Cell 89:1165-1173.
24. Hill-Kapturczak N, Truong L, Thamilselvan V, Visner GA, Nick HS, Agarwal A. 2000. Smad7-dependent regulation of heme oxygenase-1 by transforming growth factor-beta in human renal epithelial cells. J Biol Chem 275:40904-40909.
25. Hung CC, Liu X, Kwon MY, Kang YH, Chung SW, Perrella MA. 2010. Regulation of heme oxygenase-1 gene by peptidoglycan involves the interaction of Elk-1 and C/EBPalpha to increase expression. Am J Physiol Lung Cell Mol Physiol 298:L870-L879.
26. Huynh ML, Fadok VA, Henson PM. 2002. Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-beta1 secretion and the resolution of inflammation. J Clin Invest 109:41-50.
27. Jao HC, Lin YT, Tsai LY, Wang CC, Liu HW, Hsu C. 2005. Early expression of heme oxygenase-1 in leukocytes correlates negatively with oxidative stress and predicts hepatic and renal dysfunction at late stage of sepsis. Shock 23:464-469.
28. Kulkarni AB, Huh C-G, Becker D, Geiser A, Lyght M, Flanders KC, Roberts AB, Sporn MB, Ward JM, Karlsson S. 1993. Transforming growth factor b1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci USA 90:770-774.
29. Li MO, Wan YY, Sanjabi S, Robertson AK, Flavell RJ. 2006. Transforming growth factor-beta regulation of immune responses. Annu Rev Immunol 24:99-146.
30. Lin CC, Chiang LL, Lin CH, Shih CH, Liao YT, Hsu MJ, Chen BC. 2007. Transforming growth factor-beta1 stimulates heme oxygenase-1 expression via the PI3K/Akt and NF-kappaB pathways in human lung epithelial cells. Eur J Pharmacol 560:101-109.
31. Maines MD, Gibbs PEM. 2005. 30 years of heme oxygenase: From a "molecular wrecking ball" to a "mesmerizing" trigger of cellular events. Biochem Biophys Res Commun 338:568-577.
32. Martinez FO, Sica A, Mantovani A, Locati M. 2008. Macrophage activation and polarization. Front Biosci 13:453-461.
33. Ning W, Song R, Li C, Park E, Mohesenin A, Choi AMK, Choi ME. 2002. TGF-b1 stimulates HO-1 via the p38 mitogen-activated protein kinase in A549 pulmonary epithelial cells. Am J Physiol (Lung Cell Mol Physiol) 283:L1094-L1102.
34. Otterbein L, Sylvester SL, Choi AMK. 1995. Hemoglobin provides protection against lethal endotoxemia in rats: The role of heme oxygenase-1. Am J Respir Cell Mol Biol 13:595-601.
35. Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA, Choi AM. 2000. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 6:422-428.
36. Overhaus M, Moore BA, Barbato JE, Behrendt FF, Doering JG, Bauer AJ. 2006. Biliverdin protects against polymicrobial sepsis by modulating inflammatory mediators. Am J Physiol (Gastrointest Liver Physiol) 290:G295-G703.
37. Pellacani A, Wiesel P, Sharma A, Foster LC, Huggins GS, Yet S-F, Perrella MA. 1998. Induction of heme oxygenase-1 during endotoxemia is downregulated by transforming growth factor-β1. Circ Res 83:396-403.
38. Pinsky MR. 2001. Sepsis: A pro- and anti-inflammatory disequilibrium syndrome. Contrib Nephrol 132:354-366.
39. Rushworth SA, Chen XL, Mackman N, Ogborne RM, O'Connell MA. 2005. Lipopolysaccharide-induced heme oxygenase-1 expression in human monocytic cells is mediated via Nrf2 and protein kinase C. J Immunol 175:4408-4415.
40. Rushworth SA, MacEwan DJ, O'Connell MA. 2008. Lipopolysaccharide-induced expression of NAD(P)H:quinone oxidoreductase 1 and heme oxygenase-1 protects against excessive inflammatory responses in human monocytes. J Immunol 181:6730-6737.
41. Ryter SW, Alam J, Choi AMK. 2006. Heme oxygenase-1/carbon monoxide: From basic science to therapeutic implications. Physiol Rev 86:583-650.
42. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, Allen R, Sidman C, Proetzel G, Calvin D, Annunziata N, Doetschman T. 1992. Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature 359:693-699.
43. Sikorski EM, Hock T, Hill-Kapturczak N, Agarwal A. 2004. The story so far: Molecular regulation of the heme oxygenase-1 gene in renal injury. Am J Physiol Renal Physiol 286:F425-F441.
44. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN. 1987. Bilirubin is an antioxidant of possible physiological importance. Science 235:1042-1046.
45. Takimoto T, Wakabayashi Y, Sekiya T, Inoue N, Morita R, Ichiyama K, Takahashi R, Asakawa M, Muto G, Mori T, Hasegawa E, Shizuya S, Hara T, Nomura M, Yoshimura A. 2010. Smad2 and Smad3 are redundantly essential for the TGF-beta-mediated regulation of regulatory T plasticity and Th1 development. J Immunol 185:842-855.
46. Tenhunen R, Marver HS, Schmid R. 1968. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 61:748-755.
47. Tenhunen R, Marver H, Schmid R. 1969. Microsomal heme oxygenase, characterization of the enzyme. J Biol Chem 244:6388-6394.
48. Traylor A, Hock T, Hill-Kapturczak N. 2007. Specificity protein 1 and Smad-dependent regulation of human heme oxygenase-1 gene by transforming growth factor-b1 in renal epithelial cells. Am J Physiol Renal Physiol 293:F885-F894.
49. Tsunawaki S, Sporn M, Ding A, Nathan C. 1988. Deactivation of macrophages by transforming growth factor-β. Nature 334:260-262.
50. Vile GF, Tyrrell RM. 1993. Oxidative stress resulting from ultraviolet A irradiation of human skin fibroblasts leads to a heme oxygenase-dependent increase in ferritin. J Biol Chem 268:14678-14681.
51. Werner F, Jain MK, Feinberg MW, Sibinga NES, Pellacani A, Wiesel P, Chin MT, Topper JN, Perrella MA, Lee M-E. 2000. Transforming growth factor-b1 inhibition of macrophage activation is mediated via Smad3. J Biol Chem 275:36653-36658.
52. Wiesel P, Foster LC, Pellacani A, Layne MD, Hsieh C-M, Huggins GS, Strauss P, Yet S-F, Perrella MA. 2000a. Thioredoxin facilitates the induction of heme oxygenase-1 in response to inflammatory mediators. J Biol Chem 275:24840-24846.
53. Wiesel P, Patel AP, DiFonzo N, Marria PB, Sim CU, Pellacani A, Maemura K, LeBlanc BW, Marino K, Doerschuk CM, Yet S-F, Lee M-E, Perrella MA. 2000b. Endotoxin-induced mortality is related to increased oxidative stress and end-organ dysfunction, not refractory hypotension, in heme oxygenase-1 deficient mice. Circulation 102:3015-3022.
54. Yang X, Letterio JJ, Lechleider RJ, Chen L, Hayman R, Gu H, Roberts AB, Deng C. 1999. Targeted disruption of SMAD3 results in impaired mucosal immunity and diminished T cell responsiveness to TGF-beta. EMBO J 18:1280-1291.
55. Yet S-F, Pellacani A, Patterson C, Tan L, Folta SC, Foster L, Lee W-S, Hsieh C-M, Perrella MA. 1997. Induction of heme oxygenase-1 expression in vascular smooth muscle cells. A link to endotoxic shock. J Biol Chem 272:4295-4301.
56. Yoshimura A, Wakabayashi Y, Mori T. 2010. Cellular and molecular basis for the regulation of inflammation by TGF-b. J Biochem 147:781-792.
57. Zhang L, Eddy A, Teng YT, Fritzler M, Kluppel M, Melet F, Bernstein A. 1995. An immunological renal disease in transgenic mice that overexpress Fli-1, a member of the Ets family of transcription factor genes. Mol Cell Biol 15:6961-6970.