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Erschienen in: Inflammation 5/2014

01.10.2014

Therapeutic Potential of HO-1 in Autoimmune Diseases

verfasst von: Bao-Zhu Li, Biao Guo, Hai-Yan Zhang, Juan Liu, Sha-Sha Tao, Hai-Feng Pan, Dong-Qing Ye

Erschienen in: Inflammation | Ausgabe 5/2014

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Abstract

Heme oxygenase-1 (HO-1), the inducible isoform of heme oxygenase (HO), has raised a lot of concerns in recent years due to its multiple functions. HO-1 was found to be a pivotal cytoprotective, antioxidant, anti-apoptotic, immunosuppressive, as well as anti-inflammatory molecule. Recent studies have clarified its significant functions in many diseases with substantial findings. In autoimmune diseases, HO-1 may have promising therapeutic potential. Here, we briefly reviewed recent advances in this field, aiming at hopefully exploring the potential therapeutic roles of HO-1, and design HO-1-based strategies for the treatment of autoimmune diseases.
Literatur
1.
Zurück zum Zitat Kapturczak, M.H., C. Wasserfall, T. Brusko, et al. 2004. Heme oxygenase-1 modulates early inflammatory responses: Evidence from the heme oxygenase-1-deficient mouse. The American Journal of Pathology 165: 1045–1053.PubMedCrossRefPubMedCentral Kapturczak, M.H., C. Wasserfall, T. Brusko, et al. 2004. Heme oxygenase-1 modulates early inflammatory responses: Evidence from the heme oxygenase-1-deficient mouse. The American Journal of Pathology 165: 1045–1053.PubMedCrossRefPubMedCentral
2.
Zurück zum Zitat Tenhunen, R., H.S. Marver, and R. Schmid. 1968. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proceedings of the National Academy of Sciences of the United States of America 61: 748–755.PubMedCrossRefPubMedCentral Tenhunen, R., H.S. Marver, and R. Schmid. 1968. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proceedings of the National Academy of Sciences of the United States of America 61: 748–755.PubMedCrossRefPubMedCentral
3.
Zurück zum Zitat Durante, W. 2011. Protective role of heme oxygenase-1 against inflammation in atherosclerosis. Frontiers in Bioscience (Landmark Ed) 16: 2372–2388.CrossRef Durante, W. 2011. Protective role of heme oxygenase-1 against inflammation in atherosclerosis. Frontiers in Bioscience (Landmark Ed) 16: 2372–2388.CrossRef
4.
Zurück zum Zitat Kobayashi, H., M. Takeno, T. Saito, et al. 2006. Regulatory role of heme oxygenase 1 in inflammation of rheumatoid arthritis. Arthritis and Rheumatism 54: 1132–1142.PubMedCrossRef Kobayashi, H., M. Takeno, T. Saito, et al. 2006. Regulatory role of heme oxygenase 1 in inflammation of rheumatoid arthritis. Arthritis and Rheumatism 54: 1132–1142.PubMedCrossRef
5.
Zurück zum Zitat Minamino, T., H. Christou, C.M. Hsieh, et al. 2001. Targeted expression of heme oxygenase-1 prevents the pulmonary inflammatory and vascular responses to hypoxia. Proceedings of the National Academy of Sciences of the United States of America 98: 8798–8803.PubMedCrossRefPubMedCentral Minamino, T., H. Christou, C.M. Hsieh, et al. 2001. Targeted expression of heme oxygenase-1 prevents the pulmonary inflammatory and vascular responses to hypoxia. Proceedings of the National Academy of Sciences of the United States of America 98: 8798–8803.PubMedCrossRefPubMedCentral
6.
Zurück zum Zitat Haines, D.D., I. Lekli, P. Teissier, I. Bak, and A. Tosaki. 2012. Role of haeme oxygenase-1 in resolution of oxidative stress-related pathologies: Focus on cardiovascular, lung, neurological and kidney disorders. Acta Physiologica (Oxford, England) 204: 487–501.CrossRef Haines, D.D., I. Lekli, P. Teissier, I. Bak, and A. Tosaki. 2012. Role of haeme oxygenase-1 in resolution of oxidative stress-related pathologies: Focus on cardiovascular, lung, neurological and kidney disorders. Acta Physiologica (Oxford, England) 204: 487–501.CrossRef
7.
Zurück zum Zitat Blancou, P., V. Tardif, T. Simon, et al. 2011. Immunoregulatory properties of heme oxygenase-1. Methods in Molecular Biology 677: 247–268.PubMedCrossRef Blancou, P., V. Tardif, T. Simon, et al. 2011. Immunoregulatory properties of heme oxygenase-1. Methods in Molecular Biology 677: 247–268.PubMedCrossRef
8.
Zurück zum Zitat Fagone, P., F. Patti, K. Mangano, et al. 2013. Heme oxygenase-1 expression in peripheral blood mononuclear cells correlates with disease activity in multiple sclerosis. Journal of Neuroimmunology 261: 82–86.PubMedCrossRef Fagone, P., F. Patti, K. Mangano, et al. 2013. Heme oxygenase-1 expression in peripheral blood mononuclear cells correlates with disease activity in multiple sclerosis. Journal of Neuroimmunology 261: 82–86.PubMedCrossRef
9.
Zurück zum Zitat Simon, T., I. Anegon, and P. Blancou. 2011. Heme oxygenase and carbon monoxide as an immunotherapeutic approach in transplantation and cancer. Immunotherapy 3: 15–18.PubMedCrossRef Simon, T., I. Anegon, and P. Blancou. 2011. Heme oxygenase and carbon monoxide as an immunotherapeutic approach in transplantation and cancer. Immunotherapy 3: 15–18.PubMedCrossRef
10.
Zurück zum Zitat Poss, K.D., and S. Tonegawa. 1997. Heme oxygenase 1 is required for mammalian iron reutilization. Proceedings of the National Academy of Sciences of the United States of America 94: 10919–10924.PubMedCrossRefPubMedCentral Poss, K.D., and S. Tonegawa. 1997. Heme oxygenase 1 is required for mammalian iron reutilization. Proceedings of the National Academy of Sciences of the United States of America 94: 10919–10924.PubMedCrossRefPubMedCentral
11.
Zurück zum Zitat Yachie, A., Y. Niida, T. Wada, et al. 1999. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. The Journal of Clinical Investigation 103: 129–135.PubMedCrossRefPubMedCentral Yachie, A., Y. Niida, T. Wada, et al. 1999. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. The Journal of Clinical Investigation 103: 129–135.PubMedCrossRefPubMedCentral
12.
Zurück zum Zitat Pae, H.O., G.S. Oh, B.M. Choi, et al. 2004. Carbon monoxide produced by heme oxygenase-1 suppresses T cell proliferation via inhibition of IL-2 production. Journal of Immunology 172: 4744–4751.CrossRef Pae, H.O., G.S. Oh, B.M. Choi, et al. 2004. Carbon monoxide produced by heme oxygenase-1 suppresses T cell proliferation via inhibition of IL-2 production. Journal of Immunology 172: 4744–4751.CrossRef
13.
Zurück zum Zitat Burt, T.D., L. Seu, J.E. Mold, A. Kappas, and J.M. McCune. 2010. Naive human T cells are activated and proliferate in response to the heme oxygenase-1 inhibitor tin mesoporphyrin. Journal of Immunology 185: 5279–5288.CrossRef Burt, T.D., L. Seu, J.E. Mold, A. Kappas, and J.M. McCune. 2010. Naive human T cells are activated and proliferate in response to the heme oxygenase-1 inhibitor tin mesoporphyrin. Journal of Immunology 185: 5279–5288.CrossRef
14.
Zurück zum Zitat Hu, C.M., H.H. Lin, M.T. Chiang, P.F. Chang, and L.Y. Chau. 2007. Systemic expression of heme oxygenase-1 ameliorates type 1 diabetes in NOD mice. Diabetes 56: 1240–1247.PubMedCrossRef Hu, C.M., H.H. Lin, M.T. Chiang, P.F. Chang, and L.Y. Chau. 2007. Systemic expression of heme oxygenase-1 ameliorates type 1 diabetes in NOD mice. Diabetes 56: 1240–1247.PubMedCrossRef
15.
Zurück zum Zitat Xia, Z.W., W.W. Zhong, L.Q. Xu, et al. 2006. Heme oxygenase-1-mediated CD4+CD25high regulatory T cells suppress allergic airway inflammation. Journal of Immunology 177: 5936–5945.CrossRef Xia, Z.W., W.W. Zhong, L.Q. Xu, et al. 2006. Heme oxygenase-1-mediated CD4+CD25high regulatory T cells suppress allergic airway inflammation. Journal of Immunology 177: 5936–5945.CrossRef
16.
Zurück zum Zitat Gu, Q., Q. Wu, M. Jin, et al. 2012. Heme oxygenase-1 alleviates mouse hepatic failure through suppression of adaptive immune responses. The Journal of Pharmacology and Experimental Therapeutics 340: 2–10.PubMedCrossRef Gu, Q., Q. Wu, M. Jin, et al. 2012. Heme oxygenase-1 alleviates mouse hepatic failure through suppression of adaptive immune responses. The Journal of Pharmacology and Experimental Therapeutics 340: 2–10.PubMedCrossRef
17.
Zurück zum Zitat Chauveau, C., S. Remy, P.J. Royer, et al. 2005. Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood 106: 1694–1702.PubMedCrossRef Chauveau, C., S. Remy, P.J. Royer, et al. 2005. Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood 106: 1694–1702.PubMedCrossRef
18.
Zurück zum Zitat Remy, S., P. Blancou, L. Tesson, et al. 2009. Carbon monoxide inhibits TLR-induced dendritic cell immunogenicity. Journal of Immunology 182: 1877–1884.CrossRef Remy, S., P. Blancou, L. Tesson, et al. 2009. Carbon monoxide inhibits TLR-induced dendritic cell immunogenicity. Journal of Immunology 182: 1877–1884.CrossRef
19.
Zurück zum Zitat George, J.F., A. Braun, T.M. Brusko, et al. 2008. Suppression by CD4+ CD25+ regulatory T cells is dependent on expression of heme oxygenase-1 in antigen-presenting cells. The American Journal of Pathology 173: 154–160.PubMedCrossRefPubMedCentral George, J.F., A. Braun, T.M. Brusko, et al. 2008. Suppression by CD4+ CD25+ regulatory T cells is dependent on expression of heme oxygenase-1 in antigen-presenting cells. The American Journal of Pathology 173: 154–160.PubMedCrossRefPubMedCentral
20.
Zurück zum Zitat Park, D.J., A. Agarwal, and J.F. George. 2010. Heme oxygenase-1 expression in murine dendritic cell subpopulations: Effect on CD8+ dendritic cell differentiation in vivo. The American Journal of Pathology 176: 2831–2839.PubMedCrossRefPubMedCentral Park, D.J., A. Agarwal, and J.F. George. 2010. Heme oxygenase-1 expression in murine dendritic cell subpopulations: Effect on CD8+ dendritic cell differentiation in vivo. The American Journal of Pathology 176: 2831–2839.PubMedCrossRefPubMedCentral
21.
Zurück zum Zitat Tardif, V., S.A. Riquelme, S. Remy, et al. 2013. Carbon monoxide decreases endosome-lysosome fusion and inhibits soluble antigen presentation by dendritic cells to T cells. European Journal of Immunology 43(11): 2832–2844.PubMedCrossRef Tardif, V., S.A. Riquelme, S. Remy, et al. 2013. Carbon monoxide decreases endosome-lysosome fusion and inhibits soluble antigen presentation by dendritic cells to T cells. European Journal of Immunology 43(11): 2832–2844.PubMedCrossRef
22.
Zurück zum Zitat Chora, A.A., P. Fontoura, A. Cunha, et al. 2007. Heme oxygenase-1 and carbon monoxide suppress autoimmune neuroinflammation. The Journal of Clinical Investigation 117: 438–447.PubMedCrossRefPubMedCentral Chora, A.A., P. Fontoura, A. Cunha, et al. 2007. Heme oxygenase-1 and carbon monoxide suppress autoimmune neuroinflammation. The Journal of Clinical Investigation 117: 438–447.PubMedCrossRefPubMedCentral
23.
Zurück zum Zitat Xia, Z.W., W.W. Zhong, J.S. Meyrowitz, and Z.L. Zhang. 2008. The role of heme oxygenase-1 in T cell-mediated immunity: The all encompassing enzyme. Current Pharmaceutical Design 14: 454–464.PubMedCrossRef Xia, Z.W., W.W. Zhong, J.S. Meyrowitz, and Z.L. Zhang. 2008. The role of heme oxygenase-1 in T cell-mediated immunity: The all encompassing enzyme. Current Pharmaceutical Design 14: 454–464.PubMedCrossRef
24.
Zurück zum Zitat Weaver, C.T., L.E. Harrington, P.R. Mangan, M. Gavrieli, and K.M. Murphy. 2006. Th17: An effector CD4 T cell lineage with regulatory T cell ties. Immunity 24: 677–688.PubMedCrossRef Weaver, C.T., L.E. Harrington, P.R. Mangan, M. Gavrieli, and K.M. Murphy. 2006. Th17: An effector CD4 T cell lineage with regulatory T cell ties. Immunity 24: 677–688.PubMedCrossRef
25.
Zurück zum Zitat Deenick, E.K., and S.G. Tangye. 2007. Autoimmunity: IL-21: A new player in Th17-cell differentiation. Immunology and Cell Biology 85: 503–505.PubMedCrossRef Deenick, E.K., and S.G. Tangye. 2007. Autoimmunity: IL-21: A new player in Th17-cell differentiation. Immunology and Cell Biology 85: 503–505.PubMedCrossRef
26.
Zurück zum Zitat Bettelli, E., Y. Carrier, W. Gao, et al. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235–238.PubMedCrossRef Bettelli, E., Y. Carrier, W. Gao, et al. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235–238.PubMedCrossRef
27.
Zurück zum Zitat Zhang, Y., L. Zhang, J. Wu, C. Di, and Z. Xia. 2013. Heme oxygenase-1 exerts a protective role in ovalbumin-induced neutrophilic airway inflammation by inhibiting response in the immune cells Th17. The Journal of Biological Chemistry 288(48): 34612–34626.PubMedCrossRef Zhang, Y., L. Zhang, J. Wu, C. Di, and Z. Xia. 2013. Heme oxygenase-1 exerts a protective role in ovalbumin-induced neutrophilic airway inflammation by inhibiting response in the immune cells Th17. The Journal of Biological Chemistry 288(48): 34612–34626.PubMedCrossRef
28.
Zurück zum Zitat Otterbein, L.E., M.P. Soares, K. Yamashita, and F.H. Bach. 2003. Heme oxygenase-1: Unleashing the protective properties of heme. Trends in Immunology 24: 449–455.PubMedCrossRef Otterbein, L.E., M.P. Soares, K. Yamashita, and F.H. Bach. 2003. Heme oxygenase-1: Unleashing the protective properties of heme. Trends in Immunology 24: 449–455.PubMedCrossRef
29.
Zurück zum Zitat Lee, T.S., and L.Y. Chau. 2002. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nature Medicine 8: 240–246.PubMedCrossRef Lee, T.S., and L.Y. Chau. 2002. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nature Medicine 8: 240–246.PubMedCrossRef
30.
Zurück zum Zitat Mackern-Oberti, J.P., C. Llanos, L.J. Carreno, et al. 2013. Carbon monoxide exposure improves immune function in lupus-prone mice. Immunology 140: 123–132.PubMedCrossRefPubMedCentral Mackern-Oberti, J.P., C. Llanos, L.J. Carreno, et al. 2013. Carbon monoxide exposure improves immune function in lupus-prone mice. Immunology 140: 123–132.PubMedCrossRefPubMedCentral
31.
Zurück zum Zitat Otterbein, L.E., F.H. Bach, J. Alam, et al. 2000. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nature Medicine 6: 422–428.PubMedCrossRef Otterbein, L.E., F.H. Bach, J. Alam, et al. 2000. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nature Medicine 6: 422–428.PubMedCrossRef
32.
Zurück zum Zitat Bilban, M., F.H. Bach, S.L. Otterbein, et al. 2006. Carbon monoxide orchestrates a protective response through PPARgamma. Immunity 24: 601–610.PubMedCrossRef Bilban, M., F.H. Bach, S.L. Otterbein, et al. 2006. Carbon monoxide orchestrates a protective response through PPARgamma. Immunity 24: 601–610.PubMedCrossRef
33.
Zurück zum Zitat Woo, C.H., M.P. Massett, T. Shishido, et al. 2006. ERK5 activation inhibits inflammatory responses via peroxisome proliferator-activated receptor delta (PPARdelta) stimulation. The Journal of Biological Chemistry 281: 32164–32174.PubMedCrossRef Woo, C.H., M.P. Massett, T. Shishido, et al. 2006. ERK5 activation inhibits inflammatory responses via peroxisome proliferator-activated receptor delta (PPARdelta) stimulation. The Journal of Biological Chemistry 281: 32164–32174.PubMedCrossRef
34.
Zurück zum Zitat Nakahira, K., H.P. Kim, X.H. Geng, et al. 2006. Carbon monoxide differentially inhibits TLR signaling pathways by regulating ROS-induced trafficking of TLRs to lipid rafts. The Journal of Experimental Medicine 203: 2377–2389.PubMedCrossRefPubMedCentral Nakahira, K., H.P. Kim, X.H. Geng, et al. 2006. Carbon monoxide differentially inhibits TLR signaling pathways by regulating ROS-induced trafficking of TLRs to lipid rafts. The Journal of Experimental Medicine 203: 2377–2389.PubMedCrossRefPubMedCentral
35.
Zurück zum Zitat Wang, X.M., H.P. Kim, K. Nakahira, S.W. Ryter, and A.M. Choi. 2009. The heme oxygenase-1/carbon monoxide pathway suppresses TLR4 signaling by regulating the interaction of TLR4 with caveolin-1. Journal of Immunology 182: 3809–3818.CrossRef Wang, X.M., H.P. Kim, K. Nakahira, S.W. Ryter, and A.M. Choi. 2009. The heme oxygenase-1/carbon monoxide pathway suppresses TLR4 signaling by regulating the interaction of TLR4 with caveolin-1. Journal of Immunology 182: 3809–3818.CrossRef
36.
Zurück zum Zitat Chin, B.Y., G. Jiang, B. Wegiel, et al. 2007. Hypoxia-inducible factor 1alpha stabilization by carbon monoxide results in cytoprotective preconditioning. Proceedings of the National Academy of Sciences of the United States of America 104: 5109–5114.PubMedCrossRefPubMedCentral Chin, B.Y., G. Jiang, B. Wegiel, et al. 2007. Hypoxia-inducible factor 1alpha stabilization by carbon monoxide results in cytoprotective preconditioning. Proceedings of the National Academy of Sciences of the United States of America 104: 5109–5114.PubMedCrossRefPubMedCentral
37.
Zurück zum Zitat Rahman, A., and D.A. Isenberg. 2008. Systemic lupus erythematosus. The New England Journal of Medicine 358: 929–939.PubMedCrossRef Rahman, A., and D.A. Isenberg. 2008. Systemic lupus erythematosus. The New England Journal of Medicine 358: 929–939.PubMedCrossRef
38.
Zurück zum Zitat Herrada, A.A., C. Llanos, J.P. Mackern-Oberti, et al. 2012. Haem oxygenase 1 expression is altered in monocytes from patients with systemic lupus erythematosus. Immunology 136: 414–424.PubMedCrossRefPubMedCentral Herrada, A.A., C. Llanos, J.P. Mackern-Oberti, et al. 2012. Haem oxygenase 1 expression is altered in monocytes from patients with systemic lupus erythematosus. Immunology 136: 414–424.PubMedCrossRefPubMedCentral
39.
Zurück zum Zitat Chung, S.W., X. Liu, A.A. Macias, R.M. Baron, and M.A. Perrella. 2008. Heme oxygenase-1-derived carbon monoxide enhances the host defense response to microbial sepsis in mice. The Journal of Clinical Investigation 118: 239–247.PubMedCrossRefPubMedCentral Chung, S.W., X. Liu, A.A. Macias, R.M. Baron, and M.A. Perrella. 2008. Heme oxygenase-1-derived carbon monoxide enhances the host defense response to microbial sepsis in mice. The Journal of Clinical Investigation 118: 239–247.PubMedCrossRefPubMedCentral
40.
Zurück zum Zitat Avihingsanon, Y., T. Benjachat, A. Tassanarong, P. Sodsai, V. Kittikovit, and N. Hirankarn. 2009. Decreased renal expression of vascular endothelial growth factor in lupus nephritis is associated with worse prognosis. Kidney International 75: 1340–1348.PubMedCrossRef Avihingsanon, Y., T. Benjachat, A. Tassanarong, P. Sodsai, V. Kittikovit, and N. Hirankarn. 2009. Decreased renal expression of vascular endothelial growth factor in lupus nephritis is associated with worse prognosis. Kidney International 75: 1340–1348.PubMedCrossRef
41.
Zurück zum Zitat Takeda, Y., M. Takeno, M. Iwasaki, et al. 2004. Chemical induction of HO-1 suppresses lupus nephritis by reducing local iNOS expression and synthesis of anti-dsDNA antibody. Clinical and Experimental Immunology 138: 237–244.PubMedCrossRefPubMedCentral Takeda, Y., M. Takeno, M. Iwasaki, et al. 2004. Chemical induction of HO-1 suppresses lupus nephritis by reducing local iNOS expression and synthesis of anti-dsDNA antibody. Clinical and Experimental Immunology 138: 237–244.PubMedCrossRefPubMedCentral
42.
Zurück zum Zitat Burmester, G.R., B. Stuhlmuller, G. Keyszer, and R.W. Kinne. 1997. Mononuclear phagocytes and rheumatoid synovitis. Mastermind or workhorse in arthritis? Arthritis and Rheumatism 40: 5–18.PubMedCrossRef Burmester, G.R., B. Stuhlmuller, G. Keyszer, and R.W. Kinne. 1997. Mononuclear phagocytes and rheumatoid synovitis. Mastermind or workhorse in arthritis? Arthritis and Rheumatism 40: 5–18.PubMedCrossRef
43.
Zurück zum Zitat Feldmann, M., F.M. Brennan, and R.N. Maini. 1996. Role of cytokines in rheumatoid arthritis. Annual Review of Immunology 14: 397–440.PubMedCrossRef Feldmann, M., F.M. Brennan, and R.N. Maini. 1996. Role of cytokines in rheumatoid arthritis. Annual Review of Immunology 14: 397–440.PubMedCrossRef
44.
Zurück zum Zitat Choy, E.H., and G.S. Panayi. 2001. Cytokine pathways and joint inflammation in rheumatoid arthritis. The New England Journal of Medicine 344: 907–916.PubMedCrossRef Choy, E.H., and G.S. Panayi. 2001. Cytokine pathways and joint inflammation in rheumatoid arthritis. The New England Journal of Medicine 344: 907–916.PubMedCrossRef
45.
Zurück zum Zitat Devesa, I., M.L. Ferrandiz, M.C. Terencio, L.A. Joosten, W.B. van den Berg, and M.J. Alcaraz. 2005. Influence of heme oxygenase 1 modulation on the progression of murine collagen-induced arthritis. Arthritis and Rheumatism 52: 3230–3238.PubMedCrossRef Devesa, I., M.L. Ferrandiz, M.C. Terencio, L.A. Joosten, W.B. van den Berg, and M.J. Alcaraz. 2005. Influence of heme oxygenase 1 modulation on the progression of murine collagen-induced arthritis. Arthritis and Rheumatism 52: 3230–3238.PubMedCrossRef
46.
Zurück zum Zitat Kirino, Y., M. Takeno, S. Murakami, et al. 2007. Tumor necrosis factor alpha acceleration of inflammatory responses by down-regulating heme oxygenase 1 in human peripheral monocytes. Arthritis and Rheumatism 56: 464–475.PubMedCrossRef Kirino, Y., M. Takeno, S. Murakami, et al. 2007. Tumor necrosis factor alpha acceleration of inflammatory responses by down-regulating heme oxygenase 1 in human peripheral monocytes. Arthritis and Rheumatism 56: 464–475.PubMedCrossRef
47.
Zurück zum Zitat Kitamura, A., K. Nishida, T. Komiyama, et al. 2011. Increased level of heme oxygenase-1 in rheumatoid arthritis synovial fluid. Modern Rheumatology 21: 150–157.PubMedCrossRef Kitamura, A., K. Nishida, T. Komiyama, et al. 2011. Increased level of heme oxygenase-1 in rheumatoid arthritis synovial fluid. Modern Rheumatology 21: 150–157.PubMedCrossRef
48.
Zurück zum Zitat Devesa, I., M.L. Ferrandiz, I. Guillen, J.M. Cerda, and M.J. Alcaraz. 2005. Potential role of heme oxygenase-1 in the progression of rat adjuvant arthritis. Laboratory Investigation 85: 34–44.PubMedCrossRef Devesa, I., M.L. Ferrandiz, I. Guillen, J.M. Cerda, and M.J. Alcaraz. 2005. Potential role of heme oxygenase-1 in the progression of rat adjuvant arthritis. Laboratory Investigation 85: 34–44.PubMedCrossRef
49.
Zurück zum Zitat Benallaoua, M., M. Francois, F. Batteux, et al. 2007. Pharmacologic induction of heme oxygenase 1 reduces acute inflammatory arthritis in mice. Arthritis and Rheumatism 56: 2585–2594.PubMedCrossRef Benallaoua, M., M. Francois, F. Batteux, et al. 2007. Pharmacologic induction of heme oxygenase 1 reduces acute inflammatory arthritis in mice. Arthritis and Rheumatism 56: 2585–2594.PubMedCrossRef
50.
Zurück zum Zitat Chi, P.L., Y.W. Chen, L.D. Hsiao, Y.L. Chen, and C.M. Yang. 2012. Heme oxygenase 1 attenuates interleukin-1beta-induced cytosolic phospholipase A2 expression via a decrease in NADPH oxidase/reactive oxygen species/activator protein 1 activation in rheumatoid arthritis synovial fibroblasts. Arthritis and Rheumatism 64: 2114–2125.PubMedCrossRef Chi, P.L., Y.W. Chen, L.D. Hsiao, Y.L. Chen, and C.M. Yang. 2012. Heme oxygenase 1 attenuates interleukin-1beta-induced cytosolic phospholipase A2 expression via a decrease in NADPH oxidase/reactive oxygen species/activator protein 1 activation in rheumatoid arthritis synovial fibroblasts. Arthritis and Rheumatism 64: 2114–2125.PubMedCrossRef
51.
Zurück zum Zitat Bonelli, M., A. Savitskaya, C.W. Steiner, et al. 2012. Heme oxygenase-1 end-products carbon monoxide and biliverdin ameliorate murine collagen induced arthritis. Clinical and Experimental Rheumatology 30: 73–78.PubMed Bonelli, M., A. Savitskaya, C.W. Steiner, et al. 2012. Heme oxygenase-1 end-products carbon monoxide and biliverdin ameliorate murine collagen induced arthritis. Clinical and Experimental Rheumatology 30: 73–78.PubMed
52.
Zurück zum Zitat Noseworthy, J.H., C. Lucchinetti, M. Rodriguez, and B.G. Weinshenker. 2000. Multiple sclerosis. The New England Journal of Medicine 343: 938–952.PubMedCrossRef Noseworthy, J.H., C. Lucchinetti, M. Rodriguez, and B.G. Weinshenker. 2000. Multiple sclerosis. The New England Journal of Medicine 343: 938–952.PubMedCrossRef
53.
Zurück zum Zitat Le, W.D., W.J. Xie, and S.H. Appel. 1999. Protective role of heme oxygenase-1 in oxidative stress-induced neuronal injury. Journal of Neuroscience Research 56: 652–658.PubMedCrossRef Le, W.D., W.J. Xie, and S.H. Appel. 1999. Protective role of heme oxygenase-1 in oxidative stress-induced neuronal injury. Journal of Neuroscience Research 56: 652–658.PubMedCrossRef
54.
Zurück zum Zitat Schluesener, H.J., and K. Seid. 2000. Heme oxygenase-1 in lesions of rat experimental autoimmune encephalomyelitis and neuritis. Journal of Neuroimmunology 110: 114–120.PubMedCrossRef Schluesener, H.J., and K. Seid. 2000. Heme oxygenase-1 in lesions of rat experimental autoimmune encephalomyelitis and neuritis. Journal of Neuroimmunology 110: 114–120.PubMedCrossRef
55.
Zurück zum Zitat Liu, Y., B. Zhu, L. Luo, P. Li, D.W. Paty, and M.S. Cynader. 2001. Heme oxygenase-1 plays an important protective role in experimental autoimmune encephalomyelitis. Neuroreport 12: 1841–1845.PubMedCrossRef Liu, Y., B. Zhu, L. Luo, P. Li, D.W. Paty, and M.S. Cynader. 2001. Heme oxygenase-1 plays an important protective role in experimental autoimmune encephalomyelitis. Neuroreport 12: 1841–1845.PubMedCrossRef
56.
Zurück zum Zitat Swanborg, R.H. 1995. Experimental autoimmune encephalomyelitis in rodents as a model for human demyelinating disease. Clinical Immunology and Immunopathology 77: 4–13.PubMedCrossRef Swanborg, R.H. 1995. Experimental autoimmune encephalomyelitis in rodents as a model for human demyelinating disease. Clinical Immunology and Immunopathology 77: 4–13.PubMedCrossRef
57.
Zurück zum Zitat Rivers, T.M., and F.F. Schwentker. 1935. Encephalomyelitis accompanied by myelin destruction experimentally produced in monkeys. The Journal of Experimental Medicine 61: 689–702.PubMedCrossRefPubMedCentral Rivers, T.M., and F.F. Schwentker. 1935. Encephalomyelitis accompanied by myelin destruction experimentally produced in monkeys. The Journal of Experimental Medicine 61: 689–702.PubMedCrossRefPubMedCentral
58.
Zurück zum Zitat Chen, S.J., Y.L. Wang, W.T. Lo, et al. 2010. Erythropoietin enhances endogenous haem oxygenase-1 and represses immune responses to ameliorate experimental autoimmune encephalomyelitis. Clinical and Experimental Immunology 162: 210–223.PubMedCrossRefPubMedCentral Chen, S.J., Y.L. Wang, W.T. Lo, et al. 2010. Erythropoietin enhances endogenous haem oxygenase-1 and represses immune responses to ameliorate experimental autoimmune encephalomyelitis. Clinical and Experimental Immunology 162: 210–223.PubMedCrossRefPubMedCentral
59.
Zurück zum Zitat DeVry, C.G., M. Valdez, L. Gao, et al. 2004. RDP58, a novel immunomodulatory peptide, ameliorates clinical signs of disease in the Lewis rat model of acute experimental autoimmune encephalomyelitis. Journal of Neuroimmunology 152: 33–43.PubMedCrossRef DeVry, C.G., M. Valdez, L. Gao, et al. 2004. RDP58, a novel immunomodulatory peptide, ameliorates clinical signs of disease in the Lewis rat model of acute experimental autoimmune encephalomyelitis. Journal of Neuroimmunology 152: 33–43.PubMedCrossRef
60.
Zurück zum Zitat Tzima, S., P. Victoratos, K. Kranidioti, M. Alexiou, and G. Kollias. 2009. Myeloid heme oxygenase-1 regulates innate immunity and autoimmunity by modulating IFN-beta production. The Journal of Experimental Medicine 206: 1167–1179.PubMedCrossRefPubMedCentral Tzima, S., P. Victoratos, K. Kranidioti, M. Alexiou, and G. Kollias. 2009. Myeloid heme oxygenase-1 regulates innate immunity and autoimmunity by modulating IFN-beta production. The Journal of Experimental Medicine 206: 1167–1179.PubMedCrossRefPubMedCentral
61.
Zurück zum Zitat Chakrabarty, A., M.R. Emerson, and S.M. LeVine. 2003. Heme oxygenase-1 in SJL mice with experimental allergic encephalomyelitis. Multiple Sclerosis 9: 372–381.PubMedCrossRef Chakrabarty, A., M.R. Emerson, and S.M. LeVine. 2003. Heme oxygenase-1 in SJL mice with experimental allergic encephalomyelitis. Multiple Sclerosis 9: 372–381.PubMedCrossRef
62.
63.
Zurück zum Zitat Di Filippo, C., R. Marfella, S. Cuzzocrea, et al. 2005. Hyperglycemia in streptozotocin-induced diabetic rat increases infarct size associated with low levels of myocardial HO-1 during ischemia/reperfusion. Diabetes 54: 803–810.PubMedCrossRef Di Filippo, C., R. Marfella, S. Cuzzocrea, et al. 2005. Hyperglycemia in streptozotocin-induced diabetic rat increases infarct size associated with low levels of myocardial HO-1 during ischemia/reperfusion. Diabetes 54: 803–810.PubMedCrossRef
64.
Zurück zum Zitat Rodella, L., B.D. Lamon, R. Rezzani, et al. 2006. Carbon monoxide and biliverdin prevent endothelial cell sloughing in rats with type I diabetes. Free Radical Biology & Medicine 40: 2198–2205.CrossRef Rodella, L., B.D. Lamon, R. Rezzani, et al. 2006. Carbon monoxide and biliverdin prevent endothelial cell sloughing in rats with type I diabetes. Free Radical Biology & Medicine 40: 2198–2205.CrossRef
65.
Zurück zum Zitat Li, M., S. Peterson, D. Husney, et al. 2007. Long-lasting expression of HO-1 delays progression of type I diabetes in NOD mice. Cell Cycle 6: 567–571.PubMedCrossRef Li, M., S. Peterson, D. Husney, et al. 2007. Long-lasting expression of HO-1 delays progression of type I diabetes in NOD mice. Cell Cycle 6: 567–571.PubMedCrossRef
66.
Zurück zum Zitat Huang, S.H., C.H. Chu, J.C. Yu, et al. 2010. Transgenic expression of haem oxygenase-1 in pancreatic beta cells protects non-obese mice used as a model of diabetes from autoimmune destruction and prolongs graft survival following islet transplantation. Diabetologia 53: 2389–2400.PubMedCrossRef Huang, S.H., C.H. Chu, J.C. Yu, et al. 2010. Transgenic expression of haem oxygenase-1 in pancreatic beta cells protects non-obese mice used as a model of diabetes from autoimmune destruction and prolongs graft survival following islet transplantation. Diabetologia 53: 2389–2400.PubMedCrossRef
67.
Zurück zum Zitat Abdel Aziz, M.T., M.F. El-Asmar, E.G. El Nadi, et al. 2010. The effect of curcumin on insulin release in rat-isolated pancreatic islets. Angiology 61: 557–566.PubMedCrossRef Abdel Aziz, M.T., M.F. El-Asmar, E.G. El Nadi, et al. 2010. The effect of curcumin on insulin release in rat-isolated pancreatic islets. Angiology 61: 557–566.PubMedCrossRef
68.
Zurück zum Zitat Abdel Aziz, M.T., M.F. El-Asmar, I.N. El-Ibrashy, et al. 2012. Effect of novel water soluble curcumin derivative on experimental type- 1 diabetes mellitus (short term study). Diabetology and Metabolic Syndrome 4: 30.PubMedCrossRefPubMedCentral Abdel Aziz, M.T., M.F. El-Asmar, I.N. El-Ibrashy, et al. 2012. Effect of novel water soluble curcumin derivative on experimental type- 1 diabetes mellitus (short term study). Diabetology and Metabolic Syndrome 4: 30.PubMedCrossRefPubMedCentral
69.
Zurück zum Zitat Shibahara, S. 2003. The heme oxygenase dilemma in cellular homeostasis: New insights for the feedback regulation of heme catabolism. The Tohoku Journal of Experimental Medicine 200: 167–186.PubMedCrossRef Shibahara, S. 2003. The heme oxygenase dilemma in cellular homeostasis: New insights for the feedback regulation of heme catabolism. The Tohoku Journal of Experimental Medicine 200: 167–186.PubMedCrossRef
70.
Zurück zum Zitat Wagener, F.A., E.J. Toonen, L. Wigman, et al. 2008. HMOX1 promoter polymorphism modulates the relationship between disease activity and joint damage in rheumatoid arthritis. Arthritis and Rheumatism 58: 3388–3393.PubMedCrossRef Wagener, F.A., E.J. Toonen, L. Wigman, et al. 2008. HMOX1 promoter polymorphism modulates the relationship between disease activity and joint damage in rheumatoid arthritis. Arthritis and Rheumatism 58: 3388–3393.PubMedCrossRef
71.
Zurück zum Zitat Cordova, E.J., A. Martinez-Hernandez, J. Ramirez-Bello, et al. 2012. HMOX1 promoter (GT)n polymorphim is associated with childhood-onset systemic lupus erythematosus but not with juvenile rheumatoid arthritis in a Mexican population. Clinical and Experimental Rheumatology 30: 297–301.PubMed Cordova, E.J., A. Martinez-Hernandez, J. Ramirez-Bello, et al. 2012. HMOX1 promoter (GT)n polymorphim is associated with childhood-onset systemic lupus erythematosus but not with juvenile rheumatoid arthritis in a Mexican population. Clinical and Experimental Rheumatology 30: 297–301.PubMed
72.
Zurück zum Zitat Rueda, B., J. Oliver, G. Robledo, et al. 2007. HO-1 promoter polymorphism associated with rheumatoid arthritis. Arthritis and Rheumatism 56: 3953–3958.PubMedCrossRef Rueda, B., J. Oliver, G. Robledo, et al. 2007. HO-1 promoter polymorphism associated with rheumatoid arthritis. Arthritis and Rheumatism 56: 3953–3958.PubMedCrossRef
Metadaten
Titel
Therapeutic Potential of HO-1 in Autoimmune Diseases
verfasst von
Bao-Zhu Li
Biao Guo
Hai-Yan Zhang
Juan Liu
Sha-Sha Tao
Hai-Feng Pan
Dong-Qing Ye
Publikationsdatum
01.10.2014
Verlag
Springer US
Erschienen in
Inflammation / Ausgabe 5/2014
Print ISSN: 0360-3997
Elektronische ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-014-9908-z

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