Dendritic cell function in transplantation arteriosclerosis is regulated by heme oxygenase 1

Circulation Research

Volumn 106, Issue 10, 2010, Pages 1656-1666

  Cheng, Caroline ^a   Noorderloos, M ^a   Van Deel, Elza D ^b   Tempel, Dennie ^a   Den Dekker, Wijnand ^a   Wagtmans, Kim ^a   Duncker, Dirk J ^b   Soares, Miguel P ^c,d   Laman, Jon D ^a   Duckers, Henricus J ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b Thoraxcenter ^*  (Russian Federation)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

CD4; Dendritic cells; Heme oxygenase 1; T cell response; Transplantation arteriosclerosis

Indexed keywords

HEME OXYGENASE 1; IMMUNOGLOBULIN G; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; SMALL INTERFERING RNA;

ALLOGRAFT; ALLOIMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTERIOSCLEROSIS; ARTERY INTIMA PROLIFERATION; ARTICLE; ATHEROGENESIS; CD4+ T LYMPHOCYTE; CELL FUNCTION; CHRONIC DISEASE; CONTROLLED STUDY; DENDRITIC CELL; GENE ACTIVITY; GENE LOSS; GENE SILENCING; GRAFT DYSFUNCTION; IMMUNOGLOBULIN DEPOSITION; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION REGULATION; TRANSPLANTATION ARTERIOSCLEROSIS; UPREGULATION; VASCULAR DISEASE;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CROSSES, GENETIC; DENDRITIC CELLS; GENE SILENCING; HEME OXYGENASE-1; HUMANS; IMMUNOGLOBULIN G; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CULTURE TEST, MIXED; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RATS; RNA, SMALL INTERFERING; TRANSPLANTATION, HOMOLOGOUS;

EID: 77953027742     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.110.216945     Document Type: Article

References (29)

1. Land WG. Innate immunity-mediated allograft rejection and strategies to prevent it. Transplant Proc. 2007;39:667-672.
2. Kunter U, Floege J, von Jurgensonn AS, Stojanovic T, Merkel S, Grone HJ, Ferran C. Expression of A20 in the vessel wall of rat-kidney allografts correlates with protection from transplant arteriosclerosis. Transplantation. 2003;75:3-9.
3. Akyurek LM, Fellstrom BC, Yan ZQ, Hansson GK, Funa K, Larsson E. Inducible and endothelial nitric oxide synthase expression during development of transplant arteriosclerosis in rat aortic grafts. Am J Pathol. 1996;149:1981-1990.
4. Chen S, Kapturczak MH, Wasserfall C, Glushakova OY, Campbell-Thompson M, Deshane JS, Joseph R, Cruz PE, Hauswirth WW, Madsen KM, Croker BP, Berns KI, Atkinson MA, Flotte TR, Tisher CC, Agarwal A. Interleukin 10 attenuates neointimal proliferation and inflammation in aortic allografts by a heme oxygenase-dependent pathway. Proc Natl Acad Sci USA. 2005;102:7251-7256.
5. Otterbein LE, Soares MP, Yamashita K, Bach FH. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol. 2003;24: 449-455.
6. Orozco LD, Kapturczak MH, Barajas B, Wang X, Weinstein MM, Wong J, Deshane J, Bolisetty S, Shaposhnik Z, Shih DM, Agarwal A, Lusis AJ, Araujo JA. Heme oxygenase-1 expression in macrophages plays a beneficial role in atherosclerosis. Circ Res. 2007;100:1703-1711.
7. Yet SF, Perrella MA, Layne MD, Hsieh CM, Maemura K, Kobzik L, Wiesel P, Christou H, Kourembanas S, Lee ME. Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. J Clin Invest. 1999;103:R23-R29.
8. Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, Romani N, Schuler G. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods. 1999;223:77-92.
9. Dietrich H, Hu Y, Zou Y, Dirnhofer S, Kleindienst R, Wick G, Xu Q. Mouse model of transplant arteriosclerosis: role of intercellular adhesion molecule-1. Arterioscler Thromb Vasc Biol. 2000;20:343-352.
10. Chang CH, Guerder S, Hong SC, van Ewijk W, Flavell RA. Mice lacking the MHC class II transactivator (CIITA) show tissue-specific impairment of MHC class II expression. Immunity. 1996;4:167-178.
11. Cheng C, Noordeloos AM, Jeney V, Soares MP, Moll F, Pasterkamp G, Serruys PW, Duckers HJ. Heme oxygenase 1 determines atherosclerotic lesion progression into a vulnerable plaque. Circulation. 2009;119: 3017-3027.
12. Johnson DE, Alderman EL, Schroeder JS, Gao SZ, Hunt S, DeCampli WM, Stinson E, Billingham M. Transplant coronary artery disease: his-topathologic correlations with angiographic morphology. J Am Coll Cardiol. 1991;17:449-457.
13. Gao SZ, Alderman EL, Schroeder JS, Silverman JF, Hunt SA. Accelerated coronary vascular disease in the heart transplant patient: coronary arteriographic findings. J Am Coll Cardiol. 1988;12:334-340.
14. Olivari MT, Homans DC, Wilson RF, Kubo SH, Ring WS. Coronary artery disease in cardiac transplant patients receiving triple-drug immu-nosuppressive therapy. Circulation. 1989;80(5 Pt 2):III-111-III-115.
15. Kolb F, Heudes D, Mandet C, Plissonnier D, Osborne-Pellegrin M, Bariety J, Michel JB. Presensitization accelerates allograft arteriosclerosis. Transplantation. 1996;62:1401-1410.
16. Lechler RI, Batchelor JR. Restoration of immunogenicity to passenger cell-depleted kidney allografts by the addition of donor strain dendritic cells. J Exp Med. 1982;155:31-41.
17. Hackstein H, Steinschulte C, Fiedel S, Eisele A, Rathke V, Stadlbauer T, Taner T, Thomson AW, Tillmanns H, Bein G, Holschermann H. San-glifehrin a blocks key dendritic cell functions in vivo and promotes long-term allograft survival together with low-dose CsA. Am J Transplant. 2007;7:789-798.
18. Isik FF, McDonald TO, Ferguson M, Yamanaka E, Gordon D. Transplant arteriosclerosis in a rat aortic model. Am J Pathol. 1992;141:1139-1149.
19. Thaunat O, Louedec L, Dai J, Bellier F, Groyer E, Delignat S, Gaston AT, Caligiuri G, Joly E, Plissonnier D, Michel JB, Nicoletti A. Direct and indirect effects of alloantibodies link neointimal and medial remodeling in graft arteriosclerosis. Arterioscler Thromb Vasc Biol. 2006;26: 2359-2365.
20. Chauveau C, Remy S, Royer PJ, Hill M, Tanguy-Royer S, Hubert FX, Tesson L, Brion R, Beriou G, Gregoire M, Josien R, Cuturi MC, Anegon I. Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood. 2005; 106:1694-1702.
21. Mashreghi MF, Klemz R, Knosalla IS, Gerstmayer B, Janssen U, Buelow R, Jozkowicz A, Dulak J, Volk HD, Kotsch K. Inhibition of dendritic cell maturation and function is independent of heme oxygenase 1 but requires the activation of STAT3. J Immunol. 2008;180:7919-7930.
22. Chora AA, Fontoura P, Cunha A, Pais TF, Cardoso S, Ho PP, Lee LY, Sobel RA, Steinman L, Soares MP. Heme oxygenase-1 and carbon monoxide suppress autoimmune neuroinflammation. J Clin Invest. 2007; 117:438-447.
23. Kotsch K, Martins PN, Klemz R, Janssen U, Gerstmayer B, Dernier A, Reutzel-Selke A, Kuckelkorn U, Tullius SG, Volk HD. Heme oxygen-ase-1 ameliorates ischemia/reperfusion injury by targeting dendritic cell maturation and migration. Antioxid Redox Signal. 2007;9:2049-2063.
24. Poss KD, Tonegawa S. Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci USA. 1997;94:10919-10924.
25. Schaer CA, Schoedon G, Imhof A, Kurrer MO, Schaer DJ. Constitutive endocytosis of CD163 mediates hemoglobin-heme uptake and determines the noninflammatory and protective transcriptional response of macro-phages to hemoglobin. Circ Res. 2006;99:943-950.
26. Feng Y, Jacobs F, Van Craeyveld E, Brunaud C, Snoeys J, Tjwa M, Van Linthout S, De Geest B. Human ApoA-I transfer attenuates transplant arteriosclerosis via enhanced incorporation of bone marrow-derived en-dothelial progenitor cells. Arterioscler Thromb Vasc Biol. 2008;28: 278-283.
27. Otterbein LE, Zuckerbraun BS, Haga M, Liu F, Song R, Usheva A, Stachulak C, Bodyak N, Smith RN, Csizmadia E, Tyagi S, Akamatsu Y, Flavell RJ, Billiar TR, Tzeng E, Bach FH, Choi AM, Soares MP. Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury. Nat Med. 2003;9:183-190.
28. Hu Y, Davison F, Ludewig B, Erdel M, Mayr M, Url M, Dietrich H, Xu Q. Smooth muscle cells in transplant atherosclerotic lesions are originated from recipients, but not bone marrow progenitor cells. Circulation. 2002; 106:1834-1839.
29. Remy S, Blancou P, Tesson L, Tardif V, Brion R, Royer PJ, Motterlini R, Foresti R, Painchaut M, Pogu S, Gregoire M, Bach JM, Anegon I, Chauveau C. Carbon monoxide inhibits TLR-induced dendritic cell immunogenicity. J Immunol. 2009;182:1877-1884.