Hepcidin-ferroportin axis controls toll-like receptor 4 dependent macrophage inflammatory responses in human atherosclerotic plaques

Atherosclerosis

Volumn 241, Issue 2, 2015, Pages 692-700

  Habib, Anwer ^a   Polavarapu, Rohini ^a   Karmali, Vinit ^a   Guo, Liang ^b   Van Dam, Richard ^a   Cheng, Qi ^b   Akahori, Hirokuni ^a   Saeed, Omar ^a   Nakano, Masataka ^b   Pachura, Kimberly ^a   Hong, Charles C ^c   Shin, Eric ^a   Kolodgie, Frank ^b   Virmani, Renu ^b   Finn, Aloke V ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CVPATH INSTITUTE   (United States)

^c VANDERBILT UNIVERSITY   (United States)

Author keywords

Atherosclerosis; Inflammation; Macrophage

Indexed keywords

BETA INTERFERON; CD163 ANTIGEN; CD31 ANTIGEN; CD34 ANTIGEN; CD68 ANTIGEN; FERROPORTIN 1; HAPTOGLOBIN; HEMOGLOBIN; HEPCIDIN; MYELOID DIFFERENTIATION FACTOR 88; OXIDIZED LOW DENSITY LIPOPROTEIN; STAT3 PROTEIN; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TUMOR NECROSIS FACTOR ALPHA; CATION TRANSPORT PROTEIN; CELL SURFACE RECEPTOR; DIFFERENTIATION ANTIGEN; IRON; LEUKOCYTE ANTIGEN; LIPOPOLYSACCHARIDE; LOW DENSITY LIPOPROTEIN; METAL TRANSPORTING PROTEIN 1; MYD88 PROTEIN, HUMAN; TLR4 PROTEIN, HUMAN; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ARTICLE; ATHEROSCLEROTIC PLAQUE; CELL DIFFERENTIATION; CELL MEMBRANE; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; FOAM CELL; GENE REPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; IRON METABOLISM; LIPID RAFT; MALE; MONOCYTE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CHEMISTRY; CYTOLOGY; GENETICS; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM;

ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; CATION TRANSPORT PROTEINS; FOAM CELLS; HAPTOGLOBINS; HEMOGLOBINS; HEPCIDINS; HUMANS; INFLAMMATION; IRON; LIPOPOLYSACCHARIDES; LIPOPROTEINS, LDL; MACROPHAGES; MACROPHAGES, PERITONEAL; MALE; MEMBRANE MICRODOMAINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; PLAQUE, ATHEROSCLEROTIC; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84934966234     PISSN: 00219150     EISSN: 18791484     Source Type: Journal    
DOI: 10.1016/j.atherosclerosis.2015.06.025     Document Type: Article

References (26)

1. Ross R. Atherosclerosis-an inflammatory disease. N.Engl. J. Med. 1999, 340:115-126.
2. Akira S., Takeda K., Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2001, 2:675-680.
3. Kim F., Pham M., Luttrell I., Bannerman D.D., Tupper J., Thaler J., Hawn T.R., Raines E.W., Schwartz M.W. Toll-like receptor-4 mediates vascular inflammation and insulin resistance in diet-induced obesity. Circ. Res. 2007, 100:1589-1596.
4. Michelsen K.S., Wong M.H., Shah P.K., Zhang W., Yano J., Doherty T.M., Akira S., Rajavashisth T.B., Arditi M. Lack of toll-like receptor 4 or myeloid differentiation factor 88 reduces atherosclerosis and alters plaque phenotype in mice deficient in apolipoprotein e. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:10679-10684.
5. Coenen K.R., Gruen M.L., Lee-Young R.S., Puglisi M.J., Wasserman D.H., Hasty A.H. Impact of macrophage toll-like receptor 4 deficiency on macrophage infiltration into adipose tissue and the artery wall in mice. Diabetologia 2009, 52:318-328.
6. Orr J.S., Puglisi M.J., Ellacott K.L., Lumeng C.N., Wasserman D.H., Hasty A.H. Toll-like receptor 4 deficiency promotes the alternative activation of adipose tissue macrophages. Diabetes 2012, 61:2718-2727.
7. Kiechl S., Lorenz E., Reindl M., Wiedermann C.J., Oberhollenzer F., Bonora E., Willeit J., Schwartz D.A. Toll-like receptor 4 polymorphisms and atherogenesis. N.Engl. J. Med. 2002, 347:185-192.
8. Stewart C.R., Stuart L.M., Wilkinson K., van Gils J.M., Deng J., Halle A., Rayner K.J., Boyer L., Zhong R., Frazier W.A., Lacy-Hulbert A., El Khoury J., Golenbock D.T., Moore K.J. Cd36 ligands promote sterile inflammation through assembly of a toll-like receptor 4 and 6 heterodimer. Nat. Immunol. 2010, 11:155-161.
9. Branen L., Hovgaard L., Nitulescu M., Bengtsson E., Nilsson J., Jovinge S. Inhibition of tumor necrosis factor-alpha reduces atherosclerosis in apolipoprotein e knockout mice. Arterioscler. Thromb. Vasc. Biol. 2004, 24:2137-2142.
10. Goossens P., Gijbels M.J., Zernecke A., Eijgelaar W., Vergouwe M.N., van der Made I., Vanderlocht J., Beckers L., Buurman W.A., Daemen M.J., Kalinke U., Weber C., Lutgens E., de Winther M.P. Myeloid type i interferon signaling promotes atherosclerosis by stimulating macrophage recruitment to lesions. Cell. Metab. 2010, 12:142-153.
11. Finn A.V., Nakano M., Polavarapu R., Karmali V., Saeed O., Zhao X., Yazdani S., Otsuka F., Davis T., Habib A., Narula J., Kolodgie F.D., Virmani R. Hemoglobin directs macrophage differentiation and prevents foam cell formation in human atherosclerotic plaques. J.Am. Coll. Cardiol. 2012, 59(2):166-177.
12. Kramer M.C., Rittersma S.Z., de Winter R.J., Ladich E.R., Fowler D.R., Liang Y.H., Kutys R., Carter-Monroe N., Kolodgie F.D., van der Wal A.C., Virmani R. Relationship of thrombus healing to underlying plaque morphology in sudden coronary death. J.Am. Coll. Cardiol. 2010, 55:122-132.
13. Virmani R., Kolodgie F.D., Burke A.P., Farb A., Schwartz S.M. Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler. Thromb. Vasc. Biol. 2000, 20:1262-1275.
14. Yu P.B., Deng D.Y., Lai C.S., Hong C.C., Cuny G.D., Bouxsein M.L., Hong D.W., McManus P.M., Katagiri T., Sachidanandan C., Kamiya N., Fukuda T., Mishina Y., Peterson R.T., Bloch K.D. Bmp type i receptor inhibition reduces heterotopic [corrected] ossification. Nat. Med. 2008, 14:1363-1369.
15. Saeed O., Otsuka F., Polavarapu R., Karmali V., Weiss D., Davis T., Rostad B., Pachura K., Adams L., Elliott J., Taylor W.R., Narula J., Kolodgie F., Virmani R., Hong C.C., Finn A.V. Pharmacological suppression of hepcidin increases macrophage cholesterol efflux and reduces foam cell formation and atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2012, 32(2):299-307.
16. Donovan A., Lima C.A., Pinkus J.L., Pinkus G.S., Zon L.I., Robine S., Andrews N.C. The iron exporter ferroportin/slc40a1 is essential for iron homeostasis. Cell. Metab. 2005, 1:191-200.
17. Wang L., Harrington L., Trebicka E., Shi H.N., Kagan J.C., Hong C.C., Lin H.Y., Babitt J.L., Cherayil B.J. Selective modulation of tlr4-activated inflammatory responses by altered iron homeostasis in mice. J.Clin. Invest 2009, 119:3322-3328.
18. Nemeth E., Tuttle M.S., Powelson J., Vaughn M.B., Donovan A., Ward D.M., Ganz T., Kaplan J. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 2004, 306:2090-2093.
19. De Domenico I., Zhang T.Y., Koening C.L., Branch R.W., London N., Lo E., Daynes R.A., Kushner J.P., Li D., Ward D.M., Kaplan J. Hepcidin mediates transcriptional changes that modulate acute cytokine-induced inflammatory responses in mice. J.Clin. Invest 2010, 120:2395-2405.
20. Nakahira K., Kim H.P., Geng X.H., Nakao A., Wang X., Murase N., Drain P.F., Sasidhar M., Nabel E.G., Takahashi T., Lukacs N.W., Ryter S.W., Morita K., Choi A.M. Carbon monoxide differentially inhibits tlr signaling pathways by regulating ros-induced trafficking of tlrs to lipid rafts. J.Exp. Med. 2006, 203:2377-2389.
21. Brown D.A., London E. Functions of lipid rafts in biological membranes. Annu Rev. Cell. Dev. Biol. 1998, 14:111-136.
22. Bi K., Tanaka Y., Coudronniere N., Sugie K., Hong S., van Stipdonk M.J., Altman A. Antigen-induced translocation of pkc-theta to membrane rafts is required for t cell activation. Nat. Immunol. 2001, 2:556-563.
23. Rivera S., Nemeth E., Gabayan V., Lopez M.A., Farshidi D., Ganz T. Synthetic hepcidin causes rapid dose-dependent hypoferremia and is concentrated in ferroportin-containing organs. Blood 2005, 106:2196-2199.
24. Wilson H.M. Macrophages heterogeneity in atherosclerosis - implications for therapy. J.Cell. Mol. Med. 2010, 14:2055-2065.
25. Komohara Y., Hirahara J., Horikawa T., Kawamura K., Kiyota E., Sakashita N., Araki N., Takeya M. Am-3k, an anti-macrophage antibody, recognizes cd163, a molecule associated with an anti-inflammatory macrophage phenotype. J.Histochem Cytochem 2006, 54:763-771.
26. Murray P.J. Understanding and exploiting the endogenous interleukin-10/stat3-mediated anti-inflammatory response. Curr. Opin. Pharmacol. 2006, 6:379-386.