Conditional targeting of tumor necrosis factor receptor-associated factor 6 reveals opposing functions of toll-like receptor signaling in endothelial and myeloid cells in a mouse model of atherosclerosis

Circulation

Volumn 126, Issue 14, 2012, Pages 1739-1751

  Polykratis, Apostolos ^a,b,c   Van Loo, Geert ^d   Xanthoulea, Sofia ^a,e   Hellmich, Martin ^a   Pasparakis, Manolis ^a,b,c  

^a UNIVERSITY OF COLOGNE   (Germany)

^b Centre for Molecular Medicine   (United States)

^c UNIVERSITY OF COLOGNE   (Germany)

^d GHENT UNIVERSITY   (Belgium)

^e MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

atherosclerosis; cytokines; endothelium; inflammation; macrophages

Indexed keywords

APOLIPOPROTEIN E; CRE RECOMBINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; OXIDIZED LOW DENSITY LIPOPROTEIN; RECOMBINANT INTERLEUKIN 10; TAMOXIFEN; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; AORTA ATHEROSCLEROSIS; APOPTOSIS; ARTICLE; ATHEROSCLEROTIC PLAQUE; BONE MARROW CELL; CELL ADHESION; CELL PROLIFERATION; CELL SPECIFICITY; CELL SURVIVAL; CONTROLLED STUDY; DISEASE EXACERBATION; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIUM CELL; FEMALE; GENE EXPRESSION; GENE TARGETING; GROWTH INHIBITION; LOXP SITE; MALE; MONOCYTE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; ATHEROSCLEROSIS; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; FEMALE; GENE TARGETING; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID CELLS; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 6; TOLL-LIKE RECEPTORS;

EID: 84866983411     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.112.100339     Document Type: Article

References (37)

1. Murray CJ, Lopez AD. Global mortality, disability, and the contribution of risk factors: global burden of disease study. Lancet. 1997;349:1436-1442. (Pubitemid 27212192)
2. Libby P. Inflammation in atherosclerosis. Nature. 2002;420:868-874. (Pubitemid 36019640)
3. Ogata J, Masuda J, Yutani C, Yamaguchi T. Rupture of atheromatous plaque as a cause of thrombotic occlusion of stenotic internal carotid artery. Stroke. 1990;21:1740-1745.
4. Hansson GK, Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol. 2006;6:508-519. (Pubitemid 43980523)
5. Buhlin K, Hultin M, Norderyd O, Persson L, Pockley AG, Rabe P, Klinge B, Gustafsson A. Risk factors for atherosclerosis in cases with severe periodontitis. J Clin Periodontol. 2009;36:541-549.
6. Ma Z, Choudhury A, Kang SA, Monestier M, Cohen PL, Eisenberg RA. Accelerated atherosclerosis in ApoE deficient lupus mouse models. Clin Immunol. 2008;127:168-175.
7. Kumar H, Kawai T, Akira S. Toll-like receptors and innate immunity. Biochem Biophys Res Commun. 2009;388:621-625.
8. Michelsen KS, Doherty TM, Shah PK, Arditi M. Role of Toll-like receptors in atherosclerosis. Circ Res. 2004;95:e96-97.
9. Hansson GK, Robertson AK, Soderberg-Naucler C. Inflammation and atherosclerosis. Annu Rev Pathol. 2006;1:297-329.
10. Monaco C, Gregan SM, Navin TJ, Foxwell BM, Davies AH, Feldmann M. Toll-like receptor-2 mediates inflammation and matrix degradation in human atherosclerosis. Circulation. 2009;120:2462-2469.
11. Kuwahata S, Fujita S, Orihara K, Hamasaki S, Oba R, Hirai H, Nagata K, Ishida S, Kataoka T, Oketani N, Ichiki H, Iriki Y, Saihara K, Okui H, Ninomiya Y, Tei C. High expression level of Toll-like receptor 2 on monocytes is an important risk factor for arteriosclerotic disease. Atherosclerosis. 2010;209:248-254.
12. Bjorkbacka H, Kunjathoor VV, Moore KJ, Koehn S, Ordija CM, Lee MA, Means T, Halmen K, Luster AD, Golenbock DT, Freeman MW. Reduced atherosclerosis in MyD88-null mice links elevated serum cholesterol levels to activation of innate immunity signaling pathways. Nat Med. 2004;10:416-421. (Pubitemid 38508522)
13. Michelsen KS, Wong MH, Shah PK, Zhang W, Yano J, Doherty TM, Akira S, Rajavashisth TB, Arditi M. Lack of Toll-like receptor 4 or myeloid differentiation factor 88 reduces atherosclerosis and alters plaque phenotype in mice deficient in apolipoproteine. Proc Natl Acad Sci U S A. 2004;101:10679-10684. (Pubitemid 38955802)
14. Mullick AE, Tobias PS, Curtiss LK. Modulation of atherosclerosis in mice by Toll-like receptor 2. J Clin Invest. 2005;115:3149-3156. (Pubitemid 41567579)
15. Hasu M, Thabet M, Tam N, Whitman SC. Specific loss of Toll-like receptor 2 on bone marrow derived cells decreases atherosclerosis in LDL receptor null mice. Can J Physiol Pharmacol. 2011;89:737-742.
16. Madan M, Amar S. Toll-like receptor-2 mediates diet and/or pathogen associated atherosclerosis: proteomic findings. PLoS One. 2008;3:e3204.
17. Cole JE, Navin TJ, Cross AJ, Goddard ME, Alexopoulou L, Mitra AT, Davies AH, Flavell RA, Feldmann M, Monaco C. Unexpected protective role for toll-like receptor 3 in the arterial wall. Proc Natl Acad Sci U S A. 2011;108:2372-2377.
18. Chung JY, Lu M, Yin Q, Lin SC, Wu H. Molecular basis for the unique specificity of traf6. Adv Exp Med Biol. 2007;597:122-130.
19. Hostager BS. Roles of traf6 in cd40 signaling. Immunol Res. 2007;39:105-114. (Pubitemid 47574878)
20. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell. 2010;140:805-820.
21. Forde A, Constien R, Grone HJ, Hammerling G, Arnold B. Temporal Cre-mediated recombination exclusively in endothelial cells using Tie2 regulatory elements. Genesis. 2002;33:191-197. (Pubitemid 34966841)
22. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 1999;8:265-277. (Pubitemid 29523965)
23. Gareus R, Kotsaki E, Xanthoulea S, van der Made I, Gijbels MJ, Kardakaris R, Polykratis A, Kollias G, de Winther MP, Pasparakis M. Endothelial cell-specific NF-kappab inhibition protects mice from atherosclerosis. Cell Metab. 2008;8:372-383.
24. Stewart CR, Stuart LM, Wilkinson K, van Gils JM, Deng J, Halle A, Rayner KJ, Boyer L, Zhong R, Frazier WA, Lacy-Hulbert A, El Khoury J, Golenbock DT, Moore KJ. Cd36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol. 2010;11:155-161.
25. Matsunaga T, Hokari S, Koyama I, Harada T, Komoda T. NF-kappa B activation in endothelial cells treated with oxidized high-density lipo-protein. Biochem Biophys Res Commun. 2003;303:313-319. (Pubitemid 36338242)
26. Caligiuri G, Rudling M, Ollivier V, Jacob MP, Michel JB, Hansson GK, Nicoletti A. Interleukin-10 deficiency increases atherosclerosis, thrombosis, and low-density lipoproteins in apolipoprotein E knockout mice. Mol Med. 2003;9:10-17. (Pubitemid 36667687)
27. Kanters E, Pasparakis M, Gijbels MJ, Vergouwe MN, Partouns-Hendriks I, Fijneman RJ, Clausen BE, Forster I, Kockx MM, Rajewsky K, Kraal G, Hofker MH, de Winther MP. Inhibition of NF-kappaB activation in macrophages increases atherosclerosis in LDL receptor-deficient mice. J Clin Invest. 2003;112:1176-1185. (Pubitemid 38056294)
28. Woo CW, Cui D, Arellano J, Dorweiler B, Harding H, Fitzgerald KA, Ron D, Tabas I. Adaptive suppression of the ATF4-chop branch of the unfolded protein response by Toll-like receptor signalling. Nat Cell Biol. 2009;11:1473-1480.
29. Tabas I. Macrophage death and defective inflammation resolution in atherosclerosis. Nat Rev Immunol. 2010;10:36-46.
30. Moore KJ, Freeman MW. Scavenger receptors in atherosclerosis: beyond lipid uptake. Arterioscler Thromb Vasc Biol. 2006;26:1702-1711. (Pubitemid 44305322)
31. Vandivier RW, Henson PM, Douglas IS. Burying the dead: the impact of failed apoptotic cell removal (efferocytosis) on chronic inflammatory lung disease. Chest. 2006;129:1673-1682. (Pubitemid 43895000)
32. Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I. Immunosuppressive effects of apoptotic cells. Nature. 1997;390:350-351.
33. Thorp E, Li G, Seimon TA, Kuriakose G, Ron D, Tabas I. Reduced apoptosis and plaque necrosis in advanced atherosclerotic lesions of ApoE\-/\- and LDLR\-/\- mice lacking chop. Cell Metab. 2009;9:474-481.
34. Stachon P, Missiou A, Walter C, Varo N, Colberg C, Wolf D, Buchner M, von Zur Muhlen C, Zirlik K, Bode C, Zirlik A. Tumor necrosis factor receptor associated factor 6 is not required for atherogenesis in mice and does not associate with atherosclerosis in humans. PLoS One. 2010;5:e11589.
35. Chiffoleau E, Kobayashi T, Walsh MC, King CG, Walsh PT, Hancock WW, Choi Y, Turka LA. TNF receptor-associated factor 6 deficiency during hemopoiesis induces TH2-polarized inflammatory disease. J Immunol. 2003;171:5751-5759. (Pubitemid 37467190)
36. King CG, Kobayashi T, Cejas PJ, Kim T, Yoon K, Kim GK, Chiffoleau E, Hickman SP, Walsh PT, Turka LA, Choi Y. TRAF6 is a T cell-intrinsic negative regulator required for the maintenance of immune homeostasis. Nat Med. 2006;12:1088-1092. (Pubitemid 44353391)
37. Lutgens E, Lievens D, Beckers L, Wijnands E, Soehnlein O, Zernecke A, Seijkens T, Engel D, Cleutjens J, Keller AM, Naik SH, Boon L, Oufella HA, Mallat Z, Ahonen CL, Noelle RJ, de Winther MP, Daemen MJ, Biessen EA, Weber C. Deficient CD40-TRAF6 signaling in leukocytes prevents atherosclerosis by skewing the immune response toward an antiinflammatory profile. J Exp Med. 2010;207:391-404.