Activation of an innate immune receptor, Nod1, accelerates atherogenesis in Apoe2/2 mice

Journal of Immunology

Volumn 194, Issue 2, 2015, Pages 773-780

  Kanno, Shunsuke ^a   Nishio, Hisanori ^a,b   Tanaka, Tamami ^a   Motomura, Yoshitomo ^c   Murata, Kenji ^a   Ihara, Kenji ^a   Onimaru, Mitsuho ^c   Yamasaki, Sho ^c   Kono, Hajime ^d   Sueishi, Katsuo ^e   Hara, Toshiro ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY HOSPITAL   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

^d TEIKYO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e NATIONAL HOSPITAL ORGANIZATION   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 4; HEPTANOYL GAMMA DEXTRO GLUTAMYL 2,6 DIAMINOPIMELOYL DEXTRO ALANINE; RANTES; APOLIPOPROTEIN E; CARD4 PROTEIN, MOUSE; IMMUNOLOGICAL ADJUVANT; OLIGOPEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ROOT; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CCL5 GENE; CD3+ T LYMPHOCYTE; CELL INFILTRATION; CONTROLLED STUDY; DISEASE ASSOCIATION; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MACROPHAGE ACTIVATION; MACROPHAGE MIGRATION; MALE; MOUSE; NONHUMAN; PROTEIN DETERMINATION; PROTEIN FUNCTION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; ANIMAL; AORTA; BONE MARROW CELL; DEFICIENCY; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; MACROPHAGE; PATHOLOGY; T LYMPHOCYTE;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; AORTA; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BONE MARROW CELLS; MACROPHAGES; MICE; MICE, KNOCKOUT; NOD1 SIGNALING ADAPTOR PROTEIN; OLIGOPEPTIDES; T-LYMPHOCYTES;

EID: 84920501880     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302841     Document Type: Article

References (49)

1. Ross, R. 1999. Atherosclerosis-an inflammatory disease. N. Engl. J. Med. 340: 115-126.
2. + T-cell priming efficacy under hypercholesterolemic conditions associated with atherosclerosis. Circ. Res. 103: 965-973.
3. + T cells aggravates atherosclerosis in immunodeficient apolipoprotein E knockout mice. Circulation 102: 2919-2922.
4. Edfeldt, K., J. Swedenborg, G. K. Hansson, and Z. Q. Yan. 2002. Expression of Toll-like receptors in human atherosclerotic lesions: A possible pathway for plaque activation. Circulation 105: 1158-1161.
5. Naiki, Y., R. Sorrentino, M. H. Wong, K. S. Michelsen, K. Shimada, S. Chen, A. Yilmaz, A. Slepenkin, N. W. J. Schröder, T. R. Crother, et al. 2008. TLR/MyD88 and liver X receptor a signaling pathways reciprocally control Chlamydia pneumoniae-induced acceleration of atherosclerosis. J. Immunol. 181: 7176-7185.
6. Gibson, F. C. III, C. Hong, H. H. Chou, H. Yumoto, J. Chen, E. Lien, J. Wong, and C. A. Genco. 2004. Innate immune recognition of invasive bacteria accelerates atherosclerosis in apolipoprotein E-deficient mice. Circulation 109: 2801- 2806.
7. Mullick, A. E., P. S. Tobias, and L. K. Curtiss. 2005. Modulation of atherosclerosis in mice by Toll-like receptor 2. J. Clin. Invest. 115: 3149-3156.
8. Takeuchi, O., and S. Akira. 2010. Pattern recognition receptors and inflammation. Cell 140: 805-820.
9. Michelsen, K. S., M. H. Wong, P. K. Shah, W. Zhang, J. Yano, T. M. Doherty, S. Akira, T. B. Rajavashisth, and M. Arditi. 2004. 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. USA 101: 10679-10684.
10. Björkbacka, H., V. V. Kunjathoor, K. J. Moore, S. Koehn, C. M. Ordija, M. A. Lee, T. Means, K. Halmen, A. D. Luster, D. T. Golenbock, and M. W. Freeman. 2004. Reduced atherosclerosis in MyD88-null mice links elevated serum cholesterol levels to activation of innate immunity signaling pathways. Nat. Med. 10: 416-421.
11. Duewell, P., H. Kono, K. J. Rayner, C. M. Sirois, G. Vladimer, F. G. Bauernfeind, G. S. Abela, L. Franchi, G. Nuñez, M. Schnurr, et al. 2010. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464: 1357-1361.
12. Opitz, B., S. Förster, A. C. Hocke, M. Maass, B. Schmeck, S. Hippenstiel, N. Suttorp, and M. Krüll. 2005. Nod1-mediated endothelial cell activation by Chlamydophila pneumoniae. Circ. Res. 96: 319-326.
13. Girardin, S. E., I. G. Boneca, L. A. M. Carneiro, A. Antignac, M. Jéhanno, J. Viala, K. Tedin, M. K. Taha, A. Labigne, U. Zähringer, et al. 2003. Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 300: 1584-1587.
14. Inohara, N., T. Koseki, L. del Peso, Y. Hu, C. Yee, S. Chen, R. Carrio, J. Merino, D. Liu, J. Ni, and G. Núñez. 1999. Nod1, an Apaf-1-like activator of caspase-9 and nuclear factor-kB. J. Biol. Chem. 274: 14560-14567.
15. Bertin, J., W. J. Nir, C. M. Fischer, O. V. Tayber, P. R. Errada, J. R. Grant, J. J. Keilty, M. L. Gosselin, K. E. Robison, G. H. Wong, et al. 1999. Human CARD4 protein is a novel CED-4/Apaf-1 cell death family member that activates NF-kB. J. Biol. Chem. 274: 12955-12958.
16. Nishio, H., S. Kanno, S. Onoyama, K. Ikeda, T. Tanaka, K. Kusuhara, Y. Fujimoto, K. Fukase, K. Sueishi, and T. Hara. 2011. Nod1 ligands induce sitespecific vascular inflammation. Arterioscler. Thromb. Vasc. Biol. 31: 1093-1099.
17. Shigeoka, A. A., A. Kambo, J. C. Mathison, A. J. King, W. F. Hall, J. da Silva Correia, R. J. Ulevitch, and D. B. McKay. 2010. Nod1 and Nod2 are expressed in human and murine renal tubular epithelial cells and participate in renal ischemia reperfusion injury. J. Immunol. 184: 2297-2304.
18. Veillard, N. R., B. Kwak, G. Pelli, F. Mulhaupt, R. W. James, A. E. Proudfoot, and F. Mach. 2004. Antagonism of RANTES receptors reduces atherosclerotic plaque formation in mice. Circ. Res. 94: 253-261.
19. Goossens, P., M. J. Gijbels, A. Zernecke, W. Eijgelaar, M. N. Vergouwe, I. van der Made, J. Vanderlocht, L. Beckers, W. A. Buurman, M. J. Daemen, et al. 2010. Myeloid type I interferon signaling promotes atherosclerosis by stimulating macrophage recruitment to lesions. Cell Metab. 12: 142-153.
20. Liou, J. T., C. C. Mao, D. Ching-Wah Sum, F. C. Liu, Y. S. Lai, J. C. Li, and Y. J. Day. 2013. Peritoneal administration of Met-RANTES attenuates inflammatory and nociceptive responses in a murine neuropathic pain model. J. Pain 14: 24-35.
21. Reikvam, D. H., A. Erofeev, A. Sandvik, V. Grcic, F. L. Jahnsen, P. Gaustad, K. D. McCoy, A. J. Macpherson, L. A. Meza-Zepeda, and F. E. Johansen. 2011. Depletion of murine intestinal microbiota: effects on gut mucosa and epithelial gene expression. PLoS ONE 6: e17996.
22. Paigen, B., A. Morrow, P. A. Holmes, D. Mitchell, and R. A. Williams. 1987. Quantitative assessment of atherosclerotic lesions in mice. Atherosclerosis 68: 231-240.
23. Nakashima, Y., A. S. Plump, E. W. Raines, J. L. Breslow, and R. Ross. 1994. ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler. Thromb. 14: 133-140.
24. Lutgens, E., B. Faber, K. Schapira, C. T. Evelo, R. van Haaften, S. Heeneman, K. B. Cleutjens, A. P. Bijnens, L. Beckers, J. G. Porter, et al. 2005. Gene profiling in atherosclerosis reveals a key role for small inducible cytokines: validation using a novel monocyte chemoattractant protein monoclonal antibody. Circulation 111: 3443-3452.
25. Cartwright, N., O. Murch, S. K. McMaster, M. J. Paul-Clark, D. A. van Heel, B. Ryffel, V. F. Quesniaux, T. W. Evans, C. Thiemermann, and J. A. Mitchell. 2007. Selective NOD1 agonists cause shock and organ injury/dysfunction in vivo. Am. J. Respir. Crit. Care Med. 175: 595-603.
26. Moreno, L., S. K. McMaster, T. Gatheral, L. K. Bailey, L. S. Harrington, N. Cartwright, P. C. Armstrong, T. D. Warner, M. Paul-Clark, and J. A. Mitchell. 2010. Nucleotide oligomerization domain 1 is a dominant pathway for NOS2 induction in vascular smooth muscle cells: comparison with Toll-like receptor 4 responses in macrophages. Br. J. Pharmacol. 160: 1997-2007.
27. Maass, M., C. Bartels, P. M. Engel, U. Mamat, and H. H. Sievers. 1998. Endovascular presence of viable Chlamydia pneumoniae is a common phenomenon in coronary artery disease. J. Am. Coll. Cardiol. 31: 827-832.
28. Levin, M. C., P. Jirholt, A. Wramstedt, M. E. Johansson, A. M. Lundberg, M. G. Trajkovska, M. Stahlman, P. Fogelstrand, M. Brisslert, L. Fogelstrand, et al. 2011. Rip2 deficiency leads to increased atherosclerosis despite decreased inflammation. Circ. Res. 109: 1210-1218.
29. Johansson, M. E., X. Y. Zhang, K. Edfeldt, A. M. Lundberg, M. C. Levin, J. Borén, W. Li, X. M. Yuan, L. Folkersen, P. Eriksson, et al. 2014. Innate immune receptor NOD2 promotes vascular inflammation and formation of lipid-rich necrotic cores in hypercholesterolemic mice. Eur. J. Immunol. 44: 3081-3092.
30. Appay, V., and S. L. Rowland-Jones. 2001. RANTES: A versatile and controversial chemokine. Trends Immunol. 22: 83-87.
31. Weber, C., and H. Noels. 2011. Atherosclerosis: current pathogenesis and therapeutic options. Nat. Med. 17: 1410-1422.
32. Braunersreuther, V., A. Zernecke, C. Arnaud, E. A. Liehn, S. Steffens, E. Shagdarsuren, K. Bidzhekov, F. Burger, G. Pelli, B. Luckow, et al. 2007. Ccr5 but not Ccr1 deficiency reduces development of diet-induced atherosclerosis in mice. Arterioscler. Thromb. Vasc. Biol. 27: 373-379.
33. Potteaux, S., C. Combadière, B. Esposito, C. Lecureuil, H. Ait-Oufella, R. Merval, P. Ardouin, A. Tedgui, and Z. Mallat. 2006. Role of bone marrowderived CC-chemokine receptor 5 in the development of atherosclerosis of lowdensity lipoprotein receptor knockout mice. Arterioscler. Thromb. Vasc. Biol. 26: 1858-1863.
34. Saikku, P., M. Leinonen, L. Tenkanen, E. Linnanmäki, M. R. Ekman, V. Manninen, M. Mänttäri, M. H. Frick, and J. K. Huttunen. 1992. Chronic Chlamydia pneumoniae infection as a risk factor for coronary heart disease in the Helsinki Heart Study. Ann. Intern. Med. 116: 273-278.
35. Chiu, B., E. Viira, W. Tucker, and I. W. Fong. 1997. Chlamydia pneumoniae, cytomegalovirus, and herpes simplex virus in atherosclerosis of the carotid artery. Circulation 96: 2144-2148.
36. Kiechl, S., G. Egger, M. Mayr, C. J. Wiedermann, E. Bonora, F. Oberhollenzer, M. Muggeo, Q. Xu, G. Wick, W. Poewe, and J. Willeit. 2001. Chronic infections and the risk of carotid atherosclerosis: prospective results from a large population study. Circulation 103: 1064-1070.
37. Laman, J. D., A. H. Schoneveld, F. L. Moll, M. van Meurs, and G. Pasterkamp. 2002. Significance of peptidoglycan, a proinflammatory bacterial antigen in atherosclerotic arteries and its association with vulnerable plaques. Am. J. Cardiol. 90: 119-123.
38. Ott, S. J., N. E. El Mokhtari, M. Musfeldt, S. Hellmig, S. Freitag, A. Rehman, T. Kühbacher, S. Nikolaus, P. Namsolleck, M. Blaut, et al. 2006. Detection of diverse bacterial signatures in atherosclerotic lesions of patients with coronary heart disease. Circulation 113: 929-937.
39. Koren, O., A. Spor, J. Felin, F. Fak, J. Stombaugh, V. Tremaroli, C. J. Behre, R. Knight, B. Fagerberg, R. E. Ley, and F. Bäckhed. 2011. Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc. Natl. Acad. Sci. USA 108(Suppl. 1): 4592-4598.
40. Karlsson, F. H., F. Fak, I. Nookaew, V. Tremaroli, B. Fagerberg, D. Petranovic, F. Bäckhed, and J. Nielsen. 2012. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat. Commun. 3: 1245.
41. Clarke, T. B., K. M. Davis, E. S. Lysenko, A. Y. Zhou, Y. Yu, and J. N. Weiser. 2010. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat. Med. 16: 228-231.
42. Ohashi, K., V. Burkart, S. Flohé, and H. Kolb. 2000. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. J. Immunol. 164: 558-561.
43. Kanwar, R. K., J. R. Kanwar, D. Wang, D. J. Ormrod, and G. W. Krissansen. 2001. Temporal expression of heat shock proteins 60 and 70 at lesion-prone sites during atherogenesis in ApoE-deficient mice. Arterioscler. Thromb. Vasc. Biol. 21: 1991-1997.
44. Smiley, S. T., J. A. King, and W. W. Hancock. 2001. Fibrinogen stimulates macrophage chemokine secretion through Toll-like receptor 4. J. Immunol. 167: 2887-2894.
45. Okamura, Y., M. Watari, E. S. Jerud, D. W. Young, S. T. Ishizaka, J. Rose, J. C. Chow, and J. F. StraussIII. 2001. The extra domain A of fibronectin activates Toll-like receptor 4. J. Biol. Chem. 276: 10229-10233.
46. Koeth, R. A., Z. Wang, B. S. Levison, J. A. Buffa, E. Org, B. T. Sheehy, E. B. Britt, X. Fu, Y. Wu, L. Li, et al. 2013. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat. Med. 19: 576- 585.
47. Bouskra, D., C. Brézillon, M. Bérard, C. Werts, R. Varona, I. G. Boneca, and G. Eberl. 2008. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 456: 507-510.
48. Robertson, S. J., J. Y. Zhou, K. Geddes, S. J. Rubino, J. H. Cho, S. E. Girardin, and D. J. Philpott. 2013. Nod1 and Nod2 signaling does not alter the composition of intestinal bacterial communities at homeostasis. Gut Microbes 4: 222-231.
49. Higashimori, M., J. B. Tatro, K. J. Moore, M. E. Mendelsohn, J. B. Galper, and D. Beasley. 2011. Role of Toll-like receptor 4 in intimal foam cell accumulation in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 31: 50-57.