CXCR3-dependent accumulation and activation of perivascular macrophages is necessary for homeostatic arterial remodeling to hemodynamic stresses

Journal of Experimental Medicine

Volumn 207, Issue 9, 2010, Pages 1951-1966

  Zhou, Jing ^a   Tang, Paul C Y ^a   Qin, Lingfeng ^a   Gayed, Peter M ^a   Li, Wei ^a   Skokos, Eleni A ^a   Kyriakides, Themis R ^a   Pober, Jordan S ^a   Tellides, George ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 13; CD14 ANTIGEN; CD16 ANTIGEN; CHEMOKINE RECEPTOR CXCR3; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GELATINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTERY BLOOD FLOW; ARTICLE; BLOOD VESSEL WALL; BONE MARROW CELL; CELL INFILTRATION; CELL TRANSFER; COMMON CAROTID ARTERY; EXTERNAL CAROTID ARTERY; EXTRACELLULAR MATRIX; FEMALE; HEMODYNAMIC STRESS; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN TISSUE; MACROPHAGE; MACROPHAGE ACTIVATION; MALE; MONOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

ADOLESCENT; ADULT; AGED; ANIMALS; ARTERIES; CHILD; CHILD, PRESCHOOL; FEMALE; HOMEOSTASIS; HUMANS; MACROPHAGES; MALE; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, CXCR3; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; THROMBOPLASTIN; YOUNG ADULT;

EID: 77956244520     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20100098     Document Type: Article

References (62)

1. Auffray, C., D. Fogg, M. Garfa, G. Elain, O. Join-Lambert, S. Kayal, S. Sarnacki, A. Cumano, G. Lauvau, and F. Geissmann. 2007. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science. 317:666-670. doi:10.1126/science.1142883
2. Bakker, E.N., A. Pistea, J.A. Spaan, T. Rolf, C.J. de Vries, N. van Rooijen, E. Candi, and E. VanBavel. 2006. Flow-dependent remodeling of small arteries in mice deficient for tissue-type transglutaminase: possible compensation by macrophage-derived factor XIII. Circ. Res. 99:86-92. doi:10.1161/01.RES.0000229657.83816.a7
3. Bakker, E.N., H.L. Matlung, P. Bonta, C.J. de Vries, N. van Rooijen, and E. Vanbavel. 2008. Blood flow-dependent arterial remodelling is facilitated by inflammation but directed by vascular tone. Cardiovasc. Res. 78:341-348. doi:10.1093/cvr/cvn050
4. Bassiouny, H.S., R.H. Song, X.F. Hong, A. Singh, H. Kocharyan, and S. Glagov. 1998. Flow regulation of 72-kD collagenase IV (MMP-2) after experimental arterial injury. Circulation. 98:157-163.
5. Baumbach, G.L., and D.D. Heistad. 1989. Remodeling of cerebral arterioles in chronic hypertension. Hypertension. 13:968-972.
6. Cho, H.J., P. Shashkin, C.A. Gleissner, D. Dunson, N. Jain, J.K. Lee, Y. Miller, and K. Ley. 2007. Induction of dendritic cell-like phenotype in macrophages during foam cell formation. Physiol. Genomics. 29:149-160.
7. Combadière, C., S. Potteaux, M. Rodero, T. Simon, A. Pezard, B. Esposito, R. Merval, A. Proudfoot, A. Tedgui, and Z. Mallat. 2008. Combined inhibition of CCL2, CX3CR1, and CCR5 abrogates Ly6C(hi) and Ly6C(lo) monocytosis and almost abolishes atherosclerosis in hypercholesterolemic mice. Circulation. 117:1649-1657. doi:10.1161/CIRCULATIONAHA.107.745091
8. Fleming, T.J., M.L. Fleming, and T.R. Malek. 1993. Selective expression of Ly-6G on myeloid lineage cells in mouse bone marrow. RB6-8C5 mAb to granulocyte-differentiation antigen (Gr-1) detects members of the Ly-6 family. J. Immunol. 151:2399-2408.
9. Galis, Z.S., C. Johnson, D. Godin, R. Magid, J.M. Shipley, R.M. Senior, and E. Ivan. 2002. Targeted disruption of the matrix metalloproteinase-9 gene impairs smooth muscle cell migration and geometrical arterial remodeling. Circ. Res. 91:852-859. doi:10.1161/01.RES.0000041036.86977.14
10. Galkina, E., A. Kadl, J. Sanders, D. Varughese, I.J. Sarembock, and K. Ley. 2006. Lymphocyte recruitment into the aortic wall before and during development of atherosclerosis is partially L-selectin dependent. J. Exp. Med. 203:1273-1282. doi:10.1084/jem.20052205
11. Geissmann, F., S. Jung, and D.R. Littman. 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity. 19:71-82. doi:10.1016/S1074-7613(03)00174-2
12. Gleissner, C.A., I. Shaked, K.M. Little, and K. Ley. 2010. CXC chemokine ligand 4 induces a unique transcriptome in monocyte-derived macrophages. J. Immunol. 184:4810-4818. doi:10.4049/jimmunol.0901368
13. Gordon, S., and P.R. Taylor. 2005. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5:953-964. doi:10.1038/nri1733
14. Gratchev, A., J. Kzhyshkowska, J. Utikal, and S. Goerdt. 2005. Interleukin-4 and dexamethasone counterregulate extracellular matrix remodelling and phagocytosis in type-2 macrophages. Scand. J. Immunol. 61:10-17. doi:10.1111/j.0300-9475.2005.01524.x
15. Guzik, T.J., N.E. Hoch, K.A. Brown, L.A. McCann, A. Rahman, S. Dikalov, J. Goronzy, C. Weyand, and D.G. Harrison. 2007. Role of the T cell in the genesis of angiotensin II-induced hypertension and vascular dysfunction. J. Exp. Med. 204:2449-2460. doi:10.1084/jem.20070657
16. Hancock, W.W., B. Lu, W. Gao, V. Csizmadia, K. Faia, J.A. King, S.T. Smiley, M. Ling, N.P. Gerard, and C. Gerard. 2000. Requirement of the chemokine receptor CXCR3 for acute allograft rejection. J. Exp. Med. 192:1515-1520. doi:10.1084/jem.192.10.1515
17. Heller, E.A., E. Liu, A.M. Tager, Q. Yuan, A.Y. Lin, N. Ahluwalia, K. Jones, S.L. Koehn, V.M. Lok, E. Aikawa, et al. 2006. Chemokine CXCL10 promotes atherogenesis by modulating the local balance of effector and regulatory T cells. Circulation. 113:2301-2312. doi:10.1161/CIRCULATIONAHA.105.605121
18. Hong, H., S. Aksenov, X. Guan, J.T. Fallon, D. Waters, and C. Chen. 2002. Remodeling of small intramyocardial coronary arteries distal to a severe epicardial coronary artery stenosis. Arterioscler. Thromb. Vasc. Biol. 22:2059-2065. doi:10.1161/01.ATV.0000041844.54849.7E
19. Janatpour, M.J., S. Hudak, M. Sathe, J.D. Sedgwick, and L.M. McEvoy. 2001. Tumor necrosis factor-dependent segmental control of MIG expression by high endothelial venules in inflamed lymph nodes regulates monocyte recruitment. J. Exp. Med. 194:1375-1384. doi:10.1084/jem.194.9.1375
20. Kamiya, A., and T. Togawa. 1980. Adaptive regulation of wall shear stress to flow change in the canine carotid artery. Am. J. Physiol. 239:H14-H21.
21. Katschke, K.J. Jr., J.B. Rottman, J.H. Ruth, S. Qin, L. Wu, G. LaRosa, P. Ponath, C.C. Park, R.M. Pope, and A.E. Koch. 2001. Differential expression of chemokine receptors on peripheral blood, synovial fluid, and synovial tissue monocytes/macrophages in rheumatoid arthritis. Arthritis Rheum. 44:1022-1032. doi:10.1002/1529-0131(200105)44:5〈1022::AIDANR181〉3.0.CO;2-N
22. Kim, W.K., X. Alvarez, J. Fisher, B. Bronfin, S. Westmoreland, J. McLaurin, and K. Williams. 2006. CD163 identifies perivascular macrophages in normal and viral encephalitic brains and potential precursors to perivascular macrophages in blood. Am. J. Pathol. 168:822-834. doi:10.2353/ajpath.2006.050215
23. Koh, K.P., Y. Wang, T. Yi, S.L. Shiao, M.I. Lorber, W.C. Sessa, G. Tellides, and J.S. Pober. 2004. T cell-mediated vascular dysfunction of human allografts results from IFN-gamma dysregulation of NO synthase. J. Clin. Invest. 114:846-856.
24. Kohrgruber, N., M. Gröger, P. Meraner, E. Kriehuber, P. Petzelbauer, S. Brandt, G. Stingl, A. Rot, and D. Maurer. 2004. Plasmacytoid dendritic cell recruitment by immobilized CXCR3 ligands. J. Immunol. 173:6592-6602.
25. Korshunov, V.A., and B.C. Berk. 2003. Flow-induced vascular remodeling in the mouse: a model for carotid intima-media thickening. Arterioscler. Thromb. Vasc. Biol. 23:2185-2191. doi:10.1161/01.ATV.0000103120.06092.14
26. Langheinrich, A.C., M. Kampschulte, T. Buch, and R.M. Bohle. 2007. Vasa vasorum and atherosclerosis - Quid novi? Thromb. Haemost. 97:873-879.
27. Langille, B.L. 1996. Arterial remodeling: relation to hemodynamics. Can. J. Physiol. Pharmacol. 74:834-841. doi:10.1139/cjpp-74-7-834
28. Langille, B.L., M.P. Bendeck, and F.W. Keeley. 1989. Adaptations of carotid arteries of young and mature rabbits to reduced carotid blood flow. Am. J. Physiol. 256:H931-H939.
29. le Noble, F., D. Moyon, L. Pardanaud, L. Yuan, V. Djonov, R. Matthijsen, C. Bréant, V. Fleury, and A. Eichmann. 2004. Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development. 131:361-375. doi:10.1242/dev.00929
30. Lessner, S.M., H.L. Prado, E.K. Waller, and Z.S. Galis. 2002. Atherosclerotic lesions grow through recruitment and proliferation of circulating monocytes in a murine model. Am. J. Pathol. 160:2145-2155.
31. Liu, P., Y.R. Yu, J.A. Spencer, A.E. Johnson, C.T. Vallanat, A.M. Fong, C. Patterson, and D.D. Patel. 2008. CX3CR1 deficiency impairs dendritic cell accumulation in arterial intima and reduces atherosclerotic burden. Arterioscler. Thromb. Vasc. Biol. 28:243-250. doi:10.1161/ATVBAHA.107.158675
32. Luster, A.D., and P. Leder. 1993. IP-10, a -C-X-C- chemokine, elicits a potent thymus-dependent antitumor response in vivo. J. Exp. Med. 178:1057-1065. doi:10.1084/jem.178.3.1057
33. Luster, A.D., S.M. Greenberg, and P. Leder. 1995. The IP-10 chemokine binds to a specific cell surface heparan sulfate site shared with platelet factor 4 and inhibits endothelial cell proliferation. J. Exp. Med. 182:219-231. doi:10.1084/jem.182.1.219
34. Martinez, F.O., S. Gordon, M. Locati, and A. Mantovani. 2006. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 177:7303-7311.
35. Martinez, F.O., A. Sica, A. Mantovani, and M. Locati. 2008. Macrophage activation and polarization. Front. Biosci. 13:453-461. doi:10.2741/2692
36. Medzhitov, R. 2008. Origin and physiological roles of inflammation. Nature. 454:428-435. doi:10.1038/nature07201
37. Mosser, D.M., and J.P. Edwards. 2008. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8:958-969. doi:10.1038/nri2448
38. Nahrendorf, M., F.K. Swirski, E. Aikawa, L. Stangenberg, T. Wurdinger, J.L. Figueiredo, P. Libby, R. Weissleder, and M.J. Pittet. 2007. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J. Exp. Med. 204:3037-3047. doi:10.1084/jem.20070885
39. Nair, M.G., D.W. Cochrane, and J.E. Allen. 2003. Macrophages in chronic type 2 inflammation have a novel phenotype characterized by the abundant expression of Ym1 and Fizz1 that can be partly replicated in vitro. Immunol. Lett. 85:173-180. doi:10.1016/S0165-2478(02)00225-0
40. Nuki, Y., M.M. Matsumoto, E. Tsang, W.L. Young, N. van Rooijen, C. Kurihara, and T. Hashimoto. 2009. Roles of macrophages in flow-induced outward vascular remodeling. J. Cereb. Blood Flow Metab. 29: 495-503. doi:10.1038/jcbfm.2008.136
41. Oppenheim, J.J., and D. Yang. 2005. Alarmins: chemotactic activators of immune responses. Curr. Opin. Immunol. 17:359-365. doi:10.1016/j.coi.2005.06.002
42. Ranjbaran, H., Y. Wang, T.D. Manes, A.O. Yakimov, S. Akhtar, M.S. Kluger, J.S. Pober, and G. Tellides. 2006. Heparin displaces interferon-gamma-inducible chemokines (IP-10, I-TAC, and Mig) sequestered in the vasculature and inhibits the transendothelial migration and arterial recruitment of T cells. Circulation. 114:1293-1300. doi:10.1161/CIRCULATIONAHA.106.631457
43. Rudic, R.D., E.G. Shesely, N. Maeda, O. Smithies, S.S. Segal, and W.C. Sessa. 1998. Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling. J. Clin. Invest. 101:731-736. doi:10.1172/JCI1699
44. Rudic, R.D., M. Bucci, D. Fulton, S.S. Segal, and W.C. Sessa. 2000. Temporal events underlying arterial remodeling after chronic flow reduction in mice: correlation of structural changes with a deficit in basal nitric oxide synthesis. Circ. Res. 86:1160-1166.
45. Saederup, N., L. Chan, S.A. Lira, and I.F. Charo. 2008. Fractalkine deficiency markedly reduces macrophage accumulation and atherosclerotic lesion formation in CCR2-/- mice: evidence for independent chemokine functions in atherogenesis. Circulation. 117:1642-1648. doi:10.1161/CIRCULATIONAHA.107.743872
46. Schwarz, J.B., N. Langwieser, N.N. Langwieser, M.J. Bek, S. Seidl, H.H. Eckstein, B. Lu, A. Schömig, H. Pavenstädt, and D. Zohlnhöfer. 2009. Novel role of the CXC chemokine receptor 3 in inflammatory response to arterial injury: involvement of mTORC1. Circ. Res. 104:189-200. doi:10.1161/CIRCRESAHA.108.182683
47. Selzman, C.H., B.D. Shames, L.L. Reznikov, S.A. Miller, X. Meng, H.A. Barton, A. Werman, A.H. Harken, C.A. Dinarello, and A. Banerjee. 1999. Liposomal delivery of purified inhibitory-kappaBalpha inhibits tumor necrosis factor-alpha-induced human vascular smooth muscle proliferation. Circ. Res. 84:867-875.
48. Sunderkötter, C., T. Nikolic, M.J. Dillon, N. Van Rooijen, M. Stehling, D.A. Drevets, and P.J. Leenen. 2004. Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J. Immunol. 172:4410-4417.
49. hi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J. Clin. Invest. 117:195-205. doi:10.1172/JCI29950
50. Swirski, F.K., M. Nahrendorf, M. Etzrodt, M. Wildgruber, V. Cortez-Retamozo, P. Panizzi, J.L. Figueiredo, R.H. Kohler, A. Chudnovskiy, P. Waterman, et al. 2009. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science. 325:612-616. doi:10.1126/science. 1175202
51. Tacke, F., D. Alvarez, T.J. Kaplan, C. Jakubzick, R. Spanbroek, J. Llodra, A. Garin, J. Liu, M. Mack, N. van Rooijen, et al. 2007. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J. Clin. Invest. 117:185-194. doi:10.1172/JCI28549
52. Tang, P.C., L. Qin, J. Zielonka, J. Zhou, C. Matte-Martone, S. Bergaya, N. van Rooijen, W.D. Shlomchik, W. Min, W.C. Sessa, et al. 2008. MyD88-dependent, superoxide-initiated inflammation is necessary for flow-mediated inward remodeling of conduit arteries. J. Exp. Med. 205:3159-3171. doi:10.1084/jem.20081298
53. Taub, D.D., A.R. Lloyd, K. Conlon, J.M. Wang, J.R. Ortaldo, A. Harada, K. Matsushima, D.J. Kelvin, and J.J. Oppenheim. 1993. Recombinant human interferon-inducible protein 10 is a chemoattractant for human monocytes and T lymphocytes and promotes T cell adhesion to endothelial cells. J. Exp. Med. 177:1809-1814. doi:10.1084/jem.177.6.1809
54. Taub, D.D., D.L. Longo, and W.J. Murphy. 1996. Human interferon-inducible protein-10 induces mononuclear cell infiltration in mice and promotes the migration of human T lymphocytes into the peripheral tissues and human peripheral blood lymphocytes-SCID mice. Blood. 87:1423-1431.
55. Töröcsik, D., H. Bárdos, L. Nagy, and R. Adány. 2005. Identification of factor XIII-A as a marker of alternative macrophage activation. Cell. Mol. Life Sci. 62:2132-2139. doi:10.1007/s00018-005-5242-9
56. van Wanrooij, E.J., H. Happé, A.D. Hauer, P. de Vos, T. Imanishi, H. Fujiwara, T.J. van Berkel, and J. Kuiper. 2005. HIV entry inhibitor TAK-779 attenuates atherogenesis in low-density lipoprotein receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol. 25:2642-2647. doi:10.1161/01.ATV.0000192018. 90021.c0
57. van Wanrooij, E.J., S.C. de Jager, T. van Es, P. de Vos, H.L. Birch, D.A. Owen, R.J. Watson, E.A. Biessen, G.A. Chapman, T.J. van Berkel, and J. Kuiper. 2008. CXCR3 antagonist NBI-74330 attenuates atherosclerotic plaque formation in LDL receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol. 28:251-257. doi:10.1161/ATVBAHA.107.147827
58. Veillard, N.R., S. Steffens, G. Pelli, B. Lu, B.R. Kwak, C. Gerard, I.F. Charo, and F. Mach. 2005. Differential influence of chemokine receptors CCR2 and CXCR3 in development of atherosclerosis in vivo. Circulation. 112:870-878. doi:10.1161/CIRCULATIONAHA.104.520718
59. Waeckel, L., Z. Mallat, S. Potteaux, C. Combadière, M. Clergue, M. Duriez, L. Bao, C. Gerard, B.J. Rollins, A. Tedgui, et al. 2005. Impairment in postischemic neovascularization in mice lacking the CXC chemokine receptor 3. Circ. Res. 96:576-582. doi:10.1161/01.RES.0000159389.55544.20
60. Whiting, D., G. Hsieh, J.J. Yun, A. Banerji, W. Yao, M.C. Fishbein, J. Belperio, R.M. Strieter, B. Bonavida, and A. Ardehali. 2004. Chemokine monokine induced by IFN-gamma/CXC chemokine ligand 9 stimulates T lymphocyte proliferation and effector cytokine production. J. Immunol. 172:7417-7424.
61. Zaba, L.C., J. Fuentes-Duculan, R.M. Steinman, J.G. Krueger, and M.A. Lowes. 2007. Normal human dermis contains distinct populations of CD11c+BDCA-1+ dendritic cells and CD163+FXIIIA+ macrophages. J. Clin. Invest. 117:2517-2525. doi:10.1172/JCI32282
62. Zhou, Y., T. Kurihara, R.P. Ryseck, Y. Yang, C. Ryan, J. Loy, G. Warr, and R. Bravo. 1998. Impaired macrophage function and enhanced T cell-dependent immune response in mice lacking CCR5, the mouse homologue of the major HIV-1 coreceptor. J. Immunol. 160:4018-4025.