Chemokine CXCL10 promotes atherogenesis by modulating the local balance of effector and regulatory T cells

Circulation

Volumn 113, Issue 19, 2006, Pages 2301-2312

  Heller, Eric A ^a   Liu, Emerson ^a   Tager, Andrew M ^a   Yuan, Qian ^a   Lin, Alexander Y ^a   Ahluwalia, Neil ^a   Jones, Krister ^a   Koehn, Stephanie L ^a,b   Lok, Vincent M ^a,b   Aikawa, Elena ^a,b   Moore, Kathryn J ^a,b   Luster, Andrew D ^a   Gerszten, Robert E ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Atherosclerosis; Chemokines; Immunology; Inflammation; Leukocytes

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; APOLIPOPROTEIN E; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR4; CHEMOKINE RECEPTOR CXCR3; CHOLESTEROL; CXCL9 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA1; TRIACYLGLYCEROL; ALPHA CHEMOKINE; CHEMOKINE RECEPTOR; CXC CHEMOKINE IP 10; CXC CHEMOKINE IP-10; CXC CHEMOKINE RECEPTOR 3; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; TGFB1 PROTEIN, HUMAN; TGFB1 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BACKCROSSING; BODY WEIGHT; CD4+ T LYMPHOCYTE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIET; EFFECTOR CELL; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RNA ISOLATION; SEX DIFFERENCE; STATISTICAL ANALYSIS; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; AORTA; CD4 LYMPHOCYTE COUNT; CHEMISTRY; CORONARY ARTERY ATHEROSCLEROSIS; CORONARY BLOOD VESSEL; GENETICS; MOUSE MUTANT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; AORTA; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CD4 LYMPHOCYTE COUNT; CD4-POSITIVE T-LYMPHOCYTES; CHEMOKINES, CXC; CORONARY ARTERIOSCLEROSIS; CORONARY VESSELS; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-10; MICE; MICE, MUTANT STRAINS; POLYMERASE CHAIN REACTION; RECEPTORS, CHEMOKINE; RNA, MESSENGER; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

EID: 33744981802     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.105.605121     Document Type: Article

References (47)

1. Daugherty A, Pure E, Delfel-Butteiger D, Chen S, Leferovich J, Roselaar SE, Rader DJ. The effects of total lymphocyte deficiency on the extent of atherosclerosis in apolipoprotein E-/- mice. J Clin Invest. 1997;100:1575-1580.
2. Dansky HM, Charlton SA, Harper MM, Smith JD. T and B lymphocytes play a minor role in atherosclerotic plaque formation in the apolipoprotein E-deficient mouse. Proc Natl Acad Sci U S A. 1997;94:4642-4646.
3. Shaw PX, Horkko S, Chang MK, Curtiss LK, Palinski W, Silverman GJ, Witztum JL. Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity. J Clin Invest. 2000;105:1731-1740.
4. Binder CJ, Hartvigsen K, Chang MK, Miller M, Broide D, Palinski W, Curtiss LK, Corr M, Witztum JL. IL-5 links adaptive and natural immunity specific for epitopes of oxidized LDL and protects from atherosclerosis. J Clin Invest. 2004;114:427-437.
5. Caligiuri G, Nicoletti A, Poirier B, Hansson GK. Protective immunity against atherosclerosis carried by B cells of hypercholesterolemic mice. J Clin Invest. 2002;109:745-753.
6. Binder CJ, Horkko S, Dewan A, Chang MK, Kieu EP, Goodyear CS, Shaw PX, Palinski W, Witztum JL, Silverman GJ. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat Med. 2003;9:736-743.
7. Luster AD, Unkeless JC, Ravetch JV. Gamma-interferon transcriptionally regulates an early-response gene containing homology to platelet proteins. Nature. 1985;315:672-676.
8. Luster AD, Ravetch JV. Biochemical characterization of a gamma interferon-inducible cytokine (IP-10). J Exp Med. 1987;166:1084-1097.
9. Gattass CR, King LB, Luster AD, Ashwell JD. Constitutive expression of Interferon gamma-inducible protein 10 in lymphoid organs and inducible expression in T cells and thymocytes. J Exp Med. 1994;179:1373-1378.
10. Gottlieb AB, Luster AD, Posnett DN, Carter DM. Detection of a gamma interferon-induced protein TP-10 in psoriatic plaques. J Exp Med. 1988;168:941-948.
11. Mach F, Sauty A, Iarossi AS, Sukhova GK, Neote K, Libby P, Luster AD. Differential expression of three T lymphocyte-activating CXC chemokines by human atheroma-associated cells. J Clin Invest. 1999;104:1041-1050.
12. Kawamura A, Miura S, Fujino M, Nishikawa H, Matsuo Y, Tanigawa H, Tomita S, Tsuchiya Y, Matsuo K, Saku K. CXCR3 chemokine receptor-plasma IP10 interaction in patients with coronary artery disease. Circ J. 2003;67:851-854.
13. Fernandes JL, Mamoni RL, Orford JL, Garcia C, Selwyn AP, Coelho OR, Blotta MH. Increased Th1 activity in patients with coronary artery disease. Cytokine. 2004;26:131-137.
14. Loetscher M, Gerber B, Loetscher P, Jones SA, Piali L, Clark-Lewis I, Baggiolini M, Moser B. Chemokine receptor specific for TP10 and MIG: structure, function, and expression in activated T-lymphocytes. J Exp Med. 1996;184:963-969.
15. Loetscher M, Loetscher P, Brass N, Meese E, Moser B. Lymphocyte-specific chemokine receptor CXCR3: regulation, chemokine binding and gene localization. Eur J Immunol. 1998;28:3696-3705.
16. Lu B, Humbles A, Bota D, Gerard C, Moser B, Soler D, Luster AD, Gerard NP. Structure and function of the murine chemokine receptor CXCR3. Eur J Immunol. 1999;29:3804-3812.
17. Veillard NR, Steffens S, Pelli G, Lu B, Kwak BR, Gerard C, Charo TF, Mach F. Differential influence of chemokine receptors CCR2 and CXCR3 in development of atherosclerosis in vivo. Circulation. 2005;112:870-878.
18. Sauty A, Colvin RA, Wagner L, Rochat S, Spertini F, Luster AD. CXCR3 intemalization following T cell-endothelial cell contact: preferential role of TFN-inducible T cell alpha chemoattractant (CXCL11). J Immunol. 2001;167:7084-7093.
19. Liu MT, Keirstead HS, Lane TE. Neutralization of the chemokine CXCL10 reduces inflammatory cell invasion and demyelination and improves neurological function in a viral model of multiple sclerosis. J Immunol. 2001;167:4091-4097.
20. Khan IA, MacLean JA, Lee FS, Casciotti L, DeHaan E, Schwartzman JD, Luster AD. TP-10 is critical for effector T cell trafficking and host survival in Toxoplasma gondii infection. Immunity. 2000;12:483-494.
21. Ohmori Y, Hamilton TA. Cooperative interaction between interferon (IFN) stimulus response element and kappa B sequence motifs controls IFN gamma- and lipopolysaccharide-stimulated transcription from the murine IP-10 promoter. J Biol Chem. 1993;268:6677-6688.
22. Tager AM, Dufour JH, Goodarzi K, Bercury SD, von Andrian UH, Luster AD. BLTR mediates leukotriene B(4)-induced chemotaxis and adhesion and plays a dominant role in eosinophil accumulation in a murine model of peritonitis. J Exp Med. 2000;192:439-446.
23. Plump AS, Smith JD, Hayek T, Aalto-Setala K, Walsh A, Verstuyft JG, Rubin EM, Breslow JL. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell. 1992;71:343-353.
24. Heller EA, Liu E, Tager AM, Sinha S, Roberts JD, Koehn SL, Libby P, Aikawa ER, Chen JQ, Huang P, Freeman MW, Moore KJ, Luster AD, Gerszten RE. Inhibition of atherogenesis in BLT1-deficient mice reveals a role for LTB4 and BLT1 in smooth muscle cell recruitment. Circulation. 2005;112:578-586.
25. Kuhlencordt PJ, Chen J, Han F, Astern J, Huang PL. Genetic deficiency of inducible nitric oxide synthase reduces atherosclerosis and lowers plasma lipid peroxides in apolipoprotein E-knockout mice. Circulation. 2001;103:3099-3104.
26. Peirson SN, Butler JN, Foster RG. Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis. Nucleic Acids Res. 2003;31:e73.
27. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science. 2003;299:1057-1061.
28. Khattri R, Cox T, Yasayko SA, Ramsdell F. An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat Immunol. 2003;4:337-42.
29. Fontenot JD, Rudensky AY. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat Immunol. 2005;6:331-337.
30. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol. 2003;4:330-336.
31. Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, McGrady G, Wahl SM. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med. 2003;198:1875-1886.
32. Peng Y, Laouar Y, Li MO, Green EA, Flavell RA. TGF-beta regulates in vivo expansion of Foxp3-expressing CD4+CD25+ regulatory T cells responsible for protection against diabetes. Proc Natl Acad Sci U S A. 2004;101:4572-4577.
33. Lee I, Wang L, Wells AD, Dorf ME, Ozkaynak E, Hancock WW. Recruitment of Foxp3+ T regulatory cells mediating allograft tolerance depends on the CCR4 chemokine receptor. J Exp Med. 2005;201:1037-1044.
34. Iellem A, Mariani M, Lang R, Recalde H, Panina-Bordignon P, Sinigaglia F, D'Ambrosio D. Unique chemotactic response profile and specific expression of chemokine receptors CCR4 and CCR8 by CD4(+)CD25(+) regulatory T cells. J Exp Med. 2001;194:847-853.
35. Freeman CM, Chiu BC, Stolberg VR, Hu J, Zeibecoglou K, Lukacs NW, Lira SA, Kunkel SL, Chensue SW. CCR8 is expressed by antigen-elicited, IL-10-producing CD4+CD25+ T cells, which regulate Th2-mediated granuloma formation in mice. J Immunol. 2005;174:1962-1970.
36. Abi-Younes S, Si-Tahar M, Luster AD. The CC chemokines MDC and TARC induce platelet activation via CCR4. Thromb Res. 2001;101:279-289.
37. Roncador G, Brown PJ, Maestre L, Hue S, Martinez-Torrecuadrada JL, Ling KL, Pratap S, Toms C, Fox BC, Cerundolo V, Powrie F, Banham AH. Analysis of FOXP3 protein expression in human CD4(+)CD25(+) regulatory T cells at the single-cell level. Eur J Immunol. 2005;35:1681-1691.
38. Reardon CA, Blachowicz L, White T, Cabana V, Wang Y, Lukens J, Bluestone J, Getz GS. Effect of immune deficiency on lipoproteins and atherosclerosis in male apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2001;21:1011-1016.
39. Buono C, Pang H, Uchida Y, Libby P, Sharpe AH, Lichtman AH. B7-1/B7-2 costimulation regulates plaque antigen-specific T-cell responses and atherogenesis in low-density lipoprotein receptor-deficient mice. Circulation. 2004;109:2009-2015.
40. Buono C, Binder CJ, Stavrakis G, Witztum JL, Glimcher LH, Lichtman AH. T-bet deficiency reduces atherosclerosis and alters plaque antigen-specific immune responses. Proc Natl Acad Sci U S A. 2005;102:1596-601.
41. O'Garra A, Vieira P. Regulatory T cells and mechanisms of immune system control. Nat Med. 2004;10:801-805.
42. Groux H, O'Garra A, Bigler M, Rouleau M, Antonenko S, de Vries JE, Roncarolo MG. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature. 1997;389:737-742.
43. Mallat Z, Gojova A, Brun V, Esposito B, Fournier N, Cottrez F, Tedgui A, Groux H. Induction of a regulatory T cell type 1 response reduces the development of atherosclerosis in apolipoprotein E-knockout mice. Circulation. 2003;108:1232-1237.
44. Nagler-Anderson C, Bhan AK, Podolsky DK, Terhorst C. Control freaks: immune regulatory cells. Nat Immunol. 2004;5:119-122.
45. Mallat Z, Besnard S, Duriez M, Deleuze V, Emmanuel F, Bureau MF, Soubrier F, Esposito B, Duez H, Fievet C, Staels B, Duverger N, Scherman D, Tedgui A. Protective role of interleukin-10 in atherosclerosis. Circ Res. 1999;85:e17-e24.
46. Pinderski LJ, Fischbein MP, Subbanagounder G, Fishbein MC, Kubo N, Cheroutre H, Curtiss LK, Berliner JA, Boisvert WA. Overexpression of interleukin-10 by activated T lymphocytes inhibits atherosclerosis in LDL receptor-deficient mice by altering lymphocyte and macrophage phenotypes. Circ Res. 2002;90:1064-1071.
47. Ait-Oufella H, Salomon BL, Potteaux S, Robertson AK, Gourdy P, Zoll J, Merval R, Esposito B, Cohen JL, Fisson S, Flavell RA, Hansson GK, Klatzmann D, Tedgui A, Mallat Z. Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med. 2006;12:178-180.