Innate response activator b cells aggravate atherosclerosis by stimulating t helper-1 adaptive immunity

Circulation

Volumn 129, Issue 16, 2014, Pages 1677-1687

  Hilgendorf, Ingo ^a   Theurl, Igor ^a,b   Gerhardt, Louisa M S ^a   Robbins, Clinton S ^a,c   Weber, Georg F ^a   Gonen, Ayelet ^d   Iwamoto, Yoshiko ^a   Degousee, Norbert ^c   Holderried, Tobias A W ^e   Winter, Carla ^f   Zirlik, Andreas ^f   Lin, Herbert Y ^a   Sukhova, Galina K ^g   Butany, Jagdish ^h   Rubin, Barry B ^h   Witztum, Joseph L ^d   Libby, Peter ^g   Nahrendorf, Matthias ^a   Weissleder, Ralph ^a,i   Swirski, Filip K ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY HOSPITAL INNSBRUCK   (Austria)

^c UNIVERSITY HEALTH NETWORK   (Canada)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e HEINRICH HEINE UNIVERSITY   (Germany)

^f UNIVERSITY HEART CENTER FREIBURG BAD KROZINGEN   (Germany)

^g BRIGHAM AND WOMEN S HOSPITAL   (United States)

^h UNIVERSITY HEALTH NETWORK   (Canada)

ⁱ HARVARD MEDICAL SCHOOL   (United States)

Author keywords

atherosclerosis; B lymphocytes; dendritic cells; granulocyte macrophage colony stimulating factor; immunology; T lymphocytes

Indexed keywords

ATHEROSCLEROSIS; B-LYMPHOCYTES; DENDRITIC CELLS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; IMMUNOLOGY; T-LYMPHOCYTES;

ADAPTIVE IMMUNITY; ANIMALS; ATHEROSCLEROSIS; B-LYMPHOCYTES; BONE MARROW CELLS; CHOLESTEROL, DIETARY; COCULTURE TECHNIQUES; HUMANS; IMMUNITY, INNATE; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RADIATION CHIMERA; TH1 CELLS;

EID: 84899075437     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.113.006381     Document Type: Article

References (50)

1. 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. (Pubitemid 43214743)
2. 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 USA. 2005;102:1596-1601. (Pubitemid 40209213)
3. Herbin O, Ait-Oufella H, Yu W, Fredrikson GN, Aubier B, Perez N, Barateau V, Nilsson J, Tedgui A, Mallat Z. Regulatory T-cell response to apolipoprotein B100-derived peptides reduces the development and progression of atherosclerosis in mice. Arterioscler Thromb Vasc Biol. 2012;32:605-612.
4. Klingenberg R, Gerdes N, Badeau RM, Gisterå A, Strodthoff D, Ketelhuth DF, Lundberg AM, Rudling M, Nilsson SK, Olivecrona G, Zoller S, Lohmann C, Lüscher TF, Jauhiainen M, Sparwasser T, Hansson GK. Depletion of FOXP3+ regulatory T cells promotes hypercholesterolemia and atherosclerosis. J Clin Invest. 2013;123:1323-1334.
5. Kyaw T, Tay C, Krishnamurthi S, Kanellakis P, Agrotis A, Tipping P, Bobik A, Toh BH. B1a B lymphocytes are atheroprotective by secreting natural IgM that increases IgM deposits and reduces necrotic cores in atherosclerotic lesions. Circ Res. 2011;109:830-840.
6. Perry HM, McNamara CA. Refining the role of B cells in atherosclerosis. Arterioscler Thromb Vasc Biol. 2012;32:1548-1549.
7. Subramanian M, Thorp E, Hansson GK, Tabas I. Treg-mediated suppression of atherosclerosis requires MYD88 signaling in DCs. J Clin Invest. 2013;123:179-188.
8. Swirski FK, Libby P, Aikawa E, Alcaide P, Luscinskas FW, Weissleder R, Pittet MJ. Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest. 2007;117:195-205. (Pubitemid 46048466)
9. Swirski FK, Nahrendorf M. Leukocyte behavior in atherosclerosis, myocardial infarction, and heart failure. Science. 2013;339:161-166.
10. Whitman SC, Ravisankar P, Elam H, Daugherty A. Exogenous interferon-gamma enhances atherosclerosis in apolipoprotein E-/-mice. Am J Pathol. 2000;157:1819-1824.
11. Rauch PJ, Chudnovskiy A, Robbins CS, Weber GF, Etzrodt M, Hilgendorf I, Tiglao E, Figueiredo JL, Iwamoto Y, Theurl I, Gorbatov R, Waring MT, Chicoine AT, Mouded M, Pittet MJ, Nahrendorf M, Weissleder R, Swirski FK. Innate response activator B cells protect against microbial sepsis. Science. 2012;335:597-601.
12. Stanley E, Lieschke GJ, Grail D, Metcalf D, Hodgson G, Gall JA, Maher DW, Cebon J, Sinickas V, Dunn AR. Granulocyte/macrophage colony-stimulating factor-deficient mice show no major perturbation of hematopoiesis but develop a characteristic pulmonary pathology. Proc Natl Acad Sci USA. 1994;91:5592-5596. (Pubitemid 24174374)
13. Hamilton JA, Achuthan A. Colony stimulating factors and myeloid cell biology in health and disease. Trends Immunol. 2013;34:81-89.
14. Robbins CS, Chudnovskiy A, Rauch PJ, Figueiredo JL, Iwamoto Y, Gorbatov R, Etzrodt M, Weber GF, Ueno T, van Rooijen N, Mulligan-Kehoe MJ, Libby P, Nahrendorf M, Pittet MJ, Weissleder R, Swirski FK. Extramedullary hematopoiesis generates Ly-6C(high) monocytes that infiltrate atherosclerotic lesions. Circulation. 2012;125:364-374.
15. Ditiatkovski M, Toh BH, Bobik A. GM-CSF deficiency reduces macrophage PPAR-gamma expression and aggravates atherosclerosis in ApoE-deficient mice. Arterioscler Thromb Vasc Biol. 2006;26:2337-2344. (Pubitemid 44465731)
16. Shaposhnik Z, Wang X, Weinstein M, Bennett BJ, Lusis AJ. Granulocyte macrophage colony-stimulating factor regulates dendritic cell content of atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 2007;27:621-627.
17. Haghighat A, Weiss D, Whalin MK, Cowan DP, Taylor WR. Granulocyte colony-stimulating factor and granulocyte macrophage colony-stimulating factor exacerbate atherosclerosis in apolipoprotein E-deficient mice. Circulation. 2007;115:2049-2054. (Pubitemid 46625956)
18. Zhu SN, Chen M, Jongstra-Bilen J, Cybulsky MI. GM-CSF regulates intimal cell proliferation in nascent atherosclerotic lesions. J Exp Med. 2009;206:2141-2149.
19. Murphy AJ, Akhtari M, Tolani S, Pagler T, Bijl N, Kuo CL, Wang M, Sanson M, Abramowicz S, Welch C, Bochem AE, Kuivenhoven JA, Yvan-Charvet L, Tall AR. ApoE regulates hematopoietic stem cell proliferation, monocytosis, and monocyte accumulation in atherosclerotic lesions in mice. J Clin Invest. 2011;121:4138-4149.
20. Doran AC, Lipinski MJ, Oldham SN, Garmey JC, Campbell KA, Skaflen MD, Cutchins A, Lee DJ, Glover DK, Kelly KA, Galkina EV, Ley K, Witztum JL, Tsimikas S, Bender TP, McNamara CA. B-cell aortic homing and atheroprotection depend on Id3. Circ Res. 2012;110:e1-e12.
21. Sugiyama S, Okada Y, Sukhova GK, Virmani R, Heinecke JW, Libby P. Macrophage myeloperoxidase regulation by granulocyte macrophage colony-stimulating factor in human atherosclerosis and implications in acute coronary syndromes. Am J Pathol. 2001;158:879-891. (Pubitemid 32221781)
22. Gupta S, Pablo AM, Jiang Xc, Wang N, Tall AR, Schindler C. IFN-gamma potentiates atherosclerosis in ApoE knock-out mice. J Clin Invest. 1997;99:2752-2761. (Pubitemid 27259823)
23. McLaren JE, Ramji DP. Interferon gamma: a master regulator of atherosclerosis. Cytokine Growth Factor Rev. 2009;20:125-135.
24. Hermansson A, Ketelhuth DF, Strodthoff D, Wurm M, Hansson EM, Nicoletti A, Paulsson-Berne G, Hansson GK. Inhibition of T cell response to native low-density lipoprotein reduces atherosclerosis. J Exp Med. 2010;207:1081-1093.
25. Stemme S, Faber B, Holm J, Wiklund O, Witztum JL, Hansson GK. T lymphocytes from human atherosclerotic plaques recognize oxidized low density lipoprotein. Proc Natl Acad Sci USA. 1995;92:3893-3897.
26. Zhou X, Robertson AK, Hjerpe C, Hansson GK. Adoptive transfer of CD4+ T cells reactive to modified low-density lipoprotein aggravates atherosclerosis. Arterioscler Thromb Vasc Biol. 2006;26:864-870. (Pubitemid 43732164)
27. Binder CJ, Hörkkö 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. (Pubitemid 36749223)
28. Zhou X, Caligiuri G, Hamsten A, Lefvert AK, Hansson GK. LDL immunization induces T-cell-dependent antibody formation and protection against atherosclerosis. Arterioscler Thromb Vasc Biol. 2001;21:108-114. (Pubitemid 32061934)
29. Chou MY, Fogelstrand L, Hartvigsen K, Hansen LF, Woelkers D, Shaw PX, Choi J, Perkmann T, Bäckhed F, Miller YI, Hörkkö S, Corr M, Witztum JL, Binder CJ. Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans. J Clin Invest. 2009;119:1335-1349.
30. Stavnezer J, Amemiya CT. Evolution of isotype switching. Semin Immunol. 2004;16:257-275. (Pubitemid 39445624)
31. Rosas M, Gordon S, Taylor PR. Characterisation of the expression and function of the GM-CSF receptor alpha-chain in mice. Eur J Immunol. 2007;37:2518-2528. (Pubitemid 47423621)
32. Mallat Z, Taleb S, Ait-Oufella H, Tedgui A. The role of adaptive T cell immunity in atherosclerosis. J Lipid Res. 2009;50(suppl):S364-S369.
33. Vremec D, Lieschke GJ, Dunn AR, Robb L, Metcalf D, Shortman K. The influence of granulocyte/macrophage colony-stimulating factor on dendritic cell levels in mouse lymphoid organs. Eur J Immunol. 1997;27:40-44. (Pubitemid 27046056)
34. Greter M, Helft J, Chow A, Hashimoto D, Mortha A, Agudo-Cantero J, Bogunovic M, Gautier EL, Miller J, Leboeuf M, Lu G, Aloman C, Brown BD, Pollard JW, Xiong H, Randolph GJ, Chipuk JE, Frenette PS, Merad M. GM-CSF controls nonlymphoid tissue dendritic cell homeostasis but is dispensable for the differentiation of inflammatory dendritic cells. Immunity. 2012;36:1031-1046.
35. Hamilton JA. Colony-stimulating factors in inflammation and autoimmunity. Nat Rev Immunol. 2008;8:533-544. (Pubitemid 351913679)
36. Daro E, Pulendran B, Brasel K, Teepe M, Pettit D, Lynch DH, Vremec D, Robb L, Shortman K, McKenna HJ, Maliszewski CR, Maraskovsky E. Polyethylene glycol-modified GM-CSF expands CD11b(high) CD11c(high) but notCD11b(low) CD11c(high) murine dendritic cells in vivo: a comparative analysis with Flt3 ligand. J Immunol. 2000;165:49-58. (Pubitemid 30429489)
37. Hansson GK, Hermansson A. The immune system in atherosclerosis. Nat Immunol. 2011;12:204-212.
38. Campbell IK, Rich MJ, Bischof RJ, Dunn AR, Grail D, Hamilton JA. Protection from collagen-induced arthritis in granulocyte-macrophage colony-stimulating factor-deficient mice. J Immunol. 1998;161:3639-3644.
39. McQualter JL, Darwiche R, Ewing C, Onuki M, Kay TW, Hamilton JA, Reid HH, Bernard CC. Granulocyte macrophage colony-stimulating factor: a new putative therapeutic target in multiple sclerosis. J Exp Med. 2001;194:873-882.
40. Sonderegger I, Iezzi G, Maier R, Schmitz N, Kurrer M, Kopf M. GM-CSF mediates autoimmunity by enhancing IL-6-dependent Th17 cell development and survival. J Exp Med. 2008;205:2281-2294.
41. King IL, Kroenke MA, Segal BM. GM-CSF-dependent, CD103+ dermal dendritic cells play a critical role in Th effector cell differentiation after subcutaneous immunization. J Exp Med. 2010;207:953-961.
42. Witztum JL, Lichtman AH. The influence of innate and adaptive immune responses on atherosclerosis. Annu Rev Pathol. 2014;9:73-102.
43. Ravandi A, Boekholdt SM, Mallat Z, Talmud PJ, Kastelein JJ, Wareham NJ, Miller ER, Benessiano J, Tedgui A, Witztum JL, Khaw KT, Tsimikas S. Relationship of IgG and IgM autoantibodies and immune complexes to oxidized LDL with markers of oxidation and inflammation and cardiovascular events: results from the EPIC-Norfolk Study. J Lipid Res. 2011;52:1829-1836.
44. Tsimikas S, Brilakis ES, Lennon RJ, Miller ER, Witztum JL, McConnell JP, Kornman KS, Berger PB. Relationship of IgG and IgM autoantibodies to oxidized low density lipoprotein with coronary artery disease and cardiovascular events. J Lipid Res. 2007;48:425-433. (Pubitemid 46220609)
45. Nimmerjahn F, Ravetch JV. Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science. 2005;310:1510-1512. (Pubitemid 41746349)
46. Zouggari Y, Ait-Oufella H, Bonnin P, Simon T, Sage AP, Guérin C, Vilar J, Caligiuri G, Tsiantoulas D, Laurans L, Dumeau E, Kotti S, Bruneval P, Charo IF, Binder CJ, Danchin N, Tedgui A, Tedder TF, Silvestre JS, Mallat Z. B lymphocytes trigger monocyte mobilization and impair heart function after acute myocardial infarction. Nat Med. 2013;19:1273-1280.
47. Balázs M, Martin F, Zhou T, Kearney J. Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity. 2002;17:341-352. (Pubitemid 35279554)
48. Teichmann LL, Schenten D, Medzhitov R, Kashgarian M, Shlomchik MJ. Signals via the adaptor MyD88 in B cells and DCs make distinct and synergistic contributions to immune activation and tissue damage in lupus. Immunity. 2013;38:528-540.
49. Barr TA, Brown S, Mastroeni P, Gray D. B cell intrinsic MyD88 signals drive IFN-gamma production from T cells and control switching to IgG2c. J Immunol. 2009;183:1005-1012.
50. Ponomarev ED, Shriver LP, Maresz K, Pedras-Vasconcelos J, Verthelyi D, Dittel BN. GM-CSF production by autoreactive T cells is required for the activation of microglial cells and the onset of experimental autoimmune encephalomyelitis. J Immunol. 2007;178:39-48. (Pubitemid 46039660)