Helix-loop-helix factor inhibitor of differentiation 3 regulates interleukin-5 expression and B-1a B cell proliferation

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 12, 2013, Pages 2771-2779

  Perry, Heather M ^a,b   Oldham, Stephanie N ^a,b   Fahl, Shawn P ^b   Que, Xuchu ^c   Gonen, Ayelet ^c   Harmon, Daniel B ^a   Tsimikas, Sotirios ^c   Witztum, Joseph L ^c   Bender, Timothy P ^a,b   McNamara, Coleen A ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Arteriosclerosis; Basic helix loop helix transcription factors; Immune system

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CD5 ANTIGEN; HELIX LOOP HELIX PROTEIN; IMMUNOGLOBULIN M; INHIBITOR OF DIFFERENTIATION 3; INTERLEUKIN 33; INTERLEUKIN 5; LEUKOSIALIN;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; E BOX ELEMENT; FLOW CYTOMETRY; INNATE IMMUNITY; LYMPHOCYTE PROLIFERATION; LYMPHOID CELL; MAST CELL; MOUSE; NONHUMAN; PERITONEAL CAVITY; PERITONEAL FLUID; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SPLEEN; TH2 CELL; WESTERN BLOTTING;

ARTERIOSCLEROSIS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; MMUNE SYSTEM;

ANIMALS; ANTIGENS, CD19; AORTA; AORTIC DISEASES; APOLIPOPROTEINS E; ATHEROSCLEROSIS; B-LYMPHOCYTE SUBSETS; CELL PROLIFERATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; IMMUNITY, INNATE; INHIBITOR OF DIFFERENTIATION PROTEINS; INTERLEUKIN-5; INTERLEUKINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOPLASM PROTEINS; T-LYMPHOCYTES, HELPER-INDUCER; TRANSFECTION;

EID: 84888206176     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.302571     Document Type: Article

References (71)

1. Roger VL, Go AS, Lloyd-Jones DM, et al; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics-2012 update: A report from the American Heart Association. Circulation. 2012;125:e2-e220
2. Libby P. Inflammation in atherosclerosis. Arterioscler Thromb Vasc Biol. 2012;32:2045-2051
3. Hansson GK, Hermansson A. The immune system in atherosclerosis. Nat Immunol. 2011;12:204-212
4. Lahoute C, Herbin O, Mallat Z, Tedgui A. Adaptive immunity in atherosclerosis: Mechanisms and future therapeutic targets. Nat Rev Cardiol. 2011;8:348-358
5. Campbell KA, Lipinski MJ, Doran AC, Skaflen MD, Fuster V, McNamara CA. Lymphocytes and the adventitial immune response in atherosclerosis. Circ Res. 2012;110:889-900
6. Tabas I. Macrophage death and defective inflammation resolution in atherosclerosis. Nat Rev Immunol. 2010;10:36-46
7. Palinski W, Miller E, Witztum JL. Immunization of low density lipoprotein (LDL) receptor-deficient rabbits with homologous malondialdehyde-modified LDL reduces atherogenesis. Proc Natl Acad Sci USA. 1995;92:821-825
8. Freigang S, Hörkkö S, Miller E, Witztum JL, Palinski W. Immunization of LDL receptor-deficient mice with homologous malondialdehyde- modified and native LDL reduces progression of atherosclerosis by mechanisms other than induction of high titers of antibodies to oxidative neoepitopes. Arterioscler Thromb Vasc Biol. 1998;18:1972-1982
9. Nicoletti A, Kaveri S, Caligiuri G, Bariéty J, Hansson GK. Immunoglobulin treatment reduces atherosclerosis in apo E knockout mice. J Clin Invest. 1998;102:910-918
10. 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
11. 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
12. Faria-Neto JR, Chyu KY, Li X, Dimayuga PC, Ferreira C, Yano J, Cercek B, Shah PK. Passive immunization with monoclonal IgM antibodies against phosphorylcholine reduces accelerated vein graft atherosclerosis in apolipoprotein E-null mice. Atherosclerosis. 2006;189:83-90
13. Ameli S, Hultgårdh-Nilsson A, Regnström J, Calara F, Yano J, Cercek B, Shah PK, Nilsson J. Effect of immunization with homologous LDL and oxidized LDL on early atherosclerosis in hypercholesterolemic rabbits. Arterioscler Thromb Vasc Biol. 1996;16:1074-1079
14. 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
15. 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
16. Major AS, Fazio S, Linton MF. B-lymphocyte deficiency increases atherosclerosis in LDL receptor-null mice. Arterioscler Thromb Vasc Biol. 2002;22:1892-1898
17. Perry HM, Bender TP, McNamara CA. B cell subsets in atherosclerosis. Front Immunol. 2012;3:373
18. Montecino-Rodriguez E, Dorshkind K. B-1 B cell development in the fetus and adult. Immunity. 2012;36:13-21
19. Baumgarth N. The double life of a B-1 cell: Self-reactivity selects for protective effector functions. Nat Rev Immunol. 2011;11:34-46
20. 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
21. Esplin BL, Welner RS, Zhang Q, Borghesi LA, Kincade PW. A differentiation pathway for B1 cells in adult bone marrow. Proc Natl Acad Sci USA. 2009;106:5773-5778
22. Holodick NE, Repetny K, Zhong X, Rothstein TL. Adult BM generates CD5+ B1 cells containing abundant N-region additions. Eur J Immunol. 2009;39:2383-2394
23. Barber CL, Montecino-Rodriguez E, Dorshkind K. Reduced production of B-1-specified common lymphoid progenitors results in diminished potential of adult marrow to generate B-1 cells. Proc Natl Acad Sci USA. 2011;108:13700-13704
24. Ghosn EE, Sadate-Ngatchou P, Yang Y, Herzenberg LA, Herzenberg LA. Distinct progenitors for B-1 and B-2 cells are present in adult mouse spleen. Proc Natl Acad Sci USA. 2011;108:2879-2884
25. 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
26. Miller YI, Choi SH, Wiesner P, Fang L, Harkewicz R, Hartvigsen K, Boullier A, Gonen A, Diehl CJ, Que X, Montano E, Shaw PX, Tsimikas S, Binder CJ, Witztum JL. Oxidation-specific epitopes are danger-Associated molecular patterns recognized by pattern recognition receptors of innate immunity. Circ Res. 2011;108:235-248
27. Ehrenstein MR, Notley CA. The importance of natural IgM: Scavenger, protector and regulator. Nat Rev Immunol. 2010;10:778-786
28. Bird DA, Gillotte KL, Hörkkö S, Friedman P, Dennis EA, Witztum JL, Steinberg D. Receptors for oxidized low-density lipoprotein on elicited mouse peritoneal macrophages can recognize both the modified lipid moieties and the modified protein moieties: Implications with respect to macrophage recognition of apoptotic cells. Proc Natl Acad Sci USA. 1999;96:6347-6352
29. Hörkkö S, Bird DA, Miller E, Itabe H, Leitinger N, Subbanagounder G, Berliner JA, Friedman P, Dennis EA, Curtiss LK, Palinski W, Witztum JL. Monoclonal autoantibodies specific for oxidized phospholipids or oxidized phospholipid-protein adducts inhibit macrophage uptake of oxidized low-density lipoproteins. J Clin Invest. 1999;103:117-128
30. Boullier A, Friedman P, Harkewicz R, Hartvigsen K, Green SR, Almazan F, Dennis EA, Steinberg D, Witztum JL, Quehenberger O. Phosphocholine as a pattern recognition ligand for CD36. J Lipid Res. 2005;46:969-976
31. Chang MK, Bergmark C, Laurila A, Hörkkö S, Han KH, Friedman P, Dennis EA, Witztum JL. Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: Evidence that oxidation-specific epitopes mediate macrophage recognition. Proc Natl Acad Sci USA. 1999;96:6353-6358
32. Erickson LD, Foy TM, Waldschmidt TJ. Murine B1 B cells require IL-5 for optimal T cell-dependent activation. J Immunol. 2001;166:1531-1539
33. Moon BG, Takaki S, Miyake K, Takatsu K. The role of IL-5 for mature B-1 cells in homeostatic proliferation, cell survival, and Ig production. J Immunol. 2004;172:6020-6029
34. Kopf M, Brombacher F, Hodgkin PD, Ramsay AJ, Milbourne EA, Dai WJ, Ovington KS, Behm CA, Köhler G, Young IG, Matthaei KI. IL-5-deficient mice have a developmental defect in CD5+ B-1 cells and lack eosinophilia but have normal antibody and cytotoxic T cell responses. Immunity. 1996;4:15-24
35. Moro K, Yamada T, Tanabe M, Takeuchi T, Ikawa T, Kawamoto H, Furusawa J, Ohtani M, Fujii H, Koyasu S. Innate production of T(H)2 cytokines by adipose tissue-Associated c-Kit(+)Sca-1(+) lymphoid cells. Nature. 2010;463:540-544
36. Spits H, Di Santo JP. The expanding family of innate lymphoid cells: Regulators and effectors of immunity and tissue remodeling. Nat Immunol. 2011;12:21-27
37. Monticelli LA, Sonnenberg GF, Artis D. Innate lymphoid cells: Critical regulators of allergic inflammation and tissue repair in the lung. Curr Opin Immunol. 2012;24:284-289
38. Mjösberg J, Bernink J, Peters C, Spits H. Transcriptional control of innate lymphoid cells. Eur J Immunol. 2012;42:1916-1923
39. Mjösberg JM, Trifari S, Crellin NK, Peters CP, Van Drunen CM, Piet B, Fokkens WJ, Cupedo T, Spits H. Human IL-25-And IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161. Nat Immunol. 2011;12:1055-1062
40. Monticelli LA, Sonnenberg GF, Abt MC, et al. Innate lymphoid cells promote lung-Tissue homeostasis after infection with influenza virus. Nat Immunol. 2011;12:1045-1054
41. Halim TY, MacLaren A, Romanish MT, Gold MJ, McNagny KM, Takei F. Retinoic-Acid-receptor-related orphan nuclear receptor alpha is required for natural helper cell development and allergic inflammation. Immunity. 2012;37:463-474
42. Kee BL. E and ID proteins branch out. Nat Rev Immunol. 2009;9:175-184
43. Ji Y, Pos Z, Rao M, Klebanoff CA, Yu Z, Sukumar M, Reger RN, Palmer DC, Borman ZA, Muranski P, Wang E, Schrump DS, Marincola FM, Restifo NP, Gattinoni L. Repression of the DNA-binding inhibitor Id3 by Blimp-1 limits the formation of memory CD8+ T cells. Nat Immunol. 2011;12:1230-1237
44. Jones-Mason ME, Zhao X, Kappes D, Lasorella A, Iavarone A, Zhuang Y. E protein transcription factors are required for the development of CD4(+) lineage T cells. Immunity. 2012;36:348-361
45. Lauritsen JP, Wong GW, Lee SY, Lefebvre JM, Ciofani M, Rhodes M, Kappes DJ, Zúñiga-Pflücker JC, Wiest DL. Marked induction of the helix-loop-helix protein Id3 promotes the gammadelta T cell fate and renders their functional maturation Notch independent. Immunity. 2009;31:565-575
46. Li J, Maruyama T, Zhang P, Konkel JE, Hoffman V, Zamarron B, Chen W. Mutation of inhibitory helix-loop-helix protein Id3 causes ?d T-cell lymphoma in mice. Blood. 2010;116:5615-5621
47. Maruyama T, Li J, Vaque JP, Konkel JE, Wang W, Zhang B, Zhang P, Zamarron BF, Yu D, Wu Y, Zhuang Y, Gutkind JS, Chen W. Control of the differentiation of regulatory T cells and T(H)17 cells by the DNA-binding inhibitor Id3. Nat Immunol. 2011;12:86-95
48. Miyazaki M, Rivera RR, Miyazaki K, Lin YC, Agata Y, Murre C. The opposing roles of the transcription factor E2A and its antagonist Id3 that orchestrate and enforce the naive fate of T cells. Nat Immunol. 2011;12:992-1001
49. Pan L, Sato S, Frederick JP, Sun XH, Zhuang Y. Impaired immune responses and B-cell proliferation in mice lacking the Id3 gene. Mol Cell Biol. 1999;19:5969-5980
50. Yang CY, Best JA, Knell J, Yang E, Sheridan AD, Jesionek AK, Li HS, Rivera RR, Lind KC, D'Cruz LM, Watowich SS, Murre C, Goldrath AW. The transcriptional regulators Id2 and Id3 control the formation of distinct memory CD8+ T cell subsets. Nat Immunol. 2011;12:1221-1229
51. Lin YC, Jhunjhunwala S, Benner C, Heinz S, Welinder E, Mansson R, Sigvardsson M, Hagman J, Espinoza CA, Dutkowski J, Ideker T, Glass CK, Murre C. A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate. Nat Immunol. 2010;11:635-643
52. Murre C. Helix-loop-helix proteins and lymphocyte development. Nat Immunol. 2005;6:1079-1086
53. Doran AC, Lehtinen AB, Meller N, Lipinski MJ, Slayton RP, Oldham SN, Skaflen MD, Yeboah J, Rich SS, Bowden DW, McNamara CA. Id3 is a novel atheroprotective factor containing a functionally significant single-nucleotide polymorphism associated with intima-media thickness in humans. Circ Res. 2010;106:1303-1311
54. Doran AC, Lipinski MJ, Oldham SN, et al. B-cell aortic homing and atheroprotection depend on Id3. Circ Res. 2012;110:e1-e12
55. Lipinski MJ, Campbell KA, Duong SQ, Welch TJ, Garmey JC, Doran AC, Skaflen MD, Oldham SN, Kelly KA, McNamara CA. Loss of Id3 increases VCAM-1 expression, macrophage accumulation, and atherogenesis in Ldlr-/-mice. Arterioscler Thromb Vasc Biol. 2012;32:2855-2861
56. Chang MK, Binder CJ, Miller YI, Subbanagounder G, Silverman GJ, Berliner JA, Witztum JL. Apoptotic cells with oxidation-specific epitopes are immunogenic and proinflammatory. J Exp Med. 2004;200:1359-1370
57. Shaw PX, Hörkkö 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
58. Fahl SP, Crittenden RB, Allman D, Bender TP. c-Myb is required for pro-B cell differentiation. J Immunol. 2009;183:5582-5592
59. Sasaki Y, Casola S, Kutok JL, Rajewsky K, Schmidt-Supprian M. TNF family member B cell-Activating factor (BAFF) receptor-dependent and-independent roles for BAFF in B cell physiology. J Immunol. 2004;173:2245-2252
60. Rajsheker S, Manka D, Blomkalns AL, Chatterjee TK, Stoll LL, Weintraub NL. Crosstalk between perivascular adipose tissue and blood vessels. Curr Opin Pharmacol. 2010;10:191-196
61. Gräbner R, Lötzer K, Döpping S, et al. Lymphotoxin beta receptor signaling promotes tertiary lymphoid organogenesis in the aorta adventitia of aged ApoE-/-mice. J Exp Med. 2009;206:233-248
62. Miller AM, Xu D, Asquith DL, Denby L, Li Y, Sattar N, Baker AH, McInnes IB, Liew FY. IL-33 reduces the development of atherosclerosis. J Exp Med. 2008;205:339-346
63. Miller AM, Liew FY. The IL-33/ST2 pathway-A new therapeutic target in cardiovascular disease. Pharmacol Ther. 2011;131:179-186
64. Smithgall MD, Comeau MR, Yoon BR, Kaufman D, Armitage R, Smith DE. IL-33 amplifies both Th1-And Th2-Type responses through its activity on human basophils, allergen-reactive Th2 cells, iNKT and NK cells. Int Immunol. 2008;20:1019-1030
65. Allakhverdi Z, Smith DE, Comeau MR, Delespesse G. Cutting edge: The ST2 ligand IL-33 potently activates and drives maturation of human mast cells. J Immunol. 2007;179:2051-2054
66. Schwartz CJ, Mitchell JR. Cellular infiltration of the human arterial adventitia associated with atheromatous plaques. Circulation. 1962;26:73-78
67. Zhou X, Hansson GK. Detection of B cells and proinflammatory cytokines in atherosclerotic plaques of hypercholesterolaemic apolipoprotein E knockout mice. Scand J Immunol. 1999;50:25-30
68. Hamze M, Desmetz C, Berthe ML, Roger P, Boulle N, Brancherau P, Picard E, Guzman C, Tolza C, Guglielmi P. Characterization of resident B cells of vascular walls in human atherosclerotic patients. J Immunol. 2013;191:3006-3016
69. Koltsova EK, Garcia Z, Chodaczek G, Landau M, McArdle S, Scott SR, von Vietinghoff S, Galkina E, Miller YI, Acton ST, Ley K. Dynamic T cell-APC interactions sustain chronic inflammation in atherosclerosis. J Clin Invest. 2012;122:3114-3126
70. Huan T, Zhang B, Wang Z, et al; Coronary ARteryDIsease Genome wide Replication and Meta-Analysis (CARDIoGRAM) Consortium, International Consortium for Blood Pressure GWAS (ICBP). A systems biology framework identifies molecular underpinnings of coronary heart disease. Arterioscler Thromb Vasc Biol. 2013;33:1427-1434
71. Welch CL, Bretschger S, Latib N, Bezouevski M, Guo Y, Pleskac N, Liang CP, Barlow C, Dansky H, Breslow JL, Tall AR. Localization of atherosclerosis susceptibility loci to chromosomes 4 and 6 using the Ldlr knockout mouse model. Proc Natl Acad Sci USA. 2001;98:7946-7951