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B cell depletion reduces the development of atherosclerosis in mice

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Ait-Oufella, Hafid Herbin, Olivier Bouaziz, Jean-David Binder, Christoph J. Uyttenhove, Catherine [UCL] Van Snick, Jacques [UCL] Mallat, Ziad

B cell depletion significantly reduces the burden of several immune-mediated diseases. However, B cell activation has been until now associated with a protection against atherosclerosis, suggesting that B cell-depleting therapies would enhance cardiovascular risk. We unexpectedly show that mature B cell depletion using a CD20-specific monoclonal antibody induces a significant reduction of atherosclerosis in various mouse models of the disease. This treatment preserves the production of natural and potentially protective anti-oxidized low-density lipoprotein (oxLDL) IgM autoantibodies over IgG type anti-oxLDL antibodies, and markedly reduces pathogenic T cell activation. B cell depletion diminished T cell-derived IFN-gamma secretion and enhanced production of IL-17; neutralization of the latter abrogated CD20 antibody-mediated atheroprotection. These results challenge the current paradigm that B cell activation plays an overall protective role in atherogenesis and identify new antiatherogenic strategies based on B cell modulation.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2010
Language Anglais
Journal information "The Journal of Experimental Medicine" - Vol. 207, no. 8, p. 1579-1587 (2010)
Peer reviewed yes
Publisher Rockefeller Univ Press (New York)
issn 0022-1007
e-issn 1540-9538
Publication status Publié
Affiliation UCL
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  1. Chou Meng-Yun, Fogelstrand Linda, Hartvigsen Karsten, Hansen Lotte F., Woelkers Douglas, Shaw Peter X., Choi Jeomil, Perkmann Thomas, Bäckhed Fredrik, Miller Yury I., Hörkkö Sohvi, Corr Maripat, Witztum Joseph L., Binder Christoph J., Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans, 10.1172/jci36800
  2. AbuAttieh M., Rebrovich M., Wettstein P. J., Vuk-Pavlovic Z., Limper A. H., Platt J. L., Cascalho M., Fitness of Cell-Mediated Immunity Independent of Repertoire Diversity, 10.4049/jimmunol.178.5.2950
  3. Dansky H. M., Charlton S. A., Harper M. M., Smith J. D., T and B lymphocytes play a minor role in atherosclerotic plaque formation in the apolipoprotein E-deficient mouse, 10.1073/pnas.94.9.4642
  4. Daugherty A, Puré E, Delfel-Butteiger D, Chen S, Leferovich J, Roselaar S E, Rader D J, The effects of total lymphocyte deficiency on the extent of atherosclerosis in apolipoprotein E-/- mice., 10.1172/jci119681
  5. DiLillo D. J., Hamaguchi Y., Ueda Y., Yang K., Uchida J., Haas K. M., Kelsoe G., Tedder T. F., Maintenance of Long-Lived Plasma Cells and Serological Memory Despite Mature and Memory B Cell Depletion during CD20 Immunotherapy in Mice, 10.4049/jimmunol.180.1.361
  6. Fisson Sylvain, Darrasse-Jèze Guillaume, Litvinova Elena, Septier Franck, Klatzmann David, Liblau Roland, Salomon Benoît L., Continuous Activation of Autoreactive CD4+CD25+Regulatory T Cells in the Steady State, 10.1084/jem.20030686
  7. Friguet Bertrand, Chaffotte Alain F., Djavadi-Ohaniance Lisa, Goldberg Michel E., Measurements of the true affinity constant in solution of antigen-antibody complexes by enzyme-linked immunosorbent assay, 10.1016/0022-1759(85)90044-4
  8. Gupta S, Pablo A M, Jiang X c, Wang N, Tall A R, Schindler C, IFN-gamma potentiates atherosclerosis in ApoE knock-out mice., 10.1172/jci119465
  9. Hamaguchi Y., Uchida J., Cain D. W., Venturi G. M., Poe J. C., Haas K. M., Tedder T. F., The Peritoneal Cavity Provides a Protective Niche for B1 and Conventional B Lymphocytes during Anti-CD20 Immunotherapy in Mice, 10.4049/jimmunol.174.7.4389
  10. Hansson Göran K., Libby Peter, The immune response in atherosclerosis: a double-edged sword, 10.1038/nri1882
  11. Hernandez-Vargas P., Ortiz-Munoz G., Lopez-Franco O., Suzuki Y., Gallego-Delgado J., Sanjuan G., Lazaro A., Lopez-Parra V., Ortega L., Egido J., Gomez-Guerrero C., Fc  Receptor Deficiency Confers Protection Against Atherosclerosis in Apolipoprotein E Knockout Mice, 10.1161/01.res.0000250556.07796.6c
  12. Ait-Oufella Hafid, Salomon Benoît L, Potteaux Stéphane, Robertson Anna-Karin L, Gourdy Pierre, Zoll Joffrey, Merval Régine, Esposito Bruno, Cohen José L, Fisson Sylvain, Flavell Richard A, Hansson Göran K, Klatzmann David, Tedgui Alain, Mallat Ziad, Natural regulatory T cells control the development of atherosclerosis in mice, 10.1038/nm1343
  13. Joao C., Ogle B. M., Gay-Rabinstein C., Platt J. L., Cascalho M., B Cell-Dependent TCR Diversification, 10.4049/jimmunol.172.8.4709
  14. Karvonen J., Immunoglobulin M Type of Autoantibodies to Oxidized Low-Density Lipoprotein Has an Inverse Relation to Carotid Artery Atherosclerosis, 10.1161/01.cir.0000092891.55157.a7
  15. Lewis M. J., Malik T. H., Ehrenstein M. R., Boyle J. J., Botto M., Haskard D. O., Immunoglobulin M Is Required for Protection Against Atherosclerosis in Low-Density Lipoprotein Receptor-Deficient Mice, 10.1161/circulationaha.109.868158
  16. Major A. S., B-Lymphocyte Deficiency Increases Atherosclerosis in LDL Receptor-Null Mice, 10.1161/01.atv.0000039169.47943.ee
  17. McGeachy Mandy J, Bak-Jensen Kristian S, Chen Yi, Tato Cristina M, Blumenschein Wendy, McClanahan Terrill, Cua Daniel J, TGF-β and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain TH-17 cell–mediated pathology, 10.1038/ni1539
  18. Miller Ashley M., Xu Damo, Asquith Darren L., Denby Laura, Li Yubin, Sattar Naveed, Baker Andrew H., McInnes Iain B., Liew Foo Y., IL-33 reduces the development of atherosclerosis, 10.1084/jem.20071868
  19. Moos M. P.W., The Lamina Adventitia Is the Major Site of Immune Cell Accumulation in Standard Chow-Fed Apolipoprotein E-Deficient Mice, 10.1161/01.atv.0000187470.31662.fe
  20. Moulin Véronique, Andris Fabienne, Thielemans Kris, Maliszewski Charlie, Urbain Jacques, Moser Muriel, B Lymphocytes Regulate Dendritic Cell (Dc) Function in Vivo : Increased Interleukin 12 Production by DCs from B Cell–Deficient Mice Results in T Helper Cell Type 1 Deviation, 10.1084/jem.192.4.475
  21. Ngo Vu N., Cornall Richard J., Cyster Jason G., Splenic T Zone Development Is B Cell Dependent, 10.1084/jem.194.11.1649
  22. O'Connor Jr William, Kamanaka Masahito, Booth Carmen J, Town Terrence, Nakae Susumu, Iwakura Yoichiro, Kolls Jay K, Flavell Richard A, A protective function for interleukin 17A in T cell–mediated intestinal inflammation, 10.1038/ni.1736
  23. Palinski W., Ord V. A., Plump A. S., Breslow J. L., Steinberg D., Witztum J. L., ApoE-deficient mice are a model of lipoprotein oxidation in atherogenesis. Demonstration of oxidation-specific epitopes in lesions and high titers of autoantibodies to malondialdehyde-lysine in serum, 10.1161/01.atv.14.4.605
  24. Aubry Marie-Christine, Riehle Darren L, Edwards William D, Maradit-Kremers Hilal, Roger Veronique L, Sebo Thomas J, Gabriel Sherine E, B-Lymphocytes in plaque and adventitia of coronary arteries in two patients with rheumatoid arthritis and coronary atherosclerosis, 10.1016/j.carpath.2004.02.005
  25. Palinski W, Hörkkö S, Miller E, Steinbrecher U P, Powell H C, Curtiss L K, Witztum J L, Cloning of monoclonal autoantibodies to epitopes of oxidized lipoproteins from apolipoprotein E-deficient mice. Demonstration of epitopes of oxidized low density lipoprotein in human plasma., 10.1172/jci118853
  26. Roman Mary J., Salmon Jane E., Sobel Rachel, Lockshin Michael D., Sammaritano Lisa, Schwartz Joseph E., Devereux Richard B., Prevalence and relation to risk factors of carotid atherosclerosis and left ventricular hypertrophy in systemic lupus erythematosus and antiphospholipid antibody syndrome, 10.1016/s0002-9149(00)01453-3
  27. Shaw Peter X., Hörkkö Sohvi, Chang Mi-Kyung, Curtiss Linda K., Palinski Wulf, Silverman Gregg J., Witztum Joseph L., Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity, 10.1172/jci8472
  28. Smith J. D., Trogan E., Ginsberg M., Grigaux C., Tian J., Miyata M., Decreased atherosclerosis in mice deficient in both macrophage colony-stimulating factor (op) and apolipoprotein E., 10.1073/pnas.92.18.8264
  29. Taleb S., Herbin O., Ait-Oufella H., Verreth W., Gourdy P., Barateau V., Merval R., Esposito B., Clement K., Holvoet P., Tedgui A., Mallat Z., Defective Leptin/Leptin Receptor Signaling Improves Regulatory T Cell Immune Response and Protects Mice From Atherosclerosis, 10.1161/atvbaha.107.149567
  30. Taleb Soraya, Romain Mélissa, Ramkhelawon Bhama, Uyttenhove Catherine, Pasterkamp Gerard, Herbin Olivier, Esposito Bruno, Perez Nicolas, Yasukawa Hideo, Van Snick Jacques, Yoshimura Akihiko, Tedgui Alain, Mallat Ziad, Loss of SOCS3 expression in T cells reveals a regulatory role for interleukin-17 in atherosclerosis, 10.1084/jem.20090545
  31. Tedgui A., Cytokines in Atherosclerosis: Pathogenic and Regulatory Pathways, 10.1152/physrev.00024.2005
  32. Tsimikas Sotirios, Brilakis Emmanouil S., Lennon Ryan J., Miller Elizabeth R., Witztum Joseph L., McConnell Joseph P., Kornman Kenneth S., Berger Peter B., Relationship of IgG and IgM autoantibodies to oxidized low density lipoprotein with coronary artery disease and cardiovascular events, 10.1194/jlr.m600361-jlr200
  33. Uchida Junji, Hamaguchi Yasuhito, Oliver Julie A., Ravetch Jeffrey V., Poe Jonathan C., Haas Karen M., Tedder Thomas F., The Innate Mononuclear Phagocyte Network Depletes B Lymphocytes through Fc Receptor–dependent Mechanisms during Anti-CD20 Antibody Immunotherapy, 10.1084/jem.20040119
  34. Uchida J., Mouse CD20 expression and function, 10.1093/intimm/dxh009
  35. Binder Christoph J., Chang Mi-Kyung, Shaw Peter X., Miller Yury I., Hartvigsen Karsten, Dewan Asheesh, Witztum Joseph L., Innate and acquired immunity in atherogenesis, 10.1038/nm1102-1218
  36. Uyttenhove Catherine, Van Snick Jacques, Development of an anti-IL-17A auto-vaccine that prevents experimental auto-immune encephalomyelitis, 10.1002/eji.200636662
  37. UYTTENHOVE C., SOMMEREYNS C., THEATE I., MICHIELS T., VAN SNICK J., Anti-IL-17A Autovaccination Prevents Clinical and Histological Manifestations of Experimental Autoimmune Encephalomyelitis, 10.1196/annals.1423.035
  38. Yanaba Koichi, Bouaziz Jean-David, Haas Karen M., Poe Jonathan C., Fujimoto Manabu, Tedder Thomas F., A Regulatory B Cell Subset with a Unique CD1dhiCD5+ Phenotype Controls T Cell-Dependent Inflammatory Responses, 10.1016/j.immuni.2008.03.017
  39. Zhou X., Nicoletti A., Elhage R., Hansson G. K., Transfer of CD4+ T Cells Aggravates Atherosclerosis in Immunodeficient Apolipoprotein E Knockout Mice, 10.1161/01.cir.102.24.2919
  40. Binder Christoph J, Hörkkö Sohvi, Dewan Asheesh, Chang Mi-Kyung, Kieu Emily P, Goodyear Carl S, Shaw Peter X, Palinski Wulf, Witztum Joseph L, Silverman Gregg J, Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL, 10.1038/nm876
  41. Binder Christoph J., Hartvigsen Karsten, Chang Mi-Kyung, Miller Marina, Broide David, Palinski Wulf, Curtiss Linda K., Corr Maripat, Witztum Joseph L., IL-5 links adaptive and natural immunity specific for epitopes of oxidized LDL and protects from atherosclerosis, 10.1172/jci200420479
  42. Bouaziz J.-D., Yanaba K., Venturi G. M., Wang Y., Tisch R. M., Poe J. C., Tedder T. F., Therapeutic B cell depletion impairs adaptive and autoreactive CD4+ T cell activation in mice, 10.1073/pnas.0709205105
  43. Buono C., Binder C. J., Stavrakis G., Witztum J. L., Glimcher L. H., Lichtman A. H., T-bet deficiency reduces atherosclerosis and alters plaque antigen-specific immune responses, 10.1073/pnas.0409015102
  44. Caligiuri G., Protective immunity against atherosclerosis carried by B cells of hypercholesterolemic mice, 10.1172/jci200207272
Bibliographic reference Ait-Oufella, Hafid ; Herbin, Olivier ; Bouaziz, Jean-David ; Binder, Christoph J. ; Uyttenhove, Catherine ; et. al. B cell depletion reduces the development of atherosclerosis in mice. In: The Journal of Experimental Medicine, Vol. 207, no. 8, p. 1579-1587 (2010)
Permanent URL http://hdl.handle.net/2078.1/33605