Subcutaneous immunization with heat shock protein-65 reduces atherosclerosis in Apoe -/- mice

Immunobiology

Volumn 217, Issue 5, 2012, Pages 540-547

  Klingenberg, Roland ^a   Ketelhuth, Daniel F J ^a   Strodthoff, Daniela ^a   Gregori, Silvia ^b   Hansson, Göran K ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b SAN RAFFAELE SCIENTIFIC INSTITUTE   (Italy)

Author keywords

Atherosclerosis; Immune system; Immunomodulation; Leukocytes; Vascular biology

Indexed keywords

ALUMINUM HYDROXIDE; APOLIPOPROTEIN E; CD4 ANTIGEN; CD45RB ANTIGEN; CHOLESTEROL; GAMMA INTERFERON; HEAT SHOCK PROTEIN 65; IMMUNOGLOBULIN G2A; INTERLEUKIN 17; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CD45RB; TRANSCRIPTION FACTOR FOXP3; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY TITER; ANTIGEN EXPRESSION; AORTA ROOT; ARTICLE; ATHEROSCLEROSIS; B LYMPHOCYTE; BODY WEIGHT; CD4+ T LYMPHOCYTE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; FEMALE; FOOD INTAKE; HUMORAL IMMUNITY; LEUKOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TREATMENT OUTCOME; TRIACYLGLYCEROL BLOOD LEVEL;

ADJUVANTS, IMMUNOLOGIC; ALUM COMPOUNDS; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD45; APOLIPOPROTEINS E; ATHEROSCLEROSIS; DISEASE MODELS, ANIMAL; FEMALE; HEAT-SHOCK PROTEINS; HYPERCHOLESTEROLEMIA; IMMUNOTHERAPY, ACTIVE; MICE; MICE, KNOCKOUT;

EID: 84858797859     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2011.06.006     Document Type: Article

References (39)

1. Afek A., George J., Gilburd B., Rauova L., Goldberg I., Kopolovic J., Harats D., Shoenfeld Y. Immunization of low-density lipoprotein receptor deficient (LDL-RD) mice with heat shock protein 65 (HSP-65) promotes early atherosclerosis. J. Autoimmun. 2000, 14:115.
2. Ait-Oufella H., Salomon B.L., Potteaux S., Robertson A.K., Gourdy P., Zoll J., Merval R., Esposito B., Cohen J.L., Fisson S., Flavell R.A., Hansson G.K., Klatzmann D., Tedgui A., Mallat Z. Natural regulatory T cells control the development of atherosclerosis in mice. Nat. Med. 2006, 12:178.
3. Binder C.J., Horkko S., Dewan A., Chang M.K., Kieu E.P., Goodyear C.S., Shaw P.X., Palinski W., Witztum J.L., Silverman G.J. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat. Med. 2003, 9:736.
4. Bulut Y., Michelsen K.S., Hayrapetian L., Naiki Y., Spallek R., Singh M., Arditi M. Mycobacterium tuberculosis heat shock proteins use diverse Toll-like receptor pathways to activate pro-inflammatory signals. J. Biol. Chem. 2005, 280:20961.
5. Cohen-Sfady M., Nussbaum G., Pevsner-Fischer M., Mor F., Carmi P., Zanin-Zhorov A., Lider O., Cohen I.R. Heat shock protein 60 activates B cells via the TLR4-MyD88 pathway. J. Immunol. 2005, 175:3594.
6. Fredrikson G.N., Bjorkbacka H., Soderberg I., Ljungcrantz I., Nilsson J. Treatment with apo B peptide vaccines inhibits atherosclerosis in human apo B-100 transgenic mice without inducing an increase in peptide-specific antibodies. J. Intern. Med. 2008, 264:563.
7. George J., Shoenfeld Y., Afek A., Gilburd B., Keren P., Shaish A., Kopolovic J., Wick G., Harats D. Enhanced fatty streak formation in C57BL/6J mice by immunization with heat shock protein-65. Arterioscler. Thromb. Vasc. Biol. 1999, 19:505.
8. George J., Shoenfeld Y., Gilburd B., Afek A., Shaish A., Harats D. Requisite role for interleukin-4 in the acceleration of fatty streaks induced by heat shock protein 65 or Mycobacterium tuberculosis. Circ. Res. 2000, 86:1203.
9. George J., Afek A., Gilburd B., Shoenfeld Y., Harats D. Cellular and humoral immune responses to heat shock protein 65 are both involved in promoting fatty-streak formation in LDL-receptor deficient mice. J. Am. Coll. Cardiol. 2001, 38:900.
10. Gregori S., Mangia P., Bacchetta R., Tresoldi E., Kolbinger F., Traversari C., Carballido J.M., de Vries J.E., Korthauer U., Roncarolo M.G. An anti-CD45RO/RB monoclonal antibody modulates T cell responses via induction of apoptosis and generation of regulatory T cells. J. Exp. Med. 2005, 201:1293.
11. Hansen P.R., Chew M., Zhou J., Daugherty A., Heegaard N., Jensen P., Mouritsen S., Falk E. Freunds adjuvant alone is antiatherogenic in apoE-deficient mice and specific immunization against TNFalpha confers no additional benefit. Atherosclerosis 2001, 158:87.
12. Hansson G.K., Hermansson A. The immune system in atherosclerosis. Nat. Immunol. 2011, 12:204.
13. Harats D., Yacov N., Gilburd B., Shoenfeld Y., George J. Oral tolerance with heat shock protein 65 attenuates Mycobacterium tuberculosis-induced and high-fat-diet-driven atherosclerotic lesions. J. Am. Coll. Cardiol. 2002, 40:1333.
14. Henderson B., Pockley A.G. Molecular chaperones and protein-folding catalysts as intercellular signaling regulators in immunity and inflammation. J. Leukoc. Biol. 2010, 88:445.
15. Holmgren J., Czerkinsky C. Mucosal immunity and vaccines. Nat. Med. 2005, 11:S45.
16. Khallou-Laschet J., Tupin E., Caligiuri G., Poirier B., Thieblemont N., Gaston A.T., Vandaele M., Bleton J., Tchapla A., Kaveri S.V., Rudling M., Nicoletti A. Atheroprotective effect of adjuvants in apolipoprotein E knockout mice. Atherosclerosis 2006, 184:330.
17. Klingenberg R., Lebens M., Hermansson A., Fredrikson G.N., Strodthoff D., Rudling M., Ketelhuth D.F., Gerdes N., Holmgren J., Nilsson J., Hansson G.K. Intranasal immunization with an apolipoprotein B-100 fusion protein induces antigen-specific regulatory T cells and reduces atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2010, 30:946.
18. Li H., Nookala S., Re F. Aluminum hydroxide adjuvants activate caspase-1 and induce IL-1beta and IL-18 release. J. Immunol. 2007, 178:5271.
19. Luke P.P., Deng J.P., Lian D., O'Connell P.J., Garcia B., Jevnikar A.M., Zhong R. Prolongation of allograft survival by administration of anti-CD45RB monoclonal antibody is due to alteration of CD45RBhi: CD45RBlo T-cell proportions. Am. J. Transplant. 2006, 6:2023.
20. Maron R., Sukhova G., Faria A.M., Hoffmann E., Mach F., Libby P., Weiner H.L. Mucosal administration of heat shock protein-65 decreases atherosclerosis and inflammation in aortic arch of low-density lipoprotein receptor-deficient mice. Circulation 2002, 106:1708.
21. Matsutake T., Sawamura T., Srivastava P.K. High efficiency CD91- and LOX-1-mediated re-presentation of gp96-chaperoned peptides by MHC II molecules. Cancer Immun. 2010, 10:7.
22. Nakashima Y., Plump A.S., Raines E.W., Breslow J.L., Ross R. ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler. Thromb. 1994, 14:133.
23. Paigen B., Ishida B.Y., Verstuyft J., Winters R.B., Albee D. Atherosclerosis susceptibility differences among progenitors of recombinant inbred strains of mice. Arteriosclerosis 1990, 10:316.
24. Peetermans W.E., Raats C.J., Langermans J.A., van Furth R. Mycobacterial heat-shock protein 65 induces proinflammatory cytokines but does not activate human mononuclear phagocytes. Scand. J. Immunol. 1994, 39:613.
25. Powrie F., Correa-Oliveira R., Mauze S., Coffman R.L. Regulatory interactions between CD45RBhigh and CD45RBlow CD4+ T cells are important for the balance between protective and pathogenic cell-mediated immunity. J. Exp. Med. 1994, 179:589.
26. Powrie F., Carlino J., Leach M.W., Mauze S., Coffman R.L. A critical role for transforming growth factor-beta but not interleukin 4 in the suppression of T helper type 1-mediated colitis by CD45RB(low) CD4+ T cells. J. Exp. Med. 1996, 183:2669.
27. Pulendran B. Modulating TH1/TH2 responses with microbes, dendritic cells, and pathogen recognition receptors. Immunol. Res. 2004, 29:187.
28. Pulendran B., Ahmed R. Translating innate immunity into immunological memory: implications for vaccine development. Cell 2006, 124:849.
29. Quintana F.J., Carmi P., Mor F., Cohen I.R. Inhibition of adjuvant arthritis by a DNA vaccine encoding human heat shock protein 60. J. Immunol. 2002, 169:3422.
30. Rha Y.H., Taube C., Haczku A., Joetham A., Takeda K., Duez C., Siegel M., Aydintug M.K., Born W.K., Dakhama A., Gelfand E.W. Effect of microbial heat shock proteins on airway inflammation and hyperresponsiveness. J. Immunol. 2002, 169:5300.
31. Srivastava P. Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Annu. Rev. Immunol. 2002, 20:395.
32. Stary H.C., Chandler B., Glagov S., Guyton J.R., Insull W., Rosenfeld M.E., Schaffer S.A., Schwartz C.J., Wagner W.D., Wissler R.W. A definition of initial, fatty streak, and intermediate lesions of atherosclerosis. A report from the committee on vascular lesions of the Council on Arteriosclerosis, American Heart Association. Circulation 1994, 89:2462.
33. Tabas I., Williams K.J., Boren J. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation 2007, 116:1832.
34. Ten Hove T., The Olle F., Berkhout M., Bruggeman J.P., Vyth-Dreese F.A., Slors J.F., Van Deventer S.J., Te Velde A.A. Expression of CD45RB functionally distinguishes intestinal T lymphocytes in inflammatory bowel disease. J. Leukoc. Biol. 2004, 75:1010.
35. Trowbridge I.S., Thomas M.L. CD45: an emerging role as a protein tyrosine phosphatase required for lymphocyte activation and development. Annu. Rev. Immunol. 1994, 12:85.
36. van Puijvelde G.H., van Es T., van Wanrooij E.J., Habets K.L., de Vos P., van der Zee R., van Eden W., van Berkel T.J., Kuiper J. Induction of oral tolerance to HSP60 or an HSP60-peptide activates T cell regulation and reduces atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2007, 27:2677.
37. Verdegaal M.E., Zegveld S.T., van Furth R. Heat shock protein 65 induces CD62e CD106, and CD54 on cultured human endothelial cells and increases their adhesiveness for monocytes and granulocytes. J. Immunol. 1996, 157:369.
38. Wigren M., Bengtsson D., Duner P., Olofsson K., Bjorkbacka H., Bengtsson E., Fredrikson G.N., Nilsson J. Atheroprotective effects of Alum are associated with capture of oxidized LDL antigens and activation of regulatory T cells. Circ. Res. 2009, 104:e62.
39. Xu Q., Kleindienst R., Waitz W., Dietrich H., Wick G. Increased expression of heat shock protein 65 coincides with a population of infiltrating T lymphocytes in atherosclerotic lesions of rabbits specifically responding to heat shock protein 65. J. Clin. Invest. 1993, 91:2693.