Heat-shock protein 90: A novel autoantigen in human carotid atherosclerosis

Atherosclerosis

Volumn 207, Issue 1, 2009, Pages 74-83

  Businaro, Rita ^a   Profumo, Elisabetta ^b   Tagliani, Angela ^a   Buttari, Brigitta ^b   Leone, Stefano ^c   D'Amati, Giulia ^d   Ippoliti, Flora ^d   Leopizzi, Martina ^d   D'Arcangelo, Daniela ^e   Capoano, Raffaele ^a   Fumagalli, Lorenzo ^a   Salvati, Bruno ^a   Riganò, Rachele ^b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c ROMA TRE UNIVERSITY   (Italy)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

Author keywords

Antibodies; Atherosclerosis; Carotid plaque; Heat shock protein 90; T lymphocytes

Indexed keywords

AUTOANTIGEN; CYTOKINE; GAMMA INTERFERON; HEAT SHOCK PROTEIN 90; INTERLEUKIN 4; PARAFFIN; PROTEIN ANTIBODY;

ADULT; AGED; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CAROTID ATHEROSCLEROSIS; CELL ISOLATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFLAMMATORY INFILTRATE; LYMPHOCYTE ACTIVATION; MALE; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE; TH1 CELL; TH2 CELL;

AGED; AGED, 80 AND OVER; AUTOANTIBODIES; AUTOANTIGENS; CAROTID ARTERY DISEASES; CASE-CONTROL STUDIES; CELL PROLIFERATION; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HSP90 HEAT-SHOCK PROTEINS; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; INTERFERON-GAMMA; INTERLEUKIN-4; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; T-LYMPHOCYTES;

EID: 70350566676     PISSN: 00219150     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.atherosclerosis.2009.04.026     Document Type: Article

References (48)

1. Wick G., Knoflach M., and Xu Q. Autoimmune and inflammatory mechanisms in atherosclerosis. Annu Rev Immunol 22 (2004) 361-403
2. Margutti P., Delunardo F., Sorice M., et al. Screening of a HUAEC cDNA library identifies actin as a candidate autoantigen associated with carotid atherosclerosis. Clin Exp Immunol 137 (2004) 209-215
3. Pockley A.G., and Frostegard J. Heat shock proteins in cardiovascular disease and the prognostic value of heat shock protein related measurements. Heart 91 (2005) 1124-1126
4. Mehta T.A., Greenman J., Ettelaie C., Venkatasubramaniam A., Chetter I.C., and McCollum P.T. Heat shock proteins in vascular disease - a review. Eur J Vasc Endovasc Surg 29 (2005) 395-402
5. Wick G. The heat is on: heat-shock proteins and atherosclerosis. Circulation 114 (2006) 870-872
6. Tsan M.F., and Gao B. Heat shock protein and innate immunity. Cell Mol Immunol 1 (2004) 274-279
7. Pockley A.G. Heat shock proteins, inflammation, and cardiovascular disease. Circulation 105 (2002) 1012-1017
8. Park H.K., Park E.-C., Bae S.W., et al. Expression of heat shock protein 27 in human atherosclerotic plaques and increased plasma level of heat shock protein 27 in patients with acute coronary syndrome. Circulation 114 (2006) 886-893
9. Biasucci L.M., Liuzzo G., Ciervo A., et al. Antibody response to chlamydial heat shock protein 60 is strongly associated with acute coronary syndromes. Circulation 107 (2003) 3015-3017
10. Benagiano M., D'Elios M.M., Amedei A., et al. Human 60-kDa heat shock protein is a target autoantigen of T cells derived from atherosclerotic plaques. J Immunol 174 (2005) 6509-6517
11. Binder C.J., Horkko S., Dewan A., et al. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat Med 9 (2003) 736-743
12. Sreedhar A.S., Kalmar E., Csermely P., and Shen Y.F. Hsp90 isoforms: functions, expression and clinical importance. FEBS Lett 562 (2004) 11-15
13. Liao D.F., Jin Z.G., Baas A.S., et al. Purification and identification of secreted oxidative stress-induced factors from vascular smooth muscle cells. J Biol Chem 275 (2000) 189-196
14. Terasawa K., Minami M., and Minami Y. Constantly updated knowledge of Hsp90. J Biochem (Tokyo) 137 (2005) 443-447
15. Panaretou B., Sinclair K., Prodromou C., et al. The Hsp90 of Candida albicans can confer Hsp90 functions in Saccharomyces cerevisiae: a potential model for the processes that generate immunogenic fragments of this molecular chaperone in C. albicans infections. Microbiology 145 (1999) 3455-3463
16. Hayem G., De Bandt M., Palazzo E., et al. Anti-heat shock protein 70 kDa and 90 kDa antibodies in serum of patients with rheumatoid arthritis. Ann Rheum Dis 58 (1999) 291-296
17. Qin H.Y., Mahon J.L., Atkinson M.A., et al. Type 1 diabetes alters anti-hsp90 autoantibody isotype. J Autoimmun 20 (2003) 237-245
18. Riganò R., Profumo E., Buttari B., et al. Heat shock proteins and autoimmunity in patients with carotid atherosclerosis. Ann N Y Acad Sci 1107 (2007) 1-10
19. Stary H.C., Chandler A.B., Dinsmore R.E., et al. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler Thromb Vasc Biol 15 (1995) 1512-1531
20. Benagiano M., Azzurri A., Ciervo A., et al. T helper type 1 lymphocytes drive inflammation in human atherosclerotic lesions. Proc Natl Acad Sci USA 100 (2003) 6658-6663
21. Stummvoll G.H., Fritsch R.D., Meyer B., Hoefler E., Aringer M., Smolen J.S., and Steiner G. Characterization of cellular and humoral autoimmune responses to histone H1 and core histones in human systemic lupus erythematosus. Ann Rheum Dis 68 (2009) 110-116
22. Fritsch R., Eselböck D., Skriner K., et al. Characterization of autoreactive T cells to the autoantigens heterogeneous nuclear ribonucleoprotein A2 (RA33) and filaggrin in patients with rheumatoid arthritis. J Immunol 169 (2002) 1068-1076
23. Profumo E., Esposito C., Buttari B., et al. Intracellular expression of cytokines in peripheral blood from patients with atherosclerosis before and after carotid endarterectomy. Atherosclerosis 191 (2007) 340-347
24. Erkeller-Yuksel F.M., Isenberg D.A., Dhillon V.B., Latchman D.S., and Lydyard P.M. Surface expression of heat shock protein 90 by blood mononuclear cells from patients with systemic lupus erythematosus. J Autoimmun 5 (1992) 803-814
25. Stemme S., Faber B., Holm J., Wiklund O., Witztum J.L., and Hansson G.K. T lymphocytes from human atherosclerotic plaques recognize oxidized low density lipoprotein. Proc Natl Acad Sci USA 92 (1995) 3893-3897
26. Choi J.I., Chung S.W., Kang H.S., Rhim B.Y., Kim S.J., and Kim S.J. Establishment of Porphyromonas gingivalis heat-shock-protein-specific T-cell lines from atherosclerosis patients. J Dent Res 81 (2002) 344-348
27. Ford P., Gemmell E., Walker P., West M., Cullinan M., and Seymour G. Characterization of heat shock protein-specific T cells in atherosclerosis. Clin Diagn Lab Immunol 12 (2005) 259-267
28. Keller T.T., van der Meer J.J., Teeling P., et al. Selective expansion of influenza A virus-specific T cells in symptomatic human carotid artery atherosclerotic plaques. Stroke 39 (2008) 174-179
29. Jonasson L., Holm J., Skalli O., Bondjers G., and Hansson G.K. Regional accumulations of T cells, macrophages, and smooth muscle cells in the human atherosclerotic plaque. Arteriosclerosis 6 2 (1986) 131-138
30. de Boer O.J., Becker A.E., and van der Wal A.C. T lymphocytes in atherogenesis-functional aspects and antigenic repertoire. Cardiovasc Res 60 1 (2003) 78-86
31. van der Wal A.C., Das P.K., Bentz van de Berg D., van der Loos C.M., and Becker A.E. Atherosclerotic lesions in humans. In situ immunophenotypic analysis suggesting an immune mediated response. Lab Invest 61 2 (1989) 166-170
32. George Y., Shoenfeld Y., Gilburd B., Afek A., Shaish A., and Harats D. Requisite role for interleukin-4 in the acceleration of fatty streaks induced by Heat Shock Protein 65 or Mycobacterium tuberculosis. Circ Res 86 (2000) 1203-1210
33. King V.L., Szilvassy S.J., and Daugherty A. Interleukin-4 deficiency decreases atherosclerotic lesion formation in a site-specific manner in female LDL receptor-/- mice. Arterioscler Thromb Vasc Biol 22 (2002) 456-461
34. Binder R.J., Vatner R., and Srivastava P. The heat-shock protein receptors: some answers and more questions. Tissue Antigens 64 (2004) 442-451
35. Hart J.P., Gunn M.D., and Pizzo S.V. A CD91-positive subset of CD11c+ blood dendritic cells: characterization of the APC that functions to enhance adaptive immune responses against CD91-targeted antigens. J Immunol 172 (2004) 70-78
36. Vabulas R.M., Braedel S., Hilf N., et al. The endoplasmic reticulum-resident heat shock protein Gp96 activates dendritic cells via the Toll-like receptor 2/4 pathway. J Biol Chem 277 (2002) 20847-20853
37. Ayada K., Yokota K., Kobayashi K., et al. Chronic infections and atherosclerosis. Ann N Y Acad Sci 1108 (2007) 594-602
38. Xu Q., Dietrich H., Steiner H.J., et al. Induction of arteriosclerosis in normocholesterolemic rabbits by immunization with heat shock protein 65. Arterioscler Thromb 12 (1992) 789-799
39. George J., Shoenfeld Y., Afek A., et al. Enhanced fatty streak formation in C57BL/6J mice by immunization with heat shock protein-65. Arterioscler Thromb Vasc Biol 19 (1999) 505-510
40. Afek A., George J., Gilburd B., et al. Immunization of low-density lipoprotein receptor deficient (LDL-RD) mice with heat shock protein 65 (HSP-65) promotes early atherosclerosis. J Autoimmun 14 (2000) 115-121
41. George J., Afek A., Gilburd B., Shoenfeld Y., and 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 38 (2001) 900-905
42. Harats D., Yacov N., Gilburd B., Shoenfeld Y., and George J. Oral tolerance with heat shock protein 65 attenuates Mycobacterium tuberculosis-induced and high-fat-diet-driven atherosclerotic lesions. J Am Coll Cardiol 40 (2002) 1333-1338
43. Xu Q., Willeit J., Marosi M., et al. Association of serum antibodies to heat-shock protein 65 with carotid atherosclerosis. Lancet 341 (1993) 255-259
44. Hoppichler F., Lechleitner M., Traweger C., et al. Changes of serum antibodies to heat-shock protein 65 in coronary heart disease and acute myocardial infarction. Atherosclerosis 126 (1996) 333-338
45. Alard J.E., Dueymes M., Youinou P., and Jamin C. Modulation of endothelial cell damages by anti-Hsp60 autoantibodies in systemic autoimmune diseases. Autoimmun Rev 6 (2007) 438-443
46. Okada T., Ayada K., Usui S., et al. Antibodies against heat shock protein 60 derived from Helicobacter pylori: diagnostic implications in cardiovascular disease. J Autoimmun 29 (2007) 106-115
47. Jin Z.G., Melaragno M.G., Liao D.F., et al. A is a secreted growth factor induced by oxidative stress. Circ Res 87 (2000) 789-796
48. Liu D.H., Yuan H.Y., Cao C.Y., et al. Heat shock protein 90 acts as a molecular chaperone in late-phase activation of extracellular signal-regulated kinase 1/2 stimulated by oxidative stress in vascular smooth muscle cells. Acta Pharmacol Sin 28 (2007) 1907-1913