Regulation of cellular immunity prevents Helicobacter pylori-induced atherosclerosis

Lupus

Volumn 18, Issue 13, 2009, Pages 1154-1168

  Ayada, K ^a   Yokota, K ^b   Hirai, K ^a   Fujimoto, K ^a   Kobayashi, K ^a   Ogawa, H ^a   Hatanaka, K ^a   Hirohata, S ^a   Yoshino, T ^a   Shoenfeld, Y ^c,d   Matsuura, Eiji ^a   Oguma, K ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c SHEBA MEDICAL CENTER   (Israel)

^d TEL AVIV UNIVERSITY   (Israel)

Author keywords

Atherosclerosis; Autoimmunity; Heat shock protein 60 (HSP60); Helicobacter pylori (H. pylori; Hp); Transendothelial migration

Indexed keywords

ANTIBIOTIC AGENT; HEAT SHOCK PROTEIN 60;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CELL MIGRATION; CELLULAR IMMUNITY; CHEMOTAXIS; CONTROLLED STUDY; DISEASE ASSOCIATION; ENDOTHELIUM CELL; ERADICATION THERAPY; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HETEROZYGOSITY; IMMUNIZATION; LIPID DIET; LYMPHOCYTE DIFFERENTIATION; MALE; MOUSE; MOUTH INFECTION; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TH1 CELL;

ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CELL MOVEMENT; CHAPERONIN 60; CHEMOKINES; DIETARY FATS; ENDOTHELIAL CELLS; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; IMMUNITY, CELLULAR; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, CXCR3; RECEPTORS, LDL; TH1 CELLS;

EID: 71049183037     PISSN: 09612033     EISSN: None     Source Type: Journal    
DOI: 10.1177/0961203309106600     Document Type: Article

References (74)

1. Ross R. Atherosclerosis - an inflammatory disease. N Engl J Med 1999; 340: 115-126.
2. Libby P. Inflammation in atherosclerosis. Nature 2002; 420: 868-874.
3. Saikku P., Leinonen M., Mattila K., et al. Serological evidence of an association of a novel Chlamydia, TWAR, with chronic coronary heart disease and acute myocardial infarction. Lancet 1988; 2: 983-986.
4. Altannavch T., Roubalova K., Broz J., Hruba D., Andel M. Serological markers of Chlamydia pneumoniae, cytomegalovirus and Helicobacter pylori infection in diabetic and non-diabetic patients with unstable angina pectoris. Cent Eur J Public Health 2003; 11: 102-106.
5. Epstein SE, Zhou YF, Zhu J. Infection and atherosclerosis: Emerging mechanistic paradigms. Circulation 1999; 100: E20-e28.
6. Erkkila L., Laitinen K., Haasio K., et al. Heat shock protein 60 autoimmunity and early lipid lesions in cholesterol-fed C57BL/6JBom mice during Chlamydia pneumoniae infection. Atherosclerosis 2004; 177: 321-328.
7. Choi JI, Chung SW, Kang HS, Rhim BY, Kim SJ, Kim SJ Establishment of Porphyromonas gingivalis heat-shock-protein-specific T-cell lines from atherosclerosis patients. J Dent Res 2002; 81: 344-348.
8. Bason C., Corrocher R., Lunardi C., et al. Interaction of antibodies against cytomegalovirus with heat-shock protein 60 in pathogenesis of atherosclerosis. Lancet 2003; 362: 1971-1977.
9. 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: 1333-1338.
10. Braig K., Otwinowski Z., Hegde R., et al. The crystal structure of the bacterial chaperonin GroEL at 2.8 A. Nature 1994; 371: 578-586.
11. Xu Z., Horwich AL, Sigler PB The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature 1997; 388: 741-750.
12. Jindal S., Dudani AK, Singh B., Harley CB, Gupta RS Primary structure of a human mitochondrial protein homologous to the bacterial and plant chaperonins and to the 65-kilodalton mycobacterial antigen. Mol Cell Biol 1989; 9: 2279-2283.
13. Sobel DO, Creswell K. Characterization of anti-islet cytotoxic human T-cell clones from patients with type 1 diabetes mellitus. Autoimmunity 2006; 39: 323-332.
14. Yin Ji X., Kang MR, Choi JS, et al. Levels of intra- and extracellular heat shock protein 60 in Kawasaki disease patients treated with intravenous immunoglobulin. Clin Immunol 2007; 124: 304-310.
15. Imamura Y., Kurokawa MS, Yoshikawa H., et al. Involvement of Th1 cells and heat shock protein 60 in the pathogenesis of intestinal Behcet's disease. Clin Exp Immunol 2005; 139: 371 - 378.
16. Krause I., Blank M., Shoenfeld Y. Immunomodulation of experimental autoimmune diseases via oral tolerance. Crit Rev Immunol 2000; 20: 1-16.
17. Pockley AG Heat shock proteins, anti-heat shock protein reactivity and allograft rejection. Transplantation 2001; 71: 1503-1507.
18. Ford P., Gemmell E., Walker P., West M., Cullinan M., Seymour G. Characterization of heat shock protein-specific T cells in atherosclerosis. Clin Diagn Lab Immunol 2005; 12: 259-267.
19. Xu Q., Schett G., Seitz CS, Hu Y., Gupta RS, Wick G. Surface staining and cytotoxic activity of heat-shock protein 60 antibody in stressed aortic endothelial cells. Circ Res 1994; 75: 1078-1085.
20. Schett G., Xu Q., Amberger A., et al. Autoantibodies against heat shock protein 60 mediate endothelial cytotoxicity. J Clin Invest 1995; 96: 2569-2577.
21. Xu Q., Willeit J., Marosi M., et al. Association of serum antibodies to heat-shock protein 65 with carotid atherosclerosis. Lancet 1993; 341: 255-259.
22. Xu Q., Kiechl S., Mayr M., et al. Association of serum antibodies to heat-shock protein 65 with carotid atherosclerosis: Clinical significance determined in a follow-up study. Circulation 1999; 100: 1169-1174.
23. Knoflach M., Kiechl S., Kind M., et al. Cardiovascular risk factors and atherosclerosis in young males: ARMY study (Atherosclerosis Risk-Factors in Male Youngsters). Circulation 2003; 108: 1064-1069.
24. Benagiano M., D'Elios MM, Amedei A., et al. Human 60-kDa heat shock protein is a target autoantigen of T cells derived from atherosclerotic plaques. J Immunol 2005; 174: 6509-6517.
25. Zal B., Kaski JC, Arno G., et al. Heat-shock protein 60-reactive CD4+ CD28null T cells in patients with acute coronary syndromes. Circulation 2004; 109: 1230-1235.
26. Marshall BJ, Warren JR Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1984; 1: 1311-1315.
27. Take S., Mizuno M., Ishiki K., et al. The effect of eradicating helicobacter pylori on the development of gastric cancer in patients with peptic ulcer disease. Am J Gastroenterol 2005; 100: 1037-1042.
28. Kawahara Y., Yokota K., Mizuno M., et al. Antibodies to human gastric epithelial cells and heat shock protein 60 in Helicobacter pylori positive mucosa associated lymphoid tissue lymphoma. Gut 1999; 45: 20-23.
29. Inaba T., Mizuno M., Take S., et al. Eradication of Helicobacter pylori increases platelet count in patients with idiopathic thrombocytopenic purpura in Japan. Eur J Clin Invest 2005; 35: 214-219.
30. Farkas H., Fust G., Fekete B., Karadi I., Varga L. Eradication of Helicobacter pylori and improvement of hereditary angioneurotic oedema. Lancet 2001; 358: 1695-1696.
31. Nagashima R., Maeda K., Yuda F., Kudo K., Saitoh M., Takahashi T. Helicobacter pylori antigen in the glomeruli of patients with membranous nephropathy. Virchows Arch 1997; 431: 235-239.
32. Rowland M., Daly L., Vaughan M., Higgins A., Bourke B., Drumm B. Age-specific incidence of Helicobacter pylori. Gastroenterology 2006; 130:65-72.
33. Eck M., Schmausser B., Scheller K., et al. CXC chemokines Gro(alpha)/ IL-8 and IP-10/MIG in Helicobacter pylori gastritis. Clin Exp Immunol 2000; 122: 192-199.
34. Yokota K., Hirai Y., Haque M., et al. Heat shock protein produced by Helicobacter pylori. Microbiol Immunol 1994; 38: 403-405.
35. Kobayashi K., Yokota K., Yoshino T., et al. Detection of Helicobacter pylori associated antigen and heat shock protein 60 on follicular dendritic cells in the germinal centres of low grade B cell lymphoma of gastric mucosa associated lymphoid tissue (MALT). J Clin Pathol 1998; 51: 396-398.
36. Ishii E., Yokota K., Sugiyama T. Immunoglobulin G1 antibody response to Helicobacter pylori heat shock protein 60 is closely associated with low-grade gastric mucosa-associated lymphoid tissue lymphoma. Clin Diagn Lab Immunol 2001; 8: 1056-1059.
37. 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 2007; 29: 106-115.
38. Sawayama Y., Ariyama I., Hamada M., et al. Association between chronic Helicobacter pylori infection and acute ischemic stroke: Fukuoka Harasanshin Atherosclerosis Trial (FHAT). Atherosclerosis 2005; 178: 303- 309.
39. Shmuely H., Passaro DJ, Vaturi M., et al. Association of CagA+ Helicobacter pylori infection with aortic atheroma. Atherosclerosis 2005; 179: 127-132.
40. Zhu J., Katz RJ, Quyyumi AA, et al. Association of serum antibodies to heat-shock protein 65 with coronary calcification levels: Suggestion of pathogen-triggered autoimmunity in early atherosclerosis. Circulation 2004; 109: 36-41.
41. Heuschmann PU, Neureiter D., Gesslein M., et al. Association between infection with Helicobacter pylori and Chlamydia pneumoniae and risk of ischemic stroke subtypes: Results from a population-based case-control study. Stroke 2001; 32: 2253-2258.
42. O'Connor CM, Dunne MW, Pfeffer MA, et al. Azithromycin for the secondary prevention oA coronary heart disease events: The WIZARD study: a randomized controlled trial. JAMA 2003; 290: 1459-1466.
43. Vainas T., Stassen FR, Schurink GW, et al. Secondary prevention of atherosclerosis through chlamydia pneumoniae eradication (SPACE Trial): a randomised clinical trial in patients with peripheral arterial disease. Eur J Vasc Endovasc Surg 2005; 29: 403-411.
44. Foteinos G., Afzal AR, Mandal K., Jahangiri M., Xu Q. Anti-heat shock protein 60 autoantibodies induce atherosclerosis in apolipoprotein E-deficient mice via endothelial damage. Circulation 2005; 112: 1206-1213.
45. Lee A., O'Rourke J., De Ungria MC, Robertson B., Daskalopoulos G., Dixon MF A standardized mouse model of Helicobacter pylori infection: introducing the Sydney strain. Gastroenterology 1997; 112: 1386-1397.
46. Dey A., Yokota K., Kobayashi K., Oguma K., Hirai Y., Akagi T. Antibody and cytokine responses in Helicobacter pylori-infected various mouse strains. Acta Med Okayama 1998; 52: 41-48.
47. Yamaguchi H., Osaki T., Kai M., Taguchi H., Kamiya S. Immune response against a cross-reactive epitope on the heat shock protein 60 homologue of Helicobacter pylori. Infect Immun 2000; 68: 3448-3454.
48. Watanabe K., Murakami K., Sato R., et al. Effect of sucralfate on antibiotic therapy for Helicobacter pylori infection in mice. Antimicrob Agents Chemother 2004; 48: 4582-4588.
49. Matsuura E., Kobayashi K., Tabuchi M., Lopez LR Oxidative modification of low-density lipoprotein and immune regulation of atherosclerosis. Prog Lipid Res 2006; 45: 466-486.
50. Hollestelle SC, De Vries MR, Van Keulen JK Toll-like receptor 4 is involved in outward arterial remodeling. Circulation 2004; 109: 393-398.
51. Shi W., Haberland ME, Jien ML, Shih DM, Lusis AJ Endothelial responses to oxidized lipoproteins determine genetic susceptibility to atherosclerosis in mice. Circulation 2000; 102: 75-81.
52. Mach F., Sukhova GK, Michetti M., Libby P., Michetti P. Influence of Helicobacter pylori infection during atherogenesis in vivo in mice. Circ Res 2002; 90: E1-E4.
53. Gupta S., Pablo AM, Jiang X., Wang N., Tall AR, Schindler C. IFN-gamma potentiates atherosclerosis in ApoE knock-out mice. J Clin Invest 1997; 99: 2752-2761.
54. Li L., Messas E., Batista EL Jr, Levine RA, Amar S. Porphyromonas gingivalis infection accelerates the progression of atherosclerosis in a heterozygous apolipoprotein E-deficient murine model. Circulation 2002; 105: 861-867.
55. Wick G., Knoflach M., Xu Q. Autoimmune and inflammatory mechanisms in atherosclerosis. Annu Rev Immunol 2004; 22: 361-403.
56. Shoenfeld Y., Gerli R., Doria A., et al. Accelerated atherosclerosis in autoimmune rheumatic diseases. Circulation 2005; 112: 3337-3347.
57. Shoenfeld Y., Sherer Y., Harats D. Artherosclerosis as an infectious, inflammatory and autoimmune disease. Trends Immunol 2001; 22: 293-295.
58. 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 U S A 2005; 102: 1596-1601.
59. Cheng C., Tempel D., van Haperen R., et al. Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation 2006; 113: 2744-2753.
60. Kawakami A., Aikawa M., Alcaide P., Luscinskas FW, Libby P., Sacks FM Apolipoprotein CIII induces expression of vascular cell adhesion molecule-1 in vascular endothelial cells and increases adhesion of monocytic cells. Circulation 2006; 114: 681-687.
61. Yamawaki H., Lehoux S., Berk BC Chronic physiological shear stress inhibits tumor necrosis factor-induced proinflammatory responses in rabbit aorta perfused ex vivo. Circulation 2003; 108: 1619-1625.
62. Gu L., Okada Y., Clinton SK, et al. Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol Cell 1998; 2: 275-281.
63. Boring L., Gosling J., Cleary M., Charo IF Decreased lesion formation in CCR2-/- mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 1998; 394: 894-897.
64. Pfister G., Stroh CM, Perschinka H., et al. Detection of HSP60 on the membrane surface of stressed human endothelial cells by atomic force and confocal microscopy. J Cell Sci 2005; 118: 1587-1594.
65. Perschinka H., Mayr M., Millonig G., et al. Cross-reactive B-cell epitopes of microbial and human heat shock protein 60/65 in atherosclerosis. Arterioscler Thromb Vasc Biol 2003; 23: 1060-1065.
66. Chung SW, Kang HS, Park HR, Kim SJ, Kim SJ, Choi JI Immune responses to heat shock protein in Porphyromonas gingivalis-infected periodontitis and atherosclerosis patients. J Periodontal Res 2003; 38: 388-393.
67. Evans Jr DJ, Evans DG, Engstrand L., Graham DY Urease-associated heat shock protein of Helicobacter pylori. Infect Immun 1992; 60: 2125-2127.
68. Collins T., Korman AJ, Wake CT, et al. Immune interferon activates multiple class II major histocompatibility complex genes and the associated invariant chain gene in human endothelial cells and dermal fibroblasts. Proc Natl Acad Sci U S A 1984; 81: 4917-4921.
69. Schmid D., Pypaert M., Munz C. Antigen-loading compartments for major histocompatibility complex class II molecules continuously receive input from autophagosomes. Immunity 2007; 26: 79-92.
70. Levine B., Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132: 27-42.
71. Veillard NR, Steffens S., Pelli G., et al. Differential influence of chemokine receptors CCR2 and CXCR3 in development of atherosclerosis in vivo. Circulation 2005; 112: 870-878.
72. Buono C., Pang H., Uchida Y., Libby P., Sharpe AH, Lichtman AH B7-1/B7-2 costimulation regulates plaque antigen-specific T-cell responses and atherogenesis in low-density lipoprotein receptor-deficient mice. Circulation 2004; 109: 2009-2015.
73. Afek A., George J., Gilburd B., Rauova L., et al. Immunization of low-density lipoprotein receptor deficient (LDL-RD) mice with heat shock protein 65 (HSP-65) promotes early atherosclerosis. J Autoimmun 2000; 14: 115-121.
74. 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: 900-905.