Promotion of atherosclerosis by Helicobacter cinaedi infection that involves macrophage-driven proinflammatory responses

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Khan, Shahzada ^a   Rahman, H N Ashiqur ^b   Okamoto, Tatsuya ^b   Matsunaga, Tetsuro ^c   Fujiwara, Yukio ^b   Sawa, Tomohiro ^c   Yoshitake, Jun ^d   Ono, Katsuhiko ^e   Ahmed, Khandaker Ahtesham ^b   Rahaman, Md Mizanur ^b   Oyama, Kohta ^b   Takeya, Motohiro ^b   Ida, Tomoaki ^c   Kawamura, Yoshiaki ^f   Fujii, Shigemoto ^b   Akaike, Takaaki ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KUMAMOTO UNIVERSITY   (Japan)

^c TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d NATIONAL CENTER FOR GERIATRICS AND GERONTOLOGY   (Japan)

^e SONOMA STATE UNIVERSITY   (United States)

^f AICHI GAKUIN UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL RNA; ENDOTHELIAL NITRIC OXIDE SYNTHASE; LOW DENSITY LIPOPROTEIN RECEPTOR;

ANIMAL; AORTA; ARTICLE; ATHEROSCLEROSIS; BIOSYNTHESIS; C57BL MOUSE; CARDIOVASCULAR DISEASE; CELL CULTURE; CELL DIFFERENTIATION; FOAM CELL; GENETICS; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HYPERLIPIDEMIA; IMMUNOLOGY; INFLAMMATION; KNOCKOUT MOUSE; MACROPHAGE; MALE; MICROBIOLOGY; MONOCYTE; MOUSE; NEUTROPHIL; PATHOGENICITY; PATHOLOGY;

ANIMALS; AORTA; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASES; CELL DIFFERENTIATION; CELLS, CULTURED; DNA, BACTERIAL; FOAM CELLS; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HYPERLIPIDEMIAS; INFLAMMATION; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; NEUTROPHILS; NITRIC OXIDE SYNTHASE TYPE III; RECEPTORS, LDL; RNA, BACTERIAL;

EID: 84906747356     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep04680     Document Type: Article

References (67)

1. Libby, P., Ridker, P. M. & Hansson, G. K. Inflammation in atherosclerosis: from pathophysiology to practice. J. Am. Coll. Cardiol. 54, 2129-2138 (2009).
2. Tabas, I. Macrophage death and defective inflammation resolution in atherosclerosis. Nat. Rev. Immunol. 10, 36-46 (2010).
3. Rosenfeld, M. E. & Campbell, L. A. Pathogens and atherosclerosis: update on the potential contribution of multiple infectious organisms to the pathogenesis of atherosclerosis. Thromb. Haemost. 106, 858-867 (2011).
4. Hansson, G. K. & Hermansson, A. The immune system in atherosclerosis. Nat. Immunol. 12, 204-212 (2011).
5. Moazed, T. C., Kuo, C., Grayston, J. T. & Campbell, L. A. Murine models of Chlamydia pneumoniae infection and atherosclerosis. J. Infect. Dis. 175, 883-890 (1997).
6. Hsich, E. et al. Cytomegalovirus infection increases development of atherosclerosis in apolipoprotein-E knockout mice. Atherosclerosis 156, 23-28 (2001).
7. Alber, D. G., Powell, K. L., Vallance, P., Goodwin, D. A. & Grahame-Clarke, C. Herpesvirus infection accelerates atherosclerosis in the apolipoprotein Edeficient mouse. Circulation 102, 779-785 (2000).
8. Naghavi, M. et al. Influenza infection exerts prominent inflammatory and thrombotic effects on the atherosclerotic plaques of apolipoprotein E-deficient mice. Circulation 107, 762-768 (2003).
9. Li, L., Messas, E., Batista, E. L., Jr., Levine, R. A. & Amar, S. Porphyromonas gingivalis infection accelerates the progression of atherosclerosis in a heterozygous apolipoprotein E-deficient murine model. Circulation 105, 861-867 (2002).
10. Zhang, T. et al. Aggregatibacter actinomycetemcomitans accelerates atherosclerosis with an increase in atherogenic factors in spontaneously hyperlipidemic mice. FEMS Immunol. Med. Microbiol. 59, 143-151 (2010).
11. Portugal, L. R. et al. Infection with Toxoplasma gondii increases atherosclerotic lesion in ApoE-deficient mice. Infect. Immun. 72, 3571-3576 (2004).
12. Daus, H. et al. Lack of evidence for a pathogenic role of Chlamydia pneumoniae and cytomegalovirus infection in coronary atheroma formation. Cardiology 90, 83-88 (1998).
13. Ayada, K. et al. Chronic infections and atherosclerosis. Ann. N. Y. Acad. Sci. 1108, 594-602 (2007).
14. Brenner, H., Berg, G., Frohlich, M., Boeing, H. & Koenig, W. Chronic infection with Helicobacter pylori does not provoke major systemic inflammation in healthy adults: results from a large population-based study. Atherosclerosis 147, 399-403 (1999).
15. Morre, S. A., Stooker, W., Lagrand, W. K., van den Brule, A. J. & Niessen, H. W. Microorganisms in the aetiology of atherosclerosis. J. Clin. Pathol. 53, 647-654 (2000).
16. Epstein, S. E., Zhu, J., Najafi, A. H. & Burnett, M. S. Insights into the role of infection in atherogenesis and in plaque rupture. Circulation 119, 3133-3141 (2009).
17. Fox, J. G. The non-H pylori helicobacters: their expanding role in gastrointestinal and systemic diseases. Gut 50, 273-283 (2002).
18. Kitamura, T. et al. Helicobacter cinaedi cellulitis and bacteremia in immunocompetent hosts after orthopedic surgery. J. Clin. Microbiol. 45, 31-38 (2007).
19. Iwashita, H. et al. Identification of the major antigenic protein of Helicobacter cinaedi and its immunogenicity in humans with H. cinaedi infections. Clin. Vaccine Immunol. 15, 513-521 (2008).
20. Solnick, J. V. Clinical significance of Helicobacter species other than Helicobacter pylori. Clin. Infect. Dis. 36, 349-354 (2003).
21. Uckay, I. et al. Recurrent bacteremia with Helicobacter cinaedi: case report and review of the literature. BMC Infect. Dis. 6, 86 (2006).
22. Vandamme, P., Harrington, C. S., Jalava, K. & On, S. L. Misidentifying helicobacters: the Helicobacter cinaedi example. J. Clin. Microbiol. 38, 2261-2266 (2000).
23. Fernandez, K. R., Hansen, L. M., Vandamme, P., Beaman, B. L. & Solnick, J. V. Captive rhesus monkeys (Macaca mulatta) are commonly infected with Helicobacter cinaedi. J. Clin. Microbiol. 40, 1908-1912 (2002).
24. Fennell, C. L. et al. Characterization of Campylobacter-like organisms isolated from homosexual men. J. Infect. Dis. 149, 58-66 (1984).
25. Khan, S. et al. Potential association of Helicobacter cinaedi with atrial arrhythmias and atherosclerosis. Microbiol. Immunol. 56, 145-154 (2012).
26. Totten, P. A. et al. Campylobacter cinaedi (sp. nov.) and Campylobacter fennelliae (sp. nov.): two new Campylobacter species associated with enteric disease in homosexual men. J. Infect. Dis. 151, 131-139 (1985).
27. Oyama, K. et al. Identification of and screening for human Helicobacter cinaedi infections and carriers via nested PCR. J. Clin. Microbiol. 50, 3893-3900 (2012).
28. van der Ven, A. J., Kullberg, B. J., Vandamme, P. & Meis, J. F. Helicobacter cinaedi bacteremia associated with localized pain but not with cellulitis. Clin. Infect. Dis. 22, 710-711 (1996).
29. Lewis, G. D., Holmes, C. B., Holmvang, G. & Butterton, J. R. Case records of the Massachusetts General Hospital. Case 8-2007. A 48-year-old man with chest pain followed by cardiac arrest. N. Engl. J. Med. 356, 1153-1162 (2007).
30. Matsushima, Y., Hayashi, S. & Tachibana, M. Spontaneously hyperlipidemic (SHL) mice: Japanese wild mice with apolipoprotein E deficiency. Mamm. Genome 10, 352-357 (1999).
31. Linton, M. F. & Fazio, S. Macrophages, inflammation, and atherosclerosis. Int. J. Obes. Relat. Metab. Disord. 27 Suppl 3, S35-40 (2003).
32. Nakashima, Y., Raines, E. W., Plump, A. S., Breslow, J. L. & Ross, R. Upregulation of VCAM-1 and ICAM-1 at atherosclerosis-prone sites on the endothelium in the ApoE-deficient mouse. Arterioscler. Thromb. Vasc. Biol. 18, 842-851 (1998).
33. Cuccherini, B. et al. Bacteremia and skin/bone infections in two patients with Xlinked agammaglobulinemia caused by an unusual organism related to Flexispira/Helicobacter species. Clin. Immunol. 97, 121-129 (2000).
34. Rayner, M. G. et al. Evidence of bacterial metabolic activity in culture-negative otitis media with effusion. JAMA 279, 296-299 (1998).
35. Shen, Z. et al. Cytolethal distending toxin promotes Helicobacter cinaediassociated typhlocolitis in interleukin-10-deficient mice. Infect. Immun. 77, 2508-2516 (2009).
36. Sawa, T. et al. Protein S-guanylation by the biological signal 8-nitroguanosine 39,59-cyclic monophosphate. Nat. Chem. Biol. 3, 727-735 (2007).
37. Zaki, M. H. et al. Cytoprotective function of heme oxygenase 1 induced by a nitrated cyclic nucleotide formed during murine salmonellosis. J. Immunol. 182, 3746-3756 (2009).
38. Nishida, M. et al.Hydrogen sulfide anion regulates redox signaling via electrophile sulfhydration. Nat. Chem. Biol. 8, 714-724 (2012).
39. Ito, C. et al. Endogenous nitrated nucleotide is a key mediator of autophagy and innate defense against bacteria. Mol. Cell 52, 794-804 (2013).
40. Cao, F., Castrillo, A., Tontonoz, P., Re, F. & Byrne, G. I. Chlamydia pneumoniaeinduced macrophage foam cell formation is mediated by Toll-like receptor 2. Infect. Immun. 75, 753-759 (2007).
41. Aiello, R. J. et al. Increased atherosclerosis in hyperlipidemic mice with inactivation of ABCA1 in macrophages. Arterioscler. Thromb. Vasc. Biol. 22, 630-637 (2002).
42. Meurs, I. et al. The effect of ABCG1 deficiency on atherosclerotic lesion development in LDL receptor knockout mice depends on the stage of atherogenesis. Atherosclerosis 221, 41-47 (2012).
43. Herijgers, N., Van Eck, M., Groot, P. H., Hoogerbrugge, P. M. & Van Berkel, T. J. Low density lipoprotein receptor of macrophages facilitates atherosclerotic lesion formation in C57Bl/6 mice. Arterioscler. Thromb. Vasc. Biol. 20, 1961-1967 (2000).
44. Fong, L. G. & Le, D. The processing of ligands by the class A scavenger receptor is dependent on signal information located in the cytoplasmic domain. J. Biol. Chem. 274, 36808-36816 (1999).
45. Valacchi, G., Sticozzi, C., Lim, Y.&Pecorelli, A. Scavenger receptor class B type I: a multifunctional receptor. Ann. N. Y. Acad. Sci. 1229, E1-7 (2011).
46. Tacke, F. & Randolph, G. J. Migratory fate and differentiation of blood monocyte subsets. Immunobiology 211, 609-618 (2006).
47. Yamaguchi, H., Haranaga, S., Widen, R., Friedman, H. & Yamamoto, Y. Chlamydia pneumoniae infection induces differentiation of monocytes into macrophages. Infect. Immun. 70, 2392-2398 (2002).
48. Mullick, A. E., Tobias, P. S. & Curtiss, L. K. Modulation of atherosclerosis in mice by Toll-like receptor 2. J. Clin. Invest. 115, 3149-3156 (2005).
49. Campbell, L. A., Blessing, E., Rosenfeld,M., Lin, T. & Kuo, C.Mouse models of C. pneumoniae infection and atherosclerosis. J. Infect. Dis. 181 Suppl 3, S508-513 (2000).
50. Shesely, E. G. et al. Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc. Natl. Acad. Sci. USA 93, 13176-13181 (1996).
51. Wang, Z. et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472, 57-63 (2011).
52. Koren, O. et al. Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc. Natl. Acad. Sci. USA 108, 4592-4598 (2011).
53. Goto, T. et al. Complete genome sequence of Helicobacter cinaedi strain PAGU611, isolated in a case of human bacteremia. J. Bacteriol. 194, 3744-3745 (2012).
54. Whetzel, A. M. et al. ABCG1 deficiency in mice promotes endothelial activation and monocyte-endothelial interactions. Arterioscler. Thromb. Vasc. Biol. 30, 809-817 (2010).
55. Wiersma, H. et al. Lack of Abcg1 results in decreased plasma HDL cholesterol levels and increased biliary cholesterol secretion in mice fed a high cholesterol diet. Atherosclerosis 206, 141-147 (2009).
56. Baldan, A. et al. Impaired development of atherosclerosis in hyperlipidemic Ldlr2/2 and ApoE2/2 mice transplanted with Abcg12/2 bone marrow. Arterioscler. Thromb. Vasc. Biol. 26, 2301-2307 (2006).
57. Out, R. et al. Macrophage ABCG1 deletion disrupts lipid homeostasis in alveolar macrophages and moderately influences atherosclerotic lesion development in LDL receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol. 26, 2295-2300 (2006).
58. Li, L., Thompson, P. A. & Kitchens, R. L. Infection induces a positive acute phase apolipoprotein E response from a negative acute phase gene: role of hepatic LDL receptors. J. Lipid Res. 49, 1782-1793 (2008).
59. Monaco, C. et al. Toll-like receptor-2 mediates inflammation and matrix degradation in human atherosclerosis. Circulation 120, 2462-2469 (2009).
60. Fox, J. G. et al.Gastroenteritis in NF-kB-deficient mice is produced with wild-type Camplyobacter jejuni but not with C. jejuni lacking cytolethal distending toxin despite persistent colonization with both strains. Infect. Immun. 72, 1116-1125 (2004).
61. Pratt, J. S., Sachen, K. L., Wood, H. D., Eaton, K. A. & Young, V. B. Modulation of host immune responses by the cytolethal distending toxin of Helicobacter hepaticus. Infect. Immun. 74, 4496-4504 (2006).
62. Yagyu, H. et al. Overexpressed lipoprotein lipase protects against atherosclerosis in apolipoprotein E knockout mice. J. Lipid Res. 40, 1677-1685 (1999).
63. Allen, J. M., Thompson, G. R., Myant, N. B., Steiner, R. & Oakley, C. M. Cardiovascular complications of homozygous familial hypercholesterolaemia. Br. Heart J. 44, 361-368 (1980).
64. Nakashima, Y., Plump, A. S., Raines, E. W., Breslow, J. L. & Ross, R. ApoEdeficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler. Thromb. 14, 133-140 (1994).
65. Tangirala, R. K., Rubin, E. M. & Palinski, W. Quantitation of atherosclerosis in murine models: correlation between lesions in the aortic origin and in the entire aorta, and differences in the extent of lesions between sexes in LDL receptordeficient and apolipoprotein E-deficient mice. J. Lipid Res. 36, 2320-2328 (1995).
66. Untergasser, A. et al. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res. 35, W71-74 (2007).
67. Schaffner, T. et al. Arterial foam cells with distinctive immunomorphologic and histochemical features of macrophages. Am. J. Pathol. 100, 57-80 (1980).