Infection of vascular endothelial cells with human cytomegalovirus under fluid shear stress reveals preferential entry and spread of virus in flow conditions simulating atheroprone regions of the artery

Journal of Virology

Volumn 86, Issue 24, 2012, Pages 13745-13755

  DuRose, Jenny B ^a   Li, Julie ^b,c   Chien, Shu ^b,c   Spector, Deborah H ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; DNA REPLICATION; EXON; FLOW RATE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; IMMUNOFLUORESCENCE TEST; IN VIVO STUDY; MICROVASCULAR ENDOTHELIAL CELL; PRIORITY JOURNAL; PROGENY; PROMOTER REGION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHEAR STRESS; VIRION; VIRUS ASSEMBLY; VIRUS ENTRY; VIRUS INFECTIVITY; VIRUS MORPHOLOGY; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TITRATION; VIRUS TRANSMISSION; WESTERN BLOTTING;

ARTERIES; BASE SEQUENCE; BLOTTING, WESTERN; CELLS, CULTURED; CYTOMEGALOVIRUS; DNA PRIMERS; DNA, VIRAL; ENDOTHELIUM, VASCULAR; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, VIRAL; GENES, VIRAL; HUMANS; MEMBRANE FUSION; MICROSCOPY, ELECTRON, TRANSMISSION; POLYMERASE CHAIN REACTION;

HUMAN HERPESVIRUS 5;

EID: 84870664962     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02244-12     Document Type: Article

References (49)

1. Adam E, et al. 1987. High levels of cytomegalovirus antibody in patients requiring vascular surgery for atherosclerosis. Lancet ii:291-293.
2. Bate SL, Dollard SC, Cannon MJ. 2010. Cytomegalovirus seroprevalence in the United States: the national health and nutrition examination surveys, 1988-2004. Clin. Infect. Dis. 50:1439 -1447.
3. Bentz GL, Yurochko AD. 2008. Human CMV infection of endothelial cells induces an angiogenic response through viral binding to EGF receptor and beta1 and beta3 integrins. Proc. Natl. Acad. Sci. U. S. A. 105:5531-5536.
4. Berencsi K, et al. 1998. Early atherosclerotic plaques in the aorta following cytomegalovirus infection of mice. Cell Adhes. Commun. 5:39-47.
5. Blum A, et al. 1998. High anti-cytomegalovirus (CMV) IgG antibody titer is associated with coronary artery disease and may predict post-coronary balloon angioplasty restenosis. Am. J. Cardiol. 81:866-868.
6. Bodaghi B, et al. 1999. Entry of human cytomegalovirus into retinal pigment epithelial and endothelial cells by endocytosis. Investig. Ophthalmol. Visual Sci. 40:2598 -2607.
7. Boon RA, Horrevoets AJ. 2009. Key transcriptional regulators of the vasoprotective effects of shear stress. Hamostaseologie 29:39-43.
8. Burnett MS, et al. 2004. Murine cytomegalovirus infection increases aortic expression of proatherosclerotic genes. Circulation 109:893- 897.
9. Cheng J, et al. 2009. Cytomegalovirus infection causes an increase of arterial blood pressure. PLoS Pathog. 5:e1000427. doi:10.1371/journal.ppat.1000427.
10. Chiu B, Viira E, Tucker W, Fong IW. 1997. Chlamydia pneumoniae, cytomegalovirus, and herpes simplex virus in atherosclerosis of the carotid artery. Circulation 96:2144 -2148.
11. Chiu JJ, Chien S. 2011. Effects of disturbed flow on vascular endothelium: pathophysiological basis and clinical perspectives. Physiol. Rev. 91:327-387.
12. Compton T, Nowlin DM, Cooper NR. 1993. Initiation of human cytomegalovirus infection requires initial interaction with cell surface heparan sulfate. Virology 193:834-841.
13. Conway DE, Williams MR, Eskin SG, McIntire LV. 2010. Endothelial cell responses to atheroprone flow are driven by two separate flow components: low time-average shear stress and fluid flow reversal. Am. J. Physiol. Heart Circ. Physiol. 298:H367-H374.
14. DeMeritt IB, Milford LE, Yurochko AD. 2004. Activation of the NFkappaB pathway in human cytomegalovirus-infected cells is necessary for efficient transactivation of the major immediate-early promoter. J. Virol. 78:4498-4507.
15. Dumortier J, et al. 2008. Human cytomegalovirus secretome contains factors that induce angiogenesis and wound healing. J. Virol. 82:6524-6535.
16. Feire AL, Koss H, Compton T. 2004. Cellular integrins function as entry receptors for human cytomegalovirus via a highly conserved disintegrinlike domain. Proc. Natl. Acad. Sci. U. S. A. 101:15470 -15475.
17. Frangos JA, Eskin SG, McIntire LV, Ives CL. 1985. Flow effects on prostacyclin production by cultured human endothelial cells. Science 227: 1477-1479.
18. Gimbrone MA. 2010. The Gordon Wilson lecture. Understanding vascular endothelium: a pilgrim's progress. Endothelial dysfunction, biomechanical forces and the pathobiology of atherosclerosis. Trans Am. Clin. Climatol. Assoc. 121:115-127.
19. Gredmark S, Jonasson L, Van Gosliga D, Ernerudh J, Soderberg-Naucler C. 2007. Active cytomegalovirus replication in patients with coronary disease. Scand. Cardiovasc. J. 41:230 -234.
20. Grudzinska MK, et al. 2010. RCMV increases intimal hyperplasia by inducing inflammation, MCP-1 expression and recruitment of adventitial cells to intima. Herpesviridae 1:7.
21. Hendrix MG, Daemen M, Bruggeman CA. 1991. Cytomegalovirus nucleic acid distribution within the human vascular tree. Am. J. Pathol. 138: 563-567.
22. Hsich E, et al. 2001. Cytomegalovirus infection increases development of atherosclerosis in apolipoprotein-E knockout mice. Atherosclerosis 156: 23-28.
23. Isern E, et al. 2011. The activator protein 1 binding motifs within the human cytomegalovirus major immediate-early enhancer are functionally redundant and act in a cooperative manner with the NF-{kappa}B sites during acute infection. J. Virol. 85:1732-1746.
24. Kloppenburg G, et al. 2005. Cytomegalovirus aggravates intimal hyperplasia in rats by stimulating smooth muscle cell proliferation. Microbes Infect. 7:164 -170.
25. Lamon BD, Hajjar DP. 2008. Inflammation at the molecular interface of atherogenesis: an anthropological journey. Am. J. Pathol. 173:1253-1264.
26. Liu R, et al. 2006. Presence and severity of Chlamydia pneumoniae and cytomegalovirus infection in coronary plaques are associated with acutecoronary syndromes. Int. Heart J. 47:511-519.
27. Melnick JL, et al. 1983. Cytomegalovirus antigen within human arterial smooth muscle cells. Lancet ii:644-647.
28. Merigan TC, et al. 1992. A controlled trial of ganciclovir to prevent cytomegalovirus disease after heart transplantation. New Engl. J. Med. 326:1182-1186.
29. Mocarski ES, Shenk T, Pass RF. 2007. Cytomegaloviruses, fifth ed, vol 2. Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia, PA.
30. Napoli C, et al. 1999. Influence of maternal hypercholesterolaemia during pregnancy on progression of early atherosclerotic lesions in childhood: Fate of Early Lesions in Children (FELIC) study. Lancet 354:1234 -1241.
31. Pampou S, et al. 2000. Cytomegalovirus genome and the immediate-early antigen in cells of different layers of human aorta. Virchows Arch. 436: 539-552.
32. Raines EW, Ross R. 1993. Smooth muscle cells and the pathogenesis of the lesions of atherosclerosis. Br. Heart J. 69:S30 -S37.
33. Reinhardt B, et al. 2005. HCMV infection of human vascular smooth muscle cells leads to enhanced expression of functionally intact PDGF beta-receptor. Cardiovasc. Res. 67:151-160.
34. Ridker PM, Hennekens CH, Buring JE, Kundsin R, Shih J. 1999. Baseline IgG antibody titers to Chlamydia pneumoniae, Helicobacter pylori, herpes simplex virus, and cytomegalovirus and the risk for cardiovascular disease in women. Ann. Intern. Med. 131:573-577.
35. Ross R. 1999. Atherosclerosis-an inflammatory disease. New Engl. J. Med. 340:115-126.
36. Ryckman BJ, Jarvis MA, Drummond DD, Nelson JA, Johnson DC. 2006. Human cytomegalovirus entry into epithelial and endothelial cells depends on genes UL128 to UL150 and occurs by endocytosis and low-pH fusion. J. Virol. 80:710 -722.
37. Ryckman BJ, et al. 2008. Characterization of the human cytomegalovirus gH/gL/UL128-131 complex that mediates entry into epithelial and endothelial cells. J. Virol. 82:60 -70.
38. Schmolke S, Kern HF, Drescher P, Jahn G, Plachter B. 1995. The dominant phosphoprotein pp65 (UL83) of human cytomegalovirus is dispensable for growth in cell culture. J. Virol. 69:5959 -5968.
39. Soroceanu L, Akhavan A, Cobbs CS. 2008. Platelet-derived growth factor-alpha receptor activation is required for human cytomegalovirus infection. Nature 455:391-395.
40. Stinski MF, Petrik DT. 2008. Functional roles of the human cytomegalovirus essential IE86 protein. Curr. Top. Microbiol. Immunol. 325:133-152.
41. Streblow DN, et al. 1999. The human cytomegalovirus chemokine receptor US28 mediates vascular smooth muscle cell migration. Cell 99:511-520.
42. Tilton C, Clippinger AJ, Maguire T, Alwine JC. 2011. Human cytomegalovirus induces multiple means to combat reactive oxygen species. J. Virol. 85:12585-12593.
43. Valantine HA, et al. 1999. Impact of prophylactic immediate posttransplant ganciclovir on development of transplant atherosclerosis: a post hoc analysis of a randomized, placebo-controlled study. Circulation 100:61- 66.
44. van de Berg PJ, Yong SL, Remmerswaal EB, van Lier RA, ten Berge IJ. 2012. Cytomegalovirus-induced effector T cells cause endothelial cell damage. Clin. Vaccine Immunol. 19:772-779.
45. Vliegen I, Stassen F, Grauls G, Blok R, Bruggeman C. 2002. MCMV infection increases early T-lymphocyte influx in atherosclerotic lesions in apoE knockout mice. J. Clin. Virol. 25(Suppl 2):S159-S171.
46. Wang X, Huang DY, Huong SM, Huang ES. 2005. Integrin alphavbeta3 is a coreceptor for human cytomegalovirus. Nat. Med. 11:515-521.
47. Wang X, Huong SM, Chiu ML, Raab-Traub N, Huang ES. 2003. Epidermal growth factor receptor is a cellular receptor for human cytomegalovirus. Nature 424:456-461.
48. Yamashiroya HM, Ghosh L, Yang R, Robertson AL, Jr. 1988. Herpesviridae in the coronary arteries and aorta of young trauma victims. Am. J. Pathol. 130:71-79.
49. Yi L, Wang DX, Feng ZJ. 2008. Detection of human cytomegalovirus in atherosclerotic carotid arteries in humans. J. Formosan Med. Assoc. 107: 774-781.