Persistent Infection of Human Fetal Endothelial Cells with Rubella Virus

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Perelygina, Ludmila ^a   Zheng, Qi ^a   Metcalfe, Maureen ^a   Icenogle, Joseph ^a  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN;

ARTICLE; CELL ASSAY; CELL CYCLE ARREST; CELL PROLIFERATION; CONTROLLED STUDY; CULTURE MEDIUM; FETUS CELL; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PERSISTENT INFECTION; PROTEIN SYNTHESIS; RUBELLA VIRUS; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL; VIRION; VIRUS CULTURE; VIRUS IDENTIFICATION; VIRUS INFECTION; VIRUS REPLICATION; VIRUS STRAIN; WILD TYPE;

CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; FETUS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; PROTEIN BIOSYNTHESIS; RUBELLA SYNDROME, CONGENITAL; RUBELLA VIRUS; VIRUS REPLICATION;

EID: 84881107393     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073014     Document Type: Article

References (75)

1. Plotkin S, Reef S, Cooper L, Alford CA, (2011) Rubella. In: Remington JS, Klein JO, Wilson C, Nizet V, Maldonado YA, eds. Infectious diseases of the fetus and newborn infant. Philadelphia, PA: Elsveier. pp. pp. 861-898.
2. Reef SE, Strebel P, Dabbagh A, Gacic-Dobo M, Cochi S, (2011) Progress toward control of rubella and prevention of congenital rubella syndrome--worldwide, 2009. J Infect Dis 204 (Suppl 1):: S24-S27. doi:10.1093/infdis/jir155. PubMed: 21666168.
3. Rawls WE, (1968) Congenital rubella: the significance of virus persistence. Prog Med Virol 10: 238-285. PubMed: 4304589.
4. Webster WS, (1998) Teratogen update: congenital rubella. Teratology 58: 13-23. doi:10.1002/(SICI)1096-9926(199807)58:1. PubMed: 9699240.
5. Monif GR, Sever JL, Schiff GM, Traub RG, (1965) Isolation of Rubella Virus from Products of Conception. Am J Obstet Gynecol 91: 1143-1146. PubMed: 14280166.
6. Töndury G, Smith DW, (1966) Fetal rubella pathology. J Pediatr 68: 867-879. doi:10.1016/S0022-3476(66)80204-4. PubMed: 5949097.
7. Driscoll SG, (1969) Histopathology of gestational rubella. Am J Dis Child 118: 49-53. PubMed: 5790245.
8. Esterly JR, Oppenheimer EH, (1967) Vascular lesions in infants with congenital rubella. Circulation 36: 544-554. doi:10.1161/01.CIR.36.4.544. PubMed: 6041868.
9. Singer DB, Rudolph AJ, Rosenberg HS, Rawls WE, Boniuk M, (1967) Pathology of the congenital rubella syndrome. J Pediatr 71: 665-675. doi:10.1016/S0022-3476(67)80202-6. PubMed: 6054754.
10. Menser MA, Reye RD, (1974) The pathology of congenital rubella: a review written by request. Pathology 6: 215-222. doi:10.3109/00313027409068988. PubMed: 4607215.
11. Rowe RD, (1973) Cardiovascular disease in the rubella syndrome. Cardiovasc Clin 5: 61-80. PubMed: 4589966.
12. Oster ME, Riehle-Colarusso T, Correa A, (2010) An update on cardiovascular malformations in congenital rubella syndrome. Birth Defects Res A Clin Mol Teratol 88: 1-8. PubMed: 19697432.
13. Varghese PJ, Izukawa T, Rowe RD, (1969) Supravalvular aortic stenosis as part of rubella syndrome, with discussion of pathogenesis. Br Heart J 31: 59-62. doi:10.1136/hrt.31.1.59. PubMed: 5764966.
14. Rosenberg HS, Oppenheimer EH, Esterly JR, (1981) Congenital rubella syndrome: the late effects and their relation to early lesions. Perspect Pediatr Pathol 6: 183-202. PubMed: 7322827.
15. Garcia AG, Marques RL, Lobato YY, Fonseca ME, Wigg MD, (1985) Placental pathology in congenital rubella. Placenta 6: 281-295. doi:10.1016/S0143-4004(85)80038-2. PubMed: 3903730.
16. Cooper LZ, Green RH, Krugman S, Giles JP, Mirick GS, (1965) Neonatal thrombocytopenic purpura and other manifestations of rubella contracted in utero. Am J Dis Child 110: 416-427. PubMed: 5890932.
17. Delahunt CS, Rieser N, (1967) Rubella-induced embryopathies in monkeys. Am J Obstet Gynecol 99: 580-588. PubMed: 4963690.
18. Kono R, Hayakawa Y, Hibi M, Ishii K, (1969) Experimental vertical transmission of rubella virus in rabbits. Lancet 1: 343-347. PubMed: 4179354.
19. Plotkin SA, Boue A, Boue JG, (1965) The in vitro growth of rubella virus in human embryo cells. Am J Epidemiol 81: 71-85. PubMed: 14246083.
20. Yoneda T, Urade M, Sakuda M, Miyazaki T, (1986) Altered growth, differentiation, and responsiveness to epidermal growth factor of human embryonic mesenchymal cells of palate by persistent rubella virus infection. J Clin Invest 77: 1613-1621. doi:10.1172/JCI112477. PubMed: 3009547.
21. Abernathy ES, Wang CY, Frey TK, (1990) Effect of antiviral antibody on maintenance of long-term rubella virus persistent infection in Vero cells. J Virol 64: 5183-5187. PubMed: 2398541.
22. Miki NP, Chantler JK, (1992) Differential ability of wild-type and vaccine strains of rubella virus to replicate and persist in human joint tissue. Clin Exp Rheumatol 10: 3-12. PubMed: 1551276.
23. Oker-Blom C, Kalkkinen N, Kääriäinen L, Pettersson RF, (1983) Rubella virus contains one capsid protein and three envelope glycoproteins, E1, E2a, and E2b. J Virol 46: 964-973. PubMed: 6854740.
24. Chen MH, Zhu Z, Zhang Y, Favors S, Xu WB, et al. (2007) An indirect immunocolorimetric assay to detect rubella virus infected cells. J Virol Methods 146: 414-418. doi:10.1016/j.jviromet.2007.08.021. PubMed: 17919742.
25. Hübschen JM, Kremer JR, De Landtsheer S, Muller CP, (2008) A multiplex TaqMan PCR assay for the detection of measles and rubella virus. J Virol Methods 149: 246-250. doi:10.1016/j.jviromet.2008.01.032. PubMed: 18353451.
26. Abernathy E, Chen MH, Bera J, Shrivastava S, Kirkness E, et al. (2013) Analysis of whole genome sequences of 16 strains of rubella virus from the United States, 1961--2009. Virol J 10: 32. doi:10.1186/1743-422X-10-32. PubMed: 23351667.
27. Marin V, Kaplanski G, Grès S, Farnarier C, Bongrand P, (2001) Endothelial cell culture: protocol to obtain and cultivate human umbilical endothelial cells. J Immunol Methods 254: 183-190. doi:10.1016/S0022-1759(01)00408-2. PubMed: 11406163.
28. Abernathy ES, Hübschen JM, Muller CP, Jin L, Brown D, et al. (2011) Status of global virologic surveillance for rubella viruses. J Infect Dis 204 (Suppl 1):: S524-S532. doi:10.1093/infdis/jir099. PubMed: 21666209.
29. Liebhaber H, Riordan JT, Horstmann DM, (1967) Replication of rubella virus in a continuous line of African green monkey kidney cells (Vero). Proc Soc Exp Biol Med 125: 636-643. doi:10.3181/00379727-125-32167. PubMed: 4961494.
30. Hemphill ML, Forng RY, Abernathy ES, Frey TK, (1988) Time course of virus-specific macromolecular synthesis during rubella virus infection in Vero cells. Virology 162: 65-75. doi:10.1016/0042-6822(88)90395-9. PubMed: 3336944.
31. Bardeletti G, Tektoff J, Gautheron D, (1979) Rubella virus maturation and production in two host cell systems. Intervirology 11: 97-103. doi:10.1159/000149019. PubMed: 107143.
32. Liang Y, Gillam S, (2001) Rubella virus RNA replication is cis-preferential and synthesis of negative- and positive-strand RNAs is regulated by the processing of nonstructural protein. Virology 282: 307-319. doi:10.1006/viro.2001.0862. PubMed: 11289813.
33. Lee JY, Marshall JA, Bowden DS, (1992) Replication complexes associated with the morphogenesis of rubella virus. Arch Virol 122: 95-106. doi:10.1007/BF01321120. PubMed: 1729987.
34. Lee JY, Bowden DS, Marshall JA, (1996) Membrane junctions associated with rubella virus infected cells. J Submicrosc Cytol Pathol 28: 101-108. PubMed: 8929632.
35. Frey TK, (1994) Molecular biology of rubella virus. Adv Virus Res 44: 69-160. doi:10.1016/S0065-3527(08)60328-0. PubMed: 7817880.
36. Ilkow CS, Goping IS, Hobman TC, (2011) The Rubella Virus Capsid Is an Anti-Apoptotic Protein that Attenuates the Pore-Forming Ability of Bax. PLOS Pathog 7: e1001291. PubMed: 21379337.
37. Dieterich DC, Link AJ, Graumann J, Tirrell DA, Schuman EM, (2006) Selective identification of newly synthesized proteins in mammalian cells using bioorthogonal noncanonical amino acid tagging (BONCAT). Proc Natl Acad Sci U S A 103: 9482-9487. doi:10.1073/pnas.0601637103. PubMed: 16769897.
38. Sinzger C, Schmidt K, Knapp J, Kahl M, Beck R, et al. (1999) Modification of human cytomegalovirus tropism through propagation in vitro is associated with changes in the viral genome. J Gen Virol 80(Pt 11):: 2867-2877. PubMed: 10580048.
39. Pugachev KV, Abernathy ES, Frey TK, (1997) Improvement of the specific infectivity of the rubella virus (RUB) infectious clone: determinants of cytopathogenicity induced by RUB map to the nonstructural proteins. J Virol 71: 562-568. PubMed: 8985384.
40. Mo XY, Ma W, Zhang Y, Zhao H, Deng Y, et al. (2007) Microarray analyses of differentially expressed human genes and biological processes in ECV304 cells infected with rubella virus. J Med Virol 79: 1783-1791. doi:10.1002/jmv.20942. PubMed: 17854033.
41. Drexler HG, Quentmeier H, Dirks WG, MacLeod RA, (2002) Bladder carcinoma cell line ECV304 is not a model system for endothelial cells. In Vitro Cell Dev Biol Anim 38: 185-186; author reply 187 doi:10.1290/1071-2690(2002)038. PubMed: 12197766.
42. Vaheri A, Sedwick WD, Plotkin SA, Maes R, (1965) Cytopathic effect of rubella virus in BHK21 cells and growth to high titers in suspension culture. Virology 27: 239-241. doi:10.1016/0042-6822(65)90170-4. PubMed: 5320494.
43. Cunningham AL, Fraser JR, (1985) Persistent rubella virus infection of human synovial cells cultured in vitro. J Infect Dis 151: 638-645. doi:10.1093/infdis/151.4.638. PubMed: 3973414.
44. Numazaki K, Goldman H, Wong I, Wainberg MA, (1989) Infection of cultured human fetal pancreatic islet cells by rubella virus. Am J Clin Pathol 91: 446-451. PubMed: 2648801.
45. Sedwick WD, Sokol F, (1970) Nucleic acid of rubella virus and its replication in hamster kidney cells. J Virol 5: 478-489. PubMed: 5465639.
46. Adamo MP, Zapata M, Frey TK, (2008) Analysis of gene expression in fetal and adult cells infected with rubella virus. Virology 370: 1-11. doi:10.1016/j.virol.2007.08.003. PubMed: 17920097.
47. Maes R, Vaheri A, Sedwick D, Plotkin S, (1966) Synthesis of virus and macromolecules by rubella-infected cells. Nature 210: 384-385. doi:10.1038/210384a0. PubMed: 4960358.
48. Esterly JR, Slusser RJ, Ruebner BH, (1967) Hepatic lesions in the congenital rubella syndrome. J Pediatr 71: 676-685. doi:10.1016/S0022-3476(67)80203-8. PubMed: 6069661.
49. Seno A, Tada J, Matsuura H, Arata J, Isomura H, et al. (1994) Congenital rubella syndrome with rubella virus-associated generalized brownish macules, indurated erythemas, papules, and pigmentation. J Dermatol 21: 323-328. PubMed: 8051318.
50. Urade M, Hamada S, Sugi M, Shirasuna K, Komatsu M, et al. (1981) Persistent rubella virus infection in primary rat embryonic cells. I. Biological properties of the persistently infected cells. J Osaka Univ Dent Sch 21: 165-173. PubMed: 6954266.
51. Domegan LM, Atkins GJ, (2002) Apoptosis induction by the Therien and vaccine RA27/3 strains of rubella virus causes depletion of oligodendrocytes from rat neural cell cultures. J Gen Virol 83: 2135-2143. PubMed: 12185266.
52. Datta YH, Ewenstein BM, (2001) Regulated secretion in endothelial cells: biology and clinical implications. Thromb Haemost 86: 1148-1155. PubMed: 11816699.
53. Boué JG, Boué A, (1969) Effects of rubella virus infection on the division of human cells. Am J Dis Child 118: 45-48. PubMed: 5790244.
54. Stanwick TL, Hallum JV, (1974) Role of interferon in six cell lines persistently infected with rubella virus. Infect Immun 10: 810-815. PubMed: 4214783.
55. Heggie AD, (1977) Growth inhibition of human embryonic and fetal rat bones in organ culture by rubella virus. Teratology 15: 47-55. doi:10.1002/tera.1420150107. PubMed: 138959.
56. Atreya CD, Kulkarni S, Mohan KV, (2004) Rubella virus P90 associates with the cytokinesis regulatory protein Citron-K kinase and the viral infection and constitutive expression of P90 protein both induce cell cycle arrest following S phase in cell culture. Arch Virol 149: 779-789. doi:10.1007/s00705-003-0267-6. PubMed: 15045564.
57. Mifune K, Desmyter J, Rawls WE, (1970) Effect of Exogenous Interferon on Rubella Virus Production in Carrier Cultures of Cells Defective in Interferon Production. Infect Immun 2: 132-138. PubMed: 16557810.
58. Andzhdaparidze OG, Desiatskova RG, Bogomolova NN, Cheliapov NV, Boriskin IuS, (1981) Chronic rubella virus-induced infection of human continuous cells. Vopr Virusol: pp. 586-592. PubMed: 6278775.
59. Friedman HM, (1989) Infection of endothelial cells by common human viruses. Rev Infect Dis 11 (Suppl 4):: S700-S704. doi:10.1093/clinids/11.Supplement_4.S700. PubMed: 2665008.
60. Conaldi PG, Serra C, Mossa A, Falcone V, Basolo F, et al. (1997) Persistent infection of human vascular endothelial cells by group B coxsackieviruses. J Infect Dis 175: 693-696. doi:10.1093/infdis/175.3.693. PubMed: 9041346.
61. Kahl M, Siegel-Axel D, Stenglein S, Jahn G, Sinzger C, (2000) Efficient lytic infection of human arterial endothelial cells by human cytomegalovirus strains. J Virol 74: 7628-7635. doi:10.1128/JVI.74.16.7628-7635.2000. PubMed: 10906217.
62. Suárez AL, van Dyk LF, (2008) Endothelial cells support persistent gammaherpesvirus 68 infection. PLOS Pathog 4: e1000152. PubMed: 18787698.
63. Rima BK, Duprex WP, (2005) Molecular mechanisms of measles virus persistence. Virus Res 111: 132-147. doi:10.1016/j.virusres.2005.04.005. PubMed: 15893837.
64. Griffin DE, Lin WH, Pan CH, (2012) Measles virus, immune control, and persistence. FEMS Microbiol Rev 36: 649-662. doi:10.1111/j.1574-6976.2012.00330.x. PubMed: 22316382.
65. Campbell PE, (1965) Vascular abnormalities following maternal rubella. Br Heart J 27: 134-138. doi:10.1136/hrt.27.1.134. PubMed: 14242155.
66. Malek AM, Alper SL, Izumo S, (1999) Hemodynamic shear stress and its role in atherosclerosis. JAMA 282: 2035-2042. doi:10.1001/jama.282.21.2035. PubMed: 10591386.
67. Davies PF, (2009) Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat Clin Pract Cardiovasc Med 6: 16-26. doi:10.1038/ncpcardio1397. PubMed: 19029993.
68. Gabrielli L, Bonasoni MP, Lazzarotto T, Lega S, Santini D, et al. (2009) Histological findings in foetuses congenitally infected by cytomegalovirus. J Clin Virol 46 (Suppl 4):: S16-S21. doi:10.1016/S1386-6532(09)70088-5. PubMed: 19879801.
69. Cheeran MC, Lokensgard JR, Schleiss MR, (2009) Neuropathogenesis of congenital cytomegalovirus infection: disease mechanisms and prospects for intervention. Clin Microbiol Rev 22: 99-126, Table of Contents doi:10.1128/CMR.00023-08. PubMed: 19136436.
70. Ricotta D, Alessandri G, Pollara C, Fiorentini S, Favilli F, et al. (2001) Adult human heart microvascular endothelial cells are permissive for non-lytic infection by human cytomegalovirus. Cardiovasc Res 49: 440-448. doi:10.1016/S0008-6363(00)00258-3. PubMed: 11164854.
71. Jarvis MA, Nelson JA, (2002) Human cytomegalovirus persistence and latency in endothelial cells and macrophages. Curr Opin Microbiol 5: 403-407. doi:10.1016/S1369-5274(02)00334-X. PubMed: 12160860.
72. Adler B, Sinzger C, (2009) Endothelial cells in human cytomegalovirus infection: one host cell out of many or a crucial target for virus spread? Thromb Haemost 102: 1057-1063. PubMed: 19967135.
73. Streblow DN, Dumortier J, Moses AV, Orloff SL, Nelson JA, (2008) Mechanisms of cytomegalovirus-accelerated vascular disease: induction of paracrine factors that promote angiogenesis and wound healing. Curr Top Microbiol Immunol 325: 397-415. doi:10.1007/978-3-540-77349-8_22. PubMed: 18637518.
74. Epstein SE, Zhu J, Najafi AH, Burnett MS, (2009) Insights into the role of infection in atherogenesis and in plaque rupture. Circulation 119: 3133-3141. doi:10.1161/CIRCULATIONAHA.109.849455. PubMed: 19546396.
75. Popović M, Smiljanić K, Dobutović B, Syrovets T, Simmet T, et al. (2012) Human cytomegalovirus infection and atherothrombosis. J Thromb Thrombolysis 33: 160-172. doi:10.1007/s11239-011-0662-x. PubMed: 22161772.