Human astrocytic cells support persistent coxsackievirus B3 infection

Journal of Virology

Volumn 87, Issue 22, 2013, Pages 12407-12421

  Zhang, Xiaowei ^a   Zheng, Zhenhua ^a   Shu, Bo ^a   Liu, Xijuan ^a   Zhang, Zhenfeng ^a   Liu, Yan ^a   Bai, Bingke ^b   Hu, Qinxue ^a   Mao, Panyong ^b   Wang, Hanzhong ^a  

^a WUHAN INSTITUTE OF VIROLOGY   (China)

^b BEIJING 302 HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CHONDROITIN SULFATE; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; DECAY ACCELERATING FACTOR; GENOMIC RNA; GREEN FLUORESCENT PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; VASCULAR CELL ADHESION MOLECULE 1; VIRUS ANTIGEN; VIRUS RNA; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR LIKE MEMBRANE PROTEIN; MESSENGER RNA; VIRUS PROTEIN;

ARTICLE; ASTROCYTE; BRAIN CELL; CANCER CELL CULTURE; CELL SURFACE; CONTROLLED STUDY; COXSACKIE VIRUS A; COXSACKIE VIRUS A9; COXSACKIE VIRUS INFECTION; CYTOKINE RELEASE; DISEASE PREDISPOSITION; ENTEROVIRUS 71; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; NUCLEOTIDE SEQUENCE; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; UPREGULATION; VIRION; VIRUS INHIBITION; CELL CULTURE; ENTEROVIRUS; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; PATHOGENICITY; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL; VIROLOGY; VIRUS REPLICATION; WESTERN BLOTTING;

ADENOVIRIDAE; COXSACKIEVIRUS; ENTEROVIRUS; HUMAN ENTEROVIRUS 71;

ANTIGENS, CD55; ASTROCYTES; BLOTTING, WESTERN; CELLS, CULTURED; COXSACKIE AND ADENOVIRUS RECEPTOR-LIKE MEMBRANE PROTEIN; COXSACKIEVIRUS INFECTIONS; ENTEROVIRUS B, HUMAN; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; INTERFERON-BETA; INTERLEUKIN-6; INTERLEUKIN-8; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, VIRAL; STEM CELLS; VIRAL PROTEINS; VIRION; VIRUS REPLICATION;

EID: 84886265514     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02090-13     Document Type: Article

References (74)

1. Nasri D, Bouslama L, Pillet S, Bourlet T, Aouni M, Pozzetto B. 2007. Basic rationale, current methods and future directions for molecular typing of human enterovirus. Expert Rev. Mol. Diagn. 7:419-434.
2. Knowles NJ, Hovi T, Hyypiä T, King AMQ, Lindberg AM, Pallansch MA, Palmenberg AC, Simmonds P, Skern T, Stanway G, Yamashita T, Zell R. 2012. Picornaviridae, p 855-880. In King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (ed), Virus taxonomy: classification and nomenclature of viruses. Ninth report of the International Committee on Taxonomy of Viruses. Elsevier, San Diego, CA.
3. Hober D, Sauter P. 2010. Pathogenesis of type 1 diabetes mellitus: interplay between enterovirus and host. Nat. Rev. Endocrinol. 6:279-289.
4. Baboonian C, Treasure T. 1997. Meta-analysis of the association of enteroviruses with human heart disease. Heart 78:539-543.
5. Jacques J, Moret H, Minette D, Leveque N, Jovenin N, Deslee G, Lebargy F, Motte J, Andreoletti L. 2008. Epidemiological, molecular, and clinical features of enterovirus respiratory infections in French children between 1999 and 2005. J. Clin. Microbiol. 46:206-213.
6. Michos AG, Syriopoulou VP, Hadjichristodoulou C, Daikos GL, Laguna E, Douridas P, Mostrou G, Theodoridou M. 2007. Aseptic meningitis in children: analysis of 506 cases. PLoS One 2:e674. doi:10.1371/journal.pone.0000674.
7. Rhoades RE, Tabor-Godwin JM, Tsueng G, Feuer R. 2011. Enterovirus infections of the central nervous system. Virology 411:288-305.
8. Whitton JL, Cornell CT, Feuer R. 2005. Host and virus determinants of picornavirus pathogenesis and tropism. Nat. Rev. Microbiol. 3:765-776.
9. Kim K-S, Tracy S, Tapprich W, Bailey J, Lee C-K, Kim K, Barry W, Chapman N. 2005. 5=-terminal deletions occur in coxsackievirus B3 during replication in murine hearts and cardiac myocyte cultures and correlate with encapsidation of negative-strand viral RNA. J. Virol. 79:7024-7041.
10. Chia J, Chia A, Voeller M, Lee T, Chang R. 2010. Acute enterovirus infection followed by myalgic encephalomyelitis/chronic fatigue syndrome (ME/CFS) and viral persistence. J. Clin. Pathol. 63:165-168.
11. Chapman NM, Kim KS. 2008. Persistent coxsackievirus infection: enterovirus persistence in chronic myocarditis and dilated cardiomyopathy. Curr. Top. Microbiol. 323:275-292.
12. Muir P, Nicholson F, Tilzey AJ, Signy M, English TA, Banatvala JE. 1989. Chronic relapsing pericarditis and dilated cardiomyopathy: serological evidence of persistent enterovirus infection. Lancet i:804-807.
13. Bridgens R, Sturman S, Davidson C, Expert BPFs. 2010. Post-polio syndrome-polio's legacy. Clin. Med. 10:213-214.
14. Leparc-Goffart I, Julien J, Fuchs F, Janatova I, Aymard M, Kopecka H. 1996. Evidence of presence of poliovirus genomic sequences in cerebrospinal fluid from patients with postpolio syndrome. J. Clin. Microbiol. 34:2023-2026.
15. Jaidane H, Caloone D, Lobert PE, Sane F, Dardenne O, Naquet P, Gharbi J, Aouni M, Geenen V, Hober D. 2012. Persistent infection of thymic epithelial cells with coxsackievirus B4 results in decreased expression of type 2 insulin-like growth factor. J. Virol. 86:11151-11162.
16. Brilot F, Chehadeh W, Charlet-Renard C, Martens H, Geenen V, Hober D. 2002. Persistent infection of human thymic epithelial cells by coxsackievirus B4. J. Virol. 76:5260-5265.
17. Zanone MM, Favaro E, Conaldi PG, Greening J, Bottelli A, Perin PC, Klein NJ, Peakman M, Camussi G. 2003. Persistent infection of human microvascular endothelial cells by coxsackie B viruses induces increased expression of adhesion molecules. J. Immunol. 171:438-446.
18. Heim A, Canu A, Kirschner P, Simon T, Mall G, Hofschneider PH, Kandolf R. 1992. Synergistic interaction of interferon-beta and interferon-gamma in coxsackievirus B3-infected carrier cultures of human myocardial fibroblasts. J. Infect. Dis. 166:958-965.
19. Heim A, Grumbach I, Pring-Akerblom P, Stille-Siegener M, Muller G, Kandolf R, Figulla HR. 1997. Inhibition of coxsackievirus B3 carrier state infection of cultured human myocardial fibroblasts by ribavirin and human natural interferon-alpha. Antiviral Res. 34:101-111.
20. Heim A, Brehm C, Stille-Siegener M, Muller G, Hake S, Kandolf R, Figulla HR. 1995. Cultured human myocardial fibroblasts of pediatric origin: natural human interferon-alpha is more effective than recombinant interferon-alpha 2a in carrier-state coxsackievirus B3 replication. J. Mol. Cell. Cardiol. 27:2199-2208.
21. Conaldi PG, Biancone L, Bottelli A, De Martino A, Camussi G, Toniolo A. 1997. Distinct pathogenic effects of group B coxsackieviruses on human glomerular and tubular kidney cells. J. Virol. 71:9180-9187.
22. Pinkert S, Klingel K, Lindig V, Dorner A, Zeichhardt H, Spiller OB, Fechner H. 2011. Virus-host coevolution in a persistently coxsackievirus B3-infected cardiomyocyte cell line. J. Virol. 85:13409-13419.
23. Chapman NM, Kim K-S, Drescher KM, Oka K, Tracy S. 2008. 5= terminal deletions in the genome of a coxsackievirus B2 strain occurred naturally in human heart. Virology 375:480-491.
24. Tam PE, Messner RP. 1999. Molecular mechanisms of coxsackievirus persistence in chronic inflammatory myopathy: viral RNA persists through formation of a double-stranded complex without associated genomic mutations or evolution. J. Virol. 73:10113-10121.
25. Feuer R, Ruller CM, An N, Tabor-Godwin JM, Rhoades RE, Maciejewski S, Pagarigan RR, Cornell CT, Crocker SJ, Kiosses WB. 2009. Viral persistence and chronic immunopathology in the adult central nervous system following coxsackievirus infection during the neonatal period. J. Virol. 83:9356-9369.
26. Gosselin A-S, Simonin Y, Guivel-Benhassine F, Rincheval V, Vayssiere J-L, Mignotte B, Colbere-Garapin F, Couderc T, Blondel B. 2003. Poliovirus-induced apoptosis is reduced in cells expressing a mutant CD155 selected during persistent poliovirus infection in neuroblastoma cells. J. Virol. 77:790-798.
27. Pavio N, Couderc T, Girard S, Sgro JY, Blondel B, Colbere-Garapin F. 2000. Expression of mutated poliovirus receptors in human neuroblastoma cells persistently infected with poliovirus. Virology 274:331-342.
28. Gibson JP, Righthand VF. 1985. Persistence of echovirus 6 in cloned human cells. J. Virol. 54:219-223.
29. Griffin DE. 2003. Immune responses to RNA-virus infections of the CNS. Nat. Rev. Immunol. 3:493-502.
30. Bergmann CC, Lane TE, Stohlman SA. 2006. Coronavirus infection of the central nervous system: host-virus stand-off. Nat. Rev. Microbiol. 4:121-132.
31. Muir P, Nicholson F, Sharief MK, Thompson EJ, Cairns NJ, Lantos P, Spencer GT, Kaminski HJ, Banatvala JE. 1995. Evidence for persistent enterovirus infection of the central nervous system in patients with previous paralytic poliomyelitis. Ann. N. Y. Acad. Sci. 753:219-232.
32. Berger MM, Kopp N, Vital C, Redl B, Aymard M, Lina B. 2000. Detection and cellular localization of enterovirusRNAsequences in spinal cord of patients with ALS. Neurology 54:20-25.
33. Stacey G, Viviani B. 2001. Cell culture models for neurotoxicology. Cell Biol. Toxicol. 17:319-334.
34. Stein GH. 1979. T98G: an anchorage-independent human tumor cell line that exhibits stationary phase G1 arrest in vitro. J. Cell. Physiol. 99:43-54.
35. Chen L, Zhang X, Zhou G, Xiang X, Ji X, Zheng Z, He Z, Wang H. 2012. Simultaneous determination of human enterovirus 71 and coxsackievirus B3 by dual-color quantum dots and homogeneous immunoassay. Anal. Chem. 84:3200-3207.
36. Luo MH, Hannemann H, Kulkarni AS, Schwartz PH, O'Dowd JM, Fortunato EA. 2010. Human cytomegalovirus infection causes premature and abnormal differentiation of human neural progenitor cells. J. Virol. 84:3528-3541.
37. Luo MH, Schwartz PH, Fortunato EA. 2008. Neonatal neural progenitor cells and their neuronal and glial cell derivatives are fully permissive for human cytomegalovirus infection. J. Virol. 82:9994-10007.
38. Arndt U, Wennemuth G, Barth P, Nain M, Al-Abed Y, Meinhardt A, Gemsa D, Bacher M. 2002. Release of macrophage migration inhibitory factor and CXCL8/interleukin-8 from lung epithelial cells rendered necrotic by influenza A virus infection. J. Virol. 76:9298-9306.
39. Lee C-J, Lin H-R, Liao C-L, Lin Y-L. 2008. Cholesterol effectively blocks entry of flavivirus. J. Virol. 82:6470-6480.
40. Huber S, Haisch C, Lodge P. 1990. Functional diversity in vascular endothelial cells: role in coxsackievirus tropism. J. Virol. 64:4516-4522.
41. Bessaud M, Autret A, Jegouic S, Balanant J, Joffret ML, Delpeyroux F. 2008. Development of a TaqMan RT-PCR assay for the detection and quantification of negatively stranded RNA of human enteroviruses: evidence for false-priming and improvement by tagged RT-PCR. J. Virol. Methods 153:182-189.
42. Shafren DR, Williams DT, Barry RD. 1997. A decay-accelerating factorbinding strain of coxsackievirus B3 requires the coxsackievirusadenovirus receptor protein to mediate lytic infection of rhabdomyosarcoma cells. J. Virol. 71:9844-9848.
43. Schowalter RM, Pastrana DV, Buck CB. 2011. Glycosaminoglycans and sialylated glycans sequentially facilitate Merkel cell polyomavirus infectious entry. PLoS Pathog. 7:e1002161. doi:10.1371/journal.ppat.1002161.
44. Klump WM, Bergmann I, Muller BC, Ameis D, Kandolf R. 1990. Complete nucleotide sequence of infectious coxsackievirus B3 cDNA: two initial 5= uridine residues are regained during plus-strand RNA synthesis. J. Virol. 64:1573-1583.
45. Melchers WJ, Hoenderop JG, Bruins Slot HJ, Pleij CW, Pilipenko EV, Agol VI, Galama JM. 1997. Kissing of the two predominant hairpin loops in the coxsackie B virus 3= untranslated region is the essential structural feature of the origin of replication required for negative-strand RNA synthesis. J. Virol. 71:686-696.
46. Harkins S, Cornell CT, Whitton JL. 2005. Analysis of translational initiation in coxsackievirus B3 suggests an alternative explanation for the high frequency of R+4 in the eukaryotic consensus motif. J. Virol. 79:987-996.
47. Sawicki SG, Lu JH, Holmes KV. 1995. Persistent infection of cultured cells with mouse hepatitis virus (MHV) results from the epigenetic expression of the MHV receptor. J. Virol. 69:5535-5543.
48. Chehadeh W, Kerr-Conte J, Pattou F, Alm G, Lefebvre J, Wattre P, Hober D. 2000. Persistent infection of human pancreatic islets by coxsackievirus B is associated with alpha interferon synthesis in beta cells. J. Virol. 74:10153-10164.
49. Ferenczy MW, Johnson KR, Marshall LJ, Monaco MC, Major EO. 2013. Differentiation of human fetal multipotential neural progenitor cells to astrocytes reveals susceptibility factors for JC virus. J. Virol. 87:6221-6231.
50. Khetsuriani N, Lamonte-Fowlkes A, Oberst S, Pallansch MA. 2006. Enterovirus surveillance-United States, 1970-2005. MMWR Surveill Summ. 55(SS-08):1-20.
51. Tao Z, Song Y, Li Y, Liu Y, Jiang P, Lin X, Liu G, Song L, Wang H, Xu A. 2012. Coxsackievirus B3, Shandong Province, China, 1990-2010. Emerg. Infect. Dis. 18:1865-1867.
52. Wang YF, Chou CT, Lei HY, Liu CC, Wang SM, Yan JJ, Su IJ, Wang JR, Yeh TM, Chen SH, Yu CK. 2004. A mouse-adapted enterovirus 71 strain causes neurological disease in mice after oral infection. J. Virol. 78:7916-7924.
53. Wen YY, Chang TY, Chen ST, Li C, Liu HS. 2003. Comparative study of enterovirus 71 infection of human cell lines. J. Med. Virol. 70:109-118.
54. Girard S, Couderc T, Destombes J, Thiesson D, Delpeyroux F, Blondel B. 1999. Poliovirus induces apoptosis in the mouse central nervous system. J. Virol. 73:6066-6072.
55. Tabor-Godwin JM, Ruller CM, Bagalso N, An N, Pagarigan RR, Harkins S, Gilbert PE, Kiosses WB, Gude NA, Cornell CT, Doran KS, Sussman MA, Whitton JL, Feuer R. 2010. A novel population of myeloid cells responding to coxsackievirus infection assists in the dissemination of virus within the neonatal CNS. J. Neurosci. 30:8676-8691.
56. Feuer R, Mena I, Pagarigan RR, Harkins S, Hassett DE, Whitton JL. 2003. Coxsackievirus B3 and the neonatal CNS: the roles of stem cells, developing neurons, and apoptosis in infection, viral dissemination, and disease. Am. J. Pathol. 163:1379-1393.
57. Conaldi PG, Serra C, Mossa A, Falcone V, Basolo F, Camussi G, Dolei A, Toniolo A. 1997. Persistent infection of human vascular endothelial cells by group B coxsackieviruses. J. Infect. Dis. 175:693-696.
58. Matteucci D, Paglianti M, Giangregorio AM, Capobianchi MR, Dianzani F, Bendinelli M. 1985. Group B coxsackieviruses readily establish persistent infections in human lymphoid cell lines. J. Virol. 56:651-654.
59. Werk D, Schubert S, Lindig V, Grunert HP, Zeichhardt H, Erdmann VA, Kurreck J. 2005. Developing an effective RNA interference strategy against a plus-strand RNA virus: silencing of coxsackievirus B3 and its cognate coxsackievirus-adenovirus receptor. Biol. Chem. 386:857-863.
60. Fechner H, Pinkert S, Wang X, Sipo I, Suckau L, Kurreck J, Dorner A, Sollerbrant K, Zeichhardt H, Grunert HP, Vetter R, Schultheiss HP, Poller W. 2007. Coxsackievirus B3 and adenovirus infections of cardiac cells are efficiently inhibited by vector-mediated RNA interference targeting their common receptor. Gene Ther. 14:960-971.
61. Zautner AE, Korner U, Henke A, BadorffC, Schmidtke M. 2003. Heparan sulfates and coxsackievirus-adenovirus receptor: each one mediates coxsackievirus B3 PD infection. J. Virol. 77:10071-10077.
62. Tan CW, Poh CL, Sam IC, Chan YF. 2013. Enterovirus 71 uses cell surface heparan sulfate glycosaminoglycan as an attachment receptor. J. Virol. 87:611-620.
63. de Boer SM, Kortekaas J, de Haan CA, Rottier PJ, Moormann RJ, Bosch BJ. 2012. Heparan sulfate facilitates Rift Valley fever virus entry into the cell. J. Virol. 86:13767-13771.
64. McLeish NJ, Williams CH, Kaloudas D, Roivainen MM, Stanway G. 2012. Symmetry-related clustering of positive charges is a common mechanism for heparan sulfate binding in enteroviruses. J. Virol. 86:11163-11170.
65. Zautner AE, Jahn B, Hammerschmidt E, Wutzler P, Schmidtke M. 2006. N- and 6-O-sulfated heparan sulfates mediate internalization of coxsackievirus B3 variant PD into CHO-K1 cells. J. Virol. 80:6629-6636.
66. Goodfellow IG, Sioofy AB, Powell RM, Evans DJ. 2001. Echoviruses bind heparan sulfate at the cell surface. J. Virol. 75:4918-4921.
67. Misinzo G, Delputte PL, Meerts P, Lefebvre DJ, Nauwynck HJ. 2006. Porcine circovirus 2 uses heparan sulfate and chondroitin sulfate B glycosaminoglycans as receptors for its attachment to host cells. J. Virol. 80:3487-3494.
68. Kim E, Okumura M, Sawa H, Miyazaki T, Fujikura D, Yamada S, Sugahara K, Sasaki M, Kimura T. 2011. Paradoxical effects of chondroitin sulfate-E on Japanese encephalitis viral infection. Biochem. Biophys. Res. Commun. 409:717-722.
69. Dow KE, Wang W. 1998. Cell biology of astrocyte proteoglycans. Cell. Mol. Life Sci. 54:567-581.
70. Tanaka N, Sato M, Lamphier MS, Nozawa H, Oda E, Noguchi S, Schreiber RD, Tsujimoto Y, Taniguchi T. 1998. Type I interferons are essential mediators of apoptotic death in virally infected cells. Genes Cells 3:29-37.
71. Balachandran S, Roberts PC, Kipperman T, Bhalla KN, Compans RW, Archer DR, Barber GN. 2000. Alpha/beta interferons potentiate virusinduced apoptosis through activation of the FADD/caspase-8 death signaling pathway. J. Virol. 74:1513-1523.
72. Nair A, Frederick TJ, Miller SD. 2008. Astrocytes in multiple sclerosis: a product of their environment. Cell. Mol. Life Sci. 65:2702-2720.
73. Hosking MP, Lane TE. 2010. The role of chemokines during viral infection of the CNS. PLoS Pathog. 6:e1000937. doi:10.1371/journal.ppat.1000937.
74. Narasipura SD, Henderson LJ, Fu SW, Chen L, Kashanchi F, Al-Harthi L. 2012. Role of beta-catenin and TCF/LEF family members in transcriptional activity of HIV in astrocytes. J. Virol. 86:1911-1921.