Morphology and Molecular Composition of Purified Bovine Viral Diarrhea Virus Envelope

PLoS Pathogens

Volumn 12, Issue 3, 2016, Pages

  Callens, Nathalie ^a   Brügger, Britta ^b   Bonnafous, Pierre ^c   Drobecq, Hervé ^a   Gerl, Mathias J ^b   Krey, Thomas ^d,e,h   Roman Sosa, Gleyder ^f   Rümenapf, Till ^g   Lambert, Olivier ^c   Dubuisson, Jean ^a   Rouillé, Yves ^a  

^a UNIV LILLE   (France)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d INSTITUT PASTEUR   (France)

^e Institut Pasteur   (France)

^f FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^g UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^h HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CD9 ANTIGEN; CHOLESTEROL; GLYCOPROTEIN E1; GLYCOPROTEIN E2; HEXOSYL CERAMIDE; IMMUNOGLOBULIN G ANTIBODY; LACTADHERIN; LIPID; LIPOCORTIN 2; METHYL BETA CYCLODEXTRIN; MONOCLONAL ANTIBODY; POLYCLONAL ANTIBODY; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE; UNCLASSIFIED DRUG; VIRUS ANTIBODY; CAPSID PROTEIN; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOCHEMICAL COMPOSITION; BOVINE VIRAL DIARRHEA; CELL CULTURE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; DIMERIZATION; ENDOPLASMIC RETICULUM; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOFLUORESCENCE TEST; LIPID COMPOSITION; LIPID RAFT; MASS SPECTROMETRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; RABBIT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRION; VIRUS ENVELOPE; VIRUS MORPHOGENESIS; VIRUS NEUTRALIZATION; VIRUS PARTICLE; VIRUS PURIFICATION; VIRUS TITRATION; WESTERN BLOTTING; ANIMAL; BOVINE; CELL LINE; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; PESTIVIRUS; ULTRASTRUCTURE;

ANIMALS; CAPSID PROTEINS; CATTLE; CELL LINE; CRYOELECTRON MICROSCOPY; DIARRHEA VIRUSES, BOVINE VIRAL; ENDOPLASMIC RETICULUM; VIRAL ENVELOPE PROTEINS; VIRION;

EID: 84962428831     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005476     Document Type: Article

References (61)

1. Lindenbach BD, Thiel H-J, Rice CM. Flaviviridae: the viruses and their replication. Knipe DM, Howley PM, editors. Fields Virology. 5 ed. Philadelphia; 2007;: 1101–1152.
2. Rey FA, Heinz FX, Mandl C, Kunz C, Harrison SC, The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature. 1995;375: 291–298. doi: 10.1038/375291a07753193
3. Kuhn RJ, Zhang W, Rossmann MG, Pletnev SV, Corver J, Lenches E, et al. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell. 2002;108: 717–725. 11893341
4. Bartenschlager R, Penin F, Lohmann V, André P, Assembly of infectious hepatitis C virus particles. Trends Microbiol. 2011;19: 95–103. doi: 10.1016/j.tim.2010.11.00521146993
5. Lindenbach BD, Rice CM, The ins and outs of hepatitis C virus entry and assembly. Nat Rev Micro. 2013;11: 688–700. doi: 10.1038/nrmicro3098
6. Merz A, Long G, Hiet M-S, Brügger B, Chlanda P, André P, et al. Biochemical and morphological properties of hepatitis C virus particles and determination of their lipidome. J Biol Chem. 2011;286: 3018–3032. doi: 10.1074/jbc.M110.17501821056986
7. Catanese MT, Uryu K, Kopp M, Edwards TJ, Andrus L, Rice WJ, et al. Ultrastructural analysis of hepatitis C virus particles. Proc Natl Acad Sci USA. 2013;110: 9505–9510. doi: 10.1073/pnas.130752711023690609
8. Scholtes C, Ramière C, Rainteau D, Perrin-Cocon L, Wolf C, Humbert L, et al. High plasma level of nucleocapsid-free envelope glycoprotein-positive lipoproteins in hepatitis C patients. Hepatology. 2012;56: 39–48. doi: 10.1002/hep.2562822290760
9. Icard V, Diaz O, Scholtes C, Perrin-Cocon L, Ramière C, Bartenschlager R, et al. Secretion of hepatitis C virus envelope glycoproteins depends on assembly of apolipoprotein B positive lipoproteins. PLoS ONE. 2009;4: e4233. doi: 10.1371/journal.pone.000423319156195
10. Omari El K, Iourin O, Harlos K, Grimes JM, Stuart DI, Structure of a pestivirus envelope glycoprotein E2 clarifies its role in cell entry. Cell Rep. 2013;3: 30–35. doi: 10.1016/j.celrep.2012.12.00123273918
11. Li Y, Wang J, Kanai R, Modis Y, Crystal structure of glycoprotein E2 from bovine viral diarrhea virus. Proc Natl Acad Sci USA. 2013;110: 6805–6810. doi: 10.1073/pnas.130052411023569276
12. Kong L, Giang E, Nieusma T, Kadam RU, Cogburn KE, Hua Y, et al. Hepatitis C virus e2 envelope glycoprotein core structure. Science. 2013;342: 1090–1094. doi: 10.1126/science.124387624288331
13. Khan AG, Whidby J, Miller MT, Scarborough H, Zatorski AV, Cygan A, et al. Structure of the core ectodomain of the hepatitis C virus envelope glycoprotein 2. Nature. 2014;509: 381–384. doi: 10.1038/nature1311724553139
14. Tautz N, Tews BA, Meyers G, The Molecular Biology of Pestiviruses. Adv Virus Res. 2015;93: 47–160. doi: 10.1016/bs.aivir.2015.03.00226111586
15. Weiland F, Weiland E, Unger G, Saalmüller A, Thiel HJ, Localization of pestiviral envelope proteins E(rns) and E2 at the cell surface and on isolated particles. J Gen Virol. 1999;80: 1157–1165. 10355762
16. Schmeiser S, Mast J, Thiel H-J, König M, Morphogenesis of pestiviruses: new insights from ultrastructural studies of strain Giraffe-1. J Virol. 2014;88: 2717–2724. doi: 10.1128/JVI.03237-1324352462
17. Riedel C, Lamp B, Heimann M, König M, Blome S, Moennig V, et al. The core protein of classical Swine Fever virus is dispensable for virus propagation in vitro. PLoS Pathog. 2012;8: e1002598. doi: 10.1371/journal.ppat.100259822457622
18. Pritchett R, Manning JS, Zee YC, Characterization of bovine viral diarrhea virus RNA. J Virol. 1975;15: 1342–1347. 1170338
19. Laude H, Nonarbo-togaviridae: comparative hydrodynamic properties of the pestivirus genus. Brief report. Arch Virol. 1979;62: 347–352. 232414
20. Ganser-Pornillos BK, Yeager M, Sundquist WI, The structural biology of HIV assembly. Curr Opin Struct Biol. 2008;18: 203–217. doi: 10.1016/j.sbi.2008.02.00118406133
21. Bonnafous P, Perrault M, Le Bihan O, Bartosch B, Lavillette D, Penin F, et al. Characterization of hepatitis C viral pseudoparticles by cryo-electron microscopy usingfunctionalized magnetic nanobeads. Journal of General Virology. 2010;91 (Pt 8): 1919–1930. doi: 10.1099/vir.0.021071–020375221
22. Krey T, Thiel H-J, Rümenapf T, Acid-resistant bovine pestivirus requires activation for pH-triggered fusion during entry. J Virol. 2005;79: 4191–4200. doi: 10.1128/JVI.79.7.4191–4200.200515767420
23. Weiland E, Stark R, Haas B, Rümenapf T, Meyers G, Thiel HJ, Pestivirus glycoprotein which induces neutralizing antibodies forms part of a disulfide-linked heterodimer. J Virol. 1990;64: 3563–3569. 2370675
24. Branza-Nichita N, Durantel D, Carrouee-Durantel S, Dwek RA, Zitzmann N, Antiviral effect of N-butyldeoxynojirimycin against bovine viral diarrhea virus correlates with misfolding of E2 envelope proteins and impairment of their association into E1-E2 heterodimers. J Virol. 2001;75: 3527–3536. doi: 10.1128/JVI.75.8.3527–3536.200111264342
25. Thiel HJ, Stark R, Weiland E, Rümenapf T, Meyers G, Hog cholera virus: molecular composition of virions from a pestivirus. J Virol. 1991;65: 4705–4712. 1870198
26. Langedijk JPM, van Veelen PA, Schaaper WMM, de Ru AH, Meloen RH, Hulst MM, A structural model of pestivirus E(rns) based on disulfide bond connectivity and homology modeling reveals an extremely rare vicinal disulfide. J Virol. 2002;76: 10383–10392. 12239315
27. Simpson RJ, Jensen SS, Lim JWE, Proteomic profiling of exosomes: current perspectives. Proteomics. 2008;8: 4083–4099. doi: 10.1002/pmic.20080010918780348
28. van Niel G, Porto-Carreiro I, Simoes S, Raposo G, Exosomes: a common pathway for a specialized function. J Biochem. 2006;140: 13–21. doi: 10.1093/jb/mvj12816877764
29. Brügger B, Glass B, Haberkant P, Leibrecht I, Wieland FT, Kräusslich H-G, The HIV lipidome: a raft with an unusual composition. Proc Natl Acad Sci USA. 2006;103: 2641–2646. doi: 10.1073/pnas.051113610316481622
30. Kalvodova L, Sampaio JL, Cordo S, Ejsing CS, Shevchenko A, Simons K, The lipidomes of vesicular stomatitis virus, semliki forest virus, and the host plasma membrane analyzed by quantitative shotgun mass spectrometry. J Virol. 2009;83: 7996–8003. doi: 10.1128/JVI.00635-0919474104
31. Gerl MJ, Sampaio JL, Urban S, Kalvodova L, Verbavatz J-M, Binnington B, et al. Quantitative analysis of the lipidomes of the influenza virus envelope and MDCK cell apical membrane. J Cell Biol. 2012;196: 213–221. doi: 10.1083/jcb.20110817522249292
32. van Meer G, Voelker DR, Feigenson GW, Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol. 2008;9: 112–124. doi: 10.1038/nrm233018216768
33. Lingwood D, Simons K, Lipid Rafts As a Membrane-Organizing Principle. Science. 2010;327: 46–50. doi: 10.1126/science.117462120044567
34. Brown DA, Rose JK, Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 1992;68: 533–544. 1531449
35. Zhang X, Ge P, Yu X, Brannan JM, Bi G, Zhang Q, et al. Cryo-EM structure of the mature dengue virus at 3.5-Å resolution. Nat Struct Mol Biol. 2013;20: 105–110. doi: 10.1038/nsmb.246323241927
36. Zhang X, Sheng J, Austin SK, Hoornweg TE, Smit JM, Kuhn RJ, et al. Structure of acidic pH dengue virus showing the fusogenic glycoprotein trimers. J Virol. 2015;89: 743–750. doi: 10.1128/JVI.02411-1425355881
37. Battisti AJ, Yoder JD, Plevka P, Winkler DC, Prasad VM, Kuhn RJ, et al. Cryo-electron tomography of rubella virus. J Virol. 2012;86: 11078–11085. doi: 10.1128/JVI.01390-1222855483
38. Crowther RA, Kiselev NA, Böttcher B, Berriman JA, Borisova GP, Ose V, et al. Three-dimensional structure of hepatitis B virus core particles determined by electron cryomicroscopy. Cell. 1994;77: 943–950. 8004680
39. Wang Z, Nie Y, Wang P, Ding M, Deng H, Characterization of classical swine fever virus entry by using pseudotyped viruses: E1 and E2 are sufficient to mediate viral entry. Virology. 2004;330: 332–341. doi: 10.1016/j.virol.2004.09.02315527858
40. Ronecker S, Zimmer G, Herrler G, Greiser-Wilke I, Grummer B, Formation of bovine viral diarrhea virus E1-E2 heterodimers is essential for virus entry and depends on charged residues in the transmembrane domains. J Gen Virol. 2008;89: 2114–2121. doi: 10.1099/vir.0.2008/001792-018753220
41. Yang X, Kurteva S, Ren X, Lee S, Sodroski J, Stoichiometry of envelope glycoprotein trimers in the entry of human immunodeficiency virus type 1. J Virol. 2005;79: 12132–12147. doi: 10.1128/JVI.79.19.12132–12147.200516160141
42. Magnus C, Rusert P, Bonhoeffer S, Trkola A, Regoes RR, Estimating the stoichiometry of human immunodeficiency virus entry. J Virol. 2009;83: 1523–1531. doi: 10.1128/JVI.01764-0819019953
43. Le Duff Y, Blanchet M, Sureau C, The pre-S1 and antigenic loop infectivity determinants of the hepatitis B virus envelope proteins are functionally independent. J Virol. 2009;83: 12443–12451. doi: 10.1128/JVI.01594-0919759159
44. Ivanovic T, Choi JL, Whelan SP, van Oijen AM, Harrison SC, Influenza-virus membrane fusion by cooperative fold-back of stochastically induced hemagglutinin intermediates. Elife. 2013;2: e00333. doi: 10.7554/eLife.0033323550179
45. Rümenapf T, Unger G, Strauss JH, Thiel HJ, Processing of the envelope glycoproteins of pestiviruses. J Virol. 1993;67: 3288–3294. 8388499
46. Chan R, Uchil PD, Jin J, Shui G, Ott DE, Mothes W, et al. Retroviruses human immunodeficiency virus and murine leukemia virus are enriched in phosphoinositides. J Virol. 2008;82: 11228–11238. doi: 10.1128/JVI.00981-0818799574
47. Pike LJ, Han X, Chung K-N, Gross RW, Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: a quantitative electrospray ionization/mass spectrometric analysis. Biochemistry. 2002;41: 2075–2088. doi: 10.1021/bi015655711827555
48. Greiser-Wilke I, Dittmar KE, Liess B, Moennig V, Immunofluorescence studies of biotype-specific expression of bovine viral diarrhoea virus epitopes in infected cells. J Gen Virol. 1991;72: 2015–2019. doi: 10.1099/0022-1317-72-8-20151714946
49. Köhl W, Zimmer G, Greiser-Wilke I, Haas L, Moennig V, Herrler G, The surface glycoprotein E2 of bovine viral diarrhoea virus contains an intracellular localization signal. J Gen Virol. 2004;85: 1101–1111. doi: 10.1099/vir.0.19740–015105527
50. Macovei A, Zitzmann N, Lazar C, Dwek RA, Branza-Nichita N, Brefeldin A inhibits pestivirus release from infected cells, without affecting its assembly and infectivity. Biochem Biophys Res Commun. 2006;346: 1083–1090. doi: 10.1016/j.bbrc.2006.06.02316782064
51. van Meer G, de Kroon AIPM, Lipid map of the mammalian cell. J Cell Sci. 2011;124: 5–8. doi: 10.1242/jcs.07123321172818
52. Martín-Acebes MA, Merino-Ramos T, Blázquez A- B, Casas J, Escribano-Romero E, Sobrino F, et al. The composition of West Nile virus lipid envelope unveils a role of sphingolipid metabolism in flavivirus biogenesis. J Virol. 2014;88: 12041–12054. doi: 10.1128/JVI.02061-1425122799
53. Weiskircher E, Aligo J, Ning G, Konan KV, Bovine viral diarrhea virus NS4B protein is an integral membrane protein associated with Golgi markers and rearranged host membranes. Virol J. 2009;6: 185. doi: 10.1186/1743-422X-6-18519887001
54. Browman DT, Resek ME, Zajchowski LD, Robbins SM, Erlin-1 and erlin-2 are novel members of the prohibitin family of proteins that define lipid-raft-like domains of the ER. J Cell Sci. 2006;119: 3149–3160. doi: 10.1242/jcs.0306016835267
55. Friesland M, Mingorance L, Chung J, Chisari FV, Gastaminza P, Sigma-1 receptor regulates early steps of viral RNA replication at the onset of hepatitis C virus infection. J Virol. 2013;87: 6377–6390. doi: 10.1128/JVI.03557-1223536676
56. Krey T, Moussay E, Thiel H-J, Rümenapf T, Role of the low-density lipoprotein receptor in entry of bovine viral diarrhea virus. J Virol. 2006;80: 10862–10867. doi: 10.1128/JVI.01589-0616928760
57. Mendez E, Ruggli N, Collett MS, Rice CM, Infectious bovine viral diarrhea virus (strain NADL) RNA from stable cDNA clones: a cellular insert determines NS3 production and viral cytopathogenicity. J Virol. 1998;72: 4737–4745. 9573238
58. Lamp B, Riedel C, Roman-Sosa G, Heimann M, Jacobi S, Becher P, et al. Biosynthesis of classical swine fever virus nonstructural proteins. J Virol. 2011;85: 3607–3620. doi: 10.1128/JVI.02206-1021270154
59. Boulanger D, Waxweiler S, Karelle L, Loncar M, Mignon B, Dubuisson J, et al. Characterization of monoclonal antibodies to bovine viral diarrhoea virus: evidence of a neutralizing activity against gp48 in the presence of goat anti-mouse immunoglobulin serum. J Gen Virol. 1991;72: 1195–1198. doi: 10.1099/0022-1317-72-5-11951851819
60. Özbalci C, Sachsenheimer T, Brügger B, Quantitative Analysis of Cellular Lipids by Nano-Electrospray Ionization Mass Spectrometry. gate1inistfr. Totowa, NJ: Humana Press; 2013. pp. 3–20. doi: 10.1007/978-1-62703-487-6_1
61. Paltauf F, Hermetter A, Strategies for the synthesis of glycerophospholipids. Prog Lipid Res. 1994;33: 239–328. 8022845