Visualization and analysis of Hepatitis C Virus structural proteins at lipid droplets by super-resolution microscopy

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Eggert, Dennis ^a   Rösch, Kathrin ^a   Reimer, Rudolph ^a   Herker, Eva ^a  

^a UNIVERSITY OF HAMBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

E2 PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; FAT DROPLET;

ARTICLE; BINDING SITE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; HEPATITIS C; HEPATITIS C VIRUS; LIPID ANALYSIS; MICROSCOPY; MOLECULAR CLONING; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SUPER RESOLUTION MICROSCOPY; VALIDATION PROCESS; CHEMISTRY; FLUORESCENCE MICROSCOPY; HEPACIVIRUS; METABOLISM; PROCEDURES; ULTRASTRUCTURE; VIROLOGY;

HEPACIVIRUS; LIPID DROPLETS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; VIRAL STRUCTURAL PROTEINS;

EID: 84908429857     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102511     Document Type: Article

References (42)

1. Lauer GM, Walker BD (2001) Hepatitis C virus infection. N Engl J Med 345:41-52.
2. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, et al. (2005) Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11:791-796.
3. Lindenbach BD, Evans MJ, Syder AJ, Wolk B, Tellinghuisen TL, et al. (2005) Complete replication of hepatitis C virus in cell culture. Science 309:623-626.
4. Herker E, Ott M (2011) Unique ties between hepatitis C virus replication and intracellular lipids. Trends Endocrinol Metab 22:241-248.
5. Miyanari Y, Atsuzawa K, Usuda N, Watashi K, Hishiki T, et al. (2007) The lipid droplet is an important organelle for hepatitis C virus production. Nat Cell Biol 9:1089-1097.
6. Boulant S, Targett-Adams P, McLauchlan J (2007) Disrupting the association of hepatitis C virus core protein with lipid droplets correlates with a loss in production of infectious virus. J Gen Virol 88:2204-2213.
7. Herker E, Harris C, Hernandez C, Carpentier A, Kaehlcke K, et al. (2010) Efficient hepatitis C virus particle formation requires diacylglycerol acyltransferase-1. Nat Med 16:1295-1298.
8. Barba G, Harper F, Harada T, Kohara M, Goulinet S, et al. (1997) Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc Natl Acad Sci U S A 94:1200-1205.
9. Shi ST, Polyak SJ, Tu H, Taylor DR, Gretch DR, et al. (2002) Hepatitis C virus NS5A colocalizes with the core protein on lipid droplets and interacts with apolipoproteins. Virology 292:198-210.
10. Camus G, Herker E, Modi AA, Haas JT, Ramage HR, et al. (2013) Diacylglycerol acyltransferase-1 localizes hepatitis C virus NS5A protein to lipid droplets and enhances NS5A interaction with the viral capsid core. J Biol Chem 288:9915-9923.
11. Hope RG, McLauchlan J (2000) Sequence motifs required for lipid droplet association and protein stability are unique to the hepatitis C virus core protein. J Gen Virol 81:1913-1925.
12. McLauchlan J, Lemberg MK, Hope G, Martoglio B (2002) Intramembrane proteolysis promotes trafficking of hepatitis C virus core protein to lipid droplets. EMBO J 21:3980-3988.
13. Schwer B, Ren S, Pietschmann T, Kartenbeck J, Kaehlcke K, et al. (2004) Targeting of hepatitis C virus core protein to mitochondria through a novel Cterminal localization motif. J Virol 78:7958-7968.
14. Targett-Adams P, Hope G, Boulant S, McLauchlan J (2008) Maturation of hepatitis C virus core protein by signal peptide peptidase is required for virus production. J Biol Chem 283:16850-16859.
15. Counihan NA, Rawlinson SM, Lindenbach BD (2011) Trafficking of hepatitis C virus core protein during virus particle assembly. PLoS Pathog 7:e1002302.
16. Rouille Y, Helle F, Delgrange D, Roingeard P, Voisset C, et al. (2006) Subcellular localization of hepatitis C virus structural proteins in a cell culture system that efficiently replicates the virus. J Clin Virol 36:S53-S54.
17. Coller KE, Heaton NS, Berger KL, Cooper JD, Saunders JL, et al. (2012) Molecular determinants and dynamics of hepatitis C virus secretion. PLoS Pathog 8:e1002466.
18. Popescu CI, Rouille Y, Dubuisson J (2011) Hepatitis C virus assembly imaging. Viruses 3:2238-2254.
19. Abbe E (1873) Beiträge zur Theorie des Mikroskops und der mikroskopischen Wahrnehmung. Archiv für mikroskopische Anatomie 9:413-418.
20. Hell SW (2007) Far-field optical nanoscopy. Science 316:1153-1158.
21. Hell SW, Wichmann J (1994) Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt Lett 19:780-782.
22. Gustafsson MG (2000) Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J Microsc 198:82-87.
23. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, et al. (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:1642-1645.
24. Hess ST, Girirajan TP, Mason MD (2006) Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys J 91:4258-4272.
25. Rust MJ, Bates M, Zhuang X (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3:793-795.
26. Heilemann M, van de Linde S, Schuttpelz M, Kasper R, Seefeldt B, et al. (2008) Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes. Angew Chem Int Ed Engl 47:6172-6176.
27. Huang B, Wang W, Bates M, Zhuang X (2008) Three-dimensional superresolution imaging by stochastic optical reconstruction microscopy. Science 319:810-813.
28. Flottmann B, Gunkel M, Lisauskas T, Heilemann M, Starkuviene V, et al. (2013) Correlative light microscopy for high-content screening. BioTechniques 55:243-252.
29. Wang W, Li GW, Chen C, Xie XS, Zhuang X (2011) Chromosome organization by a nucleoid-associated protein in live bacteria. Science 333:1445-1449.
30. Han JJ, Kunde YA, Hong-Geller E, Werner JH (2014) Actin restructuring during Salmonella typhimurium infection investigated by confocal and superresolution microscopy. J Biomed Opt 19:16011.
31. Eggert D, Naumann M, Reimer R, Voigt CA (2014) Nanoscale glucan polymer network causes pathogen resistance. Sci Rep 4:4159.
32. Pereira CF, Rossy J, Owen DM, Mak J, Gaus K (2012) HIV taken by STORM: super-resolution fluorescence microscopy of a viral infection. Virol J 9:84.
33. Muranyi W, Malkusch S, Muller B, Heilemann M, Krausslich HG (2013) Superresolution microscopy reveals specific recruitment of HIV-1 envelope proteins to viral assembly sites dependent on the envelope C-terminal tail. PLoS Pathog 9:e1003198.
34. Van Engelenburg SB, Shtengel G, Sengupta P, Waki K, Jarnik M, et al. (2014) Distribution of ESCRT machinery at HIV assembly sites reveals virus scaffolding of ESCRT subunits. Science 343:653-656.
35. Shavinskaya A, Boulant S, Penin F, McLauchlan J, Bartenschlager R (2007) The lipid droplet binding domain of hepatitis C virus core protein is a major determinant for efficient virus assembly. J Biol Chem 282:37158-37169.
36. Ohsaki Y, Maeda T, Fujimoto T (2005) Fixation and permeabilization protocol is critical for the immunolabeling of lipid droplet proteins. HistochemCell Biol 124:445-452.
37. Dempsey GT, Vaughan JC, Chen KH, Bates M, Zhuang X (2011) Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging. Nat Methods 8:1027-1036.
38. Merz A, Long G, Hiet MS, Brugger B, Chlanda P, et al. (2011) Biochemical and morphological properties of hepatitis C virus particles and determination of their lipidome. J Biol Chem 286:3018-3032.
39. Wakita T, Suzuki T, Takahashi H (2009) Production and use of epitope-tagged hepatitis c virus particle. In: Organization WIP, editor.
40. Koutsoudakis G, Herrmann E, Kallis S, Bartenschlager R, Pietschmann T (2007) The level of CD81 cell surface expression is a key determinant for productive entry of hepatitis C virus into host cells. J Virol 81:588-598.
41. Longin A, Souchier C, Ffrench M, Bryon PA (1993) Comparison of anti-fading agents used in fluorescence microscopy: image analysis and laser confocal microscopy study. J Histochem Cytochem 41:1833-1840.
42. Bolte S, Cordelieres FP (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224:213-232.