Capsid Protein VP4 of Human Rhinovirus Induces Membrane Permeability by the Formation of a Size-Selective Multimeric Pore

PLoS Pathogens

Volumn 10, Issue 8, 2014, Pages

  Panjwani, Anusha ^a,b   Strauss, Mike ^c   Gold, Sarah ^a   Wenham, Hannah ^a   Jackson, Terry ^a   Chou, James J ^c   Rowlands, David J ^b   Stonehouse, Nicola J ^b   Hogle, James M ^c   Tuthill, Tobias J ^a  

^a INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYFLUORESCEIN; GLUTATHIONE TRANSFERASE; LIPOSOME; MELITTIN; PROTEIN VP4; CAPSID PROTEIN; RECOMBINANT PROTEIN;

ARTICLE; CROSS LINKING; ELECTRON MICROSCOPY; FLUORESCENCE; GENETIC RECOMBINATION; HUMAN RHINOVIRUS; MEMBRANE PERMEABILITY; NONHUMAN; NUCLEAR PORE; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; WESTERN BLOTTING; CELL MEMBRANE PERMEABILITY; HELA CELL LINE; HUMAN; METABOLISM; PATHOGENICITY; RHINOVIRUS; TRANSMISSION ELECTRON MICROSCOPY;

BLOTTING, WESTERN; CAPSID PROTEINS; CELL MEMBRANE PERMEABILITY; HELA CELLS; HUMANS; LIPOSOMES; MICROSCOPY, ELECTRON, TRANSMISSION; RECOMBINANT PROTEINS; RHINOVIRUS;

EID: 84922276707     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004294     Document Type: Article

References (54)

1. Plemper RK, (2011) Cell entry of enveloped viruses. Current Opinion in Virology 1: 92–100.
2. Harrison SC, (2008) Viral membrane fusion. Nature Structural & Molecular Biology 15: 690–698.
3. Moyer CL, Nemerow GR, (2011) Viral weapons of membrane destruction: variable modes of membrane penetration by non-enveloped viruses. Current Opinion in Virology 1: 44–49.
4. Johnson JE (2010) Cell Entry by Non-Enveloped Viruses. In: Johnson JE, editor. Cell Entry by Non-Enveloped Viruses. pp. 1–229.
5. Makela MJ, Puhakka T, Ruuskanen O, Leinonen M, Saikku P, et al. (1998) Viruses and bacteria in the etiology of the common cold. Journal of Clinical Microbiology 36: 539–542.
6. Gern JE, (2010) The ABCs of Rhinoviruses, Wheezing, and Asthma. Journal of Virology 84: 7418–7426.
7. Jackson DJ, Johnston SL, (2010) The role of viruses in acute exacerbations of asthma. Journal of Allergy and Clinical Immunology 125: 1178–1187.
8. Chow M, Newman JFE, Filman D, Hogle JM, Rowlands DJ, et al. (1987) Myristylation of picornavirus capsid protein VP4 and its structural significance. Nature, UK 237: 482–486.
9. Hogle JM, (2002) Poliovirus cell entry: Common structural themes in viral cell entry pathways. Annual Review of Microbiology 56: 677–702.
10. Tuthill TJ, Groppelli E, Hogle JM, Rowlands DJ, (2010) Picornaviruses. Curr Top Microbiol Immunol
11. Fuchs R, Blaas D, (2010) Uncoating of human rhinoviruses. Reviews in Medical Virology 20: 281–297.
12. Fricks CE, Hogle JM, (1990) Cell-induced conformational change in poliovirus - externalization of the amino terminus of vp1 is responsible for liposome binding. Journal of Virology 64: 1934–1945.
13. Tuthill TJ, Bubeck D, Rowlands DJ, Hogle JM, (2006) Characterization of early steps in the poliovirus infection process: Receptor-decorated liposomes induce conversion of the virus to membrane-anchored entry-intermediate particles. Journal of Virology 80: 172–180.
14. Danthi P, Tosteson M, Li QH, Chow M, (2003) Genome delivery and ion channel properties are altered in VP4 mutants of poliovirus. Journal of Virology 77: 5266–5274.
15. Moscufo N, Yafal AG, Rogove A, Hogle J, Chow M, (1993) A mutation in VP4 defines a new step in the late stages of cell entry by poliovirus. Journal of Virology 67: 5075–5078.
16. Strauss M, Levy HC, Bostina M, Filman DJ, Hogle JM, (2013) RNA Transfer from Poliovirus 135S Particles across Membranes Is Mediated by Long Umbilical Connectors. Journal of virology 87: 3903–3914.
17. Brabec M, Schober D, Wagner E, Bayer N, Murphy RF, et al. (2005) Opening of size-selective pores in endosomes during human rhinovirus serotype 2 in vivo uncoating monitored by single-organelle flow analysis. Journal of Virology 79: 1008–1016.
18. Davis MP, Bottley G, Beales LP, Killington RA, Rowlands DJ, et al. (2008) Recombinant VP4 of human rhinovirus induces permeability in model membranes. Journal of Virology 82: 4169–4174.
19. Tosteson MT, Wang H, Naumov A, Chow M, (2004) Poliovirus binding to its receptor in lipid bilayers results in particle-specific, temperature-sensitive channels. Journal of General Virology 85: 1581–1589.
20. Prchla E, Kuechler E, Blaas D, Fuchs R, (1994) Uncoating of human rhinovirus serotype-2 from late endosomes. Journal of Virology 68: 3713–3723.
21. Bayer N, Prchla E, Schwab M, Blaas D, Fuchs R, (1999) Human rhinovirus HRV14 uncoats from early endosomes in the presence of bafilomycin. Febs Letters 463: 175–178.
22. Huotari J, Helenius A, (2011) Endosome maturation. Embo Journal 30: 3481–3500.
23. Bello J, Bello HR, Granados E, (1982) Conformation and aggregation of melittin - dependence on pH and concentration. Biochemistry 21: 461–465.
24. Ladokhin AS, Selsted ME, White SH, (1997) Sizing membrane pores in lipid vesicles by leakage of co-encapsulated markers: Pore formation by melittin. Biophysical Journal 72: 1762–1766.
25. Parente RA, Nir S, Szoka FC, (1990) Mechanism of leakage of phospholipid vesicle contents induced by the peptide GALA. Biochemistry 29: 8720–8728.
26. Nicol F, Nir S, Szoka FC, (2000) Effect of phospholipid composition on an amphipathic peptide-mediated pore formation in bilayer vesicles. Biophysical Journal 78: 818–829.
27. Park SC, Kim JY, Shin SO, Jeong CY, Kim MH, et al. (2006) Investigation of toroidal pore and oligomerization by melittin using transmission electron microscopy. Biochemical and Biophysical Research Communications 343: 222–228.
28. Tosteson MT, Chow M, (1997) Characterization of the ion channels formed by poliovirus in planar lipid membranes. Journal of Virology 71: 507–511.
29. Li Q, Yafal AG, Lee YM, Hogle J, Chow M, (1994) Poliovirus neutralization by antibodies to internal epitopes of VP4 and VP1 results from reversible exposure of these sequences at physiological temperature. J Virol 68: 3965–3970.
30. Lewis JK, Bothner B, Smith TJ, Siuzdak G, (1998) Antiviral agent blocks breathing of the common cold virus. Proc Natl Acad Sci U S A 95: 6774–6778.
31. Resh MD, (1999) Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochimica Et Biophysica Acta-Molecular Cell Research 1451: 1–16.
32. Yalovsky S, Rodriguez-Concepcion M, Gruissem W, (1999) Lipid modifications of proteins - slipping in and out of membranes. Trends in Plant Science 4: 439–445.
33. Martin-Belmonte F, Lopez-Guerrero JA, Carrasco L, Alonso MA, (2000) The amino-terminal nine amino acid sequence of poliovirus capsid VP4 protein is sufficient to confer N-myristoylation and targeting to detergent-insoluble membranes. Biochemistry 39: 1083–1090.
34. Xiao C, Tuthill TJ, Kelly CMB, Challinor LJ, Chipman PR, et al. (2004) Discrimination among rhinovirus serotypes for a variant ICAM-1 receptor molecule. Journal of Virology 78: 10034–10044.
35. Hooverlitty H, Greve JM, (1993) Formation of rhinovirus-soluble ICAM-1 complexes and conformational-changes in the virion. Journal of Virology 67: 390–397.
36. Bilek G, Matscheko NM, Pickl-Herk A, Weiss VU, Subirats X, et al. (2011) Liposomal Nanocontainers as Models for Viral Infection: Monitoring Viral Genomic RNA Transfer through Lipid Membranes. Journal of Virology 85: 8368–8375.
37. Bubeck D, Filman DJ, Cheng NQ, Steven AC, Hogle JM, et al. (2005) The structure of the poliovirus 135S cell entry intermediate at 10-Angstrom resolution reveals the location of an externalized polypeptide that binds to membranes. Journal of Virology 79: 7745–7755.
38. Lin J, Lee LY, Roivainen M, Filman DJ, Hogle JM, et al. (2012) Structure of the Fab-Labeled “Breathing” State of Native Poliovirus. Journal of Virology 86: 5959–5962.
39. Bostina M, Levy H, Filman DJ, Hogle JM, (2011) Poliovirus RNA Is Released from the Capsid near a Twofold Symmetry Axis. Journal of Virology 85: 776–783.
40. Wang X, Peng W, Ren J, Hu Z, Xu J, et al. (2012) A sensor-adaptor mechanism for enterovirus uncoating from structures of EV71. Nature Structural & Molecular Biology 19: 424–429.
41. Ren J, Wang X, Hu Z, Gao Q, Sun Y, et al. (2013) Picornavirus uncoating intermediate captured in atomic detail. Nature communications 4: 1929–1929.
42. Katpally U, Fu TM, Freed DC, Casimiro DR, Smith TJ, (2009) Antibodies to the Buried N Terminus of Rhinovirus VP4 Exhibit Cross-Serotypic Neutralization. Journal of Virology 83: 7040–7048.
43. Clarke D, Griffin S, Beales L, Gelais CS, Burgess S, et al. (2006) Evidence for the formation of a heptameric ion channel complex by the hepatitis C virus p7 protein in vitro. Journal of Biological Chemistry 281: 37057–37068.
44. Andrecka J, Lewis R, Bruckner F, Lehmann E, Cramer P, et al. (2008) Single-molecule tracking of mRNA exiting from RNA polymerase II. Proc Natl Acad Sci U S A 105: 135–140.
45. Korzheva N, Mustaev A, Kozlov M, Malhotra A, Nikiforov V, et al. (2000) A structural model of transcription elongation. Science 289: 619–625.
46. Akeson M, Branton D, Kasianowicz JJ, Brandin E, Deamer DW, (1999) Microsecond time-scale discrimination among polycytidylic acid, polyadenylic acid, and polyuridylic acid as homopolymers or as segments within single RNA molecules. Biophys J 77: 3227–3233.
47. Poh MK, Yip A, Zhang S, Priestle JP, Ma NL, et al. (2009) A small molecule fusion inhibitor of dengue virus. Antiviral Research 84: 260–266.
48. Schmidt AG, Lee K, Yang PL, Harrison SC, (2012) Small-Molecule Inhibitors of Dengue-Virus Entry. Plos Pathogens 8: e1002627 doi:10.1371/journal.ppat.1002627
49. Liu S, Wu S, Jiang S, (2007) HIV entry inhibitors targeting gp41: From polypeptides to small-molecule compounds. Current Pharmaceutical Design 13: 143–162.
50. Zhou G, Chu S, (2013) Discovery of Small Molecule Fusion Inhibitors Targeting HIV-1 gp41. Current Pharmaceutical Design 19: 1818–1826.
51. Lee WM, Wang WS, Rueckert RR, (1995) Complete sequence of the RNA genome of human rhinovirus-16, a clinically useful common cold virus belonging to the ICAM-1 receptor group. Virus Genes 9: 177–181.
52. Tuthill TJ, Harlos K, Walter TS, Knowles NJ, Groppelli E, et al. (2009) Equine rhinitis A virus and its low pH empty particle: clues towards an aphthovirus entry mechanism? PLoS Pathog 5: e1000620.
53. Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, et al. (2007) EMAN2: An extensible image processing suite for electron microscopy. Journal of Structural Biology 157: 38–46.
54. Hohn M, Tang G, Goodyear G, Baldwin PR, Huang Z, et al. (2007) SPARX, a new environment for Cryo-EM image processing. Journal of Structural Biology 157: 47–55.