Cell permeabilization by poliovirus 2B viroporin triggers bystander permeabilization in neighbouring cells through a mechanism involving gap junctions

Cellular Microbiology

Volumn 12, Issue 8, 2010, Pages 1144-1157

  Madan, Vanesa ^a,b   Redondo, Natalia ^a   Carrasco, Luis ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 43; FLUORESCENT DYE; POLIOMYELITIS VIRUS 2B PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; 2B PROTEIN, POLIOVIRUS; 6K PROTEIN, SINDBIS VIRUS; CARRIER PROTEIN; NS4A COFACTOR PEPTIDE, HEPATITIS C VIRUS; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ARTICLE; BYSTANDER EFFECT; CELL COMMUNICATION; CELL CONTACT; CELL PERMEABILIZATION; COCULTURE; CONTROLLED STUDY; GAP JUNCTION; HEPATITIS C VIRUS; MEMBRANE TRANSPORT; MOUSE; MURINE HEPATITIS CORONAVIRUS; NONHUMAN; POLIOMYELITIS VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SINDBIS VIRUS; ANIMAL; CELL LINE; CELL MEMBRANE PERMEABILITY; DRUG EFFECTS; HAMSTER; HEPACIVIRUS; HUMAN; METABOLISM; PATHOGENICITY;

ANIMALS; CARRIER PROTEINS; CELL LINE; CELL MEMBRANE PERMEABILITY; COCULTURE TECHNIQUES; CRICETINAE; GAP JUNCTIONS; HEPACIVIRUS; HUMANS; MURINE HEPATITIS VIRUS; POLIOVIRUS; SINDBIS VIRUS; VIRAL ENVELOPE PROTEINS; VIRAL NONSTRUCTURAL PROTEINS; VIRAL PROTEINS;

CRICETINAE; HEPATITIS C VIRUS; MAMMALIA; MURINE HEPATITIS VIRUS; POLIOVIRUS; SINDBIS VIRUS;

EID: 77957161828     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01460.x     Document Type: Article

References (45)

1. Agirre A, Barco A, Carrasco L, Nieva JL. Viroporin-mediated membrane permeabilization. Pore formation by nonstructural poliovirus 2B protein. J Biol Chem 2002, 277:40434-40441.
2. Aldabe R, Carrasco L. Induction of membrane proliferation by poliovirus proteins 2C and 2BC. Biochem Biophys Res Commun 1995, 206:64-76.
3. Aldabe R, Barco A, Carrasco L. Membrane permeabilization by poliovirus proteins 2B and 2 BC. J Biol Chem 1996, 271:23134-23137.
4. Asklund T, Appelskog IB, Ammerpohl O, Langmoen IA, Dilber MS, Aints A. Gap junction-mediated bystander effect in primary cultures of human malignant gliomas with recombinant expression of the HSVtk gene. Exp Cell Res 2003, 284:185-195.
5. Barco A, Carrasco L. A human virus protein, poliovirus protein 2 BC, induces membrane proliferation and blocks the exocytic pathway in the yeast Saccharomyces cerevisiae. EMBO J 1995, 14:3349-3364.
6. Barco A, Carrasco L. Identification of regions of poliovirus 2 BC protein that are involved in cytotoxicity. J Virol 1998, 72:3560-3570.
7. Bienz K, Egger D, Pfister T, Troxler M. Structural and functional characterization of the poliovirus replication complex. J Virol 1992, 66:2740-2747.
8. Choe SS, Dodd DA, Kirkegaard K. Inhibition of cellular protein secretion by picornaviral 3A proteins. Virology 2005, 337:18-29.
9. Davidson JS, Baumgarten IM, Harley EH. Reversible inhibition of intercellular junctional communication by glycyrrhetinic acid. Biochem Biophys Res Commun 1986, 134:29-36.
10. Dilber MS, Abedi MR, Christensson B, Bjorkstrand B, Kidder GM, Naus CC. Gap junctions promote the bystander effect of herpes simplex virus thymidine kinase in vivo. Cancer Res 1997, 57:1523-1528.
11. Ewart GD, Sutherland T, Gage PW, Cox GB. The Vpu protein of human immunodeficiency virus type 1 forms cation-selective ion channels. J Virol 1996, 70:7108-7115.
12. Gan SW, Ng L, Lin X, Gong X, Torres J. Structure and ion channel activity of the human respiratory syncytial virus (hRSV) small hydrophobic protein transmembrane domain. Protein Sci 2008, 17:813-820.
13. Gonzalez ME, Carrasco L. The human immunodeficiency virus type 1 Vpu protein enhances membrane permeability. Biochemistry 1998, 37:13710-13719.
14. Griffin S, Stgelais C, Owsianka AM, Patel AH, Rowlands D, Harris M. Genotype-dependent sensitivity of hepatitis C virus to inhibitors of the p7 ion channel. Hepatology 2008, 48:1779-1790.
15. Guinea R, Carrasco L. Influenza virus M2 protein modifies membrane permeability in E. coli cells. FEBS Lett 1994, 343:242-246.
16. van den Hoff MJ, Moorman AF, Lamers WH. Electroporation in 'intracellular' buffer increases cell survival. Nucleic Acids Res 1992, 20:2902.
17. Huang C, Narayanan K, Ito N, Peters CJ, Makino S. Severe acute respiratory syndrome coronavirus 3a protein is released in membranous structures from 3a protein-expressing cells and infected cells. J Virol 2006, 80:210-217.
18. Huang MB, Weeks O, Zhao LJ, Saltarelli M, Bond VC. Effects of extracellular human immunodeficiency virus type 1 vpr protein in primary rat cortical cell cultures. J Neurovirol 2000, 6:202-220.
19. de Jong AS, Visch HJ, de Mattia F, van Dommelen MM, Swarts HG, Luyten T. The coxsackievirus 2B protein increases efflux of ions from the endoplasmic reticulum and Golgi, thereby inhibiting protein trafficking through the Golgi. J Biol Chem 2006, 281:14144-14150.
20. Klimkait T, Strebel K, Hoggan MD, Martin MA, Orenstein JM. The human immunodeficiency virus type 1-specific protein vpu is required for efficient virus maturation and release. J Virol 1990, 64:621-629.
21. Kumar NM, Gilula NB. The gap junction communication channel. Cell 1996, 84:381-388.
22. van Kuppeveld FJ, Hoenderop JG, Smeets RL, Willems PH, Dijkman HB, Galama JM, Melchers WJ. Coxsackievirus protein 2B modifies endoplasmic reticulum membrane and plasma membrane permeability and facilitates virus release. EMBO J 1997, 16:3519-3532.
23. Liljestrom P, Garoff H. Internally located cleavable signal sequences direct the formation of Semliki Forest virus membrane proteins from a polyprotein precursor. J Virol 1991, 65:147-154.
24. Luik P, Chew C, Aittoniemi J, Chang J, Wentworth P, Dwek RA. The 3-dimensional structure of a hepatitis C virus p7 ion channel by electron microscopy. Proc Natl Acad Sci USA 2009, 106:12712-12716.
25. Madan V, Garcia Mde J, Sanz MA, Carrasco L. Viroporin activity of murine hepatitis virus E protein. FEBS Lett 2005, 579:3607-3612.
26. Madan V, Sanchez-Martinez S, Vedovato N, Rispoli G, Carrasco L, Nieva JL. Plasma membrane-porating domain in poliovirus 2B protein. A short peptide mimics viroporin activity. J Mol Biol 2007, 374:951-964.
27. Madan V, Castello A, Carrasco L. Viroporins from RNA viruses induce caspase-dependent apoptosis. Cell Microbiol 2008, 10:437-451.
28. Maeda J, Maeda A, Makino S. Release of coronavirus E protein in membrane vesicles from virus-infected cells and E protein-expressing cells. Virology 1999, 263:265-272.
29. Melton JV, Ewart GD, Weir RC, Board PG, Lee E, Gage PW. Alphavirus 6K proteins form ion channels. J Biol Chem 2002, 277:46923-46931.
30. Moon H, Yang J. Role of HIV Vpr as a regulator of apoptosis and an effector on bystander cells. Mol Cells 2006, 21:7-20.
31. Pavlovic D, Neville DC, Argaud O, Blumberg B, Dwek RA, Fischer WB, Zitzmann N. The hepatitis C virus p7 protein forms an ion channel that is inhibited by long-alkyl-chain iminosugar derivatives. Proc Natl Acad Sci USA 2003, 100:6104-6108.
32. Pielak RM, Schnell JR, Chou JJ. Mechanism of drug inhibition and drug resistance of influenza A M2 channel. Proc Natl Acad Sci USA 2009, 106:7379-7384.
33. Pinto LH, Holsinger LJ, Lamb RA. Influenza virus M2 protein has ion channel activity. Cell 1992, 69:517-528.
34. Rose CR, Ransom BR. Gap junctions equalize intracellular Na+ concentration in astrocytes. Glia 1997, 20:299-307.
35. Sanz MA, Madan V, Carrasco L, Nieva JL. Interfacial domains in Sindbis virus 6K protein. Detection and functional characterization. J Biol Chem 2003, 278:2051-2057.
36. Sanz MA, Castello A, Carrasco L. Viral translation is coupled to transcription in Sindbis virus-infected cells. J Virol 2007, 81:7061-7068.
37. Schlegel A, Giddings TH, Ladinsky MS, Kirkegaard K. Cellular origin and ultrastructure of membranes induced during poliovirus infection. J Virol 1996, 70:6576-6588.
38. Suhy DA, Giddings TH, Kirkegaard K. Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles. J Virol 2000, 74:8953-8965.
39. Udawatte C, Ripps H. The spread of apoptosis through gap-junctional channels in BHK cells transfected with Cx32. Apoptosis 2005, 10:1019-1029.
40. Wang C, Lamb RA, Pinto LH. Direct measurement of the influenza A virus M2 protein ion channel activity in mammalian cells. Virology 1994, 205:133-140.
41. Wilson L, McKinlay C, Gage P, Ewart G. SARS coronavirus E protein forms cation-selective ion channels. Virology 2004, 330:322-331.
42. Xiao Y, Chen G, Richard J, Rougeau N, Li H, Seidah NG, Cohen EA. Cell-surface processing of extracellular human immunodeficiency virus type 1 Vpr by proprotein convertases. Virology 2008, 372:384-397.
43. Yamasaki H. Gap junctional intercellular communication and carcinogenesis. Carcinogenesis 1990, 11:1051-1058.
44. Ye Y, Hogue BG. Role of the coronavirus E viroporin protein transmembrane domain in virus assembly. J Virol 2007, 81:3597-3607.
45. Zhang D, Kaneda M, Nakahama K, Arii S, Morita I. Connexin 43 expression promotes malignancy of HuH7 hepatocellular carcinoma cells via the inhibition of cell-cell communication. Cancer Lett 2007, 252:208-215.