Orthopoxvirus species and strain differences in cell entry

Virology

Volumn 433, Issue 2, 2012, Pages 506-512

  Bengali, Zain ^a,b   Satheshkumar, P S ^a   Moss, Bernard ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b INTREXON CORPORATION   (United States)

Author keywords

Bafilomycin A1; Cowpox virus; Endocytosis; Fusion; Monkeypox virus; Vaccinia virus

Indexed keywords

A25 PROTEIN; A26 PROTEIN; BAFILOMYCIN A1; HEPARIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; COWPOX VIRUS; ENDOSOME; GENE DELETION; HUMAN; HUMAN CELL; IN VITRO STUDY; MONKEYPOX VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOPOXVIRUS; PH; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; STRAIN DIFFERENCE; VACCINIA VIRUS; VIRUS ATTACHMENT; VIRUS ENTRY;

ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; COWPOX VIRUS; ENDOSOMES; GLYCOSAMINOGLYCANS; HELA CELLS; HEPARIN; HUMANS; HYDROGEN-ION CONCENTRATION; MACROLIDES; MONKEYPOX VIRUS; OPEN READING FRAMES; ORTHOPOXVIRUS; SPECIES SPECIFICITY; VACCINIA VIRUS; VIRUS INTERNALIZATION;

COWPOX VIRUS; MONKEYPOX VIRUS; ORTHOPOXVIRUS; VACCINIA VIRUS;

EID: 84867209465     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.08.044     Document Type: Article

References (49)

1. Armstrong J.A., Metz D.H., Young M.R. The mode of entry of vaccinia virus into L cells. J. Gen. Virol. 1973, 21:533-537.
2. Bengali Z., Townsley A.C., Moss B. Vaccinia virus strain differences in cell attachment and entry. Virology 2009, 389:132-140.
3. Bisht H., Weisberg A.S., Moss B. Vaccinia virus L1 protein is required for cell entry and membrane fusion. J. Virol. 2008, 82:8687-8694.
4. Breman J.G., Kalisa R., Steniowski M.V., Zanotto E., Gromyko A.I., Arita I. Human monkeypox, 1970-79. Bull. WHO 1980, 58:165-182.
5. Brown E., Senkevich T.G., Moss B. Vaccinia virus F9 virion membrane protein is required for entry but not virus assembly, in contrast to the related l1 protein. J. Virol. 2006, 80:9455-9464.
6. Carroll D.S., Emerson G.L., Li Y., Sammons S., Olson V., Frace M., Nakazawa Y., Czerny C.P., Tryland M., Kolodziejek J., Nowotny N., Olsen-Rasmussen M., Khristova M., Govil D., Karem K., Damon I.K., Meyer H. Chasing Jenner's vaccine: revisiting cowpox virus classification. Plos One 2011, 6:e23086.
7. Carter G.C., Law M., Hollinshead M., Smith G.L. Entry of the vaccinia virus intracellular mature virion and its interactions with glycosaminoglycans. J. Gen. Virol. 2005, 86:1279-1290.
8. Chang S.J., Chang Y.X., Izmailyan R., Tang Y.L., Chang W. Vaccinia virus A25 and A26 proteins are fusion suppressors for mature virions and determine strain-specific virus entry pathways into HeLa, CHO-K1, and L cells. J. Virol. 2010, 84:8422-8432.
9. Chang S.J., Shih A.C., Tang Y.L., Chang W. Vaccinia mature virus fusion regulator A26 protein binds to A16 and G9 proteins of the viral entry fusion complex and dissociates from mature virions at low pH. J. Virol. 2012, 86:3809-3818.
10. Ching Y.C., Chung C.S., Huang C.Y., Hsia Y., Tang Y.L., Chang W. Disulfide bond formation at the C termini of vaccinia virus A26 and A27 proteins does not require viral redox enzymes and suppresses glycosaminoglycan-mediated cell fusion. J. Virol. 2009, 83:6464-6476.
11. Chiu W.L., Lin C.L., Yang M.H., Tzou D.L.M., Chang W. Vaccinia virus 4c (A26L) protein on intracellular mature virus binds to the extracellular cellular matrix laminin. J. Virol. 2007, 81:2149-2157.
12. Chung C.-S., Hsiao J.-C., Chang Y.-S., Chang W. A27L protein mediates vaccinia virus interaction with cell surface heparin sulfate. J. Virol. 1998, 72:1577-1585.
13. Condit R.C., Moussatche N., Traktman P. In a nutshell: structure and assembly of the vaccinia virion. Adv. Virus Res. 2006, 66:31-124.
14. Gong S.C., Lai C.F., Esteban M. Vaccinia virus induces cell fusion at acid pH and this activity is mediated by the N-terminus of the 14-kDa virus envelope protein. Virology 1990, 178:81-91.
15. Howard A.R., Senkevich T.G., Moss B. Vaccinia virus A26 and A27 proteins form a stable complex tethered to mature virions by association with the A17 transmembrane protein. J. Virol. 2008, 82:12384-12391.
16. Hsiao J.C., Chung C.S., Chang W. Cell surface proteoglycans are necessary for A27L protein- mediated cell fusion: identification of the N-terminal region of A27L protein as the glycosaminoglycan-binding domain. J. Virol. 1998, 72:8374-8379.
17. Huang C.Y., Lu T.Y., Bair C.H., Chang Y.S., Jwo J.K., Chang W. A novel cellular protein, VPEF, facilitates vaccinia virus penetration into HeLa cells through fluid phase endocytosis. J. Virol. 2008, 82:7988-7999.
18. Ichihashi Y. Extracellular enveloped vaccinia virus escapes neutralization. Virology 1996, 217:478-485.
19. Izmailyan R.A., Huang C.Y., Mohammad S., Isaacs S.N., Chang W. The envelope G3L protein is essential for entry of vaccinia virus into host cells. J. Virol. 2006, 80:8402-8410.
20. Laliberte J.P., Weisberg A.S., Moss B. The membrane fusion step of vaccinia virus entry is cooperatively mediated by multiple viral proteins and host cell components. PLoS Pathog. 2011, 7:e1002446.
21. Law M., Carter G.C., Roberts K.L., Hollinshead M., Smith G.L. Ligand-induced and non-fusogenic dissolution of a viral membrane. Proc. Natl. Acad. Sci. USA 2006, 103:5989-5994.
22. Lin C.L., Chung C.S., Heine H.G., Chang W. Vaccinia virus envelope H3L protein binds to cell surface heparan sulfate and is important for intracellular mature virion morphogenesis and virus infection in vitro and in vivo. J. Virol. 2000, 74:3353-3365.
23. McKelvey T.A., Andrews S.C., Miller S.E., Ray C.A., Pickup D.J. Identification of the orthopoxvirus p4c gene, which encodes a structural protein that directs intracellular mature virus particles into A-type inclusions. J. Virol. 2002, 76:11216-11225.
24. Mercer J., Helenius A. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 2008, 320:531-535.
25. Mercer J., Knebel S., Schmidt F.I., Crouse J., Burkard C., Helenius A. Vaccinia virus strains use distinct forms of macropinocytosis for host-cell entry. Proc. Natl. Acad. Sci. USA 2010, 107:9346-9351.
26. Mercer J., Schelhaas M., Helenius A. Virus entry by endocytosis. Annu. Rev. Biochem. 2010, 79:803-833.
27. Meyer H., Schay C., Mahnel H., Pfeffer M. Characterization of orthopoxviruses isolated from man and animals in Germany. Arch. Virol. 1999, 144:491-501.
28. Moser T.S., Jones R.G., Thompson C.B., Coyne C.B., Cherry S. A kinome RNAi screen identified AMPK as promoting poxvirus entry through the control of actin dynamics. PLoS Pathog. 2010, 6:e1000954.
29. Moss B. Poxvirus entry and membrane fusion. Virology 2006, 344:48-54.
30. Moss B. Poxviridae: the viruses and their replication. Fields Virology 2007, 2905-2946. Lippincott Williams and Wilkins, Philadelphia, (2 vols.).
31. Nichols R.J., Stanitsa E., Unger B., Traktman P. The vaccinia I2L gene encodes a membrane protein with an essential role in virion entry. J. Virol. 2008, 82:10247-10261.
32. Ojeda S., Domi A., Moss B. Vaccinia virus G9 protein is an essential component of the poxvirus entry-fusion complex. J. Virol. 2006, 80:9822-9830.
33. Ojeda S., Senkevich T.G., Moss B. Entry of vaccinia virus and cell-cell fusion require a highly conserved cysteine-rich membrane protein encoded by the A16L gene. J. Virol. 2006, 80:51-61.
34. Patel D.D., Pickup D.J., Joklik W.K. Isolation of cowpox virus A-type inclusions and characterization of their major protein component. Virology 1986, 149:174-189.
35. Sandgren K.J., Wilkinson J., Miranda-Saksena M., McInerney G.M., Byth-Wilson K., Robinson P.J., Cunningham A.L. A differential role for macropinocytosis in mediating entry of the two forms of vaccinia virus into dendritic cells. Plos Pathog. 2010, 6:e1000866.
36. Satheshkumar P.S., Moss B. Characterization of a newly Identified 35 amino acid component of the vaccinia virus entry/fusion complex conserved in all chordopoxviruses. J. Virol. 2009, 83:12822-12832.
37. Schmidt F.I., Bleck C.K., Helenius A., Mercer J. Vaccinia extracellular virions enter cells by macropinocytosis and acid-activated membrane rupture. EMBO J. 2011, 30:3647-3661.
38. Schmidt F.I., Bleck C.K., Mercer J. Poxvirus host cell entry. Curr. Opinion Virol. 2012, 2:20-27.
39. Senkevich T.G., Moss B. Vaccinia virus H2 protein is an essential component of a complex involved in virus entry and cell-cell fusion. J. Virol. 2005, 79:4744-4754.
40. Senkevich T.G., Ojeda S., Townsley A., Nelson G.E., Moss B. Poxvirus multiprotein entry-fusion complex. Proc. Natl. Acad. Sci. USA 2005, 102:18572-18577.
41. Senkevich T.G., Ward B.M., Moss B. Vaccinia virus A28L gene encodes an essential protein component of the virion membrane with intramolecular disulfide bonds formed by the viral cytoplasmic redox pathway. J. Virol. 2004, 78:2348-2356.
42. Townsley A., Senkevich T.G., Moss B. The product of the vaccinia virus L5R gene is a fourth membrane protein encoded by all poxviruses that is requried for cell entry and cell-cell fusion. J. Virol. 2005, 79:10988-10998.
43. Townsley A., Senkevich T.G., Moss B. Vaccinia virus A21 virion membrane protein is required for cell entry and fusion. J. Virol. 2005, 79:9458-9469.
44. Townsley A.C., Moss B. Two distinct low-pH steps promote entry of vaccinia virus. J. Virol. 2007, 81:8613-8620.
45. Townsley A.C., Weisberg A.S., Wagenaar T.R., Moss B. Vaccinia virus entry into cells via a low pH-dependent-endosomal pathway. J. Virol. 2006, 80:8899-8908.
46. Ulaeto D., Grosenbach D., Hruby D.E. The vaccinia virus 4c and A-type inclusion proteins are specific markers for the intracellular mature virus particle. J. Virol. 1996, 70:3372-3375.
47. Villa N.Y., Bartee E., Mohamed M.R., Rahman M.M., Barrett J.W., McFadden G. Myxoma and vaccinia viruses exploit different mechanisms to enter and infect human cancer cells. Virology 2010, 401:266-279.
48. White J.M., Delos S.E., Brecher M., Schornberg K. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit. Rev. Biochem. Mol. Biol. 2008, 43:189-219.
49. Wolfe C.L., Ojeda S., Moss B. Transcriptional repression and RNA silencing act synergistically to demonstrate the function of the eleventh component of the vaccinia virus entry-fusion complex. J. Virol. 2012, 86:293-301.