The Autographa californica multicapsid nucleopolyhedrovirus GP64 protein: Analysis of transmembrane domain length and sequence requirements

Journal of Virology

Volumn 83, Issue 9, 2009, Pages 4447-4461

  Li, Zhaofei ^a   Blissard, Gary W ^a  

^a United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; AUTOGRAPHA CALIFORNICA; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CONTROLLED STUDY; NONHUMAN; POINT MUTATION; POLYHEDROSIS VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; VIRION; VIRUS INFECTION;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CELL MEMBRANE; GENE DELETION; GLYCOPROTEINS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEOPOLYHEDROVIRUS; SHEEP; SPODOPTERA;

AUTOGRAPHA CALIFORNICA; NUCLEOPOLYHEDROVIRUS;

EID: 66149118534     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02252-08     Document Type: Article

References (61)

1. Adams, G. A., and J. K. Rose. 1985. Structural requirements of a membrane-spanning domain for protein anchoring and cell surface transport. Cell 41:1007-1015.
2. Arkin, I. T., and A. T. Brunger. 1998. Statistical analysis of predicted transmembrane alpha-helices. Biochim. Biophys. Acta 1429:113-128.
3. Armstrong, R. T., A. S. Kushnir, and J. M. White. 2000. The transmembrane domain of influenza hemagglutinin exhibits a stringent length requirement to support the hemifusion to fusion transition. J. Cell Biol. 151:425-437.
4. Blissard, G. W., and G. F. Rohrmann. 1991. Baculovirus gp64 gene expression: analysis of sequences modulating early transcription and transactivation by IE1. J. Virol. 65:5820-5827.
5. Blissard, G. W., and J. R. Wenz. 1992. Baculovirus gp64 envelope glycoprotein is sufficient to mediate pH-dependent membrane fusion. J. Virol. 66:6829-6835.
6. Bos, E. C., L. Heijnen, W. Luytjes, and W. J. Spaan. 1995. Mutational analysis of the murine coronavirus spike protein: effect on cell-to-cell fusion. Virology 214:453-463.
7. Caballero, M., J. Carabana, J. Ortego, R. Fernandez-Munoz, and M. L. Celma. 1998. Measles virus fusion protein is palmitoylated on transmembrane- intracytoplasmic cysteine residues which participate in cell fusion. J. Virol. 72:8198-8204. (Pubitemid 28421816)
8. Chang, K. W., Y. Sheng, and J. L. Gombold. 2000. Coronavirus-induced membrane fusion requires the cysteine-rich domain in the spike protein. Virology 269:212-224.
9. Chiu, J., P. E. March, R. Lee, and D. Tillett. 2004. Site-directed, ligase-independent mutagenesis (SLIM): a single-tube methodology approaching 100% efficiency in 4 h. Nucleic Acids Res. 32:e174.
10. Cleverley, D. Z., and J. Lenard. 1998. The transmembrane domain in viral fusion: essential role for a conserved glycine residue in vesicular stomatitis virus G protein. Proc. Natl. Acad. Sci. USA 95:3425-3430.
11. de Planque, M. R., J. W. Boots, D. T. Rijkers, R. M. Liskamp, D. V. Greathouse, and J. A. Killian. 2002. The effects of hydrophobic mismatch between phosphatidylcholine bilayers and transmembrane alpha-helical peptides depend on the nature of interfacially exposed aromatic and charged residues. Biochemistry 41:8396-8404.
12. de Planque, M. R., E. Goormaghtigh, D. V. Greathouse, R. E. Koeppe II, J. A. Kruijtzer, R. M. Liskamp, B. de Kruijff, and J. A. Killian. 2001. Sensitivity of single membrane-spanning alpha-helical peptides to hydrophobic mismatch with a lipid bilayer: effects on backbone structure, orientation, and extent of membrane incorporation. Biochemistry 40:5000-5010.
13. de Planque, M. R., and J. A. Killian. 2003. Protein-lipid interactions studied with designed transmembrane peptides: role of hydrophobic matching and interfacial anchoring. Mol. Membr. Biol. 20:271-284.
14. Epand, R. M. 2003. Fusion peptides and the mechanism of viral fusion. Biochim. Biophys. Acta 1614:116-121.
15. Harzer, U., and B. Bechinger. 2000. Alignment of lysine-anchored membrane peptides under conditions of hydrophobic mismatch: a CD, 15N and 31P solid-state NMR spectroscopy investigation. Biochemistry 39:13106-13114.
16. Hefferon, K., A. Oomens, S. Monsma, C. Finnerty, and G. Blissard. 1999. Host cell receptor binding by baculovirus GP64 and kinetics of virion entry. Virology 258:455-468.
17. Herniou, E. A., J. A. Olszewski, J. S. Cory, and D. R. O'Reilly. 2003. The genome sequence and evolution of baculoviruses. Annu. Rev. Entomol. 48:211-234. (Pubitemid 37365392)
18. Hink, W. F. 1970. Established insect cell line from the cabbage looper, Trichoplusia ni. Nature 226:466-467.
19. Hohmann, A. W., and P. Faulkner. 1983. Monoclonal antibodies to baculovirus structural proteins: determination of specificities by Western blot analysis. Virology 125:432-444.
20. Jarvis, D. L., L. Wills, G. Burow, and D. A. Bohlmeyer. 1998. Mutational analysis of the N-linked glycans on Autographa californica nucleopolyhedrovirus gp64. J. Virol. 72:9459-9469. (Pubitemid 28520809)
21. Kadlec, J., S. Loureiro, N. G. Abrescia, D. I. Stuart, and I. M. Jones. 2008. The postfusion structure of baculovirus gp64 supports a unified view of viral fusion machines. Nat. Struct. Mol. Biol. 15:1024-1030.
22. Langosch, D., M. Hofmann, and C. Ungermann. 2007. The role of transmembrane domains in membrane fusion. Cell. Mol. Life Sci. 64:850-864. (Pubitemid 46597757)
23. Li, Z., and G. W. Blissard. 2008. Functional analysis of the transmembrane (TM) domain of the Autographa californica multicapsid nucleopolyhedrovirus GP64 protein: substitution of heterologous TM domains. J. Virol. 82: 3329-3341.
24. Liao, M., and M. Kielian. 2005. The conserved glycine residues in the transmembrane domain of the Semliki Forest virus fusion protein are not required for assembly and fusion. Virology 332:430-437.
25. Long, G., X. Pan, R. Kormelink, and J. M. Vlak. 2006. Functional entry of baculovirus into insect and mammalian cells is dependent on clathrin-mediated endocytosis. J. Virol. 80:8830-8833. (Pubitemid 44384892)
26. Lorin, A., B. Charloteaux, Y. Fridmann-Sirkis, A. Thomas, Y. Shai, and R. Brasseur. 2007. Mode of membrane interaction and fusogenic properties of a de novo transmembrane model peptide depend on the length of the hydrophobic core. J. Biol. Chem. 282:18388-18396. (Pubitemid 47100240)
27. Luckow, V. A., S. C. Lee, G. F. Barry, and P. O. Olins. 1993. Efficient generation of infectious recombinant baculoviruses by site- specific transposon- mediated insertion of foreign genes into a baculovirus genome propagated in Escherichia coli. J. Virol. 67:4566-4579. (Pubitemid 23215935)
28. Lung, O., M. Westenberg, J. M. Vlak, D. Zuidema, and G. W. Blissard. 2002. Pseudotyping Autographa californica multicapsid nucleopolyhedrovirus (AcMNPV): F proteins from group II NPVs are functionally analogous to AcMNPV GP64. J. Virol. 76:5729-5736.
29. Marheineke, K., S. Grunewald, W. Christie, and H. Reilander. 1998. Lipid composition of Spodoptera frugiperda (Sf9) and Trichoplusia ni (Tn) insect cells used for baculovirus infection. FEBS Lett. 441:49-52. (Pubitemid 29012370)
30. Maruniak, J. W., and M. D. Summers. 1981. Autographa californica nuclear polyhedrosis virus phosphoproteins and synthesis of intracellular proteins after virus infection. Virology 109:25-34.
31. McGinnes, L., T. Sergel, and T. Morrison. 1993. Mutations in the transmembrane domain of the HN protein of Newcastle disease virus affect the structure and activity of the protein. Virology 196:101-110.
32. Melikyan, G. B., S. A. Brener, D. C. Ok, and F. S. Cohen. 1997. Inner but not outer membrane leaflets control the transition from glycosylphosphatidylinositol- anchored influenza hemagglutinin-induced hemifusion to full fusion. J. Cell Biol. 136:995-1005. (Pubitemid 27131732)
33. Melikyan, G. B., S. Lin, M. G. Roth, and F. S. Cohen. 1999. Amino acid sequence requirements of the transmembrane and cytoplasmic domains of influenza virus hemagglutinin for viable membrane fusion. Mol. Biol. Cell 10:1821-1836.
34. Melikyan, G. B., J. M. White, and F. S. Cohen. 1995. GPI-anchored influenza hemagglutinin induces hemifusion to both red blood cell and planar bilayer membranes. J. Cell Biol. 131:679-691.
35. Monsma, S. A., and G. W. Blissard. 1995. Identification of a membrane fusion domain and an oligomerization domain in the baculovirus GP64 envelope fusion protein. J. Virol. 69:2583-2595.
36. Monsma, S. A., A. G. Oomens, and G. W. Blissard. 1996. The GP64 envelope fusion protein is an essential baculovirus protein required for cell-to-cell transmission of infection. J. Virol. 70:4607-4616. (Pubitemid 26191147)
37. Oomens, A. G. P., and G. W. Blissard. 1999. Requirement for GP64 to drive efficient budding of Autographa californica multicapsid nucleopolyhedrovirus. Virology 254:297-314.
38. Oomens, A. G. P., S. A. Monsma, and G. W. Blissard. 1995. The baculovirus GP64 envelope fusion protein: synthesis, oligomerization, and processing. Virology 209:592-603.
39. Owens, R. J., C. Burke, and J. K. Rose. 1994. Mutations in the membrane- spanning domain of the human immunodeficiency virus envelope glycoprotein that affect fusion activity. J. Virol. 68:570-574. (Pubitemid 24974668)
40. Ozdirekcan, S., D. T. Rijkers, R. M. Liskamp, and J. A. Killian. 2005. Influence of flanking residues on tilt and rotation angles of transmembrane peptides in lipid bilayers. A solid-state 2H NMR study. Biochemistry 44: 1004-1012.
41. Pietschmann, T., H. Zentgraf, A. Rethwilm, and D. Lindemann. 2000. An evolutionarily conserved positively charged amino acid in the putative membrane- spanning domain of the foamy virus envelope protein controls fusion activity. J. Virol. 74:4474-4482. (Pubitemid 30237872)
42. Plonsky, I., M. S. Cho, A. G. P. Oomens, G. W. Blissard, and J. Zimmerberg. 1999. An analysis of the role of the target membrane on the gp64-induced fusion pore. Virology 253:65-76.
43. Plonsky, I., and J. Zimmerberg. 1996. The initial fusion pore induced by baculovirus GP64 is large and forms quickly. J. Cell Biol. 135:1831-1839. (Pubitemid 27036444)
44. Ragheb, J. A., and W. F. Anderson. 1994. Uncoupled expression of Moloney murine leukemia virus envelope polypeptides SU and TM: a functional analysis of the role of TM domains in viral entry. J. Virol. 68:3207-3219.
45. Ren, J., S. Lew, Z. Wang, and E. London. 1997. Transmembrane orientation of hydrophobic alpha-helices is regulated both by the relationship of helix length to bilayer thickness and by the cholesterol concentration. Biochemistry 36:10213-10220.
46. Senes, A., M. Gerstein, and D. M. Engelman. 2000. Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently and in association with beta-branched residues at neighboring positions. J. Mol. Biol. 296:921-936.
47. Sharpe, S., K. R. Barber, C. W. Grant, D. Goodyear, and M. R. Morrow. 2002. Organization of model helical peptides in lipid bilayers: insight into the behavior of single-span protein transmembrane domains. Biophys. J. 83:345-358.
48. Sparr, E., W. L. Ash, P. V. Nazarov, D. T. Rijkers, M. A. Hemminga, D. P. Tieleman, and J. A. Killian. 2005. Self-association of transmembrane alpha-helices in model membranes: importance of helix orientation and role of hydrophobic mismatch. J. Biol. Chem. 280:39324-39331.
49. Strandberg, E., S. Ozdirekcan, D. T. Rijkers, P. C. van der Wel, R. E. Koeppe II, R. M. Liskamp, and J. A. Killian. 2004. Tilt angles of transmembrane model peptides in oriented and non-oriented lipid bilayers as determined by 2H solid-state NMR. Biophys. J. 86:3709-3721. (Pubitemid 38780249)
50. Tamm, L. K., J. Crane, and V. Kiessling. 2003. Membrane fusion: a structural perspective on the interplay of lipids and proteins. Curr. Opin. Struct. Biol. 13:453-466.
51. Taylor, G. M., and D. A. Sanders. 1999. The role of the membrane-spanning domain sequence in glycoprotein-mediated membrane fusion. Mol. Biol. Cell 10:2803-2815.
52. Ujike, M., K. Nakajima, and E. Nobusawa. 2004. Influence of acylation sites of influenza B virus hemagglutinin on fusion pore formation and dilation. J. Virol. 78:11536-11543. (Pubitemid 39390739)
53. Unterreitmeier, S., A. Fuchs, T. Schaffler, R. G. Heym, D. Frishman, and D. Langosch. 2007. Phenylalanine promotes interaction of transmembrane domains via GxxxG motifs. J. Mol. Biol. 374:705-718. (Pubitemid 350018773)
54. Volkman, L. E., and P. A. Goldsmith. 1984. Budded Autographa californica NPV 64K protein: further biochemical analysis and effects of postimmunoprecipitation sample preparation conditions. Virology 139:295-302.
55. Volkman, L. E., and P. A. Goldsmith. 1985. Mechanism of neutralization of budded Autographa californica nuclear polyhedrosis virus by a monoclonal antibody: inhibition of entry by adsorptive endocytosis. Virology 143:185-195.
56. Webb, R. J., J. M. East, R. P. Sharma, and A. G. Lee. 1998. Hydrophobic mismatch and the incorporation of peptides into lipid bilayers: a possible mechanism for retention in the Golgi. Biochemistry 37:673-679.
57. Weiss, T. M., P. C. van der Wel, J. A. Killian, R. E. Koeppe II, and H. W. Huang. 2003. Hydrophobic mismatch between helices and lipid bilayers. Biophys. J. 84:379-385. (Pubitemid 36026406)
58. Xu, Y., F. Zhang, Z. Su, J. A. McNew, and Y. K. Shin. 2005. Hemifusion in SNARE-mediated membrane fusion. Nat. Struct. Mol. Biol. 12:417-422. (Pubitemid 43085901)
59. Zhang, S. X., Y. Han, and G. W. Blissard. 2003. Palmitoylation of the Autographa californica multicapsid nucleopolyhedrovirus envelope glycoprotein GP64: mapping, functional studies, and lipid rafts. J. Virol. 77:6265-6273.
60. Zhou, J., and G. W. Blissard. 2008. Identification of a GP64 subdomain involved in receptor binding by budded virions of the baculovirus AcMNPV. J. Virol. 82:4449-4460.
61. Zhou, J., and G. W. Blissard. 2006. Mapping the conformational epitope of a neutralizing antibody (AcV1) directed against the AcMNPV GP64 protein. Virology 352:427-437.