Contribution of topology determinants of a viral movement protein to its membrane association, intracellular traffic, and viral cell-to-cell movement

Journal of Virology

Volumn 85, Issue 15, 2011, Pages 7797-7809

  Genoves A ^a,b   Pallas V ^a   Navarro, J A ^a  

^a Universitat Politècnica de València   (Spain)

^b CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PLANT VIRUS MOVEMENT PROTEIN; PROLINE; PROTEIN P7B; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MOTION; CELL TRANSPORT; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HYDROPHOBICITY; MELON NECROTIC SPOT VIRUS; MEMBRANE STRUCTURE; NICOTIANA BENTHAMIANA; NONHUMAN; PLANT VIRUS; PLASMODESMA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; RNA VIRUS; VIRUS MUTATION;

AMINO ACID SEQUENCE; CARMOVIRUS; CELL MOVEMENT; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; OPEN READING FRAMES; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT; VIRAL PROTEINS;

MELON NECROTIC SPOT VIRUS;

EID: 79960397172     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02465-10     Document Type: Article

References (62)

1. Adams, M. J., and J. F. Antoniw. 2005. Membrane proteins from plant viruses, p. 3-20. In W. B. Fischer (ed.),Viral membrane proteins: structure, function, and drug design. Kluwer Academic-Plenum Publishers, New York, NY.
2. Aparicio, F., V. Pallás, and J. A. Sánchez-Navarro. 2010. Implication of the C terminus of the Prunus necrotic ringspot virus movement protein in cellto-cell transport and in its interaction with the coat protein. J. Gen. Virol. 91:1865-1870.
3. Aparicio, F., J. A. Sánchez-Navarro, and V. Pallás. 2006. In vitro and in vivo mapping of the Prunus necrotic ringspot virus coat protein C-terminal dimerization domain by bimolecular fluorescence complementation. J. Gen. Virol. 87:1745-1750.
4. Barlowe, C. 2003. Signals for COPII-dependent export from the ER: what's the ticket out? Trends Cell Biol. 13:295-300.
5. Bechinger, B. 2001. Membrane insertion and orientation of polyalanine peptides: a 15N solid-state NMR spectroscopy investigation. Biophys. J. 81:2251-2256.
6. Brambillasca, S., et al. 2005. Transmembrane topogenesis of a tail-anchored protein is modulated by membrane lipid composition. EMBO J. 24:2533-2542.
7. Brandizzi, F., et al. 2002. The destination for single-pass membrane proteins is influenced markedly by the length of the hydrophobic domain. Plant Cell 14:1077-1092.
8. Brill, L. M., R. S. Nunn, T. W. Kahn, M. Yeager, and R. N. Beachy. 2000. Recombinant Tobacco mosaic virus movement protein is an RNA-binding, alpha-helical membrane protein. Proc. Natl. Acad. Sci. U. S. A. 97:7112-7117.
9. Byers, J. T., R. M. Guzzo, M. Salih, and B. S. Tuana. 2009. Hydrophobic profiles of the tail anchors in SLMAP dictate subcellular targeting. BMC Cell Biol. 10:48.
10. Cai, Y., et al. 2011. Multiple cytosolic and transmembrane determinants are required for the trafficking of SCAMP1 via an ER-Golgi-TGN-PM pathway. Plant J. doi:10.1111/j.1365-313X.2010.04469.x.
11. Chamberlain, A. K., Y. Lee, S. Kim, and J. U. Bowie. 2004. Snorkeling preferences foster an amino acid composition bias in transmembrane helices. J. Mol. Biol. 339:471-479.
12. Ciczora, Y., N. Callens, K. Séron, Y. Rouillé, and J. Dubuisson. 2010. Identification of a dominant endoplasmic reticulum-retention signal in yellow fever virus pre-membrane protein. J. Gen. Virol. 91:404-414.
13. Deber, C. M., and A. G. Therien. 2002. Putting the β-breaks on membrane protein misfolding. Nat. Struct. Biol. 9:318-319.
14. Dowhan, W., and M. Bogdanov. 2009. Lipid-dependent membrane protein topogenesis. Annu. Rev. Biochem. 78:515-540.
15. Dunlop, J., P. C. Jones, and M. E. Finbow. 1995. Membrane insertion and assembly of ductin: a polytopic channel with dual orientation. EMBO J. 14:3609-3616.
16. Fujiki, M., S. Kawakami, R. W. Kim, and R. N. Beachy. 2006. Domains of tobacco mosaic virus movement protein essential for its membrane association. J. Gen. Virol. 9:2699-2707.
17. Gavel, Y., and G. von Heijne. 1992. The distribution of charged amino acids in mitochondrial inner-membrane proteins suggests different modes of membrane integration for nuclearly and mitochondrially encoded proteins. Eur. J. Biochem. 205:1207-1215.
18. Genovés, A., J. A. Navarro, and V. Pallás. 2006. Functional analysis of the five Melon necrotic spot virus genome-encoded proteins. J. Gen. Virol. 87:2371-2380.
19. Genovés, A., J. A. Navarro, and V. Pallás. 2009. A self-interacting carmovirus movement protein plays a role in binding of viral RNA during the cell-to-cell movement and shows an actin cytoskeleton dependent location in cell periphery. Virology 395:133-142.
20. Genovés, A., J. A. Navarro, and V. Pallás. 2010. The intra- and intercellular movement of Melon necrotic spot virus (MNSV) depends on an active secretory pathway. Mol. Plant Microbe Interact. 23:263-272.
21. Goder, V., and M. Spiess. 2003. Molecular mechanism of signal sequence orientation in the endoplasmic reticulum. EMBO J. 22:3645-3653.
22. Granseth, E., G. von Heijne, and A. Elofsson. 2005. A study of the membrane-water interface region of membrane proteins. J. Mol. Biol. 346:377-385.
23. Guenoune-Gelbart, D., M. Elbaum, G. Sagi, A. Levy, and B. L. Epel. 2008. Tobacco mosaic virus (TMV) replicase and movement protein function synergistically in facilitating TMV spread by lateral diffusion in the plasmodesmal desmotubule of Nicotiana benthamiana. Mol. Plant Microbe Interact. 21:335-345.
24. Harries, P. A., et al. 2009. Differing requirements for actin and myosin by plant viruses for sustained intercellular movement. Proc. Natl. Acad. Sci. U. S. A. 106:17594-17599.
25. Hessa, T., et al. 2005. Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433:377-381.
26. Hessa, T., S. H. White, and G. von Heijne. 2005. Membrane insertion of a potassium channel voltage sensor. Science 307:1427.
27. Hessa, T., et al. 2007. Molecular code for transmembrane-helix recognition by the Sec61 translocon. Nature 450:1026-1030.
28. Higy, M., T. Junne, and M. Spiess. 2004. Topogenesis of membrane proteins at the endoplasmic reticulum. Biochemistry 43:12716-12722.
29. Huang, M., L. Jongejan, H. Zheng, L. Zhang, and J. F. Bol. 2001. Intracellular localization and movement phenotypes of Alfalfa mosaic virus movement protein mutants. Mol. Plant Microbe Interact. 14:1063-1074.
30. Huang, M., and L. Zhang. 1999. Association of the movement protein of Alfalfa mosaic virus with the endoplasmic reticulum and its trafficking in epidermal cells of onion bulb scales. Mol. Plant Microbe Interact. 12:680-690.
31. Kawakami, S., Y. Watanabe, and R. N. Beachy. 2004. Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc. Natl. Acad. Sci. U. S. A. 101:6291-6296.
32. Knoester, M., et al. 1998. Ethylene-insensitive tobacco lacks non-host resistance against soil-borne fungi. Proc. Natl. Acad. Sci. U. S. A. 95:1933-1937.
33. Laliberté, J. F., and H. Sanfaçon. 2010. Cellular remodeling during plant virus infection. Annu. Rev. Phytopathol. 48:69-91.
34. Lerch-Bader, M., C. Lundin, H. Kim, I. Nilsson, and G. von Heijne. 2008. Contribution of positively charged flanking residues to the insertion of transmembrane helices into the endoplasmic reticulum. Proc. Natl. Acad. Sci. U. S. A. 105:4127-4132.
35. Liang, J., L. Adamian, and R. Jackups, Jr. 2005. The membrane-water interface region of membrane proteins: structural bias and the anti-snorkeling effect. Trends Biochem. Sci. 30:355-357.
36. Liu, L. P., and C. M. Deber. 1999. Combining hydrophobicity and helicity: a novel approach to membrane protein structure prediction. Bioorg. Med. Chem. 7:1-7.
37. Lucas, W. J. 2006. Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344:169-184.
38. Lundin, C., H. Kim, I. Nilsson, S. White, and G. von Heijne. 2008. The molecular code for protein insertion in the ER membrane is similar for Nin-Cout and Nout-Cin transmembrane helices. Proc. Natl. Acad. Sci. U. S. A. 105:15702-15707.
39. Mandahar, C. L. 2006. Multiplication of RNA plant virus. Springer-Verlag, Dordrecht, The Netherlands.
40. Martínez-Gil, L., A. Saurí, M. Vilar, V. Pallás, and I. Mingarro. 2007. Membrane insertion of the p7B movement protein of Melon necrotic spot virus (MNSV). Virology 367:348-357.
41. Martínez-Gil, L., et al. 2009. Plant virus cell-to-cell movement is not dependent on the transmembrane disposition of its movement protein. J. Virol. 83:5535-5543.
42. Navarro, J. A., et al. 2006. RNA-binding properties and membrane insertion of Melon necrotic spot virus (MNSV) double gene block movement proteins. Virology 356:57-67.
43. Nilsson, J., B. Persson, and G. von Heijne. 2005. Comparative analysis of amino acid distributions in integral membrane proteins from 107 genomes. Proteins 60:606-616.
44. Peremyslov, V. V., Y. W. Pan, and V. V. Dolja. 2004. Movement protein of a closterovirus is a type III integral transmembrane protein localized to the endoplasmic reticulum. J. Virol. 78:3704-3709.
45. Reichel, C., and R. N. Beachy. 1998. Tobacco mosaic virus infection induces severe morphological changes of the endoplasmic reticulum. Proc. Natl. Acad. Sci. U. S. A. 19:11169-11174.
46. Ren, J., S. Lew, Z. Wang, and E. London. 1997. Transmembrane orientation of hydrophobic α-helices is regulated both by the relationships of helix length to bilayer thickness and by cholesterol concentration. Biochemestry 36: 10213-10220.
47. Riek, R. P., I. Rigoutsos, J. Novotny, and R. M. Graham. 2001. Non-alphahelical elements modulate polytopic membrane protein architecture. J. Mol. Biol. 306:349-362.
48. Sagi, G., A. Katz, D. Guenoune-Gelbart, and B. L. Epel. 2005. Class 1 reversibly glycosylated polypeptides are plasmodesmal-associated proteins delivered to plasmodesmata via the Golgi apparatus. Plant Cell 17:1788-1800.
49. Sambade, A., and M. Heinlein. 2009. Approaching the cellular mechanism that supports the intercellular spread of Tobacco mosaic virus. Plant Signal Behav. 4:35-38.
50. Saurí, A., P. J. McCormick, A. E. Johnson, and I. Mingarro. 2007. Sec61alpha and TRAM are sequentially adjacent to a nascent viral membrane protein during its ER integration. J. Mol. Biol. 366:366-374.
51. Saurí, A., S. Tamborero, L. Martínez-Gil, A. E. Johnson, and I. Mingarro. 2009. Viral membrane topology is dictated by multiple determinants in its sequence. J. Mol. Biol. 387:113-128.
52. Scholthof, H. B. 2005. Plant virus transport: motions of functional equivalence. Trends Plant Sci. 10:376-382.
53. Schwartz, M., J. Chen, W.-M. Lee, M. Janda, and P. Ahlquist. 2004. Alternate, virus-induced membrane rearrangements support positive-strand RNA virus genome replication. Proc. Natl. Acad. Sci. U. S. A. 101:11263-11268.
54. Szczesna-Skorupa, E., and B. Kemper. 2000. Endoplasmic reticulum retention determinants in the transmembrane and linker domains of cytochrome P450 2C1. J. Biol. Chem. 275:19409-19415.
55. Taliansky, M., L. Torrance, and N. O. Kalinina. 2008. Role of plant virus movement proteins. Methods Mol. Biol. 451:33-54.
56. Thomas, C., E. M. Bayer, C. Ritzenthaler, L. Fernandez-Calvino, and A. J. Maule. 2008. Specific targeting of a plasmodesmal protein affecting cell-tocell communication. PLoS Biol. 6:1-11.
57. Verchot-Lubicz, J., et al. 2010. Varied movement strategies employed by triple gene block-encoding viruses. Mol. Plant Microbe Interact. 23:1231-1247.
58. von Heijne, G. 1991. Proline kinks in transmembrane α-helices. J. Mol. Biol. 218:499-503.
59. von Heijne, G. 2006. Membrane-protein topology. Nat. Rev. Mol. Cell Biol. 7:909-918.
60. von Heijne, G. 2007. Formation of transmembrane helices in vivo-is hydrophobicity all that matters? J. Gen. Physiol. 129:353-356.
61. White, S. H., and G. von Heijne. 2005. Transmembrane helices before, during and after insertion. Curr. Opin. Struct. Biol. 15:378-386.
62. Zamyatnin, A. A., Jr., et al. 2006. Assessment of the integral membrane protein topology in living cells. Plant J. 46:145-154.