Rous sarcoma virus gag has no specific requirement for phosphatidylinositol-(4,5)-bisphosphate for plasma membrane association in vivo or for liposome interaction in vitro

Journal of Virology

Volumn 85, Issue 20, 2011, Pages 10851-10860

  Chan, Jany ^a   Dick, Robert A ^a   Vogt, Volker M ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; GREEN FLUORESCENT PROTEIN; LIPOSOME; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHATIDYLSERINE;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CHICKEN; CONTROLLED STUDY; FIBROBLAST; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; QUAIL; ROUS SARCOMA ONCOVIRUS; VIRUS LIKE AGENT;

ANIMALS; BIRDS; CELL LINE; CELL MEMBRANE; GENE PRODUCTS, GAG; HIV-1; LIPOSOMES; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN BINDING; ROUS SARCOMA VIRUS; VIRUS RELEASE;

ALPHARETROVIRUS; AVES; HUMAN IMMUNODEFICIENCY VIRUS 1; PIPS; RICE STRIPE VIRUS; ROUS SARCOMA VIRUS;

EID: 80054992503     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00760-11     Document Type: Article

References (68)

1. Alfadhli, A., A. Still, and E. Barklis. 2009. Analysis of human immunodeficiency virus type 1 matrix binding to membranes and nucleic acids. J. Virol. 83:12196-12203.
2. Aloia, R. C., H. Tian, and F. C. Jensen. 1993. Lipid composition and fluidity of the human immunodeficiency virus envelope and host cell plasma membranes. Proc. Natl. Acad. Sci. U. S. A. 90:5181-5185.
3. Anraku, K., et al. 2010. Highly sensitive analysis of the interaction between HIV-1 Gag and phosphoinositide derivatives based on surface plasmon resonance. Biochemistry 49:5109-5116.
4. Brugger, B., et al. 2006. The HIV lipidome: a raft with an unusual composition. Proc. Natl. Acad. Sci. U. S. A. 103:2641-2646.
5. Callahan, E., and J. Wills. 2003. Link between genome packaging and rate of budding for Rous sarcoma virus. J. Virol. 77:9388-9398.
6. Callahan, E., and J. Wills. 2000. Repositioning basic residues in the M domain of the Rous sarcoma virus gag protein. J. Virol. 74:11222-11229.
7. Campbell, S., et al. 2001. Modulation of HIV-like particle assembly in vitro by inositol phosphates. Proc. Natl. Acad. Sci. U. S. A. 98:10875-10879.
8. Campbell, S., and V. M. Vogt. 1997. In vitro assembly of virus-like particles with Rous sarcoma virus Gag deletion mutants: identification of the p10 domain as a morphological determinant in the formation of spherical particles. J. Virol. 71:4425-4435.
9. Chan, R., et al. 2008. Retroviruses human immunodeficiency virus and murine leukemia virus are enriched in phosphoinositides. J. Virol. 82:11228-11238.
10. Chen, K., et al. 2008. Solution NMR characterizations of oligomerization and dynamics of equine infectious anemia virus matrix protein and its interaction with PIP2. Biochemistry 47:1928-1937.
11. Chukkapalli, V., I. Hogue, V. Boyko, W. Hu, and A. Ono. 2008. Interaction between the human immunodeficiency virus type 1 Gag matrix domain and phosphatidylinositol-(4,5)-bisphosphate is essential for efficient Gag membrane binding. J. Virol. 82:2405-2417.
12. Chukkapalli, V., S. J. Oh, and A. Ono. 2010. Opposing mechanisms involving RNA and lipids regulate HIV-1 Gag membrane binding through the highly basic region of the matrix domain. Proc. Natl. Acad. Sci. U. S. A. 107:1600-1605.
13. Dalton, A., P. Murray, D. Murray, and V. Vogt. 2005. Biochemical characterization of Rous sarcoma virus MA protein interaction with membranes. J. Virol. 79:6227-6238.
14. Dalton, A. K., D. Ako-Adjei, P. S. Murray, D. Murray, and V. M. Vogt. 2007. Electrostatic interactions drive membrane association of the human immunodeficiency virus type 1 Gag MA domain. J. Virol. 81:6434-6445.
15. del Alamo, M., J. L. Neira, and M. G. Mateu. 2003. Thermodynamic dissection of a low affinity protein-protein interface involved in human immunodeficiency virus assembly. J. Biol. Chem. 278:27923-27929.
16. DiNitto, J., and D. Lambright. 2006. Membrane and juxtamembrane targeting by PH and PTB domains. Biochim. Biophys. Acta 1761:850-867.
17. Dong, X., et al. 2005. AP-3 directs the intracellular trafficking of HIV-1 Gag and plays a key role in particle assembly. Cell 120:663-674.
18. Dou, J., et al. 2009. Characterization of a myristoylated, monomeric HIV Gag protein. Virology 387:341-352.
19. Ferguson, K., M. Lemmon, J. Schlessinger, and P. Sigler. 1995. Structure of the high affinity complex of inositol trisphosphate with a phospholipase C pleckstrin homology domain. Cell 83:1037-1046.
20. Fernandes, F., et al. 2011. Phosphoinositides direct equine infectious anemia virus gag trafficking and release. Traffic 12:438-451.
21. Finzi, A., A. Orthwein, J. Mercier, and E. A. Cohen. 2007. Productive human immunodeficiency virus type 1 assembly takes place at the plasma membrane. J. Virol. 81:7476-7490.
22. Freed, E., J. Orenstein, A. Buckler-White, and M. Martin. 1994. Single amino acid changes in the human immunodeficiency virus type 1 matrix protein block virus particle production. J. Virol. 68:5311-5320.
23. Freed, E. O. 2006. HIV-1 Gag: flipped out for PI(4,5)P(2). Proc. Natl. Acad. Sci. U. S. A. 103:11101-11102.
24. Gamble, T. R., et al. 1997. Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science 278:849-853.
25. Hamard-Peron, E., et al. 2010. Targeting of murine leukemia virus gag to the plasma membrane is mediated by PI(4,5)P2/PS and a polybasic region in the matrix. J. Virol. 84:503-515.
26. Hatanaka, H., et al. 2002. Structure of equine infectious anemia virus matrix protein. J. Virol. 76:1876-1883.
27. Heo, W. D., et al. 2006. PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314:1458-1461.
28. Hom, R. A., et al. 2007. pH-dependent binding of the Epsin ENTH domain and the AP180 ANTH domain to PI(4,5)P2-containing bilayers. J. Mol. Biol. 373:412-423.
29. Inlora, J., V. Chukkapalli, D. Derse, and A. Ono. 2011. Gag localization and virus-like particle release mediated by the matrix domain of human Tlymphotropic virus type-1 Gag are less dependent on phosphatidylinositol-(4,5)-bisphosphate than those mediated by the matrix domain of human immunodeficiency virus type-1 Gag. J. Virol. 85:3802-3810.
30. Jouvenet, N., et al. 2006. Plasma membrane is the site of productive HIV-1 particle assembly. PLoS Biol. 4:e435.
31. Kingston, R. L., et al. 2000. Structure and self-association of the Rous sarcoma virus capsid protein. Structure 8:617-628.
32. Kisseleva, M. V., M. P. Wilson, and P. W. Majerus. 2000. The isolation and characterization of a cDNA encoding phospholipid-specific inositol polyphosphate 5-phosphatase. J. Biol. Chem. 275:20110-20116.
33. Kutateladze, T. 2010. Translation of the phosphoinositide code by PI effectors. Nat. Chem. Biol. 6:507-513.
34. Lemmon, M. A., K. M. Ferguson, R. O'Brien, P. B. Sigler, and J. Schlessinger. 1995. Specific and high-affinity binding of inositol phosphates to an isolated pleckstrin homology domain. Proc. Natl. Acad. Sci. U. S. A. 92: 10472-10476.
35. Leventis, P. A., and S. Grinstein. 2010. The distribution and function of phosphatidylserine in cellular membranes. Annu. Rev. Biophys. 39:407-427.
36. Maldonado, R., and H. Blough. 1980. A comparative study of the lipids of plasma membranes of normal cells and those infected and transformed by Rous sarcoma virus. Virology 102:62-70.
37. Manna, D., et al. 2008. Differential roles of phosphatidylserine, PtdIns(4,5)P2, and PtdIns(3,4,5)P3 in plasma membrane targeting of C2 domains. Molecular dynamics simulation, membrane binding, and cell translocation studies of the PKCalpha C2 domain. J. Biol. Chem. 283:26047-26058.
38. McDonnell, J. M., et al. 1998. Solution structure and dynamics of the bioactive retroviral M domain from Rous sarcoma virus. J. Mol. Biol. 279:921-928.
39. McLaughlin, S., and D. Murray. 2005. Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438:605-611.
40. Murray, P., et al. 2005. Retroviral matrix domains share electrostatic homology: models for membrane binding function throughout the viral life cycle. Structure 13:1521-1531.
41. Nelle, T., and J. Wills. 1996. A large region within the Rous sarcoma virus matrix protein is dispensable for budding and infectivity. J. Virol. 70:2269-2276.
42. Ono, A., S. Ablan, S. Lockett, K. Nagashima, and E. Freed. 2004. Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 Gag targeting to the plasma membrane. Proc. Natl. Acad. Sci. U. S. A. 101:14889-14894.
43. Ono, A., J. Orenstein, and E. Freed. 2000. Role of the Gag matrix domain in targeting human immunodeficiency virus type 1 assembly. J. Virol. 74:2855-2866.
44. Parent, L., C. Wilson, M. Resh, and J. Wills. 1996. Evidence for a second function of the MA sequence in the Rous sarcoma virus Gag protein. J. Virol. 70:1016-1026.
45. Perez-Caballero, D., T. Hatziioannou, J. Martin-Serrano, and P. Bieniasz. 2004. Human immunodeficiency virus type 1 matrix inhibits and confers cooperativity on gag precursor-membrane interactions. J. Virol. 78:9560-9563.
46. Perlman, M., and M. Resh. 2006. Identification of an intracellular trafficking and assembly pathway for HIV-1 gag. Traffic 7:731-745.
47. Pessin, J. E., and M. Glaser. 1980. Budding of Rous sarcoma virus and vesicular stomatitis virus from localized lipid regions in the plasma membrane of chicken embryo fibroblasts. J. Biol. Chem. 255:9044-9050.
48. Provitera, P., F. Bouamr, D. Murray, C. Carter, and S. Scarlata. 2000. Binding of equine infectious anemia virus matrix protein to membrane bilayers involves multiple interactions. J. Mol. Biol. 296:887-898.
49. Quigley, J. P., D. B. Rifkin, and E. Reich. 1971. Phospholipid composition of Rous sarcoma virus, host cell membranes and other enveloped RNA viruses. Virology 46:106-116.
50. Rose, S., et al. 1992. Characterization of HIV-1 p24 self-association using analytical affinity chromatography. Proteins 13:112-119.
51. Saad, J., et al. 2008. Structure of the myristylated human immunodeficiency virus type 2 matrix protein and the role of phosphatidylinositol-(4,5)-bisphosphate in membrane targeting. J. Mol. Biol. 382:434-447.
52. Saad, J., et al. 2007. Mutations that mimic phosphorylation of the HIV-1 matrix protein do not perturb the myristyl switch. Protein Sci. 16:1793-1797.
53. Saad, J., et al. 2007. Point mutations in the HIV-1 matrix protein turn off the myristyl switch. J. Mol. Biol. 366:574-585.
54. Saad, J., et al. 2006. Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. Proc. Natl. Acad. Sci. U. S. A. 103: 11364-11369.
55. Scheifele, L., J. Rhoads, and L. Parent. 2003. Specificity of plasma membrane targeting by the Rous sarcoma virus gag protein. J. Virol. 77:470-480.
56. Scholz, I., et al. 2008. Analysis of human immunodeficiency virus matrix domain replacements. Virology 371:322-335.
57. Shkriabai, N., et al. 2006. Interactions of HIV-1 Gag with assembly cofactors. Biochemistry 45:4077-4083.
58. Soneoka, Y., S. Kingsman, and A. Kingsman. 1997. Mutagenesis analysis of the murine leukemia virus matrix protein: identification of regions important for membrane localization and intracellular transport. J. Virol. 71:5549-5559.
59. Spearman, P., J. J. Wang, N. Vander Heyden, and L. Ratner. 1994. Identification of human immunodeficiency virus type 1 Gag protein domains essential to membrane binding and particle assembly. J. Virol. 68:3232-3242.
60. Stansell, E., et al. 2007. Basic residues in the Mason-Pfizer monkey virus gag matrix domain regulate intracellular trafficking and capsid-membrane interactions. J. Virol. 81:8977-8988.
61. Tang, C., et al. 2004. Entropic switch regulates myristate exposure in the HIV-1 matrix protein. Proc. Natl. Acad. Sci. U. S. A. 101:517-522.
62. Uekama, N., T. Sugita, M. Okada, H. Yagisawa, and S. Tuzi. 2007. Phosphatidylserine induces functional and structural alterations of the membrane-associated pleckstrin homology domain of phospholipase C-delta1. FEBS J. 274:177-187.
63. Varnai, P., and T. Balla. 1998. Visualization of phosphoinositides that bind pleckstrin homology domains: calcium- and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J. Cell Biol. 143:501-510.
64. Wills, J., R. Craven, R. J. Weldon, T. Nelle, and C. Erdie. 1991. Suppression of retroviral MA deletions by the amino-terminal membrane-binding domain of p60src. J. Virol. 65:3804-3812.
65. Wiradjaja, F., et al. 2007. Inactivation of the phosphoinositide phosphatases Sac1p and Inp54p leads to accumulation of phosphatidylinositol 4,5-bisphosphate on vacuole membranes and vacuolar fusion defects. J. Biol. Chem. 282:16295-16307.
66. Yagisawa, H. 2006. Nucleocytoplasmic shuttling of phospholipase C-delta1: a link to Ca2+. J. Cell. Biochem. 97:233-243.
67. Yeung, T., et al. 2008. Membrane phosphatidylserine regulates surface charge and protein localization. Science 319:210-213.
68. Zhou, W., L. J. Parent, J. W. Wills, and M. D. Resh. 1994. Identification of a membrane-binding domain within the amino-terminal region of human immunodeficiency virus type 1 Gag protein which interacts with acidic phospholipids. J. Virol. 68:2556-2569.