Basic residues in the Mason-Pfizer monkey virus gag matrix domain regulate intracellular trafficking and capsid-membrane interactions

Journal of Virology

Volumn 81, Issue 17, 2007, Pages 8977-8988

  Stansell, Elizabeth ^a,d   Apkarian, Robert ^a   Haubova, Sarka ^b   Diehl, William E ^a   Tytler, Ewan M ^c   Hunter, Eric ^a  

^a EMORY UNIVERSITY   (United States)

^b INSTITUTE OF CHEMICAL TECHNOLOGY   (Czech Republic)

^c Kentucky   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; AMINO ACID; ARGININE; GAG PROTEIN; LYSINE; MATRIX PROTEIN; MUTANT PROTEIN;

ANIMAL CELL; ARTICLE; CELL SURFACE; CELLULAR DISTRIBUTION; CYTOPLASM; ELECTRON MICROSCOPY; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; LIPID BILAYER; MASON PFIZER MONKEY VIRUS; MEMBRANE VESICLE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; REGULATORY MECHANISM; VIRION; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS ENVELOPE; VIRUS INFECTIVITY; WILD TYPE;

AMINO ACID SUBSTITUTION; AMINO ACIDS, BASIC; ANIMALS; CELL LINE; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOPLASM; CYTOPLASMIC VESICLES; GENE PRODUCTS, GAG; HUMANS; MASON-PFIZER MONKEY VIRUS; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT;

MASON-PFIZER MONKEY VIRUS; MIRIDAE; PAPAYA MOSAIC VIRUS;

EID: 34548182230     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00657-07     Document Type: Article

References (67)

1. Ames, J. B., R. Ishima, T. Tanaka, J. I. Gordon, L. Stryer, and M. Ikura. 1997. Molecular mechanics of calcium-myristoyl switches. Nature 389:198-202.
2. Bennett, R. P., T. D. Nelle, and J. W. Wills. 1993. Functional chimeras of the Rous sarcoma virus and human immunodeficiency virus Gag proteins. J. Virol. 67:6487-6498.
3. Bradac, J., and E. Hunter. 1984. Polypeptides of Mason-Pfizer monkey virus. 1. Synthesis and processing of the gag-gene products. Virology 138:260-275.
4. Brody, B. A., and E. Hunter. 1992. Mutations within the env gene of Mason-Pfizer monkey virus: effects on protein transport and SU-TM association. J. Virol. 66:3466-3475.
5. Bryant, M., and L. Ratner. 1990. Myristoylation-dependent replication and assembly of human immunodeficiency virus 1. Proc. Natl. Acad. Sci. USA 87:523-527.
6. Callahan, E. M., and J. W. Wills. 2000. Repositioning basic residues in the M domain of the Rous sarcoma virus Gag protein. J. Virol. 74:11222-11229.
7. Conte, M. R., M. Klikova, E. Hunter, T. Ruml, and S. Matthews. 1997. The three-dimensional solution structure of the matrix protein from the type D retrovirus, the Mason-Pfizer monkey virus, and implications for the morphology of retroviral assembly. EMBO J. 16:5819-5826.
8. Gag 1 domain mediates Gag-Gag interactions. J. Virol. 78:1230-1242.
9. Escola, J. M., M. J. Kleijmeer, W. Stoorvogel, J. M. Griffith, O. Yoshie, and H. J. Geuze. 1998. Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J. Biol. Chem. 273:20121-20127.
10. Facke, M., A. Janetzko, R. L. Shoeman, and H. G. Krausslich. 1993. A large deletion in the matrix domain of the human immunodeficiency virus gag gene redirects virus particle assembly from the plasma membrane to the endoplasmic reticulum. J. Virol. 67:4972-4980.
11. Freed, E. O., J. M. Orenstein, A. J. Buckler-White, and M. A. Martin. 1994. Single amino acid changes in the human immunodeficiency virus type 1 matrix protein block virus particle production. J. Virol. 68:5311-5320.
12. Fukuda, M. 1991. Lysosomal membrane glycoproteins. Structure, biosynthesis, and intracellular trafficking. J. Biol. Chem. 266:21327- 21330.
13. George, D. J., and P. J. Blackshear. 1992. Membrane association of the myristoylated alanine-rich C kinase substrate (MARCKS) protein appears to involve myristate-dependent binding in the absence of a myristoyl protein receptor. J. Biol. Chem. 267:24879-24885.
14. Gottlinger, H. G., J. G. Sodroski, and W. A. Haseltine. 1989. Role of capsid precursor processing and myristoylation in morphogenesis and infectivity of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 86:5781-5785.
15. Gottwein, E., J. Bodem, B. Muller, A. Schmechel, H. Zentgraf, and H. G. Krausslich. 2003. The Mason-Pfizer monkey virus PPPY and PSAP motifs both contribute to virus release. J. Virol. 77:9474-9485.
16. Guex, N., and M. C. Peitsch. 1997. SWISS-MODEL and the Swiss-Pdb-Viewer: an environment for comparative protein modeling. Electrophoresis 18:2714-2723.
17. Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science 279:509-514.
18. Hartwig, J. H., M. Thelen, A. Rosen, P. A. Janmey, A. C. Nairn, and A. Aderem. 1992. MARCKS is an actin filament crosslinking protein regulated by protein kinase C and calcium-calmodulin. Nature 356:618-622.
19. Hill, C. P., D. Worthylake, D. P. Bancroft, A. M. Christensen, and W. I. Sundquist. 1996. Crystal structures of the trimeric human immunodeficiency virus type 1 matrix protein: implications for membrane association and assembly. Proc. Natl. Acad. Sci. USA 93:3099-3104.
20. Hunter, E., J. Casey, B. Hahn, M. Hayami, B. Korber, R. Kurth, J. Neil, A. Rethwilm, P. Sonigo, and J. Stoye. 2000. Retroviridae, p. 369-387. In M. H. V. van Regenmortel, C. M. Fauquet, D. L. Bishop, E. B. Carstens, M. K. Estes, S. M. Lemon, J. Maniloff, M. A. Mayo, D. J. McGeoch, C. R. Pringle, and R. B. Wickner (ed.), Virus taxonomy. Seventh report of the International Committee on Taxonomy of Viruses. Academic Press, London, United Kingdom.
21. Katzmann, D. J., G. Odorizzi, and S. D. Emr. 2002. Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3:893-905.
22. McLaughlin, S., and A. Aderem. 1995. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. Trends Biochem. Sci. 20:272-276.
23. Morita, E., and W. I. Sundquist. 2004. Retrovirus budding. Annu. Rev. Cell Dev. Biol. 20:395-425.
24. Mura, M., P. Murcia, M. Caporale, T. E. Spencer, K. Nagashima, A. Rein, and M. Palmarini. 2004. Late viral interference induced by transdominant Gag of an endogenous retrovirus. Proc. Natl. Acad. Sci. USA 101:11117-11122.
25. Newman, R. M., L. Hall, M. Connole, G. L. Chen, S. Sato, E. Yuste, W. Diehl, E. Hunter, A. Kaur, G. M. Miller, and W. E. Johnson. 2006. Balancing selection and the evolution of functional polymorphism in Old World monkey TRIM5alpha. Proc. Natl. Acad. Sci. USA 103:19134-19139.
26. Ono, A., S. D. Ablan, S. J. Lockett, K. Nagashima, and E. O. Freed. 2004. Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 Gag targeting to the plasma membrane. Proc. Natl. Acad. Sci. USA 101:14889-14894.
27. Ono, A., and E. O. Freed. 2004. Cell-type-dependent targeting of human immunodeficiency virus type 1 assembly to the plasma membrane and the multivesicular body. J. Virol. 78:1552-1563.
28. Ono, A., M. Huang, and E. O. Freed. 1997. Characterization of human immunodeficiency virus type 1 matrix revertants: effects on virus assembly, Gag processing, and Env incorporation into virions. J. Virol. 71:4409-4418.
29. Ono, A., J. M. Orenstein, and E. O. Freed. 2000. Role of the Gag matrix domain in targeting human immunodeficiency virus type 1 assembly. J. Virol. 74:2855-2866.
30. Paillart, J. C., and H. G. Gottlinger. 1999. Opposing effects of human immunodeficiency virus type 1 matrix mutations support a myristyl switch model of Gag membrane targeting. J. Virol. 73:2604-2612.
31. Parker, S. D., and E. Hunter. 2001. Activation of the Mason-Pfizer monkey virus protease within immature capsids in vitro. Proc. Natl. Acad. Sci. USA 98:14631-14636.
32. Parker, S. D., J. S. Wall, and E. Hunter. 2001. Analysis of Mason-Pfizer monkey virus Gag particles by scanning transmission electron microscopy. J. Virol. 75:9543-9548.
33. Peitzsch, R. M., and S. McLaughlin. 1993. Binding of acylated peptides and fatty acids to phospholipid vesicles: pertinence to myristoylated proteins. Biochemistry 32:10436-10443.
34. Perez-Caballero, D., T. Hatziioannou, J. Martin-Serrano, and P. D. Bieniasz. 2004. Human immunodeficiency virus type 1 matrix inhibits and confers cooperativity on Gag precursor-membrane interactions. J. Virol. 78:9560-9563.
35. Rao, Z., A. S. Belyaev, E. Fry, P. Roy, I. M. Jones, and D. I. Stuart. 1995. Crystal structure of SIV matrix antigen and implications for virus assembly. Nature 378:743-747.
36. Rauch, M. E., C. G. Ferguson, G. D. Prestwich, and D. S. Cafiso. 2002. Myristoylated alanine-rich C kinase substrate (MARCKS) sequesters spin-labeled phosphatidylinositol 4,5-bisphosphate in lipid bilayers. J. Biol. Chem. 277:14068-14076.
37. Ray, S., S. Zozulya, G. A. Niemi, K. M. Flaherty, D. Brolley, A. M. Dizhoor, D. B. McKay, J. Hurley, and L. Stryer. 1992. Cloning, expression, and crystallization of recoverin, a calcium sensor in vision. Proc. Natl. Acad. Sci. USA 89:5705-5709.
38. Reil, H., A. A. Bukovsky, H. R. Gelderblom, and H. G. Gottlinger. 1998. Efficient HIV-1 replication can occur in the absence of the viral matrix protein. EMBO J. 17:2699-2708.
39. Rhee, S. S., and E. Hunter. 1990. A single amino acid substitution within the matrix protein of a type D retrovirus converts its morphogenesis to that of a type C retrovirus. Cell 63:77-86.
40. Rhee, S. S., and E. Hunter. 1991. Amino acid substitutions within the matrix protein of type D retroviruses affect assembly, transport and membrane association of a capsid. EMBO J. 10:535-546.
41. Rhee, S. S., and E. Hunter. 1987. Myristylation is required for intracellular transport but not for assembly of D-type retrovirus capsids. J. Virol. 61:1045-1053.
42. Rinnerthaler, G., M. Herzog, M. Klappacher, H. Kunka, and J. V. Small. 1991. Leading edge movement and ultrastructure in mouse macrophages. J. Struct. Biol 106:1-16.
43. Saad, J. S., J. Miller, J. Tai, A. Kim, R. H. Ghanam, and M. F. Summers. 2006. Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. Proc. Natl. Acad. Sci. USA 103:11364-11369.
44. Sakalian, M., S. D. Parker, R. A. Weldon, Jr., and E. Hunter. 1996. Synthesis and assembly of retrovirus Gag precursors into immature capsids in vitro. J. Virol. 70:3706-3715.
45. Gag. J. Virol. 72:2723-2732.
46. Scalettar, B. A., J. R. Swedlow, J. W. Sedat, and D. A. Agard. 1996. Dispersion, aberration and deconvolution in multi-wavelength fluorescence images. J. Microsc. 182:50-60.
47. Seykora, J. T., M. M. Myat, L. A. Allen, J. V. Ravetch, and A. Aderem. 1996. Molecular determinants of the myristoyl-electrostatic switch of MARCKS. J. Biol. Chem. 271:18797-18802.
48. Sfakianos, J. N., and E. Hunter. 2003. M-PMV capsid transport is mediated by Env/Gag interactions at the pericentriolar recycling endosome. Traffic 4:671-680.
49. Sfakianos, J. N., R. A. LaCasse, and E. Hunter. 2003. The M-PMV cytoplasmic targeting-retention signal directs nascent Gag polypeptides to a pericentriolar region of the cell. Traffic 4:660-670.
50. Song, C., S. R. Dubay, and E. Hunter. 2003. A tyrosine motif in the cytoplasmic domain of Mason-Pfizer monkey virus is essential for the incorporation of glycoprotein into virions. J. Virol. 77:5192-5200.
51. Song, C., and E. Hunter. 2003. Variable sensitivity to substitutions in the N-terminal heptad repeat of Mason-Pfizer monkey virus transmembrane protein. J. Virol. 77:7779-7785.
52. Song, C., K. Micoli, H. Bauerova, I. Pichova, and E. Hunter. 2005. Amino acid residues in the cytoplasmic domain of the Mason-Pfizer monkey virus glycoprotein critical for its incorporation into virions. J. Virol. 79:11559-11568.
53. Sonigo, P., C. Barker, E. Hunter, and S. Wain-Hobson. 1986. Nucleotide sequence of Mason-Pfizer monkey virus: an immunosuppressive D-type retrovirus. Cell 45:375-385.
54. Sonnichsen, B., S. De Renzis, E. Nielsen, J. Rietdorf, and M. Zerial. 2000. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 149:901-914.
55. Spearman, P., R. Horton, L. Ratner, and I. Kuli-Zade. 1997. Membrane binding of human immunodeficiency virus type 1 matrix protein in vivo supports a conformational myristyl switch mechanism. J. Virol. 71:6582-6592.
56. Stansell, E., E. Tytler, M. R. Walter, and E. Hunter. 2004. An early stage of Mason-Pfizer monkey virus budding is regulated by the hydrophobicity of the Gag matrix domain core. J. Virol. 78:5023-5031.
57. Stumpo, D. J., J. M. Graff, K. A. Albert, P. Greengard, and P. J. Blackshear. 1989. Molecular cloning, characterization, and expression of a cDNA encoding the "80- to 87-kDa" myristoylated alanine-rich C kinase substrate: a major cellular substrate for protein kinase C. Proc. Natl. Acad. Sci. USA 86:4012-4016.
58. Tanaka, T., J. B. Ames, T. S. Harvey, L. Stryer, and M. Ikura. 1995. Sequestration of the membrane-targeting myristoyl group of recoverin in the calcium-free state. Nature 376:444-447.
59. Tang, C., E. Loeliger, P. Luncsford, I. Kinde, D. Beckett, and M. F. Summers. 2004. Entropic switch regulates myristate exposure in the HIV-1 matrix protein. Proc. Natl. Acad. Sci. USA 101:517-522.
60. Taniguchi, H., and S. Manenti. 1993. Interaction of myristoylated alanine-rich protein kinase C substrate (MARCKS) with membrane phospholipids. J. Biol. Chem. 268:9960-9963.
61. von Schwedler, U. K., M. Stuchell, B. Muller, D. M. Ward, H. Y. Chung, E. Morita, H. E. Wang, T. Davis, G. P. He, D. M. Cimbora, A. Scott, H. G. Krausslich, J. Kaplan, S. G. Morham, and W. I. Sundquist. 2003. The protein network of HIV budding. Cell 114:701-713.
62. Wang, J., A. Arbuzova, G. Hangyas-Mihalyne, and S. McLaughlin. 2001. The effector domain of myristoylated alanine-rich C kinase substrate binds strongly to phosphatidylinositol 4,5-bisphosphate. J. Biol. Chem. 276:5012-5019.
63. Weed, S. A., and J. T. Parsons. 2001. Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene 20:6418-6434.
64. Yasuda, J., and E. Hunter. 1998. A proline-rich motif (PPPY) in the Gag polyprotein of Mason-Pfizer monkey virus plays a maturation-independent role in virion release. J. Virol. 72:4095-4103.
65. Yuan, X., X. Yu, T. H. Lee, and M. Essex. 1993. Mutations in the N-terminal region of human immunodeficiency virus type 1 matrix protein block intracellular transport of the Gag precursor. J. Virol. 67:6387-6394.
66. 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.
67. Zozulya, S., and L. Stryer. 1992. Calcium-myristoyl protein switch. Proc. Natl. Acad. Sci. USA 89:11569-11573.