Structure of the Myristylated Human Immunodeficiency Virus Type 2 Matrix Protein and the Role of Phosphatidylinositol-(4,5)-Bisphosphate in Membrane Targeting

Journal of Molecular Biology

Volumn 382, Issue 2, 2008, Pages 434-447

  Saad, Jamil S ^a   Ablan, Sherimay D ^b   Ghanam, Ruba H ^a   Kim, Andrew ^a   Andrews, Kalola ^a   Nagashima, Kunio ^c   Soheilian, Ferri ^c   Freed, Eric O ^b   Summers, Michael F ^a  

^a UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c SAIC FREDERICK INC   (United States)

Author keywords

Gag; HIV 1, HIV 2; MA; matrix; myr; myristyl; phosphatidylinositol 4,5 bisphosphate; PI(4,5)P2

Indexed keywords

GAG PROTEIN; MATRIX PROTEIN; MYRISTIC ACID; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; IN VIVO STUDY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN TARGETING;

HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2;

EID: 50049091709     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.07.027     Document Type: Article

References (71)

1. Lemey P., Pybus O.G., Wang B., Saksena N.K., Salemi M., and Vandamme A.-M. Tracing the origin and history of the HIV-2 epidemic. Proc. Natl Acad. Sci. USA 100 (2003) 6588-6592
2. Poulsen A.G., Aaby P., Larsen O., Jensen H., Naucler A., Lisse I.M., et al. 9-year HIV-2-associated mortality in an urban community in Bissau, West Africa. Lancet 349 (1997) 911-914
3. Schim van der Loeff M.F., Jaffar S., Aveika A.A., Sabally S., Corrah T., Harding E., et al. Mortality of HIV-1, HIV-2 and HIV-1/HIV-2 dually infected patients in a clinic-based cohort in The Gambia. AIDS 16 (2002) 1775-1783
4. Ariyoshi K., Jaffar S., Alabi A.S., Berry N., Schim van der Loeff M.F., Sabally S., et al. Plasma RNA viral load predicts the rate of CD4 T cell decline and death in HIV-2-infected patients in West Africa. AIDS 14 (2000) 339-344
5. Mellors J.W., Rinaldo C.R., Gupta Jr. P., White R.M., Todd J.A., and Kingsley L.A. Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 272 (1996) 1167-1170
6. Popper S.J., Sarr A.D., Travers K.U., Gueye-Ndiaye A., Mboup S., Essex M.E., and Kanki P.J. Lower human immunodeficiency virus (HIV) type 2 viral load reflects the difference in pathogenicity of HIV-1 and HIV-2. J. Infect. Dis. 180 (1999) 1116-1121
7. Vesanen M., Stevens C.E., Taylor P.E., Rubinstein P., and Saksela K. Stability in controlling viral replication identifies long-term nonprogressors as a distinct subgroup among human immunodeficiency virus type 1-infected persons. J. Virol. 70 (1996) 9035-9040
8. Duvall M.G., Precopio M.L., Ambrozak D.A., Jaye A., McMichael A.J., Whittle H.C., et al. Polyfunctional T cell responses are a hallmark of HIV-2 infection. Eur. J. Immunol. 38 (2008) 350-363
9. Blaak H., van der Ende M.E., Boers P.H.M., Schuitemaker H., and Osterhaus A.D.M.E. In vitro replication capacity of HIV-2 variants from long-term aviremic individuals. Virology 353 (2006) 144-154
10. Blaak H., Boers P.H.M., van der Ende M.E., Schuitemaker H., and Osterhaus A.D.M.E. CCR5-restricted HIV type 2 variants from long-term aviremic individuals are less sensitive to inhibition by β-chemokines than low pathogenic HIV type 1 variants. AIDS Res. Human Retroviruses 24 (2008) 473-484
11. Morikawa Y., Goto T., Yasuoka D., Momose F., and Matano T. Defect of human immunodeficiency virus type 2 Gag assembly in Saccharomyces cerevisiae. J. Virol. 81 (2007) 9911-9921
12. gag virus-like particles from recombinant baculovirus-infected insect cells. Cell 59 (1989) 103-112
13. Ganser-Pomillos B.K., Yeager M., and Sundquist W.I. The structural biology of HIV assembly. Curr. Opin. Struct. Biol. 18 (2008) 203-217
14. Dong X., Li H., Derdowski A., Ding L., Burnett A., Chen X., et al. AP-3 directs the intracellular trafficking of HIV-1 Gag and plays a key role in particle assembly. Cell 120 (2005) 663-674
15. Hermida-Matsumoto L., and Resh M.D. Localization of human immunodeficiency virus type 1 Gag and Env at the plasma membrane by confocal imagine. J. Virol. 74 (2000) 8670-8679
16. Kiernan R.E., Ono A., Englund G., and Freed E.O. Role of matrix in an early postentry step in the human immunodeficiency virus type 1 life cycle. J. Virol. 72 (1998) 4116-4126
17. Kiernan R.E., Ono A., and Freed E.O. Reversion of a human immunodeficiency virus type 1 matrix mutation affecting Gag membrane binding, endogenous reverse transcriptase activity, and virus infectivity. J. Virol. 73 (1999) 4728-4737
18. Ono A., Orenstein J.M., and Freed E.O. Role of the Gag matrix domain in targeting human immunodeficiency virus type 1 assembly. J. Virol. 74 (2000) 2855-2866
19. Scarlata S., and Cater C. Role of HIV-1 Gag domains in viral assembly. Biochim. Biophys. Acta 1614 (2003) 62-72
20. Ehrlich L.S., Fong S., Scarlata S., Zybarth G., and Carter C. Partitioning of HIV-1 Gag and Gag-related proteins to membranes. Biochemistry 35 (1996) 3933-3943
21. Ono A., and Freed E.O. Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc. Natl. Acad. Sci. USA 98 (2001) 13925-13930
22. Spearman P., Horton R., Ratner L., and Kuli-Zade I. Membrane binding of human immunodeficiency virus type 1 matrix protein in vivo supports a conformational myristyl switch mechanism. J. Virol. 71 (1997) 6582-6592
23. Zhou W., Parent L.J., Wills J.W., and Resh M.D. 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 (1994) 2556-2569
24. Bouamr F., Scarlata S., and Carter C.A. Role of myristylation in HIV-1 Gag assembly. Biochemistry 42 (2003) 6408-6417
25. Ono A., Ablan S.D., Lockett S.J., Nagashima K., and Freed E.O. Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 Gag targeting to the plasma membrane. Proc. Natl Acad. Sci. USA 101 (2004) 14889-14894
26. Jouvenet N., Neil S.J.D., Bess C., Johnson M.C., Virgen C.A., Simon S.M., and Bieniasz P.D. Plasma membrane is the site of productive HIV-1 particle assembly. PLoS Biol. 4 (2006) e435
27. Demirov D., and Freed E.O. Retrovirus budding. Virus Res. 106 (2004) 87-102
28. Freed E.O. HIV-1 Gag proteins: diverse functions in the virus life cycle. Virology 251 (1998) 1-15
29. Saad J.S., Miller J., Tai J., Kim A., Ghanam R.H., and Summers M.F. Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. Proc. Natl Acad. Sci. USA 103 (2006) 11364-11369
30. Saad J.S., Loeliger E., Luncsford P., Liriano M., Tai J., Kim A., et al. Point mutations in the HIV-1 matrix protein turn off the myristyl switch. J. Mol. Biol. 366 (2007) 574-585
31. Adamson C.S., and Freed E.O. Human immunodeficiency virus type 1 assembly, release and maturation. Adv. Pharmacol. 55 (2007) 347-387
32. Tang C., Loeliger E., Luncsford P., Kinde I., Beckett D., and Summers M.F. Entropic switch regulates myristate exposure in the HIV-1 matrix protein. Proc. Natl Acad. Sci. USA 101 (2004) 517-522
33. Zhou W., and Resh M.D. Differential membrane binding of the human immunodeficiency virus type 1 matrix protein. J. Virol. 70 (1996) 8540-8548
34. gag and p17MA. J. Virol. 73 (1999) 1902-1908
35. Paillart J.-C., and Gottlinger H.G. Opposing effects of human immunodeficiency virus type 1 matrix mutations support a myristyl switch model of Gag membrane targeting. J. Virol. 73 (1999) 2604-2612
36. Resh M.D. A myristoyl switch regulates membrane binding of HIV-1 Gag. Proc. Natl Acad. Sci. USA 101 (2004) 417-418
37. Ebbets-Reed D., Scarlata S., and Carter C.A. The major homology region of the HIV-1 Gag precursor influences membrane affinity. Biochemistry 35 (1996) 14268-14275
38. Liang C., Hu J., Russell R.S., Roldan A., Kleiman L., and Wainberg M.A. Characterization of a putative α-helix across the capsid-SP1 boundary that is critical for the multimerization of human immunodeficiency virus type 1 Gag. J. Virol. 76 (2002) 11729-11737
39. Accola M.A., Hoglund S., and Gottlinger H.G. A putative α-helical structure which overlaps the capsid-p2 boundary in the human immunodeficiency virus type-1 Gag precursor is crucial for viral particle assembly. J. Virol. 72 (1998) 2072-2078
40. Ono A., Demirov D., and Freed E.O. Relationship between human immunodeficiency virus type-1 Gag multimerization and membrane binding. J. Virol. 74 (2000) 5142-5150
41. 2 regulation of surface membrane traffic. Curr. Opin. Cell Biol. 13 (2001) 493-499
42. Behnia R., and Munro S. Organelle identity and the signposts for membrane traffic. Nature 438 (2005) 597-604
43. McLaughlin S., and Murray D. Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438 (2005) 605-611
44. Rao Z., Belyaev A.S., Fry E., Roy P., Jones I.M., and Stuart D.I. Crystal structure of SIV matrix antigen and implications for virus assembly. Nature 378 (1995) 743-747
45. Janmey P.A., IIda K., Yin H.L., and Stossel T.P. Phosphoinositide micelles and polyphosphoinositide-containing vesicles dissociate endogenous gelsolin-actin complexes and promote actin assembly from the fast-growing end of actin filaments blocked by gelsolin. J. Biol. Chem. 262 (1987) 12228-12236
46. Kutateladze T., and Overduin M. Structural mechanism of endosome docking by the FYVE domain. Science 291 (2001) 1793-1796
47. Kutateladze T. Phosphatidylinositol 3-phosphate recognition and membrane docking by the FYVE domain. Biochim. Biophys. Acta 1761 (2006) 868-877
48. Lee S.A., Kovacs J., Stahelin R.V., Cheever M.L., Overduin M., Setty T.G., et al. Molecular mechanism of membrane docking by the Vam7p PX domain. J. Biol. Chem. 281 (2006) 37091-37101
49. Wüthrich K. NMR of Proteins and Nucleic Acids (1986), John Wiley & Sons, New York, NY
50. Kay L.E., Clore G.M., Bax A., and Gronenborn A.M. Four-dimensional heteronuclear triple-resonance NMR spectroscopy of interleukin-1β in solution. Science 249 (1990) 411-414
51. Hill C.P., Worthylake D., Bancroft D.P., Christensen A.M., and Sundquist W.I. Crystal structures of the trimeric HIV-1 matrix protein: implications for membrane association. Proc. Natl Acad. Sci. USA 93 (1996) 3099-3104
52. Massiah M.A., Starich M.R., Paschall C., Summers M.F., Christensen A.M., and Sundquist W.I. Three-dimensional structure of the human immunodeficiency virus type 1 matrix protein. J. Mol. Biol. 244 (1994) 198-223
53. Kinnunen P.K.J., Koiv A., Lehtonen J.Y.A., Rytomaa M., and Mustonen P. Lipid dynamics and peripheral interactions of proteins with membrane surfaces. Chem. Phys. Lipids 73 (1994) 181-207
54. Rytomaa M., and Kinnunen P.K.J. Reversibility of the binding of cytochrome c to liposomes. J. Biol. Chem. 270 (1995) 3197-3202
55. Touminen E.K.J., Wallace C.J.A., and Kinnunen P.K.J. Phospholipid-cytochrome c interaction. J. Biol. Chem. 277 (2002) 8822-8826
56. Freed E.O., Orenstein J.M., Buckler-White A.J., and Martin M.A. Single amino acid changes in the human immunodeficiency virus type 1 matrix protein block virus particle production. J. Virol. 68 (1994) 5311-5320
57. Ono A., and Freed E.O. Binding of human immunodeficiency virus type 1 Gag to membrane: role of the matrix amino terminus. J. Virol. 73 (1999) 4136-4144
58. Ono A., Huang M., and Freed E.O. Characterization of human immunodeficiency virus type 1 matrix revertants: effects on virus assembly, Gag processing, and Env incorporation into virions. J. Virol. 71 (1997) 4409-4418
59. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6 (1995) 277-293
60. Johnson B.A., and Blevins R.A. NMRView: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4 (1994) 603-614
61. Folkers P.J.M., Folmer R.H.A., Konings R.N.H., and Hilbers C.W. Overcoming the ambiguity problem encountered in the analysis of nuclear Overhauser magnetic resonance spectra of symmetric dimer proteins. J. Am. Chem. Soc. 115 (1993) 3798-3799
62. Ishii Y., Markus M.A., and Tycko R. Controlling residual dipolar couplings in high-resolution NMR of proteins by strain induced alignment in a gel. J. Biomol. NMR 21 (2001) 141-151
63. Chou J.J., Gaemers S., Howder B., Louis J.M., and Bax A. A simple apparatus for generating stretched polyacrylamide gels, yielding uniform alignment of proteins and detergent micelles. J. Biomol. NMR 21 (2001) 377-382
64. Johnson M.L., and Faunt L.M. Parameter estimation by least-squares methods. Methods Enzymol. 210 (1992) 1-37
65. Adachi A., Gendelman H.E., Koenig S., Folks T., Willey R., Rabson A., and Martin M.A. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59 (1986) 284-291
66. Clavel F., Guyader M., Guetard D., Salle M., Montagnier L., and Alizon M. Molecular cloning and polymorphism of the human immune deficiency virus type 2. Nature 324 (1986) 691-695
67. Kisseleva M.V., Cao L., and Majerus P.W. Phosphoinositide-specific inositol polyphosphate 5-phosphatase IV inhibits Akt/protein kinase B phosphorylation and leads to apoptotic cell death. J. Biol. Chem. 277 (2002) 6266-6272
68. Brown F.D., Rozelle A.L., Yin H.L., Balla T., and Donaldson J.G. Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic. J. Cell Biol. 154 (2001) 1007-1017
69. Freed E.O., and Martin M.A. Evidence for a functional interaction between the V1/V2 and C4 domains of human immunodeficiency virus type 1 envelope glycoprotein gp120. J. Virol. 68 (1994) 2503-2512
70. Minassian A.A., Kalyanaraman V.S., Gallo R.C., and Popovic M. Monoclonal antibodies against human immunodeficiency virus (HIV) type 2 core proteins: cross-reactivity with HIV type 1 and simian immunodeficiency virus. Proc. Natl Acad. Sci. USA 85 (1988) 6939-6943
71. Gonda M.A., Aaronson S.A., Ellmore N., Zeve V.H., and Nagashima K. Ultrastructural studies of surface features of human normal and tumor cells in tissue culture by scanning transmission electron microscopy. J. Natl Cancer Inst. 56 (1976) 245-263