The structure of myristoylated mason-pfizer monkey virus matrix protein and the role of phosphatidylinositol-(4,5)-bisphosphate in its membrane binding

Journal of Molecular Biology

Volumn 423, Issue 3, 2012, Pages 427-438

  Prchal, Jan ^a   Srb, Pavel ^b   Hunter, Eric ^c   Ruml, Tomáš ^a   Hrabal, Richard ^a  

^a INSTITUTE OF CHEMICAL TECHNOLOGY   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c EMORY UNIVERSITY   (United States)

Author keywords

M PMV; myristoylated; phosphatidylinositol; protein structure; retrovirus

Indexed keywords

AMINO ACID; FATTY ACID; MATRIX PROTEIN; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL (4,5) BISPHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; HETERONUCLEAR SINGLE QUANTUM COHERENCE; MASON PFIZER MONKEY VIRUS; MEMBRANE BINDING; MYRISTYLATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE;

MASON-PFIZER MONKEY VIRUS; PAPAYA MOSAIC VIRUS;

EID: 84867071581     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.07.021     Document Type: Article

References (44)

1. J.N. Sfakianos, R.A. LaCasse, and E. Hunter The M-PMV cytoplasmic targeting-retention signal directs nascent Gag polypeptides to a pericentriolar region of the cell Traffic 4 2003 660 670
2. D. Gheysen, E. Jacobs, F. Deforesta, C. Thiriart, M. Francotte, D. Thines, and M. Dewilde Assembly and release of HIV-1 precursor Pr55Gag virus-like particles from recombinant baculovirus-infected insect cells Cell 59 1989 103 112
3. E.O. Freed Viral late domains J. Virol. 76 2002 4679 4687
4. W. Zhou, L.J. Parent, J.W. Wills, and M.D. Resh 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
5. L. Hermida-Matsumoto, and M.D. Resh Human immunodeficiency virus type 1 protease triggers a myristoyl switch that modulates membrane binding of Pr55(gag) and p17MA J. Virol. 73 1999 1902 1908
6. P. Spearman, R. Horton, L. Ratner, and I. Kuli-Zade Membrane binding of human immunodeficiency virus type 1 matrix protein in vivo supports a conformational myristyl switch mechanism J. Virol. 71 1997 6582 6592
7. W. Zhou, and M.D. Resh Differential membrane binding of the human immunodeficiency virus type 1 matrix protein J. Virol. 70 1996 8540 8548
8. F. Bouamr, S. Scarlata, and C. Carter Role of myristylation in HIV-1 Gag assembly Biochemistry 42 2003 6408 6417
9. J.B. Ames, R. Ishima, T. Tanaka, J.I. Gordon, L. Stryer, and M. Ikura Molecular mechanics of calcium-myristoyl switches Nature 389 1997 198 202
10. B. Nagar, O. Hantschel, M.A. Young, K. Scheffzec, D. Veach, and W. Bornmann Structural basis for the autoinhibition of c-Abl tyrosine kinase Cell 112 2003 859 871
11. C. Tang, E. Loeliger, P. Luncsford, I. Kinde, D. Beckett, and M.F. Summers Entropic switch regulates myristate exposure in the HIV-1 matrix protein Proc. Natl Acad. Sci. USA 101 2004 517 522
12. J.S. Saad, J. Miller, J. Tai, A. Kim, R.H. Ghanam, and M.F. Summers Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly Proc. Natl Acad. Sci. USA 103 2006 11364 11369
13. J.S. Saad, S.D. Ablan, R.H. Ghanam, A. Kim, K. Andrews, and K. Nagashima 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 2008 434 447
14. J.W. Wills, and R.C. Craven Form, function, and use of retroviral gag proteins AIDS 5 1991 639 654
15. R.H. Ghanam, T.F. Fernandez, E.L. Fledderman, and J.S. Saad Binding of calmodulin to the HIV-1 matrix protein triggers myristate exposure J. Biol. Chem. 285 2010 41911 41920
16. K. Chen, I. Bachtair, G. Piszczek, F. Bouamr, C. Carter, and N. Tjandra Solution NMR characterizations of oligomerization and dynamics of equine infectious anemia virus matrix protein and its interaction with PIP2 Biochemistry 47 2008 1928 1937
17. 2/PS and a polybasic region in the matrix J. Virol. 84 2010 503 515
18. E. Stansell, R. Apkarian, S. Haubova, W.E. Diehl, E.M. Tytler, and E. Hunter Basic residues in the Mason-Pfizer monkey virus gag matrix domain regulate intracellular trafficking and capsid-membrane interactions J. Virol. 81 2007 8977 8988
19. S.S. Rhee, and E. Hunter Amino acid substitutions within the matrix protein of type D retroviruses affect assembly, transport and membrane association of a capsid EMBO J. 10 1991 535 546
20. E. Stansell, E. Tytler, M.R. Walter, and E. Hunter An early stage of Mason-Pfizer monkey virus budding is regulated by the hydrophobicity of the Gag matrix domain core J. Virol. 78 2004 5023 5031
21. J. Vlach, P. Srb, J. Prchal, M. Grocky, J. Lang, T. Ruml, and R. Hrabal Nonmyristoylated matrix protein from the Mason-Pfizer monkey virus forms oligomers J. Mol. Biol. 390 2009 967 980
22. P. Srb, J. Vlach, J. Prchal, M. Grocky, T. Ruml, J. Lang, and R. Hrabal Oligomerization of a retroviral matrix protein is facilitated by backbone flexibility on nanosecond time scale J. Phys. Chem. B 115 2011 2634 2644
23. J. Prchal, P. Junkova, M. Strmiskova, J. Lipov, R. Hynek, T. Ruml, and R. Hrabal Expression and purification of myristoylated matrix protein of Mason-Pfizer monkey virus for NMR and MS measurements Protein Expression Purif. 79 2011 122 127
24. Y. Shen, F. Delaglio, G. Cornilescu, and A. Bax TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts J. Biomol. NMR 44 2009 213 223
25. A.L. Breeze Isotope-filtered NMR methods for the study of biomolecular structure and interactions Prog. Nucl. Magn. Reson. Spectrosc. 36 2000 323 372
26. J. Vlach, J. Lipov, M. Rumlova, V. Veverka, J. Lang, and P. Srb D-retrovirus morphogenetic switch driven by the targeting signal accessibility to Tctex-1 of dynein Proc. Natl Acad. Sci. USA 105 2008 10565 10570
27. P.S. Murray, Z. Li, J. Wang, C.L. Tang, B. Honig, and D. Murray Retroviral matrix domains share electrostatic homology: models for membrane binding function throughout the viral life cycle Structure 13 2005 1521 1531
28. J. Yasuda, and E. Hunter Role of matrix protein in the type D retrovirus replication cycle: importance of the arginine residue at position 55 Virology 268 2000 533 538
29. M.J. Forster, B. Mulloy, and M.V. Nermut Molecular modellingstudy of HIV p17gag (MA) protein shell utilising data from electron microscopy and X-ray crystallography J. Mol. Biol. 298 2000 841 857
30. A. Alfadhli, D. Huseby, E. Kapit, D. Colman, and E. Barklis Human immunodeficiency virus type 1 matrix protein assembles on membranes as a hexamer J. Virol. 81 2007 1472 1478
31. J.N. Sfakianos, and E. Hunter M-PMV capsid transport is mediated by Env/Gag interactions at the pericentriolar recycling endosome Traffic 4 2003 671 680
32. F. Delaglio, S. Grzesiek, G.W. Vuister, and G. Zhu NMRPipe: a multidimensional spectra processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
33. T.D. Goddard, and D.G. Kneller Sparky 3 2006 University of California San Francisco, CA
34. W.F. Vranken, W. Boucher, T.J. Stevens, R.H. Fogh, A. Pajon, and P. Llinas The CCPN data model for NMR spectroscopy: development of a software pipeline Proteins: Struct., Funct., Bioinformatics 59 2005 687 696
35. C.D. Schwieters, J.J. Kuszewsky, Tjandra, and G.M. Clore The Xplor-NIH NMR molecular structure determination package J. Magn. Reson. 160 2003 66 74
36. A.W. Schuttelkopf, and D.M.F. van Aalten PRODRG: a tool for high-throughput crystallography of protein-ligand complexes Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 2004 1355 1363
37. G.J. Kleywegt, and M.R. Harris ValLigURL: a server for ligand-structure comparison and validation Acta Crystallogr., Sect. D: Biol. Crystallogr. 63 2007 935 938
38. W.L. DeLano The PyMOL Molecular Graphics System 2002 DeLano Scientific San Carlos, CA
39. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graphics 14 1996 33 38
40. J.F. Doreleijers, W.F. Vranken, C. Schulte, J.L. Markley, E.L. Ulrich, G. Vriend, and G.W. Vuister NRG-CING: integrated validation reports of remediated experimental biomolecular NMR data and coordinates in wwPDB Nucleic Acids Res. 40 2012 D519 D524
41. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
42. The Mathworks (2007). MATLAB.
43. L. Fielding NMR methods for the determination of protein-ligand dissociation constants Prog. Nucl. Magn. Reson. Spectrosc. 51 2007 219 242
44. S.J. De Vries, A.D.J. van Dijk, M. Krzeminski, M. van Dijk, A. Thureau, and V. Hsu HADDOCK versus HADDOCK: new features and performance of HADDOCK2.0 on the CAPRI targets Proteins: Struct., Funct., Bioinformatics 69 2007 726 733