Refined solution structure and backbone dynamics of HIV-1 Nef

Protein Science

Volumn 6, Issue 6, 1997, Pages 1248-1263

  Grzesiek, Stephan ^a,c   Bax, A D ^a   Hu, Jin Shan ^a   Kaufman, Joshua ^b   Palmer, Ira ^b   Stahl, Stephen J ^b   Tjandra, Nico ^a   Wingfield, Paul T ^b  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

Heteronuclear NMR; HIV 1; Multi dimensional NMR; Nef; Protein dynamics; Protein structure

Indexed keywords

NEF PROTEIN; VIRUS PROTEIN;

ARTICLE; DELETION MUTANT; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 0030980288     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1002/pro.5560060613     Document Type: Article

References (90)

1. Adzubei AA, Sternberg MJE. 1993. Left-handed polyproline II helices commonly occur in globular proteins. J Mol Biol 229:472-493.
2. Ahmad N, Venkatesan S. 1988. Nef protein of HIV-1 is a transcriptional repressor of HIV-1 LTR. Science 241:1481-1485.
3. Aiken C, Konner J, Landau NR, Lenburg ME, Trono D. 1994. Nef induces CD4 endocytosis: Requirement for a critical di-leucine motif in the membrane-proximal CD4 cytoplasmic domain. Cell 76:853-864.
4. Aiken C, Krause L, Chen YL, Trono D. 1996. Mutational analysis of HIV-1 Nef: Identification of two mutants that are temperature-sensitive for CD4 down-regulation. Virology 217:293-300.
5. Anderson SJ, Lenburg M, Landau NR, Garcia JV. 1994. The cytoplasmic domain of CD4 is sufficient for its down-regulation from the cell surface by human immunodeficiency virus type 1 Nef. J Virol 68:3092-3101.
6. 15N nuclear magnetic resonance backbone assignments and secondary structure of human calcineurin B. Biochemistry 33:3540-3547.
7. Bai Y, Milne JS, Mayne L, Englander SW. 1993. Primary structure effects on peptide group hydrogen exchange. Proteins Struct Funct Genet 17:75-86.
8. 13C-labeled proteins. J Magn Reson 87:620-627.
9. 13C-enriched proteins. J Magn Reson 88:425-431.
10. Bax A, Grzesiek S, Gronenborn AM, Clore GM. 1994. Isotope-filtered 2D HOHAHA spectroscopy of a peptide-protein complex using heteronuclear Hartmann-Hahn dephasing. J Magn Reson Ser A 106:269-273.
11. Benson RE, Sanfridson A, Ottinger JS, Doyle C, Cullen BR. 1993. Downregulation of cell-surface CD4 expression by simian immunodeficiency virus Nef prevents viral super infection. J Exp Med 177:1561-1566.
12. Bothner-By AA, Stephens RL, Lee J, Warren CD, Jeanloz RW. 1984. Structure determination of a Tetrasaccharide: Transient nuclear overhauser effects in the rotating frame. J Am Chem Soc 106:811-813.
13. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, Karplus M. 1983. CHARMM: A program for macromolecular energy minimization and dynamics calculations. J Comput Chem 4:187-217.
14. Brünger AT. 1992. X-PLOR Version 3.1: A system for crystallography and NMR. New Haven, Connecticut: Yale University.
15. Cheng-Mayer C, Iannello P, Shaw K, Luciw PA, Levy JA. 1989. Differential effects of nef on HIV replication: Implications for viral pathogenesis in the host. Science 246:1629-1632.
16. Chowers MY, Spina CA, Kwoh TJ, Fitch NJ, Richman DD, Guatelli JC. 1994. Optimal infectivity in vitro of human immunodeficiency virus type 1 requires an intact nef gene. Virology 68:2906-2914.
17. Chowers MY, Pandori MW, Spina CA, Richman DD, Guatelli JC. 1995. The growth advantage conferred by HIV-1 nef is determined at the level of viral DNA formation and is independent of CD4 downregulation. Virology 212:451-457.
18. Cullen BR. 1994. The role of Nef in the replication cycle of the human and simian immunodeficiency viruses. Virology 205:1-6.
19. Daniel MD, Kirchhoff F, Czajak SC, Sehgal PK, Desrosiers RC. 1992. Protective effects of a live attenuated SIV vaccine with a deletion in the nef gene. Science 258:1938-1941.
20. Deacon NJ, Tsykin A, Solomon A, Smith K, Ludford-Menting M, Hooker DJ, McPhee DA, Greenway AL, Ellett A, Chatfield C, Lawson VA, Crowe S, Maerz A, Sonza S, Learmont J, Sullivan JS, Cunnningham A, Dwyer D, Dowton D, Mills J. 1995. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science 270:988-991.
21. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A. 1995. NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6:277-293.
22. deRonde A, Klaver B, Keulen W, Smit L, Goudsmit J. 1992. Natural HIV-1 Nef accelerates virus replication in primary human lymphocytes. Virology 188:391-395.
23. Foster JL, Anderson SJ, Frazier AL, Garcia JV. 1994. Specific suppression of human CD4 surface expression by Nef from the pathogenic simian immunodeficiency virus SIVmac239open. Virology 201:373-379.
24. Freund J, Kellner R, Houthaeve T, Kalbitzer HR. 1994a. Stability and proteolytic domains of Nef protein from human immunodeficiency virus (HIV) type 1. Eur J Biochem 221:811-819.
25. Freund J, Kellner R, Konvalinka J, Wolber V, Krausslich HG, Kalbitzer HR. 1994b. A possible regulation of negative factor (Nef) activity of human immunodeficiency virus type 1 by the viral protease. Eur J Biochem 223:589-593.
26. Garcia JV, Miller AD. 1991. Serine phosphorylation-independent downregulation of cell-surface CD4 by nef. Nature 350:508-511.
27. Garcia JV, Alfano J, Miller AD. 1993. The negative effect of human immunodeficiency virus type 1 Nef on cell surface CD4 expression is not species specific and requires the cytoplasmic domain of CD4. J Virol 67:1511-1516.
28. Garrett DS, Powers R, Gronenborn AM, Clore GM. 1991. A common sense approach to peak picking in two-, three-, and four-dimensional spectra using automatic computer analysis of contour diagrams. J Magn Reson 95:214-220.
29. Garrett DS, Kuszewski J, Hancock, TJ, Lodi PJ, Vuister GW, Gronenborn AM, Clore GM. 1994. The impact of direct refinement against three-bond HN-CaH coupling constants on protein structure determination by NMR. J Magn Reson B104:99-103.
30. Goldsmith MA, Warmerdam MT, Atchison RE, Miller MD, Greene WC. 1995. Dissociation of the CD4 downregulation and viral infectivity enhancement functions of human immunodeficiency virus type 1 Nef. J Virol 69:4112-4121.
31. 13C chemical shifts. J Biomol NMR 4:455-458.
32. Grzesiek S, Bax A. 1992a. Improved 3D triple-resonance NMR techniques applied to a 31 kDa protein. J Magn Reson 96:432-440.
33. Grzesiek S, Bax A. 1992b. Correlating backbone amide and side chain resonances in larger proteins by multiple relayed triple resonance NMR. J Am Chem Soc 114:6291-6293.
34. 15N-enriched proteins. J Biomol NMR 3:185-204.
35. Grzesiek S, Bax A. 1993b. The importance of not saturating water in protein NMR. Application to sensitivity enhancement and NOE measurements. J Am Chem Soc 115:12593-12594.
36. Grzesiek S, Vuister GW, Bax A. 1993. A simple and sensitive experiment for measurement of JCC couplings between backbone carbonyl and methyl carbons in isotopically enriched proteins. J Biomol NMR 3:487-493.
37. 15N-enriched proteins. Application to HIV-1 Nef. J Am Chem Soc 117:9594-9595.
38. Grzesiek S, Kuboniwa H, Hinck AP, Bax A. 1995b. Multiple-quantum line narrowing for measurement of Hα-Hβ J couplings in isotopically enriched proteins. J Am Chem Soc 117:5312-5315.
39. Grzesiek S, Bax A, Clore GM, Gronenborn AM, Hu JS, Kaufman J, Palmer I, Stahl SJ, Wingfield PT. 1996a. The solution structure of HIV-1 Nef reveals an unexpected fold and permits delineation of the binding surface for the SH3 domain of Hck tyrosine protein kinase. Nat Struct Biol 3:340-345.
40. Grzesiek S, Stahl SJ, Wingfield PT, Bax A. 1996b. The CD4 determinant for downregulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR. Biochemistry 35:10256-10261.
41. Grzesiek S, Bax A. 1997. A three-dimensional NMR experiment with improved sensitivity for carbonyl-carbonyl J correlations in proteins. J Biomol NMR 9:207-211.
42. Guy B, Kieny MP, Riviere Y, Le Peuch C, Dott K, Girard M, Montagnier L, Lecocq JP. 1987. HIV F/3′ orf encodes a phosphorylated GTP-binding protein resembling an oncogene product. Nature 330:266-269.
43. Harper ET, Rose GD. 1993. Helix stop signals in proteins and peptides: The capping box. Biochemistry 32:7605-7609.
44. Hiroaki H, Klaus W, Senn H. 1996. Determination of the solution structure of the SH3 domain of human p56 Lck tyrosine kinase. J Biomol NMR 8:105-122.
45. 13C J couplings between carbonyl/carboxyl carbons in isotopically enriched proteins. J Am Chem Soc 118:8170-8171.
46. NCγ couplings. J Am Chem Soc 119:1803-1804.
47. 13C-labeled protein. J Magn Reson 56:204-209.
48. 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease. Biochemistry 28:8972-8979.
49. 2 values in proteins: Pulse sequences for the removal of such effects. J Magn Reson 97:359-375.
50. 2O saturation. J Magn Reson A109:129-133.
51. Kestler HW, Ringler DJ, Mori K, Panicali DL, Sehgal PK, Daniel MD, Desrosiers RC. 1991. Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 65:651-662.
52. Kirchhoff F, Greenough TC, Brettler DB, Sullivan JL, Desrosiers RC. 1995. Absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection. N Engl J Med 332:228-232.
53. Koradi R, Billeter M, Wüthrich K. 1996. MOLMOL: A program for display and analysis of macromolecular structures. J Mol Graphics 14:51-55.
54. Kuboniwa H, Grzesiek S, Delaglio F, Bax A. 1994. Measurement of HN-H alpha J couplings in calcium-free calmodulin using new 2D and 3D water-flip-back methods. J Biomol NMR 4:871-878.
55. Kuboniwa H, Tjandra N, Grzesiek S, Ren H, Klee CB, Bax A. 1995. Solution structure of calcium-free calmodulin. Nat Struct Biol 2:768-776.
56. 13Cβ chemical shifts on protein structure determination by NMR. J Magn Reson B106:92-96.
57. Laskowski R, Rullmann JAC, MacArthur MW, Kaptein R, Thornton JM. 1996. AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8:477-486.
58. Lee CH, Leung B, Lemmon MA, Zheng J, Cowbum D, Kuriyan J, Saksela K. 1995. A single amino acid in the SH3 domain of Hck determines its high affinity and specificity in binding to HIV-1 Nef protein. EMBO J 14:5006-5015.
59. Lee CH, Saksela K, Mirza UA, Chait BT, Kuriyan J. 1996. Crystal structure of the conserved core of HIV-1 Nef complexed with a Src family SH3 domain. Cell 85:931-942.
60. Lipari G, Szabo A. 1982a. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J Am Chem Soc 104:4546-4559.
61. Lipari G, Szabo A. 1982b. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Analysis of experimental results. J Am Chem Soc 104:4559-4570.
62. Lippens G, Dhalluin C, Wieruszeski JM. 1995. Use of a water flip-back pulse in the homonuclear NOESY experiment. J Biomol NMR 5:327-331.
63. Luciw PA, Cheng-Mayer C, Levy JA. 1987. Mutational analysis of the human immunodeficiency virus: The orf-B region down-regulates virus replication. Proc Natl Acad Sci USA 84:1434-1438.
64. Mariani R, Kirchhoff F, Greenough TC, Sullivan JL, Desrosiers RC, Skowronski J. 1996. High frequency of defective nef alleles in a long-term survivor with nonprogressive human immunodeficiency virus type 1 infection. J Virol 70:7752-7764.
65. 15N Hartmann-Hahn-multiple quantum coherence and nuclear Overhauser-multiple quantum coherence spectroscopy: Application to interleukin 1-β. Biochemistry 28.6150-6156.
66. Miller MD, Warmerdam MT, Gaston I, Greene WC, Feinberg MB. 1994. The human immunodeficiency virus-1 nef gene product: A positive factor for viral infection and replication in primary lymphocytes and macrophages. J Exp Med 179:101-113.
67. Neri D, Szyperski T, Otting G, Senn H, Wuethrich K. 1989. Stereospecific nuclear magnetic resonance assignments of the methyl groups of valine and leucine in the DNA-binding domain of the 434 repressor by biosynthetically directed fractional carbon-13 labeling. Biochemistry 28:7510-7516.
68. Nicholson LK, Yamazaki T, Torchia DA, Grzesiek S, Bax A, Stahl SJ, Kaufman JD, Wingfield PT, Lam PY, Jadhav PK. 1995. Flexibility and function in HIV-1 protease. Nat Struct Biol 2:274-280.
69. Niederman TM, Thielan BJ, Ratner L. 1989. Human immunodeficiency virus type 1 negative factor is a transcriptional silencer. Proc Natl Acad Sci USA 86:1128-1132.
70. Nilges M, Clore GM, Gronenborn AM. 1988. Determination of three-dimensional structures of proteins from interproton distance data by hybrid distance geometry-dynamical simulated annealing calculations. FEBS Lett 229:317-324.
71. Piotto M, Saudek V, Sklenar V. 1992. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J Biomol NMR 2:661-665.
72. Prekumar DRD, Ma XZ, Maitra RK, Chakrabarti BK, Salkowitz J, Yen-Lieberman B, Hirsch MS, Kestler HW. 1996. The nef gene from a long-term HIV type 1 nonprogressor. AIDS Res Hum Retroviruses 12:337-345.
73. Saksela K, Cheng G, Baltimore D. 1995. Proline-rich (PxxP) motifs in HIV-1 Nef bind to SH3 domains of a subset of Src kinases and are required for the enhanced growth of Nef+ viruses but not for down-regulation of CD4. EMBO J 14:484-491.
74. Salghetti S, Mariani R, Skowronski J. 1995. Human immunodeficiency virus type 1 Nef and p56lck protein-tyrosine kinase interact with a common element in CD4 cytoplasmic tail. Proc Natl Acad Sci USA 92:349-353.
75. Santoro J, King GC. 1992. A constant-time 2D overbodenhausen experiment for inverse correlation of isotopically enriched species. J Magn Reson 97:202-207.
76. Shugars DC, Smith MS, Glueck DH, Nantermet PV, Seillier-Moiseiwitsch F, Swanstrom R. 1993. Analysis of human immunodeficiency virus type 1 nef gene sequences present in vivo. J Virol 67:4639-4650.
77. Skowronski J, Parks D, Mariani R. 1993. Altered T cell activation and development in transgenic mice expressing the HIV-1 nef gene. EMBO J 12:703-713.
78. 13C nuclear magnetic resonance chemical shifts. J Am Chem Soc 113:5490-5492.
79. Spina CA, Kwoh TJ, Chowers MY, Guatelli JC, Richman DD. 1994. The importance of nef in the induction of human immunodeficiency virus type 1 replication from primary quiescent CD4 lymphocytes. J Exp Med 179:115-123.
80. Van de Ven FJM, Philippens MEP. 1992. Optimization of constant-time evolution in multidimensional experiments. J Magn Reson 97:637-644.
81. 13-enriched proteins by homonuclear broadband carbon-13 decoupling. J Magn Reson 98:428-435.
82. Vuister GW, Wang AC, Bax A. 1993. Measurement of three-bond nitrogen-carbon J couplings in proteins uniformly enriched in nitrogen-15 and carbon-13. J Am Chem Soc 115:5334-5335.
83. Vuister GW, Kim SJ, Wu C, Bax A. 1994. 2D and 3D NMR study of phenylalanine residues in proteins by reverse isotopic labeling. J Am Chem Soc 166:9206-9210.
84. Welker R, Kottler H, Kalbitzer HR, Kräusslich HG. 1996. Human immunodeficiency virus type 1 Nef protein is incorporated into virus particles and specifically cleaved by the viral proteinase. Virology 219:228-236.
85. Wilmot CM, Thomton JM 1988. Analysis and prediction of the different types of b-turn in proteins. J Mol Biol 203:221-232.
86. Wishart DS, Sykes BD, Richards FM. 1991. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J Mol Biol 222:311-333.
87. Wittekind M, Mueller L. 1993. HNCACB a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha-and beta-carbon resonances in proteins. J Magn Reson B101:201-205.
88. Whatmore AM, Cook N, Hall GA, Sharpe S, Rud EW, Cranage MP. 1995. Repair and evolution of nef in vivo modulates simian immunodeficiency virus virulence. J Virol 69:5117-5123.
89. Wüthrich K. 1986. NMR of proteins and nucleic acids. New York: John Wiley & Sons.
90. 13C-labeled proteins for the NMR assignment and structure determination of larger molecules. J Magn Reson 86:210-216.