High yield expression and purification of HIV-1 Tat1-72 for structural studies

Journal of Virological Methods

Volumn 164, Issue 1-2, 2010, Pages 35-42

  Shojania, Shaheen ^a   Henry, Gillian D ^a   Chen, Vincent C ^a   Vo, Thach N ^a   Perreault, Hélène ^a   O'Neil, Joe D ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Cysteine rich; HIV; Intrinsically disordered protein; NMR spectroscopy; Tat; Transcriptional regulator

Indexed keywords

TRANSACTIVATOR PROTEIN;

AFFINITY CHROMATOGRAPHY; ARTICLE; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATION; PHYSICAL CHEMISTRY; PLASMID; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; TRANSACTIVATION; TRANSCRIPTION REGULATION; VISCOSITY;

HIV-1; HUMANS; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; RECOMBINANT FUSION PROTEINS; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

BACTERIA (MICROORGANISMS); HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 77249169687     PISSN: 01660934     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jviromet.2009.11.021     Document Type: Article

References (62)

1. Albini A., Benelli R., Presta M., Rusnati M., Ziche M., Rubartelli A., Paglialunga G., Bussolino F., and Noonan D. HIV-Tat protein is a heparin-binding angiogenic growth factor. Oncogene 12 January(2) (1996) 289-297
2. Albini A., Soldi R., Giunciuglio D., Giraudo E., Benelli R., Primo L., Noonan D., Salio M., Camussi G., Rockl W., and Bussolino F. The angiogenesis induced by HIV-1 Tat protein is mediated by the flk-1/kdr receptor on vascular endothelial cells. Nature Medicine 2 December(12) (1996) 1371-1375
3. Anand K., Schulte A., Vogel-Bachmayr K., Scheffzek K., and Geyer M. Structural insights into the cyclin T1-Tat-TAR RNA transcription activation complex from EIAV. Nat. Struct. Mol. Biol. 15 12 (2008) 1287-1292
4. Avraham H.K., Jiang S., Lee T.H., Prakash O., and Avraham S. HIV-1 Tat-mediated effects on focal adhesion assembly and permeability in brain microvascular endothelial cells. Journal of Immunology 173 November(10) (2004) 6228-6233
5. Bannwarth S., and Gatignol A. HIV-1 Tat RNA: the target of molecular interactions between the virus and its host. Current HIV Research 3 January(1) (2005) 61-71
6. Bourgeois C.F., Kim Y.K., Churcher M.J., West M.J., and Karn J. Spt5 cooperates with human immunodeficiency virus type 1 Tat by preventing premature RNA release at terminator sequences. Molecular and Cellular Biology 22 February(4) (2002) 1079-1093
7. Cavanagh J., Fairbrother W.J., Palmer A.G., and Skelton N.J. Protein NMR Spectroscopy: Principles and Practice (1996), Academic Press, San Diego
8. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. Nmrpipe: a multidimensional spectral processing system based on unix pipes. Journal of Biomolecular NMR 6 November(3) (1995) 277-293
9. Derse D., Carvalho M., Carroll R., and Peterlin B.M. A minimal lentivirus Tat. Journal of Virology 65 December(12) (1991) 7012-7015
10. Dingwall C., Ernberg I., Gait M.J., Green S.M., Heaphy S., Karn J., Lowe A.D., Singh M., and Skinner M.A. HIV-1 Tat protein stimulates transcription by binding to a u-rich bulge in the stem of the TAR RNA structure. EMBO Journal 9 December(12) (1990) 4145-4153
11. Dyson H.J., and Wright P.E. Equilibrium NMR studies of unfolded and partially folded proteins. Nature Structural Biology 5 July (1998) 499-503
12. Dyer M.D., Murali T.M., and Sobral B.W. The landscape of human proteins interacting with viruses and other pathogens. PLoS Pathog 4 2 (2008) e32
13. Edwards A.M., Arrowsmith C.H., Christendat D., Dharamsi A., Friesen J.D., Greenblatt J.F., and Vedadi M. Protein production: feeding the crystallographers and NMR spectroscopists. Nature Structural Biology 7 (2000) 970-972
14. Ensoli B., Barillari G., Salahuddin S.Z., Gallo R.C., and Wong-Staal F. Tat protein of HIV-1 stimulates growth of cells derived from Kaposi's sarcoma lesions of aids patients. Nature 345 May(6270) (1990) 84-86
15. Eriksson M.A., Härd T., and Nilsson L. On the pH dependence of amide proton exchange rates in proteins. Biophysical Journal 69 August(2) (1995) 329-339
16. 15N NMR relaxation. Biochemistry 33 May(19) (1994) 5984-6003
17. Frankel A.D., and Pabo C.O. Cellular uptake of the Tat protein from human immunodeficiency virus. Cell 55 December(6) (1988) 1189-1193
18. Garcia J.A., Harrich D., Pearson L., Mitsuyasu R., and Gaynor R.B. Functional domains required for Tat-induced transcriptional activation of the HIV-1 long terminal repeat. EMBO Journal 7 October(10) (1988) 3143-3147
19. Gill S.C., and von Hippel P.H. Calculation of protein extinction coefficients from amino acid sequence data. Analytical Biochemistry 182 November(2) (1989) 319-326
20. Goldstein G. HIV-1 Tat protein as a potential aids vaccine. Nature Medicine 2 September(9) (1996) 960-964
21. Gough J.D.R.H., Donofrio J.W., and Lees A.E.W.J. Folding disulfide-containing proteins faster with an aromatic thiol. Journal of the American Chemical Society 124 April(15) (2002) 3885-3892
22. Guo X., Kameoka M., Wei X., Roques B., Gotte M., Liang C., and Wainberg M.A. Suppression of an intrinsic strand transfer activity of HIV-1 Tat protein by its second-exon sequences. Virology 307 March(1) (2003) 154-163
23. Hakansson S., and Caffrey M. Structural and dynamic properties of the HIV-1 Tat transduction domain in the free and heparin-bound states. Biochemistry 42 August(30) (2003) 8999-9006
24. Hakansson S., Jacobs A., and Caffrey M. Heparin binding by the HIV-1 Tat protein transduction domain. Protein Science 10 10 (2001) 2138-2139
25. Han J.C., and Han G.Y. A procedure for quantitative determination of tris(2-carboxyethyl)phosphine, an odorless reducing agent more stable and effective than dithiothreitol. Analytical Biochemistry 220 July(1) (1994) 5-10
26. Harris J.L., Backes B.J., Leonetti F., Mahrus S., Ellman J.A., and Craik C.S. Rapid and general profiling of protease specificity by using combinatorial fluorogenic substrate libraries. Proceedings of the National Academy of Sciences of U.S.A. 97 July(14) (2000) 7754-7759
27. Hasan A.A.K., Amenta S., and Schmaier A.H. Bradykinin and its metabolite, arg-pro-pro-gly-phe, are selective inhibitors of α-thrombininduced platelet activation. Circulation 94 3 (1996) 517-528
28. Jeang K.-T. HIV-1 Tat: structure and function. In: Myers G., Korber B.T., Foley B.T., Jeang K.-T., Mellors J.W., and Wain-Hobson S. (Eds). Human Retroviruses and AIDS 1996: A Compilation and Analysis of Nucleic Acid and Amino Acid Sequences (1996), Los Alamos National Laboratories, Los Alamos 11-26 (Chapter III)
29. Jeang K.-T., Xiao H., and Rich E.A. Multifaceted activities of the HIV-1 transactivator of transcription, Tat. Journal of Biological Chemistry 274 October(41) (1999) 28837-28840
30. Kay L.E., Keifer P., and Saarinen T. Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. Journal of the American Chemical Society 114 December(26) (1992) 10663-10665
31. Kim Y.K., Bourgeois C.F., Isel C., Churcher M.J., and Karn J. Phosphorylation of the RNA polymerase ii carboxyl-terminal domain by cdk9 is directly responsible for human immunodeficiency virus type 1 Tat-activated transcriptional elongation. Molecular and Cellular Biology 22 July(13) (2002) 4622-4637
32. Kuppuswamy M., Subramanian T., Srinivasan A., and Chinnadurai G. Multiple functional domains of Tat, the trans-activator of HIV-1, defined by mutational analysis. Nucleic Acids Research 17 May(9) (1989) 3551-3561
33. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 5259 (1970) 680-685
34. Lassen K., Han Y., Zhou Y., Siliciano J., and Siliciano R.F. The multifactorial nature of HIV-1 latency. Trends in Molecular Medicine 10 November(11) (2004) 525-531
35. Liang C., and Wainberg M.A. The role of Tat in HIV-1 replication: an activator and/or a suppressor?. AIDS Reviews 4 January-March(1) (2002) 41-49
36. Magnuson D.S.K., Knudsen B.E., Geiger J.D., Brownstone R.M., and Nath A. Human immunodeficiency virus type 1 Tat activates non-N-methyl-d-aspartate excitatory amino acid receptors and causes neurotoxicity. Annals of Neurology 37 3 (1995) 373-380
37. Marley J., Lu M., and Bracken C. A method for efficient isotopic labeling of recombinant proteins. Journal of Biomolecular NMR 20 May(1) (2001) 71-75
38. Mujtaba S., He Y., Zeng L., Farooq A., Carlson J.E., Ott M., Verdin E., and Zhou M.M. Structural basis of lysine-acetylated HIV-1 Tat recognition by pcaf bromodomain. Molecular and Cellular Biology 9 March(3) (2002) 575-586
39. Nath A., Psooy K., Martin C., Knudsen B., Magnuson D.S., Haughey N., and Geiger J.D. Identification of a human immunodeficiency virus type 1 Tat epitope that is neuroexcitatory and neurotoxic. Journal of Virology 70 March(3) (1996) 1475-1480
40. Neidhardt F.C., Bloch P.L., and Smith D.F. Culture medium for enterobacteria. Journal of Bacteriology 119 September(3) (1974) 736-747
41. Neuveut C., and Jeang K.T. Recombinant human immunodeficiency virus type 1 genomes with Tat unconstrained by overlapping reading frames reveal residues in Tat important for replication in tissue culture. Journal of Virology 70 August(8) (1996) 5572-5581
42. Opi S., Péloponèse J.-M., Esquieu D., Watkins J., Campbell G., De Mareuil J., Jeang K.T., Yirrell D.L., Kaleebu P., and Loret E.P. Full-length HIV-1 Tat protein necessary for a vaccine. Vaccine 22 August(23-24) (2004) 3105-3111
43. Peti W., Smith L.J., Redfield C., and Schwalbe H. Chemical shifts in denatured proteins: resonance assignments for denatured ubiquitin and comparisons with other denatured proteins. Journal of Biomolecular NMR 19 February(2) (2001) 153-165
44. Pocernich C.B., Sultana R., Mohmmad-Abdul H., Nath A., and Butterfield D.A. HIV-dementia, Tat-induced oxidative stress, and antioxidant therapeutic considerations. Brain Research Reviews 50 December(1) (2005) 14-26
45. Pumfery A., Deng L., Maddukuri A., de la Fuente C., Li H., Wade J.D., Lambert P., Kumar A., and Kashanchi F. Chromatin remodeling and modification during HIV-1 Tat-activated transcription. Current HIV Research 1 July(3) (2003) 343-362
46. Schulte A., Czudnochowski N., Barboric M., Schonichen A., Blazek D., Peterlin B.M., and Geyer M. Identification of a cyclin T-binding domain in hexim1 and biochemical analysis of its binding competition with HIV-1 Tat. Journal of Biological Chemistry 280 July(26) (2005) 24968-24977
47. Schwarzinger S., Kroon G.J., Foss T.R., Wright P.E., and Dyson H.J. Random coil chemical shifts in acidic 8 M urea: implementation of random coil shift data in nmrview. Journal of Biomolecular NMR 18 September(1) (2000) 43-48
48. Shaka A.J., Keeler J., Frenkiel T., and Freeman R. An improved sequence for broad-band decoupling - WALTZ-16. Journal of Magnetic Resonance 52 2 (1983) 335-338
49. Shojania S., and O'Neil J.D. HIV-1 Tat is a natively unfolded protein: the solution conformation and dynamics of reduced HIV-1 Tat-(1-72) by NMR spectroscopy. Journal of Biological Chemistry 281 March(13) (2006) 8347-8356
50. Siddappa N., Venkatramanan M., Venkatesh P., Janki M., Jayasuryan N., Desai A., Ravi V., and Ranga U. Transactivation and signaling functions of Tat are not correlated: biological and immunological characterization of HIV-1 subtype-c Tat protein. Retrovirology (2006) 3 (1)
51. Smith S.M., Pentlicky S., Klase Z., Singh M., Neuveut C., Lu C.Y., Reitz M.S., Yarchoan R., Marx P.A., and Jeang K.T. An in vivo replication-important function in the second coding exon of Tat is constrained against mutation despite cytotoxic T lymphocyte selection. Journal of Biological Chemistry 278 November(45) (2003) 44816-44825
52. Studier F.W., Rosenberg A.H., Dunn J.J., and Dubendorff J.W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods in Enzymology 185 (1990) 60-89
53. Swanson C.M., and Malim M.H. Snapshot: Hiv-1 proteins. Cell 133 4 (2008) 742-742.e1
54. Triboulet R., Mari B., Lin Y.-L., Chable-Bessia C., Bennasser Y., Lebrigand K., Cardinaud B., Maurin T., Barbry P., Baillat V., Reynes J., Corbeau P., Jeang K.-T., and Benkirane M. Suppression of MicroRNA-Silencing Pathway by HIV-1 During Virus Replication. Science 315 5818 (2007) 1579-1582
55. Vertes A., Benscura A., Sadeghi M., and Wu X. Adduct formation and energy redistribution in UV and IR matrix-assisted laser desorption. In: Haglund R.F., and Wood R.F. (Eds). Proceedings of the Society of Photo-optical Instrumentation Engineers: Laser Plasma Generation and Diagnostics, vol. 3935. SPIE, Bellingham (2000) 76-84
56. Westendorp M.O., Shatrov V.A., Schulze-Osthoff K., Frank R., Kraft M., Los M., Krammer P.H., Droge W., and Lehmann V. HIV-1 Tat potentiates tnf-induced nf-κβ activation and cytotoxicity by altering the cellular redox state. EMBO Journal 14 February(3) (1995) 546-554
57. 15N chemical shift referencing in biomolecular NMR. Journal of Biomolecular NMR 6 September(2) (1995) 135-140
58. Wittekind M., and Mueller L. Hncacb, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha- and beta-carbon resonances in proteins. Journal of Magnetic Resonance Series B 101 April(2) (1993) 201-205
59. Wüthrich K. NMR of Proteins and Nucleic Acids (1986), Wiley, New York
60. Yamaguchi Y., Takagi T., Wada T., Yano K., Furuya A., Sugimoto S., Hasegawa J., and Handa H. NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 97 April(1) (1999) 41-51
61. Yao J., Dyson H.J., and Wright P.E. Chemical shift dispersion and secondary structure prediction in unfolded and partly folded proteins. FEBS Letters 419 December(2-3) (1997) 285-289
62. Zhang O., Forman-Kay J.D., Shortle D., and Kay L.E. Triple-resonance NOESY-based experiments with improved spectral resolution: applications to structural characterization of unfolded, partially folded and folded proteins. Journal of Biomolecular NMR 9 February(2) (1997) 181-200