Solution structure of the HIV-2 TAR-argininamide complex.

The trans-activating region (TAR) RNA-Tat protein interaction is important for activation of transciption in the human immunodeficiency virus (HIV). A model complex for this interaction composed of the two base bulge HIV-2 TAR and the amide derivative of arginine was studied by multidimensional heteronuclear NMR. Because of the improved spectral properties of the HIV-2 TAR complex, a larger number of NOEs in the bulge region were observed than in earlier studies of the HIV-1 TAR-argininamide complex. A total of 681 NOE distance restraints were collected and used to determine the solution structure of the HIV-2 TAR-argininamide complex. As observed in the previously proposed model from this lab, the two A-form stems co-axially stack and the critical U23 and the argininamide are located in the major groove. Model calculations including non-experimental restraints indicate that U23 is within hydrogen bonding distance to A27 consistent with the formation of a U x A x U base-triple. Base-triple formation helps open the major groove to increase the accessibility of G26 to hydrogen bond donors from the guanidinium group of argininamide. Argininamide binding is stabilized by stacking of the guanidinium group between the bases of A22 and U23, forming an argininamide sandwich.

[1]  S. Grzesiek,et al.  NMRPipe: A multidimensional spectral processing system based on UNIX pipes , 1995, Journal of biomolecular NMR.

[2]  Gabriele Varani,et al.  NMR investigation of RNA structure , 1996 .

[3]  A. Frankel,et al.  Electrostatic interactions modulate the RNA-binding and transactivation specificities of the human immunodeficiency virus and simian immunodeficiency virus Tat proteins. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[4]  J. Karn,et al.  The structure of the human immunodeficiency virus type-1 TAR RNA reveals principles of RNA recognition by Tat protein. , 1995, Journal of molecular biology.

[5]  C. Pabo,et al.  Zif268 protein-DNA complex refined at 1.6 A: a model system for understanding zinc finger-DNA interactions. , 1996, Structure.

[6]  D. Crothers,et al.  RNA binding assays for Tat-derived peptides: implications for specificity. , 1992, Biochemistry.

[7]  O. Uhlenbeck,et al.  Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. , 1987, Nucleic acids research.

[8]  N. Sonenberg,et al.  Structural requirements for trans activation of human immunodeficiency virus type 1 long terminal repeat-directed gene expression by tat: importance of base pairing, loop sequence, and bulges in the tat-responsive sequence , 1990, Journal of virology.

[9]  N. Sonenberg,et al.  Critical chemical features in trans-acting-responsive RNA are required for interaction with human immunodeficiency virus type 1 Tat protein , 1991, Journal of virology.

[10]  Lars Liljas,et al.  Crystal structure of an RNA bacteriophage coat protein–operator complex , 1994, Nature.

[11]  S. Wijmenga,et al.  Sequential Backbone Assignment in C-13-Labeled RNA Via through-Bond Coherence Transfer Using 3-Dimensional Triple-Resonance Spectroscopy (H-1, C-13, P-31) and 2-Dimensional Hetero Tocsy , 1994 .

[12]  A. Frankel,et al.  Arginine-binding RNAs resembling TAR identified by in vitro selection. , 1996, Biochemistry.

[13]  J. Wieruszeski,et al.  Use of a water flip-back pulse in the homonuclear NOESY experiment , 1995, Journal of biomolecular NMR.

[14]  M. Singh,et al.  HIV‐1 tat protein stimulates transcription by binding to a U‐rich bulge in the stem of the TAR RNA structure. , 1990, The EMBO journal.

[15]  P. Kollman,et al.  An all atom force field for simulations of proteins and nucleic acids , 1986, Journal of computational chemistry.

[16]  Ray Freeman,et al.  Band-selective radiofrequency pulses , 1991 .

[17]  Patel,et al.  Molecular recognition in the bovine immunodeficiency virus Tat peptide-TAR RNA complex. , 1995, Chemistry & biology.

[18]  J. Karn,et al.  High affinity binding of TAR RNA by the human immunodeficiency virus type-1 tat protein requires base-pairs in the RNA stem and amino acid residues flanking the basic region. , 1993, Journal of molecular biology.

[19]  M. Garcia-Blanco,et al.  Structural features of an RNA containing the CUGGGA loop of the human immunodeficiency virus type 1 trans-activation response element. , 1993, Biochemistry.

[20]  D. Crothers,et al.  RNA recognition by Tat-derived peptides: Interaction in the major groove? , 1991, Cell.

[21]  A. Bax,et al.  Assignment of the 31P and 1H resonances in oligonucleotides by two‐dimensional NMR spectroscopy , 1986, FEBS letters.

[22]  P. V. van Zijl,et al.  Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation. , 1995, Journal of magnetic resonance. Series B.

[23]  A. Pardi,et al.  Solution structure of the CUUG hairpin loop: a novel RNA tetraloop motif. , 1995, Biochemistry.

[24]  A. Pardi,et al.  Simple procedure for resonance assignment of the sugar protons in 13C-labeled RNAs , 1992 .

[25]  D. Crothers,et al.  Three-Dimensional Triple-Resonance 1H, 13C, 31P Experiment: Sequential Through-Bond Correlation of Ribose Protons and Intervening Phosphorus along the RNA Oligonucleotide Backbone , 1994 .

[26]  J. Puglisi,et al.  Solution Structure of a Bovine Immunodeficiency Virus Tat-TAR Peptide-RNA Complex , 1995, Science.

[27]  Nobutoshi Ito,et al.  Crystal structure at 1.92 Å resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin , 1994, Nature.

[28]  D. Crothers,et al.  Interaction of human immunodeficiency virus type 1 Tat-derived peptides with TAR RNA. , 1995, Biochemistry.

[29]  B. Peterlin,et al.  Control of RNA initiation and elongation at the HIV-1 promoter. , 1994, Annual review of biochemistry.

[30]  D. Draper,et al.  Protein-RNA recognition. , 1995, Annual review of biochemistry.

[31]  A. Frankel,et al.  Specific binding of arginine to TAR RNA. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[32]  A. Frankel Activation of HIV transcription by Tat , 1992, Current Biology.

[33]  A. R. Srinivasan,et al.  The nucleic acid database. A comprehensive relational database of three-dimensional structures of nucleic acids. , 1992, Biophysical journal.

[34]  D M Crothers,et al.  Fragments of the HIV-1 Tat protein specifically bind TAR RNA. , 1990, Science.

[35]  J. Karn,et al.  Human immunodeficiency virus 1 tat protein binds trans-activation-responsive region (TAR) RNA in vitro. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[36]  V. Saudek,et al.  Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions , 1992, Journal of biomolecular NMR.

[37]  D. S. Garrett,et al.  Increased Resolution and Improved Spectral Quality in Four-Dimensional 13C/13C-Separated HMQC-NOESY-HMQC Spectra Using Pulsed Field Gradients , 1993 .

[38]  Michael J. Gait,et al.  Methylphosphonate mapping of phosphate contacts critical for RNA recognition by the human immunodeficiency virus tat and rev proteins , 1994, Nucleic Acids Res..

[39]  M. Zacharias,et al.  The bend in RNA created by the trans-activation response element bulge of human immunodeficiency virus is straightened by arginine and by Tat-derived peptide. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[40]  D. Patel,et al.  Molecular recognition in the FMN-RNA aptamer complex. , 1996, Journal of molecular biology.

[41]  R. Batey,et al.  Preparation of isotopically enriched RNAs for heteronuclear NMR. , 1995, Methods in enzymology.

[42]  J Grasby,et al.  Hydrogen-bonding contacts in the major groove are required for human immunodeficiency virus type-1 tat protein recognition of TAR RNA. , 1993, Journal of molecular biology.

[43]  T. Nguyen,et al.  Sequence-specific interaction of Tat protein and Tat peptides with the transactivation-responsive sequence element of human immunodeficiency virus type 1 in vitro. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[44]  E Westhof,et al.  Structural Basis of Ligand Discrimination by Two Related RNA Aptamers Resolved by NMR Spectroscopy , 1996, Science.

[45]  G. Varani,et al.  RNA structure and NMR spectroscopy , 1991, Quarterly Reviews of Biophysics.

[46]  Robert Powers,et al.  A common sense approach to peak picking in two-, three-, and four-dimensional spectra using automatic computer analysis of contour diagrams , 1991 .

[47]  J. Puglisi,et al.  Role of RNA structure in arginine recognition of TAR RNA. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[48]  J. Feigon,et al.  Proton nuclear magnetic resonance assignments and structural characterization of an intramolecular DNA triplex. , 1992, Journal of molecular biology.

[49]  B. Clark,et al.  Structure of yeast phenylalanine tRNA at 3 Å resolution , 1974, Nature.

[50]  L. Kay,et al.  α Helix-RNA Major Groove Recognition in an HIV-1 Rev Peptide-RRE RNA Complex , 1996, Science.

[51]  G. Varani,et al.  Specificity of ribonucleoprotein interaction determined by RNA folding during complex formation , 1996, Nature.

[52]  J. A. Jaeger,et al.  An NMR study of the HIV-1 TAR element hairpin. , 1993, Biochemistry.

[53]  N. Sonenberg,et al.  A bulge structure in HIV-1 TAR RNA is required for Tat binding and Tat-mediated trans-activation. , 1990, Disease markers.

[54]  A. J. Shaka,et al.  Evaluation of a new broadband decoupling sequence: WALTZ-16 , 1983 .

[55]  B Tidor,et al.  Arginine-mediated RNA recognition: the arginine fork , 1991, Science.

[56]  J. Puglisi,et al.  Conformation of the TAR RNA-arginine complex by NMR spectroscopy. , 1992, Science.

[57]  H. Berman,et al.  Geometric Parameters in Nucleic Acids: Sugar and Phosphate Constituents , 1996 .