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Impact of subtype C-specific amino acid variants on HIV-1 Tat-TAR interaction: insights from molecular modelling and dynamics – Virology Journal
Faria NR, Rambaut A, Suchard MA, Baele G, Bedford T, Ward MJ, Tatem AJ, Sousa JD, Arinaminpathy N, Pépin J, et al. HIV epidemiology. The early spread and epidemic ignition of HIV-1 in human populations. Science. 2014;346:56–61.
Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, Cummins LB, Arthur LO, Peeters M, Shaw GM, et al. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature. 1999;397:436–41.
UNAIDS. UNAIDS DATA. Geneva: Joint United Nations Programme on HIV/AIDS; 2022.
Govender RD, Hashim MJ, Khan MA, Mustafa H, Khan G. Global Epidemiology of HIV/AIDS: A Resurgence in North America and Europe. J Epidemiol Glob Health. 2021;11:296–301.
Kharsany AB, Karim QA. HIV Infection and AIDS in Sub-Saharan Africa: Current Status Challenges and Opportunities. Open AIDS J. 2016;10:34–48.
Hemelaar J. The origin and diversity of the HIV-1 pandemic. Trends Mol Med. 2012;18:182–92.
Hemelaar J, Elangovan R, Yun J, Dickson-Tetteh L, Fleminger I, Kirtley S, Williams B, Gouws-Williams E, Ghys PD. Global and regional molecular epidemiology of HIV-1, 1990–2015: a systematic review, global survey, and trend analysis. Lancet Infect Dis. 2019;19:143–55.
Sharp PM, Hahn BH. Origins of HIV and the AIDS pandemic. Cold Spring Harb Perspect Med. 2011;1:a006841.
Taylor BS, Hammer SM. The challenge of HIV-1 subtype diversity. N Engl J Med. 2008;359:1965–6.
Gartner MJ, Roche M, Churchill MJ, Gorry PR, Flynn JK. Understanding the mechanisms driving the spread of subtype C HIV-1. EBioMedicine. 2020;53:102682.
Bbosa N, Kaleebu P, Ssemwanga D. HIV subtype diversity worldwide. Curr Opin HIV AIDS. 2019;14:153–60.
Korber B, Gaschen B, Yusim K, Thakallapally R, Kesmir C, Detours V. Evolutionary and immunological implications of contemporary HIV-1 variation. Br Med Bull. 2001;58:19–42.
Roy CN, Khandaker I, Oshitani H. Evolutionary Dynamics of Tat in HIV-1 Subtypes B and C. PLoS One. 2015;10:e0129896.
Maljkovic Berry I, Ribeiro R, Kothari M, Athreya G, Daniels M, Lee HY, Bruno W, Leitner T. Unequal evolutionary rates in the human immunodeficiency virus type 1 (HIV-1) pandemic: the evolutionary rate of HIV-1 slows down when the epidemic rate increases. J Virol. 2007;81:10625–35.
Cuevas JM, Geller R, Garijo R, López-Aldeguer J, Sanjuán R. Extremely High Mutation Rate of HIV-1 In Vivo. PLoS Biol. 2015;13:e1002251.
Spector C, Mele AR, Wigdahl B, Nonnemacher MR. Genetic variation and function of the HIV-1 Tat protein. Med Microbiol Immunol. 2019;208:131–69.
Li W, Li G, Steiner J, Nath A. Role of Tat protein in HIV neuropathogenesis. Neurotoxicity research. 2009;16:205–20.
Yang M. Discoveries of Tat-TAR interaction inhibitors for HIV-1. Curr Drug Targets Infect Disord. 2005;5:433–44.
Li L, Dahiya S, Kortagere S, Aiamkitsumrit B, Cunningham D, Pirrone V, Nonnemacher MR, Wigdahl B. Impact of Tat Genetic Variation on HIV-1 Disease. Adv Virol. 2012;2012:123605.
Gotora PT, van der Sluis R, Williams ME. HIV-1 Tat amino acid residues that influence Tat-TAR binding affinity: a scoping review. BMC Infectious Diseases. 2023;23:164.
Greenbaum NL. How Tat targets TAR: structure of the BIV peptide-RNA complex. Structure. 1996;4:5–9.
Siddappa NB, Venkatramanan M, Venkatesh P, Janki MV, Jayasuryan N, Desai A, Ravi V, Ranga U. Transactivation and signaling functions of Tat are not correlated: biological and immunological characterization of HIV-1 subtype-C Tat protein. Retrovirology. 2006;3:53.
Johri MK, Sharma N, Singh SK. HIV Tat protein: Is Tat-C much trickier than Tat-B? J Med Virol. 2015;87:1334–43.
Saylor D, Dickens AM, Sacktor N, Haughey N, Slusher B, Pletnikov M, Mankowski JL, Brown A, Volsky DJ, McArthur JC. HIV-associated neurocognitive disorder – pathogenesis and prospects for treatment. Nat Rev Neurol. 2016;12:309.
Campbell GR, Watkins JD, Singh KK, Loret EP, Spector SA. Human immunodeficiency virus type 1 subtype C Tat fails to induce intracellular calcium flux and induces reduced tumor necrosis factor production from monocytes. Journal of virology. 2007;81:5919–28.
Williams ME, Zulu SS, Stein DJ, Joska JA, Naudé PJW. Signatures of HIV-1 subtype B and C Tat proteins and their effects in the neuropathogenesis of HIV-associated neurocognitive impairments. Neurobiol Dis. 2020;136:104701.
Santerre M, Wang Y, Arjona S, Allen C, Sawaya BE. Differential Contribution of HIV-1 Subtypes B and C to Neurological Disorders: Mechanisms and Possible Treatments. AIDS Rev. 2019;21:76–83.
Ruiz AP, Ajasin DO, Ramasamy S, DesMarais V, Eugenin EA, Prasad VR. A Naturally Occurring Polymorphism in the HIV-1 Tat Basic Domain Inhibits Uptake by Bystander Cells and Leads to Reduced Neuroinflammation. Sci Rep. 2019;9:3308.
Kurosu T, Mukai T, Komoto S, Ibrahim MS. Li Yg, Kobayashi T, Tsuji S, Ikuta K: Human immunodeficiency virus type 1 subtype C exhibits higher transactivation activity of Tat than subtypes B and E. Microbiology and immunology. 2002;46:787–99.
Borkar AN, Bardaro MF Jr, Camilloni C, Aprile FA, Varani G, Vendruscolo M. Structure of a low-population binding intermediate in protein-RNA recognition. Proc Natl Acad Sci U S A. 2016;113:7171–6.
Chaloin O, Peter JC, Briand JP, Masquida B, Desgranges C, Muller S, Hoebeke J. The N-terminus of HIV-1 Tat protein is essential for Tat-TAR RNA interaction. Cell Mol Life Sci. 2005;62:355–61.
Long KS, Crothers DM. Interaction of human immunodeficiency virus type 1 Tat-derived peptides with TAR RNA. Biochemistry. 1995;34:8885–95.
Ronsard L, Rai T, Rai D, Ramachandran VG, Banerjea AC. In silico Analyses of Subtype Specific HIV-1 Tat-TAR RNA Interaction Reveals the Structural Determinants for Viral Activity. Front Microbiol. 2017;8:1467.
Williams ME, Cloete R. Molecular Modeling of Subtype-Specific Tat Protein Signatures to Predict Tat-TAR Interactions That May Be Involved in HIV-Associated Neurocognitive Disorders. Front Microbiol. 2022;13:866611.
Muvenda T, Williams AA, Williams ME. Transactivator of Transcription (Tat)-Induced Neuroinflammation as a key pathway in neuronal dysfunction: a scoping review. Mol Neurobiol. 2024:1–27.
Mele AR, Marino J, Dampier W, Wigdahl B, Nonnemacher MR. HIV-1 Tat Length: Comparative and Functional Considerations. Front Microbiol. 2020;11:444.
Dingwall C, Ernberg I, Gait MJ, Green SM, Heaphy S, Karn J, Lowe AD, Singh M, Skinner MA, Valerio R. Human immunodeficiency virus 1 tat protein binds trans-activation-responsive region (TAR) RNA in vitro. Proc Natl Acad Sci U S A. 1989;86:6925–9.
Arab SS, Dantism A. EasyModel: a user-friendly web-based interface based on MODELLER. Sci Rep. 2023;13:17185.
Shen MY, Sali A. Statistical potential for assessment and prediction of protein structures. Protein Sci. 2006;15:2507–24.
John B, Sali A. Comparative protein structure modeling by iterative alignment, model building and model assessment. Nucleic Acids Res. 2003;31:3982–92.
Huang J, Rauscher S, Nawrocki G, Ran T, Feig M, de Groot BL, Grubmüller H, MacKerell AD. CHARMM36m: an improved force field for folded and intrinsically disordered proteins. Nat Methods. 2017;14:71–3.
Jo S, Kim T, Iyer VG, Im W. CHARMM-GUI: a web-based graphical user interface for CHARMM. J Comput Chem. 2008;29:1859–65.
Ranganathan S, Nakai K, Schonbach C. Encyclopedia of bioinformatics and computational biology: ABC of bioinformatics. Elsevier; 2018.
Ramachandran GN, Ramakrishnan C, Sasisekharan V. Stereochemistry of polypeptide chain configurations. J Mol Biol. 1963;7:95–9.
Wiederstein M, Sippl MJ. ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res. 2007;35:W407–410.
Havel TF, Snow ME. A new method for building protein conformations from sequence alignments with homologues of known structure. J Mol Biol. 1991;217:1–7.
de Almeida SM, Rotta I, Vidal LRR, Dos Santos JS, Nath A, Johnson K, Letendre S, Ellis RJ. HIV-1C and HIV-1B Tat protein polymorphism in Southern Brazil. J Neurovirol. 2021;27:126–36.
Morris GM, Lim-Wilby M. Molecular docking. Methods Mol Biol. 2008;443:365–82.
Yan Y, Tao H, He J, Huang SY. The HDOCK server for integrated protein-protein docking. Nat Protoc. 2020;15:1829–52.
Calnan BJ, Tidor B, Biancalana S, Hudson D, Frankel AD. Arginine-mediated RNA recognition: the arginine fork. Science. 1991;252:1167–71.
Salentin S, Schreiber S, Haupt VJ, Adasme MF, Schroeder M. PLIP: fully automated protein-ligand interaction profiler. Nucleic Acids Res. 2015;43:W443–447.
Adasme MF, Linnemann KL, Bolz SN, Kaiser F, Salentin S, Haupt VJ, Schroeder M. PLIP 2021: expanding the scope of the protein-ligand interaction profiler to DNA and RNA. Nucleic Acids Res. 2021;49:W530–w534.
Lee J, Cheng X, Swails JM, Yeom MS, Eastman PK, Lemkul JA, Wei S, Buckner J, Jeong JC, Qi Y, et al. CHARMM-GUI Input Generator for NAMD, GROMACS, AMBER, OpenMM, and CHARMM/OpenMM Simulations Using the CHARMM36 Additive Force Field. J Chem Theory Comput. 2016;12:405–13.
Jo S, Cheng X, Lee J, Kim S, Park SJ, Patel DS, Beaven AH, Lee KI, Rui H, Park S, et al. CHARMM-GUI 10 years for biomolecular modeling and simulation. J Comput Chem. 2017;38:1114–24.
Park C, Robinson F, Kim D. On the choice of different water model in molecular dynamics simulations of nanopore transport phenomena. Membranes. 2022;12:1109.
Etheve L, Martin J, Lavery R. Protein-DNA interfaces: a molecular dynamics analysis of time-dependent recognition processes for three transcription factors. Nucleic Acids Res. 2016;44:9990–10002.
Harrison RL. Introduction To Monte Carlo Simulation. AIP Conf Proc. 2010;1204:17–21.
Cheng Y, Korolev N, Nordenskiöld L. Similarities and differences in interaction of K+ and Na+ with condensed ordered DNA. A molecular dynamics computer simulation study. Nucleic Acids Res. 2006;34:686–96.
Lindahl E, Abraham M, Hess B, Van der Spoel D. Gromacs 2020 Manual. Stockholm, Sweden: GROMACS Development Team; 2020.
Batut B, Hiltemann S, Bagnacani A, Baker D, Bhardwaj V, Blank C, Bretaudeau A, Brillet-Guéguen L, Čech M, Chilton J. Community-driven data analysis training for biology. Cell systems. 2018;6(752–758):e751.
Parrinello M, Rahman A. Polymorphic transitions in single crystals: A new molecular dynamics method. J Appl Physics. 1981;52:7182–90.
Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG. A smooth particle mesh Ewald method. J Chem Physics. 1995;103:8577–93.
Paissoni C, Spiliotopoulos D, Musco G, Spitaleri A. GMXPBSA 2.1: A GROMACS tool to perform MM/PBSA and computational alanine scanning. Comput Phys Commun. 2015;186:105–7.
Valdés-Tresanco MS, Valdés-Tresanco ME, Valiente PA, Moreno E. gmx_MMPBSA: a new tool to perform end-state free energy calculations with GROMACS. J Chem Theory Computat. 2021;17:6281–91.
Bradshaw RT, Patel BH, Tate EW, Leatherbarrow RJ, Gould IR. Comparing experimental and computational alanine scanning techniques for probing a prototypical protein–protein interaction. Protein Eng Des Sel. 2011;24:197–207.
Gilson MK, Zhou H-X. Calculation of protein-ligand binding affinities. Annu Rev Biophys Biomol Struct. 2007;36:21–42.
Huo S, Massova I, Kollman PA. Computational alanine scanning of the 1: 1 human growth hormone–receptor complex. J Computat Chem. 2002;23:15–27.
Moreira IS, Fernandes PA, Ramos MJ. Protein–protein docking dealing with the unknown. J Computat Chem. 2010;31:317–42.
Reddy AR, Venkateswarulu T, Babu DJ, Indira M. Homology modeling studies of human genome receptor using modeller, Swiss-model server and esypred-3D tools. Int J Pharmaceut Sci Rev Res. 2015;30:1–6.
Cloete R, Akurugu WA, Werely CJ, van Helden PD, Christoffels A. Structural and functional effects of nucleotide variation on the human TB drug metabolizing enzyme arylamine N-acetyltransferase 1. J Mole Graph Model. 2017;75:330–9.
Galaxy_Community. he Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2022 update. Nucleic Acids Res. 2022;2022(50):W345–w351.
Smilgies DM, Folta-Stogniew E. Molecular weight-gyration radius relation of globular proteins: a comparison of light scattering, small-angle X-ray scattering and structure-based data. J Appl Crystallogr. 2015;48:1604–6.
David CC, Jacobs DJ. Principal component analysis: a method for determining the essential dynamics of proteins. Methods Mol Biol. 2014;1084:193–226.
Hubbard RE, Haider MK: Hydrogen bonds in proteins: role and strength. eLS 2010.
Chen D, Oezguen N, Urvil P, Ferguson C, Dann SM, Savidge TC. Regulation of protein-ligand binding affinity by hydrogen bond pairing. Sci Adv. 2016;2:e1501240.
Itoh Y, Nakashima Y, Tsukamoto S, Kurohara T, Suzuki M, Sakae Y, Oda M, Okamoto Y, Suzuki T. N+-CH··· O Hydrogen bonds in protein-ligand complexes. Sci Rep. 2019;9:767.
ur Rehman MF, Shaeer A, Batool AI, Aslam M: Structure-function relationship of extremozymes. In Microbial Extremozymes. Elsevier; 2022: 9-30
Yu B, Pettitt BM, Iwahara J. Dynamics of Ionic Interactions at Protein-Nucleic Acid Interfaces. Acc Chem Res. 2020;53:1802–10.
Cordingley MG, LaFemina RL, Callahan PL, Condra JH, Sardana VV, Graham DJ, Nguyen TM, LeGrow K, Gotlib L, Schlabach AJ. Sequence-specific interaction of Tat protein and Tat peptides with the transactivation-responsive sequence element of human immunodeficiency virus type 1 in vitro. Proc Nat Acad Sci. 1990;87:8985–9.
Metzger AU, Bayer P, Willbold D, Hoffmann S, Frank RW, Goody RS, Rösch P. The interaction of HIV-1 Tat(32–72) with its target RNA: a fluorescence and nuclear magnetic resonance study. Biochem Biophys Res Commun. 1997;241:31–6.
Tao J, Frankel AD. Electrostatic interactions modulate the RNA-binding and transactivation specificities of the human immunodeficiency virus and simian immunodeficiency virus Tat proteins. Proc Nat Acad Sci. 1993;90:1571–5.
Ranga U, Shankarappa R, Siddappa NB, Ramakrishna L, Nagendran R, Mahalingam M, Mahadevan A, Jayasuryan N, Satishchandra P, Shankar SK, Prasad VR. Tat protein of human immunodeficiency virus type 1 subtype C strains is a defective chemokine. J Virol. 2004;78:2586–90.
Gandhi N, Saiyed Z, Thangavel S, Rodriguez J, Rao K, Nair MP. Differential effects of HIV type 1 clade B and clade C Tat protein on expression of proinflammatory and antiinflammatory cytokines by primary monocytes. AIDS Res Hum Retroviruses. 2009;25:691–9.
Mishra M, Vetrivel S, Siddappa NB, Ranga U, Seth P. Clade-specific differences in neurotoxicity of human immunodeficiency virus-1 B and C Tat of human neurons: significance of dicysteine C30C31 motif. Ann Neurol. 2008;63:366–76.
Lessells RJ, Katzenstein DK, de Oliveira T. Are subtype differences important in HIV drug resistance? Curr Opin Virol. 2012;2:636–43.
Gatell JM. Antiretroviral Therapy for HIV: Do Subtypes Matter? Clin Infect Dis. 2011;53:1153–5.
Poon AFY, Ndashimye E, Avino M, Gibson R, Kityo C, Kyeyune F, Nankya I, Quiñones-Mateu ME, Arts EJ, Paton NI, et al. First-line HIV treatment failures in non-B subtypes and recombinants: a cross-sectional analysis of multiple populations in Uganda. AIDS Res Therapy. 2019;16:3.
Nightingale S, Ances B, Cinque P, Dravid A, Dreyer AJ, Gisslén M, Joska JA, Kwasa J, Meyer A-C, Mpongo N, et al. Cognitive impairment in people living with HIV: consensus recommendations for a new approach. Nat Rev Neurol. 2023;19:424–33.
Nastri BM, Pagliano P, Zannella C, Folliero V, Masullo A, Rinaldi L, et al. HIV and drug-resistant subtypes. Microorganisms. 2023;11:221.
Dominguez C, Boelens R, Bonvin AM. HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J Am Chem Soc. 2003;125:1731–7.
Wang C, Greene DA, Xiao L, Qi R, Luo R. Recent developments and applications of the MMPBSA method. Front Mol Biosci. 2018;4:87.