Rad5 HIRAN domain: Structural insights into its interaction with ssDNA through molecular modeling approaches

References

• Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindahl, E. (2015). GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1-2, 19–25. https://doi.org/10.1016/j.softx.2015.06.001[Mismatch]
   Google Scholar
• Achar, Y. J., Balogh, D., Neculai, D., Juhasz, S., Morocz, M., Gali, H., Dhe-Paganon, S., Venclovas, Č., & Haracska, L. (2015). Human HLTF  mediates postreplication repair by its HIRAN domain-dependent replication fork remodelling. Nucleic Acids Research, 43(21), 10277–10291. https://doi.org/10.1093/nar/gkv896
   Google Scholar
• Allen, W. J., Balius, T. E., Mukherjee, S., Brozell, S. R., Moustakas, D. T., Lang, P. T., Case, D. A., Kuntz, I. D., & Rizzo, R. C. (2015). DOCK 6: Impact of new features and current docking performance. Journal of Computational Chemistry, 36(15), 1132–1156. https://doi.org/10.1002/jcc.23905
   PubMed Web of Science ®Google Scholar
• Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
   PubMed Web of Science ®Google Scholar
• Bavi, R., Kumar, R., Rampogu, S., Son, M., Park, C., Baek, A., Kim, H.-H., Suh, J.-K., Park, S. J., & Lee, K. W. (2016). Molecular interactions of UvrB protein and DNA from Helicobacter pylori: Insight into a molecular modeling approach. Computers in Biology and Medicine, 75, 181–189. https://doi.org/10.1016/j.compbiomed.2016.06.005
   PubMed Web of Science ®Google Scholar
• Bhattacharya, D., Nowotny, J., Cao, R., & Cheng, J. (2016). 3Drefine: An interactive web server for efficient protein structure refinement. Nucleic Acids Research, 44(W1), W406–W409. https://doi.org/10.1093/nar/gkw336
   PubMed Web of Science ®Google Scholar
• Blastyák, A., Hajdú, I., Unk, I., & Haracska, L. (2010). Role of double-stranded DNA translocase activity of human HLTF in replication of damaged DNA. Molecular and Cellular Biology, 30(3), 684–693. https://doi.org/10.1128/MCB.00863-09
   PubMed Web of Science ®Google Scholar
• Blastyák, A., Pintér, L., Unk, I., Prakash, L., Prakash, S., & Haracska, L. (2007). Yeast Rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression. Molecular Cell, 28(1), 167–175. https://doi.org/10.1016/j.molcel.2007.07.030
   PubMed Web of Science ®Google Scholar
• Bussi, G., Donadio, D., & Parrinello, M. (2007). Canonical sampling through velocity rescaling. The Journal of Chemical Physics, 126(1), 014101. https://doi.org/10.1063/1.2408420
   PubMed Web of Science ®Google Scholar
• Case, D. A., Ben-Shalom, I. Y., Brozell, S. R., Cerutti, D. S., Cheatham, T. E., III, Cruzeiro, V. W. D., Darden, T. A., Duke, R. E., Ghoreishi, D., & Gilson, M. K. (2018). AMBER 2018. ; University of California.
   Google Scholar
• Chavez, D. A., Greer, B. H., & Eichman, B. F. (2018). The HIRAN domain of helicase-like transcription factor positions the DNA translocase motor to drive efficient DNA fork regression. J Biol Chem, 293(22), 8484–8494. https://doi.org/10.1074/jbc.RA118.002905
   PubMed Web of Science ®Google Scholar
• Colovos, C., & Yeates, T. O. (1993). Verification of protein structures: Patterns of nonbonded atomic interactions. Protein Science : a Publication of the Protein Society, 2(9), 1511–1519. https://doi.org/10.1002/pro.5560020916
   PubMed Web of Science ®Google Scholar
• Coskuner, O., & Uversky, V. N. (2017). Tyrosine Regulates β-Sheet Structure Formation in Amyloid-β42: A New Clustering Algorithm for Disordered Proteins. Journal of Chemical Information and Modeling, 57(6), 1342–1358. https://doi.org/10.1021/acs.jcim.6b00761
   PubMed Web of Science ®Google Scholar
• Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N⋅log(N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/10.1063/1.464397
   Web of Science ®Google Scholar
• Daura, X., Gademann, K., Jaun, B., Seebach, D., Gunsteren, W. F., van., & Mark, A. E. (1999). Peptide Folding: When Simulation Meets Experiment. Angewandte Chemie International Edition, 38(1-2), 236–240. https://doi.org/10.1002/(SICI)1521-3773(19990115)38:1/2<236::AID-ANIE236>3.0.CO;2-M
   PubMed Web of Science ®Google Scholar
• Dauter, Z., & Wlodawer, A. (2016). Progress in protein crystallography. Protein and Peptide Letters, 23(3), 201–210.
   PubMed Web of Science ®Google Scholar
• Du, X., Li, Y., Xia, Y.-L., Ai, S.-M., Liang, J., Sang, P., Ji, X.-L., & Liu, S.-Q. (2016). Insights into Protein–Ligand Interactions: Mechanisms, Models, and Methods. International Journal of Molecular Sciences, 17(2), 144. https://doi.org/10.3390/ijms17020144
   PubMed Web of Science ®Google Scholar
• Elserafy, M., Abugable, A. A., Atteya, R., & El-Khamisy, S. F. (2018). Rad5, HLTF, and SHPRH: A Fresh View of an Old Story. Trends in Genetics : TIG, 34(8), 574–577. https://doi.org/10.1016/j.tig.2018.04.006
   PubMed Web of Science ®Google Scholar
• Finn, R. D., Bateman, A., Clements, J., Coggill, P., Eberhardt, R. Y., Eddy, S. R., Heger, A., Hetherington, K., Holm, L., Mistry, J., Sonnhammer, E. L. L., Tate, J., & Punta, M. (2014). Pfam: The protein families database. Nucleic Acids Research, 42(Database issue), D222–D230. https://doi.org/10.1093/nar/gkt1223
   PubMed Web of Science ®Google Scholar
• Galindo-Murillo, R., Robertson, J. C., Zgarbová, M., Šponer, J., Otyepka, M., Jurečka, P., & Cheatham, T. E. (2016). Assessing the Current State of Amber Force Field Modifications for DNA. Journal of Chemical Theory and Computation, 12(8), 4114–4127. https://doi.org/10.1021/acs.jctc.6b00186
   PubMed Web of Science ®Google Scholar
• Ganesan, A., Coote, M. L., & Barakat, K. (2017). Molecular dynamics-driven drug discovery: Leaping forward with confidence. Drug Discovery Today, 22(2), 249–269. https://doi.org/10.1016/j.drudis.2016.11.001
   PubMed Web of Science ®Google Scholar
• Gildenberg, M. S., & Washington, M. T. (2019). Conformational flexibility of fork-remodeling helicase Rad5 shown by full-ensemble hybrid methods. PLOS One, 14(10), e0223875. https://doi.org/10.1371/journal.pone.0223875
   PubMed Web of Science ®Google Scholar
• Hamed, M. Y. (2018). Role of protein structure and the role of individual fingers in zinc finger protein-DNA recognition: a molecular dynamics simulation study and free energy calculations. J Comput Aided Mol Des , 32(6), 657–669. https://doi.org/10.1007/s10822-018-0119-9
   PubMed Web of Science ®Google Scholar
• Hargreaves, D. C., & Crabtree, G. R. (2011). ATP-dependent chromatin remodeling: Genetics, genomics and mechanisms. Cell Research, 21(3), 396–420. https://doi.org/10.1038/cr.2011.32
   PubMed Web of Science ®Google Scholar
• Hayashi, M., Keyamura, K., & Hishida, T. (2018). Cyclin-dependent kinase modulates budding yeast Rad5 stability during cell cycle. PLOS One, 13(9), e0204680. https://doi.org/10.1371/journal.pone.0204680
   PubMed Web of Science ®Google Scholar
• Hishiki, A., Hara, K., Ikegaya, Y., Yokoyama, H., Shimizu, T., Sato, M., & Hashimoto, H. (2015). Structure of a Novel DNA-binding Domain of Helicase-like Transcription Factor (HLTF) and Its Functional Implication in DNA Damage Tolerance. J Biol Chem, 290(21), 13215–13223. https://doi.org/10.1074/jbc.M115.643643
   PubMed Web of Science ®Google Scholar
• Hishiki, A., Sato, M., & Hashimoto, H. (2020). Structure of the HLTF HIRAN domain and its functional implications in regression of a stalled replication fork. Acta Crystallographica. Section D, Structural Biology, 76(Pt 8), 729–735. https://doi.org/10.1107/S2059798320008074
   PubMedGoogle Scholar
• Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., & Simmerling, C. (2006). Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins, 65(3), 712–725. https://doi.org/10.1002/prot.21123
   PubMed Web of Science ®Google Scholar
• Iyer, L. M., Babu, M., & Aravind, L. (2006). The HIRAN Domain and Recruitment of Chromatin Remodeling and Repair activities to Damaged DNA. Cell Cycle (Georgetown, Tex.), 5(7), 775–782. https://doi.org/10.4161/cc.5.7.2629
   PubMed Web of Science ®Google Scholar
• Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. The Journal of Chemical Physics, 79(2), 926–935. https://doi.org/10.1063/1.445869
   Web of Science ®Google Scholar
• Kabsch, W., & Sander, C. (1983). Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22(12), 2577–2637. https://doi.org/10.1002/bip.360221211
   PubMed Web of Science ®Google Scholar
• Kamaraj, B., & Bogaerts, A. (2015). Structure and Function of p53-DNA Complexes with Inactivation and Rescue Mutations: A Molecular Dynamics Simulation Study. PLOS One, 10(8), e0134638. https://doi.org/10.1371/journal.pone.0134638
   PubMed Web of Science ®Google Scholar
• Katoh, K., Misawa, K., Kuma, K-i., & Miyata, T. (2002). MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res, 30(14), 3059–3066. https://doi.org/10.1093/nar/gkf436
   PubMed Web of Science ®Google Scholar
• Kile, A. C., Chavez, D. A., Bacal, J., Eldirany, S., Korzhnev, D. M., Bezsonova, I., Eichman, B. F., & Cimprich, K. A. (2015). HLTF's Ancient HIRAN Domain Binds 3' DNA Ends to Drive Replication Fork Reversal. Molecular Cell, 58(6), 1090–1100. https://doi.org/10.1016/j.molcel.2015.05.013
   PubMed Web of Science ®Google Scholar
• Kobbe, D., Kahles, A., Walter, M., Klemm, T., Mannuss, A., Knoll, A., Focke, M., & Puchta, H. (2016). AtRAD5A is a DNA translocase harboring a HIRAN domain which confers binding to branched DNA structures and is required for DNA repair in vivo. The Plant Journal : For Cell and Molecular Biology, 88(4), 521–530. https://doi.org/10.1111/tpj.13283
   PubMed Web of Science ®Google Scholar
• Korzhnev, D. M., Neculai, D., Dhe-Paganon, S., Arrowsmith, C. H., & Bezsonova, I. (2016). Solution NMR structure of the HLTF HIRAN domain: A conserved module in SWI2/SNF2 DNA damage tolerance proteins. Journal of Biomolecular NMR, 66(3), 209–219. https://doi.org/10.1007/s10858-016-0070-9
   PubMed Web of Science ®Google Scholar
• Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Molecular Biology and Evolution, 35(6), 1547–1549. https://doi.org/10.1093/molbev/msy096
   PubMed Web of Science ®Google Scholar
• Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: A program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26(2), 283–291. https://doi.org/10.1107/S0021889892009944
   Web of Science ®Google Scholar
• Maciejewski, M. W., Schuyler, A. D., Gryk, M. R., Moraru, I. I., Romero, P. R., Ulrich, E. L., Eghbalnia, H. R., Livny, M., Delaglio, F., & Hoch, J. C. (2017). NMRbox: A Resource for Biomolecular NMR Computation. Biophysical Journal, 112(8), 1529–1534. https://doi.org/10.1016/j.bpj.2017.03.011
   PubMed Web of Science ®Google Scholar
• Maier, J. A., Martinez, C., Kasavajhala, K., Wickstrom, L., Hauser, K. E., & Simmerling, C. (2015). ff14SB: Improving the Accuracy of Protein Side Chain and Backbone Parameters from ff99SB. Journal of Chemical Theory and Computation, 11(8), 3696–3713. https://doi.org/10.1021/acs.jctc.5b00255
   PubMed Web of Science ®Google Scholar
• Mary, V., Haris, P., Varghese, M. K., Aparna, P., & Sudarsanakumar, C. (2017). Experimental Probing and Molecular Dynamics Simulation of the Molecular Recognition of DNA Duplexes by the Flavonoid Luteolin. Journal of Chemical Information and Modeling, 57(9), 2237–2249. https://doi.org/10.1021/acs.jcim.6b00747
   PubMed Web of Science ®Google Scholar
• Newberry, R. W., & Raines, R. T. (2019). Secondary Forces in Protein Folding. ACS Chemical Biology, 14(8), 1677–1686. https://doi.org/10.1021/acschembio.9b00339
   PubMed Web of Science ®Google Scholar
• Oprzeska-Zingrebe, E. A., & Smiatek, J. (2018). Preferential Binding of Urea to Single-Stranded DNA Structures: A Molecular Dynamics Study. Biophysical Journal, 114(7), 1551–1562. https://doi.org/10.1016/j.bpj.2018.02.013
   PubMed Web of Science ®Google Scholar
• Parrinello, M., & Rahman, A. (1981). Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics, 52(12), 7182–7190. https://doi.org/10.1063/1.328693
   Web of Science ®Google Scholar
• Parulekar, R. S., Barage, S. H., Jalkute, C. B., Dhanavade, M. J., Fandilolu, P. M., & Sonawane, K. D. (2013). Homology Modeling, Molecular Docking and DNA Binding Studies of Nucleotide Excision Repair UvrC Protein from M. tuberculosis. The Protein Journal, 32(6), 467–476. https://doi.org/10.1007/s10930-013-9506-1
   PubMed Web of Science ®Google Scholar
• Petrović, D., Wang, X., & Strodel, B. (2018). How accurately do force fields represent protein side chain ensembles? Proteins, 86(9), 935–944. https://doi.org/10.1002/prot.25525
   PubMed Web of Science ®Google Scholar
• Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera-a visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. https://doi.org/10.1002/jcc.20084
   PubMed Web of Science ®Google Scholar
• Pitta, K., & Krishnan, M. (2018). Molecular Mechanism, Dynamics, and Energetics of Protein-Mediated Dinucleotide Flipping in a Mismatched DNA: A Computational Study of the RAD4-DNA Complex. Journal of Chemical Information and Modeling, 58(3), 647–660. https://doi.org/10.1021/acs.jcim.7b00636
   PubMed Web of Science ®Google Scholar
• Pradhan, S., Das, P., & Mattaparthi, V. S. K. (2018). Characterizing the Binding Interactions between DNA-Binding Proteins, XPA and XPE: A Molecular Dynamics Approach. ACS Omega, 3(11), 15442–15454. https://doi.org/10.1021/acsomega.8b01793
   PubMed Web of Science ®Google Scholar
• Roe, D. R., & Cheatham, T. E. (2013). PTRAJ and CPPTRAJ: Software for Processing and Analysis of Molecular Dynamics Trajectory Data. Journal of Chemical Theory and Computation, 9(7), 3084–3095. https://doi.org/10.1021/ct400341p
   PubMed Web of Science ®Google Scholar
• Sali, A., & Blundell, T. L. (1993). Comparative protein modelling by satisfaction of spatial restraints. Journal of Molecular Biology, 234(3), 779–815. https://doi.org/10.1006/jmbi.1993.1626
   PubMed Web of Science ®Google Scholar
• Sanner, M. F., Olson, A. J., & Spehner, J. C. (1996). Reduced surface: An efficient way to compute molecular surfaces. Biopolymers, 38(3), 305–320. https://doi.org/10.1002/(SICI)1097-0282(199603)38:3<305::AID-BIP4>3.0.CO;2-Y
   PubMed Web of Science ®Google Scholar
• Shen, M., & Sali, A. (2006). Statistical potential for assessment and prediction of protein structures. Protein Science : a Publication of the Protein Society, 15(11), 2507–2524. https://doi.org/10.1110/ps.062416606
   PubMed Web of Science ®Google Scholar
• Shin, S., Hyun, K., Kim, J., & Hohng, S. (2018). ATP Binding to Rad5 Initiates Replication Fork Reversal by Inducing the Unwinding of the Leading Arm and the Formation of the Holliday Junction. Cell Reports, 23(6), 1831–1839. https://doi.org/10.1016/j.celrep.2018.04.029
   PubMed Web of Science ®Google Scholar
• Shrivastava, N., Nag, J. K., Pandey, J., Tripathi, R. P., Shah, P., Siddiqi, M. I., & Misra-Bhattacharya, S. (2015). Homology Modeling of NAD+ -Dependent DNA Ligase of the Wolbachia Endosymbiont of Brugia malayi and Its Drug Target Potential Using Dispiro-Cycloalkanones. Antimicrobial Agents and Chemotherapy, 59(7), 3736–3747. https://doi.org/10.1128/AAC.03449-14
   PubMed Web of Science ®Google Scholar
• Song, Y., DiMaio, F., Wang, R. Y.-R., Kim, D., Miles, C., Brunette, T., Thompson, J., & Baker, D. (2013). High-Resolution Comparative Modeling with RosettaCM. Structure (London, England : 1993), 21(10), 1735–1742. https://doi.org/10.1016/j.str.2013.08.005
   PubMed Web of Science ®Google Scholar
• Su, X.-D., Zhang, H., Terwilliger, T. C., Liljas, A., Xiao, J., & Dong, Y. (2015). Protein Crystallography from the Perspective of Technology Developments. Crystallography Reviews, 21(1-2), 122–153. https://doi.org/10.1080/0889311X.2014.973868
   PubMed Web of Science ®Google Scholar
• Verma, S., Grover, S., Tyagi, C., Goyal, S., Jamal, S., Singh, A., & Grover, A. (2016). Hydrophobic Interactions Are a Key to MDM2 Inhibition by Polyphenols as Revealed by Molecular Dynamics Simulations and MM/PBSA Free Energy Calculations. PLOS One, 11(2), e0149014. https://doi.org/10.1371/journal.pone.0149014
   PubMed Web of Science ®Google Scholar
• Wagih, O. (2017). ggseqlogo: A versatile R package for drawing sequence logos. Bioinformatics (Oxford, England), 33(22), 3645–3647. https://doi.org/10.1093/bioinformatics/btx469
   PubMed Web of Science ®Google Scholar
• Weber, O. C., & Uversky, V. N. (2017). How accurate are your simulations? Effects of confined aqueous volume and AMBER FF99SB and CHARMM22/CMAP force field parameters on structural ensembles of intrinsically disordered proteins: Amyloid-β42 in water. Intrinsically Disordered Proteins, 5(1), e1377813. https://doi.org/10.1080/21690707.2017.1377813
   PubMedGoogle Scholar
• Wickham, H. (2016). ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York. https://ggplot2.tidyverse.org
   Google Scholar
• Worth, C. L., Gong, S., & Blundell, T. L. (2009). Structural and functional constraints in the evolution of protein families. Nat Rev Mol Cell Biol, 10(10), 709–720. https://doi.org/10.1038/nrm2762
   PubMed Web of Science ®Google Scholar
• Xu, X., Lin, A., Zhou, C., Blackwell, S. R., Zhang, Y., Wang, Z., Feng, Q., Guan, R., Hanna, M. D., Chen, Z., & Xiao, W. (2016). Involvement of budding yeast Rad5 in translesion DNA synthesis through physical interaction with Rev1. Nucleic Acids Research, 44(11), 5231–5245. https://doi.org/10.1093/nar/gkw183
   PubMed Web of Science ®Google Scholar
• Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., & Zhang, Y. (2015). The I-TASSER Suite: Protein structure and function prediction. Nature Methods, 12(1), 7–8. https://doi.org/10.1038/nmeth.3213
   PubMed Web of Science ®Google Scholar