Structural and dynamical correlations in PfHGXPRT oligomers: A molecular dynamics simulation study

References

• Amaro, R. E., Minh, D. D., Cheng, L. S., Lindstrom, W. M., Olson, A. J., Lin, J.-H., ... McCammon, J. A. (2007). Remarkable loop flexibility in avian influenza n1 and its implications for antiviral drug design. Journal of the American Chemical Society, 129, 7764–7765.
   PubMed Web of Science ®Google Scholar
• Andricioaei, I., & Karplus, M. (2001). On the calculation of entropy from covariance matrices of the atomic fluctuations. Journal of Chemical Physics, 115, 6289–6292.
   Web of Science ®Google Scholar
• Balendiran, G. K., Molina, J., Xu, Y., Torres-Martinez, J., Stevens, R., Focia, P. J., ... Craig, S. P. (1999). Ternary complex structure of human HGPRTase, PRPP, Mg2+, and the inhibitor HPP reveals the involvement of the flexible loop in substrate binding. Protein Science, 8, 1023–1031.
   PubMed Web of Science ®Google Scholar
• Bayly, C. I., Cieplak, P., Cornell, W., & Kollman, P. A. (1993). A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: The RESP model. The Journal of Physical Chemistry, 97, 10269–10280.
   Web of Science ®Google Scholar
• Berteotti, A., Cavalli, A., Branduardi, D., Gervasio, F. L., Recanatini, M., & Parrinello, M. (2008). Protein conformational transitions: The closure mechanism of a kinase explored by atomistic simulations. Journal of the American Chemical Society, 131, 244–250.
   Web of Science ®Google Scholar
• Butterworth, A. C., Medrano, F. J., Eakin, A. E. & Craig, S. P. (2004). Saturation mutagenesis, complement selection, and steady-state kinetic studies illuminate the roles of invariant residues in active site loop i of the hypoxanthine phosphoribosyltransferase from trypanosoma cruzi. Biochimica et Biophysica Acta (BBA) - Proteins & Proteomics, 1699, 87–94.
   Web of Science ®Google Scholar
• Canyuk, B., Medrano, F. J., Wenck, M. A., Focia, P. J., Eakin, A. E., & Craig, S. P. (2004). Interactions at the dimer interface influence the relative efficiencies for purine nucleotide synthesis and pyrophosphorolysis in a phosphoribosyltransferase. Journal of Molecular Biology, 335, 905–921.
   PubMed Web of Science ®Google Scholar
• Cembran, A., Masterson, L. R., McClendon, C. L., Taylor, S. S., Gao, J., & Veglia, G. (2012). Conformational equilibrium of n-myristoylated campdependent protein kinase a by molecular dynamics simulations. Biochemistry, 51, 10186–10196.
   PubMed Web of Science ®Google Scholar
• Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Ferguson, D. M., ... Kollman, P. A. (1995). A second generation force field for the simulation of proteins nucleic acids, and organic molecules. Journal of the American Chemical Society, 117, 5179–5197.
   Web of Science ®Google Scholar
• Da, L.-T., Wang, D., & Huang, X. (2012). Dynamics of pyrophosphate ion release and its coupled trigger loop motion from closed to open state in RNA polymerase II. Journal of the American Chemical Society, 134, 2399–2406.
   PubMed Web of Science ®Google Scholar
• Damle, N. P., & Mohanty, D. (2014). Mechanism of autophosphorylation of mycobacterial pknb explored by molecular dynamics simulations. Biochemistry, 53, 4715–4726.
   PubMed Web of Science ®Google Scholar
• Davulcu, O., Skalicky, J. J., & Chapman, M. S. (2011). Rate-limiting domain and loop motions in arginine kinase. Biochemistry, 50, 4011–4018.
   PubMed Web of Science ®Google Scholar
• de Souza Dantas, D., Ramos dos Santos, C., Guimarães Pereira, G. A., & Medrano, F. J. (2008). Biochemical and structural characterization of the hypoxanthine-guanine-xanthine phosphoribosyltransferase from pyrococcus horikoshii. Biochimica et Biophysica Acta (BBA) - Protein. Structure, 1784, 953–960.
   Google Scholar
• Dupradeau, F.-Y., Pigache, A., Zaffran, T., Savineau, C., Lelong, R., Grivel, N., ... Cieplak, P. (2010). The R.E.D. tools: advances in resp and esp charge derivation and force field library building. Physical Chemistry Chemical Physics, 12, 7821–7839.
   PubMed Web of Science ®Google Scholar
• Eads, J. C., Scapin, G., Xu, Y., Grubmeyer, C., & Sacchettini, J. C. (1994). The crystal structure of human hypoxanthine-guanine phosphoribosyltransferase with bound GMP. Cell, 78, 325–334.
   PubMed Web of Science ®Google Scholar
• Fabrini, R., De Luca, A., Stella, L., Mei, G., Orioni, B., Ciccone, S., ... Ricci, G. (2009). Monomer-dimer equilibrium in glutathione transferases: A critical re-examination. Biochemistry, 48, 10473–10482.
   PubMed Web of Science ®Google Scholar
• Fatmi, M. Q., & Chia-en, A. C. (2010). The role of oligomerization and cooperative regulation in protein function: the case of tryptophan synthase. PLoS Computational Biology, 6, e1000994.
   PubMed Web of Science ®Google Scholar
• Gayathri, P., Sujay Subbayya, I., Ashok, C. S., Selvi, T. S., Balaram, H., & Murthy, M. (2008). Crystal structure of a chimera of human and plasmodium falciparum hypoxanthine guanine phosphoribosyltransferases provides insights into oligomerization. Proteins Structure Function and Bioinformatics, 73, 1010–1020.
   PubMed Web of Science ®Google Scholar
• Georgescauld, F., Moynié, L., Habersetzer, J., Cervoni, L., Mocan, I., Borza, T., ... Lascu, I. (2013). Intersubunit ionic interactions stabilize the nucleoside diphosphate kinase of mycobacterium tuberculosis. PloS one, 8, e57867.
   Google Scholar
• Guddat, L. W., Vos, S., Martin, J. L., Keough, D. T., & de Jersey, J. (2002). Crystal structures of free, IMP-, and GMP-bound Escherichia coli hypoxanthine phosphoribosyltransferase. Protein Science, 11, 1626–1638.
   PubMed Web of Science ®Google Scholar
• Hart, K. M., Harms, M. J., Schmidt, B. H., Elya, C., Thornton, J. W., & Marqusee, S. (2014). Thermodynamic system drift in protein evolution. PLoS Biology, 12, e1001994.
   Google Scholar
• Hazleton, K. Z., Ho, M.-C., Cassera, M. B., Clinch, K., Crump, D. R., Rosario, I., Jr, ... Schramm, V. L. (2012). Acyclic immucillin phosphonates: Second-generation inhibitors of plasmodium falciparum hypoxanthine-guanine-xanthine phosphoribosyltransferase. Chemistry & Biology, 19, 721–730.
   PubMed Web of Science ®Google Scholar
• Hess, B., Bekker, H., Berendsen, H. J., & Fraaije, J. G. (1997). Lincs: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18, 1463–1472.
   Web of Science ®Google Scholar
• Hess, B., Kutzner, C., Van Der Spoel, D., & Lindahl, E. (2008). Gromacs 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory Computation, 4, 435–447.
   PubMed Web of Science ®Google Scholar
• Héroux, A., White, E. L., Ross, L. J., & Borhani, D. W. (1999). Crystal structures of the Toxoplasma gondii hypoxanthine-guanine phosphoribosyltransferase- GMP and-IMP complexes: comparison of purine binding interactions with the XMP complex. Biochemistry, 38, 14485–14494.
   PubMed Web of Science ®Google Scholar
• Héroux, A., White, E. L., Ross, L. J., Kuzin, A. P., & Borhani, D. W. (2000). Substrate deformation in a hypoxanthine-guanine phosphoribosyltransferase ternary complex: the structural basis for catalysis. Structure, 8, 1309–1318.
   PubMed Web of Science ®Google 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 Structure Function and Bioinformatics, 65, 712–725.
   PubMed Web of Science ®Google Scholar
• Hsu, S.-T. D., Peter, C., van Gunsteren, W. F., & Bonvin, A. M. (2005). Entropy calculation of hiv-1 env gp120, its receptor cd4, and their complex: an analysis of configurational entropy changes upon complexation. Biophysical Journal, 88, 15–24.
   PubMed Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). Vmd: Visual molecular dynamics. Jounal of Molecular Graphics, 14, 33–38.
   PubMed Web of Science ®Google Scholar
• Jiang, W., & Ghosh, D. (2012). Motion and flexibility in human cytochrome P450 aromatase. PloS one, 7, e32565.
   PubMed Web of Science ®Google Scholar
• Keller, M. A., Zander, U., Fuchs, J. E., Kreutz, C., Watschinger, K., Mueller, T., ... Marquez, J. A. (2014). A gatekeeper helix determines the substrate specificity of Sjögren-Larsson syndrome enzyme fatty aldehyde dehydrogenase. Nature Communications, 5.
   Google Scholar
• Keough, D. T., Brereton, I. M., De Jersey, J., & Guddat, L. W. (2005). The crystal structure of free human hypoxanthine-guanine phosphoribosyltransferase reveals extensive conformational plasticity throughout the catalytic cycle. Journal of Molecular Biology, 351, 170–181.
   PubMed Web of Science ®Google Scholar
• Keough, D. T., Hocková, D., Holy, A., Naesens, L. M., Skinner-Adams, T. S., Jersey, J. d., & Guddat, L. W. (2009). Inhibition of hypoxanthine-guanine phosphoribosyltransferase by acyclic nucleoside phosphonates: a new class of antimalarial therapeutics. Journal of Medicinal Chemistry, 52, 4391–4399.
   PubMed Web of Science ®Google Scholar
• Keough, D. T., Špaček, P., Hocková, D., Tichy, T., Vrbková, Slavětínská, L., ... Guddat, L. (2013). Acyclic nucleoside phosphonates containing a second phosphonate group are potent inhibitors of 6-oxopurine phosphoribosyltransferases and have antimalarial activity. Journal of Medicinal Chemistry, 56, 2513–2526.
   PubMed Web of Science ®Google Scholar
• Kidera, A., & Gō, N. (1992). Normal mode refinement: Crystallographic refinement of protein dynamic structure: I. Theory and test by simulated diffraction data. Journal of Molecular Biology, 225, 457–475.
   PubMed Web of Science ®Google Scholar
• Kidera, A., Inaka, K., Matsushima, M., & Gō, N. (1992). Normal mode refinement: Crystallographic refinement of protein dynamic structure: II. Application to human lysozyme. Journal of Molecular Biology, 225, 477–486.
   PubMed Web of Science ®Google Scholar
• Knaggs, M. H., Salsbury, F. R., Edgell, M. H., & Fetrow, J. S. (2007). Insights into correlated motions and long-range interactions in chey derived from molecular dynamics simulations. Biophysical Journal, 92, 2062–2079.
   PubMed Web of Science ®Google Scholar
• Krissinel, E., & Henrick, K. (2005). Detection of protein assemblies in crystals. Computational Life Sciences , 3695, 163–174.
   Google Scholar
• Lee, Y., Jeong, L. S., Choi, S., & Hyeon, C. (2011). Link between allosteric signal transduction and functional dynamics in a multisubunit enzyme: Sadenosylhomocysteine hydrolase. Journal of the American Chemical Society, 133, 19807–19815.
   PubMed Web of Science ®Google Scholar
• Lindorff-Larsen, K., Piana, S., Palmo, K., Maragakis, P., Klepeis, J. L., Dror, R. O., & Shaw, D. E. (2010). Improved side-chain torsion potentials for the amber ff99sb protein force field. Proteins Structure Function and Bioinformatics, 78, 1950–1958.
   PubMed Web of Science ®Google Scholar
• Marianayagam, N. J., Sunde, M., & Matthews, J. M. (2004). The power of two: protein dimerization in biology. Trends in Biochemical Sciences, 29, 618–625.
   PubMed Web of Science ®Google Scholar
• Matsuoka, D., Sugiyama, S., Murata, M., & Matsuoka, S. (2015). Molecular dynamics simulations of heart-type fatty acid-binding protein in apo and holo forms, and hydration structure analyses in the binding cavity. The Journal of Physical Chemistry B, 119, 114–127.
   PubMed Web of Science ®Google Scholar
• Moynié, L., Giraud, M.-F., Breton, A., Boissier, F., Daignan-Fornier, B., & Dautant, A. (2012). Functional significance of four successive glycine residues in the pyrophosphate binding loop of fungal 6-oxopurine phosphoribosyltransferases. Protein Science, 21, 1185–1196.
   PubMed Web of Science ®Google Scholar
• Munagala, N., Basus, V. J., & Wang, C. C. (2001). Role of the flexible loop of hypoxanthine-guanine-xanthine phosphoribosyltransferase from Tritrichomonas foetus in enzyme catalysis. Biochemistry, 40, 4303–4311.
   PubMed Web of Science ®Google Scholar
• Novak, B. R., Moldovan, D., Waldrop, G. L., & de Queiroz, M. S. (2011). Behavior of the atp grasp domain of biotin carboxylase monomers and dimers studied using molecular dynamics simulations. Proteins Structure Functions and Bioinformatics, 79, 622–632.
   PubMed Web of Science ®Google Scholar
• Perica, T., Kondo, Y., Tiwari, S. P., McLaughlin, S. H., Kemplen, K. R., Zhang, X., ... Teichmann, S. A. (2014). Evolution of oligomeric state through allosteric pathways that mimic ligand binding. Science, 346, 1254346.
   PubMed Web of Science ®Google Scholar
• Petruk, A. A., Labanda, M. S., Alvarez, R. M. & Marti, M. A. (2013). The allosteric modulation of thyroxine-binding globulin affinity is entropy driven. Biochimica et Biophysica Acta (BBA)-General Subjects, 1830, 3570–3577.
   PubMed Web of Science ®Google Scholar
• Pineda, J., Callender, R., & Schwartz, S. D. (2007). Ligand binding and protein dynamics in lactate dehydrogenase. Biophysical Journal, 93, 1474–1483.
   PubMed Web of Science ®Google Scholar
• Pitera, J. W., Munagala, N. R., Wang, C. C., & Kollman, P. A. (1999). Understanding substrate specificity in human and parasite phosphoribosyltransferases through calculation and experiment. Biochemistry, 38, 10298–10306.
   PubMed Web of Science ®Google Scholar
• Pronk, S., Páll, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., ... Lindahl, E. (2013). Gromacs 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics, 29, 845–854.
   PubMed Web of Science ®Google Scholar
• Roy, S. (2014). Understanding conformational dynamics and kinetic behaviour in plasmodium falciparum hypoxanthine guanine xanthine phosphoribosyltransferase,. Chapter 5 (PhD thesis). Jawaharlal Nehru Centre for Advanced Scientific Research, India.
   Google Scholar
• Roy, S., Karmakar, T., Rao, V. S. P., Nagappa, L. K., Balasubramanian, S., & Balaram, H. (2015). Slow ligand-induced conformational switch increases the catalytic rate in plasmodium falciparum hypoxanthine guanine xanthine phosphoribosyltransferase. Molecular Biosystems, 11, 1410–1424.
   PubMed Web of Science ®Google Scholar
• Schrödinger, L. (2010). The PyMOL molecular graphics system, version 1.3 r1, Py-MOL, The PyMOL Molecular Graphics System, Version 1
   Google Scholar
• Schulz, R., & Kleinekathöfer, U. (2009). Transitions between closed and open conformations of tolc: The effects of ions in simulations. Biophysical Journal, 96, 3116–3125.
   PubMed Web of Science ®Google Scholar
• Seamon, K. J., Hansen, E. C., Kadina, A. P., Kashemirov, B. A., McKenna, C. E., Bumpus, N. N., & Stivers, J. T. (2014). Small molecule inhibition of samhd1 dntpase by tetramer destabilization. Journal of the American Chemical Society, 136, 9822–9825.
   PubMed Web of Science ®Google Scholar
• Shi, W., Li, C. M., Tyler, P. C., Furneaux, R. H., Cahill, S. M., Girvin, M. E., & Almo, S. C. (1999a). The 2.0 A structure of a malarial purine phosphoribosyltransferase in complex with a transition-state analogue inhibitor. Biochemistry, 38, 9872–9880.
   PubMed Web of Science ®Google Scholar
• Shi, W., Li, C. M., Tyler, P. C., Furneaux, R. H., Cahill, S. M., Girvin, M. E., & Almo, S. C. (1999b). The 2.0 Å structure of human hypoxanthine-guanine phosphoribosyltransferase in complex with a transition-state analog inhibitor. Nature Structural & Molecular Biology, 6, 588–593.
   Web of Science ®Google Scholar
• Subbayya, I. & Balaram, H. (2002). A point mutation at the subunit interface of hypoxanthine-guanine-xanthine phosphoribosyltransferase impairs activity: Role of oligomerization in catalysis. FEBS Letter, 521, 72–76.
   PubMed Web of Science ®Google Scholar
• Thomas, A. & Field, M. J. (2002). Reaction mechanism of the HGXPRTase from plasmodium falciparum: A hybrid potential quantum mechanical/molecular mechanical study. Journal of the American Chemical Society, 124, 12432–12438.
   PubMed Web of Science ®Google Scholar
• Thomas, A. & Field, M. J. (2006). A comparative QM/MM simulation study of the reaction mechanisms of human and plasmodium falciparum HG(X)PRTases. Journal of the American Chemical Society, 128, 10096–10102.
   PubMed Web of Science ®Google Scholar
• Vanquelef, E., Simon, S., Marquant, G., Garcia, E., Klimerak, G., Delepine, J. C., ... Dupradeau, F.-Y. (2011). Red server: A web service for deriving RESP and ESP charges and building force field libraries for new molecules and molecular fragments. Nucleic Acids Research, 39, W511–W517.
   PubMed Web of Science ®Google Scholar
• Vehlow, C., Stehr, H., Winkelmann, M., Duarte, J. M., Petzold, L., Dinse, J., & Lappe, M. (2011). CMView: Interactive contact map visualization and analysis. Bioinformatics, 27, 1573–1574.
   PubMed Web of Science ®Google Scholar
• von Grafenstein, S., Wallnoefer, H. G., Kirchmair, J., Fuchs, J. E., Huber, R. G., Schmidtke, M., ... Liedl, K. R. (2015). Interface dynamics explain assembly dependency of influenza neuraminidase catalytic activity. Journal of Biomolecular Structure and Dynamics, 33, 104–120.
   PubMed Web of Science ®Google Scholar
• Vos, S., de Jersey, J., & Martin, J. L. (1997). Crystal structure of Escherichia coli xanthine phosphoribosyltransferase. Biochemistry, 36, 4125–4134.
   PubMed Web of Science ®Google Scholar
• Vos, S., Parry, R. J., Burns, M. R., de Jersey, J., & Martin, J. L. (1998). Structures of free and complexed forms of Escherichia coli xanthine-guanine phosphoribosyltransferase. Journal of Molecular Biology, 282, 875–889.
   PubMed Web of Science ®Google Scholar
• Wallnoefer, H. G., Lingott, T., Gutirrez, J. M., Merfort, I., & Liedl, K. R. (2010). Backbone flexibility controls the activity and specificity of a protein-protein interface: Specificity in snake venom metalloproteases. Journal of the American Chemical Society, 132, 10330–10337.
   PubMed Web of Science ®Google Scholar
• Wang, F., Shi, W., Nieves, E., Angeletti, R. H., Schramm, V. L., & Grubmeyer, C. (2001). A transition-state analogue reduces protein dynamics in hypoxanthine-guanine phosphoribosyltransferase. Biochemistry, 40, 8043–8054.
   PubMed Web of Science ®Google Scholar
• Xu, W., Ping, J., Li, W., & Mu, Y. (2009). Assembly dynamics of two- sheets revealed by molecular dynamics simulations. Journal of Chemical Physics, 130, 164709.
   PubMed Web of Science ®Google Scholar
• Xu, X. L. & Grant, G. A. (2014). Regulation of mycobacterium tuberculosis d3-phosphoglycerate dehydrogenase by phosphate-modulated quaternary structure dynamics and a potential role for polyphosphate in enzyme regulation. Biochemistry, 53, 4239–4249.
   PubMed Web of Science ®Google Scholar
• Yamada, K., Ishikawa, H., Mizuno, M., Shibayama, N., & Mizutani, Y. (2013). Intersubunit communication via changes in hemoglobin quaternary structures revealed by time-resolved resonance raman spectroscopy: Direct observation of the perutz mechanism. The Journal of Physical Chemistry B, 117, 12461–12468.
   PubMed Web of Science ®Google Scholar
• Zhang, P., Smith-Nguyen, E. V., Keshwani, M. M., Deal, M. S., Kornev, A. P., & Taylor, S. S. (2012). Structure and allostery of the PKA RII tetrameric holoenzyme. Science, 335, 712–716.
   PubMed Web of Science ®Google Scholar