Unraveling the conformational dynamics of glycerol 3-phosphate dehydrogenase, a nicotinamide adenine dinucleotide-dependent enzyme of Leishmania mexicana

References

• Ahmad, E., Rabbani, G., Zaidi, N., Khan, M. A., Qadeer, A., Ishtikhar, M., Singh, S., Khan, R. H. (2013). Revisiting ligand-induced conformational changes in proteins: Essence, advancements, implications and future challenges. Journal of Biomolecular Structure and Dynamics, 31(6), 630–648. doi:10.1080/07391102.2012.706081
   PubMed Web of Science ®Google Scholar
• Alarcon, D. A., Nandi, M., Carpena, X., Fita, I., & Loewen, P. C. (2012). Structure of glycerol-3-phosphate dehydrogenase (GPD1) from Saccharomyces cerevisiae at 2.45 Å resolution. Acta Crystallographica Section F Structural Biology and Crystallization Communications, 68(11), 1279–1283. doi:10.1107/S1744309112037736
   PubMedGoogle Scholar
• Andersen, H. C. (1983). Rattle: A “velocity” version of the shake algorithm for molecular dynamics calculations. Journal of Computational Physics, 52(1), 24–34. doi:10.1016/0021-9991(83)90014-1
   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(40), 10269–10280. doi:10.1021/j100142a004
   Web of Science ®Google Scholar
• Belluti, F., Uliassi, E., Veronesi, G., Bergamini, C., Kaiser, M., Brun, R., Viola A., Fato R., Michels P. A., Krauth-Siegel R. L., Cavalli A., Bolognesi, M. L. (2014). Toward the development of dual-targeted glyceraldehyde-3-phosphate dehydrogenase/trypanothione reductase inhibitors against Trypanosoma brucei and Trypanosoma cruzi. ChemMedChem., 9(2), 371–382. doi:10.1002/cmdc.201300399
   PubMed Web of Science ®Google Scholar
• Brannigan, J. A., Smith, B. A., Yu, Z., Brzozowski, A. M., Hodgkinson, M. R., Maroof, A., Price, H. P., Meier, F., Leatherbarrow, R. J., Tate, E. W., Smith, D. F., Wilkinson, A. J. (2010). N-Myristoyltransferase from Leishmania donovani: Structural and functional characterisation of a potential drug target for visceral leishmaniasis. Journal of Molecular Biology, 396(4), 985–999. doi:10.1016/j.jmb.2009.12.032
   PubMed Web of Science ®Google Scholar
• Buurman, E. T., Laganas, V. A., Liu, C. F., & Manchester, J. I. (2012). Antimicrobial activity of adenine-based inhibitors of NAD + -dependent DNA ligase. ACS Medicinal Chemistry Letters, 3(8), 663–667. doi:10.1021/ml300169x
   PubMed Web of Science ®Google Scholar
• Câmara, A. S., & Horjales, E. (2018). Computer simulations reveal changes in the conformational space of the transcriptional regulator MosR upon the formation of a disulphide bond and in the collective motions that regulate its DNA-binding affinity. PLoS One, 13(2), e0192826. doi:10.1371/journal.pone.0192826
   PubMed Web of Science ®Google Scholar
• Carlson, H. A., & McCammon, J. A. (2000). Accommodating protein flexibility in computational drug design. Molecular Pharmacology, 57(2), 213–218. http://www.ncbi.nlm.nih.gov/pubmed/10648630
   PubMed Web of Science ®Google Scholar
• Case, D. A., Cheatham, T. E., Darden, T., Gohlke, H., Luo, R., Merz, K. M., Onufriev A., Simmerling C., Wang B., Woods, R. J. (2005). The amber biomolecular simulation programs. Journal of Computational Chemistry, 26(16), 1668–1688. doi:10.1002/jcc.20290
   PubMed Web of Science ®Google Scholar
• Chauhan, N., & Poddar, R. (2019). In silico pharmacophore modeling and simulation studies for searching potent antileishmanials targeted against Leishmania donovani nicotinamidase. Computational Biology and Chemistry, 83, 107150. doi:10.1016/j.compbiolchem.2019.107150
   PubMed Web of Science ®Google Scholar
• Choe, J., Guerra, D., Michels, P. A. M., & Hol, W. G. J. (2003). Leishmania mexicana glycerol-3-phosphate dehydrogenase showed conformational changes upon binding a bi-substrate adduct. Journal of Molecular Biology, 329(2), 335–349. doi:10.1016/S0022-2836(03)00421-2
   PubMed Web of Science ®Google Scholar
• Costa, C. H. S., Oliveira, A. R. S., dos Santos, A. M., da Costa, K. S., Lima, A. H. L. e., Alves, C. N., & Lameira, J. (2019). Computational study of conformational changes in human 3-hydroxy-3-methylglutaryl coenzyme reductase induced by substrate binding. Journal of Biomolecular Structure and Dynamics, 37(16), 4374–4383. doi:10.1080/07391102.2018.1549508
   PubMed Web of Science ®Google Scholar
• Cruz, M. C., Souza-Melo, N., da Silva, C. V., DaRocha, W. D., Bahia, D., Araújo, P. R., Teixeira, S. R., & Mortara, R. A. (2012). Trypanosoma cruzi: Role of δ-Amastin on extracellular amastigote cell invasion and differentiation. PLoS One., 7(12), e51804. doi:10.1371/journal.pone.0051804
   PubMed Web of Science ®Google Scholar
• Cui, Q., Sulea, T., Schrag, J. D., Munger, C., Hung, M.-N., Naïm, M., Cygler, M., & Purisima, E. O. (2008). Molecular dynamics—solvated interaction energy studies of protein–protein interactions: The MP1–p14 scaffolding complex. Journal of Molecular Biology, 379(4), 787–802. doi:10.1016/j.jmb.2008.04.035
   PubMed Web of Science ®Google Scholar
• da Costa, K. S., Galúcio, J. M. P., Leonardo, E. S., Cardoso, G., Leal, É., Conde, G., & Lameira, J. (2017). Structural and evolutionary analyses of Leishmania Alba proteins. Molecular and Biochemical Parasitology, 217, 23–31. doi:10.1016/j.molbiopara.2017.08.006
   PubMed Web of Science ®Google Scholar
• da Silva, M. F. L., Zampieri, R. A., Muxel, S. M., Beverley, S. M., & Floeter-Winter, L. M. (2012). Leishmania amazonensis arginase compartmentalization in the glycosome is important for parasite infectivity. PLoS One., 7(3), e34022. doi:10.1371/journal.pone.0034022
   PubMed Web of Science ®Google Scholar
• De Oliveira, O. V., Dos Santos, J. D., & Freitas, L. C. G. (2012). Molecular dynamics simulation of the gGAPDH-NAD + complex from Trypanosoma cruzi. Molecular Simulation, 38(13), 1124–1131. doi:10.1080/08927022.2012.696112
   Web of Science ®Google Scholar
• Felczak, K., Vince, R., & Pankiewicz, K. W. (2014). NAD-based inhibitors with anticancer potential. Bioorganic & Medicinal Chemistry Letters, 24(1), 332–336. doi:10.1016/j.bmcl.2013.11.005
   PubMed Web of Science ®Google Scholar
• Frisch, M. J., et al. (2009). Gaussian 09. Gaussian, Inc. Gaussian Inc. https://doi.org/111
   Google Scholar
• Gabaldón, T., Ginger, M. L., & Michels, P. A. M. (2016). Peroxisomes in parasitic protists. Molecular and Biochemical Parasitology, 209(1-2), 35–45. doi:10.1016/j.molbiopara.2016.02.005
   PubMed Web of Science ®Google Scholar
• Genheden, S., & Ryde, U. (2015). The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities. Expert Opinion on Drug Discovery, 10(5), 449–461. doi:10.1517/17460441.2015.1032936
   PubMed Web of Science ®Google Scholar
• Gerwert, K., Freier, E., & Wolf, S. (2014). The role of protein-bound water molecules in microbial rhodopsins. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1837(5), 606–613. doi:10.1016/j.bbabio.2013.09.006
   PubMed Web of Science ®Google Scholar
• Giangreco, I., & Packer, M. J. (2013). Pharmacophore binding motifs for nicotinamide adenine dinucleotide analogues across multiple protein families: A detailed contact-based analysis of the interaction between proteins and NAD(P) cofactors. Journal of Medicinal Chemistry, 56(15), 6175–6189. doi:10.1021/jm400644z
   PubMed Web of Science ®Google Scholar
• Grant, B. J., Rodrigues, A. P. C., ElSawy, K. M., McCammon, J. A., & Caves, L. S. D. (2006). Bio3d: An R package for the comparative analysis of protein structures. Bioinformatics, 22(21), 2695–2696. doi:10.1093/bioinformatics/btl461
   PubMed Web of Science ®Google Scholar
• He, R., Reyes, A. C., Amyes, T. L., & Richard, J. P. (2018). Enzyme architecture: The role of a flexible loop in activation of glycerol-3-phosphate dehydrogenase for catalysis of hydride transfer. Biochemistry, 57(23), 3227–3236. doi:10.1021/acs.biochem.7b01282
   PubMed Web of Science ®Google Scholar
• Hestenes, M. R., & Stiefel, E. (1952). Methods of conjugate gradients for solving linear systems. Journal of Research of the National Bureau of Standards, 49(6), 409. doi:10.6028/jres.049.044
   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(3), 712–725. doi:10.1002/prot.21123
   PubMed Web of Science ®Google Scholar
• Hou, T., Wang, J., Li, Y., & Wang, W. (2011). Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations. Journal of Chemical Information and Modeling, 51(1), 69–82. doi:10.1021/ci100275a
   PubMed Web of Science ®Google Scholar
• Jorgensen, W. L., Maxwell, D. S., & Tirado-Rives, J. (1996). Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. Journal of the American Chemical Society, 118(45), 11225–11236. doi:10.1021/ja9621760
   Web of Science ®Google Scholar
• Khan, M. O. F. (2007). Trypanothione reductase: A viable chemotherapeutic target for antitrypanosomal and antileishmanial drug design. Drug Target Insights, 2, 117739280700200. doi:10.1177/117739280700200007
   Google Scholar
• Knight, J. D. R., Hamelberg, D., McCammon, J. A., & Kothary, R. (2009). The role of conserved water molecules in the catalytic domain of protein kinases. Proteins: Structure, Function, and Bioinformatics, 76(3), 527–535. doi:10.1002/prot.22451
   PubMed Web of Science ®Google Scholar
• Kovářová, J., & Barrett, M. P. (2016). The pentose phosphate pathway in parasitic trypanosomatids. Trends in Parasitology, 32(8), 622–634. doi:10.1016/j.pt.2016.04.010
   PubMed Web of Science ®Google Scholar
• Kumari, P., & Poddar, R. (2019). A comparative multivariate analysis of nitrilase enzymes: An ensemble based computational approach. Computational Biology and Chemistry, 83, 107095. doi:10.1016/j.compbiolchem.2019.107095
   PubMed Web of Science ®Google Scholar
• Mandal, H., Vijayakumar, S., Yadav, S., Kumar Singh, S., & Das, P. (2019). Validation of NAD synthase inhibitors for inhibiting the cell viability of Leishmania donovani: In silico and in vitro approach. Journal of Biomolecular Structure and Dynamics, 37, 4481–4493. doi:10.1080/07391102.2018.1552199
   PubMed Web of Science ®Google Scholar
• Maugeri, D. A., Cazzulo, J. J., Burchmore, R. J. S., Barrett, M. P., & Ogbunude, P. O. J. (2003). Pentose phosphate metabolism in Leishmania mexicana. Molecular and Biochemical Parasitology, 130(2), 117–125. doi:10.1016/S0166-6851(03)00173-7
   PubMed Web of Science ®Google Scholar
• Moreno, M. A., Alonso, A., Alcolea, P. J., Abramov, A., de Lacoba, M. G., Abendroth, J., Zhang, S., Edwards, T., Lorimer, D., Myler, P. J., Larraga, V. (2014). Tyrosine aminotransferase from Leishmania infantum: A new drug target candidate. International Journal for Parasitology: Drugs and Drug Resistance, 4(3), 347–354. doi:10.1016/j.ijpddr.2014.06.001
   PubMed Web of Science ®Google Scholar
• Naderer, T., Heng, J., & McConville, M. J. (2010). Evidence that intracellular stages of Leishmania major utilize amino sugars as a major carbon source. PLoS Pathogens, 6(12), e1001245. doi:10.1371/journal.ppat.1001245
   PubMed Web of Science ®Google Scholar
• Nagle A. S., Khare S., Kumar A. B., Supek F., Buchynskyy A., Mathison C. J., Chennamaneni N. K., Pendem N., Buckner F. S., Gelb M. H., Molteni V. (2014). Recent developments in drug discovery for leishmaniasis and human African trypanosomiasis. Chemical Reviews, 114(22), 11305–11347. doi:10.1021/cr500365f
   PubMed Web of Science ®Google Scholar
• Naïm, M., Bhat, S., Rankin, K. N., Dennis, S., Chowdhury, S. F., Siddiqi, I., Drabik, P., Sulea, T., Bayly, C. I., Jakalian, A., & Purisima, E. O. (2007). Solvated Interaction Energy (SIE) for scoring protein-ligand binding affinities. 1. Exploring the parameter space. Journal of Chemical Information and Modeling, 47(1), 122–133. doi:10.1021/ci600406v
   PubMed Web of Science ®Google Scholar
• Neves Cruz, J., da Costa, K. S., de Carvalho, T. A. A., & de Alencar, N. A. N. (2020). Measuring the structural impact of mutations on cytochrome P450 21A2, the major steroid 21-hydroxylase related to congenital adrenal hyperplasia. Journal of Biomolecular Structure and Dynamics, 38, 1425-1434. doi:10.1080/07391102.2019.1607560
   PubMed Web of Science ®Google Scholar
• Ogungbe, I. V., Erwin, W. R., & Setzer, W. N. (2014). Antileishmanial phytochemical phenolics: Molecular docking to potential protein targets. Journal of Molecular Graphics and Modelling, 48, 105–117. doi:10.1016/j.jmgm.2013.12.010
   PubMed Web of Science ®Google Scholar
• Ogungbe, I. V., & Setzer, W. N. (2013). In-silico Leishmania target selectivity of antiparasitic terpenoids. Molecules, 18(7), 7761–7847. doi:10.3390/molecules18077761
   PubMed Web of Science ®Google Scholar
• Ou, X., Ji, C., Han, X., Zhao, X., Li, X., Mao, Y., Wong, L.-L., Bartlam, M., & Rao, Z. (2006). Crystal structures of human glycerol 3-phosphate dehydrogenase 1 (GPD1). Journal of Molecular Biology, 357(3), 858–869. doi:10.1016/j.jmb.2005.12.074
   PubMed Web of Science ®Google Scholar
• Passalacqua, T. G., Torres, F. A. E., Nogueira, C. T., de Almeida, L., Del Cistia, M. L., dos Santos, M. B., Dutra L. A., Bolzani V.S., Regasini L.O., Graminha M.A., Marchetto R., Zottis, A. (2015). The 2′,4′-dihydroxychalcone could be explored to develop new inhibitors against the glycerol-3-phosphate dehydrogenase from Leishmania species. Bioorganic & Medicinal Chemistry Letters, 25(17), 3564–3568. doi:10.1016/j.bmcl.2015.06.085
   PubMed Web of Science ®Google Scholar
• Rackham, M. D., Yu, Z., Brannigan, J. A., Heal, W. P., Paape, D., Barker, K. V., Wilkinson, A. J., Smith, D. F., Leatherbarrow, R. J., & Tate, E. W. (2015). Discovery of high affinity inhibitors of Leishmania donovani N-myristoyltransferase. MedChemComm, 6(10), 1761–1766. doi:10.1039/C5MD00241A
   PubMed Web of Science ®Google Scholar
• Reguer, R. M., Elmahallaw, E. K., Garcia-Estrada, C., Carbajo-Andres, R., & Balana-Fouce, R. (2018). DNA Topoisomerases of Leishmania parasites; druggable targets for drug discovery. Current Medicinal Chemistry, 26(32), 5900-5923. doi:10.2174/0929867325666180518074959
   Web of Science ®Google Scholar
• Reyes, A. C., Amyes, T. L., & Richard, J. P. (2016a). Enzyme architecture: A startling role for Asn270 in glycerol 3-phosphate dehydrogenase-catalyzed hydride transfer. Biochemistry, 55(10), 1429–1432. doi:10.1021/acs.biochem.6b00116
   PubMed Web of Science ®Google Scholar
• Reyes, A. C., Amyes, T. L., & Richard, J. P. (2016b). Enzyme architecture: Self-assembly of enzyme and substrate pieces of glycerol-3-phosphate dehydrogenase into a robust catalyst of hydride transfer. Journal of the American Chemical Society, 138(46), 15251–15259. doi:10.1021/jacs.6b09936
   PubMed Web of Science ®Google Scholar
• Ronin, C., Costa, D. M., Tavares, J., Faria, J., Ciesielski, F., Ciapetti, P., Smith, T. K., MacDougall, J., Cordeiro-da-Silva, A., & Pemberton, I. K. (2018). The crystal structure of the Leishmania infantum silent information regulator 2 related protein 1: Implications to protein function and drug design. PLoS One, 13(3), e0193602. doi:10.1371/journal.pone.0193602
   PubMed Web of Science ®Google Scholar
• Sahoo, G. C., Dikhit, M. R., Rani, M., Ansari, M. Y., Jha, C., Rana, S., & Das, P. (2013). Analysis of sequence, structure of GAPDH of Leishmania donovani and its interactions. Journal of Biomolecular Structure and Dynamics, 31(3), 258–275. doi:10.1080/07391102.2012.698189
   PubMed Web of Science ®Google Scholar
• Sittel, F., Jain, A., & Stock, G. (2014). Principal component analysis of molecular dynamics: On the use of Cartesian vs. internal coordinates. The Journal of Chemical Physics, 141(1), 014111. doi:10.1063/1.4885338
   PubMed Web of Science ®Google Scholar
• Škodová, I., Verner, Z., Bringaud, F., Fabian, P., Lukeš, J., & Horváth, A. (2013). Characterization of Two Mitochondrial Flavin Adenine Dinucleotide-Dependent Glycerol-3-Phosphate Dehydrogenases in Trypanosoma brucei. Eukaryotic Cell, 12(12), 1664–1673. doi:10.1128/EC.00152-13
   PubMedGoogle Scholar
• Suresh, S., Bressi, J. C., Kennedy, K. J., Verlinde, C. L. M. J., Gelb, M. H., & Hol, W. G. J. (2001). Conformational changes in Leishmania mexicana glyceraldehyde-3-phosphate dehydrogenase induced by designed inhibitors. Journal of Molecular Biology, 309(2), 423–435. doi:10.1006/jmbi.2001.4588
   PubMed Web of Science ®Google Scholar
• Suresh, S., Turley, S., Opperdoes, F. R., Michels, P. A. M., & Hol, W. G. J. (2000). A potential target enzyme for trypanocidal drugs revealed by the crystal structure of NAD-dependent glycerol-3-phosphate dehydrogenase from Leishmania mexicana. Structure, 8(5), 541–552. doi:10.1016/S0969-2126(00)00135-0
   PubMed Web of Science ®Google Scholar
• Szöör, B., Haanstra, J. R., Gualdrón-López, M., & Michels, P. A. (2014). Evolution, dynamics and specialized functions of glycosomes in metabolism and development of trypanosomatids. Current Opinion in Microbiology, 22, 79–87. doi:10.1016/j.mib.2014.09.006
   PubMed Web of Science ®Google Scholar
• Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., & Case, D. A. (2004). Development and testing of a general amber force field. Journal of Computational Chemistry, 25(9), 1157–1174. doi:10.1002/jcc.20035
   PubMed Web of Science ®Google Scholar
• Zhao, B., Guengerich, F. P., Voehler, M., & Waterman, M. R. (2005). Role of active site water molecules and substrate hydroxyl groups in oxygen activation by cytochrome P450 158A2. Journal of Biological Chemistry, 280(51), 42188–42197. doi:10.1074/jbc.M509220200
   PubMed Web of Science ®Google Scholar
• Zhao, Y., Li, X., Wang, F., Zhao, X., Gao, Y., Zhao, C., He, L., Li, Z., & Xu, J. (2018). Glycerol-3-phosphate dehydrogenase (GPDH) gene family in Zea mays L.: Identification, subcellular localization, and transcriptional responses to abiotic stresses. PLoS One, 13(7), e0200357. doi:10.1371/journal.pone.0200357
   PubMed Web of Science ®Google Scholar