In-silico profiling and structural insights into the impact of nSNPs in the P. falciparum acetyl-CoA transporter gene to understand the mechanism of drug resistance in malaria

References

• Abdul Samad, F., Suliman, B. A., Basha, S. H., Manivasagam, T., & Essa, M. M. (2016). A comprehensive in silico analysis on the structural and functional impact of SNPs in the congenital heart defects associated with NKX2-5 Gene-A molecular dynamic simulation approach. PloS One, 11(5), e0153999. doi:10.1371/journal.pone.0153999
   PubMed Web of Science ®Google Scholar
• Adzhubei, I., Jordan, D. M., & Sunyaev, S. R. (2013). Predicting functional effect of human missense mutations using PolyPhen-2. Current Protocols in Human Genetics, 76(1), 7.20.1–7.20.41. Unit 7.20. doi:10.1002/0471142905.hg0720s76
   Google Scholar
• Ahamad, S., Hassan, M. I., & Dwivedi, N. (2018). Designing of phenol-based β − carbonic anhydrase1 inhibitors through QSAR, molecular docking, and MD simulation approach. 3 Biotech, 8(5), 256. doi:10.1007/s13205-018-1278-z
   PubMedGoogle Scholar
• Amir, M., Ahmad, S., Ahamad, S., Kumar, V., Mohammad, T., Dohare, R., … Hassan, M. I. (2019). Impact of Gln94Glu mutation on the structure and function of protection of telomere 1, a cause of cutaneous familial melanoma. Journal of Biomolecular Structure and Dynamics, 37, 1–11. doi:10.1080/07391102.2019.1610500
   PubMed Web of Science ®Google Scholar
• Bahl, A., Brunk, B., Crabtree, J., Fraunholz, M. J., Gajria, B., Grant, G. R., … Whetzel, P. (2003). PlasmoDB: The Plasmodium genome resource. A database integrating experimental and computational data. Nucleic Acids Research, 31(1), 212–215. doi:10.1093/nar/gkg081
   PubMed Web of Science ®Google Scholar
• Basore, K., Cheng, Y., Kushwaha, A. K., Nguyen, S. T., & Desai, S. A. (2015). How do antimalarial drugs reach their intracellular targets? Frontiers in Pharmacology, 6, 91. doi:10.3389/fphar.2015.00091
   PubMed Web of Science ®Google Scholar
• Bendl, J., Stourac, J., Salanda, O., Pavelka, A., Wieben, E. D., Zendulka, J., … Damborsky, J. (2014). PredictSNP: Robust and accurate consensus classifier for prediction of disease-related mutations. PLoS Computational Biology, 10(1), e1003440. doi:10.1371/journal.pcbi.1003440
   PubMed Web of Science ®Google Scholar
• Berendsen, H. J. C., Postma, J. P. M., Van Gunsteren, W. F., Dinola, A., & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81(8), 3684–3690. doi:10.1063/1.448118
   Web of Science ®Google Scholar
• Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., & Hermans, J. (1981). Interaction models for water in relation to protein hydration. In Intermolecular forces (pp. 331–342). Dordrecht: Springer. Retrieved from 10.1007/978-94-015-7658-1_21
   Google Scholar
• Blasco, B., Leroy, D., & Fidock, D. A. (2017). Antimalarial drug resistance: Linking Plasmodium falciparum parasite biology to the clinic. Nature Medicine, 23(8), 917–928. doi:10.1038/nm.4381
   PubMed Web of Science ®Google Scholar
• Capriotti, E., Fariselli, P., & Casadio, R. (2005). I-Mutant2.0: Predicting stability changes upon mutation from the protein sequence or structure. Nucleic Acids Research, 33(Web Server issue), W306–W310. doi:10.1093/nar/gki375
   PubMed Web of Science ®Google Scholar
• Cheng, J., Randall, A., & Baldi, P. (2006). Prediction of protein stability changes for single-site mutations using support vector machines. Proteins: Structure, Function, and Bioinformatics 62(4), 1125–1132. Retrieved from. doi:10.1002/prot.20810
   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. doi:10.1063/1.464397
   Web of Science ®Google Scholar
• Dobson, P., Lanthaler, K., Oliver, S., & Kell, D. (2009). Implications of the dominant role of transporters in drug uptake by cells (supplementary material). Current Topics in Medicinal Chemistry, 9(2), 163–181. doi:10.2174/156802609787521616
   PubMed Web of Science ®Google Scholar
• Ehrnstorfer, I. A., Manatschal, C., Arnold, F. M., Laederach, J., & Dutzler, R. (2017). Structural and mechanistic basis of proton-coupled metal ion transport in the SLC11/NRAMP family. Nature Communications, 8(1), 14033. doi:10.1038/ncomms14033
   PubMed Web of Science ®Google Scholar
• Gomes, A. R., Ravenhall, M., Benavente, E. D., Talman, A., Sutherland, C., Roper, C., … Campino, S. (2017). Genetic diversity of next generation antimalarial targets: A baseline for drug resistance surveillance programmes. International Journal for Parasitology: Drugs and Drug Resistance, 7(2), 174–180. doi:10.1016/j.ijpddr.2017.03.001
   PubMed Web of Science ®Google Scholar
• Gómez-Díaz, E., Yerbanga, R. S., Lefèvre, T., Cohuet, A., Rowley, M. J., Ouedraogo, J. B., & Corces, V. G. (2017). Epigenetic regulation of Plasmodium falciparum clonally variant gene expression during development in Anopheles gambiae. Scientific Reports, 7(1), 40655. doi:10.1038/srep40655
   PubMed Web of Science ®Google Scholar
• Hediger, M. A., Romero, M. F., Peng, J.-B., Rolfs, A., Takanaga, H., & Bruford, E. A. (2004). The ABCs of solute carriers: Physiological, pathological and therapeutic implications of human membrane transport proteinsIntroduction. Pflugers Archiv: European Journal of Physiology, 447(5), 465–468. doi:10.1007/s00424-003-1192-y
   PubMed Web of Science ®Google Scholar
• Hess, B., Bekker, H., Berendsen, H. J. C., & Fraaije, J. G. E. M. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18(12), 1463–1472. doi:10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H
   Web of Science ®Google Scholar
• Katyal, N., & Deep, S. (2014). Revisiting the conundrum of trehalose stabilization. Physical Chemistry Chemical Physics 16(48), 26746–26761. Retrieved from 10.1039/c4cp02914c.
   PubMed Web of Science ®Google Scholar
• Khare, S. D., & Dokholyan, N. V. (2006). Common dynamical signatures of familial amyotrophic lateral sclerosis-associated structurally diverse Cu, Zn superoxide dismutase mutants. Proceedings of the National Academy of Sciences of the United States of America, 103(9), 3147–3152. doi:10.1073/pnas.0511266103
   PubMed Web of Science ®Google Scholar
• Kirk, K. (2004). Channels and transporters as drug targets in the Plasmodium-infected erythrocyte. Acta Tropica, 89(3), 285–298. doi:10.1016/j.actatropica.2003.10.002
   PubMed Web of Science ®Google Scholar
• Knight, J. L., & Brooks, C. L. (2009). λ-dynamics free energy simulation methods. Journal of Computational Chemistry, 30(11), 1692–1700. doi:10.1002/jcc.21295
   PubMed Web of Science ®Google Scholar
• Krawczak, M., Ball, E. V., Fenton, I., Stenson, P. D., Abeysinghe, S., Thomas, N., & Cooper, D. N. (2000). Human gene mutation database-a biomedical information and research resource. Human Mutation, 15(1), 45–51. (SICI)1098-1004(200001)15:1 < 45::AID-HUMU10 > 3.0.CO;2-T doi:10.1002/(SICI)1098-1004(200001)15:1<45::AID-HUMU10>3.0.CO;2-T
   PubMed Web of Science ®Google Scholar
• Li, L., Vorobyov, I., & Allen, T. W. (2013). The different interactions of lysine and arginine side chains with lipid membranes. Journal of Physical Chemistry B 17(40), 11906–11920. Retrieved from 10.1021/jp405418y.
   Google Scholar
• Lim, M. Y.-X., LaMonte, G., Lee, M. C. S., Reimer, C., Tan, B. H., Corey, V., … Bifani, P. (2016). UDP-galactose and acetyl-CoA transporters as Plasmodium multidrug resistance genes. Nature Microbiology, 1 (12), 16166. Retrieved from. doi:10.1038/nmicrobiol.2016.166
   PubMed Web of Science ®Google Scholar
• Lovell, S. C., Davis, I. W., Arendall, W. B., de Bakker, P. I. W., Word, J. M., Prisant, M. G., … Richardson, D. C. (2003). Structure validation by C alpha geometry: Phi, psi and C beta deviation. Proteins: Structure, Function, and Bioinformatics, 50(3), 437–450. doi:10.1002/prot.10286
   PubMed Web of Science ®Google Scholar
• Matthews, C. R. (1987). Effect of point mutations of the folding of globular proteins. Methods in Enzymology, 154, 498–511. 10.1016/0076-6879.
   Google Scholar
• Molina, D. M., Jafari, R., Ignatushchenko, M., Seki, T., Larsson, E. A., Dan, C., … Nordlund, P. (2013). Monitoring drug target engagement in cells and tissues using the cellular thermal shift assay. Science, 341(6141), 84–87. doi:10.1126/science.1233606
   PubMed Web of Science ®Google Scholar
• Nagasundaram, N., Zhu, H., Liu, J., Karthick, V., George Priya Doss, C., Chakraborty, C., & Chen, L. (2015). Analysing the effect of mutation on protein function and discovering potential inhibitors of CDK4: Molecular modelling and dynamics studies. PLoS One 10(8), e0133969. doi:10.1371/journal.pone.0133969
   Google Scholar
• Ng, P. C., & Henikoff, S. (2003). SIFT: Predicting amino acid changes that affect protein function. Nucleic Acids Research, 31(13), 3812–3814. doi:10.1093/nar/gkg509
   PubMed Web of Science ®Google Scholar
• O’Boyle, N. M., Banck, M., James, C. A., Morley, C., Vandermeersch, T., & Hutchison, G. R. (2011). Open Babel: An open chemical toolbox. Journal of Cheminformatics, 3(1), 33. doi:10.1186/1758-2946-3-33
   Web of Science ®Google Scholar
• Pandey, S., Dhusia, K., Katara, P., Singh, S., & Gautam, B. (2019). An in-silico analysis of deleterious single nucleotide polymorphisms and molecular dynamics simulation of disease linked mutations in genes responsible for neurodegenerative disorder. Journal of Biomolecular Structure and Dynamics, 37, 1–14. doi:10.1080/07391102.2019.1682047
   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. doi:10.1063/1.328693
   Web of Science ®Google Scholar
• Pedersen, B. P., Kumar, H., Waight, A. B., Risenmay, A. J., Roe-Zurz, Z., Chau, B. H., … Stroud, R. M. (2013). Crystal structure of a eukaryotic phosphate transporter. Nature, 496(7446), 533–536. doi:10.1038/nature12042
   PubMed Web of Science ®Google Scholar
• Pejaver, V., Urresti, J., Lugo-Martinez, J., Pagel, K. A., Lin, G. N., Nam, H.-J., … Radivojac, P. (2017). MutPred2: Inferring the molecular and phenotypic impact of amino acid variants. BioRxiv, 134981. 10.1101/134981.
   Google Scholar
• Pillai, D. R., Lau, R., Khairnar, K., Lepore, R., Via, A., Staines, H. M., & Krishna, S. (2012). Artemether resistance in vitro is linked to mutations in PfATP6 that also interact with mutations in PfMDR1 in travellers returning with Plasmodium falciparum infections. Malaria Journal, 11(1), 131. doi:10.1186/1475-2875-11-131
   PubMed Web of Science ®Google Scholar
• Piovesan, D., Minervini, G., & Tosatto, S. C. E. (2016). The RING 2.0 web server for high quality residue interaction networks. Nucleic Acids Research, 44(W1), W367–74. doi:10.1093/nar/gkw315
   PubMed Web of Science ®Google Scholar
• Posch, H. A., Hoover, W. G., & Vesely, F. J. (1986). Canonical dynamics of the Nosé oscillator: Stability, order, and chaos. Physical Review A, 33(6), 4253–4265. doi:10.1103/PhysRevA.33.4253
   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(7), 845–854. doi:10.1093/bioinformatics/btt055
   PubMed Web of Science ®Google Scholar
• Rajendran, V., Purohit, R., & Sethumadhavan, R. (2012). In silico investigation of molecular mechanism of laminopathy caused by a point mutation (R482W) in lamin A/C protein. Amino Acids, 43(2), 603–615. doi:10.1007/s00726-011-1108-7
   PubMed Web of Science ®Google Scholar
• Rédei, G. P. (2008). Blast (basic local alignment search tool). Encyclopedia of Genetics, Genomics, Proteomics and Informatics (p. 221).
   Google Scholar
• Šali, A., & Blundell, T. L.(1993). Comparative Protein Modelling by Satisfaction of Spatial Restraints. Journal of Molecular Biology, 234(3), 779–815. doi:10.1006/jmbi.1993.1626.
   PubMed Web of Science ®Google Scholar
• Santos, G., & Torres, N. V. (2013). New targets for drug discovery against malaria. PLoS One 8(3), e59968. doi:10.1371/journal.pone.0059968
   Google Scholar
• Schmidt, T. H., & Kandt, C. (2012). LAMBADA and InflateGRO2: Efficient membrane alignment and insertion of membrane proteins for molecular dynamics simulations. Journal of Chemical Information and Modeling, 52(10), 2657–2669. doi:10.1021/ci3000453
   PubMed Web of Science ®Google Scholar
• Sherlach, K. S., & Roepe, P. D. (2014). Drug resistance associated membrane proteins. Frontiers in Physiology, 5, 108. doi:10.3389/fphys.2014.00108
   PubMed Web of Science ®Google Scholar
• Thomas, P. D., Campbell, M. J., Kejariwal, A., Mi, H., Karlak, B., Daverman, R., … Narechania, A. (2003). PANTHER: A library of protein families and subfamilies indexed by function. Genome Research, 13(9), 2129–2141. doi:10.1101/gr.772403
   PubMed Web of Science ®Google Scholar
• Trott, O., & Olson, A. J. (2010). AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry, 31(2), 455–461. doi:10.1002/jcc.21334
   PubMed Web of Science ®Google Scholar
• Tse, M. T. (2010). Antimalarial drugs: A treasure trove of potential antimalarials. Nature Reviews Drug Discovery, 9(7), 516–517. doi:10.1038/nrd3209
   PubMed Web of Science ®Google Scholar
• Viereck, M., Gaulton, D. D., & Vienna, A. (2017). Insights into transporter classifications: An outline of transporters as drug targets. Retrieved from https://application.wiley-vch.de/books/sample/3527333843_c01.pdf
   Google Scholar
• Waingeh, V. F., Groves, A. T., & Eberle, J. A. (2013). Binding of quinoline-based inhibitors to Plasmodium falciparum lactate dehydrogenase: A molecular docking study. Open Journal of Biophysics 3(04), 285. doi:10.4236/ojbiphy.2013.34034
   PubMedGoogle Scholar
• Wijsman, E. M. (2012). The role of large pedigrees in an era of high-throughput sequencing. Human Genetics, 131(10), 1555–1563. doi:10.1007/s00439-012-1190-2
   PubMed Web of Science ®Google Scholar
• Wilkins, M. R., Gasteiger, E., Bairoch, A., Sanchez, J. C., Williams, K. L., Appel, R. D., & Hochstrasser, D. F. (1999). Protein identification and analysis tools in the ExPASy server. Methods in Molecular Biology (Clifton, N.J.), 571–607.
   Google Scholar
• Wimley, W. C., & White, S. H. (1996). Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nature Structural & Molecular Biology, 3(10), 842–848. doi:10.1038/nsb1096-842
   Web of Science ®Google Scholar
• World Health Organization. (2015). World Malaria Report 2015 - Summary. World Health Organization. Retrieved from https://www.who.int/malaria/publications/world-malaria-report-2015/report/en/
   Google Scholar
• Yang, J., & Zhang, Y. (2015). Protein structure and function prediction using I-TASSER. Current Protocols in Bioinformatics, 52(1), 1–15. doi:10.1002/0471250953.bi0508s52
   PubMedGoogle Scholar
• Yuan, Y. X. (2006). A new stepsize for the steepest descent method. Journal of Computational Mathematics 24(2), 149–156.
   Google Scholar
• Zhang, Y. (2008). I-TASSER server for protein 3D structure prediction. BMC Bioinformatics, 9(1), 40. doi:10.1186/1471-2105-9-40
   PubMed Web of Science ®Google Scholar