How do the mutations in PfK13 protein promote anti-malarial drug resistance?

References

• Acosta-Tapia, N., Galindo, J. F., & Baldiris, R. (2020). Insights into the effect of lowe syndrome-causing mutation p. Asn591Lys of OCRL-1 through protein–protein interaction networks and molecular dynamics simulations. Journal of Chemical Information and Modeling, 60(2), 1019–1027.
   PubMed Web of Science ®Google Scholar
• Adams, J., Kelso, R., & Cooley, L. (2000). The kelch repeat superfamily of proteins: Propellers of cell function. Trends in Cell Biology, 10(1), 17–24.
   PubMed Web of Science ®Google Scholar
• Amaratunga, C., Witkowski, B., Khim, N., Menard, D., & Fairhurst, R. M. (2014). Artemisinin resistance in Plasmodium falciparum. The Lancet Infectious Diseases, 14(6), 449–450. https://doi.org/10.1016/S1473-3099(14)70777-7
   PubMedGoogle Scholar
• Anderson, T. J., Nair, S., McDew-White, M., Cheeseman, I. H., Nkhoma, S., Bilgic, F., McGready, R., Ashley, E., Pyae Phyo, A., White, N. J., & Nosten, F. (2017). Population parameters underlying an ongoing soft sweep in Southeast Asian malaria parasites. Molecular Biology and Evolution, 34, 131–144.
   PubMed Web of Science ®Google Scholar
• Appadurai, R., & Senapati, S. (2016). Dynamical network of HIV-1 protease mutants reveals the mechanism of drug resistance and unhindered activity. Biochemistry, 55(10), 1529–1540.
   PubMed Web of Science ®Google Scholar
• Ariey, F., Witkowski, B., Amaratunga, C., Beghain, J., Langlois, A. C., Khim, N., Kim, S., Duru, V., Bouchier, C., Ma, L., Lim, P., Leang, R., Duong, S., Sreng, S., Suon, S., Chuor, C. M., Bout, D. M., Ménard, S., Rogers, W. O., … Ménard, D. (2014). A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature, 505, 50–55.
   PubMed Web of Science ®Google Scholar
• Ashley, E. A., Dhorda, M., Fairhurst, R. M., Amaratunga, C., Lim, P., Suon, S., Sreng, S., Anderson, J. M., Mao, S., Sam, B., Sopha, C., Chuor, C. M., Nguon, C., Sovannaroth, S., Pukrittayakamee, S., Jittamala, P., Chotivanich, K., Chutasmit, K., Suchatsoonthorn, C., … White, N. J. (2014). Spread of artemisinin resistance in Plasmodium falciparum malaria. The New England Journal of Medicine, 371, 411–423.
   PubMed Web of Science ®Google Scholar
• Bhatt, A., & Ali, M. E. (2021). Understanding the role of R266K mutation in cystathionine β-synthase (CBS) enzyme: an in silico study. Journal of Biomolecular Structure and Dynamics, 1–9. https://doi.org/10.1080/07391102.2021.1975564
   Google Scholar
• Bingöl, E. N., Serçinoğlu, O., & Ozbek, P. (2021). Unraveling the allosteric communication mechanisms in T-cell receptor–peptide-loaded major histocompatibility complex dynamics using molecular dynamics simulations: An approach based on dynamic cross correlation maps and residue interaction energy calculations. Journal of Chemical Information and Modeling, 61(5), 2444–2453.
   PubMed Web of Science ®Google Scholar
• Bisht, A., Sharma, M., Sharma, S., Ali, M. E., & Panda, J. J. (2019). Carrier-free self-built aspirin nanorods as anti-aggregation agents towards alpha-crystallin-derived peptide aggregates: potential implications in non-invasive cataract therapy. Journal of Materials Chemistry B, 7(44), 6945–6954.
   PubMed Web of Science ®Google Scholar
• Canning, P., Cooper, C. D. O., Krojer, T., Murray, J. W., Pike, A. C. W., Chaikuad, A., Keates, T., Thangaratnarajah, C., Hojzan, V., Marsden, B. D., Gileadi, O., Knapp, S., von Delft, F., & Bullock, A. N. (2013). Structural basis for Cul3 protein assembly with the BTB-Kelch family of E3 ubiquitin ligases. Journal of Biological Chemistry, 288, 7803–7814.
   PubMed Web of Science ®Google Scholar
• Chen, H.-Y., & Chen, R.-H. (2016). Cullin 3 ubiquitin ligases in cancer biology: Functions and therapeutic implications. Frontiers in Oncology, 6, 113.
   PubMed Web of Science ®Google Scholar
• Coppée, R., Jeffares, D. C., Miteva, M. A., Sabbagh, A., & Clain, J. (2019). Comparative structural and evolutionary analyses predict functional sites in the artemisinin resistance malaria protein K13. Scientific Reports, 9, 1–17.
   PubMed Web of Science ®Google Scholar
• Dafalla, O. M., Alzahrani, M., Sahli, A., Al Helal, M. A., Alhazmi, M. M., Noureldin, E. M., Mohamed, W. S., Hamid, T. B., Abdelhaleem, A. A., Hobani, Y. A., Arif, O. A., Bokar, I. M., Hakami, A. M., & Eisa, Z. M. (2020). Kelch 13-propeller polymorphisms in Plasmodium falciparum from Jazan region, southwest Saudi Arabia. Malaria Journal, 19, 397.
   PubMedGoogle Scholar
• Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An Nlog (N) method for Ewald sums in large systems. Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/10.1063/1.464397
   Web of Science ®Google Scholar
• Das, S., Saha, B., Hati, A. K., & Roy, S. (2018). Evidence of artemisinin-resistant Plasmodium falciparum malaria in Eastern India. The New England Journal of Medicine, 379(20), 1962–1964.
   PubMed Web of Science ®Google Scholar
• DeLano, W. L. (2002). Pymol: An open-source molecular graphics tool. CCP4 Newsletter on Protein Crystallography, 40, 82–92.
   Google Scholar
• Dhorda, M., Amaratunga, C., & Dondorp, A. M. (2021). Artemisinin and multidrug-resistant Plasmodium falciparum – A threat for malaria control and elimination. Current Opinion in Infectious Diseases, 34(5), 432–439.
   PubMed Web of Science ®Google Scholar
• Dolinsky, T. J., Czodrowski, P., Li, H., Nielsen, J. E., Jensen, J. H., Klebe, G., & Baker, N. A. (2007). PDB2PQR: Expanding and upgrading automated preparation of biomolecular structures for molecular simulations. Nucleic Acids Research, 35(Web Server issue), W522–W525.
   PubMed Web of Science ®Google Scholar
• Dondorp, A. M., Fairhurst, R. M., Slutsker, L., Macarthur, J. R., Breman, J. G., Guerin, P. J., Wellems, T. E., Ringwald, P., Newman, R. D., & Plowe, C. V. (2011). The threat of artemisinin-resistant malaria. The New England Journal of Medicine, 365(12), 1073–1075.
   PubMed Web of Science ®Google Scholar
• Dondorp, A. M., Nosten, F., Yi, P., Das, D., Phyo, A. P., Tarning, J., Lwin, K. M., Ariey, F., Hanpithakpong, W., Lee, S. J., Ringwald, P., Silamut, K., Imwong, M., Chotivanich, K., Lim, P., Herdman, T., An, S. S., Yeung, S., Singhasivanon, P.,… White, N. J. (2009). Artemisinin resistance in Plasmodium falciparum malaria. The New England Journal of Medicine, 361, 455–467.
   PubMed Web of Science ®Google Scholar
• Fairhurst, R. M. (2015). Understanding artemisinin-resistant malaria: What a difference a year makes. Current Opinion in Infectious Diseases, 28(5), 417–425.
   PubMed Web of Science ®Google Scholar
• Fairhurst, R. M., & Dondorp, A. M. (2016). Artemisinin-resistant Plasmodium falciparum malaria. Microbiology Spectrum, 4, 4–3.
   Web of Science ®Google Scholar
• Fairhurst, R. M., Nayyar, G. M., Breman, J. G., Hallett, R., Vennerstrom, J. L., Duong, S., Ringwald, P., Wellems, T. E., Plowe, C. V., & Dondorp, A. M. (2012). Artemisinin-resistant malaria: Research challenges, opportunities, and public health implications. The American Journal of Tropical Medicine and Hygiene, 87(2), 231–241.
   PubMed Web of Science ®Google Scholar
• Geyer, R., Wee, S., Anderson, S., Yates, I. I. I., J., & Wolf, D. A. (2003). BTB/POZ domain proteins are putative substrate adaptors for cullin 3 ubiquitin ligases. Molecular Cell, 12(3), 783–790.
   PubMed Web of Science ®Google Scholar
• Ghorbal, M., Gorman, M., Macpherson, C. R., Martins, R. M., Scherf, A., & Lopez-Rubio, J.-J. (2014). Genome editing in the human malaria parasite Plasmodium falciparum using the CRISPR-Cas9 system. Nature Biotechnology, 32(8), 819–821.
   PubMed Web of Science ®Google Scholar
• Goga, N., Rzepiela, A., De Vries, A., Marrink, S., & Berendsen, H. (2012). Efficient algorithms for Langevin and DPD dynamics. Journal of Chemical Theory and Computation, 8(10), 3637–3649.
   PubMed Web of Science ®Google Scholar
• Grant, B. J., Rodrigues, A. P., ElSawy, K. M., McCammon, J. A., & Caves, L. S. (2006). Bio3d: An R package for the comparative analysis of protein structures. Bioinformatics, 22(21), 2695–2696. https://doi.org/10.1093/bioinformatics/btl461
   PubMed Web of Science ®Google Scholar
• Haldar, K., Bhattacharjee, S., & Safeukui, I. (2018). Drug resistance in Plasmodium. Nature Reviews Microbiology, 16(3), 156–170. https://doi.org/10.1038/nrmicro.2017.161
   PubMed Web of Science ®Google Scholar
• Hien, T. T., Thuy-Nhien, N. T., Phu, N. H., Boni, M. F., Thanh, N. V., Nha-Ca, N. T., Thai le, H., Thai, C. Q., Toi, P. V., Thuan, P. D., Long le, T., Dong le, T., Merson, L., Dolecek, C., Stepniewska, K., Ringwald, P., White, N. J., Farrar, J., & Wolbers, M. (2012). In vivo susceptibility of Plasmodium falciparum to artesunate in Binh Phuoc Province, Vietnam. Malaria Journal, 11, 355.
   PubMedGoogle Scholar
• Huang, F., Takala-Harrison, S., Jacob, C. G., Liu, H., Sun, X., Yang, H., Nyunt, M. M., Adams, M., Zhou, S., Xia, Z., Ringwald, P., Bustos, M. D., Tang, L., & Plowe, C. V. (2015). A single mutation in K13 predominates in southern China and is associated with delayed clearance of Plasmodium falciparum following artemisinin treatment. Journal of Infectious Diseases, 212, 1629–1635.
   PubMed Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38.
   PubMedGoogle Scholar
• Jiang, D. Q., Tempel, W., Loppnau, P., Gräslund, S., He, H., Ravichandran, M., Seitova, A., Arrowsmith, C. H., Edwards, A. M., Bountra, C., El Bakkouri, M. E., Senisterra, G. A., Osman, K. T., Lovato, D. V., Hui, R., Hutchinson, A., & Lin, Y. H. (2015a). Crystal structure analysis of Kelch protein from Plasmodium falciparum. https://doi.org/10.2210/pdb4YY8/pdb. https://www.rcsb.org/structure/4YY8 (accession no. 4YY8)
   Google Scholar
• Jiang, D. Q., Tempel, W., Loppnau, P., Gräslund, S., He, H., Ravichandran, M., Seitova, A., Arrowsmith, C. H., Edwards, A. M., Bountra, C., El Bakkouri, M. E., Senisterra, G. A., Osman, K. T., Lovato, D. V., Hui, R., Hutchinson, A., & Lin, Y. H. (2015b). Crystal structure analysis of Kelch protein (with disulfide bond) from Plasmodium falciparum. https://doi.org/10.2210/pdb4ZGC/pdb. https://www.rcsb.org/structure/4ZGC (accession no. 4ZGC)
   Google Scholar
• Kasahara, K., Fukuda, I., & Nakamura, H. (2014). A novel approach of dynamic cross correlation analysis on molecular dynamics simulations and its application to Ets1 dimer–DNA complex. PLoS One, 9(11), e112419. https://doi.org/10.1371/journal.pone.0112419
   PubMed Web of Science ®Google Scholar
• Keskin, O., Gursoy, A., Ma, B., & Nussinov, R. (2008). Principles of protein–protein interactions: What are the preferred ways for proteins to interact? Chemical Reviews, 108(4), 1225–1244.
   PubMed Web of Science ®Google Scholar
• Kour, A., Sharma, S., Dube, T., Bisht, A., Sharma, M., Mishra, J., Ali, M. E., & Panda, J. J. (2020). l-3, 4-Dihydroxyphenylalanine templated anisotropic gold nano/micro-roses as potential disrupters/inhibitors of α-crystallin protein and its gleaned model peptide aggregates. International Journal of Biological Macromolecules, 163, 2374–2391.
   PubMed Web of Science ®Google Scholar
• Kyaw, M. P., Nyunt, M. H., Chit, K., Aye, M. M., Aye, K. H., Aye, M. M., Lindegardh, N., Tarning, J., Imwong, M., Jacob, C. G., Rasmussen, C., Perin, J., Ringwald, P., & Nyunt, M. M. (2013). Reduced susceptibility of Plasmodium falciparum to artesunate in southern Myanmar. PLoS One, 8, e57689.
   PubMed Web of Science ®Google Scholar
• Maier, J. A., Martinez, C., Kasavajhala, K., Wickstrom, L., Hauser, K. E., & Simmerling, C. (2015). Simmerling, C. 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
• MalariaGEN Plasmodium falciparum Community Project. (2016). Genomic epidemiology of artemisinin resistant malaria. eLife, 5, e08714.
   PubMed Web of Science ®Google Scholar
• Mark, P., & Nilsson, L. (2001). Structure and dynamics of the TIP3P, SPC, and SPC/E water models at 298 K. The Journal of Physical Chemistry A, 105(43), 9954–9960. https://doi.org/10.1021/jp003020w
   Web of Science ®Google Scholar
• Mbengue, A., Bhattacharjee, S., Pandharkar, T., Liu, H., Estiu, G., Stahelin, R. V., Rizk, S. S., Njimoh, D. L., Ryan, Y., Chotivanich, K., Nguon, C., Ghorbal, M., Lopez-Rubio, J. J., Pfrender, M., Emrich, S., Mohandas, N., Dondorp, A. M., Wiest, O., & Haldar, K. (2015). A molecular mechanism of artemisinin resistance in Plasmodium falciparum malaria. Nature, 520, 683–687.
   PubMed Web of Science ®Google Scholar
• Ménard, D., Khim, N., Beghain, J., Adegnika, A. A., Shafiul-Alam, M., Amodu, O., Rahim-Awab, G., Barnadas, C., Berry, A., Boum, Y., Bustos, M. D., Cao, J., Chen, J. H., Collet, L., Cui, L., Thakur, G. D., Dieye, A., Djallé, D., Dorkenoo, M. A.,… Mercereau-Puijalon, O.; KARMA Consortium. (2016). A worldwide map of Plasmodium falciparum K13-propeller polymorphisms. The New England Journal of Medicine, 374, 2453–2464.
   PubMed Web of Science ®Google Scholar
• Mishra, N., Prajapati, S. K., Kaitholia, K., Bharti, R. S., Srivastava, B., Phookan, S., Anvikar, A. R., Dev, V., Sonal, G. S., Dhariwal, A. C., White, N. J., & Valecha, N. (2015). Surveillance of artemisinin resistance in Plasmodium falciparum in India using the kelch13 molecular marker. Antimicrobial Agents and Chemotherapy, 59, 2548–2553.
   PubMed Web of Science ®Google Scholar
• Nelson, M. T., Humphrey, W., Gursoy, A., Dalke, A., Kalé, L. V., Skeel, R. D., & Schulten, K. (1996). NAMD: A parallel, object-oriented molecular dynamics program. International Journal of High Performance Computing Applications, 10, 251–268.
   Web of Science ®Google Scholar
• Paloque, L., Coppée, R., Stokes, B. H., Gnädig, N. F., Niaré, K., Augereau, J.-M., Fidock, D. A., & Clain, J. (2022). Benoit-Vical, F. mutation in Plasmodium falciparum BTB/POZ domain of K13 protein confers artemisinin resistance. Antimicrobial Agents and Chemotherapy, 66(1), 01320–01321.
   Web of Science ®Google Scholar
• Papaleo, E., Saladino, G., Lambrughi, M., Lindorff-Larsen, K., Gervasio, F. L., & Nussinov, R. (2016). The role of protein loops and linkers in conformational dynamics and allostery. Chemical Reviews, 116(11), 6391–6423.
   PubMed Web of Science ®Google Scholar
• Peters, W. B., Edmondson, S. P., & Shriver, J. W. (2005). Effect of mutation of the Sac7d intercalating residues on the temperature dependence of DNA distortion and binding thermodynamics. Biochemistry, 44(12), 4794–4804.
   PubMed Web of Science ®Google Scholar
• Phyo, A. P., Nkhoma, S., Stepniewska, K., Ashley, E. A., Nair, S., McGready, R., ler Moo, C., Al-Saai, S., Dondorp, A. M., Lwin, K. M., Singhasivanon, P., Day, N. P., White, N. J., Anderson, T. J., & Nosten, F. (2012). Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study. Lancet, 379, 1960–1966.
   PubMed Web of Science ®Google Scholar
• Pinkas, D. M., Sanvitale, C. E., Bufton, J. C., Sorrell, F. J., Solcan, N., Chalk, R., Doutch, J., & Bullock, A. N. (2017). Structural complexity in the KCTD family of Cullin3-dependent E3 ubiquitin ligases. The Biochemical Journal, 474(22), 3747–3761.
   PubMedGoogle Scholar
• Prag, S., & Adams, J. C. (2003). Molecular phylogeny of the kelch-repeat superfamily reveals an expansion of BTB/kelch proteins in animals. BMC Bioinform, 4, 1–20.
   PubMed Web of Science ®Google Scholar
• Rathee, J., Kanwar, R., Kumari, L., Pawar, S. V., Sharma, S., Ali, M. E., Salunke, D. B., & Mehta, S. K. (2022). Development of nanostructured lipid carriers as a promising tool for methotrexate delivery: Physicochemical and in vitro evaluation. Journal of Biomolecular Structure and Dynamics, 1–12. https://doi.org/10.1080/07391102.2022.2037465
   Google Scholar
• Roper, C., Alifrangis, M., Ariey, F., Talisuna, A., Menard, D., Mercereau-Puijalon, O., & Ringwald, P. (2014). Molecular surveillance for artemisinin resistance in Africa. The Lancet. Infectious Diseases, 14(8), 668–670.
   PubMed Web of Science ®Google Scholar
• Rosenthal, P. J. (2018). Artemisinin resistance outside of Southeast Asia. The American Journal of Tropical Medicine and Hygiene, 99(6), 1357–1359. https://doi.org/10.4269/ajtmh.18-0845
   PubMed Web of Science ®Google Scholar
• Ryckaert, J.-P., Ciccotti, G., & Berendsen, H. J. (1977). Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. Journal of Computational Physics, 23(3), 327–341. https://doi.org/10.1016/0021-9991(77)90098-5
   Web of Science ®Google Scholar
• Singh, G. P., Goel, P., & Sharma, A. (2016). Structural mapping of Kelch13 mutations associated with artemisinin resistance in malaria. Journal of Structural and Functional Genomics, 17(2–3), 51–56.
   PubMedGoogle Scholar
• Straimer, J., Gnädig, N. F., Witkowski, B., Amaratunga, C., Duru, V., Ramadani, A. P., Dacheux, M., Khim, N., Zhang, L., Lam, S., Gregory, P. D., Urnov, F. D., Mercereau-Puijalon, O., Benoit-Vical, F., Fairhurst, R. M., Ménard, D., & Fidock, D. A. (2015). K13-propeller mutations confer artemisinin resistance in Plasmodium falciparum clinical isolates. Science, 347, 428–431.
   PubMed Web of Science ®Google Scholar
• Suresh, N., & Haldar, K. (2018). Mechanisms of artemisinin resistance in Plasmodium falciparum malaria. Current Opinion in Pharmacology, 42, 46–54.
   PubMed Web of Science ®Google Scholar
• Talisuna, A. O., Karema, C., Ogutu, B., Juma, E., Logedi, J., Nyandigisi, A., Mulenga, M., Mbacham, W. F., Roper, C., Guerin, P. J., D'Alessandro, U., & Snow, R. W. (2012). Mitigating the threat of artemisinin resistance in Africa: improvement of drug-resistance surveillance and response systems. Lancet Infectious Diseases, 12, 888–896.
   PubMed Web of Science ®Google Scholar
• Taylor, S. M., Parobek, C. M., DeConti, D. K., Kayentao, K., Coulibaly, S. O., Greenwood, B. M., Tagbor, H., Williams, J., Bojang, K., Njie, F., Desai, M., Kariuki, S., Gutman, J., Mathanga, D. P., Mårtensson, A., Ngasala, B., Conrad, M. D., Rosenthal, P. J., Tshefu, A. K., … Juliano, J. J. (2015). Absence of putative artemisinin resistance mutations among Plasmodium falciparum in sub-Saharan Africa: A molecular epidemiologic study. Journal of Infectious Diseases, 211, 680–688.
   PubMed Web of Science ®Google Scholar
• Thriemer, K., Hong, N. V., Rosanas-Urgell, A., Phuc, B. Q., Ha do, M., Pockele, E., Guetens, P., Van, N. V., Duong, T. T., Amambua-Ngwa, A., D'Alessandro, U., & Erhart, A. (2014). Delayed parasite clearance after treatment with dihydroartemisinin-piperaquine in Plasmodium falciparum malaria patients in central Vietnam. Antimicrobial Agents and Chemotherapy, 58, 7049–7055.
   PubMed Web of Science ®Google Scholar
• Turschner, S., & Efferth, T. (2009). Drug resistance in Plasmodium: Natural products in the fight against malaria. Mini Reviews in Medicinal Chemistry, 9(2), 206–2124.
   PubMed Web of Science ®Google Scholar
• Wang, L., Jiang, C., Cai, R., Chen, X.-Z., & Peng, J.-B. (2019). Unveiling the distinct mechanisms by which disease-causing mutations in the Kelch domain of KLHL3 disrupt the interaction with the acidic motif of WNK4 through molecular dynamics simulation. Biochemistry, 58(16), 2105–2115.
   PubMed Web of Science ®Google Scholar
• Zhang, D. D., Lo, S.-C., Cross, J. V., Templeton, D. J., & Hannink, M. (2004). Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Molecular and Cellular Biology, 24(24), 10941–10953. https://doi.org/10.1128/MCB.24.24.10941-10953.2004
   PubMed Web of Science ®Google Scholar
• Zhang, H., Song, T., Yang, Y., Fu, C., & Li, J. (2018). Exploring the interaction mechanism between cyclopeptide dc3 and androgen receptor using molecular dynamics simulations and free energy calculations. Frontiers in Chemistry, 6, 119.
   PubMed Web of Science ®Google Scholar