Understanding the mechanism of atovaquone drug resistance in plasmodium falciparum cytochrome b mutation Y268S using computational methods

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Akhoon, Bashir A ^a   Singh, Krishna P ^a   Varshney, Megha ^b   Gupta, Shishir K ^c   Shukla, Yogeshwar ^d,e   Gupta, Shailendra K ^a,e,f  

^a CSIR INDIAN INSTITUTE OF TOXICOLOGY RESEARCH   (India)

^b ALIGARH MUSLIM UNIVERSITY   (India)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d Indian Institute of Toxicological Research   (India)

^e ACADEMY OF SCIENTIFIC AND INNOVATIVE RESEARCH ACSIR   (India)

^f UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ATOVAQUONE; CYTOCHROME B; IRON SULFUR PROTEIN; UBIQUINOL CYTOCHROME C REDUCTASE; ANTIMALARIAL AGENT;

AB INITIO CALCULATION; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANTIBIOTIC RESISTANCE; ARTICLE; BINDING AFFINITY; COMPUTER MODEL; DRUG BINDING SITE; GENE MUTATION; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; WILD TYPE; COMPUTER SIMULATION; DRUG RESISTANCE; GENETICS; MALARIA, FALCIPARUM; MUTATION;

PLASMODIUM FALCIPARUM;

ANTIMALARIALS; ATOVAQUONE; COMPUTER SIMULATION; CYTOCHROMES B; DRUG RESISTANCE; MALARIA, FALCIPARUM; MUTATION; PLASMODIUM FALCIPARUM;

EID: 84908079786     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110041     Document Type: Article

References (59)

1. Singh B, Kim Sung L, Matusop A, Radhakrishnan A, Shamsul SS, et al. (2004) A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Lancet 363: 1017-1024.
2. Daneshvar C, Davis TM, Cox-Singh J, Rafa'ee MZ, Zakaria SK, et al. (2009) Clinical and laboratory features of human Plasmodium knowlesi infection. Clin Infect Dis 49: 852-860.
3. Crowther GJ, Napuli AJ, Gilligan JH, Gagaring K, Borboa R, et al. (2011) Identification of inhibitors for putative malaria drug targets among novel antimalarial compounds. Mol Biochem Parasitol 175: 21-29.
4. Garcia LS (2010) Malaria. Clin Lab Med 30: 93-129.
5. Fry M, Pudney M (1992) Site of action of the antimalarial hydroxynaphthoquinone, 2-[trans-4-(4'-chlorophenyl) cyclohexyl]-3-hydroxy-1,4-naphthoquinone (566C80). Biochem Pharmacol 43: 1545-1553.
6. Srivastava IK, Rottenberg H, Vaidya AB (1997) Atovaquone, a broad spectrum antiparasitic drug, collapses mitochondrial membrane potential in a malarial parasite. J BiolChem 272: 3961-3966.
7. Vaidya AB, Lashgari MS, Pologe LG, Morrisey J (1993) Structural features of Plasmodium cytochrome b that may underlie susceptibility to 8-aminoquinolines and hydroxynaphthoquinones. Mol Biochem Parasitol 58: 33-42.
8. Musset L, Bouchaud O, Matheron S, Massias L, Le Bras J (2006) Clinical atovaquone-proguanil resistance of Plasmodium falciparum associated with cytochrome b codon 268 mutations. Microbes Infect 8: 2599-2604.
9. Kessl JJ, Ha KH, Merritt AK, Lange BB, Hill P, et al. (2005) Cytochrome b mutations that modify the ubiquinol-binding pocket of the cytochrome bc1 complex and confer anti-malarial drug resistance in Saccharomyces cerevisiae. J Biol Chem 280: 17142-17148.
10. Kessl JJ, Meshnick SR, Trumpower BL (2007) Modeling the molecular basis of atovaquone resistance in parasites and pathogenic fungi. Trends Parasitol 23: 494-501.
11. Fisher N, Abd Majid R, Antoine T, Al-Helal M, Warman AJ, et al.(2012) Cytochrome b mutation Y268S conferring atovaquone resistance phenotype in malaria parasite results in reduced parasite bc1 catalytic turnover and protein expression. J Biol Chem287: 9731-41.
12. Hill P, Kessl J, Fisher N, Meshnick S, Trumpower BL, et al. (2003) Recapitulation in Saccharomyces cerevisiae of cytochrome b mutations conferring resistance to atovaquone in Pneumocystis jiroveci. Antimicrob Agents Chemother 47: 2725-31.
13. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9: 40.
14. Das R, Qian B, Raman S, Vernon R, Thompson J, et al. (2007) Structure prediction for CASP7 targets using extensive all-atom refinement with Rosetta@home. Proteins 69: 118-28.
15. Zhang Y (2007) Template-based modeling and free modeling by I-TASSER in CASP7. Proteins 69: 108-117.
16. Zhou H, Pandit SB, Lee SY, Borreguero J, Chen H, et al. (2007) Analysis of TASSER-based CASP7 protein structure prediction results. Proteins 69: 90-97.
17. Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5: 725-738.
18. Zhang Y, Skolnick J (2004) Scoring function for automated assessment of protein structure template quality. Proteins 57: 702-10.
19. Spassov VZ, Bashford D (1999) Multiple-Site Ligand Binding to Flexible Macromolecules: Separation of Global and Local Conformational Change and an Iterative Mobile Clustering Approach J Comput Chem 2: 1091-1111.
20. Solmaz SR, Hunte C (2008) Structure of complex III with bound cytochrome c in reduced state and definition of a minimal core interface for electron transfer.J Biol Chem 283: 17542-17549.
21. Korsinczky M, Chen N, Kotecka B, Saul A, Rieckmann K, et al. (2000) Mutations in Plasmodium falciparum cytochrome b that are associated with atovaquone resistance are located at a putative drug-binding site. Antimicrob Agents Chemother 44: 2100-2108.
22. Wu G, Robertson DH, Brooks CL 3rd, Vieth M (2003) Detailed analysis of gridbased molecular docking: A case study of CDOCKER-A CHARMm-based MD docking algorithm. J Comput Chem 24: 1549-1562.
23. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, et al. (1995) A smooth particle mesh Ewald method. J Chem Phys 103: 8577-8593.
24. Merlino A, Mazzarella L, Carannante A, Di Fiore A, Di Donato A, et al. (2005) The importance of dynamic effects on the enzyme activity: X-ray structure and molecular dynamics of onconase mutants. J Biol Chem 280: 17953-1760.
25. Taly JF, Marin A, Gibrat JF (2008) Can molecular dynamics simulations help in discriminating correct from erroneous protein 3D models? BMC Bioinformatics 9: 6.
26. Malek K, Odijk T, Coppens MO (2005) Diffusion of water and sodium counterions in nanopores of a b-lactoglobulin crystal: a molecular dynamics study. Nanotechnology 16: S522-530.
27. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM (1997) LINCS: A linear constraint solver for molecular simulations. J Comput Chem 18: 1463-1472.
28. Berendsen HJC, Postma JPM, Van Gunsteren WF, DiNola A, Haak JR (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81: 3684-3690.
29. Parrinello M, Rahman A (1980) Crystal Structure and Pair Potentials: A Molecular-Dynamics Study. Phys Rev Lett 45: 1196-1199.
30. Massova I, Kollman PA (1999) Computational alanine scanning to probe protein-protein interactions: A novel approach to evaluate binding free energies. J Am Chem Soc 121: 8133-8143.
31. Spiliotopoulos D, Spitaleri A, Musco G (2012) Exploring PHD fingers and H3K4me0 interactions with molecular dynamics simulations and binding free energy calculations: AIRE-PHD1, a comparative study. PLoS One 7: e46902.
32. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: Application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98: 10037-1004.
33. Brown SP, Muchmore SW (2009) Large-scale application of high-throughput molecular mechanics with poisson-boltzmann surface area for routine physicsbased scoring of protein-ligand complexes. J Med Chem 52: 3159-3165.
34. Schwöbel B, Alifrangis M, Salanti A, Jelinek T (2003) Different mutation patterns of atovaquone resistance to Plasmodium falciparum in vitro and in vivo: rapid detection of codon 268 polymorphisms in the cytochrome b as potential in vivo resistance marker. Malar J 2: 5.
35. Fivelman QL, Butcher GA, Adagu IS, Warhurst DC, Pasvol G (2002) Malarone treatment failure and in vitro confirmation of resistance of Plasmodium falciparum isolate from Lagos, Nigeria. Malar J 1: 1.
36. Wells JA (1990) Additivity of mutational effects in proteins. Biochemistry 29: 8509-17.
37. Lo TP, Komar-Panicucci S, Sherman F, McLendon G, Brayer GD (1995) Structural and functional effects of multiple mutations at distal sites in cytochrome c. Biochemistry 34: 5259-5268.
38. Schreiber G, Fersht AR (1995) Energetics of protein-protein interactions: analysis of the barnase-barstar interface by single mutations and double mutant cycles. J Mol Biol 248: 478-486.
39. Baloria U, Akhoon BA, Gupta SK, Sharma S, Verma V (2012) In silico proteomic characterization of human epidermal growth factor receptor 2 (HER-2) for the mapping of high affinity antigenic determinants against breast cancer. Amino Acids 42: 1349-60.
40. Ma B, Tsai CJ, Nussinov R (2000) Binding and folding: in search of intramolecular chaperone-like building block fragments. Protein Eng 13: 617-27.
41. Sham YY, Ma B, Tsai CJ, Nussinov R (2001) Molecular dynamics simulation of Escherichia coli dihydrofolate reductase and its protein fragments: relative stabilities in experiment and simulations. Protein Sci 10: 135-148.
42. Kumar S, Sham YY, Tsai C-J, Nussinov R (2001) Protein folding and function: the N-terminal fragment in adenylate kinase. Biophys J 80: 2439-2454.
43. Feyfant E, Sali A, Fiser A (2007) Modeling mutations in protein structures. ProtSci 16: 2030-2041.
44. Gupta SK, Srivastava M, Akhoon BA, Gupta SK, Grabe N (2012) Insilico accelerated identification of structurally conserved CD8+ and CD4+ T-cell epitopes in high-risk HPV types. Infect Genet Evol 12: 1513-8.
45. Srivastava M, Gupta SK, Abhilash PC, Singh N (2012) Structure prediction and binding sites analysis of curcin protein of Jatrophacurcas using computational approaches. J Mol Model. 18: 2971-9.
46. Akhoon BA, Gupta SK, Verma V, Dhaliwal G, Srivastava M, et al. (2010) In silico designing and optimization of anti-breast cancer antibody mimetic oligopeptide targeting HER-2 in women. J Mol Graph Model 28: 664-9.
47. Cherkis KA, Temple BR, Chung EH, Sondek J, Dangl JL (2012) AvrRpm1 missense mutations weakly activate RPS2-mediated immune response in Arabidopsis thaliana. PLoS One 7:e42633.
48. Frauer C, Rottach A, Meilinger D, Bultmann S, Fellinger K, et al. (2012) Different binding properties and function of CXXC zinc finger domains in Dnmt1 and Tet1. PLoS One 6:e16627.
49. Laskowski RA (2003) Structural quality assurance. In Structural Bioinformatics. Edited by Bourne P, Weissig H. Wiley-Liss, Inc. 292 p.
50. Fisher N, Meunier B (2008) Molecular basis of resistance to cytochrome bc1 inhibitors. FEMS Yeast Res 8: 183-192.
51. Khositnithikul R, Tan-Ariya P, Mungthin M (2008) In vitro atovaquone/ proguanil susceptibility and characterization of the cytochrome b gene of Plasmodium falciparum from different endemic regions of Thailand. Malar J 28: 7: 23.
52. Friedman SH, DeCamp DL, Sijbesma RP, Srdanov G, Wudl F, et al. (1993) Inhibition of the HIV-1 protease by fullerene derivatives: model building studies and experimental verification. J Am Chem Soc 115: 6506-6509.
53. Friedman SH, Ganapathi PS, Rubin Y, Kenyon GL (1998) Optimizing the binding of fullerene inhibitors of the HIV-1 protease through predicted increases in hydrophobic desolvation. J Med Chem 41: 2424-9.
54. Cheng Y, Li D, Ji B, Shi X, Gao H (2010) Structure-based design of carbon nanotubes as HIV-1 protease inhibitors: atomistic and coarse-grained simulations. J Mol Graph Model 29: 171-7.
55. Lee VS, Nimmanpipug P, Aruksakunwong O, Promsri S, Sompornpisut P, et al. (2007) Structural analysis of lead fullerene-based inhibitor bound to human immunodeficiency virus type 1 protease in solution from molecular dynamics simulations. J Mol Graph Model 26: 558-70.
56. Laberge M, Yonetani T (2008) Molecular dynamics simulations of hemoglobin A in different states and bound to DPG: Effector-linked perturbation of tertiary conformations and HbA concerted dynamics. Biophys J 94: 2737-2751.
57. Huo S, Massova I, Kollman PA (2002) Computational alanine scanning of the 1:1 human growth hormone-receptor complex. J Comput Chem 23: 15-27.
58. Bradshaw RT, Patel BH, Tate EW, Leatherbarrow RJ, Gould IR (2011) Comparing experimental and computational alanine scanning techniques for probing a prototypical protein-protein interaction. Protein Eng Des Sel 24: 197-207.
59. Chiappori F, Merelli I, Milanesi L, Marabotti A (2013) Static and dynamic interactions between GALK enzyme and known inhibitors: Guidelines to design new drugs for galactosemic patients. Eur J Med Chem 63C: 423-434.