Integrated analysis of residue coevolution and protein structure in ABC transporters

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Gulyás Kovács, Attila ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER B; ABC TRANSPORTER C; GLYCOPROTEIN P; TRANSMEMBRANE CONDUCTANCE REGULATOR; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; COEVOLUTION; CONCEPTUAL FRAMEWORK; CONTROLLED STUDY; PHYLOGENETIC TREE; PHYLOGENY; PROCESS OPTIMIZATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

EID: 84871447564     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036546     Document Type: Article

References (74)

1. Sadovsky E, Yifrach O, (2007) Principles underlying energetic coupling along an allosteric communication trajectory of a voltage-activated k+ channel. Proc Natl Acad Sci U S A 104: 19813-8.
2. Ackers GK, Smith FR, (1985) Effects of site-specific amino acid modi_cation on protein interactions and biological function. Annu Rev Biochem 54: 597-629.
3. Locher KP, (2009) Structure and mechanism of atp-binding cassette transporters. Philos Trans R Soc Lond B Biol Sci 364: 239-45.
4. Oldham ML, Davidson AL, Chen J, (2008) Structural insights into abc transporter mechanism. Curr Opin Struct Biol 18: 726-33.
5. Higgins CF, Linton KJ, (2004) The atp switch model for abc transporters. Nat Struct Mol Biol 11: 918-26.
6. Codoñer FM, Fares MA, (2008) Why should we care about molecular coevolution? Evol Bioinform Online 4: 29-38.
7. Galtier N, Dutheil J, (2007) Coevolution within and between genes. Genome Dyn 3: 1-12.
8. Morcos F, Pagnani A, Lunt B, Bertolino A, Marks DS, et al. (2011) Direct-coupling analysis of residue coevolution captures native contacts across many protein families. Proc Natl Acad Sci U S A 108 (49): E1293-E1301.
9. Marks DS, Colwell LJ, Sheridan R, Hopf TA, Pagnani A, et al. (2011) Protein 3d structure computed from evolutionary sequence variation. PLoS One 6: e28766.
10. Horner DS, Pirovano W, Pesole G, (2008) Correlated substitution analysis and the prediction of amino acid structural contacts. Brief Bioinform 9: 46-56.
11. Yeang CH, Haussler D, (2007) Detecting coevolution in and among protein domains. PLoS Comput Biol 3: e211.
12. Shackelford G, Karplus K, (2007) Contact prediction using mutual information and neural nets. Proteins 69 (Suppl 8): 159-64.
13. Göbel U, Sander C, Schneider R, Valencia A, (1994) Correlated mutations and residue contacts in proteins. Proteins 18: 309-17.
14. Shindyalov IN, Kolchanov NA, Sander C, (1994) Can three-dimensional contacts in protein structures be predicted by analysis of correlated mutations? Protein Eng 7: 349-58.
15. Taylor WR, Hatrick K, (1994) Compensating changes in protein multiple sequence alignments. Protein Eng 7: 341-8.
16. Neher E, (1994) How frequent are correlated changes in families of protein sequences? Proc Natl Acad Sci U S A 91: 98-102.
17. Jeon J, Yang JS, Kim S, (2009) Integration of evolutionary features for the identification of functionally important residues in major facilitator superfamily transporters. PLoS Comput Biol 5: e1000522.
18. Fleishman SJ, Yifrach O, Ben-Tal N, (2004) An evolutionarily conserved network of amino acids mediates gating in voltage-dependent potassium channels. J Mol Biol 340: 307-18.
19. Dutheil J, Galtier N, (2007) Detecting groups of coevolving positions in a molecule: a clustering approach. BMC Evol Biol 7: 242.
20. Poon AFY, Lewis FI, Pond SLK, Frost SDW, (2007) An evolutionary-network model reveals strati fied interactions in the v3 loop of the hiv-1 envelope. PLoS Comput Biol 3: e231.
21. Carlson JM, Brumme ZL, Rousseau CM, Brumme CJ, Matthews P, et al. (2008) Phylogenetic dependency networks: inferring patterns of ctl escape and codon covariation in hiv-1 gag. PLoS Comput Biol 4: e1000225.
22. Buslje CM, Santos J, Delfino JM, Nielsen M, (2009) Correction for phylogeny, small number of observations and data redundancy improves the identification of coevolving amino acid pairs using mutual information. Bioinformatics 25: 1125-31.
23. Little DY, Chen L, (2009) Identification of coevolving residues and coevolution potentials emphasizing structure, bond formation and catalytic coordination in protein evolution. PLoS One 4: e4762.
24. Gloor GB, Tyagi G, Abrassart DM, Kingston AJ, Fernandes AD, et al. (2010) Functionally compensating coevolving positions are neither homoplasic nor conserved in clades. Mol Biol Evol 27: 1181-91.
25. Poon AFY, Swenson LC, Dong WWY, Deng W, Kosakovsky Pond SL, et al. (2010) Phylogenetic analysis of population-based and deep sequencing data to identify coevolving sites in the nef gene of hiv-1. Mol Biol Evol 27: 819-32.
26. Szollosi A, Muallem DR, Csanády L, Vergani P, (2011) Mutant cycles at cftr's non-canonical atpbinding site support little interface separation during gating. J Gen Physiol 137: 549-62.
27. Szollosi A, Vergani P, Csanády L, (2010) Involvement of f1296 and n1303 of cftr in induced-fit conformational change in response to atp binding at nbd2. J Gen Physiol 136: 407-23.
28. Vergani P, Lockless SW, Nairn AC, Gadsby DC, (2005) Cftr channel opening by atp-driven tight dimerization of its nucleotide-binding domains. Nature 433: 876-80.
29. Caporaso JG, Smit S, Easton BC, Hunter L, Huttley GA, et al. (2008) Detecting coevolution without phylogenetic trees? tree-ignorant metrics of coevolution perform as well as tree-aware metrics. BMC Evol Biol 8: 327.
30. Fuchs A, Martin-Galiano AJ, Kalman M, Fleishman S, Ben-Tal N, et al. (2007) Co-evolving residues in membrane proteins. Bioinformatics 23: 3312-9.
31. Dunn SD, Wahl LM, Gloor GB, (2008) Mutual information without the inuence of phylogeny or entropy dramatically improves residue contact prediction. Bioinformatics 24: 333-40.
32. Tillier ERM, Lui TWH, (2003) Using multiple interdependency to separate functional from phylogenetic correlations in protein alignments. Bioinformatics 19: 750-5.
33. Felsenstein J, (1985) Phylogenies and the comparative method. American Naturalist 125: 1.
34. Martin LC, Gloor GB, Dunn SD, Wahl LM, (2005) Using information theory to search for coevolving residues in proteins. Bioinformatics 21: 4116-24.
35. Fodor AA, Aldrich RW, (2004) Inuence of conservation on calculations of amino acid covariance in multiple sequence alignments. Proteins 56: 211-21.
36. Pollock DD, Taylor WR, Goldman N, (1999) Coevolving protein residues: maximum likelihood identification and relationship to structure. J Mol Biol 287: 187-98.
37. Dimmic MW, Hubisz MJ, Bustamante CD, Nielsen R, (2005) Detecting coevolving amino acid sites using bayesian mutational mapping. Bioinformatics 21 (Suppl 1): i126-35.
38. Dutheil J, Pupko T, Jean-Marie A, Galtier N, (2005) A model-based approach for detecting coevolving positions in a molecule. Mol Biol Evol 22: 1919-28.
39. Gouveia-Oliveira R, Pedersen AG, (2007) Finding coevolving amino acid residues using row and column weighting of mutual information and multi-dimensional amino acid representation. Algorithms Mol Biol 2: 12.
40. Weigt M, White RA, Szurmant H, Hoch JA, Hwa T, (2009) Identification of direct residue contacts in protein-protein interaction by message passing. Proc Natl Acad Sci U S A 106: 67-72.
41. Lee BC, Kim D, (2009) A new method for revealing correlated mutations under the structural and functional constraints in proteins. Bioinformatics 25: 2506-13.
42. Burger L, van Nimwegen E, (2010) Disentangling direct from indirect co-evolution of residues in protein alignments. PLoS Comput Biol 6: e1000633.
43. Fawcett T, (2004) ROC graphs: Notes and practical considerations for researchers. Machine Learning 31.
44. Dawson RJP, Locher KP, (2006) Structure of a bacterial multidrug abc transporter. Nature 443: 180-5.
45. Mornon JP, Lehn P, Callebaut I, (2008) Atomic model of human cystic fibrosis transmembrane conductance regulator: membrane-spanning domains and coupling interfaces. Cell Mol Life Sci 65: 2594-612.
46. Aller SG, Yu J, Ward A, Weng Y, Chittaboina S, et al. (2009) Structure of p-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323: 1718-22.
47. O'Mara ML, Tieleman DP, (2007) P-glycoprotein models of the apo and atp-bound states based on homology with sav1866 and malk. FEBS Lett 581: 4217-22.
48. Mornon JP, Lehn P, Callebaut I, (2009) Molecular models of the open and closed states of the whole human cftr protein. Cell Mol Life Sci 66: 3469-86.
49. Stamatakis A, Ludwig T, Meier H, (2005) Raxml-iii: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21: 456-63.
50. Whelan S, Goldman N, (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18: 691-9.
51. Yang Z, (2006) Computational molecular evolution. New York Oxford University Press USA.
52. Eddy SR, (1998) Profile hidden markov models. Bioinformatics 14: 755-63.
53. Katoh K, Kuma Ki, Toh H, Miyata T, (2005) Mafft version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33: 511-8.
54. Korber BT, Farber RM, Wolpert DH, Lapedes AS, (1993) Covariation of mutations in the v3 loop of human immunodeficiency virus type 1 envelope protein: an information theoretic analysis. Proc Natl Acad Sci U S A 90: 7176-80.
55. Fares MA, Travers SAA, (2006) A novel method for detecting intramolecular coevolution: adding a further dimension to selective constraints analyses. Genetics 173: 9-23.
56. Ward A, Reyes CL, Yu J, Roth CB, Chang G, (2007) Flexibility in the abc transporter msba: Alternating access with a twist. Proc Natl Acad Sci U S A 104: 19005-10.
57. Haq O, Levy RM, Morozov AV, Andrec M, (2009) Pairwise and higher-order correlations among drug-resistance mutations in hiv-1 subtype b protease. BMC Bioinformatics 10 (Suppl 8): S10.
58. Kosiol C, Goldman N, (2011) Markovian and non-markovian protein sequence evolution: Aggregated markov process models. J Mol Biol 411 (4-6): 910-23.
59. Jordan IK, Kota KC, Cui G, Thompson CH, McCarty NA, (2008) Evolutionary and functional divergence between the cystic fibrosis transmembrane conductance regulator and related atp-binding cassette transporters. Proc Natl Acad Sci U S A 105: 18865-70.
60. Halabi N, Rivoire O, Leibler S, Ranganathan R, (2009) Protein sectors: evolutionary units of three-dimensional structure. Cell 138: 774-86.
61. Jeon J, Nam HJ, Choi YS, Yang JS, Hwang J, et al. (2011) Molecular evolution of protein conformational changes revealed by a network of evolutionarily coupled residues. Mol Biol Evol 28: 2675-85.
62. Csanády L, Vergani P, Gadsby DC, (2010) Strict coupling between cftr's catalytic cycle and gating of its cl- ion pore revealed by distributions of open channel burst durations. Proc Natl Acad Sci U S A 107: 1241-6.
63. Gadsby DC, Vergani P, Csanády L, (2006) The abc protein turned chloride channel whose failure causes cystic fibrosis. Nature 440: 477-83.
64. Rich DP, Gregory RJ, Anderson MP, Manavalan P, Smith AE, et al. (1991) Effect of deleting the r domain on cftr-generated chloride channels. Science 253: 205-7.
65. Accardi A, Picollo A, (2010) Clc channels and transporters: proteins with borderline personalities. Biochim Biophys Acta 1798: 1457-64.
66. Serohijos AWR, Hegedus T, Riordan JR, Dokholyan NV, (2008) Diminished self-chaperoning activity of the deltaf508 mutant of cftr results in protein misfolding. PLoS Comput Biol 4: e1000008.
67. Loo TW, Bartlett MC, Clarke DM, (2010) The v510d suppressor mutation stabilizes deltaf508-cftr at the cell surface. Biochemistry 49: 6352-7.
68. Pagant S, Halliday JJ, Kougentakis C, Miller EA, (2010) Intragenic suppressing mutations correct the folding and intracellular traffic of misfolded mutants of yor1p, a eukaryotic drug transporter. J Biol Chem 285 (47): 36304-14.
69. Wang Y, Loo TW, Bartlett MC, Clarke DM, (2007) Correctors promote maturation of cystic fibrosis transmembrane conductance regulator (cftr)-processing mutants by binding to the protein. J Biol Chem 282: 33247-51.
70. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) Ucsf chimera{a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-12.
71. Cotten JF, Ostedgaard LS, Carson MR, Welsh MJ, (1996) Effect of cystic fibrosis-associated mutations in the fourth intracellular loop of cystic fibrosis transmembrane conductance regulator. J Biol Chem 271: 21279-84.
72. Seibert FS, Linsdell P, Loo TW, Hanrahan JW, Clarke DM, et al. (1996) Disease-associated mutations in the fourth cytoplasmic loop of cystic fibrosis transmembrane conductance regulator compromise biosynthetic processing and chloride channel activity. J Biol Chem 271: 15139-45.
73. Serohijos AWR, Hegedus T, Aleksandrov AA, He L, Cui L, et al. (2008) Phenylalanine-508 mediates a cytoplasmic-membrane domain contact in the cftr 3d structure crucial to assembly and channel function. Proc Natl Acad Sci U S A 105: 3256-61.
74. Lewis HA, Buchanan SG, Burley SK, Conners K, Dickey M, et al. (2004) Structure of nucleotidebinding domain 1 of the cystic fibrosis transmembrane conductance regulator. EMBO J 23: 282-93.