Comparison of tertiary structures of proteins in protein-protein complexes with unbound forms suggests prevalence of allostery in signalling proteins

BMC Structural Biology

Volumn 12, Issue , 2012, Pages

  Swapna, Lakshmipuram S ^a   Mahajan, Swapnil ^b,c   De Brevern, Alexandre G ^c,d,e   Srinivasan, Narayanaswamy ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b UNIVERSITÉ DE LA RÉUNION   (France)

^c INSERM   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e INSTITUT NATIONAL DE LA TRANSFUSION SANGUINE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ALPHA 1 ANTITRYPSIN; ANTHRAX TOXIN; COMPLEMENT COMPONENT C3; CYSTATIN; CYSTEINE PROTEINASE; ENZYME INHIBITOR; GLYCOPROTEIN IB ALPHA; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN G1; LYSOZYME; PROTEIN; PROTEIN KINASE; RAB PROTEIN; RAC PROTEIN; RAN PROTEIN; TRANSFERRIN RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; VITAMIN D BINDING PROTEIN; XYLAN ENDO 1,3 BETA XYLOSIDASE;

ALLOSTERISM; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DATA BASE; HUMAN; NONHUMAN; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING;

ALLOSTERIC SITE; ANIMALS; DATABASES, PROTEIN; LIGANDS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEINS; SIGNAL TRANSDUCTION;

EID: 84860360907     PISSN: None     EISSN: 14726807     Source Type: Journal    
DOI: 10.1186/1472-6807-12-6     Document Type: Article

References (112)

1. The molecular architecture of protein-protein binding sites. Reichmann D, Rahat O, Cohen M, Neuvirth H, Schreiber G, Curr Opin Struct Biol 2007 17 1 67 76 (Pubitemid 46240815)
2. Evolution and dynamics of protein interactions and networks. Levy ED, Pereira-Leal JB, Curr Opin Struct Biol 2008 18 3 349 357
3. Interactome networks and human disease. Vidal M, Cusick ME, Barabasi AL, Cell 2011 144 6 986 998
4. Protein binding specificity versus promiscuity. Schreiber G, Keating AE, Curr Opin Struct Biol 2011 21 1 50 61
5. Protein modules and protein-protein interaction. Introduction. Janin J, Wodak SJ, Adv Protein Chem 2002 61 1 8 (Pubitemid 35303452)
6. Protein-protein interactions in human disease. Ryan DP, Matthews JM, Curr Opin Struct Biol 2005 15 4 441 446 (Pubitemid 41073836)
7. The changing landscape of protein allostery. Swain JF, Gierasch LM, Curr Opin Struct Biol 2006 16 1 102 108 (Pubitemid 43221878)
8. Allostery and cooperativity revisited. Cui Q, Karplus M, Protein Sci 2008 17 8 1295 1307
9. The structural basis of allosteric regulation in proteins. Laskowski RA, Gerick F, Thornton JM, FEBS Lett 2009 583 11 1692 1698
10. Protein allostery, signal transmission and dynamics: a classification scheme of allosteric mechanisms. Tsai CJ, Del Sol A, Nussinov R, Mol Biosyst 2009 5 3 207 216
11. Protein dynamics and allostery: an NMR view. Tzeng SR, Kalodimos CG, Curr Opin Struct Biol 2011 21 1 62 67
12. Allosteric mechanisms of signal transduction. Changeux JP, Edelstein SJ, Science 2005 308 5727 1424 1428 (Pubitemid 40791288)
13. Regulating transcription regulators via allostery and flexibility. Beckett D, Proc Natl Acad Sci U S A 2009 106 52 22035 22036
14. Global approaches to protein-protein interactions. Drewes G, Bouwmeester T, Curr Opin Cell Biol 2003 15 2 199 205 (Pubitemid 36332195)
15. New methodologies for measuring protein interactions in vivo and in vitro. Piehler J, Curr Opin Struct Biol 2005 15 1 4 14 (Pubitemid 40249503)
16. Protein-protein interactions: methods for detection and analysis. Phizicky EM, Fields S, Microbiol Rev 1995 59 1 94 123
17. Measuring protein-protein interactions. Lakey JH, Raggett EM, Curr Opin Struct Biol 1998 8 1 119 123 (Pubitemid 28107924)
18. Comparative assessment of large-scale data sets of protein-protein interactions. von Mering C, Krause R, Snel B, Cornell M, Oliver SG, Fields S, Bork P, Nature 2002 417 6887 399 403 (Pubitemid 34563526)
19. Remediation of the protein data bank archive. Henrick K, Feng Z, Bluhm WF, Dimitropoulos D, Doreleijers JF, Dutta S, Flippen-Anderson JL, Ionides J, Kamada C, Krissinel E, et al. Nucleic Acids Res 2008 36 Database issue 426 D433
20. Macromolecular recognition in the Protein Data Bank. Janin J, Rodier F, Chakrabarti P, Bahadur RP, Acta Crystallogr D: Biol Crystallogr 2007 63 Pt 1 1 8
21. Comprehensive inventory of protein complexes in the Protein Data Bank from consistent classification of interfaces. Bordner AJ, Gorin AA, BMC Bioinf 2008 9 234
22. The many faces of protein-protein interactions: A compendium of interface geometry. Kim WK, Henschel A, Winter C, Schroeder M, PLoS Comput Biol 2006 2 9 124
23. iPfam: visualization of protein-protein interactions in PDB at domain and amino acid resolutions. Finn RD, Marshall M, Bateman A, Bioinformatics 2005 21 3 410 412 (Pubitemid 40246619)
24. SNAPPI-DB: a database and API of Structures, iNterfaces and Alignments for Protein-Protein Interactions. Jefferson ER, Walsh TP, Roberts TJ, Barton GJ, Nucleic Acids Res 2007 35 Database issue 580 D589
25. 3D complex: a structural classification of protein complexes. Levy ED, Pereira-Leal JB, Chothia C, Teichmann SA, PLoS Comput Biol 2006 2 11 155
26. InterEvol database: exploring the structure and evolution of protein complex interfaces. Faure G, Andreani J, Guerois R, Nucleic Acids Res 2011 40 Database issue 847 D856
27. The protein common interface database (ProtCID) - a comprehensive database of interactions of homologous proteins in multiple crystal forms. Xu Q, Dunbrack RL, Nucleic Acids Res 2011 39 Database issue 761 D770
28. Diversity of protein-protein interactions. Nooren IM, Thornton JM, EMBO J 2003 22 14 3486 3492 (Pubitemid 36898326)
29. Statistical analysis of predominantly transient protein-protein interfaces. Ansari S, Helms V, Proteins 2005 61 2 344 355 (Pubitemid 41429142)
30. Structure, function, and evolution of transient and obligate protein-protein interactions. Mintseris J, Weng Z, Proc Natl Acad Sci U S A 2005 102 31 10930 10935 (Pubitemid 41105970)
31. Transient protein-protein interactions: structural, functional, and network properties. Perkins JR, Diboun I, Dessailly BH, Lees JG, Orengo C, Structure 2010 18 10 1233 1243
32. The Protein Data Bank. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE, Nucleic Acids Res 2000 28 1 235 242 (Pubitemid 30047768)
33. A protein-protein docking benchmark. Chen R, Mintseris J, Janin J, Weng Z, Proteins 2003 52 1 88 91 (Pubitemid 36648855)
34. Protein-protein docking benchmark version 3.0. Hwang H, Pierce B, Mintseris J, Janin J, Weng Z, Proteins 2008 73 3 705 709 (Pubitemid 352788651)
35. ComSin: database of protein structures in bound (complex) and unbound (single) states in relation to their intrinsic disorder. Lobanov MY, Shoemaker BA, Garbuzynskiy SO, Fong JH, Panchenko AR, Galzitskaya OV, Nucleic Acids Res 2010 38 Database issue 283 D287
36. An analysis of conformational changes on protein-protein association: implications for predictive docking. Betts MJ, Sternberg MJ, Protein Eng 1999 12 4 271 283 (Pubitemid 29209937)
37. Structural deformation upon protein-protein interaction: a structural alphabet approach. Martin J, Regad L, Lecornet H, Camproux AC, BMC Struct Biol 2008 8 12
38. Taking advantage of local structure descriptors to analyze interresidue contacts in protein structures and protein complexes. Martin J, Regad L, Etchebest C, Camproux AC, Proteins 2008 73 3 672 689 (Pubitemid 352788649)
39. Characterization of conformational patterns in active and inactive forms of kinases using protein blocks approach. Agarwal A, Dinesh DC, Srinivasan N, de Brevern AG, Computational Intelligence and Pattern Analysis in Biological Informatics Wiley, New Jersey, Maulik U, Bandyopadhyay S, Wang JTL, 2010 169 187
40. The relationship between the flexibility of proteins and their conformational states on forming protein-protein complexes with an application to protein-protein docking. Smith GR, Sternberg MJ, Bates PA, J Mol Biol 2005 347 5 1077 1101 (Pubitemid 40387454)
41. Complementarity of structure ensembles in protein-protein binding. Grunberg R, Leckner J, Nilges M, Structure 2004 12 12 2125 2136 (Pubitemid 39593192)
42. Large conformational changes in proteins: signaling and other functions. Grant BJ, Gorfe AA, McCammon JA, Curr Opin Struct Biol 2010 20 2 142 147
43. Accounting for conformational changes during protein-protein docking. Zacharias M, Curr Opin Struct Biol 2010 20 2 180 186
44. Protein flexibility: coordinate uncertainties and interpretation of structural differences. Rashin AA, Rashin AH, Jernigan RL, Acta Crystallogr D: Biol Crystallogr 2009 65 Pt 11 1140 1161
45. Functional aspects of protein flexibility. Teilum K, Olsen JG, Kragelund BB, Cell Mol Life Sci 2009 66 14 2231 2247
46. PCDB: a database of protein conformational diversity. Juritz EI, Alberti SF, Parisi GD, Nucleic Acids Res 2011 39 Database issue 475 D479
47. SCOP: a structural classification of proteins database for the investigation of sequences and structures. Murzin AG, Brenner SE, Hubbard T, Chothia C, J Mol Biol 1995 247 4 536 540
48. Bayesian probabilistic approach for predicting backbone structures in terms of protein blocks. de Brevern AG, Etchebest C, Hazout S, Proteins 2000 41 3 271 287
49. A short survey on Protein Blocks. Joseph AP, Agarwal G, Mahajan S, Gelly J-C, Swapna LS, Offmann B, Cadet F, Bornot A, Tyagi M, Valadié H, et al. Biophys Rev 2010 2 3 137 145
50. Improvement of protein structure comparison using a structural alphabet. Joseph AP, Srinivasan N, de Brevern AG, Biochimie 2011 93 9 1434 1445
51. Einfluss der configuration auf die wirkung der enzyme. Fischer E, Ber Dtsch Chem Ges 1894 27 2985 2993
52. Application of a Theory of Enzyme Specificity to Protein Synthesis. Koshland DE, Proc Natl Acad Sci U S A 1958 44 2 98 104
53. A new, structurally nonredundant, diverse data set of protein-protein interfaces and its implications. Keskin O, Tsai CJ, Wolfson H, Nussinov R, Protein Sci 2004 13 4 1043 1055 (Pubitemid 38429226)
54. Protein-protein interactions: a review of protein dimer structures. Jones S, Thornton JM, Prog Biophys Mol Biol 1995 63 1 31 65
55. The Catalytic Site Atlas: a resource of catalytic sites and residues identified in enzymes using structural data. Porter CT, Bartlett GJ, Thornton JM, Nucleic Acids Res 2004 32 Database issue 129 D133
56. Crystal structure and functional analysis of Ras binding to its effector phosphoinositide 3-kinase gamma. Pacold ME, Suire S, Perisic O, Lara-Gonzalez S, Davis CT, Walker EH, Hawkins PT, Stephens L, Eccleston JF, Williams RL, Cell 2000 103 6 931 943
57. Structural evidence for ammonia tunneling across the (beta alpha)(8) barrel of the imidazole glycerol phosphate synthase bienzyme complex. Douangamath A, Walker M, Beismann-Driemeyer S, Vega-Fernandez MC, Sterner R, Wilmanns M, Structure 2002 10 2 185 193 (Pubitemid 34164597)
58. NMR structure of human erythropoietin and a comparison with its receptor bound conformation. Cheetham JC, Smith DM, Aoki KH, Stevenson JL, Hoeffel TJ, Syed RS, Egrie J, Harvey TS, Nat Struct Biol 1998 5 10 861 866 (Pubitemid 28467406)
59. Crystal structure of a deubiquitinating enzyme (human UCH-L3) at 1.8 A resolution. Johnston SC, Larsen CN, Cook WJ, Wilkinson KD, Hill CP, EMBO J 1997 16 13 3787 3796 (Pubitemid 27280994)
60. A Ras-induced conformational switch in the Ras activator Son of sevenless. Freedman TS, Sondermann H, Friedland GD, Kortemme T, Bar-Sagi D, Marqusee S, Kuriyan J, Proc Natl Acad Sci U S A 2006 103 45 16692 16697 (Pubitemid 44737315)
61. Crystal structure of the human TbetaR2 ectodomain-TGF-beta3 complex. Hart PJ, Deep S, Taylor AB, Shu Z, Hinck CS, Hinck AP, Nat Struct Biol 2002 9 3 203 208 (Pubitemid 34171313)
62. X-ray structure of a bifunctional protein kinase in complex with its protein substrate HPr. Fieulaine S, Morera S, Poncet S, Mijakovic I, Galinier A, Janin J, Deutscher J, Nessler S, Proc Natl Acad Sci U S A 2002 99 21 13437 13441 (Pubitemid 35215399)
63. The DH and PH domains of Trio coordinately engage Rho GTPases for their efficient activation. Chhatriwala MK, Betts L, Worthylake DK, Sondek J, J Mol Biol 2007 368 5 1307 1320 (Pubitemid 46617588)
64. Canonical inhibitor-like interactions explain reactivity of alpha1-proteinase inhibitor Pittsburgh and antithrombin with proteinases. Dementiev A, Simonovic M, Volz K, Gettins PG, J Biol Chem 2003 278 39 37881 37887 (Pubitemid 37175317)
65. The TGF beta receptor activation process: an inhibitor- to substrate-binding switch. Huse M, Muir TW, Xu L, Chen YG, Kuriyan J, Massague J, Mol Cell 2001 8 3 671 682 (Pubitemid 32946943)
66. Madhusudan, Hoch JA, Varughese KI: A transient interaction between two phosphorelay proteins trapped in a crystal lattice reveals the mechanism of molecular recognition and phosphotransfer in signal transduction. Zapf J, Sen U, Structure 2000 8 8 851 862
67. Structural basis for molecular recognition between nuclear transport factor 2 (NTF2) and the GDP-bound form of the Ras-family GTPase Ran. Stewart M, Kent HM, McCoy AJ, J Mol Biol 1998 277 3 635 646 (Pubitemid 28190863)
68. Crystal structure of the hereditary haemochromatosis protein HFE complexed with transferrin receptor. Bennett MJ, Lebron JA, Bjorkman PJ, Nature 2000 403 6765 46 53 (Pubitemid 30038514)
69. The 3.2-A crystal structure of the human IgG1 Fc fragment-Fc gammaRIII complex. Sondermann P, Huber R, Oosthuizen V, Jacob U, Nature 2000 406 6793 267 273 (Pubitemid 30604397)
70. Structural basis for Rab GTPase activation by VPS9 domain exchange factors. Delprato A, Lambright DG, Nat Struct Mol Biol 2007 14 5 406 412 (Pubitemid 46685882)
71. Global dynamics of proteins: bridging between structure and function. Bahar I, Lezon TR, Yang LW, Eyal E, Annu Rev Biophys 2010 39 23 42
72. Usefulness and limitations of normal mode analysis in modeling dynamics of biomolecular complexes. Ma J, Structure 2005 13 3 373 380 (Pubitemid 40342876)
73. Coarse-grained normal mode analysis in structural biology. Bahar I, Rader AJ, Curr Opin Struct Biol 2005 15 5 586 592 (Pubitemid 41393491)
74. Structural changes involved in protein binding correlate with intrinsic motions of proteins in the unbound state. Tobi D, Bahar I, Proc Natl Acad Sci U S A 2005 102 52 18908 18913 (Pubitemid 43049540)
75. oGNM: online computation of structural dynamics using the Gaussian Network Model. Yang LW, Rader AJ, Liu X, Jursa CJ, Chen SC, Karimi HA, Bahar I, Nucleic Acids Res 2006 34 Web Server issue 24 W31
76. Signal propagation in proteins and relation to equilibrium fluctuations. Chennubhotla C, Bahar I, PLoS Comput Biol 2007 3 9 1716 1726 (Pubitemid 47502976)
77. Delano WL, The PyMOL Molecular Graphics System DeLano Scientific, San Carlos, CA, USA 2002
78. Structure of the Escherichia coli TolB protein determined by MAD methods at 1.95 A resolution. Abergel C, Bouveret E, Claverie JM, Brown K, Rigal A, Lazdunski C, Benedetti H, Structure 1999 7 10 1291 1300 (Pubitemid 29482990)
79. Molecular mimicry enables competitive recruitment by a natively disordered protein. Bonsor DA, Grishkovskaya I, Dodson EJ, Kleanthous C, J Am Chem Soc 2007 129 15 4800 4807 (Pubitemid 46648779)
80. Allosteric beta-propeller signalling in TolB and its manipulation by translocating colicins. Bonsor DA, Hecht O, Vankemmelbeke M, Sharma A, Krachler AM, Housden NG, Lilly KJ, James R, Moore GR, Kleanthous C, EMBO J 2009 28 18 2846 2857
81. Structure of complement receptor 2 in complex with its C3d ligand. Szakonyi G, Guthridge JM, Li D, Young K, Holers VM, Chen XS, Science 2001 292 5522 1725 1728 (Pubitemid 32506247)
82. Structural basis for guanine nucleotide exchange on Ran by the regulator of chromosome condensation (RCC1). Renault L, Kuhlmann J, Henkel A, Wittinghofer A, Cell 2001 105 2 245 255 (Pubitemid 32429514)
83. Cell biology: Ran, mitosis and the cancer connection. Sanderson HS, Clarke PR, Curr Biol 2006 16 12 466 R468
84. The origin of allosteric functional modulation: multiple pre-existing pathways. del Sol A, Tsai CJ, Ma B, Nussinov R, Structure 2009 17 8 1042 1050
85. Dynamic interactions of proteins in complex networks: a more structured view. Stein A, Pache RA, Bernado P, Pons M, Aloy P, FEBS J 2009 276 19 5390 5405
86. Side-chain conformational changes upon Protein-Protein Association. Ruvinsky AM, Kirys T, Tuzikov AV, Vakser IA, J Mol Biol 2011 408 2 356 365
87. Induction of flexibility through protein-protein interactions. Fayos R, Melacini G, Newlon MG, Burns L, Scott JD, Jennings PA, J Biol Chem 2003 278 20 18581 18587 (Pubitemid 36799485)
88. Backbone dynamics of the C-terminal domain of Escherichia coli topoisomerase I in the absence and presence of single-stranded DNA. Yu L, Zhu CX, Tse-Dinh YC, Fesik SW, Biochemistry 1996 35 30 9661 9666 (Pubitemid 26302978)
89. Increased backbone mobility in beta-barrel enhances entropy gain driving binding of N-TIMP-1 to MMP-3. Arumugam S, Gao G, Patton BL, Semenchenko V, Brew K, Van Doren SR, J Mol Biol 2003 327 3 719 734 (Pubitemid 36299074)
90. Structural stability of binding sites: consequences for binding affinity and allosteric effects. Luque I, Freire E, Proteins 2000 41 S4 63 71
91. Implications of protein flexibility for drug discovery. Teague SJ, Nat Rev Drug Discov 2003 2 7 527 541 (Pubitemid 37361745)
92. Flexibility and conformational entropy in protein-protein binding. Grunberg R, Nilges M, Leckner J, Structure 2006 14 4 683 693
93. Analysis of protein contacts into Protein Units. Faure G, Bornot A, de Brevern AG, Biochimie 2009 91 7 876 887
94. Dynamically driven protein allostery. Popovych N, Sun S, Ebright RH, Kalodimos CG, Nat Struct Mol Biol 2006 13 9 831 838 (Pubitemid 44338778)
95. Dominant negative role of the glutamic acid residue conserved in the pyruvate kinase M(1) isozyme in the heterotropic allosteric effect involving fructose-1,6-bisphosphate. Ikeda Y, Taniguchi N, Noguchi T, J Biol Chem 2000 275 13 9150 9156 (Pubitemid 30185130)
96. Is allostery an intrinsic property of all dynamic proteins? Gunasekaran K, Ma B, Nussinov R, Proteins 2004 57 3 433 443 (Pubitemid 39390799)
97. Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Lange OF, Lakomek NA, Fares C, Schroder GF, Walter KF, Becker S, Meiler J, Grubmuller H, Griesinger C, de Groot BL, Science 2008 320 5882 1471 1475 (Pubitemid 351929422)
98. Allostery: absence of a change in shape does not imply that allostery is not at play. Tsai CJ, del Sol A, Nussinov R, J Mol Biol 2008 378 1 1 11
99. Binding leverage as a molecular basis for allosteric regulation. Mitternacht S, Berezovsky IN, PLoS Comput Biol 2011 7 9 1002148
100. Allostery and population shift in drug discovery. Kar G, Keskin O, Gursoy A, Nussinov R, Curr Opin Pharmacol 2010 10 6 715 722
101. Conformational ensembles, signal transduction and residue hot spots: application to drug discovery. Acuner Ozbabacan SE, Gursoy A, Keskin O, Nussinov R, Curr Opin Drug Discov Devel 2010 13 5 527 537
102. Inference of macromolecular assemblies from crystalline state. Krissinel E, Henrick K, J Mol Biol 2007 372 3 774 797 (Pubitemid 47321791)
103. Structural invariants in protein folding. Chothia C, Nature 1975 254 5498 304 308
104. The interpretation of protein structures: estimation of static accessibility. Lee B, Richards FM, J Mol Biol 1971 55 3 379 400
105. Molecular recognition. Conformational analysis of limited proteolytic sites and serine proteinase protein inhibitors. Hubbard SJ, Campbell SF, Thornton JM, J Mol Biol 1991 220 2 507 530
106. The accessible surface area and stability of oligomeric proteins. Miller S, Lesk AM, Janin J, Chothia C, Nature 1987 328 6133 834 836 (Pubitemid 17125965)
107. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Thompson JD, Higgins DG, Gibson TJ, Nucleic Acids Res 1994 22 22 4673 4680 (Pubitemid 24354800)
108. Analysis of temperature factor distribution in high-resolution protein structures. Parthasarathy S, Murthy MR, Protein Sci 1997 6 12 2561 2567 (Pubitemid 28006693)
109. Flexibility analysis of enzyme active sites by crystallographic temperature factors. Yuan Z, Zhao J, Wang ZX, Protein Eng 2003 16 2 109 114 (Pubitemid 36458649)
110. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ, Nucleic Acids Res 1997 25 17 3389 3402 (Pubitemid 27359211)
111. UniRef: comprehensive and non-redundant UniProt reference clusters. Suzek BE, Huang H, McGarvey P, Mazumder R, Wu CH, Bioinformatics 2007 23 10 1282 1288 (Pubitemid 47050545)
112. Predicting functionally important residues from sequence conservation. Capra JA, Singh M, Bioinformatics 2007 23 15 1875 1882 (Pubitemid 47299827)