Predicting flexible loop regions that interact with ligands: The challenge of accurate scoring

Proteins: Structure, Function and Bioinformatics

Volumn 80, Issue 1, 2012, Pages 246-260

  Danielson, Matthew L ^a   Lill, Markus A ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Computational; CorLps; Loop prediction; Loop ligand interaction; Protein flexibility; Scoring

Indexed keywords

CYTOCHROME P450; ENOLASE; LIGAND; PHOSPHORIBOSYLGLYCINAMIDE FORMYLTRANSFERASE;

ARTICLE; BINDING SITE; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE;

AMINO ACID MOTIFS; ARCHAEAL PROTEINS; COMPUTER SIMULATION; CYTOCHROME P-450 ENZYME SYSTEM; ESCHERICHIA COLI PROTEINS; HYDROGEN BONDING; MODELS, MOLECULAR; PHOSPHOPYRUVATE HYDRATASE; PHOSPHORIBOSYLGLYCINAMIDE FORMYLTRANSFERASE; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; SACCHAROMYCES CEREVISIAE PROTEINS; SOFTWARE; THERMODYNAMICS;

EID: 83555177246     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.23199     Document Type: Article

References (60)

1. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The Protein Data Bank. Nucleic Acids Res 2000; 28: 235-242.
2. The Universal Protein Resource (UniProt) in 2010. Nucleic Acids Res 2010; 38: D142-D148.
3. Marti-Renom MA, Stuart AC, Fiser A, Sanchez R, Melo F, Sali A. Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct 2000; 29: 291-325.
4. Wong S, Jacobson MP. Conformational selection in silico: loop latching motions and ligand binding in enzymes. Proteins 2008; 71: 153-164.
5. Audoly L, Breyer RM. The second extracellular loop of the prostaglandin EP3 receptor is an essential determinant of ligand selectivity. J Biol Chem 1997; 272: 13475-13478.
6. Ahn KH, Bertalovitz AC, Mierke DF, Kendall DA. Dual role of the second extracellular loop of the cannabinoid receptor 1: ligand binding and receptor localization. Mol Pharmacol 2009; 76: 833-842.
7. Dittus J, Cooper S, Obermair G, Pulakat L. Role of the third intracellular loop of the angiotensin II receptor subtype AT2 in ligand-receptor interaction. FEBS Lett 1999; 445: 23-26.
8. Han KH, Green SR, Tangirala RK, Tanaka S, Quehenberger O. Role of the first extracellular loop in the functional activation of CCR2. The first extracellular loop contains distinct domains necessary for both agonist binding and transmembrane signaling. J Biol Chem 1999; 274: 32055-32062.
9. Hauser M, Kauffman S, Lee BK, Naider F, Becker JM. The first extracellular loop of the Saccharomyces cerevisiae G protein-coupled receptor Ste2p undergoes a conformational change upon ligand binding. J Biol Chem 2007; 282: 10387-10397.
10. Hellal-Levy C, Fagart J, Souque A, Wurtz JM, Moras D, Rafestin-Oblin ME. Crucial role of the H11-H12 loop in stabilizing the active conformation of the human mineralocorticoid receptor. Mol Endocrinol 2000; 14: 1210-1221.
11. Mailfait S, Thoreau E, Belaiche D, Formstecher And BS. Critical role of the H6-H7 loop in the conformational adaptation of all-trans retinoic acid and synthetic retinoids within the ligand-binding site of RARalpha. J Mol Endocrinol 2000; 24: 353-364.
12. Naganathan S, Beckett D. Nucleation of an allosteric response via ligand-induced loop folding. J Mol Biol 2007; 373: 96-111.
13. Pless SA, Lynch JW. Magnitude of a conformational change in the glycine receptor beta1-beta2 loop is correlated with agonist efficacy. J Biol Chem 2009; 284: 27370-27376.
14. Shi J, Radic' Z, Taylor P. Inhibitors of different structure induce distinguishing conformations in the omega loop, Cys69-Cys96, of mouse acetylcholinesterase. J Biol Chem 2002; 277: 43301-43308.
15. Shi L, Javitch JA. The binding site of aminergic G protein-coupled receptors: the transmembrane segments and second extracellular loop. Annu Rev Pharmacol Toxicol 2002; 42: 437-467.
16. Shi L, Javitch JA. The second extracellular loop of the dopamine D2 receptor lines the binding-site crevice. Proc Natl Acad Sci U S A 2004; 101: 440-445.
17. Miura T, Nishinaka T, Terada T. Importance of the substrate-binding loop region of human monomeric carbonyl reductases in catalysis and coenzyme binding. Life Sci 2009; 85: 303-308.
18. Wang Y, Berlow RB, Loria JP. Role of loop-loop interactions in coordinating motions and enzymatic function in triosephosphate isomerase. Biochemistry 2009; 48: 4548-4556.
19. Fukamizo T, Miyake R, Tamura A, Ohnuma T, Skriver K, Pursiainen NV, Juffer AH. A flexible loop controlling the enzymatic activity and specificity in a glycosyl hydrolase family 19 endochitinase from barley seeds (Hordeum vulgare L.). Biochim Biophys Acta 2009; 1794: 1159-1167.
20. Gunasekaran K, Nussinov R. Modulating functional loop movements: the role of highly conserved residues in the correlated loop motions. ChemBioChem 2004; 5: 224-230.
21. Oka T, Hakoshima T, Itakura M, Yamamori S, Takahashi M, Hashimoto Y, Shiosaka S, Kato K. Role of loop structures of neuropsin in the activity of serine protease and regulated secretion. J Biol Chem 2002; 277: 14724-14730.
22. Funhoff EG, Klaassen CH, Samyn B, Van BJ, Averill BA. The highly exposed loop region in mammalian purple acid phosphatase controls the catalytic activity. ChemBioChem 2001; 2: 355-363.
23. Gautam JK, Ashish, Comeau LD, Krueger JK, Smith MF, Jr. Structural and functional evidence for the role of the TLR2 DD loop in TLR1/TLR2 heterodimerization and signaling. J Biol Chem 2006; 281: 30132-30142.
24. Bastard K, Prevost C, Zacharias M. Accounting for loop flexibility during protein-protein docking. Proteins 2006; 62: 956-969.
25. Kojima S, Furukubo S, Kumagai I, Miura K. Effects of deletion in the flexible loop of the protease inhibitor SSI (Streptomyces subtilisin inhibitor) on interactions with proteases. Protein Eng 1993; 6: 297-303.
26. Kufareva I, Abagyan R. Type-II kinase inhibitor docking, screening, and profiling using modified structures of active kinase states. J Med Chem 2008; 51: 7921-7932.
27. Ma B, Kumar S, Tsai CJ, Nussinov R. Folding funnels and binding mechanisms. Protein Eng 1999; 12: 713-720.
28. Lou H, Cukier RI. Molecular dynamics of apo-adenylate kinase: a principal component analysis. J Phys Chem B 2006; 110: 12796-12808.
29. Lou H, Cukier RI. Molecular dynamics of apo-adenylate kinase: a distance replica exchange method for the free energy of conformational fluctuations. J Phys Chem B 2006; 110: 24121-24137.
30. Cukier RI. Apo adenylate kinase encodes its holo form: a principal component and varimax analysis. J Phys Chem B 2009; 113: 1662-1672.
31. Lill MA. Efficient incorporation of protein flexibility and dynamics into molecular docking simulations. Biochemistry 2011; 50: 6157-6169.
32. Carlson HA, McCammon JA. Accommodating protein flexibility in computational drug design. Mol Pharmacol 2000; 57: 213-218.
33. Cavasotto CN, Kovacs JA, Abagyan RA. Representing receptor flexibility in ligand docking through relevant normal modes. J Am Chem Soc 2005; 127: 9632-9640.
34. Koshland DE. Application of a theory of enzyme specificity to protein synthesis. Proc Natl Acad Sci U S A 1958; 44: 98-104.
35. Danielson ML, Lill MA. New computational method for prediction of interacting protein loop regions. Proteins 2010; 78: 1748-1759.
36. Zhang C, Liu S, Zhou Y. Accurate and efficient loop selections by the DFIRE-based all-atom statistical potential. Protein Sci 2004; 13: 391-399.
37. Zhou H, Zhou Y. Distance-scaled, finite ideal-gas reference state improves structure-derived potentials of mean force for structure selection and stability prediction. Protein Sci 2002; 11: 2714-2726.
38. Massova I, Kollman PA. Combined molecular mechanical and continuum solvent approach (MM-PBSA/GBSA) to predict ligand binding. Perspect Drug Discov 2000; 18: 113-135.
39. Wroblewska L, Jagielska A, Skolnick J. Development of a physics-based force field for the scoring and refinement of protein models. Biophys J 2008; 94: 3227-3240.
40. Soto CS, Fasnacht M, Zhu J, Forrest L, Honig B. Loop modeling: sampling, filtering, and scoring. Proteins 2008; 70: 834-843.
41. Heyer LJ, Kruglyak S, Yooseph S. Exploring expression data: identification and analysis of coexpressed genes. Genome Res 1999; 9: 1106-1115.
42. Xiang ZX, Honig B. Extending the accuracy limits of prediction for side-chain conformations. J Mol Biol 2001; 311: 421-430.
43. DeLano WL. The PyMOL molecular graphics system. Palo Alto, CA: DeLano Scientific; 2002.
44. Word JM, Lovell SC, Richardson JS, Richardson DC. Asparagine and glutamine: using hydrogen atom contacts in the choice of side-chain amide orientation. J Mol Biol 1999; 285: 1735-1747.
45. Case DA, Cheatham TE, III, Darden T, Gohlke H, Luo R, Merz KM, Jr., Onufriev A, Simmerling C, Wang B, Woods RJ. The Amber biomolecular simulation programs. J Comput Chem 2005; 26: 1668-1688.
46. Pearlman DA, Case DA, Caldwell JW, Ross WS, Cheatham TE, Debolt S, Ferguson D, Seibel G, Kollman P. Amber, A package of computer-programs for applying molecular mechanics, normal-mode analysis, molecular-dynamics and free-energy calculations to simulate the structural and energetic properties of molecules. Comput Phys Commun 1995; 91: 1-41.
47. Mongan J, Simmerling C, McCammon JA, Case DA, Onufriev A. Generalized born model with a simple, robust molecular volume correction. J Chem Theory Comput 2007; 3: 156-169.
48. Rastelli G, Del RA, Degliesposti G, Sgobba M. Fast and accurate predictions of binding free energies using MM-PBSA and MM-GBSA. J Comput Chem 2010; 31: 797-810.
49. Weis A, Katebzadeh K, Soderhjelm P, Nilsson I, Ryde U. Ligand affinities predicted with the MM/PBSA method: dependence on the simulation method and the force field. J Med Chem 2006; 49: 6596-6606.
50. Singh N, Warshel A. Absolute binding free energy calculations: on the accuracy of computational scoring of protein-ligand interactions. Proteins 2010; 78: 1705-1723.
51. Ryckaert JP, Ciccotti G, Berendsen HJC. Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 1977; 23: 327-341.
52. Mandell DJ, Coutsias EA, Kortemme T. Sub-angstrom accuracy in protein loop reconstruction by robotics-inspired conformational sampling. Nat Methods 2009; 6: 551-552.
53. Arnautova YA, Abagyan RA, Totrov M. Development of a new physics-based internal coordinate mechanics force field and its application to protein loop modeling. Proteins 2011; 79: 477-498.
54. Merz KM. Limits of free energy computation for protein-ligand interactions. J Chem Theory Comput 2010; 6: 1018-1027.
55. Chen P, Schulze-Gahmen U, Stura EA, Inglese J, Johnson DL, Marolewski A, Benkovic SJ, Wilson IA. Crystal structure of glycinamide ribonucleotide transformylase from Escherichia coli at 3.0 A resolution. A target enzyme for chemotherapy. J Mol Biol 1992; 227: 283-292.
56. Almassy RJ, Janson CA, Kan CC, Hostomska Z. Structures of apo and complexed Escherichia coli glycinamide ribonucleotide transformylase. Proc Natl Acad Sci U S A 1992; 89: 6114-6118.
57. Park SY, Yamane K, Adachi S, Shiro Y, Weiss KE, Maves SA, Sligar SG. Thermophilic cytochrome P450 (CYP119) from Sulfolobus solfataricus: high resolution structure and functional properties. J Inorg Biochem 2002; 91: 491-501.
58. Yano JK, Koo LS, Schuller DJ, Li H, Ortiz de Montellano PR, Poulos TL. Crystal structure of a thermophilic cytochrome P450 from the archaeon Sulfolobus solfataricus. J Biol Chem 2000; 275: 31086-31092.
59. Wedekind JE, Reed GH, Rayment I. Octahedral coordination at the high-affinity metal site in enolase: crystallographic analysis of the MgII-enzyme complex from yeast at 1.9 A resolution. Biochemistry 1995; 34: 4325-4330.
60. Wedekind JE, Poyner RR, Reed GH, Rayment I. Chelation of serine 39 to Mg2+ latches a gate at the active site of enolase: structure of the bis(Mg2+) complex of yeast enolase and the intermediate analog phosphonoacetohydroxamate at 2.1-A resolution. Biochemistry 1994; 33: 9333-9342.