The role of protein structural analysis in the next generation sequencing era

Topics in Current Chemistry

Volumn 336, Issue , 2014, Pages 67-98

  Yue, Wyatt W ^a   Froese, D Sean ^a   Brennan, Paul E ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Drug development; Genetic diseases; Misfolding; Missense mutations; Mutation analysis; Protein structures; Structure based drug design

Indexed keywords

PROTEIN;

ARTICLE; CHEMISTRY; DRUG DEVELOPMENT; HIGH THROUGHPUT SEQUENCING; HUMAN; METHODOLOGY; PROTEIN CONFORMATION; PROTEIN FOLDING;

DRUG DISCOVERY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEINS;

EID: 84890951425     PISSN: 03401022     EISSN: None     Source Type: Book Series    
DOI: 10.1007/128-2012-326     Document Type: Article

References (138)

1. Kendrew JC, Bodo G, Dintzis HM, Parrish RG, Wyckoff H, Phillips DC (1958) A threedimensional model of the myoglobin molecule obtained by X-ray analysis. Nature 181(4610):662-666
2. Savitsky P, Bray J, Cooper CD, Marsden BD, Mahajan P, Burgess-Brown NA et al (2010) High-throughput production of human proteins for crystallization: The SGC experience. J Struct Biol 172(1):3-13
3. Page R, Stevens RC (2004) Crystallization data mining in structural genomics: Using positive and negative results to optimize protein crystallization screens. Methods 34(3):373-389
4. Joachimiak A (2009) High-throughput crystallography for structural genomics. Curr Opin Struct Biol 19(5):573-584
5. Manjasetty BA, Turnbull AP, Panjikar S, Bussow K, Chance MR (2008) Automated technologies and novel techniques to accelerate protein crystallography for structural genomics. Proteomics 8(4):612-625
6. Pellecchia M, Sem DS, Wuthrich K (2002) NMR in drug discovery. Nat Rev Drug Discov 1(3):211-219
7. Billeter M, Wagner G, Wuthrich K (2008) Solution NMR structure determination of proteins revisited. J Biomol NMR 42(3):155-158
8. Frank J (2002) Single-particle imaging of macromolecules by cryo-electron microscopy. Annu Rev Biophys Biomol Struct 31:303-319
9. Marti-Renom MA, Stuart AC, Fiser A, Sanchez R, Melo F, Sali A (2000) Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct 29:291-325
10. Chothia C, Lesk AM (1986) The relation between the divergence of sequence and structure in proteins. EMBO J 5(4):823-826
11. Cavasotto CN, Phatak SS (2009) Homology modeling in drug discovery: Current trends and applications. Drug Discov Today 14(13-14):676-683
12. Yue P, Li Z, Moult J (2005) Loss of protein structure stability as a major causative factor in monogenic disease. J Mol Biol 353(2):459-473
13. Yip YL, Scheib H, Diemand AV, Gattiker A, Famiglietti LM, Gasteiger E et al (2004) The Swiss-Prot variant page and the ModSNP database: A resource for sequence and structure information on human protein variants. Hum Mutat 23(5):464-470
14. Tramontano A, Morea V (2003) Assessment of homology-based predictions in CASP5. Proteins 53(Suppl 6):352-368
15. Metzker ML (2010) Sequencing technologies - The next generation. Nat Rev Genet 11(1):31-46
16. Ng SB, Nickerson DA, Bamshad MJ, Shendure J (2010) Massively parallel sequencing and rare disease. Hum Mol Genet 19(R2):R119-R124
17. Ku CS, Naidoo N, Pawitan Y (2011) Revisiting Mendelian disorders through exome sequencing. Hum Genet 129(4):351-370
18. Ng SB, Buckingham KJ, Lee C, Bigham AW, Tabor HK, Dent KM et al (2010) Exome sequencing identifies the cause of a mendelian disorder. Nat Genet 42(1):30-35
19. Ng SB, Turner EH, Robertson PD, Flygare SD, Bigham AW, Lee C et al (2009) Targeted capture and massively parallel sequencing of 12 human exomes. Nature 461(7261):272-276
20. Ng SB, Bigham AW, Buckingham KJ, Hannibal MC, McMillin MJ, Gildersleeve HI et al (2010) Exome sequencing identifies MLL2 mutations as a cause of Kabuki syndrome. Nat Genet 42(9):790-793
21. International HapMap Consortium (2003) The International HapMap Project. Nature 426 (6968):789-796
22. Hamosh A, Scott AF, Amberger JS, Bocchini CA, McKusick VA (2005) Online Mendelian Inheritance in Man (OMIM), a knowledgebase of human genes and genetic disorders. Nucleic Acids Res 33(Database issue):D514-D517
23. Stenson PD, Ball EV, Mort M, Phillips AD, Shiel JA, Thomas NS et al (2003) Human Gene Mutation Database (HGMD): 2003 update. Hum Mutat 21(6):577-581
24. Thusberg J, Vihinen M (2009) Pathogenic or not And if so, then how Studying the effects of missense mutations using bioinformatics methods. Hum Mutat 30(5):703-714
25. Jordan DM, Ramensky VE, Sunyaev SR (2010) Human allelic variation: Perspective from protein function, structure, and evolution. Curr Opin Struct Biol 20(3):342-350
26. Karchin R (2009) Next generation tools for the annotation of human SNPs. Brief Bioinform 10(1):35-52
27. Sunyaev S, Ramensky V, Bork P (2000) Towards a structural basis of human nonsynonymous single nucleotide polymorphisms. Trends Genet 16(5):198-200
28. Miller MP, Kumar S (2001) Understanding human disease mutations through the use of interspecific genetic variation. Hum Mol Genet 10(21):2319-2328
29. Hicks S, Wheeler DA, Plon SE, Kimmel M (2011) Prediction of missense mutation functionality depends on both the algorithm and sequence alignment employed. Hum Mutat 32(6):661-668
30. Calabrese R, Capriotti E, Fariselli P, Martelli PL, Casadio R (2009) Functional annotations improve the predictive score of human disease-related mutations in proteins. Hum Mutat 30(8):1237-1244
31. Yue P, Moult J (2006) Identification and analysis of deleterious human SNPs. J Mol Biol 356(5):1263-1274
32. Lobo PA, Van Petegem F (2009) Crystal structures of the N-terminal domains of cardiac and skeletal muscle ryanodine receptors: Insights into disease mutations. Structure 17(11):1505-1514
33. Lew ED, Bae JH, Rohmann E, Wollnik B, Schlessinger J (2007) Structural basis for reduced FGFR2 activity in LADD syndrome: Implications for FGFR autoinhibition and activation. Proc Natl Acad Sci USA 104(50):19802-19807
34. Chaikuad A, Froese DS, Berridge G, von Delft F, Oppermann U, Yue WW (2011) Conformational plasticity of glycogenin and its maltosaccharide substrate during glycogen biogenesis. Proc Natl Acad Sci USA 108(52):21028-21033
35. Malay AD, Procious SL, Tolan DR (2002) The temperature dependence of activity and structure for the most prevalent mutant aldolase B associated with hereditary fructose intolerance. Arch Biochem Biophys 408(2):295-304
36. Zhang Z, Norris J, Schwartz C, Alexov E (2011) In silico and in vitro investigations of the mutability of disease-causing missense mutation sites in spermine synthase. PLoS One 6(5): E20373
37. Anderson PC, Daggett V (2008) Molecular basis for the structural instability of human DJ-1 induced by the L166P mutation associated with Parkinson's disease. Biochemistry 47 (36):9380-9393
38. Niesen FH, Berglund H, Vedadi M (2007) The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat Protoc 2(9):2212-2221
39. Froese DS, Kochan G, Muniz JR, Wu X, Gileadi C, Ugochukwu E et al (2010) Structures of the human GTPase MMAA and vitamin B12-dependent methylmalonyl-CoA mutase and insight into their complex formation. J Biol Chem 285(49):38204-38213
40. Wu L, Pan L, Wei Z, Zhang M (2011) Structure of MyTH4-FERM domains in myosin VIIa tail bound to cargo. Science 331(6018):757-760
41. Bridwell-Rabb J, Winn AM, Barondeau DP (2011) Structure-function analysis of Friedreich's ataxia mutants reveals determinants of frataxin binding and activation of the Fe-S assembly complex. Biochemistry 50(33):7265-7274
42. Wang Z, Moult J (2001) SNPs, protein structure, and disease. Hum Mutat 17(4):263-270
43. Gregersen N, Bross P, Vang S, Christensen JH (2006) Protein misfolding and human disease. Annu Rev Genomics Hum Genet 7:103-124
44. Mitchell JJ, Trakadis YJ, Scriver CR (2011) Phenylalanine hydroxylase deficiency. Genet Med 13(8):697-707
45. Dobson CM (2004) Principles of protein folding, misfolding and aggregation. Semin Cell Dev Biol 15(1):3-16
46. Jennings IG, Cotton RG, Kobe B (2000) Structural interpretation of mutations in phenylalanine hydroxylase protein aids in identifying genotype-phenotype correlations in phenylketonuria. Eur J Hum Genet 8(9):683-696
47. Erlandsen H, Stevens RC (1999) The structural basis of phenylketonuria. Mol Genet Metab 68(2):103-125
48. Dobrowolski SF, Pey AL, Koch R, Levy H, Ellingson CC, Naylor EW et al (2009) Biochemical characterization of mutant phenylalanine hydroxylase enzymes and correlation with clinical presentation in hyperphenylalaninaemic patients. J Inherit Metab Dis 32(1):10-21
49. Pey AL, Stricher F, Serrano L, Martinez A (2007) Predicted effects of missense mutations on native-state stability account for phenotypic outcome in phenylketonuria, a paradigm of misfolding diseases. Am J Hum Genet 81(5):1006-1024
50. Gersting SW, Kemter KF, Staudigl M, Messing DD, Danecka MK, Lagler FB et al (2008) Loss of function in phenylketonuria is caused by impaired molecular motions and conformational instability. Am J Hum Genet 83(1):5-17
51. Matthews BW (1993) Structural and genetic analysis of protein stability. Annu Rev Biochem 62:139-160
52. Xiao J, Madhan B, Li Y, Brodsky B, Baum J (2011) Osteogenesis imperfecta model peptides: Incorporation of residues replacing Gly within a triple helix achieved by renucleation and local flexibility. Biophys J 101(2):449-458
53. Tang NL, Hui J, Young E, Worthington V, To KF, Cheung KL et al (2003) A novel mutation (G233D) in the glycogen phosphorylase gene in a patient with hepatic glycogen storage disease and residual enzyme activity. Mol Genet Metab 79(2):142-145
54. Wu WW, Molday RS (2003) Defective discoidin domain structure, subunit assembly, and endoplasmic reticulum processing of retinoschisin are primary mechanisms responsible for X-linked retinoschisis. J Biol Chem 278(30):28139-28146
55. Malay AD, Allen KN, Tolan DR (2005) Structure of the thermolabile mutant aldolase B, A149P: Molecular basis of hereditary fructose intolerance. J Mol Biol 347(1):135-144
56. Jeyabalan J, Nesbit MA, Galvanovskis J, Callaghan R, Rorsman P, Thakker RV (2010) SEDLIN forms homodimers: Characterisation of SEDLIN mutations and their interactions with transcription factors MBP1, PITX1 and SF1. PLoS One 5(5):e10646
57. Joerger AC, Fersht AR (2007) Structural biology of the tumor suppressor p53 and cancerassociated mutants. Adv Cancer Res 97:1-23
58. Cho Y, Gorina S, Jeffrey PD, Pavletich NP (1994) Crystal structure of a p53 tumor suppressor- DNA complex: Understanding tumorigenic mutations. Science 265(5170):346-355
59. Amador FJ, Liu S, Ishiyama N, Plevin MJ, Wilson A, MacLennan DH et al (2009) Crystal structure of type I ryanodine receptor amino-terminal beta-trefoil domain reveals a diseaseassociated mutation "hot spot" loop. Proc Natl Acad Sci USA 106(27):11040-11044
60. Li S, Duan J, Li D, Yang B, Dong M, Ye K (2011) Reconstitution and structural analysis of the yeast box H/ACA RNA-guided pseudouridine synthase. Genes Dev 25(22):2409-2421
61. Picaud S, Kavanagh KL, Yue WW, Lee WH, Muller-Knapp S, Gileadi O et al (2011) Structural basis of fumarate hydratase deficiency. J Inherit Metab Dis 34(3):671-676
62. Lee WH, Yue WW, Raush E, Totrov M, Abagyan R, Oppermann U et al (2011) Interactive JIMD articles using the iSee concept: Turning a new page on structural biology data. J Inherit Metab Dis 34(3):565-567
63. Lahiry P, Torkamani A, Schork NJ, Hegele RA (2010) Kinase mutations in human disease: Interpreting genotype-phenotype relationships. Nat Rev Genet 11(1):60-74
64. Gong S, Blundell TL (2010) Structural and functional restraints on the occurrence of single amino acid variations in human proteins. PLoS One 5(2):e9186
65. Hurst JM, McMillan LE, Porter CT, Allen J, Fakorede A, Martin AC (2009) The SAAPdb web resource: A large-scale structural analysis of mutant proteins. Hum Mutat 30(4):616-624
66. Khan S, Vihinen M (2007) Spectrum of disease-causing mutations in protein secondary structures. BMC Struct Biol 7:56
67. Hopkins AL, Groom CR (2002) The druggable genome. Nat Rev Drug Discov 1(9):727-730
68. Overington JP, Al-Lazikani B, Hopkins AL (2006) How many drug targets are there Nat Rev Drug Discov 5(12):993-996
69. Imming P, Sinning C, Meyer A (2006) Drugs, their targets and the nature and number of drug targets. Nat Rev Drug Discov 5(10):821-834
70. Rask-Andersen M, Almen MS, Schioth HB (2011) Trends in the exploitation of novel drug targets. Nat Rev Drug Discov 10(8):579-590
71. Morgan S, Grootendorst P, Lexchin J, Cunningham C, Greyson D (2011) The cost of drug development: A systematic review. Health Policy 100(1):4-17
72. Paul SM, Mytelka DS, Dunwiddie CT, Persinger CC, Munos BH, Lindborg SR et al (2010) How to improve R&D productivity: The pharmaceutical industry's grand challenge. Nat Rev Drug Discov 9(3):203-214. doi:10.1038/nrd3078
73. Hassall CH, Krohn A, Moody CJ, Thomas WA (1982) The design of a new group of angiotensin-converting enzyme inhibitors. FEBS Lett 147(2):175-179
74. Lapatto R, Blundell T, Hemmings A, Overington J, Wilderspin A, Wood S et al (1989) X-Ray analysis of HIV-1 proteinase at 2.7 A resolution confirms structural homology among retroviral enzymes. Nature 342(6247):299-302
75. Miller M, Schneider J, Sathyanarayana BK, Toth MV, Marshall GR, Clawson L et al (1989) Structure of complex of synthetic HIV-1 protease with a substrate-based inhibitor at 2.3 A resolution. Science 246(4934):1149-1152
76. Supuran CT, Scozzafava A, Casini A (2003) Carbonic anhydrase inhibitors. Med Res Rev 23 (2):146-189
77. von Itzstein M, Wu W-Y, Kok GB, Pegg MS, Dyason JC, Jin B et al (1993) Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature 363(6428):418-423. doi:10.1038/363418a0
78. Lew W, Chen X, Kim CU (2000) Discovery and development of GS 4104 (oseltamivir) an orally active influenza neuraminidase inhibitor. Curr Med Chem 7(6):663-672
79. Tokarski JS, Newitt JA, Chang CY, Cheng JD, Wittekind M, Kiefer SE et al (2006) The structure of Dasatinib (BMS-354825) bound to activated ABL kinase domain elucidates its inhibitory activity against imatinib-resistant ABL mutants. Cancer Res 66(11):5790-5797
80. Schindler T, Bornmann W, Pellicena P, Miller WT, Clarkson B, Kuriyan J (2000) Structural mechanism for STI-571 inhibition of abelson tyrosine kinase. Science 289(5486):1938-1942
81. Chen L, Jiao ZH, Zheng LS, Zhang YY, Xie ST, Wang ZX et al (2009) Structural insight into the autoinhibition mechanism of AMP-activated protein kinase. Nature 459(7250):1146-1149
82. Yuan P, Bartlam M, Lou Z, Chen S, Zhou J, He X et al (2009) Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 458(7240):909-913
83. Williams PA, Cosme J, Vinkovic DM, Ward A, Angove HC, Day PJ et al (2004) Crystal structures of human cytochrome P450 3A4 bound to metyrapone and progesterone. Science 305(5684):683-686
84. Zhang H, Tweel B, Li J, Tong L (2004) Crystal structure of the carboxyltransferase domain of acetyl-coenzyme A carboxylase in complex with CP-640186. Structure 12(9):1683-1691
85. Warne T, Serrano-Vega MJ, Baker JG, Moukhametzianov R, Edwards PC, Henderson R et al (2008) Structure of a beta1-adrenergic G-protein-coupled receptor. Nature 454 (7203):486-491
86. Cammer SA, Hoffman BT, Speir JA, Canady MA, Nelson MR, Knutson S et al (2003) Structure-based active site profiles for genome analysis and functional family subclassification. J Mol Biol 334(3):387-401
87. Grabowski M, Chruszcz M, Zimmerman MD, Kirillova O, Minor W (2009) Benefits of structural genomics for drug discovery research. Infect Disord Drug Targets 9(5):459-474
88. Shin DH, Hou J, Chandonia JM, Das D, Choi IG, Kim R et al (2007) Structure-based inference of molecular functions of proteins of unknown function from Berkeley Structural Genomics Center. J Struct Funct Genomics 8(2-3):99-105
89. Weigelt J (2010) Structural genomics-impact on biomedicine and drug discovery. Exp Cell Res 316(8):1332-1338
90. Dessailly BH, Nair R, Jaroszewski L, Fajardo JE, Kouranov A, Lee D et al (2009) PSI-2: Structural genomics to cover protein domain family space. Structure 17(6):869-881
91. Chim N, Habel JE, Johnston JM, Krieger I, Miallau L, Sankaranarayanan R et al (2011) The TB structural genomics consortium: A decade of progress. Tuberculosis (Edinb) 91 (2):155-172
92. Ehebauer MT, Wilmanns M (2011) The progress made in determining the Mycobacterium tuberculosis structural proteome. Proteomics 11(15):3128-3133
93. Yue WW, Oppermann U (2011) High-throughput structural biology of metabolic enzymes and its impact on human diseases. J Inherit Metab Dis 34(3):575-581
94. Edwards A (2009) Large-scale structural biology of the human proteome. Annu Rev Biochem 78:541-568
95. Filippakopoulos P, Qi J, Picaud S, Shen Y, Smith WB, Fedorov O et al (2010) Selective inhibition of BET bromodomains. Nature 468(7327):1067-1073
96. Perot S, Sperandio O, Miteva MA, Camproux AC, Villoutreix BO (2010) Druggable pockets and binding site centric chemical space: A paradigm shift in drug discovery. Drug Discov Today 15(15-16):656-667
97. Hammes-Schiffer S, Benkovic SJ (2006) Relating protein motion to catalysis. Annu Rev Biochem 75:519-541
98. Keller TH, Pichota A, Yin Z (2006) A practical view of druggability. Curr Opin Chem Biol 10(4):357-361
99. Lipinski CA, Lombardo F, Dominy BW, Feeney PJ (2001) Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 46(1-3):3-26
100. Hajduk PJ, Huth JR, Fesik SW (2005) Druggability indices for protein targets derived from NMR-based screening data. J Med Chem 48(7):2518-2525
101. Cheng AC, Coleman RG, Smyth KT, Cao Q, Soulard P, Caffrey DR et al (2007) Structurebased maximal affinity model predicts small-molecule druggability. Nat Biotechnol 25(1):71-75
102. Ciulli A, Williams G, Smith AG, Blundell TL, Abell C (2006) Probing hot spots at proteinligand binding sites: A fragment-based approach using biophysical methods. J Med Chem 49(16):4992-5000
103. Wells JA, McClendon CL (2007) Reaching for high-hanging fruit in drug discovery at protein-protein interfaces. Nature 450(7172):1001-1009. doi:10.1038/nature06526
104. Bleicher KH, Bohm HJ, Muller K, Alanine AI (2003) Hit and lead generation: Beyond highthroughput screening. Nat Rev Drug Discov 2(5):369-378
105. Macarron R, Banks MN, Bojanic D, Burns DJ, Cirovic DA, Garyantes T et al (2011) Impact of high-throughput screening in biomedical research. Nat Rev Drug Discov 10(3):188-195. doi:10.1038/nrd3368
106. Klebe G (2006) Virtual ligand screening: Strategies, perspectives and limitations. Drug Discov Today 11(13-14):580-594
107. Kalyaanamoorthy S, Chen YP (2011) Structure-based drug design to augment hit discovery. Drug Discov Today 16(17-18):831-839
108. Cavasotto CN, Ortiz MA, Abagyan RA, Piedrafita FJ (2006) In silico identification of novel EGFR inhibitors with antiproliferative activity against cancer cells. Bioorg Med Chem Lett 16(7):1969-1974
109. Dooley AJ, Shindo N, Taggart B, Park JG, Pang YP (2006) From genome to drug lead: Identification of a small-molecule inhibitor of the SARS virus. Bioorg Med Chem Lett 16 (4):830-833
110. McLean LR, Zhang Y, Degnen W, Peppard J, Cabel D, Zou C et al (2010) Discovery of novel inhibitors for DHODH via virtual screening and X-ray crystallographic structures. Bioorg Med Chem Lett 20(6):1981-1984
111. Ferreira RS, Simeonov A, Jadhav A, Eidam O, Mott BT, Keiser MJ et al (2010) Complementarity between a docking and a high-throughput screen in discovering new cruzain inhibitors. J Med Chem 53(13):4891-4905
112. SchneiderG,HartenfellerM,ReutlingerM, Tanrikulu Y, Proschak E, Schneider P (2009) Voyages to the (un)known: Adaptive design of bioactive compounds. Trends Biotechnol 27(1):18-26
113. Hartenfeller M, Schneider G (2011) De novo drug design. Methods Mol Biol 672:299-323
114. Fink T, Bruggesser H, Reymond JL (2005) Virtual exploration of the small-molecule chemical universe below 160 Daltons. Angew Chem Int Ed Engl 44(10):1504-1508
115. Heikkila T, Thirumalairajan S, Davies M, Parsons MR, McConkey AG, Fishwick CW et al (2006) The first de novo designed inhibitors of Plasmodium falciparum dihydroorotate dehydrogenase. Bioorg Med Chem Lett 16(1):88-92
116. Ni S, Yuan Y, Huang J, Mao X, Lv M, Zhu J et al (2009) Discovering potent small molecule inhibitors of cyclophilin A using de novo drug design approach. J Med Chem 52(17):5295-5298
117. Blundell TL, Jhoti H, Abell C (2002) High-throughput crystallography for lead discovery in drug design. Nat Rev Drug Discov 1(1):45-54
118. Hann MM, Leach AR, Harper G (2001) Molecular complexity and its impact on the probability of finding leads for drug discovery. J Chem Inf Comput Sci 41(3):856-864
119. Hartshorn MJ, Murray CW, Cleasby A, Frederickson M, Tickle IJ, Jhoti H (2005) Fragmentbased lead discovery using X-ray crystallography. J Med Chem 48(2):403-413
120. Shuker SB, Hajduk PJ, Meadows RP, Fesik SW (1996) Discovering high-affinity ligands for proteins: SAR by NMR. Science 274(5292):1531-1534
121. Wada CK, Holms JH, Curtin ML, Dai Y, Florjancic AS, Garland RB et al (2002) Phenoxyphenyl sulfone N-formylhydroxylamines (retrohydroxamates) as potent, selective, orally bioavailable matrix metalloproteinase inhibitors. J Med Chem 45(1):219-232
122. Howard S, Berdini V, Boulstridge JA, Carr MG, Cross DM, Curry J et al (2009) Fragmentbased discovery of the pyrazol-4-yl urea (AT9283), a multitargeted kinase inhibitor with potent aurora kinase activity. J Med Chem 52(2):379-388
123. Wyatt PG, Woodhead AJ, Berdini V, Boulstridge JA, Carr MG, Cross DM et al (2008) Identification of N-(4-piperidinyl)-4-(2,6-dichlorobenzoylamino)-1H- pyrazole-3-carboxamide (AT7519), a novel cyclin dependent kinase inhibitor using fragment-based X-ray crystallography and structure based drug design. J Med Chem 51(16):4986-4999
124. Artis DR, Lin JJ, Zhang C, Wang W, Mehra U, Perreault M et al (2009) Scaffold-based discovery of indeglitazar, a PPAR pan-active anti-diabetic agent. Proc Natl Acad Sci USA 106(1):262-267
125. de Kloe GE, Bailey D, Leurs R, de Esch IJ (2009) Transforming fragments into candidates: Small becomes big in medicinal chemistry. Drug Discov Today 14(13-14):630-646
126. Strong M, Sawaya MR, Wang S, Phillips M, Cascio D, Eisenberg D (2006) Toward the structural genomics of complexes: Crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis. Proc Natl Acad Sci USA 103(21):8060-8065
127. Brooun A, Foster SA, Chrencik JE, Chien EY, Kolatkar AR, Streiff M et al (2007) Remedial strategies in structural proteomics: Expression, purification, and crystallization of the Vav1/ Rac1 complex. Protein Expr Purif 53(1):51-62
128. Mukherjee S, Zhang Y (2011) Protein-protein complex structure predictions by multimeric threading and template recombination. Structure 19(7):955-966
129. Wells JA, McClendon CL (2007) Reaching for high-hanging fruit in drug discovery at protein-protein interfaces. Nature 450(7172):1001-1009
130. Rosenbaum DM, Cherezov V, Hanson MA, Rasmussen SG, Thian FS, Kobilka TS et al (2007) GPCR engineering yields high-resolution structural insights into beta2-adrenergic receptor function. Science 318(5854):1266-1273
131. Cherezov V, Rosenbaum DM, Hanson MA, Rasmussen SG, Thian FS, Kobilka TS et al (2007) High-resolution crystal structure of an engineered human beta2-adrenergic G proteincoupled receptor. Science 318(5854):1258-1265
132. Jaakola VP, Griffith MT, Hanson MA, Cherezov V, Chien EY, Lane JR et al (2008) The 2.6 angstrom crystal structure of a human A2A adenosine receptor bound to an antagonist. Science 322(5905):1211-1217
133. Wu B, Chien EY, Mol CD, Fenalti G, Liu W, Katritch V et al (2010) Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science 330 (6007):1066-1071
134. Chien EY, Liu W, Zhao Q, Katritch V, Han GW, Hanson MA et al (2010) Structure of the human dopamine D3 receptor in complex with a D2/D3 selective antagonist. Science 330 (6007):1091-1095
135. Chaudhuri TK, Paul S (2006) Protein-misfolding diseases and chaperone-based therapeutic approaches. FEBS J 273(7):1331-1349
136. Pey AL, Ying M, Cremades N, Velazquez-Campoy A, Scherer T, Thony B et al (2008) Identification of pharmacological chaperones as potential therapeutic agents to treat phenylketonuria. J Clin Invest 118(8):2858-2867
137. Bateman KS, Cherney MM, Mahuran DJ, Tropak M, James MN (2011) Crystal structure of beta-hexosaminidase B in complex with pyrimethamine, a potential pharmacological chaperone. J Med Chem 54(5):1421-1429
138. Lieberman RL, Wustman BA, Huertas P, Powe AC Jr, Pine CW, Khanna R et al (2007) Structure of acid beta-glucosidase with pharmacological chaperone provides insight into Gaucher disease. Nat Chem Biol 3(2):101-107