Discovery and characterization of Non-ATP site inhibitors of the mitogen activated protein (MAP) kinases

ACS Chemical Biology

Volumn 6, Issue 3, 2011, Pages 234-244

  Comess, Kenneth M ^a   Sun, Chaohong ^a   Abad Zapatero, Cele ^a   Goedken, Eric R ^a   Gum, Rebecca J ^a   Borhani, David W ^a   Argiriadi, Maria ^a   Groebe, Duncan R ^a   Jia, Yong ^a   Clampit, Jill E ^a   Haasch, Deanna L ^a   Smith, Harriet T ^a   Wang, Sanyi ^a   Song, Danying ^a   Coen, Michael L ^a   Cloutier, Timothy E ^a   Tang, Hua ^a   Cheng, Xueheng ^a   Quinn, Christopher ^a   Liu, Bo ^a   Xin, Zhili ^a   Liu, Gang ^a   Fry, Elizabeth H ^a   Stoll, Vincent ^a   Ng, Teresa I ^a   Banach, David ^a   Marcotte, Doug ^a   Burns, David J ^a   Calderwood, David J ^a   Hajduk, Philip J ^a   more..

^a ABBOTT LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE DERIVATIVE; ADENOSINE TRIPHOSPHATE INHIBITOR; ADIPONECTIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 14; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; ROSIGLITAZONE; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE 1; UNCLASSIFIED DRUG;

ADIPOCYTE; ARTICLE; BINDING SITE; DRUG STRUCTURE; DRUG TARGETING; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LIGAND BINDING; LIVER CELL; MOLECULAR LIBRARY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SURFACE PROPERTY;

ADENOSINE TRIPHOSPHATE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DRUG DISCOVERY; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 8; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN KINASE INHIBITORS; SMALL MOLECULE LIBRARIES; STEREOISOMERISM; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 79955617610     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb1002619     Document Type: Article

References (67)

1. Zhang, J., Yang, P. L., and Gray, N. S. (2009) Targeting cancer with small molecule kinase inhibitors. Nat. Rev. Cancer 9, 28-39.
2. Landry, Y., and Gies, J. P. (2008) Drugs and their molecular targets: an updated overview. Fundam. Clin. Pharmacol. 22, 1-18. (Pubitemid 351171284)
3. Fabian, M. A., Biggs, W. H., 3rd, Treiber, D. K., Atteridge, C. E., Azimioara, M. D., Benedetti, M. G., Carter, T. A., Ciceri, P., Edeen, P. T., Floyd, M., Ford, J. M., Galvin, M., Gerlach, J. L., Grotzfeld, R. M., Herrgard, S., Insko, D. E., Insko, M. A., Lai, A. G., Lelias, J. M., Mehta, S. A., Milanov, Z. V., Velasco, A. M., Wodicka, L. M., Patel, H. K., Zarrinkar, P. P., and Lockhart, D. J. (2005) A small molecule-kinase interaction map for clinical kinase inhibitors. Nat. Biotechnol. 23, 329-336. (Pubitemid 41094421)
4. Oishi, J., Han, X., Kang, J.-H., Asami, Y., Mori, T., Niidome, T., and Katayama, Y. (2008) High-throughput colorimetric detection of tyrosine kinase inhibitors based on the aggregation of gold nanoparticles. Anal. Biochem. 373, 161-163. (Pubitemid 350251325)
5. Card, A., Caldwell, C., Min, H., Lokchander, B., Hualin, X., Sciabola, S., Kamath, A. V., Clugston, S. L., Tschantz, W. R., Leyu, W., and Moshinsky, D. J. (2009) High-throughput biochemical kinase selectivity assays: panel development and screening applications. J. Biomol. Screening 14, 31-42.
6. Hopkins, A. L., Mason, J. S., and Overington, J. P. (2006) Can we rationally design promiscuous drugs? Curr. Opin. Struct. Biol. 16, 127-136. (Pubitemid 43221881)
7. Bilanges, B., Torbett, N., and Vanhaesebroeck, B. (2008) Killing two kinase families with one stone. Nat. Chem. Biol. 4, 648-649.
8. Manning, G., Whyte, D. B., Martinez, R., Hunter, T., and Sudarsanam, S. (2002) The protein kinase complement of the human genome. Science 298, 1912-1934. (Pubitemid 35425239)
9. Fedorov, O., Marsden, B., Pogacic, V., Rellos, P., Muller, S., Bullock, A. N., Schwaller, J., Sundstrom, M., and Knapp, S. (2007) A systematic interaction map of validated kinase inhibitors with Ser/Thr kinases. Proc. Natl. Acad. Sci. U.S.A. 104, 20523-20528.
10. Widakowich, C., de Castro, G., Jr., de Azambuja, E., Dinh, P., and Awada, A. (2007) Review: side effects of approved molecular targeted therapies in solid cancers. Oncologist 12, 1443-1455.
11. Akritopoulou-Zanze, I., and Hajduk, P. J. (2009) Kinasetargeted libraries: the design and synthesis of novel, potent, and selective kinase inhibitors. Drug Discovery Today 14, 291-297.
12. Bogoyevitch, M. A., and Arthur, P. G. (2008) Inhibitors of c-Jun N-terminal kinases: JuNK no more? Biochim. Biophys. Acta 1784, 76-93.
13. Aguirre, V., Uchida, T., Yenush, L., Davis, R., and White, M. F. (2000) The c-Jun NH(2)-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser(307). J. Biol. Chem. 275, 9047-9054. (Pubitemid 30180265)
14. Aguirre, V., Werner, E. D., Giraud, J., Lee, Y. H., Shoelson, S. E., and White, M. F. (2002) Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J. Biol. Chem. 277, 1531-1537. (Pubitemid 34968910)
15. Hirosumi, J., Tuncman, G., Chang, L., Gorgun, C. Z., Uysal, K. T., Maeda, K., Karin, M., and Hotamisligil, G. S. (2002) A central role for JNK in obesity and insulin resistance. Nature 420, 333-336. (Pubitemid 35398190)
16. Bennett, B. L., Sasaki, D. T., Murray, B. W., O'Leary, E. C., Sakata, S. T., Xu, W., Leisten, J. C., Motiwala, A., Pierce, S., Satoh, Y., Bhagwat, S. S., Manning, A. M., and Anderson, D. W. (2001) SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. U.S.A. 98, 13681-13686. (Pubitemid 33115958)
17. Heo, Y. S., Kim, S. K., Seo, C. I., Kim, Y. K., Sung, B. J., Lee, H. S., Lee, J. I., Park, S. Y., Kim, J. H., Hwang, K. Y., Hyun, Y. L., Jeon, Y. H., Ro, S., Cho, J. M., Lee, T. G., and Yang, C. H. (2004) Structural basis for the selective inhibition of JNK1 by the scaffolding protein JIP1 and SP600125. EMBO J. 23, 2185-2195. (Pubitemid 38833228)
18. Kaneto,H.,Nakatani, Y., Miyatsuka, T., Kawamori,D.,Matsuoka, T. A., Matsuhisa, M., Kajimoto, Y., Ichijo, H., Yamasaki, Y., and Hori, M. (2004) Possible novel therapy for diabetes with cell-permeable JNKinhibitory peptide. Nat. Med. 10, 1128-1132. (Pubitemid 39424876)
19. Ruckle, T., Biamonte, M., Grippi-Vallotton, T., Arkinstall, S., Cambet, Y., Camps, M., Chabert, C., Church, D. J., Halazy, S., Jiang, X., Martinou, I., Nichols, A., Sauer, W., and Gotteland, J. P. (2004) Design, synthesis, and biological activity of novel, potent, and selective (benzoylaminomethyl) thiophene sulfonamide inhibitors of c-Jun-Nterminal kinase. J. Med. Chem. 47, 6921-6934. (Pubitemid 40053780)
20. Gaillard, P., Jeanclaude-Etter, I., Ardissone, V., Arkinstall, S., Cambet, Y., Camps, M., Chabert, C., Church, D., Cirillo, R., Gretener, D., Halazy, S., Nichols, A., Szyndralewiez, C., Vitte, P. A., and Gotteland, J. P. (2005) Design and synthesis of the first generation of novel potent, selective, and in vivo active (benzothiazol-2-yl)acetonitrile inhibitors of the c-Jun N-terminal kinase. J. Med. Chem. 48, 4596-4607. (Pubitemid 40993420)
21. Stocks, M. J., Barber, S., Ford, R., Leroux, F., St-Gallay, S., Teague, S., and Xue, Y. (2005) Structure-driven HtL: design and synthesis of novel aminoindazole inhibitors of c-Jun N-terminal kinase activity. Bioorg. Med. Chem. Lett. 15, 3459-3462. (Pubitemid 40835756)
22. Liu, M., Xin, Z., Clampit, J. E., Wang, S., Gum, R. J., Haasch, D. L., Trevillyan, J. M., Abad-Zapatero, C., Fry, E. H., Sham, H. L., and Liu, G. (2006) Synthesis and SAR of 1,9-dihydro-9-hydroxypyrazolo- [3,4-b]quinolin-4- ones as novel, selective c-Jun N-terminal kinase inhibitors. Bioorg. Med. Chem. Lett. 16, 2590-2594.
23. Szczepankiewicz, B. G., Kosogof, C., Nelson, L. T., Liu, G., Liu, B., Zhao, H., Serby, M. D., Xin, Z., Liu, M., Gum, R. J., Haasch, D. L., Wang, S., Clampit, J. E., Johnson, E. F., Lubben, T. H., Stashko, M. A., Olejniczak, E. T., Sun, C., Dorwin, S. A., Haskins, K., Abad-Zapatero, C., Fry, E. H., Hutchins, C. W., Sham, H. L., Rondinone, C. M., and Trevillyan, J. M. (2006) Aminopyridine-based c-Jun N-terminal kinase inhibitors with cellular activity and minimal cross-kinase activity. J. Med. Chem. 49, 3563-3580. (Pubitemid 43902462)
24. Zhao, H., Serby, M. D., Xin, Z., Szczepankiewicz, B. G., Liu, M., Kosogof, C., Liu, B., Nelson, L. T., Johnson, E. F., Wang, S., Pederson, T., Gum, R. J., Clampit, J. E., Haasch, D. L., Abad-Zapatero, C., Fry, E. H., Rondinone, C., Trevillyan, J. M., Sham, H. L., and Liu, G. (2006) Discovery of potent, highly selective, and orally bioavailable pyridine carboxamide c-Jun NH2-terminal kinase inhibitors. J. Med. Chem. 49, 4455-4458. (Pubitemid 44162671)
25. Liu, M., Wang, S., Clampit, J. E., Gum, R. J., Haasch, D. L., Rondinone, C. M., Trevillyan, J. M., Abad-Zapatero, C., Fry, E. H., Sham, H. L., and Liu, G. (2007) Discovery of a new class of 4-anilinopyrimidines as potent c-Jun N-terminal kinase inhibitors: Synthesis and SAR studies. Bioorg. Med. Chem. Lett. 17, 668-672. (Pubitemid 46108565)
26. Asano, Y., Kitamura, S., Ohra, T., Aso, K., Igata, H., Tamura, T., Kawamoto, T., Tanaka, T., Sogabe, S., Matsumoto, S., Yamaguchi, M., Kimura, H., and Itoh, F. (2008) Discovery, synthesis and biological evaluation of isoquinolones as novel and highly selective JNK inhibitors (1). Bioorg. Med. Chem. 16, 4715-4732. (Pubitemid 351539017)
27. Stebbins, J. L., De, S. K., Machleidt, T., Becattini, B., Vazquez, J., Kuntzen, C., Chen, L. H., Cellitti, J. F., Riel-Mehan, M., Emdadi, A., Solinas, G., Karin, M., and Pellecchia, M. (2008) Identification of a new JNK inhibitor targeting the JNK-JIP interaction site. Proc. Natl. Acad. Sci. U.S.A. 105, 16809-16813.
28. Comess, K. M., Schurdak, M. E., Voorbach, M. J., Coen, M., Trumbull, J. D., Yang, H., Gao, L., Tang, H., Cheng, X., Lerner, C. G., McCall, J. O., Burns, D. J., and Beutel, B. A. (2006) An ultraefficient affinity-based high-throughout screening process: application to bacterial cell wall biosynthesis enzyme MurF. J. Biomol. Screening 11, 743-754. (Pubitemid 44562315)
29. Comess, K. M., Trumbull, J. D., Park, C., Chen, Z., Judge, R. A., Voorbach, M. J., Coen, M., Gao, L., Tang, H., Kovar, P., Cheng, X., Schurdak, M. E., Zhang, H., Sowin, T., and Burns, D. J. (2006) Kinase drug discovery by affinity selection/mass spectrometry (ASMS): application to DNA damage checkpoint kinase Chk1. J. Biomol. Screening 11, 755-764. (Pubitemid 44562316)
30. Xie, X., Gu, Y., Fox, T., Coll, J. T., Fleming, M. A., Markland, W., Caron, P. R., Wilson, K. P., and Su, M. S. (1998) Crystal structure of JNK3: a kinase implicated in neuronal apoptosis. Structure 6, 983-991. (Pubitemid 28397920)
31. Scapin, G., Patel, S. B., Lisnock, J., Becker, J. W., and LoGrasso, P. V. (2003) The structure of JNK3 in complex with small molecule inhibitors: structural basis for potency and selectivity. Chem. Biol. 10, 705-712. (Pubitemid 37089845)
32. Dominguez, C., Powers, D. A., and Tamayo, N. (2005) p38 MAP kinase inhibitors: many are made, but few are chosen. Curr. Opin. Drug Discovery Dev. 8, 421-430. (Pubitemid 40921741)
33. Genovese, M. C. (2009) Inhibition of p38: Has the fat lady sung? Arthritis Rheum. 60, 317-320.
34. Cottrell, J. A., Meyenhofer, M., Medicherla, S., Higgins, L., and O'Connor, J. P. (2009) Analgesic effects of p38 kinase inhibitor treatment on bone fracture healing. Pain 142, 116-126.
35. Davies, S. P., Reddy, H., Caivano, M., and Cohen, P. (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351, 95-105.
36. Lee, M. R., and Dominguez, C. (2005) MAP kinase p38 inhibitors: clinical results and an intimate look at their interactions with p38alpha protein. Curr. Med. Chem. 12, 2979-2994. (Pubitemid 41672487)
37. Pargellis, C., Tong, L., Churchill, L., Cirillo, P. F., Gilmore, T., Graham, A. G., Grob, P. M., Hickey, E. R., Moss, N., Pav, S., and Regan, J. (2002) Inhibition of p38 MAP kinase by utilizing a novel allosteric binding site. Nat. Struct. Biol. 9, 268-272. (Pubitemid 34289898)
38. Coleman, R. G., Salzberg, A. C., and Cheng, A. C. (2006) Structure-based identification of small molecule binding sites using a free energy model. J. Chem. Inf. Model 46, 2631-2637. (Pubitemid 46008133)
39. Jackson, J. R., Bolognese, B., Hillegass, L., Kassis, S., Adams, J., Griswold, D. E., and Winkler, J. D. (1998) Pharmacological effects of SB 220025, a selective inhibitor of P38 mitogen-activated protein kinase, in angiogenesis and chronic inflammatory disease models. J. Pharmacol. Exp. Ther. 284, 687-692. (Pubitemid 28086659)
40. Karaman, M. W., Herrgard, S., Treiber, D. K., Gallant, P., Atteridge, C. E., Campbell, B. T., Chan, K. W., Ciceri, P., Davis, M. I., Edeen, P. T., Faraoni, R., Floyd, M., Hunt, J. P., Lockhart, D. J., Milanov, Z. V., Morrison, M. J., Pallares, G., Patel, H. K., Pritchard, S., Wodicka, L. M., and Zarrinkar, P. P. (2008) A quantitative analysis of kinase inhibitor selectivity. Nat. Biotechnol. 26, 127-132.
41. Cuenda, A., Rouse, J., Doza, Y. N., Meier, R., Cohen, P., Gallagher, T. F., Young, P. R., and Lee, J. C. (1995) SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 364, 229-233.
42. Wang, Z., Harkins, P. C., Ulevitch, R. J., Han, J., Cobb,M. H., and Goldsmith, E. J. (1997) The structure of mitogen-activated protein kinase p38 at 2.1-A resolution. Proc. Natl. Acad. Sci. U.S.A. 94, 2327-2332.
43. Diskin, R., Engelberg, D., and Livnah, O. (2008) A novel lipid binding site formed by the MAP kinase insert in p38 alpha. J. Mol. Biol. 375, 70-79. (Pubitemid 350160682)
44. Wang, Z., Canagarajah, B. J., Boehm, J. C., Kassisa, S., Cobb, M. H., Young, P. R., Abdel-Meguid, S., Adams, J. L., and Goldsmith, E. J. (1998) Structural basis of inhibitor selectivity in MAP kinases. Structure 6, 1117-1128. (Pubitemid 28434115)
45. Wilson, K. P., Fitzgibbon, M. J., Caron, P. R., Griffith, J. P., Chen, W., McCaffrey, P. G., Chambers, S. P., and Su, M. S. (1996) Crystal structure of p38 mitogen-activated protein kinase. J. Biol. Chem. 271, 27696-27700. (Pubitemid 26367339)
46. White, A., Pargellis, C. A., Studts, J. M., Werneburg, B. G., and Farmer, B. T., 2nd (2007) Molecular basis of MAPK-activated protein kinase 2:p38 assembly. Proc. Natl. Acad. Sci. U.S.A. 104, 6353-6358. (Pubitemid 47186098)
47. Lebakken, C. S., Riddle, S. M., Singh, U., Frazee, W. J., Eliason, H. C., Gao, Y., Reichling, L. J., Marks, B. D., and Vogel, K. W. (2009) Development and applications of a broad-coverage, TR-FRET-based kinase binding assay platform. J. Biomol. Screening 14, 924-935.
48. Huth, J. R., Yu, L., Collins, I., Mack, J., Mendoza, R., Isaac, B., Braddock, D. T., Muchmore, S. W., Comess, K. M., Fesik, S. W., Clore, G. M., Levens, D., and Hajduk, P. J. (2004) NMR-driven discovery of benzoylanthranilic acid inhibitors of far upstream element binding protein binding to the human oncogene c-myc promoter. J. Med. Chem. 47, 4851-4857. (Pubitemid 39238259)
49. Qian, J., Voorbach, M. J., Huth, J. R., Coen, M. L., Zhang, H., Ng, S.-C., Comess, K. M., Petros, A. M., Rosenberg, S. H., Warrior, U., and Burns, D. J. (2004) Discovery of novel inhibitors of Bcl-xL using multiple high-throughput screening platforms. Anal. Biochem. 328, 131-138. (Pubitemid 38542928)
50. Kawai, M., BaMaung, N. Y., Fidanze, S. D., Erickson, S. A., Tedrow, J. S., Sanders, W. J., Vasudevan, A., Park, C., Hutchins, C., Comess, K. M., Kalvin, D., Wang, J., Zhang, Q., Lou, P., Tucker-Garcia, L., Bouska, J., Bell, R. L., Lesniewski, R., Henkin, J., and Sheppard, G. S. (2006) Development of sulfonamide compounds as potent methionine aminopeptidase type II inhibitors with antiproliferative properties. Bioorg. Med. Chem. Lett. 16, 3574-3577. (Pubitemid 43777096)
51. Lerner, C. G., Hajduk, P. J., Wagner, R., Wagenaar, F. L., Woodall, C., Gu, Y. G., Searle, X. B., Florjancic, A. S., Zhang, T., Clark, R. F., Cooper, C. S., Mack, J. C., Yu, L., Cai, M., Betz, S. F., Chovan, L. E., McCall, J. O., Black-Schaefer, C. L., Kakavas, S. J., Schurdak, M. E., Comess, K. M., Walter, K. A., Edalji, R., Dorwin, S. A., Smith, R. A., Hebert, E. J., Harlan, J. E., Metzger, R. E., Merta, P. J., Baranowski, J. L., Coen, M. L., Thornewell, S. J., Shivakumar, A. G., Saiki, A. Y., Soni, N., Bui, M., Balli, D. J., Sanders, W. J., Nilius, A. M., Holzman, T. F., Fesik, S. W., and Beutel, B. A. (2007) From bacterial genomes to novel antibacterial agents: discovery, characterization, and antibacterial activity of compounds that bind to HI0065 (YjeE) from Haemophilus influenzae. Chem. Biol. Drug Des. 69, 395-404. (Pubitemid 46955535)
52. Wendt, M. D., Sun, C., Kunzer, A., Sauer, D., Sarris, K., Hoff, E., Yu, L., Nettesheim, D. G., Chen, J., Jin, S., Comess, K. M., Fan, Y., Anderson, S. N., Isaac, B., Olejniczak, E. T., Hajduk, P. J., Rosenberg, S. H., and Elmore, S. W. (2007) Discovery of a novel small molecule binding site of human survivin. Bioorg. Med. Chem. Lett. 17, 3122-3129. (Pubitemid 46702624)
53. Hajduk, P. J., Augeri, D. J., Mack, J., Mendoza, R., Yang, J., Betz, S. F., and Fesik, S. W. (2000) NMR-Based screening of proteins containing 13C-labeled methyl groups. J. Am. Chem. Soc. 122, 7898-7904. (Pubitemid 30659411)
54. Seidler, J., McGovern, S. L., Doman, T. N., and Shoichet, B. K. (2003) Identification and prediction of promiscuous aggregating inhibitors among known drugs. J. Med. Chem. 46, 4477-4486. (Pubitemid 37238749)
55. Feng, B. Y., and Shoichet, B. K. (2006) Synergy and antagonism of promiscuous inhibition in multiple-compound mixtures. J. Med. Chem. 49, 2151-2154.
56. Shoichet, B. K. (2006) Screening in a spirit haunted world. Drug Discovery Today 11, 607-615.
57. Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2, 661-665.
58. Hajduk, P. J., Gerfin, T., Boehlen, J. M., Haberli, M., Marek, D., and Fesik, S. W. (1999) High-throughput nuclear magnetic resonancebased screening. J. Med. Chem. 42, 2315-2317. (Pubitemid 29305164)
59. Gupta, S., Barrett, T., Whitmarsh, A. J., Cavanagh, J., Sluss, H. K., Derijard, B., and Davis, R. J. (1996) Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J. 15, 2760-2770. (Pubitemid 26176253)
60. Barr, R. K., Kendrick, T. S., and Bogoyevitch, M. A. (2002) Identification of the critical features of a small peptide inhibitor of JNK activity. J. Biol. Chem. 277, 10987-10997. (Pubitemid 34952855)
61. Vagin, A., and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025. (Pubitemid 127485985)
62. CCP4. (1994) The CCP4 Suite: Programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. D50, 760-763.
63. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000) The Protein Data Bank. Nucleic Acids Res. 28, 235-242. (Pubitemid 30047768)
64. Potterton, E., Briggs, P., Turkenburg, M., and Dodson, E. (2003) A graphical user interface to the CCP4 program suite. Acta Crystallogr. Sect. D: Biol. Crystallogr. 59, 1131-1137. (Pubitemid 36872348)
65. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr., Sect. A: Found. Crystallogr. 47, 110-119.
66. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D57, 240-255. (Pubitemid 27235885)
67. De, B., Winn,M., Zydowsky, T.M., Kerkman,D. J.,DeBernardis, J. F., Lee, J., Buckner, S.,Warner, R., Brune,M., Hancock, A., Opgenorth, T., and Marsh, K. (1992) Discovery of a novel class of orally active, nonpeptide angiotensin II antagonists. J. Med. Chem. 35, 3714-3717.