Winning the arms race by improving drug discovery against mutating targets

ACS Chemical Biology

Volumn 7, Issue 2, 2012, Pages 278-288

  Anderson, Amy C ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DELAVIRDINE; DIHYDROFOLATE REDUCTASE; EFAVIRENZ; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; GEFITINIB; MUTANT PROTEIN; NEVIRAPINE; NONNUCLEOSIDE REVERSE TRANSCRIPTASE INHIBITOR; OSELTAMIVIR; PROTEIN TYROSINE KINASE; PYRIMETHAMINE; PYRIMIDINE DERIVATIVE; RNA DIRECTED DNA POLYMERASE; SIALIDASE; SULFADOXINE; SULFAMETHOXAZOLE; TRIMETHOPRIM; UNCLASSIFIED DRUG; WZ 3146; WZ 4002; WZ 8040; ZANAMIVIR;

CRYSTAL STRUCTURE; DRUG TARGETING; ENZYME KINETICS; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MUTATION; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; REVIEW; STAPHYLOCOCCUS AUREUS; STEREOSPECIFICITY; STRUCTURE ANALYSIS; WILD TYPE;

ANIMALS; DRUG DISCOVERY; DRUG RESISTANCE; ENZYME INHIBITORS; HUMANS; MODELS, MOLECULAR; MUTATION; PROTEINS;

PLASMODIUM FALCIPARUM; STAPHYLOCOCCUS AUREUS;

EID: 84857584191     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb200394t     Document Type: Review

References (95)

1. Copeland, R., Harpel, M., and Tummino, P. (2007) Targeting enzyme inhibitors in drug discovery Expert Opin. Ther. Targets 11, 967-978 (Pubitemid 47054490)
2. Hopkins, A. and Groom, C. (2002) The druggable genome Nat. Rev. Drug Discovery 1, 727-730 (Pubitemid 37361545)
3. Soskine, M. and Tawfik, D. (2010) Mutational effects and the evolution of new protein functions Nat. Rev. Genetics 11, 572-582
4. Arahoni, A., Gaidudov, L., Khersonsky, O., Gould, S., Roodveldt, C., and Tawfik, D. (2005) The "evolvability" of promiscous protein functions Nat. Genet. 37, 73-76
5. Wang, X., Minasov, G., and Shoichet, B. (2002) Evolution of an antibiotic resistance enzyme constrained by stability and activity trade-offs J. Mol. Biol. 320, 85-95 (Pubitemid 34722236)
6. Falconer, S., Czarny, T., and Brown, E. (2011) Antibiotics as probes of biological complexity Nat. Chem. Biol. 7, 415-423
7. Staub, I. and Sieber, S. (2008) β-Lactams as selective chemical probes for the in vivo labeling of bacterial enzymes involved in cell wall biosynthesis, antibiotic resistance and virulence J. Am. Chem. Soc. 130, 13400-13409
8. Weinrich, D., Delaney, N., DePristo, M., and Hartl, D. (2006) Darwinian evolution can follow only very few mutational paths to fitter proteins Science 312, 111-114
9. Lozovsky, E., Chookajorn, T., Brown, K., Imwong, M., Shaw, P., Kamchonwongpaisan, S., Neafsey, D., Weinrich, D., and Hartl, D. (2009) Stepwise acquisition of pyrimethamine resistance in the malaria parasite Proc. Natl. Acad. Sci. U.S.A. 106, 12025-12030
10. Carneiro, M. and Hartl, D. (2010) Adaptive landscapes and protein evolution Proc. Natl. Acad. Sci. U.S.A. 107, 1747-1751
11. Colman, P. (2009) New antivirals and drug resistance Annu. Rev. Biochem. 78, 95-118
12. Kozisek, M., Bray, J., Rezacova, P., Saskova, K., Brynda, J., Pokorna, J., Mammano, F., Rulisek, L., and Konvalinka, J. (2007) Molecular analysis of the HIV-1 resistance development: enzymatic activities, crystal structures and thermodynamics of nelfinavir-resistance HIV protease mutants J. Mol. Biol. 374, 1005-1016 (Pubitemid 350052096)
13. Piana, S., Carloni, P., and Rothlisberger, U. (2002) Drug resistance in HIV-1 protease: flexibility-assisted mechanism of compensatory mutations Protein Sci. 11, 2392-2402
14. Shafer, R. and Schapiro, J. (2008) HIV-1 drug resistance mutations: an updated framework for the second decade of HAART AIDS Rev. 10, 67-84
15. Arribas, J. (2009) Drugs in traditional drug classes (nucleoside reverse transcriptase inhibitor/nonnucleoside reverse transcriptase inhibitor/protease inhibitors) with activity against drug -resistant virus (tipranavir, darunavir, etravirine) Curr. Opin. HIV AIDS 4, 507-512
16. Das, K., Clark, A. D., Lewi, P. J., Heeres, J., de Jonge, M. R., Koymans, L. M. H., Vinkers, H. M., Daeyaert, F., Ludovici, D. W., Kukla, M. J., De Corte, B., Kavash, R. W., Ho, C. Y., Ye, H., Lichtenstein, M. A., Andries, K., Pauwels, R., de Bethune, M.-P., Boyer, P. L., Clark, P., Hughes, S. H., Janssen, P. A. J., and Arnold, E. (2004) Roles of conformational and positional adaptability in structure-based design of TMC125-R165335 (etravirine) and related non-nucleoside reverse transcriptase inhibitors that are highly potent and effective against wild-type and drug-resistant HIV-1 Variants J. Med. Chem. 47, 2550-2560 (Pubitemid 38580092)
17. Gorre, M., Mohammed, M., Ellwood, K., Hsu, N., Paquette, R., Rao, N., and Sawyers, C. (2001) Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification Science 293, 876-880 (Pubitemid 32743979)
18. Krishnamurty, R. and Maly, D. (2010) Biochemical mechanisms of resistance to small-molecule protein kinase inhibitors ACS Chem. Biol. 5, 121-138
19. Azam, M., Seeliger, M., Gray, N., Kuriyan, J., and Daley, G. (2008) Activation of tyrosine kinases by mutation of the gatekeeper threonine Nat. Struct. Mol. Biol. 15, 1109-1118
20. Brooks, D., Wang, P., Read, M., Watkins, W., Sims, P., and Hyde, J. (1994) Sequence variation of the hydroxymethyldihydropterin pyrophosphokinase: dihydropteroate synthase gene in lines of the human malaria parasite, Plasmodium falciparum, with differing resistance to sulfadoxine Eur. J. Biochem. 224, 397-405 (Pubitemid 24282821)
21. deBeer, T., Louw, A., and Joubert, F. (2006) Elucidation of sulfadoxine resistance with structural models of the bifunctional Plasmodium falciparum dihydropterin pyrophosphokinase-dihydropteroate synthase Bioorg. Med. Chem. 14, 4433-4443 (Pubitemid 43728659)
22. Dasgupta, T., Chitnumsub, P., Kamchonwongpaisan, S., Maneeruttanarungroj, C., Nichols, S. E., Lyons, T. M., Tirado-Rives, J., Jorgensen, W. L., Yuthavong, Y., and Anderson, K. S. (2009) Exploiting structural analysis, in silico screening, and serendipity to identify novel inhibitors of drug-resistant Falciparum malaria ACS Chem. Biol. 4, 29-40
23. Sirawaraporn, W., Sathitkul, T., Sirawaraporn, R., Yuthavong, Y., and Santi, D. (1997) Antifolate-resistant mutants of Plasmodium falciparum dihydrofolate reductase Proc. Natl. Acad. Sci. U.S.A. 94, 1124-1129 (Pubitemid 27087815)
24. Yuvaniyama, J., Chitnumsub, P., Kamchonwongpaisan, S., Vanichtanankul, J., Sirawaraporn, W., Taylor, P., Walkinshaw, M., and Yuthavong, Y. (2003) Insights into antifolate resistance from malarial DHFR-TS structures Nat. Struct. Biol. 10, 357-365 (Pubitemid 36523270)
25. Oliveira, J., Pereira, J., Canduri, F., Rodrigues, N., DeSouza, O., DeAzevedo, W., Basso, L. A., and Santos, D. S. (2006) Crystallographic and pre-steady state kinetics structures on binding of NADH to wild-type and isoniazid-resistant enoyl-ACP(CoA) reductase enzyme from Mycobacterium tuberculosis J. Mol. Biol. 359, 646-666 (Pubitemid 43786403)
26. Vilcheze, C., Weisbrod, T., Chen, B., Kremer, L., Hazbon, M., Wang, F., Alland, D., Sacchettini, J., and Jacobs, W. (2005) Altered NADH/NAD+ ratio mediates coresistance to isoniazid and ethionamide in mycobacteria Antimicrob. Agents Chemother. 49, 708-720 (Pubitemid 40175684)
27. Dias, M. V. B., Vasconcelos, I. B., Prado, A. M. X., Fadel, V., Basso, L. A., de Azevedo, W. F., Jr., and Santos, D. S. (2007) Crystallographic studies on the binding of isonicotinyl-NAD adduct to wild-type and isoniazid resistant 2-trans-enoyl-ACP (CoA) reductase from Mycobacterium tuberculosis J. Struc. Biol. 159, 369-380 (Pubitemid 47348298)
28. Varghese, J. (1997) The Design of Anti-Influenza Virus Drugs from the X-Ray Molecular Structure of Influenza Virus Neuraminidase, in Structure-Based Drug Design: Diseases, Targets, Techniques and Development (Verrapandian, P., Ed.), pp 459-486, Marcel Dekker, New York.
29. Varghese, J., Epa, V., and Colman, P. (1995) Three-dimensional structure of the complex of 4-guanidino-Neu5Ac2en and influenza virus neuraminidase Protein Sci. 4, 1081-1087
30. Varghese, J., McKimm-Breschkin, J., Caldwell, J., Kortt, A., and Colman, P. (1992) The structure of the complex between influenza virus neuraminidase and sialic acid, the viral receptor Proteins 14, 327-332
31. Collins, P., Haire, L., Lin, Y., Liu, J., Russell, R., Walker, P., Skehel, J., Martin, S., Hay, A., and Gamblin, S. (2008) Crystal structures of oseltamivir-resistant influenza virus neuraminidase mutants Nature 453, 1258-1262
32. Varghese, J., Smith, P., Sollis, S., Blick, T., Saharabudhe, A., McKimm-Breschkin, J., and Colman, P. (1998) Drug design against a shifting target: a structural basis for resistance to inhibitors in a variant of influenza virus neuraminidase Structure 6, 735-746 (Pubitemid 28301207)
33. Frey, K., Liu, J., Lombardo, M., Bolstad, D., Wright, D., and Anderson, A. (2009) Crystal structures of wild-type and mutant methicillin-resistant Staphylococcus aureus dihydrofolate reductase reveal an alternative conformation of NADPH that may be linked to trimethoprim resistance J. Mol. Biol. 387, 1298-1308
34. Yun, C., Boggon, T., Li, Y., Woo, M., Greulich, H., Meyerson, M., and Eck, M. (2007) Structures of lung cancer-derived EGFR mutants and inhibitor complexes: mechanism of activation and insights into differential inhibitor sensitivity Cancer Cell 11, 217-227 (Pubitemid 46349842)
35. Podust, L., Poulos, T., and Waterman, M. (2001) Crystal strucutre of cytochrome P450 14α-sterol demethylase (CYP51) from Mycobacterium tuberculosis in complex with azole inhibitors Proc. Natl. Acad. Sci. U.S.A. 98, 3068-3073 (Pubitemid 32220800)
36. Podust, L., Yermalitskaya, L., Lepesheva, G., Podust, V., Dalmasso, E., and Waterman, M. (2004) Estriol bound and ligand-free structures of sterol 14-α demethylase Structure 12, 1937-1945 (Pubitemid 39469391)
37. Wohlkonig, A., Chan, P., Fosberry, A., Homes, P., Huang, J., Kranz, M., Leydon, V., Miles, T., Pearson, N., Perera, R., Shillings, A., Gwynn, M., and Bax, B. (2010) Structural basis of quinolone inhibition of type IIA topoisomerases and target-mediated resistance Nat. Struc. Mol. Biol. 17, 1152-1153
38. Hampele, I., D'Arcy, A., Dale, G., Kostrewa, D., Nielsen, J., Oefner, C., Page, M., Schonfeld, H.-J., Stuber, D., and Then, R. (1997) Structure and function of the dihydropteroate synthase from Staphylococcus aureus J. Mol. Biol. 268, 21-30 (Pubitemid 27192675)
39. Dale, G., Broger, C., D'Arcy, A., Hartman, P., DeHoogt, R., Jolidon, S., Kompis, I., Labhardt, A., Langen, H., Locher, H., Page, M., Stuber, D., Then, R., Wipf, B., and Oefner, C. (1997) A single amino acid substitution in Staphylococcus aureus dihydrofolate reductase determines trimethoprim resistance J. Mol. Biol. 266, 23-30 (Pubitemid 27170515)
40. Frey, K., Lombardo, M., Wright, D., and Anderson, A. (2010) Towards the understanding of resistance mechanisms in clinically isolated trimethoprim-resistant, methicillin-resistant Staphylococcus aureus dihydrofolate reductase J. Struc. Biol. 170, 93-97
41. Oefner, C., Bandera, M., Haldimann, A., Laue, H., Schulz, H., Mukhija, S., Parisi, S., Weiss, L., Lociuro, S., and Dale, G. (2009) Increased hydrophobic interactions of iclaprim with Staphylococcus aureus dihydrofolate reductase are responsible for the increase in affinity and antibacterial activity J. Antimicrob. Chemother. 63, 687-698
42. Piton, J., Petrella, S., Delarue, M., Andre-Leroux, G., Jarlier, V., Aubry, A., and Mayer, C. (2010) Structural insights into the quinolone resistance mechanism of Mycobacterium tuberculosis DNA gyrase PLoS One 5, e12245
43. Janne, P. (2008) Challenges of detecting EGFR T790M in gefitinib/erlotinib-resistant tumors Lung Cancer 60, S3-S9
44. Kobayashi, S., Boggon, T., Dayaram, T., Janne, P., Kocher, O., Meyerson, M., Johnson, B., Eck, M., Tenen, D., and Halmos, B. (2005) EGFR mutation and resistance of non-small-cell lung cancer to gefitinib N. Engl. J. Med. 352, 786-792 (Pubitemid 40271173)
45. Nguyen, K., Kobayashi, S., and Costa, D. (2009) Acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancers dependent on the epidermal growth factor receptor pathway Clin. Lung Cancer 10, 281-289
46. Paez, J., Janne, P., Lee, J., Tracy, S., Greulich, H., Gabriel, S., Herman, P., Kaye, F., Lindeman, N., Boggon, T., Naoki, K., Sasaki, H., Fujii, Y., Eck, M., Sellers, W., Johnson, B., and Meyerson, M. (2004) EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy Science 304, 1497-1500 (Pubitemid 38720929)
47. Pao, W., Miller, V., Politi, K., Riely, g., Somwar, R., Zakowski, M., Kris, M., and Varmus, H. (2005) Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain PLoS Med. 2, e73
48. Wheeler, D., Dunn, E., and Harari, P. (2010) Understanding resistance to EGFR inhibitors-impact on future treatment strategies, Nat. Rev Clin. Oncol. 7, 493-507
49. Yun, C., Mengwasser, K., Toms, A., Woo, M., Greulich, H., Wong, K., Meyerson, M., and Eck, M. (2008) The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP Proc. Natl. Acad. Sci. U.S.A. 105, 2070-2075 (Pubitemid 351439466)
50. King, N., Prabu-Jeyabalan, M., Nalivaika, E., and Schiffer, C. (2004) Combating susceptibility to drug resistance: lessons from HIV-1 protease Chem. Biol. 11, 1333-1338 (Pubitemid 39351371)
51. Chellappan, S., Kairys, V., Fernandes, M., Schiffer, C., and Gilson, M. (2007) Evaluation of the substrate envelope hypothesis for inhibitors of HIV-1 protease Proteins 68, 561-567 (Pubitemid 46981948)
52. Romano, K., Ali, A., Royer, W., and Schiffer, C. (2010) Drug resistance against HCV NS3/4A inhibitors defined by the balance of substrate recognition versus inhibitor binding Proc. Natl. Acad. Sci. U.S.A. 107, 20986-20991
53. Ren, J., Nichols, C., Chamberlain, P., Weaver, K., Short, S., and Stammers, D. (2004) Crystal structures of HIV-1 reverse transcriptases mutated at codons 100, 106 and 108 and mechanisms of resistance to non-nucleoside inhibitors J. Mol. Biol. 336, 569-578 (Pubitemid 38183013)
54. Ren, J., Chamberlain, P., Nichols, C., Douglas, L., Stuart, D., and Stammers, D. (2002) Crystal structures of Zidovudine- or Lamivudine-resistant human immunodeficiency virus type 1 reverse transcriptases containing mutations at codons 41, 184 and 215 J. Virol. 76, 10015-10019 (Pubitemid 35006540)
55. Ren, J., Nichols, C., Bird, L., Chamberlain, P., Weaver, K., Short, S., Stuart, D., and Stammers, D. (2001) Crystal structure of Y181C mutant HIV-1 reverse transcriptase in complex with DMP-266 (Efavirenz) J. Mol. Biol. 312, 795-805
56. Wang, J., Bambara, R., Demeter, L., and Dykes, C. (2010) Reduced fitness in cell culture of HIV-1 with nonnucleoside reverse transcriptase inhibitor-resistant mutations correlates with relative levels of reverse transcriptase content and RNase H activity in virions J. Virol. 84, 9377-9389
57. Xu, H., Oliveira, M., Quan, Y., Bar-Magen, T., and Wainberg, M. (2010) Differential impact of the HIV-1 non-nucleoside reverse transcriptatse inhibitor mutations K103N and M230L on viral replication and enzyme function J. Antimicrob. Chemother. 65, 2291-2299
58. Johnson, L. and Saravolatz, L. (2009) Etravirine, a next-generation nonnucleoside reverse transcriptase inhibitor Clin. Inf. Dis 48, 1123-1128
59. Brunton, L. (2011) Goodman and Gilman's The Pharmacological Basis of Therapeutics (Brunton, L., Ed.), pp 1399-1400, McGraw-Hill Companies, New York.
60. Sandefur, C., Wooden, J., Quaye, I., Sirawaraporn, R., and Sibley, C. (2007) Pyrimethamine-resistant dihydrofolate reductase enzymes of P. falciparum are not enzymatically compromised in vitro Mol. Biochem. Parasitol. 154, 1-5 (Pubitemid 46879943)
61. Brown, K., Costanzo, M., Xu, W., Roy, S., Lozovsky, E., and Hartl, D. (2010) Compensatory mutations restore fitness during the evolution of dihydrofolate reductase Mol. Biol. Evol. 27, 2682-2690
62. Canfield, C., Milhous, W., Ager, a., Rossan, R., Sweeney, T., Lewis, N., and Jacobus, D. (1993) PS-15: a potent, orally active antimalarial from a new class of folic acid antagonists Am. J. Trop. Med. Hyg. 49, 121-126 (Pubitemid 23242766)
63. Childs, G. and Lambros, C. (1986) Analogues of N- benzyloxydihydrotrizaines: in vitro antimalarial activity against Plasmodium falciparum Ann. Trop. Med. Parasitol. 80, 177-181 (Pubitemid 16083549)
64. Hankins, E., Warhurst, D., and Sibley, C. (2001) Novel alleles of the Plasmodium falciparum DHFR highly resistant to pyrimethamine and chlorcycloguanil, but not WR99210 Mol. Biochem. Parasitol. 117, 91-102 (Pubitemid 32823486)
65. Warhurst, D. (2002) Resistance to antifolates in Plasmodium falciparum, the causative agent of tropical malaria Sci. Prog. 85, 89-111
66. von Itzstein, M., Wu, W.-Y., Kok, G., Pegg, M., Dyason, J., Jin, B., Phan, t., Smythe, M., White, H., Oliver, S., Colman, P., Varghese, J., Ryan, D. M., Woods, J., Bethell, R., Hotham, V., Cameron, J., and Penn, C. (1993) Rational design of potent sialidase-based inhibitors of influenza virus replication Nature 363, 418-423 (Pubitemid 23179386)
67. Kim, C. U., Lew, W., Williams, M. A., Liu, H., Zhang, L., Swaminathan, S., Bischofberger, N., Chen, M. S., Mendel, D. B., Tai, C. Y., Laver, W. G., and Stevens, R. C. (1997) Influenza neuraminidase inhibitors possessing a novel hydrophobic interaction in the enzyme active site: design, synthesis, and structural analysis of carbocyclic sialic acid analogues with potent anti-influenza activity J. Am. Chem. Soc. 119, 681-690 (Pubitemid 27101232)
68. Herlocher, M., Truscon, R., Elias, S., Yen, H.-L., Roberts, N., Ohmit, S., and Monto, A. (2004) Influenza viruses resistant to the antiviral drug oseltamivir: transmission studies in ferrets J. Infect. Dis 190, 1627-1630 (Pubitemid 39411012)
69. Ives, J., Carr, J., Mendel, D., Tai, C., Lambkin, R., Kelly, L., Oxford, J., Hayden, F., and roberts, N. (2002) The H274Y mutation in the influenza A/H1N1 neuraminidase active site following oseltamivir phosphate treatment leave virus severely compromised both in vitro and in vivo Antiviral Res. 55, 307-317 (Pubitemid 34718130)
70. Yen, H., Ilyushina, N., Salomon, R., Hoffman, E., Webster, R., and Govorkova, E. (2007) Neuraminidase inhibitor-resistant recombinant A/Vietnam/1203/04 (H5N1) influenza viruses retain their replication efficiency and pathogenicity in vitro and in vivo J. Virol. 81, 12418-12426 (Pubitemid 350085855)
71. Bloom, J., Gong, L., and Baltimore, D. (2010) Permissive secondary mutations enable the evolution of influenza oseltamivir resistance Science 328, 1272-1275
72. Moscona, A. (2005) Neuraminidase Inhibitors for Influenza N. Engl. J. Med. 353, 1363-1373 (Pubitemid 41362704)
73. Babu, Y. S., Chand, P., Bantia, S., Kotian, P., Dehghani, A., El-Kattan, Y., Lin, T.-H., Hutchison, T. L., Elliott, A. J., Parker, C. D., Ananth, S. L., Horn, L. L., Laver, G. W., and Montgomery, J. A. (2000) BCX-1812 (RWJ-270201): Discovery of a novel, highly potent, orally active, and selective influenza neuraminidase inhibitor through structure-based drug design J. Med. Chem. 43, 3482-3486
74. Bantia, S., Arnold, C., Parker, C., Upshaw, R., and Chand, P. (2006) Anti-influenza virus activity of peramivir in mice with single intramuscular injection Antiviral Res. 69, 39-45 (Pubitemid 41790480)
75. Russell, R., Haire, L., Stevens, D., Collins, P., Lin, Y., Blackburn, G., Hay, A., Gamblin, S., and Skehel, J. (2006) The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design Nature 443, 45-49 (Pubitemid 44344043)
76. Drew, R. (2007) Emerging Options for treatment of invasive, multidrug-resistant Staphylococcus aureus infections Pharmacotherapy 27, 227-249 (Pubitemid 46214584)
77. Huovinen, P., Sundstrom, L., Swedberg, G., and Skold, O. (1995) Trimethoprim and sulfonamide resistance Antimicrob. Agents Chemother. 39, 279-289
78. Vickers, A., Potter, N., Fishwick, C., Chopra, I., and O'Neill, A. (2009) Analysis of mutational resistance to trimethoprim in Staphylococcus aureus by genetic and structural modelling techniques J. Antimicrob. Chemother. 63, 1112-1117
79. Schneider, P., Hawser, S., and Islam, K. (2003) Iclaprim, a novel diaminopyrimidine with potent activity on trimethoprim sensitive and resistant bacteria Bioorg. Med. Chem. Lett. 13, 4217-4221 (Pubitemid 37410316)
80. Frey, K., Georgiev, I., Donald, B., and Anderson, A. (2010) Predicting resistance mutations using protein design algorithms Proc. Natl. Acad. Sci. U.S.A. 107, 13707-13712
81. Hynes, N. and Lane, H. (2005) ERBB receptors and cancer: the complexity of targeted inhibitors Nat. Rev. Cancer 5, 341-354 (Pubitemid 40637826)
82. Matthews, D. and Gerritsen, M. (2010) Targeting Protein Kinases for Cancer Therapy, John Wiley & Sons, Hoboken, NJ.
83. Olayioye, M., Neve, R., Lane, H., and Hynes, N. (2000) The ErbB signaling network: receptor heterodimerization in development and cancer EMBO J. 19, 3159-3167 (Pubitemid 30428195)
84. Schlessinger, J. (2004) Common and distinct elements in cellular signaling via EGF and FGF receptors Science 306, 1506-1507 (Pubitemid 39564935)
85. Lynch, T., Bell, D., Sordella, R., Gurubhagavatula, S., Okimoto, R., Brannigan, B., Harris, P., Haslat, S., Supko, J., Haluska, F., Louis, D., Christiani, D., Selleman, J., and Haber, D. (2004) Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib N. Engl. J. Med. 350, 2129-2139 (Pubitemid 38637993)
86. Pao, W., Miller, V., AZakowski, M., Doherty, J., Politi, K., Sarkaria, I., Singh, B., Heelan, R., Rusch, V., Fulton, L., Mardis, E., Kupfer, D., Wilson, R., Kris, M., and Varmus, H. (2004) EGF receptor gene mutations are common in lung cancers from "never smokers" and are associated with sensitivity of tumors to gefitinib and erlotinib Proc. Natl. Acad. Sci. U.S.A. 101, 13306-13311 (Pubitemid 39209661)
87. Kwak, E., Sordella, R., Bell, D., Godin-Heymann, N., Okimoto, R., Brannigan, B., Harris, P., Driscoll, D., Fidias, P., Lynch, T., Rabindran, S., McGinnis, J., Wissner, a., Sharma, S., Isselbacher, K., Settleman, J., and Haber, D. (2005) Irreversible inhibitors of the EGF receptor may circumvent acquired resistance to gefitinib Proc. Natl. Acad. Sci. U.S.A. 102, 7665-7670 (Pubitemid 40741028)
88. Anderson, A., Pollastri, M., Schiffer, C., and Peet, N. (2011) The challenge of developing robust drugs to overcome resistance Drug Discovery. Today 16, 755-761
89. Engelman, J., Zejnullahu, K., Gale, C.-M., Lifshits, E., Gonzales, A., Shimamura, T., Zhao, F., Vincent, P., Naumov, G., Bradner, J., Althaus, I., Gandhi, L., Shapiro, G., Nelson, J., Heymach, J., Meyerson, M., Wong, K., and Janne, P. (2007) PF00299804, an irreversible pan-ERBB inhibitor, is effective in lung cancer models with EGFR and ERBB2 mutations that are resistant to gefitinib Cancer Res. 67, 11924-11932
90. Fry, D., Bridges, A., Denny, W., Doherty, A., Greis, K., Hicks, J., Hook, K., Keller, P., Leopold, W., Loo, J., McNamara, D., Nelson, J., Sherwood, V., Smaill, J., Trump-Kallmeyer, S., and Dobrusin, E. (1998) Specific, irreversible inactivation of the epidermal growth factor receptor and ERBB2, by a new class of tyrosine kinase inhibitor Proc. Natl. Acad. Sci. U.S.A. 95, 12022-12027 (Pubitemid 28460532)
91. Godin-Heymann, N., Ulkus, L., Brannigan, B., McDermott, U., Lamb, J., Maheswaran, S., Settleman, J., and Haber, D. (2008) The T790M "gatekeeper" mutation in EGFR mediates resistance to low concentrations of an irreversible EGFR inhibitor Mol Cancer Ther 7, 874-879 (Pubitemid 351551040)
92. Singh, J., Petter, R., and Kluge, A. (2010) Targeted covalent drugs of the kinase family Curr. Opin. Chem. Biol. 14, 475-480
93. Besse, B., Eaton, K., Soria, J., Lynch, T., Miller, V., Wong, K.-K., Powell, C., Quinn, S., Zacharchuk, C., and Sequist, L. (2008) 203 Poster Neratinib (HKI-272), an irrreversible pan-ErbB receptor tyrosine kinase inhibitor: preliminary results of a phase 2 trial in patients with advanced non-small cell lung cancer Eur. J. Cancer Suppl 6) 64
94. Janne, P., Pawel, J., Cohen, R., Crino, L., Butts, C., Olson, S., Eiseman, I., Chiappori, A., Yeap, B., Lenehan, P., Dasse, K., Sheeran, M., and Bonomi, P. (2007) Multicenter, randomize, phase II trial of CI-1033, an irreversible pan-ERBB inhibitor, for previously treated advanced non small-cell lung cancer J. Clin. Oncol. 25, 3936-3944 (Pubitemid 47477271)
95. Zhou, W., Ercan, D., Chen, L., Yun, C., Li, D., Capelletti, M., Cortot, A., Chirieac, L., Iacob, R., Padera, R., Engen, J., Wong, K., Eck, M., Gray, N., and Janne, P. (2009) Novel mutant-selective EGFR kinase inhibitors against EGFR T790M Nature 462, 1070-1074