Overcoming EGFR(T790M) and EGFR(C797S) resistance with mutant-selective allosteric inhibitors

An allosteric inhibitor, EAI045, is reported that is selective for certain drug-resistant EGFR mutants, but spares the wild-type receptor; combination therapy of EAI045 with EGFR-dimerization-blocking antibodies is effective in mouse models of lung cancer driven by mutant versions of EGFR that are r...

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Vydáno v:Nature (London) Ročník 534; číslo 7605; s. 129 - 132
Hlavní autoři: Jia, Yong, Yun, Cai-Hong, Park, Eunyoung, Ercan, Dalia, Manuia, Mari, Juarez, Jose, Xu, Chunxiao, Rhee, Kevin, Chen, Ting, Zhang, Haikuo, Palakurthi, Sangeetha, Jang, Jaebong, Lelais, Gerald, DiDonato, Michael, Bursulaya, Badry, Michellys, Pierre-Yves, Epple, Robert, Marsilje, Thomas H., McNeill, Matthew, Lu, Wenshuo, Harris, Jennifer, Bender, Steven, Wong, Kwok-Kin, Jänne, Pasi A., Eck, Michael J.
Médium: Journal Article
Jazyk:angličtina
Vydáno: London Nature Publishing Group UK 02.06.2016
Nature Publishing Group
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49/47
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631/535/1266
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631/92/275
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Allosteric Regulation - drug effects
Allosteric Site - drug effects
Animals
Antineoplastic Agents - pharmacology
ATP
Benzeneacetamides - pharmacology
Carcinoma, Non-Small-Cell Lung - drug therapy
Carcinoma, Non-Small-Cell Lung - enzymology
Carcinoma, Non-Small-Cell Lung - pathology
Cell Line, Tumor
Cell Proliferation - drug effects
Cetuximab - pharmacology
Disease Models, Animal
Drug Resistance, Multiple - drug effects
Drug Resistance, Multiple - genetics
Drug Resistance, Neoplasm - drug effects
Drug Resistance, Neoplasm - genetics
Drug Synergism
Enzyme kinetics
Epidermal growth factor
ErbB Receptors - antagonists & inhibitors
ErbB Receptors - chemistry
ErbB Receptors - genetics
ErbB Receptors - metabolism
Humanities and Social Sciences
Inhibitors
Kinases
letter
Lung cancer
Lung Neoplasms - drug therapy
Lung Neoplasms - enzymology
Lung Neoplasms - pathology
Mice
multidisciplinary
Mutant Proteins - antagonists & inhibitors
Mutant Proteins - chemistry
Mutant Proteins - genetics
Mutant Proteins - metabolism
Mutants
Mutation
NMR
Nuclear magnetic resonance
Phosphorylation
Protein Conformation - drug effects
Protein Kinase Inhibitors - pharmacology
Protein Multimerization - drug effects
Science
Studies
Thiazoles - pharmacology
Tumors
ISSN:0028-0836, 1476-4687, 1476-4687
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Abstract An allosteric inhibitor, EAI045, is reported that is selective for certain drug-resistant EGFR mutants, but spares the wild-type receptor; combination therapy of EAI045 with EGFR-dimerization-blocking antibodies is effective in mouse models of lung cancer driven by mutant versions of EGFR that are resistant to all previously developed inhibitors. Novel EGFR-directed therapeutics Currently available small-molecule inhibitors targeting epidermal growth factor receptor (EGFR) and other receptor tyrosine kinases bind the ATP site of the kinase, and therefore typically inhibit a number of 'off-target' kinases owing to the high conservation of this site. In addition, the common binding site of these drugs leads to shared susceptibility to resistance-conferring mutations in EGFR. Here, Michael Eck and colleagues describe an allosteric inhibitor, EAI045, that is selective for certain drug-resistant EGFR mutants but spares the wild-type receptor. Although EAI045 is not effective in blocking EGFR-driven cell proliferation as a single agent, it has synergistic inhibitory activity when combined with an antibody that blocks EGFR dimerization. This combination therapy is effective in mouse models of lung cancer driven by mutant versions of EGFR that are resistant to all previously developed inhibitors. The epidermal growth factor receptor (EGFR)-directed tyrosine kinase inhibitors (TKIs) gefitinib, erlotinib and afatinib are approved treatments for non-small cell lung cancers harbouring activating mutations in the EGFR kinase 1 , 2 , but resistance arises rapidly, most frequently owing to the secondary T790M mutation within the ATP site of the receptor 3 , 4 . Recently developed mutant-selective irreversible inhibitors are highly active against the T790M mutant 5 , 6 , but their efficacy can be compromised by acquired mutation of C797, the cysteine residue with which they form a key covalent bond 7 . All current EGFR TKIs target the ATP-site of the kinase, highlighting the need for therapeutic agents with alternative mechanisms of action. Here we describe the rational discovery of EAI045, an allosteric inhibitor that targets selected drug-resistant EGFR mutants but spares the wild-type receptor. The crystal structure shows that the compound binds an allosteric site created by the displacement of the regulatory C-helix in an inactive conformation of the kinase. The compound inhibits L858R/T790M-mutant EGFR with low-nanomolar potency in biochemical assays. However, as a single agent it is not effective in blocking EGFR-driven proliferation in cells owing to differential potency on the two subunits of the dimeric receptor, which interact in an asymmetric manner in the active state 8 . We observe marked synergy of EAI045 with cetuximab, an antibody therapeutic that blocks EGFR dimerization 9 , 10 , rendering the kinase uniformly susceptible to the allosteric agent. EAI045 in combination with cetuximab is effective in mouse models of lung cancer driven by EGFR(L858R/T790M) and by EGFR(L858R/T790M/C797S), a mutant that is resistant to all currently available EGFR TKIs. More generally, our findings illustrate the utility of purposefully targeting allosteric sites to obtain mutant-selective inhibitors.
AbstractList The epidermal growth factor receptor (EGFR)-directed tyrosine kinase inhibitors (TKIs) gefitinib, erlotinib and afatinib are approved treatments for non-small cell lung cancers harbouring activating mutations in the EGFR kinase, but resistance arises rapidly, most frequently owing to the secondary T790M mutation within the ATP site of the receptor. Recently developed mutant-selective irreversible inhibitors are highly active against the T790M mutant, but their efficacy can be compromised by acquired mutation of C797, the cysteine residue with which they form a key covalent bond. All current EGFR TKIs target the ATP-site of the kinase, highlighting the need for therapeutic agents with alternative mechanisms of action. Here we describe the rational discovery of EAI045, an allosteric inhibitor that targets selected drug-resistant EGFR mutants but spares the wild-type receptor. The crystal structure shows that the compound binds an allosteric site created by the displacement of the regulatory C-helix in an inactive conformation of the kinase. The compound inhibits L858R/T790M-mutant EGFR with low-nanomolar potency in biochemical assays. However, as a single agent it is not effective in blocking EGFR-driven proliferation in cells owing to differential potency on the two subunits of the dimeric receptor, which interact in an asymmetric manner in the active state. We observe marked synergy of EAI045 with cetuximab, an antibody therapeutic that blocks EGFR dimerization, rendering the kinase uniformly susceptible to the allosteric agent. EAI045 in combination with cetuximab is effective in mouse models of lung cancer driven by EGFR(L858R/T790M) and by EGFR(L858R/T790M/C797S), a mutant that is resistant to all currently available EGFR TKIs. More generally, our findings illustrate the utility of purposefully targeting allosteric sites to obtain mutant-selective inhibitors.The epidermal growth factor receptor (EGFR)-directed tyrosine kinase inhibitors (TKIs) gefitinib, erlotinib and afatinib are approved treatments for non-small cell lung cancers harbouring activating mutations in the EGFR kinase, but resistance arises rapidly, most frequently owing to the secondary T790M mutation within the ATP site of the receptor. Recently developed mutant-selective irreversible inhibitors are highly active against the T790M mutant, but their efficacy can be compromised by acquired mutation of C797, the cysteine residue with which they form a key covalent bond. All current EGFR TKIs target the ATP-site of the kinase, highlighting the need for therapeutic agents with alternative mechanisms of action. Here we describe the rational discovery of EAI045, an allosteric inhibitor that targets selected drug-resistant EGFR mutants but spares the wild-type receptor. The crystal structure shows that the compound binds an allosteric site created by the displacement of the regulatory C-helix in an inactive conformation of the kinase. The compound inhibits L858R/T790M-mutant EGFR with low-nanomolar potency in biochemical assays. However, as a single agent it is not effective in blocking EGFR-driven proliferation in cells owing to differential potency on the two subunits of the dimeric receptor, which interact in an asymmetric manner in the active state. We observe marked synergy of EAI045 with cetuximab, an antibody therapeutic that blocks EGFR dimerization, rendering the kinase uniformly susceptible to the allosteric agent. EAI045 in combination with cetuximab is effective in mouse models of lung cancer driven by EGFR(L858R/T790M) and by EGFR(L858R/T790M/C797S), a mutant that is resistant to all currently available EGFR TKIs. More generally, our findings illustrate the utility of purposefully targeting allosteric sites to obtain mutant-selective inhibitors.
The epidermal growth factor receptor (EGFR)-directed tyrosine kinase inhibitors (TKIs) gefitinib, erlotinib and afatinib are approved treatments for non-small cell lung cancers harbouring activating mutations in the EGFR kinase, but resistance arises rapidly, most frequently owing to the secondary T790M mutation within the ATP site of the receptor. Recently developed mutant-selective irreversible inhibitors are highly active against the T790M mutant, but their efficacy can be compromised by acquired mutation of C797, the cysteine residue with which they form a key covalent bond. All current EGFR TKIs target the ATP-site of the kinase, highlighting the need for therapeutic agents with alternative mechanisms of action. Here we describe the rational discovery of EAI045, an allosteric inhibitor that targets selected drug-resistant EGFR mutants but spares the wild-type receptor. The crystal structure shows that the compound binds an allosteric site created by the displacement of the regulatory C-helix in an inactive conformation of the kinase. The compound inhibits L858R/T790M-mutant EGFR with low-nanomolar potency in biochemical assays. However, as a single agent it is not effective in blocking EGFR-driven proliferation in cells owing to differential potency on the two subunits of the dimeric receptor, which interact in an asymmetric manner in the active state. We observe marked synergy of EAI045 with cetuximab, an antibody therapeutic that blocks EGFR dimerization, rendering the kinase uniformly susceptible to the allosteric agent. EAI045 in combination with cetuximab is effective in mouse models of lung cancer driven by EGFR(L858R/T790M) and by EGFR(L858R/T790M/C797S), a mutant that is resistant to all currently available EGFR TKIs. More generally, our findings illustrate the utility of purposefully targeting allosteric sites to obtain mutant-selective inhibitors.
An allosteric inhibitor, EAI045, is reported that is selective for certain drug-resistant EGFR mutants, but spares the wild-type receptor; combination therapy of EAI045 with EGFR-dimerization-blocking antibodies is effective in mouse models of lung cancer driven by mutant versions of EGFR that are resistant to all previously developed inhibitors. Novel EGFR-directed therapeutics Currently available small-molecule inhibitors targeting epidermal growth factor receptor (EGFR) and other receptor tyrosine kinases bind the ATP site of the kinase, and therefore typically inhibit a number of 'off-target' kinases owing to the high conservation of this site. In addition, the common binding site of these drugs leads to shared susceptibility to resistance-conferring mutations in EGFR. Here, Michael Eck and colleagues describe an allosteric inhibitor, EAI045, that is selective for certain drug-resistant EGFR mutants but spares the wild-type receptor. Although EAI045 is not effective in blocking EGFR-driven cell proliferation as a single agent, it has synergistic inhibitory activity when combined with an antibody that blocks EGFR dimerization. This combination therapy is effective in mouse models of lung cancer driven by mutant versions of EGFR that are resistant to all previously developed inhibitors. The epidermal growth factor receptor (EGFR)-directed tyrosine kinase inhibitors (TKIs) gefitinib, erlotinib and afatinib are approved treatments for non-small cell lung cancers harbouring activating mutations in the EGFR kinase 1 , 2 , but resistance arises rapidly, most frequently owing to the secondary T790M mutation within the ATP site of the receptor 3 , 4 . Recently developed mutant-selective irreversible inhibitors are highly active against the T790M mutant 5 , 6 , but their efficacy can be compromised by acquired mutation of C797, the cysteine residue with which they form a key covalent bond 7 . All current EGFR TKIs target the ATP-site of the kinase, highlighting the need for therapeutic agents with alternative mechanisms of action. Here we describe the rational discovery of EAI045, an allosteric inhibitor that targets selected drug-resistant EGFR mutants but spares the wild-type receptor. The crystal structure shows that the compound binds an allosteric site created by the displacement of the regulatory C-helix in an inactive conformation of the kinase. The compound inhibits L858R/T790M-mutant EGFR with low-nanomolar potency in biochemical assays. However, as a single agent it is not effective in blocking EGFR-driven proliferation in cells owing to differential potency on the two subunits of the dimeric receptor, which interact in an asymmetric manner in the active state 8 . We observe marked synergy of EAI045 with cetuximab, an antibody therapeutic that blocks EGFR dimerization 9 , 10 , rendering the kinase uniformly susceptible to the allosteric agent. EAI045 in combination with cetuximab is effective in mouse models of lung cancer driven by EGFR(L858R/T790M) and by EGFR(L858R/T790M/C797S), a mutant that is resistant to all currently available EGFR TKIs. More generally, our findings illustrate the utility of purposefully targeting allosteric sites to obtain mutant-selective inhibitors.
The epidermal growth factor receptor (EGFR)-directed tyrosine kinase inhibitors (TKIs) gefitinib, erlotinib and afatinib are approved treatments for non-small cell lung cancers harbouring activating mutations in the EGFR kinase^sup 1,2^, but resistance arises rapidly, most frequently owing to the secondary T790M mutation within the ATP site of the receptor^sup 3,4^. Recently developed mutant-selective irreversible inhibitors are highly active against the T790M mutant^sup 5,6^, but their efficacy can be compromised by acquired mutation of C797, the cysteine residue with which they form a key covalent bond^sup 7^. All current EGFR TKIs target the ATP-site of the kinase, highlighting the need for therapeutic agents with alternative mechanisms of action. Here we describe the rational discovery of EAI045, an allosteric inhibitor that targets selected drug-resistant EGFR mutants but spares the wild-type receptor. The crystal structure shows that the compound binds an allosteric site created by the displacement of the regulatory C-helix in an inactive conformation of the kinase. The compound inhibits L858R/T790M-mutant EGFR with low-nanomolar potency in biochemical assays. However, as a single agent it is not effective in blocking EGFR-driven proliferation in cells owing to differential potency on the two subunits of the dimeric receptor, which interact in an asymmetric manner in the active state^sup 8^. We observe marked synergy of EAI045 with cetuximab, an antibody therapeutic that blocks EGFR dimerization^sup 9,10^, rendering the kinase uniformly susceptible to the allosteric agent. EAI045 in combination with cetuximab is effective in mouse models of lung cancer driven by EGFR(L858R/T790M) and by EGFR(L858R/T790M/C797S), a mutant that is resistant to all currently available EGFR TKIs. More generally, our findings illustrate the utility of purposefully targeting allosteric sites to obtain mutant-selective inhibitors.
Author Jänne, Pasi A.
Lu, Wenshuo
Jang, Jaebong
Juarez, Jose
Yun, Cai-Hong
Zhang, Haikuo
Epple, Robert
Bursulaya, Badry
Palakurthi, Sangeetha
Marsilje, Thomas H.
Rhee, Kevin
DiDonato, Michael
Wong, Kwok-Kin
Jia, Yong
Park, Eunyoung
Xu, Chunxiao
Eck, Michael J.
McNeill, Matthew
Harris, Jennifer
Manuia, Mari
Lelais, Gerald
Ercan, Dalia
Bender, Steven
Chen, Ting
Michellys, Pierre-Yves
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  givenname: Yong
  surname: Jia
  fullname: Jia, Yong
  organization: Genomics Institute of the Novartis Research Foundation
– sequence: 2
  givenname: Cai-Hong
  surname: Yun
  fullname: Yun, Cai-Hong
  organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, †Present address: Peking University Institute of Systems Biomedicine and Department of Biophysics, Peking University Health Science Center, Beijing 100191, China
– sequence: 3
  givenname: Eunyoung
  surname: Park
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  organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School
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  givenname: Dalia
  surname: Ercan
  fullname: Ercan, Dalia
  organization: Lowe Center for Thoracic Oncology, Dana-Farber Cancer Institute
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  givenname: Mari
  surname: Manuia
  fullname: Manuia, Mari
  organization: Genomics Institute of the Novartis Research Foundation
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  surname: Juarez
  fullname: Juarez, Jose
  organization: Genomics Institute of the Novartis Research Foundation
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  givenname: Chunxiao
  surname: Xu
  fullname: Xu, Chunxiao
  organization: Lowe Center for Thoracic Oncology, Dana-Farber Cancer Institute
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  givenname: Kevin
  surname: Rhee
  fullname: Rhee, Kevin
  organization: Lowe Center for Thoracic Oncology, Dana-Farber Cancer Institute
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  givenname: Ting
  surname: Chen
  fullname: Chen, Ting
  organization: Lowe Center for Thoracic Oncology, Dana-Farber Cancer Institute
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  givenname: Haikuo
  surname: Zhang
  fullname: Zhang, Haikuo
  organization: Lowe Center for Thoracic Oncology, Dana-Farber Cancer Institute
– sequence: 11
  givenname: Sangeetha
  surname: Palakurthi
  fullname: Palakurthi, Sangeetha
  organization: Belfer Center for Applied Cancer Science, Dana-Farber Cancer Institute
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  givenname: Jaebong
  surname: Jang
  fullname: Jang, Jaebong
  organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School
– sequence: 13
  givenname: Gerald
  surname: Lelais
  fullname: Lelais, Gerald
  organization: Genomics Institute of the Novartis Research Foundation
– sequence: 14
  givenname: Michael
  surname: DiDonato
  fullname: DiDonato, Michael
  organization: Genomics Institute of the Novartis Research Foundation
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  surname: Bursulaya
  fullname: Bursulaya, Badry
  organization: Genomics Institute of the Novartis Research Foundation
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  givenname: Pierre-Yves
  surname: Michellys
  fullname: Michellys, Pierre-Yves
  organization: Genomics Institute of the Novartis Research Foundation
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  surname: Epple
  fullname: Epple, Robert
  organization: Genomics Institute of the Novartis Research Foundation
– sequence: 18
  givenname: Thomas H.
  surname: Marsilje
  fullname: Marsilje, Thomas H.
  organization: Genomics Institute of the Novartis Research Foundation
– sequence: 19
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  surname: McNeill
  fullname: McNeill, Matthew
  organization: Genomics Institute of the Novartis Research Foundation
– sequence: 20
  givenname: Wenshuo
  surname: Lu
  fullname: Lu, Wenshuo
  organization: Genomics Institute of the Novartis Research Foundation
– sequence: 21
  givenname: Jennifer
  surname: Harris
  fullname: Harris, Jennifer
  organization: Genomics Institute of the Novartis Research Foundation
– sequence: 22
  givenname: Steven
  surname: Bender
  fullname: Bender, Steven
  organization: Genomics Institute of the Novartis Research Foundation
– sequence: 23
  givenname: Kwok-Kin
  surname: Wong
  fullname: Wong, Kwok-Kin
  organization: Lowe Center for Thoracic Oncology, Dana-Farber Cancer Institute, Belfer Center for Applied Cancer Science, Dana-Farber Cancer Institute
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  organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School
BackLink https://www.ncbi.nlm.nih.gov/pubmed/27251290$$D View this record in MEDLINE/PubMed
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Snippet An allosteric inhibitor, EAI045, is reported that is selective for certain drug-resistant EGFR mutants, but spares the wild-type receptor; combination therapy...
The epidermal growth factor receptor (EGFR)-directed tyrosine kinase inhibitors (TKIs) gefitinib, erlotinib and afatinib are approved treatments for non-small...
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42/109
49/47
59/36
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631/535/1266
631/67
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Allosteric Regulation - drug effects
Allosteric Site - drug effects
Animals
Antineoplastic Agents - pharmacology
ATP
Benzeneacetamides - pharmacology
Carcinoma, Non-Small-Cell Lung - drug therapy
Carcinoma, Non-Small-Cell Lung - enzymology
Carcinoma, Non-Small-Cell Lung - pathology
Cell Line, Tumor
Cell Proliferation - drug effects
Cetuximab - pharmacology
Disease Models, Animal
Drug Resistance, Multiple - drug effects
Drug Resistance, Multiple - genetics
Drug Resistance, Neoplasm - drug effects
Drug Resistance, Neoplasm - genetics
Drug Synergism
Enzyme kinetics
Epidermal growth factor
ErbB Receptors - antagonists & inhibitors
ErbB Receptors - chemistry
ErbB Receptors - genetics
ErbB Receptors - metabolism
Humanities and Social Sciences
Inhibitors
Kinases
letter
Lung cancer
Lung Neoplasms - drug therapy
Lung Neoplasms - enzymology
Lung Neoplasms - pathology
Mice
multidisciplinary
Mutant Proteins - antagonists & inhibitors
Mutant Proteins - chemistry
Mutant Proteins - genetics
Mutant Proteins - metabolism
Mutants
Mutation
NMR
Nuclear magnetic resonance
Phosphorylation
Protein Conformation - drug effects
Protein Kinase Inhibitors - pharmacology
Protein Multimerization - drug effects
Science
Studies
Thiazoles - pharmacology
Tumors
Title Overcoming EGFR(T790M) and EGFR(C797S) resistance with mutant-selective allosteric inhibitors
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