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Research ArticleArticle

Small Molecule Inhibitors of ERCC1-XPF Protein-Protein Interaction Synergize Alkylating Agents in Cancer Cells

Lars Petter Jordheim, Khaled H. Barakat, Laurence Heinrich-Balard, Eva-Laure Matera, Emeline Cros-Perrial, Karima Bouledrak, Rana El Sabeh, Rolando Perez-Pineiro, David S. Wishart, Richard Cohen, Jack Tuszynski and Charles Dumontet
Molecular Pharmacology July 2013, 84 (1) 12-24; DOI: https://doi.org/10.1124/mol.112.082347
Lars Petter Jordheim
Université de Lyon (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), Université Lyon 1 (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), INSERM U1052, Centre de Recherche en Cancérologie de Lyon (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.), and CNRS UMR 5286, Centre de Recherche en Cancérologie de Lyon, Lyon, France (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.); Department of Physics, University of Alberta, Edmonton, Alberta, Canada (K.H.B., J.T.); Department of Engineering Mathematics and Physics, Fayoum University, Fayoum, Egypt (K.H.B.); MATEIS UMR-CNRS 5510, ISPB Faculté de Pharmacie, Lyon, France (L.H.-B., R.C.); Department of Biological Sciences (R.P.-P., D.S.W.) and Department of Computing Sciences, University of Alberta, Edmonton, Alberta, Canada (R.P.-P., D.S.W.); Hospices Civils de Lyon, Hôpital Edouard Herriot, Laboratoire de Biochimie et de Biologie Moléculaire, Lyon Cedex 03, France (R.C.); and Department of Oncology, University of Alberta, Edmonton, Alberta, Canada (J.T.)
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Khaled H. Barakat
Université de Lyon (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), Université Lyon 1 (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), INSERM U1052, Centre de Recherche en Cancérologie de Lyon (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.), and CNRS UMR 5286, Centre de Recherche en Cancérologie de Lyon, Lyon, France (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.); Department of Physics, University of Alberta, Edmonton, Alberta, Canada (K.H.B., J.T.); Department of Engineering Mathematics and Physics, Fayoum University, Fayoum, Egypt (K.H.B.); MATEIS UMR-CNRS 5510, ISPB Faculté de Pharmacie, Lyon, France (L.H.-B., R.C.); Department of Biological Sciences (R.P.-P., D.S.W.) and Department of Computing Sciences, University of Alberta, Edmonton, Alberta, Canada (R.P.-P., D.S.W.); Hospices Civils de Lyon, Hôpital Edouard Herriot, Laboratoire de Biochimie et de Biologie Moléculaire, Lyon Cedex 03, France (R.C.); and Department of Oncology, University of Alberta, Edmonton, Alberta, Canada (J.T.)
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Laurence Heinrich-Balard
Université de Lyon (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), Université Lyon 1 (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), INSERM U1052, Centre de Recherche en Cancérologie de Lyon (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.), and CNRS UMR 5286, Centre de Recherche en Cancérologie de Lyon, Lyon, France (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.); Department of Physics, University of Alberta, Edmonton, Alberta, Canada (K.H.B., J.T.); Department of Engineering Mathematics and Physics, Fayoum University, Fayoum, Egypt (K.H.B.); MATEIS UMR-CNRS 5510, ISPB Faculté de Pharmacie, Lyon, France (L.H.-B., R.C.); Department of Biological Sciences (R.P.-P., D.S.W.) and Department of Computing Sciences, University of Alberta, Edmonton, Alberta, Canada (R.P.-P., D.S.W.); Hospices Civils de Lyon, Hôpital Edouard Herriot, Laboratoire de Biochimie et de Biologie Moléculaire, Lyon Cedex 03, France (R.C.); and Department of Oncology, University of Alberta, Edmonton, Alberta, Canada (J.T.)
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Eva-Laure Matera
Université de Lyon (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), Université Lyon 1 (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), INSERM U1052, Centre de Recherche en Cancérologie de Lyon (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.), and CNRS UMR 5286, Centre de Recherche en Cancérologie de Lyon, Lyon, France (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.); Department of Physics, University of Alberta, Edmonton, Alberta, Canada (K.H.B., J.T.); Department of Engineering Mathematics and Physics, Fayoum University, Fayoum, Egypt (K.H.B.); MATEIS UMR-CNRS 5510, ISPB Faculté de Pharmacie, Lyon, France (L.H.-B., R.C.); Department of Biological Sciences (R.P.-P., D.S.W.) and Department of Computing Sciences, University of Alberta, Edmonton, Alberta, Canada (R.P.-P., D.S.W.); Hospices Civils de Lyon, Hôpital Edouard Herriot, Laboratoire de Biochimie et de Biologie Moléculaire, Lyon Cedex 03, France (R.C.); and Department of Oncology, University of Alberta, Edmonton, Alberta, Canada (J.T.)
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Emeline Cros-Perrial
Université de Lyon (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), Université Lyon 1 (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), INSERM U1052, Centre de Recherche en Cancérologie de Lyon (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.), and CNRS UMR 5286, Centre de Recherche en Cancérologie de Lyon, Lyon, France (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.); Department of Physics, University of Alberta, Edmonton, Alberta, Canada (K.H.B., J.T.); Department of Engineering Mathematics and Physics, Fayoum University, Fayoum, Egypt (K.H.B.); MATEIS UMR-CNRS 5510, ISPB Faculté de Pharmacie, Lyon, France (L.H.-B., R.C.); Department of Biological Sciences (R.P.-P., D.S.W.) and Department of Computing Sciences, University of Alberta, Edmonton, Alberta, Canada (R.P.-P., D.S.W.); Hospices Civils de Lyon, Hôpital Edouard Herriot, Laboratoire de Biochimie et de Biologie Moléculaire, Lyon Cedex 03, France (R.C.); and Department of Oncology, University of Alberta, Edmonton, Alberta, Canada (J.T.)
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Karima Bouledrak
Université de Lyon (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), Université Lyon 1 (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), INSERM U1052, Centre de Recherche en Cancérologie de Lyon (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.), and CNRS UMR 5286, Centre de Recherche en Cancérologie de Lyon, Lyon, France (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.); Department of Physics, University of Alberta, Edmonton, Alberta, Canada (K.H.B., J.T.); Department of Engineering Mathematics and Physics, Fayoum University, Fayoum, Egypt (K.H.B.); MATEIS UMR-CNRS 5510, ISPB Faculté de Pharmacie, Lyon, France (L.H.-B., R.C.); Department of Biological Sciences (R.P.-P., D.S.W.) and Department of Computing Sciences, University of Alberta, Edmonton, Alberta, Canada (R.P.-P., D.S.W.); Hospices Civils de Lyon, Hôpital Edouard Herriot, Laboratoire de Biochimie et de Biologie Moléculaire, Lyon Cedex 03, France (R.C.); and Department of Oncology, University of Alberta, Edmonton, Alberta, Canada (J.T.)
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Rana El Sabeh
Université de Lyon (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), Université Lyon 1 (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), INSERM U1052, Centre de Recherche en Cancérologie de Lyon (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.), and CNRS UMR 5286, Centre de Recherche en Cancérologie de Lyon, Lyon, France (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.); Department of Physics, University of Alberta, Edmonton, Alberta, Canada (K.H.B., J.T.); Department of Engineering Mathematics and Physics, Fayoum University, Fayoum, Egypt (K.H.B.); MATEIS UMR-CNRS 5510, ISPB Faculté de Pharmacie, Lyon, France (L.H.-B., R.C.); Department of Biological Sciences (R.P.-P., D.S.W.) and Department of Computing Sciences, University of Alberta, Edmonton, Alberta, Canada (R.P.-P., D.S.W.); Hospices Civils de Lyon, Hôpital Edouard Herriot, Laboratoire de Biochimie et de Biologie Moléculaire, Lyon Cedex 03, France (R.C.); and Department of Oncology, University of Alberta, Edmonton, Alberta, Canada (J.T.)
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Rolando Perez-Pineiro
Université de Lyon (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), Université Lyon 1 (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), INSERM U1052, Centre de Recherche en Cancérologie de Lyon (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.), and CNRS UMR 5286, Centre de Recherche en Cancérologie de Lyon, Lyon, France (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.); Department of Physics, University of Alberta, Edmonton, Alberta, Canada (K.H.B., J.T.); Department of Engineering Mathematics and Physics, Fayoum University, Fayoum, Egypt (K.H.B.); MATEIS UMR-CNRS 5510, ISPB Faculté de Pharmacie, Lyon, France (L.H.-B., R.C.); Department of Biological Sciences (R.P.-P., D.S.W.) and Department of Computing Sciences, University of Alberta, Edmonton, Alberta, Canada (R.P.-P., D.S.W.); Hospices Civils de Lyon, Hôpital Edouard Herriot, Laboratoire de Biochimie et de Biologie Moléculaire, Lyon Cedex 03, France (R.C.); and Department of Oncology, University of Alberta, Edmonton, Alberta, Canada (J.T.)
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David S. Wishart
Université de Lyon (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), Université Lyon 1 (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), INSERM U1052, Centre de Recherche en Cancérologie de Lyon (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.), and CNRS UMR 5286, Centre de Recherche en Cancérologie de Lyon, Lyon, France (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.); Department of Physics, University of Alberta, Edmonton, Alberta, Canada (K.H.B., J.T.); Department of Engineering Mathematics and Physics, Fayoum University, Fayoum, Egypt (K.H.B.); MATEIS UMR-CNRS 5510, ISPB Faculté de Pharmacie, Lyon, France (L.H.-B., R.C.); Department of Biological Sciences (R.P.-P., D.S.W.) and Department of Computing Sciences, University of Alberta, Edmonton, Alberta, Canada (R.P.-P., D.S.W.); Hospices Civils de Lyon, Hôpital Edouard Herriot, Laboratoire de Biochimie et de Biologie Moléculaire, Lyon Cedex 03, France (R.C.); and Department of Oncology, University of Alberta, Edmonton, Alberta, Canada (J.T.)
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Richard Cohen
Université de Lyon (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), Université Lyon 1 (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), INSERM U1052, Centre de Recherche en Cancérologie de Lyon (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.), and CNRS UMR 5286, Centre de Recherche en Cancérologie de Lyon, Lyon, France (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.); Department of Physics, University of Alberta, Edmonton, Alberta, Canada (K.H.B., J.T.); Department of Engineering Mathematics and Physics, Fayoum University, Fayoum, Egypt (K.H.B.); MATEIS UMR-CNRS 5510, ISPB Faculté de Pharmacie, Lyon, France (L.H.-B., R.C.); Department of Biological Sciences (R.P.-P., D.S.W.) and Department of Computing Sciences, University of Alberta, Edmonton, Alberta, Canada (R.P.-P., D.S.W.); Hospices Civils de Lyon, Hôpital Edouard Herriot, Laboratoire de Biochimie et de Biologie Moléculaire, Lyon Cedex 03, France (R.C.); and Department of Oncology, University of Alberta, Edmonton, Alberta, Canada (J.T.)
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Jack Tuszynski
Université de Lyon (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), Université Lyon 1 (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), INSERM U1052, Centre de Recherche en Cancérologie de Lyon (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.), and CNRS UMR 5286, Centre de Recherche en Cancérologie de Lyon, Lyon, France (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.); Department of Physics, University of Alberta, Edmonton, Alberta, Canada (K.H.B., J.T.); Department of Engineering Mathematics and Physics, Fayoum University, Fayoum, Egypt (K.H.B.); MATEIS UMR-CNRS 5510, ISPB Faculté de Pharmacie, Lyon, France (L.H.-B., R.C.); Department of Biological Sciences (R.P.-P., D.S.W.) and Department of Computing Sciences, University of Alberta, Edmonton, Alberta, Canada (R.P.-P., D.S.W.); Hospices Civils de Lyon, Hôpital Edouard Herriot, Laboratoire de Biochimie et de Biologie Moléculaire, Lyon Cedex 03, France (R.C.); and Department of Oncology, University of Alberta, Edmonton, Alberta, Canada (J.T.)
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Charles Dumontet
Université de Lyon (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), Université Lyon 1 (L.P.J., L.H.-B., E.-L.M., E.C.-P., K.B., R.E.S., R.C., C.D.), INSERM U1052, Centre de Recherche en Cancérologie de Lyon (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.), and CNRS UMR 5286, Centre de Recherche en Cancérologie de Lyon, Lyon, France (L.P.J., E.-L.M., E.C.-P., K.B., R.E.S., C.D.); Department of Physics, University of Alberta, Edmonton, Alberta, Canada (K.H.B., J.T.); Department of Engineering Mathematics and Physics, Fayoum University, Fayoum, Egypt (K.H.B.); MATEIS UMR-CNRS 5510, ISPB Faculté de Pharmacie, Lyon, France (L.H.-B., R.C.); Department of Biological Sciences (R.P.-P., D.S.W.) and Department of Computing Sciences, University of Alberta, Edmonton, Alberta, Canada (R.P.-P., D.S.W.); Hospices Civils de Lyon, Hôpital Edouard Herriot, Laboratoire de Biochimie et de Biologie Moléculaire, Lyon Cedex 03, France (R.C.); and Department of Oncology, University of Alberta, Edmonton, Alberta, Canada (J.T.)
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Abstract

The benefit of cancer chemotherapy based on alkylating agents is limited because of the action of DNA repair enzymes, which mitigate the damage induced by these agents. The interaction between the proteins ERCC1 and XPF involves two major components of the nucleotide excision repair pathway. Here, novel inhibitors of this interaction were identified by virtual screening based on available structures with use of the National Cancer Institute diversity set and a panel of DrugBank small molecules. Subsequently, experimental validation of the in silico screening was undertaken. Top hits were evaluated on A549 and HCT116 cancer cells. In particular, the compound labeled NSC 130813 [4-[(6-chloro-2-methoxy-9-acridinyl)amino]-2-[(4-methyl-1-piperazinyl)methyl]] was shown to act synergistically with cisplatin and mitomycin C; to increase UVC-mediated cytotoxicity; to modify DNA repair as indicated by the staining of phosphorylated H2AX; and to disrupt interaction between ERCC1 and XPF in cells. In addition, using the Biacore technique, we showed that this compound interacts with the domain of XPF responsible for interaction with ERCC1. This study shows that small molecules targeting the protein-protein interaction of ERCC1 and XPF can be developed to enhance the effects of alkylating agents on cancer cells.

Footnotes

    • Received September 11, 2012.
    • Accepted April 11, 2013.
  • L.P.J. and K.H.B. contributed equally to this work.

  • This work was supported by Ligue Contre le Cancer comité du Rhône; Lise og Arnfinn Hejes fond (to L.P.J.); the Allard Foundation; the Canadian Breast Cancer Foundation; and the Alberta Advanced Education and Technology (to J.A.T.).

  • dx.doi.org/10.1124/mol.112.082347.

  • ↵Embedded ImageThis article has supplemental material available at molpharm.aspetjournals.org.

  • Copyright © 2013 by The American Society for Pharmacology and Experimental Therapeutics
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Molecular Pharmacology: 84 (1)
Molecular Pharmacology
Vol. 84, Issue 1
1 Jul 2013
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Research ArticleArticle

Inhibitors of ERCC1-XPF Interaction

Lars Petter Jordheim, Khaled H. Barakat, Laurence Heinrich-Balard, Eva-Laure Matera, Emeline Cros-Perrial, Karima Bouledrak, Rana El Sabeh, Rolando Perez-Pineiro, David S. Wishart, Richard Cohen, Jack Tuszynski and Charles Dumontet
Molecular Pharmacology July 1, 2013, 84 (1) 12-24; DOI: https://doi.org/10.1124/mol.112.082347

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Research ArticleArticle

Inhibitors of ERCC1-XPF Interaction

Lars Petter Jordheim, Khaled H. Barakat, Laurence Heinrich-Balard, Eva-Laure Matera, Emeline Cros-Perrial, Karima Bouledrak, Rana El Sabeh, Rolando Perez-Pineiro, David S. Wishart, Richard Cohen, Jack Tuszynski and Charles Dumontet
Molecular Pharmacology July 1, 2013, 84 (1) 12-24; DOI: https://doi.org/10.1124/mol.112.082347
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