Computationally Driven Discovery of a BCR-ABL1 Kinase Inhibitor with Activity in Multidrug-Resistant Chronic Myeloid Leukemia

Hill, Jarvis; Givhan, R. Houston; Yi, Bin; Jones, Robert M.; Douglass, Eugene F.; Xi, Yaguang; Schaefer, III, Henry F.; Crich, David

doi:10.1021/acs.jmedchem.4c01852

Computationally Driven Discovery of a BCR-ABL1 Kinase Inhibitor with Activity in Multidrug-Resistant Chronic Myeloid Leukemia

Journal Article · Mon Sep 23 00:00:00 EDT 2024 · Journal of Medicinal Chemistry

DOI:https://doi.org/10.1021/acs.jmedchem.4c01852· OSTI ID:2447489

^[1]; Givhan, R. Houston ^[2]; Yi, Bin ^[3]; Jones, Robert M. ^[4]; Douglass, Eugene F. ^[3]; Xi, Yaguang ^[3]; ^[2]; ^[5]

Department of Pharmaceutical and Biomedical Sciences, University of Georgia, 250 West Green Street, Athens, Georgia 30602, United States, Department of Chemistry, University of Georgia, 302 East Campus Road, Athens, Georgia 30602, United States
Department of Chemistry, University of Georgia, 302 East Campus Road, Athens, Georgia 30602, United States, Center for Computational Quantum Chemistry, University of Georgia, 1004 Cedar Street, Athens, Georgia 30602, United States
Department of Pharmaceutical and Biomedical Sciences, University of Georgia, 250 West Green Street, Athens, Georgia 30602, United States
Independent consultant, P.O. Box 568, Oakley, Utah 84055-0568, United States
Department of Pharmaceutical and Biomedical Sciences, University of Georgia, 250 West Green Street, Athens, Georgia 30602, United States, Department of Chemistry, University of Georgia, 302 East Campus Road, Athens, Georgia 30602, United States, Complex Carbohydrate Research Center, University of Georgia, 315 Riverbend Road, Athens, Georgia 30602, United States

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Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0018412

OSTI ID:: 2447489

Alternate ID(s):: OSTI ID: 2462680

Journal Information:: Journal of Medicinal Chemistry, Journal Name: Journal of Medicinal Chemistry Journal Issue: 19 Vol. 67; ISSN 0022-2623

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (55)

The role of databases in support of computational chemistry calculations Feller, David Journal of Computational Chemistry, Vol. 17, Issue 13 https://doi.org/10.1002/(SICI)1096-987X(199610)17:13<1571::AID-JCC9>3.0.CO;2-P	journal	October 1996
Substituent effects on the physical properties and pKa of aniline Gross, Kevin C.; Seybold, Paul G. International Journal of Quantum Chemistry, Vol. 80, Issue 4-5 https://doi.org/10.1002/1097-461X(2000)80:4/5<1107::AID-QUA60>3.0.CO;2-T	journal	January 2000
Structural Studies of Crystalline Enamines Brown, Kevin L.; Damm, Lorenz; Dunitz, Jack D. Helvetica Chimica Acta, Vol. 61, Issue 8 https://doi.org/10.1002/hlca.19780610839	journal	December 1978
Overexpression of P‐glycoprotein and resistance to Imatinib in chronic myeloid leukemia patients Ammar, Mariam; Louati, Nour; Frikha, Imen Journal of Clinical Laboratory Analysis, Vol. 34, Issue 9 https://doi.org/10.1002/jcla.23374	journal	July 2020
Jaguar: A high-performance quantum chemistry software program with strengths in life and materials sciences Bochevarov, Art D.; Harder, Edward; Hughes, Thomas F. International Journal of Quantum Chemistry, Vol. 113, Issue 18 https://doi.org/10.1002/qua.24481	journal	July 2013
Constitutive Overexpression of P-glycoprotein, Rather than Breast Cancer Resistance Protein or Organic Cation Transporter 1, Contributes to Acquisition of Imatinib-Resistance in K562 Cells Hirayama, Chie; Watanabe, Hiroshi; Nakashima, Reiko Pharmaceutical Research, Vol. 25, Issue 4 https://doi.org/10.1007/s11095-007-9376-3	journal	October 2007
A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants Juliano, R. L.; Ling, V. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 455, Issue 1 https://doi.org/10.1016/0005-2736(76)90160-7	journal	November 1976
Preferential cytotoxicity for multidrug-resistant K562 cells using the combination of a photosensitizer and a cyanine dye Kanofsky, Jeffrey R.; Sima, Paul D. Journal of Photochemistry and Photobiology B: Biology, Vol. 54, Issue 2-3 https://doi.org/10.1016/S1011-1344(00)00008-7	journal	February 2000
New heterocyclic analogues of 4-(2-chloro-5-methoxyanilino)quinazolines as potent and selective c-Src kinase inhibitors Barlaam, Bernard; Fennell, Mike; Germain, Hervé Bioorganic & Medicinal Chemistry Letters, Vol. 15, Issue 24 https://doi.org/10.1016/j.bmcl.2005.08.106	journal	December 2005
Discovery of TAK-960: An orally available small molecule inhibitor of polo-like kinase 1 (PLK1) Nie, Zhe; Feher, Victoria; Natala, Srinivasa Bioorganic & Medicinal Chemistry Letters, Vol. 23, Issue 12 https://doi.org/10.1016/j.bmcl.2013.02.083	journal	June 2013
Bond stability of the “undesirable” heteroatom–heteroatom molecular moieties for high-throughput screening libraries Yu, Bo; Reynisson, Jóhannes European Journal of Medicinal Chemistry, Vol. 46, Issue 12 https://doi.org/10.1016/j.ejmech.2011.09.044	journal	December 2011
Weighted Averaging Scheme and Local Atomic Descriptor for pK_a Prediction Based on Density Functional Theory Yu, Haoyu S.; Watson, Mark A.; Bochevarov, Art D. Journal of Chemical Information and Modeling, Vol. 58, Issue 2 https://doi.org/10.1021/acs.jcim.7b00537	journal	February 2018
New Basis Set Exchange: An Open, Up-to-Date Resource for the Molecular Sciences Community Pritchard, Benjamin P.; Altarawy, Doaa; Didier, Brett Journal of Chemical Information and Modeling, Vol. 59, Issue 11 https://doi.org/10.1021/acs.jcim.9b00725	journal	October 2019
Multiconformation, Density Functional Theory-Based p K _a Prediction in Application to Large, Flexible Organic Molecules with Diverse Functional Groups Bochevarov, Art D.; Watson, Mark A.; Greenwood, Jeremy R. Journal of Chemical Theory and Computation, Vol. 12, Issue 12 https://doi.org/10.1021/acs.jctc.6b00805	journal	November 2016
Discovery and Evaluation of Clinical Candidate AZD3759, a Potent, Oral Active, Central Nervous System-Penetrant, Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitor Zeng, Qingbei; Wang, Jiabing; Cheng, Ziqiang Journal of Medicinal Chemistry, Vol. 58, Issue 20 https://doi.org/10.1021/acs.jmedchem.5b01073	journal	October 2015
Synthesis of Trialkylhydroxylamines by Stepwise Reduction of O-Acyl N,N-Disubstituted Hydroxylamines: Substituent Effects on the Reduction of O-(1-Acyloxyalkyl)hydroxylamines and on the Conformational Dynamics of N-Alkoxypiperidines Dhanju, Sandeep; Blazejewski, Brendan W.; Crich, David The Journal of Organic Chemistry, Vol. 82, Issue 10 https://doi.org/10.1021/acs.joc.7b00717	journal	May 2017
Synthesis of O-tert-Butyl-N,N-disubstituted Hydroxylamines by N–O Bond Formation Hill, Jarvis; Crich, David Organic Letters, Vol. 23, Issue 16 https://doi.org/10.1021/acs.orglett.1c02215	journal	July 2021
Basis Set Exchange: A Community Database for Computational Sciences Schuchardt, Karen L.; Didier, Brett T.; Elsethagen, Todd Journal of Chemical Information and Modeling, Vol. 47, Issue 3 https://doi.org/10.1021/ci600510j	journal	March 2007
Synthesis and Evaluation of Di- and Trimeric Hydroxylamine-Based β-(1→3)-Glucan Mimetics Ferry, Angélique; Malik, Gaëlle; Guinchard, Xavier Journal of the American Chemical Society, Vol. 136, Issue 42 https://doi.org/10.1021/ja507084t	journal	October 2014
Diversity-Oriented Synthesis of N,N,O-Trisubstituted Hydroxylamines from Alcohols and Amines by N–O Bond Formation Hill, Jarvis; Hettikankanamalage, Asiri A.; Crich, David Journal of the American Chemical Society, Vol. 142, Issue 35 https://doi.org/10.1021/jacs.0c05991	journal	August 2020
7-Alkoxy-4-phenylamino-3-quinolinecar-bonitriles as Dual Inhibitors of Src and Abl Kinases Boschelli, Diane H.; Wang, Yanong D.; Johnson, Steve Journal of Medicinal Chemistry, Vol. 47, Issue 7 https://doi.org/10.1021/jm0499458	journal	February 2004
Synthesis and Src Kinase Inhibitory Activity of 2-Phenyl- and 2-Thienyl-7-phenylaminothieno[3,2-b]pyridine-6-carbonitriles Boschelli, Diane H.; Wu, Biqi; Barrios Sosa, Ana Carolina Journal of Medicinal Chemistry, Vol. 48, Issue 11 https://doi.org/10.1021/jm050175p	journal	May 2005
Design and Synthesis of β-Site Amyloid Precursor Protein Cleaving Enzyme (BACE1) Inhibitors with in Vivo Brain Reduction of β-Amyloid Peptides Swahn, Britt-Marie; Kolmodin, Karin; Karlström, Sofia Journal of Medicinal Chemistry, Vol. 55, Issue 21 https://doi.org/10.1021/jm3009025	journal	September 2012
Rules for Identifying Potentially Reactive or Promiscuous Compounds Bruns, Robert F.; Watson, Ian A. Journal of Medicinal Chemistry, Vol. 55, Issue 22 https://doi.org/10.1021/jm301008n	journal	October 2012
Rapid chromatographic technique for preparative separations with moderate resolution Still, W. Clark; Kahn, Michael; Mitra, Abhijit The Journal of Organic Chemistry, Vol. 43, Issue 14 https://doi.org/10.1021/jo00408a041	journal	July 1978
An NMR Method for the Quantitative Assessment of Intramolecular Hydrogen Bonding; Application to Physicochemical, Environmental, and Biochemical Properties Abraham, Michael H.; Abraham, Raymond J.; Acree, William E. The Journal of Organic Chemistry, Vol. 79, Issue 22 https://doi.org/10.1021/jo502080p	journal	November 2014
Accurate Prediction of Acidity Constants in Aqueous Solution via Density Functional Theory and Self-Consistent Reaction Field Methods Klicić, Jasna J.; Friesner, Richard A.; Liu, Shi-Yi The Journal of Physical Chemistry A, Vol. 106, Issue 7 https://doi.org/10.1021/jp012533f	journal	February 2002
Intramolecular Hydrogen Bonding in ortho-Substituted Arylamide Oligomers: A Computational and Experimental Study of ortho-Fluoro- and ortho-Chloro-N-methylbenzamides Galan, Jhenny F.; Brown, Jodian; Wildin, Jayme L. The Journal of Physical Chemistry B, Vol. 113, Issue 38 https://doi.org/10.1021/jp905261p	journal	September 2009
Potent Vinblastine C20′ Ureas Displaying Additionally Improved Activity Against a Vinblastine-Resistant Cancer Cell Line Barker, Timothy J.; Duncan, Katharine K.; Otrubova, Katerina ACS Medicinal Chemistry Letters, Vol. 4, Issue 10 https://doi.org/10.1021/ml400281w	journal	September 2013
Global target profile of the kinase inhibitor bosutinib in primary chronic myeloid leukemia cells Remsing Rix, L. L.; Rix, U.; Colinge, J. Leukemia, Vol. 23, Issue 3 https://doi.org/10.1038/leu.2008.334	journal	November 2008
The clinical significance of ABCB1 overexpression in predicting outcome of CML patients undergoing first-line imatinib treatment Eadie, L. N.; Dang, P.; Saunders, V. A. Leukemia, Vol. 31, Issue 1 https://doi.org/10.1038/leu.2016.179	journal	June 2016
Comprehensive analysis of kinase inhibitor selectivity Davis, Mindy I.; Hunt, Jeremy P.; Herrgard, Sanna Nature Biotechnology, Vol. 29, Issue 11 https://doi.org/10.1038/nbt.1990	journal	October 2011
Cancer drug resistance: an evolving paradigm Holohan, Caitriona; Van Schaeybroeck, Sandra; Longley, Daniel B. Nature Reviews Cancer, Vol. 13, Issue 10 https://doi.org/10.1038/nrc3599	journal	September 2013
Multidrug resistance in cancer: role of ATP–dependent transporters Gottesman, Michael M.; Fojo, Tito; Bates, Susan E. Nature Reviews Cancer, Vol. 2, Issue 1 https://doi.org/10.1038/nrc706	journal	January 2002
Targeting multidrug resistance in cancer Szakács, Gergely; Paterson, Jill K.; Ludwig, Joseph A. Nature Reviews Drug Discovery, Vol. 5, Issue 3 https://doi.org/10.1038/nrd1984	journal	March 2006
Targeted inhibitors of P-glycoprotein increase chemotherapeutic-induced mortality of multidrug resistant tumor cells Nanayakkara, Amila K.; Follit, Courtney A.; Chen, Gang Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-19325-x	journal	January 2018
P-glycoprotein-mediated drug efflux is a resistance mechanism of chronic myelogenous leukemia cells to treatment with imatinib mesylate Illmer, T.; Schaich, M.; Platzbecker, U. Leukemia, Vol. 18, Issue 3 https://doi.org/10.1038/sj.leu.2403257	journal	January 2004
Multidrug resistance mediated by the breast cancer resistance protein BCRP (ABCG2) Austin Doyle, L.; Ross, Douglas D. Oncogene, Vol. 22, Issue 47 https://doi.org/10.1038/sj.onc.1206938	journal	October 2003
Organic Fluorine as a Hydrogen-Bond Acceptor: Recent Examples and Applications Paquin, Jean-François; Champagne, Pier; Desroches, Justine Synthesis, Vol. 47, Issue 03 https://doi.org/10.1055/s-0034-1379537	journal	November 2014
Gaussian basis sets for use in correlated molecular calculations. I. The atoms boron through neon and hydrogen Dunning, Thom H. The Journal of Chemical Physics, Vol. 90, Issue 2 https://doi.org/10.1063/1.456153	journal	January 1989
Gaussian basis sets for use in correlated molecular calculations. V. Core‐valence basis sets for boron through neon Woon, David E.; Dunning, Thom H. The Journal of Chemical Physics, Vol. 103, Issue 11 https://doi.org/10.1063/1.470645	journal	September 1995
A multidrug resistance transporter from human MCF-7 breast cancer cells Doyle, L. A.; Yang, W.; Abruzzo, L. V. Proceedings of the National Academy of Sciences, Vol. 95, Issue 26 https://doi.org/10.1073/pnas.95.26.15665	journal	December 1998
Effects of Orally Active Taxanes on P-Glycoprotein Modulation and Colon and Breast Carcinoma Drug Resistance Vredenburg, M. R.; Ojima, I.; Veith, J. JNCI Journal of the National Cancer Institute, Vol. 93, Issue 16 https://doi.org/10.1093/jnci/93.16.1234	journal	August 2001
The Conduct of in Vitro Studies to Address Time-Dependent Inhibition of Drug-Metabolizing Enzymes: A Perspective of the Pharmaceutical Research and Manufacturers of America Grimm, Scott W.; Einolf, Heidi J.; Hall, Steven D. Drug Metabolism and Disposition, Vol. 37, Issue 7 https://doi.org/10.1124/dmd.109.026716	journal	April 2009
Interaction of Imatinib Mesilate with Human P-Glycoprotein Hamada, Akinobu; Miyano, Hideto; Watanabe, Hiroshi Journal of Pharmacology and Experimental Therapeutics, Vol. 307, Issue 2 https://doi.org/10.1124/jpet.103.055574	journal	September 2003
Dasatinib Cellular Uptake and Efflux in Chronic Myeloid Leukemia Cells: Therapeutic Implications Hiwase, Devendra K.; Saunders, Verity; Hewett, Duncan Clinical Cancer Research, Vol. 14, Issue 12 https://doi.org/10.1158/1078-0432.CCR-07-5095	journal	June 2008
The Novel BCR-ABL and FLT3 Inhibitor Ponatinib Is a Potent Inhibitor of the MDR-Associated ATP-Binding Cassette Transporter ABCG2 Sen, Rupashree; Natarajan, Karthika; Bhullar, Jasjeet Molecular Cancer Therapeutics, Vol. 11, Issue 9 https://doi.org/10.1158/1535-7163.MCT-12-0302	journal	September 2012
Mechanisms of Resistance to Cabazitaxel Duran, George E.; Wang, Yan C.; Francisco, E. Brian Molecular Cancer Therapeutics, Vol. 14, Issue 1 https://doi.org/10.1158/1535-7163.MCT-14-0155	journal	January 2015
Cyclosporine inhibition of P-glycoprotein in chronic myeloid leukemia blast phase List, Alan F.; Kopecky, Kenneth J.; Willman, Cheryl L. Blood, Vol. 100, Issue 5 https://doi.org/10.1182/blood.V100.5.1910.h81702001910_1910_1912	journal	September 2002
MDR1 gene overexpression confers resistance to imatinib mesylate in leukemia cell line models Mahon, François-Xavier; Belloc, Francis; Lagarde, Valérie Blood, Vol. 101, Issue 6 https://doi.org/10.1182/blood.V101.6.2368	journal	March 2003
Tumor heterogeneity and drug resistance. Dexter, D. L.; Leith, J. T. Journal of Clinical Oncology, Vol. 4, Issue 2 https://doi.org/10.1200/JCO.1986.4.2.244	journal	February 1986
The Role of ABC Transporters in Clinical Practice Leonard, Gregory D.; Fojo, Tito; Bates, Susan E. The Oncologist, Vol. 8, Issue 5 https://doi.org/10.1634/theoncologist.8-5-411	journal	October 2003
The new allosteric inhibitor asciminib is susceptible to resistance mediated by ABCB1 and ABCG2 overexpression in vitro Eadie, Laura N.; Saunders, Verity A.; Branford, Susan Oncotarget, Vol. 9, Issue 17 https://doi.org/10.18632/oncotarget.24393	journal	February 2018
Topological Polar Surface Area: A Useful Descriptor in 2D-QSAR Prasanna, S.; Doerksen, R. Current Medicinal Chemistry, Vol. 16, Issue 1 https://doi.org/10.2174/092986709787002817	journal	January 2009
Three Decades of P-gp Inhibitors: Skimming Through Several Generations and Scaffolds Palmeira, A.; Sousa, E.; H. Vasconcelos, M. Current Medicinal Chemistry, Vol. 19, Issue 13 https://doi.org/10.2174/092986712800167392	journal	March 2012

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