Russian version English version
Volume 15   Issue 2   Year 2020
Anrdrianov A.M.1, Kornoushenko Yu.V.1, Karpenko A.D.2, Bosko I.P.2, Ignatovich Zh.V.3, Koroleva E.V.3

Rational Design of Potential Bcr-Abl Tyrosine Kinase Inhibitors by the Methods of Molecular Modeling

Mathematical Biology & Bioinformatics. 2020;15(2):396-415.

doi: 10.17537/2020.15.396.

References

  1. Köstler W.J., Zielinski C.C. Targeting Receptor Tyrosine Kinases in Cancer. In: Receptor Tyrosine Kinases: Structure, Functions and Role in Human Disease. Eds.: Wheeler D.L., Yarden Y. New York: Springer Science & Business Media, 2015. P. 78–225.
  2. Maurer G., Tarkowski B., Baccarini M. Raf kinases in cancer-roles and therapeutic opportunities. Oncogene. 2011;30:3477–3488. doi: 10.1038/onc.2011.160
  3. Bardelli A., Parsons D.W., Silliman N., Ptak J., Szabo S., Saha S., Markowitz S., Willson J.K.V., Parmigiani G., Kinzler K.W., Vogelstein B., Velculescu V.E. Mutational analysis of the tyrosine kinome in colorectal cancers. Science. 2003;300(5621):949. doi: 10.1126/science.1082596
  4. Bartram C.R., de Klein A., Hagemeijer A., van Agthoven T., Geurts van Kessel A., Bootsma D., Grosveld G., Ferguson-Smith M.A., Davies T., Stone M., et al. Translocation of c-abl oncogene correlates with the presence of a Philadelphia chromosome in chronic myelocytic leukaemia. Nature. 1983;306:277–280. doi: 10.1038/306277a0
  5. Futreal P.A., Coin L., Marshall M., Down T., Hubbard T., Wooster R., Rahman N., Stratton M.R. A census of human cancer genes. Nat. Rev. Cancer. 2004;4:177–183. doi: 10.1038/nrc1299
  6. Kittler H., Tschand P. Driver mutations in the mitogen-activated protein kinase pathway: the seeds of good and evil. Br. J. Dermat. 2018;178:26–27.
  7. Sato S., Sanjo H., Takeda K., Ninomiya-Tsuji J., Yamamoto M., Kawai T., Matsumoto K., Takeuchi O., Akira S. Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat. Immunol. 2005;6(11):1087–1095. doi: 10.1038/ni1255
  8. Mueller B.K., Mack H., Teusch N. Rho kinase, a promising drug target for neurological disorders. Nat. Rev. Drug. Discov. 2005;4:98–387.
  9. Chong Z.Z., Shang Y.C., Wang S., Maiese K. A critical kinase cascade in neurological disorders: PI 3-K, Akt and Mtor. Future Neurol. 2012;7:733–748. doi: 10.2217/fnl.12.72
  10. Tabit C.E., Shenouda S.M., Holbrook M., Fetterman J.L., Kiani S., Frame A.A., Kluge M.A., Held A., Dohadwala M.M., Gokce N., Farb M.G., Rosenzweig J., Ruderman N., Vita J.A., Hamburg N.M. Protein kinase C-β contributes to impaired endothelial insulin signaling in humans with diabetes mellitus. Circulation. 2013;127:86–95. doi: 10.1161/CIRCULATIONAHA.112.127514
  11. Bhullar K.S., Lagarón N.O., McGowan E.M., Parmar I., Jha A., Hubbard B.P., Rupasinghe H.P. V. Kinase-targeted cancer therapies: progress, challenges and future directions. Mol. Cancer. 2018;17. Article No. 48. doi: 10.1186/s12943-018-0804-2
  12. Dar A.C., Shokat K.M. The evolution of protein kinase inhibitors from antagonists to agonists of cellular signaling. Annu. Rev. Biochem. 2011;80:769–795. doi: 10.1146/annurev-biochem-090308-173656
  13. Roskoski R. Classification of small molecule protein kinase inhibitors based upon the structures of their drug-enzyme complexes. Pharmacol. Res. 2016;103:26–48. doi: 10.1016/j.phrs.2015.10.021
  14. Kantarjian H., Sawyers C., Hochhaus A., Guilhot F., Schiffer C., Gambacorti-Passerini C., Niederwieser D., Resta D., Capdeville R., Zoellner U. et al. Hematologic and cytogenetic responses to imatinib mesylate in chronic leukemia. New Engl. J. Med. 2002;346:645–652. doi: 10.1056/NEJMoa011573
  15. Imatinib. New indications, but not robust evidence. Prescrire Int. 2008;95:91–94.
  16. O'Brien S.G., Guilhot F., Larson R.A., Gathmann I., Baccarani M., Cervantes F., Cornelissen J.J., Fischer T., Hochhaus A., Hughes T. et al.; IRIS Investigators. Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase chronic myeloid leukemia. New Engl. J. Med. 2003;348:994–1004. doi: 10.1056/NEJMoa022457
  17. Druker B.J., Guilhot F., O’Brien S.G., Gathmann I., Kantarjian H., Gattermann N., Deininger M.W.N., Silver R.T., Goldman J.M., Stone R.M. et al. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. New Engl. J. Med. 2006;355:2408–2417. doi: 10.1056/NEJMoa062867
  18. Hochhaus A., Larson R.A., Guilhot F., Radich J.P., Branford S., Hughes T.P., Baccarani M., Deininger M.W., Cervantes F., Fujihara S. et al. Long-term outcomes of imatinib treatment for chronic myeloid leukemia. New Engl. J. Med. 2017;376(10):917–927. doi: 10.1056/NEJMoa1609324
  19. Shah N.P., Tran C., Lee F.Y., Chen P., Norris D., Sawyers C.L. Overriding imatinib resistance with a novel ABL kinase inhibitor. Science. 2004;305(5682):399–401. doi: 10.1126/science.1099480
  20. Lombardo L.J., Lee F.Y., Chen P., Norris D., Barrish J.C., Behnia K., Castaneda S., Cornelius L.A.M., Das J., Doweyko A.M. et al. Discovery of N-(2-chloro-6-methyl-phenyl)-2-(6-(4-(2-hydroxyethyl)-piperazin-1-yl)-2-methylpyrimidin-4-ylamino) thiazole-5-carboxamide (BMS-354825), a dual Src/Abl kinase inhibitor with potent antitumor activity in preclinical assays. J. Med. Chem. 2004;47(27):6658–6661. doi: 10.1021/jm049486a
  21. Hochhaus A., Larson R.A., Guilhot F., Radich J.P., Branford S., Hughes T.P., Baccarani M., Deininger M.W., Cervantes F., Fujihara S. et al. Long-term outcomes of imatinib treatment for chronic myeloid leukemia. N. Engl. J. Med. 2017;376:917–927. doi: 10.1056/NEJMoa1609324
  22. Davies S., Reddy H., Caivano M., Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 2000;351:95–105. doi: 10.1042/0264-6021:3510095
  23. O’Hare T. A decade of nilotinib and dasatinib: From in vitro studies to first-line tyrosine kinase inhibitors. Cancer Res. 2016;76(20):5911–5913. doi: 10.1158/0008-5472.CAN-16-2483
  24. Saglio G., Kim D.W., Issaragrisil S., le Coutre P., Etienne G., Lobo C., Pasquini R., Clark R.E., Hochhaus A., Hughes T.P. et al. Nilotinib versus imatinib for newly diagnosed chronic myeloid leukemia. New Engl. J. Med. 2010;362(24):2251–2259. doi: 10.1056/NEJMoa0912614
  25. Kantarjian H.M., Hochhaus A., Saglio G., De Souza C., Flinn I.W., Stenke L., Goh Y.-T., Rosti G., Nakamae H., Gallagher N.J. et al. Nilotinib versus imatinib for the treatment of patients with newly diagnosed chronic phase, Philadelphia chromosome-positive, chronic myeloid leukaemia: 24-month minimum follow-up of the phase 3 randomised ENESTnd trial. The Lancet Oncol. 2011;12(9):841–851. doi: 10.1016/S1470-2045(11)70201-7
  26. Tan F.H., Putoczki T.L., Stylli S.S., Luwor R.B. Ponatinib: a novel multi-tyrosine kinase inhibitor against human malignancies. OncoTargets Ther. 2019;12:635–645. doi: 10.2147/OTT.S189391
  27. Lipton J.H., Chuah C., Guerci-Bresler A., Rosti G., Simpson D., Assouline S., Etienne G. et al. Ponatinib versus imatinib for newly diagnosed chronic myeloid leukaemia: An international, randomised, open-label, phase 3 trial. The Lancet Oncol. 2016;17(5):612–621. doi: 10.1016/S1470-2045(16)00080-2
  28. Wang D., Pan H., Wang Y. T315L: a novel mutation within BCR-ABL kinase domain confers resistance against ponatinib. Leuk. Lymphoma. 2017;58(7):1733–1735. doi: 10.1080/10428194.2016.1251591
  29. Kantarjian H.M., Cortes J.E., Kim D.W., Khoury H.J., Brümmendorf T.H., Porkka K., Martinelli G., Durrant S., Leip E., Kelly V. et al. Bosutinib safety and management of toxicity in leukemia patients with resistance or intolerance to imatinib and other tyrosine kinase inhibitors. Blood. 2014;123(9):1309–1318. doi: 10.1182/blood-2013-07-513937
  30. Cortes J.E., Kim D.W., Kantarjian H.M., Brümmendorf T.H., Dyagil I., Griskevicius L., Malhotra H., Powell C., Gogat K., Countouriotis A.M., Gambacorti-Passerini C.J. Bosutinib versus imatinib in newly diagnosed chronic-phase chronic myeloid leukemia: Results from the BELA trial. Clin. Oncol. 2012;30(28):3486–3492. doi: 10.1200/JCO.2011.38.7522
  31. Brümmendorf T.H., Cortes J.E., de Souza C.A., Guilhot F., Duvillié L., Pavlov D., Gogat K., Countouriotis A.M., Gambacorti-Passerini C. Bosutinib versus imatinib in newly diagnosed chronic-phase chronic myeloid leukaemia: Results from the 24-month follow-up of the BELA trial. Br. J. Haematol. 2015;168(1):69–81. doi: 10.1111/bjh.13108
  32. Kantarjian H.M., Cortes J.E., Kim D.W., Khoury H.J., Brümmendorf T.H., Porkka K., Martinelli G., Durrant S., Leip E., Kelly V., Turnbull K., Besson N., Gambacorti-Passerini C. Bosutinib safety and management of toxicity in leukemia patients with resistance or intolerance to imatinib and other tyrosine kinase inhibitors. Blood. 2014;123(9):1309–1318. doi: 10.1182/blood-2013-07-513937
  33. Stewart J.J.P. Optimization of parameters for semiempirical methods VI: more modifications to the NDDO approximations and re-optimization of parameters. J. Mol. Model. 2013;19:1–32. doi: 10.1007/s00894-012-1667-x
  34. Cousins K.R. Computer review of ChemDraw Ultra 12.0. J. Am. Chem. Soc. 2011;133(21):8388. doi: 10.1021/ja204075s
  35. Open Babel: The Open Source Chemistry Toolbox. http://openbabel.org/wiki/Main_Page (accessed 02.12.2020).
  36. Rappe A.K., Casewit C.J., Colwell K.S., Goddard III W.A., Skiff W.M. UFF, a full periodic table force field for molecular mechanics and molecular dynamics simulations. J. Am. Chem. Soc. 1992;114(25):10024–10035. doi: 10.1021/ja00051a040
  37. Alhossary A., Handoko S.D., Mu Y., Kwoh C.K. Fast, accurate, and reliable molecular docking with QuickVina 2. Bioinformatics. 2015;31(13):2214–2216. doi: 10.1093/bioinformatics/btv082
  38. Zhou T., Commodore L., Huang W.S., Wang Y., Thomas M., Keats J., Xu Q., Rivera V.M., Shakespeare W.C., Clackson T. et al. Structural mechanism of the Pan-BCR-ABL inhibitor ponatinib (AP24534): Lessons for overcoming kinase inhibitor resistance. Chem. Biol. Drug Des. 2011;77(1):1–11. doi: 10.1111/j.1747-0285.2010.01054.x
  39. Seeliger M.A., Nagar B., Frank F., Cao X., Henderson M.N., Kuriyan J. C-Src binds to the cancer drug imatinib with an inactive Abl/c-Kit conformation and a distributed thermodynamic penalty. Structure. 2007;15(3):299–311. doi: 10.1016/j.str.2007.01.015
  40. Weisberg E., Manley P.W., Breitenstein W., Brueggen J., Cowan-Jacob S.W., Ray A., Huntly B., Fabbro D., Fendrich G., Hall-Meyers E., Kung A.L., Mestan J., Daley G.Q., Callahan L., Catley L., Cavazza C., Azam M., Neuberg D., Wright R.D., Gilliland D.G., Griffin J.D. Characterization of AMN107, a selective inhibitor of native and mutant Bcr-Abl. Cancer Cell. 2005;7(2):129–141. doi: 10.1016/j.ccr.2005.01.007
  41. Tokarski J.S., Newitt J., Chang C.Y.J., Cheng J.D., Wittekind M., Kiefer S.E., Kish K., Lee F.Y.F., Borzilerri R., Lombardo L.J., Xie D., Zhang Y., Klei H.E. The Structure of Dasatinib (BMS-354825) Bound to Activated ABL Kinase Domain Elucidates Its Inhibitory Activity against Imatinib-Resistant ABL Mutants. Cancer Res. 2006;66:5790–5797. doi: 10.1158/0008-5472.CAN-05-4187
  42. Horio T., Hamasaki T., Inoue T., Wakayama T., Itou S., Naito H., Asaki T., Hayase H., Niwa T. Structural factors contributing to the Abl/Lyn dual inhibitory activity of 3-substituted benzamide derivatives. Bioorg. Med. Chem. Lett. 2007;17. 2712–2717. doi: 10.1016/j.bmcl.2007.03.002
  43. Stewart J.J.P. MOPAC2016. Stewart Computational Chemistry, Colorado Springs, Google Scholar, 2016.
  44. Klamt A., Schüürmann G.J. COSMO: a new approach to dielectric screening in solvents with explicit expressions for the screening energy and its gradient. Chem. Soc. Perkin Trans. 1993;2:799–805. doi: 10.1039/P29930000799
  45. Høyvik I.-M., Jansik B., Jørgensen P. Trust region minimization of orbital localization functions. J. Chem. Theory Comput. 2012;8:3137–3146. doi: 10.1021/ct300473g
  46. Case D.A., Belfon K., Ben-Shalom I.Y., Brozell S.R., Cerutti D.S., Cheatham III T.E., Cruzeiro V.W.D., Darden T.A., Duke R.E., Giambasu G. et al. AMBER 2020. San Francisco: University of California, 2020.
  47. Wang J., Wolf R.M., Caldwell J.W., Kollman P.A., Case D.A. Development and testing of a general Amber force field. J. Comput. Chem. 2004;25:1157–1174. doi: 10.1002/jcc.20035
  48. Jorgensen W.L., Chandrasekhar J., Madura J.D., Impey R.W., Klein M.L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 1983;79(2):926–935. doi: 10.1063/1.445869
  49. Ryckaert J.P., Ciccotti G., Berendsen H.J.C. Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 1977;23(3):327–341. doi: 10.1016/0021-9991(77)90098-5
  50. Essmann U., Perera L., Berkowitz M.L., Darden T., Lee H., Pedersen L.G. A smooth particle mesh Ewald method. J. Chem. Phys. 1995;103:8577–8593. doi: 10.1063/1.470117
  51. Durrant J.D., McCammon J.A. BINANA: A novel algorithm for ligand-binding characterization. J. Mol. Graph. Model. 2011;29(6):888–893. doi: 10.1016/j.jmgm.2011.01.004
  52. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF Chimera − a visualization system for exploratory research and analysis. J. Comput. Chem. 2004;25(13):1605–1612. doi: 10.1002/jcc.20084
  53. McDonald I.K., Thornton J.M. Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 1994;238(5):777–793. doi: 10.1006/jmbi.1994.1334
  54. Durrant J.D., McCammon J.A. NNScore 2.0: A neural-network receptor–ligand scoring function. J. Chem. Inf. Model. 2011;51(11):2897–2903. doi: 10.1021/ci2003889
  55. Sharma G., First E.A. Thermodynamic analysis reveals a temperature-dependent change in the catalytic mechanism of Bacillus stearothermophilus tyrosyl-tRNA synthetase. J. Biol. Chem. 2009;284(7):4179–4190. doi: 10.1074/jbc.M808500200
  56. Genheden S., Ryde U. The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinity. Expert Opin. Drug Discov. 2015;10(5):449–461. doi: 10.1517/17460441.2015.1032936
  57. Xu L., Sun H., Li Y., Wang J., Hou T. Assessing the performance of MM/PBSA and MM/GBSA methods. 3. The impact of force fields and ligand charge models. J. Phys. Chem. B. 2013;117(28):8408−8421. doi: 10.1021/jp404160y
  58. Sun H., Li Y., Tian S., Xu L., Hou T. Assessing the performance of MM/PBSA and MM/GBSA methods. 4. Accuracies of MM/PBSA and MM/GBSA methodologies evaluated by various simulation protocols using PDBbind data set. Phys. Chem. Chem. Phys. 2014;16:16719−16729. doi: 10.1039/C4CP01388C
  59. Lipinski C.A., Lombardo F., Dominy B.W., Feeney P.J. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug Del. Rev. 2001;46(1–3):3–26. PMID: 11259830. doi: 10.1016/S0169-409X(00)00129-0
  60. Christensen A.S., Kubař T., Cui Q., Elstner M. Semiempirical quantum mechanical methods for noncovalent interactions for chemical and biochemical applications. Chem. Rev. 2016;116(9):5301–5337. doi: 10.1021/acs.chemrev.5b00584
  61. Cherkasov A., Muratov E.N., Fourches D., Varnek A., Baskin II., Cronin M., Dearden J., Gramatica P., Martin Y.C., Todeschini R., Consonni V., Kuz'min V.E., Cramer R., Benigni R., Yang C., Rathman J., Terfloth L., Gasteiger J., Richard A., Tropsha A. QSAR modeling: where have you been? Where are you going to? J. Med. Chem. 2014;57(12):4977–5010. doi: 10.1021/jm4004285
  62. Kuseva C., Schultz T.W., Yordanova D., Tankova K., Kutsarova S., Pavlov T., Chapkanov A., Georgiev M., Gissi A., Sobanski T., Mekenyan O.G. The implementation of RAAF in the OECD QSAR Toolbox. Reg. Toxicol. Pharmacol. 2019;105:51–61. doi: 10.1016/j.yrtph.2019.03.018
Table of Contents Original Article
Math. Biol. Bioinf.
2020;15(2):396-415
doi: 10.17537/2020.15.396
published in Russian

Abstract (rus.)
Abstract (eng.)
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References

 

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