Design of substrate-based BCR-ABL kinase inhibitors using the cyclotide scaffold

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Huang, Yen Hua ^a   Henriques, Sónia T ^a   Wang, Conan K ^a   Thorstholm, Louise ^a   Daly, Norelle L ^a,b   Kaas, Quentin ^a   Craik, David J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b JAMES COOK UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; PROTEIN KINASE INHIBITOR;

AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; CHEMISTRY; ENZYME SPECIFICITY; HUMAN; K-562 CELL LINE; MOLECULAR GENETICS; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; FUSION PROTEINS, BCR-ABL; HUMANS; K562 CELLS; MOLECULAR SEQUENCE DATA; PROTEIN KINASE INHIBITORS; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY;

EID: 84939213771     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep12974     Document Type: Article

References (65)

1. An, X. et al. BCR-ABL tyrosine kinase inhibitors in the treatment of Philadelphia chromosome positive chronic myeloid leukemia: a review. Leuk Res. 34, 1255-1268 (2010).
2. Lugo, T. G., Pendergast, A. M., Muller, A. J. & Witte, O. N. Tyrosine kinase activity and transformation potency of bcr-abl oncogene products. Science. 247, 1079-1082 (1990).
3. Quintas-Cardama, A., Kantarjian, H. & Cortes, J. Flying under the radar: the new wave of BCR-ABL inhibitors. Nat Rev Drug Discov. 6, 834-848 (2007).
4. Daley, G. Q., Van Etten, R. A. & Baltimore, D. Induction of chronic myelogenous leukemia in mice by the P210bcr/abl gene of the Philadelphia chromosome. Science. 247, 824-830 (1990).
5. Levinson, N. M. et al. A Src-like inactive conformation in the abl tyrosine kinase domain. PLoS Biol. 4, e144 (2006).
6. Gorre, M. E. et al. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science. 293, 876-880 (2001).
7. Soverini, S. et al. ABL mutations in late chronic phase chronic myeloid leukemia patients with up-front cytogenetic resistance to imatinib are associated with a greater likelihood of progression to blast crisis and shorter survival: a study by the GIMEMA Working Party on Chronic Myeloid Leukemia. J Clin Oncol. 23, 4100-4109 (2005).
8. Talpaz, M. et al. Dasatinib in imatinib-resistant Philadelphia chromosome-positive leukemias. N Engl J Med. 354, 2531-2541 (2006).
9. Kantarjian, H. et al. Nilotinib in imatinib-resistant CML and Philadelphia chromosome-positive ALL. N Engl J Med. 354, 2542-2551 (2006).
10. Weisberg, E. et al. Characterization of AMN107, a selective inhibitor of native and mutant Bcr-Abl. Cancer Cell. 7, 129-141 (2005).
11. Shah, N. P. et al. Overriding imatinib resistance with a novel ABL kinase inhibitor. Science. 305, 399-401 (2004).
12. Golas, J. M. et al. SKI-606, a 4-anilino-3-quinolinecarbonitrile dual inhibitor of Src and Abl kinases, is a potent antiproliferative agent against chronic myelogenous leukemia cells in culture and causes regression of K562 xenografts in nude mice. Cancer Res. 63, 375-381 (2003).
13. O'Hare, T. et al. AP24534, a pan-BCR-ABL inhibitor for chronic myeloid leukemia, potently inhibits the T315I mutant and overcomes mutation-based resistance. Cancer Cell. 16, 401-412 (2009).
14. O'Hare, T., Zabriskie, M. S., Eiring, A. M. & Deininger, M. W. Pushing the limits of targeted therapy in chronic myeloid leukaemia. Nat Rev Cancer. 12, 513-526 (2012).
15. Zabriskie, M. S. et al. BCR-ABL1 compound mutations combining key kinase domain positions confer clinical resistance to ponatinib in Ph chromosome-positive leukemia. Cancer Cell. 26, 428-442 (2014).
16. Levitzki, A. & Mishani, E. Tyrphostins and other tyrosine kinase inhibitors. Annu Rev Biochem. 75, 93-109 (2006).
17. Chapelat, J. et al. The Substrate-Activity-Screening methodology applied to receptor tyrosine kinases: a proof-of-concept study. Eur J Med Chem. 57, 1-9 (2012).
18. Eldar-Finkelman, H. & Eisenstein, M. Peptide inhibitors targeting protein kinases. Curr Pharm Des. 15, 2463-2470 (2009).
19. Songyang, Z. et al. Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr Biol. 4, 973-982 (1994).
20. Songyang, Z. et al. Catalytic specificity of protein-tyrosine kinases is critical for selective signalling. Nature. 373, 536-539 (1995).
21. Sato, A. K., Viswanathan, M., Kent, R. B. & Wood, C. R. Therapeutic peptides: technological advances driving peptides into development. Curr Opin Biotechnol. 17, 638-642 (2006).
22. Colgrave, M. L. & Craik, D. J. Thermal, chemical, and enzymatic stability of the cyclotide kalata B1: the importance of the cyclic cystine knot. Biochemistry. 43, 5965-5975 (2004).
23. Felizmenio-Quimio, M. E., Daly, N. L. & Craik, D. J. Circular proteins in plants: solution structure of a novel macrocyclic trypsin inhibitor from Momordica cochinchinensis. J Biol Chem. 276, 22875-22882 (2001).
24. Greenwood, K. P., Daly, N. L., Brown, D. L., Stow, J. L. & Craik, D. J. The cyclic cystine knot miniprotein MCoTI-II is internalized into cells by macropinocytosis. Int J Biochem Cell Biol. 39, 2252-2264 (2007).
25. Contreras, J., Elnagar, A. Y., Hamm-Alvarez, S. F. & Camarero, J. A. Cellular uptake of cyclotide MCoTI-I follows multiple endocytic pathways. J Controll Release. 155, 134-143 (2011).
26. Cascales, L. et al. Identification and characterization of a new family of cell-penetrating peptides: cyclic cell-penetrating peptides. J Biol Chem. 286, 36932-36943 (2011).
27. Gunasekera, S. et al. Engineering stabilized vascular endothelial growth factor-A antagonists: synthesis, structural characterization, and bioactivity of grafted analogues of cyclotides. J Med Chem. 51, 7697-7704 (2008).
28. Chan, L. Y. et al. Engineering pro-angiogenic peptides using stable, disulfide-rich cyclic scaffolds. Blood. 118, 6709-6717 (2011).
29. Aboye, T. L. et al. Design of a novel cyclotide-based CXCR4 antagonist with anti-human immunodeficiency virus (HIV)-1 activity. J Med Chem. 55, 10729-10734 (2012).
30. Wong, C. T. et al. Orally active peptidic bradykinin B1 receptor antagonists engineered from a cyclotide scaffold for inflammatory pain treatment. Angewandte Chemie. 51, 5620-5624 (2012).
31. Ji, Y. et al. In vivo activation of the p53 tumor suppressor pathway by an engineered cyclotide. J Am Chem Soc. 135, 11623-11633 (2013).
32. Thongyoo, P., Roque-Rosell, N., Leatherbarrow, R. J. & Tate, E. W. Chemical and biomimetic total syntheses of natural and engineered MCoTI cyclotides. Org Biomol Chem. 6, 1462-1470 (2008).
33. Henriques, S. T. et al. A novel quantitative kinase assay using bacterial surface display and flow cytometry. PLoS One. 8, e80474 (2013).
34. Parang, K. et al. Mechanism-based design of a protein kinase inhibitor. Nat Struct Biol. 8, 37-41 (2001).
35. Ward, B. C., Kavalukas, S., Brugnano, J., Barbul, A. & Panitch, A. Peptide inhibitors of MK2 show promise for inhibition of abdominal adhesions. J Surg Res. 169, e27-36 (2011).
36. Torcato, I. M. et al. The antimicrobial activity of Sub3 is dependent on membrane binding and cell-penetrating ability. Chembiochem. 14, 2013-2022 (2013).
37. Madani, F., Lindberg, S., Langel, U., Futaki, S. & Graslund, A. Mechanisms of cellular uptake of cell-penetrating peptides. J Biophys. 2011, 414729 (2011).
38. Lozzio, C. B. & Lozzio, B. B. Human chronic myelogenous leukemia cell-line with positive Philadelphia chromosome. Blood. 45, 321-334 (1975).
39. Avrahami, L., Licht-Murava, A., Eisenstein, M. & Eldar-Finkelman, H. GSK-3 inhibition: achieving moderate efficacy with high selectivity. Biochimica Et Biophysica Acta. 1834, 1410-1414 (2013).
40. Licht-Murava, A. & Eldar-Finkelman, H. Exploiting substrate recognition for selective inhibition of protein kinases. Curr Pharm Des. 18, 2914-2920 (2012).
41. Hantschel, O. et al. BCR-ABL uncouples canonical JAK2-STAT5 signaling in chronic myeloid leukemia. Nat. Chem. Biol. 8, 285-293 (2012).
42. Conibear, A. C. et al. The cyclic cystine ladder of theta-defensins as a stable, bifunctional scaffold: a proof-of-concept study using the integrin-binding RGD motif. Chembiochem. 15, 451-459 (2014).
43. Skaggs, B. J. et al. Phosphorylation of the ATP-binding loop directs oncogenicity of drug-resistant BCR-ABL mutants. Proc Natl Acad Sci USA. 103, 19466-19471 (2006).
44. D'Souza, C., Henriques, S. T., Wang, C. K. & Craik, D. J. Structural parameters modulating the cellular uptake of disulfide-rich cyclic cell-penetrating peptides: MCoTI-II and SFTI-1. Eur J Med Chem. (2014).
45. Huang, Y. H., Chaousis, S., Cheneval, O., Craik, D. J. & Henriques, S. T. Optimization of the cyclotide framework to improve cell penetration properties. Front Pharmacol. 6, 17, doi: 10.3389/fphar.2015.00017 (2015).
46. Olsson, M. H. M., Søndergaard, C. R., Rostkowski, M. & Jensen, J. H. PROPKA3: Consistent treatment of internal and surface residues in empirical pKa predictions. J Chem Theory Comput. 7, 525-537 (2011).
47. Beglov, D. & Roux, B. An integral equation to describe the solvation of polar molecules in liquid water. J Phys Chem. B. 101, 7821-7826 (1997).
48. Kovalenko, A. & Hirata, F. Potential of mean force between two molecular ions in a polar molecular solvent: a study by the three-dimensional reference interaction site model. J Phys Chem. B. 103, 7942-7957 (1999).
49. Case, D. A. et al. AMBER 13. (University of California, San Francisco, 2012).
50. Sindhikara, D. J., Yoshida, N. & Hirata, F. Placevent: an algorithm for prediction of explicit solvent atom distribution-application to HIV-1 protease and F-ATP synthase. J Comput Chem. 33, 1536-1543 (2012).
51. Hubbard, S. J. & Thornton, J. M. NACCESS, Computer Program. (Department of Biochemistry and Molecular Biology, University College London, 1993).
52. Schmid, N. et al. Definition and testing of the GROMOS force-field versions 54A7 and 54B7. Eur Biophys J. 40, 843-856 (2011).
53. Heinz, T. N., Gunsteren, W. F. V. & Hünenberger, P. H. Comparison of four methods to compute the dielectric permittivity of liquids from molecular dynamics simulations. J Chem Phys. 115, 1125-1136 (2001).
54. Bussi, G., Donadio, D. & Parrinello, M. Canonical sampling through velocity rescaling. J Chem Phys. 126, 014101, doi: 10.1063/1.2408420 (2007).
55. Berendsen, H. J. C., Postma, J. P. M., Van Gunsteren, W. F., DiNola, A. & Haak, J. R. Molecular dynamics with coupling to an external bath. J Chem Phys. 81, 3684-3690 (1984).
56. Hess, B., Bekker, H., Berendsen, H. J. C. & Fraaije, J. G. E. M. LINCS: A linear constraint solver for molecular simulations. J Comput Chem. 18, 1463-1472 (1997).
57. Pronk, S. et al. GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics (Oxford, England). 29, 845-854 (2013).
58. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J Mol Graph. 14, 33-38 27-28 (1996).
59. Baker, N. A., Sept, D., Joseph, S., Holst, M. J. & McCammon, J. A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA. 98, 10037-10041 (2001).
60. Dawson, P. E., Muir, T. W., Clark-Lewis, I. & Kent, S. B. Synthesis of proteins by native chemical ligation. Science. 266, 776-779 (1994).
61. Tam, J. P. & Lu, Y. A. A biomimetic strategy in the synthesis and fragmentation of cyclic protein. Protein Sci. 7, 1583-1592 (1998).
62. Vranken, W. F. et al. The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins. 59, 687-696 (2005).
63. Guntert, P., Mumenthaler, C. & Wuthrich, K. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J Mol Biol. 273, 283-298 (1997).
64. Brünger, A. T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr. 54, 905-921 (1998).
65. Troeira Henriques, S., Huang, Y. H., Chaousis, S., Wang, C. K. & Craik, D. J. Anticancer and toxic properties of cyclotides are dependent on phosphatidylethanolamine phospholipid targeting. Chembiochem. 15, 1956-1965 (2014).