Molecular basis underlying resistance to Mps1/TTK inhibitors

Oncogene

Volumn 35, Issue 19, 2016, Pages 2518-2528

  Koch, A ^a   Maia, A ^a   Janssen, A ^a,b   Medema, R H ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; MPI 0479605; NMS P 715; NOCODAZOLE; PHOSPHOTRANSFERASE; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN MPS1; REVERSINE; UNCLASSIFIED DRUG; WO 2009156315A 1; CELL CYCLE PROTEIN; PROTEIN KINASE INHIBITOR; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; TTK PROTEIN, HUMAN;

ARTICLE; CANCER CELL; CANCER INHIBITION; CANCER RESISTANCE; CENTROMERE; CONTROLLED STUDY; CROSS RESISTANCE; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME INHIBITION; FEMALE; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; IC50; IN VITRO STUDY; KINASE ASSAY; M PHASE CELL CYCLE CHECKPOINT; MPS1 GENE; POINT MUTATION; PRIORITY JOURNAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG DESIGN; DRUG RESISTANCE; GENETICS; MOLECULAR MODEL; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN CONFORMATION; TUMOR CELL LINE;

BASE SEQUENCE; CELL CYCLE PROTEINS; CELL LINE, TUMOR; DRUG DESIGN; DRUG RESISTANCE, NEOPLASM; HUMANS; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES;

EID: 84941686776     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.319     Document Type: Article

References (43)

1. Abrieu A, Magnaghi-Jaulin L, Kahana JA, Peter M, Castro A, Vigneron S et al. Mps1 is a kinetochore-associated kinase essential for the vertebrate mitotic checkpoint. Cell 2001; 106: 83-93.
2. Hardwick KG, Weiss E, Luca FC, Winey M, Murray AW. Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption. Science 1996; 273: 953-956.
3. Stucke VM, Sillje HH, Arnaud L, Nigg EA. Human Mps1 kinase is required for the spindle assembly checkpoint but not for centrosome duplication. EMBO J 2002; 21: 1723-1732.
4. Musacchio A, Salmon ED. The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 2007; 8: 379-393.
5. London N, Ceto S, Ranish JA, Biggins S. Phosphoregulation of Spc105 by Mps1 and PP1 regulates Bub1 localization to kinetochores. Curr Biol 2012; 22: 900-906.
6. Shepperd LA, Meadows JC, Sochaj AM, Lancaster TC, Zou J, Buttrick GJ et al. Phosphodependent recruitment of Bub1 and Bub3 to Spc7/KNL1 by Mph1 kinase maintains the spindle checkpoint. Curr Biol 2012; 22: 891-899.
7. Yamagishi Y, Yang CH, Tanno Y, Watanabe Y. MPS1/Mph1 phosphorylates the kinetochore protein KNL1/Spc7 to recruit SAC components. Nat Cell Biol 2012; 14: 746-752.
8. Janssen A, Kops GJ, Medema RH. Elevating the frequency of chromosome missegregation as a strategy to kill tumor cells. Proc Natl Acad Sci USA 2009; 106: 19108-19113.
9. Daniel J, Coulter J, Woo JH, Wilsbach K, Gabrielson E. High levels of the Mps1 checkpoint protein are protective of aneuploidy in breast cancer cells. Proc Natl Acad Sci USA 2011; 108: 5384-5389.
10. Lan W, Cleveland DW. A chemical tool box defines mitotic and interphase roles for Mps1 kinase. J Cell Biol 2010; 190: 21-24.
11. Liu X, Winey M. The MPS1 family of protein kinases. Annu Rev Biochem 2012; 81: 561-585.
12. Colombo R, Caldarelli M, Mennecozzi M, Giorgini ML, Sola F, Cappella P et al. Targeting the mitotic checkpoint for cancer therapy with NMS-P715, an inhibitor of MPS1 kinase. Cancer Res 2010; 70: 10255-10264.
13. Jemaa M, Galluzzi L, Kepp O, Senovilla L, Brands M, Boemer U et al. Characterization of novel MPS1 inhibitors with preclinical anticancer activity. Cell Death Differ 2013; 20: 1532-1545.
14. Tannous BA, Kerami M, Van der Stoop PM, Kwiatkowski N, Wang J, Zhou W et al. Effects of the selective MPS1 inhibitor MPS1-IN-3 on glioblastoma sensitivity to antimitotic drugs. J Natl Cancer Inst 2013; 105: 1322-1331.
15. Tardif KD, Rogers A, Cassiano J, Roth BL, Cimbora DM, McKinnon R et al. Characterization of the cellular and antitumor effects of MPI-0479605, a smallmolecule inhibitor of the mitotic kinase Mps1. Mol Cancer Ther 2011; 10: 2267-2275.
16. Hewitt L, Tighe A, Santaguida S, White AM, Jones CD, Musacchio A et al. Sustained Mps1 activity is required in mitosis to recruit O-Mad2 to the Mad1-C-Mad2 core complex. J Cell Biol 2010; 190: 25-34.
17. Santaguida S, Tighe A, D'Alise AM, Taylor SS, Musacchio A. Dissecting the role of MPS1 in chromosome biorientation and the spindle checkpoint through the small molecule inhibitor reversine. J Cell Biol 2010; 190: 73-87.
18. Barouch-Bentov R, Sauer K. Mechanisms of drug resistance in kinases. Expert Opin Investig Drugs 2011; 20: 153-208.
19. Liu Y, Gray NS. Rational design of inhibitors that bind to inactive kinase conformations. Nat Chem Biol 2006; 2: 358-364.
20. Chong CR, Janne PA. The quest to overcome resistance to EGFR-targeted therapies in cancer. Nat Med 2013; 19: 1389-1400.
21. Gorre ME, Mohammed M, Ellwood K, Hsu N, Paquette R, Rao PN et al. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 2001; 293: 876-880.
22. Weisberg E, Manley PW, Cowan-Jacob SW, Hochhaus A, Griffin JD. Second generation inhibitors of BCR-ABL for the treatment of imatinib-resistant chronic myeloid leukaemia. Nat Rev Cancer 2007; 7: 345-356.
23. Girdler F, Sessa F, Patercoli S, Villa F, Musacchio A, Taylor S. Molecular basis of drug resistance in aurora kinases. Chem Biol 2008; 15: 552-562.
24. Wacker SA, Houghtaling BR, Elemento O, Kapoor TM. Using transcriptome sequencing to identify mechanisms of drug action and resistance. Nat Chem Biol 2012; 8: 235-237.
25. Scutt PJ, Chu ML, Sloane DA, Cherry M, Bignell CR, Williams DH et al. Discovery and exploitation of inhibitor-resistant aurora and polo kinase mutants for the analysis of mitotic networks. J Biol Chem 2009; 284: 15880-15893.
26. Marina Caldarelli MA, Colombo R, Disingrini T, Nuvoloni S, Posteri H, Salsa M et al. Pyrazolo-quinazolines 2009; WO 2009156315 A1.
27. Glaab WE, Tindall KR. Mutation rate at the hprt locus in human cancer cell lines with specific mismatch repair-gene defects. Carcinogenesis 1997; 18: 1-8.
28. Vleugel M, Tromer E, Omerzu M, Groenewold V, Nijenhuis W, Snel B et al. Arrayed BUB recruitment modules in the kinetochore scaffold KNL1 promote accurate chromosome segregation. J Cell Biol 2013; 203: 943-955.
29. Kornev AP, Taylor SS, Ten Eyck LF. A helix scaffold for the assembly of active protein kinases. Proc Natl Acad Sci USA 2008; 105: 14377-14382.
30. Chu ML, Lang Z, Chavas LM, Neres J, Fedorova OS, Tabernero L et al. Biophysical and X-ray crystallographic analysis of Mps1 kinase inhibitor complexes. Biochemistry 2010; 49: 1689-1701.
31. Schmidt M, Budirahardja Y, Klompmaker R, Medema RH. Ablation of the spindle assembly checkpoint by a compound targeting Mps1. EMBO Rep 2005; 6: 866-872.
32. Cho SW, Kim S, Kim JM, Kim JS. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol 2013; 31: 230-232.
33. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE et al. RNA-guided human genome engineering via Cas9. Science 2013; 339: 823-826.
34. Forbes SA, Beare D, Gunasekaran P, Leung K, Bindal N, Boutselakis H et al. COSMIC: exploring the world's knowledge of somatic mutations in human cancer. Nucleic Acids Res 2015; 43: D805-D811.
35. Eyers PA, Churchill ME, Maller JL. The Aurora A and Aurora B protein kinases: a single amino acid difference controls intrinsic activity and activation by TPX2. Cell Cycle 2005; 4: 784-789.
36. Sloane DA, Trikic MZ, Chu ML, Lamers MB, Mason CS, Mueller I et al. Drug-resistant aurora A mutants for cellular target validation of the small molecule kinase inhibitors MLN8054 and MLN8237. ACS Chem Biol 2010; 5: 563-576.
37. D'Alise AM, Amabile G, Iovino M, Di Giorgio FP, Bartiromo M, Sessa F et al. Reversine, a novel Aurora kinases inhibitor, inhibits colony formation of human acute myeloid leukemia cells. Mol Cancer Ther 2008; 7: 1140-1149.
38. Vijay Kumar D, Hoarau C, Bursavich M, Slattum P, Gerrish D, Yager K et al. Lead optimization of purine based orally bioavailable Mps1 (TTK) inhibitors. Bioorg Med Chem Lett 2012; 22: 4377-4385.
39. Naud S, Westwood IM, Faisal A, Sheldrake P, Bavetsias V, Atrash B et al. Structure-based design of orally bioavailable 1H-pyrrolo[3,2-c]pyridine inhibitors of mitotic kinase monopolar spindle 1 (MPS1). J Med Chem 2013; 56: 10045-10065.
40. Nijenhuis W, Vallardi G, Teixeira A, Kops GJ, Saurin AT. Negative feedback at kinetochores underlies a responsive spindle checkpoint signal. Nat Cell Biol 2014; 16: 1257-1264.
41. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N et al. Multiplex genome engineering using CRISPR/Cas systems. Science 2013; 339: 819-823.
42. Kwiatkowski N, Jelluma N, Filippakopoulos P, Soundararajan M, Manak MS, Kwon M et al. Small-molecule kinase inhibitors provide insight into Mps1 cell cycle function. Nat Chem Biol 2010; 6: 359-368.
43. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of coot. Acta Crystallogr D Biol Crystallogr 2010; 66: 486-501.