Protein kinase CK-1 inhibitors as new potential drugs for amyotrophic lateral sclerosis

Journal of Medicinal Chemistry

Volumn 57, Issue 6, 2014, Pages 2755-2772

  Salado, Irene G ^a   Redondo, Miriam ^a   Bello, Murilo L ^a,b   Perez, Concepción ^a   Liachko, Nicole F ^c,d   Kraemer, Brian C ^c,d,e   Miguel, Laetitia ^f,g   Lecourtois, Magalie ^f,g   Gil, Carmen ^a   Martinez, Ana ^a   Perez, Daniel I ^a  

^a INSTITUTO DE QUÍMICA MÉDICA   (Spain)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

^e UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^f INSERM   (France)

^g UNIVERSITY OF ROUEN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE I; CASEIN KINASE I INHIBITOR; PROTEIN KINASE INHIBITOR; TAR DNA BINDING PROTEIN; UNCLASSIFIED DRUG;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BLOOD BRAIN BARRIER; CELL STRAIN HEK293; DROSOPHILA; DRUG INDICATION; HUMAN; LIFESPAN; NEUROTOXICITY; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; TDP 43 PROTEINOPATHY;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BENZOTHIAZOLES; BLOOD-BRAIN BARRIER; CASEIN KINASE I; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; DNA-BINDING PROTEINS; DROSOPHILA; DRUG DESIGN; DRUG DISCOVERY; HEK293 CELLS; HETEROCYCLIC COMPOUNDS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR CONFORMATION; NEURONS; NEUROTOXICITY SYNDROMES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; SUBSTRATE SPECIFICITY;

EID: 84897437573     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm500065f     Document Type: Article

References (49)

1. Miller, R. G.; Mitchell, J. D.; Lyon, M.; Moore, D. H. Riluzole for amyotrophic lateral sclerosis (ALS)/motor neuron disease (MND) Cochrane Database Syst. Rev. 2007, CD001447
2. Robberecht, W.; Philips, T. The changing scene of amyotrophic lateral sclerosis Nature Rev. Neurosci. 2013, 14, 248-264
3. Regal, L.; Vanopdenbosch, L.; Tilkin, P.; Van den Bosch, L.; Thijs, V.; Sciot, R.; Robberecht, W. The G93C mutation in superoxide dismutase 1: clinicopathologic phenotype and prognosis Arch. Neurol. 2006, 63, 262-267
4. Venkova-Hristova, K.; Christov, A.; Kamaluddin, Z.; Kobalka, P.; Hensley, K. Progress in therapy development for amyotrophic lateral sclerosis. Neurol. Res. Int. 2012, 2012, Article ID 187234.
5. Rosen, D. R.; Siddique, T.; Patterson, D.; Figlewicz, D. A.; Sapp, P.; Hentati, A.; Donaldson, D.; Goto, J.; O'Regan, J. P.; Deng, H. X.; Rahman, Z.; Krizus, A.; McKenna-Yasek, D.; Cayabyab, A.; Gaston, S. M.; Berger, R.; Tanzi, R. E.; Halperin, J. J.; Herzfeldt, B.; Van Den Bergh, R.; Hung, W. Y.; Bird, T.; Deng, D.; Mulder, D. W.; Smyth, C.; Laing, N. G.; Soriano, E.; Pericak-Vance, M. A.; Haines, J.; Rouleau, G. A.; Gusella, J. S.; Horvitz, H. R.; Brown, R. H. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis Nature 1993, 362, 59-62
6. Kabashi, E.; Valdmanis, P. N.; Dion, P.; Spiegelman, D.; McConkey, B. J.; Vande Velde, C.; Bouchard, J. P.; Lacomblez, L.; Pochigaeva, K.; Salachas, F.; Pradat, P. F.; Camu, W.; Meininger, V.; Dupre, N.; Rouleau, G. A. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis Nature Genet. 2008, 40, 572-574
7. DeJesus-Hernandez, M.; MacKenzie, I. R.; Boeve, B. F.; Boxer, A. L.; Baker, M.; Rutherford, N. J.; Nicholson, A. M.; Finch, N. A.; Flynn, H.; Adamson, J.; Kouri, N.; Wojtas, A.; Sengdy, P.; Hsiung, G. Y.; Karydas, A.; Seeley, W. W.; Josephs, K. A.; Coppola, G.; Geschwind, D. H.; Wszolek, Z. K.; Feldman, H.; Knopman, D. S.; Petersen, R. C.; Miller, B. L.; Dickson, D. W.; Boylan, K. B.; Graff-Radford, N. R.; Rademakers, R. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS Neuron 2011, 72, 245-256
8. Renton, A. E.; Majounie, E.; Waite, A.; Simon-Sanchez, J.; Rollinson, S.; Gibbs, J. R.; Schymick, J. C.; Laaksovirta, H.; van Swieten, J. C.; Myllykangas, L.; Kalimo, H.; Paetau, A.; Abramzon, Y.; Remes, A. M.; Kaganovich, A.; Scholz, S. W.; Duckworth, J.; Ding, J.; Harmer, D. W.; Hernandez, D. G.; Johnson, J. O.; Mok, K.; Ryten, M.; Trabzuni, D.; Guerreiro, R. J.; Orrell, R. W.; Neal, J.; Murray, A.; Pearson, J.; Jansen, I. E.; Sondervan, D.; Seelaar, H.; Blake, D.; Young, K.; Halliwell, N.; Callister, J. B.; Toulson, G.; Richardson, A.; Gerhard, A.; Snowden, J.; Mann, D.; Neary, D.; Nalls, M. A.; Peuralinna, T.; Jansson, L.; Isoviita, V. M.; Kaivorinne, A. L.; Holtta-Vuori, M.; Ikonen, E.; Sulkava, R.; Benatar, M.; Wuu, J.; Chio, A.; Restagno, G.; Borghero, G.; Sabatelli, M.; Consortium, I.; Heckerman, D.; Rogaeva, E.; Zinman, L.; Rothstein, J. D.; Sendtner, M.; Drepper, C.; Eichler, E. E.; Alkan, C.; Abdullaev, Z.; Pack, S. D.; Dutra, A.; Pak, E.; Hardy, J.; Singleton, A.; Williams, N. M.; Heutink, P.; Pickering-Brown, S.; Morris, H. R.; Tienari, P. J.; Traynor, B. J. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD Neuron 2011, 72, 257-268
9. Neumann, M.; Sampathu, D. M.; Kwong, L. K.; Truax, A. C.; Micsenyi, M. C.; Chou, T. T.; Bruce, J.; Schuck, T.; Grossman, M.; Clark, C. M.; McCluskey, L. F.; Miller, B. L.; Masliah, E.; MacKenzie, I. R.; Feldman, H.; Feiden, W.; Kretzschmar, H. A.; Trojanowski, J. Q.; Lee, V. M. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis Science 2006, 314, 130-133
10. Sreedharan, J.; Blair, I. P.; Tripathi, V. B.; Hu, X.; Vance, C.; Rogelj, B.; Ackerley, S.; Durnall, J. C.; Williams, K. L.; Buratti, E.; Baralle, F.; de Belleroche, J.; Mitchell, J. D.; Leigh, P. N.; Al-Chalabi, A.; Miller, C. C.; Nicholson, G.; Shaw, C. E. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis Science 2008, 319, 1668-1672
11. Ash, P. E.; Zhang, Y. J.; Roberts, C. M.; Saldi, T.; Hutter, H.; Buratti, E.; Petrucelli, L.; Link, C. D. Neurotoxic effects of TDP-43 overexpression in C. elegans Hum. Mol. Genet. 2010, 19, 3206-3218
12. Li, Y.; Ray, P.; Rao, E. J.; Shi, C.; Guo, W.; Chen, X.; Woodruff, E. A., III; Fushimi, K.; Wu, J. Y. A Drosophila model for TDP-43 proteinopathy Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 3169-3174
13. Kabashi, E.; Lin, L.; Tradewell, M. L.; Dion, P. A.; Bercier, V.; Bourgouin, P.; Rochefort, D.; Bel Hadj, S.; Durham, H. D.; Vande Velde, C.; Rouleau, G. A.; Drapeau, P. Gain and loss of function of ALS-related mutations of TARDBP (TDP-43) cause motor deficits in vivo Hum. Mol. Genet. 2010, 19, 671-683
14. Wegorzewska, I.; Bell, S.; Cairns, N. J.; Miller, T. M.; Baloh, R. H. TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 18809-18814
15. Zhou, H.; Huang, C.; Chen, H.; Wang, D.; Landel, C. P.; Xia, P. Y.; Bowser, R.; Liu, Y. J.; Xia, X. G. Transgenic rat model of neurodegeneration caused by mutation in the TDP gene PLoS Genet. 2010, 6, e1000887
16. Uchida, A.; Sasaguri, H.; Kimura, N.; Tajiri, M.; Ohkubo, T.; Ono, F.; Sakaue, F.; Kanai, K.; Hirai, T.; Sano, T.; Shibuya, K.; Kobayashi, M.; Yamamoto, M.; Yokota, S.; Kubodera, T.; Tomori, M.; Sakaki, K.; Enomoto, M.; Hirai, Y.; Kumagai, J.; Yasutomi, Y.; Mochizuki, H.; Kuwabara, S.; Uchihara, T.; Mizusawa, H.; Yokota, T. Non-human primate model of amyotrophic lateral sclerosis with cytoplasmic mislocalization of TDP-43 Brain 2012, 135, 833-846
17. Bilican, B.; Serio, A.; Barmada, S. J.; Nishimura, A. L.; Sullivan, G. J.; Carrasco, M.; Phatnani, H. P.; Puddifoot, C. A.; Story, D.; Fletcher, J.; Park, I. H.; Friedman, B. A.; Daley, G. Q.; Wyllie, D. J.; Hardingham, G. E.; Wilmut, I.; Finkbeiner, S.; Maniatis, T.; Shaw, C. E.; Chandran, S. Mutant induced pluripotent stem cell lines recapitulate aspects of TDP-43 proteinopathies and reveal cell-specific vulnerability Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 5803-5808
18. Mackenzie, I. R.; Rademakers, R.; Neumann, M. TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia Lancet Neurol. 2010, 9, 995-1007
19. Lee, E. B.; Lee, V. M.; Trojanowski, J. Q. Gains or losses: molecular mechanisms of TDP43-mediated neurodegeneration Nature Rev. Neurosci. 2012, 13, 38-50
20. Neumann, M.; Kwong, L. K.; Lee, E. B.; Kremmer, E.; Flatley, A.; Xu, Y.; Forman, M. S.; Troost, D.; Kretzschmar, H. A.; Trojanowski, J. Q.; Lee, V. M. Phosphorylation of S409/410 of TDP-43 is a consistent feature in all sporadic and familial forms of TDP-43 proteinopathies Acta Neuropathol. 2009, 117, 137-149
21. Liachko, N. F.; Guthrie, C. R.; Kraemer, B. C. Phosphorylation promotes neurotoxicity in a Caenorhabditis elegans model of TDP-43 proteinopathy J. Neurosci. 2010, 30, 16208-16219
22. Liachko, N. F.; McMillan, P. J.; Guthrie, C. R.; Bird, T. D.; Leverenz, J. B.; Kraemer, B. C. CDC7 inhibition blocks pathological TDP-43 phosphorylation and neurodegeneration Ann. Neurol. 2013, 74, 39-52
23. Choksi, D. K.; Roy, B.; Chatterjee, S.; Yusuff, T.; Bakhoum, M. F.; Sengupta, U.; Ambegaokar, S.; Kayed, R.; Jackson, G. R. TDP-43 phosphorylation by casein kinase I{varepsilon} promotes oligomerization and enhances toxicity in vivo Hum. Mol. Genet. 2013, 23, 1025-1035
24. Hasegawa, M.; Arai, T.; Nonaka, T.; Kametani, F.; Yoshida, M.; Hashizume, Y.; Beach, T. G.; Buratti, E.; Baralle, F.; Morita, M.; Nakano, I.; Oda, T.; Tsuchiya, K.; Akiyama, H. Phosphorylated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis Ann. Neurol. 2008, 64, 60-70
25. Hu, J. H.; Zhang, H.; Wagey, R.; Krieger, C.; Pelech, S. L. Protein kinase and protein phosphatase expression in amyotrophic lateral sclerosis spinal cord J. Neurochem. 2003, 85, 432-442
26. Peters, J. M.; McKay, R. M.; McKay, J. P.; Graff, J. M. Casein kinase I transduces Wnt signals Nature 1999, 401, 345-350
27. Knippschild, U.; Gocht, A.; Wolff, S.; Huber, N.; Lohler, J.; Stoter, M. The casein kinase 1 family: participation in multiple cellular processes in eukaryotes Cell. Signalling 2005, 17, 675-689
28. Perez, D. I.; Gil, C.; Martinez, A. Protein kinases CK1 and CK2 as new targets for neurodegenerative diseases Med. Res. Rev. 2011, 31, 924-954
29. Kametani, F.; Nonaka, T.; Suzuki, T.; Arai, T.; Dohmae, N.; Akiyama, H.; Hasegawa, M. Identification of casein kinase-1 phosphorylation sites on TDP-43 Biochem. Biophys. Res. Commun. 2009, 382, 405-409
30. Walsh, D. P.; Chang, Y. T. Chemical genetics Chem. Rev. 2006, 106, 2476-2530
31. Baki, A.; Bielik, A.; Molnar, L.; Szendrei, G.; Keseru, G. M. A high throughput luminescent assay for glycogen synthase kinase-3beta inhibitors Assay Drug Dev. Technol. 2007, 5, 75-83
32. Mashhoon, N.; DeMaggio, A. J.; Tereshko, V.; Bergmeier, S. C.; Egli, M.; Hoekstra, M. F.; Kuret, J. Crystal structure of a conformation-selective casein kinase-1 inhibitor J. Biol. Chem. 2000, 275, 20052-20060
33. Drewry, D. H.; Bamborough, P.; Schneider, K.; Smith, G. K. The kinome and its impact on medicinal chemistry. In Kinase Drug Discovery; Ward, R. A.; Goldberg, F. W., Eds.; Royal Society of Chemistry: Cambridge, UK, 2012; pp 1-53.
34. Karaman, M. W.; Herrgard, S.; Treiber, D. K.; Gallant, P.; Atteridge, C. E.; Campbell, B. T.; Chan, K. W.; Ciceri, P.; Davis, M. I.; Edeen, P. T.; Faraoni, R.; Floyd, M.; Hunt, J. P.; Lockhart, D. J.; Milanov, Z. V.; Morrison, M. J.; Pallares, G.; Patel, H. K.; Pritchard, S.; Wodicka, L. M.; Zarrinkar, P. P. A quantitative analysis of kinase inhibitor selectivity Nature Biotechnol. 2008, 26, 127-132
35. Iguchi, Y.; Katsuno, M.; Takagi, S.; Ishigaki, S.; Niwa, J.; Hasegawa, M.; Tanaka, F.; Sobue, G. Oxidative stress induced by glutathione depletion reproduces pathological modifications of TDP-43 linked to TDP-43 proteinopathies Neurobiol. Dis. 2012, 45, 862-870
36. Di, L.; Kerns, E. H.; Fan, K.; McConnell, O. J.; Carter, G. T. High throughput artificial membrane permeability assay for blood-brain barrier Eur. J. Med. Chem. 2003, 38, 223-232
37. Crivori, P.; Cruciani, G.; Carrupt, P. A.; Testa, B. Predicting blood-brain barrier permeation from three-dimensional molecular structure J. Med. Chem. 2000, 43, 2204-2216
38. Miguel, L.; Frebourg, T.; Campion, D.; Lecourtois, M. Both cytoplasmic and nuclear accumulations of the protein are neurotoxic in Drosophila models of TDP-43 proteinopathies Neurobiol. Dis. 2011, 41, 398-406
39. Romano, M.; Feiguin, F.; Buratti, E. Drosophila Answers to TDP-43 Proteinopathies. J. Amino Acids 2012, 2012, Article ID 356081.
40. Osterwalder, T.; Yoon, K. S.; White, B. H.; Keshishian, H. A conditional tissue-specific transgene expression system using inducible GAL4 Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 12596-12601
41. Hemdan, M. M.; Fahmy, A. F.; Ali, N. F.; Hegazi, E.; Abd-Elhaleem, A. Synthesis of some new heterocycles derived from phenylacetyl isothiocyanate Chin. J. Chem. 2008, 26, 388-391
42. Halgren, T. A. Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94 J. Comput. Chem. 1996, 17, 490-519
43. Stewart, J. J. Optimization of parameters for semiempirical methods V: modification of NDDO approximations and application to 70 elements J. Mol. Model. 2007, 13, 1173-1213
44. SYBYL 8.0; Tripos International: 1699 South Hanley Rd., St., Louis, MO 63144 USA.
45. Trott, O.; Olson, A. J. AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading J. Comput. Chem. 2010, 31, 455-461
46. Seeliger, D.; de Groot, B. L. Ligand docking and binding site analysis with PyMOL and Autodock/Vina J. Comput.-Aided Mol. Des. 2010, 24, 417-422
47. ADP-Glo Kinase Assay Technical Manual; http://www.promega.com/tbs/.
48. Lasbleiz, J.; Burgun, A.; Marin, F.; Rolland, Y.; Duvauferrier, R. Vertebral trabecular network analysis on CT images J. Radiol. 2005, 86, 645-649
49. Yang, J. S.; Nam, H. J.; Seo, M.; Han, S. K.; Choi, Y.; Nam, H. G.; Lee, S. J.; Kim, S. OASIS: online application for the survival analysis of lifespan assays performed in aging research PLoS One 2011, 6, e23525