Screening of drugs that suppress Ste11 MAPKKK activation in yeast identified a c-Abl tyrosine kinase inhibitor

Bioscience, Biotechnology and Biochemistry

Volumn 71, Issue 3, 2007, Pages 772-782

  Kitagawa, Takao ^a   Hashizume, Yuko ^a   Murakane, Tatsuhiko ^a   Koga, Emi ^a   Nomura, Yuki ^a   Kakihara, Yoshito ^a,d   Fujieda, Ayako ^b   Uchida, Motoyuki ^b   Takahashi, Hidetoshi ^c,e   Hoshida, Hisashi ^a   Akada, Rinji ^a  

^a YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KUREHA CORPORATION   (Japan)

^c SNOW BRAND MILK PRODUCTS CO LTD   (Japan)

^d UNIVERSITY OF TORONTO   (Canada)

^e Strategic and Regulatory Affairs Consulting Department   (Japan)

Author keywords

c Abl tyrosine kinase; Drug screening; Genome wide analysis; Saccharomyces cerevisiae; Ste11

Indexed keywords

C-ABL TYROSINE KINASE; DRUG SCREENING; GENOME-WIDE ANALYSIS; STE11;

ACTIVATION ENERGY; CELLS; ENZYME INHIBITION; GROWTH KINETICS; SCREENING; YEAST;

DRUG PRODUCTS;

ABELSON KINASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; PHEROMONE; PROTEIN KINASE INHIBITOR; STE11 PROTEIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; DIPLOIDY; DRUG ANTAGONISM; DRUG EFFECT; DRUG SCREENING; ENZYME ACTIVATION; GENOME; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; YEAST;

DIPLOIDY; DRUG EVALUATION, PRECLINICAL; ENZYME ACTIVATION; GENOME, FUNGAL; HUMANS; MAP KINASE KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; PHEROMONES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-ABL; SIGNAL TRANSDUCTION; YEASTS;

SACCHAROMYCES CEREVISIAE;

EID: 33947585184     PISSN: 09168451     EISSN: 13476947     Source Type: Journal    
DOI: 10.1271/bbb.60610     Document Type: Article

References (49)

1. Bennasroune, A., Gardin, A., Aunis, D., Cremel, G., and Hubert, P., Tyrosine kinase receptors as attractive targets of cancer therapy. Crit. Rev. Oncol. Hematol., 50, 23-38 (2004).
2. Ishizawar, R., and Parsons, S. J., c-Src and cooperating partners in human cancer. Cancer Cell, 6, 209-214 (2004).
3. Blume-Jensen, P., and Hunter, T., Oncogenic kinase signalling. Nature, 411, 355-365 (2001).
4. Qi, M., and Elion, E. A., MAP kinase pathways, J. Cell Sci., 118, 3569-3572 (2005).
5. Herbst, R. S., Fukuoka, M., and Baselga, J., Gefitinib: a novel targeted approach to treating cancer. Nat. Rev. Cancer, 4, 956-965 (2004).
6. Hantschel, O., and Superti-Furga, G., Regulation of the c-Abl and Bcr-Abl tyrosine kinases. Nat. Rev. Mol. Cell. Biol., 5, 33-44 (2004).
7. Siegel-Lakhai, W. S., Beijnen, J. H., and Shellens, J. H. M., Current knowledge and future directions of the selective epidermal growth factor receptor inhibitors Erlotinib (Tarceva) and Gefitinib (Iressa). Oncologist, 10, 579-589 (2005).
8. Simon, J. A., and Bedalov, A., Yeast as a model system for anticancer drug discovery. Nat. Rev. Cancer, 4, 481-492 (2004).
9. 2+-signaling activity on the basis of the growth promoting effect on a yeast mutant with a peculiar phenotype. Biosci. Biotechnol. Biochem., 64, 1942-1946 (2000).
10. Tsuchiya, E., Yukawa, M., Miyakawa, T., Kimura, K. I., and Takahashi, H., Borrelidin inhibits a cyclin-dependent kinase (CDK), Cdc28/Cln2, of Saccharomyces cerevisiae. J. Antibiotics, 54, 84-90 (2001).
11. Miyamoto, Y., Machida, K., Mizunuma, M., Emoto, Y., Sato, N., Miyahara, K., Hirata, D., Usui, T., Takahashi, H., Osada, H., and Miyakawa, T., Identification of Saccharomyces cerevisiae isoleucyl-tRNA synthetase as a target of the G1-specific inhibitor Reveromycin A. J. Biol. Chem., 277, 28810-28814 (2002).
12. Kobayashi, Y., Mizunuma, M., Osada, H., and Miyakawa, T., Identification of Saccharomyces cerevisiae ribosomal protein L3 as a target of curvularol, a G1-specific inhibitor of mammalian cells. Biosci. Biotechnol. Biochem., 70, 2451-2459 (2006).
13. Stevenson, B. J., Rhodes, N., Errede, B., and Sprague, G. F., Jr., Constitutive mutants of the protein kinase STE11 activate the yeast pheromone response pathway in the absence of the G protein. Genes Dev., 6, 1293-1304 (1992).
14. Ramer, S. W., Elledge, S. J., and Davis, R. W., Dominant genetics using a yeast genomic library under the control of a strong inducible promoter. Proc. Natl. Acad. Sci. USA, 89, 11589-11593 (1992).
15. Cairns, B. R., Ramer, S. W., and Kornberg, R. D., Order of action of components in the yeast pheromone response pathway revealed with a dominant allele of the STE11 kinase and the multiple phosphorylation of the STE7 kinase. Genes Dev., 6, 1305-1318 (1992).
16. O'Rouke, S., and Herskowitz, I., The Hog1 MAPK prevents cross talk between the HOG and pheromone response MAPK pathways in Saccharomyces cerevisiae. Genes Dev., 12, 2874-2886 (1998).
17. Liu, H., Styles, C. A., and Fink, G. R., Elements of the yeast pheromone response pathway required for filamentous growth of diploids. Science, 262, 1741-1744 (1993).
18. Willingham, S., Outeiro, T. F., DeVit, M. J., Lindquist, S. L., and Muchowski, P. J., Yeast genes that enhance the toxicity of a mutant huntingtin fragment or α-synuclein. Science, 302, 1769-1772 (2003).
19. Krushner, D. B., Lindenbach, B. D., Grdzelishvili, V. Z., Noueiry, A. O., Poul, S. M., and Ahlquist, P., Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. Proc. Natl. Acad. Sci. USA, 100, 15764-15769 (2003).
20. Giorgini, F., Guidetti, P., Nguyen, Q., Bennett, S. C., and Muchowski, P. J., A genomic screen in yeast implicates kynurenine 3-monooxygenase as a therapeutic target for huntington's disease. Nat. Genet., 37, 526-531 (2005).
21. Panavas, T., Serviene, E., Brasher, J., and Nagy, P. D., Yeast genome-wide screen reveals dissimilar sets of host genes affecting replication of RNA viruses. Proc. Natl. Acad. Sci. USA, 102, 7326-7331 (2005).
22. Serviene, E., Shapka, N., Cheng, C., Panavas, T., Phuangrat, B., Baker, J., and Nagy, P. D., Genome-wide screen identifies host genes affecting viral RNA recombination. Proc. Natl. Acad. Sci. USA, 102, 10545-10550 (2005).
23. Ren, R., Mechanisms of BCR-ABL in the pathogenesis of chronic myelogenous leukaemia. Nat. Rev. Cancer, 5, 172-183 (2005).
24. Walkenhorst, J., Goga, A., Witte, O. N., and Superti-Furga, G., Analysis of human c-Abl tyrosine kinase activity and regulation in S. pombe. Oncogene, 12, 1513-1520 (1996).
25. Akada, R., Kallel, L., Johnson, D. I., and Kurjan, J., Genetic relationships between the G protein βγ complex, Ste5p, Ste20p and Cdc42p: investigation of effector roles in the yeast pheromone response pathway. Genetics, 143, 103-117 (1996).
26. Sikorski, R. S., and Hieter, P., A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics, 122, 19-27 (1989).
27. Akada, R., Yamamoto, J., and Yamashita, I., Screening and identification of yeast sequences that cause growth inhibition when overexpressed. Mol. Gen. Genet., 254, 267-274 (1997).
28. Whiteway, M., Hougan, L., and Thomas, D. Y., Overexpression of the STE4 gene leads to mating response in haploid Saccharomyces cerevisiae. Mol. Biol. Cell, 10, 217-222 (1990).
29. Kawahata, M., Amari, S., Nishizawa, Y., and Akada, R., A positive selection for plasmid loss in Saccharomyces cerevisiae using galactose-inducible growth inhibitory sequences. Yeast, 15, 1-10 (1999).
30. Rose, M. D., Winston, F., and Hieter, P., "Methods in Yeast Genetics: A Laboratory Course Manual," Cold Spring Harbor Laboratory Press, Cold Spring Harbor (1990).
31. Chen, D. C., Yang, B. C., and Kuo, T. T., One-step transformation of yeast in stationary phase. Curr. Genet., 21, 83-84 (1992).
32. Louvion, J. F., Abbas-Terki, T., and Picard, D., Hsp90 is required for pheromone signaling in yeast. Mol. Biol. Cell, 9, 3071-3083 (1998).
33. Sharma, S. V., Agatsuma, T., and Nakano, H., Targeting of the protein chaperone, HSP90, by the transformation suppressing agent, radicicol. Oncogene, 16, 2639-2645 (1998).
34. Schulte, T. W., Akinaga, S., Soga, S., Sullivan, W., Stensgard, B., Toft, D., and Neckers, L. M., Antibiotic radicicol binds to the N-terminal domain of Hsp90 and shares important biologic activities with geldanamycin. Cell Stress Chaperones, 3, 100-108 (1998).
35. Soga, S., Kozawa, T., Narumi, H., Akinaga, S., Irie, K., Matsumoto, K., Sharma, S. V., Nakano, H., Mizukami, T., and Hara, M., Radicicol leads to selective depletion of Raf kinase and disrupts K-Ras-activated aberrant signaling pathway. J. Biol. Chem., 273, 822-828 (1998).
36. Fry, D. W., Kraker, A. J., McMichael, A., Ambroso, L. A., Nelson, J. M., Leopold, W. R., Connors, R. W., and Bridges, A. J., A specific inhibitor of the epidermal growth factor receptor tyrosine kinase. Science, 265, 1093-1095 (1994).
37. Jackson, P., and Baltimore, D., N-terminal mutations activate the leukemogenic potential of the myristoylated form of c-abl. EMBO J., 8, 449-456 (1989).
38. Wilson, L. K., Benton, B. M., Zhou, S., Thorner, J., and Martin, G. S., The yeast immunophilin Fpr3 is a physiological substrate of the tyrosine-specific phosphoprotein phosphatase Ptp1. J. Biol. Chem., 270, 25185-25193 (1995).
39. Abbas-Terki, T., Donze, O., and Picard, D., The molecular chaperone Cdc37 is required for Ste11 function and pheromone-induced cell cycle arrest. FEBS Lett., 4, 111-116 (2000).
40. Lee, P., Shabbir, A., Cardozo, C., and Caplan, A. J., Sti1 and Cdc37 can stabilize Hsp90 in chaperone complexes with a protein kinase. Mol. Biol. Cell, 15, 1785-1792 (2004).
41. Persons, A. B., Brost, R. L., Ding, H., Li, Z., Zhang, C., Sheikh, B., Brown, G. W., Kane, P. M., Hughes, T. R., and Boone, C., Integration of chemical-genetic and genetic interaction data links bioactive compounds to cellular target pathways. Nat. Biotech., 22, 62-69 (2004).
42. Neckers, L., Schulte, T. W., and Mimnaugh, E., Geldanamycin as a potential anti-cancer agent: its molecular target and biochemical activity. Invest. New Drugs, 17, 361-373 (1999).
43. Ronnen, E. A., Kondagunta, G. V., Ishill, N., Sweeney, S. M., DeLuca, J. K., Schwartz, L., Bacik, J., and Motzer, R. J., A phase II trial of 17-(Allylamino)-17demethoxygeldanamycin in patients with papillary and clear cell renal cell carcinoma. Invest. New Drugs, 24, 543-546 (2006).
44. Chang, H. J., Nathan, D. F., and Lindquist, S., In vivo analysis of the Hsp90 cochaperone Sti1 (p60). Mol. Cell. Biol., 17, 318-325 (1997).
45. Yamamoto, A., Mizukami, Y., and Sakurai, H., Identi-fication of a novel class of target genes and a novel type of binding sequence of heat shock transcription factor in Saccharomyces cerevisiae. J. Biol. Chem., 280, 11911-11919 (2005).
46. Zhao, R., Davey, M., Hsu, Y., Kaplanek, P., Tong, A., Parsons, A. B., Krogan, N., Cagney, G., Mai, D., Greenblatt, J., Boone, C., Emili, A., and Houry, W. A., Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the Hsp90 chaperone. Cell, 120, 715-727 (2005).
47. Wurgler-Murphy, S. M., Maeda, T., Witten, E. A., and Saito, H., Regulation of the Saccharomyces cerevisiae HOG1 mitogen-activated protein kinase by the PTP2 and PTP3 protein tyrosine phosphatase. Mol. Cell. Biol., 17, 1289-1297 (1997).
48. Boshelli, D. H., Wang, Y. D., Fei, W. Y., Wu, B., Zhang, N., Dutia, M., Powell, D. W., Wissner, A., Arndt, K., Weber, J. M., and Boschelli, F., Synthesis and Src kinase inhibitory activity of a series of 4-phenylamino-3- quinolinecarbonitriles. J. Med. Chem., 44, 822-833 (2001).
49. Sebolt-Leopold, J. S., and English, J. M., Mechanisms of drug inhibition of signalling molecules. Nature, 441, 457-462 (2006).