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Research ArticleArticle

Screening of Transient Receptor Potential Canonical Channel Activators Identifies Novel Neurotrophic Piperazine Compounds

Seishiro Sawamura, Masahiko Hatano, Yoshinori Takada, Kyosuke Hino, Tetsuya Kawamura, Jun Tanikawa, Hiroshi Nakagawa, Hideharu Hase, Akito Nakao, Mitsuru Hirano, Rachapun Rotrattanadumrong, Shigeki Kiyonaka, Masayuki X. Mori, Motohiro Nishida, Yaopeng Hu, Ryuji Inoue, Ryu Nagata and Yasuo Mori
Molecular Pharmacology March 2016, 89 (3) 348-363; DOI: https://doi.org/10.1124/mol.115.102863
Seishiro Sawamura
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Masahiko Hatano
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Yoshinori Takada
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Kyosuke Hino
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Tetsuya Kawamura
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Jun Tanikawa
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Hiroshi Nakagawa
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Hideharu Hase
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Akito Nakao
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Mitsuru Hirano
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Rachapun Rotrattanadumrong
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Shigeki Kiyonaka
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Masayuki X. Mori
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Motohiro Nishida
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Yaopeng Hu
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Ryuji Inoue
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Ryu Nagata
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Yasuo Mori
Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering (S.S., Ma.H., Y.T., H.H., Mi.H., R.R., S.K., M.X.M., Y.M.), and Department of Technology and Ecology, Hall of Global Environmental Studies (S.K., Y.M.), Kyoto University, Kyoto, Japan; Sumitomo Dainippon Pharma Co., Ltd., Osaka, Japan (Y.T., K.H., T.K., J.T., H.N., R.N.); Division of Systems Medical Science, Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Japan (A.N.); Division of Cardiocirculatory Signaling, Okazaki Institute for Integrative Bioscience (National Institute for Physiological Sciences), National Institutes of Natural Sciences, Okazaki, Japan (M.N.); and Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, Japan (Y.H., R.I.)
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Abstract

Transient receptor potential canonical (TRPC) proteins form Ca2+-permeable cation channels activated upon stimulation of metabotropic receptors coupled to phospholipase C. Among the TRPC subfamily, TRPC3 and TRPC6 channels activated directly by diacylglycerol (DAG) play important roles in brain-derived neurotrophic factor (BDNF) signaling, promoting neuronal development and survival. In various disease models, BDNF restores neurologic deficits, but its therapeutic potential is limited by its poor pharmacokinetic profile. Elucidation of a framework for designing small molecules, which elicit BDNF-like activity via TRPC3 and TRPC6, establishes a solid basis to overcome this limitation. We discovered, through library screening, a group of piperazine-derived compounds that activate DAG-activated TRPC3/TRPC6/TRPC7 channels. The compounds [4-(5-chloro-2-methylphenyl)piperazin-1-yl](3-fluorophenyl)methanone (PPZ1) and 2-[4-(2,3-dimethylphenyl)piperazin-1-yl]-N-(2-ethoxyphenyl)acetamide (PPZ2) activated, in a dose-dependent manner, recombinant TRPC3/TRPC6/TRPC7 channels, but not other TRPCs, in human embryonic kidney cells. PPZ2 activated native TRPC6-like channels in smooth muscle cells isolated from rabbit portal vein. Also, PPZ2 evoked cation currents and Ca2+ influx in rat cultured central neurons. Strikingly, both compounds induced BDNF-like neurite growth and neuroprotection, which were abolished by a knockdown or inhibition of TRPC3/TRPC6/TRPC7 in cultured neurons. Inhibitors of Ca2+ signaling pathways, except calcineurin, impaired neurite outgrowth promotion induced by PPZ compounds. PPZ2 increased activation of the Ca2+-dependent transcription factor, cAMP response element–binding protein. These findings suggest that Ca2+ signaling mediated by activation of DAG-activated TRPC channels underlies neurotrophic effects of PPZ compounds. Thus, piperazine-derived activators of DAG-activated TRPC channels provide important insights for future development of a new class of synthetic neurotrophic drugs.

Footnotes

    • Received December 9, 2015.
    • Accepted January 4, 2016.
  • This work was supported by a Grant-in-Aid for Scientific Research on Innovative Areas “Oxygen Biology: A New Criterion for Integrated Understanding of Life” [Grant 26111004] of The Ministry of Education, Culture, Sports, Science and Technology, Japan; and a Grant-in-Aid for Scientific Research (A) [Grant 24249017] of Japan Society for the Promotion of Science. This work was funded by Sumitomo Dainippon Pharma Co., Ltd. Y.T., K.H., T.K., J.T., H.N., and R.N. were full-time employees of Sumitomo Dainippon Pharma Co., Ltd., when this study was conducted.

  • dx.doi.org/10.1124/mol.115.102863.

  • ↵Embedded ImageThis article has supplemental material available at (molpharm.aspetjournals.org).

  • Copyright © 2016 by The American Society for Pharmacology and Experimental Therapeutics
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Molecular Pharmacology: 89 (3)
Molecular Pharmacology
Vol. 89, Issue 3
1 Mar 2016
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Research ArticleArticle

Neurotrophic Action of Novel TRPC Channel Activators

Seishiro Sawamura, Masahiko Hatano, Yoshinori Takada, Kyosuke Hino, Tetsuya Kawamura, Jun Tanikawa, Hiroshi Nakagawa, Hideharu Hase, Akito Nakao, Mitsuru Hirano, Rachapun Rotrattanadumrong, Shigeki Kiyonaka, Masayuki X. Mori, Motohiro Nishida, Yaopeng Hu, Ryuji Inoue, Ryu Nagata and Yasuo Mori
Molecular Pharmacology March 1, 2016, 89 (3) 348-363; DOI: https://doi.org/10.1124/mol.115.102863

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Research ArticleArticle

Neurotrophic Action of Novel TRPC Channel Activators

Seishiro Sawamura, Masahiko Hatano, Yoshinori Takada, Kyosuke Hino, Tetsuya Kawamura, Jun Tanikawa, Hiroshi Nakagawa, Hideharu Hase, Akito Nakao, Mitsuru Hirano, Rachapun Rotrattanadumrong, Shigeki Kiyonaka, Masayuki X. Mori, Motohiro Nishida, Yaopeng Hu, Ryuji Inoue, Ryu Nagata and Yasuo Mori
Molecular Pharmacology March 1, 2016, 89 (3) 348-363; DOI: https://doi.org/10.1124/mol.115.102863
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