publication . Article . 2018

Direct Binding between Pre-S1 and TRP-like Domains in TRPP Channels Mediates Gating and Functional Regulation by PIP2

Wang Zheng; Ruiqi Cai; Laura Hofmann; Vasyl Nesin; Qiaolin Hu; Wentong Long; Mohammad Fatehi; Xiong Liu; Shaimaa Hussein; Tim Kong; ...
Open Access
  • Published: 01 Feb 2018 Journal: Cell Reports, volume 22, pages 1,560-1,573 (issn: 2211-1247, Copyright policy)
  • Publisher: Elsevier BV
Abstract
SUMMARY Transient receptor potential (TRP) channels are regulated by diverse stimuli comprising thermal, chemical, and mechanical modalities. They are also commonly regulated by phosphatidylinositol-4,5-bisphosphate (PIP2), with underlying mechanisms largely unknown. We here revealed an intramolecular interaction of the TRPP3 N and C termini (N-C) that is functionally essential. The interaction was mediated by aromatic Trp81 in pre-S1 domain and cationic Lys568 in TRP-like domain. Structure-function analyses revealed similar N-C interaction in TRPP2 as well as TRPM8/-V1/-C4 via highly conserved tryptophan and lysine/arginine residues. PIP2 bound to cationic resi...
Persistent Identifiers
Subjects
Medical Subject Headings: lipids (amino acids, peptides, and proteins)
free text keywords: General Biochemistry, Genetics and Molecular Biology, Article, TRP, pre-S1, TRP domain, intramolecular interaction, electrophysiology, Lysine, TRPM8, Arginine, TRPP, Transient receptor potential channel, Intramolecular force, Gating, Chemistry, Tryptophan, Biophysics, lcsh:Biology (General), lcsh:QH301-705.5
Related Organizations
Funded by
NSERC
Project
  • Funder: Natural Sciences and Engineering Research Council of Canada (NSERC)
46 references, page 1 of 4

Arif Pavel, M., Lv, C., Ng, C., Yang, L., Kashyap, P., Lam, C., Valentino, V., Fung, H.Y., Campbell, T., Møller, S.G., et al. (2016). Function and regulation of TRPP2 ion channel revealed by a gain-of-function mutant. Proc. Natl. Acad. Sci. USA 113, E2363-E2372.

Beck, A., Speicher, T., Stoerger, C., Sell, T., Dettmer, V., Jusoh, S.A., Abdulmughni, A., Cavalie´ , A., Philipp, S.E., Zhu, M.X., et al. (2013). Conserved gating elements in TRPC4 and TRPC5 channels. J. Biol. Chem. 288, 19471-19483.

Bousova, K., Jirku, M., Bumba, L., Bednarova, L., Sulc, M., Franek, M., Vyklicky, L., Vondrasek, J., and Teisinger, J. (2015). PIP2 and PIP3 interact with N-terminus region of TRPM4 channel. Biophys. Chem. 205, 24-32.

Cao, E., Liao, M., Cheng, Y., and Julius, D. (2013). TRPV1 structures in distinct conformations reveal activation mechanisms. Nature 504, 113-118. [OpenAIRE]

Chen, X.Z., Vassilev, P.M., Basora, N., Peng, J.B., Nomura, H., Segal, Y., Brown, E.M., Reeders, S.T., Hediger, M.A., and Zhou, J. (1999). Polycystin-L is a calcium-regulated cation channel permeable to calcium ions. Nature 401, 383-386.

Clapham, D.E., Runnels, L.W., and Stru€bing, C. (2001). The TRP ion channel family. Nat. Rev. Neurosci. 2, 387-396. [OpenAIRE]

Czirja´ k, G., Petheo, G.L., Spa¨ t, A., and Enyedi, P. (2001). Inhibition of TASK-1 potassium channel by phospholipase C. Am. J. Physiol. Cell Physiol. 281, C700-C708.

Gao, Y., Cao, E., Julius, D., and Cheng, Y. (2016). TRPV1 structures in nanodiscs reveal mechanisms of ligand and lipid action. Nature 534, 347-351. [OpenAIRE]

Garcia-Elias, A., Berna-Erro, A., Rubio-Moscardo, F., Pardo-Pastor, C., Mrkonjic, S., Sepu´ lveda, R.V., Vicente, R., Gonza´ lez-Nilo, F., and Valverde, M.A. (2015). Interaction between the linker, pre-S1, and TRP domains determines folding, assembly, and trafficking of TRPV channels. Structure 23, 1404-1413.

Grieben, M., Pike, A.C., Shintre, C.A., Venturi, E., El-Ajouz, S., Tessitore, A., Shrestha, L., Mukhopadhyay, S., Mahajan, P., Chalk, R., et al. (2017). Structure of the polycystic kidney disease TRP channel Polycystin-2 (PC2). Nat. Struct. Mol. Biol. 24, 114-122.

Holendova, B., Grycova, L., Jirku, M., and Teisinger, J. (2012). PtdIns(4,5)P2 interacts with CaM binding domains on TRPM3 N-terminus. Channels (Austin) 6, 479-482. [OpenAIRE]

Huynh, K.W., Cohen, M.R., Jiang, J., Samanta, A., Lodowski, D.T., Zhou, Z.H., and Moiseenkova-Bell, V.Y. (2016). Structure of the full-length TRPV2 channel by cryo-EM. Nat. Commun. 7, 11130.

Jin, P., Bulkley, D., Guo, Y., Zhang, W., Guo, Z., Huynh, W., Wu, S., Meltzer, S., Cheng, T., Jan, L.Y., et al. (2017). Electron cryo-microscopy structure of the mechanotransduction channel NOMPC. Nature 547, 118-122.

Jirku, M., Bumba, L., Bednarova, L., Kubala, M., Sulc, M., Franek, M., Vyklicky, L., Vondrasek, J., Teisinger, J., and Bousova, K. (2015). Characterization of the part of N-terminal PIP2 binding site of the TRPM1 channel. Biophys. Chem. 207, 135-142.

Kim, S., Nie, H., Nesin, V., Tran, U., Outeda, P., Bai, C.X., Keeling, J., Maskey, D., Watnick, T., Wessely, O., and Tsiokas, L. (2016). The polycystin complex mediates Wnt/Ca(2+) signalling. Nat. Cell Biol. 18, 752-764. [OpenAIRE]

46 references, page 1 of 4
Abstract
SUMMARY Transient receptor potential (TRP) channels are regulated by diverse stimuli comprising thermal, chemical, and mechanical modalities. They are also commonly regulated by phosphatidylinositol-4,5-bisphosphate (PIP2), with underlying mechanisms largely unknown. We here revealed an intramolecular interaction of the TRPP3 N and C termini (N-C) that is functionally essential. The interaction was mediated by aromatic Trp81 in pre-S1 domain and cationic Lys568 in TRP-like domain. Structure-function analyses revealed similar N-C interaction in TRPP2 as well as TRPM8/-V1/-C4 via highly conserved tryptophan and lysine/arginine residues. PIP2 bound to cationic resi...
Persistent Identifiers
Subjects
Medical Subject Headings: lipids (amino acids, peptides, and proteins)
free text keywords: General Biochemistry, Genetics and Molecular Biology, Article, TRP, pre-S1, TRP domain, intramolecular interaction, electrophysiology, Lysine, TRPM8, Arginine, TRPP, Transient receptor potential channel, Intramolecular force, Gating, Chemistry, Tryptophan, Biophysics, lcsh:Biology (General), lcsh:QH301-705.5
Related Organizations
Funded by
NSERC
Project
  • Funder: Natural Sciences and Engineering Research Council of Canada (NSERC)
46 references, page 1 of 4

Arif Pavel, M., Lv, C., Ng, C., Yang, L., Kashyap, P., Lam, C., Valentino, V., Fung, H.Y., Campbell, T., Møller, S.G., et al. (2016). Function and regulation of TRPP2 ion channel revealed by a gain-of-function mutant. Proc. Natl. Acad. Sci. USA 113, E2363-E2372.

Beck, A., Speicher, T., Stoerger, C., Sell, T., Dettmer, V., Jusoh, S.A., Abdulmughni, A., Cavalie´ , A., Philipp, S.E., Zhu, M.X., et al. (2013). Conserved gating elements in TRPC4 and TRPC5 channels. J. Biol. Chem. 288, 19471-19483.

Bousova, K., Jirku, M., Bumba, L., Bednarova, L., Sulc, M., Franek, M., Vyklicky, L., Vondrasek, J., and Teisinger, J. (2015). PIP2 and PIP3 interact with N-terminus region of TRPM4 channel. Biophys. Chem. 205, 24-32.

Cao, E., Liao, M., Cheng, Y., and Julius, D. (2013). TRPV1 structures in distinct conformations reveal activation mechanisms. Nature 504, 113-118. [OpenAIRE]

Chen, X.Z., Vassilev, P.M., Basora, N., Peng, J.B., Nomura, H., Segal, Y., Brown, E.M., Reeders, S.T., Hediger, M.A., and Zhou, J. (1999). Polycystin-L is a calcium-regulated cation channel permeable to calcium ions. Nature 401, 383-386.

Clapham, D.E., Runnels, L.W., and Stru€bing, C. (2001). The TRP ion channel family. Nat. Rev. Neurosci. 2, 387-396. [OpenAIRE]

Czirja´ k, G., Petheo, G.L., Spa¨ t, A., and Enyedi, P. (2001). Inhibition of TASK-1 potassium channel by phospholipase C. Am. J. Physiol. Cell Physiol. 281, C700-C708.

Gao, Y., Cao, E., Julius, D., and Cheng, Y. (2016). TRPV1 structures in nanodiscs reveal mechanisms of ligand and lipid action. Nature 534, 347-351. [OpenAIRE]

Garcia-Elias, A., Berna-Erro, A., Rubio-Moscardo, F., Pardo-Pastor, C., Mrkonjic, S., Sepu´ lveda, R.V., Vicente, R., Gonza´ lez-Nilo, F., and Valverde, M.A. (2015). Interaction between the linker, pre-S1, and TRP domains determines folding, assembly, and trafficking of TRPV channels. Structure 23, 1404-1413.

Grieben, M., Pike, A.C., Shintre, C.A., Venturi, E., El-Ajouz, S., Tessitore, A., Shrestha, L., Mukhopadhyay, S., Mahajan, P., Chalk, R., et al. (2017). Structure of the polycystic kidney disease TRP channel Polycystin-2 (PC2). Nat. Struct. Mol. Biol. 24, 114-122.

Holendova, B., Grycova, L., Jirku, M., and Teisinger, J. (2012). PtdIns(4,5)P2 interacts with CaM binding domains on TRPM3 N-terminus. Channels (Austin) 6, 479-482. [OpenAIRE]

Huynh, K.W., Cohen, M.R., Jiang, J., Samanta, A., Lodowski, D.T., Zhou, Z.H., and Moiseenkova-Bell, V.Y. (2016). Structure of the full-length TRPV2 channel by cryo-EM. Nat. Commun. 7, 11130.

Jin, P., Bulkley, D., Guo, Y., Zhang, W., Guo, Z., Huynh, W., Wu, S., Meltzer, S., Cheng, T., Jan, L.Y., et al. (2017). Electron cryo-microscopy structure of the mechanotransduction channel NOMPC. Nature 547, 118-122.

Jirku, M., Bumba, L., Bednarova, L., Kubala, M., Sulc, M., Franek, M., Vyklicky, L., Vondrasek, J., Teisinger, J., and Bousova, K. (2015). Characterization of the part of N-terminal PIP2 binding site of the TRPM1 channel. Biophys. Chem. 207, 135-142.

Kim, S., Nie, H., Nesin, V., Tran, U., Outeda, P., Bai, C.X., Keeling, J., Maskey, D., Watnick, T., Wessely, O., and Tsiokas, L. (2016). The polycystin complex mediates Wnt/Ca(2+) signalling. Nat. Cell Biol. 18, 752-764. [OpenAIRE]

46 references, page 1 of 4
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