Structure, inhibition and regulation of two-pore channel TPC1 from Arabidopsis thaliana

Nature

Volumn 531, Issue 7593, 2016, Pages 258-262

  Kintzer, Alexander F ^a   Stroud, Robert M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; CALCIUM; PHOSPHOPROTEIN; TWO PORE CHANNEL 1 PROTEIN; UNCLASSIFIED DRUG; 1-(3-((4-(2-FLUOROPHENYL)PIPERAZIN-1-YL)METHYL)-4-METHOXYPHENYL)-2,3,4,9-TETRAHYDRO-1H-PYRIDO(3,4-B)INDOLE-3-CARBOXYLIC ACID; CALCIUM CHANNEL; CARBOLINE DERIVATIVE; PIPERAZINE DERIVATIVE; TPC1 PROTEIN, ARABIDOPSIS;

CALCIUM; CONCENTRATION (COMPOSITION); CYTOPLASM; EUKARYOTE; HERB; INHIBITION; LIGAND; SODIUM; VIRAL DISEASE; VIRUS;

ARABIDOPSIS THALIANA; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; CYTOPLASM; HUMAN; ION TRANSPORT; NONHUMAN; PHARMACOPHORE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; ALLOSTERISM; ANTAGONISTS AND INHIBITORS; ARABIDOPSIS; CHANNEL GATING; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; EBOLAVIRUS; ENDOSOME; METABOLISM; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE; VIROLOGY; X RAY CRYSTALLOGRAPHY;

ANIMALIA; ARABIDOPSIS THALIANA; EBOLA VIRUS; EUKARYOTA;

ALLOSTERIC REGULATION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BINDING SITES; CALCIUM; CALCIUM CHANNELS; CARBOLINES; CRYSTALLOGRAPHY, X-RAY; EBOLAVIRUS; ENDOSOMES; ION CHANNEL GATING; ION TRANSPORT; MODELS, MOLECULAR; PHOSPHORYLATION; PIPERAZINES; PROTEIN STRUCTURE, TERTIARY;

EID: 84960887968     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature17194     Document Type: Article

References (52)

1. Hedrich, R. & Neher, E. Cytoplasmic calcium regulates voltage-dependent ion channels in plant vacuoles. Nature 329, 833-836 (1987).
2. Calcraft, P. J. et al. NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459, 596-600 (2009).
3. Hedrich, R. & Marten, I. TPC1-SV Channels Gain Shape. Mol. Plant 4, 428-441 (2011).
4. Patel, S. Function and dysfunction of two-pore channels. Sci. Signal. 8, re7 (2015).
5. Wang, X. et al. TPC proteins are phosphoinositide-activated sodium-selective ion channels in endosomes and lysosomes. Cell 151, 372-383 (2012).
6. Pitt, S. J. et al. TPC2 is a novel NAADP-sensitive Ca2+ release channel, operating as a dual sensor of luminal pH and Ca2+. J. Biol. Chem. 285, 35039-35046 (2010).
7. Sakurai, Y. et al. Two-pore channels control Ebola virus host cell entry and are drug targets for disease treatment. Science 347, 995-998 (2015).
8. Hedrich, R., Flügge, U. I. & Fernandez, J. M. Patch-clamp studies of ion transport in isolated plant vacuoles. FEBS Lett. 204, 228-232 (1986).
9. Cang, C., Bekele, B. & Ren, D. The voltage-gated sodium channel TPC1 confers endolysosomal excitability. Nature Chem. Biol. 10, 463-469 (2014).
10. Guo, J. et al. Structure of the voltage-gated two-pore channel TPC1 from Arabidopsis thaliana. Nature http://dx.doi.org/10.1038/nature16446 (this issue).
11. Beyhl, D. et al. The fou2 mutation in the major vacuolar cation channel TPC1 confers tolerance to inhibitory luminal calcium. Plant J. 58, 715-723 (2009).
12. Cang, C. et al. mTOR regulates lysosomal ATP-sensitive two-pore Na+ channels to adapt to metabolic state. Cell 152, 778-790 (2013).
13. Morgan, A. J., Davis, L. C., Ruas, M. & Galione, A. TPC: the NAADP discovery channel? Biochem. Soc. Trans. 43, 384-389 (2015).
14. Schulze, C., Sticht, H., Meyerhoff, P. & Dietrich, P. Differential contribution of EF-hands to the Ca2+-dependent activation in the plant two-pore channel TPC1. Plant J. 68, 424-432 (2011).
15. Long, S. B., Campbell, E. B. & Mackinnon, R. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309, 897-903 (2005).
16. Payandeh, J., Scheuer, T., Zheng, N. & Catterall, W. A. The crystal structure of a voltage-gated sodium channel. Nature 475, 353-358 (2011).
17. Naylor, E. et al. Identification of a chemical probe for NAADP by virtual screening. Nature Chem. Biol. 5, 220-226 (2009).
18. Kamb, A., Iverson, L. E. & Tanouye, M. A. Molecular characterization of Shaker, a Drosophila gene that encodes a potassium channel. Cell 50, 405-413 (1987).
19. Papazian, D. M., Schwarz, T. L., Tempel, B. L., Jan, Y. N. & Jan, L. Y. Cloning of genomic and complementary DNA from Shaker, a putative potassium channel gene from Drosophila. Science 237, 749-753 (1987).
20. Wu, J. et al. Structure of the voltage-gated calcium channel Cav1.1 complex. Science 350, aad2395 (2015).
21. Catterall, W. A., Perez-Reyes, E., Snutch, T. P. & Striessnig, J. International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol. Rev. 57, 411-425 (2005).
22. Brailoiu, E. et al. Essential requirement for two-pore channel 1 in NAADPmediated calcium signaling. J. Cell Biol. 186, 201-209 (2009).
23. Peterson, B. Z., Tanada, T. N. & Catterall, W. A. Molecular determinants of high affinity dihydropyridine binding in L-type calcium channels. J. Biol. Chem. 271, 5293-5296 (1996).
24. Pitt, S. J., Lam, A. K. M., Rietdorf, K., Galione, A. & Sitsapesan, R. Reconstituted human TPC1 is a proton-permeable ion channel and is activated by NAADP or Ca2+. Sci. Signal. 7, ra46 (2014).
25. Tang, L. et al. Structural basis for Ca2+ selectivity of a voltage-gated calcium channel. Nature 505, 56-61 (2014).
26. Armstrong, C. M. Time course of TEA+-induced anomalous rectification in squid giant axons. J. Gen. Physiol. 50, 491-503 (1966).
27. Holmgren, M., Smith, P. L. & Yellen, G. Trapping of organic blockers by closing of voltage-dependent K+ channels: evidence for a trap door mechanism of activation gating. J. Gen. Physiol. 109, 527-535 (1997).
28. Perozo, E., Cortes, D. M. & Cuello, L. G. Three-dimensional architecture and gating mechanism of a K+ channel studied by EPR spectroscopy. Nature Struct. Mol. Biol. 5, 459-469 (1998).
29. Clayton, G. M., Altieri, S., Heginbotham, L., Unger, V. M. & Morais-Cabral, J. H. Structure of the transmembrane regions of a bacterial cyclic nucleotideregulated channel. Proc. Natl Acad. Sci. USA 105, 1511-1515 (2008).
30. Zhou, Y., Morais-Cabral, J. H., Kaufman, A. & MacKinnon, R. Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0 Å resolution. Nature 414, 43-48 (2001).
31. Mumberg, D., Müller, R. & Funk, M. Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res. 22, 5767-5768 (1994).
32. Hattori, M., Hibbs, R. E. & Gouaux, E. A fluorescence-detection size-exclusion chromatography-based thermostability assay for membrane protein precrystallization screening. Structure 20, 1293-1299 (2012).
33. Gourdon, P. et al. HiLiDe - systematic approach to membrane protein crystallization in lipid and detergent. Cryst. Growth Des. 11, 2098-2106 (2011).
34. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D 67, 235-242 (2011).
35. Strong, M. et al. Toward the structural genomics of complexes: crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 103, 8060-8065 (2006).
36. Kabsch, W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Cryst. 26, 795-800 (1993).
37. Sheldrick, G. M. Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr. D 66, 479-485 (2010).
38. Bricogne, G., Vonrhein, C., Flensburg, C., Schiltz, M. & Paciorek, W. Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr. D 59, 2023-2030 (2003).
39. Abrahams, J. P. & Leslie, A. G. W. Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr. D 52, 30-42 (1996).
40. Cowtan, K. 'dm': an automated procedure for phase improvement by density modification, in Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography. 31, 34-38 http://www.ccp4.ac.uk/newsletters/ newsletter36/07-dm.html (1994).
41. Pedersen, B. P., Morth, J. P. & Nissen, P. Structure determination using poorly diffracting membrane-protein crystals: the H+-ATPase and Na+,K+-ATPase case history. Acta Crystallogr. D 66, 309-313 (2010).
42. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
43. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).
44. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
45. Bond, C. S. & Schüttelkopf, A. W. ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments. Acta Crystallogr. D 65, 510-512 (2009).
46. Pettersen, E. F. et al. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
47. Smart, O. S., Neduvelil, J. G., Wang, X., Wallace, B. A. & Sansom, M. S. P. HOLE: A program for the analysis of the pore dimensions of ion channel structural models. J. Mol. Graph. 14, 354-360 (1996).
48. Jones, D. T. Protein secondary structure prediction based on position-specific scoring matrices1. J. Mol. Biol. 292, 195-202 (1999).
49. Cuff, J. A., Clamp, M. E., Siddiqui, A. S., Finlay, M. & Barton, G. J. JPred: a consensus secondary structure prediction server. Bioinformatics 14, 892-893 (1998).
50. Blom, N., Sicheritz-Pontén, T., Gupta, R., Gammeltoft, S. & Brunak, S. Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4, 1633-1649 (2004).
51. Liao, M., Cao, E., Julius, D. & Cheng, Y. Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 504, 107-112 (2013).
52. Paulsen, C. E., Armache, J.-P., Gao, Y., Cheng, Y. & Julius, D. Structure of the TRPA1 ion channel suggests regulatory mechanisms. Nature 520, 511-517 (2015).