Reconstituted Human TPC1 is a proton-permeable ion channel and is activated by NAADP or Ca2+

Science Signaling

Volumn 7, Issue 326, 2014, Pages

  Pitt, Samantha J ^a   Lam, Andy K M ^b   Rietdorf, Katja ^b   Galione, Antony ^b   Sitsapesan, Rebecca ^b  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; ION CHANNEL; NICOTINIC ACID ADENINE DINUCLEOTIDE PHOSPHATE; PHOSPHATE; PHOSPHATIDYLINOSITOL 3,5 BISPHOSPHATE; POTASSIUM ION; PROTON; SODIUM ION; TWO PORE CHANNEL 1; TWO PORE CHANNEL 2; UNCLASSIFIED DRUG; CALCIUM; CALCIUM CHANNEL; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PHOSPHATIDYLINOSITOL 3,5-DIPHOSPHATE; POLYPHOSPHOINOSITIDE; TPCN1 PROTEIN, HUMAN;

ARTICLE; LYSOSOME; PERMEABILITY; PRIORITY JOURNAL; ANALOGS AND DERIVATIVES; CHEMISTRY; ENDOSOME; GENETICS; HEK293 CELL LINE; HUMAN; ION TRANSPORT; METABOLISM; PH; PHYSIOLOGY;

CALCIUM; CALCIUM CHANNELS; ENDOSOMES; HEK293 CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; ION TRANSPORT; LYSOSOMES; NADP; PERMEABILITY; PHOSPHATIDYLINOSITOL PHOSPHATES; PROTONS;

EID: 84901191676     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004854     Document Type: Article

References (53)

1. 2+ from reserve granules, lysosome-related organelles, in sea urchin eggs. Cell 111, 703-708 (2002).
2. 2+ trigger. Sci. Signal. 1, re10 (2008).
3. A. Galione, A. J. Morgan, A. Arredouani, L. C. Davis, K. Rietdorf, M. Ruas, J. Parrington, NAADP as an intracellular messenger regulating lysosomal calcium-release channels. Biochem. Soc. Trans. 38, 1424-1431 (2010).
4. P. J. Calcraft,M. Ruas, Z. Pan, X. T. Cheng, A. Arredouani, X. M. Hao, J. S. Tang, K. Rietdorf, L. Teboul, K. T. Chuang, P. H. Lin, R. Xiao, C. B. Wang, Y. M. Zhu, Y. K. Lin, C. N. Wyatt, J. Parrington, J. J. Ma, A. M. Evans, A. Galione, M. X. Zhu, NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459, 596-600 (2009).
5. 2+ release channels. Pflugers Arch. 458, 869-876 (2009).
6. 2+ mobilization from acidic organelles triggered by NAADP. FEBS Lett. 584, 1966-1974 (2010).
7. 2+-release from lysosomal stores. Pflugers Arch. 458, 891-899 (2009).
8. E. Brailoiu, R. Hooper, X. Cai, G. C. Brailoiu, M. V. Keebler, N. J. Dun, J. S. Marchant, S. Patel, An ancestral deuterostome family of two-pore channels mediates nicotinic acid adenine dinucleotide phosphate-dependent calcium release from acidic organelles. J. Biol. Chem. 285, 2897-2901 (2010).
9. 2+. J. Biol. Chem. 285, 35039-35046 (2010).
10. 2+ signals. J. Biol. Chem. 285, 38511-38516 (2010).
11. 2+ currents in isolated lysosomes. J. Biol. Chem. 285, 21219-21222 (2010).
12. M. X. Zhu, A. M. Evans, J. Ma, J. Parrington, A. Galione, Two-pore channels for integrative Ca signaling. Commun. Integr. Biol. 3, 12-17 (2010).
13. M. X. Zhu, J. Ma, J. Parrington, P. J. Calcraft, A. Galione, A. M. Evans, Calcium signaling via two-pore channels: Local or global, that is the question. Am. J. Physiol. Cell Physiol. 298, C430-C441 (2010).
14. R. Hedrich, I. Marten, TPC1-SV channels gain shape. Mol. Plant 4, 428-441 (2011).
15. E. Brailoiu, D. Churamani, X. J. Cai, M. G. Schrlau, G. C. Brailoiu, X. Gao, R. Hooper, M. J. Boulware, N. J. Dun, J. S. Marchant, S. Patel, Essential requirement for twopore channel 1 in NAADP-mediated calcium signaling. J. Cell Biol. 186, 201 -209 (2009).
16. 2+- sensitive organellar two-pore channel TPC1. J. Biol. Chem. 287, 20407-20416 (2012).
17. + channels to adapt to metabolic state. Cell 152, 778- 790 (2013).
18. X. Wang, X. Zhang, X. P. Dong, M. Samie, X. Li, X. Cheng, A. Goschka, D. Shen, Y. Zhou, J. Harlow, M. X. Zhu, D. E. Clapham, D. Ren, H. Xu, TPC proteins are phosphoinositide-activated sodium-selective ion channels in endosomes and lysosomes. Cell 151, 372-383 (2012).
19. 2+ signalling in health and disease. Biochem. J. 439, 349-374 (2011).
20. A. J. Morgan, Sea urchin eggs in the acid reign. Cell Calcium 50, 147-156 (2011).
21. 2+ stores. Biochem. J. 402, 301-310 (2007).
22. 2+ mobilization from lysosomes in pancreatic acinar cells. J. Biol. Chem. 285, 38251-38259 (2010).
23. T. P. Collins, R. Bayliss, G. C. Churchill, A. Galione, D. A. Terrar, NAADP influences excitation-contraction coupling by releasing calcium from lysosomes in atrial myocytes. Cell Calcium 50, 449-458 (2011).
24. A. E. Oliver, D.W. Deamer, Alpha-helical hydrophobic polypeptides form proton-selective channels in lipid bilayers. Biophys. J. 66, 1364-1379 (1994).
25. V. Vijayvergiya, R. Wilson, A. Chorak, P. F. Gao, T. A. Cross, D. D. Busath, Proton conductance of influenza virus M2 protein in planar lipid bilayers. Biophys. J. 87, 1697-1704 (2004).
26. M. Koivusalo, B. E. Steinberg, D. Mason, S. Grinstein, In situ measurement of the electrical potential across the lysosomal membrane using FRET. Traffic 12, 972-982 (2011).
27. E. Lloyd-Evans, A. J. Morgan, X. X. He, D. A. Smith, E. Elliot-Smith, D. J. Sillence, G. C. Churchill, E. H. Schuchman, A. Galione, F. M. Platt, Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat. Med. 14, 1247 -1255 (2008).
28. J. V. Gerasimenko, A. V. Tepikin, O. H. Petersen, O. V. Gerasimenko, Calcium uptake via endocytosis with rapid release from acidifying endosomes. Curr. Biol. 8, 1335-1338 (1998).
29. B. E. Steinberg, K. K. Huynh, A. Brodovitch, S. Jabs, T. Stauber, T. J. Jentsch, S. Grinstein, A cation counterflux supports lysosomal acidification. J. Cell Biol. 189, 1171-1186 (2010).
30. M. Grabe, G. Oster, Regulation of organelle acidity. J. Gen. Physiol. 117, 329-344 (2001).
31. 2+ signaling occurs between the endoplasmic reticulum and acidic organelles. J. Cell Biol. 200, 789-805 (2013).
32. Y. Y. Lu, B. X. Hao, R. Graeff, C. W. M. Wong, W. T. Wu, J. Yue, Two pore channel 2 (TPC2) inhibits autophagosomal-lysosomal fusion by alkalinizing lysosomal pH. J. Biol. Chem. 288, 24247-24263 (2013).
33. 2+-release channel (ryanodine receptor) by mono- and divalent ions. Am. J. Physiol. 274, C120-C128 (1998).
34. E. Richard, C. Miller, Steady-state coupling of ion-channel conformations to a transmembrane ion gradient. Science 247, 1208-1210 (1990).
35. D. F. Van Helden, O. P. Hamill, P. W. Gage, Permeant cations alter endplate channel characteristics. Nature 269, 711-713 (1977).
36. M. Moroni, I. Biro, M. Giugliano, R. Vijayan, P. C. Biggin, M. Beato, L. G. Sivilotti, chloride ions in the pore of glycine and GABA channels shape the time course and voltage dependence of agonist currents. J. Neurosci. 31, 14095-14106 (2011).
37. M. Holmgren, Influence of permeant ions on gating in cyclic nucleotide-gated channels. J. Gen. Physiol. 121, 61-72 (2003).
38. 2+-release channel with unique gating characteristics. Biophys. J. 100, 433a (2011).
39. + channels and calcium-induced calcium release by slow vacuolar ion channels in guard cell vacuoles implicated in the control of stomatal closure. Plant Cell 6, 669-683 (1994).
40. 2+ flux in Arabidopsis leaf cells. Plant Cell Physiol. 42, 900-905 (2001).
41. 2+ stores in pulmonary arterial myocytes. J. Biol. Chem. 288, 10381-10394 (2013).
42. O. A. Ogunbayo, Y. Zhu, D. Rossi, V. Sorrentino, J. Ma, M. X. Zhu, A. M. Evans, Cyclic adenosine diphosphate ribose activates ryanodine receptors, whereas NAADP activates two-pore domain channels. J. Biol. Chem. 286, 9136- 9140 (2011).
43. N. Tugba Durlu-Kandilci, M. Ruas, K. T. Chuang, A. Brading, J. Parrington, A. Galione, TPC2 proteins mediate nicotinic acid adenine dinucleotide phosphate (NAADP)- and agonist-evoked contractions of smooth muscle. J. Biol. Chem. 285, 24925-24932 (2010).
44. D. Churamani, R. Hooper, T. Rahman, E. Brailoiu, S. Patel, The N-terminal region of two-pore channel 1 regulates trafficking and activation by NAADP. Biochem. J. 453, 147-151 (2013).
45. M. D. Carrithers, S. Dib-Hajj, L. M. Carrithers, G. Tokmoulina, M. Pypaert, E. A. Jonas, S.G. Waxman, Expression of the voltage-gated sodium channel NaV1.5 in themacrophage late endosome regulates endosomal acidification. J. Immunol. 178, 7822-7832 (2007).
46. 2+ release channels in the endolysosome. Nat. Commun. 1, 38 (2010).
47. P. Harikumar, J. P. Reeves, The lysosomal proton pump is electrogenic. J. Biol. Chem. 258, 10403-10410 (1983).
48. 2+, NAADP, PI(3,5)P2 and multiple protein kinases. EMBO J. 33, 501-511 (2014).
49. R. Sitsapesan, R. A. P. Montgomery, K. T. MacLeod, A. J. Williams, Sheep cardiac sarcoplasmic reticulum calcium-release channels: Modification of conductance and gating by temperature. J. Physiol. 434, 469-488 (1991).
50. D. Colquhoun, F. J. Sigworth, in Single-Channel Recording, B. Sakmann, E. Neher, Eds. (Plenum, New York, 1983), vol. 1, pp. 191-263.
51. A. L. Hodgkin, B. Katz, The effect of sodium ions on the electrical activity of the giant axon of the squid. J. Physiol. 108, 37-77 (1949).
52. P. Fatt, B. L. Ginsborg, The ionic requirements for the production of action potentials in crustacean muscle fibres. J. Physiol. 142, 516-543 (1958).
53. R. Aarhus, R. M. Graeff, D. M. Dickey, T. F. Walseth, H. C. Lee, ADP-ribosyl cyclase and CD38 catalyze the synthesis of a calcium-mobilizing metabolite from NADP. J. Biol. Chem. 270, 30327-30333 (1995).