Function and dysfunction of two-pore channels

Science Signaling

Volumn 8, Issue 384, 2015, Pages

  Patel, Sandip ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; NICOTINIC ACID ADENINE DINUCLEOTIDE PHOSPHATE; RAB7 PROTEIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TWO PORE CHANNEL; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; CALCIUM; CALCIUM CHANNEL; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TPCN1 PROTEIN, HUMAN; TPCN2 PROTEIN, HUMAN;

AFFINITY LABELING; AUTOPHAGOSOME; AUTOPHAGY; CELL MIGRATION; DOPAMINERGIC NERVE CELL; EBOLA HEMORRHAGIC FEVER; EBOLAVIRUS; ENDOPLASMIC RETICULUM; ENDOSOME; GLYCOSYLATION; GOLD STANDARD; HOMOGENATE; ION PERMEABILITY; LYSOSOME; MOLECULAR WEIGHT; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SYNAPSE VESICLE; VIRUS ENTRY; ANALOGS AND DERIVATIVES; ANIMAL; BIOLOGICAL MODEL; CALCIUM SIGNALING; DRUG EFFECTS; HUMAN; METABOLISM;

EBOLA VIRUS;

ANIMALS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; ENDOSOMES; HUMANS; LYSOSOMES; MODELS, BIOLOGICAL; NADP;

EID: 84936860974     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aab3314     Document Type: Review

References (96)

1. F. H. Yu, W. A. Catterall, The VGL-chanome: A protein superfamily specialized for electrical signaling and ionic homeostasis. Sci. STKE 2004, re15 (2004).
2. K. Ishibashi, M. Suzuki, M. Imai, Molecular cloning of a novel form (two-repeat) protein related to voltage-gated sodium and calcium channels. Biochem. Biophys. Res. Commun. 270, 370-376 (2000).
3. 2+ flux in Arabidopsis leaf cells. Plant Cell Physiol. 42, 900-905 (2001).
4. F. H. Yu, V. Yarov-Yarovoy, G. A. Gutman, W. A. Catterall, Overview of molecular relationships in the voltage-gated ion channel superfamily. Pharmacol. Rev. 57, 387-395 (2005).
5. D. Churamani, R. Hooper, E. Brailoiu, S. Patel, Domain assembly of NAADP-gated two-pore channels. Biochem. J. 441, 317-323 (2012).
6. K. Rietdorf, T. M. Funnell, M. Ruas, J. Heinemann, J. Parrington, A. Galione, Two-pore channels form homo- and heterodimers. J. Biol. Chem. 286, 37058-37062 (2011).
7. R. Hooper, D. Churamani, E. Brailoiu, C. W. Taylor, S. Patel, Membrane topology of NAADP-sensitive two-pore channels and their regulation by N-linked glycosylation. J. Biol. Chem. 286, 9141-9149 (2011).
8. M. Strong, K. G. Chandy, G. A. Gutman, Molecular evolution of voltage-sensitive ion channel genes: On the origins of electrical excitability. Mol. Biol. Evol. 10, 221-242 (1993).
9. + channels. Sci. Signal. 7, ra109 (2014).
10. 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).
11. X. Cai, S. Patel, Degeneration of an intracellular ion channel in the primate lineage by relaxation of selective constraints. Mol. Biol. Evol. 27, 2352-2359 (2010).
12. P. J. Calcraft, M. Ruas, Z. Pan, X. Cheng, A. Arredouani, X. Hao, J. Tang, K. Rietdorf, L. Teboul, K. T. Chuang, P. Lin, R. Xiao, C. Wang, Y. Zhu, Y. Lin, C. N. Wyatt, J. Parrington, 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).
13. E. Brailoiu, D. Churamani, X. 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 two-pore channel 1 in NAADP-mediated calcium signaling. J. Cell Biol. 186, 201-209 (2009).
14. 2+-release from lysosomal stores. Pflugers Arch. 458, 891-899 (2009).
15. 2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434, 404-408 (2005).
16. 2+ signals. J. Biol. Chem. 285, 38511-38516 (2010).
17. N. Larisch, C. Schulze, A. Galione, P. Dietrich, An N-terminal dileucine motif directs two-pore channels to the tonoplast of plant cells. Traffic 13, 1012-1022 (2012).
18. 2+ signaling. Trends Cell Biol. 20, 277-286 (2010).
19. 2+ signalling in health and disease. Biochem. J. 439, 349-374 (2011).
20. 2+-permeable channels. Cell Calcium 57, 222-230 (2015).
21. H. C. Lee, Nicotinic acid adenine dinucleotide phosphate (NAADP)-mediated calcium signaling. J. Biol. Chem. 280, 33693-33696 (2005).
22. 2+ signalling by NAADP. Trends Biochem. Sci. 26, 482-489 (2001).
23. 2+ trigger. Sci. Signal. 1, re10 (2008).
24. 2+ signalling: From sea urchin eggs to mammalian cells. Cell Calcium 58, 27-47 (2015).
25. H. C. Lee, R. Aarhus, A derivative of NADP mobilizes calcium stores insensitive to inositol trisphosphate and cyclic ADP-ribose. J. Biol. Chem. 270, 2152-2157 (1995).
26. E. N. Chini, K. W. Beers, T. P. Dousa, Nicotinate adenine dinucleotide phosphate (NAADP) triggers a specific calcium release system in sea urchin eggs. J. Biol. Chem. 270, 3216-3223 (1995).
27. 2+ from reserve granules, lysosome-related organelles, in sea urchin eggs. Cell 111, 703-708 (2002).
28. 2+-signalling patterns by NAADP in pancreatic acinar cells. Nature 398, 74-76 (1999).
29. 2+ signals. J. Cell Sci. 126, 60-66 (2013).
30. 2+ microdomains. J. Cell Sci. 127, 2934-2943 (2014).
31. A. Galione, O. H. Petersen, The NAADP receptor: New receptors or new regulation? Mol. Interv. 5, 73-79 (2005).
32. A. H. Guse, Linking NAADP to ion channel activity: A unifying hypothesis. Sci. Signal. 5, e18 (2012).
33. 2+ signaling and endolysosomal trafficking. Curr. Biol. 20, 703-709 (2010).
34. 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).
35. L. C. Davis, A. J. Morgan, J. L. Chen, C. M. Snead, D. Bloor-Young, E. Shenderov, M. N. Stanton-Humphreys, S. J. Conway, G. C. Churchill, J. Parrington, V. Cerundolo, A. Galione, NAADP activates two-pore channels on T cell cytolytic granules to stimulate exocytosis and killing. Curr. Biol. 22, 2331-2337 (2012).
36. O. A. Ogunbayo, Y. Zhu, B. Shen, E. Agbani, J. Li, J. Ma, M. X. Zhu, A. M. Evans, Organelle-specific subunit interactions of the vertebrate two-pore channel family. J. Biol. Chem. 290, 1086-1095 (2015).
37. 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).
38. 2+ entry. Biochim. Biophys. Acta 1823, 1976-1983 (2012).
39. 2+ currents in isolated lysosomes. J. Biol. Chem. 285, 21219-21222 (2010).
40. 2+. J. Biol. Chem. 285, 35039-35046 (2010).
41. 2+-sensitive organellar two-pore channel TPC1. J. Biol. Chem. 287, 20407-20416 (2012).
42. S. Yamaguchi, Y. Jha, Q. Li, A. A. Soyombo, G. D. Dickinson, D. Churamani, E. Brailoiu, S. Patel, S. Muallem, Transient receptor potential mucolipin 1 (TRPML1) and two-pore channels are functionally independent organellar ion channels. J. Biol. Chem. 286, 22934-22942 (2011).
43. 2+. Sci. Signal. 7, ra46 (2014).
44. 2+stores. Biochem. J. 402, 301-310 (2007).
45. Y. Lin-Moshier, M. V. Keebler, R. Hooper, M. J. Boulware, X. Liu, D. Churamani, M. E. Abood, T. F. Walseth, E. Brailoiu, S. Patel, J. S. Marchant, The two-pore channel (TPC) interactome unmasks isoform-specific roles for TPCs in endolysosomal morphology and cell pigmentation. Proc.Natl.Acad.Sci.U.S.A.111, 13087-13092 (2014).
46. G.J.Pereira,H.Hirata,G.M.Fimia,L.G.doCarmo,C.Bincoletto,S.W.Han,R.S.Stilhano, R. P. Ureshino, D. Bloor-Young, G. Churchill, M. Piacentini, S. Patel, S. S. Smaili, Nicotinic acid adenine dinucleotide phosphate (NAADP) regulates autophagy in cultured astrocytes. J. Biol. Chem. 286, 27875-27881 (2011).
47. 2+ compartments in the megakaryoblastic cell line MEG01. Biochim. Biophys. Acta 1813, 1483-1494 (2011).
48. Z. H. Zhang, Y. Y. Lu, J. Yue, Two pore channel 2 differentially modulates neural differentiation of mouse embryonic stem cells. PLOS One 8, e66077 (2013).
49. Y. Lu, B. X. Hao, R. Graeff, C. W. 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).
50. G. J. Pereira, H. Hirata, L. G. do Carmo, R. S. Stilhano, R. P. Ureshino, N. C. Medaglia, S. W. Han, G. Churchill, C. Bincoletto, S. Patel, S. S. Smaili, NAADP-sensitive two-pore channels are present and functional in gastric smooth muscle cells. Cell Calcium 56, 51-58 (2014).
51. 2+ release. Cell Calcium pii: S0143-4160(15)00095-0 (2015).
52. 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).
53. +channels to adapt to metabolic state. Cell 152, 778-790 (2013).
54. C. Cang, B. Bekele, D. Ren, The voltage-gated sodium channel TPC1 confers endolysosomal excitability. Nat. Chem. Biol. 10, 463-469 (2014).
55. +channel that supports ultra-long action potentials and membrane bistability. Nat. Commun. 5, 5015 (2014).
56. 2+ release channels in the endolysosome. Nat. Commun. 1, 38 (2010).
57. 2 mediates activation of mammalian but not plant TPC proteins: Functional expression of endolysosomal channels in yeast and plant cells. Cell. Mol. Life Sci. 71, 4275-4283 (2014).
58. 2 and multiple protein kinases. EMBO J. 33, 501-511 (2014).
59. C. Grimm, L. M. Holdt, C. C. Chen, S. Hassan, C. Muller, S. Jors, H. Cuny, S. Kissing, B. Schroder, E. Butz, B. Northoff, J. Castonguay, C. A. Luber, M. Moser, S. Spahn, R. Lullmann-Rauch, C. Fendel, N. Klugbauer, O. Griesbeck, A. Haas, M. Mann, F. Bracher, D. Teupser, P. Saftig, M. Biel, C. Wahl-Schott, High susceptibility to fatty liver disease in two-pore channel 2-deficient mice. Nat. Commun. 5, 4699 (2014).
60. 2+-permeable two-pore channels rescues NAADP signalling in TPC-deficient cells. EMBO J. 14, e201490009 (2015).
61. 2+ release channel from liver lysosomes of rats. J. Biol. Chem. 282, 25259-25269 (2007).
62. 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).
63. M. Ruas, K. T. Chuang, L. C. Davis, A. Al-Douri, P. W. Tynan, R. Tunn, L. Teboul, A. Galione, J. Parrington, TPC1 has two variant isoforms and their removal has different effects on endo-lysosomal functions compared to loss of TPC2. Mol. Cell. Biol. 34, 3981-3992 (2014).
64. R. Hooper, D. Churamani, S. M. Davidson, Y. Lin-Moshier, T. F. Walseth, S. Patel, J. S. Marchant, TPC1 knockout knocks out TPC1. Mol. Cell. Biol. 35, 1882-1883 (2015).
65. Y. Lin-Moshier, T. F. Walseth, D. Churamani, S. M. Davidson, J. T. Slama, R. Hooper, E. Brailoiu, S. Patel, J. S. Marchant, Photoaffinity labeling of nicotinic acid adenine dinucleotide phosphate (NAADP) targets in mammalian cells. J. Biol. Chem. 287, 2296-2307 (2012).
66. T. F. Walseth, Y. Lin-Moshier, P. Jain, M. Ruas, J. Parrington, A. Galione, J. S. Marchant, J. T. Slama, Photoaffinity labeling of high affinity nicotinic acid adenine dinucleotide phosphate (NAADP)-binding proteins in sea urchin egg. J. Biol. Chem. 287, 2308-2315 (2012).
67. T. F. Walseth, Y. Lin-Moshier, K. Weber, J. S. Marchant, J. T. Slama, A. H. Guse, Nicotinic acid adenine dinucleotide 2′-phosphate (NAADP) binding proteins in T-lymphocytes. Messenger 1, 86-94 (2012).
68. R. Hooper, S. Patel, NAADP on target. Adv. Exp. Med. Biol. 740, 325-347 (2012).
69. E. Brailoiu, D. Churamani, V. Pandey, G. C. Brailoiu, F. Tuluc, S. Patel, N. J. Dun, Messenger-specific role for nicotinic acid adenine dinucleotide phosphate in neuronal differentiation. J. Biol. Chem. 281, 15923-15928 (2006).
70. 2+ signals and contraction in arterial smooth muscle via a two-pool mechanism. Circ. Res. 91, 1168-1175 (2003).
71. G. C. Brailoiu, B. Gurzu, X. Gao, R. Parkesh, P. K. Aley, D. I. Trifa, A. Galione, N. J. Dun, M. Madesh, S. Patel, G. C. Churchill, E. Brailoiu, Acidic NAADP-sensitive calcium stores in the endothelium: Agonist-specific recruitment and role in regulating blood pressure. J. Biol. Chem. 285, 37133-37137 (2010).
72. P. K. Aley, A. M. Mikolajczyk, B. Munz, G. C. Churchill, A. Galione, F. Berger, Nicotinic acid adenine dinucleotide phosphate regulates skeletal muscle differentiation via action at two-pore channels. Proc. Natl. Acad. Sci. U.S.A. 107, 19927-19932 (2010).
73. T. Notomi, Y. Ezura, M. Noda, Identification of two-pore channel 2 as a novel regulator of osteoclastogenesis. J. Biol. Chem. 287, 35057-35064 (2012).
74. B. Esposito, G. Gambara, A. M. Lewis, F. Palombi, A. D'Alessio, L. X. Taylor, A. A. Genazzani, E. Ziparo, A. Galione, G. C. Churchill, A. Filippini, NAADP links histamine H1 receptors to secretion of von Willebrand factor in human endothelial cells. Blood 117, 4968-4977 (2011).
75. P. H. Lin, P. Duann, S. Komazaki, K. H. Park, H. Li, M. Sun, M. Sermersheim, K. Gumpper, J. Parrington, A. Galione, A. M. Evans, M. X. Zhu, J. Ma, Lysosomal two-pore channel subtype 2 (TPC2) regulates skeletal muscle autophagic signaling. J. Biol. Chem. 290, 3377-3389 (2015).
76. L. Arndt, J. Castonguay, E. Arlt, D. Meyer, S. Hassan, H. Borth, S. Zierler, G. Wennemuth, A. Breit, M. Biel, C. Wahl-Schott, T. Gudermann, N. Klugbauer, I. Boekhoff, NAADP and the two-pore channel protein 1 participate in the acrosome reaction in mammalian spermatozoa. Mol. Biol. Cell 25, 948-964 (2014).
77. 2+ signaling. Proc. Natl. Acad. Sci. U.S.A. 111, E4706-E4715 (2014).
78. I. Ramos, A. Reich, G. M. Wessel, Two-pore channels function in calcium regulation in sea star oocytes and embryos. Development 141, 4598-4609 (2014).
79. J. S. Horton, C. T. Wakano, M. Speck, A. J. Stokes, Two-pore channel 1 interacts with citron kinase, regulating completion of cytokinesis. Channels 9, 21-29 (2015).
80. L. N. Hockey, B. S. Kilpatrick, E. R. Eden, Y. Lin-Moshier, G. C. Brailoiu, E. Brailoiu, C. Futter, A. H. Schapira, J. S. Marchant, S. Patel, Dysregulation of lysosomal morphology by pathogenic LRRK2 is corrected by TPC2 inhibition. J. Cell Sci. 128, 232-238 (2015).
81. Y. Sakurai, A. A. Kolokolstov, C. C. Chen, M. W. Tidwell, W. E. Bauta, N. Klugbauer, C. Grimm, C. Wahl-Schott, M. Biel, R. A. Davey, Two-pore channels control Ebola virus host cell entry and are drug targets for disease treatment. Science 347, 995-998 (2015).
82. B. Dehay, M. Martinez-Vicente, G. A. Caldwell, K. A. Caldwell, Z. Yue, M. R. Cookson, C. Klein, M. Vila, E. Bezard, Lysosomal impairment in Parkinson's disease. Mov. Disord. 28, 725-732 (2013).
83. G. K. Tofaris, Lysosome-dependent pathways as a unifying theme in Parkinson's disease. Mov. Disord. 27, 1364-1369 (2012).
84. P. Gómez-Suaga, B. Luzón-Toro, D. Churamani, L. Zhang, D. Bloor-Young, S. Patel, P. G. Woodman, G. C. Churchill, S. Hilfiker, Leucine-rich repeat kinase 2 regulates autophagy through a calcium-dependent pathway involving NAADP. Hum. Mol. Genet. 21, 511-525 (2012).
85. J. S. Marchant, S. Patel, Two-pore channels at the intersection of endolysosomal membrane traffic. Biochem. Soc. Trans. 43, 434-441 (2015).
86. M. Cote, J. Misasi, T. Ren, A. Bruchez, K. Lee, C. M. Filone, L. Hensley, Q. Li, D. Ory, K. Chandran, J. Cunningham, Small molecule inhibitors reveal Niemann-Pick C1 is essential for Ebola virus infection. Nature 477, 344-348 (2011).
87. M. Lavanya, C. D. Cuevas, M. Thomas, S. Cherry, S. R. Ross, siRNA screen for genes that affect Junín virus entry uncovers voltage-gated calcium channels as a therapeutic target. Sci. Transl. Med. 5, 204ra131 (2013).
88. 2δ subunits of voltage-gated calcium channels. Biochim. Biophys. Acta 1828, 1541-1549 (2013).
89. J. P. Luzio, N. A. Bright, P. R. Pryor, The role of calcium and other ions in sorting and delivery in the late endocytic pathway. Biochem. Soc. Trans. 35, 1088-1091 (2007).
90. X. Li, A. G. Garrity, H. Xu, Regulation of membrane trafficking by signalling on endosomal and lysosomal membranes. J. Physiol. 591, 4389-4401 (2013).
91. T. Burgoyne, S. Patel, E. R. Eden, Calcium signaling at ER membrane contact sites. Biochim. Biophys. Acta pii: S0167-4889(15)00037-3 (2015).
92. A. H. Schapira, C. W. Olanow, J. T. Greenamyre, E. Bezard, Slowing of neurodegeneration in Parkinson's disease and Huntington's disease: Future therapeutic perspectives. Lancet 384, 545-555 (2014).
93. C. C. Chen, M. Keller, M. Hess, R. Schiffmann, N. Urban, A. Wolfgardt, M. Schaefer, F. Bracher, M. Biel, C. Wahl-Schott, C. Grimm, A small molecule restores function to TRPML1 mutant isoforms responsible for mucolipidosis type IV. Nat. Commun. 5, 4681 (2014).
94. K. M. Neely Kayala, G. D. Dickinson, A. Minassian, K. C. Walls, K. N. Green, F. M. Laferla, Presenilin-null cells have altered two-pore calcium channel expression and lysosomal calcium: Implications for lysosomal function. Brain Res. 1489, 8-16 (2012).
95. S. W. Tsaih, K. Holl, S. Jia, M. Kaldunski, M. Tschannen, H. He, J. W. Andrae, S. H. Li, A. Stoddard, A. Wiederhold, J. Parrington, S. M. Ruas da, A. Galione, J. Meigs, R. G. Hoffmann, P. Simpson, H. Jacob, M. Hessner, L. C. Solberg Woods, Identification of a novel gene for diabetic traits in rats, mice, and humans. Genetics 198, 17-29 (2014).
96. P. V. Lear, D. Gonzalez-Touceda, C. B. Porteiro, P. Viano, V. Guymer, E. Remzova, R. Tunn, A. Chalasani, T. Garcia-Caballero, I. P. Hargreaves, P. W. Tynan, H. C. Christian, R. Nogueiras, J. Parrington, C. Dieguez, Absence of intracellular ion channels TPC1 and TPC2 leads to mature-onset obesity in male mice, due to impaired lipid availability for thermogenesis in brown adipose tissue. Endocrinology 156, 975-986 (2015).