Evolution of acidic Ca2+ stores and their resident Ca2+-permeable channels

Cell Calcium

Volumn 57, Issue 3, 2015, Pages 222-230

  Patel, Sandip ^a   Cai, Xinjiang ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Acidic Ca2+ stores; Acidocalcisomes; Evolution; IP3 receptor; LRRK2; Lysosome related organelles; Lysosomes; Membrane traffic; Mucolipin; NAADP; P2X4; Ryanodine receptor; Secretion; Secretory vesicles; TPC; TRP; Vacuoles

Indexed keywords

CALCIUM CHANNEL; PROTON; PURINERGIC P2X RECEPTOR; RAB PROTEIN; RYANODINE RECEPTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL M2; TWO PORE CHANNEL; UNCLASSIFIED DRUG; CALCIUM;

ACIDIC CALCIUM STORE; ACIDOCALCISOME; AUTOPHAGY; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL COMPARTMENTALIZATION; CELL ORGANELLE; CELL VACUOLE; CELLULAR SECRETION; CYTOTOXIC T LYMPHOCYTE; DEUTEROSTOMIA; FUSION ACTIVATED CALCIUM ENTRY; HUMAN; ION PERMEABILITY; LYSOSOME; MEMBRANE TRANSPORT; MOLECULAR BIOLOGY; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEOMICS; PROTOSTOMIA; REVIEW; SECRETORY VESICLE; TRYPANOSOMA; ANIMAL; CELL MEMBRANE PERMEABILITY; EVOLUTION; METABOLISM; PHYSIOLOGY;

ANIMALS; BIOLOGICAL EVOLUTION; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL MEMBRANE PERMEABILITY; HUMANS; PHYLOGENY;

EID: 84924065856     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2014.12.005     Document Type: Review

References (155)

1. Berridge M.J., Lipp P., Bootman M.D. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell. Biol. 2000, 1:11-21.
2. 2+ oscillations. Trends Biochem. Sci. 2011, 36:78-87.
3. Ringer S. A further contribution regarding the influence of the different constituents of the blood on the contraction of the heart. J. Physiol. 1883, 4:29-42.
4. Kashir J., Deguchi R., Jones C., Coward K., Stricker S.A. Comparative biology of sperm factors and fertilization-induced calcium signals across the animal kingdom. Mol. Reprod. Dev. 2013, 80:787-815.
5. Kudla J., Batistic O., Hashimoto K. Calcium signals: the lead currency of plant information processing. Plant Cell 2010, 22:541-563.
6. 2+ transport in Saccharomyces cerevisiae. J. Exp. Biol. 1994, 196:157-166.
7. Malchow D., Mutzel R., Schlatterer C. On the role of calcium during chemotactic signalling and differentiation of the cellular slime mould Dictyostelium discoideum. Int. J. Dev. Biol. 1996, 40:135-139.
8. Plattner H. Calcium regulation in the protozoan model, Paramecium tetraurelia. J. Eukaryot. Microbiol. 2014, 61:95-114.
9. Moreno S.N., Docampo R. Calcium regulation in protozoan parasites. Curr. Opin. Microbiol. 2003, 6:359-364.
10. Dominguez D.C. Calcium signalling in bacteria. Mol. Microbiol. 2004, 54:291-297.
11. Clapham D.E. Calcium signaling. Cell 2007, 131:1047-1058.
12. Berridge M.J. The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 2002, 32:235-249.
13. 2+ signaling. Trends Cell Biol. 2010, 20:277-286.
14. 2+ signalling in health and disease. Biochem. J. 2011, 439:349-374.
15. 2+ store: role for the two-pore channels. Cell Calcium 2011, 50:157-167.
16. 2+ stores come to the fore. Cell Calcium 2011, 50:109-112.
17. 2+ signalling in the golgi apparatus. Cell Calcium 2011, 50:184-192.
18. Christensen K.A., Myers J.T., Swanson J.A. pH-dependent regulation of lysosomal calcium in macrophages. J. Cell Sci. 2002, 115:599-607.
19. Lloyd-Evans E., Morgan A.J., He X., et al. Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat. Med. 2008, 14:1247-1255.
20. Jadot M., Colmant C., Wattiaux-de C.S., Wattiaux R. Intralysosomal hydrolysis of glycyl-l-phenylalanine 2-naphthylamide. Biochem. J. 1984, 219:965-970.
21. Blott E.J., Griffiths G.M. Secretory lysosomes. Nat. Rev. Mol. Cell. Biol. 2002, 3:122-131.
22. 2+ inside platelet secretory granules. Measurements employing a novel double null point technique. J. Biol. Chem. 1983, 258:14774-14777.
23. 2+. Nature 1998, 395:908-912.
24. 2+ store in neuroendocrine cells with a vesicle-associated membrane protein aequorin chimaera. J. Cell Biol. 2001, 155:41-51.
25. Santodomingo J., Vay L., Camacho M., et al. Calcium dynamics in bovine adrenal medulla chromaffin cell secretory granules. Eur. J. Neurosci. 2008, 28:1265-1274.
26. 2+ and pH. Planta 1988, 176:248-255.
27. 2+ fluxes in situ. J. Exp. Bot. 2008, 59:3845-3855.
28. Docampo R., Moreno S.N. Acidocalcisomes. Cell Calcium 2011, 50:113-119.
29. Docampo R., de S.W., Miranda K., Rohloff P., Moreno S.N. Acidocalcisomes-conserved from bacteria to man. Nat. Rev. Microbiol. 2005, 3:251-261.
30. Seufferheld M., Vieira M.C., Ruiz F.A., Rodrigues C.O., Moreno S.N., Docampo R. Identification of organelles in bacteria similar to acidocalcisomes of unicellular eukaryotes. J. Biol. Chem. 2003, 278:29971-29978.
31. Venkatachalam K., Montell C. TRP channels. Annu. Rev. Biochem. 2007, 76:387-417.
32. Kiselyov K., Chen J., Rbaibi Y., et al. TRP-ML1 is a lysosomal monovalent cation channel that undergoes proteolytic cleavage. J. Biol. Chem. 2005, 280:43218-43223.
33. Karacsonyi C., Miguel A.S., Puertollano R. Mucolipin-2 localizes to the Arf6-associated pathway and regulates recycling of GPI-APs. Traffic 2007, 8:1404-1414.
34. Nagata K., Zheng L., Madathany T., Castiglioni A.J., Bartles J.R., Garcia-Anoveros J. The varitint-waddler (Va) deafness mutation in TRPML3 generates constitutive, inward rectifying currents and causes cell degeneration. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:353-358.
35. Puertollano R., Kiselyov K. TRPMLs: in sickness and in health. Am. J. Physiol. Renal. Physiol. 2009, 296:F1245-F1254.
36. Garcia-Anoveros J., Wiwatpanit T. TRPML2 and mucolipin evolution. Handb. Exp. Pharmacol. 2014, 222:647-658.
37. Fares H., Greenwald I. Regulation of endocytosis by CUP-5, the Caenorhabditis elegans mucolipin-1 homolog. Nat. Genet. 2001, 28:64-68.
38. Lima W.C., Leuba F., Soldati T., Cosson P. Mucolipin controls lysosome exocytosis in Dictyostelium. J. Cell Sci. 2012, 125:2315-2322.
39. 2+ release channel from liver lysosomes of rats. J. Biol. Chem. 2007, 282:25259-25269.
40. Yamaguchi S., Jha Y., Li Q., et al. Transient Receptor Potential Mucolipin 1 (TRPML1) and two-pore channels are functionally independent organellar ion channels. J. Biol. Chem. 2011, 286:22934-22942.
41. 2+ release channels in the endolysosome. Nat. Commun. 2010, 1. pii:38.
42. Perraud A.L., Fleig A., Dunn C.A., et al. ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature 2001, 411:595-599.
43. 2+-release channel in beta cells. Sci. Signal. 2009, 2:ra23.
44. 2+ release. FASEB J. 2011, 25:3529-3542.
45. Faouzi M., Penner R. TRPM2. Handb. Exp. Pharmacol. 2014, 222:403-426.
46. 2+ release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue. J. Cell Biol. 2002, 156:29-34.
47. Zhou X.L., Batiza A.F., Loukin S.H., Palmer C.P., Kung C., Saimi Y. The transient receptor potential channel on the yeast vacuole is mechanosensitive. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:7105-7110.
48. 2+-permeable channel in the yeast vacuolar membrane. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:7801-7805.
49. Hooper R., Churamani D., Brailoiu E., Taylor C.W., Patel S. Membrane topology of NAADP-sensitive two-pore channels and their regulation by N-linked glycosylation. J. Biol. Chem. 2011, 286:9141-9149.
50. Rietdorf K., Funnell T.M., Ruas M., Heinemann J., Parrington J., Galione A. Two-pore channels form homo- and hetero-dimers. J. Biol. Chem. 2011, 286:37058-37062.
51. Churamani D., Hooper R., Brailoiu E., Patel S. Domain assembly of NAADP-gated two-pore channels. Biochem. J. 2012, 441:317-323.
52. Hille B. Ionic Channels of Excitable Membranes 1984, Sinauer Associates, Sunderland, Massachusets.
53. Ishibashi K., Suzuki M., Imai M. Molecular cloning of a novel form (two-repeat) protein related to voltage-gated sodium and calcium channels. Biochem. Biophys. Res. Commun. 2000, 270:370-376.
54. + channels. Sci. Signal. 2014, 7:ra109.
55. Calcraft P.J., Ruas M., Pan Z., et al. NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 2009, 459:596-600.
56. Brailoiu E., Hooper R., Cai X., et al. An ancestral deuterostome family of two-pore channels mediate nicotinic acid adenine dinucleotide phosphate-dependent calcium release from acidic organelles. J. Biol. Chem. 2010, 285:2897-2901.
57. Cai X., Patel S. Degeneration of an intracellular ion channel in the primate lineage by relaxation of selective constraints. Mol. Biol. Evol. 2010, 27:2352-2359.
58. Brailoiu E., Churamani D., Cai X., et al. Essential requirement for two-pore channel 1 in NAADP-mediated calcium signaling. J. Cell Biol. 2009, 186:201-209.
59. Davis L.C., Morgan A.J., Chen J.L., et al. NAADP activates two-pore channels on T cell cytolytic granules to stimulate exocytosis and killing. Curr. Biol. 2012, 22:2331-2337.
60. 2+-activated channel TPC1 regulates germination and stomatal movement. Nature 2005, 434:404-408.
61. 2+ influx and production of phytoalexins by a putative voltage-gated cation channel, OsTPC1, in cultured rice cells. J. Biol. Chem. 2012, 287:9931-9939.
62. 2+ signals. J. Biol. Chem. 2010, 285:38511-38516.
63. 2+ currents in isolated lysosomes. J. Biol. Chem. 2010, 285:21219-21222.
64. 2+. J. Biol. Chem. 2010, 285:24925-24932.
65. Wang X., Zhang X., Dong X.P., et al. TPC proteins are phosphoinositide-activated sodium-selective ion channels in endosomes and lysosomes. Cell 2012, 151:372-383.
66. 2+. Sci. Signal. 2014, 7:ra46.
67. 2+ dependence of transient receptor potential melastatin 2 (TRPM2) cation channel activation. J. Biol. Chem. 2003, 278:11002-11006.
68. 2+ mobilization from acidic organelles triggered by NAADP. FEBS Lett. 2010, 584:1966-1974.
69. Hooper R., Patel S. NAADP on target. Adv. Exp. Med. Biol. 2012, 740:325-347.
70. Lin-Moshier Y., Walseth T.F., Churamani D., et al. Photoaffinity labeling of nicotinic acid adenine dinucleotide phosphate (NAADP) targets in mammalian cells. J. Biol. Chem. 2012, 287:2296-2307.
71. Walseth T.F., Lin-Moshier Y., Jain P., et al. Photoaffinity labeling of high affinity nicotinic acid adenine dinucleotide 2'-phosphate (NAADP) proteins in sea urchin egg. J. Biol. Chem. 2012, 287:2308-2315.
72. 2+ signalling by NAADP: two-pore channels in a complex. Messenger 2012, 1:63-76.
73. Cang C., Bekele B., Ren D. The voltage-gated sodium channel TPC1 confers endolysosomal excitability. Nat. Chem. Biol. 2014, 10:463-469.
74. Marchant J.S., Patel S. Questioning regulation of two-pore channels by NAADP. Messenger 2013, 2:113-119.
75. Morgan A.J., Galione A. Two-pore channels (TPCs): current controversies. BioEssays 2013, 36:173-183.
76. 2 and multiple protein kinases. E.M.B.O. J. 2014, 33:501-511.
77. 2+ flux in Arabidopsis leaf cells. Plant Cell Physiol. 2001, 42:900-905.
78. Hedrich R., Neher E. Cytoplasmic calcium regulates voltage-dependent ion channels in plant vacuoles. Nature 1987, 329:833-836.
79. 2+-dependent activation in the plant two-pore channel TPC1. Plant J. 2011, 68:424-432.
80. Hedrich R., Marten I. TPC1-SV channels gain shape. Mol. Plant 2011, 4:428-441.
81. Peiter E. The plant vacuole: emmitter and receiver of calcium signals. Cell Calcium 2011, 50:120-128.
82. Khakh B.S., North R.A. P2X receptors as cell-surface ATP sensors in health and disease. Nature 2006, 442:527-532.
83. Fountain S.J., Parkinson K., Young M.T., Cao L., Thompson C.R., North R.A. An intracellular P2X receptor required for osmoregulation in Dictyostelium discoideum. Nature 2007, 448:200-203.
84. Fountain S.J., Burnstock G. An evolutionary history of P2X receptors. Purinergic Signal 2009, 5:269-272.
85. Qureshi O.S., Paramasivam A., Yu J.C., Murrell-Lagnado R.D. Regulation of P2X4 receptors by lysosomal targeting, glycan protection and exocytosis. J. Cell Sci. 2007, 120:3838-3849.
86. Huang P., Zou Y., Zhong X.Z., et al. P2X4 forms functional ATP-activated cation channels on lysosomal membranes regulated by luminal pH. J. Biol. Chem. 2014, 289:17658-17667.
87. 2+ entry via vesicular P2X4 receptors promotes fusion pore opening and exocytotic content release in pneumocytes. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:14503-14508.
88. Cai X. P2X receptor homologs in basal fungi. Purinergic Signal 2012, 8:11-13.
89. Sivaramakrishnan V., Fountain S.J. A mechanism of intracellular P2X receptor activation. J. Biol. Chem. 2012, 287:28315-28326.
90. Zhang Z., Chen G., Zhou W., et al. Regulated ATP release from astrocytes through lysosome exocytosis. Nat. Cell Biol. 2007, 9:945-953.
91. Patel S., Joseph S.K., Thomas A.P. Molecular properties of inositol 1,4,5-trisphosphate receptors. Cell Calcium 1999, 25:247-264.
92. 2+ release channels. Physiol. Rev. 2007, 87:593-658.
93. Fill M., Copello J.A. Ryanodine receptor calcium release channels. Physiol. Rev. 2002, 82:893-922.
94. 2+ from single isolated pancreatic zymogen granules. Cell 1996, 84:473-480.
95. Yule D.I., Ernst S.A., Ohnishi H., Wojcikiewicz R.J. Evidence that zymogen granules are not a physiologically relevant calcium pool. Defining the distribution of inositol 1,4,5-trisphosphate receptors in pancreatic acinar cells. J. Biol. Chem. 1997, 272:9093-9098.
96. Blondel O., Moody M.M., Depaoli A.M., et al. Localization of inositol trisphosphate receptor subtype 3 to insulin and somatostatin secretory granules and regulation of expression in islets and insulinoma cells. Proc. Natl. Acad. Sci. 1994, 91:7777-7781.
97. Ravazzola M., Halban P.A., Orci L. Inositol 1,4,5-trisphosphate receptor subtype 3 in pancreatic islet cell secretory granules revisited. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:2745-2748.
98. 2+ signalling is not required for chemotaxis in Dictyostelium. E.M.B.O. J. 2000, 19:4846-4854.
99. 2+, but not through cAMP, and has a fundamental role in natural aggregation. J. Cell Sci. 2012, 125:1770-1783.
100. 2+ release channels participate in the secretory cycle of Paramecium cells. Mol. Cell. Biol. 2009, 29:3605-3622.
101. Ladenburger E.M., Korn I., Kasielke N., Wassmer T., Plattner H. An Ins(1,4,5)P3 receptor in Paramecium is associated with the osmoregulatory system. J. Cell Sci. 2006, 119:3705-3717.
102. Ladenburger E.M., Plattner H. Calcium-release channels in paramecium. Genomic expansion, differential positioning and partial transcriptional elimination. PLoS One 2011, 6:e27111.
103. Huang G., Bartlett P.J., Thomas A.P., Moreno S.N., Docampo R. Acidocalcisomes of Trypanosoma brucei have an inositol 1,4,5-trisphosphate receptor that is required for growth and infectivity. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:1887-1892.
104. Hashimoto M., Enomoto M., Morales J., et al. Inositol 1,4,5-trisphosphate receptor regulates replication, differentiation, infectivity and virulence of the parasitic protist Trypanosoma cruzi. Mol. Microbiol. 2013, 87:1133-1150.
105. 2+ from reserve granules, lysosome-related organelles, in sea urchin eggs. Cell 2002, 111:703-708.
106. 2+-signalling patterns by NAADP in pancreatic acinar cells. Nature 1999, 398:74-76.
107. 2+ signalling by NAADP. Trends Biochem. Sci. 2001, 26:482-489.
108. Brailoiu E., Hoard J.L., Filipeanu C.M., et al. NAADP potentiates neurite outgrowth. J. Biol. Chem. 2005, 280:5646-5650.
109. Brailoiu E., Churamani D., Pandey V., et al. Messenger-specific role for NAADP in neuronal differentiation. J. Biol. Chem. 2006, 281:15923-15928.
110. Brailoiu G.C., Brailoiu E., Parkesh R., et al. NAADP-mediated channel chatter in neurons of the rat medulla oblongata. Biochem. J. 2009, 419:91-97.
111. 2+ signals. J. Cell Sci. 2013, 126:60-66.
112. 2+ microdomains. J. Cell Sci. 2014, 127:2934-2943.
113. Churchill G.C., O'Neil J.S., Masgrau R., et al. Sperm deliver a new messenger: NAADP. Curr. Biol. 2003, 13:125-128.
114. 2+ Spiking in mouse pancreatic acinar cells. Curr. Biol. 2005, 15:874-878.
115. 2+ stores by glutamate. Biochem. J. 2009, 422:503-512.
116. Galione A., Morgan A.J., Arredouani A., et al. NAADP as an intracellular messenger regulating lysosomal calcium-release channels. Biochem. Soc. Trans. 2010, 38:1424-1431.
117. 2+ signaling machinery in early animal and fungal evolution. Mol. Biol. Evol. 2012, 29:91-100.
118. 2+ transients and defense responses in tobacco BY-2 cells. Biochem. Biophys. Res. Commun. 2004, 317:823-830.
119. 2+ channels. Biochem. Biophys. Res. Commun. 2004, 324:40-45.
120. 2+ signals induced by abiotic and biotic stresses. Plant J. 2008, 53:287-299.
121. 2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:6497-6502.
122. de Castro P.A., Chiaratto J., Winkelstroter L.K., et al. The involvement of the Mid1/Cch1/Yvc1 calcium channels in Aspergillus fumigatus virulence. PLoS One 2014, 9:e103957.
123. Bargal R., Avidan N., Ben-Asher E., et al. Identification of the gene causing mucolipidosis type IV. Nat. Genet. 2000, 26:118-123.
124. Platt F.M., Boland B., van der Spoel A.C. The cell biology of disease: lysosomal storage disorders: the cellular impact of lysosomal dysfunction. J. Cell Biol. 2012, 199:723-734.
125. 2+ channels of membrane traffic. Channels (Austin) 2012, 6.
126. 2+ in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J. Cell Biol. 2000, 149:1053-1062.
127. Luzio J.P., Pryor P.R., Bright N.A. Lysosomes: fusion and function. Nat. Rev. Mol. Cell. Biol. 2007, 8:622-632.
128. Shen D., Wang X., Li X., et al. Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release. Nat. Commun. 2012, 3:731.
129. Martina J.A., Lelouvier B., Puertollano R. The calcium channel mucolipin-3 is a novel regulator of trafficking along the endosomal pathway. Traffic 2009, 10:1143-1156.
130. 2+ channel TRPML3 regulates membrane trafficking and autophagy. Traffic 2009, 10:1157-1167.
131. Cuajungco M.P., Samie M.A. The varitint-waddler mouse phenotypes and the TRPML3 ion channel mutation: cause and consequence. Pflug. Arch. 2008, 457:463-473.
132. Corvera S., D'Arrigo A., Stenmark H. Phosphoinositides in membrane traffic. Curr. Opin. Cell. Biol. 1999, 11:460-465.
133. Grimm C., Holdt L.M., Chen C.C., et al. High susceptibility to fatty liver disease in two-pore channel 2-deficient mice. Nat. Commun. 2014, 5:4699.
134. 2+ signaling and endolysosomal trafficking. Curr. Biol. 2010, 20:703-709.
135. Ruas M., Chuang K.T., Davis L.C., et al. TPC1 has two variant isoforms and their removal has different effects on endo-lysosomal functions compared to loss of TPC2. Mol. Cell. Biol. 2014.
136. Lin-Moshier Y., Keebler M.V., Hooper R., et al. The two-pore channel (TPC) interactome unmasks isoform-specific roles for TPCs in endolysosomal morphology and cell pigmentation. Proc. Natl. Acad. Sci. 2014, 111:13087-13092.
137. Patel S., Docampo R. In with the TRP channels: intracellular functions for TRPM1 and TRPM2. Sci. Signal. 2009, 2:e69.
138. Sulem P., Gudbjartsson D.F., Stacey S.N., et al. Two newly identified genetic determinants of pigmentation in Europeans. Nat. Genet. 2008, 40:835-837.
139. Bucci C., Thomsen P., Nicoziani P., McCarthy J., van D.B. Rab7: a key to lysosome biogenesis. Mol. Biol. Cell 2000, 11:467-480.
140. Hutagalung A.H., Novick P.J. Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 2011, 91:119-149.
141. Gomez-Suaga P., Luzon-Toro B., Churamani D., et al. Leucine-rich repeat kinase 2 regulates autophagy through a calcium-dependent pathway involving NAADP. Hum. Mol. Genet. 2012, 21:511-525.
142. Hockey L.N., Kilpatrick B.S., Eden E.R., et al. Dysregulation of lysosomal morphology by pathogenic LRRK2 is corrected by two-pore channel 2 inhibition. J. Cell Sci. 2014, in press (see http://www.ncbi.nlm.nih.gov/pubmed/?term=patel+s+hockey).
143. Marchant J.S., Patel S. Two-pore channels at the intersection of endolysosomal membrane traffic. Biochem. Soc. Trans. 2015, in press (not on pubmed yet).
144. Parkinson K., Baines A.E., Keller T., et al. Calcium-dependent regulation of Rab activation and vesicle fusion by an intracellular P2X ion channel. Nat. Cell Biol. 2014, 16:87-98.
145. 2+ signaling: from phytoplankton to mammals. Cell Calcium 2010.
146. 2+ release from bovine adrenal medullary secretory vesicles. J. Biol. Chem. 1990, 265:13446-13448.
147. 2+ storage proteins chromogranins A and B. J. Biol. Chem. 2001, 276:45806-45812.
148. Huh Y.H., Yoo J.A., Bahk S.J., Yoo S.H. Distribution profile of inositol 1,4,5-trisphosphate receptor isoforms in adrenal chromaffin cells. FEBS Lett. 2005, 579:2597-2603.
149. 3 receptors. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:10758-10763.
150. 2+ release from insulin-containing vesicles in living pancreatic b cells (MIN6). J. Biol. Chem. 2003, 278:11057-11064.
151. 2+ during the postfusion stage of lamellar body exocytosis in rat type II pneumocytes. PLoS One 2010, 5:e10982.
152. Samie M., Wang X., Zhang X., et al. A TRP channel in the lysosome regulates large particle phagocytosis via focal exocytosis. Dev. Cell 2013, 26:511-524.
153. 2+ signaling in Dictyostelium discoideum. Eukaryot. Cell 2005, 4:1513-1525.
154. Plattner H., Sehring I.M., Mohamed I.K., et al. Calcium signaling in closely related protozoan groups (Alveolata): non-parasitic ciliates (Paramecium, Tetrahymena) vs. parasitic Apicomplexa (Plasmodium, Toxoplasma). Cell Calcium 2012, 51:351-382.
155. Prole D.L., Taylor C.W. Identification of intracellular and plasma membrane calcium channel homologues in pathogenic parasites. PLoS One 2011, 6:e26218.