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Review

Ion channels in the regulation of autophagy

ORCID Icon, , , ORCID Icon &
Pages 3-21 | Received 16 Feb 2017, Accepted 21 Sep 2017, Published online: 23 Nov 2017

References

  • Klionsky DJ, Codogno P. The mechanism and physiological function of macroautophagy. J Innate Immun. 2013;5:427–33. doi:10.1159/000351979. PMID:23774579.
  • Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, Jimenez-Sanchez M, Korolchuk VI, Lichtenberg M, Luo S, et al. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev. 2010;90:1383–435. doi:10.1152/physrev.00030.2009. PMID:20959619.
  • Singh R, Cuervo AM. Autophagy in the cellular energetic balance. Cell Metab. 2011;13:495–504. doi:10.1016/j.cmet.2011.04.004. PMID:21531332.
  • Choi AMK, Ryter SW, Levine B. Autophagy in human health and disease. N Engl J Med. 2013;368:1845–6. doi:10.1056/NEJMra1205406. PMID:23656658.
  • Kroemer G, Mariño G, Levine B. Autophagy and the integrated stress response. Mol Cell. 2010;40:280–93. doi:10.1016/j.molcel.2010.09.023. PMID:20965422.
  • Li W, Li J, Bao J. Microautophagy: lesser-known self-eating. Cell Mol Life Sci. 2012;69:1125–36. doi:10.1007/s00018-011-0865-5. PMID:22080117.
  • Cuervo AM, Wong E. Chaperone-mediated autophagy: roles in disease and aging. Cell Res. 2014;24:92–104. doi:10.1038/cr.2013.153. PMID:24281265.
  • Yin Z, Pascual C, Klionsky DJ. Autophagy: machinery and regulation. Microb cell (Graz, Austria). 2016;3:588–96. doi:10.15698/mic2016.12.546.
  • Gallagher LE, Chan EYW. Early signalling events of autophagy. Essays Biochem. 2013;55:1–15. doi:10.1042/bse0550001. PMID:24070467.
  • Tooze SA. Current views on the source of the autophagosome membrane. Essays Biochem. 2013;55:29–38. doi:10.1042/bse0550029. PMID:24070469.
  • Abada A, Elazar Z. Getting ready for building: signaling and autophagosome biogenesis. EMBO Rep. 2014;15:839–52. doi:10.15252/embr.201439076. PMID:25027988.
  • Lamb CA, Yoshimori T, Tooze SA. The autophagosome: origins unknown, biogenesis complex. Nat Rev Mol Cell Biol. 2013;14:759–74. doi:10.1038/nrm3696. PMID:24201109.
  • Kim J, Kundu M, Viollet B, Guan K-L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011;13:132–41. doi:10.1038/ncb2152. PMID:21258367.
  • Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, Iemura S -i., Natsume T, Takehana K, Yamada N, et al. Nutrient-dependent mTORC1 Association with the ULK1-Atg13-FIP200 Complex Required for Autophagy. Mol Biol Cell. 2009;20:1981–91. doi:10.1091/mbc.E08-12-1248. PMID:19211835.
  • Inoki K, Zhu T, Guan K-L. TSC2 mediates cellular energy response to control cell growth and survival. Cell. 2003;115:577–90. doi:10.1016/S0092-8674(03)00929-2. PMID:14651849.
  • Russell RC, Tian Y, Yuan H, Park HW, Chang Y-Y, Kim J, Kim H, Neufeld TP, Dillin A, Guan K-L. ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat Cell Biol. 2013;15:741–50. doi:10.1038/ncb2757. PMID:23685627.
  • Mizushima N, Yoshimori T, Ohsumi Y. The Role of Atg Proteins in Autophagosome Formation. Annu Rev Cell Dev Biol. 2011;27:107–32. doi:10.1146/annurev-cellbio-092910-154005. PMID:21801009.
  • Proikas-Cezanne T, Takacs Z, Donnes P, Kohlbacher O. WIPI proteins: essential PtdIns3P effectors at the nascent autophagosome. J Cell Sci. 2015;128:207–17. doi:10.1242/jcs.146258. PMID:25568150.
  • Polson HEJ, de Lartigue J, Rigden DJ, Reedijk M, Urbé S, Clague MJ, Tooze SA. Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy. 2010;6:506–22. doi:10.4161/auto.6.4.11863. PMID:20505359.
  • Hanada T, Noda NN, Satomi Y, Ichimura Y, Fujioka Y, Takao T, Inagaki F, Ohsumi Y. The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem. 2007;282:37298–302. doi:10.1074/jbc.C700195200. PMID:17986448.
  • Fujita N, Itoh T, Omori H, Fukuda M, Noda T, Yoshimori T. The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol Biol Cell. 2008;19:2092–100. doi:10.1091/mbc.E07-12-1257. PMID:18321988.
  • Lee Y-K, Lee J-A. Role of the mammalian ATG8/LC3 family in autophagy: differential and compensatory roles in the spatiotemporal regulation of autophagy. BMB Rep. 2016;49:424–30. doi:10.5483/BMBRep.2016.49.8.081. PMID:27418283.
  • Rogov V, Dötsch V, Johansen T, Kirkin V. Interactions between Autophagy Receptors and Ubiquitin-like Proteins Form the Molecular Basis for Selective Autophagy. Mol Cell. 2014;53:167–78. doi:10.1016/j.molcel.2013.12.014. PMID:24462201.
  • Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, Adachi H, Adams CM, Adams PD, Adeli K, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12:1–222. doi:10.1080/15548627.2015.1100356. PMID:26799652.
  • Arcangeli A, Becchetti A. Ion Channels and the Cell Cycle. In: Janigro D, editor. The Cell Cycle in the Central Nervous System. Totowa (NJ): Humana Press; 2006. p. 81–94.
  • Lang F, Föller M, Lang KS, Lang PA, Ritter M, Gulbins E, Vereninov A, Huber SM. Ion channels in cell proliferation and apoptotic cell death. J Membr Biol. 2005;205:147–57. doi:10.1007/s00232-005-0780-5. PMID:16362503.
  • Kondratskyi A, Kondratska K, Skryma R, Prevarskaya N. Ion channels in the regulation of apoptosis. Biochim Biophys Acta. 2015;1848:2532–46. doi:10.1016/j.bbamem.2014.10.030. PMID:25450339.
  • Jentsch TJ, Hübner CA, Fuhrmann JC. Ion channels: Function unravelled by dysfunction. Nat Cell Biol. 2004;6:1039–47. doi:10.1038/ncb1104-1039. PMID:15516997.
  • Bagal SK, Brown AD, Cox PJ, Omoto K, Owen RM, Pryde DC, Sidders B, Skerratt SE, Stevens EB, Storer RI, et al. Ion Channels as Therapeutic Targets: A Drug Discovery Perspective. J Med Chem. 2013;56:593–624. doi:10.1021/jm3011433. PMID:23121096.
  • Alexander SP, Kelly E, Marrion N, Peters JA, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Southan C, Buneman OP, et al. The Concise Guide to PHARMACOLOGY 2015/16: Overview. Br J Pharmacol. 2015;172:5729–43. doi:10.1111/bph.13347. PMID:26650438.
  • Kondratskyi A, Yassine M, Kondratska K, Skryma R, Slomianny C, Prevarskaya N. Calcium-permeable ion channels in control of autophagy and cancer. Front Physiol. 2013;4:272. doi:10.3389/fphys.2013.00272. PMID:24106480.
  • Berridge MJ, Lipp P, Bootman MD. The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol. 2000;1:11–21. doi:10.1038/35036035. PMID:11413485.
  • Clapham DE, Abzhanov A, Kuo WP, Hartmann C, Grant BR, Grant PR, Tabin CJ, Alvarez VA, Sabatini BL, Bamji SX, et al. Calcium Signaling. Cell. 2007;131:1047–58. doi:10.1016/j.cell.2007.11.028. PMID:18083096.
  • Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol. 2003;4:517–29. doi:10.1038/nrm1155. PMID:12838335.
  • La Rovere RML, Roest G, Bultynck G, Parys JB. Intracellular Ca(2+) signaling and Ca(2+) microdomains in the control of cell survival, apoptosis and autophagy. Cell Calcium. 2016;60:74–87. doi:10.1016/j.ceca.2016.04.005. PMID:27157108.
  • East DA, Campanella M. Ca2+ in quality control: an unresolved riddle critical to autophagy and mitophagy. Autophagy. 2013;9:1710–9. doi:10.4161/auto.25367. PMID:24121708.
  • Decuypere J-P, Bultynck G, Parys JB. A dual role for Ca(2+) in autophagy regulation. Cell Calcium. 2011;50:242–50. doi:10.1016/j.ceca.2011.04.001. PMID:21571367.
  • Gordon PB, Holen I, Fosse M, Røtnes JS, Seglen PO. Dependence of hepatocytic autophagy on intracellularly sequestered calcium. J Biol Chem. 1993;268:26107–12. PMID:8253727.
  • Høyer-Hansen M, Bastholm L, Szyniarowski P, Campanella M, Szabadkai G, Farkas T, Bianchi K, Fehrenbacher N, Elling F, Rizzuto R, et al. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol Cell. 2007;25:193–205. doi:10.1016/j.molcel.2006.12.009. PMID:17244528.
  • Law BYK, Wang M, Ma D-L, Al-Mousa F, Michelangeli F, Cheng S-H, Ng MHL, To K-F, Mok AYF, Ko RYY, et al. Alisol B, a novel inhibitor of the sarcoplasmic/endoplasmic reticulum Ca(2+) ATPase pump, induces autophagy, endoplasmic reticulum stress, and apoptosis. Mol Cancer Ther. 2010;9:718–30. doi:10.1158/1535-7163.MCT-09-0700. PMID:20197400.
  • Gómez-Suaga P, Luzón-Toro B, Churamani D, Zhang L, Bloor-Young D, Patel S, Woodman PG, Churchill GC, Hilfiker S. Leucine-rich repeat kinase 2 regulates autophagy through a calcium-dependent pathway involving NAADP. Hum Mol Genet. 2012;21:511–25. doi:10.1093/hmg/ddr481. PMID:22012985.
  • Ghislat G, Patron M, Rizzuto R, Knecht E. Withdrawal of essential amino acids increases autophagy by a pathway involving Ca2+/calmodulin-dependent kinase kinase-β (CaMKK-β). J Biol Chem. 2012;287:38625–36. doi:10.1074/jbc.M112.365767. PMID:23027865.
  • Son SM, Jung ES, Shin HJ, Byun J, Mook-Jung I. Aβ-induced formation of autophagosomes is mediated by RAGE-CaMKKβ-AMPK signaling. Neurobiol Aging. 2012;33:1006.e11–23. doi:10.1016/j.neurobiolaging.2011.09.039.
  • Sakaki K, Wu J, Kaufman RJ. Protein kinase Ctheta is required for autophagy in response to stress in the endoplasmic reticulum. J Biol Chem. 2008;283:15370–80. doi:10.1074/jbc.M710209200. PMID:18356160.
  • Grotemeier A, Alers S, Pfisterer SG, Paasch F, Daubrawa M, Dieterle A, Viollet B, Wesselborg S, Proikas-Cezanne T, Stork B. AMPK-independent induction of autophagy by cytosolic Ca2+ increase. Cell Signal. 2010;22:914–25. doi:10.1016/j.cellsig.2010.01.015. PMID:20114074.
  • Gao W, Ding W-X, Stolz DB, Yin X-M. Induction of macroautophagy by exogenously introduced calcium. Autophagy. 2008;4:754–61. doi:10.4161/auto.6360. PMID:18560273.
  • Gulati P, Gaspers LD, Dann SG, Joaquin M, Nobukuni T, Natt F, Kozma SC, Thomas AP, Thomas G. Amino acids activate mTOR complex 1 via Ca2+/CaM signaling to hVps34. Cell Metab. 2008;7:456–65. doi:10.1016/j.cmet.2008.03.002. PMID:18460336.
  • Khan MT, Joseph SK. Role of inositol trisphosphate receptors in autophagy in DT40 cells. J Biol Chem. 2010;285:16912–20. doi:10.1074/jbc.M110.114207. PMID:20308071.
  • Ivanova H, Vervliet T, Missiaen L, Parys JB, De Smedt H, Bultynck G. Inositol 1,4,5-trisphosphate receptor-isoform diversity in cell death and survival. Biochim Biophys Acta. 2014;1843:2164–83. doi:10.1016/j.bbamcr.2014.03.007. PMID:24642269.
  • Parys JB, Decuypere J-P, Bultynck G. Role of the inositol 1,4,5-trisphosphate receptor/Ca2+-release channel in autophagy. Cell Commun Signal. 2012;10:17. doi:10.1186/1478-811X-10-17. PMID:22770472.
  • Decuypere J-P, Parys JB, Bultynck G. ITPRs/inositol 1,4,5-trisphosphate receptors in autophagy: From enemy to ally. Autophagy. 2015;11:1944–8. doi:10.1080/15548627.2015.1083666. PMID:26291777.
  • Sarkar S, Floto RA, Berger Z, Imarisio S, Cordenier A, Pasco M, Cook LJ, Rubinsztein DC. Lithium induces autophagy by inhibiting inositol monophosphatase. J Cell Biol. 2005;170:1101–11. doi:10.1083/jcb.200504035. PMID:16186256.
  • Vicencio JM, Ortiz C, Criollo A, Jones AWE, Kepp O, Galluzzi L, Joza N, Vitale I, Morselli E, Tailler M, et al. The inositol 1,4,5-trisphosphate receptor regulates autophagy through its interaction with Beclin 1. Cell Death Differ. 2009;16:1006–17. doi:10.1038/cdd.2009.34. PMID:19325567.
  • Criollo A, Maiuri MC, Tasdemir E, Vitale I, Fiebig AA, Andrews D, Molgó J, Díaz J, Lavandero S, Harper F, et al. Regulation of autophagy by the inositol trisphosphate receptor. Cell Death Differ. 2007;14:1029–39. PMID:17256008.
  • Cárdenas C, Miller RA, Smith I, Bui T, Molgó J, Müller M, Vais H, Cheung K-H, Yang J, Parker I, et al. Essential regulation of cell bioenergetics by constitutive InsP3 receptor Ca2+ transfer to mitochondria. Cell. 2010;142:270–83. doi:10.1016/j.cell.2010.06.007. PMID:20655468.
  • Rowland AA, Voeltz GK. Endoplasmic reticulum–mitochondria contacts: function of the junction. Nat Rev Mol Cell Biol. 2012;13:607–25. doi:10.1038/nrm3440. PMID:22992592.
  • Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM, Tuft RA, Pozzan T. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science. 1998;280:1763–6. doi:10.1126/science.280.5370.1763. PMID:9624056.
  • Rizzuto R, Brini M, Murgia M, Pozzan T. Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science. 1993;262:744–7. doi:10.1126/science.8235595. PMID:8235595.
  • Szabadkai G, Bianchi K, Várnai P, De Stefani D, Wieckowski MR, Cavagna D, Nagy AI, Balla T, Rizzuto R. Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels. J Cell Biol. 2006;175:901–11. doi:10.1083/jcb.200608073. PMID:17178908.
  • De Stefani D, Raffaello A, Teardo E, Szabò I, Rizzuto R. A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature. 2011;476:336–40. doi:10.1038/nature10230. PMID:21685888.
  • Hamasaki M, Furuta N, Matsuda A, Nezu A, Yamamoto A, Fujita N, Oomori H, Noda T, Haraguchi T, Hiraoka Y, et al. Autophagosomes form at ER–mitochondria contact sites. Nature. 2013;495:389–93. doi:10.1038/nature11910. PMID:23455425.
  • Decuypere J-P, Welkenhuyzen K, Luyten T, Ponsaerts R, Dewaele M, Molgó J, Agostinis P, Missiaen L, De Smedt H, Parys JB, et al. Ins(1,4,5)P3 receptor-mediated Ca2+ signaling and autophagy induction are interrelated. Autophagy. 2011;7:1472–89. doi:10.4161/auto.7.12.17909. PMID:22082873.
  • Lam D, Kosta A, Luciani M-F, Golstein P. The Inositol 1,4,5-Trisphosphate Receptor Is Required to Signal Autophagic Cell Death. Mol Biol Cell. 2008;19:691–700. doi:10.1091/mbc.E07-08-0823. PMID:18077554.
  • Messai Y, Noman MZ, Hasmim M, Janji B, Tittarelli A, Boutet M, Baud V, Viry E, Billot K, Nanbakhsh A, et al. ITPR1 protects renal cancer cells against natural killer cells by inducing autophagy. Cancer Res. 2014;74:6820–32. doi:10.1158/0008-5472.CAN-14-0303. PMID:25297632.
  • Phillips MJ, Voeltz GK. Structure and function of ER membrane contact sites with other organelles. Nat Rev Mol Cell Biol. 2015;17:69–82. doi:10.1038/nrm.2015.8. PMID:26627931.
  • Medina DL, Ballabio A. Lysosomal calcium regulates autophagy. Autophagy. 2015;11:970–1. doi:10.1080/15548627.2015.1047130. PMID:26000950.
  • Morgan AJ, Davis LC, Wagner SKTY, Lewis AM, Parrington J, Churchill GC, Galione A. Bidirectional Ca2+ signaling occurs between the endoplasmic reticulum and acidic organelles. J Cell Biol. 2013;200:789–805. doi:10.1083/jcb.201204078. PMID:23479744.
  • Garrity AG, Wang W, Collier CM, Levey SA, Gao Q, Xu H. The endoplasmic reticulum, not the pH gradient, drives calcium refilling of lysosomes. Elife. 2016;55. pii: e15887. doi:10.7554/eLife.15887.
  • Min CK, Yeom DR, Lee K-E, Kwon H-K, Kang M, Kim Y-S, Park ZY, Jeon H, Kim DH. Coupling of ryanodine receptor 2 and voltage-dependent anion channel 2 is essential for Ca2+ transfer from the sarcoplasmic reticulum to the mitochondria in the heart. Biochem J. 2012;447:371–9. doi:10.1042/BJ20120705. PMID:22867515.
  • Beutner G, Sharma VK, Giovannucci DR, Yule DI, Sheu SS. Identification of a ryanodine receptor in rat heart mitochondria. J Biol Chem. 2001;276:21482–8. doi:10.1074/jbc.M101486200. PMID:11297554.
  • O-Uchi J, Jhun BS, Hurst S, Bisetto S, Gross P, Chen M, Kettlewell S, Park J, Oyamada H, Smith GL, et al. Overexpression of ryanodine receptor type 1 enhances mitochondrial fragmentation and Ca2+-induced ATP production in cardiac H9c2 myoblasts. Am J Physiol Heart Circ Physiol. 2013;305:H1736–51. doi:10.1152/ajpheart.00094.2013. PMID:24124188.
  • Bround MJ, Wambolt R, Luciani DS, Kulpa JE, Rodrigues B, Brownsey RW, Allard MF, Johnson JD. Cardiomyocyte ATP production, metabolic flexibility, and survival require calcium flux through cardiac ryanodine receptors in vivo. J Biol Chem. 2013;288:18975–86. doi:10.1074/jbc.M112.427062. PMID:23678000.
  • Yuan Q, Chen Z, Santulli G, Gu L, Yang Z-G, Yuan Z-Q, Zhao Y-T, Xin H-B, Deng K-Y, Wang S-Q, et al. Functional role of Calstabin2 in age-related cardiac alterations. Sci Rep. 2014;4:7425. doi:10.1038/srep07425. PMID:25502776.
  • Liou B, Peng Y, Li R, Inskeep V, Zhang W, Quinn B, Dasgupta N, Blackwood R, Setchell KDR, Fleming S, et al. Modulating ryanodine receptors with dantrolene attenuates neuronopathic phenotype in Gaucher disease mice. Hum Mol Genet. 2016;25:5126–41. PMID:27655403.
  • Vervliet T, Pintelon I, Welkenhuyzen K, Bootman MD, Bannai H, Mikoshiba K, Martinet W, Nadif Kasri N, Parys JB, Bultynck G. Basal ryanodine receptor activity suppresses autophagic flux. Biochem Pharmacol. 2017;132:133–42. doi:10.1016/j.bcp.2017.03.011. PMID:28322744.
  • Kinnear NP, Wyatt CN, Clark JH, Calcraft PJ, Fleischer S, Jeyakumar LH, Nixon GF, Evans AM. Lysosomes co-localize with ryanodine receptor subtype 3 to form a trigger zone for calcium signalling by NAADP in rat pulmonary arterial smooth muscle. Cell Calcium. 2008;44:190–201. doi:10.1016/j.ceca.2007.11.003. PMID:18191199.
  • Park H-W, Park H, Semple IA, Jang I, Ro S-H, Kim M, Cazares VA, Stuenkel EL, Kim J-J, Kim JS, et al. Pharmacological correction of obesity-induced autophagy arrest using calcium channel blockers. Nat Commun. 2014;5:4834. doi:10.1038/ncomms5834. PMID:25189398.
  • Mauvezin C, Nagy P, Juhász G, Neufeld TP. Autophagosome-lysosome fusion is independent of V-ATPase-mediated acidification. Nat Commun. 2015;6:7007. doi:10.1038/ncomms8007. PMID:25959678.
  • Chung KM, Jeong E-J, Park H, An H-K, Yu S-W. Mediation of Autophagic Cell Death by Type 3 Ryanodine Receptor (RyR3) in Adult Hippocampal Neural Stem Cells. Front Cell Neurosci. 2016;10:116. doi:10.3389/fncel.2016.00116. PMID:27199668.
  • Zou Y, Liang Y, Gong H, Zhou N, Ma H, Guan A, Sun A, Wang P, Niu Y, Jiang H, et al. Ryanodine receptor type 2 is required for the development of pressure overload-induced cardiac hypertrophy. Hypertens (Dallas, Tex 1979). 2011;58:1099–110. doi:10.1161/HYPERTENSIONAHA.111.173500.
  • Kamer KJ, Mootha VK. The molecular era of the mitochondrial calcium uniporter. Nat Rev Mol Cell Biol. 2015;16:545–53. doi:10.1038/nrm4039. PMID:26285678.
  • Baughman JM, Perocchi F, Girgis HS, Plovanich M, Belcher-Timme CA, Sancak Y, Bao XR, Strittmatter L, Goldberger O, Bogorad RL, et al. Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature. 2011;476:341–5. doi:10.1038/nature10234. PMID:21685886.
  • Giorgi C, Baldassari F, Bononi A, Bonora M, De Marchi E, Marchi S, Missiroli S, Patergnani S, Rimessi A, Suski JM, et al. Mitochondrial Ca2+ and apoptosis. Cell Calcium. 2012;52:36–43. doi:10.1016/j.ceca.2012.02.008. PMID:22480931.
  • Bonora M, Patergnani S, Rimessi A, De Marchi E, Suski JM, Bononi A, Giorgi C, Marchi S, Missiroli S, Poletti F, et al. ATP synthesis and storage. Purinergic Signal. 2012;8:343–57. doi:10.1007/s11302-012-9305-8. PMID:22528680.
  • Mallilankaraman K, Cárdenas C, Doonan PJ, Chandramoorthy HC, Irrinki KM, Golenár T, Csordás G, Madireddi P, Yang J, Müller M, et al. MCUR1 is an essential component of mitochondrial Ca2+ uptake that regulates cellular metabolism. Nat Cell Biol. 2012;14:1336–43. doi:10.1038/ncb2622. PMID:23178883.
  • Tomar D, Dong Z, Shanmughapriya S, Koch DA, Thomas T, Hoffman NE, Timbalia SA, Goldman SJ, Breves SL, Corbally DP, et al. MCUR1 Is a Scaffold Factor for the MCU Complex Function and Promotes Mitochondrial Bioenergetics. Cell Rep. 2016;15:1673–85. doi:10.1016/j.celrep.2016.04.050. PMID:27184846.
  • Huang G, Vercesi AE, Docampo R. Essential regulation of cell bioenergetics in Trypanosoma brucei by the mitochondrial calcium uniporter. Nat Commun. 2013;4:2865. doi:10.1038/ncomms3865. PMID:24305511.
  • Catterall WA. Voltage-gated calcium channels. Cold Spring Harb Perspect Biol. 2011;3:a003947. doi:10.1101/cshperspect.a003947. PMID:21746798.
  • Lacinová L. Voltage-dependent calcium channels. Gen Physiol Biophys. 2005;24 Suppl 1:1–78. PMID:16096350.
  • Williams A, Sarkar S, Cuddon P, Ttofi EK, Saiki S, Siddiqi FH, Jahreiss L, Fleming A, Pask D, Goldsmith P, et al. Novel targets for Huntington's disease in an mTOR-independent autophagy pathway. Nat Chem Biol. 2008;4:295–305. doi:10.1038/nchembio.79. PMID:18391949.
  • Xia H-G, Zhang L, Chen G, Zhang T, Liu J, Jin M, Ma X, Ma D, Yuan J. Control of basal autophagy by calpain1 mediated cleavage of ATG5. Autophagy. 2010;6:61–6. doi:10.4161/auto.6.1.10326. PMID:19901552.
  • Anekonda TS, Quinn JF. Calcium channel blocking as a therapeutic strategy for Alzheimer's disease: the case for isradipine. Biochim Biophys Acta. 2011;1812:1584–90. doi:10.1016/j.bbadis.2011.08.013. PMID:21925266.
  • Rim H-K, Cho S, Shin D-H, Chung K-S, Cho Y-W, Choi J-H, Lee JY, Lee K-T. T-type Ca2+ channel blocker, KYS05090 induces autophagy and apoptosis in A549 cells through inhibiting glucose uptake. Molecules. 2014;19:9864–75. doi:10.3390/molecules19079864. PMID:25006791.
  • Lim J-A, Li L, Kakhlon O, Myerowitz R, Raben N. Defects in calcium homeostasis and mitochondria can be reversed in Pompe disease. Autophagy. 2015;11:385–402. doi:10.1080/15548627.2015.1009779. PMID:25758767.
  • Das A, Pushparaj C, Herreros J, Nager M, Vilella R, Portero M, Pamplona R, Matias-Guiu X, Martí RM, Cantí C. T-type calcium channel blockers inhibit autophagy and promote apoptosis of malignant melanoma cells. Pigment Cell Melanoma Res. 2013;26:874–85. doi:10.1111/pcmr.12155. PMID:23931340.
  • Ardizzone TD, Lu X-H, Dwyer DS. Calcium-independent inhibition of glucose transport in PC-12 and L6 cells by calcium channel antagonists. AJP Cell Physiol. 2002;283:C579–86. doi:10.1152/ajpcell.00451.2001.
  • Lemieux B, Percival MD, Falgueyret J-P. Quantitation of the lysosomotropic character of cationic amphiphilic drugs using the fluorescent basic amine Red DND-99. Anal Biochem. 2004;327:247–51. doi:10.1016/j.ab.2004.01.010. PMID:15051542.
  • Pushparaj C, Das A, Purroy R, Nàger M, Herreros J, Pamplona R, Cantí C. Voltage-gated calcium channel blockers deregulate macroautophagy in cardiomyocytes. Int J Biochem Cell Biol. 2015;68:166–75. doi:10.1016/j.biocel.2015.09.010. PMID:26429067.
  • Shcheglovitov A, Zhelay T, Vitko Y, Osipenko V, Perez-Reyes E, Kostyuk P, Shuba Y. Contrasting the effects of nifedipine on subtypes of endogenous and recombinant T-type Ca2+ channels. Biochem Pharmacol. 2005;69:841–54. doi:10.1016/j.bcp.2004.11.024. PMID:15710361.
  • Tian X, Gala U, Zhang Y, Shang W, Nagarkar Jaiswal S, di Ronza A, Jaiswal M, Yamamoto S, Sandoval H, Duraine L, et al. A voltage-gated calcium channel regulates lysosomal fusion with endosomes and autophagosomes and is required for neuronal homeostasis. PLoS Biol. 2015;13:e1002103. doi:10.1371/journal.pbio.1002103. PMID:25811491.
  • Marchant JS, Patel S. Two-pore channels at the intersection of endolysosomal membrane traffic. Biochem Soc Trans. 2015;43:434–41. doi:10.1042/BST20140303. PMID:26009187.
  • Morgan AJ, Davis LC, Ruas M, Galione A. TPC: the NAADP discovery channel? Biochem Soc Trans 2015;43:384–9. doi:10.1042/BST20140300. PMID:26009180.
  • Brailoiu E, Churamani D, Cai X, Schrlau MG, Brailoiu GC, Gao X, Hooper R, Boulware MJ, Dun NJ, Marchant JS, et al. Essential requirement for two-pore channel 1 in NAADP-mediated calcium signaling. J Cell Biol. 2009;186:201–9. doi:10.1083/jcb.200904073. PMID:19620632.
  • Calcraft PJ, Ruas M, Pan Z, Cheng X, Arredouani A, Hao X, Tang J, Rietdorf K, Teboul L, Chuang K-T, et al. NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature. 2009;459:596–600. doi:10.1038/nature08030. PMID:19387438.
  • Pereira GJS, Hirata H, Fimia GM, do Carmo LG, Bincoletto C, Han SW, Stilhano RS, Ureshino RP, Bloor-Young D, Churchill G, et al. Nicotinic acid adenine dinucleotide phosphate (NAADP) regulates autophagy in cultured astrocytes. J Biol Chem. 2011;286:27875–81. doi:10.1074/jbc.C110.216580. PMID:21610076.
  • Alegre-Abarrategui J, Christian H, Lufino MMP, Mutihac R, Venda LL, Ansorge O, Wade-Martins R. LRRK2 regulates autophagic activity and localizes to specific membrane microdomains in a novel human genomic reporter cellular model. Hum Mol Genet. 2009;18:4022–34. doi:10.1093/hmg/ddp346. PMID:19640926.
  • Pereira GJS, Antonioli M, Hirata H, Ureshino RP, Nascimento AR, Bincoletto C, Vescovo T, Piacentini M, Maria Fimia G, Smaili SS. Glutamate induces autophagy via the two-pore channels in neural cells. Oncotarget. 2017;8:12730–40. PMID:28055974.
  • Lu Y, Hao B-X, Graeff R, Wong CWM, Wu W-T, Yue J. Two pore channel 2 (TPC2) inhibits autophagosomal-lysosomal fusion by alkalinizing lysosomal pH. J Biol Chem. 2013;288:24247–63. doi:10.1074/jbc.M113.484253. PMID:23836916.
  • Lin P-H, Duann P, Komazaki S, Park KH, Li H, Sun M, Sermersheim M, Gumpper K, Parrington J, Galione A, et al. Lysosomal two-pore channel subtype 2 (TPC2) regulates skeletal muscle autophagic signaling. J Biol Chem. 2015;290:3377–89. doi:10.1074/jbc.M114.608471. PMID:25480788.
  • Garcia-Rua V, Feijoo-Bandin S, Rodriguez-Penas D, Mosquera-Leal A, Abu-Assi E, Beiras A, Maria Seoane L, Lear P, Parrington J, Portoles M, et al. Endolysosomal two-pore channels regulate autophagy in cardiomyocytes. J Physiol. 2016;594:3061–77. doi:10.1113/JP271332. PMID:26757341.
  • Pedersen SF, Owsianik G, Nilius B. TRP channels: An overview. Cell Calcium. 2005;38:233–52. doi:10.1016/j.ceca.2005.06.028. PMID:16098585.
  • Ramsey IS, Delling M, Clapham DE. An introduction to TRP channels. Annu Rev Physiol. 2006;68:619–47. doi:10.1146/annurev.physiol.68.040204.100431. PMID:16460286.
  • Cheng X, Shen D, Samie M, Xu H. Mucolipins: Intracellular TRPML1-3 channels. FEBS Lett. 2010;584:2013–21. doi:10.1016/j.febslet.2009.12.056. PMID:20074572.
  • LaPlante JM, Falardeau J, Sun M, Kanazirska M, Brown EM, Slaugenhaupt SA, Vassilev PM. Identification and characterization of the single channel function of human mucolipin-1 implicated in mucolipidosis type IV, a disorder affecting the lysosomal pathway. FEBS Lett. 2002;532:183–7. doi:10.1016/S0014-5793(02)03670-0. PMID:12459486.
  • Dong X-P, Cheng X, Mills E, Delling M, Wang F, Kurz T, Xu H. The type IV mucolipidosis-associated protein TRPML1 is an endolysosomal iron release channel. Nature. 2008;455:992–6. doi:10.1038/nature07311. PMID:18794901.
  • Bach G. Mucolipidosis type IV. Mol Genet Metab. 2001;73:197–203. doi:10.1006/mgme.2001.3195. PMID:11461186.
  • Altarescu G, Sun M, Moore DF, Smith JA, Wiggs EA, Solomon BI, Patronas NJ, Frei KP, Gupta S, Kaneski CR, et al. The neurogenetics of mucolipidosis type IV. Neurology. 2002;59:306–13. doi:10.1212/WNL.59.3.306. PMID:12182165.
  • Curcio-Morelli C, Charles FA, Micsenyi MC, Cao Y, Venugopal B, Browning MF, Dobrenis K, Cotman SL, Walkley SU, Slaugenhaupt SA. Macroautophagy is defective in mucolipin-1-deficient mouse neurons. Neurobiol Dis. 2010;40:370–7. doi:10.1016/j.nbd.2010.06.010. PMID:20600908.
  • Jennings JJ, Zhu J-H, Rbaibi Y, Luo X, Chu CT, Kiselyov K. Mitochondrial aberrations in mucolipidosis Type IV. J Biol Chem. 2006;281:39041–50. doi:10.1074/jbc.M607982200. PMID:17056595.
  • Soyombo AA, Tjon-Kon-Sang S, Rbaibi Y, Bashllari E, Bisceglia J, Muallem S, Kiselyov K. TRP-ML1 regulates lysosomal pH and acidic lysosomal lipid hydrolytic activity. J Biol Chem. 2006;281:7294–301. doi:10.1074/jbc.M508211200. PMID:16361256.
  • Vergarajauregui S, Connelly PS, Daniels MP, Puertollano R. Autophagic dysfunction in mucolipidosis type IV patients. Hum Mol Genet. 2008;17:2723–37. doi:10.1093/hmg/ddn174. PMID:18550655.
  • Venugopal B, Mesires NT, Kennedy JC, Curcio-Morelli C, Laplante JM, Dice JF, Slaugenhaupt SA. Chaperone-mediated autophagy is defective in mucolipidosis type IV. J Cell Physiol. 2009;219:344–53. doi:10.1002/jcp.21676. PMID:19117012.
  • Sun T, Wang X, Lu Q, Ren H, Zhang H. CUP-5, the C. elegans ortholog of the mammalian lysosomal channel protein MLN1/TRPML1, is required for proteolytic degradation in autolysosomes. Autophagy. 2011;7:1308–15. doi:10.4161/auto.7.11.17759. PMID:21997367.
  • Wong C-O, Li R, Montell C, Venkatachalam K. Drosophila TRPML is required for TORC1 activation. Curr Biol. 2012;22:1616–21. doi:10.1016/j.cub.2012.06.055. PMID:22863314.
  • Onyenwoke RU, Sexton JZ, Yan F, Díaz MCH, Forsberg LJ, Major MB, Brenman JE. The mucolipidosis IV Ca2+ channel TRPML1 (MCOLN1) is regulated by the TOR kinase. Biochem J. 2015;470(3):331–42. doi:10.1042/BJ20150219. PMID:26195823.
  • Wang W, Gao Q, Yang M, Zhang X, Yu L, Lawas M, Li X, Bryant-Genevier M, Southall NT, Marugan J, et al. Up-regulation of lysosomal TRPML1 channels is essential for lysosomal adaptation to nutrient starvation. Proc Natl Acad Sci U S A. 2015;112:E1373–81. doi:10.1073/pnas.1419669112. PMID:25733853.
  • Zeevi DA, Lev S, Frumkin A, Minke B, Bach G. Heteromultimeric TRPML channel assemblies play a crucial role in the regulation of cell viability models and starvation-induced autophagy. J Cell Sci. 2010;123:3112–24. doi:10.1242/jcs.067330. PMID:20736310.
  • Medina DL, Di Paola S, Peluso I, Armani A, De Stefani D, Venditti R, Montefusco S, Scotto-Rosato A, Prezioso C, Forrester A, et al. Lysosomal calcium signalling regulates autophagy through calcineurin and ​TFEB. Nat Cell Biol. 2015;17:288–99. doi:10.1038/ncb3114. PMID:25720963.
  • Zhang X, Cheng X, Yu L, Yang J, Calvo R, Patnaik S, Hu X, Gao Q, Yang M, Lawas M, et al. MCOLN1 is a ROS sensor in lysosomes that regulates autophagy. Nat Commun. 2016;7:12109. doi:10.1038/ncomms12109. PMID:27357649.
  • Di Palma F, Belyantseva IA, Kim HJ, Vogt TF, Kachar B, Noben-Trauth K. Mutations in Mcoln3 associated with deafness and pigmentation defects in varitint-waddler (Va) mice. Proc Natl Acad Sci U S A. 2002;99:14994–9. doi:10.1073/pnas.222425399. PMID:12403827.
  • Kim HJ, Soyombo AA, Tjon-Kon-Sang S, So I, Muallem S. The Ca(2+) channel TRPML3 regulates membrane trafficking and autophagy. Traffic. 2009;10:1157–67. doi:10.1111/j.1600-0854.2009.00924.x. PMID:19522758.
  • Choi S, Kim HJ. The Ca2+ channel TRPML3 specifically interacts with the mammalian ATG8 homologue GATE16 to regulate autophagy. Biochem Biophys Res Commun. 2014;443:56–61. doi:10.1016/j.bbrc.2013.11.044. PMID:24269818.
  • Zeevi DA, Frumkin A, Offen-Glasner V, Kogot-Levin A, Bach G. A potentially dynamic lysosomal role for the endogenous TRPML proteins. J Pathol. 2009;219:153–62. doi:10.1002/path.2587. PMID:19557826.
  • Lange I, Yamamoto S, Partida-Sanchez S, Mori Y, Fleig A, Penner R. TRPM2 functions as a lysosomal Ca2+-release channel in beta cells. Sci Signal. 2009;2:ra23.
  • Sumoza-Toledo A, Penner R. TRPM2: a multifunctional ion channel for calcium signalling. J Physiol. 2011;589:1515–25. doi:10.1113/jphysiol.2010.201855. PMID:21135052.
  • Wyrsch P, Blenn C, Bader J, Althaus FR. Cell death and autophagy under oxidative stress: roles of poly(ADP-Ribose) polymerases and Ca(2+). Mol Cell Biol. 2012;32:3541–53. doi:10.1128/MCB.00437-12. PMID:22751932.
  • Wang Q, Guo W, Hao B, Shi X, Lu Y, Wong CWM, Ma VWS, Yip TTC, Au JSK, Hao Q, et al. Mechanistic study of TRPM2-Ca(2+)-CAMK2-BECN1 signaling in oxidative stress-induced autophagy inhibition. Autophagy. 2016;12:1340–54. doi:10.1080/15548627.2016.1187365. PMID:27245989.
  • Hall DP, Cost NG, Hegde S, Kellner E, Mikhaylova O, Stratton Y, Ehmer B, Abplanalp WA, Pandey R, Biesiada J, et al. TRPM3 and miR-204 establish a regulatory circuit that controls oncogenic autophagy in clear cell renal cell carcinoma. Cancer Cell. 2014;26:738–53. doi:10.1016/j.ccell.2014.09.015. PMID:25517751.
  • Runnels LW, Yue L, Clapham DE. TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science. 2001;291:1043–7. doi:10.1126/science.1058519. PMID:11161216.
  • Schmitz C, Perraud A-L, Johnson CO, Inabe K, Smith MK, Penner R, Kurosaki T, Fleig A, Scharenberg AM. Regulation of vertebrate cellular Mg2+ homeostasis by TRPM7. Cell. 2003;114:191–200. doi:10.1016/S0092-8674(03)00556-7. PMID:12887921.
  • Ryazanova L V, Rondon LJ, Zierler S, Hu Z, Galli J, Yamaguchi TP, Mazur A, Fleig A, Ryazanov AG. TRPM7 is essential for Mg(2+) homeostasis in mammals. Nat Commun. 2010;1:109. doi:10.1038/ncomms1108. PMID:21045827.
  • Visser D, Middelbeek J, van Leeuwen FN, Jalink K. Function and regulation of the channel-kinase TRPM7 in health and disease. Eur J Cell Biol. 2014;93:455–65. doi:10.1016/j.ejcb.2014.07.001. PMID:25073440.
  • Oh HG, Chun YS, Park C-S, Kim T-W, Park MK, Chung S. Regulation of basal autophagy by transient receptor potential melastatin 7 (TRPM7) channel. Biochem Biophys Res Commun. 2015;463:7–12. doi:10.1016/j.bbrc.2015.05.007. PMID:25983327.
  • Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature. 1997;389:816–24. doi:10.1038/39807. PMID:9349813.
  • Farfariello V, Amantini C, Santoni G. Transient receptor potential vanilloid 1 activation induces autophagy in thymocytes through ROS-regulated AMPK and Atg4C pathways. J Leukoc Biol. 2012;92:421–31. doi:10.1189/jlb.0312123. PMID:22753949.
  • Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J. 2007;26:1749–60. doi:10.1038/sj.emboj.7601623. PMID:17347651.
  • Li B-H, Yin Y-W, Liu Y, Pi Y, Guo L, Cao X-J, Gao C-Y, Zhang L-L, Li J-C. TRPV1 activation impedes foam cell formation by inducing autophagy in oxLDL-treated vascular smooth muscle cells. Cell Death Dis. 2014;5:e1182. doi:10.1038/cddis.2014.146. PMID:24743737.
  • Lu S, Xu D. Cold stress accentuates pressure overload-induced cardiac hypertrophy and contractile dysfunction: role of TRPV1/AMPK-mediated autophagy. Biochem Biophys Res Commun. 2013;442:8–15. doi:10.1016/j.bbrc.2013.10.128. PMID:24211590.
  • Li Q, Li L, Wang F, Chen J, Zhao Y, Wang P, Nilius B, Liu D, Zhu Z. Dietary capsaicin prevents nonalcoholic fatty liver disease through transient receptor potential vanilloid 1-mediated peroxisome proliferator-activated receptor δ activation. Pfluügers Arch Eur J Physiol. 2013;465:1303–16. doi:10.1007/s00424-013-1274-4.
  • Chien C-S, Ma K-H, Lee H-S, Liu P-S, Li Y-H, Huang Y-S, Chueh S-H. Dual effect of capsaicin on cell death in human osteosarcoma G292 cells. Eur J Pharmacol. 2013;718:350–60. doi:10.1016/j.ejphar.2013.08.011. PMID:24012930.
  • Liu A-J, Wang S-H, Hou S-Y, Lin C-J, Chiu W-T, Hsiao S-H, Chen T-H, Shih C-M. Evodiamine Induces Transient Receptor Potential Vanilloid-1-Mediated Protective Autophagy in U87-MG Astrocytes. Evid Based Complement Alternat Med. 2013;2013:354840. doi:10.1155/2013/354840. PMID:24454492.
  • Ahn S, Park J, An I, Jung SJ, Hwang J. Transient receptor potential cation channel V1 (TRPV1) is degraded by starvation- and glucocorticoid-mediated autophagy. Mol Cells. 2014;37:257–63. doi:10.14348/molcells.2014.2384. PMID:24658385.
  • Nabissi M, Morelli MB, Amantini C, Liberati S, Santoni M, Ricci-Vitiani L, Pallini R, Santoni G. Cannabidiol stimulates Aml-1a-dependent glial differentiation and inhibits glioma stem-like cells proliferation by inducing autophagy in a TRPV2-dependent manner. Int J cancer. 2015;137:1855–69. doi:10.1002/ijc.29573. PMID:25903924.
  • Zhan L, Yang Y, Ma T-T, Huang C, Meng X-M, Zhang L, Li J. Transient receptor potential vanilloid 4 inhibits rat HSC-T6 apoptosis through induction of autophagy. Mol Cell Biochem. 2015;402:9–22. doi:10.1007/s11010-014-2298-6. PMID:25600591.
  • Sukumaran P, Sun Y, Vyas M, Singh BB. TRPC1-mediated Ca2+ entry is essential for the regulation of hypoxia and nutrient depletion-dependent autophagy. Cell Death Dis. 2015;6:e1674. doi:10.1038/cddis.2015.7. PMID:25741599.
  • Azimi I, Milevskiy MJG, Kaemmerer E, Turner D, Yapa KTDS, Brown MA, Thompson EW, Roberts-Thomson SJ, Monteith GR. TRPC1 is a differential regulator of hypoxia-mediated events and Akt signalling in PTEN-deficient breast cancer cells. J Cell Sci. 2017;130:2292–305. doi:10.1242/jcs.196659. PMID:28559303.
  • Zhang L, Dai F, Cui L, Jing H, Fan P, Tan X, Guo Y, Zhou G. Novel role for TRPC4 in regulation of macroautophagy by a small molecule in vascular endothelial cells. Biochim Biophys Acta. 2015;1853:377–87. doi:10.1016/j.bbamcr.2014.10.030. PMID:25476892.
  • Orhon I, Dupont N, Zaidan M, Boitez V, Burtin M, Schmitt A, Capiod T, Viau A, Beau I, Wolfgang Kuehn E, et al. Primary-cilium-dependent autophagy controls epithelial cell volume in response to fluid flow. Nat Cell Biol. 2016;18:657–67. doi:10.1038/ncb3360. PMID:27214279.
  • Delmas P, Padilla F, Osorio N, Coste B, Raoux M, Crest M. Polycystins, calcium signaling, and human diseases. Biochem Biophys Res Commun. 2004;322:1374–83. doi:10.1016/j.bbrc.2004.08.044. PMID:15336986.
  • Cebotaru V, Cebotaru L, Kim H, Chiaravalli M, Boletta A, Qian F, Guggino WB. Polycystin-1 negatively regulates Polycystin-2 expression via the aggresome/autophagosome pathway. J Biol Chem. 2014;289:6404–14. doi:10.1074/jbc.M113.501205. PMID:24459142.
  • Prakriya M, Lewis RS. Store-Operated Calcium Channels. Physiol Rev. 2015;95:1383–436. doi:10.1152/physrev.00020.2014. PMID:26400989.
  • Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan PG. Orai1 is an essential pore subunit of the CRAC channel. Nature. 2006;443:230–3. doi:10.1038/nature05122. PMID:16921383.
  • Zhang SL, Yu Y, Roos J, Kozak JA, Deerinck TJ, Ellisman MH, Stauderman KA, Cahalan MD. STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature. 2005;437:902–5. doi:10.1038/nature04147. PMID:16208375.
  • Abdelmohsen K, Srikantan S, Tominaga K, Kang M-J, Yaniv Y, Martindale JL, Yang X, Park S-S, Becker KG, Subramanian M, et al. Growth inhibition by miR-519 via multiple p21-inducing pathways. Mol Cell Biol. 2012;32:2530–48. doi:10.1128/MCB.00510-12. PMID:22547681.
  • Tang B-D, Xia X, Lv X-F, Yu B-X, Yuan J-N, Mai X-Y, Shang J-Y, Zhou J-G, Liang S-J, Pang R-P. Inhibition of Orai1-mediated Ca 2+ entry enhances chemosensitivity of HepG2 hepatocarcinoma cells to 5-fluorouracil. J Cell Mol Med. 2017;21:904–15. doi:10.1111/jcmm.13029. PMID:27878958.
  • Chen Y-W, Chen Y-F, Chen Y-T, Chiu W-T, Shen M-R. The STIM1-Orai1 pathway of store-operated Ca2+ entry controls the checkpoint in cell cycle G1/S transition. Sci Rep. 2016;6:22142. doi:10.1038/srep22142. PMID:26917047.
  • Selvaraj S, Sun Y, Sukumaran P, Singh BB. Resveratrol activates autophagic cell death in prostate cancer cells via downregulation of STIM1 and the mTOR pathway. Mol Carcinog. 2016;55:818–31. doi:10.1002/mc.22324. PMID:25917875.
  • Singh A, Hildebrand ME, Garcia E, Snutch TP. The transient receptor potential channel antagonist SKF96365 is a potent blocker of low-voltage-activated T-type calcium channels. Br J Pharmacol. 2010;160:1464–75. doi:10.1111/j.1476-5381.2010.00786.x. PMID:20590636.
  • Kondratskyi A, Yassine M, Slomianny C, Kondratska K, Gordienko D, Dewailly E, Lehen'kyi V, Skryma R, Prevarskaya N. Identification of ML-9 as a lysosomotropic agent targeting autophagy and cell death. Cell Death Dis. 2014;5:e1193. doi:10.1038/cddis.2014.156. PMID:24763050.
  • Gusarova GA, Trejo HE, Dada LA, Briva A, Welch LC, Hamanaka RB, Mutlu GM, Chandel NS, Prakriya M, Sznajder JI. Hypoxia leads to Na,K-ATPase downregulation via Ca(2+) release-activated Ca(2+) channels and AMPK activation. Mol Cell Biol. 2011;31:3546–56. doi:10.1128/MCB.05114-11. PMID:21730292.
  • Mungai PT, Waypa GB, Jairaman A, Prakriya M, Dokic D, Ball MK, Schumacker PT. Hypoxia triggers AMPK activation through reactive oxygen species-mediated activation of calcium release-activated calcium channels. Mol Cell Biol. 2011;31:3531–45. doi:10.1128/MCB.05124-11. PMID:21670147.
  • Yang J, Yu J, Li D, Yu S, Ke J, Wang L, Wang Y, Qiu Y, Gao X, Zhang J, et al. Store-operated calcium entry-activated autophagy protects EPC proliferation via the CAMKK2-MTOR pathway in ox-LDL exposure. Autophagy 2017;13:82–98. doi:10.1080/15548627.2016.1245261. PMID:27791458.
  • Yu FH, Catterall WA. Overview of the voltage-gated sodium channel family. Genome Biol. 2003;4:207. doi:10.1186/gb-2003-4-3-207. PMID:12620097.
  • Wemmie JA, Taugher RJ, Kreple CJ. Acid-sensing ion channels in pain and disease. Nat Rev Neurosci. 2013;14:461–71. doi:10.1038/nrn3529. PMID:23783197.
  • Kellenberger S, Schild L. Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol Rev. 2002;82:735–67. doi:10.1152/physrev.00007.2002. PMID:12087134.
  • Cochet-Bissuel M, Lory P, Monteil A. The sodium leak channel, NALCN, in health and disease. Front Cell Neurosci. 2014;8:132. doi:10.3389/fncel.2014.00132. PMID:24904279.
  • Sun X, Cao Y-B, Hu L-F, Yang Y-P, Li J, Wang F, Liu C-F. ASICs mediate the modulatory effect by paeoniflorin on alpha-synuclein autophagic degradation. Brain Res. 2011;1396:77–87. doi:10.1016/j.brainres.2011.04.011. PMID:21529788.
  • Cang C, Zhou Y, Navarro B, Seo Y-J, Aranda K, Shi L, Battaglia-Hsu S, Nissim I, Clapham DE, Ren D. mTOR regulates lysosomal ATP-sensitive two-pore Na(+) channels to adapt to metabolic state. Cell. 2013;152:778–90. doi:10.1016/j.cell.2013.01.023. PMID:23394946.
  • Shieh CC, Coghlan M, Sullivan JP, Gopalakrishnan M. Potassium channels: molecular defects, diseases, and therapeutic opportunities. Pharmacol Rev. 2000;52:557–94. PMID:11121510.
  • Klein B, Wörndl K, Lütz-Meindl U, Kerschbaum HH. Perturbation of intracellular K(+) homeostasis with valinomycin promotes cell death by mitochondrial swelling and autophagic processes. Apoptosis. 2011;16:1101–17. doi:10.1007/s10495-011-0642-9. PMID:21877215.
  • Kim S-H, Choi Y-J, Kim K-Y, Yu S-N, Seo Y-K, Chun S-S, Noh K-T, Suh J-T, Ahn S-C. Salinomycin simultaneously induces apoptosis and autophagy through generation of reactive oxygen species in osteosarcoma U2OS cells. Biochem Biophys Res Commun. 2016;473:607–13. doi:10.1016/j.bbrc.2016.03.132. PMID:27033598.
  • Yu K-Y, Wang Y-P, Wang L-H, Jian Y, Zhao X-D, Chen J-W, Murao K, Zhu W, Dong L, Wang G-Q, et al. Mitochondrial KATP channel involvement in angiotensin II-induced autophagy in vascular smooth muscle cells. Basic Res Cardiol. 2014;109:416. doi:10.1007/s00395-014-0416-y. PMID:24847907.
  • Perez-Neut M, Haar L, Rao V, Santha S, Lansu K, Rana B, Jones WK, Gentile S. Activation of hERG3 channel stimulates autophagy and promotes cellular senescence in melanoma. Oncotarget. 2016;7:21991–2004. doi:10.18632/oncotarget.7831. PMID:26942884.
  • Cang C, Aranda K, Seo Y, Gasnier B, Ren D. TMEM175 Is an Organelle K+ Channel Regulating Lysosomal Function. Cell. 2015;162:1101–12. doi:10.1016/j.cell.2015.08.002. PMID:26317472.
  • Nilius B, Droogmans G. Amazing chloride channels: an overview. Acta Physiol Scand. 2003;177:119–47. doi:10.1046/j.1365-201X.2003.01060.x. PMID:12558550.
  • Duran C, Thompson CH, Xiao Q, Hartzell HC. Chloride channels: often enigmatic, rarely predictable. Annu Rev Physiol 2010; 72:95–121. doi:10.1146/annurev-physiol-021909-135811. PMID:19827947.
  • Zhong J, Kong X, Zhang H, Yu C, Xu Y, Kang J, Yu H, Yi H, Yang X, Sun L. Inhibition of CLIC4 enhances autophagy and triggers mitochondrial and ER stress-induced apoptosis in human glioma U251 cells under starvation. PLoS One. 2012;7:e39378. doi:10.1371/journal.pone.0039378. PMID:22761775.
  • Luciani A, Villella VR, Esposito S, Brunetti-Pierri N, Medina D, Settembre C, Gavina M, Pulze L, Giardino I, Pettoello-Mantovani M, et al. Defective CFTR induces aggresome formation and lung inflammation in cystic fibrosis through ROS-mediated autophagy inhibition. Nat Cell Biol. 2010;12:863–75. doi:10.1038/ncb2090. PMID:20711182.
  • Xia D, Qu L, Li G, Hongdu B, Xu C, Lin X, Lou Y, He Q, Ma D, Chen Y. MARCH2 regulates autophagy by promoting CFTR ubiquitination and degradation and PIK3CA-AKT-MTOR signaling. Autophagy. 2016;12:1614–30. doi:10.1080/15548627.2016.1192752. PMID:27308891.
  • Wang L, Shen M, Guo X, Wang B, Xia Y, Wang N, Zhang Q, Jia L, Wang X. Volume-sensitive outwardly rectifying chloride channel blockers protect against high glucose-induced apoptosis of cardiomyocytes via autophagy activation. Sci Rep. 2017;7:44265. doi:10.1038/srep44265. PMID:28300155.
  • Wartosch L, Fuhrmann JC, Schweizer M, Stauber T, Jentsch TJ. Lysosomal degradation of endocytosed proteins depends on the chloride transport protein ClC-7. FASEB J. 2009;23:4056–68. doi:10.1096/fj.09-130880. PMID:19661288.
  • Graves AR, Curran PK, Smith CL, Mindell JA. The Cl-/H+ antiporter ClC-7 is the primary chloride permeation pathway in lysosomes. Nature. 2008;453:788–92. doi:10.1038/nature06907. PMID:18449189.
  • Stobrawa SM, Breiderhoff T, Takamori S, Engel D, Schweizer M, Zdebik AA, Bösl MR, Ruether K, Jahn H, Draguhn A, et al. Disruption of ClC-3, a chloride channel expressed on synaptic vesicles, leads to a loss of the hippocampus. Neuron. 2001;29:185–96. doi:10.1016/S0896-6273(01)00189-1. PMID:11182090.
  • Su J, Xu Y, Zhou L, Yu H-M, Kang J-S, Liu N, Quan C-S, Sun L-K. Suppression of chloride channel 3 expression facilitates sensitivity of human glioma U251 cells to cisplatin through concomitant inhibition of Akt and autophagy. Anat Rec (Hoboken). 2013;296:595–603. doi:10.1002/ar.22665. PMID:23408563.
  • Westermann B. The mitochondria-plasma membrane contact site. Curr Opin Cell Biol. 2015;35:1–6. doi:10.1016/j.ceb.2015.03.001. PMID:25801776.
  • Okeke E, Dingsdale H, Parker T, Voronina S, Tepikin A V. Endoplasmic reticulum-plasma membrane junctions: structure, function and dynamics. J Physiol. 2016;594:2837–47. doi:10.1113/JP271142. PMID:26939537.
  • Nascimbeni AC, Giordano F, Dupont N, Grasso D, Vaccaro MI, Codogno P, Morel E. ER-plasma membrane contact sites contribute to autophagosome biogenesis by regulation of local PI3P synthesis. EMBO J. 2017;:e201797006.
  • Xu H, Ren D. Lysosomal Physiology. Annu Rev Physiol. 2015;77:57–80. doi:10.1146/annurev-physiol-021014-071649. PMID:25668017.
  • Dimroth P, Kaim G, Matthey U. Crucial role of the membrane potential for ATP synthesis by F(1)F(o) ATP synthases. J Exp Biol. 2000;203:51–9. PMID:10600673.
  • Moreau K, Ravikumar B, Renna M, Puri C, Rubinsztein D. Autophagosome Precursor Maturation Requires Homotypic Fusion. Cell. 2011;146:303–17. doi:10.1016/j.cell.2011.06.023. PMID:21784250.
  • Puri C, Renna M, Bento CF, Moreau K, Rubinsztein DC. Diverse Autophagosome Membrane Sources Coalesce in Recycling Endosomes. Cell. 2013;154:1285–99. doi:10.1016/j.cell.2013.08.044. PMID:24034251.

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