MCOLN1/TRPML1 finely controls oncogenic autophagy in cancer by mediating zinc influx

References

• Dong XP, Cheng X, Mills E, et al. The type IV mucolipidosis-associated protein TRPML1 is an endolysosomal iron release channel. Nature. 2008;455(7215):992–996.
   PubMed Web of Science ®Google Scholar
• Fares H, Greenwald I. Regulation of endocytosis by CUP-5, the Caenorhabditis elegans mucolipin-1 homolog. Nat Genet. 2001;28(1):64–68.
   PubMed Web of Science ®Google Scholar
• Medina DL, Fraldi A, Bouche V, et al. Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev Cell. 2011;21(3):421–430.
   PubMed Web of Science ®Google Scholar
• LaPlante JM, Sun M, Falardeau J, et al. Lysosomal exocytosis is impaired in mucolipidosis type IV. Mol Genet Metab. 2006;89(4):339–348.
   PubMed Web of Science ®Google Scholar
• Wang W, Gao Q, Yang M, 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(11):E1373–81.
   PubMed Web of Science ®Google Scholar
• Pryor PR, Mullock BM, Bright NA, et al. The role of intraorganellar Ca(2+) in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J Cell Biol. 2000;149(5):1053–1062.
   PubMed Web of Science ®Google Scholar
• Luzio JP, Rous BA, Bright NA, et al. Lysosome-endosome fusion and lysosome biogenesis. J Cell Sci. 2000;113(Pt 9):1515–1524.
   PubMed Web of Science ®Google Scholar
• LaPlante JM, Ye CP, Quinn SJ, et al. Functional links between mucolipin-1 and Ca2+-dependent membrane trafficking in mucolipidosis IV. Biochem Biophys Res Commun. 2004;322(4):1384–1391.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ. Autophagy revisited: a conversation with Christian de Duve. Autophagy. 2008;4(6):740–743.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol. 2007;8(11):931–937.
   PubMed Web of Science ®Google Scholar
• Vergarajauregui S, Connelly PS, Daniels MP, et al. Autophagic dysfunction in mucolipidosis type IV patients. Hum Mol Genet. 2008;17(17):2723–2737.
   PubMed Web of Science ®Google Scholar
• Sardiello M, Palmieri M, di Ronza A, et al. A gene network regulating lysosomal biogenesis and function. Science. 2009;325(5939):473–477.
   PubMed Web of Science ®Google Scholar
• Medina DL, Di Paola S, Peluso I, et al. Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat Cell Biol. 2015;17(3):288–299.
   PubMed Web of Science ®Google Scholar
• Schmiege P, Fine M, Blobel G, et al. Human TRPML1 channel structures in open and closed conformations. Nature. 2017;550(7676):366–370.
   PubMed Web of Science ®Google Scholar
• Sahoo N, Gu M, Zhang X, et al. Gastric acid secretion from parietal cells is mediated by a Ca(2+) efflux channel in the tubulovesicle. Dev Cell. 2017;41(3):262–73 e6.
   PubMed Web of Science ®Google Scholar
• Chen CC, Keller M, Hess M, et al. A small molecule restores function to TRPML1 mutant isoforms responsible for mucolipidosis type IV. Nat Commun. 2014;5(1):4681.
   PubMedGoogle Scholar
• Garrity AG, Wang W, Collier CM, et al. The endoplasmic reticulum, not the pH gradient, drives calcium refilling of lysosomes. Elife. 2016;5. DOI:https://doi.org/10.7554/eLife.15887
   Web of Science ®Google Scholar
• Itakura E, Kishi-Itakura C, Mizushima N. The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell. 2012;151(6):1256–1269.
   PubMed Web of Science ®Google Scholar
• McLelland GL, Lee SA, McBride HM, et al. Syntaxin-17 delivers PINK1/parkin-dependent mitochondrial vesicles to the endolysosomal system. J Cell Biol. 2016;214(3):275–291.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Abdel-Aziz AK, Abdelfatah S, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition). Autophagy. 2021;17(1):1–382.
   Web of Science ®Google Scholar
• Zhang X, Cheng X, Yu L, et al. MCOLN1 is a ROS sensor in lysosomes that regulates autophagy. Nat Commun. 2016;7(1):12109.
   PubMedGoogle Scholar
• Wang W, Zhang X, Gao Q, et al. A voltage-dependent K+ channel in the lysosome is required for refilling lysosomal Ca2+ stores. J Cell Biol. 2017;216(6):1715–1730.
   PubMed Web of Science ®Google Scholar
• Elsasser HP, Lehr U, Agricola B, et al. Establishment and characterisation of two cell lines with different grade of differentiation derived from one primary human pancreatic adenocarcinoma. Virchows Arch B Cell Pathol Incl Mol Pathol. 1992;61(1):295–306.
   PubMedGoogle Scholar
• Sugarman BJ, Aggarwal BB, Hass PE, et al. Recombinant human tumor necrosis factor-alpha: effects on proliferation of normal and transformed cells in vitro. Science. 1985;230(4728):943–945.
   PubMed Web of Science ®Google Scholar
• Yamamoto A, Tagawa Y, Yoshimori T, et al. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct. 1998;23(1):33–42.
   PubMed Web of Science ®Google Scholar
• Shen D, Wang X, Xu H. Pairing phosphoinositides with calcium ions in endolysosomal dynamics: phosphoinositides control the direction and specificity of membrane trafficking by regulating the activity of calcium channels in the endolysosomes. Bioessays. 2011;33(6):448–457.
   PubMed Web of Science ®Google Scholar
• Malhotra R, Warne JP, Salas E, et al. Loss of Atg12, but not Atg5, in pro-opiomelanocortin neurons exacerbates diet-induced obesity. Autophagy. 2015;11(1):145–154.
   PubMed Web of Science ®Google Scholar
• 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(52):43218–43223.
   PubMed Web of Science ®Google Scholar
• Dong XP, Shen D, Wang X, et al. PI(3,5)P(2) controls membrane trafficking by direct activation of mucolipin Ca(2+) release channels in the endolysosome. Nat Commun. 2010;1(1):38.
   PubMedGoogle Scholar
• Yoon YH, Cho KS, Hwang JJ, et al. Induction of lysosomal dilatation, arrested autophagy, and cell death by chloroquine in cultured ARPE-19 cells. Invest Ophthalmol Vis Sci. 2010;51(11):6030–6037.
   PubMed Web of Science ®Google Scholar
• Ni HM, Bockus A, Wozniak AL, et al. Dissecting the dynamic turnover of GFP-LC3 in the autolysosome. Autophagy. 2011;7(2):188–204.
   PubMed Web of Science ®Google Scholar
• Lee SB, Kim S, Lee J, et al. ATG1, an autophagy regulator, inhibits cell growth by negatively regulating S6 kinase. EMBO Rep. 2007;8(4):360–365.
   PubMed Web of Science ®Google Scholar
• Nyfeler B, Bergman P, Triantafellow E, et al. Relieving autophagy and 4EBP1 from rapamycin resistance. Mol Cell Biol. 2011;31(14):2867–2876.
   PubMed Web of Science ®Google Scholar
• Bach M, Larance M, James DE, et al. The serine/threonine kinase ULK1 is a target of multiple phosphorylation events. Biochem J. 2011;440(2):283–291.
   PubMed Web of Science ®Google Scholar
• Kang SA, Pacold ME, Cervantes CL, et al. mTORC1 phosphorylation sites encode their sensitivity to starvation and rapamycin. Science. 2013;341(6144):1236566.
   PubMed Web of Science ®Google Scholar
• Xu H, Ren D. Lysosomal physiology. Annu Rev Physiol. 2015;77(1):57–80.
   PubMedGoogle Scholar
• Radford RJ, Lippard SJ. Chelators for investigating zinc metalloneurochemistry. Curr Opin Chem Biol. 2013;17(2):129–136.
   PubMed Web of Science ®Google Scholar
• Schatten H, Eisenstark A. Salmonella: methods and protocols. Methods Mol Biol. 2007;394:v–vi.
   PubMedGoogle Scholar
• Tsien RY. New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry. 1980;19(11):2396–2404.
   PubMed Web of Science ®Google Scholar
• Chouyyok W, Yantasee W, Shin Y, et al. Transition metal ion capture using functional mesoporous carbon made with 1,10-phenanthroline. Inorg Chem Commun. 2009;12(11):1099–1103.
   PubMed Web of Science ®Google Scholar
• Smirnova J, Kabin E, Jarving I, et al. Copper(I)-binding properties of de-coppering drugs for the treatment of Wilson disease. alpha-Lipoic acid as a potential anti-copper agent. Sci Rep. 2018;8(1):1463.
   PubMedGoogle Scholar
• Khan G, Merajver S. Copper chelation in cancer therapy using tetrathiomolybdate: an evolving paradigm. Expert Opin Investig Drugs. 2009;18(4):541–548.
   PubMed Web of Science ®Google Scholar
• Kontoghiorghe CN, Kontoghiorghes GJ. Efficacy and safety of iron-chelation therapy with deferoxamine, deferiprone, and deferasirox for the treatment of iron-loaded patients with non-transfusion-dependent thalassemia syndromes. Drug Des Devel Ther. 2016;10:465–481.
   PubMed Web of Science ®Google Scholar
• Heath JL, Weiss JM, Lavau CP, et al. Iron deprivation in cancer–potential therapeutic implications. Nutrients. 2013;5(8):2836–2859.
   PubMed Web of Science ®Google Scholar
• Planalp RP, Przyborowska AM, Park G, et al. Novel cytotoxic chelators that bind iron(II) selectively over zinc(II) under aqueous aerobic conditions. Biochem Soc Trans. 2002;30(4):758–762.
   PubMedGoogle Scholar
• Schwiebert EM, Liang L, Cheng NL, et al. Extracellular zinc and ATP-gated P2X receptor calcium entry channels: new zinc receptors as physiological sensors and therapeutic targets. Purinergic Signal. 2005;1(4):299–310.
   PubMedGoogle Scholar
• Eichelsdoerfer JL, Evans JA, Slaugenhaupt SA, et al. Zinc dyshomeostasis is linked with the loss of mucolipidosis IV-associated TRPML1 ion channel. J Biol Chem. 2010;285(45):34304–34308.
   PubMed Web of Science ®Google Scholar
• Kukic I, Lee JK, Coblentz J, et al. Zinc-dependent lysosomal enlargement in TRPML1-deficient cells involves MTF-1 transcription factor and ZnT4 (Slc30a4) transporter. Biochem J. 2013;451(2):155–163.
   PubMedGoogle Scholar
• Minckley TF, Zhang C, Fudge DH, et al. Sub-nanomolar sensitive GZnP3 reveals TRPML1-mediated neuronal Zn(2+) signals. Nat Commun. 2019;10(1):4806.
   PubMedGoogle Scholar
• Oyama TM, Ishida S, Okano Y, et al. Clioquinol-induced increase and decrease in the intracellular Zn2+ level in rat thymocytes. Life Sci. 2012;91(23–24):1216–1220.
   PubMed Web of Science ®Google Scholar
• Mathew R, Karantza-Wadsworth V, White E. Role of autophagy in cancer. Nat Rev Cancer. 2007;7(12):961–967.
   PubMed Web of Science ®Google Scholar
• Lotze MT, Maranchie J, Appleman L. Inhibiting autophagy: a novel approach for the treatment of renal cell carcinoma. Cancer J. 2013;19(4):341–347.
   PubMed Web of Science ®Google Scholar
• Chude CI, Amaravadi RK. Targeting autophagy in cancer: update on clinical trials and novel inhibitors. Int J Mol Sci. 2017;18(6). DOI:https://doi.org/10.3390/ijms18061279
   PubMed Web of Science ®Google Scholar
• Yang S, Wang X, Contino G, et al. Pancreatic cancers require autophagy for tumor growth. Genes Dev. 2011;25(7):717–729.
   PubMed Web of Science ®Google Scholar
• Garbar C, Mascaux C, Giustiniani J, et al. Chemotherapy treatment induces an increase of autophagy in the luminal breast cancer cell MCF7, but not in the triple-negative MDA-MB231. Sci Rep. 2017;7(1):7201.
   PubMedGoogle Scholar
• Cota D, Proulx K, Smith KA, et al. Hypothalamic mTOR signaling regulates food intake. Science. 2006;312(5775):927–930.
   PubMed Web of Science ®Google Scholar
• Ouyang H, Mou L, Luk C, et al. Immortal human pancreatic duct epithelial cell lines with near normal genotype and phenotype. Am J Pathol. 2000;157(5):1623–1631.
   PubMed Web of Science ®Google Scholar
• Miedel MT, Rbaibi Y, Guerriero CJ, et al. Membrane traffic and turnover in TRP-ML1-deficient cells: a revised model for mucolipidosis type IV pathogenesis. J Exp Med. 2008;205(6):1477–1490.
   PubMed Web of Science ®Google Scholar
• Maiuri MC, Zalckvar E, Kimchi A, et al. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol. 2007;8(9):741–752.
   PubMed Web of Science ®Google Scholar
• Slee EA, Zhu H, Chow SC, et al. Benzyloxycarbonyl-Val-Ala-Asp (OMe) fluoromethylketone (Z-VAD.FMK) inhibits apoptosis by blocking the processing of CPP32. Biochem J. 1996;315(1):21–24.
   PubMedGoogle Scholar
• 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(5):511–524.
   PubMed Web of Science ®Google Scholar
• Cheng X, Zhang X, Gao Q, et al. The intracellular Ca(2)(+) channel MCOLN1 is required for sarcolemma repair to prevent muscular dystrophy. Nat Med. 2014;20(10):1187–1192.
   PubMed Web of Science ®Google Scholar
• Scotto Rosato A, Montefusco S, Soldati C, et al. TRPML1 links lysosomal calcium to autophagosome biogenesis through the activation of the CaMKKbeta/VPS34 pathway. Nat Commun. 2019;10:5630.
   PubMed Web of Science ®Google Scholar
• Zhang X, Chen W, Gao Q, et al. Rapamycin directly activates lysosomal mucolipin TRP channels independent of mTOR. PLoS Biol. 2019;17(5):e3000252.
   PubMed Web of Science ®Google Scholar
• Sun X, Yang Y, Zhong XZ, et al. A negative feedback regulation of MTORC1 activity by the lysosomal Ca2+ channel MCOLN1 (mucolipin 1) using a CALM (calmodulin)-dependent mechanism. Autophagy. 2018;14(1):38–52.
   PubMed Web of Science ®Google Scholar
• Abiria SA, Krapivinsky G, Sah R, et al. TRPM7 senses oxidative stress to release Zn2+ from unique intracellular vesicles. Proc Natl Acad Sci U S A. 2017;114(30):E6079–E88.
   PubMed Web of Science ®Google Scholar
• Kochanczyk T, Drozd A, Krezel A. Relationship between the architecture of zinc coordination and zinc binding affinity in proteins–insights into zinc regulation. Metallomics. 2015;7(2):244–257.
   PubMed Web of Science ®Google Scholar
• Barth J, Zimmermann H, Volknandt W. SV31 is a Zn2+-binding synaptic vesicle protein. J Neurochem. 2011;118(4):558–570.
   PubMed Web of Science ®Google Scholar
• Lorincz P, Juhasz G. Autophagosome-Lysosome Fusion. J Mol Biol. 2020;432(8):2462–2482.
   PubMed Web of Science ®Google Scholar
• Jiang P, Nishimura T, Sakamaki Y, et al. The HOPS complex mediates autophagosome-lysosome fusion through interaction with syntaxin 17. Mol Biol Cell. 2014;25(8):1327–1337.
   PubMed Web of Science ®Google Scholar
• Hunter MR, Scourfield EJ, Emmott E, et al. VPS18 recruits VPS41 to the human HOPS complex via a RING-RING interaction. Biochem J. 2017;474(21):3615–3626.
   PubMedGoogle Scholar
• Chimienti F, Aouffen M, Favier A, et al. Zinc homeostasis-regulating proteins: new drug targets for triggering cell fate. Curr Drug Targets. 2003;4(4):323–338.
   PubMed Web of Science ®Google Scholar
• Dar AA, Belkhiri A, Ecsedy J, et al. Aurora kinase A inhibition leads to p73-dependent apoptosis in p53-deficient cancer cells. Cancer Res. 2008;68(21):8998–9004.
   PubMed Web of Science ®Google Scholar
• Cerny J, Feng Y, Yu A, et al. The small chemical vacuolin-1 inhibits Ca2+-dependent lysosomal exocytosis but not cell resealing. EMBO Rep. 2004;5(9):883–888.
   PubMed Web of Science ®Google Scholar
• Yue W, Hamai A, Tonelli G, et al. Inhibition of the autophagic flux by salinomycin in breast cancer stem-like/progenitor cells interferes with their maintenance. Autophagy. 2013;9(5):714–729.
   PubMed Web of Science ®Google Scholar