Acknowledgement
This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. 2021R1C1C1012076) and by the Chung-Ang University Research Grants in 2020.
References
- Di Resta C and Becchetti A (2010) Introduction to ion channels. Adv Exp Med Biol 674, 9-21 https://doi.org/10.1007/978-1-4419-6066-5_2
- Clapham DE (1995) Calcium signaling. Cell 80, 259-268 https://doi.org/10.1016/0092-8674(95)90408-5
- Hetherington AM and Brownlee C (2004) The generation of Ca(2+) signals in plants. Annu Rev Plant Biol 55, 401-427 https://doi.org/10.1146/annurev.arplant.55.031903.141624
- Pandey GK, Cheong YH, Kim KN et al (2004) The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell 16, 1912-1924 https://doi.org/10.1105/tpc.021311
- Dodd AN, Kudla J and Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61, 593-620 https://doi.org/10.1146/annurev-arplant-070109-104628
- Berridge MJ, Bootman MD and Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4, 517-529 https://doi.org/10.1038/nrm1155
- Singh S, Dodt J, Volkers P et al (2019) Structure functional insights into calcium binding during the activation of coagulation factor XIII A. Sci Rep 9, 11324
- Cashman KD (2002) Calcium intake, calcium bioavailability and bone health. Br J Nutr 87 Suppl 2, S169-177 https://doi.org/10.1079/BJN/2002534
- Balaban RS (2009) The role of Ca2+ signaling in the coordination of mitochondrial ATP production with cardiac work. Biochim Biophys Acta 1787, 1334-1341 https://doi.org/10.1016/j.bbabio.2009.05.011
- Denton RM (2009) Regulation of mitochondrial dehydrogenases by calcium ions. Biochim Biophys Acta 1787, 1309-1316 https://doi.org/10.1016/j.bbabio.2009.01.005
- Orrenius S, Zhivotovsky B and Nicotera P (2003) Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 4, 552-565 https://doi.org/10.1038/nrm1150
- Szalai G, Krishnamurthy R and Hajnoczky G (1999) Apoptosis driven by IP(3)-linked mitochondrial calcium signals. EMBO J 18, 6349-6361 https://doi.org/10.1093/emboj/18.22.6349
- Pinton P, Ferrari D, Rapizzi E, Di Virgilio F, Pozzan T and Rizzuto R (2001) The Ca2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: significance for the molecular mechanism of Bcl-2 action. EMBO J 20, 2690-2701 https://doi.org/10.1093/emboj/20.11.2690
- Scorrano L, Oakes SA, Opferman JT et al (2003) BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 300, 135-139 https://doi.org/10.1126/science.1081208
- Chernorudskiy AL and Zito E (2017) Regulation of calcium homeostasis by ER redox: a close-up of the ER/mitochondria connection. J Mol Biol 429, 620-632 https://doi.org/10.1016/j.jmb.2017.01.017
- Bustos G, Ahumada-Castro U, Silva-Pavez E, Puebla A, Lovy A and Cesar Cardenas J (2021) The ER-mitochondria Ca2+ signaling in cancer progression: Fueling the monster. Int Rev Cell Mol Biol 363, 49-121
- Ahumada-Castro U, Puebla-Huerta A, Cuevas-Espinoza V, Lovy A and Cardenas JC (2021) Keeping zombies alive: The ER-mitochondria Ca2+ transfer in cellular senescence. Biochim Biophys Acta Mol Cell Res 1868, 119099
- Smaili SS, Pereira GJ, Costa MM et al (2013) The role of calcium stores in apoptosis and autophagy. Curr Mol Med 13, 252-265 https://doi.org/10.2174/156652413804810772
- Kaufman RJ and Malhotra JD (2014) Calcium trafficking integrates endoplasmic reticulum function with mitochondrial bioenergetics. Biochim Biophys Acta 1843, 2233-2239 https://doi.org/10.1016/j.bbamcr.2014.03.022
- Duchen MR, Verkhratsky A and Muallem S (2008) Mitochondria and calcium in health and disease. Cell Calcium 44, 1-5 https://doi.org/10.1016/j.ceca.2008.02.001
- East DA and Campanella M (2013) Ca2+ in quality control: an unresolved riddle critical to autophagy and mitophagy. Autophagy 9, 1710-1719 https://doi.org/10.4161/auto.25367
- Gottlieb RA and Bernstein D (2016) Mitochondrial remodeling: Rearranging, recycling, and reprogramming. Cell Calcium 60, 88-101 https://doi.org/10.1016/j.ceca.2016.04.006
- Crompton M, Kunzi M and Carafoli E (1977) The calcium-induced and sodium-induced effluxes of calcium from heart mitochondria. Evidence for a sodium-calcium carrier. Eur J Biochem 79, 549-558 https://doi.org/10.1111/j.1432-1033.1977.tb11839.x
- Palty R, Silverman WF, Hershfinkel M et al (2010) NCLX is an essential component of mitochondrial Na+/Ca2+ exchange. Proc Natl Acad Sci U S A 107, 436-441 https://doi.org/10.1073/pnas.0908099107
- Jiang D, Zhao L and Clapham DE (2009) Genome-wide RNAi screen identifies Letm1 as a mitochondrial Ca2+/H+ antiporter. Science 326, 144-147 https://doi.org/10.1126/science.1175145
- Kirichok Y, Krapivinsky G and Clapham DE (2004) The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427, 360-364 https://doi.org/10.1038/nature02246
- Baughman JM, Perocchi F, Girgis HS et al (2011) Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476, 341-345 https://doi.org/10.1038/nature10234
- De Stefani D, Raffaello A, Teardo E, Szabo I and Rizzuto R (2011) A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476, 336-340 https://doi.org/10.1038/nature10230
- Perocchi F, Gohil VM, Girgis HS et al (2010) MICU1 encodes a mitochondrial EF hand protein required for Ca2+ uptake. Nature 467, 291-296 https://doi.org/10.1038/nature09358
- Plovanich M, Bogorad RL, Sancak Y et al (2013) MICU2, a paralog of MICU1, resides within the mitochondrial uniporter complex to regulate calcium handling. PLoS One 8, e55785
- Sancak Y, Markhard AL, Kitami T et al (2013) EMRE is an essential component of the mitochondrial calcium uniporter complex. Science 342, 1379-1382 https://doi.org/10.1126/science.1242993
- Bick AG, Calvo SE and Mootha VK (2012) Evolutionary diversity of the mitochondrial calcium uniporter. Science 336, 886
- Kamer KJ and Mootha VK (2015) The molecular era of the mitochondrial calcium uniporter. Nat Rev Mol Cell Biol 16, 545-553 https://doi.org/10.1038/nrm4039
- Baradaran R, Wang C, Siliciano AF and Long SB (2018) Cryo-EM structures of fungal and metazoan mitochondrial calcium uniporters. Nature 559, 580-584 https://doi.org/10.1038/s41586-018-0331-8
- Fan C, Fan M, Orlando BJ et al (2018) X-ray and cryo-EM structures of the mitochondrial calcium uniporter. Nature 559, 575-579 https://doi.org/10.1038/s41586-018-0330-9
- Nguyen NX, Armache JP, Lee C et al (2018) Cryo-EM structure of a fungal mitochondrial calcium uniporter. Nature 559, 570-574 https://doi.org/10.1038/s41586-018-0333-6
- Yoo J, Wu M, Yin Y, Herzik MA Jr, Lander GC and Lee SY (2018) Cryo-EM structure of a mitochondrial calcium uniporter. Science 361, 506-511 https://doi.org/10.1126/science.aar4056
- Oxenoid K, Dong Y, Cao C et al (2016) Architecture of the mitochondrial calcium uniporter. Nature 533, 269-273 https://doi.org/10.1038/nature17656
- Cao C, Wang S, Cui T, Su XC and Chou JJ (2017) Ion and inhibitor binding of the double-ring ion selectivity filter of the mitochondrial calcium uniporter. Proc Natl Acad Sci U S A 114, E2846-E2851
- Paillard M, Csordas G, Huang KT, Varnai P, Joseph SK and Hajnoczky G (2018) MICU1 interacts with the D-ring of the MCU pore to control its Ca2+ flux and sensitivity to Ru360. Mol Cell 72, 778-785 e773
- Wang Y, Nguyen NX, She J et al (2019) Structural Mechanism of EMRE-Dependent Gating of the Human Mitochondrial Calcium Uniporter. Cell 177, 1252-1261 e1213
- Lee SK, Shanmughapriya S, Mok MCY et al (2016) Structural insights into mitochondrial calcium uniporter regulation by divalent cations. Cell Chem Biol 23, 1157-1169 https://doi.org/10.1016/j.chembiol.2016.07.012
- Yuan Y, Cao C, Wen M et al (2020) Structural characterization of the N-terminal domain of the Dictyostelium discoideum mitochondrial calcium uniporter. ACS Omega 5, 6452-6460 https://doi.org/10.1021/acsomega.9b04045
- Van Keuren AM, Tsai CW, Balderas E, Rodriguez MX, Chaudhuri D and Tsai MF (2020) Mechanisms of EMRE-dependent MCU opening in the mitochondrial calcium uniporter complex. Cell Rep 33, 108486
- Raffaello A, De Stefani D, Sabbadin D et al (2013) The mitochondrial calcium uniporter is a multimer that can include a dominant-negative pore-forming subunit. EMBO J 32, 2362-2376 https://doi.org/10.1038/emboj.2013.157
- Lambert JP, Luongo TS, Tomar D et al (2019) MCUB regulates the molecular composition of the mitochondrial calcium uniporter channel to limit mitochondrial calcium overload during stress. Circulation 140, 1720-1733 https://doi.org/10.1161/CIRCULATIONAHA.118.037968
- Mallilankaraman K, Cardenas C, Doonan PJ et al (2012) MCUR1 is an essential component of mitochondrial Ca2+ uptake that regulates cellular metabolism. Nat Cell Biol 14, 1336-1343 https://doi.org/10.1038/ncb2622
- Patron M, Granatiero V, Espino J, Rizzuto R and De Stefani D (2019) MICU3 is a tissue-specific enhancer of mitochondrial calcium uptake. Cell Death Differ 26, 179-195 https://doi.org/10.1038/s41418-018-0113-8
- Paupe V, Prudent J, Dassa EP, Rendon OZ and Shoubridge EA (2015) CCDC90A (MCUR1) is a cytochrome c oxidase assembly factor and not a regulator of the mitochondrial calcium uniporter. Cell Metab 21, 109-116 https://doi.org/10.1016/j.cmet.2014.12.004
- Csordas G, Golenar T, Seifert EL et al (2013) MICU1 controls both the threshold and cooperative activation of the mitochondrial Ca2+ uniporter. Cell Metab 17, 976-987 https://doi.org/10.1016/j.cmet.2013.04.020
- Mallilankaraman K, Doonan P, Cardenas C et al (2012) MICU1 is an essential gatekeeper for MCU-mediated mitochondrial Ca2+ uptake that regulates cell survival. Cell 151, 630-644 https://doi.org/10.1016/j.cell.2012.10.011
- Tsai MF, Phillips CB, Ranaghan M et al (2016) Dual functions of a small regulatory subunit in the mitochondrial calcium uniporter complex. Elife 5, e15545
- Pittis AA, Goh V, Cebrian-Serrano A, Wettmarshausen J, Perocchi F and Gabaldon T (2020) Discovery of EMRE in fungi resolves the true evolutionary history of the mitochondrial calcium uniporter. Nat Commun 11, 4031
- Kamer KJ and Mootha VK (2014) MICU1 and MICU2 play nonredundant roles in the regulation of the mitochondrial calcium uniporter. EMBO Rep 15, 299-307 https://doi.org/10.1002/embr.201337946
- Patron M, Checchetto V, Raffaello A et al (2014) MICU1 and MICU2 finely tune the mitochondrial Ca2+ uniporter by exerting opposite effects on MCU activity. Mol Cell 53, 726-737 https://doi.org/10.1016/j.molcel.2014.01.013
- Fan M, Zhang J, Tsai CW et al (2020) Structure and mechanism of the mitochondrial Ca2+ uniporter holocomplex. Nature 582, 129-133 https://doi.org/10.1038/s41586-020-2309-6
- Wu W, Shen Q, Zhang R et al (2020) The structure of the MICU1-MICU2 complex unveils the regulation of the mitochondrial calcium uniporter. EMBO J 39, e104285
- Wang C, Jacewicz A, Delgado BD, Baradaran R and Long SB (2020) Structures reveal gatekeeping of the mitochondrial Ca2+ uniporter by MICU1-MICU2. Elife 9, e59991