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Taxonomic Features of Specific Ca2+ Transport Mechanisms in Mitochondria

  • M. V. DubininEmail author
  • K. N. Belosludtsev
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Abstract

Mitochondria play an important role in the regulation of intracellular Ca2+ homeostasis in Eukaryotes. Progress in the development of molecular and genetic methods for the study of living systems made it possible to identify the structures that carry specific Ca2+ transport in mitochondria, including Ca2+ uniporter (MCU), Na+/Ca2+ exchanger (NCLX) and Ca2+/H+ antiporter (Letm1). The study of the architecture and functioning of these systems at different levels of the organization of living organisms can provide insight into the origin and evolution of the systems of Ca2+ homeostasis and also reveal general mechanisms of regulation and control of these systems in normal and pathological conditions. This review is focused on the taxonomic features of the structure and functioning of specific calcium transport systems in eukaryotic mitochondria and provides evidence of the presence of homologous structures in prokaryotic organisms.

Keywords:

mitochondria Ca2+ transport Ca2+ uniporter Na+/Ca2+ exchanger evolutionary biochemistry 

Notes

ACKNOWLEDGMENTS

The work was supported by the Russian Science Foundation (project no. 18-75-00011, Chapter 1), Russian Foundation for Basic Research (project no. 18-315-20011), and Ministry of Education and Science of the Russian Federation (State Task no. 6.5170.2017/8.9).

COMPLIANCE WITH ETHICAL STANDARDS

The authors declare that they have no conflict of interest.

This article does not contain any studies involving animals or human participants performed by any of the authors.

REFERENCES

  1. 1.
    Jiang D., Zhao L., Clapham D.E. 2009. Genome-wide RNAi screen identifies Letm1 as a mitochondrial Ca2+/H+ antiporter. Science. 326, 144–147.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Palty R., Silverman W.F., Hershfinkel M., Caporale T., Sensi S.L., Parnis J., Nolte C., Fishman D., Shoshan-Barmatz V., Herrmann S., Khananshvili D., Sekler I. 2010. NCLX is an essential component of mitochondrial Na+/Ca2+ exchange. Proc. Natl. Acad Sci. USA. 107, 436–441.CrossRefPubMedGoogle Scholar
  3. 3.
    Perocchi F., Gohil V.M., Girgis H.S., Bao X.R., McCombs J.E., Palmer A.E., Mootha V.K. 2010. MICU1 encodes a mitochondrial EF hand protein required for Ca2+ uptake. Nature. 467, 291–296.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    De Stefani D., Raffaello A., Teardo E., Szabo I., Rizzuto R. 2011. A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature. 476, 336–340.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Raffaello A., De Stefani D., Sabbadin D., Teardo E., Merli G., Picard A., Checchetto V., Moro S., Szabo I., Rizzuto R. 2013.The mitochondrial calcium uniporter is a multimer that can include a dominant-negative pore-forming subunit. EMBO J. 32, 2362–2376.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Plovanich M., Bogorad R.L., Sancak Y., Kamer K.J., Strittmatter L., Li A.A., Girgis H.S., Kuchimanchi S., De Groot J., Speciner L., Taneja N., Oshea J., Koteliansky V., Mootha V.K. 2013. MICU2, a paralog of MICU1, resides within the mitochondrial uniporter complex to regulate calcium handling. PLoS ONE. 8, e55785.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Mallilankaraman K., Cardenas C., Doonan P.J., Chandramoorthy H.C., Irrinki K.M., Golenar T., Csordas G., Madireddi P., Yang J., Müller M., Miller R., Kolesar J.E., Molgo J., Kaufman B., Hajnoczky G., Foskett J.K., Madesh M. 2012. MCUR1 is an essential component of mitochondrial Ca2+ uptake that regulates cellular metabolism. Nat. Cell Biol. 14, 1336–1343.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Sancak Y., Markhard A.L., Kitami T., Kovacs-Bogdan E., Kame K.J., Udeshi N.D., Carr S.A., Chaudhuri D., Clapham D.E., Li A.A., Calvo S.E., Goldberger O., Mootha V.K. 2013. EMRE is an essential component of the mitochondrial calcium uniporter complex. Science. 342, 1379‒1382.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Hoffman N.E., Chandramoorthy H.C., Shanmughapriya S., Zhang X.Q., Vallem S., Doonan P.J., Malliankaraman K., Guo S., Rajan S., Elrod J.W., Koch W.J., Cheung J.Y., Madesh M. 2014. SLC25A23 augments mitochondrial Ca2+ uptake, interacts with MCU, and induces oxidative stress-mediated cell death. Mol. Biol. Cell. 25, 936–947.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Halestrap A.P., Richardson A.P. 2015. The mitochondrial permeability transition: A current perspective on its identity and role in ischaemia/reperfusion injury. J. Mol. Cell Cardiol. 78, 129‒141.CrossRefPubMedGoogle Scholar
  11. 11.
    Briston T., Selwood D.L., Szabadkai G., Duchen M.R. 2019. Mitochondrial permeability transition: A molecular lesion with multiple drug targets. Trends Pharmacol. Sci. 40, 50‒70.CrossRefPubMedGoogle Scholar
  12. 12.
    Bick A.G., Calvo S.E., Mootha V.K. 2012. Evolutionary diversity of the mitochondrial calcium uniporter. Science. 336, 886.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Marchi S., Pinton P. 2014. The mitochondrial calcium uniporter complex: Molecular components, structure and physiopathological implications. J. Physiol. 592, 829‒839.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Carafoli E., Lehninger A.L. 1971. A survey of the interaction of calcium ions with mitochondria from different tissues and species. Biochem. J. 122, 681–690.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Toninello A., Salvi M., Colombo L. 2000. The membrane permeability transition in liver mitochondria of the great green goby Zosterisessor ophiocephalus (Pallas). J. Exp. Biol. 203, 3425‒3434.PubMedGoogle Scholar
  16. 16.
    Azzolin L., Basso E., Argenton F., Bernardi P. 2010. Mitochondrial Ca2+ transport and permeability transition in zebrafish (Danio rerio). Biochim. Biophys. Acta. 1797, 1775‒1779.CrossRefPubMedGoogle Scholar
  17. 17.
    Vedernikov A.A., Dubinin M.V., Zabiakin V.A., Samartsev V.N. 2015. Ca2+-dependent nonspecific permeability of the inner membrane of liver mitochondria in the guinea fowl (Numida meleagris). J. Bioenerg. Biomembr. 47, 235‒242.CrossRefPubMedGoogle Scholar
  18. 18.
    Deryabina Y.I., Isakova E.P., Zvyagilskaya R.A. 2004. Mitochondrial calcium transport systems: Properties, regulation, and taxonomic features. Biokhimiya (Rus.). 69 (1), 114‒127.Google Scholar
  19. 19.
    De Stefani D., Rizzuto R., Pozzan T. 2016. Enjoy the trip: Calcium in mitochondria back and forth. Annu. Rev. Biochem. 85, 161‒192.CrossRefPubMedGoogle Scholar
  20. 20.
    Dubinin M.V., Vedernikov A.A., Khoroshavina E.I., Adakeeva S.I., Samartsev V.N. 2015. Induction of calcium-dependent nonspecific permeability of the inner membrane in liver mitochondria of mammals and birds: A comparative study. Biol. membrany (Rus.). 32 (5‒6), 328‒337.Google Scholar
  21. 21.
    Brustovetsky N.N., Egorova M.V., Grishina E.V., Mayevsky E.I. 1992. Analysis of the causes of the suppression of oxidative phosphorylation and energy-dependent cationic transport into liver mitochondria of hibernating gophers, Citellus undulatus. Comp. Biochem. Physiol. B. 103, 755‒758.CrossRefPubMedGoogle Scholar
  22. 22.
    Hansford R.G. 1971. Some properties of mitochondria isolated from the flight muscle of the periodical cicada, Magicicada septendecim. Biochem. J. 121, 771‒780.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    von Stockum S., Basso E., Petronilli V., Sabatelli P., Forte M.A., Bernardi P. 2011. Properties of Ca2+ transport in mitochondria of Drosophila melanogaster. J. Biol. Chem. 286, 41163‒41170.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Choi S., Quan X., Bang S., Yoo H., Kim J., Park J., Park K.S., Chung J. 2017. Mitochondrial calcium uniporter in Drosophila transfers calcium between the endoplasmic reticulum and mitochondria in oxidative stress-induced cell death. J. Biol. Chem. 292, 14473‒14485.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    M’Angale P.G., Staveley B.E. 2017. Inhibition of mitochondrial calcium uptake 1 in Drosophila neurons. Genet. Mol. Res. 16, gmr16019436.CrossRefGoogle Scholar
  26. 26.
    Menze M.A., Hutchinson K., Laborde S.M., Hand S.C. 2005. Mitochondrial permeability transition in the crustacean Artemia franciscana: Absence of a calcium-regulated pore in the face of profound calcium storage. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, 68‒76.CrossRefGoogle Scholar
  27. 27.
    Holman J.D., Hand S.C. 2009. Metabolic depression is delayed and mitochondrial impairment averted during prolonged anoxia in the ghost shrimp, Lepidophthalmus louisianensis (Schmitt, 1935). J. Exp. Mar. Biol. Ecol. 376, 85‒93.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Mammucari C., Raffaello A., Vecellio Reane D., Rizzuto R. 2016. Molecular structure and pathophysiological roles of the mitochondrial calcium uniporter. Biochim. Biophys. Acta. 1863, 2457‒2464.CrossRefPubMedGoogle Scholar
  29. 29.
    Vercesi A.E., Macedo D.V., Lima S.A., Gadelha F.R., Docampo R. 1990. Ca2+ transport in digitonin-permeabilized trypanosomatids. Mol. Biochem. Parasitol. 42, 119‒124.CrossRefPubMedGoogle Scholar
  30. 30.
    Vercesi A.E., Docampo R. 1992. Ca2+ transport by digitonin-permeabilized Leishmania donovani. Effects of Ca2+, pentamidine and WR-6026 on mitochondrial membrane potential in situ. Biochem. J. 284, 463‒467.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Moreno S.N., Vercesi A.E., Pignataro O.P., Docampo R. 1992. Calcium homeostasis in Trypanosoma cruzi amastigotes: Presence of inositol phosphates and lack of an inositol 1,4,5-trisphosphate-sensitive calcium pool. Mol. Biochem. Parasitol. 52, 251‒261.CrossRefPubMedGoogle Scholar
  32. 32.
    Sodre C.L., Moreira B.L., Nobrega F.B., Gadelha F.R., Meyer-Fernandes J.R., Dutra P.M., Vercesi A.E., Lopes A.H., Scofano H.M., Barrabin H. 2000. Characterization of the intracellular Ca2+ pools involved in the calcium homeostasis in Herpetomonas sp. Promastigotes. Arch. Biochem. Biophys. 380, 85‒91.CrossRefPubMedGoogle Scholar
  33. 33.
    Benaim G., Bermudez R., Urbina J.A. 1990. Ca2+ transport in isolated mitochondrial vesicles from Leishmania braziliensis Promastigotes. Mol. Biochem. Parasitol. 39, 61‒68.CrossRefPubMedGoogle Scholar
  34. 34.
    Docampo R., Vercesi A.E., Huang G. 2014. Mitochondrial calcium transport in trypanosomes. Mol. Biochem. Parasitol. 196, 108‒116.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Huang G., Docampo R. 2018. The mitochondrial Ca2+ uniporter complex (MCUC) of Trypanosoma brucei is a hetero-oligomer that contains novel subunits essential for Ca2+ uptake. MBio. 9, e01700‒18.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Chiurillo M.A., Lander N., Bertolini M.S., Storey M., Vercesi A.E., Docampo R. 2017. Different roles of mitochondrial calcium uniporter complex subunits in growth and infectivity of Trypanosoma cruzi. MBio. 8, e00574‒17.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Uribe S., Rangel P., Pardo J.P. 1992. Interactions of calcium with yeast mitochondria. Cell Calcium. 13, 211‒217.CrossRefPubMedGoogle Scholar
  38. 38.
    Kovaleva M.V., Sukhanova E.I., Trendeleva T.A., Popova K.M., Zylkova M.V., Uralskaya L.A., Zvyagilskaya R.A. 2010. Induction of permeability of the inner membrane of yeast mitochondria. Biokhimiya (Rus). 75 (3), 365‒372.Google Scholar
  39. 39.
    Zvyagilskaya R.A., Zelenshchikova V.A., Burbaev D.Sh. 1983. Reverse electron transfer in mitochondria of the yeast Endomyces magnusii grown on sucrose. Biokhimiya (Rus.). 48 (1), 3‒10.Google Scholar
  40. 40.
    Bazhenova E.N., Saris N.-E.L., Zvyagilskaya R.A. 1998. Stimulation of the yeast mitochondrial calcium uniporter by hypotonicity and by ruthenium red. Biochim. Biophys. Acta. 1371, 96‒100.CrossRefPubMedGoogle Scholar
  41. 41.
    Hodges T.K., Hanson J.B. 1965. Calcium accumulation by maize mitochondria. Plant Physiol. 40, 101‒109.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Dieter P., Marme D. 1980. Ca2+ transport in mitochondrial and microsomal fractions from higher plants. Planta. 150, 1‒8.CrossRefPubMedGoogle Scholar
  43. 43.
    Akerman K.E., Moore A.L. 1983. Phosphate dependent, ruthenium red insensitive Ca2+ uptake in mung bean mitochondria. Biochem. Biophys. Res. Commun. 114, 1176‒1181.CrossRefPubMedGoogle Scholar
  44. 44.
    Moore A.L., Bonner W.D. 1977. The effect of calcium on the respiratory responses of mung bean mitochondria. Biochim. Biophys. Acta. 460, 455‒466.CrossRefPubMedGoogle Scholar
  45. 45.
    Martins I.S., Vercesi A.E. 1985. Some characteristics of Ca2+ transport in plant mitochondria. Biochem. Biophys. Res. Commun. 129, 943‒948.CrossRefPubMedGoogle Scholar
  46. 46.
    Day D.A., Bertagnolli B.L., Hanson J.B. 1978. The effect of calcium on the respiratory responses of corn mitochondria. Biochim. Biophys. Acta. 502, 289‒297.CrossRefPubMedGoogle Scholar
  47. 47.
    Silva M.A., Carnieri E.G., Vercesi A.E. 1992. Calcium transport by corn mitochondria: Evaluation of the role of phosphate. Plant Physiol. 98, 452‒457.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Zottini M., Zannoni D. 1993. The use of fura-2 fluorescence to monitor the movement of free calcium ions into the matrix of plant mitochondria (Pisum sativum and Helianthus tuberosus). Plant Physiol. 102, 573‒578.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    de Oliveira H.C., Saviani E.E., de Oliveira J.F.P., Salgado I. 2007. Cyclosporin A inhibits calcium uptake by Citrus sinensis mitochondria. Plant Sci. 172, 665‒670.CrossRefGoogle Scholar
  50. 50.
    Stael S., Wurzinger B., Mair A., Mehlmer N., Vothknecht U.C., Teige M. 2012. Plant organellar calcium signalling: An emerging field. J. Exp. Bot. 63, 1525‒1542.CrossRefPubMedGoogle Scholar
  51. 51.
    Meng Q., Chen Y., Zhang M., Chen Y., Yuan J., Murray S.C. 2015. Molecular characterization and phylogenetic analysis of ZmMCUs in maize. Biologia. 70, 599‒605.CrossRefGoogle Scholar
  52. 52.
    Teardo E., Carraretto L., Wagner S., Formentin E., Behera S., De Bortoli S., Larosa V., Fuchs P., Lo Schiavo F., Raffaello A., Rizzuto R., Costa A., Schwarzlander M., Szabo I. 2017. Physiological characterization of a plant mitochondrial calcium uniporter in vitro and in vivo. Plant Physiol. 173, 1355‒1370.CrossRefPubMedGoogle Scholar
  53. 53.
    Selles B., Michaud C., Xiong T.C., Leblanc O., Ingouff M. 2018. Arabidopsis pollen tube germination and growth depend on the mitochondrial calcium uniporter complex. New Phytol. 219, 58‒65.CrossRefPubMedGoogle Scholar
  54. 54.
    Wagner S., Bortoli S.D., Schwarzlander M., Szabo I. 2016. Regulation of mitochondrial calcium in plants versus animals. J. Exp. Bot. 67, 3809‒3829.CrossRefPubMedGoogle Scholar
  55. 55.
    Wagner S., Behera S., De Bortoli S., Logan D.C., Fuchs P., Carraretto L., Teardo E., Cendron L., Nietzel T., Fussl M., Doccula F.G., Navazio L., Fricker M.D., Van Aken O., Finkemeier I., Meyer A.J., Szabò I., Costa A., Schwarzländer M. 2015. The EF-hand Ca2+ binding protein MICU choreographs mitochondrial Ca2+ dynamics in Arabidopsis. Plant Cell. 27, 3190‒3212.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Paupe V., Prudent J., Dassa E.P., Rendon O.Z., Shoubridge E.A. 2015. CCDC90A (MCUR1) is a cytochrome c oxidase assembly factor and not a regulator of the mitochondrial calcium uniporter. Cell Metab. 21, 109‒116.CrossRefPubMedGoogle Scholar
  57. 57.
    Vais H., Tanis J.E., Muller M., Payne R., Mallilankaraman K., Foskett J.K. 2015. MCUR1, CCDC90A, is a regulator of the mitochondrial calcium uniporter. Cell Metab. 22, 533‒535.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Teardo E., Carraretto L., De Bortoli S., Costa A., Behera S., Wagner R., Lo Schiavo F., Formentin E. 2015. Alternative splicing-mediated targeting of the Arabidopsis GLUTAMATE RECEPTOR3.5 to mitochondria affects organelle morphology. Plant Physiol. 167, 216‒227.CrossRefPubMedGoogle Scholar
  59. 59.
    Korde A.S., Maragos W.F. 2012. Identification of an N‑methyl-D-aspartate receptor in isolated nervous system mitochondria. J. Biol. Chem. 287, 35192‒35200.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Lee A., Vastermark A., Saier M.H. 2014. Establishing homology between mitochondrial calcium uniporters, prokaryotic magnesium channels and chlamydial IncA proteins. Microbiology. 160, 1679‒1689.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Wingrove D.E., Gunter T.E. 1986. Kinetics of mitochondrial calcium transport. I. Characteristics of the sodium-independent calcium efflux mechanism of liver mitochondria. J. Biol. Chem. 261, 15159‒15165.PubMedGoogle Scholar
  62. 62.
    Wingrove D.E., Gunter T.E. 1986. Kinetics of mitochondrial calcium transport. II. A kinetic description of the sodium-dependent calcium efflux mechanism of liver mitochondria and inhibition by ruthenium red and by tetraphenylphosphonium. J. Biol. Chem. 261, 15166‒15171.PubMedGoogle Scholar
  63. 63.
    Khananshvili D. 2013. The SLC8 gene family of sodium-calcium exchangers (NCX): Structure, function, and regulation in health and disease. Mol. Aspects Med. 34, 220‒235.CrossRefPubMedGoogle Scholar
  64. 64.
    Lin Q.T., Stathopulos P.B. 2019. Molecular mechanisms of leucine zipper EF-hand containing transmembrane protein-1 function in health and disease. Int. J. Mol. Sci. 20, E286.CrossRefPubMedGoogle Scholar
  65. 65.
    Pozos T.C., Sekler I., Cyert M.S. 1996. The product of HUM1, a novel yeast gene, is required for vacuolar Ca2+/H+ exchange and is related to mammalian Na+/Ca2+ exchangers. Mol. Cell Biol. 16, 3730‒3741.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Emery L., Whelan S., Hirschi K.D., Pittman J.K. 2012. Protein phylogenetic analysis of Ca2+/cation antiporters and insights into their evolution in plants. Front. Plant Sci. 3, 1.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Sano S., Aoyama M., Nakai K., Shimotani K., Yamasaki K., Sato M.H., Tojo D., Suwastika I.N., Nomura H., Shiina T. 2014. Light-dependent expression of flg22-induced defense genes in Arabidopsis. Front. Plant Sci. 5.  https://doi.org/10.3389/fpls.2014.00531
  68. 68.
    Zhang B., Carrie C., Ivanova A., Narsai R., Murcha M.W., Duncan O., Wang Y., Law S.R., Albrecht V., Pogson B., Giraud E., Van Aken O., Whelan J. 2012. LETM proteins play a role in the accumulation of mitochondrially encoded proteins in Arabidopsis thaliana and AtLETM2 displays parent of origin effects. J. Biol. Chem. 287, 41757‒41773.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Frazier A.E., Taylor R.D., Mick D.U., Warscheid B., Stoepel N., Meyer H.E., Ryan M.T., Guiard B., Rehling P. 2006. Mdm38 interacts with ribosomes and is a component of the mitochondrial protein export machinery. J. Cell Biol. 172, 553‒564.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Patron M., Granatiero V., Espino J., Rizzuto R., De Stefani D. 2019. MICU3 is a tissue-specific enhancer of mitochondrial calcium uptake. Cell Death Differ. 26, 179‒195.CrossRefPubMedGoogle Scholar
  71. 71.
    Cai X., Clapham D.E. 2012. Ancestral Ca2+ signaling machinery in early animal and fungal evolution. Mol. Biol. Evol. 29, 91‒100.CrossRefPubMedGoogle Scholar
  72. 72.
    Galagan J.E., Calvo S.E., Borkovich K.A., Selker E.U., Read N.D., Jaffe D., FitzHugh W., Ma L.J., Smirnov S., Purcell S., Rehman B., Elkins T., Engels R., Wang S., Nielsen C.B., Butler J., Endrizzi M., Qui D., Ianakiev P., Bell-Pedersen D., Nelson M.A., Werner-Washburne M., Selitrennikoff C.P., Kinsey J.A., Braun E.L., Zelter A., Schulte U., Kothe G.O., Jedd G., Mewes W., Staben C., Marcotte E., Greenberg D., Roy A., Foley K., Naylor J., Stange-Thomann N., Barrett R., Gnerre S., Kamal M., Kamvysselis M., Mauceli E., Bielke C., Rudd S., Frishman D., Krystofova S., Rasmussen C., Metzenberg R.L., Perkins D.D., Kroken S., Cogoni C., Macino G., Catcheside D., Li W., Pratt R.J., Osmani S.A., DeSouza C.P., Glass L., Orbach M.J., Berglund J.A., Voelker R., Yarden O., Plamann M., Seiler S., Dunlap J., Radford A., Aramayo R., Natvig D.O., Alex L.A., Mannhaupt G., Ebbole D.J., Freitag M., Paulsen I., Sachs M.S., Lander E.S., Nusbaum C., Birren B. 2003. The genome sequence of the filamentous fungus Neurospora crassa. Nature. 422, 859‒868.CrossRefPubMedGoogle Scholar
  73. 73.
    Mishra J., Jhun B.S., Hurst S., O-Uchi J., Csordas G., Sheu S.S. 2017. The mitochondrial Ca2+ uniporter: Structure, function and pharmacology. Handb. Exp. Pharmacol. 240, 129–156.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Jung D.W., Bradshaw P.C., Pfeiffer D.R. 1997. Properties of a cyclosporin-insensitive permeability transition pore in yeast mitochondria. J. Biol. Chem. 272, 21104‒21112.CrossRefPubMedGoogle Scholar
  75. 75.
    Bradshaw P.C., Jung D.W., Pfeiffer D.R. 2001. Free fatty acids activate a vigorous Ca2+:2H+ antiport activity in yeast mitochondria. J. Biol. Chem. 276, 40502‒40509.CrossRefPubMedGoogle Scholar
  76. 76.
    Merchant S.S., Prochnik S.E., Vallon O., Harris E.H., Karpowicz S.J., Witman G.B., Terry A., Salamov A., Fritz-Laylin L.K., Maréchal-Drouard L., Marshall W.F., Qu L.H., Nelson D.R., Sanderfoot A.A., Spalding M.H., Kapitonov V.V., Ren Q., Ferris P., Lindquist E., Shapiro H., Lucas S.M., Grimwood J.,Schmutz J., Cardol P., Cerutti H., Chanfreau G., Chen C.L., Cognat V., Croft M.T., Dent R., Dutcher S., Fernández E., Fukuzawa H., González-Ballester D., González-Halphen D., Hallmann A., Hanikenne M., Hippler M., Inwood W., Jabbari K., Kalanon M., Kuras R., Lefebvre P.A., Lemaire S.D., Lobanov A.V., Lohr M., Manuell A., Meier I., Mets L., Mittag M., Mittelmeier T., Moroney J.V., Moseley J., Napoli C., Nedelcu A.M., Niyogi K., Novoselov S.V., Paulsen I.T., Pazour G., Purton S., Ral J.P., Riaño-Pachón D.M., Riekhof W., Rymarquis L., Schroda M., Stern D., Umen J., Willows R., Wilson N., Zimmer S.L., Allmer J., Balk J., Bisova K., Chen C.J., Elias M., Gendler K., Hauser C., Lamb M.R., Ledford H., Long J.C., Minagawa J., Page M.D., Pan J., Pootakham W., Roje S., Rose A., Stahlberg E., Terauchi A.M., Yang P., Ball S., Bowler C., Dieckmann C.L., Gladyshev V.N., Green P., Jorgensen R., Mayfield S., Mueller-Roeber B., Rajamani S., Sayre R.T., Brokstein P., Dubchak I., Goodstein D., Hornick L., Huang Y.W., Jhaveri J., Luo Y., Martínez D., Ngau W.C., Otillar B., Poliakov A., Porter A., Szajkowski L., Werner G., Zhou K., Grigoriev I.V., Rokhsar D.S., Grossman A.R. 2007. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science. 318, 245‒250.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Subbaiah C.C., Bush D.S., Sachs M.M. 1998. Mitochondrial contribution to the anoxic Ca2+ signal in maize suspension-cultured cells. Plant Physiology. 118, 759‒771.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Logan D.C., Knight M.R. 2003. Mitochondrial and cytosolic calcium dynamics are differentially regulated in plants. Plant Physiology. 133, 21–24.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Kovacs-Bogdan E., Sancak Y., Kamer K.J., Plovanich M., Jambhekar A., Huber R.J., Myre M.A., Blower M.D., Mootha V.K. Reconstitution of the mitochondrial calcium uniporter in yeast. Proc. Natl. Acad. Sci. USA. 111, 8985‒8990.Google Scholar
  80. 80.
    Ramakrishnan S., Docampo R. 2018. Membrane proteins in Trypanosomatids involved in Ca2+ homeostasis and signaling. Genes (Basel). 9, 304.CrossRefGoogle Scholar
  81. 81.
    Docampo R., Vercesi A.E. 1989. Ca2+ transport by coupled Trypanosoma cruzi mitochondria in situ. J. Biol. Chem. 264, 108‒111.PubMedGoogle Scholar
  82. 82.
    Alvarez-Illera P., García-Casas P., Arias-del-Val J., Fonteriz R.I., Alvarez J., Montero V. 2017. Pharynx mitochondrial [Ca2+] dynamics in live C. elegans worms during aging. Oncotarget. 8, 55889‒55900.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Liu C., Zhang Y., Ren Y., Wang H., Li S., Jiang F., Yin L., Qiao X., Zhang G., Qian W., Liu B., Fan W. 2017. The genome of the golden apple snail Pomacea canaliculata provides insight into stress tolerance and invasive adaptation. Gigascience. 7, giy101.Google Scholar
  84. 84.
    Regier J.C., Shultz J.W., Zwick A., Hussey A., Ball B., Wetzer R., Martin J.W., Cunningham C.W. 2010. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature. 463, 1079‒1083.CrossRefGoogle Scholar
  85. 85.
    McQuibban A.G., Joza N., Megighian A., Scorzeto M., Zanini D., Reipert S., Richter C., Schweyen R.J., Nowikovsky K. 2010. A Drosophila mutant of LETM1, a candidate gene for seizures in Wolf-Hirschhorn syndrome. Hum. Mol. Genet. 19, 987‒1000.CrossRefPubMedGoogle Scholar
  86. 86.
    Tufi R., Gleeson T., von Stockum S., Hewitt V., Lee J., Terriente-Felix A., Sanchez-Martinez A., Ziviani E., Whitworth A. 2018. A comprehensive genetic characterisation of the mitochondrial Ca2+ uniporter in Drosophila. bioRxiv.  https://doi.org/10.1101/458174
  87. 87.
    Baradaran R., Wang C., Siliciano A.F., Long S.B. 2018. Cryo-EM structures of fungal and metazoan mitochondrial calcium uniporters. Nature. 559, 580‒584.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Shimizu H., Schredelseker J., Huang J., Lu K., Naghdi S., Lu F., Franklin S., Fiji H., Wang K., Zhu H., Tian C., Lin B., Nakano H., Ehrlich A., Nakai J., Stieg A.Z., Gimzewski J.K, Nakano A, Goldhaber J.I., Vondriska T.M., Hajnóczky G., Kwon O., Chen J.N. 2015. Mitochondrial Ca2+ uptake by the voltage-dependent anion channel 2 regulates cardiac rhythmicity. Elife. 4, e04801.CrossRefPubMedCentralGoogle Scholar
  89. 89.
    Lamason R.L., Mohideen M.A., Mest J.R., Wong A.C., Norton H.L., Aros M.C., Jurynec M.J., Mao X., Humphreville V.R., Humbert J.E., Sinha S., Moore J.L., Jagadeeswaran P., Zhao W., Ning G., Makalowska I., McKeigue P.M., O’donnell D., Kittles R., Parra E.J., Mangini N.J., Grunwald D.J., Shriver M.D., Canfield V.A., Cheng K.C. 2005. SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science. 310, 1782‒1786.CrossRefPubMedGoogle Scholar
  90. 90.
    Bayes A., Collins M.O., Reig-Viader R., Gou G., Goulding D., Izquierdo A., Choudhary J.S., Emes R.D., Grant S.G.N. 2017. Evolution of complexity in the zebrafish synapse proteome. Nat. Commun. 8, 14613.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Han Y., Ishibashi S., Iglesias-Gonzalez J., Chen Y., Love N.R., Amaya E. 2018. Ca2+-induced mitochondrial ROS regulate the early embryonic cell cycle. Cell Rep. 22, 218‒231.CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Hellsten U., Harland R.M., Gilchrist M.J., Hendrix D., Jurka J., Kapitonov V., Ovcharenko I., Putnam N.H., Shu S., Taher L., Blitz I.L., Blumberg B., Dichmann D.S., Dubchak I., Amaya E., Detter J.C., Fletcher R., Gerhard D.S., Goodstein D., Graves T., Grigoriev I.V., Grimwood J., Kawashima T., Lindquist E., Lucas S.M., Mead P.E., Mitros T., Ogino H., Ohta Y., Poliakov A.V., Pollet N., Robert J., Salamov A., Sater A.K., Schmutz J., Terry A., Vize P.D., Warren W.C., Wells D., Wills A., Wilson R.K., Zimmerman L.B., Zorn A.M., Grainger R., Grammer T., Khokha M.K., Richardson P.M., Rokhsar D.S. 2010. The genome of the Western clawed frog Xenopus tropicalis. Science. 328, 633‒636.CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Alfoldi J., Di Palma F., Grabherr M., Williams C., Kong L., Mauceli E., Russell P., Lowe C.B., Glor R.E., Jaffe J.D., Ray D.A., Boissinot S., Shedlock A.M., Botka C. 2011. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature. 477, 587‒591.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Shanmughapriya S., Rajan S., Hoffman N.E., Zhang X., Guo S., Kolesar J.E., Hines K.J., Ragheb J., Jog N.R., Caricchio R., Baba Y., Zhou Y., Kaufman B.A., Cheung J.Y., Kurosaki T., Gill D.L., Madesh M. 2015. Ca2+ signals regulate mitochondrial metabolism by stimulating CREB-mediated expression of the mitochondrial Ca2+ uniporter gene MCU. Sci. Signal. 8, ra23.CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Kim B., Takeuchi A., Koga O., Hikida M., Matsuoka S. 2012. Pivotal role of mitochondrial Na+,Ca2+-exchange in antigen receptor mediated Ca2+ signalling in DT40 and A20 B lymphocytes. J. Physiol. 590, 459‒474.CrossRefPubMedGoogle Scholar
  96. 96.
    Holt C., Campbell M., Keays D.A., Edelman N., Kapusta A., Maclary E., Domyan E.T., Suh A., Warren W.C., Yandell M., Gilbert M.T.P., Shapiro M.D. 2018. Improved genome assembly and annotation for the rock pigeon (Columba livia). G3 (Bethesda). 8, 1391‒1398.CrossRefGoogle Scholar
  97. 97.
    Gunter T., Pfeiffer D. 1990. Mechanisms by which mitochondria transport calcium. Physiol. 258, 755‒786.Google Scholar
  98. 98.
    Michels G., Khan I.F., Endres-Becker J., Rottlaender D., Herzig S., Ruhparwar A., Wahlers T., Hoppe U.C. 2009. Regulation of the human cardiac mitochondrial Ca2+ uptake by 2 different voltage-gated Ca2+ channels. Circulation. 119, 2435‒2443.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  1. 1.Mari State UniversityYoshkar-OlaRussia
  2. 2.Institute of Theoretical and Experimental Biophysics, Russian Academy of SciencesPushchinoRussia

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