WAYS AND MECHANISMS OF TRANSMEMBRANE EXCHANGE OF Ca2 + IN MITOCHONDRIA
О.V. Кolomiets , Yu.V. Danylovych, Н.V. Danylovych, S.О. Кosterin
Palladin Institute of Biochemistry, National Academy of Sciences
of Ukraine, Kyiv, Ukraine
DOI: https://doi.org/10.15407/fz63.04.087
Abstract
The review analyzed published data about transport of ions of
calcium in the mitochondria and presented some own results
of experiments conducted on the smooth muscle of the uterus
(myometrium). In particular, it was described the systems
of mitochondrial Са2+- uniporter, «rapid mode uptake»,
mitochondrial ryanodine receptor, Na+-Са2+- and Н+-Са2+-
exchangers, mitochondrial permeability transition pore. The
possible functional role of Са2+ in mitochondria and their
significance in maintaining of cell’s Са2+-homeostasis have
been considered. The features of transmembrane exchange of
Ca2 + in mitochondria for various pathologies was discussed.
Keywords:
mitochondria; Са2+-uniporter; «rapid mode uptake»; mitochondrial ryanodine receptor; Na+-Са2+-exchanger; Н+-Са2+-exchanger; mitochondrial permeability transition pore; smooth muscle; myometrium.
References
- Kostyuk PG, Kostyuk OP, Lukyanets EA. Intracellular calcium signaling: structures and functions. Kiev: Nauk. Dumka; 2010. [Ukrainian].
PubMedCentral
- Santo-Domingo J, Demaurex N. Calcium uptake mechanisms of mitochondria. Biochim Biophys Acta. 2010; 1797(6-7):907-12.
CrossRef
PubMed
- Kosterin SA, Burdyga ThV. Transport and intracellular homeostasis of Sa2+ in myometrium. Biol Bul Rev. 1993;113(4) :485-506. [Russian].
- Bernardi P, Rasola A. Calcium and cell death: the mitochondrial connection. Subcell Biochem. 2007;45:481-506.
CrossRef
PubMed
- Chalmers S, Nicholls DG. The relationship between free and total calcium concentrations in the matrix of liver and brain mitochondria. J Biol Chem 2003;278(21):19062-70.
CrossRef
PubMed
- Rizzuto R., Marchi S., Bonora M., Aguiary P., Bononi A. Ca2+ transfer from the ER to mitochondria: When, how and why. Biochim Biophys Acta. 2009;1787(11):1342-51.
CrossRef
PubMed PubMedCentral
- Graier WF, Frieden M, Malli R.. Mitochondria and Ca2+ signaling: old quests, new functions. Eur J Physiol. 2007;455(3):375-96.
CrossRef
PubMed PubMedCentral
- Takeuchi A, Kim B, Matsuoka S. The destiny of Ca2+ released by mitochondria. J Physiol Sci. 2015;65(1):11-24.
CrossRef
PubMed PubMedCentral
- Gunter TE, Pfeiffer DR. Mechanisms by which mitochondrria transport calcium. Am J Physiol. 1990;258(5 Pt 1):C755-86.
- DeLuca HF, Engstrom GW. Calcium uptake by rat kidney mitochondria. Proc Nat Acad Sci USA. 1961;47(11): 1744-1750.
CrossRef
- Lehninger A. L, Rossi CS, Greenawalt JW. Respirationdependent accumulation of inorganic phosphate and Ca ion by rat liver mitochondria. Biochem Biophys Rec Commun. 1963;10(3):444-8.
CrossRef
- Carafoli E, Rossi CS, Lehninger AL. Uptake of adenine nucleotides by respiring mitochondria during active accumulation of Ca2+ and phosphate. J Biol Chem. 1965;240(5):2254-61.
PubMed
- Kosterin SO. Transport of calcium in the smooth muscles. Kiev: Nauk. Dumka; 1990. [Russian].
- Pan S, Ryu S-Y, Sheu S-S. Distinctive characteristics and functions of multiple mitochondrial Ca2+ influx mechanisms. Sci China Life Sci. 2011;54(8):763-9.
CrossRef
PubMed PubMedCentral
- Szabadkai G, Duchen MR. Mitochondria: The Hub of Cellular Ca2+ Signaling. Physiol. 2008; 23(2):84-94.
CrossRef
PubMed
- Vernardi R. Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol Rev. 1999;79(4):1127-55.
CrossRef
PubMed
- Malli R, Graier WF. Mitochondrial Ca2+ channels: Great unknowns with important functions. FEBS Lett. 2010;584(10):1942-7.
CrossRef
PubMed PubMedCentral
- Feissner RF, Skalska J, Gaum WE, Sheu SS.Crosstalk signaling between mitochondrial Ca2+ and ROS. Front Biosci. 2009;14:1197-218.
CrossRef
- Veklich TO. Transport of Ca2+ in the smooth muscle cells mitochondria: Manuscript. Kiev: Palladin Institute of Biochemistry of the NASU; 2003. [Ukrainian].
- Ryu SY, Beutner G, Dirksen RT, Kinnally KW, Sheu SS. Mitochondrial ryanodine receptors and other mitochondrial Ca2+ permeable shannels. FEBS Lett. 2010;584(10):1948-55.
CrossRef
PubMed PubMedCentral
- Gunter TE, Yule DI, Gunter KK, Eliseev RA, Salter JD. Calcium and mitochondria. FEBS Letters. 2004;567(1):96-
CrossRef
PubMed
- Hoppe UC. Mitochondrial calcium channels. FEBS Lett. 2010;584(10):1975-81.
CrossRef
PubMed
- Csordás G, Várnai P, Golenár T, Sheu S-S, Hajnóczky G. Calcium transport across the inner mitochondrial membrane: molecular mechanisms and pharmacology. Mol Cell Endocrinol. 2012; 353(1-2):109-13.
CrossRef
PubMed PubMedCentral
- Akopova OV, Sahach VF. The influence of nitric oxide donors on Ca2+-uptake in rat heart and liver mitochondria. Ukr Biokhim Zh. 2005;77(2):82-7. [Russian].
- Danylovych YuV, Kolomiets' OV, Danylovych GV, Kosterin SO. Nitric oxide as a possible regulator of energydependent Ca2+ transport in mitochondria of uterine smooth muscle. Fiziol Zh. 2014;60(2):12-7. [Ukrainian].
PubMed
- Kolomiets OV, Danylovych YuV, Danylovych GV, Kosterin SO. Ca2+ accumulation study in isolated smooth muscle mitochondria using Fluo-4 AM. Ukr Biokhim Zh 2013;85(4):30-9. [Ukrainian].
- Kolomiets' OV, Danylovych YuV, Danylovych GV, Kosterin SO. Ca2+/H+-exchange in myometrium mitochondria. Ukr Biochem J. 2014;86(3):41-8. [Ukrainian].
CrossRef
- Foskett JK, Philipson B. The Mitochondrial Ca2+ Uniporter Complex. J Mol Cell Cardiol. 2015;78:3-8.
CrossRef
PubMed PubMedCentral
- De Stefani D, Patron M, Rizzuto R. Structure and function of the Mitochondrial Calcium Uniporter complex. Biochim Biophys Acta. 2015;1853(9):2006-11.
CrossRef
PubMed PubMedCentral
- Santo-Domingo J, Wiederkehr A, De Marchi U. Modulation of the matrix redox signaling by mitochondrial Ca2+. World J Biol Chem. 2015;6(4):310-23.
CrossRef
PubMed PubMedCentral
- Baughman JM, Perocchi F, Girgis HS, Plovanich M, Belcher-Timme CA, Sancak Y, Bao XR, Strittmatter L, Goldberger O, Bogorad RL, Koteliansky V, Mootha VK. Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature. 2011;476(7360):341-5.
CrossRef
PubMed PubMedCentral
- Bernardi P, von Stockum S. The permeability transition pore as a Ca2+ release channel: New answers to an old question. Cell Calcium. 2012;52(1):22-7.
CrossRef
PubMed PubMedCentral
- Rasola A, Bernardi P. Mitochondrial permeability transition in Ca2+-dependent apoptosis and necrosis. Cell Calcium. 2011;50(3):222-33.
CrossRef
PubMed
- Kursky MD, Kosterin SA, Burchinskaya NF, Shlykov SG. Passive transport of Sa2+ into fractions of myometrium mitochondria. Ukr Biokhim Zh. 1987;59(3):35-9. [Russian].
- Kolomiets' OV, Danylovych YuV, Danylovych GV. H+- Ca2+-exchanger in the myometrium mitochondria: modulation of exogenous and endogenous compounds. Fiziol Zh. 2014;60(5):33-42. [Ukrainian].
- Palty R, Hershfinkel M, Sekler I. Molecular Identity and Functional Properties of the Mitochondrial Na+/Ca2+ Exchanger. J Biol Chem. 2012;287(38):31650-7.
CrossRef
PubMed PubMedCentral
- Nowikovsky K, Pozzan T, Rizzuto R, Scorrano L, Bernardi P. The pathophysiology of LETM1. J Gen Physiol. 2012;139(6):445-54.
CrossRef
PubMed PubMedCentral
- Jiang D, Zhao L, Clapham DE. Genome-wide RNAi screen identifies Letm1 as a mitochondrial Ca2+/H+ antiporter. Science. 2009;326(5949):144-7.
CrossRef
PubMed PubMedCentral
- Vinogradov AD. Energy transduction in mitochondria. Soros Educ J. 1999 (9):11-19.
- Wingrove DE, Gunter TE. Kinetics of mitochondrial calcium transport. I. Characteristics of the sodium-independent calcium efflux mechanism of liver mitochondria. J Biol Chem. 1986;261(32):15159-65.
PubMed
- Vovkanych LS, Dubytsky LO. Kinetical properties of the H+-stimulated rat liver mitochondria Ca2+ efflux. Exp Clin Physiol Biochem 2001;15(3):34-37. [Ukrainian].
- Tsai MF, Jiang D, Zhao L, Clapham D, Miller C. Functional reconstitution of the mitochondrial Ca2+/H+ antiporter Letm1. J Gen Physiol. 2014;143(1):67-73.
CrossRef
PubMed PubMedCentral
- Schlickum S, Moghekar A, Simpson JC, Steglich C, O'Brien RJ, Winterpacht A, Endele SU. LETM1, a gene deleted in Wolf-Hirschhorn syndrome, encodes an evolutionarily conserved mitochondrial protein. Genomics. 2004;83(2):254-61.
CrossRef
PubMed
- Dimmer KS, Navoni F, Casarin A, Trevisson E, Endele S, Winterpacht A, Salviati L, Scorrano L. LETM1, deleted in Wolf-Hirschhorn syndrome is required for normal mitochondrial morphology and cellular viability. Hum Mol Genet. 2008;17(2):201-14.
CrossRef
PubMed
- Shao J, Fu Z, Ji Y, Guan X, Guo S, Ding Z, Yang X, Cong Y, Shen Y. Leucine zipper-EF-hand containing transmembrane protein 1 (LETM1) forms a Ca2+/H+ antiporter. Sci Rep. 2016;6:34174.
CrossRef
PubMed PubMedCentral
- Piao L, Li Y, Kim SJ, Byun HS, Huang SM. Association of LETM1 and MRPL36 contributes to the regulation of mitochondrial ATP production and necrotic cell death. Cancer Res. 2009;69(8):3397-404.
CrossRef
PubMed
- Doonan PJ, Chandramoorthy HC, Hoffman NE, Zhang X, Cárdenas C, Shanmughapriya S, Rajan S, Vallem S, Chen X, Foskett JK, Cheung JY, Houser SR, Madesh M. LETM1-dependent mitochondrial Ca2+ flux modulates cellular bioenergetics and proliferation. FASEB J. 2014;28(11):4936-49.
CrossRef
PubMed PubMedCentral
- Akopova OV. The role of permeability transition pore in transmembrane Ca2+-exchange in mitochondria. Ukr Biokhim Zh. 2008;80(3):40-47. [Ukrainian]. Giulivi C, Kato K, Cooper CE. Nitric oxide regulation of mitochondrial oxygen consumption I: cellular physiology. Am J Physiol Cell Physiol. 2006;291(6):C1225-31.
- Llorente-Folch I, Rueda CB, Pardo B, Szabadkai G, Duchen MR, Satrustegui J. The regulation of neuronal mitochondrial metabolism by calcium. J Physiol. 2015;593(16):3447-62.
CrossRef
PubMed PubMedCentral
- Giulivi C, Kato K, Cooper CE. Nitric oxide regulation of mitochondrial oxygen consumption I: cellular physiology. Am J Physiol Cell Physiol. 2006;291(6):C1225-31.
CrossRef
- Danylovych YuV, Karakhim SA, Danylovych HV, Kolomiets OV, Kosterin SO. Electrochemical potential of the inner mitochondrial membrane and Ca2+ homeostasis of myometrium cells. Ukr Biochem J. 2015;87(5):61-71.
CrossRef
- Campos JC, Bozi LH, Bechara LR, Lima VM, Ferreira JC. Mitochondrial Quality Control in Cardiac Diseases. Front Physiol. 2016;7:479.
CrossRef
PubMed PubMedCentral
- El-Hattab AW, Scaglia F. Mitochondrial Cardiomyopathies. Front Cardiovasc Med. 2016;3:25.
CrossRef
- Picard M, Wallace DC, Burelle Y. The rise of mitochondria in medicine. Mitochondrion. 2016;30:105-16.
CrossRef
PubMed PubMedCentral
- Tocchi A, Quarles EK, Basisty N, Gitari L, Rabinovitch PS. Mitochondrial dysfunction in cardiac aging. Biochim Biophys Acta. 2015;1847(11):1424-33.
CrossRef
PubMed PubMedCentral
- Niyazov DM, Kahler SG, Frye RE. Primary Mitochondrial Disease and Secondary Mitochondrial Dysfunction: Importance of Distinction for Diagnosis and Treatment. Mol Syndromol. 2016;7(3):122-37.
CrossRef
PubMed PubMedCentral
- Pathak D, Berthet A, Nakamura K. Energy failure: does it contribute to neurodegeneration? Ann Neurol. 2013;74(4):506-16.
CrossRef
PubMed PubMedCentral
- Calì T, Ottolini D, Brini M. See comment in PubMed Commons belowCell Calcium. Mitochondrial Ca2+ and neurodegeneration. Cell Calcium. 2012;52(1):73-85.
CrossRef
PubMed PubMedCentral
- Görlach A, Bertram K, Hudecova S, Krizanova O. Calcium and ROS: A mutual interplay. Redox Biol. 2015;6:260-71.
CrossRef
PubMed PubMedCentral
- Maléth J, Hegyi P. Ca2+ toxicity and mitochondrial damage in acute pancreatitis: translational overview. Philos Trans R Soc Lond B Biol Sci. 2016;371(1700) .
- Cui C, Merritt R, Fu L, Pan Z. Targeting calcium signaling in cancer therapy. Acta Pharm Sin B. 2017;7(1):3-17.
CrossRef
PubMed PubMedCentral
- Rimessi A, Patergnani S, Bonora M, Wieckowski MR, Pinton P. Mitochondrial Ca2+ Remodeling is a Prime Factor in Oncogenic Behavior. Front Oncol. 2015;5:143.
CrossRef
PubMed PubMedCentral
- Rasola a, Bernardi P. The mitochondrial permeability transition pore and its adaptive responses in tumor cells. Cell Calcium. 2014; 56(6): 437–445.
CrossRef
PubMed PubMedCentral
- Logan CV, Szabadkai G, Sharpe JA et al. Loss-of-function mutations in MICU1 cause a brain and muscle disorder linked to primary alterations in mitochondrial calcium signaling. Nat Genet. 2014;46(2):188-93.
CrossRef
PubMed
- Lewis-Smith D, Kamer KJ, Griffin H. Homozygous deletion in MICU1 presenting with fatigue and lethargy in childhood. Neurol Genet. 2016;2(2):e59.
CrossRef
PubMed PubMedCentral
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