Home LiteratureArticle Details
PMID: 21685888 Published · epublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter.

Nature ·Vol. 476 ·No. 7360 ·2011-06-19 ·Pages 336-40

De Stefani D, Raffaello A, Teardo E, Szabò I, Rizzuto R

Abstract

Mitochondrial Ca(2+) homeostasis has a key role in the regulation of aerobic metabolism and cell survival, but the molecular identity of the Ca(2+) channel, the mitochondrial calcium uniporter, is still unknown. Here we have identified in silico a protein (named MCU) that shares tissue distribution with MICU1 (also known as CBARA1), a recently characterized uniporter regulator, is present in organisms in which mitochondrial Ca(2+) uptake was demonstrated and whose sequence includes two transmembrane domains. Short interfering RNA (siRNA) silencing of MCU in HeLa cells markedly reduced mitochondrial Ca(2+) uptake. MCU overexpression doubled the matrix Ca(2+) concentration increase evoked by inositol 1,4,5-trisphosphate-generating agonists, thus significantly buffering the cytosolic elevation. The purified MCU protein showed channel activity in planar lipid bilayers, with electrophysiological properties and inhibitor sensitivity of the uniporter. A mutant MCU, in which two negatively charged residues of the putative pore-forming region were replaced, had no channel activity and reduced agonist-dependent matrix Ca(2+) concentration transients when overexpressed in HeLa cells. Overall, these data demonstrate that the 40-kDa protein identified is the channel responsible for ruthenium-red-sensitive mitochondrial Ca(2+) uptake, thus providing a molecular basis for this process of utmost physiological and pathological relevance.

MeSH Terms
Amino Acid Sequence Animals Apoptosis Calcium/metabolism Calcium Channels/chemistry,deficiency,genetics,metabolism Cell Membrane Permeability Conserved Sequence Gene Silencing HeLa Cells Humans Inositol 1,4,5-Trisphosphate/metabolism Ion Transport Lipid Bilayers/metabolism Membrane Potential, Mitochondrial/physiology Mice Mitochondria/metabolism Mitochondrial Membranes/metabolism Molecular Sequence Data Molecular Weight Protein Structure, Tertiary Protein Transport
Chemicals
Calcium Channels Lipid Bilayers mitochondrial calcium uniporter Inositol 1,4,5-Trisphosphate Calcium
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
De Stefani Diego
Department of Biomedical Science, University of Padua, 35121 Padua, Italy.
Raffaello Anna
Teardo Enrico
Szabò Ildikò
Rizzuto Rosario
References (32)
32 references, click to expand
  1. Mitochondria suppress local feedback activation of inositol 1,4, 5-trisphosphate receptors by Ca2+.
    J Biol Chem. 1999 May 14;274(20):14157-62 PMID: 10318833
  2. MICU1 encodes a mitochondrial EF hand protein required for Ca(2+) uptake.
    Nature. 2010 Sep 16;467(7313):291-6 PMID: 20693986
  3. Propagation of the apoptotic signal by mitochondrial waves.
    EMBO J. 2001 Aug 1;20(15):4107-21 PMID: 11483514
  4. Automatic and quantitative measurement of protein-protein colocalization in live cells.
    Biophys J. 2004 Jun;86(6):3993-4003 PMID: 15189895
  5. Mitochondria and calcium signaling.
    Cell Calcium. 2005 Sep-Oct;38(3-4):311-7 PMID: 16087232
  6. Mitochondria: the hub of cellular Ca2+ signaling.
    Physiology (Bethesda). 2008 Apr;23:84-94 PMID: 18400691
  7. Mitochondria exert a negative feedback on the propagation of intracellular Ca2+ waves in rat cortical astrocytes.
    J Cell Biol. 1999 May 17;145(4):795-808 PMID: 10330407
  8. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes.
    J Mol Biol. 2001 Jan 19;305(3):567-80 PMID: 11152613
  9. Biosensors for the detection of calcium and pH.
    Methods Cell Biol. 2007;80:297-325 PMID: 17445701
  10. A guided tour into subcellular colocalization analysis in light microscopy.
    J Microsc. 2006 Dec;224(Pt 3):213-32 PMID: 17210054
  11. Quasi-synaptic calcium signal transmission between endoplasmic reticulum and mitochondria.
    EMBO J. 1999 Jan 4;18(1):96-108 PMID: 9878054
  12. Selective transfer of calcium from an acidic compartment to the mitochondrion of Trypanosoma brucei. Measurements with targeted aequorins.
    J Biol Chem. 1997 Dec 5;272(49):31022-8 PMID: 9388251
  13. Mitofusin 2 tethers endoplasmic reticulum to mitochondria.
    Nature. 2008 Dec 4;456(7222):605-10 PMID: 19052620
  14. The mitochondrial calcium uniporter is a highly selective ion channel.
    Nature. 2004 Jan 22;427(6972):360-4 PMID: 14737170
  15. Regulation of the human cardiac mitochondrial Ca2+ uptake by 2 different voltage-gated Ca2+ channels.
    Circulation. 2009 May 12;119(18):2435-43 PMID: 19398664
  16. Imaging interorganelle contacts and local calcium dynamics at the ER-mitochondrial interface.
    Mol Cell. 2010 Jul 9;39(1):121-32 PMID: 20603080
  17. Isolation of mitochondria-associated membranes and mitochondria from animal tissues and cells.
    Nat Protoc. 2009;4(11):1582-90 PMID: 19816421
  18. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses.
    Science. 1998 Jun 12;280(5370):1763-6 PMID: 9624056
  19. Ca2+ transport in isolated mitochondrial vesicles from Leishmania braziliensis promastigotes.
    Mol Biochem Parasitol. 1990 Feb;39(1):61-8 PMID: 2304488
  20. Characterization of a plant glutamate receptor activity.
    Cell Physiol Biochem. 2010;26(2):253-62 PMID: 20798509
  21. Decoding of cytosolic calcium oscillations in the mitochondria.
    Cell. 1995 Aug 11;82(3):415-24 PMID: 7634331
  22. Single-point mutations of a lysine residue change function of Bax and Bcl-xL expressed in Bax- and Bak-less mouse embryonic fibroblasts: novel insights into the molecular mechanisms of Bax-induced apoptosis.
    Cell Death Differ. 2011 Mar;18(3):427-38 PMID: 20885444
  23. Active mitochondria surrounding the pancreatic acinar granule region prevent spreading of inositol trisphosphate-evoked local cytosolic Ca(2+) signals.
    EMBO J. 1999 Sep 15;18(18):4999-5008 PMID: 10487752
  24. Interactions of calcium with yeast mitochondria.
    Cell Calcium. 1992 Apr;13(4):211-7 PMID: 1586938
  25. CHELATOR: an improved method for computing metal ion concentrations in physiological solutions.
    Biotechniques. 1992 Jun;12(6):870-4, 876-9 PMID: 1642895
  26. Historical review: mitochondria and calcium: ups and downs of an unusual relationship.
    Trends Biochem Sci. 2003 Apr;28(4):175-81 PMID: 12713900
  27. Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria.
    Science. 1993 Oct 29;262(5134):744-7 PMID: 8235595
  28. 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. 2001 Jun 1;20(11):2690-701 PMID: 11387204
  29. Control of apoptosis by IP(3) and ryanodine receptor driven calcium signals.
    Cell Calcium. 2000 Nov-Dec;28(5-6):349-63 PMID: 11115374
  30. Calcium signalling: dynamics, homeostasis and remodelling.
    Nat Rev Mol Cell Biol. 2003 Jul;4(7):517-29 PMID: 12838335
  31. Regulation of mitochondrial ATP synthesis by calcium: evidence for a long-term metabolic priming.
    Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):13807-12 PMID: 10570154
  32. Ca2+ hot spots on the mitochondrial surface are generated by Ca2+ mobilization from stores, but not by activation of store-operated Ca2+ channels.
    Mol Cell. 2010 Apr 23;38(2):280-90 PMID: 20417605
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2011-06-19
Epub
2011-00-19
Pages
336-40
Language
English
Region
England
NLM ID
0410462
PMCID
PMC4141877
Subset
IM
Grants
Telethon · GPP10005 · Italy
NIA NIH HHS · P01 AG025532 · United States
NIA NIH HHS · P01 AG025532-01A1 · United States
NIA NIH HHS · 1P01AG025532-01A1 · United States
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com