DOI: 10.1042/bj20050738. Agonist-induced regulation of mitochondrial and endoplasmic reticulum motility

Agonist-induced regulation of mitochondrial and endoplasmic reticulum motility

10.1042/bj20050738

Crossref journal-article

Portland Press Ltd.

Biochemical Journal (288)

Abstract

Using fluorescently tagged markers for organelles in conjunction with confocal microscopy, we have studied the effects of agonist-induced Ca2+ signals on the motility of mitochondria and the ER (endoplasmic reticulum). We observed that the muscarinic agonist carbachol produced a rapid, simultaneous and reversible cessation of the movements of both organelles, which was dependent on a rise in cytosolic Ca2+. This rise in Ca2+ was shown to cause a fall in cellular ATP levels, and the effect of carbachol on organelle movement could be mimicked by depleting ATP with metabolic inhibitors in the absence of any such rise in Ca2+. However, a Ca2+-sensing process independent of ATP appears also to be involved, because we identified conditions where the ATP depletion was blocked (by inhibitors of the Ca2+ pumps), but the organelle movements still ceased following a rise in cytosolic Ca2+. We conclude that the co-ordinated cessation of mitochondria and ER motility is a process regulated by the cytosolic concentration of both Ca2+ and ATP, and that these two parameters are likely to synergize to regulate the localization of the two organelles, and to facilitate the transfer of Ca2+ between them.

Bibliography

Brough, D., Schell, M. J., & Irvine, R. F. (2005). Agonist-induced regulation of mitochondrial and endoplasmic reticulum motility. Biochemical Journal, 392(2), 291â297.

Authors 3

David Brough (first)
Michael J. Schell (additional)
Robin F. Irvine (additional)

References 28 Referenced 72

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10.1093/emboj/18.18.4999 / EMBO J. / Active mitochondria surrounding the pancreatic acinar granule region prevent spreading of inositol trisphosphate-evoked local cytosolic Ca2+ signals by Tinel (1999)
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10.1523/JNEUROSCI.23-21-07881.2003 / J. Neurosci. / Glutamate decreases mitochondrial size and movement in primary forebrain neurons by Rintoul (2003)
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10.1083/jcb.103.4.1557 / J. Cell Biol. / Microtubules and the endoplasmic reticulum are highly interdependent structures by Terasaki (1986)
10.1016/0092-8674(88)90177-8 / Cell / Dynamic behavior of endoplasmic reticulum in living cells by Lee (1988)
10.1016/S0960-9822(98)70321-5 / Curr. Biol. / Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms by Waterman-Storer (1998)
10.1126/science.283.5407.1493 / Science / The machinery of mitochondrial inheritance and behavior by Yaffe (1999)
10.1016/j.cub.2004.06.045 / Curr. Biol. / Bidirectional transport along microtubules by Welte (2004)
10.1126/stke.2512004pe46 / Science STKE / Mitochondrial stop and go: signals that regulate organelle movement by Reynolds (2004)
10.1242/jcs.109.5.971 / J. Cell Sci. / Organelle motility and metabolism in axons vs. dendrites of cultured hippocampal neurons by Overly (1996)
10.1054/ceca.2000.0108 / Cell Calcium / Effects of elevated cytoplasmic calcium and protein kinase C on endoplasmic reticulum structure and function in HEK293 cells by Pedrosa Ribeiro (2000)
10.1016/S0960-9822(02)00609-7 / Curr. Biol. / Subcellular Ca2+ signals underlying waves and graded responses in HeLa cells by Bootman (1996)
10.1113/jphysiol.2004.077289 / J. Physiol. / Capacitative calcium entry supports calcium oscillations in Human Embryonic Kidney Cells by Bird (2005)
10.1523/JNEUROSCI.16-17-05425.1996 / J. Neurosci. / Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism by Xia (1996)
{'key': '2021112217150665800_B19', 'first-page': '2', 'article-title': 'Increased expression and convenience with the new pGL3 luciferase reporter vectors', 'volume': '50', 'author': 'Groskreutz', 'year': '1995', 'journal-title': 'Promega Notes Magazine'} / Promega Notes Magazine / Increased expression and convenience with the new pGL3 luciferase reporter vectors by Groskreutz (1995)
10.1073/pnas.96.24.13807 / Proc. Natl. Acad. Sci. U.S.A. / Regulation of mitochondrial ATP synthesis by calcium: evidence for a long-term metabolic priming by Jouaville (1999)
10.1042/bj2950165 / Biochem. J. / Continuous bioluminescent monitoring of cytoplasmic ATP in single isolated rat hepatocytes during metabolic poisoning by Koop (1993)
10.1042/bj3190463 / Biochem. J. / Evidence for rapid consumption of millimolar concentrations of cytoplasmic ATP during rigor-contracture of metabolically compromised single cardiomyocytes by Allue (1996)
10.1016/j.cub.2004.10.046 / Curr. Biol. / Molecular motors: strategies to get along by Mallik (2004)
10.1016/S1367-5931(99)00069-1 / Curr. Opin. Chem. Biol. / Calcium pumps: structural basis for and mechanism of calcium transmembrane transport by Carafoli (2000)
10.1016/0092-8674(95)90430-1 / Cell / Decoding of cytosolic calcium oscillations in the mitochondria by Hajnoczky (1995)
10.1002/1096-9861(20001120)427:3<340::AID-CNE2>3.0.CO;2-Y / J. Comp. Neurol. / Movement of mitochondria in the axons and dendrites of cultured hippocampal neurons by Ligon (2000)
10.1242/jcs.104.3.917 / J. Cell Sci. / The regulation of bidirectional mitochondrial transport is co-ordinated with axonal outgrowth by Morris (1993)
10.1016/j.cell.2004.11.003 / Cell / The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses by Li (2004)

Dates

Type	When
Created	19 years, 8 months ago (Dec. 2, 2005, 7:23 a.m.)
Deposited	3 years, 9 months ago (Nov. 22, 2021, 7:33 p.m.)
Indexed	1 month, 1 week ago (July 11, 2025, 6:16 a.m.)
Issued	19 years, 9 months ago (Nov. 22, 2005)
Published	19 years, 9 months ago (Nov. 22, 2005)
Published Online	19 years, 9 months ago (Nov. 22, 2005)
Published Print	19 years, 8 months ago (Dec. 1, 2005)

Funders 0

None

BibTeX

@article{Brough_2005, title={Agonist-induced regulation of mitochondrial and endoplasmic reticulum motility}, volume={392}, ISSN={1470-8728}, url={http://dx.doi.org/10.1042/bj20050738}, DOI={10.1042/bj20050738}, number={2}, journal={Biochemical Journal}, publisher={Portland Press Ltd.}, author={Brough, David and Schell, Michael J. and Irvine, Robin F.}, year={2005}, month=nov, pages={291–297} }

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