Coordinated Behavior of Mitochondria in Both Space and Time: A Reactive Oxygen Species-Activated Wave of Mitochondrial Depolarization
Open accessAbstract
Reactive oxygen species (ROS) can trigger a transient burst of mitochondrial ROS production via ROS activation of the mitochondrial permeability transition pore (MPTP), a phenomenon termed ROS-induced ROS release (RIRR). The goal of this study was to investigate if the generation of ROS in a discrete region of a cardiomyocyte could serve to propagate RIRR-mediated mitochondrial depolarizations throughout a cell. Our experiments revealed that localized RIRR activated either RIRR-mediated fluctuations in mitochondrial membrane potential (time period: 3-10 min) or a traveling wave of depolarization of the cell's mitochondria (velocity: approximately 5 microm/min). Both phenomena appeared to be mediated by the mitochondrial permeability transition pore and eventually encompassed the majority of the mitochondrial population of both isolated rat and rabbit cardiomyocytes. Furthermore, depolarization was often reversible; the waves of depolarization were then followed by a rapid (approximately 40 microm/min) repolarization wave of the mitochondria. We show that the RIRR can function to communicate the mitochondrial permeability transition from one mitochondrion to another in the isolated adult cardiomyocyte.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The text we found for this paper looks like another document, so the self-check wasn’t run.
Cites
Oxyl radicals, redox-sensitive signalling cascades and antioxidants
Genestra, M. (2007) · Cellular Signalling · doi:10.1016/j.cellsig.2007.04.009 · Cited by 4,930 · see citing works
LeBel, C. P., Ischiropoulos, H., & Bondy, S. C. (1992) · Chemical Research in Toxicology · doi:10.1021/tx00026a012 · Cited by 2,694 · see citing works
The mitochondrial permeability transition pore and its role in cell death
CROMPTON, M. (1999) · Biochemical Journal · doi:10.1042/bj3410233 · Cited by 2,432 · see citing works
The mitochondrial permeability transition
Zoratti, M., & Szabó, I. (1995) · Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes · doi:10.1016/0304-4157(95)00003-a · Cited by 2,395 · see citing works
The cellular production of hydrogen peroxide
Boveris, A., Oshino, N., & Chance, B. (1972) · Biochemical Journal · doi:10.1042/bj1280617 · Cited by 1,549 · see citing works
Reactive Oxygen Species (Ros-Induced) Ros Release
Zorov, D. B., Filburn, C. R., Klotz, L.-O., Zweier, J. L., & Sollott, S. J. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.7.1001 · Cited by 1,412 · see citing works
Lemasters, J. J., Nieminen, A.-L., Qian, T., Trost, L. C., Elmore, S. P., Nishimura, Y., Crowe, R. A., Cascio, W. E., Bradham, C. A., Brenner, D. A., et al. (1998) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(98)00112-1 · Cited by 1,387 · see citing works
Self-citationDirect measurement of free radical generation following reperfusion of ischemic myocardium.
Zweier, J. L., Flaherty, J. T., & Weisfeldt, M. L. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.5.1404 · Cited by 1,189 · see citing works
Ichas, F., Jouaville, L. S., & Mazat, J. (1997) · Cell · doi:10.1016/s0092-8674(00)80301-3 · Cited by 754 · see citing works
Vanden Hoek, T. L., Becker, L. B., Shao, Z., Li, C., & Schumacker, P. T. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.29.18092 · Cited by 721 · see citing works
Han, D., Antunes, F., Canali, R., Rettori, D., & Cadenas, E. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m210269200 · Cited by 711 · see citing works
The mitochondrial permeability transition initiates autophagy in rat hepatocytes
Elmore, S. P., Qian, T., Grissom, S. F., & Lemasters, J. J. (2001) · The FASEB Journal · doi:10.1096/fj.01-0206fje · Cited by 607 · see citing works
Self-citationAon, M. A., Cortassa, S., Marbán, E., & O'Rourke, B. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m302673200 · Cited by 521 · see citing works
Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen.
Leach, J. K., Tuyle, G. V., Lin, P.-S., Schmidt‐Ullrich, R., & Mikkelsen, R. B. (2001) · PubMed · Cited by 511 · see citing works
Mitochondrial filaments and clusters as intracellular power-transmitting cables
Skulachev, V. P. (2001) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(00)01735-7 · Cited by 477 · see citing works
Generation of superoxide in cardiomyocytes during ischemia before reperfusion
Becker, L. B., Hoek, T. L. V., Shao, Z., Li, C., & Schumacker, P. T. (1999) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1999.277.6.h2240 · Cited by 413 · see citing works
Hoek, T. L. V., Li, C., Shao, Z., Schumacker, P. T., & Becker, L. B. (1997) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1997.0497 · Cited by 398 · see citing works
Modulation of Mitochondrial Function by Hydrogen Peroxide
Nulton-Persson, A. C., & Szweda, L. I. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m100320200 · Cited by 393 · see citing works
Nieminen, A. L., Saylor, A. K., Tesfai, S. A., Herman, B. A., & Lemasters, J. J. (1995) · Biochemical Journal · doi:10.1042/bj3070099 · Cited by 381 · see citing works
Henzler, T., & Steudle, E. (2000) · Journal of Experimental Botany · doi:10.1093/jexbot/51.353.2053 · Cited by 376 · see citing works
Ratio‐fluorescence microscopy of lipid oxidation in living cells using C11‐BODIPY 581/591
Pap, E. H. W., Drummen, G. P. C., Winter, V. J., Kooij, T. W. A., Rijken, P. J., WIRTZ, K. W. A., den Kamp, J. A. F. O., Hage, W. J., & Post, J. A. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)00696-1 · Cited by 332 · see citing works
Boitier, E., Rea, R., & Duchen, M. R. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.145.4.795 · Cited by 298 · see citing works
Mitochondrial ROS initiate phosphorylation of p38 MAP kinase during hypoxia in cardiomyocytes
Kulisz, A., Chen, N., Chandel, N. S., Shao, Z., & Schumacker, P. T. (2002) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00326.2001 · Cited by 287 · see citing works
Amchenkova, A. A., Bakeeva, L. E., Chentsov, Y. S., Skulachev, V. P., & Zorov, D. B. (1988) · The Journal of cell biology · doi:10.1083/jcb.107.2.481 · Cited by 284 · see citing works
Imaging the Permeability Pore Transition in Single Mitochondria
Hüser, J., Rechenmacher, C. E., & Blatter, L. A. (1998) · Biophysical Journal · doi:10.1016/s0006-3495(98)77920-2 · Cited by 269 · see citing works
HüSER, J., & BLATTER, L. A. (1999) · Biochemical Journal · doi:10.1042/bj3430311 · Cited by 266 · see citing works
Giorgi, F. D., Lartigue, L., Bauer, M. K. A., Schubert, A., Grimm, S., Hanson, G. T., Remington, S. J., Youle, R. J., & Ichas, F. (2002) · The FASEB Journal · doi:10.1096/fj.01-0269fje · Cited by 259 · see citing works
Duchen, M. R., Leyssens, A., & Crompton, M. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.142.4.975 · Cited by 246 · see citing works
Propagation of the apoptotic signal by mitochondrial waves
Pacher, P., & Hajnóczky, G. (2001) · The EMBO Journal · doi:10.1093/emboj/20.15.4107 · Cited by 240 · see citing works
Armstrong, J. S., & Jones, D. P. (2002) · The FASEB Journal · doi:10.1096/fj.02-0097fje · Cited by 220 · see citing works
Subcellular metabolic transients and mitochondrial redox waves in heart cells
Romashko, D. N., Marbán, E., & O'Rourke, B. P. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.4.1618 · Cited by 211 · see citing works
Šutovský, P., Navara, C. S., & Schatten, G. P. (1996) · Biology of Reproduction · doi:10.1095/biolreprod55.6.1195 · Cited by 206 · see citing works
Contribution of L-type Ca2+current to electrical activity in sinoatrial nodal myocytes of rabbits
Verheijck, E. E., van Ginneken, A. C. G., Wilders, R., et al. (1999) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1999.276.3.h1064 · Cited by 121 · see citing works
Mitochondria are morphologically heterogeneous within cells
Collins, T. J., & Bootman, M. D. (2003) · Journal of Experimental Biology · doi:10.1242/jeb.00244 · Cited by 116 · see citing works
Koretsune, Y., & Marbán, E. (1990) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1990.258.1.h9 · Cited by 111 · see citing works
Swift, L., & Sarvazyan, N. A. (2000) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2000.278.3.h982 · Cited by 102 · see citing works
Ruled by waves? Intracellular and intercellular calcium signalling
Røttingen, & IVERSEN (2000) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.2000.00732.x · Cited by 94 · see citing works
Selective inactivation of redox-sensitive mitochondrial enzymes during cardiac reperfusion
Sadek, H. A., Humphries, K. M., Szweda, P. A., & Szweda, L. I. (2002) · Archives of Biochemistry and Biophysics · doi:10.1016/s0003-9861(02)00446-0 · Cited by 91 · see citing works
Signaling Pathway Involved in the Activation of Heart 6-Phosphofructo-2-kinase by Insulin
Lefebvre, V., Máchin, M.-C., Louckx, M. P., Rider, M. H., & Hue, L. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.37.22289 · Cited by 68 · see citing works
Self-citationThe mitochondrial inner membrane anion channel is inhibited by DIDS
Beavis, A. D., & Davatol-Hag, H. (1996) · Journal of Bioenergetics and Biomembranes · doi:10.1007/bf02110652 · Cited by 62 · see citing works
Fall, C. P., & Bennett, J. P. (1999) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(98)00177-7 · Cited by 44 · see citing works
Aronis, A., Komarnitsky, R., Shilo, S., & Tirosh, O. (2002) · Antioxidants and Redox Signaling · doi:10.1089/15230860260220157 · Cited by 37 · see citing works
Kinetic Modeling of Energy Metabolism and Superoxide Generation in Hepatocyte Mitochondria
Demin, O. V., Goryanin, I., Kholodenko, B. Ν., & Westerhoff, H. V. (2001) · Molecular Biology · doi:10.1023/a:1013211007465 · Cited by 25 · see citing works
Self-citationDemin, O. V., Горянин, И. И., Kholodenko, B. Ν., et al. (2002) · PubMed · Cited by 21 · see citing works
野崎, 哲., Kagaya, Y., Ishide, N., et al. (2001) · Cardiovascular Pathology · doi:10.1016/s1054-8807(01)00071-0 · Cited by 20 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Redox regulation of mitochondrial function
Handy, D. E., & Loscalzo, J. (2012) · Antioxidants & Redox Signaling · doi:10.1089/ars.2011.4123 · Cited by 588 · see citing works
Effects of ionizing radiation on mitochondria
Kam, W. W.-Y., & Banati, R. B. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.07.024 · Cited by 386 · see citing works
Loss of Mitofusin 2 Promotes Endoplasmic Reticulum Stress
Ngoh, G. A., Papanicolaou, K. N., & Walsh, K. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.359174 · Cited by 183 · see citing works
- Authors
- Brady, N. R., Elmore, S. P., van Beek, J. J. H. G. M., Krab, K., Courtoy, P. J., Hue, L., & Westerhoff, H. V.
- Affiliations
- Amsterdam Cardiovascular Sciences (NL)
- UCLouvain (BE)
- Corresponding author
- Westerhoff, Hans V.
- Venue
- Biophysical Journal
- Publisher
- Elsevier BV
- Published
- 2004-09
- Volume
- 87
- Issue
- 3
- Pages
- 2022-2034
- ISSN
- 0006-3495 (ISSN-L)
- PMC
- PMC1304605
- OpenAlex
- W2112524117
- Cited by
- 118
- References
- 45
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 2 · 2023: 1 · 2022: 3 · 2021: 1 · 2020: 3 · 2019: 5 · 2018: 4 · 2017: 7 · 2016: 3 · 2015: 7 · 2014: 6 · 2013: 8 · 2012: 10
- FWCI
- 2.13
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Biophysical Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam) (submittedVersion, public-domain)
- VU Research Portal (submittedVersion, other-oa)
- DIAL (Catholic University of Leuven) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- Fédération Wallonie-Bruxelles
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Pathology and Forensic Medicine › Cardiac Ischemia and Reperfusion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Keywords
- reactive oxygen species, mitochondrial permeability transition pore, mitochondrial depolarization, traveling waves, cardiomyocytes, mitochondrial membrane potential, mitochondrial reactive oxygen species, depolarization wave
- MeSH terms
- Animals, Calcium, Image Processing, Computer-Assisted, Kinetics, Light, Membrane Potentials, Mitochondria, Models, Biological, Rabbits, Rotenone, Time Factors, 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine, Reactive Oxygen Species, Microscopy, Confocal, Myocytes, Cardiac
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review