The DOI matches its Crossref record; 63 of the 63 references it cites were found in a registry or an index.
Cooperative and independent roles of the Drp1 adaptors Mff, MiD49 and MiD51 in mitochondrial fission
Open accessAbstract
Cytosolic dynamin-related protein 1 (Drp1, also known as DNM1L) is required for both mitochondrial and peroxisomal fission. Drp1-dependent division of these organelles is facilitated by a number of adaptor proteins at mitochondrial and peroxisomal surfaces. To investigate the interplay of these adaptor proteins, we used gene-editing technology to create a suite of cell lines lacking the adaptors MiD49 (also known as MIEF2), MiD51 (also known as MIEF1), Mff and Fis1. Increased mitochondrial connectivity was observed following loss of individual adaptors, and this was further enhanced following the combined loss of MiD51 and Mff. Moreover, loss of adaptors also conferred increased resistance of cells to intrinsic apoptotic stimuli, with MiD49 and MiD51 showing the more prominent role. Using a proximity-based biotin labeling approach, we found close associations between MiD51, Mff and Drp1, but not Fis1. Furthermore, we found that MiD51 can suppress Mff-dependent enhancement of Drp1 GTPase activity. Our data indicates that Mff and MiD51 regulate Drp1 in specific ways to promote mitochondrial fission.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“In mammals, there are no orthologues for MDV1 and Cav 4, and recent evidence suggests that Fis1 is not required for fission [89, 90].”
From The connection between the dynamic remodeling of the mitochondrial network and the regulation of muscle mass (2021) · cites this paper as [89]
Citations
Cites
NIH Image to ImageJ: 25 years of image analysis
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012) · Nature Methods · doi:10.1038/nmeth.2089 · Cited by 64,638
Andromeda: A Peptide Search Engine Integrated into the MaxQuant Environment
Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V., & Mann, M. (2011) · Journal of Proteome Research · doi:10.1021/pr101065j · Cited by 5,520
The BCL-2 protein family: opposing activities that mediate cell death
Youle, R. J., & Strasser, A. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2308 · Cited by 4,806
Rappsilber, J., Mann, M., & Ishihama, Y. (2007) · Nature Protocols · doi:10.1038/nprot.2007.261 · Cited by 4,641
Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity
Ran, F. A., Hsu, P. D., Lin, C.-Y., Gootenberg, J. S., Konermann, S., Trevino, A. E., Scott, D. A., Inoue, A., Matoba, S., Zhang, Y., et al. (2013) · Cell · doi:10.1016/j.cell.2013.08.021 · Cited by 3,299
The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy
Lazarou, M., Sliter, D. A., Kane, L. A., Sarraf, S. A., Wang, C., Burman, J. L., Sideris, D. P., Fogel, A. I., & Youle, R. J. (2015) · Nature · doi:10.1038/nature14893 · Cited by 2,774
ER Tubules Mark Sites of Mitochondrial Division
Friedman, J. R., Lackner, L. L., West, M., DiBenedetto, J. R., Nunnari, J., & Voeltz, G. K. (2011) · Science · doi:10.1126/science.1207385 · Cited by 2,072
Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases
Chen, H., & Chan, D. C. (2009) · Human Molecular Genetics · doi:10.1093/hmg/ddp326 · Cited by 1,506
Mitochondria in Apoptosis: Bcl-2 Family Members and Mitochondrial Dynamics
Martinou, J., & Youle, R. J. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.06.017 · Cited by 1,395
CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing
Montague, T. G., Cruz, J. M. B. S., Gagnon, J. A., Church, G. M., & Valen, E. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku410 · Cited by 1,246
Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission
Losón, O. C., Song, Z., Chen, H., & Chan, D. C. (2013) · Molecular Biology of the Cell · doi:10.1091/mbc.e12-10-0721 · Cited by 1,235
Otera, H., Wang, C., Cleland, M. M., Setoguchi, K., Yokota, S., Youle, R. J., & Mihara, K. (2010) · Journal of Cell Biology · doi:10.1083/jcb.201007152 · Cited by 1,110 · cited 7×
“…cytosolic GTPase that is recruited to the surface of the organelle by the adaptors Mff, MiD49 (also known as MIEF2) and MiD51 (also known as MIEF1) (Gandre-Babbe and van der Bliek, 2008; Ingerman et al., 2005; Legesse-Miller et al., 2003; Otera et al., 2010; Palmer et al., 2011; Zhao et al., 2011).”
BackgroundResultInfluentialAMP-activated protein kinase mediates mitochondrial fission in response to energy stress
Toyama, E. Q., Herzig, S., Courchet, J., Lewis, T. L., Losón, O. C., Hellberg, K., Young, N. P., Chen, H., Polleux, F., Chan, D. C., et al. (2016) · Science · doi:10.1126/science.aab4138 · Cited by 1,085
Mitochondrial dynamics and inheritance during cell division, development and disease
Mishra, P., & Chan, D. C. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3877 · Cited by 1,076
Ishihara, N., Nomura, M., Jofuku, A., Kato, H., Suzuki, S. O., Masuda, K., Otera, H., Nakanishi, Y., Nonaka, I., Goto, Y.-I., et al. (2009) · Nature Cell Biology · doi:10.1038/ncb1907 · Cited by 1,066
Karbowski, M., Lee, Y.-J., Gaume, B., Jeong, S.-Y., Frank, S., Nechushtan, A., Santel, A., Fuller, M., Smith, C. L., & Youle, R. J. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200209124 · Cited by 846
An Actin-Dependent Step in Mitochondrial Fission Mediated by the ER-Associated Formin INF2
Korobova, F., Ramabhadran, V., & Higgs, H. N. (2013) · Science · doi:10.1126/science.1228360 · Cited by 817
Mitochondrial fission in apoptosis
Youle, R. J., & Karbowski, M. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1697 · Cited by 773
Gandre-Babbe, S., & van der Bliek, A. M. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-12-1287 · Cited by 769
Mozdy, A. D., McCaffery, J. M., & Shaw, J. M. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.2.367 · Cited by 731
The dynamin-related GTPase Drp1 is required for embryonic and brain development in mice
Wakabayashi, J., Zhang, Z., Wakabayashi, N., Tamura, Y., Fukaya, M., Kensler, T. W., Iijima, M., & Sesaki, H. (2009) · Journal of Cell Biology · doi:10.1083/jcb.200903065 · Cited by 667
hFis1, a Novel Component of the Mammalian Mitochondrial Fission Machinery
James, D. I., Parone, P. A., Mattenberger, Y., & Martinou, J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m303758200 · Cited by 653
MiD49 and MiD51, new components of the mitochondrial fission machinery
Palmer, C. S., Osellame, L. D., Laine, D., Koutsopoulos, O. S., Frazier, A. E., & Ryan, M. T. (2011) · The EMBO Reports · doi:10.1038/embor.2011.54 · Cited by 649 · cited 8×
“…cytosolic GTPase that is recruited to the surface of the organelle by the adaptors Mff, MiD49 (also known as MIEF2) and MiD51 (also known as MIEF1) (Gandre-Babbe and van der Bliek, 2008; Ingerman et al., 2005; Legesse-Miller et al., 2003; Otera et al., 2010; Palmer et al., 2011; Zhao et al., 2011).”
BackgroundInfluentialSelf-citationDnm1 forms spirals that are structurally tailored to fit mitochondria
Ingerman, E., Perkins, E. M., Marino, M., Mears, J. A., McCaffery, J. M., Hinshaw, J. E., & Nunnari, J. (2005) · Journal of Cell Biology · doi:10.1083/jcb.200506078 · Cited by 621
Imbalanced OPA1 processing and mitochondrial fragmentation cause heart failure in mice
Wai, T., García-Prieto, J., Baker, M. J., Merkwirth, C., Benit, P., Rustin, P., Rupérez, F. J., Barbas, C., Ibañez, B., & Langer, T. (2015) · Science · doi:10.1126/science.aad0116 · Cited by 551
BioID: A Screen for Protein‐Protein Interactions
Roux, K. J., Kim, D. I., & Burke, B. E. (2013) · Current Protocols in Protein Science · doi:10.1002/0471140864.ps1923s74 · Cited by 505
Dynamin-like protein 1 is involved in peroxisomal fission
Koch, A., Thiemann, M., Grabenbauer, M., Yoon, Y., McNiven, M. A., & Schrader, M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211761200 · Cited by 374
Zhao, J., Liu, T., Jin, S., Wang, X., Qu, M., Uhlén, P., Tomilin, N., Shupliakov, O., Lendahl, U., & Nistér, M. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.198 · Cited by 370
Ji, W.-K., Hatch, A. L., Merrill, R. A., Strack, S., & Higgs, H. N. (2015) · eLife · doi:10.7554/elife.11553 · Cited by 347
Manor, U., Bartholomew, S. R., Golani, G., Christenson, E. T., Kozlov, M. M., Higgs, H. N., Spudich, J. A., & Lippincott‐Schwartz, J. (2015) · eLife · doi:10.7554/elife.08828 · Cited by 342
MAPL SUMOylation of Drp1 Stabilizes an ER/Mitochondrial Platform Required for Cell Death
Prudent, J., Zunino, R., Sugiura, A., Mattie, S., Shore, G. C., & McBride, H. M. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.08.001 · Cited by 335
Levels of human Fis1 at the mitochondrial outer membrane regulate mitochondrial morphology
Stojanovski, D., Koutsopoulos, O. S., Okamoto, K., & Ryan, M. T. (2004) · Journal of Cell Science · doi:10.1242/jcs.01058 · Cited by 332
Self-citationDeterminants and Functions of Mitochondrial Behavior
Labbè, K., Murley, A., & Nunnari, J. M. (2014) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-101011-155756 · Cited by 324
Mitochondrial Rab GAPs govern autophagosome biogenesis during mitophagy
Yamano, K., Fogel, A. I., Wang, C., van der Bliek, A. M., & Youle, R. J. (2014) · eLife · doi:10.7554/elife.01612 · Cited by 307
Palmer, C. S., Elgass, K. D., Parton, R. G., Osellame, L. D., Stojanovski, D., & Ryan, M. T. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.479873 · Cited by 301
Self-citationHigh levels of Fis1, a pro-fission mitochondrial protein, trigger autophagy
Gomes, L. C., & Scorrano, L. (2008) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2008.05.442 · Cited by 242
Ban-Ishihara, R., Ishihara, T., Sasaki, N., Mihara, K., & Ishihara, N. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301951110 · Cited by 231
miR-484 regulates mitochondrial network through targeting Fis1
Wang, K., Long, B., Jiao, J.-Q., Wang, J., Liu, J., Li, Q., & Li, P. (2012) · Nature Communications · doi:10.1038/ncomms1770 · Cited by 230
Drp1-dependent mitochondrial fission via MiD49/51 is essential for apoptotic cristae remodeling
Otera, H., Miyata, N., Kuge, O., & Mihara, K. (2016) · Journal of Cell Biology · doi:10.1083/jcb.201508099 · Cited by 229
Mitochondrial division and fusion in metabolism
Roy, M., Reddy, P. H., Iijima, M., & Sesaki, H. (2015) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2015.02.001 · Cited by 215
Li, S., Xu, S., Roelofs, B. A., Boyman, L., Lederer, W. J., Sesaki, H., & Karbowski, M. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201404050 · Cited by 214
Mutations in Fis1 disrupt orderly disposal of defective mitochondria
Shen, Q., Yamano, K., Head, B. P., Kawajiri, S., Cheung, J. T. M., Wang, C., Cho, J.-H., Hattori, N., Youle, R. J., & van der Bliek, A. M. (2014) · Molecular Biology of the Cell · doi:10.1091/mbc.e13-09-0525 · Cited by 209
Interchangeable adaptors regulate mitochondrial dynamin assembly for membrane scission
Koirala, S., Guo, Q., Kalia, R., Bui, H., Eckert, D. M., Frost, A. S., & Shaw, J. M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1300855110 · Cited by 201
Constriction and Dnm1p Recruitment Are Distinct Processes in Mitochondrial Fission
Legesse-Miller, A., Massol, R., & Kirchhausen, T. L. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-10-0657 · Cited by 197
The mitochondrial fission receptor Mff selectively recruits oligomerized Drp1
Liu, R., & Chan, D. C. (2015) · Molecular Biology of the Cell · doi:10.1091/mbc.e15-08-0591 · Cited by 193
A Role for the Ancient SNARE Syntaxin 17 in Regulating Mitochondrial Division
Arasaki, K., Shimizu, H., Mogari, H., Nishida, N., Hirota, N., Furuno, A., Kudo, Y., Baba, M., Baba, N., Cheng, J., et al. (2015) · Developmental Cell · doi:10.1016/j.devcel.2014.12.011 · Cited by 173
A dimeric equilibrium intermediate nucleates Drp1 reassembly on mitochondrial membranes for fission
Macdonald, P. J., Stepanyants, N., Mehrotra, N., Mears, J. A., Qi, X., Sesaki, H., & Ramachandran, R. (2014) · Molecular Biology of the Cell · doi:10.1091/mbc.e14-02-0728 · Cited by 169
Self-citationTitration of mitochondrial fusion rescues Mff -deficient cardiomyopathy
Chen, H., Ren, S., Clish, C., Jain, M., Mootha, V., McCaffery, J. M., & Chan, D. C. (2015) · Journal of Cell Biology · doi:10.1083/jcb.201507035 · Cited by 168
Shaping the dynamic mitochondrial network
Lackner, L. L. (2014) · BMC Biology · doi:10.1186/1741-7007-12-35 · Cited by 156
Mitochondrial Dynamics and Apoptosis—the ER Connection
Hoppins, S. C., & Nunnari, J. M. (2012) · Science · doi:10.1126/science.1224709 · Cited by 137
Johnston, A. J., Hoogenraad, J., Dougan, D. A., Truscott, K. N., Yano, M., Mori, M., Hoogenraad, N. J., & Ryan, M. T. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m205613200 · Cited by 133
Self-citationFrancy, C. A., Alvarez, F. J. D., Zhou, L., Ramachandran, R., & Mears, J. A. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.610881 · Cited by 116
Self-citationStrack, S., & Cribbs, J. T. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.342105 · Cited by 113
Clinton, R. W., Francy, C. A., Ramachandran, R., Qi, X., & Mears, J. A. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.680025 · Cited by 107
Self-citationElgass, K., Smith, E. A., LeGros, M., Larabell, C. A., & Ryan, M. T. (2015) · Journal of Cell Science · doi:10.1242/jcs.169136 · Cited by 106
Self-citationStructural and functional analysis of MiD51, a dynamin receptor required for mitochondrial fission
Richter, V., Palmer, C. S., Osellame, L. D., Singh, A. P., Elgass, K., Stroud, D. A., Sesaki, H., Kvansakul, M., & Ryan, M. T. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201311014 · Cited by 106
Self-citationMacdonald, P. J., Francy, C. A., Stepanyants, N., Lehman, L., Baglio, A. J., Mears, J. A., Qi, X., & Ramachandran, R. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.680181 · Cited by 100
Self-citationOpening the doors to cytochrome c: Changes in mitochondrial shape and apoptosis
Scorrano, L. (2009) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2009.04.016 · Cited by 96
The Mitochondrial Fission Receptor MiD51 Requires ADP as a Cofactor
Losón, O. C., Liu, R., Rome, M. E., Meng, S., Kaiser, J. T., Shan, S., & Chan, D. C. (2014) · Structure · doi:10.1016/j.str.2014.01.001 · Cited by 94
Stroud, D. A., Formosa, L. E., Wijeyeratne, X. W., Nguyen, T. N., & Ryan, M. T. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.c112.436766 · Cited by 82
Self-citationCharacterization of mitochondrial FOXRED1 in the assembly of respiratory chain complex I
Formosa, L. E., Mimaki, M., Frazier, A. E., McKenzie, M., Stait, T. L., Thorburn, D. R., Stroud, D. A., & Ryan, M. T. (2015) · Human Molecular Genetics · doi:10.1093/hmg/ddv058 · Cited by 75
Self-citationSplitting up the powerhouse: structural insights into the mechanism of mitochondrial fission
Richter, V., Singh, A. P., Kvansakul, M., Ryan, M. T., & Osellame, L. D. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1950-y · Cited by 48
Self-citationLackner, L. L. (2013) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2013.02.011 · Cited by 48
Flagged first, then by citations
Cited by
Sorted by citations
The cell biology of mitochondrial membrane dynamics
Giacomello, M., Pyakurel, A., Glytsou, C., & Scorrano, L. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0210-7 · Cited by 1,550
Mitochondrial Dynamics and Its Involvement in Disease
Chan, D. C. (2020) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev-pathmechdis-012419-032711 · Cited by 1,416
Mitochondrial dynamics: overview of molecular mechanisms
Tilokani, L., Nagashima, S., Paupe, V., & Prudent, J. (2018) · Essays in Biochemistry · doi:10.1042/ebc20170104 · Cited by 1,397
Distinct fission signatures predict mitochondrial degradation or biogenesis.
Kleele, T., Rey, T., Winter, J., Zaganelli, S., Mahecic, D., Perreten Lambert, H., Ruberto, F. P., Nemir, M., Wai, T., Pedrazzini, T., et al. (2021) · Nature · doi:10.1038/s41586-021-03510-6 · Cited by 794
The functional universe of membrane contact sites
Prinz, W. A., Toulmay, A., & Balla, T. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0180-9 · Cited by 770
Metadata
- Authors
- Osellame, L. D., Singh, A. P., Stroud, D. A., Palmer, C. S., Stojanovski, D., Ramachandran, R., & Ryan, M. T.
- Affiliations
- Monash University (AU)
- La Trobe University (AU)
- Burnet Institute (AU)
- The University of Melbourne (AU)
- Case Western Reserve University (US)
- ORCID
- Venue
- Journal of Cell Science
- Publisher
- The Company of Biologists
- Published
- 2016-06-01
- Volume
- 129
- Issue
- 11
- Pages
- 2170-2181
- ISSN
- 0021-9533 (ISSN-L)
- 1477-9137
- PMC
- PMC6919635
- OpenAlex
- W2415256624
- Cited by
- 336
- References
- 63
- Citations by year
- 2026: 18 · 2025: 34 · 2024: 28 · 2023: 30 · 2022: 35 · 2021: 48 · 2020: 36 · 2019: 31 · 2018: 37 · 2017: 29 · 2016: 9
- FWCI
- 18.36
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Cell Science (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- National Health and Medical Research Council (1049968)
- American Heart Association (13BGIA14810010)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Keywords
- mitochondrial fission, Drp1, Mff, MiD51, Fis1, apoptosis resistance, protein-protein interaction
- MeSH terms
- Gene Editing, Animals, Cell Line, Membrane Proteins, Mice, Inbred C57BL, Staining and Labeling, Cell Death, Receptors, Cytoplasmic and Nuclear, Mice, Knockout, Peroxisomes, Mitochondrial Proteins, Dynamins, Mitochondrial Dynamics
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
