Kinesin-1–syntaphilin coupling mediates activity-dependent regulation of axonal mitochondrial transport
Open accessAbstract
Axonal mitochondria are recruited to synaptic terminals in response to neuronal activity, but the mechanisms underlying activity-dependent regulation of mitochondrial transport are largely unknown. In this paper, using genetic mouse model combined with live imaging, we demonstrate that syntaphilin (SNPH) mediates the activity-dependent immobilization of axonal mitochondria through binding to KIF5. In vitro analysis showed that the KIF5–SNPH coupling inhibited the motor adenosine triphosphatase. Neuronal activity further recruited SNPH to axonal mitochondria. This motor-docking interplay was induced by Ca2+ and synaptic activity and was necessary to establish an appropriate balance between motile and stationary axonal mitochondria. Deleting snph abolished the activity-dependent immobilization of axonal mitochondria. We propose an “Engine-Switch and Brake” model, in which SNPH acts both as an engine off switch by sensing mitochondrial Rho guanosine triphosphatase-Ca2+ and as a brake by anchoring mitochondria to the microtubule track. Altogether, our study provides new mechanistic insight into the molecular interplay between motor and docking proteins, which arrests axonal mitochondrial transport in response to changes in neuronal activity.
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Ca2+ is a key regulator of mitochondria motility and docking.
“it has been largely described that Ca2+ is a key regulator of mitochondria motility and docking44–49,107.”
From CYFIP1 governs the development of cortical axons by modulating calcium availability (2025) · cites this paper as [44]
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Cites
The Molecular Motor Toolbox for Intracellular Transport
Vale, R. D. (2003) · Cell · doi:10.1016/s0092-8674(03)00111-9 · Cited by 1,982 · see citing works
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 1,455 · see citing works
The axonal transport of mitochondria
Saxton, W. M., & Hollenbeck, P. J. (2012) · Journal of Cell Science · doi:10.1242/jcs.053850 · Cited by 1,198 · see citing works
Organelle isolation: functional mitochondria from mouse liver, muscle and cultured filroblasts
Frezza, C., Cipolat, S., & Scorrano, L. (2007) · Nature Protocols · doi:10.1038/nprot.2006.478 · Cited by 1,188 · see citing works
Hirokawa, N., Niwa, S., & Tanaka, Y. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.039 · Cited by 1,138 · see citing works
Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration
Sheng, Z., & Cai, Q. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3156 · Cited by 906 · see citing works
Self-citationThe Mechanism of Ca2+-Dependent Regulation of Kinesin-Mediated Mitochondrial Motility
Wang, X., & Schwarz, T. L. (2009) · Cell · doi:10.1016/j.cell.2008.11.046 · Cited by 871 · see citing works
Verstreken, P., Ly, C. V., Venken, K. J. T., Koh, T.-W., Zhou, Y., & Bellen, H. J. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.018 · Cited by 841 · see citing works
The axonal transport of mitochondria
Hollenbeck, P. J., & Saxton, W. M. (2005) · Journal of Cell Science · doi:10.1242/jcs.02745 · Cited by 771 · see citing works
Pilling, A. D., Horiuchi, D., Lively, C. M., & Saxton, W. M. (2006) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-06-0526 · Cited by 696 · see citing works
Miro1 Is a Calcium Sensor for Glutamate Receptor-Dependent Localization of Mitochondria at Synapses
MacAskill, A. F., Rinholm, J. E., Twelvetrees, A. E., Arancibia‐Cárcamo, I. L., Muir, J., Fransson, Å., Aspenström, P., Attwell, D., & Kittler, J. T. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.030 · Cited by 677 · see citing works
Axonal Transport of Mitochondria to Synapses Depends on Milton, a Novel Drosophila Protein
Stowers, R. S., Megeath, L. J., Górska‐Andrzejak, J., Meinertzhagen, I. A., & Schwarz, T. L. (2002) · Neuron · doi:10.1016/s0896-6273(02)01094-2 · Cited by 643 · see citing works
Misko, A. L., Jiang, S., Wegorzewska, I., Milbrandt, J., & Baloh, R. H. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.6248-09.2010 · Cited by 643 · see citing works
The GTPase dMiro Is Required for Axonal Transport of Mitochondria to Drosophila Synapses
Guo, X., Macleod, G. T., Wellington, A. J., Hu, F., Panchumarthi, S., Schoenfield, M., Marin, L., Charlton, M. P., Atwood, H. L., & Zinsmaier, K. E. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.027 · Cited by 619 · see citing works
Kang, J.-S., Tian, J.-H., Pan, P.-Y., Zald, P., Li, C., Deng, C., & Sheng, Z.-H. (2008) · Cell · doi:10.1016/j.cell.2007.11.024 · Cited by 598 · see citing works
Self-citationProtein–RNA interactions: new genomic technologies and perspectives
König, J., Zarnack, K., Luscombe, N. M., & Ule, J. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3141 · Cited by 555 · see citing works
Bidirectional Ca <sup>2+</sup> -dependent control of mitochondrial dynamics by the Miro GTPase
Saotome, M., Safiulina, D., Szabadkai, G., Das, S., Fransson, Å., Aspenstrom, P., Rizzuto, R., & Hajnóczky, G. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808953105 · Cited by 538 · see citing works
Axonal mitochondrial transport and potential are correlated
Miller, K. E., & Sheetz, M. P. (2004) · Journal of Cell Science · doi:10.1242/jcs.01130 · Cited by 512 · see citing works
The atypical Rho GTPases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking.
Fransson, S., Ruusala, A., & Aspenström, P. (2006) · Biochemical and Biophysical Research Communications - BBRC · doi:10.1016/j.bbrc.2006.03.163 · Cited by 479 · see citing works
Control of mitochondrial motility and distribution by the calcium signal
Yi, M., Weaver, D., & Hajnóczky, G. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200406038 · Cited by 476 · see citing works
Mitochondrial Involvement in Post-Tetanic Potentiation of Synaptic Transmission
Tang, Y.-G., & Zucker, R. S. (1997) · Neuron · doi:10.1016/s0896-6273(00)81248-9 · Cited by 441 · see citing works
Mitochondrial Trafficking to Synapses in Cultured Primary Cortical Neurons
Chang, D. T. W., Honick, A. S., & Reynolds, I. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1012-06.2006 · Cited by 391 · see citing works
Control of mitochondrial transport and localization in neurons
MacAskill, A. F., & Kittler, J. T. (2009) · Trends in Cell Biology · doi:10.1016/j.tcb.2009.11.002 · Cited by 372 · see citing works
Cai, Q., Zakaria, H. M., Simone, A., & Sheng, Z. (2012) · Current Biology · doi:10.1016/j.cub.2012.02.005 · Cited by 332 · see citing works
Self-citationGlutamate Decreases Mitochondrial Size and Movement in Primary Forebrain Neurons
Rintoul, G. L., Filiano, A. J., Brocard, J. B., Kress, G. J., & Reynolds, I. J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-21-07881.2003 · Cited by 326 · see citing works
High Ca2+-phosphate transfection efficiency in low-density neuronal cultures
Jiang, M., & Chen, G. (2006) · Nature Protocols · doi:10.1038/nprot.2006.86 · Cited by 304 · see citing works
Further observations on hippocampal neurons in dispersed cell culture
Banker, G. A., & Cowan, W. M. (1979) · Journal of Comparative Neurology · doi:10.1002/cne.901870302 · Cited by 285 · see citing works
Hirokawa, N., Sato-Yoshitake, R., Yoshida, T., & Kawashima, T. (1990) · The Journal of Cell Biology · doi:10.1083/jcb.111.3.1027 · Cited by 269 · see citing works
Differential trafficking of Kif5c on tyrosinated and detyrosinated microtubules in live cells
Dunn, S., Morrison, E. E., Liverpool, T. B., Molina-París, C., Cross, R. A., Alonso, M. C., & Peckham, M. (2008) · Journal of Cell Science · doi:10.1242/jcs.026492 · Cited by 242 · see citing works
Cai, Q., Lü, L., Tian, J.-H., Zhu, Y.-B., Qiao, H., & Sheng, Z. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.022 · Cited by 241 · see citing works
Self-citation<i>Drosophila</i>Miro Is Required for Both Anterograde and Retrograde Axonal Mitochondrial Transport
Russo, G. J., Louie, K., Wellington, A., Macleod, G. T., Hu, F., Panchumarthi, S., & Zinsmaier, K. E. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5417-08.2009 · Cited by 217 · see citing works
Cargo Transport: Two Motors Are Sometimes Better Than One
Gross, S. P., Vershinin, M. D., & Shubeita, G. T. (2007) · Current Biology · doi:10.1016/j.cub.2007.04.025 · Cited by 216 · see citing works
Identification of SCF Ubiquitin Ligase Substrates by Global Protein Stability Profiling
Yen, H.-C. S., & Elledge, S. J. (2008) · Science · doi:10.1126/science.1160462 · Cited by 209 · see citing works
Stable kinesin and dynein assemblies drive the axonal transport of mammalian prion protein vesicles
Encalada, S. E., Szpankowski, L., Xia, C.-H., & Goldstein, L. S. B. (2011) · Cell · doi:10.1016/j.cell.2011.01.021 · Cited by 206 · see citing works
Brickley, K., & Stephenson, F. A. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.236018 · Cited by 176 · see citing works
Popov, V. I., Medvedev, N. I., Davies, H. A., & Stewart, M. G. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20682 · Cited by 175 · see citing works
MacAskill, A. F., Brickley, K., Stephenson, F. A., & Kittler, J. T. (2008) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2008.10.016 · Cited by 171 · see citing works
A Direct Interaction between Cytoplasmic Dynein and Kinesin I May Coordinate Motor Activity
Ligon, L. A., Tokito, M. K., Finklestein, J. M., Grossman, F. E., & Holzbaur, E. L. F. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313472200 · Cited by 164 · see citing works
Gauvreau, K., & Pagano, M. (1993) · PubMed · Cited by 111 · see citing works
KIF5B Motor Adaptor Syntabulin Maintains Synaptic Transmission in Sympathetic Neurons
Ma, H., Cai, Q., Lu, W., Sheng, Z., & Mochida, S. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.2517-09.2009 · Cited by 101 · see citing works
Self-citationLao, G., Scheuß, V., Gerwin, C. M., Su, Q., Mochida, S., Rettig, J., & Sheng, Z. (2000) · Neuron · doi:10.1016/s0896-6273(00)80882-x · Cited by 93 · see citing works
Self-citationDynein Light Chain LC8 Regulates Syntaphilin-Mediated Mitochondrial Docking in Axons
Chen, Y., Gerwin, C. M., & Sheng, Z. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1472-09.2009 · Cited by 88 · see citing works
Self-citationSmith, M. J., Pozo, K., Brickley, K., & Stephenson, F. A. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m600522200 · Cited by 82 · see citing works
Moving or Stopping Mitochondria: Miro as a Traffic Cop by Sensing Calcium
Cai, Q., & Sheng, Z. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.003 · Cited by 66 · see citing works
Self-citationCho, K., Yi, H., Desai, R. M., Hand, A. R., Haas, A. L., & Ferreira, P. A. (2009) · EMBO Reports · doi:10.1038/embor.2009.29 · Cited by 58 · see citing works
Structure and Dynamics of the Homodimeric Dynein Light Chain km23
Ilangovan, U., Ding, W., Zhong, Y., Wilson, C. L., Groppe, J. C., Trbovich, J. T., Zúñiga, J. E., Demeler, B., Tang, Q., Gao, G., et al. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.07.002 · Cited by 35 · see citing works
Helical and Expanded Conformation of Equine β-Lactoglobulin in the Cold-denatured State
Yamada, Y., Yajima, T., Fujiwara, K., Arai, M., Ito, K., Shimizu, A., Kihara, H., Kuwajima, K., Amemiya, Y., & Ikeguchi, M. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.05.003 · Cited by 29 · see citing works
An Improved Microscope for Bead and Surface-Based Motility Assays
Carter, N., & Cross, R. A. (2001) · Humana Press eBooks · doi:10.1385/1-59259-069-1:73 · Cited by 7 · see citing works
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Friedman, J. R., & Nunnari, J. (2014) · Nature · doi:10.1038/nature12985 · Cited by 1,803 · see citing works
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Mishra, P., & Chan, D. C. (2016) · The Journal of Cell Biology · doi:10.1083/jcb.201511036 · Cited by 1,096 · see citing works
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 1,038 · see citing works
Mitochondrial dynamics and mitochondrial quality control
Ni, H.-M., Williams, J. A., & Ding, W.-X. (2015) · Redox Biology · doi:10.1016/j.redox.2014.11.006 · Cited by 931 · see citing works
Axonal transport: cargo-specific mechanisms of motility and regulation
Maday, S., Twelvetrees, A. E., Moughamian, A. J., & Holzbaur, E. L. F. (2014) · Neuron · doi:10.1016/j.neuron.2014.10.019 · Cited by 683 · see citing works
Mitochondrial dynamics in adaptive and maladaptive cellular stress responses
Eisner, V., Picard, M., & Hajnóczky, G. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0133-0 · Cited by 622 · see citing works
Mitochondria at the neuronal presynapse in health and disease
Devine, M. J., & Kittler, J. T. (2018) · Nature reviews. Neuroscience · doi:10.1038/nrn.2017.170 · Cited by 615 · see citing works
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Sheng, Z. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201312123 · Cited by 409 · see citing works
Self-citationAxonal transport: Driving synaptic function
Guedes-Dias, P., & Holzbaur, E. L. F. (2019) · Science · doi:10.1126/science.aaw9997 · Cited by 355 · see citing works
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López‐Doménech, G., Covill‐Cooke, C., Ivankovic, D., Halff, E. F., Sheehan, D. F., Norkett, R., Birsa, N., & Kittler, J. T. (2018) · The EMBO Journal · doi:10.15252/embj.201696380 · Cited by 336 · see citing works
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Labbè, K., Murley, A., & Nunnari, J. M. (2014) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-101011-155756 · Cited by 315 · see citing works
Facilitation of axon regeneration by enhancing mitochondrial transport and rescuing energy deficits
Zhou, B., Yu, P., Lin, M.-Y., Sun, T., Chen, Y., & Sheng, Z. (2016) · The Journal of Cell Biology · doi:10.1083/jcb.201605101 · Cited by 321 · see citing works
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Li, S., & Sheng, Z. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00535-8 · Cited by 273 · see citing works
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Fu, M., & Holzbaur, E. L. F. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2014.05.002 · Cited by 266 · see citing works
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Barlan, K., & Gelfand, V. I. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a025817 · Cited by 261 · see citing works
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Chen, C., Turnbull, D. M., & Reeve, A. K. (2019) · Biology · doi:10.3390/biology8020038 · Cited by 253 · see citing works
Programming axonal mitochondrial maintenance and bioenergetics in neurodegeneration and regeneration
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Self-citationHan, Q., Xie, Y., Ordaz, J. D., Huh, A., Huang, N., Wu, W., Liu, N., Chamberlain, K. A., Sheng, Z., & Xu, X. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2020.02.002 · Cited by 221 · see citing works
Self-citationRegulation of mitochondrial transport in neurons
Lin, M.-Y., & Sheng, Z. (2015) · Experimental Cell Research · doi:10.1016/j.yexcr.2015.01.004 · Cited by 223 · see citing works
Self-citationThe Interplay of Axonal Energy Homeostasis and Mitochondrial Trafficking and Anchoring
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Self-citationAlterations in Mitochondrial Quality Control in Alzheimer’s Disease
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Loss of Miro1-directed mitochondrial movement results in a novel murine model for neuron disease
Nguyen, T., Oh, S. S., Weaver, D., Lewandowska, A., Maxfield, D., Schuler, M.-H., Smith, N. K., Macfarlane, J. L., Saunders, G. W., Palmer, C. A., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1402449111 · Cited by 219 · see citing works
Axon Regeneration in the Central Nervous System: Facing the Challenges from the Inside
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Lin, M.-Y., Cheng, X., Tammineni, P., Xie, Y., Zhou, B., Cai, Q., & Sheng, Z. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.004 · Cited by 183 · see citing works
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Tammineni, P., Ye, X., Feng, T., Aikal, D., & Cai, Q. (2017) · eLife · doi:10.7554/elife.21776 · Cited by 169 · see citing works
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Li, S., Xiong, G.-J., Huang, N., & Sheng, Z. (2020) · Nature Metabolism · doi:10.1038/s42255-020-00289-0 · Cited by 144 · see citing works
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Ito, Y. A., & Di Polo, A. (2017) · Mitochondrion · doi:10.1016/j.mito.2017.08.014 · Cited by 142 · see citing works
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Canty, J. T., Hensley, A., Aslan, M., Jack, A., & Yildiz, A. (2023) · Nature Communications · doi:10.1038/s41467-023-36945-8 · Cited by 131 · see citing works
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Connecting mitochondrial dynamics and life-or-death events via Bcl-2 family proteins
Aouacheria, A., Baghdiguian, S., Lamb, H. M., Huska, J. D., Pineda, F. J., & Hardwick, J. M. (2017) · Neurochemistry International · doi:10.1016/j.neuint.2017.04.009 · Cited by 81 · see citing works
Tesco, G., & Lomoio, S. (2022) · Seminars in Immunology · doi:10.1016/j.smim.2022.101628 · Cited by 91 · see citing works
MIRO GTPases in Mitochondrial Transport, Homeostasis and Pathology
Tang, B. L. (2015) · Cells · doi:10.3390/cells5010001 · Cited by 82 · see citing works
Mitochondrial dynamics involves molecular and mechanical events in motility, fusion and fission
Green, A., Hossain, T., & Eckmann, D. M. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1010232 · Cited by 83 · see citing works
Miro: A molecular switch at the center of mitochondrial regulation
Eberhardt, E. L., Ludlam, A. V., Tan, Z., & Cianfrocco, M. A. (2020) · Protein Science · doi:10.1002/pro.3839 · Cited by 78 · see citing works
Mitochondria and sensory processing in inflammatory and neuropathic pain
Ribeiro, P. S. S., Willemen, H. L. D. M., & Eijkelkamp, N. (2022) · Frontiers in Pain Research · doi:10.3389/fpain.2022.1013577 · Cited by 86 · see citing works
Neuronal sub‐compartmentalization: a strategy to optimize neuronal function
Donato, A., Kagias, K., Zhang, Y., & Hilliard, M. A. (2019) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12487 · Cited by 72 · see citing works
Mitochondrial regulation of local supply of energy in neurons
López‐Doménech, G., & Kittler, J. T. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102747 · Cited by 71 · see citing works
Regulation of mitochondria-dynactin interaction and mitochondrial retrograde transport in axons
Drerup, C. M., Herbert, A. L., Monk, K. R., & Nechiporuk, A. V. (2017) · eLife · doi:10.7554/elife.22234 · Cited by 70 · see citing works
Zheng, Y., Zhang, X., & Chen, Z. (2019) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13122 · Cited by 69 · see citing works
Mandal, A., Wong, H.-T., Pinter, K. L., Mosqueda, N., Beirl, A. J., Lomash, R. M., Won, S., Kindt, K. S., & Drerup, C. M. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1316-20.2020 · Cited by 68 · see citing works
Mechanics of mitochondrial motility in neurons
Barnhart, E. L. (2016) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2016.02.022 · Cited by 68 · see citing works
Mitochondrial dynamics, positioning and function mediated by cytoskeletal interactions
Shah, M., Chacko, L. A., Joseph, J. P., & Ananthanarayanan, V. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03762-5 · Cited by 67 · see citing works
Miro sculpts mitochondrial dynamics in neuronal health and disease
Devine, M. J., Birsa, N., & Kittler, J. T. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.12.008 · Cited by 67 · see citing works
Moutaux, E., Christaller, W., Scaramuzzino, C., Genoux, A., Charlot, B., Cazorla, M., & Saudou, F. (2018) · Scientific Reports · doi:10.1038/s41598-018-31759-x · Cited by 66 · see citing works
Intracellular and Intercellular Mitochondrial Dynamics in Parkinson’s Disease
Valdinocci, D., Simões, R. F., Kovářová, J., Cunha‐Oliveira, T., Neužil, J., & Pountney, D. L. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00930 · Cited by 65 · see citing works
Li, L., Nadanaciva, S., Berger, Z., Shen, W., Paumier, K. L., Schwartz, J. W., Mou, K., Loos, P., Milici, A. J., Dunlop, J., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0085815 · Cited by 64 · see citing works
Vagnoni, A., Hoffmann, P. C., & Bullock, S. L. (2015) · Journal of Cell Science · doi:10.1242/jcs.179184 · Cited by 65 · see citing works
Shaping mitochondrial dynamics: The role of cAMP signalling
Benedetto, G. D., Gerbino, A., & Lefkimmiatis, K. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.05.041 · Cited by 65 · see citing works
FHL2 anchors mitochondria to actin and adapts mitochondrial dynamics to glucose supply
Basu, H., Pekkurnaz, G., Falk, J. E., Wei, W., Chin, M., Steen, J. A. J., & Schwarz, T. L. (2021) · The Journal of Cell Biology · doi:10.1083/jcb.201912077 · Cited by 59 · see citing works
Rojas-Charry, L., Nardi, L., Methner, A., & Schmeißer, M. J. (2020) · Journal of Molecular Medicine · doi:10.1007/s00109-020-02018-2 · Cited by 59 · see citing works
Synaptic activity controls autophagic vacuole motility and function in dendrites
Kulkarni, V. V., Anand, A., Herr, J. B., Miranda, C., Vogel, M. C., & Maday, S. (2021) · The Journal of Cell Biology · doi:10.1083/jcb.202002084 · Cited by 59 · see citing works
Regulation and roles of mitophagy at synapses
Palikaras, K., & Tavernarakis, N. (2020) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2020.111216 · Cited by 58 · see citing works
Actin/Myosin-V- and Activity-Dependent Inter-synaptic Vesicle Exchange in Central Neurons
Gramlich, M. W., & Klyachko, V. A. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.02.010 · Cited by 56 · see citing works
Koppers, M., Özkan, N., & Farías, G. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.618733 · Cited by 38 · see citing works
Microtubule-Based Mitochondrial Dynamics as a Valuable Therapeutic Target in Cancer
Vona, R., Mileo, A. M., & Matarrese, P. (2021) · Cancers · doi:10.3390/cancers13225812 · Cited by 56 · see citing works
New splicing variants of mitochondrial Rho GTPase-1 (Miro1) transport peroxisomes
Okumoto, K., Ono, T., Toyama, R., Shimomura, A., Nagata, A., & Fujiki, Y. (2017) · The Journal of Cell Biology · doi:10.1083/jcb.201708122 · Cited by 54 · see citing works
Mehta, K., Chacko, L. A., Chug, M. K., Jhunjhunwala, S., & Ananthanarayanan, V. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.006799 · Cited by 54 · see citing works
Engholm‐Keller, K., Waardenberg, A. J., Müller, J. A., Wark, J. R., Fernando, R. N., Arthur, J. W., Robinson, P. J., Dietrich, D., Schoch, S., & Graham, M. E. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000170 · Cited by 52 · see citing works
Rumora, A. E., Savelieff, M. G., Sakowski, S. A., & Feldman, E. L. (2019) · International review of neurobiology · doi:10.1016/bs.irn.2019.05.002 · Cited by 51 · see citing works
Leung, M. R., Chiozzi, R. Z., Roelofs, M. C., Hevler, J. F., Ravi, R. T., Maitan, P. P., Zhang, M., Henning, H. H. W., Bromfield, E. G., Howes, S. C., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2110996118 · Cited by 51 · see citing works
Deletion of a kinesin I motor unmasks a mechanism of homeostatic branching control by neurotrophin-3
Auer, T. O., Xiao, T., Bercier, V., Gebhardt, C., Duroure, K., Concordet, J., Wyart, C., Suster, M. L., Kawakami, K., Wittbrodt, J., et al. (2015) · eLife · doi:10.7554/elife.05061 · Cited by 50 · see citing works
Cheng, X., & Sheng, Z. (2020) · Developmental Neurobiology · doi:10.1002/dneu.22748 · Cited by 50 · see citing works
Self-citationChauss, D., Basu, S., Rajakaruna, S., Ma, Z., Gau, V., Anastas, S., Brennan, L., Hejtmancik, J. F., Menko, A. S., & Kantorow, M. (2014) · G3 Genes Genomes Genetics · doi:10.1534/g3.114.012120 · Cited by 48 · see citing works
ROS regulation of axonal mitochondrial transport is mediated by Ca2+ and JNK in Drosophila
Liao, P., Tandarich, L. C., & Hollenbeck, P. J. (2017) · PLoS ONE · doi:10.1371/journal.pone.0178105 · Cited by 49 · see citing works
Ceramides and mitochondrial homeostasis
Ding, S. Z., Li, G., Fu, T., Zhang, T., Lu, X., Li, N., & Geng, Q. (2024) · Cellular Signalling · doi:10.1016/j.cellsig.2024.111099 · Cited by 48 · see citing works
Calcium-mediated regulation of mitophagy: implications in neurodegenerative diseases
Borbolis, F., Ploumi, C., & Palikaras, K. (2025) · npj Metabolic Health and Disease · doi:10.1038/s44324-025-00049-2 · Cited by 49 · see citing works
Regulators of mitochondrial Ca2+ homeostasis in cerebral ischemia
Schäfer, M. K. E., Pfeiffer, A., Jaeckel, M., Pouya, A., Dolga, A. M., & Methner, A. (2014) · Cell and Tissue Research · doi:10.1007/s00441-014-1807-y · Cited by 47 · see citing works
Transporting mitochondria in neurons
Course, M. M., & Wang, X. (2016) · F1000Research · doi:10.12688/f1000research.7864.1 · Cited by 47 · see citing works
The role of mitochondrial defects and oxidative stress in Alzheimer’s disease
Islam, B. U., Jabir, N. R., & Tabrez, S. S. M. (2019) · Journal of drug targeting · doi:10.1080/1061186x.2019.1584808 · Cited by 48 · see citing works
Mitochondrial transport mediates survival of retinal ganglion cells in affected LHON patients
Yang, T., Yarmishyn, A. A., Yang, Y.-P., Lu, P.-C., Chou, S., Wang, M., Lin, T.-C., Hwang, D., Chou, Y.-B., Chen, S., et al. (2020) · Human Molecular Genetics · doi:10.1093/hmg/ddaa063 · Cited by 47 · see citing works
Verma, H., Gangwar, P., Yadav, A., Yadav, B., Rao, R., Kaur, S., Kumar, P., Dhiman, M., Taglialatela, G., & Mantha, A. K. (2023) · Mitochondrion · doi:10.1016/j.mito.2023.09.003 · Cited by 46 · see citing works
Mitochondrial dynamics in astrocytes
Stephen, T., Gupta, S., & Kittler, J. T. (2014) · Biochemical Society Transactions · doi:10.1042/bst20140195 · Cited by 44 · see citing works
The myriad roles of Miro in the nervous system: axonal transport of mitochondria and beyond
Lee, K.-S., & Lu, B.-W. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00330 · Cited by 46 · see citing works
Schwann Cells Provide Iron to Axonal Mitochondria and Its Role in Nerve Regeneration
Mietto, B. S., Jhelum, P., Schulz, K., & David, S. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0900-21.2021 · Cited by 44 · see citing works
Understanding Miro GTPases: Implications in the Treatment of Neurodegenerative Disorders
Kay, L., Pienaar, I., Cooray, R., Black, G., & Soundararajan, M. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-0927-x · Cited by 40 · see citing works
- Authors
- Chen, Y., & Sheng, Z.-H.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Sheng, Zu-Hang
- Venue
- Journal of Cell Biology
- Publisher
- Rockefeller University Press
- Published
- 2013-07-15
- Volume
- 202
- Issue
- 2
- Pages
- 351-364
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC3718985
- OpenAlex
- W2059473497
- Cited by
- 250
- References
- 48
- Citations by year
- 2026: 15 · 2025: 18 · 2024: 15 · 2023: 19 · 2022: 16 · 2021: 28 · 2020: 25 · 2019: 18 · 2018: 13 · 2017: 24 · 2016: 17 · 2015: 18 · 2014: 20 · 2013: 4
- FWCI
- 8.82
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-sa
- Locations
- The Journal of Cell Biology (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- syntaphilin, KIF5, kinesin-1, activity-dependent regulation, synaptic activity, calcium signaling, Rho GTPases, microtubule anchoring, synaptic mitochondria
- MeSH terms
- Animals, Axons, Biological Transport, Calcium, Carrier Proteins, Chlorocebus aethiops, Humans, Membrane Proteins, Mice, Inbred C57BL, Microtubule-Associated Proteins, Mitochondria, Nerve Tissue Proteins, Synaptic Transmission, Protein Binding, Kinesins, COS Cells, rho GTP-Binding Proteins, Protein Interaction Mapping, Mitochondrial Membranes, Mice, HEK293 Cells
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