Abstract
Mitochondria are cellular organelles of crucial importance, playing roles in cellular life and death. In certain cell types, such as neurons, mitochondria must travel long distances so as to meet metabolic demands of the cell. Mitochondrial movement is essentially microtubule (MT) based and is executed by two main motor proteins, Dynein and Kinesin. The organization of the cellular MT network and the identity of motors dictate mitochondrial transport. Tight coupling between MTs, motors, and the mitochondria is needed for the organelle precise localization. Two adaptor proteins are involved directly in mitochondria-motor coupling, namely Milton known also as TRAK, which is the motor adaptor, and Miro, which is the mitochondrial protein. Here, we discuss the active mitochondria transport process, as well as motor–mitochondria coupling in the context of MT organization in different cell types. We focus on mitochondrial trafficking in different cell types, specifically neurons, migrating cells, and polarized epithelial cells.
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Abbreviations
- Miro:
-
Mitochondrial Rho-GTPase
- MT:
-
Microtubules
- MTOC:
-
Microtubule-organizing center
- TRAK:
-
Trafficking kinesin protein
- γTuRC:
-
γ-Tubulin ring complex
References
Allan VJ (2011) Cytoplasmic dynein. Biochem Soc Trans 39:1169–1178
Antico Arciuch VG, Elguero ME, Poderoso JJ, Carreras MC (2012) Mitochondrial regulation of cell cycle and proliferation. Antioxid Redox Signal 16:1150–1180
Ashrafi G, Schlehe JS, LaVoie MJ, Schwarz TL (2014) Mitophagy of damaged mitochondria occurs locally in distal neuronal axons and requires PINK1 and Parkin. J Cell Biol 206:655–670
Auer TO, Xiao T, Bercier V, Gebhardt C, Duroure K, Concordet JP, Wyart C, Suster M, Kawakami K, Wittbrodt J, Baier H, Del Bene F (2015) Deletion of a kinesin I motor unmasks a mechanism of homeostatic branching control by neurotrophin-3. eLife 4:e05061. doi:10.7554/eLife.05061
Baas PW, Ahmad FJ (2013) Beyond taxol: microtubule-based treatment of disease and injury of the nervous system. Brain 136:2937–2951
Babic M, Russo GJ, Wellington AJ, Sangston RM, Gonzalez M, Zinsmaier KE (2015) Miro’s N-terminal GTPase domain is required for transport of mitochondria into axons and dendrites. J Neurosci 35:5754–5771
Barker AR, McIntosh KV, Dawe HR (2016) Centrosome positioning in non-dividing cells. Protoplasma 253:1007–1021
Bettencourt-Dias M, Glover DM (2007) Centrosome biogenesis and function: centrosomics brings new understanding. Nat Rev Mol Cell Biol 8:451–463
Bitan A, Rosenbaum I, Abdu U (2012) Stable and dynamic microtubules coordinately determine and maintain Drosophila bristle shape. Development. 139:1987–1996
Brickley K, Stephenson FA (2011) Trafficking kinesin protein (TRAK)-mediated transport of mitochondria in axons of hippocampal neurons. J Biol Chem 286:18079–18092
Cai Q, Gerwin C, Sheng ZH (2005) Syntabulin-mediated anterograde transport of mitochondria along neuronal processes. J Cell Biol 170:959–969
Cai Q, Zakaria HM, Simone A, Sheng ZH (2012) Spatial parkin translocation and degradation of damaged mitochondria via mitophagy in live cortical neurons. Curr Biol 22:545–552
Caino MC, Seo JH, Aguinaldo A, Wait E, Bryant KG, Kossenkov AV, Hayden JE, Vaira V, Morotti A, Ferrero S, Bosari S, Gabrilovich DI, Languino LR, Cohen AR, Altieri DC (2016) A neuronal network of mitochondrial dynamics regulates metastasis. Nat Commun 7:13730
Calkins MJ, Manczak M, Mao P, Shirendeb U, Reddy PH (2011) Impaired mitochondrial biogenesis, defective axonal transport of mitochondria, abnormal mitochondrial dynamics and synaptic degeneration in a mouse model of Alzheimer’s disease. Hum Mol Genet 20:4515–4529
Callan-Jones AC, Voituriez R (2016) Actin flows in cell migration: from locomotion and polarity to trajectories. Curr Opin Cell Biol 38:12–17
Campbell PD, Shen K, Sapio MR, Glenn TD, Talbot WS, Marlow FL (2014) Unique function of Kinesin Kif5A in localization of mitochondria in axons. J Neurosci 34:14717–14732
Campello S, Lacalle RA, Bettella M, Manes S, Scorrano L, Viola A (2006) Orchestration of lymphocyte chemotaxis by mitochondrial dynamics. J Exp Med 203:2879–2886
Cho C, Vale RD (2012) The mechanism of dynein motility: insight from crystal structures of the motor domain. Biochem Biophys Acta 1823:182–191
Conde C, Caceres A (2009) Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10:319–332
Conduit PT, Wainman A, Raff JW (2015) Centrosome function and assembly in animal cells. Nat Rev Mol Cell Biol 16:611–624
Cox RT, Spradling AC (2006) Milton controls the early acquisition of mitochondria by Drosophila oocytes. Development 133:3371–3377
Cunniff B, McKenzie AJ, Heintz NH, Howe AK (2016) AMPK activity regulates trafficking of mitochondria to the leading edge during cell migration and matrix invasion. Mol Biol Cell 27:2662–2674
da Silva AF, Mariotti FR, Maximo V, Campello S (2014) Mitochondria dynamism: of shape, transport and cell migration. Cell Mol Life Sci 71:2313–2324
Desai SP, Bhatia SN, Toner M, Irimia D (2013) Mitochondrial localization and the persistent migration of epithelial cancer cells. Biophys J 104:2077–2088
Drerup CM, Herbert AL, Monk KR, Nechiporuk AV (2017) Regulation of mitochondria-dynactin interaction and mitochondrial retrograde transport in axons. eLife 6:e22234. doi:10.7554/eLife.22234
Estaquier J, Vallette F, Vayssiere JL, Mignotte B (2012) The mitochondrial pathways of apoptosis. Adv Exp Med Biol 942:157–183
Etienne-Manneville S (2013) Microtubules in cell migration. Annu Rev Cell Dev Biol 29:471–499
Fang Y, Soares L, Teng X, Geary M, Bonini NM (2012) A novel Drosophila model of nerve injury reveals an essential role of Nmnat in maintaining axonal integrity. Curr Biol 22:590–595
Ferree AW, Trudeau K, Zik E, Benador IY, Twig G, Gottlieb RA, Shirihai OS (2013) MitoTimer probe reveals the impact of autophagy, fusion, and motility on subcellular distribution of young and old mitochondrial protein and on relative mitochondrial protein age. Autophagy 9:1887–1896
Fransson A, Ruusala A, Aspenstrom P (2003) Atypical Rho GTPases have roles in mitochondrial homeostasis and apoptosis. J Biol Chem 278:6495–6502
Frederick RL, Shaw JM (2007) Moving mitochondria: establishing distribution of an essential organelle. Traffic 8:1668–1675
Geraldo S, Gordon-Weeks PR (2009) Cytoskeletal dynamics in growth-cone steering. J Cell Sci 122:3595–3604
Glater EE, Megeath LJ, Stowers RS, Schwarz TL (2006) Axonal transport of mitochondria requires milton to recruit kinesin heavy chain and is light chain independent. J Cell Biol 173:545–557
Gong TW, Winnicki RS, Kohrman DC, Lomax MI (1999) A novel mouse kinesin of the UNC-104/KIF1 subfamily encoded by the Kif1b gene. Gene 239:117–127
Gorska-Andrzejak J, Stowers RS, Borycz J, Kostyleva R, Schwarz TL, Meinertzhagen IA (2003) Mitochondria are redistributed in Drosophila photoreceptors lacking milton, a kinesin-associated protein. J Comp Neurol 463:372–388
Guo X, Macleod GT, Wellington A, Hu F, Panchumarthi S, Schoenfield M, Marin L, Charlton MP, Atwood HL, Zinsmaier KE (2005) The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron 47:379–393
Haghnia M, Cavalli V, Shah SB, Schimmelpfeng K, Brusch R, Yang G, Herrera C, Pilling A, Goldstein LS (2007) Dynactin is required for coordinated bidirectional motility, but not for dynein membrane attachment. Mol Biol Cell 18:2081–2089
Han SM, Baig HS, Hammarlund M (2016) Mitochondria localize to injured axons to support regeneration. Neuron 92:1308–1323
Hatch AL, Gurel PS, Higgs HN (2014) Novel roles for actin in mitochondrial fission. J Cell Sci 127:4549–4560
Hill SE, Parmar M, Gheres KW, Guignet MA, Huang Y, Jackson FR, Rolls MM (2012) Development of dendrite polarity in Drosophila neurons. Neural Dev 7:34
Hirokawa N, Niwa S, Tanaka Y (2010) Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron 68:610–638
Hirokawa N, Tanaka Y (2015) Kinesin superfamily proteins (KIFs): various functions and their relevance for important phenomena in life and diseases. Exp Cell Res 334:16–25
Hollenbeck PJ (1996) The pattern and mechanism of mitochondrial transport in axons. Front Biosci 1:d91–d102
Howard J, Hyman AA (2009) Growth, fluctuation and switching at microtubule plus ends. Nat Rev Mol Cell Biol 10:569–574
Hsieh CH, Shaltouki A, Gonzalez AE, Bettencourt da Cruz A, Burbulla LF, St Lawrence E, Schule B, Krainc D, Palmer TD, Wang X (2016) Functional impairment in miro degradation and mitophagy is a shared feature in familial and sporadic Parkinson’s disease. Cell Stem Cell 19:709–724
Hurd DD, Saxton WM (1996) Kinesin mutations cause motor neuron disease phenotypes by disrupting fast axonal transport in Drosophila. Genetics 144:1075–1085
Kanai Y, Okada Y, Tanaka Y, Harada A, Terada S, Hirokawa N (2000) KIF5C, a novel neuronal kinesin enriched in motor neurons. J Neurosci 20:6374–6384
Kang JS, Tian JH, Pan PY, Zald P, Li C, Deng C, Sheng ZH (2008) Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell 132:137–148
Kapitein LC, Hoogenraad CC (2015) Building the neuronal microtubule cytoskeleton. Neuron 87:492–506
Karle KN, Mockel D, Reid E, Schols L (2012) Axonal transport deficit in a KIF5A(-/-) mouse model. Neurogenetics 13:169–179
Kimura T, Murakami F (2014) Evidence that dendritic mitochondria negatively regulate dendritic branching in pyramidal neurons in the neocortex. J Neurosci 34:6938–6951
Lee H, Yoon Y (2014) Mitochondrial fission: regulation and ER connection. Mol Cells 37:89–94
Ligon LA, Steward O (2000) Movement of mitochondria in the axons and dendrites of cultured hippocampal neurons. J Comp Neurol 427:340–350
Liu S, Sawada T, Lee S, Yu W, Silverio G, Alapatt P, Millan I, Shen A, Saxton W, Kanao T, Takahashi R, Hattori N, Imai Y, Lu B (2012) Parkinson’s disease-associated kinase PINK1 regulates Miro protein level and axonal transport of mitochondria. PLoS Genet 8:e1002537
Lopez-Domenech G, Higgs NF, Vaccaro V, Ros H, Arancibia-Carcamo IL, MacAskill AF, Kittler JT (2016) Loss of dendritic complexity precedes neurodegeneration in a mouse model with disrupted mitochondrial distribution in mature dendrites. Cell Rep 17:317–327
Loss O, Stephenson FA (2015) Localization of the kinesin adaptor proteins trafficking kinesin proteins 1 and 2 in primary cultures of hippocampal pyramidal and cortical neurons. J Neurosci Res 93:1056–1066
Loss O, Stephenson FA (2017) Developmental changes in TRAK-mediated mitochondrial transport in neurons. Mol Cell Neurosci 80:134–147
Luders J, Stearns T (2007) Microtubule-organizing centres: a re-evaluation. Nat Rev Mol Cell Biol 8:161–167
Macaskill AF, Rinholm JE, Twelvetrees AE, Arancibia-Carcamo IL, Muir J, Fransson A, Aspenstrom P, Attwell D, Kittler JT (2009) Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 61:541–555
Magrane J, Cortez C, Gan WB, Manfredi G (2014) Abnormal mitochondrial transport and morphology are common pathological denominators in SOD1 and TDP43 ALS mouse models. Hum Mol Genet 23:1413–1424
Mannella CA (2008) Structural diversity of mitochondria: functional implications. Ann N Y Acad Sci 1147:171–179
Marchi S, Patergnani S, Missiroli S, Morciano G, Rimessi A, Wieckowski MR, Giorgi C, Pinton P (2017) Mitochondrial and endoplasmic reticulum calcium homeostasis and cell death. Cell Calcium. doi:10.1016/j.ceca.2017.05.003
Margolin G, Gregoretti IV, Cickovski TM, Li C, Shi W, Alber MS, Goodson HV (2012) The mechanisms of microtubule catastrophe and rescue: implications from analysis of a dimer-scale computational model. Mol Biol Cell 23:642–656
Martin-Cofreces NB, Robles-Valero J, Cabrero JR, Mittelbrunn M, Gordon-Alonso M, Sung CH, Alarcon B, Vazquez J, Sanchez-Madrid F (2008) MTOC translocation modulates IS formation and controls sustained T cell signaling. J Cell Biol 182:951–962
Mattila PK, Lappalainen P (2008) Filopodia: molecular architecture and cellular functions. Nat Rev Mol Cell Biol 9:446–454
Melkov A, Baskar R, Alcalay Y, Abdu U (2016) A new mode of mitochondrial transport and polarized sorting regulated by Dynein, Milton and Miro. Development 143:4203–4213
Melkov A, Simchoni Y, Alcalay Y, Abdu U (2015) Dynamic microtubule organization and mitochondrial transport are regulated by distinct Kinesin-1 pathways. Biol Open 4:1696–1706
Miller KE, Sheetz MP (2004) Axonal mitochondrial transport and potential are correlated. J Cell Sci 117:2791–2804
Mitchison T, Kirschner M (1984) Dynamic instability of microtubule growth. Nature 312:237–242
Morfini G, Schmidt N, Weissmann C, Pigino G, Kins S (2016) Conventional kinesin: biochemical heterogeneity and functional implications in health and disease. Brain Res Bull 126:347–353
Morlino G, Barreiro O, Baixauli F, Robles-Valero J, Gonzalez-Granado JM, Villa-Bellosta R, Cuenca J, Sanchez-Sorzano CO, Veiga E, Martin-Cofreces NB, Sanchez-Madrid F (2014) Miro-1 links mitochondria and microtubule Dynein motors to control lymphocyte migration and polarity. Mol Cell Biol 34:1412–1426
Morotz GM, De Vos KJ, Vagnoni A, Ackerley S, Shaw CE, Miller CC (2012) Amyotrophic lateral sclerosis-associated mutant VAPBP56S perturbs calcium homeostasis to disrupt axonal transport of mitochondria. Hum Mol Genet 21:1979–1988
Nangaku M, Sato-Yoshitake R, Okada Y, Noda Y, Takemura R, Yamazaki H, Hirokawa N (1994) KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell 79:1209–1220
Nguyen MM, Stone MC, Rolls MM (2011) Microtubules are organized independently of the centrosome in Drosophila neurons. Neural Dev 6:38
Nguyen TT, Oh SS, Weaver D, Lewandowska A, Maxfield D, Schuler MH, Smith NK, Macfarlane J, Saunders G, Palmer CA, Debattisti V, Koshiba T, Pulst S, Feldman EL, Hajnoczky G, Shaw JM (2014) Loss of Miro1-directed mitochondrial movement results in a novel murine model for neuron disease. Proc Natl Acad Sci USA 111:E3631–E3640
Otera H, Ishihara N, Mihara K (2013) New insights into the function and regulation of mitochondrial fission. Biochem Biophys Acta 1833:1256–1268
Overly CC, Rieff HI, Hollenbeck PJ (1996) Organelle motility and metabolism in axons vs dendrites of cultured hippocampal neurons. J Cell Sci 109(Pt 5):971–980
Pathak D, Sepp KJ, Hollenbeck PJ (2010) Evidence that myosin activity opposes microtubule-based axonal transport of mitochondria. J Neurosci 30:8984–8992
Pilling AD, Horiuchi D, Lively CM, Saxton WM (2006) Kinesin-1 and Dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons. Mol Biol Cell 17:2057–2068
Popov V, Medvedev NI, Davies HA, Stewart MG (2005) Mitochondria form a filamentous reticular network in hippocampal dendrites but are present as discrete bodies in axons: a three-dimensional ultrastructural study. J Comp Neurol 492:50–65
Quintana A, Schwarz EC, Schwindling C, Lipp P, Kaestner L, Hoth M (2006) Sustained activity of calcium release-activated calcium channels requires translocation of mitochondria to the plasma membrane. J Biol Chem 281:40302–40309
Rawson RL, Yam L, Weimer RM, Bend EG, Hartwieg E, Horvitz HR, Clark SG, Jorgensen EM (2014) Axons degenerate in the absence of mitochondria in C. elegans. Curr Biol: CB 24:760–765
Reilein A, Yamada S, Nelson WJ (2005) Self-organization of an acentrosomal microtubule network at the basal cortex of polarized epithelial cells. J Cell Biol 171:845–855
Rice SE, Gelfand VI (2006) Paradigm lost: milton connects kinesin heavy chain to miro on mitochondria. J Cell Biol 173:459–461
Roberts AJ, Kon T, Knight PJ, Sutoh K, Burgess SA (2013) Functions and mechanics of dynein motor proteins. Nat Rev Mol Cell Biol 14:713–726
Russo GJ, Louie K, Wellington A, Macleod GT, Hu F, Panchumarthi S, Zinsmaier KE (2009) Drosophila Miro is required for both anterograde and retrograde axonal mitochondrial transport. J Neurosci 29:5443–5455
Sanchez-Madrid F, del Pozo MA (1999) Leukocyte polarization in cell migration and immune interactions. EMBO J 18:501–511
Sanchez-Madrid F, Serrador JM (2007) Mitochondrial redistribution: adding new players to the chemotaxis game. Trends Immunol 28:193–196
Satoh AK, Li BX, Xia H, Ready DF (2008) Calcium-activated Myosin V closes the Drosophila pupil. Curr Biol 18:951–955
Satoh D, Sato D, Tsuyama T, Saito M, Ohkura H, Rolls MM, Ishikawa F, Uemura T (2008) Spatial control of branching within dendritic arbors by dynein-dependent transport of Rab5-endosomes. Nat Cell Biol 10:1164–1171
Scarpa E, Mayor R (2016) Collective cell migration in development. J Cell Biol 212:143–155
Schroer TA (2004) Dynactin. Annu Rev Cell Dev Biol 20:759–779
Sheng ZH, Cai Q (2012) Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration. Nat Rev Neurosci 13:77–93
Siddiqui SS (2002) Metazoan motor models: kinesin superfamily in C. elegans. Traffic 3:20–28
Stiess M, Maghelli N, Kapitein LC, Gomis-Ruth S, Wilsch-Brauninger M, Hoogenraad CC, Tolic-Norrelykke IM, Bradke F (2010) Axon extension occurs independently of centrosomal microtubule nucleation. Science 327:704–707
Stone MC, Roegiers F, Rolls MM (2008) Microtubules have opposite orientation in axons and dendrites of Drosophila neurons. Mol Biol Cell 19:4122–4129
Stowers RS, Megeath LJ, Gorska-Andrzejak J, Meinertzhagen IA, Schwarz TL (2002) Axonal transport of mitochondria to synapses depends on Milton, a novel Drosophila protein. Neuron 36:1063–1077
Suhm T, Ott M (2017) Mitochondrial translation and cellular stress response. Cell Tissue Res 367:21–31
Sulimenko V, Hajkova Z, Klebanovych A, Draber P (2017) Regulation of microtubule nucleation mediated by gamma-tubulin complexes. Protoplasma 254:1187–1199
Tanaka K, Sugiura Y, Ichishita R, Mihara K, Oka T (2011) KLP6: a newly identified kinesin that regulates the morphology and transport of mitochondria in neuronal cells. J Cell Sci 124:2457–2465
Tanaka Y, Kanai Y, Okada Y, Nonaka S, Takeda S, Harada A, Hirokawa N (1998) Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 93:1147–1158
Tang Y, Zucker RS (1997) Mitochondrial involvement in post-tetanic potentiation of synaptic transmission. Neuron 18:483–491
Toya M, Takeichi M (2016) Organization of non-centrosomal microtubules in epithelial cells. Cell Struct Funct 41:127–135
Vagnoni A, Hoffmann PC, Bullock SL (2016) Reducing Lissencephaly-1 levels augments mitochondrial transport and has a protective effect in adult Drosophila neurons. J Cell Sci 129:178–190
Vallee RB, Williams JC, Varma D, Barnhart LE (2004) Dynein: an ancient motor protein involved in multiple modes of transport. J Neurobiol 58:189–200
van Beuningen SF, Hoogenraad CC (2016) Neuronal polarity: remodeling microtubule organization. Curr Opin Neurobiol 39:1–7
van Spronsen M, Mikhaylova M, Lipka J, Schlager MA, van den Heuvel DJ, Kuijpers M, Wulf PS, Keijzer N, Demmers J, Kapitein LC, Jaarsma D, Gerritsen HC, Akhmanova A, Hoogenraad CC (2013) TRAK/Milton motor-adaptor proteins steer mitochondrial trafficking to axons and dendrites. Neuron 77:485–502
Varadi A, Johnson-Cadwell LI, Cirulli V, Yoon Y, Allan VJ, Rutter GA (2004) Cytoplasmic dynein regulates the subcellular distribution of mitochondria by controlling the recruitment of the fission factor dynamin-related protein-1. J Cell Sci 117:4389–4400
Verhey KJ, Kaul N, Soppina V (2011) Kinesin assembly and movement in cells. Ann Rev Biophys 40:267–288
Vinogradova T, Miller PM, Kaverina I (2009) Microtubule network asymmetry in motile cells: role of Golgi-derived array. Cell Cycle 8:2168–2174
Wang X, Winter D, Ashrafi G, Schlehe J, Wong YL, Selkoe D, Rice S, Steen J, LaVoie MJ, Schwarz TL (2011) PINK1 and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 147:893–906
Wozniak MJ, Melzer M, Dorner C, Haring HU, Lammers R (2005) The novel protein KBP regulates mitochondria localization by interaction with a kinesin-like protein. BMC cell Biol 6:35
Yagi T (2009) Bioinformatic approaches to dynein heavy chain classification. Methods Cell Biol 92:1–9
Yan J, Chao DL, Toba S, Koyasako K, Yasunaga T, Hirotsune S, Shen K (2013) Kinesin-1 regulates dendrite microtubule polarity in Caenorhabditis elegans. eLife 2:e00133
Yau KW, Schatzle P, Tortosa E, Pages S, Holtmaat A, Kapitein LC, Hoogenraad CC (2016) Dendrites in vitro and in vivo contain microtubules of opposite polarity and axon formation correlates with uniform plus-end-out microtubule orientation. J Neurosci 36:1071–1085
Yau KW, van Beuningen SF, Cunha-Ferreira I, Cloin BM, van Battum EY, Will L, Schatzle P, Tas RP, van Krugten J, Katrukha EA, Jiang K, Wulf PS, Mikhaylova M, Harterink M, Pasterkamp RJ, Akhmanova A, Kapitein LC, Hoogenraad CC (2014) Microtubule minus-end binding protein CAMSAP2 controls axon specification and dendrite development. Neuron 82:1058–1073
Ye X, Sun X, Starovoytov V, Cai Q (2015) Parkin-mediated mitophagy in mutant hAPP neurons and Alzheimer’s disease patient brains. Hum Mol Genet 24:2938–2951
Yu Y, Lee HC, Chen KC, Suhan J, Qiu M, Ba Q, Yang G (2016) Inner membrane fusion mediates spatial distribution of axonal mitochondria. Sci Rep 6:18981
Zhang F, Wang W, Siedlak SL, Liu Y, Liu J, Jiang K, Perry G, Zhu X, Wang X (2015) Miro1 deficiency in amyotrophic lateral sclerosis. Front Aging Neurosci 7:100
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Melkov, A., Abdu, U. Regulation of long-distance transport of mitochondria along microtubules. Cell. Mol. Life Sci. 75, 163–176 (2018). https://doi.org/10.1007/s00018-017-2590-1
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DOI: https://doi.org/10.1007/s00018-017-2590-1