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Cell Biology of the Axon pp 361–381Cite as

Mitochondrial Transport Dynamics in Axons and Dendrites

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Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 48))

Abstract

Mitochondrial dynamics and transport have emerged as key factors in the regulation of neuronal differentiation and survival. Mitochondria are dynamically transported in and out of axons and dendrites to maintain neuronal and synaptic function. Transport proceeds through a controlled series of plus- and minus-end directed movements along microtubule tracks (MTs) that are often interrupted by short stops. This bidirectional motility of mitochondria is facilitated by plus end-directed kinesin and minus end-directed dynein motors, and may be coordinated and controlled by a number of mechanisms that integrate intracellular signals to ensure efficient transport and targeting of mitochondria. In this chapter, we discuss our understanding of mechanisms that facilitate mitochondrial transport and delivery to specific target sites in dendrites and axons.

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References

  • Adams I, Jones DG (1982) Quantitative ultrastructural changes in rat cortical synapses during early-, mid- and late-adulthood. Brain Res 239:349–363

    Article  PubMed  CAS  Google Scholar 

  • Baas PW, Deitch JS, Black MM, Banker GA (1988) Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc Natl Acad Sci USA 85:8335–8339

    Article  PubMed  CAS  Google Scholar 

  • Babcock DF, Hille B (1998) Mitochondrial oversight of cellular Ca2+ signaling. Curr Opin Neurobiol 8:398–404

    Article  PubMed  CAS  Google Scholar 

  • Beck M, Brickley K, Wilkinson HL, Sharma S, Smith M, Chazot PL, Pollard S, Stephenson FA (2002) Identification, molecular cloning, and characterization of a novel GABAA receptor-associated protein, GRIF-1. J Biol Chem 277:30079–30090

    Article  PubMed  CAS  Google Scholar 

  • Belles B, Hescheler J, Trube G (1987) Changes of membrane currents in cardiac cells induced by long whole-cell recordings and tolbutamide. Pflugers Arch 409:582–588

    Article  PubMed  CAS  Google Scholar 

  • Beltran-Parrazal L, Lopez-Valdes HE, Brennan KC, Diaz-Munoz M, de Vellis J, Charles AC (2006) Mitochondrial transport in processes of cortical neurons is independent of intracellular calcium. Am J Physiol Cell Physiol 291:C1193–1197

    Article  PubMed  CAS  Google Scholar 

  • Benshalom G, Reese TS (1985) Ultrastructural observations on the cytoarchitecture of axons processed by rapid-freezing and freeze-substitution. J Neurocytol 14:943–960

    Article  PubMed  CAS  Google Scholar 

  • Bowman AB, Patel-King RS, Benashski SE, McCaffery JM, Goldstein LS, King SM (1999) Drosophila roadblock and Chlamydomonas LC7: a conserved family of dynein-associated proteins involved in axonal transport, flagellar motility, and mitosis. J Cell Biol 146:165–180

    PubMed  CAS  Google Scholar 

  • Brady ST, Pfister KK, Bloom GS (1990) A monoclonal antibody against kinesin inhibits both anterograde and retrograde fast axonal transport in squid axoplasm. Proc Natl Acad Sci USA 87:1061–1065

    Article  PubMed  CAS  Google Scholar 

  • Brickley K, Smith MJ, Beck M, Stephenson FA (2005) GRIF-1 and OIP106, members of a novel gene family of coiled-coil domain proteins: association in vivo and in vitro with kinesin. J Biol Chem 280:14723–14732

    Article  PubMed  CAS  Google Scholar 

  • Bridgman PC (2009) Myosin motor proteins in the cell biology of axons and other neuronal compartments. Results Probl Cell Differ. doi:10.1007/400_2009_10

  • Brooks AS, Bertoli-Avella AM, Burzynski GM, Breedveld GJ, Osinga J, Boven LG, Hurst JA, Mancini GM, Lequin MH, de Coo RF et al (2005) Homozygous nonsense mutations in KIAA1279 are associated with malformations of the central and enteric nervous systems. Am J Hum Genet 77:120–126

    Article  PubMed  CAS  Google Scholar 

  • Brough D, Schell MJ, Irvine RF (2005) Agonist-induced regulation of mitochondrial and endoplasmic reticulum motility. Biochem J 392:291–297

    Article  PubMed  CAS  Google Scholar 

  • Cai Q, Gerwin C, Sheng ZH (2005) Syntabulin-mediated anterograde transport of mitochondria along neuronal processes. J Cell Biol 170:959–969

    Article  PubMed  CAS  Google Scholar 

  • Cameron HA, Kaliszewski CK, Greer CA (1991) Organization of mitochondria in olfactory bulb granule cell dendritic spines. Synapse 8:107–118

    Article  PubMed  CAS  Google Scholar 

  • Chada SR, Hollenbeck PJ (2003) Mitochondrial movement and positioning in axons: the role of growth factor signaling. J Exp Biol 206:1985–1992

    Article  PubMed  CAS  Google Scholar 

  • Chada SR, Hollenbeck PJ (2004) Nerve growth factor signaling regulates motility and docking of axonal mitochondria. Curr Biol 14:1272–1276

    Article  PubMed  CAS  Google Scholar 

  • Chan DC (2006) Mitochondrial fusion and fission in mammals. Annu Rev Cell Dev Biol 22:79–99

    Article  PubMed  CAS  Google Scholar 

  • Chang DT, Reynolds IJ (2006) Mitochondrial trafficking and morphology in healthy and injured neurons. Prog Neurobiol 80:241–268

    Article  PubMed  CAS  Google Scholar 

  • Chang DT, Honick AS, Reynolds IJ (2006) Mitochondrial trafficking to synapses in cultured primary cortical neurons. J Neurosci 26:7035–7045

    Article  PubMed  CAS  Google Scholar 

  • Chicurel ME, Harris KM (1992) Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus. J Comp Neurol 325:169–182

    Article  PubMed  CAS  Google Scholar 

  • Colin E, Zala D, Liot G, Rangone H, Borrell-Pages M, Li XJ, Saudou F, Humbert S (2008) Huntingtin phosphorylation acts as a molecular switch for anterograde/retrograde transport in neurons. EMBO J 27:2124–2134

    Article  PubMed  CAS  Google Scholar 

  • Cox RT, Spradling AC (2006) Milton controls the early acquisition of mitochondria by Drosophila oocytes. Development 133:3371–3377

    Article  PubMed  CAS  Google Scholar 

  • Danial NN, Gramm CF, Scorrano L, Zhang CY, Krauss S, Ranger AM, Datta SR, Greenberg ME, Licklider LJ, Lowell BB et al (2003) BAD and glucokinase reside in a mitochondrial complex that integrates glycolysis and apoptosis. Nature 424:952–956

    Article  PubMed  CAS  Google Scholar 

  • Das S, Boczan J, Gerwin C, Zald PB, Sheng ZH (2003) Regional and developmental regulation of syntaphilin expression in the brain: a candidate molecular element of synaptic functional differentiation. Brain Res Mol Brain Res 116:38–49

    Article  PubMed  CAS  Google Scholar 

  • De Vos K, Goossens V, Boone E, Vercammen D, Vancompernolle K, Vandenabeele P, Haegeman G, Fiers W, Grooten J (1998) The 55-kDa tumor necrosis factor receptor induces clustering of mitochondria through its membrane-proximal region. J Biol Chem 273:9673–9680

    Article  PubMed  Google Scholar 

  • De Vos K, Severin F, Van Herreweghe F, Vancompernolle K, Goossens V, Hyman A, Grooten J (2000) Tumor necrosis factor induces hyperphosphorylation of kinesin light chain and inhibits kinesin-mediated transport of mitochondria. J Cell Biol 149:1207–1214

    Article  PubMed  Google Scholar 

  • De Vos KJ, Sable J, Miller KE, Sheetz MP (2003) Expression of phosphatidylinositol (4, 5) bisphosphate-specific pleckstrin homology domains alters direction but not the level of axonal transport of mitochondria. Mol Biol Cell 14:3636–3649

    Article  PubMed  CAS  Google Scholar 

  • Deacon SW, Serpinskaya AS, Vaughan PS, Lopez Fanarraga M, Vernos I, Vaughan KT, Gelfand VI (2003) Dynactin is required for bidirectional organelle transport. J Cell Biol 160:297–301

    Article  PubMed  CAS  Google Scholar 

  • Denton RM (2009) Regulation of mitochondrial dehydrogenases by calcium ions. Biochim Biophys Acta doi: S0005-2728(09)00012-7 [pii] 10.1016/j.bbabio.2009.01.00, (in press)

    Google Scholar 

  • Detmer SA, Chan DC (2007) Functions and dysfunctions of mitochondrial dynamics. Nat Rev Mol Cell Biol 8:870–879

    Article  PubMed  CAS  Google Scholar 

  • Echeverri CJ, Paschal BM, Vaughan KT, Vallee RB (1996) Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis. J Cell Biol 132:617–633

    Article  PubMed  CAS  Google Scholar 

  • Fagarasanu A, Rachubinski RA (2007) Orchestrating organelle inheritance in Saccharomyces cerevisiae. Curr Opin Microbiol 10:528–538

    Article  PubMed  CAS  Google Scholar 

  • Fahim MA, Robbins N (1982) Ultrastructural studies of young and old mouse neuromuscular junctions. J Neurocytol 11:641–656

    Article  PubMed  CAS  Google Scholar 

  • Falnikar A, Baas PW (2009) Critical roles for microtubules in axonal development and disease. Results Probl Cell Differ. doi:10.1007/400_2009_2

  • Fichera M, Lo Giudice M, Falco M, Sturnio M, Amata S, Calabrese O, Bigoni S, Calzolari E, Neri M (2004) Evidence of kinesin heavy chain (KIF5A) involvement in pure hereditary spastic paraplegia. Neurology 63:1108–1110

    PubMed  CAS  Google Scholar 

  • Finsterer J (2006) Central nervous system manifestations of mitochondrial disorders. Acta Neurol Scand 114:217–238

    Article  PubMed  CAS  Google Scholar 

  • Fransson A, Ruusala A, Aspenstrom P (2003) Atypical Rho GTPases have roles in mitochondrial homeostasis and apoptosis. J Biol Chem 278:6495–6502

    Article  PubMed  CAS  Google Scholar 

  • Fransson S, Ruusala A, Aspenstrom P (2006) The atypical Rho GTPases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking. Bioch Biophys Res Com 344:500–510

    Article  CAS  Google Scholar 

  • Frederick RL, McCaffery JM, Cunningham KW, Okamoto K, Shaw JM (2004) Yeast Miro GTPase, Gem1p, regulates mitochondrial morphology via a novel pathway. J Cell Biol 167:87–98

    Article  PubMed  CAS  Google Scholar 

  • Frederick RL, Okamoto K, Shaw JM (2008) Multiple pathways influence mitochondrial inheritance in budding yeast. Genetics 178:825–837

    Article  PubMed  CAS  Google Scholar 

  • Gilbert SL, Zhang L, Forster ML, Anderson JR, Iwase T, Soliven B, Donahue LR, Sweet HO, Bronson RT, Davisson MT et al (2006) Trak1 mutation disrupts GABA(A) receptor homeostasis in hypertonic mice. Nat Genet 38:245–250

    Article  PubMed  CAS  Google Scholar 

  • Gindhart JG Jr, Desai CJ, Beushausen S, Zinn K, Goldstein LS (1998) Kinesin light chains are essential for axonal transport in Drosophila. J Cell Biol 141:443–454

    Article  PubMed  CAS  Google Scholar 

  • Giot L, Bader JS, Brouwer C, Chaudhuri A, Kuang B, Li Y, Hao YL, Ooi CE, Godwin B, Vitols E et al (2003) A protein interaction map of Drosophila melanogaster. Science 302:1727–1736

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Goldstein LS (2001) Kinesin molecular motors: transport pathways, receptors, and human disease. Proc Natl Acad Sci USA 98:6999–7003

    Article  PubMed  CAS  Google Scholar 

  • Goldstein LS (2003) Do disorders of movement cause movement disorders and dementia? Neuron 40:415–425

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Gross SP (2003) Dynactin: coordinating motors with opposite inclinations. Curr Biol 13:15

    Article  CAS  Google Scholar 

  • Gross SP, Welte MA, Block SM, Wieschaus EF (2000) Dynein-mediated cargo transport in vivo. A switch controls travel distance. J Biol 148:945–956

    CAS  Google Scholar 

  • Gross SP, Tuma MC, Deacon SW, Serpinskaya AS, Reilein AR, Gelfand VI (2002a) Interactions and regulation of molecular motors in Xenopus melanophores. J Cell Biol 156:855–865

    Article  PubMed  CAS  Google Scholar 

  • Gross SP, Welte MA, Block SM, Wieschaus EF (2002b) Coordination of opposite-polarity microtubule motors. J Cell Biol 156:715–724

    Article  PubMed  CAS  Google Scholar 

  • Gross SP, Guo Y, Martinez JE, Welte MA (2003) A determinant for directionality of organelle transport in Drosophila embryos. Curr Biol 13:1660–1668

    Article  PubMed  CAS  Google Scholar 

  • Gross SP, Vershinin M, Shubeita GT (2007) Cargo transport: two motors are sometimes better than one. Curr Biol 17:R478–486

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Habermann A, Schroer TA, Griffiths G, Burkhardt JK (2001) Immunolocalization of cytoplasmic dynein and dynactin subunits in cultured macrophages: enrichment on early endocytic organelles. J Cell Sci 114:229–240

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hajnoczky G, Robb-Gaspers LD, Seitz MB, Thomas AP (1995) Decoding of cytosolic calcium oscillations in the mitochondria. Cell 82:415–424

    Article  PubMed  CAS  Google Scholar 

  • He Y, Francis F, Myers KA, Yu W, Black MM, Baas PW (2005) Role of cytoplasmic dynein in the axonal transport of microtubules and neurofilaments. J Cell Biol 168:697–703

    Article  PubMed  CAS  Google Scholar 

  • Hirokawa N (1982) Cross-linker system between neurofilaments, microtubules, and membranous organelles in frog axons revealed by the quick-freeze, deep-etching method. J Cell Biol 94:129–142

    Article  PubMed  CAS  Google Scholar 

  • Hirokawa N, Yorifuji H (1986) Cytoskeletal architecture of reactivated crayfish axons, with special reference to crossbridges among microtubules and between microtubules and membrane organelles. Cell Motil Cytoskeleton 6:458–468

    Article  Google Scholar 

  • Hirokawa N, Takemura R (2005) Molecular motors and mechanisms of directional transport in neurons. Nat Rev Neurosci 6:201–214

    Article  PubMed  CAS  Google Scholar 

  • Hirokawa N, Noda Y (2008) Intracellular transport and kinesin superfamily proteins, KIFs: structure, function, and dynamics. Physiol Rev 88:1089–1118

    Article  PubMed  CAS  Google Scholar 

  • Hollenbeck PJ (1996) The pattern and mechanisms of mitochondrial transport in axons. Front Biosci 1:d91–d102

    PubMed  CAS  Google Scholar 

  • Hook P, Vallee RB (2006) The dynein family at a glance. J Cell Sci 119:4369–4371

    Article  PubMed  CAS  Google Scholar 

  • Hubley MJ, Locke BR, Moerland TS (1996) The effects of temperature, pH, and magnesium on the diffusion coefficient of ATP in solutions of physiological ionic strength. Biochim Biophys Acta 1291:115–121

    Article  PubMed  Google Scholar 

  • Hurd DD, Saxton WM (1996) Kinesin mutations cause motor neuron disease phenotypes by disrupting fast axonal transport in Drosophila. Genetics 144:1075–1085

    PubMed  CAS  Google Scholar 

  • Iyer SP, Akimoto Y, Hart GW (2003) Identification and cloning of a novel family of coiled-coil domain proteins that interact with O-GlcNAc transferase. J Biol Chem 278:5399–5409

    Article  PubMed  CAS  Google Scholar 

  • Jung D, Filliol D, Miehe M, Rendon A (1993) Interaction of brain mitochondria with microtubules reconstituted from brain tubulin and MAP2 or TAU. Cell Motil Cytoskeleton 24:245–255

    Article  PubMed  CAS  Google Scholar 

  • Kageyama GH, Wong-Riley MT (1984) The histochemical localization of cytochrome oxidase in the retina and lateral geniculate nucleus of the ferret, cat, and monkey, with particular reference to retinal mosaics and ON/OFF-center visual channels. J Neurosci 4:2445–2459

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kann O, Kovacs R (2007) Mitochondria and neuronal activity. Am J Physiol Cell Physiol 292:C641–657

    Article  PubMed  CAS  Google Scholar 

  • Kim Y, Sung JY, Ceglia I, Lee KW, Ahn JH, Halford JM, Kim AM, Kwak SP, Park JB, Ho Ryu S et al (2006) Phosphorylation of WAVE1 regulates actin polymerization and dendritic spine morphology. Nature 442:814–817

    Article  PubMed  CAS  Google Scholar 

  • King SJ, Schroer TA (2000) Dynactin increases the processivity of the cytoplasmic dynein motor. Nat Cell Biol 2:20–24

    Article  PubMed  CAS  Google Scholar 

  • King MJ, Atwood HL, Govind CK (1996) Structural features of crayfish phasic and tonic neuromuscular terminals. J Comp Neurol 372:618–626

    Article  PubMed  CAS  Google Scholar 

  • Koushika SP, Schaefer AM, Vincent R, Willis JH, Bowerman B, Nonet ML (2004) Mutations in Caenorhabditis elegans cytoplasmic dynein components reveal specificity of neuronal retrograde cargo. J Neurosci 24:3907–3916

    Article  PubMed  CAS  Google Scholar 

  • Krendel M, Sgourdas G, Bonder EM (1998) Disassembly of actin filaments leads to increased rate and frequency of mitochondrial movement along microtubules. Cell Motil Cytoskeleton 40:368–378

    Article  PubMed  CAS  Google Scholar 

  • Kumar J, Yu H, Sheetz MP (1995) Kinectin, an essential anchor for kinesin-driven vesicle motility. Science 267:1834–1837

    Article  PubMed  CAS  Google Scholar 

  • Kural C, Kim H, Syed S, Goshima G, Gelfand VI, Selvin PR (2005) Kinesin and dynein move a peroxisome in vivo: a tug-of-war or coordinated movement? Science 308:1469–1472

    Article  PubMed  CAS  Google Scholar 

  • Lai C, Lin X, Chandran J, Shim H, Yang WJ, Cai H (2007) The G59S mutation in p150(glued) causes dysfunction of dynactin in mice. J Neurosci 27:13982–13990

    Article  PubMed  CAS  Google Scholar 

  • LaMonte BH, Wallace KE, Holloway BA, Shelly SS, Ascano J, Tokito M, Van Winkle T, Howland DS, Holzbaur EL (2002) Disruption of dynein/dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron 34:715–727

    Article  PubMed  CAS  Google Scholar 

  • Langford GM (2002) Myosin-V, a versatile motor for short-range vesicle transport. Traffic 3:859–865

    Article  PubMed  CAS  Google Scholar 

  • Lao G, Scheuss V, Gerwin CM, Su Q, Mochida S, Rettig J, Sheng ZH (2000) Syntaphilin: a syntaxin-1 clamp that controls SNARE assembly. Neuron 25:191–201

    Article  PubMed  CAS  Google Scholar 

  • Lee CW, Peng HB (2006) Mitochondrial clustering at the vertebrate neuromuscular junction during presynaptic differentiation. J Neurobiol 66:522–536

    Article  PubMed  CAS  Google Scholar 

  • Leterrier JF, Rusakov DA, Linden M (1994a) Statistical analysis of the surface distribution of microtubule-associated proteins (MAPs) bound in vitro to rat brain mitochondria and labelled by 10 nm gold-coupled antibodies. Bull Assoc Anat (Nancy) 78:47–51

    CAS  Google Scholar 

  • Leterrier JF, Rusakov DA, Nelson BD, Linden M (1994b) Interactions between brain mitochondria and cytoskeleton: evidence for specialized outer membrane domains involved in the association of cytoskeleton-associated proteins to mitochondria in situ and in vitro. Microsc Res Tech 27:233–261

    Article  PubMed  CAS  Google Scholar 

  • Levy JR, Holzbaur EL (2006) Cytoplasmic dynein/dynactin function and dysfunction in motor neurons. Int J Dev Neurosci 24:103–111

    Article  PubMed  CAS  Google Scholar 

  • Li SH, Gutekunst CA, Hersch SM, Li XJ (1998) Interaction of huntingtin-associated protein with dynactin P150Glued. J Neurosci 18:1261–1269

    PubMed  CAS  Google Scholar 

  • Li Z, Okamoto K, Hayashi Y, Sheng M (2004) The importance of dentritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119:873–887

    Article  PubMed  CAS  Google Scholar 

  • Ligon LA, Steward O (2000a) Movement of mitochondria in the axons and dendrites of cultured hippocampal neurons. J Comp Neurol 427:340–350

    Article  PubMed  CAS  Google Scholar 

  • Ligon LA, Steward O (2000b) Role of microtubules and actin filaments in the movement of mitochondria in the axons and dendrites of cultured hippocampal neurons. J Comp Neurol 427:351–361

    Article  PubMed  CAS  Google Scholar 

  • Ligon LA, Tokito M, Finklestein JM, Grossman FE, Holzbaur EL (2004) A direct interaction between cytoplasmic dynein and kinesin I may coordinate motor activity. J Biol Chem 279:19201–19208

    Article  PubMed  CAS  Google Scholar 

  • Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443:787–795

    Article  PubMed  CAS  Google Scholar 

  • Linden M, Nelson BD, Leterrier JF (1989a) The specific binding of the microtubule-associated protein 2 (MAP2) to the outer membrane of rat brain mitochondria. Biochem J 261:167–173

    PubMed  CAS  Google Scholar 

  • Linden M, Nelson BD, Loncar D, Leterrier JF (1989b) Studies on the interaction between mitochondria and the cytoskeleton. J Bioenerg Biomembr 21:507–518

    Article  PubMed  CAS  Google Scholar 

  • Louie K, Russo GJ, Salkoff DB, Wellington A, Zinsmaier KE (2008) Effects of imaging conditions on mitochondrial transport and length in larval motor axons of Drosophila. Comp Biochem Physiol A Mol Integr Physiol 151:159–172

    Article  PubMed  CAS  Google Scholar 

  • Lyons DA, Naylor SG, Mercurio S, Dominguez C, Talbot WS (2008) KBP is essential for axonal structure, outgrowth and maintenance in zebrafish, providing insight into the cellular basis of Goldberg-Shprintzen syndrome. Development 135:599–608

    Article  PubMed  CAS  Google Scholar 

  • MacAskill AF, Brickley K, Stephenson FA, Kittler JT (2009a) GTPase dependent recruitment of Grif-1 by Miro1 regulates mitochondrial trafficking in hippocampal neurons. Mol Cell Neurosci 40:301–312

    Article  PubMed  CAS  Google Scholar 

  • MacAskill AF, Rinholm JE, Twelvetrees AE, Arancibia-Carcamo IL, Muir J, Fransson A, Aspenstrom P, Attwell D, Kittler JT (2009b) Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 61:541–555

    Article  PubMed  CAS  Google Scholar 

  • Mallik R, Petrov D, Lex SA, King SJ, Gross SP (2005) Building complexity: an in vitro study of cytoplasmic dynein with in vivo implications. Curr Biol 15:2075–2085

    Article  PubMed  CAS  Google Scholar 

  • Martin M, Iyadurai SJ, Gassman A, Gindhart JG Jr, Hays TS, Saxton WM (1999) Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport. Mol Biol Cell 10:3717–3728

    PubMed  CAS  Google Scholar 

  • Mather WH, Fox RF (2006) Kinesin’s biased stepping mechanism: amplification of neck linker zippering. Biophys J 91:2416–2426

    Article  PubMed  CAS  Google Scholar 

  • Mattson MP (2007) Mitochondrial regulation of neuronal plasticity. Neurochem Res 32:707–715

    Article  PubMed  CAS  Google Scholar 

  • Mattson MP, Gleichmann M, Cheng A (2008) Mitochondria in neuroplasticity and neurological disorders. Neuron 60:748–766

    Article  PubMed  CAS  Google Scholar 

  • Miller KG, Sheetz MP (2004) Axonal mitochondrial transport and potential are correlated. J Cell Sci 117:2791–2804

    Article  PubMed  CAS  Google Scholar 

  • Mironov SL (2006) Spontaneous and evoked neuronal activities regulate movements of single neuronal mitochondria. Synapse 59:403–411

    Article  PubMed  CAS  Google Scholar 

  • Misgeld T, Kerschensteiner M, Bareyre FM, Burgess RW, Lichtman JW (2007) Imaging axonal transport of mitochondria in vivo. Nat Methods 4:559–561

    Article  PubMed  CAS  Google Scholar 

  • Mok H, Shin H, Kim S, Lee JR, Yoon J, Kim E (2002) Association of the kinesin superfamily motor protein KIF1Balpha with postsynaptic density-95 (PSD-95), synapse-associated protein-97, and synaptic scaffolding molecule PSD-95/discs large/zona occludens-1 proteins. J Neurosci 22:5253–5258

    PubMed  CAS  Google Scholar 

  • Morris RL, Hollenbeck PJ (1993) The regulation of bidirectional mitochondrial transport is coordinated with axonal outgrowth. J Cell Sci 104:917–927

    PubMed  Google Scholar 

  • Morris RL, Hollenbeck PJ (1995) Axonal transport of mitochondria along microtubules and F- actin in living vertebrate neurons. J Cell Biol 131:1315–1326

    Article  PubMed  CAS  Google Scholar 

  • Muller MJ, Klumpp S, Lipowsky R (2008) Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors. Proc Natl Acad Sci USA 105:4609–4614

    Article  PubMed  Google Scholar 

  • Nan X, Sims PA, Chen P, Xie XS (2005) Observation of individual microtubule motor steps in living cells with endocytosed quantum dots. J Phys Chem B 109:24220–24224

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ong LL, Lim AP, Er CP, Kuznetsov SA, Yu H (2000) Kinectin-kinesin binding domains and their effects on organelle motility. J Biol Chem 275:32854–32860

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Pannese E, Ledda M (1991) Ribosomes in myelinated axons of the rabbit spinal ganglion neurons. J Submicrosc Cytol Pathol 23:33–38

    PubMed  CAS  Google Scholar 

  • Pannese E, Procacci P, Ledda M, Arcidiacono G, Frattola D, Rigamonti L (1986) Association between microtubules and mitochondria in myelinated axons of Lacerta muralis. A quantitative analysis. Cell Tissue Res 245:1–8

    Article  PubMed  CAS  Google Scholar 

  • Peters A, Palay S, Webster H (1991) The fine structure of the nervous system: the neurons and supporting cells. Oxford University Press, New York

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Plitz T, Pfeffer K (2001) Intact lysosome transport and phagosome function despite kinectin deficiency. Mol Cell Biol 21:6044–6055

    Article  PubMed  CAS  Google Scholar 

  • Price RL, Lasek RJ, Katz MJ (1991) Microtubules have special physical associations with smooth endoplasmic reticula and mitochondria in axons. Brain Res 540:209–216

    Article  PubMed  CAS  Google Scholar 

  • Reeve AK, Krishnan KJ, Turnbull D (2008) Mitochondrial DNA mutations in disease, aging, and neurodegeneration. Ann N Y Acad Sci 1147:21–29

    Article  PubMed  CAS  Google Scholar 

  • Rintoul GL, Filiano AJ, Brocard JB, Kress GJ, Reynolds IJ (2003) Glutamate decreases mitochondrial size and movement in primary forebrain neurons. J Neurosci 23:7881–7888

    PubMed  CAS  Google Scholar 

  • Rodionov V, Yi J, Kashina A, Oladipo A, Gross SP (2003) Switching between microtubule- and actin-based transport systems in melanophores is controlled by cAMP levels. Curr Biol 13:1837–1847

    Article  PubMed  CAS  Google Scholar 

  • Ross JL, Wallace K, Shuman H, Goldman YE, Holzbaur EL (2006) Processive bidirectional motion of dynein-dynactin complexes in vitro. Nat Cell Biol 8:562–570

    Article  PubMed  CAS  Google Scholar 

  • Rowland KC, Irby NK, Spirou GA (2000) Specialized synapse-associated structures within the calyx of Held. J Neurosci 20:9135–9144

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ruthel G, Hollenbeck PJ (2003) Response of mitochondrial traffic to axon determination and differential branch growth. J Neurosci 23:8618–8624

    PubMed  CAS  Google Scholar 

  • Safieddine S, Ly CD, Wang YX, Wang CY, Kachar B, Petralia RS, Wenthold RJ (2002) Ocsyn, a novel syntaxin-interacting protein enriched in the subapical region of inner hair cells. Mol Cell Neurosci 20:343–353

    Article  PubMed  CAS  Google Scholar 

  • Salinas S, Bilsland LG, Schiavo G (2008) Molecular landmarks along the axonal route: axonal transport in health and disease. Curr Opin Cell Biol 20:445–453

    Article  PubMed  CAS  Google Scholar 

  • Santama N, Er CP, Ong LL, Yu H (2004) Distribution and functions of kinectin isoforms. J Cell Sci 117:4537–4549

    Article  PubMed  CAS  Google Scholar 

  • Saotome M, Safiulina D, Szabadkai G, Das S, Fransson A, Aspenstrom P, Rizzuto R, Hajnoczky G (2008) Bidirectional Ca2+-dependent control of mitochondrial dynamics by the Miro GTPase. Proc Natl Acad Sci USA 105:20728–20733

    Article  PubMed  CAS  Google Scholar 

  • Saxton WM, Hicks J, Goldstein LSB, Raff EC (1991) Kinesins heavy chain is essential for viability and neuromuscular functions in Drosophila, but mutants show no defects in mitosis. Cell 64:1093–1102

    Article  PubMed  CAS  Google Scholar 

  • Scheffler IE (2008) Mitochondria, 2nd edn. J. Wiley and Sons, Inc., Hoboken, New Jersey

    Google Scholar 

  • Schroer TA (2004) Dynactin. Annu Rev Cell Dev Biol 20:759–779

    Article  PubMed  CAS  Google Scholar 

  • Sheetz MP, Dai J (1996) Modulation of membrane dynamics and cell motility by membrane tension. Trends Cell Biol 6:85–89

    Article  PubMed  CAS  Google Scholar 

  • Shepherd GM, Greer CA (1988) In: Lasek RS, Black MM (eds) Intrinsic determinants of neuronal form and function. Liss, New York, pp 245–262

    Google Scholar 

  • Shepherd GM, Harris KM (1998) Three-dimensional structure and composition of CA3−−>CA1 axons in rat hippocampal slices: implications for presynaptic connectivity and compartmentalization. J Neurosci 18:8300–8310

    PubMed  CAS  Google Scholar 

  • Smith DS, Jarlfors U, Cayer ML (1977) Structural cross-bridges between microtubules and mitochondria in central axons of an insect (Periplaneta americana). J Cell Sci 27:255–272

    PubMed  CAS  Google Scholar 

  • Smith GA, Gross SP, Enquist LW (2001) Herpesviruses use bidirectional fast-axonal transport to spread in sensory neurons. Proc Natl Acad Sci USA 98:3466–3470

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Su Q, Cai Q, Gerwin C, Smith CL, Sheng ZH (2004) Syntabulin is a microtubule-associated protein implicated in syntaxin transport in neurons. Nat Cell Biol 6:941–953

    Article  PubMed  CAS  Google Scholar 

  • Sung JY, Engmann O, Teylan MA, Nairn AC, Greengard P, Kim Y (2008) WAVE1 controls neuronal activity-induced mitochondrial distribution in dendritic spines. Proc Natl Acad Sci USA 105:3112–3116

    Article  PubMed  CAS  Google Scholar 

  • Suomalainen M, Nakano MY, Keller S, Boucke K, Stidwill RP, Greber UF (1999) Microtubule- dependent plus- and minus end-directed motilities are competing processes for nuclear targeting of adenovirus. J Cell Biol 144:657–672

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Toyoshima I, Yu H, Steuer ER, Sheetz MP (1992) Kinectin, a major kinesin-binding protein on ER. J Cell Biol 118:1121–1131

    Article  PubMed  CAS  Google Scholar 

  • Twig G, Hyde B, Shirihai OS (2008) Mitochondrial fusion, fission and autophagy as a quality control axis: the bioenergetic view. Biochim Biophys Acta 1777:1092–1097

    Article  PubMed  CAS  Google Scholar 

  • Vale RD (2003) The molecular toolbox for intracellular transport. Cell 112:467–480

    Article  PubMed  CAS  Google Scholar 

  • Valetti C, Wetzel DM, Schrader M, Hasbani MJ, Gill SR, Kreis TE, Schroer TA (1999) Role of dynactin in endocytic traffic: effects of dynamitin overexpression and colocalization with CLIP-170. Mol Biol Cell 10:4107–4120

    PubMed  CAS  Google Scholar 

  • Verburg J, Hollenbeck PJ (2008) Mitochondrial membrane potential in axons increases with local nerve growth factor or semaphorin signaling. J Neurosci 28:8306–8315

    Article  PubMed  CAS  Google Scholar 

  • Wagner OI, Lifshitz J, Janmey PA, Linden M, McIntosh TK, Leterrier JF (2003) Mechanisms of mitochondria-neurofilament interactions. J Neurosci 23:9046–9058

    PubMed  CAS  Google Scholar 

  • Wang Z, Sheetz MP (1999) One-dimensional diffusion on microtubules of particles coated with cytoplasmic dynein and immunoglobulins. Cell Struct Funct 24:373–383

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Schwarz TL (2009) The mechanism of Ca2+-dependent regulation of kinesin- mediated mitochondrial motility. Cell 136:163–174

    Article  PubMed  CAS  Google Scholar 

  • Waterman-Storer CM, Karki SB, Kuznetsov SA, Tabb JS, Weiss DG, Langford GM, Holzbaur EL (1997) The interaction between cytoplasmic dynein and dynactin is required for fast axonal transport. Proc Natl Acad Sci USA 94:12180–12185

    Article  PubMed  CAS  Google Scholar 

  • Wattenberg B, Lithgow T (2001) Targeting of C-terminal (tail)-anchored proteins: understanding how cytoplasmic activities are anchored to intracellular membranes. Traffic 2:66–71

    Article  PubMed  CAS  Google Scholar 

  • Welte MA (2004) Bidirectional transport along microtubules. Curr Biol 14:13

    Article  CAS  Google Scholar 

  • Welte MA, Gross SP, Postner M, Block SM, Wieschaus EF (1998) Developmental regulation of vesicle transport in Drosophila embryos: forces and kinetics. Cell 92:547–557

    Article  PubMed  CAS  Google Scholar 

  • Welte MA, Cermelli S, Griner J, Viera A, Guo Y, Kim DH, Gindhart JG, Gross SP (2005) Regulation of lipid-droplet transport by the perilipin homolog LSD2. Curr Biol 15:1266–1275

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Xia CH, Roberts EA, Her LS, Liu X, Williams DS, Cleveland DW, Goldstein LS (2003) Abnormal neurofilament transport caused by targeted disruption of neuronal kinesin heavy chain KIF5A. J Cell Biol 161:55–66

    Article  PubMed  CAS  Google Scholar 

  • Yi M, Weaver D, Hajnoczky G (2004) Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J Cell Biol 167:661–672

    Article  PubMed  CAS  Google Scholar 

  • Yildiz A, Tomishige M, Vale RD, Selvin PR (2004) Kinesin walks hand-over-hand. Science 303:676–678

    Article  PubMed  CAS  Google Scholar 

  • Zhao C, Takita J, Tanaka Y, Setou M, Nakagawa T, Takeda S, Yang HW, Terada S, Nakata T, Takei Y et al (2001) Charcot-Marie-Tooth disease type 2A caused by mutation in a microtubule motor KIF1Bbeta. Cell 105:587–597

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Arizona Research Laboratories, Division of Neurobiology, University of Arizona, Tucson, AZ, 85721, USA

    Konrad E. Zinsmaier

  2. Department of Molecular and Cellular Biology, University of Arizona, Tucson, AZ, 85721, USA

    Konrad E. Zinsmaier

  3. Arizona Research Laboratories, Division of Neurobiology, University of Arizona, Tucson, AZ, 85721, USA

    Milos Babic

  4. Graduate Program in Biochemistry and Molecular & Cellular Biology, University of Arizona, Tucson, AZ, 85721, USA

    Milos Babic

  5. Arizona Research Laboratories, Division of Neurobiology, University of Arizona, Tucson, AZ, 85721, USA

    Gary J. Russo

  6. Graduate Interdisciplinary Program in Neuroscience, University of Arizona, Tucson, AZ, 85721, USA

    Gary J. Russo

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  1. Konrad E. Zinsmaier
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  2. Milos Babic
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Correspondence to Konrad E. Zinsmaier .

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    Edward Koenig

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Zinsmaier, K.E., Babic, M., Russo, G.J. (2009). Mitochondrial Transport Dynamics in Axons and Dendrites. In: Koenig, E. (eds) Cell Biology of the Axon. Results and Problems in Cell Differentiation, vol 48. Springer, Berlin, Heidelberg. https://doi.org/10.1007/400_2009_20

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