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Axonal Transport Mechanisms in Cytoskeleton Formation and Regulation

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Book cover Cytoskeleton of the Nervous System

Part of the book series: Advances in Neurobiology ((NEUROBIOL,volume 3))

Abstract

Most axonal and synaptic proteins are synthesized within the cell body and must travel long distances along axons to reach their sites of function. It is widely accepted that membranous organelles are bidirectionally transported by motor proteins, including kinesins and dynein, at fast rates (50–400 mm/day) along axonal microtubules. The mechanisms underlying slow axonal transport of proteins, including components of the cytoskeleton, have been more elusive, although recent genetic and live-cell imaging approaches have yielded general principles about the dynamic behaviors of cytoskeletal elements and formation of the axonal cytoskeleton. Cytoskeletal components may undergo slow transport (0.1–10 mm/day in vivo) as short polymers or oligomeric assemblies of subunits that fully assemble during transport or after they incorporate into the axonal cytoskeleton. Slow transport rates for a particular cargo reflect a pattern of rapid movements along axons interrupted by pauses of varying short durations. In mature myelinated axons, proteins in transport represent a relatively small pool that serve as precursors to a large metabolically stable stationary cytoskeleton composed of neurofilaments networked together by cross bridging proteins along with microtubule and actin filaments. Cytoskeletal components may turn over by local subunit exchange or proteolysis or, alternatively, by detachment of a larger filament fragment that is translocated to a degradative site. Defects in specific aspects of this complex process are the basis for certain neurological disorders.

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References

  • Ackerley S, Thornhill P, Grierson AJ, Brownlees J, Anderton BH, Leigh PN, Shaw CE, Miller CC (2003) Neurofilament heavy chain side arm phosphorylation regulates axonal transport of neurofilaments. J Cell Biol 161:489–495

    Article  CAS  PubMed  Google Scholar 

  • Ahmari SE, Buchanan J, Smith SJ (2000) Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 3:445–451

    Article  CAS  PubMed  Google Scholar 

  • Aizawa H, Sekine Y, Takemura R, Zhang Z, Nangaku M, Hirokawa N (1992) Kinesin family in murine central nervous system. J Cell Biol 119:1287–1296

    Article  CAS  PubMed  Google Scholar 

  • Alami NH, Jung P, Brown A (2009) Myosin Va increases the efficiency of neurofilament transport by decreasing the duration of long-term pauses. J Neurosci 29:6625–6634

    Article  CAS  PubMed  Google Scholar 

  • Allen RD, Metuzals J, Tasaki I, Brady ST, Gilbert SP (1982) Fast axonal transport in squid giant axon. Science 218:1127–1129

    Article  CAS  PubMed  Google Scholar 

  • Alvarez J, Benech CR (1983) Axoplasmic incorporation of amino acids in a myelinated fiber exceeds that of its soma: a radioautographic study. Exp Neurol 82:25–42

    Article  CAS  PubMed  Google Scholar 

  • Austin L, Bray JJ, Young RJ (1966) Transport of proteins and ribonucleic acid along nerve axons. J Neurochem 13:1267–1269

    Article  CAS  PubMed  Google Scholar 

  • Baas PW, Brown A (1997) Slow axonal transport: the polymer transport model. Trends Cell Biol 7:380–384

    Article  CAS  PubMed  Google Scholar 

  • Bearer EL, DeGiorgis JA, Bodner RA, Kao AW, Reese TS (1993) Evidence for myosin motors on organelles in squid axoplasm. Proc Natl Acad Sci USA 90:11252–11256

    Article  CAS  PubMed  Google Scholar 

  • Bearer EL, DeGiorgis JA, Medeiros NA, Reese TS (1996) Actin-based motility of isolated axoplasmic organelles. Cell Motil Cytoskeleton 33:106–114

    Article  CAS  PubMed  Google Scholar 

  • Bisby MA (1982) Functions of retrograde axonal transport. Fed Proc 41:2307–2311

    CAS  PubMed  Google Scholar 

  • Black MM, Keyser P, Sobel E (1986) Interval between the synthesis and assembly of cytoskeletal proteins in cultured neurons. J Neurosci 6:1004–1012

    CAS  PubMed  Google Scholar 

  • Black MM, Lasek RJ (1979) Axonal transport of actin: slow component b is the principal source of actin for the axon. Brain Res 171:401–413

    Article  CAS  PubMed  Google Scholar 

  • Black MM, Lasek RJ (1980) Slow components of axonal transport: two cytoskeletal networks. J Cell Biol 86:616–623

    Article  CAS  PubMed  Google Scholar 

  • Bourke GJ, El Alami W, Wilson SJ, Yuan A, Roobol A, Carden MJ (2002) Slow axonal transport of the cytosolic chaperonin CCT with Hsc73 and actin in motor neurons. J Neurosci Res 68:29–35

    Article  CAS  PubMed  Google Scholar 

  • Brady ST (1985) A novel brain ATPase with properties expected for the fast axonal transport motor. Nature 317:73–75

    Article  CAS  PubMed  Google Scholar 

  • Brady ST, Crothers SD, Nosal C, McClure WO (1980) Fast axonal transport in the presence of high Ca2+: evidence that microtubules are not required. Proc Natl Acad Sci USA 77:5909–5913

    Article  CAS  PubMed  Google Scholar 

  • Brady ST, Lasek RJ, Allen RD (1982) Fast axonal transport in extruded axoplasm from squid giant axon. Science 218:1129–1131

    Article  CAS  PubMed  Google Scholar 

  • Brady ST, Lasek RJ, Allen RD, Yin HL, Stossel TP (1984) Gelsolin inhibition of fast axonal transport indicates a requirement for actin microfilaments. Nature 310:56–58

    Article  CAS  PubMed  Google Scholar 

  • Bray JJ, Austin L (1968) Flow of protein and ribonucleic acid in peripheral nerve. J Neurochem 15:731–740

    Article  CAS  PubMed  Google Scholar 

  • Bray JJ, Kon CM, Breckenridge BM (1971) Reversed polarity of rapid axonal transport in chicken motoneurons. Brain Res 33:560–564

    Article  CAS  PubMed  Google Scholar 

  • Bridgman PC (2004) Myosin-dependent transport in neurons. J Neurobiol 58:164–174

    Article  CAS  PubMed  Google Scholar 

  • Brown A (2000) Slow axonal transport: stop and go traffic in the axon. Nat Rev Mol Cell Biol 1:153–156

    Article  CAS  PubMed  Google Scholar 

  • Brown A (2009) Slow axonal transport. In: Squire L (ed) Encyclopedia of neuroscience. Elsevier, New York, NY, pp 1–9

    Chapter  Google Scholar 

  • Brown A, Wang L, Jung P (2005) Stochastic simulation of neurofilament transport in axons: the “stop-and-go” hypothesis. Mol Biol Cell 16:4243–4255

    Article  CAS  PubMed  Google Scholar 

  • Burridge K, Bray D (1975) Purification and structural analysis of myosins from brain and other non-muscle tissues. J Mol Biol 99:1–14

    Article  CAS  PubMed  Google Scholar 

  • Campenot RB, Eng H (2000) Protein synthesis in axons and its possible functions. J Neurocytol 29:793–798

    Article  CAS  PubMed  Google Scholar 

  • Cena V, Garcia AG, Gonzalez-Garcia C, Kirpekar SM (1984) Orthograde and retrograde axonal transport of calmodulin in a cat noradrenergic neurone. Br J Pharmacol 82:143–149

    CAS  PubMed  Google Scholar 

  • Chadan S, Le Gall JY, Di Giamberardino L, Filliatreau G (1994) Axonal transport of type III intermediate filament protein peripherin in intact and regenerating motor axons of the rat sciatic nerve. J Neurosci Res 39:127–139

    Article  CAS  PubMed  Google Scholar 

  • Cheney RE, O’Shea MK, Heuser JE, Coelho MV, Wolenski JS, Espreafico EM, Forscher P, Larson RE, Mooseker MS (1993) Brain myosin-V is a two-headed unconventional myosin with motor activity. Cell 75:13–23

    CAS  PubMed  Google Scholar 

  • Cleveland DW, Hoffman PN (1991) Slow axonal transport models come full circle: evidence that microtubule sliding mediates axon elongation and tubulin transport. Cell 67:453–456

    Article  CAS  PubMed  Google Scholar 

  • Colicos MA, Collins BE, Sailor MJ, Goda Y (2001) Remodeling of synaptic actin induced by photoconductive stimulation. Cell 107:605–616

    Article  CAS  PubMed  Google Scholar 

  • Coling DE, Espreafico EM, Kachar B (1997) Cellular distribution of myosin-V in the guinea pig cochlea. J Neurocytol 26:113–120

    Article  CAS  PubMed  Google Scholar 

  • Correia SS, Bassani S, Brown TC, Lise MF, Backos DS, El-Husseini A, Passafaro M, Esteban JA (2008) Motor protein-dependent transport of AMPA receptors into spines during long-term potentiation. Nat Neurosci 11:457–466

    Article  CAS  PubMed  Google Scholar 

  • Cui B, Wu C, Chen L, Ramirez A, Bearer EL, Li WP, Mobley WC, Chu S (2007) One at a time, live tracking of NGF axonal transport using quantum dots. Proc Natl Acad Sci USA 104:13666–13671

    Article  CAS  PubMed  Google Scholar 

  • Cyr JL, Brady ST (1992) Molecular motors in axonal transport. cellular and molecular biology of kinesin. Mol Neurobiol 6:137–155

    Article  CAS  PubMed  Google Scholar 

  • Dahlstrom AB, Pfister KK, Brady ST (1991) The axonal transport motor ‘kinesin’ is bound to anterogradely transported organelles: quantitative cytofluorimetric studies of fast axonal transport in the rat. Acta Physiol Scand 141:469–476

    Article  CAS  PubMed  Google Scholar 

  • Dillman JF 3rd, Dabney LP, Karki S, Paschal BM, Holzbaur EL, Pfister KK (1996b) Functional analysis of dynactin and cytoplasmic dynein in slow axonal transport. J Neurosci 16:6742–6752

    CAS  PubMed  Google Scholar 

  • Dillman JF 3rd, Dabney LP, Pfister KK (1996a) Cytoplasmic dynein is associated with slow axonal transport. Proc Natl Acad Sci USA 93:141–144

    Article  CAS  PubMed  Google Scholar 

  • DiStefano PS, Friedman B, Radziejewski C, Alexander C, Boland P, Schick CM, Lindsay RM, Wiegand SJ (1992) The neurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron 8:983–993

    Article  CAS  PubMed  Google Scholar 

  • Droz B, Barondes SM (1969) Nerve endings: rapid appearance of labeled protein shown by electron microscope radioautography. Science 165:1131–1133

    Article  CAS  PubMed  Google Scholar 

  • Droz B, Leblond CP (1962) Migration of proteins along the axons of the sciatic nerve. Science 137:1047–1048

    Article  CAS  PubMed  Google Scholar 

  • Droz B, Leblond CP (1963) Axonal migration of proteins in the central nervous system and peripheral nerves as shown by radioautography. J Comp Neurol 121:325–346

    Article  CAS  PubMed  Google Scholar 

  • Elluru RG, Bloom GS, Brady ST (1995) Fast axonal transport of kinesin in the rat visual system: functionality of kinesin heavy chain isoforms. Mol Biol Cell 6:21–40

    CAS  PubMed  Google Scholar 

  • Eng H, Lund K, Campenot RB (1999) Synthesis of beta-tubulin, actin, and other proteins in axons of sympathetic neurons in compartmented cultures. J Neurosci 19:1–9

    CAS  PubMed  Google Scholar 

  • Espreafico EM, Cheney RE, Matteoli M, Nascimento AA, De Camilli PV, Larson RE, Mooseker MS (1992) Primary structure and cellular localization of chicken brain myosin-V (p190), an unconventional myosin with calmodulin light chains. J Cell Biol 119:1541–1557

    Article  CAS  PubMed  Google Scholar 

  • Evans LL, Bridgman PC (1995) Particles move along actin filament bundles in nerve growth cones. Proc Natl Acad Sci USA 92:10954–10958

    Article  CAS  PubMed  Google Scholar 

  • Fine RE, Bray D (1971) Actin in growing nerve cells. Nat New Biol 234:115–118

    Article  CAS  PubMed  Google Scholar 

  • Flynn KC, Pak CW, Shaw AE, Bradke F, Bamburg JR (2009) Growth cone-like waves transport actin and promote axonogenesis and neurite branching. Dev Neurobiol 69:761–779

    Article  CAS  PubMed  Google Scholar 

  • Francis F, Roy S, Brady ST, Black MM (2005) Transport of neurofilaments in growing axons requires microtubules but not actin filaments. J Neurosci Res 79:442–450

    Article  CAS  PubMed  Google Scholar 

  • Frappier T, Derancourt J, Pradel LA (1992) Actin and neurofilament binding domain of brain spectrin beta subunit. Eur J Biochem 205:85–91

    Article  CAS  PubMed  Google Scholar 

  • Frappier T, Stetzkowski-Marden F, Pradel LA (1991) Interaction domains of neurofilament light chain and brain spectrin. Biochem J 275(Pt 2):521–527

    CAS  PubMed  Google Scholar 

  • Gainer H, Fink DJ (1982) Evidence for slow retrograde transport of serum albumin in rat sciatic nerve. Brain Res 233:404–408

    Article  CAS  PubMed  Google Scholar 

  • Galbraith JA, Gallant PE (2000) Axonal transport of tubulin and actin. J Neurocytol 29:889–911

    Article  CAS  PubMed  Google Scholar 

  • Galbraith JA, Reese TS, Schlief ML, Gallant PE (1999) Slow transport of unpolymerized tubulin and polymerized neurofilament in the squid giant axon. Proc Natl Acad Sci USA 96:11589–11594

    Article  CAS  PubMed  Google Scholar 

  • Glass JD, Griffin JW (1994) Retrograde transport of radiolabeled cytoskeletal proteins in transected nerves. J Neurosci 14:3915–3921

    CAS  PubMed  Google Scholar 

  • Goldberg DJ (1982) Microinjection into an identified axon to study the mechanism of fast axonal transport. Proc Natl Acad Sci USA 79:4818–4822

    Article  CAS  PubMed  Google Scholar 

  • Goldberg DJ, Harris DA, Lubit BW, Schwartz JH (1980) Analysis of the mechanism of fast axonal transport by intracellular injection of potentially inhibitory macromolecules: evidence for a possible role of actin filaments. Proc Natl Acad Sci USA 77:7448–7452

    Article  CAS  PubMed  Google Scholar 

  • Goodson HV, Valetti C, Kreis TE (1997) Motors and membrane traffic. Curr Opin Cell Biol 9:18–28

    Article  CAS  PubMed  Google Scholar 

  • Grafstein B (1967) Transport of protein by goldfish optic nerve fibers. Science 157:196–198

    Article  CAS  PubMed  Google Scholar 

  • Grafstein B, Forman DS (1980) Intracellular transport in neurons. Physiol Rev 60:1167–1283

    CAS  PubMed  Google Scholar 

  • Grafstein B, McEwen BS, Shelanski ML (1970) Axonal transport of neurotubule protein. Nature 227:289–290

    Article  CAS  PubMed  Google Scholar 

  • Hasson T, Mooseker MS (1994) Porcine myosin-VI: characterization of a new mammalian unconventional myosin. J Cell Biol 127:425–440

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Helfand BT, Loomis P, Yoon M, Goldman RD (2003) Rapid transport of neural intermediate filament protein. J Cell Sci 116:2345–2359

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Hirokawa N (1993) Axonal transport and the cytoskeleton. Curr Opin Neurobiol 3:724–731

    Article  CAS  PubMed  Google Scholar 

  • Hirokawa N (1998) Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279:519–526

    Article  CAS  PubMed  Google Scholar 

  • Hirokawa N, Sato-Yoshitake R, Yoshida T, Kawashima T (1990) Brain dynein (MAP1C) localizes on both anterogradely and retrogradely transported membranous organelles in vivo. J Cell Biol 111:1027–1037

    Article  CAS  PubMed  Google Scholar 

  • Hirokawa N, Terada S, Funakoshi T, Tekeda S (1997) Slow axonal transport: the subunit transport model. Trends Cell Biol 7:384–388

    Article  CAS  PubMed  Google Scholar 

  • Hodgkin AL (1976) Chance and design in electrophysiology: an informal account of certain experiments on nerve carried out between 1934 and 1952. J Physiol 263:1–21

    CAS  PubMed  Google Scholar 

  • Hodgkin AL, Huxley AF (1939) Action potentials recorded from inside a nerve fibres. Nature (Lond) 144:710–711

    Article  Google Scholar 

  • Hollenbeck PJ (1993) Products of endocytosis and autophagy are retrieved from axons by regulated retrograde organelle transport. J Cell Biol 121:305–315

    Article  CAS  PubMed  Google Scholar 

  • Hou L, Lanni F, Luby-Phelps K (1990) Tracer diffusion in F-actin and Ficoll mixtures. toward a model for cytoplasm. Biophys J 58:31–43

    Article  CAS  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

    CAS  PubMed  Google Scholar 

  • James KA, Bray JJ, Morgan IG, Austin L (1970) The effect of colchicine on the transport of axonal protein in the chicken. Biochem J 117:767–771

    CAS  PubMed  Google Scholar 

  • Jung C, Chylinski TM, Pimenta A, Ortiz D, Shea TB (2004) Neurofilament transport is dependent on actin and myosin. J Neurosci 24:9486–9496

    Article  CAS  PubMed  Google Scholar 

  • Karlsson JO, Sjostrand J (1971) Synthesis, migration and turnover of protein in retinal ganglion cells. J Neurochem 18:749–767

    Article  CAS  PubMed  Google Scholar 

  • Kim T, Chang S (2006) Quantitative evaluation of the mode of microtubule transport in Xenopus neurons. Mol Cells 21:76–81

    CAS  PubMed  Google Scholar 

  • Kimura T, Watanabe H, Iwamatsu A, Kaibuchi K (2005) Tubulin and CRMP-2 complex is transported via Kinesin-1. J Neurochem 93:1371–1382

    Article  CAS  PubMed  Google Scholar 

  • Kirkpatrick JB, Bray JJ, Palmer SM (1972) Visualization of axoplasmic flow in vitro by Nomarski microscopy. comparison to rapid flow of radioactive proteins. Brain Res 43:1–10

    Article  CAS  PubMed  Google Scholar 

  • Kuo H, Ingram DK, Crystal RG, Mastrangeli A (1995) Retrograde transfer of replication deficient recombinant adenovirus vector in the central nervous system for tracing studies. Brain Res 705:31–38

    Article  CAS  PubMed  Google Scholar 

  • Kuznetsov SA, Langford GM, Weiss DG (1992) Actin-dependent organelle movement in squid axoplasm. Nature 356:722–725

    Article  CAS  PubMed  Google Scholar 

  • Kuznetsov SA, Rivera DT, Severin FF, Weiss DG, Langford GM (1994) Movement of axoplasmic organelles on actin filaments from skeletal muscle. Cell Motil Cytoskeleton 28:231–242

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Langford GM, Kuznetsov SA, Johnson D, Cohen DL, Weiss DG (1994) Movement of axoplasmic organelles on actin filaments assembled on acrosomal processes: evidence for a barbed-end-directed organelle motor. J Cell Sci 107(8):2291–2298

    PubMed  Google Scholar 

  • Lasek RJ (1967) Bidirectional transport of radioactively labelled axoplasmic components. Nature 216:1212–1214

    Article  CAS  PubMed  Google Scholar 

  • Lasek R (1968a) Axoplasmic transport in cat dorsal root ganglion cells: as studied with [3-H]-L-leucine. Brain Res 7:360–377

    Article  CAS  PubMed  Google Scholar 

  • Lasek RJ (1968b) Axoplasmic transport of labeled proteins in rat ventral motoneurons. Exp Neurol 21:41–51

    Article  CAS  PubMed  Google Scholar 

  • Lasek RJ (1986) Polymer sliding in axons. J Cell Sci Suppl 5:161–179

    CAS  PubMed  Google Scholar 

  • Lasek RJ, Garner JA, Brady ST (1984) Axonal transport of the cytoplasmic matrix. J Cell Biol 99:212 s–221 s

    Article  Google Scholar 

  • Lasek RJ, Paggi P, Katz MJ (1992) Slow axonal transport mechanisms move neurofilaments relentlessly in mouse optic axons. J Cell Biol 117:607–616

    Article  CAS  PubMed  Google Scholar 

  • LaVail JH, LaVail MM (1972) Retrograde axonal transport in the central nervous system. Science 176:1416–1417

    Article  CAS  PubMed  Google Scholar 

  • Lee SK, Hollenbeck PJ (2003) Organization and translation of mRNA in sympathetic axons. J Cell Sci 116:4467–4478

    Article  CAS  PubMed  Google Scholar 

  • Leterrier JF, Eyer J (1987) Properties of highly viscous gels formed by neurofilaments in vitro. A possible consequence of a specific inter-filament cross-bridging. Biochem J 245:93–101

    CAS  PubMed  Google Scholar 

  • Leterrier JF, Liem RK, Shelanski ML (1982) Interactions between neurofilaments and microtubule-associated proteins: a possible mechanism for intraorganellar bridging. J Cell Biol 95:982–986

    Article  CAS  PubMed  Google Scholar 

  • Lewis TL Jr, Mao T, Svoboda K, Arnold DB (2009) Myosin-dependent targeting of transmembrane proteins to neuronal dendrites. Nat Neurosci 12:568–576

    Article  CAS  PubMed  Google Scholar 

  • Li D, Chantler PD (1992) Evidence for a new member of the myosin I family from mammalian brain. J Neurochem 59:1344–1351

    Article  CAS  PubMed  Google Scholar 

  • Li D, Miller M, Chantler PD (1994) Association of a cellular myosin II with anionic phospholipids and the neuronal plasma membrane. Proc Natl Acad Sci USA 91:853–857

    Article  CAS  PubMed  Google Scholar 

  • Lim SS, Edson KJ, Letourneau PC, Borisy GG (1990) A test of microtubule translocation during neurite elongation. J Cell Biol 111:123–130

    Article  CAS  PubMed  Google Scholar 

  • Lorenz T, Willard M (1978) Subcellular fractionation of intra-axonally transport polypeptides in the rabbit visual system. Proc Natl Acad Sci USA 75:505–509

    Article  CAS  PubMed  Google Scholar 

  • Lubinska L, Niemierko S, Oderfeld Nowak B, Szwarc L (1964) Behaviour of acetylcholinesterase in isolated nerve segments. J Neurochem 11:493–503

    Article  CAS  PubMed  Google Scholar 

  • Ma D, Himes BT, Shea TB, Fischer I (2000) Axonal transport of microtubule-associated protein 1B (MAP1B) in the sciatic nerve of adult rat: distinct transport rates of different isoforms. J Neurosci 20:2112–2120

    CAS  PubMed  Google Scholar 

  • Ma Y, Shakiryanova D, Vardya I, Popov SV (2004) Quantitative analysis of microtubule transport in growing nerve processes. Curr Biol 14:725–730

    Article  CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Mazarakis ND, Azzouz M, Rohll JB, Ellard FM, Wilkes FJ, Olsen AL, Carter EE, Barber RD, Baban DF, Kingsman SM, Kingsman AJ, O’Malley K, Mitrophanous KA (2001) Rabies virus glycoprotein pseudotyping of lentiviral vectors enables retrograde axonal transport and access to the nervous system after peripheral delivery. Hum Mol Genet 10:2109–2121

    Article  CAS  PubMed  Google Scholar 

  • Mercken M, Fischer I, Kosik KS, Nixon RA (1995) Three distinct axonal transport rates for tau, tubulin, and other microtubule-associated proteins: evidence for dynamic interactions of tau with microtubules in vivo. J Neurosci 15:8259–8267

    CAS  PubMed  Google Scholar 

  • Miani N (1960) Proximo-distal movement along the axon of protein synthesized in the perikaryon of regenerating neurons. Nature 185:541

    Article  CAS  PubMed  Google Scholar 

  • Millecamps S, Gowing G, Corti O, Mallet J, Julien JP (2007) Conditional NF-L transgene expression in mice for in vivo analysis of turnover and transport rate of neurofilaments. J Neurosci 27:4947–4956

    Article  CAS  PubMed  Google Scholar 

  • Mills RG, Minamide LS, Yuan A, Bamburg JR, Bray JJ (1996) Slow axonal transport of soluble actin with actin depolymerizing factor, cofilin, and profilin suggests actin moves in an unassembled form. J Neurochem 67:1225–1234

    Article  CAS  PubMed  Google Scholar 

  • Mitsumoto HaW B (1987) Structure and development of nerves. In: Vinken P, Bruyn GW, Klawans HL (eds) Handbook of clinnical neurology. Elsevier Health Sciences, Philadelphia, PA, pp 1–22

    Google Scholar 

  • Miyata Y, Hoshi M, Nishida E, Minami Y, Sakai H (1986) Binding of microtubule-associated protein 2 and tau to the intermediate filament reassembled from neurofilament 70-kDa subunit protein. Its regulation by calmodulin. J Biol Chem 261:13026–13030

    CAS  PubMed  Google Scholar 

  • Mochida S, Kobayashi H, Matsuda Y, Yuda Y, Muramoto K, Nonomura Y (1994) Myosin II is involved in transmitter release at synapses formed between rat sympathetic neurons in culture. Neuron 13:1131–1142

    Article  CAS  PubMed  Google Scholar 

  • Mooseker M (1993) Myosin superfamily: a multitude of myosins. Curr Biol 3:245–248

    Article  CAS  PubMed  Google Scholar 

  • Mooseker MS, Cheney RE (1995) Unconventional myosins. Annu Rev Cell Dev Biol 11:633–675

    Article  CAS  PubMed  Google Scholar 

  • Morel N, Gerard V, Shiff G (1998) Vacuolar H+-ATPase domains are transported separately in axons and assemble in Torpedo nerve endings. J Neurochem 71:1702–1708

    Article  CAS  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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Nauta HJ, Pritz MB, Lasek RJ (1974) Afferents to the rat caudoputamen studied with horseradish peroxidase. an evaluation of a retrograde neuroanatomical research method. Brain Res 67:219–238

    Article  CAS  PubMed  Google Scholar 

  • Nixon RA (1998a) The slow axonal transport of cytoskeletal proteins. Curr Opin Cell Biol 10:87–92

    Article  CAS  PubMed  Google Scholar 

  • Nixon RA (1998b) The slow axonal transport debate. Trends Cell Biol 8:100

    Article  CAS  PubMed  Google Scholar 

  • Nixon RA, Logvinenko KB (1986) Multiple fates of newly synthesized neurofilament proteins: evidence for a stationary neurofilament network distributed nonuniformly along axons of retinal ganglion cell neurons. J Cell Biol 102:647–659

    Article  CAS  PubMed  Google Scholar 

  • Nixon RA, Shea TB (1992) Dynamics of neuronal intermediate filaments: a developmental perspective. Cell Motil Cytoskeleton 22:81–91

    Article  CAS  PubMed  Google Scholar 

  • Noda Y, Sato-Yoshitake R, Kondo S, Nangaku M, Hirokawa N (1995) KIF2 is a new microtubule-based anterograde motor that transports membranous organelles distinct from those carried by kinesin heavy chain or KIF3A/B. J Cell Biol 129:157–167

    Article  CAS  PubMed  Google Scholar 

  • Ochs S (1975a) A unitary concept of axoplasmic transport based on the transport filament hypothesis. In: Bradley WG, Gardner-Medwin D, Walton JN (eds) Third international congress on muscle disease. Eccerpta Medica, Amsterdam, pp 128–133

    Google Scholar 

  • Ochs S (1975b) Retention and redistribution of proteins in mammalian nerve fibres by axoplasmic transport. J Physiol 253:459–475

    CAS  PubMed  Google Scholar 

  • Ochs S, Burger E (1958) Movement of substance proximo-distally in nerve axons as studied with spinal cord injections of radioactive phosphorus. Am J Physiol 194:499–506

    CAS  PubMed  Google Scholar 

  • Ochs S, Jersild RA Jr., Li JM (1989) Slow transport of freely movable cytoskeletal components shown by beading partition of nerve fibers in the cat. Neuroscience 33:421–430

    Article  CAS  PubMed  Google Scholar 

  • Ochs S, Johnson J, Ng MH (1967) Protein incorporation and axoplasmic flow in motoneuron fibres following intra-cord injection of labelled leucine. J Neurochem 14:317–331

    Article  CAS  PubMed  Google Scholar 

  • Okabe S, Hirokawa N (1993) Do photobleached fluorescent microtubules move? Re-evaluation of fluorescence laser photobleaching both in vitro and in growing Xenopus axon. J Cell Biol 120:1177–1186

    Article  CAS  PubMed  Google Scholar 

  • Okada Y, Yamazaki H, Sekine-Aizawa Y, Hirokawa N (1995) The neuron-specific kinesin superfamily protein KIF1A is a unique monomeric motor for anterograde axonal transport of synaptic vesicle precursors. Cell 81:769–780

    Article  CAS  PubMed  Google Scholar 

  • Pachter JS, Liem RK (1984) The differential appearance of neurofilament triplet polypeptides in the developing rat optic nerve. Dev Biol 103:200–210

    Article  CAS  PubMed  Google Scholar 

  • Pannese E (1994) Neurocytology. Thieme Publishers, New York, NY

    Google Scholar 

  • Paschal BM, Shpetner HS, Vallee RB (1987) MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties. J Cell Biol 105:1273–1282

    Article  CAS  PubMed  Google Scholar 

  • Perkins GA, Sosinsky GE, Ghassemzadeh S, Perez A, Jones Y, Ellisman MH (2008) Electron tomographic analysis of cytoskeletal cross-bridges in the paranodal region of the node of Ranvier in peripheral nerves. J Struct Biol 161:469–480

    Article  CAS  PubMed  Google Scholar 

  • Prahlad V, Helfand BT, Langford GM, Vale RD, Goldman RD (2000) Fast transport of neurofilament protein along microtubules in squid axoplasm. J Cell Sci 113(22):3939–3946

    CAS  PubMed  Google Scholar 

  • Prekeris R, Terrian DM (1997) Brain myosin V is a synaptic vesicle-associated motor protein: evidence for a Ca2+-dependent interaction with the synaptobrevin-synaptophysin complex. J Cell Biol 137:1589–1601

    Article  CAS  PubMed  Google Scholar 

  • Provance DW Jr, McDowall A, Marko M, Luby-Phelps K (1993) Cytoarchitecture of size-excluding compartments in living cells. J Cell Sci 106(2):565–577

    PubMed  Google Scholar 

  • Ramon y Cajar S (1928) Degeneration and regeneration of the nervous sytem. Oxford University Press, London

    Google Scholar 

  • Rao MV, Engle LJ, Mohan PS, Yuan A, Qiu D, Cataldo A, Hassinger L, Jacobsen S, Lee VM, Andreadis A, Julien JP, Bridgman PC, Nixon RA (2002) Myosin Va binding to neurofilaments is essential for correct myosin Va distribution and transport and neurofilament density. J Cell Biol 159:279–290

    Article  CAS  PubMed  Google Scholar 

  • Roy S, Coffee P, Smith G, Liem RK, Brady ST, Black MM (2000) Neurofilaments are transported rapidly but intermittently in axons: implications for slow axonal transport. J Neurosci 20:6849–6861

    CAS  PubMed  Google Scholar 

  • Ruthel G, Banker G (1998) Actin-dependent anterograde movement of growth-cone-like structures along growing hippocampal axons: a novel form of axonal transport? Cell Motil Cytoskeleton 40:160–173

    Article  CAS  PubMed  Google Scholar 

  • Ruthel G, Banker G (1999) Role of moving growth cone-like “wave” structures in the outgrowth of cultured hippocampal axons and dendrites. J Neurobiol 39:97–106

    Article  CAS  PubMed  Google Scholar 

  • Sankaranarayanan S, Atluri PP, Ryan TA (2003) Actin has a molecular scaffolding, not propulsive, role in presynaptic function. Nat Neurosci 6:127–135

    Article  CAS  PubMed  Google Scholar 

  • Schnapp BJ, Vale RD, Sheetz MP, Reese TS (1985) Single microtubules from squid axoplasm support bidirectional movement of organelles. Cell 40:455–462

    Article  CAS  PubMed  Google Scholar 

  • Schroer TA (1992) Motors for fast axonal transport. Curr Opin Neurobiol 2:618–621

    Article  CAS  PubMed  Google Scholar 

  • Schroer TA, Steuer ER, Sheetz MP (1989) Cytoplasmic dynein is a minus end-directed motor for membranous organelles. Cell 56:937–946

    Article  CAS  PubMed  Google Scholar 

  • Shah JV, Cleveland DW (2002) Slow axonal transport: fast motors in the slow lane. Curr Opin Cell Biol 14:58–62

    Article  CAS  PubMed  Google Scholar 

  • Shah JV, Flanagan LA, Janmey PA, Leterrier JF (2000) Bidirectional translocation of neurofilaments along microtubules mediated in part by dynein/dynactin. Mol Biol Cell 11:3495–3508

    CAS  PubMed  Google Scholar 

  • Sheetz MP, Martenson CH (1991) Axonal transport: beyond kinesin and cytoplasmic dynein. Curr Opin Neurobiol 1:393–398

    Article  CAS  PubMed  Google Scholar 

  • Sheetz MP, Spudich JA (1983) Movement of myosin-coated fluorescent beads on actin cables in vitro. Nature 303:31–35

    Article  CAS  PubMed  Google Scholar 

  • Sodeik B, Ebersold MW, Helenius A (1997) Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J Cell Biol 136:1007–1021

    Article  CAS  PubMed  Google Scholar 

  • Sotelo-Silveira JR, Calliari A, Kun A, Koenig E, Sotelo JR (2006) RNA trafficking in axons. Traffic 7:508–515

    Article  CAS  PubMed  Google Scholar 

  • Stromska DP, Ochs S (1981) Patterns of slow transport in sensory nerves. J Neurobiol 12:441–453

    Article  CAS  PubMed  Google Scholar 

  • Sun WD, Chantler PD (1991) A unique cellular myosin II exhibiting differential expression in the cerebral cortex. Biochem Biophys Res Commun 175:244–249

    Article  CAS  PubMed  Google Scholar 

  • Sun W, Chantler PD (1992) Cloning of the cDNA encoding a neuronal myosin heavy chain from mammalian brain and its differential expression within the central nervous system. J Mol Biol 224:1185–1193

    Article  CAS  PubMed  Google Scholar 

  • Svitkina TM, Verkhovsky AB, Borisy GG (1996) Plectin sidearms mediate interaction of intermediate filaments with microtubules and other components of the cytoskeleton. J Cell Biol 135:991–1007

    Article  CAS  PubMed  Google Scholar 

  • Tabb JS, Molyneaux BJ, Cohen DL, Kuznetsov SA, Langford GM (1998) Transport of ER vesicles on actin filaments in neurons by myosin V. J Cell Sci 111(21):3221–3234

    CAS  PubMed  Google Scholar 

  • Terada S, Nakata T, Peterson AC, Hirokawa N (1996) Visualization of slow axonal transport in vivo. Science 273:784–788

    Article  CAS  PubMed  Google Scholar 

  • Theiss C, Napirei M, Meller K (2005) Impairment of anterograde and retrograde neurofilament transport after anti-kinesin and anti-dynein antibody microinjection in chicken dorsal root ganglia. Eur J Cell Biol 84:29–43

    Article  CAS  PubMed  Google Scholar 

  • Trivedi N, Jung P, Brown A (2007) Neurofilaments switch between distinct mobile and stationary states during their transport along axons. J Neurosci 27:507–516

    Article  CAS  PubMed  Google Scholar 

  • Tsukita S, Ishikawa H (1980) The movement of membranous organelles in axons. Electron microscopic identification of anterogradely and retrogradely transported organelles. J Cell Biol 84:513–530

    Article  CAS  PubMed  Google Scholar 

  • Vale RD, Reese TS, Sheetz MP (1985a) Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42:39–50

    Article  CAS  PubMed  Google Scholar 

  • Vale RD, Schnapp BJ, Reese TS, Sheetz MP (1985b) Movement of organelles along filaments dissociated from the axoplasm of the squid giant axon. Cell 40:449–454

    Article  CAS  PubMed  Google Scholar 

  • Vallee RB, Bloom GS (1991) Mechanisms of fast and slow axonal transport. Annu Rev Neurosci 14:59–92

    Article  CAS  PubMed  Google Scholar 

  • Wagner OI, Ascano J, Tokito M, Leterrier JF, Janmey PA, Holzbaur EL (2004) The interaction of neurofilaments with the microtubule motor cytoplasmic dynein. Mol Biol Cell 15:5092–5100

    Article  CAS  PubMed  Google Scholar 

  • Waller AV (1850) Experiments on the section of the glossopharyngeal and hypoglossal nerves of the frog, and observations of the alterations produced thereby in the structure of their primitive fibres. Philos Trans R Soc London 140:423–429

    Article  Google Scholar 

  • Wang L, Brown A (2002) Rapid movement of microtubules in axons. Curr Biol 12:1496–1501

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Ho CL, Sun D, Liem RK, Brown A (2000) Rapid movement of axonal neurofilaments interrupted by prolonged pauses. Nat Cell Biol 2:137–141

    Article  CAS  PubMed  Google Scholar 

  • Weiss P, Hiscoe HB (1948) Experiments on the mechanism of nerve growth. J Exp Zool 107:315–395

    Article  CAS  PubMed  Google Scholar 

  • Willard M (1977) The identification of two intra-axonally transported polypeptides resembling myosin in some respects in the rabbit visual system. J Cell Biol 75:1–11

    Article  CAS  PubMed  Google Scholar 

  • Willard M, Cowan WM, Vagelos PR (1974) The polypeptide composition of intra-axonally transported proteins: evidence for four transport velocities. Proc Natl Acad Sci USA 71:2183–2187

    Article  CAS  PubMed  Google Scholar 

  • Willard MB, Hulebak KL (1977) The intra-axonal transport of polypeptide H: evidence for a fifth (very slow) group of transported proteins in the retinal ganglion cells of the rabbit. Brain Res 136:289–306

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Yabe JT, Pimenta A, Shea TB (1999) Kinesin-mediated transport of neurofilament protein oligomers in growing axons. J Cell Sci 112(21):3799–3814

    CAS  PubMed  Google Scholar 

  • Yamazaki H, Nakata T, Okada Y, Hirokawa N (1995) KIF3A/B: a heterodimeric kinesin superfamily protein that works as a microtubule plus end-directed motor for membrane organelle transport. J Cell Biol 130:1387–1399

    Article  CAS  PubMed  Google Scholar 

  • Yan Y, Brown A (2005) Neurofilament polymer transport in axons. J Neurosci 25:7014–7021

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Bauer C, Strasser G, Wollman R, Julien JP, Fuchs E (1999) Integrators of the cytoskeleton that stabilize microtubules. Cell 98:229–238

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Dowling J, Yu QC, Kouklis P, Cleveland DW, Fuchs E (1996) An essential cytoskeletal linker protein connecting actin microfilaments to intermediate filaments. Cell 86:655–665

    Article  CAS  PubMed  Google Scholar 

  • Yuan A (2007) Neurofilament protein partnership, export, transport, phosphorylation and neurodegeneration. In: Arlen RK (ed) New research on neurofilament proteins. Nova Science Publishers, Inc, New York, NY, pp 53–79

    Google Scholar 

  • Yuan A, Kumar A, Peterhoff C, Duff K, Nixon RA (2008) Axonal transport rates in vivo are unaffected by tau deletion or overexpression in mice. J Neurosci 28:1682–1687

    Article  CAS  PubMed  Google Scholar 

  • Yuan A, Mills RG, Bamburg JR, Bray JJ (1997) Axonal transport and distribution of cyclophilin A in chicken neurones. Brain Res 771:203–212

    Article  CAS  PubMed  Google Scholar 

  • Yuan A, Mills RG, Bamburg JR, Bray JJ (1999) Cotransport of glyceraldehyde-3-phosphate dehydrogenase and actin in axons of chicken motoneurons. Cell Mol Neurobiol 19:733–744

    Article  CAS  PubMed  Google Scholar 

  • Yuan A, Mills RG, Chia CP, Bray JJ (2000) Tubulin and neurofilament proteins are transported differently in axons of chicken motoneurons. Cell Mol Neurobiol 20:623–632

    Article  CAS  PubMed  Google Scholar 

  • Yuan A, Rao MV, Kumar A, Julien JP, Nixon RA (2003) Neurofilament transport in vivo minimally requires hetero-oligomer formation. J Neurosci 23:9452–9458

    CAS  PubMed  Google Scholar 

  • Yuan A, Rao MV, Sasaki T, Chen Y, Kumar A, Veeranna, Liem RK, Eyer J, Peterson AC, Julien JP, Nixon RA (2006) Alpha-internexin is structurally and functionally associated with the neurofilament triplet proteins in the mature CNS. J Neurosci 26:10006–10019

    Article  CAS  PubMed  Google Scholar 

  • Yuan A, Sasaki T, Rao MV, Kumar A, Kanumuri V, Dunlop DS, Liem RK, Nixon RA (2009) Neurofilaments form a highly stable stationary cytoskeleton after reaching a critical level in axons. J Neurosci 29:11316–11329

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We gratefully acknowledge the assistance of Nicole Piorkowski in preparing the manuscript for publication. Work cited from this laboratory has been supported by Grant AG05604 from the National Institutes on Aging.

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Authors and Affiliations

  1. Nathan Kline Institute, Center for Dementia Research, New York University School of Medicine, Orangeburg, NY, 10962, USA

    Aidong Yuan

  2. Department of Psychiatry, New York University School of Medicine, New York, NY, 10016, USA

    Aidong Yuan

  3. Center for Dementia Research, Nathan S. Kline Institute for Psychiatric Research, Orangeburg, NY, 10962, USA

    Ralph A. Nixon

  4. Departments of Psychiatry and Cell Biology, New York University Langone Medical Center and School of Medicine, New York, NY, 10016, USA

    Ralph A. Nixon

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Correspondence to Aidong Yuan .

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  1. Psychiatric Research, Nathan S. Kline Institute for, 140 Old Orangeburg Road, Orangeburg, 10962, New York, USA

    Ralph A. Nixon

  2. Psychiatric Research, Nathan S. Kline Institute for, 140 Old Orangeburg Road, Orangeburg, 10962, New York, USA

    Aidong Yuan

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Yuan, A., Nixon, R.A. (2011). Axonal Transport Mechanisms in Cytoskeleton Formation and Regulation. In: Nixon, R., Yuan, A. (eds) Cytoskeleton of the Nervous System. Advances in Neurobiology, vol 3. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-6787-9_21

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