Cytoskeletal requirements in axonal transport of slow component-b

Journal of Neuroscience

Volumn 28, Issue 20, 2008, Pages 5248-5256

  Roy, Subhojit ^a,c   Winton, Matthew J ^a   Black, Mark M ^b   Trojanowski, John Q ^a   Lee, Virginia M Y ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b TEMPLE UNIVERSITY HOSPITAL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

synuclein; Axonal transport; Protein complexes; Slow component b; Slow transport; Synapsin I

Indexed keywords

ALPHA SYNUCLEIN; F ACTIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; SYNAPSIN I; FUSED HETEROCYCLIC RINGS; GLYCERALDEHYDE 3 PHOSPHATE; LATRUNCULIN A; MOLECULAR MOTOR; SYNAPSIN; THIAZOLIDINE DERIVATIVE;

ACTIN FILAMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; HIPPOCAMPUS; MICROTUBULE; MOUSE; NERVE FIBER TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; ANIMAL; BRAIN; C57BL MOUSE; CELL CULTURE; MACROMOLECULE; METABOLISM; MICROFILAMENT; NERVE FIBER; PHYSIOLOGY; TIME; ULTRASTRUCTURE;

ALPHA-SYNUCLEIN; ANIMALS; AXONAL TRANSPORT; AXONS; BICYCLO COMPOUNDS, HETEROCYCLIC; BRAIN; CELLS, CULTURED; CYTOSKELETON; GLYCERALDEHYDE 3-PHOSPHATE; MACROMOLECULAR SUBSTANCES; MICE; MICE, INBRED C57BL; MICROFILAMENTS; MICROTUBULES; MOLECULAR MOTOR PROTEINS; SYNAPSINS; THIAZOLIDINES; TIME FACTORS;

EID: 45549099576     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0309-08.2008     Document Type: Article

References (51)

1. Allison DW, Gelfand VI, Spector I, Craig AM (1998) Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors. J Neurosci 18:2423-2436.
2. Bahler M, Greengard P (1987) Synapsin I bundles F-actin in a phosphorylation-dependent manner. Nature 326:704-707.
3. Baines AJ, Bennett V (1985) Synapsin I is a spectrin-binding protein immunologically related to erythrocyte protein 4.1. Nature 315:410-413.
4. Baitinger C, Willard M (1987) Axonal transport of synapsin I-like proteins in rabbit retinal ganglion cells. J Neurosci 7:3723-3735.
5. 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.
6. Black MM, Lasek RJ (1980) Slow components of axonal transport: two cytoskeletal networks. J Cell Biol 86:616-623.
7. Black MM, Chestnut MH, Pleasure IT, Keen JH (1991) Stable clathrin: uncoating protein (hsc70) complexes in intact neurons and their axonal transport. J Neurosci 11:1163-1172.
8. 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.
9. Brady ST, Tytell M, Heriot K, Lasek RJ (1981) Axonal transport of calmodulin: a physiologic approach to identification of long-term associations between proteins. J Cell Biol 89:607-614.
10. Bray JJ, Fernyhough P, Bamburg JR, Bray D (1992) Actin depolymerizing factor is a component of slow axonal transport. J Neurochem 58:2081-2087.
11. Cueille N, Blanc CT, Riederer IM, Riederer BM (2007) Microtubule- associated protein 1B binds glyceraldehyde-3-phosphate dehydrogenase. J Proteome Res 6:2640-2647.
12. Dillman III JF, Dabney LP, Karki S, Paschal BM, Holzbaur EL, Pfister KK (1996) Functional analysis of dynactin and cytoplasmic dynein in slow axonal transport. J Neurosci 16:6742-6752.
13. 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.
14. Fortin DL, Troyer MD, Nakamura K, Kubo S, Anthony MD, Edwards RH (2004) Lipid rafts mediate the synaptic localization of α-synuclein. J Neurosci 24:6715-6723.
15. 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.
16. Garner JA, Lasek RJ (1981) Clathrin is axonally transported as part of slow component b: the microfilament complex. J Cell Biol 88:172-178.
17. Garner JA, Lasek RJ (1982) Cohesive axonal transport of the slow component b complex of polypeptides. J Neurosci 2:1824-1835.
18. Giasson BI, Jakes R, Goedert M, Duda JE, Leight S, Trojanowski JQ, Lee VMY (2000) A panel of epitope-specific antibodies detects protein domains distributed throughout human α-synuclein in Lewy bodies of Parkinson's disease. J Neurosci Res 59:528-533.
19. Heriot K, Gambetti P, Lasek RJ (1985) Proteins transported in slow components a and b of axonal transport are distributed differently in the transverse plane of the axon. J Cell Biol 100:1167-1172.
20. Horiuchi D, Barkus RV, Pilling AD, Gassman A, Saxton WM (2005) APLIP1, a kinesin binding JIP-1/JNK scaffold protein, influences the axonal transport of both vesicles and mitochondria in Drosophila. Curr Biol 15:2137-2141.
21. Kaether C, Skehel P, Dotti CG (2000) Axonal membrane proteins are transported in distinct carriers: a two-color video microscopy study in cultured hippocampal neurons. Mol Biol Cell 11:1213-1224.
22. Koo EH, Sisodia SS, Archer DR, Martin LJ, Weidemann A, Beyreuther K, Fischer P, Masters CL, Price DL (1990) Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport. Proc Natl Acad Sci USA 87:1561-1565.
23. Lasek RJ, Garner JA, Brady ST (1984) Axonal transport of the cytoplasmic matrix. J Cell Biol 99:212s-221s.
24. Lee KD, Hollenbeck PJ (1995) Phosphorylation of kinesin in vivo correlates with organelle association and neurite outgrowth. J Biol Chem 270:5600-5605.
25. Levine J, Willard M (1981) Fodrin: axonally transported polypeptides associated with the internal periphery of many cells. J Cell Biol 90:631-642.
26. Li W, Hoffman PN, Stirling W, Price DL, Lee MK (2004) Axonal transport of human alpha-synuclein slows with aging but is not affected by familial Parkinson's disease-linked mutations. J Neurochem 88:401-410.
27. 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.
28. 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.
29. 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.
30. Minaschek G, Groschel-Stewart U, Blum S, Bereiter-Hahn J (1992) Microcompartmentation of glycolytic enzymes in cultured cells. Eur J Cell Biol 58:418-428.
31. Morfini G, Szebenyi G, Elluru R, Ratner N, Brady ST (2002) Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin-based motility. EMBO J 21:281-293.
32. Morfini G, Szebenyi G, Brown H, Pant HC, Pigino G, DeBoer S, Beffert U, Brady ST (2004) A novel CDK5-dependent pathway for regulating GSK3 activity and kinesin-driven motility in neurons. EMBO J 23:2235-2245.
33. Moss ML, Palmer RE, Kuzmic P, Dunlap BE, Henzel W, Kofron JL, Mellon WS, Royer CA, Rich DH (1992) Identification of actin and HSP 70 as cyclosporin A binding proteins by photoaffinity labeling and fluorescence displacement assays. J Biol Chem 267:22054-22059.
34. Nicol S, Rahman D, Baines AJ (1997) Ca2+-dependent interaction with calmodulin is conserved in the synapsin family: identification of a high-affinity site. Biochemistry 36:11487-11495.
35. Nixon RA, Fischer I, Lewis SE (1990) Synthesis, axonal transport, and turnover of the high molecular weight microtubule-associated protein MAP 1A in mouse retinal ganglion cells: tubulin and MAP 1A display distinct transport kinetics. J Cell Biol 110:437-448.
36. 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.
37. Roy S, Zhang B, Lee VM-Y, Trojanowski JQ (2005) Axonal transport defects: a common theme in neurodegenerative diseases. Acta Neuropathol (Berl) 109:5-13.
38. Roy S, Winton MJ, Black MM, Trojanowski JQ, Lee VM-Y (2007) Rapid and intermittent cotransport of slow component-b proteins. J Neurosci 27:3131-3138.
39. Sankaranarayanan S, Atluri PP, Ryan TA (2003) Actin has a molecular scaffolding, not propulsive, role in presynaptic function. Nat Neurosci 6:127-135.
40. Slaughter T, Wang J, Black MM (1997) Microtubule transport from the cell body into the axons of growing neurons. J Neurosci 17:5807-5819.
41. Sytnyk V, Leshchyns'ka I, Dityatev A, Schachner M (2004) Trans-Golgi network delivery of synaptic proteins in synaptogenesis. J Cell Sci 117:381-388.
42. 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.
43. Tytell M, Black MM, Garner JA, Lasek RJ (1981) Axonal transport: each major rate component reflects the movement of distinct macromolecular complexes. Science 214:179-181.
44. Utton MA, Noble WJ, Hill JE, Anderton BH, Hanger DP (2005) Molecular motors implicated in the axonal transport of tau and alpha-synuclein. J Cell Sci 118:4645-4654.
45. Wang L, Brown A (2002) Rapid movement of microtubules in axons. Curr Biol 12:1496-1501.
46. 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.
47. 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.
48. 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.
49. Willard M, Wiseman M, Levine J, Skene P (1979) Axonal transport of actin in rabbit retinal ganglion cells. J Cell Biol 81:581-591.
50. Woods WS, Boettcher JM, Zhou DH, Kloepper KD, Hartman KL, Ladror DT, Qi Z, Rienstra CM, George JM (2007) Conformation-specific binding of α-synuclein to novel protein partners detected by phage display and NMR spectroscopy. J Biol Chem 282:34555-34567.
51. 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.