Neurofilament transport is dependent on actin and myosin

Journal of Neuroscience

Volumn 24, Issue 43, 2004, Pages 9486-9496

  Jung, Cheolwha ^a   Chylinski, Teresa M ^a   Pimenta, Aurea ^a   Ortiz, Daniela ^a   Shea, Thomas B ^a  

^a UNIVERSITY OF MASSACHUSETTS LOWELL   (United States)

Author keywords

Actin; Axonal transport (axoplasmic transport); Cytoskeleton; Motor; Myosin; Neurofilament

Indexed keywords

1 (5 IODO 1 NAPHTHALENESULFONYL)HEXAHYDRO 1H 1,4 DIAZEPINE; ACTIN; CYTOCHALASIN B; DIACETYL OXIME; ENZYME INHIBITOR; MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN ANTIBODY; MYOSIN LIGHT CHAIN KINASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNOFLUORESCENCE; MOUSE; NERVE FIBER TRANSPORT; NEURITE; NEUROFILAMENT; NONHUMAN; OPTIC NERVE; PRECIPITATION; PRIORITY JOURNAL;

ACTINS; ANIMALS; AXONAL TRANSPORT; AZEPINES; CELL LINE, TUMOR; CYTOCHALASIN B; DIACETYL; GREEN FLUORESCENT PROTEINS; MICE; MYOSIN-LIGHT-CHAIN KINASE; MYOSINS; NAPHTHALENES; NEURITES; VISUAL PATHWAYS;

EID: 7444262412     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1665-04.2004     Document Type: Article

References (72)

1. 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.
2. Ahmad FJ, Echeverri RB, Vallee RB, Baas PW (1998) Cytoplasmic dynein and dynactin are required for the transport of microtubules into the axon. J Cell Biol 140:391-401.
3. Baas PW, Deitch JS, Black MM, Banker GA (1988) Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and non-uniformity in the dendrite. Proc Natl Acad Sci USA 85:8335-8339.
4. Brady ST (2000) Neurofilaments run sprints not marathons. Nat Cell Biol 2:E43-E45.
5. Bridgman PC (1999) Myosin Va movements in normal and dilute-lethal axons provide support for a dual filament motor complex. J Cell Biol 146:1045-1060.
6. Bridgman PC (2004) Myosin-dependent transport in neurons. J Neurobiol 58:164-174.
7. Bridgman PC, Elkin LL (2000) Axonal myosins. J Neurocytol 29:831-841.
8. Brown ME, Bridgman PC (2004) Myosin function in nervous and sensory systems. J Neurobiol 58:118-130.
9. Chan WK, Dickerson A, Otriz D, Pimenta A, Moran C, Malik K, Motil J, Snyder S, Pant HC, Shea TB (2004) Mitogen-activated protein kinase regulates neurofilament axonal transport. J Cell Sci, in press.
10. Chou YH, Goldman RD (2000) Intermediate filaments on the move. J Cell Biol 150:F101-F106.
11. Cramer LP, Mitchison TJ (1995) Myosin is involved in the post-mitotic cell spreading. J Cell Biol 131:179-189.
12. Dent EW, Gertler FB (2003) Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40:209-227.
13. Dillman JF, Dabney LP, Pfister KK (1996a) Cytoplasmic dynein is associated with slow axonal transport. Proc Natl Acad Sci USA 93:141-144.
14. Dillman JF, 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.
15. Frappier T, Regnouf F, Pradel L-A (1987) Binding of brain spectrin to the 70 kDa neurofilament subunit protein. Eur J Biochem 169:651-657.
16. Frappier T, Stetzkowski-Marden F, Pradel L-A (1991) Interaction domains of neurofilament light chain and brain spectrin. Biochem J 275:521-527.
17. Galbraith JA, Gallant PE (2000) Axonal transport of tubulin and actin. J Neurocytol 29:889-911.
18. Gallant PE (2000) Axonal protein synthesis and transport. J Neurocytol 29:779-782.
19. Glass JD, Griffin JW (1991) Neurofilament redistribution in transected nerves: evidence for bidirectional transport of neurofilaments. J Neurosci 11:3146-3154.
20. Gross SP, Weite MA, Block SM, Wieschaus EF (2000) Dynein-mediated cargo transport in vivo: a switch controls travel distance. J Cell Biol 148:945-955.
21. Heidemann SR, Landers JM, Hamborg MA (1981) Polarity orientation of axonal microtubules. J Cell Biol 91:661-665.
22. Helfand BT, Chang L, Goldman RD (2003a) The dynamic and motile properties of intermediate filaments. Annu Rev Cell Dev Biol 19:445-467.
23. Helfand BT, Loomis P, Yoon M, Goldman RD (2003b) Rapid transport of neural intermediate filament protein. J Cell Sci 116:2345-2359.
24. Herrmann H, Aebi U (2000) Intermediate filaments and their associates: multitalented structural elements specifying cytoarchitecture and cytodynamics. Curr Opin Cell Biol 12:79-90.
25. Hirokawa N (1993) Axonal transport and the cytoskeleton. Curr Opin Neurobiol 3:724-731.
26. Hirokawa N (1998) Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279:519-526.
27. Hirokawa N, Hisanaga S, Shiomura Y (1988) MAP2 is a component of crossbridges between microtubules and neurofilaments in the neuronal cytoskeleton: quick-freeze, deep-etch immunoelectron microscopy, and reconstitution studies. J Neurosci 8:2769-2779.
28. Huang JD, Brady ST, Richards BW, Stenoien D, Resau JH, Copeland NG, Jenkins NA (1999) Direct interaction of microtubule-and actin-based transport motors. Nature 397:267-270.
29. Jung C, Shea TB (1999) Regulation of neurofilament axonal transport by phosphorylation in optic axons in situ. Cell Motil Cytoskeleton 42:230-240.
30. Jung C, Yabe J, Wang F-S, Shea TB (1998) Neurofilaments are present within axonal neurites before incorporation into Triton-insoluble structures. Cell Motil Cytoskeleton 40:44-58.
31. Jung C, Yabe JT, Shea TB (2000a) C-terminal phosphorylation of the high molecular weight neurofilament subunit correlates with decreased neurofilament axonal transport velocity. Brain Res 856:12-19.
32. Jung C, Yabe JT, Lee S, Shea TB (2000b) Hypophosphorylated neurofilament subunits undergo axonal transport faster than extensively phosphorylated subunits. Cell Motil Cytoskeleton 47:120-129.
33. Jung CJ, Shea TB (2004) Neurofilament subunits undergo more rapid translocation within retinas than in optic axons. Mol Brain Res 122:188-192.
34. Koehnle TJ, Brown A (1999) Slow axonal transport of neurofilament protein in cultured neurons. J Cell Biol 144:447-458.
35. Kuznetsov SA, Langford GM, Weiss DG (1992) Actin-dependant organelle movement in squid axoplasm. Nature 356:722-725.
36. Lasek RJ, Paggi P, Katz MJ (1993) The maximum rate of neurofilament transport in axons: a view of molecular transport mechanisms continuously engaged. Brain Res 616:58-64.
37. Lefcort F, Bentley D (1989) Organization of cytoskeletal elements and organelles preceding growth cone emergence from an identified neuron in situ. J Cell Biol 108:1737-1749.
38. Liao G, Gundersen GG (1998) Kinesin is a candidate for cross-bridging microtubules and intermediate filaments. J Biol Chem 273:9797-9803.
39. Martin MA, Hurd DD, Saxton WM (1999) Kinesins in the nervous system. Cell Mol Life Sci 56:200-216.
40. Miyasaka H, Okabe S, Ishiguro K, Uchida T, Hirokawa N (1993) Interaction of the tail domain of high molecular weight subunits of neurofilaments with the COOH-terminal region of tubulin and its regulation by tau protein kinase II. J Biol Chem 268:22695-22702.
41. 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. J Biol Chem 261:13026-13030.
42. Morris RL, Hollenbeck PJ (1995) Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons. J Cell Biol 131:1315-1326.
43. Nixon RA (1992) Slow axonal transport. Curr Opin Cell Biol 4:8-14.
44. Nixon RA (1998) Dynamic behavior and organization of cytoskeletal proteins in neurons: reconciling old and new findings. BioEssays 20:798-807.
45. Ochs S (1975) A unitary concept of the axoplasmic transport based on the transport filament hypothesis. In: Recent advances in myology (Bradley WG, ed), pp 189-194. Amsterdam: Excerpta Medica.
46. Prahlad V, Helfand BT, Langford GM, Vale RD, Goldman RD (2000) Fast transport of neurofilament protein along microtubules. J Cell Sci 113:3939-3946.
47. Rao MV, Engle LJ, Mohan PS, Yuan A, Qiu D, Cataldo AM, Hassinger L, Jacobsen S, Lee VM-Y, Andreadis A, Julien J-P, 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 159:279-289.
48. Roy S, Coffee P, Smith G, Liem RKH, Brady ST, Black MM (2000) Neurofilaments are transported rapidly but intermittently in axons: implications for slow axonal transport. J Neurosci 20:6849-6861.
49. Shah JV, Cleveland DW (2002) Slow axonal transport: fast motors in the slow lane. Curr Opin Cell Biol 14:58-62.
50. Shah JV, Flanagan LA, Janmey PA, Leterrier JF (2000) Bidirectional translocation of neurofilaments along microtubules is mediated in part by dynein/dynactin. Mol Biol Cell 11:3495-3508.
51. Shea TB (1990) Neuritogenesis in mouse NB2a/d1 neuroblastoma cells: triggering by calcium influx and involvement of actin and tubulin dynamics. Cell Biol Int Rep 14:967-979.
52. Shea TB (2000) Microtubule motors, phosphorylation, and axonal transport of neurofilaments. J Neurocytol 29:873-887.
53. Shea TB, Beermann ML (1994) Sequential requirements for neurofilaments, microtubules, and the microtubule-associated proteins MAP1B and tau in axonal neurite initiation, elongation, and stabilization. Mol Cell Biol 5:863-875.
54. Shea TB, Flanagan L (2001) Kinesin, dynein, and neurofilament transport. Trends Neurosci 24:644-648.
55. Shea TB, Yabe J (2000) Occam's razor slices through the mysteries of neurofilament axonal transport: can it really be so simple? Traffic 1:522-523.
56. Shea TB, Sihag RK, Nixon RA (1988) Neurofilament triplet proteins of NB2a/d1 neuroblastoma: posttranslational modification and incorporation into the cytoskeleton during differentiation. Dev Brain Res 50:142-146.
57. Shea TB, Sihag RK, Nixon RA (1990) Dynamics of phosphorylation and assembly of the high molecular weight neurofilament protein subunit in NB2a/d1 neuroblastoma. J Neurochem 55:1784-1792.
58. Shea TB, Dahl DC, Nixon RA, Fischer I (1997) Triton-soluble phosphovariants of the heavy neurofilament subunit in developing and mature mouse central nervous system. J Neurosci Res 48:515-523.
59. Susalia SJ, Pfister KK (2000) Cytoplasmic dynein subunit heterogeneity: implications for axonal transport. J Neurocytol 29:819-829.
60. Vale R, Fletterick R (1997) The design plan of kinesin motors. Annu Rev Cell Dev Biol 13:745-777.
61. Vallee RB, Sheetz MP (1996) Targeting of motor proteins. Science 271:1539-1544.
62. Wang FS, Jay DG (1996) Chromophore-assisted laser inactivation (CALI): probing protein function in situ with a high degree of spatial and temporal resolution. Trends Cell Biol 6:442-445.
63. Wang L, Ho CL, Sun DM, Liem RKH, Brown A (2000) Rapid movement of axonal neurofilaments interrupted by prolonged pauses. Nat Cell Biol 2:137-141.
64. Waterman-Storer CM, Salmon ED (1997) Actomyosin-based retrograde flow of microtubules in the lamella of migrating epithelial cells influences microtubule dynamic instability and turnover and is associated with microtubule breakage and treadmilling. J Cell Biol 139:417-434.
65. Watson DF, Glass JD, Griffin JW (1993) Redistribution of cytoskeletal proteins in mammalian axons disconnected from their cell bodies. J Neurosci 13:4354-4360.
66. 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.
67. Xu Z, Tung VW (2001) Temporal and spatial variations in slow axonal transport velocity along peripheral motoneuron axons. Neuroscience 102:193-200.
68. Yabe JT, Pimenta A, Shea TB (1999) Kinesin-mediated transport of NF protein oligomers in growing axons. J Cell Sci 112:3799-3814.
69. Yabe JT, Jung C, Chan WK, Shea TB (2000) Phospho-dependent association of neurofilament proteins with kinesin in situ. Cell Motil Cytoskeleton 45:249-262.
70. Yabe JT, Chan WK, Chylinski TM, Lee S, Pimenta AF, Shea TB (2001a) The predominant form in which neurofilaments subunits undergo axonal transport varies during axonal initiation, elongation, and maturation. Cell Motil Cytoskeleton 48:61-83.
71. Yabe JT, Chylinski TM, Wang F-S, Pimenta AF, Kattar SD, Linsley M-D, Chan WK, Shea TB (2001b) Neurofilaments consist of distinct populations that can be distinguished by C-terminal phosphorylation, bundling, and axonal transport rate in growing axonal neurites. J Neurosci 21:2195-2205.
72. Yang Y, Bauer C, Strasser G, Wollman R, Julien JP, Fuchs E (1999) Integrators of the cytoskeleton that stabilize microtubules. Cell 98:229-238.