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PMID: 15509735 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Neurofilament transport is dependent on actin and myosin.

Jung C, Chylinski TM, Pimenta A, Ortiz D, Shea TB

Abstract

Real-time analyses have revealed that some newly synthesized neurofilament (NF) subunits translocate into and along axonal neurites by moving along the inner plasma membrane surface, suggesting that they may translocate against the submembrane actin cortex. We therefore examined whether or not NF axonal transport was dependent on actin and myosin. Perturbation of filamentous actin in NB2a/d1 cells with cytochalasin B inhibited translocation of subunits into axonal neurites and inhibited bidirectional translocation of NF subunits within neurites. Intravitreal injection of cytochalasin B inhibited NF axonal transport in optic axons in a dose-response manner. NF subunits were coprecipitated from NB2a/d1 cells by an anti-myosin antibody, and myosin colocalized with NFs in immunofluorescent analyses. The myosin light chain kinase inhibitor ML-7 and the myosin ATPase inhibitor 2,3-butanedione-2-monoxime perturbed NF translocation within NB2a/d1 axonal neurites. These findings suggest that some NF subunits may undergo axonal transport via myosin-mediated interactions with the actin cortex.

MeSH Terms
Actins/drug effects,physiology Animals Axonal Transport/drug effects,physiology Azepines/pharmacology Cell Line, Tumor Cytochalasin B/pharmacology Diacetyl/analogs & derivatives,pharmacology Green Fluorescent Proteins Mice Myosin-Light-Chain Kinase/antagonists & inhibitors Myosins/antagonists & inhibitors,physiology Naphthalenes/pharmacology Neurites/ultrastructure Visual Pathways/drug effects,physiology,ultrastructure
Chemicals
Actins Azepines Naphthalenes ML 7 Green Fluorescent Proteins diacetylmonoxime Cytochalasin B Myosin-Light-Chain Kinase Myosins Diacetyl
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Jung Cheolwha
Center for Cellular Neurobiology and Neurodegeneration Research, Departments of Biological Sciences and Biochemistry, University of Massachusetts Lowell, Lowell, Massachusetts 01854, USA.
Chylinski Teresa M
Pimenta Aurea
Ortiz Daniela
Shea Thomas B
References (71)
71 references, click to expand
  1. Regulation of neurofilament axonal transport by phosphorylation in optic axons in situ.
    Cell Motil Cytoskeleton. 1999;42(3):230-40 PMID: 10098936
  2. Integrators of the cytoskeleton that stabilize microtubules.
    Cell. 1999 Jul 23;98(2):229-38 PMID: 10428034
  3. Myosin Va movements in normal and dilute-lethal axons provide support for a dual filament motor complex.
    J Cell Biol. 1999 Sep 6;146(5):1045-60 PMID: 10477758
  4. Kinesin-mediated transport of neurofilament protein oligomers in growing axons.
    J Cell Sci. 1999 Nov;112 ( Pt 21):3799-814 PMID: 10523515
  5. C-terminal phosphorylation of the high molecular weight neurofilament subunit correlates with decreased neurofilament axonal transport velocity.
    Brain Res. 2000 Feb 21;856(1-2):12-9 PMID: 10677606
  6. Intermediate filaments and their associates: multi-talented structural elements specifying cytoarchitecture and cytodynamics.
    Curr Opin Cell Biol. 2000 Feb;12(1):79-90 PMID: 10679360
  7. Dynein-mediated cargo transport in vivo. A switch controls travel distance.
    J Cell Biol. 2000 Mar 6;148(5):945-56 PMID: 10704445
  8. Rapid movement of axonal neurofilaments interrupted by prolonged pauses.
    Nat Cell Biol. 2000 Mar;2(3):137-41 PMID: 10707083
  9. Neurofilaments run sprints not marathons.
    Nat Cell Biol. 2000 Mar;2(3):E43-5 PMID: 10707096
  10. Phospho-dependent association of neurofilament proteins with kinesin in situ.
    Cell Motil Cytoskeleton. 2000 Apr;45(4):249-62 PMID: 10744858
  11. Intermediate filaments on the move.
    J Cell Biol. 2000 Aug 7;150(3):F101-6 PMID: 10931880
  12. Neurofilaments are transported rapidly but intermittently in axons: implications for slow axonal transport.
    J Neurosci. 2000 Sep 15;20(18):6849-61 PMID: 10995829
  13. Hypophosphorylated neurofilament subunits undergo axonal transport more rapidly than more extensively phosphorylated subunits in situ.
    Cell Motil Cytoskeleton. 2000 Oct;47(2):120-9 PMID: 11013392
  14. Bidirectional translocation of neurofilaments along microtubules mediated in part by dynein/dynactin.
    Mol Biol Cell. 2000 Oct;11(10):3495-508 PMID: 11029051
  15. Fast transport of neurofilament protein along microtubules in squid axoplasm.
    J Cell Sci. 2000 Nov;113 ( Pt 22):3939-46 PMID: 11058081
  16. The predominant form in which neurofilament subunits undergo axonal transport varies during axonal initiation, elongation, and maturation.
    Cell Motil Cytoskeleton. 2001 Jan;48(1):61-83 PMID: 11124711
  17. Occam's Razor slices through the mysteries of neurofilament axonal transport: can it really be so simple?
    Traffic. 2000 Jun;1(6):522-3 PMID: 11208138
  18. Kinesins in the nervous system.
    Cell Mol Life Sci. 1999 Oct 15;56(3-4):200-16 PMID: 11212348
  19. Temporal and spatial variations in slow axonal transport velocity along peripheral motoneuron axons.
    Neuroscience. 2001;102(1):193-200 PMID: 11226683
  20. Neurofilaments consist of distinct populations that can be distinguished by C-terminal phosphorylation, bundling, and axonal transport rate in growing axonal neurites.
    J Neurosci. 2001 Apr 1;21(7):2195-205 PMID: 11264295
  21. Axonal protein synthesis and transport.
    J Neurocytol. 2000 Nov-Dec;29(11-12):779-82 PMID: 11466469
  22. Cytoplasmic dynein subunit heterogeneity: implications for axonal transport.
    J Neurocytol. 2000 Nov-Dec;29(11-12):819-29 PMID: 11466473
  23. Axonal myosins.
    J Neurocytol. 2000 Nov-Dec;29(11-12):831-41 PMID: 11466474
  24. Microtubule motors, phosphorylation and axonal transport of neurofilaments.
    J Neurocytol. 2000 Nov-Dec;29(11-12):873-87 PMID: 11466476
  25. Axonal transport of tubulin and actin.
    J Neurocytol. 2000 Nov-Dec;29(11-12):889-911 PMID: 11466477
  26. Kinesin, dynein and neurofilament transport.
    Trends Neurosci. 2001 Nov;24(11):644-8 PMID: 11672808
  27. Slow axonal transport: fast motors in the slow lane.
    Curr Opin Cell Biol. 2002 Feb;14(1):58-62 PMID: 11792545
  28. Myosin Va binding to neurofilaments is essential for correct myosin Va distribution and transport and neurofilament density.
    J Cell Biol. 2002 Oct 28;159(2):279-90 PMID: 12403814
  29. Abnormal neurofilament transport caused by targeted disruption of neuronal kinesin heavy chain KIF5A.
    J Cell Biol. 2003 Apr 14;161(1):55-66 PMID: 12682084
  30. Rapid transport of neural intermediate filament protein.
    J Cell Sci. 2003 Jun 1;116(Pt 11):2345-59 PMID: 12711702
  31. Neurofilament heavy chain side arm phosphorylation regulates axonal transport of neurofilaments.
    J Cell Biol. 2003 May 12;161(3):489-95 PMID: 12743103
  32. Slow axonal transport.
    Curr Opin Cell Biol. 1992 Feb;4(1):8-14 PMID: 1373067
  33. Cytoskeletal dynamics and transport in growth cone motility and axon guidance.
    Neuron. 2003 Oct 9;40(2):209-27 PMID: 14556705
  34. The dynamic and motile properties of intermediate filaments.
    Annu Rev Cell Dev Biol. 2003;19:445-67 PMID: 14570577
  35. Myosin function in nervous and sensory systems.
    J Neurobiol. 2004 Jan;58(1):118-30 PMID: 14598375
  36. Myosin-dependent transport in neurons.
    J Neurobiol. 2004 Feb 5;58(2):164-74 PMID: 14704949
  37. Neurofilament subunits undergo more rapid translocation within retinas than in optic axons.
    Brain Res Mol Brain Res. 2004 Mar 30;122(2):188-92 PMID: 15010211
  38. Chromophore-assisted laser inactivation (CALI): probing protein function in situ with a high degree of spatial and temporal resolution.
    Trends Cell Biol. 1996 Nov;6(11):442-5 PMID: 15157516
  39. Mitogen-activated protein kinase regulates neurofilament axonal transport.
    J Cell Sci. 2004 Sep 15;117(Pt 20):4629-42 PMID: 15331628
  40. Actin-dependent organelle movement in squid axoplasm.
    Nature. 1992 Apr 23;356(6371):722-5 PMID: 1570018
  41. Interaction domains of neurofilament light chain and brain spectrin.
    Biochem J. 1991 Apr 15;275 ( Pt 2):521-7 PMID: 1902666
  42. Neurofilament redistribution in transected nerves: evidence for bidirectional transport of neurofilaments.
    J Neurosci. 1991 Oct;11(10):3146-54 PMID: 1941078
  43. Dynamics of phosphorylation and assembly of the high molecular weight neurofilament subunit in NB2a/d1 neuroblastoma.
    J Neurochem. 1990 Nov;55(5):1784-92 PMID: 2213024
  44. Neuritogenesis in mouse NB2a/d1 neuroblastoma cells: triggering by calcium influx and involvement of actin and tubulin dynamics.
    Cell Biol Int Rep. 1990 Nov;14(11):967-79 PMID: 2279271
  45. Organization of cytoskeletal elements and organelles preceding growth cone emergence from an identified neuron in situ.
    J Cell Biol. 1989 May;108(5):1737-49 PMID: 2654140
  46. 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. 1988 Aug;8(8):2769-79 PMID: 3045269
  47. Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite.
    Proc Natl Acad Sci U S A. 1988 Nov;85(21):8335-9 PMID: 3054884
  48. 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. 1986 Oct 5;261(28):13026-30 PMID: 3093477
  49. Binding of brain spectrin to the 70-kDa neurofilament subunit protein.
    Eur J Biochem. 1987 Dec 15;169(3):651-7 PMID: 3121319
  50. Neurofilament triplet proteins of NB2a/d1 neuroblastoma: posttranslational modification and incorporation into the cytoskeleton during differentiation.
    Brain Res. 1988 Sep 1;471(1):97-109 PMID: 3146407
  51. Polarity orientation of axonal microtubules.
    J Cell Biol. 1981 Dec;91(3 Pt 1):661-5 PMID: 6173385
  52. Myosin is involved in postmitotic cell spreading.
    J Cell Biol. 1995 Oct;131(1):179-89 PMID: 7559774
  53. The maximum rate of neurofilament transport in axons: a view of molecular transport mechanisms continuously engaged.
    Brain Res. 1993 Jul 9;616(1-2):58-64 PMID: 7689412
  54. Respective roles of neurofilaments, microtubules, MAP1B, and tau in neurite outgrowth and stabilization.
    Mol Biol Cell. 1994 Aug;5(8):863-75 PMID: 7803854
  55. 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. 1993 Oct 25;268(30):22695-702 PMID: 8226779
  56. Axonal transport and the cytoskeleton.
    Curr Opin Neurobiol. 1993 Oct;3(5):724-31 PMID: 8260821
  57. Redistribution of cytoskeletal proteins in mammalian axons disconnected from their cell bodies.
    J Neurosci. 1993 Oct;13(10):4354-60 PMID: 8410191
  58. Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons.
    J Cell Biol. 1995 Dec;131(5):1315-26 PMID: 8522592
  59. Cytoplasmic dynein is associated with slow axonal transport.
    Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):141-4 PMID: 8552592
  60. Targeting of motor proteins.
    Science. 1996 Mar 15;271(5255):1539-44 PMID: 8599110
  61. Functional analysis of dynactin and cytoplasmic dynein in slow axonal transport.
    J Neurosci. 1996 Nov 1;16(21):6742-52 PMID: 8824315
  62. Triton-soluble phosphovariants of the heavy neurofilament subunit in developing and mature mouse central nervous system.
    J Neurosci Res. 1997 Jun 15;48(6):515-23 PMID: 9210521
  63. 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. 1997 Oct 20;139(2):417-34 PMID: 9334345
  64. Kinesin and dynein superfamily proteins and the mechanism of organelle transport.
    Science. 1998 Jan 23;279(5350):519-26 PMID: 9438838
  65. Cytoplasmic dynein and dynactin are required for the transport of microtubules into the axon.
    J Cell Biol. 1998 Jan 26;140(2):391-401 PMID: 9442114
  66. The design plan of kinesin motors.
    Annu Rev Cell Dev Biol. 1997;13:745-77 PMID: 9442886
  67. Kinesin is a candidate for cross-bridging microtubules and intermediate filaments. Selective binding of kinesin to detyrosinated tubulin and vimentin.
    J Biol Chem. 1998 Apr 17;273(16):9797-803 PMID: 9545318
  68. Neurofilament subunits can undergo axonal transport without incorporation into Triton-insoluble structures.
    Cell Motil Cytoskeleton. 1998;40(1):44-58 PMID: 9605971
  69. Dynamic behavior and organization of cytoskeletal proteins in neurons: reconciling old and new findings.
    Bioessays. 1998 Oct;20(10):798-807 PMID: 9819567
  70. Direct interaction of microtubule- and actin-based transport motors.
    Nature. 1999 Jan 21;397(6716):267-70 PMID: 9930703
  71. Slow axonal transport of neurofilament protein in cultured neurons.
    J Cell Biol. 1999 Feb 8;144(3):447-58 PMID: 9971740
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2004-10-27
Pages
9486-96
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6730143
Subset
IM
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