Dynein mediates retrograde neurofilament transport within axons and anterograde delivery of NFs from perikarya into axons: Regulation by multiple phosphorylation events

Cell Motility and the Cytoskeleton

Volumn 63, Issue 5, 2006, Pages 266-286

  Motil, Jennifer ^a   Chan, Walter K H ^a   Dubey, Maya ^a   Chaudhury, Pulkit ^a   Pimenta, Aurea ^b   Chylinski, Teresa M ^a   Ortiz, Daniela T ^a   Shea, Thomas B ^a  

^a University of Massachusetts Lowell   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Axonal transport; Dynein; Kinesin; Mirotubules; Neurofilaments; Phosphorylation; Vinblastine

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; DYNAMITIN; DYNEIN ADENOSINE TRIPHOSPHATASE; GREEN FLUORESCENT PROTEIN; KINESIN; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PROTEIN; UNCLASSIFIED DRUG; VINBLASTINE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MEMBRANE; CELL STRAIN; GENE OVEREXPRESSION; GENETIC TRANSFECTION; INTRACELLULAR TRANSPORT; MICROTUBULE; MOUSE; NERVE FIBER; NERVE FIBER TRANSPORT; NEURITE; NEUROFILAMENT; NONHUMAN; PERIKARYON; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; AXONAL TRANSPORT; AXONS; BIOLOGICAL TRANSPORT; DYNEIN ATPASE; FLAVONOIDS; GREEN FLUORESCENT PROTEINS; INTERMEDIATE FILAMENTS; KINESIN; MICE; MICROTUBULES; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NEURITES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; TUMOR CELLS, CULTURED; VINCRISTINE;

ANIMALIA;

EID: 33646257802     PISSN: 08861544     EISSN: 10970169     Source Type: Journal    
DOI: 10.1002/cm.20122     Document Type: Article

References (84)

1. Ackerley S, Grierson AJ, Banner S, Perkinton MS, Brownlees J, Byers HL, Ward M, Thornhill P, Hussain K, Waby JS, Anderton BH, Cooper JD, Dingwall C, Leigh PN, Shaw CE, Miller CC. 2004. p38α stress-activated protein kinase phosphorylates neurofilaments and is associated with neurofilament pathology in amyotrophic lateral sclerosis. Mol Cell Neurosci 26:354-364.
2. Ahmad FJ, Echeverri CJ, Vallee RB, Baas PW. 1998. Cytoplasmic dynein and dynactin are required for the transport of microtubules into the axon. J Cell Biol 140(2):391-401.
3. Ahmad FJ, Hughey J, Wittmann T, Hyman A, Greaser M, Baas PW. 2000. Motor proteins regulate force interactions between microtubules and microfilaments in the axon. Nat Cell Biol 2:276-280.
4. Anderton BH, Breinburg D, Downes MJ, Green PJ, Tomlinson BE, Ulrich J, Wood JN, Kahn J. 1982. Monoclonal antibodies show that neurofibrillary tangles and neurofilaments share antigenic determinants. Nature 298:84-86.
5. Baas PW. 1999. Microtubules and neuronal polarity: lessons from mitosis. Neuron 22:23-31.
6. Baas PW, Ahmad FJ. 1993. The transport properties of axonal microtubules establish their polarity orientation. J Cell Biol 120:1427-1437.
7. Baas PW, Buster DW. 2004. Slow axonal transport and the genesis of neuronal morphology. J Neurobiol 58:3-17.
8. Bajaj NP, Al-Sarraj ST, Anderson V, Kibble M, Leigh N, Miller CC. 1998. Cyclin-dependent kinase-5 is associated with lipofuscin in motor neurones in amyotrophic lateral sclerosis. Neurosci Lett 245:45-48.
9. Brady ST. 1993. Motor neurons and neurofilaments in sickness and health. Cell 73:1-3.
10. Srady ST. 2000. Neurofilaments run sprints not marathons. Nature Cell Biol 2:E43-E45.
11. Srown A. 1997. Visualization of single neurofilaments by immunofluorescence microscopy of splayed axonal cytoskeletons. Cell Motil Cytoskeleton 38:133-145.
12. Srown A. 1998. Continguous phosphorylated and non-phosphorylated domains along axonal neurofilaments. J Cell Sci 111:455-467.
13. Burkhardt JK, Echeverri CJ, Nilsson T, Vallee RB. 1997. Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J Cell Biol 139:469-484.
14. Chan WK-C, 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 117:4629-4642.
15. Chan WK-H, Yabe JT, Pimenta AF, Ortiz D, Shea TB. 2005. Neurofilaments can undergo transport and cytoskeletal incorporation in a discontinuous manner. Cell Motil Cytoskeleton 62:166-179.
16. DeWaegh SM, Lee VM, Brady ST. 1992. Local modulation of neurofilament phosphorylation, axonal caliber, and slow axonal transport by myelinating Schwann cells. Cell 68:451-463.
17. Dillman JF, III, Dabney LP, Pfister KK. 1996. Functional analysis of dynactin and cytoplasmic dynein in slow axonal transport. Proc Natl Acad Sci USA 93(1):141-144.
18. Francis F, Roy S, Brady ST, Black MM. 2005. Transport of neurofilaments in growing axons requires microtubules but not actin filaments. J Neurosci Res 79:442-50.
19. Galbraith JA, Reese TJ, Schlief ML, Gallant PE. 1999. Slow transport of umpolymerized tubulin and polymerized neurofilament in the squid giant axon. Proc Natl Acad Sci USA 96:11589-11594.
20. Glass JD, Griffin JW. 1991. Neurofilament redistribution in transected nerves: Evidence for bidirectional transport of neurofilaments. J Neurosci 11:3146-3154.
21. 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.
22. Helfand BT, Mikami A, Vallee RB, Goldman RD. 2002. A requirement for cytoplasmic dynein and dynactin in intermediate filament network assembly and organization. J Cell Biol 157:795-806.
23. Hisanaga S, Hirokawa N. 1990. Dephosphorylation-induced interactions of neurofilaments with microtubules. J Biol Chem 265:21852-21858.
24. Huffman PN, Griffin JW, Gold BG, Price DL. 1985. Slowing of neurofilament transport and the radial growth of developing nerve fibers. J Neurosci 5:2920-2909.
25. Julien J-P, Mushynski WE. 1998. Neurofilaments in health and disease. Prog Nucleic Acid Res Mol Biol 61:1-20.
26. 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.
27. Jung C, Yabe JT, Shea TB. 2000a. C-terminal phosphorylation of the heavy molecular weight neurofilament subunit is inversely correlated with neurofilament axonal transport velocity. Brain Res 856:12-19.
28. Jung C, Yabe JT, Lee S, Shea TB. 2002b. Hypophosphorylated neurofilament subunits undergo axonal transport more rapidly than more extensively phosphorylated subunits in situ. Cell Motil Cytoskeleton 47:120-129.
29. Jung C, Chylinski TM, Pimenta A, Ortiz D, Shea TB. 2004. Neurofilament transport is dependent on actin and myosin. J Neurosci 24:9486-9496.
30. Jung CS, Ortiz D, Zhu Q, Julien J-P, Shea TB. 2005. Phosphorylation of the high molecular weight neurofilament subunit regulates the association of neurofilaments with kinesin in situ. Brain Res 141:151-155.
31. Koehnle TJ, Brown A. 1999. Slow axonal transport of neurofilament protein in cultured neurons. J Cell Biol 144:447-458.
32. Komiya Y, Cooper NA, Kidman AD. 1986. The long-term effects of a single injection of beta,beta′-iminodipropionitrile on slow axonal transport in the rat. J Biochem (Tokyo) 100:1241-1246.
33. Lasek RJ, Paggi P, Katz MJ. 1992. Slow axonal transport mechanisms move neurofilaments relentlessly in mouse optic axons. J Cell Biol 117:607-616.
34. Leterrier J-F, Eyer J. 1987. Properties of highly vicous gels formed by neurofilaments in vitro. A possible consequence of specific inter-filament cross-bridging. Biochem J 245:93-101.
35. Leterrier J-F, Käs J, Hartwig J, Vegners R, Janmey P. 1996. Mechanical effects of neurofilament cross-bridges. J Biol Chem 271:15687-15694.
36. Lewis SE, Nixon RA. 1988. Multiple phosphorylated variants of the high molecular mass subunit of neurofilaments in axons of retinal cell neurons: Characterization and evidence for their differential association with stationary and moving neurofilaments. J Cell Biol 107:2689-2701.
37. Li BS, Veeranna, Gu J, Grant P, Pant HC. 1999. Activation of mitogen-activated protein kinases (Erk1 and Erk2) cascade results in phosphorylation of NF-M tail domains in transfected NIH 3T3 cells. Eur J Biochem 262:211-217.
38. Liao G, Gundersen GG. 1998. Kinesin is a candidate for cross-bridging microtubules and intermediate filaments: Selective binding of kinesin to detyrosinated tubulin and vimentin. J Biol Chem 273:9797-9803.
39. 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.
40. Mcllvain JM, Burkhardt JK, Hamm-Alvarez S, Argon Y, Sheetz MP. 1994. Regulation of kinesin activity by phosphorylation of kinesin-associated proteins. J Biol Chem 269:19176-19182.
41. Nixon RA. 1993. The regulation of neurofilament protein dynamics by phosphorylation: Clues to neurofibrillary pathology. Brain Pathol 3:29-38.
42. Nixon RA. 1998. The slow transport of cytoskeletal proteins. Curr Opin Cell Biol 10:87-92.
43. Nixon RA, Logvinenko KB. 1986. Multiple fates of newly synthesized neurofilament proteins: Evidence for a stationary neurofilament network distributed non-uniformly along axons of retinal ganglion cell neurons. J Cell Biol 102:647-659.
44. Pant HC, Veeranna. 1995. Neurofilament phosphorylation. Biochem Cell Biol 73:575-592.
45. Pfister KK. 1999. Cytoplasmic dynein and microtubule transport in the axon: The action connection. Mol Neurobiol 20:81-91.
46. Prahlad V, Helfand BT, Langford GM, Vale RD, Goldman RD. 2000. Fast transport of neurofilament protein along microtubules in squid axoplasm. J Cell Sci 113:3939-3946.
47. 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. 2002a. Myosin Va binding to neurofilaments is essential for correct myosin Va distribution and transport and neurofilament density. J Cell Biol 159:279-290.
48. Rao MV, Garcia ML, Miyazaki Y, Gotow T, Yuan A, Mattina S, Ward CM, Calcutt NA, Uchiyama Y, Nixon RA, Cleveland DW. 2002b. Gene replacement in mice reveals that the heavily phosphorylated tail of neurofilament heavy subunit does not affect axonal caliber or the transit of cargoes in slow axonal transport. J Cell Biol 158:681-693.
49. Rao MV, Campbell J, Yuan A, Kumar A, Gotow T, Uchiyama Y, Nixon RA. 2003. The neurofilament middle molecular mass subunit carboxyl-terminal tail domains is essential for the radial growth and cytoskeletal architecture of axons but not for regulating neurofilament transport rate. J Cell Biol 163:1021-1031.
50. Ratner N, Bloom GS, Brady ST. 1998. A role for cyclin-dependent kinases(s) in the modulation of fast axonal transport: Effects defined by olomoucine and the APC supressor protein. J Neurosci 18:7717-7726.
51. Roy S, Coffee P, Smith G, Liem RKH, Brady ST, Black MM. 2001. Neurofilaments are transported rapidly but intermittently in axons: Implications for slow axonal transport. J Neurosci 20:6849-6861.
52. Sanchez I, Hassinger L, Sihag RK, Cleveland DW, Mohan P, Nixon RA. 2000. Local control of neurofilament accumulation during radial growth of myelinating axons in vivo: Selective role of site-specific phosphorylation. J Cell Biol 151:1013-1024.
53. Shah JV, Cleveland DW. 2002. Slow axonal transport: Fast motors in the slow lane. Curr Opin Cell Biol 14:58-62.
54. Shah JV, Flanagan LA, Janmey PA, Leterrier J-FI. 2000. Bidirectional translocation of neurofilaments along microtubules mediated in part by dynein/dynactin. Mol Biol Cell 11:3495-3508.
55. Sharma M, Sharma P, Pant HC. 1999. CDK-5-mediated neurofilament phosphorylation in SHSY5Y human neuroblastoma cells. J Neurochem 73:79-86.
56. Shea TB. 1990. Transient increase in vimentin in axonal cytoskeletons during differentiation in NB2a/d1 cells. Dev Brain Res 521:343-346.
57. Shea TB. 1999. Selective stabilization of microtubules within the proximal region of developing axonal neurites. Brain Res Bull 48:255-261.
58. Shea TB, Beermann ML. 1994. Sequential requirements for NFs, MTs, and the MT-associated proteins MAP1B and τ in axonal neurite initiation, elongation and stabilization. Mol Cell Biol 5:863-875.
59. Shea TB, Yabe JT. 2000. Occam's razor slices through the mysteries of neurofilament axonal transport: Can it really be so simple? Traffic 1:522-523.
60. Shea TB, Sihag RK, Nixon RA. 1990. Dynamics of phosphorylation and assembly of the high molecular weight NF subunit in NB2a/d1 neuroblastoma. J Neurochem 55:1784-1792.
61. Shea TB, Fischer I, Paskevich PA, Beermann ML. 1993. The protein phosphatase inhibitor okadaic acid increases axonal NFs and neurite caliber, and decreases axonal MTs in NB2a/d1 cells. J Neurosci Res 35:507-521.
62. Shea TB, Dahl D, Nixon RA, Fischer I. 1997a. Triton-soluble phosphovariants of the heavy neurofilament subunit in developing and mature mouse central nervous system. J Neurosci Res 48:515-523.
63. Shea TB, Wheeler E, Jung C. 1997b. Aluminum inhibits neurofilament assembly, cytoskeletal incorporation and axonal transport: Dynamic nature of aluminum-induced perikaryal neurofilament accumulations as revealed by subunit turnover. Mol Chem Neuropath 32:17-39.
64. Shea TB, Flanagan L. 2001. Kinesin, dynein and neurofilament transport. Trends in Neurosciences:24:644-648.
65. Shea TB, Jung CJ, Pant HC. 2003. Does C-terminal phosphorylation regulate neurofilament transport? Re-evaluation of recent data suggests that it does. Trends Neurosci 26:397-400.
66. Strong MJ, Strong WL, Jaffe H, Traggert B, Sopper MM, Pant HC. 2001. Phosphorylation state of the native high-molecular-weight neurofilament subunit protein from cervical spinal cord in sporadic amyotrophic lateral sclerosis. J Neurochem 76:1315-1325.
67. Susalka SJ, Pfister KK. 2000. Cytoplasmic dynein subunit heterogeneity: Implications for axonal transport. J Neurocytol 29:819-829.
68. Theiss C, Napirei M, Karl Meller K. 2005. Impairment of anterograde and retrograde neuro lament transport after anti-kinesin and anti-dynein antibody microinjection in chicken dorsal root ganglia. Eur J Cell Biol 84:29-43.
69. Toyoshima I, Sugawara M, Kato K, Wada C, Hirota K, Hasegawa K, Kowa H, Sheetz MP, Masamune O. 1998a. Kinesin and cytoplasmic dynein in spinal spheroids with motor neuron disease. J Neural Sci 159:38-44.
70. Toyoshima I, Kato K, Sugawara M, Wada C, Masamune O. 1998b. Kinesin accumulation in chick spinal axonal swellings with β,β′- iminodipropionitrile (IDPN) intoxication. Neurosci Lett 249:103-106.
71. 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.
72. Veeranna, Amin ND, Ahn NG, Jaffe H, Winters CA, Grant P, Pant HC. 1998. Mitogen-activated protein kinases (Erk1, 2) phosphorylate Lys-Ser-Pro (KSP) repeats in neurofilament proteins NF-H and NF-M. J Neurosci 18:4008-4021.
73. 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.
74. Wang L, Brown A. 2001. Rapid intermittent movement of axonal neurofilaments observed by fluorescence photobleaching. Mol Biol Cell 12:3257-3267.
75. Wang L, Ho C-I, Sun D, Liem RKH, Brown A. 2000. Rapid movements of axonal neurofilaments interrupted by prolonged pauses. Nature Cell Biol 2:137-141.
76. Watson DF, Griffin JW, Fittro KP, Hoffman PN. 1989. Phosphorylation- dependent immunoreactivity of neurofilaments increases during axonal maturation and β,β′-iminodipropionitrile intoxication. J Neurochem 53:1818-1829.
77. 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.
78. Yabe JT, Pimenta A, Shea TB. 1999. Kinesin-mediated transport of neurofilament protein oligomers in growing axons. J Cell Sci 112:3799-3814.
79. Yabe JT, Chan W, Shea TB. 2000. Phospho-dependent association of neurofilament proteins with kinesin in situ. Cell Motil Cytoskeleton 45:249-265.
80. Yabe JT, Chan WK-H, Chylinski TM, Lee S, Pimenta AF, Shea TB. 2001a. The predominant form in which neurofilament subunits undergo axonal transport varies during axonal initiation, elongation and maturation. Cell Motil Cytoskeleton 4861-83.
81. Yabe JT, Chylinski T, Wang F-S, Pimenta A, Kattar SD, Linsley M-D, Chan WK-H, 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.
82. Yabe JT, Wang F-S, Chylinski T, Katchmar T, Shea TB. 2001c. Selective accumulation of the high molecular weight neurofilament subunit within the distal region of growing axonal neurites. Cell Motil Cytoskeleton 50:1-12.
83. Yuan A, Nixon RA, Rao MV. 2006. Deleting the phosphorylated tail domain of the neurofilament heavy subunit does not alter neurofilament transport rate in vivo. Neurosci Lett 393:264-268.
84. Zhang B, Tu P, Abtahian F, Trojanowski JQ, Lee VM-Y. 1997. Neurofilaments and orthograde transport are reduced in ventral root axons of transgenic mice that express human SOD1 with a G93A mutation. J Cell Biol 139:1307-1315.