Neurofilament cross-bridging competes with kinesin-dependent association of neurofilaments with microtubules

Journal of Cell Science

Volumn 122, Issue 19, 2009, Pages 3579-3586

  Kushkuley, Jacob ^a   Chan, Walter K H ^a   Lee, Sangmook ^a   Eyer, Joel ^b   Leterrier, Jean Francois ^c   Letournel, Franck ^b   Shea, Thomas B ^a  

^a University of Massachusetts Lowell   (United States)

^b ANGERS UNIVERSITY HOSPITAL   (France)

^c UNIVERSITÉ DE POITIERS   (France)

Author keywords

Axonal cytoskeleton; Axonal transport; Kinesin; Microtubules; Neurofilaments; Phosphorylation

Indexed keywords

CALCIUM ION; EGTAZIC ACID; KINESIN; NEUROFILAMENT PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; MICROTUBULE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER; NERVE FIBER TRANSPORT; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

ANIMALS; CELL LINE; CYTOSKELETON; FEMALE; INTERMEDIATE FILAMENTS; KINESIN; MALE; MICE; MICROTUBULES; NEUROFILAMENT PROTEINS; PHOSPHORYLATION; PROTEIN BINDING;

MUS;

EID: 70350371479     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.051318     Document Type: Article

References (61)

1. Ackerley, S., Thornhill, P., Grierson, A. J., Brownlees, J., Anderton, B. H., Leigh, P. N., Shaw, C. E. and Miller, C. C. (2003). Neurofilament heavy chain side arm phosphorylation regulates axonal transport of neurofilaments. J. Cell Biol. 161, 489-495.
2. Archer, D. R., Watson, D. F. and Griffin, J. W. (1994). Phosphorylation-dependent immunoreactivity of neurofilaments and the rate of slow axonal transport in the central and peripheral axons of the rat dorsal root ganglion. J. Neurochem. 62, 1119-1125.
3. Barry, D. M., Millecamps, S., Julien, J. P. and Garcia, M. L. (2007). New movements in neurofilament transport, turnover and disease. Exp. Cell Res. 313, 2110-2120.
4. Chan, W. K., Dickerson, A., Ortiz, D., Pimenta, A. F., Moran, C. M., Motil, J., Snyder, S. J., Malik, K., Pant, H. C. and Shea, T. B. (2004). Mitogen-activated protein kinase regulates neurofilament axonal transport. J. Cell Sci. 117, 4629-4642.
5. Chan, W. K., Yabe, J. T., Pimenta, A. F., Ortiz, D. and Shea, T. B. (2005). Neurofilaments can undergo axonal transport and cytoskeletal incorporation in a discontinuous manner. Cell Motil. Cytoskeleton 62, 166-179.
6. Collard, J. F., Cote, F. and Julien, J. P. (1995). Defective axonal transport in a transgenic mouse model of amyotrophic lateral sclerosis. Nature 375, 61-64.
7. Gou, J. P., Gotow, T., Janmey, P. A. and Leterrier, J. F. (1998). Regulation of neurofilament interactions in vitro by natural and synthetic polypeptides sharing Lys-Ser-Pro sequences with the heavy neurofilament subunit NF-H: neurofilament crossbridging by antiparallel sidearm overlapping. Med. Biol. Eng. Comput. 36, 371-387.
8. Hackney, D. D. (1994). Evidence for alternating head catalysis by kinesin during microtubule-stimulated ATP hydrolysis. Proc. Natl. Acad. Sci. USA 91, 6865-6869.
9. Hasaka, T. P., Myers, K. A. and Baas, P. W. (2004). Role of actin filaments in the axonal transport of microtubules. J. Neurosci. 24, 11291-11301.
10. He, Y., Francis, F., Myers, K. A., Yu, W., Black, M. M. and Baas, P. W. (2005). Role of cytoplasmic dynein in the axonal transport of microtubules and neurofilaments. J. Cell Biol. 168, 697-703.
11. Hisanaga, S., Yasugawa, S., Yamakawa, T., Miyamoto, E., Ikebe, M., Uchiyama, M. and Kishimoto, T. (1993). Dephosphorylation of microtubule-binding sites at the neurofilament-H tail domain by alkaline, acid, and protein phosphatases. J. Biochem. 113, 705-709.
12. Hoffman, P. N., Lasek, R. J., Griffin, J. W. and Price, D. L. (1983). Slowing of the axonal transport of neurofilament proteins during development. J. Neurosci. 3, 1694-1700.
13. Julien, J. P. and Mushynski, W. E. (1998). Neurofilaments in health and disease. Prog. Nucleic Acid Res. Mol. Biol. 61, 1-23.
14. Jung, C. and Shea, T. B. (1999). Regulation of neurofilament axonal transport by phosphorylation in optic axons in situ. Cell Motil. Cytoskeleton 42, 230-240.
15. Jung, C., Yabe, J. T., Lee, S. and Shea, T. B. (2000a). Hypophosphorylated neurofilament subunits undergo axonal transport more rapidly than more extensively phosphorylated subunits in situ. Cell Motil. Cytoskeleton 47, 120-129.
16. Jung, C., Yabe, J. T. and Shea, T. B. (2000b). C-terminal phosphorylation of the high molecular weight neurofilament subunit correlates with decreased neurofilament axonal transport velocity. Brain Res. 856, 12-19.
17. Jung, C., Chylinski, T. M., Pimenta, A., Ortiz, D. and Shea, T. B. (2004). Neurofilament transport is dependent on actin and myosin. J. Neurosci. 24, 9486-9496.
18. Lasek, R. J. (1986). Polymer sliding in axons. J. Cell Sci. Suppl. 5, 161-179.
19. Lasek, R. J., Paggi, P. and Katz, M. J. (1992). Slow axonal transport mechanisms move neurofilaments relentlessly in mouse optic axons. J. Cell Biol. 117, 607-616.
20. Lasek, R. J., Paggi, P. and Katz, M. J. (1993). The maximum rate of neurofilament transport in axons: a view of molecular transport mechanisms continuously engaged. Brain Res. 616, 58-64.
21. Leterrier, J. F. and 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.
22. Leterrier, J. F., Kas, J., Hartwig, J., Vegners, R. and Janmey, P. A. (1996). Mechanical effects of neurofilament cross-bridges: modulation by phosphorylation, lipids, and interactions with F-actin. J. Biol. Chem. 271, 15687-15694.
23. Letournel, F., Bocquet, A., Perrot, R., Dechaume, A., Guinut, F., Eyer, J. and Barthelaix, A. (2006). Neurofilament high molecular weight-green fluorescent protein fusion is normally expressed in neurons and transported in axons: a neuronal marker to investigate the biology of neurofilaments. Neuroscience 137, 103-111.
24. Lewis, S. E. and Nixon, R. A. (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.
25. Marszalek, J. R., Williamson, T. L., Lee, M. K., Xu, Z., Hoffman, P. N., Becher, M. W., Crawford, T. O. and Cleveland, D. W. (1996). Neurofilament subunit NF-H modulates axonal diameter by selectively slowing neurofilament transport. J. Cell Biol. 135, 711-724.
26. Moran, C. M., Donnelly, M., Ortiz, D., Pant, H. C., Mandelkow, E. M. and Shea, T. B. (2005). Cdk5 inhibits anterograde axonal transport of neurofilaments but not that of tau by inhibition of mitogen-activated protein kinase activity. Brain Res. Mol. Brain Res. 134, 338-344.
27. Motil, J., Chan, W. K., Dubey, M., Chaudhury, P., Pimenta, A., Chylinski, T. M., Ortiz, D. T. and Shea, T. B. (2006). Dynein mediates retrograde neurofilament transport within axons and anterograde delivery of NFs from perikarya into axons: regulation by multiple phosphorylation events. Cell Motil. Cytoskeleton 63, 266-286.
28. Myers, K. A., He, Y., Hasaka, T. P. and Baas, P. W. (2006). Microtubule transport in the axon: re-thinking a potential role for the actin cytoskeleton. Neuroscientist 12, 107-118.
29. Nixon, R. A. (1993). The regulation of neurofilament protein dynamics by phosphorylation: clues to neurofibrillary pathobiology. Brain Pathol. 3, 29-38.
30. Nixon, R. A. (1998). The slow axonal transport debate. Trends Cell Biol. 8, 100.
31. Nixon, R. A. and Logvinenko, K. B. (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.
32. Pant, H. C. and Veeranna. (1995). Neurofilament phosphorylation. Biochem. Cell Biol. 73, 575-592.
33. Prahlad, V., Helfand, B. T., Langford, G. M., Vale, R. D. and Goldman, R. D. (2000). Fast transport of neurofilament protein along microtubules in squid axoplasm. J. Cell Sci. 113, 3939-3946.
34. Rao, M. V., Garcia, M. L., Miyazaki, Y., Gotow, T., Yuan, A., Mattina, S., Ward, C. M., Calcutt, N. A., Uchiyama, Y., Nixon, R. A. et al. (2002). 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.
35. Rao, M. V., Campbell, J., Yuan, A., Kumar, A., Gotow, T., Uchiyama, Y. and Nixon, R. A. (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.
36. Roy, S., Coffee, P., Smith, G., Liem, R. K., Brady, S. T. and Black, M. M. (2000). Neurofilaments are transported rapidly but intermittently in axons: implications for slow axonal transport. J. Neurosci. 20, 6849-6861.
37. Sanui, H. and Pace, N. (2005). Effect of ATP, EDTA and EGTA on the simultaneous binding of NA, K, MG and Ca by rat live microsomes. J. Cell Phys. 69, 11-19.
38. Shah, J. V., Flanagan, L. A., Janmey, P. A. and Leterrier, J. F. (2000). Bidirectional translocation of neurofilaments along microtubules mediated in part by dynein/dynactin. Mol. Biol. Cell 11, 3495-3508.
39. Shea, T. B. and Chan, W. K. (2008). Regulation of neurofilament dynamics by phosphorylation. Eur. J. Neurosci. 27, 1893-1901.
40. Shea, T. B. and Flanagan, L. A. (2001). Kinesin, dynein and neurofilament transport. Trends Neurosci. 24, 644-648.
41. Shea, T. B. and Yabe, J. T. (2000). Occam's razor slices through the mysteries of axonal transport: Can it really be so simple? Traffic 1, 522-523.
42. Shea, T. B., Dahl, D. C., Nixon, R. A. and 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.
43. Shea, T. B., Jung, C. and Pant, H. C. (2003). Does neurofilament phosphorylation regulate axonal transport? Trends Neurosci. 26, 397-400.
44. Shea, T. B., Yabe, J. T., Ortiz, D., Pimenta, A., Loomis, P., Goldman, R. D., Amin, N. and Pant, H. C. (2004). Cdk5 regulates axonal transport and phosphorylation of neurofilaments in cultured neurons. J. Cell Sci. 117, 933-941.
45. Sihag, R. K., Inagaki, M., Yamaguchi, T., Shea, T. B. and Pant, H. C. (2007). Role of phosphorylation on the structural dynamics and function of types III and IV intermediate filaments. Exp. Cell Res. 313, 2098-2109.
46. Susalka, S. J. and Pfister, K. K. (2000). Cytoplasmic dynein subunit heterogeneity: implications for axonal transport. J. Neurocytol. 29, 819-829.
47. Theiss, C., Napirei, M. and 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.
48. Trivedi, N., Jung, P. and Brown, A. (2007). Neurofilaments switch between distinct mobile and stationary states during their transport along axons. J. Neurosci. 27, 507-516.
49. Veeranna Lee, J. H., Pareek, T. K., Jaffee, H., Boland, B., Vinod, K. Y., Amin, N., Kulkarni, A. B., Pant, H. C. and Nixon, R. A. (2008). Neurofilament tail phosphorylation: identity of the RT-97 phosphoepitope and regulation in neurons by cross-talk among proline-directed kinases. J. Neurochem. 107, 35-49.
50. Vugmeyster, Y., Berliner, E. and Gelles, J. (1998). Release of isolated single kinesin molecules from microtubules. Biochemistry 37, 747-757.
51. Wagner, O. I., Lifshitz, J., Janmey, P. A., Linden, M., McIntosh, T. K. and Leterrier, J. F. (2003). Mechanisms of mitochondria-neurofilament interactions. J. Neurosci. 23, 9046-9058.
52. Wang, L. and Brown, A. (2001). Rapid intermittent movement of axonal neurofilaments observed by fluorescence photobleaching. Mol. Biol. Cell 12, 3257-3267.
53. Wang, L., Ho, C. L., Sun, D., Liem, R. K. and Brown, A. (2000). Rapid movement of axonal neurofilaments interrupted by prolonged pauses. Nat. Cell Biol. 2, 137-141.
54. Xia, C. H., Roberts, E. A., Her, L. S., Liu, X., Williams, D. S., Cleveland, D. W. and Goldstein, L. S. (2003). Abnormal neurofilament transport caused by targeted disruption of neuronal kinesin heavy chain KIF5A. J. Cell Biol. 161, 55-66.
55. Yabe, J. T., Pimenta, A. and Shea, T. B. (1999). Kinesin-mediated transport of neurofilament protein oligomers in growing axons. J. Cell Sci. 112, 3799-3814.
56. Yabe, J. T., Jung, C., Chan, W. K. and Shea, T. B. (2000). Phospho-dependent association of neurofilament proteins with kinesin in situ. Cell Motil. Cytoskeleton 45, 249-262.
57. Yabe, J. T., Chylinski, T., Wang, F. S., Pimenta, A., Kattar, S. D., Linsley, M. D., Chan, W. K. and Shea, T. B. (2001a). 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.
58. Yabe, J. T., Wang, F. S., Chylinski, T., Katchmar, T. and Shea, T. B. (2001b). Selective accumulation of the high molecular weight neurofilament subunit within the distal region of growing axonal neurites. Cell Motil. Cytoskeleton 50, 1-12.
59. Yabe, J. T., Chan, W. K., Wang, F. S., Pimenta, A., Ortiz, D. D. and Shea, T. B. (2003). Regulation of the transition from vimentin to neurofilaments during neuronal differentiation. Cell Motil. Cytoskeleton 56, 193-205.
60. Yuan, A., Nixon, R. A. and Rao, M. V. (2006a). Deleting the phosphorylated tail domain of the neurofilament heavy subunit does not alter neurofilament transport rate in vivo. Neurosci. Lett. 393, 264-268.
61. Yuan, A., Rao, M. V., Sasaki, T., Chen, Y., Kumar, A., Veeranna Liem, R. K., Eyer, J., Peterson, A. C., Julien, J. P. et al. (2006b). Alpha-internexin is structurally and functionally associated with the neurofilament triplet proteins in the mature CNS. J. Neurosci. 26, 10006-10019.