Neurofilament subunit NF-H modulates axonal diameter by selectively slowing neurofilament transport

Journal of Cell Biology

Volumn 135, Issue 3, 1996, Pages 711-724

  Marszalek, Joseph R ^a   Williamson, Toni L ^a   Lee, Michael K ^b   Xu, Zuoshang ^c   Hoffman, Paul N ^b   Becher, Mark W ^b   Crawford, Thomas O ^b   Cleveland, Don W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; NEUROFILAMENT PROTEIN; PROTEIN SUBUNIT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; FEMALE; GENE EXPRESSION; MALE; MOTOR NEURON DISEASE; MYELINATION; NERVE CELL DEGENERATION; NERVE FIBER GROWTH; NERVE FIBER TRANSPORT; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE;

ANIMALS; AXONAL TRANSPORT; AXONS; BIOLOGICAL TRANSPORT; CELL DEATH; GANGLIA, SPINAL; GENE DOSAGE; GENE EXPRESSION; INTERMEDIATE FILAMENTS; MICE; MICE, TRANSGENIC; MOTOR NEURONS; MUSCLE, SKELETAL; MYELIN SHEATH; NERVE DEGENERATION; NEUROFILAMENT PROTEINS; NEURONS, AFFERENT; RNA, MESSENGER; SCIATIC NERVE; SPINAL CORD; TRANSGENES; TUBULIN;

ANIMALIA; MURINAE; MUS MUSCULUS;

EID: 0029807823     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.135.3.711     Document Type: Article

References (54)

1. Arbuthnott, E.R., I.A. Boyd, and K.U. Kalu. 1980. Ultrastructural dimensions of myelinated peripheral nerve fibres in the cat and their relation to conduction velocity. J. Physiol. 308:125-137.
2. Beckman, J.S., M. Carson, C.D. Smith, and W.H. Koppenol. 1993. ALS, SOD and peroxynitrite. Nature (Lond.). 364:584.
3. Brown, A., G. Bernier, M. Mathieu, J. Rossant, and R. Kothary. 1995. The mouse dystonia musculorum gene is a neural isoform of bullous pemphigoid antigen 1. Nat. Genet. 10:301-306.
4. Carpenter, S. 1968. Proximal axonal enlargement in motor neuron disease. Neurology. 18:841-851.
5. Ching, G.Y., and R.K. Liem. 1993. Assembly of type IV neuronal intermediate filaments in nonneuronal cells in the absence of preexisting cytoplasmic intermediate filaments. J. Cell Biol. 122:1323-1335.
6. Chou, S.M., and A.V. Fakadej. 1971. Ultrastructure of chromatolytic motor neurons and anterior spinal roots in a case of Werdnig-Hoffman disease. J. Neuropathol. Exp. Neurol. 30:42-55.
7. Clark, A.W., J.W. Griffin, and D.L. Price. 1980. The axonal pathology in chronic IDPN intoxication. J. Neuropathol. Exp. Neurol. 39:42-55.
8. Cleveland, D.W., M.J. Monteiro, P.C. Wong, S.R. Gill, J.D. Gearhart, and P.N. Hoffman. 1991. Involvement of neurofilaments in the radial growth of axons. J. Cell Sci. Suppl. 15:85-95.
9. Collard, J.F., F. Cote, and J.P. Julien. 1995. Defective axonal transport in a transgenic mouse model of amyotrophic lateral sclerosis. Nature (Lond.). 375:61-64.
10. Cote, F., J.F. Collard, and J.P. Julien. 1993. Progressive neuronopathy in transgenic mice expressing the human neurofilament heavy gene: a mouse model of amyotrophic lateral sclerosis. Cell. 73:35-46.
11. de Waegh, S.M., V.M. Lee, and S.T. Brady. 1992. Local modulation of neurofilament phosphorylation, axonal caliber, and slow axonal transport by myelinating Schwann cells. Cell. 68:451-463.
12. Eyer, J., and A. Peterson. 1994. Neurofilament-deficient axons and perikaryal aggregates in viable transgenic mice expressing a neurofilament-β-galactosidase fusion protein. Neuron. 12:389-405.
13. Figlewicz, D.A., A. Krizus, M.G. Martinoli, V. Meininger, M. Dib, G.A. Rouleau, and J.-P. Julien. 1994. Variants of the heavy neurofilament subunit are associated with the development of amyotrophic lateral sclerosis. Hum. Mol. Genet. 3:1757-1761.
14. Friede, R.L., and T. Samorajski. 1970. Axon caliber related to neurofilaments and microtubules in sciatic nerve fibers of rats and mice. Anat. Rec. 167:379-387.
15. Gasser, H.S., and H. Grundfest. 1939. Axon diameters in relation to the spike dimensions and the conduction velocity in mammalian A fibers. Am. J. Physiol. 127:393-414.
16. Guo, L., L. Degenstein, J. Dowling, Q.C. Yu, R. Wollmann, B. Perman, and E. Fuchs. 1995. Gene targeting of BPAG1: abnormalities in mechanical strength and cell migration in stratified epithelia and neurologic degeneration. Cell. 81:233-243.
17. Hirano, A. 1991. Cytopathology of amyotrophic lateral sclerosis. In Advances in Neurology. Volume 56. Amyotrophic Lateral Sclerosis and Other Motor Neuron Diseases. L.P. Rowland, editor. Raven Press, New York. 91-101.
18. Hirano, A., H. Donnenfeld, S. Sasaki, and I. Nakano. 1984a. Fine structural observations of neurofilamentous changes in amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 43:461-470.
19. Hirano, A., I. Nakano, L.T. Kurland, D.W. Mulder, P.W. Holley, and G. Saccomanno. 1984b. Fine structural study of neurofibrillary changes in a family with amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 43:471-480.
20. Hirokawa, N., M.A. Glicksman, and M.B. Willard. 1984. Organization of mammalian neurofilament polypeptides within the neuronal cytoskeleton. J. Cell Biol. 98:1523-1536.
21. Hoffman, P.N., and R.J. Lasek. 1975. The slow component of axonal transport. Identification of major structural polypeptides of the axon and their generality among mammalian neurons. J. Cell Biol. 66:351-366.
22. Hoffman, P.N., R.J. Lasek, J.W. Griffin, and D.L. Price. 1983. Slowing of the axonal transport of neurofilament proteins during development. J. Neurosci. 3:1694-1700.
23. Hoffman, P.N., J.W. Griffin, and D.L. Price. 1984. Control of axonal caliber by neurofilament transport. J. Cell Biol. 99:705-714.
24. Hoffman, P.N., D.W. Cleveland, J.W. Griffin, P.W. Landes, N.J. Cowan, and D.L. Price. 1987. Neurofilament gene expression: a major determinant of axonal caliber. Proc. Natl. Acad. Sci. USA. 84:3472-3476.
25. Hsieh, S.-T., G.J. Kidd, T.O. Crawford, Z.-S. Xu, B.D. Trapp, D.W. Cleveland, and J.W. Griffin. 1994. Regional modulation of neurofilament organization by myelination in normal axons. J. Neurosci. 14:6392-6401.
26. Julien, J.P., F. Cote, L. Beaudet, M. Sidky, D. Flavell, F. Grosveld, and W. Mushynski. 1988. Sequence and structure of the mouse gene coding for the largest neurofilament subunit. Gene (Amst.). 68:307-314.
27. Lasek, R.J., P. Paggi, and M.J. Katz. 1992. Slow axonal transport mechanisms move neurofilaments relentlessly in mouse optic axons. J. Cell Biol. 117: 607-616.
28. Lee, M.K., and D.W. Cleveland. 1994. Neurofilament function and dysfunction: involvement in axonal growth and neuronal disease. Curr. Opin. Cell Biol. 6: 34-40.
29. Lee, M.K., J.B. Tuttle, L.I. Rebhun, D.W. Cleveland, and A. Frankfurter. 1990. The expression and posttranslational modification of a neuron-specific β-tubulin isotype during chick embryogenesis. Cell Motil. Cytoskeleton. 17: 118-132.
30. Lee, M.K., Z. Xu, P.C. Wong, and D.W. Cleveland. 1993. Neurofilaments are obligate heteropolymers in vivo. J. Cell Biol. 122:1337-1350.
31. Lee, M.K., J.R. Marszalek, and D.W. Cleveland. 1994. A mutant neurofilament subunit causes massive, selective motor neuron death: implications for the pathogenesis of human motor neuron disease. Neuron. 13:975-988.
32. Lee, V.M., M.J. Carden, W.W. Schlaepfer, and J.Q. Trojanowski. 1987. Monoclonal antibodies distinguish several differentially phosphorylated states of the two largest rat neurofilament subunits (NF-H and NF-M) and demonstrate their existence in the normal nervous system of adult rats. J. Neurosci. 7:3474-3488.
33. Lees, J.F., P.S. Shneidman, S.F. Skuntz, M.J. Carden, and R.A. Lazzarini. 1988. The structure and organization of the human heavy neurofilament subunit (NF-H) and the gene encoding it. EMBO (Eur. Mol. Biol. Organ.) J. 7:1947-1955.
34. Lopata, M.A., and D.W. Cleveland. 1987. In vivo microtubules are copolymers of available beta-tubulin isotypes: localization of each of six vertebrate beta-tubulin isotypes using polyclonal antibodies elicited by synthetic peptide antigens. J. Cell Biol. 105:1707-1720.
35. Monteiro, M.J., P.N. Hoffman, J.D. Gearhart, and D.W. Cleveland. 1990. Expression of NF-L in both neuronal and nonneuronal cells of transgenic mice: increased neurofilament density in axons without affecting caliber. J. Cell Biol. 111:1543-1557.
36. Nixon, R.A., and K.B. Logvinenko. 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.
37. Nixon, R.A., P.A. Paskevich, R.K. Sihag, and C.Y. Thayer. 1994. Phosphorylation on carboxyl terminus domains of neurofilamertt proteins in retinal ganglion cell neurons in vivo: influences on regional neurofilament accumulation, interneurofilament spacing, and axon caliber. J. Cell Biol. 126:1031-1046.
38. Ohara, O., Y. Gahara, T. Miyake, H. Teraoka, and T. Kitamura. 1993. Neurofilament deficiency in quail caused by nonsense mutation in neurofilament-L gene. J. Cell Biol. 121:387-395.
39. Rooke, K., D.A. Figlewicz, F. Han, and G.A. Rouleau. 1996. Analysis of the KSP repeat of the neurofilament heavy subunit in familial amyotrophic lateral sclerosis. Ann. Neurol. 46:789-790.
40. Rosen, D.R., T. Siddique, D. Patterson, D.A. Figlewicz, P. Sapp, A. Hentati, D. Donaldson, J. Goto, J.P. O'Regan, H.X. Deng et al. 1993. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotropic lateral sclerosis. Nature (Lond.). 362:59-62.
41. Rouleau, G.A., A.W. Clark, K. Rooke, A. Pramatarova, A. Krizus, O. Suchowersky, J.-P. Julien, and D. Figlewicz. 1996. SOD1 mutation is associated with accumulation of neurofilaments in amyotrophic lateral scleorsis. Ann. Neurol. 39:128-131.
42. Sakaguchi, T., M. Okada, T. Kitamura, and K. Kawasaki. 1993. Reduced diameter and conduction velocity of myelinated fibers in the sciatic nerve of a neurofilament-deficient mutant quail. Neurosci. Lett. 153:65-68.
43. Schlaepfer, W.W., and J. Bruce. 1990. Neurofilament proteins are distributed in a diminishing proximodistal gradient along rat sciatic nerve. J. Neurochem. 55:453-460.
44. Shibata, N., A. Hirano, M. Kobayashi, T. Siddique, H.-X. Deng, W.-Y. Hung, T. Kato, and K. Asayama. 1996. Intense superoxide dismutase-1 immunoreactivity in intracytoplasmic hyaline inclusions of familial amyotrophic lateral sclerosis with posterior column involvement. J. Neuropathol. Exp. Neurol. 55:481-490.
45. Troncoso, J.C., J.L. March, M. Haner, and U. Aebi. 1990. Effect of aluminum and other multivalent cations on neurofilaments in vitro: an electron microscopic study. J. Struct. Biol. 103:2-12.
46. Vechio, J.V., L.I. Bruijn, Z.-S. Xu, R.H. Brown, Jr., and D.W. Cleveland. 1996. Identification of variants in human neurofilament genes: absence of linkage to familial ALS. Ann. Neurol. In press.
47. Wiedau-Pazos, M., J.J. Goto, S. Rabizadeh, E.D. Gralla, J.A. Roe, J.S. Valentine, and D.E. Bredesen. 1996. Altered reactivity of superoxide dismutase in familial amyotrophic lateral sclerosis. Science (Wash. DC). 271:515-518.
48. Willard, M., and C. Simon. 1983. Modulations of neurofilament axonal transport during the development of rabbit retinal ganglion cells. Cell. 35:551-559.
49. Wong, P.C., J. Marszalek, T.O. Crawford, Z. Xu, S.-T. Hsieh, J.W. Griffin, and D.W. Cleveland. 1995a. Increasing neurofilament subunit NF-M expression reduces axonal NF-H, inhibits radial growth, and results in neurofilamentous accumulation in motor neurons. J. Cell Biol. 130:1413-1422.
50. Wong, P.C., CA. Pardo, D.R. Borchelt, M.K. Lee, N.G. Copeland, N.A. Jenkins, S.S. Sisodia, D.W. Cleveland, and D.L. Price. 1995b. An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron. 14:1105-1116.
51. Xu, Z., L.C. Cork, J.W. Griffin, and D.W. Cleveland. 1993. Increased expression of neurofilament subunit NF-L produces morphological alterations that resemble the pathology of human motor neuron disease. Cell. 73:23-33.
52. Xu, Z.-S., J.R. Marszalek, M.K. Lee, P.C. Wong, J. Folmer, T.O. Crawford, S.-T. Hsieh, J.W. Griffin, and D.W. Cleveland. 1996. Subunit composition of neurofilaments specifies axonal diameter. J. Cell Biol. 133:1061-1069.
53. Yamasaki, H., G.S. Bennett, C. Itakura, and M. Mizutani. 1992. Defective expression of neurofilament protein subunits in hereditary hypotrophic axonopathy of quail. Lab. Invest. 66:734-743.
54. Yang, Y., J. Dowling, Q.-C. Yu, P. Kouklis, D.W. Cleveland, and E. Fuchs. 1996. An essential cytoskeletal linker protein connecting actin microfilaments to intermediate filaments. Cell. 86:655-665.