Neurofilament Transport In Vivo Minimally Requires Hetero-Oligomer Formation

Journal of Neuroscience

Volumn 23, Issue 28, 2003, Pages 9452-9458

  Yuan, Aidong ^a,b   Rao, Mala V ^a,b   Kumar, Asok ^a,b   Julien, Jean Pierre ^c   Nixon, Ralph A ^a,b  

^a NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

Cytoskeletal protein; Hetero oligomer; Intermediate filaments; Knock out mice; Neurofilament light subunit; Neurofilament medium subunit; Neurofilaments; Optic axons; Slow axonal transport; internexin

Indexed keywords

ALPHA INTERNEXIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; FEMALE; GENE DELETION; IN VIVO STUDY; INTERMEDIATE FILAMENT; MALE; MOUSE; NERVE FIBER TRANSPORT; NEUROFILAMENT; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN TRANSPORT; RETINA GANGLION CELL;

EID: 0142250822     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-28-09452.2003     Document Type: Article

References (52)

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. Alvarez J, Giuditta A, Koenig E (2000) Protein synthesis in axons and terminals: significance for maintenance, plasticity and regulation of phenotype. With a critique of slow transport theory. Prog Neurobiol 62:1-62.
3. Baas PW, Brown A (1997) Slow axonal transport: the polymer transport model. Trends Cell Biol 7:380-384.
4. Bray D (1997) The riddle of slow axonal transport-an introduction. Trends Cell Biol 7:379.
5. Brownlees J, Ackerley S, Grierson AJ, Jacobsen NJ, Shea K, Anderton BH, Leigh PN, Shaw CE, Miller CC (2002) Charcot-Marie-Tooth disease neurofilament mutations disrupt neurofilament assembly and axonal transport. Hum Mol Genet 11:2837-2844.
6. Burton PR, Wentz MA (1992) Neurofilaments are prominent in bullfrog olfactory axons but are rarely seen in those of the tiger salamander, Ambystoma tigrinum. J Comp Neurol 317:396-406.
7. Ching GY, Liem RK (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.
8. Ching GY, Liem RK (1998) Roles of head and tail domains in alpha-internexin's self-assembly and coassembly with the neurofilament triplet proteins. J Cell Sci 111:321-333.
9. Ching GY, Chien CL, Flores R, Liem RK (1999) Overexpression of α-internexin causes abnormal neurofilamentous accumulations and motor coordination deficits in transgenic mice. J Neurosci 19:2974-2986.
10. Chiu FC, Norton WT (1982) Bulk preparation of CNS cytoskeleton and the separation of individual neurofilament proteins by gel filtration: dye-binding characteristics and amino acid compositions. J Neurochem 39:1252-1260.
11. De Jonghe P, Mersivanova I, Nelis E, Del Favero J, Martin JJ, Van Broeckhoven C, Evgrafov O, Timmerman V (2001) Further evidence that neurofilament light chain gene mutations can cause Charcot-Marie-Tooth disease type 2E. Ann Neurol 49:245-249.
12. Elder GA, Friedrich VL Jr, Bosco P, Kang C, Gourov A, Tu PH, Lee VM, Lazzarini RA (1998) Absence of the mid-sized neurofilament subunit decreases axonal calibers, levels of light neurofilament (NF-L), and neurofilament content. J Cell Biol 141:727-739.
13. Eyer J, Peterson A (1994) Neurofilament-deficient axons and perikaryal aggregates in viable transgenic mice expressing a neurofilament-beta-galactosidase fusion protein. Neuron 12:389-405.
14. Faussone-Pellegrini MS, Matini P, DeFelici M (1999) The cytoskeleton of the myenteric neurons during murine embryonic life. Anat Embryol (Berl) 199:459-469.
15. Fliegner KH, Liem RK (1991) Cellular and molecular biology of neuronal intermediate filaments. Int Rev Cytol 131:109-167.
16. Fliegner KH, Kaplan MP, Wood TL, Pintar JE, Liem RK (1994) Expression of the gene for the neuronal intermediate filament protein alpha-internexin coincides with the onset of neuronal differentiation in the developing rat nervous system. J Comp Neurol 342:161-173.
17. Fuchs E, Weber K (1994) Intermediate filaments: structure, dynamics, function, and disease. Annu Rev Biochem 63:345-382.
18. Galbraith JA, Reese TS, Schlief ML, Gallant PE (1999) Slow transport of unpolymerized tubulin and polymerized neurofilament in the squid giant axon. Proc Natl Acad Sci USA 96:11589-11594.
19. Hall GF, Chu B, Lee S, Liu Y, Yao J (2000) The single neurofilament subunit of the lamprey forms filaments and regulates axonal caliber and neuronal size in vivo. Cell Motil Cytoskeleton 46:166-182.
20. Hirokawa N, Terada S, Funakoshi T, Tekeda S (1997) Slow axonal transport: the subunit transport model. Trends Cell Biol 7:384-388.
21. Jacomy H, Zhu Q, Couillard-Despres S, Beaulieu JM, Julien JP (1999) Disruption of type IV intermediate filament network in mice lacking the neurofilament medium and heavy subunits. J Neurochem 73:972-984.
22. Jordanova A, De Jonghe P, Boerkoel CF, Takashima H, De Vriendt E, Ceuterick C, Martin JJ, Butler IJ, Mancias P, Papasozomenos SC, Terespolsky D, Potocki L, Brown CW, Shy M, Rita DA, Tournev I, Kremensky I, Lupski JR, Timmerman V (2003) Mutations in the neurofilament light chain gene (NEFL) cause early onset severe Charcot-Marie-Tooth disease. Brain 126:590-597.
23. Kaplan MP, Chin SS, Fliegner KH, Liem RK (1990) Alpha-internexin, a novel neuronal intermediate filament protein, precedes the low molecular weight neurofilament protein (NF-L) in the developing rat brain. J Neurosci 10:2735-2748.
24. 1 dopamine receptor to regulate cell surface expression and desensitization. J Neurosci 22:5920-5930.
25. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
26. Lee MK, Xu Z, Wong PC, Cleveland DW (1993) Neurofilaments are obligate heteropolymers in vivo. J Cell Biol 122:1337-1350.
27. Levavasseur F, Zhu Q, Julien JP (1999) No requirement of alpha-internexin for nervous system development and for radial growth of axons. Brain Res Mol Brain Res 69:104-112.
28. Mersiyanova IV, Perepelov AV, Polyakov AV, Sitnikov VF, Dadali EL, Oparin RB, Petrin AN, Evgrafov OV (2000) A new variant of Charcot-Marie-Tooth disease type 2 is probably the result of a mutation in the neurofilament-light gene. Am J Hum Genet 67:37-46.
29. Nakagawa T, Chen J, Zhang Z, Kanai Y, Hirokawa N (1995) Two distinct functions of the carboxyl-terminal tail domain of NF-M upon neurofilament assembly: cross-bridge formation and longitudinal elongation of filaments. J Cell Biol 129:411-429.
30. Nixon RA, Logvinenko KB (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.
31. Nixon RA, Paskevich PA, Sihag RK, Thayer CY (1994) Phosphorylation on carboxyl terminus domains of neurofilament proteins in retinal ganglion cell neurons in vivo: influences on regional neurofilament accumulation, interneurofilament spacing, and axon caliber. J Cell Biol 126:1031-1046.
32. Ohara O, Gahara Y, Miyake T, Teraoka H, Kitamura T (1993) Neurofilament deficiency in quail caused by nonsense mutation in neurofilament-L gene. J Cell Biol 121:387-395.
33. Perez-Olle R, Leung CL, Liem RK (2002) Effects of Charcot-Marie-Tooth-linked mutations of the neurofilament light subunit on intermediate filament formation. J Cell Sci 115:4937-4946.
34. Popov S, Poo MM (1992) Diffusional transport of macromolecules in developing nerve processes. J Neurosci 12:77-85.
35. 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.
36. Rao MV, Houseweart MK, Williamson TL, Crawford TO, Folmer J, Cleveland DW (1998) Neurofilament-dependent radial growth of motor axons and axonal organization of neurofilaments does not require the neurofilament heavy subunit (NF-H) or its phosphorylation. J Cell Biol 143:171-181.
37. Roy S, Coffee P, Smith G, Liem RK, Brady ST, Black MM (2000) Neurofilaments are transported rapidly but intermittently in axons: implications for slow axonal transport. J Neurosci 20:6849-6861.
38. Shah JV, Cleveland DW (2002) Slow axonal transport: fast motors in the slow lane. Curr Opin Cell Biol 14:58-62.
39. Sihag RK, Nixon RA (1990) Phosphorylation of the amino-terminal head domain of the middle molecular mass 145-kDa subunit of neurofilaments. Evidence for regulation by second messenger-dependent protein kinases. J Biol Chem 265:4166-4171.
40. Sihag RK, Jaffe H, Nixon RA, Rong X (1999) Serine-23 is a major protein kinase A phosphorylation site on the amino-terminal head domain of the middle molecular mass subunit of neurofilament proteins. J Neurochem 72:491-499.
41. Takeda S, Okabe S, Funakoshi T, Hirokawa N (1994) Differential dynamics of neurofilament-H protein and neurofilament-L protein in neurons. J Cell Biol 127:173-185.
42. Terada S, Hirokawa N (2000) Moving on to the cargo problem of microtubule-dependent motors in neurons. Curr Opin Neurobiol 10:566-573.
43. Terada S, Nakata T, Peterson AC, Hirokawa N (1996) Visualization of slow axonal transport in vivo. Science 273:784-788.
44. Toyoshima I, Kato K, Sugawara M, Wada C, Okawa S, Kobayashi M, Masamune O, Watanabe S (2000) Massive accumulation of M and H subunits of neurofilament proteins in spinal motor neurons of neurofilament deficient Japanese quail, Quv. Neurosci Lett 287:175-178.
45. Undamatla J, Szaro BG (2001) Differential expression and localization of neuronal intermediate filament proteins within newly developing neurites in dissociated cultures of Xenopus laevis embryonic spinal cord. Cell Motil Cytoskeleton 49:16-32.
46. Wang L, Ho CL, Sun D, Liem RK, Brown A (2000) Rapid movement of axonal neurofilaments interrupted by prolonged pauses. Nat Cell Biol 2:137-141.
47. Williamson TL, Bruijn LI, Zhu Q, Anderson KL, Anderson SD, Julien JP, Cleveland DW (1998) Absence of neurofilaments reduces the selective vulnerability of motor neurons and slows disease caused by a familial amyotrophic lateral sclerosis-linked superoxide dismutase 1 mutant. Proc Natl Acad Sci USA 95:9631-9636.
48. Yabe JT, Pimenta A, Shea TB (1999) Kinesin-mediated transport of neurofilament protein oligomers in growing axons. J Cell Sci 112:3799-3814.
49. 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.
50. Yuan A, Mills RG, Chia CP, Bray JJ (2000) Tubulin and neurofilament proteins are transported differently in axons of chicken motoneurons. Cell Mol Neurobiol 20:623-632.
51. Zhang Z, Spencer PH, Jin LQ, Cohlberg JA, Selzer ME (2002) The single neurofilament subunit of lamprey may need another element for filaments assembly. Soc Neurosci Abstr 28:635.631.
52. Zhu Q, Couillard-Despres S, Julien JP (1997) Delayed maturation of regenerating myelinated axons in mice lacking neurofilaments. Exp Neurol 148:299-316.