Neurofilaments bind tubulin and modulate its polymerization

Journal of Neuroscience

Volumn 29, Issue 35, 2009, Pages 11043-11054

  Bocquet, Arnaud ^a   Berges, Raphael ^a   Frank, Ronald ^a   Robert, Patrick ^a,b   Peterson, Alan C ^a   Eyer, Joël ^a  

^a UNIVERSITÉ D'ANGERS   (France)

^b INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

INTERMEDIATE FILAMENT PROTEIN; NEUROFILAMENT PROTEIN; TUBULIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MICROTUBULE ASSEMBLY; MOUSE; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN POLYMERIZATION; TRANSGENIC MOUSE;

AMINO ACID SEQUENCE; ANIMALS; BRAIN; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; NEUROFILAMENT PROTEINS; PROTEIN BINDING; TUBULIN; TUBULIN MODULATORS;

EID: 69749098439     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1924-09.2009     Document Type: Article

References (53)

1. Aamodt EJ, Williams RC Jr (1984) Microtubule-associated proteins connect microtubules and neurofilaments in vitro. Biochemistry 23:6023-6031. (Pubitemid 15153476)
2. Baas PW, Qiang L (2005) Neuronal microtubules: when the MAP is the roadblock. Trends Cell Biol 15:183-187.
3. Baas PW, Vidya Nadar C, Myers KA (2006) Axonal transport of microtubules: the long and short of it. Traffic 7:490-498.
4. Bartolini F, Gundersen GG (2006) Generation of noncentrosomal microtubule arrays. J Cell Sci 119:4155-4163.
5. Carden MJ, Trojanowski JQ, Schlaepfer WW, Lee VMY (1987) Two stage expression of neurofilament polypeptides during rat neurogenesis with early establishment of adult phosphorylation patterns. J Neurosci 7:3489-3504.
6. Cassimeris L (2002) The oncoprotein 18/stathmin family of microtubule destabilizers. Curr Opin Cell Biol 14:18-24.
7. Chou YH, Opal P, Quinlan RA, Goldman RD (1996) The relative roles of specific N- and C-terminal phosphorylation sites in the disassembly of intermediate filament in mitotic BHK-21 cells. J Cell Sci 109:817-826. (Pubitemid 26134384)
8. Conde C, Caceres A (2009) Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10:319-332.
9. de Waegh 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.
10. 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. (Pubitemid 28217917)
11. Elder GA, Friedrich VL Jr, Pereira D, Tu PH, Zhang B, Lee VM, Lazzarini RA (1999) Mice with disrupted midsized and heavy neurofilament genes lack axonal neurofilaments but have unaltered numbers of axonal microtubules. J Neurosci Res 57:23-32. (Pubitemid 29293576)
12. Eyer J, Leterrier JF (1988) Influence of the phosphorylation state of neurofilament proteins on the in vitro interactions between purified filaments. Biochem J 252:655-660. (Pubitemid 18153502)
13. Eyer J, Peterson AC (1994) Neurofilament-deficient axons and perikaryal aggregates in viable transgenic mice expressing a NF-beta-galactosidase fusion protein. Neuron 12:389-405. (Pubitemid 24071303)
14. Fasani F, Bocquet A, Robert P, Peterson A, Eyer J (2004) The amount of neurofilament aggregated in the cell body is controlled by their increased sensitivity to trypsin-like proteases. J Cell Sci 117:861-869. (Pubitemid 38386943)
15. Faundez V, Alvarez J (1986) Microtubules and calibers in developing axons. J Comp Neurol 250:73-80.
16. Frank R (1992) Spot-synthesis: an easy technique for the positionally addressable, parallel chemical synthesis on a membrane support. Tetrahedron 48:9217-9232.
17. Frank R, Overwin H (1996) SPOT synthesis. Epitope analysis with arrays of synthetic peptides prepared on cellulose membranes. Methods Mol Biol 66:149-169.
18. Fukushima N, Furuta D, Hidaka Y, Moriyama R, Tsujiuchi T (2009) Post-translational modifications of tubulin in the nervous system. J Neurochem 109:683-693.
19. Georgiou DM, Zidar J, Korosec M, Middleton LT, Kyriakides T, Christodoulou K (2002) A novel NF-L mutation Pro22Ser is associated with CMT2 in a large Slovenian family. Neurogenetics 4:93-96. (Pubitemid 36019504)
20. Ginzburg I, Teichman A, Dodemont HJ, Behar L, Littauer UZ (1985) Regulation of three beta-tubulin mRNAs during rat brain development. EMBO J 30:3667-3673.
21. Goto H, Kosako H, Tanabe K, Yanagida M, Sakurai M, Amano M, Kaibuchi K, Inagaki M (1998) Phosphorylation of vimentin by Rho-associated kinase at a unique amino-terminal site that is specifically phosphorylated during cytokinesis. J Biol Chem 273:11728-11736. (Pubitemid 28272076)
22. Guillaud L, Bosc C, Fourest-Lieuvin A, Denarier E, Pirollet F, Lafanechere L, Job D (1998) STOP proteins are responsible for the high degree of microtubule stabilization observed in neuronal cells. J Cell Biol 142:167-179. (Pubitemid 28341148)
23. Hirokawa N (1982) Cross-linker system between neurofilament, microtubule, and membranous organelles in frog axons revealed by the quickfreeze, deep-etching method. J Cell Biol 94:129-142.
24. Hisanaga S, Hirokawa N (1990) Dephosphorylation-induced interactions of neurofilaments with microtubules. J Biol Chem 265:21852-21858.
25. Hoffman PN, ClevelandDW (1988) Neurofilament and tubulin expression recapitulates the developmental program during axonal regeneration: induction of a specific beta-tubulin isotype. Proc Natl Acad Sci U S A 85:4530-4533.
26. Jacomy H, Zhu Q, Couillard-Després 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. (Pubitemid 29395453)
27. Julien JP, Mushynski WE (1982) Multiple phosphorylation sites in mammalian neurofilament polypeptides. J Biol Chem 257:10467-10470.
28. Ku NO, Liao J, Omary MB (1998) Phosphorylation of human keratin 18 serine 33 regulates binding to 14-3-3 proteins. EMBO J 17:1892-1906. (Pubitemid 28154520)
29. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
30. Lee VMY, Carden MJ, Schlaepfer WW, Trojanowski JQ, Otvos L, Hollosi M, Dietzchold B, Lazzarini RA (1988) Identification of the major multiphosphorylation sites in mammalian neurofilaments. Proc Natl Acad Sci U S A 85:1998-2002. (Pubitemid 24315812)
31. Leterrier JF, 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.
32. Mandelkow E, Mandelkow EM (1995) Microtubules and microtubule-associated proteins. Curr Opin Cell Biol 7:72-81.
33. Minami Y, Murofushi H, SakaiH (1982) Interaction of tubulin with neurofilaments: formation of networks by NF-dependent tubulin polymerization. J Biochem 92:889-898.
34. 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. (Pubitemid 23110882)
35. Pérez-Ollé R,López-Toledano MA, Goryunov D, Cabrera-Poch N, Stefanis L, Brown K, Liem RK (2005) Mutations in the neurofilament light gene linked to Charcot-Marie-Tooth disease cause defects in transport. J Neurochem 93:861-874. (Pubitemid 40695745)
36. Perrot R, Lonchampt P, Peterson AC, Eyer J (2007) Axonal neurofilaments control multiple fiber properties but do not influence structure or spacing of nodes of Ranvier. J Neurosci 27:9573-9584. (Pubitemid 47492172)
37. Perrot R, Berges R, Bocquet A, Eyer J (2008) Review of the multiple aspects of neurofilaments functions, and their possible contribution to neurodegeneration. Mol Neurobiol 38:27-65.
38. Rao MV, Houseweart MK, Williamson TL, Crawford TO, Folmer J, Cleveland DW (1998) Neurofilament-dependant 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. (Pubitemid 28480526)
39. Rao MV, Garcia ML, Miyazaki Y, Gotow T, Yuan A, Mattina S, Ward CM, Calcutt NA, Uchiyama Y, Nixon RA, Cleveland DW (2002) Gene replacement in mice reveals that the heavily phosphorylated tail of neurofilament heavy subunit (NF-H) does not affect axonal caliber or the transit of cargoes in slow axonal transport. J Cell Biol 158:681-693. (Pubitemid 34920107)
40. Riederer IM, Robert P, Porchet R, Eyer J, Riederer BM (2003) Selective changes in the neurofilament and microtubule cytoskeleton of NFHLacZ mice. J Neurosci Res 71:196-207. (Pubitemid 36055464)
41. Robert P, Peterson AC, Eyer J (2001) Neurofilament cytoskeleton does not modify accumulation of trophic factors mRNA. J Neurosci Res 64:487-492. (Pubitemid 32521768)
42. Tashiro T, Komiya Y (1992) Changes in organization and axonal transport of cytoskeletal proteins under normal and regenerating conditions. Mol Neurobiol 6:301-311.
43. Tashiro T, Imai R, Komiya Y (1994) Early effects of beta, beta′- iminodipropionitrile on tubulin solubility and neurofilament phosphorylation in the axon. J Neurochem 63:291-300. (Pubitemid 24184930)
44. Toivola DM, Zhou Q, English LS, Omary MB (2002) Type II keratins are phosphorylated on a unique motif during stress and mitosis in tissues and cultured cells. Mol Biol Cell 13:1857-1870. (Pubitemid 34651477)
45. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76:4350-4354. (Pubitemid 9256559)
46. Tu PH, Robinson KA, de Snoo F, Eyer J, Peterson A, Lee VM, Trojanowski JQ (1997) Selective degeneration fo Purkinje cells with Lewy body-like inclusions in aged NFHLACZ transgenic mice. J Neurosci 17:1064-1074. (Pubitemid 27043965)
47. Wang D, Villasante A, Lewis SA, Cowan NJ (1986) The mammalian beta-tubulin repertoire: hematopoietic expression of a novel, heterologous beta-tubulin isotype. J Cell Biol 103:1903-1910. (Pubitemid 17189046)
48. Weingarten MD, Lockwood AH, Hwo SY, KirschnerMW (1975) A protein factor essential for microtubule assembly. Proc Natl Acad Sci U S A 72:1858-1862.
49. Weiser AA, Or-Guil M, Tapia V, Leichsenring A, Schuchhardt J, Frömmel C, Volkmer-Engert R (2005) SPOT synthesis: reliability of array-based measurement of peptide binding affinity. Anal Biochem 342:300-311. (Pubitemid 40884580)
50. Yoshihara T, Yamamoto M, Hattori N, Misu K, Mori K, Koike H, Sobue G (2002) Identification of novel sequence variants in the neurofilament-light gene in a Japanese population: analysis of Charcot-Marie-Tooth disease patients and normal individuals. J Peripher Nerv Syst 7:221-224. (Pubitemid 35439787)
51. Zhao JX, Ohnishi A, Itakura C, Mizutani M, Yamamoto T, Hojo T, Murai Y (1995) Smaller axon and unaltered numbers of microtubules per axon in relation to number of myelin lamellae of myelinated fibers in the mutant quail deficient in neurofilaments. Acta Neuropathol 89:305-312.
52. Zhu Q, Couillard-Després S, Julien JP (1997) Delayed maturation of regenerating myelinated axons in mice lacking neurofilaments. Exp Neurol 148:299-316. (Pubitemid 127445138)
53. Zhu Q, Lindenbaum M, Levavasseur F, Jacomy H, Julien JP (1998) Disruption of the NFH gene increases axonal microtubule content and velocity of neurofilament transport: relief of axonopathy resulting from the toxin beta,beta′-iminodipropionitrile. J Cell Biol 143:183-193. (Pubitemid 28480527)