Mutations in the neurofilament light gene linked to Charcot-Marie-Tooth disease cause defects in transport

Journal of Neurochemistry

Volumn 93, Issue 4, 2005, Pages 861-874

  Pérez Ollé, Raül ^a   López Toledano, Miguel A ^a   Goryunov, Dmitry ^a   Cabrera Poch, Noemi ^a,b   Stefanis, Leonidas ^a,c   Brown, Kristy ^a   Liem, Ronald K H ^a  

^a NewYork Presbyterian Hospital   (United States)

^b INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^c BIOMEDICAL RESEARCH FOUNDATION   (Greece)

Author keywords

Axonal transport; Charcot Marie Tooth; Intermediate filament; Intracellular trafficking; Neurofilament; Neuropathy

Indexed keywords

AMYLOID PRECURSOR PROTEIN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE; GENE MUTATION; GENE OVEREXPRESSION; GOLGI COMPLEX; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; HUMAN CELL; MOTOR NEUROPATHY; NERVE CELL CULTURE; NERVE CONDUCTION; NERVE DEGENERATION; NERVE FIBER TRANSPORT; NEUROFILAMENT; NEUROFILAMENT LIGHT GENE; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NEUROPATHY;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANIMALS, NEWBORN; AXONAL TRANSPORT; CELLS, CULTURED; CHARCOT-MARIE-TOOTH DISEASE; CLONING, MOLECULAR; DISEASE MODELS, ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GOLGI APPARATUS; HUMANS; MITOCHONDRIA; MUTAGENESIS; MUTATION; NEUROFILAMENT PROTEINS; NEURONS; RATS; SYMPATHETIC NERVOUS SYSTEM; TIME FACTORS; TRANSFECTION;

EID: 18844446126     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03095.x     Document Type: Article

References (42)

1. Ackerley S., Grierson A. J., Brownlees J., Thornhill P., Anderton B. H., Leigh P. N., Shaw C. E. and Miller C. C. (2000) Glutamate slows axonal transport of neurofilaments in transfected neurons. J. Cell Biol. 150, 165-176.
2. 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.
3. Beaulieu J. M., Jacomy H. and Julien J. P. (2000) Formation of intermediate filament protein aggregates with disparate effects in two transgenic mouse models lacking the neurofilament light subunit. J. Neurosci. 20, 5321-5328.
4. Brownlees J., Ackerley S., Grierson A. J., Jacobsen N. J., Shea K., Anderton B. H., Leigh P. N., Shaw C. E. and Miller C. C. (2002) Charcot-Marie-Tooth disease neurofilament mutations disrupt neurofilament assembly and axonal transport. Hum. Mol. Genet. 11, 2837-2844.
5. Carter J., Gragerov A., Konvicka K., Elder G., Weinstein H. and Lazzarini R. A. (1998) Neurofilament (NF) assembly; divergent characteristics of human and rodent NF-L subunits. J. Biol. Chem. 273, 5101-5108.
6. Ching G. Y., Chien C. L., Flores R. and Liem R. K. (1999) Overexpression of alpha-internexin causes abnormal neurofilamentous accumulations and motor coordination deficits in transgenic mice. J. Neurosci. 19, 2974-2986.
7. De Jonghe P., Mersivanova I., Nelis E., Del Favero J., Martin J. J., Van Broeckhoven C., Evgrafov O. and Timmerman V. (2001) Further evidence that neurofilament light chain gene mutations can cause Charcot-Marie-Tooth disease type 2E. Ann. Neurol. 49, 245-249.
8. Fabrizi G. M., Cavallaro T., Angiari C., Bertolasi L., Cabrini I., Ferrarini M. and Rizzuto N. (2004) Giant axon and neurofilament accumulation in Charcot-Marie-Tooth disease type 2E. Neurology 62, 1429-1431.
9. Frappier T., Liang N. S., Brown K., Leung C. L., Lynch T., Liem R. K. and Shelanski M. L. (1999) Abnormal microtubule packing in processes of SF9 cells expressing the FTDP-17 V337M tau mutation. FEBS Lett. 455, 262-266.
10. Gama Sosa M. A., Friedrich V. L. Jr, DeGasperi R., Kelley K., Wen P. H., Senturk E., Lazzarini R. A. and Elder G. A. (2003) Human midsized neurofilament subunit induces motor neuron disease in transgenic mice. Exp. Neurol. 184, 408-419.
11. Garcia-Mata R., Bebok Z., Sorscher E. J. and Sztul E. S. (1999) Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J. Cell Biol. 146, 1239-1254.
12. Geisler N. and Weber K. (1981) Self-assembly in Vitro of the 68,000 molecular weight component of the mammalian neurofilament triplet proteins into intermediate-sized filaments. J. Mol. Biol. 151, 565-571.
13. Georgiou D. M., Zidar J., Korosec M., Middleton L. T., Kyriakides T. and Christodoulou K. (2002) A novel NF-L mutation Pro22Ser is associated with CMT2 in a large Slovenian family. Neurogenetics 4, 93-96.
14. Goldstein L. S. and Yang Z. (2000) Microtubule-based transport systems in neurons: the roles of kinesins and dyneins. Annu. Rev. Neurosci. 23, 39-71.
15. Gonatas N. K., Gonatas J. O. and Stieber A. (1998) The involvement of the Golgi apparatus in the pathogenesis of amyotrophic lateral sclerosis, Alzheimer's disease, and ricin intoxication. Histochem. Cell. Biol. 109, 591-600.
16. Hafezparast M., Klocke R., Ruhrberg C. et al. (2003) Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science 300, 808-812.
17. Jordanova A., De Jonghe P., Boerkoel C. F. et al. (2003) Mutations in the neurofilament light chain gene (NEFL) cause early onset severe Charcot-Marie-Tooth disease. Brain 126, 590-597.
18. Kaplan M. P., Chin S. S., Macioce P., Srinawasan J., Hashim G. and Liem R. K. (1991) Characterization of a panel of neurofilament antibodies recognizing N-terminal epitopes. J. Neurosci. Res. 30, 545-554.
19. Lee M. K., Marszalek J. R. and Cleveland D. W. (1994) A mutant neurofilament subunit causes massive, selective motor neuron death: implications for the pathogenesis of human motor neuron disease. Neuron 13, 975-988.
20. Lencer W. I., Hirst T. R. and Holmes R. K. (1999) Membrane traffic and the cellular uptake of cholera toxin. Biochim. Biophys. Acta 1450, 177-190.
21. Liem R. K. (1993) Molecular biology of neuronal intermediate filaments. Curr. Opin. Cell Biol. 5, 12-16.
22. Liem R. K. and Hutchison S. B. (1982) Purification of individual components of the neurofilament triplet: filament assembly from the 70,000-dalton subunit. Biochemistry 21, 3221-3226.
23. Liem R. K. and Leung C. L. (2003) Neuronal intermediate filament overexpression and neurodegeneration in transgenic mice. Exp. Neurol. 184, 3-8.
24. Mersiyanova I. V., Perepelov A. V., Polyakov A. V., Sitnikov V. F., Dadali E. L., Oparin R. B., Petrin A. N. and Evgrafov O. V. (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.
25. Nakeff A., Valeriote F., Gray J. W. and Grabske R. J. (1979) Application of flow cytometry and cell sorting to megakaryocytopoiesis. Blood 53, 732-745.
26. Perez-Olle R., Leung C. L. and Liem R. K. (2002) Effects of Charcot-Marie-Tooth-linked mutations of the neurofilament light subunit on intermediate filament formation. J. Cell Sci. 115, 4937-4946.
27. Perez-Olle R., Jones S. T. and Liem R. K. H. (2004) Phenotypic analysis of neurofilament light gene mutations linked to Charcot-Marie-Tooth disease in cell culture models. Hum. Mol. Genet. 13, 2207-2220.
28. Puls I., Jonnakuty C., LaMonte B. H. et al. (2003) Mutant dynactin in motor neuron disease. Nat. Genet. 33, 455-456.
29. Puri V., Watanabe R., Singh R. D., Dominguez M., Brown J. C., Wheatley C. L., Marks D. L. and Pagano R. E. (2001) Clathrin-dependent and -independent internalization of plasma membrane sphingolipids initiates two Golgi targeting pathways. J. Cell Biol. 154, 535-547.
30. Qi Y., Wang J. K., McMillian M. and Chikaraishi D. M. (1997) Characterization of a CNS cell line, CAD, in which morphological differentiation is initiated by serum deprivation. J. Neurosci. 17, 1217-1225.
31. Reid E., Kloos M., Ashley-Koch A. et al. (2002) A kinesin heavy chain (KIF5A) mutation in hereditary spastic paraplegia (SPG10). Am. J. Hum. Genet. 71, 1189-1194.
32. Sasaki S. and Iwata M. (1999) Immunoreactivity of beta-amyloid precursor protein in amyotrophic lateral sclerosis. Acta Neuropathol. 97, 463-468.
33. Stefanis L., Troy C. M., Qi H. and Greene L. A. (1997) Inhibitors of trypsin-like serine proteases inhibit processing of the caspase Nedd-2 and protect PC12 cells and sympathetic neurons from death evoked by withdrawal of trophic support. J. Neurochem. 69, 1425-1437.
34. Suter U. and Scherer S. S. (2003) Disease mechanisms in inherited neuropathies. Nat. Rev. Neurosci. 4, 714-726.
35. Trojanowski J. Q., Gonatas J. O. and Gonatas N. K. (1982) Horseradish peroxidase (HRP) conjugates of cholera toxin and lectins are more sensitive retrogradely transported markers than free HRP. Brain Res. 231, 33-50.
36. 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.
37. Wagner O. I., Ascano J., Tokito M., Leterrier J. F., Janmey P. A. and Holzbaur E. L. (2004) The interaction of neurofilaments with the microtubule motor cytoplasmic dynein. Mol. Biol. Cell 15, 5092-5100.
38. Wang L., Ho C. I., Sun D., Liem R. K. H. and Brown A. (2000) Rapid movement of axonal neurofilaments interrupted by prolonged pauses. Nat. Cell Biol. 2, 137-140.
39. 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.
40. Yoshihara T., Yamamoto M., Hattori N., Misu K., Mori K., Koike H. and 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.
41. Zhao C., Takita J., Tanaka Y. et al. (2001) Charcot-Marie-Tooth disease type 2A caused by mutation in a microtubule motor KIF1Bbeta. Cell 105, 587-597.
42. Zuchner S., Vorgerd M., Sindern E. and Schroder J. M. (2004) The novel neurofilament light (NEFL) mutation Glu397Lys is associated with a clinically and morphologically heterogeneous type of Charcot-Marie-Tooth neuropathy. Neuromusc. Disord. 14, 147-157.