A neurotoxic peripherin splice variant in a mouse model of ALS

Journal of Cell Biology

Volumn 160, Issue 6, 2003, Pages 939-949

  Robertson, Janice ^a,b   Doroudchi, Mohammad M ^c   Nguyen, Minh Dang ^b   Durham, Heather D ^c   Strong, Michael J ^d   Shaw, Gerry ^e   Julien, Jean Pierre ^a   Mushynski, Walter E ^b  

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

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d UNIVERSITY OF WESTERN ONTARIO   (Canada)

^e UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

ALS; Isoforms; Peripherin; SOD1; Splicing

Indexed keywords

ISOPROTEIN; PERIPHERIN; PERIPHERIN 56; PERIPHERIN 58; PERIPHERIN 61; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENETIC TRANSFECTION; IMMUNOPRECIPITATION; INTERMEDIATE FILAMENT; MOTONEURON; MOUSE; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE;

ALTERNATIVE SPLICING; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANTERIOR HORN CELLS; AXONS; CELL DEATH; CELLS, CULTURED; DISEASE MODELS, ANIMAL; HUMANS; INTERMEDIATE FILAMENT PROTEINS; LUMBAR VERTEBRAE; MEMBRANE GLYCOPROTEINS; MICE; MICE, TRANSGENIC; MUTATION; NERVE TISSUE PROTEINS; PRECIPITIN TESTS; SUPEROXIDE DISMUTASE; TUMOR CELLS, CULTURED;

ANIMALIA; MUS MUSCULUS;

EID: 0345237912     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200205027     Document Type: Article

References (40)

1. Angelastro, J.M., C.L. Ho, T. Frappier, R.K. Liem, and L.A. Greene. 1998. Peripherin is tyrosine-phosphorylated at its carboxyl-terminal cyrosine. J. Neurochem. 70:540-549.
2. Beaulieu, J.M., M.D. Nguyen, and J.P. Julien. 1999a. Late onset death of motor neurons in mice overexpressing wild-type peripherin. J. Cell. Biol. 147:531-544.
3. Beaulieu, J.M., J. Robertson, and J.P. Julien. 1999b. Interactions between peripherin and neurofilaments in cultured cells: disruption of peripherin assembly by the NF-M and NF-H subunits. Biochem. Cell. Biol. 77:41-45.
4. Beaulieu, J.M., J. Kriz, and J.P. Julien. 2002. Induction of peripherin expression in subsets of brain neurons after lesion injury or cerebral ischemia. Brain Res. 946:153-161.
5. Brody, B.A., C.A. Ley, and L.M. Parysek. 1989. Selective distribution of the 57 kDa neural intermediate filament protein in the rat CNS. J. Neurosci. 9:2391-2401.
6. Carlsson, L., and L.E. Thornell. 2001. Desmin-related myopathies in mice and man. Acta Physiol. Scand. 171:341-348.
7. Carpenter, S. 1968. Proximal axonal enlargement in motor neuron disease. Neurology. 18:841-851.
8. Cleveland, D.W., and J.D. Rothstein. 2001. From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat. Rev. Neurosci. 2:806-819.
9. Corbo, M., and A.P. Hays. 1992. Peripherin and neurofilament protein coexist in spinal spheroids of motor neuron disease. J. Neuropathol. Exp. Neurol. 51: 531-537.
10. Cui, C., P.J. Stambrook, and L.M. Parysek. 1995. Peripherin assembles into homopolymers in SW13 cells. J. Cell. Sci. 108:3279-3284.
11. Durham, H.D., J. Roy, L. Dong, and D.A. Figlewicz. 1997. Aggregation of mutant Cu/Zn superoxide dismutase proteins in a culture model of ALS. J. Neuropathol. Exp. Neurol. 56:523-530.
12. Escurat, M., K. Djabali, M. Gumpel, F. Gros, and M.M. Portier. 1990. Differential expression of two neuronal intermediate-filament proteins, peripherin and the low-molecular-mass neurofilament protein (NF-L), during the development of the rat. J. Neurosci. 10:764-784.
13. Fisher, D.Z., N. Chaudhary, and G. Blobel. 1986. cDNA sequencing of nuclear lamins A and C reveals primary and secondary structural homology to intermediate filament proteins. Proc. Natl. Acad. Sci. USA. 83:6450-6454.
14. Foley, J., C.A. Ley, and L.M. Parysek. 1994. The structure of the human peripherin gene (PRPH) and identification of potential regulatory elements. Genomics. 22:456-461.
15. Fuchs, E. 1994. Intermediate filaments and disease: mutations that cripple cell strength. J. Cell. Biol. 125:511-516.
16. Julien, J.P. 2001. Amyotrophic lateral sclerosis. unfolding the toxicity of the misfolded. Cell. 104:581-591.
17. Julien, J.P., and W.E. Mushynski. 1998. Neurofilaments in health and disease. Prog. Nucleic Acid Res. Mol. Biol. 61:1-23.
18. Julien, J.P., and J.M. Beaulieu. 2000. Cytoskeletal abnormalities in amyotrophic lateral sclerosis: beneficial or detrimental effects? J. Neurol. Sci. 180:7-14.
19. Landon, F., M. Lemonnier, R. Benarous, C. Huc, M. Fiszman, F. Gros, and M.M. Portier. 1989. Multiple mRNAs encode peripherin, a neuronal intermediate filament protein. EMBO J. 8:1719-1726.
20. Landon, F., A. Wolff, and B. de Nechaud. 2000. Mouse peripherin isoforms. Biol. Cell. 92:397-407.
21. Lindenbaum, M.H., S. Carbonetto, and W.E. Mushynski. 1987. Nerve growth factor enhances the synthesis, phosphorylation, and metabolic stability of neurofilament proteins in PC12 cells. J. Biol. Chem. 262:605-610.
22. McKeon, F.D., M.W. Kirschner, and D. Caput. 1986. Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins, Nature. 319:463-468.
23. Migheli, A., T. Pezzulo, A. Attanasio, and D. Schiffer. 1993. Peripherin immunoreactive structures in amyotrophic lateral sclerosis. Lab. Invest. 68:185-191.
24. Nguyen, M.D., R.C. Lariviere, and J.P. Julien. 2001. Deregulation of Cdk5 in a mouse model of ALS: toxicity alleviated by perikaryal neurofilament inclusions. Neuron. 30:135-147.
25. Park, K.Y., M.C. Dalakas, H.H. Goebel, V.J. Ferrans, C. Semino-Mora, S. Litvak, K. Takeda, and L.G. Goldfarb. 2000. Desmin splice variants causing cardiac and skeletal myopathy. J. Med. Genet. 37:851-857.
26. Parysek, L.M., and R.D. Goldman. 1988. Distribution of a novel 57 kDa intermediate filament (IF) protein in the nervous system. J. Neurosci. 8:555-563.
27. Portier, M.M., P. Brachet, B. Croizat, and F. Gros. 1983a. Regulation of peripherin in mouse neuroblastoma and rat PC 12 pheochromocytoma cell lines. Dev. Neurosci. 6:215-226.
28. Portier, M.M., B. de Nechaud, and F. Gros. 1983b. Peripherin, a new member of the intermediate filament protein family. Dev. Neurosci. 6:335-344.
29. Portier, M.M., M. Escurat, F. Landon, K. Djabali, and O. Bousquet. 1993. Peripherin and neurofilaments: expression and role during neural development. C. R. Acad. Sci. III. 316:1124-1140.
30. Robertson, J., J.M. Beaulieu, M.M. Doroudchi, H.D. Durham, J.P. Julien, and W.E. Mushynski. 2001. Apoptotic death of neurons exhibiting peripherin aggregates is mediated by the proinflammatory cytokine tumor necrosis factor-α. J. Cell. Biol. 155:217-226.
31. Rosen, D.R., T. Siddique, D. Patterson, D.A. Figiewicz, 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 amyotrophic lateral sclerosis. Nature. 362:59-62.
32. Roy, J., S. Minotti, L. Dong, D.A. Figiewicz, and H.D. Durham. 1998. Glutamate potentiates the toxicity of mutant Cu/Zn-superoxide dismutase in motor neurons by postsynaptic calcium-dependent mechanisms. J. Neurosci. 18: 9673-9684.
33. Sarria, A.J., J.G. Lieber, S.K. Nordeen, and R.M. Evans. 1994. The presence or absence of a vimentin-type intermediate filament network affects the shape of the nucleus in human SW13 cells. J. Cell. Sci. 107:1593-1607.
34. Strong, M.J. 2001. Progress in clinical neurosciences: the evidence for ALS as a multisystems disorder of limited phenotypic expression. Can. J. Neurol. Sci. 28:283-298.
35. Titeux, M., V. Brocheriou, Z. Xue, J. Gao, J.F. Pellissier, P. Guicheney, D. Paulin, and Z. Li. 2001. Human synemin gene generates splice variants encoding two distinct intermediate filament proteins. Eur. J. Biochem. 268:6435-6449.
36. Troy, C.M., N.A. Muma, L.A. Greene, D.L. Price, and M.L. Shelanski. 1990. Regulation of peripherin and neurofilament expression in regenerating rat motor neurons. Brain Res. 529:232-238.
37. Tu, P.H., P. Raju, K.A. Robinson, M.E. Gurney, J.Q. Trojanowski, and V.M. Lee. 1996. Transgenic mice carrying a human mutant superoxide dismutase transgene develop neuronal cytoskeletal pathology resembling human amyotrophic lateral sclerosis lesions. Proc. Natl. Acad. Sci. USA. 93:3155-3160.
38. Wong, J., and M.M. Oblinger. 1990. Differential regulation of peripherin and neurofilament gene expression in regenerating rat DRG neurons. J. Neurosci. Res. 27:332-341.
39. Wong, P.C., C.A. Pardo, D.R. Borchelt, M.K. Lee, N.G. Copeland, N.A. Jenkins, S.S. Sisodia, D.W. Cleveland, and D.L. Price. 1995. An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron. 14:1105-1116.
40. Zelenika, D., B. Grima, M. Brenner, and B. Pessac. 1995. A novel glial fibrillary acidic protein mRNA lacking exon 1. Brain Res. Mol. Brain Res. 30:251-258.