Focal dysfunction of the proteasome: A pathogenic factor in a mouse model of amyotrophic lateral sclerosis

Journal of Neurochemistry

Volumn 89, Issue 6, 2004, Pages 1325-1335

  Kabashi, Edor ^a   Agar, Jeffrey N ^a   Taylor, David M ^a   Minotti, Sandra ^a   Durham, Heather D ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Amyotrophic lateral sclerosis; Motor neuron; Neurodegenerative disorder; Proteasome; SOD 1 Cu Zn superoxide dismutase ; Ubiquitin

Indexed keywords

CASPASE; CHYMOTRYPSIN; COPPER ZINC SUPEROXIDE DISMUTASE; PROTEASOME; TRYPSIN; UBIQUITIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEGENERATIVE DISEASE; ENZYME ACTIVITY; GENE MUTATION; LIVER; LUMBAR SPINAL CORD; MOTONEURON; MOUSE; NEUROPIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; THORACIC SPINAL CORD;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CYSTEINE ENDOPEPTIDASES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENZYME ACTIVATION; FIBROBLASTS; HUMANS; LUMBOSACRAL REGION; MICE; MICE, TRANSGENIC; MULTIENZYME COMPLEXES; NIH 3T3 CELLS; PROTEASOME ENDOPEPTIDASE COMPLEX; SPINAL CORD; SUPEROXIDE DISMUTASE;

ANIMALIA; MUS MUSCULUS;

EID: 3042515545     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02453.x     Document Type: Article

References (61)

1. Adams G. M., Crotchett B., Slaughter C. A., DeMartino G. N. and Gogol E. P. (1998) Formation of proteasome-PA700 complexes directly correlates with activation of peptidase activity. Biochemistry 37, 12927-12932.
2. Alexianu M. E., Kozovska M. and Appel S. H. (2001) Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology 57, 1282-1289.
3. Allen S., Heath P. R., Kirby J., Wharton S. B., Cookson M. R., Menzies F. M., Banks R. E. and Shaw P. J. (2003) Analysis of the cytosolic proteome in a cell culture model of familial amyotrophic lateral sclerosis reveals alterations to the proteasome, antioxidant defenses, and nitric oxide synthetic pathways. J. Biol. Chem. 278, 6371-6383.
4. Aquilano K., Rotilio G. and Ciriolo M. R. (2003) Proteasome activation and nNOS down-regulation in neuroblastoma cells expressing a Cu,Zn superoxide dismutase mutant involved in familial ALS. J. Neurochem. 85, 1324-1335.
5. Arribas J. and Castano J. G. (1990) Kinetic studies of the differential effect of detergents on the peptidase activities of the multicatalytic proteinase from rat liver. J. Biol. Chem. 265, 13969-13973.
6. Attaix D., Combaret L., Tilignac T. and Taillandier D. (1999) Adaptation of the ubiquitin-proteasome proteolytic pathway in cancer cachexia. Mol Biol. Rep 26, 77-82.
7. Batulan Z., Shinder G. A., Minotti S., He B. P., Doroudchi M. M., Nalbantoglu J., Strong M. J. and Durham H. D. (2003) High threshold for induction of the stress response in motor neurons is associated with failure to activate HSF1. J. Neurosci. 23, 5789-5798.
8. Baumeister W., Walz J., Zuhl F. and Seemuller E. (1998) The proteasome: paradigm of a self-compartmentalizing protease. Cell 92, 367-380.
9. Bruening W., Roy J., Giasson B., Figlewicz D. A., Mushynski W. E. and Durham H. D. (1999) Up-regulation of protein chaperones preserves viability of cells expressing toxic Cu/Zn-superoxide dismutase mutants associated with amyotrophic lateral sclerosis. J. Neurochem. 72, 693-699.
10. Bruijn L. I., Becher M. W., Lee M. K. et al. (1997) ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 18, 327-338.
11. Casciati A., Ferri A., Cozzolino M., Celsi F., Nencini M., Rotilio G. and Carri M. T. (2002) Oxidative modulation of nuclear factor-kappaB in human cells expressing mutant fALS-typical superoxide dismutases. J. Neurochem. 83, 1019-1029.
12. Cascio P., Call M., Petre B. M., Walz T. and Goldberg A. L. (2002) Properties of the hybrid form of the 26S proteasome containing both 19S and PA28 complexes. EMBO J. 21, 2636-2645.
13. Chiu A. Y., Zhai P., Dal Canto M. C., Peters T. M., Kwon Y. W., Prattis S. M. and Gurney M. E. (1995) Age-dependent penetrance of disease in a transgenic mouse model of familial amyotrophic lateral sclerosis. Mol. Cell. Neurosci. 6, 349-362.
14. Ciechanover A. and Brundin P. (2003) The ubiquitin proteasome system in neurodegenerative diseases. Sometimes the chicken, sometimes the egg. Neuron 40, 427-446.
15. Clement A. M., Nguyen M. D., Roberts E. A., Garcia M. L., Boillee S., Rule M., McMahon A. P., Doucette W., Siwek D., Ferrante R. J. et al. (2003) Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 302, 113-117.
16. Cleveland D. W. and Rothstein J. D. (2001) From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat. Rev. Neurosci. 2, 806-819.
17. Coux O., Tanaka K. and Goldberg A. L. (1996) Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem. 65, 801-847.
18. Dal Canto M. C. and Gurney M. E. (1995) Neuropathological changes in two lines of mice carrying a transgene for mutant human Cu,Zn SOD, and in mice overexpressing wild type human SOD: a model of familial amyotrophic lateral sclerosis (FALS). Brain Res. 676, 25-40.
19. Ding Q., Dimayuga E., Martin S., Bruce-Keller A. J., Nukala V., Cuervo A. M. and Keller J. N. (2003) Characterization of chronic low-level proteasome inhibition on neural homeostasis. J. Neurochem. 86, 489-497.
20. Durham H. D., Roy J., Dong L. and Figlewicz D. A. (1997) Aggregation of mutant Cu/Zn superoxide dismutase proteins in a culture model of ALS. J. Neuropathol Exp Neurol. 56, 523-530.
21. Fang C. H., Li B. G., Fischer D. R., Wang J. J., Runnels H. A., Monaco J. J. and Hasselgren P. O. (2000) Bum injury upregulates the activity and gene expression of the 20 S proteasome in rat skeletal muscle. Clin. Sci. (Lond.) 99, 181-187.
22. Gaczynska M., Goldberg A. L., Tanaka K., Hendil K. B. and Rock K. L. (1996) Proteasome subunits X and Y alter peptidase activities in opposite ways to the interferon-gamma-induced subunits LMP2 and LMP7. J. Biol. Chem. 271, 17275-17280.
23. Glantz S. A. (1997) Primer of Biostatistics. New York, NY: McGraw-Hill Health Profession Division.
24. Goldberg A. L., Cascio P., Saric T. and Rock K. L. (2002) The importance of the proteasome and subsequent proteolytic steps in the generation of antigenic peptides. Mol Immunol. 39, 147-164.
25. Groll M., Heinemeyer W., Jager S., Ulbich T., Bochtler M., Wolf D. H. and Huber R. (1999) The catalytic sites of 20S proteasomes and their role in subunit maturation: a mutational and crystallographic study. Proc. Natl Acad. Sci. USA 96, 10976-10983.
26. Gurney M. E., Pu H., Chiu A. Y., Dal Canto M. C., Polchow C. Y., Alexander D. D., Caliendo J., Hentati A., Kwon Y. W. and Deng H. X. (1994) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264, 1772-1775.
27. Hall E. D., Oostveen J. A. and Gurney M. E. (1998) Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 23, 249-256.
28. Hasselgren P. O., Wray C. and Mammen J. (2002) Molecular regulation of muscle cachexia: it may be more than the proteasome. Biochem. Biophys. Res. Commun. 290, 1-10.
29. Hensley K., Fedynyshyn J., Ferrell S. et al. (2003) Message and protein-level elevation of tumor necrosis factor alpha (TNFalpha) and TNFalpha-modulating cytokines in spinal cords of the G93A-SOD1 mouse model for amyotrophic lateral sclerosis. Neurobiol. Dis 14, 74-80.
30. Hershko A. and Ciechanover A. (1998) The ubiquitin system. Annu. Rev. Biochem. 67, 425-479.
31. Hoffman E. K., Wilcox H. M., Scott R. W. and Siman R. (1996) Proteasome inhibition enhances the stability of mouse Cu/Zn superoxide dismutase with mutations linked to familial amyotrophic lateral sclerosis. J. Neurol. Sci. 139, 15-20.
32. Hyun D. H., Lee M., Hattori N., Kubo S., Mizuno Y., Halliwell B. and Jenner P. (2002a) Effect of wild-type or mutant Parkin on oxidative damage, nitric oxide, antioxidant defenses, and the proteasome. J. Biol. Chem. 277, 28572-28577.
33. Hyun D. H., Lee M. H., Halliwell B. and Jenner P. (2002b) Proteasomal dysfunction induced by 4-hydroxy-2,3-trans-nonenal, an endproduct of lipid peroxidation: a mechanism contributing to neurodegeneration? J. Neurochem. 83, 360-370.
34. Jaarsma D., Rognoni F., van Duijn W., Verspaget H. W., Haasdijk E. D. and Holstege J. C. (2001) CuZn superoxide dismutase (SOD1) accumulates in vacuolated mitochondria in transgenic mice expressing amyotrophic lateral sclerosis-linked SOD1 mutations. Acta Neuropathol. (Berl.) 102, 293-305.
35. Johnston J. A., Dalton M. J., Gurney M. E. and Kopito R. R. (2000) Formation of high molecular weight complexes of mutant Cu,Zn-superoxide dismutase in a mouse model for familial amyotrophic lateral sclerosis. Proc. Natl Acad. Sci. USA 97, 12571-12576.
36. Kato S., Horiuchi S., Liu J. et al. (2000) Advanced glycation endproduct-modified superoxide dismutase-1 (SOD1)-positive inclusions are common to familial amyotrophic lateral sclerosis patients with SOD1 gene mutations and transgenic mice expressing human SOD1 with a G85R mutation. Acta Neuropathol. (Berl.) 100, 490-505.
37. Keller J. N., Huang F. F. and Markesbery W. R. (2000a) Decreased levels of proteasome activity and proteasome expression in aging spinal cord. Neuroscience 98, 149-156.
38. Keller J. N., Huang F. F., Zhu H., Yu J., Ho Y. S. and Kindy T. S. (2000b) Oxidative stress-associated impairment of proteasome activity during ischemia-reperfusion injury. J. Cereb. Blood Flow Metab. 20, 1467-1473.
39. Kopito R. R. (2000) Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 10, 524-530.
40. Lee M., Hyun D. H., Marshall K. A., Ellerby L. M., Bredesen D. E., Jenner P. and Halliwell B. (2001) Effect of oyerexpression of Bcl-2 on cellular oxidative damage, nitric oxide production, antioxidant defenses, and the proteasome. Free Radic. Biol. Med. 31, 1550-1559.
41. Lino M. M., Schneider C. and Caroni P. (2002) Accumulation of SOD1 mutants in postnatal motoneurons does not cause motoneuron pathology or motoneuron disease. J. Neurosci. 22, 4825-4832.
42. McNaught K. S., Olanow C. W., Halliwell B., Isacson O. and Jenner P. (2001) Failure of the ubiquitin-proteasome system in Parkinson's disease. Nat. Rev. Neurosci. 2, 589-594.
43. Medina R., Wing S. S. and Goldberg A. L. (1995) Increase in levels of polyubiquitin and proteasome mRNA in skeletal muscle during starvation and denervation atrophy. Biochem. J. 307, 631-637.
44. Mengual E., Arizti P., Rodrigo J., Gimenez-Amaya J. M. and Castano J. G. (1996) Immunohistochemical distribution and electron microscopic subcellular localization of the proteasome in the rat CNS. J. Neurosci. 16, 6331-6341.
45. Niwa J., Ishigaki S., Hishikawa N., Yamamoto M., Doyu M., Murata S., Tanaka K., Taniguchi N. and Sobue G. (2002) Dorfin ubiquitylates mutant SOD1 and prevents mutant SOD1-mediated neurotoxicity. J. Biol. Chem. 277, 36793-36798.
46. Pramatarova A., Laganiere J., Roussel J., Brisebois K. and Rouleau G. A. (2001) Neuron-specific expression of mutant superoxide dismutase 1 in transgenic mice does not lead to motor impairment. J. Neurosci. 21, 3369-3374.
47. Preckel T., Fung-Leung W. P., Cai Z. et al. (1999) Impaired immunoproteasome assembly and immune responses in PA28-/- mice. Science 286, 2162-2165.
48. Puttaparthi K., Wojcik C., Rajendran B., DeMartino G. N. and Elliott J. L. (2003) Aggregate formation in the spinal cord of mutant SOD1 transgenic mice is reversible and mediated by proteasomes. J. Neurochem. 87, 851-860.
49. Rock K. L. and Goldberg A. L. (1999) Degradation of cell proteins and the generation of MHC class I-presented peptides. Annu. Rev. Immunol. 17, 739-779.
50. Rock K. L., Gramm C., Rothstein L., Clark K., Stein R., Dick L., Hwang D. and Goldberg A. L. (1994) Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78, 761-771.
51. Rosen D. R., Siddique T., Patterson D., Figlewicz D. A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J. P. and Deng H. X., (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362, 59-62.
52. Sherman M. Y. and Goldberg A. L. (2001) Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases. Neuron 29, 15-32.
53. Shibata N., Asayama K., Hirano A. and Kobayashi M. (1996) Immunohistochemical study on superoxide dismutases in spinal cords from autopsied patients with amyotrophic lateral sclerosis. Dev. Neurosci. 18, 492-498.
54. Shinder G. A., Lacourse M. C., Minotti S. and Durham H. D. (2001) Mutant Cu/Zn-superoxide dismutase proteins have altered solubility and interact with heat shock/stress proteins in models of amyotrophic lateral sclerosis. J. Biol. Chem. 276, 12791-12796.
55. Sidman R. L., Angevine J. B. and Pierce E. T. (1971) Atlas of the mouse brain and spinal cord. Cambridge, MA: Harvard UP.
56. Stieber A., Gonatas J. O. and Gonatas N. K. (2000) Aggregation of ubiquitin and a mutant ALS-linked SOD1 protein correlate with disease progression and fragmentation of the Golgi apparatus. J. Neurol. Sci. 173, 53-62.
57. Urushitani M., Kurisu J., Tsukita K. and Takahashi R. (2002) Proteasomal inhibition by misfolded mutant superoxide dismutase 1 induces selective motor neuron death in familial amyotrophic lateral sclerosis. J. Neurochem. 83, 1030-1042.
58. Valentine J. S. and Hart P. J. (2003) Bioinorganic chemistry special feature: misfolded CuZnSOD and amyotrophic lateral sclerosis. Proc. Natl Acad. Sci. USA 100, 3617-3622.
59. Wang J., Xu G. and Borchelt D. R. (2002) High molecular weight complexes of mutant superoxide dismutase 1: age-dependent and tissue-specific accumulation. Neurobiol. Dis. 9, 139-148.
60. Watanabe M., Dykes-Hoberg M., Culotta V. C., Price D. L., Wong P. C. and Rothstein J. D. (2001) Histological evidence of protein aggregation in mutant SOD1 transgenic mice and in amyotrophic lateral sclerosis neural tissues. Neurobiol. Dis. 8, 933-941.
61. Wing S. S., Haas A. L. and Goldberg A. L. (1995) Increase in ubiquitin-protein conjugates concomitant with the increase in proteolysis in rat skeletal muscle during starvation and atrophy denervation. Biochem. J. 307, 639-645.