Proteasomes remain intact, but show early focal alteration in their composition in a mouse model of amyotrophic lateral sclerosis

Journal of Neurochemistry

Volumn 105, Issue 6, 2008, Pages 2353-2366

  Kabashi, Edor ^a   Agar, Jeffrey N ^a,c   Hong, Yu ^b   Taylor, David M ^a   Minotti, Sandra ^a   Figlewicz, Denise A ^b   Durham, Heather D ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c BRANDEIS UNIVERSITY   (United States)

Author keywords

Cu Zn superoxide dismutase; Cu Zn superoxide dismutase 1; Motor neuron disease; Protein aggregation; Proteolysis; Ubiquitin proteasome pathway

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; HEAT SHOCK PROTEIN 70; MESSENGER RNA; PROTEASOME; PROTEIN SUBUNIT;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; GEL ELECTROPHORESIS; GENE SEQUENCE; IMMUNOREACTIVITY; LASER CAPTURE MICRODISSECTION; LUMBAR SPINAL CORD; MOTONEURON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UBIQUITINATION;

ALANINE; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; DISEASE MODELS, ANIMAL; GLYCINE; HUMANS; MICE; MICE, TRANSGENIC; PROTEASOME ENDOPEPTIDASE COMPLEX; SPINAL CORD; SUPEROXIDE DISMUTASE; UBIQUITINATION;

MUS; MUS MUSCULUS;

EID: 44649144579     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05317.x     Document Type: Article

References (64)

1. Alexianu M. E., Kozovska M. Appel S. H. (2001) Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology 57, 1282 1289.
2. Basso M., Massignan T., Samengo G., Cheroni C., De Biasi S., Salmona M., Bendotti C. Bonetto V. (2006) Insoluble mutant SOD1 is partly oligoubiquitinated in amyotrophic lateral sclerosis mice. J. Biol. Chem. 281, 33325 33335.
3. Batulan Z., Shinder G. A., Minotti S., He B. P., Doroudchi M. M., Nalbantoglu J., Strong M. J. 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.
4. Baumeister W., Walz J., Zuhl F. Seemüller E. (1998) The proteasome: paradigm of a self-compartmentalizing protease. Cell 92, 367 380.
5. Bence N. F., Sampat R. M. Kopito R. R. (2001) Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292, 1552 1555.
6. Bennett E. J., Bence N. F., Jayakumar R. Kopito R. R. (2005) Global impairment of the ubiquitin-proteasome system by nuclear or cytoplasmic protein aggregates precedes inclusion body formation. Mol. Cell 17, 351 365.
7. Boillee S., Yamanaka K., Lobsiger C. S., Copeland N. G., Jenkins N. A., Kassiotis G., Kollias G. Cleveland D. W. (2006) Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312, 1389 1392.
8. 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.
9. Bruijn L. I., Miller T. M. Cleveland D. W. (2004) Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 27, 723 749.
10. Bulteau A. L., Petropoulos I. Friguet B. (2000) Age-related alterations of proteasome structure and function in aging epidermis. Exp. Gerontol. 35, 767 777.
11. Bulteau A. L., Lundberg K. C., Humphries K. M., Sadek H. A., Szweda P. A., Friguet B. Szweda L. I. (2001) Oxidative modification and inactivation of the proteasome during coronary occlusion/reperfusion. J. Biol. Chem. 276, 30057 30063.
12. Camacho-Carvajal M. M., Wollscheid B., Aebersold R., Steimle V. Schamel W. W. (2004) Two-dimensional blue native/SDS gel electrophoresis of multi-protein complexes from whole cellular lysates: a proteomics approach. Mol. Cell Proteomics 3, 176 182.
13. Carrard G., Dieu M., Raes M., Toussaint O. Friguet B. (2003) Impact of ageing on proteasome structure and function in human lymphocytes. Int. J. Biochem. Cell Biol. 35, 728 739.
14. Cheroni C., Peviani M., Cascio P., Debiasi S., Monti C. Bendotti C. (2005) Accumulation of human SOD1 and ubiquitinated deposits in the spinal cord of SOD1G93A mice during motor neuron disease progression correlates with a decrease of proteasome. Neurobiol. Dis. 18, 509 522.
15. Chiu A. Y., Zhai P., Dal Canto M. C., Peters T. M., Kwon Y. W., Prattis S. M. 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.
16. Chondrogianni N., Stratford F. L., Trougakos I. P., Friguet B., Rivett A. J. Gonos E. S. (2003) Central role of the proteasome in senescence and survival of human fibroblasts: induction of a senescence-like phenotype upon its inhibition and resistance to stress upon its activation. J. Biol. Chem. 278, 28026 28037.
17. Chondrogianni N., Tzavelas C., Pemberton A. J., Nezis I. P., Rivett A. J. Gonos E. S. (2005) Overexpression of proteasome beta5 assembled subunit increases the amount of proteasome and confers ameliorated response to oxidative stress and higher survival rates. J. Biol. Chem. 280, 11840 11850.
18. Ciechanover A. (2005) N-terminal ubiquitination. Methods Mol. Biol. 301, 255 270.
19. Ciechanover A. Brundin P. (2003) The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 40, 427 446.
20. Cleveland D. W. Rothstein J. D. (2001) From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat. Rev. Neurosci. 2, 806 819.
21. Dal Canto M. C. 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.
22. Dantuma N. P., Lindsten K., Glas R., Jellne M. Masucci M. G. (2000) Short-lived green fluorescent proteins for quantifying ubiquitin/proteasome- dependent proteolysis in living cells. Nat. Biotechnol. 18, 538 543.
23. DeMartino G. N. Slaughter C. A. (1999) The proteasome, a novel protease regulated by multiple mechanisms. J. Biol. Chem. 274, 22123 22126.
24. Di Giorgio F. P., Carrasco M. A., Siao M. C., Maniatis T. Eggan K. (2007) Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat. Neurosci. 10, 608 614.
25. Di Noto L., Whitson L. J., Cao X., Hart P. J. Levine R. L. (2005) Proteasomal degradation of mutant superoxide dismutases linked to amyotrophic lateral sclerosis. J. Biol. Chem. 280, 39907 39913.
26. Durham H. D., Roy J., Dong L. 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.
27. Elsasser S., Schmidt M. Finley D. (2005) Characterization of the proteasome using native gel electrophoresis. Methods Enzymol. 398, 353 363.
28. Farout L., Mary J., Vinh J., Szweda L. I. Friguet B. (2006) Inactivation of the proteasome by 4-hydroxy-2-nonenal is site specific and dependant on 20S proteasome subtypes. Arch. Biochem. Biophys. 453, 435 442.
29. Furukawa Y. O'Halloran T. V. (2005) Amyotrophic lateral sclerosis mutations have the greatest destabilizing effect on the apo- and reduced form of SOD1, leading to unfolding and oxidative aggregation. J. Biol. Chem. 280, 17266 17274.
30. Gaczynska M., Rock K. L., Spies T. Goldberg A. L. (1994) Peptidase activities of proteasomes are differentially regulated by the major histocompatibility complex-encoded genes for LMP2 and LMP7. Proc. Natl Acad. Sci. USA 91, 9213 9217.
31. Groettrup M., Khan S., Schwarz K. Schmidtke G. (2001) Interferon-gamma inducible exchanges of 20S proteasome active site subunits: why? Biochimie 83, 367 372.
32. Grune T., Jung T., Merker K. Davies K. J. (2004) Decreased proteolysis caused by protein aggregates, inclusion bodies, plaques, lipofuscin, ceroid, and 'aggresomes' during oxidative stress, aging, and disease. Int. J. Biochem. Cell Biol. 36, 2519 2530.
33. Hall E. D., Oostveen J. A. 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.
34. Hart P. J. (2006) Pathogenic superoxide dismutase structure, folding, aggregation and turnover. Curr. Opin. Chem. Biol. 10, 131 138.
35. Hoffman E. K., Wilcox H. M., Scott R. W. 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.
36. Johnston J. A., Dalton M. J., Gurney M. E. 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.
37. Kabashi E. Durham H. D. (2006) Failure of protein quality control in amyotrophic lateral sclerosis. Biochim. Biophys. Acta 1762, 1038 1050.
38. Kabashi E., Agar J. N., Taylor D. M., Minotti S. Durham H. D. (2004) Focal dysfunction of the proteasome: a pathogenic factor in a mouse model of amyotrophic lateral sclerosis. J. Neurochem. 89, 1325 1335.
39. 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.
40. Keller J. N., Huang F. F. Markesbery W. R. (2000) Decreased levels of proteasome activity and proteasome expression in aging spinal cord. Neuroscience 98, 149 156.
41. Kriz J., Nguyen M. D. Julien J. P. (2002) Minocycline slows disease progression in a mouse model of amyotrophic lateral sclerosis. Neurobiol. Dis. 10, 268 278.
42. Li L., Zhang X. Le W. (2008) Altered macroautophagy in the spinal cord of SOD1 mutant mice. Autophagy 4, 290 293.
43. Matsumoto G., Stojanovic A., Holmberg C. I., Kim S. Morimoto R. I. (2005) Structural properties and neuronal toxicity of amyotrophic lateral sclerosis-associated Cu/Zn superoxide dismutase 1 aggregates. J. Cell Biol. 171, 75 85.
44. Miyazaki K., Fujita T., Ozaki T. et al. (2004) NEDL1, a novel ubiquitin-protein isopeptide ligase for dishevelled-1, targets mutant superoxide dismutase-1. J. Biol. Chem. 279, 11327 11335.
45. Morimoto N., Nagai M., Ohta Y. et al. (2007) Increased autophagy in transgenic mice with a G93A mutant SOD1 gene. Brain Res. 1167, 112 117.
46. Nagai M., Re D. B., Nagata T., Chalazonitis A., Jessell T. M., Wichterle H. Przedborski S. (2007) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat. Neurosci. 10, 615 622.
47. Niwa J., Ishigaki S., Hishikawa N., Yamamoto M., Doyu M., Murata S., Tanaka K., Taniguchi N. Sobue G. (2002) Dorfin ubiquitylates mutant SOD1 and prevents mutant SOD1-mediated neurotoxicity. J. Biol. Chem. 277, 36793 36798.
48. Pedersen W. A., Fu W., Keller J. N., Markesbery W. R., Appel S., Smith R. G., Kasarskis E. Mattson M. P. (1998) Protein modification by the lipid peroxidation product 4-hydroxynonenal in the spinal cords of amyotrophic lateral sclerosis patients. Ann. Neurol. 44, 819 824.
49. Perluigi M., Fai Poon H., Hensley K., Pierce W. M., Klein J. B., Calabrese V., De Marco C. Butterfield D. A. (2005) Proteomic analysis of 4-hydroxy-2-nonenal-modified proteins in G93A-SOD1 transgenic mice - a model of familial amyotrophic lateral sclerosis. Free Radic. Biol. Med. 38, 960 968.
50. Poon H. F., Hensley K., Thongboonkerd V., Merchant M. L., Lynn B. C., Pierce W. M., Klein J. B., Calabrese V. Butterfield D. A. (2005) Redox proteomics analysis of oxidatively modified proteins in G93A-SOD1 transgenic mice - a model of familial amyotrophic lateral sclerosis. Free Radic. Biol. Med. 39, 453 462.
51. Puttaparthi K. Elliott J. L. (2005) Non-neuronal induction of immunoproteasome subunits in an ALS model: possible mediation by cytokines. Exp. Neurol. 196, 441 451.
52. Puttaparthi K., Wojcik C., Rajendran B., DeMartino G. N. 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.
53. Rosen D. R., Siddique T., Patterson D. et al. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362, 59 62.
54. Rubinsztein D. C. (2006) The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 443, 780 786.
55. Shaw B. F. Valentine J. S. (2007) How do ALS-associated mutations in superoxide dismutase 1 promote aggregation of the protein? Trends Biochem. Sci. 32, 78 85.
56. Shinder G. A., Lacourse M. C., Minotti S. 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.
57. Taylor D. M., Gibbs B. F., Kabashi E., Minotti S., Durham H. D. Agar J. N. (2007) Tryptophan 32 potentiates aggregation and cytotoxicity of a copper/zinc superoxide dismutase mutant associated with familial amyotrophic lateral sclerosis. J. Biol. Chem. 282, 16329 16335.
58. Urushitani M., Kurisu J., Tsukita K. 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.
59. Urushitani M., Kurisu J., Tateno M., Hatakeyama S., Nakayama K., Kato S. Takahashi R. (2004) CHIP promotes proteasomal degradation of familial ALS-linked mutant SOD1 by ubiquitinating Hsp/Hsc70. J. Neurochem. 90, 231 244.
60. Vargas M. R., Pehar M., Cassina P., Beckman J. S. Barbeito L. (2006) Increased glutathione biosynthesis by Nrf2 activation in astrocytes prevents p75NTR-dependent motor neuron apoptosis. J. Neurochem. 97, 687 696.
61. Wang J., Xu G. Borchelt D. R. (2002) High molecular weight complexes of mutant superoxide dismutase 1: age-dependent and tissue-specific accumulation. Neurobiol. Dis. 9, 139 148.
62. Wang J., Xu G., Slunt H. H., Gonzales V., Coonfield M., Fromholt D., Copeland N. G., Jenkins N. A. Borchelt D. R. (2005) Coincident thresholds of mutant protein for paralytic disease and protein aggregation caused by restrictively expressed superoxide dismutase cDNA. Neurobiol. Dis. 20, 943 952.
63. Watanabe M., Dykes-Hoberg M., Culotta V. C., Price D. L., Wong P. C. 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.
64. Zetterstrom P., Stewart H. G., Bergemalm D., Jonsson P. A., Graffmo K. S., Andersen P. M., Brannstrom T., Oliveberg M. Marklund S. L. (2007) Soluble misfolded subfractions of mutant superoxide dismutase-1s are enriched in spinal cords throughout life in murine ALS models. Proc. Natl Acad. Sci. USA 104, 14157 14162.