Partial inhibition of proteasome activity enhances remyelination after cuprizone-induced demyelination

Experimental Neurology

Volumn 217, Issue 2, 2009, Pages 282-296

  Millet, V ^a   Moiola, C P ^a   Pasquini, J M ^a   Soto, E F ^a   Pasquini, L A ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Cuprizone; Demyelination; Lactacystin; Microglial activation; Mitochondrial respiratory chain activities; NF B; Oligodendroglial differentiation; Proteasome; Remyelination

Indexed keywords

CUPRIZONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LACTACYSTIN; PROTEASOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; CONVALESCENCE; CORPUS CALLOSUM; CYTOKINE RELEASE; DEMYELINATION; ENZYME ACTIVITY; MALE; MICROGLIA; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REMYELINIZATION; RESPIRATORY CHAIN; THERAPY EFFECT; TREATMENT OUTCOME; TREATMENT RESPONSE;

ACETYLCYSTEINE; ANIMALS; CORPUS CALLOSUM; CUPRIZONE; CYSTEINE PROTEINASE INHIBITORS; DEMYELINATING DISEASES; DISEASE MODELS, ANIMAL; GLIOSIS; MALE; MICE; MYELIN SHEATH; NERVE FIBERS, MYELINATED; NERVE REGENERATION; NEUROTOXINS; NF-KAPPA B; PROTEASOME ENDOPEPTIDASE COMPLEX; TREATMENT OUTCOME;

EID: 67349144098     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2009.03.005     Document Type: Article

References (63)

1. Arnett H., Mason J., Marino M., Suzuki K., Matsushima G.K., and Ting J.P. TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat. Neurosci. 4 (2001) 1116-1122
2. Baldwin A.S. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu. Rev. Immunol. 14 (1996) 649-683
3. Barnes P.J., and Karin M. Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N. Engl. J. Med. 336 (1997) 1066-1071
4. Berti R., Williams A., Velarde L., Moffett J., Elliott P., Adams J., Yao C., Dave J., and Tortella F. Effect of the proteasome inhibitor MLN519 on the expression of inflammatory molecules following middle cerebral artery occlusion and reperfusion in the rat. Neurotox. Res. 5 7 (2003) 505-514
5. Beyette J., Mason G.G., Murray R.Z., Cohen G.M., and Rivett A.J. Proteasome activities decrease during dexamethasone-induced apoptosis of thymocytes. Biochem. J. 332 (1998) 315-320
6. Bjartmar C., Wujek J.R., and Trapp B.D. Axonal loss in the pathology of MS: consequences for understanding the progressive phase of the disease. J. Neurol. Sci. 206 (2003) 165-171
7. Blakemore W. Observations on oligodendrocyte degeneration, the resolution of status spongiosus and remyelination in cuprizone intoxication in mice. J. Neurocytol. 1 (1972) 413-426
8. Blakemore W. Remyelination of the superior cerebellar peduncle in the mouse following demyelination induced by feeding cuprizone. J. Neurol. Sci. 20 (1973) 73-83
9. Calatayud C., García C., Paez P., Soto E., Pasquini J., and Pasquini L.A. A decrease in proteasome activity induces an enhanced activation of the myelin basic protein promoter. Dev. Neurosci. (2009) 10.1159/000193393 Published online
10. Cammer W., Zhang H., and Tansey F.A. Effects of carbonic anhydrase II (CAII) deficiency on CNS structure and function in the myelin-deficient CAII-deficient double mutant mouse. J. Neurosci. Res. 40 (1995) 451-457
11. Canoll P.D., Musacchio J.M., Hardy R., Reynolds R., Marchionni M.A., and Salzer J.L. GGF/neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits the differentiation of oligodendrocyte progenitors. Neuron 17 (1996) 229-243
12. Chadwick W., Magnus T., Martin B., Keselman A., Mattson M., and Stuart M. Targeting TNF-α receptors for neurotherapeutics. Trends Neurosci. 31 10 (2008) 504-511
13. Chen P.S., Toribara T., and Warnwr H. Microdetermination of phosphorus. Anal. Chem. 28 (1956) 1756-1758
14. De Robertis E.D.F., Pellegrino de Iraldi A., Rodriguez de Lorez Arnaiz G., and Salganicoff L. Cholinergic and noncholinergic nerve ending in rat brain. J. Neurochem. 9 (1962) 23-35
15. Di Napoli M., and Papa F. The proteasome system and proteasome inhibitors in stroke: controlling the inflammatory response. Curr. Opin. Investig. Drugs 4 (2003) 1333-1342
16. Elliott P.J., Pien C.S., McCormack T.A., Chapman I.D., and Adams J. Proteasome inhibition: a novel mechanism to combat asthma. J. Allergy Clin. Immunol. 104 (1999) 294-300
17. Flann S., Hawkes R.B., Riederer B.M., Rider C.C., and Beesley P.W. Changes in ubiquitin immunoreactivity in developing rat brain: a putative role for ubiquitin and ubiquitin conjugates in dendritic outgrowth and differentiation. Neuroscience 81 (1997) 18-173
18. Folch J., Lees M., and Sloane Stanley G.H. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226 (1957) 497-509
19. Fujita N., Ishiguro H., Sato S., Kurihara T., Kuwano R., Sakimura K., Takahashi Y., and Miyatake T. Induction of myelin-associated glycoprotein mRNA in experimental remyelination. Brain Res. 513 (1990) 152-155
20. Goldbaum O., Vollmer G., and Richter-Landsberg C. Proteasome inhibition by MG-132 induces apoptotic cell death and mitochondrial dysfunction in cultured rat brain oligodendrocytes but not in astrocytes. Glia 53 (2006) 891-901
21. Goldberg A.L., Akopain T.N., Kisselev A.F., Lee D.H., and Rohrwild M. New insights into the mechanisms and importance of the proteasome in intracellular protein degradation. Biol. Chem. 378 (1997) 131-140
22. Goossens V., Grooten J., De Vos K., and Fiers W. Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 8115-8119
23. Grilli M., Chiu J.J., and Lenardo M.J. NF-kappa B and Rel: participants in a multiform transcriptional regulatory system. Int. Rev. Cytol. 143 (1993) 1-62
24. Hiremath M.M., Saito Y., Knapp G.W., Ting J.P., Suzuki K., and Matsushima G.K. Microglial/macrophage accumulation during cuprizone-induced demyelination in C57BL/6 mice. J. Neuroimmunol. 92 (1998) 38-49
25. Hosseini H., Andre P., Lefevre N., Viala L., Walzer T., Peschanski M., and Lotteau V. Protection against experimental autoimmune encephalomyelitis by a proteasome modulator. J. Neuroimmunol. 118 (2001) 233-244
26. Komoly S., Jeyasingham M.D., Pratt O.E., and Lantos P.L. Decrease in oligodendrocyte carbonic anhydrase activity preceding myelin degeneration in cuprizone induced demyelination. J. Neurol. Sci. 78 (1987) 125-137
27. Komoly S. Experimental demyelination caused by primary oligodendrocyte distrophy. Clin. Neurosci. 58 (2005) 40-43
28. Lapetina E., Soto E.F., and de Robertis E. Lipids and proteolipids in isolated subcellular membranes of rat brain cortex. J. Neurochem. 15 (1968) 437-445
29. Lewin E., and Hess H.H. Intralaminar distribution of cerebrosides in human frontal cortex. J. Neurochem. 12 (1965) 213-220
30. Ludwin S.K. Central nervous system demyelination and remyelination in the mouse: an ultrastructural study of cuprizone toxicity. Lab. Invest. 39 (1978) 597-612
31. Matsushima G.K., and Morell P. The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol. 11 (2001) 107-116
32. McKinnon R.D., Matsui T., Dubois-Dalcq M., and Aaronson S.A. FGF modulates the PDGF-driven pathway of oligodendrocyte development. Neuron 5 (1990) 603-614
33. McMorris F.A., Mozell R.L., Carson M.J., Shinar Y., Meyer R.D., and Marchetti N. Regulation of oligodendrocyte development and central nervous system myelination by insulin-like growth factors. Ann. N. Y. Acad. Sci. 27 (1993) 321-334
34. Meng L., Mohan R., Kwok B.H., Elofsson M., Sin N., and Crews C.M. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 10403-10408
35. Morais Cardoso S., Pereira C., and Resende Oliveira C. Mitochondrial function is differentially affected upon oxidative stress. Free Radic. Biol. Med. 26 (1999) 3-13
36. Morell P., Barrett C.V., Mason J.L., Toews A.D., Hostettler J.D., Knapp G.W., and Matsushima G.K. Gene expression in the brain during cuprizone-induced demyelination and remyelination. Mol. Cell Neurosci. 12 (1998) 220-227
37. Muratani M., and Tansey W.P. How the ubiquitin-proteasome system controls transcription. Nat. Rev. Mol. Cell Biol. 4 (2003) 192-201
38. Noble M., Murray K., Stroobant P., Waterfield M.D., and Riddle P. Platelet derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte type-2 astrocyte progenitor cell. Nature 333 (1988) 560-562
39. Norton W.T., and Poduslo S.E. Myelination in rat brain: method of myelin isolation. J. Neurochem. 21 (1973) 749-757
40. Obin M., Mesco E., Gong X., Haas A.L., Joseph J., and Taylor A. Neurite outgrowth in PC12 cells: distinguishing the roles of ubiquitylation and ubiquitin-dependent proteolysis. J. Biol. Chem. 274 (1999) 1-11789
41. Oberhammer F., Fritsch G., Schmied M., Pavelka M., Printz D., Purchio T., Lassmann H., and Schulte-Hermann R. Condensation of the chromatin at the membrane of an apoptotic nucleus is not associated with activation of an endonuclease. J. Cell Sci. 104 (1993) 317-326
42. Palombella V.J., Conner E.M., Fuseler J.W., Destree A., Davis J.M., Laroux F.S., Wolf R.E., Huang J., Brand S., Elliott P.J., Lazarus D., McCormack T., Parent L., Stein R., Adams J., and Grisham M.B. Role of the proteasome and NF-kappaB in streptococcal cell wall-induced polyarthritis. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 15671-15676
43. Pasquini L.A., Calatayud C.A., Bertone Uña A.L., Millet V., Pasquini J.M., and Soto E.F. The neurotoxic effect of cuprizone on oligodendrocytes depends on the presence of pro-inflammatory cytokines secreted by microglia. Neurochem. Res. 32 (2007) 279-292
44. Pasquini L.A., Besio Moreno M., Adamo A.M., Pasquini J.M., and Soto E. Lactacystin, a specific inhibitor of the proteasome induces apoptosis and activates CPP32, in cultured cerebellar granular cells. J. Neurosci. Res. 59 (2000) 601-611
45. Pasquini L.A., Besio Moreno M., Lopez Salon M., and Soto E.F. Apoptosis in Schwann cell cultures is closely interrelated with the activity of the ubiquitin-proteasome proteolytic pathway. Neurochem. Res. 27 (2002) 1401-1419
46. Pasquini L.A., Paez P., Besio Moreno M., Pasquini J.M., and Soto E.F. Inhibition of the proteasome by lactacystin enhances oligodendroglial cell differentiation. J. Neurosci. 23 (2003) 4635-4644
47. Pfeiffer S.E., Warrington A.E., and Bansal R. The oligodendrocyte and its many cellular processes. Trends Cell Biol. 3 (1993) 191-197
48. Qui J.H., Asai A., Chi S., Saito N., Hamada H., and Kirino T. Proteasome inhibitors induce cytochrome c-caspase-3-like protease-mediated apoptosis in cultured cortical neurons. J. Neurosci. 20 (2000) 259-265
49. Raff M.C., Lillien L.E., Richardson W.D., Burne J.F., and Noble M.D. Platelet-derived growth factor from astrocytes drives the clock that times oligodendrocyte development in culture. Nature 9 (1988) 562-565
50. Read M.A., Neish A.S., Luscinskas F.W., Palombella V.J., Maniatis T., and Collins T. The proteasome pathway is required for cytokine-induced endothelial-leukocyte adhesion molecule expression. Immunity 2 (1995) 493-506
51. Richardson W.D., Pringle N., Mosley M.J., Westermark B., and Dubois-Dalcq M. A role for platelet-derived growth factor in normal gliogenesis in the central nervous system. Cell 22 (1988) 309-319
52. Searcy R.L., and Bergquist L.M. Fluorescent detection of serum lipoproteins. Clin. Chim. Acta 5 (1960) 941-942
53. Shah M.H., Young D., Kindler H.L., Webb I., Kleiber B., Wright J., and Grever M. Phase II study of the proteasome inhibitor bortezomib (PS-341) in patients with metastatic neuroendocrine tumors. Clin. Cancer Res. 10 (2004) 6111-6118
54. Shih A., Fernandes H., Choi F., Kozoriz M., Liu Y., Li P., Cowan C., and Klegeris A. Policing the police: astrocytes modulate microglial activation. J. Neurosci. 26 15 (2006) 3887-3888
55. Suzuki K. Giant hepatic mitochondria: production in mice fed with cuprizone. Science 163 (1969) 81-82
56. Suzuki K., and Kikkawa Y. Status spongiosus of CNS and hepatic changes induced by cuprizone (biscyclohexanone oxalyldihydrazone). Am. J. Pathol. 54 (1969) 307-325
57. Vanderlugt C.L., Rahbe S.M., Elliott P.J., Dal Canto M.C., and Miller S.D. Treatment of established relapsing experimental autoimmune encephalomyelitis with the proteasome inhibitor PS-519. J. Autoimmun. 14 (2000) 205-211
58. Varshavsky A. The ubiquitin system. Trends Biochem. Sci. 22 (1997) 383-387
59. Venturini G. Enzymic activities and sodium, potassium and copper concentrations in mouse brain and liver after cuprizone treatment in vivo. J. Neurochem. 21 (1973) 1147-1151
60. Watts R.J., Hoopfer E.D., and Luo L. Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 38 (2003) 871-885
61. Wojcik C., and Di Napoli M. Ubiquitin-proteasome system and proteasome inhibition: new strategies in stroke therapy. Stroke 35 (2004) 1506-1518
62. Wojcik C., and Wilk S. Changes in proteasome expression and activity during differentiation of neuronal precursor NTera 2 clone D1 cells. Neurochem. Int. 34 (1999) 131-136
63. Zhai Q., Wang J., Kim A., Liu Q., Watts R., Hoopfer E., Mitchison T., Luo L., and He Z. Involvement of the ubiquitin-proteasome system in the early stages of Wallerian degeneration. Neuron 17 (2003) 217-225