Inhibition of p53 transcriptional activity: A potential target for future development of therapeutic strategies for primary demyelination

Journal of Neuroscience

Volumn 28, Issue 24, 2008, Pages 6118-6127

  Li, Jiadong ^a   Ghiani, Cristina A ^b   Jin, Young Kim ^a   Liu, Aixiao ^a   Sandoval, Juan ^a   DeVellis, Jean ^b   Casaccia Bonnefil, Patrizia ^a,c  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Demyelination; Microglia; Myelin; Myelin repair; Oligodendrocyte; Transcription

Indexed keywords

CUPRIZONE; LIPOPOLYSACCHARIDE; MYELIN; PIFITHRIN ALPHA; PROTEIN P53; TRANSCRIPTION FACTOR SOX2; BENZOTHIAZOLE DERIVATIVE; DRUG DERIVATIVE; ENZYME INHIBITOR; PIFITHRIN; TOLUENE;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTINUOUS INFUSION; CONTROLLED STUDY; CORPUS CALLOSUM; DEMYELINATION; DRUG EFFECT; DRUG MECHANISM; GENE EXPRESSION PROFILING; GENE LOSS; IN VITRO STUDY; IN VIVO STUDY; MALE; MICROGLIA; MOUSE; MYELINATED NERVE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; TRANSCRIPTION TERMINATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CHEMICALLY INDUCED DISORDER; CYTOLOGY; DEMYELINATING DISEASE; DISEASE MODEL; DNA MICROARRAY; GENETIC TRANSCRIPTION; GENETICS; LATERAL BRAIN VENTRICLE; METABOLISM; METHODOLOGY; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY;

ANIMALS; BENZOTHIAZOLES; CELLS, CULTURED; CUPRIZONE; DEMYELINATING DISEASES; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; LATERAL VENTRICLES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; OLIGODENDROGLIA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TOLUENE; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 46749090850     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0184-08.2008     Document Type: Article

References (48)

1. Aboul-Enein F, Rauschka H, Kornek B, Stadelmann C, Stefferl A, Bruck W, Lucchinetti C, Schmidbauer M, Jellinger K, Lassmann H (2003) Preferential loss of myelin-associated glycoprotein reflects hypoxia-like white matter damage in stroke and inflammatory brain diseases. J Neuropathol Exp Neurol 62:25-33.
2. Barnett MH, Prineas JW (2004) Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann Neurol 55:458-468.
3. Ben-Hur T, Rogister B, Murray K, Rougon G, Dubois-Dalcq M (1998) Growth and fate of PSA-NCAM+ precursors of the postnatal brain. J Neurosci 18:5777-5788.
4. Billon N, Terrinoni A, Jolicoeur C, McCarthy A, Richardson WD, Melino G, Raff M (2004) Roles for p53 and p73 during oligodendrocyte development. Development 131:1211-1220.
5. Blasi E, Barluzzi R, Bocchini V, Mazzolla R, Bistoni F (1990) Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus. J Neuroimmunol 27:229-237.
6. Carson MJ (2002) Microglia as liaisons between the immune and central nervous systems: functional implications for multiple sclerosis. Glia 40:218-231.
7. Culmsee C, Zhu X, Yu QS, Chan SL, Camandola S, Guo Z, Greig NH, Mattson MP (2001) A synthetic inhibitor of p53 protects neurons against death induced by ischemic and excitotoxic insults, and amyloid beta-peptide. J Neurochem 77:220-228.
8. Decker L, Avellana-Adalid V, Nait-Oumesmar B, Durbec P, Baron-Van Evercooren A (2000) Oligodendrocyte precursor migration and differentiation: combined effects of PSA residues, growth factors, and substrates. Mol Cell Neurosci 16:422-439.
9. Dijsselbloem N, Goriely S, Albarani V, Gerlo S, Francoz S, Marine JC, Goldman M, Haegeman G, Vanden Berghe W (2007) A critical role for p53 in the control of NF-kappaB-dependent gene expression in TLR4-stimulated dendritic cells exposed to Genistein. J Immunol 178:5048-5057.
10. Donehower LA (1996) The p53-deficient mouse: a model for basic and applied cancer studies. Semin Cancer Biol 7:269 -278.
11. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery Jr CA, Butel JS, Bradley A (1992) Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356:215-221.
12. Dougherty KD, Dreyfus CF, Black IB (2000) Brain-derived neurotrophic factor in astrocytes, oligodendrocytes, and microglia/macrophages after spinal cord injury. Neurobiol Dis 7:574 585.
13. Du Y, Fischer TZ, Lee LN, Lercher LD, Dreyfus CF (2003) Regionally specific effects of BDNF on oligodendrocytes. Dev Neurosci 25:116-126.
14. Garden GA, Guo W, Jayadev S, Tun C, Balcaitis S, Choi J, Montine TJ, Moller T, Morrison RS (2004) HIV associated neurodegeneration requires p53 in neurons and microglia. FASEB J 18:1141-1143.
15. Giaccia AJ, Kastan MB (1998) The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev 12:2973-2983.
16. Gil-Perotin S, Marin-Husstege M, Li J, Soriano-Navarro M, Zindy F, Roussel MF, Garcia-Verdugo JM, Casaccia-Bonnefil P (2006) Loss of p53 induces changes in the behavior of subventricular zone cells: implication for the genesis of glial tumors. J Neurosci 26:1107-1116.
17. Hiremath MM, Saito Y, Knapp GW, Ting JP, Suzuki K, Matsushima GK (1998) Microglial/macrophage accumulation during cuprizone-induced demyelination in C57BL/6 mice. J Neuroimmunol 92:38-49.
18. Jurevics H, Largent C, Hostettler J, Sammond DW, Matsushima GK, Kleindienst A, Toews AD, Morell P (2002) Alterations in metabolism and gene expression in brain regions during cuprizone-induced demyelination and remyelination. J Neurochem 82:126-136.
19. Kim SU, de Vellis J (2005) Microglia in health and disease. J Neurosci Res 81:302-313.
20. Komarova EA, Krivokrysenko V, Wang K, Neznanov N, Chernov MV, Komarov PG, Brennan ML, Golovkina TV, Rokhlin OW, Kuprash DV, Nedospasov SA, Hazen SL, Feinstein E, Gudkov AV (2005) p53 is a suppressor of inflammatory response in mice. FASEB J 19:1030-1032.
21. Kondo T, Raff M (2004) Chromatin remodeling and histone modification in the conversion of oligodendrocyte precursors to neural stem cells. Genes Dev 18:2963-2972.
22. Kotter MR, Setzu A, Sim FJ, Van Rooijen N, Franklin RJ (2001) Macrophage depletion impairs oligodendrocyte remyelination following lysolecithin-induced demyelination. Glia 35:204-212.
23. Kuhlmann T, Glas M, zum Bruch C, Mueller W, Weber A, Zipp F, Bruck W (2002) Investigation of bax, bcl-2, bcl-x and p53 gene polymorphisms in multiple sclerosis. J Neuroimmunol 129:154-160.
24. Ladiwala U, Li H, Antel JP, Nalbantoglu J (1999) p53 induction by tumor necrosis factor-alpha and involvement of p53 in cell death of human oligodendrocytes. J Neurochem 73:605-611.
25. Li WW, Setzu A, Zhao C, Franklin RJ (2005) Minocycline-mediated inhibition of microglia activation impairs oligodendrocyte progenitor cell responses and remyelination in a non-immune model of demyelination. J Neuroimmunol 158:58-66.
26. Lozano G (2007) The oncogenic roles of p53 mutants in mouse models. Curr Opin Genet Dev 17:66-70.
27. Lu DY, Tang CH, Liou HC, Teng CM, Jeng KC, Kuo SC, Lee FY, Fu WM (2007) YC-1 attenuates LPS-induced proinflammatory responses and activation of nuclear factor-kappaB in microglia. Br J Pharmacol 151:396-405.
28. Lucchinetti C, Bruck W, Parisi J, Scheithauer B, Rodriguez M, Lassmann H (2000) Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann Neurol 47:707-717.
29. Matsushima GK, Morell P (2001) The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol 11:107-116.
30. Melchior B, Puntambekar SS, Carson MJ (2006) Microglia and the control of autoreactive T cell responses. Neurochem Int 49:145-153.
31. Morell P, Barrett CV, Mason JL, Toews AD, Hostettler JD, Knapp GW, Matsushima GK (1998) Gene expression in brain during cuprizone-induced demyelination and remyelination. Mol Cell Neurosci 12:220-227.
32. Murtie JC, Zhou YX, Le TQ, Vana AC, Armstrong RC (2005) PDGF and FGF2 pathways regulate distinct oligodendrocyte lineage responses in experimental demyelination with spontaneous remyelination. Neurobiol Dis 19:171-182.
33. Nait-Oumesmar B, Decker L, Lachapelle F, Avellana-Adalid V, Bachelin C, Van Evercooren AB (1999) Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur J Neurosci 11:4357-4366.
34. Nait-Oumesmar B, Picard-Riera N, Kerninon C, Decker L, Seilhean D, Hoglinger GU, Hirsch EC, Reynolds R, Baron-Van Evercooren A (2007) Activation of the subventricular zone in multiple sclerosis: evidence for early glial progenitors. Proc Natl Acad Sci USA 104:4694-4699.
35. Okuda Y, Okuda M, Bernard CC (2002) The suppression of T cell apoptosis influences the severity of disease during the chronic phase but not the recovery from the acute phase of experimental autoimmune encephalomyelitis in mice. J Neuroimmunol 131:115-125.
36. Pasquini LA, Calatayud CA, Bertone Una AL, Millet V, Pasquini JM, Soto EF (2007) The neurotoxic effect of cuprizone on oligodendrocytes depends on the presence of pro-inflammatory cytokines secreted by microglia. Neurochem Res 32:279-292.
37. Picard-Riera N, Decker L, Delarasse C, Goude K, Nait-Oumesmar B, Liblau R, Pham-Dinh D, Evercooren AB (2002) Experimental autoimmune encephalomyelitis mobilizes neural progenitors from the subventricular zone to undergo oligodendrogenesis in adult mice. Proc Natl Acad Sci USA 99:13211-13216.
38. Popovic N, Schubart A, Goetz BD, Zhang SC, Linington C, Duncan ID (2002) Inhibition of autoimmune encephalomyelitis by a tetracycline. Ann Neurol 51:215-223.
39. Sanders P, De Keyser J (2007) Janus faces of microglia in multiple sclerosis. Brain Res Rev 54:274-285.
40. Stadelmann C, Ludwin S, Tabira T, Guseo A, Lucchinetti CF, Leel-Ossy L, Ordinario AT, Bruck W, Lassmann H (2005) Tissue preconditioning may explain concentric lesions in Balo's type of multiple sclerosis. Brain 128:979-987.
41. Trebst C, Heine S, Lienenklaus S, Lindner M, Baumgärtner W, Weiss S, Stangel M (2007) Lack of interferon-beta leads to accelerated remyelination in a toxic model of central nervous system demyelination. Acta Neuropathol 114:587-596.
42. Uberti D, Yavin E, Gil S, Ayasola KR, Goldfinger N, Rotter V (1999) Hydrogen peroxide induces nuclear translocation of p53 and apoptosis in cells of oligodendroglia origin. Brain Res Mol Brain Res 65:167-175.
43. Villapol S, Acarin L, Faiz M, Castellano B, Gonzalez B (2007) Distinct spatial and temporal activation of caspase pathways in neurons and glial cells after excitotoxic damage to the immature rat brain. J Neurosci Res 85:3545-3556.
44. Wosik K, Antel J, Kuhlmann T, Bruck W, Massie B, Nalbantoglu J (2003) Oligodendrocyte injury in multiple sclerosis: a role for p53. J Neurochem 85:635-644.
45. Yang B, Prayson RA (2000) Expression of Bax, Bcl-2, and P53 in progressive multifocal leukoencephalopathy. Mod Pathol 13:1115-1120.
46. Yong VW, Wells J, Giuliani F, Casha S, Power C, Metz LM (2004) The promise of minocycline in neurology. Lancet Neurol 3:744-751.
47. Yrjanheikki J, Keinanen R, Pellikka M, Hokfelt T, Koistinaho J (1998) Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci USA 95:15769-15774.
48. Yrjanheikki J, Tikka T, Keinanen R, Goldsteins G, Chan PH, Koistinaho J (1999) A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci USA 96:13496-13500.