Genetic ablation of Nrf2/antioxidant response pathway in alexander disease mice reduces hippocampal gliosis but does not impact survival

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Hagemann, Tracy L ^a   Jobe, Emily M ^a,b   Messing, Albee ^a,c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIN B RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; IBA1 PROTEIN; IRON; MUTANT PROTEIN; PROTEIN P62; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; ALPHA CRYSTALLIN; ANTIOXIDANT; CERULOPLASMIN; FERRITIN; GLIAL FIBRILLARY ASTROCYTIC PROTEIN, MOUSE; GTF2H1 PROTEIN, MOUSE; NERVE PROTEIN; TRANSCRIPTION FACTOR;

ALEXANDER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; ASTROCYTE; BODY WEIGHT; CELL ACTIVATION; CONTROLLED STUDY; GENE; GENE DELETION; GENE FUNCTION; GENE REPRESSION; GENETIC ABLATION; GLIOSIS; HIPPOCAMPUS; LETHALITY; LIFESPAN; MICROGLIA; MOUSE; NONHUMAN; NRF2 GENE; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHENOTYPE; PROTEIN EXPRESSION; STRESS; SURVIVAL; ANIMAL; DOWN REGULATION; GENE INACTIVATION; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGICAL STRESS;

MUS; MUS MUSCULUS;

ALEXANDER DISEASE; ALPHA-CRYSTALLIN B CHAIN; ANIMALS; ANTIOXIDANTS; ASTROCYTES; CERULOPLASMIN; DOWN-REGULATION; FERRITINS; GENE DELETION; GENE KNOCKOUT TECHNIQUES; GLIOSIS; HIPPOCAMPUS; HUMANS; IRON; MICE; MICROGLIA; NERVE TISSUE PROTEINS; NF-E2-RELATED FACTOR 2; STRESS, PHYSIOLOGICAL; SURVIVAL ANALYSIS; TRANSCRIPTION FACTORS;

EID: 84861674567     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037304     Document Type: Article

References (59)

1. Alexander WS, (1949) Progressive fibrinoid degeneration of fibrillary astrocytes associated with mental retardation in a hydrocephalic infant. Brain 72: 373-381.
2. Iwaki T, Kume-Iwaki A, Liem RK, Goldman JE, (1989) Alpha B-crystallin is expressed in non-lenticular tissues and accumulates in Alexander's disease brain. Cell 57: 71-78.
3. Tian R, Gregor M, Wiche G, Goldman JE, (2006) Plectin regulates the organization of glial fibrillary acidic protein in Alexander disease. Am J Pathol 168: 888-897.
4. Brenner M, Johnson AB, Boespflug-Tanguy O, Rodriguez D, Goldman JE, Messing A, (2001) Mutations in GFAP, encoding glial fibrillary acidic protein, are associated with Alexander disease. Nat Genet 27: 117-120.
5. Li R, Johnson AB, Salomons G, Goldman JE, Naidu S, et al. (2005) Glial fibrillary acidic protein mutations in infantile, juvenile, and adult forms of Alexander disease. Ann Neurol 57: 310-326.
6. Quinlan RA, Brenner M, Goldman JE, Messing A, (2007) GFAP and its role in Alexander disease. Exp Cell Res 313: 2077-2087.
7. Prust M, Wang J, Morizono H, Messing A, Brenner M, et al. (2011) GFAP mutations, age at onset, and clinical subtypes in Alexander disease. Neurology 77: 1287-1294.
8. Stumpf E, Masson H, Duquette A, Berthelet F, McNabb J, et al. (2003) Adult Alexander disease with autosomal dominant transmission: a distinct entity caused by mutation in the glial fibrillary acid protein gene. Arch Neurol 60: 1307-1312.
9. Messing A, Li R, Naidu S, Taylor JP, Silverman L, et al. (2011) Archetypal and New Families With Alexander Disease and Novel Mutations in GFAP. Arch Neurol.
10. Shiihara T, Sawaishi Y, Adachi M, Kato M, Hayasaka K, (2004) Asymptomatic hereditary Alexander's disease caused by a novel mutation in GFAP. J Neurol Sci 225: 125-127.
11. Hagemann TL, Connor JX, Messing A, (2006) Alexander disease-associated glial fibrillary acidic protein mutations in mice induce Rosenthal fiber formation and a white matter stress response. J Neurosci 26: 11162-11173.
12. Hagemann TL, Gaeta SA, Smith MA, Johnson DA, Johnson JA, Messing A, (2005) Gene expression analysis in mice with elevated glial fibrillary acidic protein and Rosenthal fibers reveals a stress response followed by glial activation and neuronal dysfunction. Hum Mol Genet 14: 2443-2458.
13. Tang G, Xu Z, Goldman JE, (2006) Synergistic effects of the SAPK/JNK and the proteasome pathway on glial fibrillary acidic protein (GFAP) accumulation in Alexander disease. J Biol Chem 281: 38634-38643.
14. Tang G, Yue Z, Talloczy Z, Hagemann T, Cho W, et al. (2008) Autophagy induced by Alexander disease-mutant GFAP accumulation is regulated by p38/MAPK and mTOR signaling pathways. Hum Mol Genet 17: 1540-1555.
15. Wang L, Colodner KJ, Feany MB, (2011) Protein misfolding and oxidative stress promote glial-mediated neurodegeneration in an Alexander disease model. J Neurosci 31: 2868-2877.
16. Messing A, Daniels CM, Hagemann TL, (2010) Strategies for treatment in Alexander disease. Neurotherapeutics 7: 507-515.
17. Stewart D, Killeen E, Naquin R, Alam S, Alam J, (2003) Degradation of transcription factor Nrf2 via the ubiquitin-proteasome pathway and stabilization by cadmium. J Biol Chem 278: 2396-2402.
18. Tang G, Perng MD, Wilk S, Quinlan R, Goldman JE, (2010) Oligomers of mutant glial fibrillary acidic protein (GFAP) Inhibit the proteasome system in alexander disease astrocytes, and the small heat shock protein alphaB-crystallin reverses the inhibition. J Biol Chem 285: 10527-10537.
19. Eggler AL, Liu G, Pezzuto JM, van Breemen RB, Mesecar AD, (2005) Modifying specific cysteines of the electrophile-sensing human Keap1 protein is insufficient to disrupt binding to the Nrf2 domain Neh2. Proc Natl Acad Sci U S A %19; 102: 10070-10075.
20. McMahon M, Thomas N, Itoh K, Yamamoto M, Hayes JD, (2004) Redox-regulated turnover of Nrf2 is determined by at least two separate protein domains, the redox-sensitive Neh2 degron and the redox-insensitive Neh6 degron. J Biol Chem 279: 31556-31567.
21. Rada P, Rojo AI, Chowdhry S, McMahon M, Hayes JD, Cuadrado A, (2011) SCF/{beta}-TrCP promotes glycogen synthase kinase 3-dependent degradation of the Nrf2 transcription factor in a Keap1-independent manner. Mol Cell Biol 31: 1121-1133.
22. Shih AY, Li P, Murphy TH, (2005) A small-molecule-inducible Nrf2-mediated antioxidant response provides effective prophylaxis against cerebral ischemia in vivo. J Neurosci 25: 10321-10335.
23. Lee JM, Shih AY, Murphy TH, Johnson JA, (2003) NF-E2-related factor-2 mediates neuroprotection against mitochondrial complex I inhibitors and increased concentrations of intracellular calcium in primary cortical neurons. J Biol Chem 278: 37948-37956.
24. Calkins MJ, Jakel RJ, Johnson DA, Chan K, Kan YW, Johnson JA, (2005) Protection from mitochondrial complex II inhibition in vitro and in vivo by Nrf2-mediated transcription. Proc Natl Acad Sci U S A 102: 244-249.
25. Shih AY, Imbeault S, Barakauskas V, Erb H, Jiang L, et al. (2005) Induction of the Nrf2-driven antioxidant response confers neuroprotection during mitochondrial stress in vivo. J Biol Chem 280: 22925-22936.
26. Vargas MR, Johnson DA, Sirkis DW, Messing A, Johnson JA, (2008) Nrf2 activation in astrocytes protects against neurodegeneration in mouse models of familial amyotrophic lateral sclerosis. J Neurosci 28: 13574-13581.
27. Chen PC, Vargas MR, Pani AK, Smeyne RJ, Johnson DA, et al. (2009) Nrf2-mediated neuroprotection in the MPTP mouse model of Parkinson's disease: Critical role for the astrocyte. Proc Natl Acad Sci U S A 106: 2933-2938.
28. Calkins MJ, Vargas MR, Johnson DA, Johnson JA, (2010) Astrocyte-specific overexpression of Nrf2 protects striatal neurons from mitochondrial complex II inhibition. Toxicol Sci 115: 557-568.
29. Wakabayashi N, Itoh K, Wakabayashi J, Motohashi H, Noda S, et al. (2003) Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat Genet 35: 238-245.
30. Rajasekaran NS, Varadharaj S, Khanderao GD, Davidson CJ, Kannan S, et al. (2011) Sustained activation of nuclear erythroid 2-related factor 2/antioxidant response element signaling promotes reductive stress in the human mutant protein aggregation cardiomyopathy in mice. Antioxid Redox Signal 14: 957-971.
31. Messing A, Head MW, Galles K, Galbreath EJ, Goldman JE, Brenner M, (1998) Fatal encephalopathy with astrocyte inclusions in GFAP transgenic mice. Am J Pathol 152: 391-398.
32. Johnson DA, Andrews GK, Xu W, Johnson JA, (2002) Activation of the antioxidant response element in primary cortical neuronal cultures derived from transgenic reporter mice. J Neurochem 81: 1233-1241.
33. Chan K, Lu R, Chang JC, Kan YW, (1996) NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc Natl Acad Sci U S A 93: 13943-13948.
34. Petzold A, Keir G, Green AJ, Giovannoni G, Thompson EJ, (2004) An ELISA for glial fibrillary acidic protein. J Immunol Methods 287: 169-177.
35. Hill JM, Switzer RC III, (1984) The regional distribution and cellular localization of iron in the rat brain. Neuroscience 11: 595-603.
36. Nguyen T, Yang CS, Pickett CB, (2004) The pathways and molecular mechanisms regulating Nrf2 activation in response to chemical stress. Free Radic Biol Med 37: 433-441.
37. Lee JM, Calkins MJ, Chan K, Kan YW, Johnson JA, (2003) Identification of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis. J Biol Chem 278: 12029-12038.
38. Chan JY, Kwong M, Lu R, Chang J, Wang B, et al. (1998) Targeted disruption of the ubiquitous CNC-bZIP transcription factor, Nrf-1, results in anemia and embryonic lethality in mice. EMBO J 17: 1779-1787.
39. Jakel RJ, Townsend JA, Kraft AD, Johnson JA, (2007) Nrf2-mediated protection against 6-hydroxydopamine. Brain Res 1144: 192-201.
40. Kraft AD, Lee JM, Johnson DA, Kan YW, Johnson JA, (2006) Neuronal sensitivity to kainic acid is dependent on the Nrf2-mediated actions of the antioxidant response element. J Neurochem 98: 1852-1865.
41. Johnson DA, Amirahmadi S, Ward C, Fabry Z, Johnson JA, (2010) The absence of the pro-antioxidant transcription factor Nrf2 exacerbates experimental autoimmune encephalomyelitis. Toxicol Sci 114: 237-246.
42. Fahey JW, Zhang Y, Talalay P, (1997) Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against chemical carcinogens. Proc Natl Acad Sci U S A 94: 10367-10372.
43. Hubbs AF, Benkovic SA, Miller DB, O'Callaghan JP, Battelli L, et al. (2007) Vacuolar leukoencephalopathy with widespread astrogliosis in mice lacking transcription factor Nrf2. Am J Pathol 170: 2068-2076.
44. Connor JR, Menzies SL, (1996) Relationship of iron to oligodendrocytes and myelination. Glia 17: 83-93.
45. Qian ZM, Shen X, (2001) Brain iron transport and neurodegeneration. Trends Mol Med 7: 103-108.
46. Wasserman WW, Fahl WE, (1997) Functional antioxidant responsive elements. Proc Natl Acad Sci U S A 94: 5361-5366.
47. Tsuji Y, Ayaki H, Whitman SP, Morrow CS, Torti SV, Torti FM, (2000) Coordinate transcriptional and translational regulation of ferritin in response to oxidative stress. Mol Cell Biol 20: 5818-5827.
48. Rouault TA, (2006) The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat Chem Biol 2: 406-414.
49. Rouault TA, Cooperman S, (2006) Brain iron metabolism. Semin Pediatr Neurol 13: 142-148.
50. Ishii T, Itoh K, Takahashi S, Sato H, Yanagawa T, et al. (2000) Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J Biol Chem 275: 16023-16029.
51. Jain A, Lamark T, Sjottem E, Larsen KB, Awuh JA, et al. (2010) p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J Biol Chem 285: 22576-22591.
52. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, et al. (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282: 24131-24145.
53. Zatloukal K, Stumptner C, Fuchsbichler A, Heid H, Schnoelzer M, et al. (2002) p62 Is a common component of cytoplasmic inclusions in protein aggregation diseases. Am J Pathol 160: 255-263.
54. Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, et al. (2007) Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131: 1149-1163.
55. Komatsu M, Kurokawa H, Waguri S, Taguchi K, Kobayashi A, et al. (2010) The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol 12: 213-223.
56. Levine B, Kroemer G, (2008) Autophagy in the pathogenesis of disease. Cell 132: 27-42.
57. Bailey MS, Shipley MT, (1993) Astrocyte subtypes in the rat olfactory bulb: morphological heterogeneity and differential laminar distribution. J Comp Neurol 328: 501-526.
58. Emsley JG, Macklis JD, (2006) Astroglial heterogeneity closely reflects the neuronal-defined anatomy of the adult murine CNS. Neuron Glia Biol 2: 175-186.
59. Zhang Y, Barres BA, (2010) Astrocyte heterogeneity: an underappreciated topic in neurobiology. Curr Opin Neurobiol 20: 588-594.