Glucocorticoids exacerbate cognitive deficits in TDP-25 transgenic mice via a glutathione-mediated mechanism: Implications for aging, stress and TDP-43 proteinopathies

Journal of Neuroscience

Volumn 33, Issue 3, 2013, Pages 906-913

  Caccamo, Antonella ^a   Medina, David X ^a   Oddo, Salvatore ^a  

^a Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID; GLUTATHIONE; GLUTATHIONE DISULFIDE; PROTEASOME; TAR DNA BINDING PROTEIN; TDP 25 PROTEIN; UNCLASSIFIED DRUG;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; FEMALE; MALE; MOUSE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SPATIAL MEMORY; STRESS; TDP 43 PROTEINOPATHY; TRANSGENIC MOUSE; WESTERN BLOTTING;

AGING; ANIMALS; BRAIN; DEXAMETHASONE; DNA-BINDING PROTEINS; GLUCOCORTICOIDS; GLUTATHIONE; GLUTATHIONE DISULFIDE; MAZE LEARNING; MICE; MICE, TRANSGENIC; REACTIVE OXYGEN SPECIES; TDP-43 PROTEINOPATHIES;

EID: 84872327117     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3314-12.2013     Document Type: Article

References (62)

1. Andersen PM, Al-Chalabi A (2011) Clinical genetics of amyotrophic lateral sclerosis: what do we really know? Nat Rev Neurol 7:603-615. CrossRef Medline
2. Ballatori N, Krance SM, Notenboom S, Shi S, Tieu K, Hammond CL (2009) Glutathione dysregulation and the etiology and progression of human diseases. Biol Chem 390:191-214. Medline
3. Bose JK, Huang CC, Shen CK (2011) Regulation of autophagy by neuro-pathological protein TDP-43. J Biol Chem 286:44441-44448. CrossRef Medline
4. Brady OA, Meng P, Zheng Y, Mao Y, Hu F (2011) Regulation of TDP-43 aggregation by phosphorylation and p62/SQSTM1. J Neurochem 116: 248-259. CrossRef Medline
5. Buratti E, Baralle FE (2008) Multiple roles of TDP-43 in gene expression, splicing regulation, and human disease. Front Biosci 13:867-878. CrossRef Medline
6. Caccamo A, Majumder S, Deng JJ, Bai Y, Thornton FB, Oddo S (2009) Rapamycin rescues TDP-43 mislocalization and the associated low molecular mass neurofilament instability. J Biol Chem 284:27416-27424. CrossRef Medline
7. Caccamo A, Magrí A, Oddo S (2010a) Age-dependent changes in TDP-43 levels in a mouse model of Alzheimer disease are linked to Abeta oligomers accumulation. Mol Neurodegener 5:51. CrossRef Medline
8. Caccamo A, Maldonado MA, Bokov AF, Majumder S, Oddo S (2010b) CBP gene transfer increases BDNF levels and ameliorates learning and memory deficits in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA107:22687-22692.CrossRefMedline
9. Caccamo A, Majumder S, Oddo S (2012) Cognitive decline typical of frontotemporal lobar degeneration in transgenic mice expressing the 25-kDa C-terminal fragment of TDP-43. J Pathol 180:293-302.
10. Clinton LK, Billings LM, Green KN, Caccamo A, Ngo J, Oddo S, McGaugh JL, LaFerla FM (2007) Age-dependent sexual dimorphism in cognition and stress response in the 3xTg-AD mice. Neurobiol Dis 28:76-82. CrossRef Medline
11. Cohen TJ, Lee VM, Trojanowski JQ (2011a) TDP-43 functions and pathogenic mechanisms implicated in TDP-43 proteinopathies. Trends Mol Med 17:659-667. CrossRef Medline
12. Cohen TJ, Hwang AW, Unger T, Trojanowski JQ, Lee VM (2011b) Redox signalling directly regulates TDP-43 via cysteine oxidation and disulphide cross-linking. EMBO J 31:1241-1252. CrossRef Medline
13. Dormann D, Capell A, Carlson AM, Shankaran SS, Rodde R, Neumann M, Kremmer E, Matsuwaki T, Yamanouchi K, Nishihara M, Haass C (2009) Proteolytic processing of TAR DNA binding protein-43 by caspases produces C-terminal fragments with disease defining properties independent of progranulin. J Neurochem 110:1082-1094. CrossRef Medline
14. Garrido P (2011) Aging and stress: past hypotheses, present approaches and perspectives. Aging Dis 2:80-99. Medline
15. Geser F, Lee VM, Trojanowski JQ (2010) Amyotrophic lateral sclerosis and frontotemporal lobar degeneration: a spectrum of TDP-43 proteinopathies. Neuropathology 30:103-112. CrossRef Medline
16. Ghezzi P (2005) Regulation of protein function by glutathionylation. Free Radic Res 39:573-580. CrossRef Medline
17. Green KN, Billings LM, Roozendaal B, McGaugh JL, LaFerla FM (2006) Glucocorticoids increase amyloid-beta and tau pathology in a mouse model of Alzheimer's disease. J Neurosci 26:9047-9056. CrossRef Medline
18. Hagen TM, Vinarsky V, Wehr CM, Ames BN (2000) (R)-alpha-lipoic acid reverses the age-associated increase in susceptibility of hepatocytes to tert-butylhydroperoxide both in vitro and in vivo. Antioxid Redox Signal 2:473-483. CrossRef Medline
19. Hasegawa M, Nonaka T, Tsuji H, Tamaoka A, Yamashita M, Kametani F, Yoshida M, Arai T, Akiyama H (2011) Molecular dissection of TDP-43 proteinopathies. J Mol Neurosci 45:480-485. CrossRef Medline
20. Igaz LM, Kwong LK, Xu Y, Truax AC, Uryu K, Neumann M, Clark CM, Elman LB, Miller BL, Grossman M, McCluskey LF, Trojanowski JQ, Lee VM (2008) Enrichment of C-terminal fragments in TAR DNA-binding protein-43 cytoplasmic inclusions in brain but not in spinal cord of frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Am J Pathol 173:182-194. CrossRef Medline
21. Igaz LM, Kwong LK, Chen-Plotkin A, Winton MJ, Unger TL, Xu Y, Neumann M, Trojanowski JQ, Lee VM (2009) Expression of TDP-43 C-terminal fragments in vitro recapitulates pathological features of TDP-43 proteinopathies. J Biol Chem 284:8516-8524. Medline
22. Iguchi Y, Katsuno M, Takagi S, Ishigaki S, Niwa J, Hasegawa M, Tanaka F, Sobue G (2012) Oxidative stress induced by glutathione depletion reproduces pathological modifications of TDP-43 linked to TDP-43 proteinopathies. Neurobiol Dis 45:862-870. CrossRef Medline
23. Joëls M, Krugers H, Karst H (2008) Stress-induced changes in hippocampal function. Prog Brain Res 167:3-15. Medline
24. Kabashi E, Valdmanis PN, Dion P, Spiegelman D, McConkey BJ, Vande Velde C, Bouchard JP, Lacomblez L, Pochigaeva K, Salachas F, Pradat PF, Camu W, Meininger V, Dupre N, Rouleau GA (2008) TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat Genet 40:572-574. CrossRef Medline
25. Lee EB, Lee VM, Trojanowski JQ (2012) Gains or losses: molecular mechanisms of TDP43-mediated neurodegeneration. Nat Rev Neurosci 13:38-50. Medline
26. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, et al. (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168-176. CrossRef Medline
27. Marí M, Morales A, Colell A, García-Ruiz C, Fernández-Checa JC (2009) Mitochondrial glutathione, a key survival antioxidant. Antioxid Redox Signal 11:2685-2700. CrossRef Medline
28. McIntosh LJ, Hong KE, Sapolsky RM (1998) Glucocorticoids may alter antioxidant enzyme capacity in the brain: baseline studies. Brain Res 791: 209-214. CrossRef Medline
29. Medina DX, Caccamo A, Oddo S (2011) Methylene blue reduces abeta levels and rescues early cognitive deficit by increasing proteasome activity. Brain Pathol 21:140-149. CrossRef Medline
30. Meyerowitz J, Parker SJ, Vella LJ, Ng DCh, Price KA, Liddell JR, Caragounis A, Li QX, Masters CL, Nonaka T, Hasegawa M, Bogoyevitch MA, Kanninen KM, Crouch PJ, White AR (2011) C-Jun N-terminal kinase controls TDP-43 accumulation in stress granules induced by oxidative stress. Mol Neurodegener 6:57. CrossRef Medline
31. Mizushima N, Noda T, Yoshimori T, Tanaka Y, Ishii T, George MD, Klionsky DJ, Ohsumi M, Ohsumi Y (1998) A protein conjugation system essential for autophagy. Nature 395:395-398. CrossRef Medline
32. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, Bruce J, Schuck T, Grossman M, Clark CM, McCluskey LF, Miller BL, Masliah E, Mackenzie IR, Feldman H, Feiden W, Kretzschmar HA, Trojanowski JQ, Lee VM (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314:130-133. CrossRef Medline
33. Nonaka T, Kametani F, Arai T, Akiyama H, Hasegawa M (2009) Truncation and pathogenic mutations facilitate the formation of intracellular aggregates of TDP-43. Hum Mol Genet 18:3353-3364. CrossRef Medline
34. Oddo S, Caccamo A, Cheng D, Jouleh B, Torp R, LaFerla FM (2007) Genetically augmenting tau levels does not modulate the onset or progression of Abeta pathology in transgenic mice. J Neurochem 102:1053-1063. CrossRef Medline
35. Ohsumi Y (2001) Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol 2:211-216. CrossRef Medline
36. Patel R, McIntosh L, McLaughlin J, Brooke S, Nimon V, Sapolsky R (2002) Disruptive effects of glucocorticoids on glutathione peroxidase biochemistry in hippocampal cultures. J Neurochem 82:118-125. CrossRef Medline
37. Pivtoraiko VN, Stone SL, Roth KA, Shacka JJ (2009) Oxidative stress and autophagy in the regulation of lysosome-dependent neuron death. Antioxid Redox Signal 11:481-496. CrossRef Medline
38. Puccio S, Chu J, Praticò D (2011) Involvement of 5-lipoxygenase in the corticosteroid-dependent amyloid beta formation: in vitro and in vivo evidence. PLoS One 6:e15163. CrossRef Medline
39. Reagan LP, McEwen BS (1997) Controversies surrounding glucocorticoid-mediated cell death in the hippocampus. J Chem Neuroanat 13:149-167. CrossRef Medline
40. Rebrin I, Sohal RS (2008) Pro-oxidant shift in glutathione redox state during aging. Adv Drug Deliv Rev 60:1545-1552. CrossRef Medline
41. Sapolsky RM (1996) Stress, glucocorticoids, and damage to the nervous system: the current state of confusion. Stress 1:1-19. CrossRef Medline
42. Sapolsky RM (1999) Glucocorticoids, stress, and their adverse neurological effects: relevance to aging. Exp Gerontol 34:721-732. CrossRef Medline
43. Sarabdjitsingh RA, Joëls M, de Kloet ER (2012) Glucocorticoid pulsatility and rapid corticosteroid actions in the central stress response. Physiol Behav 106:73-80. CrossRef Medline
44. Sohal RS, Sohal BH (1991) Hydrogen peroxide release by mitochondria increases during aging. Mech Ageing Dev 57:187-202. CrossRef Medline
45. Sohal RS, Ku HH, Agarwal S, Forster MJ, Lal H (1994) Oxidative damage, mitochondrial oxidant generation and antioxidant defenses during aging and in response to food restriction in the mouse. Mech Ageing Dev 74: 121-133. CrossRef Medline
46. Sohal RS, Mockett RJ, Orr WC (2002) Mechanisms of aging: an appraisal of the oxidative stress hypothesis. Free Radic Biol Med 33:575-586. CrossRef Medline
47. Sotiropoulos I, Catania C, Pinto LG, Silva R, Pollerberg GE, Takashima A, Sousa N, Almeida OF (2011) Stress acts cumulatively to precipitate Alzheimer's disease-like tau pathology and cognitive deficits. J Neurosci 31: 7840-7847. CrossRef Medline
48. Sreedharan J, Blair IP, Tripathi VB, Hu X, Vance C, Rogelj B, Ackerley S, Durnall JC, Williams KL, Buratti E, Baralle F, de Belleroche J, Mitchell JD, Leigh PN, Al-Chalabi A, Miller CC, Nicholson G, Shaw CE (2008) TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 319:1668-1672. CrossRef Medline
49. Suh JH, Wang H, Liu RM, Liu J, Hagen TM (2004) (R)-alpha-lipoic acid reverses the age-related loss in GSH redox status in post-mitotic tissues: evidence for increased cysteine requirement for GSH synthesis. Arch Biochem Biophys 423:126-135. CrossRef Medline
50. Suzuki K, Kirisako T, Kamada Y, Mizushima N, Noda T, Ohsumi Y (2001) The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J 20:5971-5981. CrossRef Medline
51. Talbot K, Ansorge O (2006) Recent advances in the genetics of amyotrophic lateral sclerosis and frontotemporal dementia: common pathways in neurodegenerative disease. Hum Mol Genet 15 Spec No 2:R182-R187.
52. Terzic N, Vujcic M, Ristic-Fira A, Krstic-Demonacos M, Milanovic D, Kanazir DT, Ruzdijic S (2003) Effects of age and dexamethasone treatment on glucocorticoid response element and activating protein-1 binding activity in rat brain. J Gerontol A Biol Sci Med Sci 58:297-303. Medline
53. Ulrich-Lai YM, Herman JP (2009) Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 10:397-409. CrossRef Medline
54. Urushitani M, Sato T, Bamba H, Hisa Y, Tooyama I (2010) Synergistic effect between proteasome and autophagosome in the clearance of polyubiquitinated TDP-43. J Neurosci Res 88:784-797. Medline
55. Valdmanis PN, Daoud H, Dion PA, Rouleau GA (2009) Recent advances in the genetics of amyotrophic lateral sclerosis. Curr Neurol Neurosci Rep 9:198-205. CrossRef Medline
56. Wang HY, Wang IF, Bose J, Shen CK (2004) Structural diversity and functional implications of the eukaryotic TDP gene family. Genomics 83:130-139. CrossRef Medline
57. Wang IF, Reddy NM, Shen CK (2002) Higher order arrangement of the eukaryotic nuclear bodies. Proc Natl Acad Sci U S A 99:13583-13588. CrossRef Medline
58. Wang IF, Wu LS, Chang HY, Shen CK (2008) TDP-43, the signature protein of FTLD-U, is a neuronal activity-responsive factor. J Neurochem 105: 797-806. CrossRef Medline
59. Wang IF, Guo BS, Liu YC, Wu CC, Yang CH, Tsai KJ, Shen CK (2012) Autophagy activators rescue and alleviate pathogenesis of a mouse model with proteinopathies of the TAR DNA-binding protein 43. Proc Natl Acad Sci U S A 109:15024-15029. CrossRef Medline
60. Wang X, Fan H, Ying Z, Li B, Wang H, Wang G (2010) Degradation of TDP-43 and its pathogenic form by autophagy and the ubiquitinproteasome system. Neurosci Lett 469:112-116. CrossRef Medline
61. Yao YY, Wu QS, Li WZ, Li WP (2011) Dexamethasone potentiated Abeta-induced learning and memory impairment in rats. Neurol Res 33:371-380. CrossRef Medline
62. Zhang YJ, Xu YF, Cook C, Gendron TF, Roettges P, Link CD, Lin WL, Tong J, Castanedes-Casey M, Ash P, Gass J, Rangachari V, Buratti E, Baralle F, Golde TE, Dickson DW, Petrucelli L (2009) Aberrant cleavage of TDP-43 enhances aggregation and cellular toxicity. Proc Natl Acad Sci USA106:7607-7612.CrossRefMedlinep