Dysfunction of the unfolded protein response increases neurodegeneration in aged rat hippocampus following proteasome inhibition

Aging Cell

Volumn 8, Issue 6, 2009, Pages 654-665

  Gavilá, María Paz ^a,b   Pintado, Cristina ^a,c,d   Gavilá, Elena ^a,b   Jiménez, Sebastián ^a,c,d   Ríos, Rosa M ^b   Vitorica, Javier ^a,c,d   Castaño, Angélica ^a,c,d   Ruano, Diego ^a,c,d  

^a UNIVERSITY OF SEVILLE   (Spain)

^b CABIMER Andalusian Center for Molecular Biology and Regenerative Medicine CSIC University of Seville UPO   (Spain)

^c HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

^d CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

Aging; Alzheimer; Apoptosis; ER stress; Neuroinflammation; UPR

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6 ALPHA; CASPASE 3; CHAPERONE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; LACTACYSTIN; MEMBRANE PROTEIN; PROTEASOME; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN IRE1 ALPHA; PROTEIN JKN; PROTEIN PERK; UNCLASSIFIED DRUG; ACETYLCYSTEINE; BIOLOGICAL MARKER; DRUG DERIVATIVE; ENZYME INHIBITOR;

AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEGENERATION; CELL STRESS; CONTROLLED STUDY; DEGENERATIVE DISEASE; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; ENZYME INHIBITION; HIPPOCAMPUS; MALE; NERVE INJURY; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN INDUCTION; PROTEIN PROCESSING; RAT; SIGNAL TRANSDUCTION; STAINING; UBIQUITINATION; ANIMAL; CHEMICALLY INDUCED DISORDER; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; NERVE DEGENERATION; PATHOLOGY; UNFOLDED PROTEIN RESPONSE; WISTAR RAT;

ANIMALIA; RATTUS;

ACETYLCYSTEINE; AGING; ANIMALS; BIOLOGICAL MARKERS; CASPASE 3; ENZYME INHIBITORS; HIPPOCAMPUS; MALE; NERVE DEGENERATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 74049104138     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2009.00519.x     Document Type: Article

References (46)

1. Calfon M, Zeng H, Urano F, Till JH, Hubbart SR, Harding HP, Clark SG, Ron D (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1mRNA. Nature 415, 92-96.
2. Cecarini V, Ding Q, Keller JN (2007) Oxidative inactivation of the proteasome in Alzheimer's disease. Free Radic. Res. 41, 673-680.
3. Davies MPA, Barraclough DL, Stewart C, Joycel KA, Eccles RM, Barraclough R, Rudland PS, Sibson DR (2008) Expression and splicing of the unfolded protein response gene XBP-1 are significantly associated with clinical outcome of endocrine-treated breast cancer. Int. J. Cancer 123, 85-88.
4. DeGracia DJ, Kumar R, Owen CR, Krause GS, White BC (2002) Molecular pathways of protein synthesis inhibition during brain reperfusion: implications for neuronal survival or death. J. Cereb. Blood Flow Metab. 22, 127-141.
5. Gavilán MP, Vela J, Castaño A, Ramos B, del Río JC, Vitorica J, Ruano D (2006) Cellular environment facilitates protein accumulation in aged rat hippocampus. Neurobiol. Aging 27, 973-982.
6. Gavilán MP, Revilla E, Pintado C, Castaño A, Vizuete ML, Moreno-González I, Baglietto-Vargas D, Sánchez-Varo R, Vitorica J, Gutiérrez A, Ruano D (2007) Molecular and cellular characterization of the age-related neuroinflammatory processes occurring in normal rat hippocampus: potential relation with the loss of somatostatin GABAergic neurons. J. Neurochem. 103, 984-996.
7. Gavilán MP, Castaño A, Torres M, Revilla E, Caballero C, Jiménez S, García-Martínez A, Parrado J, Vitorica J, Ruano D (2009) Age-related increase in the immunoproteasome content in rat hippocampus: molecular and functional aspects. J. Neurochem. 108, 260-270.
8. González TN, Sidrauski C, Dorfler S, Walter P (1999) Mechanism of non-spliceosomal mRNA splicing in the unfolded protein response pathway. EMBO J. 18, 3119-3132.
9. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6, 1099-1108.
10. Harding HP, Calfon M, Urano F, Novoa I, Ron D (2002) Transcriptional and translational control in the mammalian Unfolded Protein Response. Annu. Rev. Cell Dev. Biol. 18, 575-599.
11. Hetz C, Bernasconi P, Fisher J, Lee AH, Bassik MC, Antonsson B, Brandt GS, Iwakoshi NN, Schinzel A, Glimcher LH, Korsmeyer SJ (2006) Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science 312, 572-576.
12. Katayama T, Imaizumi K, Honda A, Yoneda T, Kudo T, Takeda M, Mori K, Rozmahel R, Fraser P, George-Hyslop PST, Tohyama M (2001) Disturbed activation of endoplasmic reticulum stress transducers by familial Alzheimer's disease-linked presenilin-1 mutations. J. Biol. Chem. 276, 43446-43454.
13. Katayama T, Imaizumi K, Manabe T, Hitomi J, Kudo T, Tohyama M (2004) Induction of neuronal death by ER stress in Alzheimer's disease. J. Chem. Neuroanat. 28, 67-78.
14. Kaufman RJ (2002) Orchestrating the unfolded protein response in health and disease. J. Clin. Invest. 110, 1389-1398.
15. Keck S, Nitsch R, Grune T, Ullrich O (2003) Proteasome inhibition by paired helical filament-tau in brains of patients with Alzheimer's disease. J. Neurochem. 85, 115-122.
16. Keller JN, Hanni KB, Markesbery WR (2000a) Impaired proteasome function in Alzheimer's disease. J. Neurochem. 75, 436-439.
17. Keller JN, Hanni KB, Markesbery WR (2000b) Possible involvement of proteasome inhibition in aging: implications for oxidative stress. Mech. Ageing Dev. 113, 61-70.
18. Lee AH, Iwakoshi NN, Anderson KC, Glimcher LH (2003) Proteasome inhibitors disrupt the unfolded protein response in myeloma cells. PNAS 100, 9946-9951.
19. Lindholm D, Wootz H, Korhonen L (2006) ER stress and neurodegenerative diseases. Cell Death Differ. 13, 385-392.
20. Lopez-Salon M, Morelli L, Castano EM, Soto EF, Pasquini JM (2000) Defective ubiquitination of cerebral proteins in Alzheimer's disease. J. Neurosci. Res. 62, 302-310.
21. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
22. Lu PD, Harding HP, Ron D (2004) Translation re-initiation at alternative open reading frames regulates gene expression in an integrated stress response. J. Cell Biol. 167, 27-33.
23. Ma Y, Brewer JW, Diehl JA, Hendershot LM (2002) Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol. 318, 1351-1365.
24. Marciniak SJ, Yun CY, Oyadomari S, Novoa I, Zhang Y, Jungreis R, Nagata K, Harding HP, Ron D (2004) CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 18, 3066-3077.
25. Mori K (2000) Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell 101, 451-454.
26. Naidoo N, Ferber M, Master M, Zhu Y, Pack AI (2008) Aging impairs the unfolded protein response to sleep deprivation and leads to proapoptotic signaling. J. Neurosci. 28, 6539-6548.
27. Nikki JL, Holbrook J (2004) Elevated gadd153/chop expression and enhanced c-Jun N-terminal protein kinase activation sensitizes aged cells to ER stress. Exp. Gerontol. 39, 735-744.
28. Nishitoh H, Matsuzawa A, Tobiume K, Saegusa K, Takeda K, Inoue K, Hori S, Kakizuka A, Ichijo H (2002) ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev. 16, 1345-1355.
29. Novoa I, Zeng H, Harding HP, Ron D (2001) Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J. Cell Biol. 153, 1011-1022.
30. Paxinos G, Watson C (1986) The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press.
31. Pines J, Lindon C (2005) Proteolysis: anytime, any place, anywhere? Nat. Cell Biol. 7, 731-735.
32. Ruano D, Araujo F, Revilla E, Vela J, Bergis O, Vitorica J (2000) GABA-A and alpha-amino-3-hydroxy-5-methylsoxazole-4-propionate receptors are differentially affected by aging in the rat hippocampus. J. Biol. Chem. 275, 19585-19593.
33. Rudner J, Jendrossek V, Belka C (2002) New insights in the role of Bcl-2 Bcl-2 and the endoplasmic reticulum. Apoptosis 7, 441-447.
34. Rutkowski DT, Kaufman RJ (2007) That which does not kill me makes me stronger: adapting to chronic ER stress. Trends Biochem. Sci. 32, 469-476.
35. Szegezdi E, Logue SE, Gorman AM, Samali A (2006) Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 7, 880-885.
36. Thomenius MJ, Wang NS, Reineks EZ, Wang Z, Distelhorst CW (2003) Bcl-2 on the endoplasmic reticulum regulates Bax activity by binding to BH3-only proteins. J. Biol. Chem. 278, 6243-6250.
37. Tirosh B, Iwakoshii NN, Glimcher LH, Ploegh HL (2006) Rapid turnover of unspliced Xbp-1 as a factor that modulates the unfolded protein response. J. Biol. Chem. 281, 5852-5860.
38. Tseng BP, Green KN, Chan JL, Blurton-Jones M, LaFerla FM (2008) Abeta inhibits the proteasome and enhances amyloid and tau accumulation. Neurobiol. Aging 29, 1607-1618.
39. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287, 664-666.
40. Vattem KM, Wek RC (2004) Reinitiation involving upstream ORFs regulates ATF4mRNA translation in mammalian cells. Proc. Natl Acad. Sci. USA 101, 11269-11274.
41. Yoshida H (2007) ER stress and diseases. FEBS J. 274, 630-658.
42. Yoshida H, Okada T, Haze K, Yanagi H, Yura T, Negishi M, Mori K (2000) ATF6 activated by proteolysis binds in the presence of NF-Y (CBF) directly to the cis-acting element responsible for the mammalian unfolded protein response. Mol. Cell. Biol. 20, 6755-6767.
43. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107, 881-891.
44. Yoshida H, Oku M, Suzuki M, Mori K (2006) pXBP1(U) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(S) in mammalian ER stress response. J. Cell Biol. 172, 565-575.
45. Yoshida H, Uemura A, Mori K (2009) pXBP1(U), a negative regulator of the unfolded protein response activator pXBP1(S), targets ATF6 but not ATF4 in proteasome-mediated degradation. Cell Struct. Funct. 34, 1-10.
46. Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL, Ron D (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12, 982-995.