Oxidative stress involving changes in Nrf2 and ER stress in early stages of Alzheimer's disease

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1852, Issue 7, 2015, Pages 1428-1441

  Mota, Sandra I ^a,b   Costa, Rui O ^a,b   Ferreira, Ildete L ^a,b   Santana, Isabel ^c,d   Caldeira, Gladys L ^a   Padovano, Carmela ^a   Fonseca, Ana C ^a   Baldeiras, Inês ^a,c   Cunha, Catarina ^d   Letra, Liliana ^d   Oliveira, Catarina R ^a,c   Pereira, Cláudia M F ^a,c   Rego, Ana Cristina ^a,c  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d CENTRO HOSPITALAR E UNIVERSITÁRIO DE COIMBRA   (Portugal)

Author keywords

Alzheimer's disease; Calcium homeostasis; Lymphocyte; Mild cognitive impairment; Oxidative stress; Peripheral blood mononuclear cell

Indexed keywords

CALCIUM ION; COPPER ZINC SUPEROXIDE DISMUTASE; DONEPEZIL; GALANTAMINE; MESSENGER RNA; RIVASTIGMINE; SERINE; TRANSCRIPTION FACTOR NRF2; NF-E2-RELATED FACTOR 2; RNA, MESSENGER; SUPEROXIDE DISMUTASE; SUPEROXIDE DISMUTASE 1;

ADULT; AGED; ALZHEIMER DISEASE; ANIMAL MODEL; ARTICLE; BLOOD SAMPLING; BRAIN CORTEX; CALCIUM HOMEOSTASIS; CONTROLLED STUDY; CORRELATIONAL STUDY; DEFENSE MECHANISM; DISEASE SEVERITY; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENE EXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; MILD COGNITIVE IMPAIRMENT; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; WILD TYPE; AGED, 80 AND OVER; ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; GENETICS; GROWTH AND DEVELOPMENT; HUMANS; METABOLISM; MICE; MICE, INBRED C57BL; MIDDLE AGED;

MUS; MUS MUSCULUS;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; ENDOPLASMIC RETICULUM STRESS; FEMALE; HUMANS; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; MILD COGNITIVE IMPAIRMENT; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; RNA, MESSENGER; SUPEROXIDE DISMUTASE;

EID: 84928128412     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2015.03.015     Document Type: Article

References (85)

1. Adunsky A., Baram D., Hershkowitz M., Mekori Y.A. Increased cytosolic free calcium in lymphocytes of Alzheimer patients. J. Neuroimmunol. 1991, 33:167-172.
2. American Psychiatric association The Diagnostic and Statistical Manual of Mental Disorders 2000, (Text revision (DSM-IV-TR)). Fourth ed.
3. Baldeiras I., Santana I., Proenca M.T., Garrucho M.H., Pascoal R., Rodrigues A., Duro D., Oliveira C.R. Peripheral oxidative damage in mild cognitive impairment and mild Alzheimer's disease. J. Alzheimers Dis. 2008, 15:117-128.
4. Baldeiras I., Santana I., Proenca M.T., Garrucho M.H., Pascoal R., Rodrigues A., Duro D., Oliveira C.R. Oxidative damage and progression to Alzheimer's disease in patients with mild cognitive impairment. J. Alzheimers Dis. 2010, 21:1165-1177.
5. Baldeiras I.E., Ribeiro M.H., Pacheco P., Machado A., Santana I., Cunha L., Oliveira C.R. Diagnostic value of CSF protein profile in a Portuguese population of sCJD patients. J. Neurol. 2009, 256:1540-1550. 10.1007/s00415-009-5160-0.
6. Bell K.F., Al-Mubarak B., Fowler J.H., Baxter P.S., Gupta K., Tsujita T., Chowdhry S., Patani R., Chandran S., Horsburgh K., Hayes J.D., Hardingham G.E. Mild oxidative stress activates Nrf2 in astrocytes, which contributes to neuroprotective ischemic preconditioning. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:E1-E2. 10.1073/pnas.1015229108.
7. Blennow K., de Leon M.J., Zetterberg H. Alzheimer's disease. Lancet 2006, 368:387-403.
8. Bloom D.A., Jaiswal A.K. Phosphorylation of Nrf2 at Ser40 by protein kinase C in response to antioxidants leads to the release of Nrf2 from INrf2, but is not required for Nrf2 stabilization/accumulation in the nucleus and transcriptional activation of antioxidant response element-mediated NAD(P)H:quinone oxidoreductase-1 gene expression. J. Biol. Chem. 2003, 278(45):44675-44682. (Nov 7).
9. Bonomo S.M., Rigamonti A.E., Giunta M., Galimberti D., Guaita A., Gagliano M.G., Muller E.E., Cella S.G. Menopausal transition: a possible risk factor for brain pathologic events. Neurobiol. Aging 2009, 30:71-80.
10. Butterfield D.A. Amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer's disease brain. A review. Free Radic. Res. 2002, 36:1307-1313.
11. Caldeira G.L., Ferreira I.L., Rego A.C. Impaired transcription in Alzheimer's disease: key role in mitochondrial dysfunction and oxidative stress. J. Alzheimers Dis. 2013, 34:115-131. 10.3233/JAD-121444.
12. Carroll J.C., Rosario E.R., Kreimer S., Villamagna A., Gentzschein E., Stanczyk F.Z., Pike C.J. Sex differences in beta-amyloid accumulation in 3xTg-AD mice: role of neonatal sex steroid hormone exposure. Brain Res. 2010, 1366:233-245. 10.1016/j.brainres.2010.10.009.
13. Chen M.L., Wu S., Tsai T.C., Wang L.K., Tsai F.M. Regulation of macrophage immune responses by antipsychotic drugs. Immunopharmacol. Immunotoxicol. 2013, 35:573-580. 10.3109/08923973.2013.828744.
14. Glover-Cutter K.M., Lin S., Blackwell T.K. Integration of the unfolded protein and oxidative stress responses through SKN-1/Nrf. PLoS Genet. 2013, 9:e1003701. 10.1371/journal.pgen.1003701.
15. Costa R.O., Lacor P.N., Ferreira I.L., Resende R., Auberson Y.P., Klein W.L., Oliveira C.R., Rego A.C., Pereira C.F. Endoplasmic reticulum stress occurs downstream of GluN2B subunit of N-methyl-d-aspartate receptor in mature hippocampal cultures treated with amyloid-beta oligomers. Aging Cell 2012, 1:823-833. 10.1111/j.1474-9726.2012.00848.x.
16. Costa R.O., Ferreiro E., Martins I., Santana I., Cardoso S.M., Oliveira C.R., Pereira C.M. Amyloid beta-induced ER stress is enhanced under mitochondrial dysfunction conditions. Neurobiol. Aging 2012, 33:824. 10.1016/j.neurobiolaging.2011.04.011.
17. Costa R.O., Ferreiro E., Oliveira C.R., Pereira C.M. Inhibition of mitochondrial cytochrome c oxidase potentiates Abeta-induced ER stress and cell death in cortical neurons. Mol. Cell. Neurosci. 2013, 52:1-8. 10.1016/j.mcn.2012.09.005.
18. Crook R., Hardy J., Duff K. Single-day apolipoprotein E genotyping. J. Neurosci. Methods 1994, 53:125-127.
19. Cullinan S.B., Zhang D., Hannink M., Arvisais E., Kaufman R.J., Diehl J.A. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol. Cell. Biol. 2003, 23:7198-7209.
20. De Felice F.G., Velasco P.T., Lambert M.P., Viola K., Fernandez S.J., Ferreira S.T., Klein W.L. Abeta oligomers induce neuronal oxidative stress through an N-methyl-d-aspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine. J. Biol. Chem. 2007, 282:11590-11601.
21. Dragunow M. CREB and neurodegeneration. Front. Biosci. 2004, 9:100-103.
22. Eckert A., Hartmann H., Forstl H., Muller W.E. Alterations of intracellular calcium regulation during aging and Alzheimer's disease in nonneuronal cells. Life Sci. 1994, 55:2019-2029.
23. Eckert A., Oster M., Zerfass R., Hennerici M., Muller W.E. Elevated levels of fragmented DNA nucleosomes in native and activated lymphocytes indicate an enhanced sensitivity to apoptosis in sporadic Alzheimer's disease. Specific differences to vascular dementia. Dement. Geriatr. Cogn. Disord. 2001, 12:98-105.
24. 2+ dysfunction in neurodegenerative disorders: Alzheimer's disease. Biofactors 2011, 37:189-196. 10.1002/biof.157.
25. Ferreira I.L., Bajouco L.M., Mota S.I., Auberson Y.P., Oliveira C.R., Rego A.C. Amyloid beta peptide 1-42 disturbs intracellular calcium homeostasis through activation of GluN2B-containing N-methyl-d-aspartate receptors in cortical cultures. Cell Calcium 2012, 51:95-106. 10.1016/j.ceca.2011.11.008.
26. Ferreira I.L., Ferreiro E., Schmidt J., Cardoso J.M., Pereira C.M.F., Carvalho A.L., Oliveira C.R., Rego A.C. Aβ and NMDAR activation cause mitochondrial dysfunction involving ER calcium release. Neurobiol. Aging 2015, 36:680-692. 10.1016/j.neurobiolaging.2014.09.006.
27. Ferreira I.L., Resende R., Ferreiro E., Rego A.C., Pereira C.F. Multiple defects in energy metabolism in Alzheimer's disease. Curr. Drug Targets 2010, 11:1193-1206.
28. Ferreiro E., Baldeiras I., Ferreira I.L., Costa R.O., Rego A.C., Pereira C.F., Oliveira C.R. Mitochondrial- and endoplasmic reticulum-associated oxidative stress in Alzheimer's disease: from pathogenesis to biomarkers. Int. J. Cell Biol. 2012, 2012:735206. 10.1155/2012/735206.
29. Ferreiro E., Oliveira C.R., Pereira C.M. The release of calcium from the endoplasmic reticulum induced by amyloid-beta and prion peptides activates the mitochondrial apoptotic pathway. Neurobiol. Dis. 2008, 30:331-342. 10.1016/j.nbd.2008.02.003.
30. Ferreiro E., Resende R., Costa R., Oliveira C.R., Pereira C.M. An endoplasmic-reticulum-specific apoptotic pathway is involved in prion and amyloid-beta peptides neurotoxicity. Neurobiol. Dis. 2006, 23:669-678.
31. Folstein M.F., Folstein S.E., McHugh P.R. Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 1975, 12:189-198.
32. Fratiglioni L., Viitanen M., von Strauss E., Tontodonati V., Herlitz A., Winblad B. Very old women at highest risk of dementia and Alzheimer's disease: incidence data from the Kungsholmen Project, Stockholm. Neurology 1997, 48:132-138.
33. Grundman M., et al. Mild cognitive impairment can be distinguished from Alzheimer disease and normal aging for clinical trials. Arch. Neurol. 2004, 61:59-66.
34. Harding H.P., Zhang Y., Zeng H., Novoa I., Lu P.D., Calfon M., Sadri N., Yun C., Popko B., Paules R., Stojdl D.F., Bell J.C., Hettmann T., Leiden J.M., Ron D. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 2003, 11:619-633.
35. Hirata-Fukae C., Li H.F., Hoe H.S., Gray A.J., Minami S.S., Hamada K., Niikura T., Hua F., Tsukagoshi-Nagai H., Horikoshi-Sakuraba Y., Mughal M., Rebeck G.W., LaFerla F.M., Mattson M.P., Iwata N., Saido T.C., Klein W.L., Duff K.E., Aisen P.S., Matsuoka Y. Females exhibit more extensive amyloid, but not tau, pathology in an Alzheimer transgenic model. Brain Res. 2008, 1216:92-103.
36. Hoozemans J.J., Veerhuis R., Van Haastert E.S., Rozemuller J.M., Baas F., Eikelenboom P., Scheper W. The unfolded protein response is activated in Alzheimer's disease. Acta Neuropathol. 2005, 110:165-172.
37. Huang H.M., Ou H.C., Hsieh S.J. Antioxidants prevent amyloid peptide-induced apoptosis and alteration of calcium homeostasis in cultured cortical neurons. Life Sci. 2000, 66:1879-1892.
38. Itoh K., Wakabayashi N., Katoh Y., Ishii T., Igarashi K., Engel J.D., Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 1999, 13(1):76-86. (Jan 1).
39. Jonsson T., Atwal J.K., Steinberg S., Snaedal J., Jonsson P.V., Bjornsson S., Stefansson H., Sulem P., Gudbjartsson D., Maloney J., Hoyte K., Gustafson A., Liu Y., Lu Y., Bhangale T., Graham R.R., Huttenlocher J., Bjornsdottir G., Andreassen O.A., Jönsson E.G., Palotie A., Behrens T.W., Magnusson O.T., Kong A., Thorsteinsdottir U., Watts R.J., Stefansson K. A mutation in APP protects against Alzheimer's disease and age-related cognitive decline. Nature 2012, 488:96-99. 10.1038/nature11283.
40. Kalyanaraman B., Darley-Usmar V., Davies K.J., Dennery P.A., Forman H.J., Grisham M.B., Mann G.E., Moore K., Roberts L.J., Ischiropoulos H. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic. Biol. Med. 2012, 52:1-6. 10.1016/j.freeradbiomed.2011.09.030.
41. Kanninen K., White A.R., Koistinaho J., Malm T. Targeting glycogen synthase kinase-3beta for therapeutic benefit against oxidative stress in Alzheimer's disease: involvement of the Nrf2-ARE pathway. Int. J. Alzheimers Dis. 2011, 2011:985085. 10.4061/2011/985085.
42. 2+ homeostasis after ER stress. J. Cell Sci. 2008, 121:3636-3648. 10.1242/jcs.028654.
43. Leuner K., Pantel J., Frey C., Schindowski K., Schulz K., Wegat T., Maurer K., Eckert A., Muller W.E. Enhanced apoptosis, oxidative stress and mitochondrial dysfunction in lymphocytes as potential biomarkers for Alzheimer's disease. J. Neural Transm. Suppl. 2007, 207-215.
44. Lombardi V.R., Garcia M., Rey L., Cacabelos R. Characterization of cytokine production, screening of lymphocyte subset patterns and in vitro apoptosis in healthy and Alzheimer's Disease (AD) individuals. J. Neuroimmunol. 1999, 97:163-171.
45. Magaki S., Mueller C., Dickson C., Kirsch W. Increased production of inflammatory cytokines in mild cognitive impairment. Exp. Gerontol. 2007, 42:233-240.
46. Malhotra J.D., Kaufman R.J. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword?. Antioxid. Redox Signal. 2007, 9:2277-2293.
47. Marchese M., Cowan D., Head E., Ma D., Karimi K., Ashthorpe V., Kapadia M., Zhao H., Davis P., Sakic B. Autoimmune manifestations in the 3xTg-AD model of Alzheimer's disease. J. Alzheimers Dis. 2014, 39:191-210. 10.3233/JAD-131490.
48. Marques S.C., Lemos R., Ferreiro E., Martins M., de MA Santana I., Outeiro T.F., Pereira C.M. Epigenetic regulation of BACE1 in Alzheimer's disease patients and in transgenic mice. Neuroscience 2012, 220:256-266. 10.1016/j.neuroscience.2012.06.029.
49. Mattson M.P. Oxidative stress, perturbed calcium homeostasis, and immune dysfunction in Alzheimer's disease. J. Neurovirol. 2002, 8:539-550.
50. Mattson M.P. Pathways towards and away from Alzheimer's disease. Nature 2004, 430:631-639.
51. Mattsson N., Andreasson U., Persson S., Arai H., Batish S.D., Bernardini S., Bocchio-Chiavetto L., Blankenstein M.A., Carrillo M.C., Chalbot S., Coart E., Chiasserini D., Cutler N., Dahlfors G., Duller S., Fagan A.M., Forlenza O., Frisoni G.B., Galasko D., Galimberti D., Hampel H., Handberg A., Heneka M.T., Herskovits A.Z., Herukka S.K., Holtzman D.M., Humpel C., Hyman B.T., Iqbal K., Jucker M., Kaeser S.A., Kaiser E., Kapaki E., Kidd D., Klivenyi P., Knudsen C.S., Lui J., Lladó A., Lewczuk P., Li Q.X., Martins R., Masters C., McAuliffe J., Mercken M., Moghekar A., Molinuevo J.L., Montine T.J., Nowatzke W., O'Brien R., Otto M., Paraskevas G.P., Parnetti L., Petersen R.C., Prvulovic D., de Reus H.P., Rissman R.A., Scarpini E., Stefani A., Soininen H., Schröder J., Shaw L.M., Skinningsrud A., Skrogstad B., Spreer A., Talib L., Teunissen C., Trojanowski J.Q., Tumani H., Umek R.M., Van Broeck B., Vanderstichele H., Vecsei L., Verbeek M.M., Windisch M., Zhang J., Zetterberg H., Blennow K. The Alzheimer's Association external quality control program for cerebrospinal fluid biomarkers. Alzheimers Dement. 2011, 7:386-395. 10.1016/j.jalz.2011.05.2243.
52. McCullough K.D., Martindale J.L., Klotz L.O., Aw T.Y., Holbrook N.J. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol. 2001, 21:1249-1259.
53. Mecocci P., Polidori M.C., Ingegni T., Cherubini A., Chionne F., Cecchetti R., Senin U. Oxidative damage to DNA in lymphocytes from AD patients. Neurology 1998, 51:1014-1017.
54. Morocz M., Kalman J., Juhasz A., Sinko I., McGlynn A.P., Downes C.S., Janka Z., Rasko I. Elevated levels of oxidative DNA damage in lymphocytes from patients with Alzheimer's disease. Neurobiol. Aging 2002, 23:47-53.
55. Mota S.I., Ferreira I.L., Pereira C., Oliveira C.R., Rego A.C. Amyloid-beta peptide 1-42 causes microtubule deregulation through N-methyl-d-aspartate receptors in mature hippocampal cultures. Curr. Alzheimer Res. 2012, 9:844-856.
56. Mota S.I., Ferreira I.L., Valero J., Ferreiro E., Carvalho A.L., Oliveira C.R., Rego A.C. Impaired Src signaling and post-synaptic actin polymerization in Alzheimer's disease mice hippocampus - linking NMDA receptors and the reelin pathway. Exp. Neurol. 2014, 261C:698-709. 10.1016/j.expneurol.2014.07.023.
57. Oddo S., Caccamo A., Kitazawa M., Tseng B.P., LaFerla F.M. Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol. Aging 2003, 24:1063-1070.
58. Oikawa D., Kimata Y., Kohno K., Iwawaki T. Activation of mammalian IRE1alpha upon ER stress depends on dissociation of BiP rather than on direct interaction with unfolded proteins. Exp. Cell Res. 2009, 315:2496-2504. 10.1016/j.yexcr.2009.06.009.
59. Paradis E., Douillard H., Koutroumanis M., Goodyer C., LeBlanc A. Amyloid beta peptide of Alzheimer's disease downregulates Bcl-2 and upregulates bax expression in human neurons. J. Neurosci. 1996, 16:7533-7539.
60. Park E.Y., Rho H.M. The transcriptional activation of the human copper/zinc superoxide dismutase gene by 2,3,7,8-tetrachlorodibenzo-p-dioxin through two different regulator sites, the antioxidant responsive element and xenobiotic responsive element. Mol. Cell. Biochem. 2002, 240:47-55.
61. Parsons C.G., Stöffler A., Danysz W. Memantine: a NMDA receptor antagonist that improves memory by restoration of homeostasis in the glutamatergic system-too little activation is bad, too much is even worse. Neuropharmacology 2007, 53(6):699-723.
62. Pereira C.M., Oliveira C.R. Glutamate toxicity on a PC12 cell line involves glutathione (GSH) depletion and oxidative stress. Free Radic. Biol. Med. 1997, 23:637-647.
63. Pino S.C., O'Sullivan-Murphy B., Lidstone E.A., Yang C., Lipson K.L., Jurczyk A., diIorio P., Brehm M.A., Mordes J.P., Greiner D.L., Rossini A.A., Bortell R. CHOP mediates endoplasmic reticulum stress-induced apoptosis in Gimap5-deficient T cells. PLoS ONE 2009, 4:e5468. 10.1371/journal.pone.0005468.
64. Portet F., Ousset P.J., Visser P.J., Frisoni G.B., Nobili F., Scheltens P., Vellas B., Touchon J. Mild cognitive impairment (MCI) in medical practice: a critical review of the concept and new diagnostic procedure. Report of the MCI Working Group of the European Consortium on Alzheimer's Disease. J. Neurol. Neurosurg. Psychiatry 2006, 77:714-718.
65. Pratico D., Clark C.M., Liun F., Rokach J., Lee V.Y., Trojanowski J.Q. Increase of brain oxidative stress in mild cognitive impairment: a possible predictor of Alzheimer disease. Arch. Neurol. 2002, 59:972-976.
66. Ramsey C.P., Glass C.A., Montgomery M.B., Lindl K.A., Ritson G.P., Chia L.A., Hamilton R.L., Chu C.T., Jordan-Sciutto K.L. Expression of Nrf2 in neurodegenerative diseases. J. Neuropathol. Exp. Neurol. 2007, 66:75-85.
67. Resende R., Ferreiro E., Pereira C., Resende de O.C. Neurotoxic effect of oligomeric and fibrillar species of amyloid-beta peptide 1-42: involvement of endoplasmic reticulum calcium release in oligomer-induced cell death. Neuroscience 2008, 155:725-737. 10.1016/j.neuroscience.2008.06.036.
68. Resende R., Moreira P.I., Proenca T., Deshpande A., Busciglio J., Pereira C., Oliveira C.R. Brain oxidative stress in a triple-transgenic mouse model of Alzheimer disease. Free Radic. Biol. Med. 2008, 44:2051-2057. 10.1016/j.freeradbiomed.2008.03.012.
69. 2+ homeostasis in cardiac cells. Biosci. Rep. 1995, 15:341-349.
70. Schapansky J., Olson K., Van Der Ploeg R., Glazner G. NF-kappaB activated by ER calcium release inhibits Abeta-mediated expression of CHOP protein: enhancement by AD-linked mutant presenilin 1. Exp. Neurol. 2007, 208:169-176.
71. Scheff S.W., Price D.A., Schmitt F.A., Dekosky S.T., Mufson E.J. Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment. Neurology 2007, 68:1501-1508.
72. Scheper W., Nijholt D.A., Hoozemans J.J. The unfolded protein response and proteostasis in Alzheimer disease: preferential activation of autophagy by endoplasmic reticulum stress. Autophagy 2011, 7:910-911.
73. Sekhar K.R., Crooks P.A., Sonar V.N., Friedman D.B., Chan J.Y., Meredith M.J., Starnes J.H., Kelton K.R., Summar S.R., Sasi S., Freeman M.L. NADPH oxidase activity is essential for Keap1/Nrf2-mediated induction of GCLC in response to 2-indol-3-yl-methylenequinuclidin-3-ols. Cancer Res. 2003, 63:5636-5645.
74. Selkoe D.J. Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 2001, 81:741-766.
75. Smith M.A., Hirai K., Hsiao K., Pappolla M.A., Harris P.L., Siedlak S.L., Tabaton M., Perry G. Amyloid-beta deposition in Alzheimer transgenic mice is associated with oxidative stress. J. Neurochem. 1998, 70:2212-2215.
76. St-Pierre J., Drori S., Uldry M., Silvaggi J.M., Rhee J., Jager S., Handschin C., Zheng K., Lin J., Yang W., Simon D.K., Bachoo R., Spiegelman B.M. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 2006, 127:397-408.
77. Tacconi S., Perri R., Balestrieri E., Grelli S., Bernardini S., Annichiarico R., Mastino A., Caltagirone C., Macchi B. Increased caspase activation in peripheral blood mononuclear cells of patients with Alzheimer's disease. Exp. Neurol. 2004, 190:254-262.
78. Tagashira H., Bhuiyan M.S., Fukunaga K. Diverse regulation of IP3 and ryanodine receptors by pentazocine through σ1-receptor in cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 2013, 305(8):H1201-H1212. (Oct 15). 10.1152/ajpheart.00300.2013.
79. Tsang K.Y., Chan D., Bateman J.F., Cheah K.S. In vivo cellular adaptation to ER stress: survival strategies with double-edged consequences. J. Cell Sci. 2010, 123:2145-2154. 10.1242/jcs.068833.
80. Umeda T., Tomiyama T., Sakama N., Tanaka S., Lambert M.P., Klein W.L., Mori H. Intraneuronal amyloid beta oligomers cause cell death via endoplasmic reticulum stress, endosomal/lysosomal leakage, and mitochondrial dysfunction in vivo. J. Neurosci. Res. 2011, 89:1031-1042. 10.1002/jnr.22640.
81. Violi F., Carnevale R., Pastori D., Pignatelli P. Antioxidant and antiplatelet effects of atorvastatin by Nox2 inhibition. Trends Cardiovasc. Med. 2014, 24(4):142-148. (May). 10.1016/j.tcm.2013.09.006.
82. Violi F., Pignatelli P. Statins as regulators of redox signaling in platelets. Antioxid. Redox Signal. 2014, 20(8):1300-1312. (Mar 10). 10.1089/ars.2013.5527.
83. Whalley L.J., Dick F.D., McNeill G. A life-course approach to the aetiology of late-onset dementias. Lancet Neurol. 2006, 5:87-96.
84. Yoshida H. ER stress response, peroxisome proliferation, mitochondrial unfolded protein response and Golgi stress response. IUBMB Life 2009, 61:871-879. 10.1002/iub.229.
85. Zhang K., Kaufman R.J. The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 2006, 66:S102-S109.