Oxidative stress during the progression of β-amyloid pathology in the neocortex of the Tg2576 mouse model of Alzheimer's disease

Oxidative Medicine and Cellular Longevity

Volumn 2015, Issue , 2015, Pages

  Porcellotti, Sara ^a   Fanelli, Francesca ^a   Fracassi, Anna ^a   Sepe, Sara ^a,b   Cecconi, Francesco ^c   Bernardi, Cinzia ^d   Cimini, Annamaria ^e   Cerù, Maria Paola ^a,e   Moreno, Sandra ^a  

^a ROMA TRE UNIVERSITY   (Italy)

^b FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d SAN FILIPPO NERI HOSPITAL   (Italy)

^e UNIVERSITY OF L'AQUILA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANTS; CYTOLOGY; DAMAGE DETECTION; FATTY ACIDS; GLYCOPROTEINS; MOBILE SECURITY; NUCLEIC ACIDS; OLIGOMERS; OXIDATIVE STRESS; PATHOLOGY;

ALZHEIMER'S DISEASE; ANTI-INFLAMMATORY ACTION; ANTIOXIDANT CAPACITY; ANTIOXIDANT DEFENCE; ANTIOXIDANT ENZYME; CYTOPLASMIC LOCALIZATION; ENERGY HOMEOSTASIS; THERAPEUTIC INTERVENTION;

NEURODEGENERATIVE DISEASES;

8 HYDROXYGUANINE; ACROLEIN; AMYLOID BETA PROTEIN; COPPER ZINC SUPEROXIDE DISMUTASE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTATHIONE PEROXIDASE 1; MANGANESE SUPEROXIDE DISMUTASE; NEURON SPECIFIC NUCLEAR PROTEIN; NUCLEIC ACID; OLIGOMER; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; ABC TRANSPORTER; ABCD3 PROTEIN, MOUSE; GLIAL FIBRILLARY ASTROCYTIC PROTEIN, MOUSE; GLUTATHIONE PEROXIDASE; NERVE PROTEIN; PPARGC1A PROTEIN, MOUSE; SOD1 PROTEIN, MOUSE; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR;

AGED; AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BRAIN NERVE CELL; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CYTOARCHITECTURE; FEMALE; GLIA CELL; MALE; MOUSE; MOUSE MODEL; NEOCORTEX; NEUROPATHOLOGY; NONHUMAN; OXIDATIVE STRESS; SENILE PLAQUE; TG2576 MOUSE; ANIMAL; C57BL MOUSE; DISEASE MODEL; DOWN REGULATION; GENETICS; GENOTYPE; IMMUNOHISTOCHEMISTRY; METABOLISM; MITOCHONDRION; PATHOLOGY; PEROXISOME; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ACROLEIN; AGING; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FEMALE; GENOTYPE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTATHIONE PEROXIDASE; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIA; NEOCORTEX; NERVE TISSUE PROTEINS; OXIDATIVE STRESS; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA COACTIVATOR 1-ALPHA; PEROXISOMES; PPAR ALPHA; SUPEROXIDE DISMUTASE; SUPEROXIDE DISMUTASE-1; TRANSCRIPTION FACTORS;

EID: 84929346992     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2015/967203     Document Type: Article

References (78)

1. H. W. Querfurth and F. M. LaFerla, "Alzheimer's disease, " The New England Journal of Medicine, vol. 362, no. 4, pp. 329-344, 2010.
2. D. M. Walsh and D. J. Selkoe, "A oligomers-a decade of discovery, " Journal of Neurochemistry, vol. 101, no. 5, pp. 1172-1184, 2007.
3. K. Bettens, K. Sleegers, and C. van Broeckhoven, "Genetic insights in Alzheimer's disease, " The Lancet Neurology, vol. 12, no. 1, pp. 92-104, 2013.
4. G. A. Elder, M. A. Gama Sosa, and R. de Gasperi, "Transgenic mouse models of Alzheimer's disease, " Mount Sinai Journal of Medicine, vol. 77, no. 1, pp. 69-81, 2010.
5. K. Hsiao, P. Chapman, S. Nilsen et al. , "Correlative memory deficits, A elevation, and amyloid plaques in transgenic mice, " Science, vol. 274, no. 5284, pp. 99-102, 1996.
6. J. S. Jacobsen, C.-C. Wu, J. M. Redwine et al. , "Earlyonset behavioral and synaptic deficits in a mouse model of Alzheimer's disease, " Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 13, pp. 5161-5166, 2006.
7. M. C. Irizarry, M. McNamara, K. Fedorchak, K. Hsiao, and B. T. Hyman, "APPSW transgenic mice develop age-related A deposits and neuropil abnormalities, but no neuronal loss in CA1, " Journal of Neuropathology and Experimental Neurology, vol. 56, no. 9, pp. 965-973, 1997.
8. M. A. Westerman, D. Cooper-Blacketer, A. Mariash et al. , "The relationship between A and memory in the Tg2576 mouse model of Alzheimer's disease, " The Journal of Neuroscience, vol. 22, no. 5, pp. 1858-1867, 2002.
9. M. D'Amelio, V. Cavallucci, S. Middei et al. , "Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer's disease, " Nature Neuroscience, vol. 14, no. 1, pp. 69-79, 2011.
10. F. Fanelli, S. Sepe, M. D'Amelio et al. , "Age-dependent roles of peroxisomes in the hippocampus of a transgenic mouse model of Alzheimer's disease, " Molecular Neurodegeneration, vol. 8, article 8, 2013.
11. R. M. J. Deacon, L. L. Cholerton, K. Talbot et al. , "Agedependent and-independent behavioral deficits in Tg2576 mice, " Behavioural Brain Research, vol. 189, no. 1, pp. 126-138, 2008.
12. Y. Zhao and B. Zhao, "Oxidative stress and the pathogenesis of Alzheimer's disease, " OxidativeMedicine and Cellular Longevity, vol. 2013, Article ID 316523, 10 pages, 2013.
13. P. H. Reddy, "Misfolded proteins, mitochondrial dysfunction, and neurodegenerative diseases, " Biochimica et Biophysica Acta, vol. 1842, no. 8, p. 1167, 2014.
14. D. Trompier, A. Vejux, A. Zarrouk et al. , "Brain peroxisomes, " Biochimie, vol. 98, no. 1, pp. 102-110, 2014.
15. J. Clark andD. K. Simon, "Transcribe to survive: transcriptional control of antioxidant defense programs for neuroprotection in Parkinson's disease, " Antioxidants & Redox Signaling, vol. 11, no. 3, pp. 509-528, 2009.
16. J. N. Feige, L. Gelman, L. Michalik, B. Desvergne, andW. Wahli, "From molecular action to physiological outputs: peroxisome proliferator-activated receptors are nuclear receptors at the crossroads of key cellular functions, " Progress in Lipid Research, vol. 45, no. 2, pp. 120-159, 2006.
17. T. Wenz, "Mitochondria and PGC-1 in aging and ageassociated diseases, " Journal of Aging Research, vol. 2011, Article ID 810619, 12 pages, 2011.
18. M. T. Heneka, E. Reyes-Irisarri, M. Hüll, and M. P. Kummer, "Impact and therapeutic potential of PPARs in Alzheimer's disease, " Current Neuropharmacology, vol. 9, no. 4, pp. 643-650, 2011.
19. M. Fidaleo, F. Fanelli, M. Cerù, and S. Moreno, "Neuroprotective properties of peroxisome proliferator-activated receptor Alpha (PPAR) and its lipid ligands, " CurrentMedicinal Chemistry, vol. 21, no. 24, pp. 2803-2821, 2014.
20. L. Katsouri, K. Blondrath, and M. Sastre, "Peroxisome proliferator-activated receptor-cofactors in neurodegeneration, " International Union of Biochemistry and Molecular Biology Life, vol. 64, no. 12, pp. 958-964, 2012.
21. A. Bagattin, L. Hugendubler, and E. Mueller, "Transcriptional coactivator PGC-1 promotes peroxisomal remodeling and biogenesis, " Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 47, pp. 20376-20381, 2010.
22. A. Cimini, S. Moreno, M. D'Amelio et al. , "Early biochemical and morphological modifications in the brain of a transgenic mouse model of Alzheimer's disease: a role for peroxisomes, " Journal of Alzheimer's Disease, vol. 18, no. 4, pp. 935-952, 2009.
23. M. M. Bradford, "A rapid and sensitive method for the quantitation ofmicrogramquantities of protein utilizing the principle of protein dye binding, " Analytical Biochemistry, vol. 72, no. 1-2, pp. 248-254, 1976.
24. M. Hartlage-Rübsamen, M. Morawski, A. Waniek et al. , "Glutaminyl cyclase contributes to the formation of focal and diffuse pyroglutamate (pGlu)-A deposits in hippocampus via distinct cellular mechanisms, " Acta Neuropathologica, vol. 121, no. 6, pp. 705-719, 2011.
25. S. Moreno, S. Farioli-vecchioli, and M. P. Cerù, "Immunolocalization of peroxisome proliferator-activated receptors and retinoidXreceptors in the adult ratCNS, " Neuroscience, vol. 123, no. 1, pp. 131-145, 2004.
26. M. Morita and T. Imanaka, "Peroxisomal ABC transporters: structure, function and role in disease, " Biochimica et Biophysica Acta, vol. 1822, no. 9, pp. 1387-1396, 2012.
27. C. W. T. van Roermund, L. Ijlst, T. Wagemans, R. J. A. Wanders, and H. R. Waterham, "A role for the human peroxisomal halftransporter ABCD3 in the oxidation of dicarboxylic acids, " Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids, vol. 1841, no. 4, pp. 563-568, 2014.
28. E. Benedetti, B. D'Angelo, L. Cristiano et al. , "Involvement of peroxisome proliferator-activated receptor/(PPAR/) in BDNF signaling during aging and in Alzheimer disease: possible role of 4-hydroxynonenal (4-HNE), " Cell Cycle, vol. 13, no. 8, pp. 1335-1344, 2014.
29. F. Tamagnini, C. Burattini, T. Casoli, M. Balietti, P. Fattoretti, and G. Aicardi, "Early impairment of long-term depression in the perirhinal cortex of a mouse model of Alzheimer's disease, " Rejuvenation Research, vol. 15, no. 2, pp. 231-234, 2012.
30. A. M. Duffy, J. Morales-Corraliza, K. M. Bermudez-Hernandez et al. , "Entorhinal cortical defects in Tg2576 mice are present as early as 2-4 months of age, " Neurobiology of Aging, vol. 36, no. 1, pp. 134-148, 2015.
31. J. Lalande, H. Halley, S. Balayssac et al. , "1H NMR metabolomic signatures in five brain regions of the aPPswe Tg2576 mouse model ofAlzheimer's disease at four ages, " Journal of Alzheimer's Disease, vol. 39, no. 1, pp. 121-143, 2014.
32. M. J. Callahan, W. J. Lipinski, F. Bian, R. A. Durham, A. Pack, and L. C. Walker, "Augmented senile plaque load in aged female-amyloid precursor protein-transgenic mice, " The American Journal of Pathology, vol. 158, no. 3, pp. 1173-1177, 2001.
33. J. St-Pierre, S. Drori, M. Uldry et al. , "Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators, " Cell, vol. 127, no. 2, pp. 397-408, 2006.
34. A. Nunomura, G. Perry, G. Aliev et al. , "Oxidative damage is the earliest event in Alzheimer disease, " Journal of Neuropathology & Experimental Neurology, vol. 60, no. 8, pp. 759-767, 2001.
35. A. M. Swomley, S. Förster, J. T. Keeney et al. , "Abeta, oxidative stress in Alzheimer disease: evidence based on proteomics studies, " Biochimica et Biophysica Acta-Molecular Basis of Disease, vol. 1842, no. 8, pp. 1248-1257, 2014.
36. X. Wang, W. Wang, L. Li, G. Perry, H. G. Lee, and X. Zhu, "Oxidative stress andmitochondrial dysfunction in Alzheimer's disease, " Biochimica et Biophysica Acta-Molecular Basis of Disease, vol. 1842, no. 8, pp. 1240-1247, 2014.
37. M. Y. Aksenov, H. M. Tucker, P. Nair et al. , "The expression of key oxidative stress-handling genes in different brain regions in Alzheimer's disease, " Journal of Molecular Neuroscience, vol. 11, no. 2, pp. 151-164, 1998.
38. C. A. Massaad, R. G. Pautler, and E. Klann, "Mitochondrial superoxide: a key player in Alzheimer's disease, " Aging, vol. 1, no. 9, pp. 758-761, 2009.
39. M. Dumont, E. Wille, C. Stack, N. Y. Calingasan, M. F. Beal, and M. T. Lin, "Reduction of oxidative stress, amyloid deposition, and memory deficit by manganese superoxide dismutase overexpression in a transgenic mousemodel of Alzheimer's disease, " The FASEB Journal, vol. 23, no. 8, pp. 2459-2466, 2009.
40. J. Hroudová, N. Singh, and Z. Fisar, "Mitochondrial dysfunctions in neurodegenerative diseases: relevance to alzheimer's disease, " BioMed Research International, vol. 2014, Article ID 175062, 9 pages, 2014.
41. J. M. Flynn and S. Melovn, "SOD2 in mitochondrial dysfunction and neurodegeneration, " Free Radical Biology & Medicine, vol. 62, pp. 4-12, 2013.
42. M. E. Poynter and R. A. Daynes, "Peroxisome proliferatoractivated receptor activation modulates cellular redox status, represses nuclear factor-B signaling, and reduces inflammatory cytokine production in aging, " The Journal of Biological Chemistry, vol. 273, no. 49, pp. 32833-32841, 1998.
43. C. Scuderi, G. Esposito, A. Blasio et al. , "Palmitoylethanolamide counteracts reactive astrogliosis induced by-amyloid peptide, " Journal of Cellular and Molecular Medicine, vol. 15, no. 12, pp. 2664-2674, 2011.
44. C. Scuderi, M. Valenza, C. Stecca, G. Esposito, M. R. Carratù, and L. Steardo, "Palmitoylethanolamide exerts neuroprotective effects in mixed neuroglial cultures and organotypic hippocampal slices via peroxisome proliferator-activated receptor-, " Journal of Neuroinflammation, vol. 9, article 49, 2012.
45. G. D'Agostino, R. Russo, C. Avagliano, C. Cristiano, R. Meli, and A. Calignano, "Palmitoylethanolamide protects against the amyloid-25-35-induced learning and memory impairment in mice, an experimental model of alzheimer disease, " Neuropsychopharmacology, vol. 37, no. 7, pp. 1784-1792, 2012.
46. M. Cuadrado-Tejedor, J. F. Cabodevilla, M. Zamarbide, T. Gómez-Isla, R. Franco, and A. Pérez-Mediavilla, "Age-related mitochondrial alterations without neuronal loss in the hippocampus of a transgenic model of Alzheimer's disease, " Current Alzheimer Research, vol. 10, no. 4, pp. 390-405, 2013.
47. G. Leipnitz, A. U. Amaral, C. G. Fernandes et al. , "Pristanic acid promotes oxidative stress in brain cortex of young rats: a possible pathophysiological mechanism for brain damage in peroxisomal disorders, " Brain Research, vol. 1382, pp. 259-265, 2011.
48. E. N. B. Busanello, A. U. Amaral, A. M. Tonin et al. , "Experimental evidence that pristanic acid disrupts mitochondrial homeostasis in brain of young rats, " The Journal of Neuroscience Research, vol. 90, no. 3, pp. 597-605, 2012.
49. G. Lizard, O. Rouaud, J. Demarquoy, M. Cherkaoui-Malki, and L. Iuliano, "Potential roles of peroxisomes in Alzheimer's disease and in dementia of the Alzheimer's type, " Journal of Alzheimer's Disease, vol. 29, no. 2, pp. 241-254, 2012.
50. M. Fransen, M. Nordgren, B. Wang, O. Apanasets, and P. P. van Veldhoven, "Aging, age-related diseases and peroxisomes, " Subcellular Biochemistry, vol. 69, pp. 45-65, 2013.
51. D. Praticò, K. Uryu, S. Leight, J. Q. Trojanoswki, and V. M.-Y. Lee, "Increased lipid peroxidation precedes amyloid plaque formation in an animal model of alzheimer amyloidosis, " The Journal of Neuroscience, vol. 21, no. 12, pp. 4183-4187, 2001.
52. M. Singh, D. T. Nam, M. Arseneault, and C. Ramassamy, "Role of by-products of lipid oxidation in Alzheimer's disease brain: a focus on acrolein, " Journal of Alzheimer's Disease, vol. 21, no. 3, pp. 741-756, 2010.
53. S. J. Baloyannis, "Mitochondrial alterations in Alzheimer's disease, " Journal of Alzheimer's Disease, vol. 9, no. 2, pp. 119-126, 2006.
54. T. Kawarabayashi, L. H. Younkin, T. C. Saido, M. Shoji, K. H. Ashe, and S. G. Younkin, "Age-dependent changes in brain, CSF, and plasma amyloid protein in the Tg2576 transgenicmouse model of Alzheimer's disease, " Journal of Neuroscience, vol. 21, no. 2, pp. 372-381, 2001.
55. S. Desagher, J. Glowinski, and J. Premont, "Astrocytes protect neurons from hydrogen peroxide toxicity, " The Journal of Neuroscience, vol. 16, no. 8, pp. 2553-2562, 1996.
56. S. Moreno, E. Mugnaini, andM. P. Cerù, "Immunocytochemical localization of catalase in the central nervous system of the rat, " Journal of Histochemistry & Cytochemistry, vol. 43, no. 12, pp. 1253-1267, 1995.
57. B. Ahlemeyer, I. Neubert, W. J. Kovacs, and E. Baumgart-Vogt, "Differential expression of peroxisomal matrix and membrane proteins during postnatal development ofmouse brain, " Journal of Comparative Neurology, vol. 505, no. 1, pp. 1-17, 2007.
58. C. Masters, "Gluconeogenesis and the peroxisome, " Molecular and Cellular Biochemistry, vol. 166, no. 1-2, pp. 159-168, 1997.
59. G. A. Brooks, "Cell-cell and intracellular lactate shuttles, " The Journal of Physiology, vol. 587, no. 23, pp. 5591-5600, 2009.
60. F. Ding, J. Yao, J. R. Rettberg, S. Chen, andR. D. Brinton, "Early decline in glucose transport and metabolism precedes shift to ketogenic system in female aging and Alzheimer'smouse brain: Implication for bioenergetic intervention, " PLoSONE, vol. 8, no. 11, Article ID e79977, 2013.
61. J. Apelt, M. Bigl, P. Wunderlich, and R. Schliebs, "Aging-related increase in oxidative stress correlates with developmental pattern of beta-secretase activity and beta-amyloid plaque formation in transgenic Tg2576 mice with Alzheimer-like pathology, " International Journal of DevelopmentalNeuroscience, vol. 22, no. 7, pp. 475-484, 2004.
62. M. Pekny, U. Wilhelmsson, and M. Pekna, "The dual role of astrocyte activation and reactive gliosis, " Neuroscience Letters, vol. 565, pp. 30-38, 2014.
63. P. Agostinho, R. A. Cunha, and C. Oliveira, "Neuroinflammation, oxidative stress and the pathogenesis of Alzheimer's disease, " Current Pharmaceutical Design, vol. 16, no. 25, pp. 2766-2778, 2010.
64. Y. Yao, C. Chinnici, H. Tang, J. Q. Trojanowski, V. M. Y. Lee, and D. Praticò, "Brain inflammation and oxidative stress in a transgenic mouse model of Alzheimer-like brain amyloidosis, " Journal of Neuroinflammation, vol. 1, no. 1, article 21, 2004.
65. H. Johnston, H. Boutin, and S. M. Allan, "Assessing the contribution of inflammation inmodels of Alzheimer's disease, " Biochemical Society Transactions, vol. 39, no. 4, pp. 886-890, 2011.
66. S. Moreno, R. Nardacci, and M. P. Cerù, "Regional and ultrastructural immunolocalization of copper-zinc superoxide dismutase in rat central nervous system, " Journal of Histochemistry and Cytochemistry, vol. 45, no. 12, pp. 1611-1622, 1997.
67. K. Murakami, N. Murata, Y. Noda et al. , "SOD1 (copper/zinc superoxide dismutase) deficiency drives amyloid protein oligomerization andmemory loss inmousemodel ofAlzheimer disease, "The Journal of Biological Chemistry, vol. 286, no. 52, pp. 44557-44568, 2011.
68. Z. Chen andC. Zhong, "Oxidative stress inAlzheimer's disease, " Neuroscience Bulletin, vol. 30, no. 2, pp. 271-281, 2014.
69. J. E. Lee and P. L. Han, "An update of animal models of Alzheimer disease with a reevaluation of plaque depositions, " Experimental Neurobiology, vol. 22, no. 2, pp. 84-95, 2013.
70. A. Belkacemi and C. Ramassamy, "Time sequence of oxidative stress in the brain fromtransgenicmousemodels ofAlzheimer's disease related to the amyloid-cascade, " Free Radical Biology and Medicine, vol. 52, no. 3, pp. 593-600, 2012.
71. H. K. Delille, R. Alves, and M. Schrader, "Biogenesis of peroxisomes and mitochondria: linked by division, " Histochemistry and Cell Biology, vol. 131, no. 4, pp. 441-446, 2009.
72. S. Thoms, S. Grønborg, and J. Gärtner, "Organelle interplay in peroxisomal disorders, " Trends in Molecular Medicine, vol. 15, no. 7, pp. 293-302, 2009.
73. B. Wang, P. P. Van Veldhoven, C. Brees et al. , "Mitochondria are targets for peroxisome-derived oxidative stress in cultured mammalian cells, " Free Radical Biology & Medicine, vol. 65, pp. 882-894, 2013.
74. I. Paterniti, M. Cordaro, M. Campolo et al. , "Neuroprotection by association of palmitoylethanolamide with luteolin in experimental Alzheimer's disease models: the control of neuroinflammation, " CNS & Neurological Disorders-Drug Targets, vol. 13, no. 9, pp. 1530-1541, 2014.
75. C. Scuderi, C. Stecca, M. Valenza et al. , "Palmitoylethanolamide controls reactive gliosis and exerts neuroprotective functions in a rat model of Alzheimer's disease, "CellDeath and Disease, vol. 5, article e1419, 2014.
76. E. Aso and I. Ferrer, "Cannabinoids for treatment of alzheimer's disease: moving toward the clinic, " Frontiers in Pharmacology, vol. 5, article 37, Article ID Article 37, 2014.
77. N. Sato and R. Morishita, "Roles of vascular and metabolic components in cognitive dysfunction of Alzheimer disease: short-and long-term modification by non-genetic risk factors, " Frontiers in Aging Neuroscience, vol. 5, 2013.
78. D. J. Selkoe, "Preventing alzheimer's disease, " Science, vol. 337, no. 6101, pp. 1488-1492, 2012.