FoxO3a governs early microglial proliferation and employs mitochondrial depolarization with caspase 3, 8, and 9 cleavage during oxidant induced apoptosis

Current Neurovascular Research

Volumn 6, Issue 4, 2009, Pages 223-238

  Yan, Chen Shang ^a   Zhao, Zhong Chong ^a   Jinling, Hou ^a   Maiese, Kenneth ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Bromodeoxyuridine; Caspases; Cytochrome c; Forkhead transcription factors; FoxO3a; Immune system; Inflammation; Microglia; Mitochondria; Oxidative stress; Proliferating cell nuclear antigen

Indexed keywords

CASPASE 3; CASPASE 8; CASPASE 9; CYTOCHROME C; OXIDIZING AGENT; TRANSCRIPTION FACTOR FKHRL1;

APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MEMBRANE DEPOLARIZATION; MICROGLIA; MITOCHONDRION; OXIDATIVE STRESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 70350284055     PISSN: 15672026     EISSN: None     Source Type: Journal    
DOI: 10.2174/156720209789630302     Document Type: Article

References (120)

1. An, J, Zhang, C, Polavarapu, R, Zhang, X, Yepes, M. (2008) Tissue-type plasminogen activator and the low-density lipoprotein receptor-related protein induce Akt phosphorylation in the ischemic brain. Blood 112: 2787-2794.
2. Bakshi, P, Margenthaler, E, Laporte, V, Crawford, F, Mullan, M. (2008) Novel role of CXCR2 in regulation of gamma-secretase activity. ACS Chem Biol 3: 777-789.
3. Barbosa, NB, Oliveira, C, Araldi, D, Folmer, V, Rocha, JB, Nogueira, CW. (2008) Acute diphenyl diselenide treatment reduces hyperglycemia but does not change delta-aminolevulinate dehydratase activity in alloxan-induced diabetes in rats. Biol Pharm Bull 31: 2200-2204.
4. Barthelemy, C, Henderson, CE, Pettmann, B. (2004) Foxo3a induces motoneuron death through the Fas pathway in cooperation with JNK. BMC Neurosci 5: 48. (Pubitemid 40177033)
5. Bureau, G, Longpre, F, Martinoli, MG. (2008) Resveratrol and quercetin, two natural polyphenols, reduce apoptotic neuronal cell death induced by neuroinflammation. J Neurosci Res 86: 403-410. (Pubitemid 351196745)
6. Caporali, A, Sala-Newby, GB, Meloni, M, Graiani, G, Pani, E, Cristofaro, B, Newby, AC, Madeddu, P, Emanueli, C. (2008) Identification of the prosurvival activity of nerve growth factor on cardiac myocytes. Cell Death Differ 15: 299-311.
7. Charvet, C, Alberti, I, Luciano, F, Jacquel, A, Bernard, A, Auberger, P, Deckert, M. (2003) Proteolytic regulation of Forkhead transcription factor FOXO3a by caspase-3-like proteases. Oncogene 22: 4557-4568. (Pubitemid 36920699)
8. Chong, ZZ, Kang, J, Li, F, Maiese, K. (2005a) mGluRI Targets Microglial Activation and Selectively Prevents Neuronal Cell Engulfment Through Akt and Caspase Dependent Pathways. Curr Neurovasc Res 2: 197-211. (Pubitemid 40980179)
9. Chong, ZZ, Kang, JQ, Maiese, K. (2002a) Erythropoietin is a novel vascular protectant through activation of Akt1 and mitochondrial modulation of cysteine proteases. Circulation 106: 2973-2979.
10. Chong, ZZ, Kang, JQ, Maiese, K. (2003a) Apaf-1, Bcl-xL, Cytochrome c, and Caspase-9 Form the Critical Elements for Cerebral Vascular Protection by Erythropoietin. J Cereb Blood Flow Metab 23: 320-330.
11. Chong, ZZ, Kang, JQ, Maiese, K. (2003b) Erythropoietin fosters both intrinsic and extrinsic neuronal protection through modulation of microglia, Akt1, Bad, and caspase-mediated pathways. Br J Pharmacol 138: 1107-1118.
12. Chong, ZZ, Kang, JQ, Maiese, K. (2003c) Metabotropic glutamate receptors promote neuronal and vascular plasticity through novel intracellular pathways. Histol Histopathol 18: 173-189.
13. Chong, ZZ, Kang, JQ, Maiese, K. (2004a) Akt1 drives endothelial cell membrane asymmetry and microglial activation through Bcl-x(L) and caspase 1, 3, and 9. Exp Cell Res 296: 196-207.
14. Chong, ZZ, Li, F, Maiese, K. (2005b) Employing new cellular therapeutic targets for Alzheimer's disease: a change for the better? Curr Neurovasc Res 2: 55-72. (Pubitemid 41419946)
15. Chong, ZZ, Li, F, Maiese, K. (2005c) Erythropoietin requires NF-kappaB and its nuclear translocation to prevent early and late apoptotic neuronal injury during beta-amyloid toxicity. Curr Neurovasc Res 2: 387-399.
16. Chong, ZZ, Li, F, Maiese, K. (2005d) Oxidative stress in the brain: Novel cellular targets that govern survival during neurodegenerative disease. Prog Neurobiol 75: 207-246.
17. Chong, ZZ, Li, F, Maiese, K. (2005e) Stress in the brain: novel cellular mechanisms of injury linked to Alzheimer's disease. Brain Res Brain Res Rev 49: 1-21.
18. Chong, ZZ, Li, F, Maiese, K. (2006a) Attempted Cell Cycle Induction in Post-Mitotic Neurons Occurs in Early and Late Apoptotic Programs Through Rb, E2F1, and Caspase 3. Curr Neurovasc Res 3: 25-39.
19. Chong, ZZ, Li, F, Maiese, K. (2006b) Group I Metabotropic Receptor Neuroprotection Requires Akt and Its Substrates that Govern FOXO3a, Bim, and beta-Catenin During Oxidative Stress. Curr Neurovasc Res 3: 107-117. (Pubitemid 43764787)
20. Chong, ZZ, Li, F, Maiese, K. (2007a) Cellular demise and inflammatory microglial activation during beta-amyloid toxicity are governed by Wnt1 and canonical signaling pathways. Cell Signal 19: 1150-1162. (Pubitemid 46561553)
21. Chong, ZZ, Li, F, Maiese, K. (2007b) The pro-survival pathways of mTOR and protein kinase B target glycogen synthase kinase-3beta and nuclear factor-kappaB to foster endogenous microglial cell protection. Int J Mol Med 19: 263-272.
22. Chong, ZZ, Lin, SH, Kang, JQ, Maiese, K. (2003d) Erythropoietin prevents early and late neuronal demise through modulation of Akt1 and induction of caspase 1, 3, and 8. J Neurosci Res 71: 659-669.
23. Chong, ZZ, Lin, SH, Li, F, Maiese, K. (2005f) The sirtuin inhibitor nicotinamide enhances neuronal cell survival during acute anoxic injury through Akt, Bad, PARP, and mitochondrial associated "anti-apoptotic" pathways. Curr Neurovasc Res 2: 271-285.
24. Chong, ZZ, Lin, SH, Maiese, K. (2002b) Nicotinamide Modulates Mitochondrial Membrane Potential and Cysteine Protease Activity during Cerebral Vascular Endothelial Cell Injury. J Vasc Res 39: 131-147.
25. Chong, ZZ, Lin, SH, Maiese, K. (2004b) The NAD+ precursor nicotinamide governs neuronal survival during oxidative stress through protein kinase B coupled to FOXO3a and mitochondrial membrane potential. J Cereb Blood Flow Metab 24: 728-743.
26. Chong, ZZ, Maiese, K. (2007) Erythropoietin involves the phosphatidylinositol 3-kinase pathway, 14-3-3 protein and FOXO3a nuclear trafficking to preserve endothelial cell integrity. Br J Pharmacol 150: 839-850.
27. Chu, K, Jung, KH, Lee, ST, Kim, JH, Kang, KM, Kim, HK, Lim, JS, Park, HK, Kim, M, Lee, SK, Roh, JK. (2008) Erythropoietin reduces epileptogenic processes following status epilepticus. Epilepsia 49: 1723-1732.
28. De Felice, FG, Velasco, PT, Lambert, MP, Viola, K, Fernandez, SJ, Ferreira, ST, Klein, WL. (2007) 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 282: 11590-11601. (Pubitemid 47100810)
29. Denes, A, Ferenczi, S, Halasz, J, Kornyei, Z, Kovacs, KJ. (2008) Role of CX3CR1 (fractalkine receptor) in brain damage and inflammation induced by focal cerebral ischemia in mouse. J Cereb Blood Flow Metab 28: 1707-1721.
30. Dombroski, D, Balasubramanian, K, Schroit, AJ. (2000) Phosphatidylserine expression on cell surfaces promotes antibody- dependent aggregation and thrombosis in beta2-glycoprotein I-immune mice. J Autoimmun 14: 221-229. (Pubitemid 30672190)
31. Dringen, R. (2005) Oxidative and antioxidative potential of brain microglial cells. Antioxid Redox Signal 7: 1223-1233.
32. Duarte, AI, Santos, P, Oliveira, CR, Santos, MS, Rego, AC. (2008) Insulin neuroprotection against oxidative stress is mediated by Akt and GSK-3beta signaling pathways and changes in protein expression. Biochim Biophys Acta 1783: 994-1002.
33. Erol, A. (2009) Unraveling the Molecular Mechanisms Behind the Metabolic Basis of Sporadic Alzheimer's Disease. J Alzheimers Dis, [ Epub ahead of print].
34. Fei, M, Lu, M, Wang, Y, Zhao, Y, He, S, Gao, S, Ke, Q, Liu, Y, Li, P, Cui, X, Shen, A, Cheng, C. (2009) Arsenic trioxide-induced growth arrest of human hepatocellular carcinoma cells involving FOXO3a expression and localization. Med Oncol 26: 178-185.
35. Gayer, CP, Chaturvedi, LS, Wang, S, Craig, DH, Flanigan, T, Basson, MD. (2009) Strain-induced proliferation requires the phosphatidylinositol 3-kinase/AKT/glycogen synthase kinase pathway. J Biol Chem 284: 2001-2011.
36. Geijtenbeek, TB, Gringhuis, SI. (2009) Signalling through C-type lectin receptors: shaping immune responses. Nat Rev Immunol 9: 465-479.
37. Gilfillan, AM, Rivera, J. (2009) The tyrosine kinase network regulating mast cell activation. Immunol Rev 228: 149-169.
38. Gomez-Gutierrez, JG, Souza, V, Hao, HY, Montes de Oca-Luna, R, Dong, YB, Zhou, HS, McMasters, KM. (2006) Adenovirus-mediated gene transfer of FKHRL1 triple mutant efficiently induces apoptosis in melanoma cells. Cancer Biol Ther 5: 875-883. (Pubitemid 44775149)
39. Gossai, D, Lau-Cam, CA. (2009) The effects of taurine, taurine homologs and hypotaurine on cell and membrane antioxidative system alterations caused by type 2 diabetes in rat erythrocytes. Adv Exp Med Biol 643: 359-368.
40. Guarnieri, G, Zanetti, M, Vinci, P, Cattin, MR, Barazzoni, R. (2009) Insulin resistance in chronic uremia. J Ren Nutr 19: 20-24.
41. Hao, J, Shen, W, Tian, C, Liu, Z, Ren, J, Luo, C, Long, J, Sharman, E, Liu, J. (2009) Mitochondrial nutrients improve immune dysfunction in the type 2 diabetic Goto-Kakizaki rats. J Cell Mol Med 13: 701-711.
42. Harris, SE, Fox, H, Wright, AF, Hayward, C, Starr, JM, Whalley, LJ, Deary, IJ. (2007) A genetic association analysis of cognitive ability and cognitive ageing using 325 markers for 109 genes associated with oxidative stress or cognition. BMC Genet 8: 43.
43. Jacobs, KM, Pennington, JD, Bisht, KS, Aykin-Burns, N, Kim, HS, Mishra, M, Sun, L, Nguyen, P, Ahn, BH, Leclerc, J, Deng, CX, Spitz, DR, Gius, D. (2008) SIRT3 interacts with the daf-16 homolog FOXO3a in the mitochondria, as well as increases FOXO3a dependent gene expression. Int J Biol Sci 4: 291-299.
44. Jessel, R, Haertel, S, Socaciu, C, Tykhonova, S, Diehl, HA. (2002) Kinetics of apoptotic markers in exogeneously induced apoptosis of EL4 cells. J Cell Mol Med 6: 82-92. (Pubitemid 44133985)
45. Jonsson, H, Allen, P, Peng, SL. (2005) Inflammatory arthritis requires Foxo3a to prevent Fas ligand-induced neutrophil apoptosis. Nat Med 11: 666-671. (Pubitemid 40868308)
46. Kang, JQ, Chong, ZZ, Maiese, K. (2003a) Akt1 protects against inflammatory microglial activation through maintenance of membrane asymmetry and modulation of cysteine protease activity. J Neurosci Res 74: 37-51.
47. Kang, JQ, Chong, ZZ, Maiese, K. (2003b) Critical role for Akt1 in the modulation of apoptotic phosphatidylserine exposure and microglial activation. Mol Pharmacol 64: 557-569.
48. Karunakaran, S, Diwakar, L, Saeed, U, Agarwal, V, Ramakrishnan, S, Iyengar, S, Ravindranath, V. (2007) Activation of apoptosis signal regulating kinase 1 (ASK1) and translocation of death-associated protein, Daxx, in substantia nigra pars compacta in a mouse model of Parkinson's disease: protection by alpha-lipoic acid. FASEB J 21: 2226-2236. (Pubitemid 47026457)
49. Kim, KH, Oudit, GY, Backx, PH. (2008) Erythropoietin protects against doxorubicin-induced cardiomyopathy via a phosphatidylinositol 3-kinase-dependent pathway. J Pharmacol Exp Ther 324: 160-169.
50. Lappas, M, Lim, R, Riley, C, Rice, GE, Permezel, M. (2009) Localisation and expression of FoxO1 proteins in human gestational tissues. Placenta 30: 256-262.
51. Lee, SJ, Cho, KS, Koh, JY. (2009) Oxidative injury triggers autophagy in astrocytes: the role of endogenous zinc. Glia 57: 1351-1361.
52. Lehtinen, MK, Tegelberg, S, Schipper, H, Su, H, Zukor, H, Manninen, O, Kopra, O, Joensuu, T, Hakala, P, Bonni, A, Lehesjoki, AE. (2009) Cystatin B deficiency sensitizes neurons to oxidative stress in progressive myoclonus epilepsy, EPM1. J Neurosci 29: 5910-5915.
53. Leuner, K, Hauptmann, S, Abdel-Kader, R, Scherping, I, Keil, U, Strosznajder, JB, Eckert, A, Muller, WE. (2007) Mitochondrial dysfunction: the first domino in brain aging and Alzheimer's disease? Antioxid Redox Signal 9: 1659-1675. (Pubitemid 47462969)
54. Li, F, Chong, ZZ, Maiese, K. (2005) Vital elements of the wnt-frizzled signaling pathway in the nervous system. Curr Neurovasc Res 2: 331-340. (Pubitemid 41297370)
55. Li, F, Chong, ZZ, Maiese, K. (2006a) Cell Life Versus Cell Longevity: The Mysteries Surrounding the NAD(+) Precursor Nicotinamide. Curr Med Chem 13: 883-895.
56. Li, F, Chong, ZZ, Maiese, K. (2006b) Microglial integrity is maintained by erythropoietin through integration of Akt and its substrates of glycogen synthase kinase-3beta, beta-catenin, and nuclear factor-kappaB. Curr Neurovasc Res 3: 187-201. (Pubitemid 44198472)
57. Lin, L, Hron, JD, Peng, SL. (2004) Regulation of NF-kappaB, Th activation, and autoinflammation by the forkhead transcription factor Foxo3a. Immunity 21: 203-213. (Pubitemid 39094050)
58. Lin, SH, Maiese, K. (2001) The metabotropic glutamate receptor system protects against ischemic free radical programmed cell death in rat brain endothelial cells. J Cereb Blood Flow Metab 21: 262-275.
59. Lu, J, Wu, DM, Zheng, YL, Sun, DX, Hu, B, Shan, Q, Zhang, ZF, Fan, SH. (2009) Trace amounts of copper exacerbate beta amyloid-induced neurotoxicity in the cholesterol-fed mice through TNF-mediated inflammatory pathway. Brain Behav Immun 23: 193-203.
60. Ludikhuize, J, de Launay, D, Groot, D, Smeets, TJ, Vinkenoog, M, Sanders, ME, Tas, SW, Tak, PP, Reedquist, KA. (2007) Inhibition of forkhead box class O family member transcription factors in rheumatoid synovial tissue. Arthritis Rheum 56: 2180-2191. (Pubitemid 47173565)
61. Maiese, K. (2008a) Diabetic stress: new triumphs and challenges to maintain vascular longevity. Expert Rev Cardiovasc Ther 6: 281-284.
62. Maiese, K. (2008b) Triple play: Promoting neurovascular longevity with nicotinamide, WNT, and erythropoietin in diabetes mellitus. Biomed Pharmacother 62: 218-232.
63. Maiese, K. (2009a) High anxiety: Recognizing stress as the stressor. Oxid Med Cell Longev 2: 61-62.
64. Maiese, K. (2009b) Marking the onset of oxidative stress: Biomarkers and novel strategies. Oxid Med Cell Longev 2: 1.
65. Maiese, K, Ahmad, I, TenBroeke, M, Gallant, J. (1999) Metabotropic glutamate receptor subtypes independently modulate neuronal intracellular calcium. J Neurosci Res 55: 472-485. (Pubitemid 29110554)
66. Maiese, K, Chong, Z, Hou, J, Shang, Y. (2009a) The "O" Class: Crafting clinical care with FoxO transcription factors. In: Forkhead Transcription Factors: Vital Elements in Biology and Medicine. Maiese, K, Ed., Landes Bioscience, Austin, TX vol 665; ISBN 978-1-4419-1598-6.
67. Maiese, K, Chong, Z, Li, F. (2009b) Reducing oxidative stress and enhancing neurovascular longevity during diabetes mellitus. In: Neurovascular Medicine: Pursuing Cellular Longevity for Healthy Aging. Maiese, K, Ed., Oxford University Press: New York, NY, pp. 540-564.
68. Maiese, K, Chong, ZZ. (2003) Nicotinamide: necessary nutrient emerges as a novel cytoprotectant for the brain. Trends Pharmacol Sci 24: 228-232. (Pubitemid 36588870)
69. Maiese, K, Chong, ZZ. (2004) Insights into oxidative stress and potential novel therapeutic targets for Alzheimer disease. Restor Neurol Neurosci 22: 87-104. (Pubitemid 38850337)
70. Maiese, K, Chong, ZZ, Hou, J, Shang, YC. (2008a) Erythropoietin and oxidative stress. Curr Neurovasc Res 5: 125-142.
71. Maiese, K, Chong, ZZ, Li, F. (2005a) Driving cellular plasticity and survival through the signal transduction pathways of metabotropic glutamate receptors. Curr Neurovasc Res 2: 425-446. (Pubitemid 41789608)
72. Maiese, K, Chong, ZZ, Li, F, Shang, YC. (2008b) Erythropoietin: Elucidating new cellular targets that broaden therapeutic strategies. Prog Neurobiol 85: 194-213.
73. Maiese, K, Chong, ZZ, Shang, YC. (2007a) Mechanistic insights into diabetes mellitus and oxidative stress. Curr Med Chem 14: 1729-1738. (Pubitemid 47163410)
74. Maiese, K, Chong, ZZ, Shang, YC. (2007b) "Sly as a FOXO": New paths with Forkhead signaling in the brain. Curr Neurovasc Res 4: 295-302. (Pubitemid 350171831)
75. Maiese, K, Chong, ZZ, Shang, YC. (2008c) OutFOXOing disease and disability: the therapeutic potential of targeting FoxO proteins. Trends Mol Med 14: 219-227.
76. Maiese, K, Chong, ZZ, Shang, YC. (2008d) Raves and risks for erythropoietin. Cytokine Growth Factor Rev 19: 145-155.
77. Maiese, K, Chong, ZZ, Shang, YC, Hou, J. (2008e) Clever cancer strategies with FoxO transcription factors. Cell Cycle 7: 3829-3839.
78. Maiese, K, Chong, ZZ, Shang, YC, Hou, J. (2008f) Rogue proliferation versus restorative protection: where do we draw the line for Wnt and forkhead signaling? Expert Opin Ther Targets 12: 905-916.
79. Maiese, K, Chong, ZZ, Shang, YC, Hou, J. (2009c) A "FOXO" in sight: targeting Foxo proteins from conception to cancer. Med Res Rev 29: 395-418.
80. Maiese, K, Chong, ZZ, Shang, YC, Hou, J. (2009d) FoxO proteins: cunning concepts and considerations for the cardiovascular system. Clin Sci Lond 116: 191-203.
81. Maiese, K, Hou, J, Chong, ZZ, Shang, YC. (2009e) A fork in the path: Developing therapeutic inroads with FoxO proteins. Oxid Med Cell Longev 2: 119-126.
82. Maiese, K, Li, F, Chong, ZZ. (2005b) New avenues of exploration for erythropoietin. JAMA 293: 90-95.
83. Maiese, K, Morhan, SD, Chong, ZZ. (2007c) Oxidative stress biology and cell injury during type 1 and type 2 diabetes mellitus. Curr Neurovasc Res 4: 63-71.
84. Maiese, K, Vincent, A, Lin, SH, Shaw, T. (2000) Group I and Group III metabotropic glutamate receptor subtypes provide enhanced neuroprotection. J Neurosci Res 62: 257-272. (Pubitemid 30775438)
85. Maiese, K, Vincent, AM. (2000a) Critical temporal modulation of neuronal programmed cell injury. Cell Mol Neurobiol 20: 383-400. (Pubitemid 30228228)
86. Maiese, K, Vincent, AM. (2000b) Membrane asymmetry and DNA degradation: functionally distinct determinants of neuronal programmed cell death. J Neurosci Res 59: 568-580. (Pubitemid 30090585)
87. Mallat, M, Marin-Teva, JL, Cheret, C. (2005) Phagocytosis in the developing CNS: more than clearing the corpses. Curr Opin Neurobiol 15: 101-107. (Pubitemid 40249968)
88. Mari, C, Karabiyikoglu, M, Goris, ML, Tait, JF, Yenari, MA, Blankenberg, FG. (2004) Detection of focal hypoxic-ischemic injury and neuronal stress in a rodent model of unilateral MCA occlusion/reperfusion using radiolabeled annexin V. Eur J Nucl Med Mol Imaging 31: 733-739. (Pubitemid 38647914)
89. Martinez-Contreras, A, Huerta, M, Lopez-Perez, S, Garcia-Estrada, J, Luquin, S, Beas Zarate, C. (2002) Astrocytic and microglia cells reactivity induced by neonatal administration of glutamate in cerebral cortex of the adult rats. J Neurosci Res 67: 200-210.
90. Miki, T, Miura, T, Yano, T, Takahashi, A, Sakamoto, J, Tanno, M, Kobayashi, H, Ikeda, Y, Nishihara, M, Naitoh, K, Ohori, K, Shimamoto, K. (2006) Alteration in erythropoietin-induced cardioprotective signaling by postinfarct ventricular remodeling. J Pharmacol Exp Ther 317: 68-75.
91. Morissette, M, Al Sweidi, S, Callier, S, Di Paolo, T. (2008a) Estrogen and SERM neuroprotection in animal models of Parkinson's disease. Mol Cell Endocrinol 290: 60-69.
92. Morissette, M, Le Saux, M, D'Astous, M, Jourdain, S, Al Sweidi, S, Morin, N, Estrada-Camarena, E, Mendez, P, Garcia-Segura, LM, Di Paolo, T. (2008b) Contribution of estrogen receptors alpha and beta to the effects of estradiol in the brain. J Steroid Biochem Mol Biol 108: 327-338. (Pubitemid 351179644)
93. Nakamura, T, Sakamoto, K. (2007) Forkhead transcription factor FOXO subfamily is essential for reactive oxygen species-induced apoptosis. Mol Cell Endocrinol 281(1-2): 47-55. (Pubitemid 350296601)
94. Newman, M, Musgrave, IF, Lardelli, M. (2007) Alzheimer disease: amyloidogenesis, the presenilins and animal models. Biochim Biophys Acta 1772: 285-297. (Pubitemid 46275437)
95. North, BJ, Marshall, BL, Borra, MT, Denu, JM, Verdin, E. (2003) The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol Cell 11: 437-444.
96. Obexer, P, Geiger, K, Ambros, PF, Meister, B, Ausserlechner, MJ. (2007) FKHRL1-mediated expression of Noxa and Bim induces apoptosis via the mitochondria in neuroblastoma cells. Cell Death Differ 14: 534-547. (Pubitemid 46259961)
97. Okouchi, M, Ekshyyan, O, Maracine, M, Aw, TY. (2007) Neuronal apoptosis in neurodegeneration. Antioxid Redox Signal 9: 1059-1096.
98. Park, SJ, Kim, HY, Kim, H, Park, SM, Joe, EH, Jou, I, Choi, YH. (2009) Oxidative stress induces lipid-raft-mediated activation of Src homology 2 domain-containing protein-tyrosine phosphatase 2 in astrocytes. Free Radic Biol Med 46: 1694-1702.
99. Power, JH, Asad, S, Chataway, TK, Chegini, F, Manavis, J, Temlett, JA, Jensen, PH, Blumbergs, PC, Gai, WP. (2008) Peroxiredoxin 6 in human brain: molecular forms, cellular distribution and association with Alzheimer's disease pathology. Acta Neuropathol 115: 611-622.
100. Rosa, RM, Hoch, NC, Furtado, GV, Saffi, J, Henriques, JA. (2007) DNA damage in tissues and organs of mice treated with diphenyl diselenide. Mutat Res 633: 35-45. (Pubitemid 47089095)
101. Ruf, TF, Quintes, S, Sternik, P, Gottmann, U. (2009) Atorvastatin reduces the expression of aldo-keto reductases in HUVEC and PTEC. A new approach to influence the polyol pathway. Clin Invest Med 32: E219-228.
102. Sales Santos, I, da Rocha Tomé, A, Saldanha, G, Ferreira, P, Militão, G, de Freitas, R. (2009) Oxidative stress in the hippocampus during experimental seizures can be ameliorated with the antioxidant ascorbic acid. Oxid Med Cell Longev 2: 23-30.
103. Salminen, A, Kaarniranta, K. (2009) Siglec receptors and hiding plaques in Alzheimer's disease. J Mol Med 87: 697-701.
104. Sanchez, PE, Navarro, FP, Fares, RP, Nadam, J, Georges, B, Moulin, C, Le Cavorsin, M, Bonnet, C, Ryvlin, P, Belmeguenai, A, Bodennec, J, Morales, A, Bezin, L. (2009) Erythropoietin receptor expression is concordant with erythropoietin but not with common beta chain expression in the rat brain throughout the life span. J Comp Neurol 514: 403-414.
105. Sela, U, Dayan, M, Hershkoviz, R, Cahalon, L, Lider, O, Mozes, E. (2006) The negative regulators Foxj1 and Foxo3a are up-regulated by a peptide that inhibits systemic lupus erythematosus-associated T cell responses. Eur J Immunol 36: 2971-2980. (Pubitemid 44782571)
106. Shang, YC, Chong, ZZ, Hou, J, Maiese, K. (2009) The forkhead transcription factor FoxO3a controls microglial inflammatory activation and eventual apoptotic injury through caspase 3. Curr Neurovasc Res 6: 20-31.
107. Szabo, C. (2009) Role of nitrosative stress in the pathogenesis of diabetic vascular dysfunction. Br J Pharmacol 156: 713-727.
108. Tajes, M, Yeste-Velasco, M, Zhu, X, Chou, SP, Smith, MA, Pallas, M, Camins, A, Casadesus, G. (2009) Activation of Akt by lithium: Pro-survival pathways in aging. Mech Ageing Dev, 130: 253-261.
109. Takahashi, H, Nakamura, S, Asano, K, Kinouchi, M, Ishida-Yamamoto, A, Iizuka, H. (1999) Fas antigen modulates ultraviolet B-induced apoptosis of SVHK cells: sequential activation of caspases 8, 3, and 1 in the apoptotic process. Exp Cell Res 249: 291-298. (Pubitemid 29397936)
110. Thomas, DD, Ridnour, LA, Isenberg, JS, Flores-Santana, W, Switzer, CH, Donzelli, S, Hussain, P, Vecoli, C, Paolocci, N, Ambs, S, Colton, CA, Harris, CC, Roberts, DD, Wink, DA. (2008) The chemical biology of nitric oxide: implications in cellular signaling. Free Radic Biol Med 45: 18-31.
111. Toledano, A, Alvarez, MI, Caballero, I, Carmona, P, De Miguel, E. (2008) Immunohistochemical increase in cyclooxygenase-2 without apoptosis in different brain areas of subchronic nicotine- and D-amphetamine-treated rats. J Neural Transm 115: 1093-1108.
112. Tsolakidou, A, Trumbach, D, Panhuysen, M, Putz, B, Deussing, J, Wurst, W, Sillaber, I, Holsboer, F, Rein, T. (2008) Acute stress regulation of neuroplasticity genes in mouse hippocampus CA3 area - possible novel signalling pathways. Mol Cell Neurosci 38: 444-452.
113. Verdaguer, E, Susana Gde, A, Clemens, A, Pallas, M, Camins, A. (2007) Implication of the transcription factor E2F-1 in the modulation of neuronal apoptosis. Biomed Pharmacother 61: 390-399. (Pubitemid 47239339)
114. Williams, K, Schwartz, A, Corey, S, Orandle, M, Kennedy, W, Thompson, B, Alvarez, X, Brown, C, Gartner, S, Lackner, A. (2002) Proliferating cellular nuclear antigen expression as a marker of perivascular macrophages in simian immunodeficiency virus encephalitis. Am J Pathol 161: 575-585. (Pubitemid 36142166)
115. Williams, R, Dhillon, NK, Hegde, ST, Yao, H, Peng, F, Callen, S, Chebloune, Y, Davis, RL, Buch, SJ. (2009) Proinflammatory cytokines and HIV-1 synergistically enhance CXCL10 expression in human astrocytes. Glia 57: 734-743.
116. Won, CK, Ji, HH, Koh, PO. (2006) Estradiol prevents the focal cerebral ischemic injury-induced decrease of forkhead transcription factors phosphorylation. Neurosci Lett 398: 39-43.
117. Wu, SY, Wang, GF, Liu, ZQ, Rao, JJ, Lu, L, Xu, W, Wu, SG, Zhang, JJ. (2009) Effect of geniposide, a hypoglycemic glucoside, on hepatic regulating enzymes in diabetic mice induced by a high-fat diet and streptozotocin. Acta Pharmacol Sin 30: 202-208.
118. Zhao, L, Ma, W, Fariss, RN, Wong, WT. (2009) Retinal vascular repair and neovascularization are not dependent on CX3CR1 signaling in a model of ischemic retinopathy. Exp Eye Res 88: 1004-1013.
119. Zheng, WH, Kar, S, Quirion, R. (2002) FKHRL1 and its homologs are new targets of nerve growth factor Trk receptor signaling. J Neurochem 80: 1049-1061. (Pubitemid 34809957)
120. Zhou, M, Xu, W, Liao, G, Bi, X, Baudry, M. (2009) Neuroprotection against neonatal hypoxia/ischemia-induced cerebral cell death by prevention of calpain-mediated mGluR1alpha truncation. Exp Neurol 218: 75-82.