Role of WWOX/WOX1 in Alzheimer's disease pathology and in cell death signaling

Frontiers in Bioscience - Elite

Volumn 4 E, Issue 5, 2012, Pages 1951-1965

  Teng, Chih Chung ^a,c   Yang, Ya Ting ^a   Chen, Yu Chi ^a   Kuo, Yu Min ^a   Sze, Chun I ^a,b  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c CHANG GUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

Author keywords

Amyloid beta; Apoptosis; GSK3 beta; Review; Serine threonine protein kinases; Tau

Indexed keywords

AMYLOID BETA PROTEIN; APOLIPOPROTEIN E; APOPTOSIS SIGNAL REGULATING KINASE 1; BETA CATENIN; CASPASE 3; COMPLEMENT COMPONENT C1Q; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; CYCLIN DEPENDENT KINASE 5; GLYCOGEN SYNTHASE KINASE 3BETA; HEAT SHOCK COGNATE PROTEIN 70; HOMEODOMAIN INTERACTING PROTEIN KINASE 2; HYALURONIDASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PEPTIDYLPROLYL ISOMERASE PIN1; PROTEIN CDC42; PROTEIN P53; TAU PROTEIN; TRANSCRIPTION FACTOR AP 1; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG; WW DOMAIN CONTAINING OXIDOREDUCTASE; OXIDOREDUCTASE; WWOX PROTEIN, HUMAN;

ALZHEIMER DISEASE; APOPTOSIS; CARBOXY TERMINAL SEQUENCE; CELL DEATH; CELL SURVIVAL; CONSENSUS SEQUENCE; CORTICOBASAL DEGENERATION; DNA FRAGMENTATION; ENVIRONMENTAL STRESS; ENZYME ACTIVATION; EXCITOTOXICITY; FRONTOTEMPORAL DEMENTIA; GENE ACTIVATION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HETEROZYGOSITY LOSS; HUMAN; MICROTUBULE ASSEMBLY; MOLECULAR INTERACTION; NERVE CELL DIFFERENTIATION; NEUROPROTECTION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; OXIDATIVE STRESS; PICK PRESENILE DEMENTIA; PROGRESSIVE SUPRANUCLEAR PALSY; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; RNA INTERFERENCE; RNA SPLICING; SIGNAL TRANSDUCTION; TAUOPATHY; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ALZHEIMER DISEASE; CELL DEATH; HUMANS; OXIDOREDUCTASES; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 84860868174     PISSN: 19450494     EISSN: 19450508     Source Type: Journal    
DOI: None     Document Type: Review

References (135)

1. G. A. Jicha and S. A. Carr: Conceptual evolution in Alzheimer's disease: Implications for understanding the clinical phenotype of progressive. J Alzheimers Dis, 19(1), 253-272 (2010)
2. C. Reitz, C. Brayne, and R. Mayeux: Epidemiology of Alzheimer disease. Nature Reviews Neurology 7 (3), 137-152 (2011)
3. H. Braak and E. Braak: Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol (Berl), 82 (4), 239-259 (1991)
4. K.P. Riley, D. A. Snowdon, and W.R. Markesbery: Alzheimer's neurofibrillary pathology and the spectrum of cognitive function: findings from the Nun Study. Ann Neurol, 51(5), 567-577 (2002)
5. P. Penzes and J. E.Vanleeuwen: Impaired regulation of synaptic actin cytoskeleton in Alzheimer's disease. Brain Res Rev, 67(1-2), 184-192 (2011)
6. L. M. Ittner and J. Götz: Amyloid-beta and tau - a toxic pas de deux in Alzheimer's disease. Nat Rev Neurosci, 12(2), 65-72 (2010)
7. VJR. de Paula1, F M. Guimarães, B. S. Diniz, and O. V.Forlenza: Neurobiological pathways to Alzheimer's disease Amyloid-beta, Tau protein or both? Dementia & Neuropsychologia, 3(3), 188-194 (2009) Views & review
8. H.C. Huang and Z. F. Jiang: Accumulated amyloid-beta peptide and hyperphosphorylated tau protein: relationship and links in Alzheimer's disease. Journal of Alzheimer's Disease, 16, 15-27 (2009)
9. D. Muyllaert, A. Kremer, T. Jaworski, P. Borghgraef, H.Devijver, S. Croes, I. Dewachter, F. Van Leuven: Glycogen synthase kinase-3beta, or a link between amyloid and tau pathology? Genes Brain Behav, 7 (Suppl 1), 57-66 (2008)
10. Z. F. Wang, H. L. Li, X. C. Li, Q. Zhang, Q. Tian, Q. Wang, H. Xu, J. Z. Wang: Effects of endogenous beta-amyloid overproduction on tau phosphorylation in cell culture. J Neurochem, 98, 1167-1175 (2006) (Pubitemid 44127792)
11. P. Hernandez, G. Lee, M. Sjoberg, and R. B. Maccioni: Tau phosphorylation by cdk5 and Fyn in response to amyloid peptide Abeta 25-35: involvement of lipid rafts. Journal of Alzheimer's Disease, 16 (1), 149-156(2009)
12. G. Amadoro, V. Corsetti, M.T. Ciotti, F. Florenzano, S. Capsoni, G. Amatob, and P. C alissano: Endogenous Abeta causes cell death via early tau hyperphosphorylation. Neurobiol Aging, 1-22 (2009)
13. Y. Zhang, Q. Tian, Q. Zhang, X. Zhou, S. Liu, and J.Z.Wang: Hyperphosphorylation of microtubuleassociated tau protein plays dual role in neurodegeneration and neuroprotection. Pathophysiology, 16,311-316 (2009)
14. L. Buée, L. Troquier, S. Burnouf, K. Belarbi, A.Van der Jeugd, T. Ahmed, F. Fernandez-Gomez, R. Caillierez, M. E. Grosjean, S. Begard, B. Barbot, D. Demeyer, H. Obriot, I. Brion, V. Buée-Scherrer, C. A. Maurage, D. Balschun, R. D'hooge, M. Hamdane, D. Blum, and N. Sergeant: From tau phosphorylation to tau aggregation: what about neuronal death? Biochem Soc Trans, 38(4), 967-72 (2010)
15. A. K. Bednarek, K. J. Laflin, R. L. Daniel, Q. Liao, K. A. Hawkins, and C. M. Aldaz: WWOX, a novel WW domain-containing protein mapping to human chromosome 16q23.3-24.1, a region frequently affected in breast cancer. Cancer Res, 60, 2140-2145 (2000) (Pubitemid 30225175)
16. K. Reid, M. Finnis, L. Hobson, M. Mangelsdorf, S. Dayan, J. K. Nancarros, E. Woollatt, G. Kremmidiotis, A. Gardner, D.Venter, E.Baker, and R.I.Richards: Common chromosomal fragile site FRAD16D sequence: identification for the FOR gene spanning FRAD16D and homozygous deletions and translcoation breakpoints in cancer cells. Hum Mol Genet. 9(11), 1651-1663 (2000) (Pubitemid 30427002)
17. N. S. Chang, J. Doherty, A. Ensign, J. Lewis, J. Heath, L. Schultz, S. T. Chen, and U. Oppermann: Molecular mechanisms underlying WOX1 activation during apoptotic and stress responses. Biochem Pharmacol, 66(8), 1347-54 (2003) Review (Pubitemid 38379588)
18. K. Huebner and C. M. Croce: FRA3B and other common fragile sites: the weakest links. Nat Rev Cancer, 1(3), 214-221 (2001) (Pubitemid 33741896)
19. N. S. Chang, J. Doherty, A. Ensign, L. Schultz, L.J. Hsu, and Q Hong: WOX1 is essential for tumor necrosis factor-, UV light-, staurosporine-, and p53- mediated cell death, and its tyrosine 33- phosphorylated form binds and stabilizes serine 46- phosphorylated p53. J Biol Chem, 280(52), 43100-8 (2005)
20. S. Strano, E. Munarriz, M. Rossi, L. Castagnoli, Y. Shaul, A. Sacchi, M. Oren, M. Sudol, G. Cesareni, and G.Blandino: Physical interaction with Yesassociated protein enhances p73 transcriptional activity. J Biol Chem, 276(18), 15164-15173 (2001)
21. A. Komuro, M. Nagai, N. E. Navin, and M. Sudol: WW domain-containing protein YAP associates with ErbB-4 and acts as a cotranscriptional activator for the carboxyl-terminal fragment of ErbB-4 that translocates to the nucleus. J Biol Chem, 278(35), 33334-33341 (2003) (Pubitemid 37055785)
22. N. S. Chang, J. Doherty, and A. Ensign: JNK1 physically interacts with WW domain- containing oxidoreductase (WOX1) and inhibits WOX1- mediated apoptosis. J Biol Chem, 278(11), 9195-202 (2003) (Pubitemid 36800401)
23. Q. Hong, L. J. Hsu, L. Schultz, N. Pratt, J. Mattison, and N. S. Chang: Zfra affects TNFmediated cell death by interacting with death domain protein TRADD and negatively regulates the activation of NF-kappaB, JNK1, p53 and WOX1 during stress response. BMC Mol Biol, 8,50 (2007)
24. K.C. Kurek, S. Del Mare, Z. Salah, S. Abdeen, H. Sadiq, S. H. Lee, E. Gaudio, N. Zanesi, K. B. Jones, B. DeYoung, G. Amir, M. Gebhardt, M. Warman, G. S. Stein, J. L. Stein, J. B. Lian, and R. I. Aqeilan: Frequent attenuation of the WWOX tumor suppressor in osteosarcoma is associated with increased tumorigenicity and aberrant RUNX2 expression. Cancer Res, 70(13), 5577-86 (2010)
25. R. I. Aqeilan, M. Q. Hassan, A. de Bruin, J. P. Hagan, S. Volinia, T. Palumbo, S. Hussain, S. H. Lee, T. Gaur, G. S. Stein, J. B. Lian, and C. M. Croce: The WWOX tumor suppressor is essential for postnatal survival and normal bone metabolism. J Biol Chem, 283(31), 21629-39 (2008)
26. N. Bouteille, K. Driouch, P. E. Hage, S. Sin, E. Formstecher, J. Camonis, R. Lidereau, and F. Lallemand: Inhibition of the Wnt/beta-catenin pathway by the WWOX tumor suppressor protein. Oncogene, 28(28), 2569-80 (2009)
27. C. Jin, L. Ge, X. Ding, Y. Chen, H. Zhu, T. Ward, F. Wu, X. Cao, Q. Wang, and X. Yao: PKA-mediated protein phosphorylation regulates ezrin-WWOX interaction. Biochem Biophys Res Commun, 341(3), 784-91 (2006) (Pubitemid 43177558)
28. N. S. Chang, N. Pratt, J. Heath, L Schultz, D. Sleve, G. B. Carey, and N. Zevotek: Hyaluronidase induction of a WW domain-containing oxidoreductase that enhances tumor necrosis factor cytotoxicity. J Biol Chem, 276(5), 3361-3370 (2001)
29. R.J. Davis: Signal transduction by the JNK group of MAP kinases. Cell, 103(2), 239-252 (2000)
30. A. Roulston, C. Reinhard, P. Amiri, and L. T. Williams: Early activation of c-Jun N-terminal kinase and p38 kinase regulate cell survival in response to tumor necrosis factor alpha. J Biol Chem, 273(17), 10232-10239 (1998) (Pubitemid 28227625)
31. G. V. De Ferrari and N. C. Inestrosa: Wnt signaling function in Alzheimer's disease. Brain Research Reviews, 33(1), 1-12(2000)
32. C. I. Sze, S. Meng, S. Pugazhenthi, P. Jambal, L. J. Hsu, J. Heath, L. Schultz, and N. S. Chang: Downregulation of WW Domain-containing oxidoreductase induces tau phosphorylation in vitro. J Biol Chem, 279(29), 30498-30506 (2004) (Pubitemid 38937980)
33. N. S. Chang: A potential role of p53 and WOX1 in mitochondrial apoptosis. Int J Mol Med, 9(1), 19 24 (2002) Review
34. N. S. Chang, L. J. Hsu, Y. S. Lin, F. J. Lai, and H. M. Sheu: WW domain-containing oxidoreductase: a candidate tumor suppressor. Trends Mol Med, 13(1), 12 22 (2007)
35. J. Y. Chang, R.Y. He, H. P. Lin, L. J. Hsu, F. J. Lai, Q. Hong, S. J. Chen, and N. S. Chang: Signaling from membrane receptors to tumor suppressor WW domain-containing oxidoreductase. Exp Biol Med, (Maywood) 235(7), 796 804 (2010) Review
36. R. I. Aqeilan and C. M. Croce: WWOX in biological control and tumorigenesis. J Cell Physiol, 212(2), 307 310 (2007) (Pubitemid 47025619)
37. J. C. Lee, D. Weissglas Volkov, M. Kyttälä, Z. Dastani, R. M. Cantor, E. M. Sobel, et al: WW domain containing oxidoreductase is associated with low plasma HDL C levels. Am J Hum Genet, 83(2), 180 192 (2008)
38. M. E. Sáez, A. González-Pérez, M. T. Martínez- Larrad, J. Gayán, L.M. Real, M. Serrano-Ríos, and A. Ruiz: WWOX gene is associated with HDL cholesterol and triglyceride levels.BMC Med Genet, 11,148 (2010)
39. Z. Dastani, P. Pajukanta, M. Marcil, N. Rudzicz, I. Ruel, S.D. Bailey, J. C. Lee, M. Lemire, J. Faith, J. Platko, J. Rioux, T. J. Hudson, D. Gaudet, J. C. Engert, and J. Genest: Fine mapping and association studies of a high-density lipoprotein cholesterol linkage region on chromosome 16 in French-Canadian subjects. Euro J Hum Genet, 18, 342-347 (2010)
40. D. Iliopoulos, K. N. Malizos, P. Oikonomou, and A. Tsezou: Integrative microRNA and proteomic approaches identify novel osteoarthritis genes and their collaborative metabolic and inflammatory networks. PLoS One, 3 (11): e3740 (2008)
41. J. H. Ludes Meyers, H. Kil, J. Parker Thornburg, D. F. Kusewitt, M. T. Bedford, and C. M. Aldaz: Generation and characterization of mice carrying a conditional allele of the Wwox tumor suppressor gene. PLoS One, 4 (11): e7775 (2009)
42. L. V. Oõkeefe, A. Colella, S. Dayan, Q. A. Chen Choo, R. Jacob, et al. Drosophila orthologue of WWOX, the chromosomal fragile site FRA16D tumour suppressor gene, functions in aerobic metabolism and regulates reactive oxygen species. Hum Mol Genet. (2010) in press
43. S. T. Chen, J. I. Chuang, J. P. Wang, M.S. Tsai, H. Li, and N. S. Chang: Expression of WW domain containing oxidoreductase WOX1 in the developing murine nervous system. Neuroscience, 124(4), 831 839 (2004) (Pubitemid 38328773)
44. S. T. Chen, J. I. Chuang, C. L. Cheng, L. J. Hsu, and N. S. Chang: Light induced retinal damage involves tyrosine 33 phosphorylation, mitochondrial and nuclear translocation of WW domain containing oxidoreductase in vivo. Neuroscience, 130(2), 397 407 (2005)
45. C. P. Lo, L. J. Hsu, M. Y.Li, S. Y. Hsu, J. I. Chuang, M. S.Tsai, S. R. Lin, N. S. Chang, and S. T. Chen: MPP+ induced neuronal death in rats involves tyrosine 33 phosphorylation of WW domain containing oxidoreductase WOX1. Eur J Neurosci, 27(7), 1634 1646 (2008)
46. M. Y. Li, F. J. Lai, L.J. Hsu, C. P. Lo, C. L. Cheng, M.S. Tsai, C. I Sze, S. Pugazhenthi, N. S. Chang, and S. T. Chen: Dramatic co activation of WOX1 with CREB and NF kB in delayed loss of small dorsal root ganglion neurons upon sciatic nerve transection in rats. PLoS One, 4: e7820 (2009)
47. H. Suzuki, K. Katayama, M. Takenaka, K. Amakasu, K. Saito, and K. Suzuki: A spontaneous mutation of the Wwox gene and audiogenic seizures in rats with lethal dwarfism and epilepsy. Genes Brain Behav, 8 (7), 650 660 (2009)
48. C. Chen and L. E. Matesic: The Nedd4-like family of E3 ubiquitin ligases and cancer. Cancer Metast Rev, 26 (3-4), 587-604 (2007) (Pubitemid 350119775)
49. L. J. Hsu, L. Schultz, Q. Hong, K. Van Moer, J. Heath, M. Y. Li, F. J. Lai, S. R. Lin, M.H. Lee, C. P. Lo, Y. S. Lin, S. T. Chen, and N.S. Chang: Transforming growth factor beta1 signaling via interaction with cell surface Hyal-2 and recruitment of WWOX/WOX1. J Biol Chem, 284,16049-16059 (2009)
50. P. Bork and M. Sudol: The WW domain: a signalling site in dystrophin? Trends Biochem Sci, 19, 531-533 (1994) (Pubitemid 24360488)
51. O. Staub and D. Rotin: WW Domains. Structure (Curr. Biol.), 4, 495-499(1996) (Pubitemid 126657542)
52. M. J. Macias, M. Hyvönen, E. Baraldi, J. Schultz, M.Sudol, M. Saraste and H. Oschkinat: Structure of the WW domain of a kinase-associated protein complexed with a proline-rich peptide. Nature, 382, 646-649 (1996) (Pubitemid 26268960)
53. H. I. Chen, A. Einbond, S. J. Kwak, H. Linn, E. Koepf, S. Peterson, J. W. Kelly and M. Sudol: Characterization of the WW domain of human Yesassociated protein and its polyproline- containing ligands. J Biol Chem, 272, 17070-17077 (1997) (Pubitemid 27289814)
54. E. K. Koepf, H. M. Petrassi1, M. Sudol, and J. W. Kelly: WW: An isolated three-stranded antiparallel beta-sheet domain that unfolds and refolds reversibly; evidence for a structured hydrophobic cluster in urea and GdnHCl and a disordered thermal unfolded state. Protein Science, 8(4), 841-853 (1999) (Pubitemid 29165414)
55. R. J. Ingham, K. Colwill, C. Howard, S. Dettwiler, C. S. H. Lim, J. Yu, K. Hersi, J. Raaijmakers, G. Gish, G. Mbamalu, L. Taylor, B. Yeung, G. Vassilovski, M. Amin, F. Chen, L. Matskova, G. Winberg, I. Ernberg, R. Linding, P. O'Donnell, A. Starostine, W. Keller, P. Metalnikov, C. Stark, and T. Pawson: WW Domains provide a platform for the assembly of multiprotein networks. Mol Cell Biol, 25(16), 7092-7106 (2005) (Pubitemid 41105907)
56. M. Sudol, C. C. Recinos, J. Abraczinskas, J. Humbert, and A. Farooq: WW or WoW: the WW domains in a union of bliss. IUBMB Life, 7,773-8 (2005) (Pubitemid 43062397)
57. K. Wang, C. Degerny, M. Xu, and X. J.Yang: YAP, TAZ, and Yorkie: a conserved family of signalresponsive transcriptional coregulators in animal development and human disease. Biochem Cell Biol, 87(1), 77-91(2009)
58. N. S. Chang, L. Schultz, L. J. Hsu, J. Lewis, M. Su, and C. I. Sze: 17beta-Estradiol upregulates and activates WOX1/WWOXv1 and WOX2/WWOXv2 in vitro: potential role in cancerous progression of breast and prostate to a premetastatic state in vivo. Oncogene, 24(4), 714-23 (2005) (Pubitemid 40188576)
59. Q. Hong, C. I. Sze, S. R. Lin, M.H. Lee, R. Y. He, L. Schultz, J. Y. Chang, S. J. Chen, R. J. Boackle, L.J. Hsu, N.S. Chang: Complement C1q activates tumor suppressor WWOX to induce apoptosis in prostate cancer cells. PLoS One, 4(6):e5755 (2009)
60. W. Chan, R. Tian, Y. F. Lee, S. T. Sit, L. Lim, and E. Manser: Down-regulation of active ACK1 is mediated by association with the E3 ubiquitin ligase Nedd4-2. J Biol Chem, 284(12), 8185-94(2009)
61. J. Y. Chang, R. Y. He, H. P. Lin, L. J. Hsu, F. J. Lai, Q. Hong, S. J. Chen, and N. S. Chang: Signaling from membrane receptors to tumor suppressor WW domain-containing oxidoreductase. Exp Biol Med, 235(7), 796-804 (2010)
62. A.N. Hegde and S.C. Upadhya: The ubiquitin- proteasome pathway in health and disease of the nervous system. TRENDS in Neurosciences, 30(11), 587-595 (2007) (Pubitemid 350051423)
63. Y. Kato, K. Nagata, M. Takahashi, L. Lian, J. J. Herrero, M. Sudol, and M. Tanokura: Common mechanism of ligand recognition by group II/III WW domains: redefining their functional classification. J Biol Chem, 279(30), 31833-41(2004)
64. M. I. Behrens, C. Lendon, and C. M. Roe: A common biological mechanism in cancer and Alzheimer's disease? Curr Alzheimer Res, 6 (3), 196- 204 (2009)
65. G. Finn and K. P. Lu: Phosphorylation-specific prolyl isomerase Pin1 as a new diagnostic and therapeutic target for cancer. Curr Cancer Drug Targets, 8(3), 223-9 (2008) (Pubitemid 351666858)
66. S. Esnault, Z. J. Shen, and J.S. Malter: Pinning down signaling in the immune system: the role of the peptidyl-prolyl isomerase Pin1 in immune cell function. Crit Rev Immunol, 28(1), 45-60 (2008) (Pubitemid 351264074)
67. H. L. Li, H. H. Wang, S. J.Liu, Y. Q. Deng, Y.J. Zhang, Q. Tian, X.C. Wang, X.Q. Chen, Y. Yang, J. Y. Zhang, J. Y. Wang, H. Xu, F.F. Liao, and J. Z. Wang: Phosphorylation of tau antagonizes apoptosis by stabilizing beta-catenin, a mechanism involved in Alzheimer's neurodegeneration. Proc Natl Acad Sci USA, 104(9), 3591-3596 (2007) (Pubitemid 46364203)
68. G. Drewes, B. Trinczek, S. Illenberger, J. Biernat, G. Schmitt-Ulms, H. E. Meyer, E. M. Mandelkow, and E. Mandelkow: Microtubule-associated protein/microtubule affinity-regulating kinase (p110mark). A novel protein kinase that regulates tau-microtubule interactions and dynamic instability by phosphorylation at the Alzheimer-specific site serine 262. J Biol Chem, 270(13), 7679-7688 (1995)
69. F. Liu, K. Iqbal, I. Grundke-Iqbal, G. W. Hart, and C. X. Gong: O-GlcNAcylation regulates phosphorylation of tau: amechanism involved in Alzheimer's disease. Proc Natl Acad Sci U.S.A, 101, 10804-10809 (2004a) (Pubitemid 38955823)
70. S. J. Liu, J.Y. Zhang, H. L. Li, Z. Y. Fang, Q. Wang, H. M. Deng, C. X. Gong, I. Grundke-Iqbal, K. Iqbal, and J. Z. Wang: Tau becomes amore favorable substrate for GSK-3 when it is prephosphorylated by PKA in rat brain. J Biol Chem, 279(48), 50078- 50088 (2004b) (Pubitemid 39577819)
71. C.H. Reynolds, J. C. Betts, W. P. Blackstock, A. R. Nebreda, and B. H. Anderton: Phosphorylation sites on tau identified by nanoelectrospray mass spectrometry:differences in vitro between the mitogen-activated protein kinases ERK2, c-Jun N-terminal kinase and P38, and glycogen synthase kinase-3beta. J Neurochem, 74(4), 1587-1595(2000) (Pubitemid 30163980)
72. T. J. Singh, J. Z. Wang, M. Novak, E. Kontzekova, I. Grundke-Iqbal, and K. Iqbal: Calcium/calmodulin-dependent protein kinase II phosphorylates tau at Ser-262 but only partially inhibits its binding to microtubules. FEBS Lett, 387(2-3), 145-148 (1996) (Pubitemid 26178911)
73. H. Yamamoto, Y. Hiragami, M. Murayama, K. Ishizuka, M. Kawahara, and A. Takashima: Phosphorylation of tau at serine 416 by Ca2+/calmodulin-dependent protein kinase II in neuronal soma in brain. J Neurochem, 94(5), 1438- 1447(2005) (Pubitemid 41232599)
74. T. Horiguchi, K. Uryu, B. I. Giasson, H. Ischiropoulos, R. LightFoot, C. Bellmann, C. Richter-Landsberg, V. M. Lee, and J. Q. Trojanowski: Nitration of tau protein is linked to neurodegeneration in tauopathies. Am J Pathol, 163(3), 1021-1031(2003) (Pubitemid 37040138)
75. C. Richter-Landsberg and O. Goldbaum: Stress proteins in neural cells: functional roles in health and disease. Cell Mol Life Sci, 60(2), 337-49 (2003) Review (Pubitemid 36343913)
76. J. N. Keller, K.B. Hanni, and W.R. Markesbery: Impaired proteasome function in Alzheimer'sdisease. J Neurochem, 75(1), 436-439 (2000)
77. Y. J. Zhang, Y. F. Xu, X. H. Liu, D. Li, J. Yin, Y. H. Liu, X.Q. Chen, and J.Z. Wang: Carboxyl terminus of heat-shock cognate 70-interacting protein degrades tau regardless it phosphorylation status without affecting the spatial memory of the rats. J Neural Transmission, 115(3), 483-491(2008)
78. J. J. Lucas, F. Herná ndez, P. Gó mez-Ramos, M. A. Morá n, R. Hen, J. Avila: Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J, 20, 27-39 (2001) (Pubitemid 32099099)
79. L. Q. Zhu, S. H. Wang, D. Liu, Y. Y. Yin, Q. Tian, X. C. Wang, Q. Wang, J.G. Chen, and J.Z. Wang: Activation of glycogen synthase kinase-3 inhibits long-term potentiation with synapseassociated impairments. J Neurosci, 27,12211-12220 (2007) (Pubitemid 350085482)
80. Z. F. Wang, H. L. Li, X. C. Li, Q. Zhang, Q. Tian, Q. Wang, H. Xu, and J.Z. Wang: Effects of endogenous beta-amyloid overproduction on tau phosphorylation in cell culture. J Neurochem, 98(4), 1167-1175 (2006) (Pubitemid 44127792)
81. Y.J. Zhang, Y. F. Xu, Y. H. Liu, J. Yin, H. L. Li, Q. Wang, and J.Z. Wang: Peroxynitrite induces Alzheimer-like tau modifications and accumulation in rat brain and its underlying mechanisms. FASEB J, 20(9), 1431-1442 (2006) (Pubitemid 44943851)
82. J. Z. Wang and F. Liu: Microtubule-associated protein tau in development, degeneration and protection of neurons. Progress in Neurobiology, 85(2), 148-175(2008)
83. J. Avila, I. Santa-María, M. Pé rez, F. Herná ndez, and F. Moreno: Tau phosphorylation, aggregation, and cell toxicity. J Biomed Biotechnol, 2006,74539 (2006)
84. I. Khlistunova, J. Biernat, Y. Wang, M. Pickhardt, M. von Bergen, Z. Gazova, E. Mandelkow, and E. M. Mandelkow: Inducible expression of tau repeat domain in cell models of tauopathy: aggregation is toxic to cells but can be reversed by inhibitor drugs. J Biol Chem, 281(2), 1205-1214 (2006)
85. Y. P. Wang, J. Biernat, M. Pickhardt, E. Mandelkow, and E.M. Mandelkow: Stepwise proteolysis liberates tau fragments that nucleate the Alzheimer-like aggregation of full-length tau in a neuronal cell model. Proc Natl Acad Sci USA, 104(24), 10252-10257(2007) (Pubitemid 47175295)
86. K. Santacruz, J. Lewis, T. Spires, J. Paulson, L. Kotilinek, M. Ingelsson, A. Guimaraes, M. DeTure, E. Ramsden McGowan, C. Forster, M. Yue, J. Orne, C. Janus, A. Mariash, M. Kuskowski, B. Hyman, M. Hutton, and H. Ashe: Tau suppression in a neurodegenerative mouse model improves memory function. Science, 309(5733), 476- 481(2005) (Pubitemid 40994688)
87. A. C. Alonso, B. Li, I. Grundke-Iqbal, and K. Iqbal: Polymerization of hyperphosphorylated tau into filaments eliminates its inhibitory activity. Proc Natl Acad Sci USA, 103(23), 8864- 8869 (2006) (Pubitemid 43878109)
88. C. Andorfer, C. M. Acker, Y. Kress, P. R. Hof, K. Duff, and P. Davies: Cell-cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms. J Neurosci, 25(22), 5446- 5454 (2005) (Pubitemid 40770926)
89. T. L. Spires, J. D. Orne, K. SantaCruz, R. Pitstick, G. A. Carlson, K. H. Ashe, and B. T. Hyman: Region-specific dissociation of neuronal loss and neurofibrillary pathology in a mouse model of tauopathy. Am J Pathol, 168(5), 1598-1607(2006)
90. A. Gomez-Ramos, J. Diaz-Nido, M. A. Smith, G. Perry, J. Avila: Effect of the lipid peroxidation product acrolein on tau phosphorylation in neural cells. J Neurosci Res, 71(6), 863-870 (2003) (Pubitemid 36293007)
91. A. Sultan, F. Nesslany, M.Violet, S. Bégard, A. Loyens, S, Talahari, Z. Mansuroglu, D. Marzin, N. Sergeant, S. Humez, M. Colin, E. Bonnefoy, L. Buée, and M. C. Galas: Nuclear Tau, a Key Player in Neuronal DNA Protection. J Biol Chem, 286 (6), 4566-4575(2011)
92. H. G. Lee, G. Perry, P. I. Moreira, M. R. Garrett, Q. Liu, X. Zhu, A. Takeda, A. Nunomura, and M.A. Smith: Tau phosphorylation in Alzheimer's disease: pathogen or protector? Trends Mol Med, 11,164-169
93. R. J. Castellani, H. G. Lee, X. Zhu, A. Nunomura, G. Perry, M.A. Smith: Neuropathology of Alzheimer disease: pathognomonic but not pathogenic. Acta Neuropathol, 111(6), 503-509 (2006) (Pubitemid 43778954)
94. M. H. Maurer, J.O. Brömme, R. E. Feldmann, Jr., A. Järve, F. Sabouri, H. F. Bürgers, D.W. Schelshorn, C. Krüger, A. Schneider, and W. Kuschinsky: Glycogen synthase kinase 3beta (GSK3beta) regulates differentiation and proliferation in neural stem cells from the rat subventricular zone. J Proteome Res, 6 (3), 1198-1208 (2007) (Pubitemid 46480485)
95. F. Massoud and S. Gauthier: Update on the Pharmacological Treatment of Alzheimer's Disease. Curr Neuropharmacol, 8(1), 69-80 (2010)
96. R. A. Boonen, P. van Tijn, and D. Zivkovic: Wnt signaling in Alzheimer's disease: up or down, that is the question. Ageing Res Rev, 8(2), 71-82 (2009)
97. W. Noble, E. Planel, C. Zehr, V.Olm, J. Meyerson, F. Suleman, K. Gaynor, L. Wang, J. LaFrancois, B. Feinstein, M. Burns, P.Krishnamurthy, Y. Wen, R. Bhat, J. Lewis, D.Dickson, and K. Duff: Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo. Proc Natl Acad Sci USA, 102, 6990-6995 (2005) (Pubitemid 40675429)
98. Y. Wang, J. X. Zhang, X. X. Du, L. Zhao, Q. Tian, L.Q. Zhu, S. H. Wang, J. Z. Wang: Temporal correlation of the memory deficit with Alzheimer-like lesions induced by activation of glycogen synthase kinase-3. J Neurochem, 106(6), 2364-2374(2008)
99. O. V. Forlenza, J. M. Spink, R. Dayanandan, B. H. Anderton, O. F. Olesen, and S. Lovestone: Muscarinic agonists reduce tau phosphorylation in non-neuronal cells via GSK-3beta inhibition and in neurons. J Neural Transm 107(10), 1201-1212 (2000)
100. R. V. Bhat and S. L.Budd: GSK3beta signaling: casting a wide net in Alzheimer's disease. Neurosignals, 11(5), 251-261(2002) (Pubitemid 37494392)
101. M. Rapoport, H. N. Dawson, L. I. Binder, M. P. Vitek, and A. Ferreira: Tau is essential to betaamyloid- induced neurotoxicity. Proc Natl Acad Sci U S A, 99(9), 6364-6369(2002) (Pubitemid 34493317)
102. R. W. Shin, K. Ogino, A. Shimabuku, T. Taki, H. Nakashima, T. Ishihara, and T. Kitamoto: Amyloid precursor protein cytoplasmic domain with phospho- Thr668 accumulates in Alzheimer's disease and its transgenic models: a role to mediate interaction of Abeta and tau. Acta Neuropathol, 113(6), 627-636(2007) (Pubitemid 46863899)
103. D. Muyllaert, A. Kremer, T. Jaworski, P. Borghgraef, H. Devijver, S. Croes, I. Dewachter, and F. Van Leuven: Glycogen synthase kinase-3beta, or a link between amyloid and tau pathology? Genes Brain Behav, 7 (Suppl 1), 57-66(2008)
104. T. Engel, J. J. Lucas, P. G'omez-Ramos, M.A. Moran, J. Avila, and F. Herńandez: Cooexpression of FTDP-17 tau and GSK-3beta in transgenic mice induce tau polymerization and neurodegeneration. Neurobiol Aging, 27(9), 1258-1268 (2006) (Pubitemid 44088576)
105. K. Leroy, Z. Yilmaz, and J. P. Brion: Increased level of active GSK-3beta in Alzheimer's disease and accumulation in argyrophilic grains and in neurons at different stages of neurofibrillary degeneration. Neuropathol Appl Neurobiol, 33(1), 43-55 (2007) (Pubitemid 46090309)
106. Y. T. Lin, J. T. Cheng, L. C. Liang, C. Y. Ko, Lo YK, and P. J. Lu: The binding and phosphorylation of Thr231 is critical for Tau's hyperphosphorylation and functional regulation by glycogen synthase kinase 3beta. J Neurochem, 103(2), 802-813(2007)
107. S. Miranda, C. Opazo, L. F. Larrondo, F. J. Muñoz, F. Ruiz, F. Leighton, and N. C. Inestrosa: The role of oxidative stress in the toxicity induced by amyloid beta-peptide in Alzheimer's disease. Prog Neurobiol, 62(6), 633-648(2000) (Pubitemid 30407138)
108. D. A. Butterfield, M. Perluigi, and R. Sultana: Oxidative stress in Alzheimer's disease brain: new insights from redox proteomics. Eur J Pharmacol, 545(1), 39-50 (2006) (Pubitemid 44215876)
109. I.G. Onyango and S. M. Khan: Oxidative stress, mitochondrial dysfunction, and stress signaling in Alzheimer's disease. Curr Alzheimer Res 3(4), 339-349(2006) (Pubitemid 44351477)
110. H. Kadowaki, H. Nishitoh, F. Urano, C. Sadamitsu, A. Matsuzawa, K. Takeda, H. Masutani, J. Yodoi, Y. Urano, T. Nagano, and H. Ichijo: Amyloid beta induces neuronal cell death through ROSmediated ASK1 activation. Cell Death Differ, 12(1), 19-24(2005) (Pubitemid 40090025)
111. C. Atzori, B. Ghetti, R. Piva, A. N. Srinivasan, P. Zolo, M. B. Delisle, S. S. Mirra, and A. Migheli: Activation of the JNK/p38 pathway occurs in diseases characterized by tau protein pathology and is related to tau phosphorylation but not to apoptosis. J Neuropathol Exp Neurol, 60(12), 1190-1197(2001) (Pubitemid 33117099)
112. M. J. Savage, Y. G. Lin, J.R. Ciallella, D. G. Flood, and R. W. Scott: Activation of c-Jun Nterminal kinase and p38 in an Alzheimer's disease model is associated with amyloid deposition. J Neurosci, 22(9), 3376-3385(2002) (Pubitemid 37465743)
113. H. Lassmann, C. Bancher, H. Breitschopf, J. Wegiel, M. Bobinski, K. Jellinger, and H. M. Wisniewski: Cell death in Alzheimer's disease evaluated by DNA fragmentation in situ. Acta Neuropathol, 89(1), 35-41(1995)
114. D. Y.Loo, A. Copani, C. J. Pike, E. R. Whittemore, A. J. Walencewicz, and C. W. Cotman: Apoptosis is induced by beta-mamyloid in cultured central nervous system neurons. Proc Natl Acad Sci U S A, 90, 7951-7955(1993) (Pubitemid 23260832)
115. K. Agerman, C. Baudet, B. Fundin, C. Willson, and P. Ernfors: Attenuation of a caspase-3 dependent cell death in NT4- and p75-deficient embryonic sensory neurons. Mol Cell Neurosci, 16(3), 258- 268(2000)
116. K. T. Akama, C. Albanese, R. G. Pestell, and L. J. Van Eldik: Amyloid b-peptide stimulates nitric oxide production in astrocytes through an NFkappaBdependent mechanism. Proc Natl Acad Sci U S A, 95(10), 5795-5800(1998) (Pubitemid 28224176)
117. O. Ghribi, M. M. Herman, D. A. DeWitt, M. S. Forbes, and J. Savory: Ab (1-42) and aluminum induce stress in the endoplasmic reticulum in rabbit hippocampus, involving nuclear translocation of gadd 153 and NF-B. Brain Res Mol Brain Res, 96(1-2), 30-38(2001) (Pubitemid 33145361)
118. Y. Shen, P. He, Z. Zhong, C. McAllister, and K. Lindholm: Distinct destructive signaling pathways of neuronal death in Alzheimer's disease. TRENDS in Molecular Medicine, 12(12), 574-579(2006) (Pubitemid 44780197)
119. T. T. Rohn, R. A. Rissman, E. Head, and C.W. Cotman: Caspase activation in the Alzheimer's disease brain: tortuous and torturous. Drug News Perspect, 15(9), 549-557(2002) (Pubitemid 36025540)
120. C. Lanni, L. Nardinocchi, R. Puca, S. Stanga, D. Uberti, M. Memo, S. Govoni, G. D'Orazi, and M. Racchi: Homeodomain interacting protein kinase 2: A target for Alzheimer's beta amyloid leading to misfolded p53 and inappropriate cell survival. PLoS ONE, 5(4): e10171(2010)
121. S. Stanga, C.Lanni, S. Govoni, D. Uberti, G. D'Orazi, and M. Racchi: Unfolded p53 in the pathogenesis of Alzheimer's disease: is HIPK2 the link? Aging, 2 (9), 545-554(2010)
122. C. Lanni, M. Racchi, G. Mazzini, A. Ranzenigo, R. Polotti, E. Sinforiani, L. Olivari, M. Barcikowska, M. Styczynska, J. Kuznicki, A. Szybinska, S. Govoni, M. Memo, and D. Uberti: Conformationally altered p53: a novel Alzheimer's disease marker? Molecular Psychiatry, 13, 641-647(2008) (Pubitemid 351704936)
123. H. Jiang, D. Burdick, C. G. Glabe, C. W. Cotman, and A. J. Tenner: Beta-Amyloid activates complement by binding to a specific region of the collagen-like domain of the C1q A chain. J Immunol 152(10), 5050-5059(1994)
124. M. I. Fonseca, S. H. Chu, A. M. Berci, M.E. Benoit, D. G. Peters, Y. Kimura, and A. J. Tenner: Contribution of complement activation pathways to neuropathology differs among mouse models of Alzheimer's disease. J Neuroinflammation, 8(4), 1-12 (2011)
125. A. J. Tenner: Complement in Alzheimer's disease: opportunities for modulating protective and pathogenic events. Neurobiol Aging, 22(6), 849- 861(2001) (Pubitemid 34066552)
126. Y. Shen, L. Lue, L. Yang, A. Roher, Y. Kuo, R. Strohmeyer, W. J. Goux, V. Lee, G. V. Johnson, S. D. Webster, N. R. Cooper, B. Bradt, and J.Rogers: Complement activation by neurofibrillary tangles in Alzheimer's disease. Neurosci Lett, 305(3), 165-168(2001) (Pubitemid 32525831)
127. A. Afagh, B. J. Cummings, D. H. Cribbs, C. W. Cotman, and A. J. Tenner: Localization and cell association of C1q in Alzheimer's disease brain. Exp Neurol, 138(1), 22-32(1996) (Pubitemid 26107986)
128. S. E. Stoltzner, T. J. Grenfell, C. Mori, K. E. Wisniewski, T. M. Wisniewski, D. J. Selkoe, and C. A. Lemere: Temporal accrual of complement proteins in amyloid plaques in Down's syndrome with Alzheimer's disease. Am J Pathol, 156(2), 489- 499(2000) (Pubitemid 30643804)
129. M. H. Lee, S.R. Lin, J. Y. Chang, L. Schultz, J. Heath, L. J. Hsu, Y. M. Kuo, Q. Hong, M. F. Chiang, C. X. Gong, C. I. Sze, and N-S Chang: TGF-beta induces TIAF1 self-aggregation via type II receptorindependent signaling that leads to generation of amyloid beta plaques in Alzheimer's disease. Cell Death and Disease, 1, e110 (2010)
130. T. Burton, B. Liang, A. Dibrov, and F. Amara: Transforming growth factor-beta-induced transcription of the Alzheimer beta-amyloid precursor protein gene involves interaction between the CTCFcomplex and Smads. Biochem Biophys Res Commun, 295(3), 713- 723(2002) (Pubitemid 34756908)
131. F. Docagne, C. Gabriel, N. Lebeurrier, S. Lesne, Y. Hommet, L. Plawinski, E. T. Mackenzie, and D. Vivien: Sp1 and Smad transcription factors cooperate to mediate TGF-beta-dependent activation of amyloid-beta precursor protein gene transcription. Biochem J, 383(pt-2), 393- 399 (2004) (Pubitemid 39446701)
132. U. Ueberham, E. Ueberham, M. K. Bruckner, G. Seeger, U. Gartner, H. Gruschka, R. Gebhardt, T. Arendt: Inducible neuronal expression of transgenic TGF-beta1 in vivo: dissection of short-term and longterm effects. Eur J Neurosci, 22(1), 50-64(2005) (Pubitemid 41059971)
133. A. G. Henriques, S. I. Vieira, E. F. da Cruz e Silva, and O. A. B. da Cruz e Silva: Abeta hinders nuclear targeting of AICD and Fe65 in primary neuronal cultures. J Mol Neurosci, 39, 248- 255(2009)
134. Caspi M, Zilberberg A, Eldar-Finkelman H, Rosin-Arbesfeld R. Nuclear GSK-3beta inhibits the canonical Wnt signaling pathway in a beta-catenin phosphorylation -independent manner. Oncogene, 27(25), 3546-55(2008)
135. S. Del Mare, Z. Salah, and R. I. Aqeilan: WWOX: Its Genomics, Partners, and Functions. J Cell Biochem, 108, 737-745(2009)