Phosphorylation of protein Tau by GSK3β prolongs survival of bigenic Tau.P301L×GSK3β mice by delaying brainstem tauopathy

Neurobiology of Disease

Volumn 67, Issue , 2014, Pages 119-132

  Crespo Biel, Natalia ^a   Theunis, Clara ^a   Borghgraef, Peter ^a   Lechat, Benoit ^a   Devijver, Herman ^a   Maurin, Hervé ^a   Van Leuven, Fred ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Brainstem; GSK3; Protein Tau; Survival; Tauopathy

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; OLIGOMER; TAU PROTEIN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA;

ADULT; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; FOREBRAIN; GENOTYPE; MALE; MORTALITY; MOUSE; NEUROFIBRILLARY TANGLE; NEUROPIL THREAD; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN PHOSPHORYLATION; TAUOPATHY; ANIMAL; BRAIN; CHEMISTRY; ENZYMOLOGY; METABOLISM; PHOSPHORYLATION; SURVIVAL; TRANSGENIC MOUSE;

ANIMALS; BRAIN; BRAIN STEM; FEMALE; GLYCOGEN SYNTHASE KINASE 3; MALE; MICE; MICE, TRANSGENIC; PHOSPHORYLATION; SURVIVAL ANALYSIS; TAU PROTEINS; TAUOPATHIES;

EID: 84899052077     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.03.016     Document Type: Article

References (74)

1. Allen B., Ingram E., Takao M., Smith M.J., Jakes R., Virdee K., Yoshida H., Holzer M., Craxton M., Emson P.C., Atzori C., Migheli A., Crowther R.A., Ghetti B., Spillantini M.G., Goedert M. Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein. J. Neurosci. 2002, 22:9340-9351.
2. Andorfer C., Kress Y., Espinoza M., de Silva R., Tucker K.L., Barde Y.A., Duff K., Davies P. Hyperphosphorylation and aggregation of tau in mice expressing normal human tau isoforms. J. Neurochem. 2003, 86:582-590.
3. Arriagada P.V., Growdon J.H., Hedley-Whyte E.T., Hyman B.T. Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 1992, 42:631-639.
4. Augustinack J.C., Schneider A., Mandelkow E.M., Hyman B.T. Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer's disease. Acta Neuropathol. 2002, 103:26-35.
5. Avila J., de Barreda E.G., Engel T., Lucas J.J., Hernandez F. Tau phosphorylation in hippocampus results in toxic gain-of-function. Biochem. Soc. Trans. 2010, 38:977-980.
6. Berger Z., Roder H., Hanna A., Carlson A., Rangachari V., Yue M., Wszolek Z., Ashe K., Knight J., Dickson D., Andorfer C., Rosenberry T.L., Lewis J., Hutton M., Janus C. Accumulation of pathological tau species and memory loss in a conditional model of tauopathy. J. Neurosci. 2007, 27:3650-3662.
7. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991, 4:239-259.
8. Cowan C.M., Mudher A. Are Tau aggregates toxic or protective in tauopathies?. Front. Neurol. 2013, 4:114.
9. Crespo-Biel N., Theunis C., Van Leuven F. Protein tau: prime cause of synaptic and neuronal degeneration in Alzheimer's disease. Int. J. Alzheimers Dis. 2012, 2012:251426.
10. de Calignon A., Fox L.M., Pitstick R., Carlson G.A., Bacskai B.J., Spires-Jones T.L., Hyman B.T. Caspase activation precedes and leads to tangles. Nature 2010, 464:1201-1204.
11. Delacourte A., Sergeant N., Wattez A., Maurage C.A., Lebert F., Pasquier F., David J.P. Tau aggregation in the hippocampal formation: an ageing or a pathological process?. Exp. Gerontol. 2002, 10-11:1291-1296.
12. Delobel P., Lavenir I., Fraser G., Ingram E., Holzer M., Ghetti B., Spillantini M.G., Crowther R.A., Goedert M. Analysis of tau phosphorylation and truncation in a mouse model of human tauopathy. Am. J. Pathol. 2008, 172:123-131.
13. Denk F., Wade-Martins R. Knock-out and transgenic mouse models of tauopathies. Neurobiol. Aging 2009, 30:1-13.
14. Dewachter I., Ris L., Jaworski T., Seymour C.M., Kremer A., Borghgraef P., De V.H., Godaux E., Van Leuven F. GSK3beta, a centre-staged kinase in neuropsychiatric disorders, modulates long term memory by inhibitory phosphorylation at serine-9. Neurobiol. Dis. 2009, 35:193-200.
15. Ding H., Johnson G.V. The last tangle of tau. J. Alzheimers Dis. 2008, 4:441-447.
16. Ding H., Matthews T.A., Johnson G.V. Site-specific phosphorylation and caspase cleavage differentially impact tau-microtubule interactions and tau aggregation. J. Biol. Chem. 2006, 281:19107-19114.
17. Dutschmann M., Menuet C., Stettner G.M., Gestreau C., Borghgraef P., Devijver H., Gielis L., Hilaire G., Van Leuven F. Upper airway dysfunction of Tau-P301L mice correlates with tauopathy in midbrain and ponto-medullary brainstem nuclei. J. Neurosci. 2010, 30:1810-1821.
18. Duyckaerts C., Potier M.C., Delatour B. Alzheimer disease models and human neuropathology: similarities and differences. Acta Neuropathol. 2008, 115:5-38.
19. Duyckaerts C., Delatour B., Potier M.C. Classification and basic pathology of Alzheimer disease. Acta Neuropathol. 2009, 118:5-36.
20. Gandy J.C., Melendez-Ferro M., Bijur G.N., Van Leuven F., Roche J.K., Lechat B., Devijver H., Demedts D., Perez-Costas E., Roberts R.C. Glycogen synthase kinase-3beta (GSK3beta) expression in a mouse model of Alzheimer's disease: a light and electron microscopy study. Synapse 2013, 67:313-327.
21. Ganguli M., Dodge H.H., Shen C., Pandav R.S., DeKosky S.T. Alzheimer disease and mortality: a 15-year epidemiological study. Arch. Neurol. 2005, 62:779-784.
22. Giannakopoulos P., Herrmann F.R., Bussiere T., Bouras C., Kovari E., Perl D.P., Morrison J.H., Gold G., Hof P.R. Tangle and neuron numbers, but not amyloid load, predict cognitive status in Alzheimer's disease. Neurology 2003, 60:1495-1500.
23. Goedert M., Crowther R.A., Spillantini M.G. Tau mutations cause frontotemporal dementias. Neuron 1998, 21:955-958.
24. Gomez-Isla T., Hollister R., West H., Mui S., Growdon J.H., Petersen R.C., Parisi J.E., Hyman B.T. Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. Ann. Neurol. 1997, 41:17-24.
25. Gotz J., Ittner L.M. Animal models of Alzheimer's disease and frontotemporal dementia. Nat. Rev. Neurosci. 2008, 9:532-544.
26. Guillozet-Bongaarts A.L., Cahill M.E., Cryns V.L., Reynolds M.R., Berry R.W., Binder L.I. Pseudophosphorylation of tau at serine 422 inhibits caspase cleavage: in vitro evidence and implications for tangle formation in vivo. J. Neurochem. 2006, 97:1005-1014.
27. Gustke N., Steiner B., Mandelkow E.M., Biernat J., Meyer H.E., Goedert M., Mandelkow E. The Alzheimer-like phosphorylation of tau protein reduces microtubule binding and involves Ser-Pro and Thr-Pro motifs. FEBS Lett. 1992, 307:199-205.
28. Hanger D.P., Anderton B.H., Noble W. Tau phosphorylation: the therapeutic challenge for neurodegenerative disease. Trends Mol. Med. 2009, 15:112-119.
29. Hernandez F., de Barreda E.G., Fuster-Matanzo A., Lucas J.J., Avila J. GSK3: a possible link between beta amyloid peptide and tau protein. Exp. Neurol. 2010, 223:322-325.
30. Heutink P. Untangling tau-related dementia. Hum. Mol. Genet. 2000, 6:979-986.
31. Hong M., Zhukareva V., Vogelsberg-Ragaglia V., Wszolek Z., Reed L., Miller B.I., Geschwind D.H., Bird T.D., McKeel D., Goate A., Morris J.C., Wilhelmsen K.C., Schellenberg G.D., Trojanowski J.Q., Lee V.M. Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 1998, 282:1914-1917.
32. Hutton M., Lendon C.L., Rizzu P., Baker M., Froelich S., Houlden H., Pickering-Brown S., Chakraverty S., Isaacs A., Grover A., Hackett J., Adamson J., Lincoln S., Dickson D., Davies P., Petersen R.C., Stevens M., de Graaff E., Wauters E., van Baren J., Hillebrand M., Joosse M., Kwon J.M., Nowotny P., Che L.K., Norton J., Morris J.C., Reed L.A., Trojanowski J., Basun H., Lannfelt L., Neystat M., Fahn S., Dark F., Tannenberg T., Dodd P.R., Hayward N., Kwok J.B., Schofield P.R., Andreadis A., Snowden J., Craufurd D., Neary D., Owen F., Oostra B.A., Hardy J., Goate A., Van Swieten J., Mann D., Lynch T., Heutink P. Association of missense and 5'-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 1998, 393:702-705.
33. Ishiguro K., Omori A., Takamatsu M., Sato K., Arioka M., Uchida T., Imahori K. Phosphorylation sites on tau by tau protein kinase I, a bovine derived kinase generating an epitope of paired helical filaments. Neurosci. Lett. 1992, 148:202-206.
34. Ittner L.M., Gotz J. Amyloid-beta and tau-a toxic pas de deux in Alzheimer's disease. Nat. Rev. Neurosci. 2011, 12:65-72.
35. Jaworski T., Dewachter I., Seymour C.M., Borghgraef P., Devijver H., Kugler S., Van Leuven F. Alzheimer's disease: old problem, new views from transgenic and viral models. Biochim. Biophys. Acta 2010, 1802:808-818.
36. Jaworski T., Kugler S., Van Leuven F. Modeling of tau-mediated synaptic and neuronal degeneration in Alzheimer's disease. Int. J. Alzheimers Dis. 2010, 2010.
37. Jicha G.A., Bowser R., Kazam I.G., Davies P. Alz-50 and MC-1, a new monoclonal antibody raised to paired helical filaments, recognize conformational epitopes on recombinant tau. J. Neurosci. Res. 1997, 48:128-132.
38. Kalia M. Dysphagia and aspiration pneumonia in patients with Alzheimer's disease. Metabolism 2003, 52:36-38.
39. Kremer A., Louis J.V., Jaworski T., Van Leuven F. GSK3 and Alzheimer's disease: facts and fiction.. .. Front. Mol. Neurosci. 2011, 4:17.
40. Kremer A., Maurin H., Demedts D., Devijver H., Borghgraef P., Van Leuven F. Early improved and late defective cognition is reflected by dendritic spines in Tau.P301L mice. J. Neurosci. 2011, 31:18036-18047.
41. Lasagna-Reeves C.A., Castillo-Carranza D.L., Sengupta U., Sarmiento J., Troncoso J., Jackson G.R., Kayed R. Identification of oligomers at early stages of tau aggregation in Alzheimer's disease. FASEB J. 2012, 26:1946-1959.
42. Lewis J., McGowan E., Rockwood J., Melrose H., Nacharaju P., Van Slegtenhorst M., Gwinn-Hardy K., Murphy P.M., Baker M., Yu X., Duff K., Hardy J., Corral A., Lin W.L., Yen S.H., Dickson D.W., Davies P., Hutton M. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat. Genet. 2000, 25:402-405.
43. Lewis J., Dickson D.W., Lin W.L., Chisholm L., Corral A., Jones G., Yen S.H., Sahara N., Skipper L., Yager D., Eckman C., Hardy J., Hutton M., McGowan E. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 2001, 293:1487-1491.
44. Lochhead P.A., Kinstrie R., Sibbet G., Rawjee T., Morrice N., Cleghon V. A chaperone-dependent GSK3beta transitional intermediate mediates activation-loop autophosphorylation. Mol. Cell 2006, 24:627-633.
45. Mandelkow E.M., Drewes G., Biernat J., Gustke N., Van Lint J., Vandenheede J.R., Mandelkow E. Glycogen synthase kinase-3 and the Alzheimer-like state of microtubule-associated protein tau. FEBS Lett. 1992, 314:315-321.
46. Maurin H., Seymour C.M., Lechat B., Borghgraef P., Devijver H., Jaworski T., Schmidt M.V., Kuegler S., Van Leuven F. Tauopathy differentially affects cell adhesion molecules in mouse brain: early down-regulation of nectin-3 in stratum lacunosum moleculare. PLoS One 2013, 8:e63589.
47. Menuet C., Borghgraef P., Matarazzo V., Gielis L., Lajard A.M., Voituron N., Gestreau C., Dutschmann M., Van Leuven F., Hilaire G. Raphe tauopathy alters serotonin metabolism and breathing activity in terminal Tau.P301L mice: possible implications for tauopathies and Alzheimer's disease. Respir. Physiol. Neurobiol. 2011, 178:290-303.
48. Menuet C., Borghgraef P., Voituron N., Gestreau C., Gielis L., Devijver H., Dutschmann M., Van Leuven F., Hilaire G. Isoflurane anesthesia precipitates tauopathy and upper airways dysfunction in pre-symptomatic Tau.P301L mice: possible implication for neurodegenerative diseases. Neurobiol. Dis. 2012, 46:234-243.
49. Mercken M., Vandermeeren M., Lubke U., Six J., Boons J., Van de Voorde A., Martin J.J., Gheuens J. Monoclonal antibodies with selective specificity for Alzheimer Tau are directed against phosphatase-sensitive epitopes. Acta Neuropathol. 1992, 84:265-272.
50. Morris M., Maeda S., Vossel K., Mucke L. The many faces of tau. Neuron 2011, 70:410-426.
51. Nelson P.T., Alafuzoff I., Bigio E.H., Bouras C., Braak H., Cairns N.J., Castellani R.J., Crain B.J., Davies P., Del Tredici K., Duyckaerts C., Frosch M.P., Haroutunian V., Hof P.R., Hulette C.M., Hyman B.T., Iwatsubo T., Jellinger K.A., Jicha G.A., Kövari E., Kukull W.A., Leverenz J.B., Love S., Mackenzie I.R., Mann D.M., Masliah E., McKee A.C., Montine T.J., Morris J.C., Schneider J.A., Sonnen J.A., Thal D.R., Trojanowski J.Q., Troncoso J.C., Wisniewski T., Woltjer R.L., Beach T.G. Correlation of Alzheimer disease neuropathologic changes with cognitive status: a review of the literature. J. Neuropathol. Exp. Neurol. 2012, 71:362-381.
52. Patterson K.R., Remmers C., Fu Y., Brooker S., Kanaan N.M., Vana L., Ward S., Reyes J.F., Philibert K., Glucksman M.J., Binder L.I. Characterization of prefibrillar Tau oligomers in vitro and in Alzheimer disease. J. Biol. Chem. 2011, 286:23063-23076.
53. Ramsden M., Kotilinek L., Forster C., Paulson J., McGowan E., SantaCruz K., Guimaraes A., Yue M., Lewis J., Carlson G., Hutton M., Ashe K.H. Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J. Neurosci. 2005, 25:10637-10647.
54. Rankin C.A., Sun Q., Gamblin T.C. Pre-assembled tau filaments phosphorylated by GSK-3b form large tangle-like structures. Neurobiol. Dis. 2008, 31:368-377.
55. Roberson E.D. Mouse models of frontotemporal dementia. Ann. Neurol. 2012, 72:837-849.
56. Sahara N., DeTure M., Ren Y., Ebrahim A.S., Kang D., Knight J., Volbracht C., Pedersen J.T., Dickson D.W., Yen S.H., Lewis J. Characteristics of TBS-extractable hyperphosphorylated Tau species: aggregation intermediates in rTg4510 mouse brain. J. Alzheimers Dis. 2013, 33:249-263.
57. Schindowski K., Bretteville A., Leroy K., Begard S., Brion J.P., Hamdane M., Buee L. Alzheimer's disease-like tau neuropathology leads to memory deficits and loss of functional synapses in a novel mutated tau transgenic mouse without any motor deficits. Am. J. Pathol. 2006, 169:599-616.
58. Schneider A., Biernat J., von Bergen M., Mandelkow E., Mandelkow E.M. Phosphorylation that detaches tau protein from microtubules (Ser262, Ser214) also protects it against aggregation into Alzheimer paired helical filaments. Biochemistry 1999, 38:3549-3558.
59. Sereno L., Coma M., Rodriguez M., Sanchez-Ferrer P., Sanchez M.B., Gich I., Agullo J.M., Perez M., Avila J., Guardia-Laguarta C., Clarimon J., Lleo A., Gomez-Isla T. A novel GSK-3beta inhibitor reduces Alzheimer's pathology and rescues neuronal loss in vivo. Neurobiol. Dis. 2009, 35:359-367.
60. Shi Y., Mowery R.A., Ashley J., Hentz M., Ramirez A.J., Bilgicer B., Slunt-Brown H., Borchelt D.R., Shaw B.F. Abnormal SDS-PAGE migration of cytosolic proteins can identify domains and mechanisms that control surfactant binding. Protein Sci. 2012, 21:1197-1209.
61. Spillantini M.G., Goedert M. Tau protein pathology in neurodegenerative diseases. Trends Neurosci. 1998, 10:428-433.
62. Spittaels K., Van den Haute C., Van Dorpe J., Bruynseels K., Vandezande K., Laenen I., Geerts H., Mercken M., Sciot R., Van Lommel A., Loos R., Van Leuven F. Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein. Am. J. Pathol. 1999, 155:2153-2165.
63. Spittaels K., Van den Haute C., Van Dorpe J., Geerts H., Mercken M., Bruynseels K., Lasrado R., Vandezande K., Laenen I., Boon T., Van Lint J., Vandenheede J., Moechars D., Loos R., Van Leuven F. Glycogen synthase kinase-3beta phosphorylates protein tau and rescues the axonopathy in the central nervous system of human four-repeat tau transgenic mice. J. Biol. Chem. 2000, 275:41340-41349.
64. Spittaels K., Van den Haute C., Van Dorpe J., Terwel D., Vandezande K., Lasrado R., Bruynseels K., Irizarry M., Verhoye M., Van Lint J., Vandenheede J.R., Ashton D., Mercken M., Loos R., Hyman B., Van der Linden A., Geerts H., Van Leuven F. Neonatal neuronal overexpression of glycogen synthase kinase-3 beta reduces brain size in transgenic mice. Neuroscience 2002, 113:797-808.
65. Takashima A. GSK-3 is essential in the pathogenesis of Alzheimer's disease. J. Alzheimers Dis. 2006, 9:309-317.
66. Tatebayashi Y., Planel E., Chui D.H., Sato S., Miyasaka T., Sahara N., Murayama M., Kikuchi N., Yoshioka K., Rivka R., Takashima A. c-jun N-terminal kinase hyperphosphorylates R406W tau at the PHF-1 site during mitosis. FASEB J. 2006, 20:762-764.
67. Terwel D., Dewachter I., Van Leuven F. Axonal transport, tau protein, and neurodegeneration in Alzheimer's disease. Neruomol. Med. 2002, 2:151-165.
68. Terwel D., Lasrado R., Snauwaert J., Vandeweert E., Van Haesendonck C., Borghgraef P., Van Leuven F. Changed conformation of mutant Tau-P301L underlies the moribund tauopathy, absent in progressive, nonlethal axonopathy of Tau-4R/2N transgenic mice. J. Biol. Chem. 2005, 280:3963-3973.
69. Terwel D., Muyllaert D., Dewachter I., Borghgraef P., Croes S., Devijver H., Van Leuven F. Amyloid activates GSK-3beta to aggravate neuronal tauopathy in bigenic mice. Am. J. Pathol. 2008, 172:786-798.
70. Theunis C., Crespo-Biel N., Gafner V., Pihlgren M., Lopez-Deber M.P., Reis P., Hickman D.T., Adolfsson O., Chuard N., Ndao D.M., Borghgraef P., Devijver H., Van Leuven F., Pfeifer A., Muhs A. Efficacy and safety of a liposome-based vaccine against Tau, assessed in Tau.P301L mice that model tauopathy. PLoS ONE 2013, 8(8):e72301.
71. Van Leuven F. Single and multiple transgenic mice as models for Alzheimer's disease. Prog. Neurobiol. 2000, 61:305-312.
72. Vana L., Kanaan N.M., Ugwu I.C., Wuu J., Mufson E.J., Binder L.I. Progression of tau pathology in cholinergic basal forebrain neurons in mild cognitive impairment and Alzheimer's disease. Am. J. Pathol. 2011, 179:2533-2550.
73. Vandebroek T., Terwel D., Vanhelmont T., Gysemans M., Van Haesendonck C., Engelborghs Y., Winderickx J., Van Leuven F. Microtubule binding and clustering of human Tau-4R and Tau-P301L proteins isolated from yeast deficient in orthologues of GSK3beta or cdk5. J. Biol. Chem. 2006, 281:25388-25397.
74. Zheng-Fischhofer Q., Biernat J., Mandelkow E.M., Illenberger S., Godemann R., Mandelkow E. Sequential phosphorylation of Tau by glycogen synthase kinase-3beta and protein kinase A at Thr212 and Ser214 generates the Alzheimer-specific epitope of antibody AT100 and requires a paired-helical-filament-like conformation. Eur. J. Biochem. 1998, 252:542-552.