AAV-tau mediates pyramidal neurodegeneration by cell-cycle re-entry without neurofibrillary tangle formation in wild-type mice

PLoS ONE

Volumn 4, Issue 10, 2009, Pages

  Jaworski, Tomasz ^a   Dewachter, Ilse ^a   Lechat, Benoit ^a   Croes, Sophie ^a,d   Termont, Annelies ^a,d   Demedts, David ^b   Borghgraef, Peter ^a   Devijver, Herman ^a   Filipkowski, Robert K ^b   Kaczmarek, Leszek ^b   Kügler, Sebastian ^c   Van Leuven, Fred ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^d ReMYND Nv   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; PARVOVIRUS VECTOR; TAU PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CYCLE; CELL DEATH; CONTROLLED STUDY; HIPPOCAMPUS; IN VIVO STUDY; MOUSE; MUTANT; NERVE DEGENERATION; NEUROFIBRILLARY TANGLE; NONHUMAN; PROTEIN AGGREGATION; PYRAMIDAL NERVE CELL; WILD TYPE; ADENO ASSOCIATED VIRUS; ANIMAL; C57BL MOUSE; CHEMISTRY; DEGENERATIVE DISEASE; HUMAN; METABOLISM; MUTATION; NERVE CELL; PROTEIN TERTIARY STRUCTURE; TRANSGENIC MOUSE;

MUS; MUS MUSCULUS;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CELL CYCLE; DEPENDOVIRUS; HIPPOCAMPUS; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; NEURODEGENERATIVE DISEASES; NEUROFIBRILLARY TANGLES; NEURONS; PROTEIN STRUCTURE, TERTIARY; TAU PROTEINS;

EID: 70349705552     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007280     Document Type: Article

References (49)

1. Lee VM, Goedert M, Trojanowski JQ (2001) Neurodegenerative tauopathies. Annu Rev Neurosci 24: 1121-1159.
2. Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82: 239-259.
3. Duyckaerts C, Delatour B, Potier MC (2009) Classification and basic pathology of Alzheimer disease Acta Neuropathol. In press.
4. Hutton M, Lendon CL, Rizzu P, Baker M, Froelich S, et al. (1998) Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393: 702-705.
5. Spillantini MG, Crowther RA, Kamphorst W, Heutink P, van Swieten JC (1998) Tau pathology in two Dutch families with mutations in the microtubule-binding region of tau. Am J Pathol 153: 1359-1363.
6. Grundke-Iqbal I, Iqbal K, Tung YC, Quinlan M, Wisniewski HM, et al. (1986) Abnormal phosphorylation of the microtubule-associated protein tau in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci U S A 83: 4913-4917.
7. Goedert M, Spillantini MG, Cairns NJ, Crowther RA (1989) Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3: 519-526.
8. Mandelkow EM, Mandelkow E (1998) Tau in Alzheimer's disease. Trends Cell Biol 8: 425-427.
9. Geschwind DH (2003) Tau phosphorylation, tangles, and neurodegeneration: the chicken or the egg? Neuron 40: 457-460.
10. Takashima A (2008) Hyperphosphorylated tau is a cause of neuronal dysfunction in tauopathy. J Alzheimers Dis 14: 371-375.
11. Terwel D, Dewachter I, Van Leuven F (2002) Axonal transport, protein tau and neurodegeneration in Alzheimer's disease. Neuro Molecular Med 2: 161-165.
12. Rosenberg KJ, Ross JL, Feinstein HE, Feinstein SC, Israelachvili J (2008) Complementary dimerization of microtubule-associated tau protein: Implications for microtubule bundling and tau-mediated pathogenesis. Proc Natl Acad Sci U S A 105: 7445-7450.
13. Dewachter I, Van Leuven F (2002) Secretases as targets for the treatment of Alzheimer's disease: the prospects. Lancet Neurol 1: 409-416.
14. Van Leuven F (2000) Single and multiple transgenic mice as models for Alzheimer's disease. Prog Neurobiol 61: 305-312.
15. Götz J, Ittner LM (2008) Animal models of Alzheimer's disease and frontotemporal dementia. Nat Rev Neurosci 9: 532-544.
16. Frank S, Clavaguera F, Tolnay M (2008) Tauopathy models and human neuropathology: similarities and differences. Acta Neuropathol 115: 39-53.
17. Morrissette DA, Parachikova A, Green KN, LaFerla FM (2009) Relevance of transgenic mouse models to human Alzheimer disease. J Biol Chem 284: 6033-6037.
18. Roberson ED, Scearce-Levie K, Palop JJ, Yan F, Cheng IH, et al. (2007) Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model. Science 316: 750-754.
19. Shevtsova Z, Malik JM, Michel U, Bähr M, Kügler S (2005) Promoters and serotypes: targeting of AAV vectors for gene transfer in the rat CNS in vitro and in vivo. Exp Physiol 90: 53-59.
20. Citron M, Oltersdorf T, Haass C, McConlogue L, Hung AY, et al. (1992) Mutation of the beta-amyloid precursor protein in familial Alzheimer's disease increases beta-protein production. Nature 360: 672-674.
21. Goate A, Chartier-Harlin MC, Mullan M, Brown J, Crawford F, et al. (1991) Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349: 704-706.
22. Kumar-Singh S, De Jonghe C, Cruts M, Kleinert R, Wang R, et al. (2000) Nonfibrillar diffuse amyloid deposition due to a gamma(42)-secretase site mutation points to an essential role for N-truncated A beta(42) in Alzheimer's disease. Hum Mol Genet 9: 2589-2598.
23. Terwel D, Lasrado R, Snauwaert J, Vandeweert E, Van Haesendonck C, et al. (2005) Changed conformation of mutant Tau-P301L underlies the moribund tauopathy, absent in progressive, nonlethal axonopathy of Tau-4R/2N transgenic mice. J Biol Chem 280: 3963-3973.
24. Terwel D, Muyllaert D, Dewachter I, Borghgraef P, Croes S, et al. (2008) Amyloid activates GSK-3beta to aggravate neuronal tauopathy in bigenic mice. Am J Pathol 172: 786-798.
25. Kim K, Miller D, Sapienza V, Chen C, Bai C, et al. (1988) Production and characterization of monoclonal antibodies reactive to synthetic cerebrovascular amyloid peptide. Neurosci Res Commun 2: 121-130.
26. Bard F, Barbour R, Cannon C, Carretto R, Fox M, et al. (2003) Epitope and isotype specificities of antibodies to beta-amyloid peptide for protection against Alzheimer's disease-like neuropathology. Proc Natl Acad Sci U S A 100: 2023-2028.
27. Schmued LC, Hopkins KJ (2000) Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 874: 123-130.
28. Muyllaert D, Terwel D, Kremer A, Sennvik K, Borghgraef P, et al. (2008) Neurodegeneration and neuroinflammation in cdk5/p25-inducible mice: a model for hippocampal sclerosis and neocortical degeneration. Am J Pathol 172: 470-485.
29. Moechars D, Dewachter I, Lorent K, Reversé D, Baekelandt V, Naidu A, et al. (1999) Early phenotypic changes in transgenic mice that overexpress different mutants of Amyloid Precursor Protein in brain. J Biol Chem 274: 6483-6492.
30. Nixon RA (2006) Autophagy in neurodegenerative disease: friend, foe or turncoat? Trends Neurosci 29: 528-535.
31. Andorfer C, Acker CM, Kress Y, Hof PR, Duff K, et al. (2005) Cell-cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms. J Neurosci 25: 5446-5454.
32. Herrup K, Yang Y (2007) Cell cycle regulation in the postmitotic neuron: oxymoron or new biology? Nat Rev Neurosci 8: 368-378.
33. Husseman JW, Nochlin D, Vincent I (2000) Mitotic activation: a convergent mechanism for a cohort of neurodegenerative diseases. Neurobiol Aging 21: 815-828.
34. Vincent I, Jicha G, Rosado M, Dickson DW (1997) Aberrant expression of mitotic cdc2/cyclin B1 kinase in degenerating neurons of Alzheimer's disease brain. J Neurosci 17: 3588-3598.
35. Kowalczyk A, Filipkowski RK, Rylski M, Wilczynski GM, Konopacki FA, et al. (2004) The critical role of cyclin D2 in adult neurogenesis. J Cell Biol 167: 209-213.
36. SantaCruz K, Lewis J, Spires T, Paulson J, Kotilinek L, et al. (2005) Tau suppression in a neurodegenerative mouse model improves memory function. Science 309: 476-481.
37. Melino G, Knight RA, Nicotera P (2005) How many ways to die? How many different models of cell death? Cell Death Differ 12: 1457-1462.
38. Khurana V, Lu Y, Steinhilb ML, Oldham S, Shulman JM, et al. (2006) TOR-mediated cell-cycle activation causes neurodegeneration in a Drosophila tauopathy model. Curr Biol 16: 230-241.
39. Hoozemans JJ, Brückner MK, Rozemuller AJ, Veerhuis R, Eikelenboom P, et al. (2002) Cyclin D1 and cyclin E are co-localized with cyclo-oxygenase 2 (COX-2) in pyramidal neurons in Alzheimer disease temporal cortex. J Neuropathol Exp Neurol 61: 678-688.
40. Hasan S, Hassa PO, Imhof R, Hottiger MO (2001) Transcription coactivator p300 binds PCNA and may have a role in DNA repair synthesis. Nature 410: 387-391.
41. Spittaels K, Van den Haute C, Van Dorpe J, Geerts H, Mercken M, et al. (2000) 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 275: 41340-41349.
42. Klein RL, Dayton RD, Diaczynsky CG, Wang DB (2009) Pronounced microgliosis and neurodegeneration in aged rats after tau gene transfer. Neurobiol Aging, Epub ahead of print.
43. Arnaud L, Robakis NK, Fiqueiredo-Pereiera ME (2006) It may take inflammation, phosphorylation and ubiquitination to 'tangle' in Alzheimer's disease. Neurodegener Dis 3: 313-319.
44. Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, et al. (2009) Transmission and spreading of tauopthy in transgenic mouse brain. Nat Cell Biol In press.
45. Spittaels K, Van den Haute C, Van Dorpe J, Bruynseels K, Vandezande K, et al. (1999) Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein. Am J Pathol 155: 2153-2165.
46. Kügler S, Hahnewald R, Garrido M, Reiss J (2007) Long-term rescue of a lethal inherited disease by adeno-associated virus-mediated gene transfer in a mouse model of molybdenum-cofactor deficiency. Am J Hum Genet 80: 291-297.
47. Sicinski P, Donaher JL, Geng Y, Parker SB, Gardner H, et al. (1996) Cyclin D2 is an FSH-responsive gene involved in gonadal cell proliferation and oncogenesis. Nature 384: 470-474.
48. Franklin KBJ, Paxinos G (1997) The Mouse Brain in Stereotaxic Coordinates. San Diego: Academic Press. pp 360.
49. Styren SD, Hamilton RL, Styren GC, Klunk WE (2000) X-34, a fluorescent derivative of Congo red: a novel histochemical stain for Alzheimer's disease pathology. J Histochem Cytochem 48: 1223-1232.