Neuronal degeneration, synaptic defects, and behavioral abnormalities in tau45-230 transgenic mice

Neuroscience

Volumn 275, Issue , 2014, Pages 322-339

  Lang, A E ^a   Riherd Methner, D N ^a   Ferreira, A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Calpain; Cell death; Neurite degeneration; NMDA receptors; Synapse loss; Tau cleavage

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; TAU PROTEIN; MAPT PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CELL DEATH; CONTROLLED STUDY; DISEASE ASSOCIATION; FEAR-POTENTIATED STARTLE TEST; FEMALE; HIPPOCAMPAL NEURONAL CULTURE; MALE; MORRIS WATER MAZE TEST; MOUSE; NERVE CELL DEGENERATION; NEUROPATHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PYRAMIDAL NERVE CELL; SYNAPTIC INHIBITION; TASK PERFORMANCE; TAUOPATHY; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; DISEASE MODEL; HIPPOCAMPUS; HUMAN; IMMUNOHISTOCHEMISTRY; MAZE TEST; METABOLISM; NERVE CELL; NERVE DEGENERATION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNAPSE; TRANSGENIC MOUSE; WESTERN BLOTTING;

ANIMALS; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE DEGENERATION; NEURONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SYNAPSES; TAU PROTEINS; TAUOPATHIES;

EID: 84903952989     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.06.017     Document Type: Article

References (77)

1. Alvarez A., Toro R., Caceres A., Maccioni R.B. Inhibition of tau phosphorylating protein kinase cdk5 prevents beta-amyloid-induced neuronal death. FEBS Lett 1999, 459:421-426.
2. 1 integrin activation: a link between β-amyloid deposition and neuronal death in aging hippocampal neurons. J Neurosci Res 2004, 75:688-697.
3. Andorfer C., Acker C.M., Kress Y., Hof P.R., Duff K., Davies P. Cell-cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms. J Neurosci 2005, 25:5446-5454.
4. Bensadoun A., Weinstein D. Assay of proteins in the presence of interfering materials. Anal Biochem 1976, 70:241-250.
5. Bottenstein J.E., Sato G.H. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc Natl Acad Sci USA 1979, 76:514-517.
6. Bramblett G.T., Goedert M., Jakes R., Merrick S.E., Trojanowski J.Q., Lee V.M.Y. Abnormal tau phosphorylation at Ser 396 in Alzheimer's disease recapitulates development and contributes to reduce microtubule binding. Neuron 1993, 10:1089-1099.
7. Busciglio J., Lorenzo A., Yeh J., Yankner B.A. Beta-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 1995, 14:879-888.
8. Caceres A., Kosik K.S. Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 1990, 343:461-463.
9. Canu N., Dus L., Barbato C., Ciotti M.T., Brancolini C., Rinaldi A.M., Novak M., Cattaneo A., Bradbury A., Calissano P. Tau cleavage and dephosphorylation in cerebellar granule neurons undergoing apoptosis. J Neurosci 1998, 18:7061-7074.
10. Chung C.W., Song Y.H., Kim I.K., Yoon W.J., Ryu B.R., Jo D.G., Woo H.N., Kwon Y.K., Kim H.H., Gwag B.J., Mook-Jung I.H., Jung Y.K. Proapoptotic effects of tau cleavage product generated by caspase-3. Neurobiol Dis 2001, 8:162-172.
11. Clinton S.M., Haroutunian V., Meador-Woodruff J.H. Up-regulation of NMDA receptor subunit and post-synaptic density protein expression in the thalamus of elderly patients with schizophrenia. J Neurochem 2006, 98:1114-1125.
12. Dawson H.N., Ferreira A., Eyster M.V., Binder L.I., Vitek M.P. Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J Cell Sci 2001, 114:1179-1187.
13. DeKosky S.T., Scheff S.W. Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol 1990, 27:457-464.
14. DeKosky S.T., Scheff S.W., Styren S.D. Structural correlates of cognition in dementia: quantification and assessment of synapse change. Neurodegeneration 1996, 5:417-421.
15. Dreschel D.N., Hyman A.A., Cobb M.H., Kirschner M.W. Modulation of dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol Biol Cell 1992, 3:1141-1154.
16. Drubin D.G., Kirschner M.W. Tau protein function in living cells. J Cell Biol 1986, 103:2739-2746.
17. d-aspartate glutamate receptors in a rat 6-hydroxydopamine model of Parkinson's disease. Mol Pharmacol 2000, 57:342-352.
18. Ekinci F.J., Malik K.U., Shea T.B. Activation of the L voltage-sensitive calcium channel by mitogen-activated protein (MAP) kinase following exposure of neuronal cells to beta-amyloid. MAP kinase mediates beta-amyloid-induced neurodegeneration. J Biol Chem 1999, 274:30322-30327.
19. Fasulo L., Ugolini G., Visintin M., Bradbury A., Brancolini C., Verzillo V., Novak M., Cattaneo A. The neuronal microtubule-associated protein tau is a substrate for caspase-3 and an effector of apoptosis. J Neurochem 2000, 75:624-633.
20. Feng G., Mellor R.H., Bernstein M., Keller-Peck C., Nguyen Q.T., Wallace M., Nerbonne J.M., Lichtman J.W., Sanes J.R. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 2000, 28:41-51.
21. Ferreira A., Bigio E.H. Calpain-mediated tau cleavage: a mechanism leading to neurodegeneration shared by multiple tauopathies. Mol Med 2011, 17:676-685.
22. Ferreira A., Busciglio J., Caceres A. Microtubule formation and neurite growth in cerebellar macroneurons which develop in vitro: evidence for the involvement of the microtubule-associated proteins, MAP-1a, HMW-MAP2 and Tau. Brain Res Dev Brain Res 1989, 49:215-228.
23. Ferreira A., Lu Q., Orecchio L., Kosik K.S. Selective phosphorylation of adult tau isoforms in mature hippocampal neurons exposed to fibrillar A beta. Mol Cell Neurosci 1997, 9:220-234.
24. Fletcher T.L., Cameron P., De Camilli P., Banker G. The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture. J Neurosci 1991, 11:1617-1626.
25. Fykse E.M., Takei K., Walch-Solimena C., Geppert M., Jahn R., De Camilli P., Sudhof T.C. Relative properties and localizations of synaptic vesicle protein isoforms: the case of the synaptophysins. J Neurosci 1993, 13:4997-5007.
26. Gamblin T.C., Chen F., Zambrano A., Abraha A., Lagalwar S., Guillozet A.L., Lu M., Fu Y., Garcia-Sierra F., LaPointe N., Miller R., Berry R.W., Binder L.I., Cryns V.L. Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc Natl Acad Sci USA 2003, 100:10032-10037.
27. Garg S., Timm T., Mandelkow E.-M., Mandelkow E., Wang Y. Cleavage of tau by calpain in Alzheimer's disease: the quest for the toxic 17kDa fragment. Neurobiol Aging 2011, 32:1-14.
28. Gazzaley A.H., Benson D.L., Huntley G.W., Morrison J.H. Differential subcellular regulation of NMDAR1 protein and mRNA in dendrites of dentate gyrus granule cells after perforant path transection. J Neurosci 1997, 17:2006-2017.
29. Geddes J.W., Chang-Chui H., Cooper S.M., Lott I.T., Cotman C.W. Density and distribution of NMDA receptors in the human hippocampus in Alzheimer's disease. Brain Res 1986, 399:156-161.
30. Gong C.X., Lidsky T., Wegiel J., Zuck L., Grundke-Iqbal I., Iqbal K. Phosphorylation of microtubule-associated protein tau is regulated by protein phosphatase 2A in mammalian brain. Implications for neurofibrillary degeneration in Alzheimer's disease. J Biol Chem 2000, 275:5535-5544.
31. Grossman S.D., Wolfe B.B., Yasuda R.P., Wrathall J.R. Changes in NMDA receptor subunit expression in response to contusive spinal cord injury. J Neurochem 2000, 75:174-184.
32. Grynspan F., Griffin W.R., Cataldo A., Katayama S., Nixon R.A. Active site-directed antibodies identify calpain II as an early-appearing and pervasive component of neurofibrillary pathology in Alzheimer's disease. Brain Res 1997, 763:145-158.
33. Harada J., Sugimoto M. Activation of caspase-3 in beta-amyloid-induced apoptosis of cultured rat cortical neurons. Brain Res 1999, 842:311-323.
34. Kelly B., Vassar R., Ferreira A. Beta-amyloid-induced dynamin I depletion in hippocampal neurons: a potential mechanisms for early cognitive decline in Alzheimer's disease. J Biol Chem 2005, 280:31746-31753.
35. King D.L., Arendash G.W. Maintained synaptophysin immunoreactivity in Tg2576 transgenic mice during aging: correlations with cognitive impairment. Brain Res 2002, 926:58-68.
36. Knops J., Kosik K.S., Lee G., Pardee J.D., Cohen-Gould L., McConlogue L. Overexpression of tau in a nonneuronal cell induces long cellular processes. J Cell Biol 1991, 114:725-733.
37. Kondo J., Honda T., Mori H., Hamada Y., Miura R., Ogawara M., Ihara Y. The carboxyl third of tau is tightly bound to paired helical filaments. Neuron 1988, 1:827-834.
38. Kosik K.S., Joachim C.L., Selkoe D.J. Microtubule-associated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease. Proc Natl Acad Sci USA 1986, 83:4044-4048.
39. Lacor P.N., Buniel M.C., Furlow P.W., Clemente A.S., Velasco P.T., Wood M., Viola K.L., Klein W.L. Aβ oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J Neurosci 2007, 27:706-807.
40. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
41. Liu M.C., Kobeissy F., Zheng W., Zhang Z., Hayes R., Wang K.K.W. Dual vulnerability of tau to calpains and caspase-3 proteolysis under neurotoxic and neurodegenerative conditions. ASN Neuro 2011, 3(1). art:e00051. 10.1042/AN20100012.
42. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem 1951, 193:265-275.
43. Marin N., Romero B., Bosch-Morell F., Llansola M., Felipo V., Roma J., Romero F.J. Beta-amyloid-induced activation of caspase-3 in primary cultures of rat neurons. Mech Ageing Dev 2000, 119:63-67.
44. Markram K., Rinaldi T., La Medola D., Sandi C., MArkram H. Abnormal fear conditioning and amygdala processing in an animal model of autism. Neuropsychopharmacology 2008, 33:901-912.
45. Martin L., Latypova X., Terro F. Post-translational modifications of tau protein: Implications for Alzheimer's disease. Neurochem Intl 2011, 58:458-471.
46. Masliah E., Miller A., Terry R.D. The synaptic organization of the neocortex in Alzheimer's disease. Med Hypothesis 1993, 41:334-340.
47. Mega M.S., Cummings J.L., Fiorello T., Gornbein J. The spectrum of behavioral changes in Alzheimer's disease. Neurology 1996, 46:130-135.
48. Mishizen-Eberz A.J., Rissman R.A., Carter T.L., Ikonomovic M.D., Wolfe B.B., Armgstrong D.M. Biochemical and molecular studies of NMDA receptor subunits NR1/2A/2B in hippocampal subregions throughout progression of Alzheimer's disease pathology. Neurobiol Dis 2004, 15:80-92.
49. Mukaetova-Ladinska E.B., Garcia-Sierra F., Hurt J., Gertz H.J., Xuereb J.H., Hills R., Brayne C., Huppert F.A., Paykel E.S., McGee M., Kjakes R., Honer W.G., Harrington C.R., Wischik C.M. Staging of cytoskeletal and β-amyloid changes in human isocortex reveals biphasic synaptic protein response during progression of Alzheimer's disease. Am J Pathol 2000, 157:623-636.
50. Navone F., Jahn R., Di Gioia G., Stunbrok H., Greengard P., De Camilli P. Protein p38: an integral membrane protein specific for small vesicles of neurons and neuroendocrine cells. J Cell Biol 1986, 103:2511-2527.
51. Parihar M.S., Hemnani T. Alzheimer's disease pathogenesis and therapeutic interventions. J Clin Neurosci 2004, 11:456-467.
52. Park S.Y., Ferreira A. The generation of a 17kDa neurotoxic fragment: an alternative mechanism by which tau mediates beta-amyloid-induced neurodegeneration. J Neurosci 2005, 25:5365-5375.
53. Park S.Y., Tournell C., Sinjoanu R.C., Ferreira A. Caspase-3- and calpain-mediated tau cleavage are differentially prevented by estrogen and testosterone in beta-amyloid-treated hippocampal neurons. Neuroscience 2007, 144:119-127.
54. Peri T., Ben-Shakhar G., Orr S.P., Shalev A.Y. Psychophysiologic assessment of adversive conditioning in posttraumatic stress disorder. Biol Psychiatry 2000, 47:512-519.
55. Pinkstaff J.K., Detterich J., Lynch G., Gall C. Integrin subunit gene expression is regionally differentiated in adult brain. J Neurosci 1999, 19:1541-1556.
56. Qiu W.Q., Ferreira A., Miller C., Koo E.H., Selkoe D.J. Cell-surface beta-amyloid precursor protein stimulates neurite outgrowth of hippocampal neurons in an isoform-dependent manner. J Neurosci 1995, 15:2157-2167.
57. Rapoport M., Ferreira A. PD98059 prevents neurite degeneration induced by fibrillar beta-amyloid in mature hippocampal neurons. J Neurochem 2000, 74:125-133.
58. Rapoport M., Dawson H.N., Binder L.I., Vitek M.P., Ferreira A. Tau is essential to beta -amyloid-induced neurotoxicity. Proc Natl Acad Sci USA 2002, 99:6364-6369.
59. Reinecke J.B., DeVos S.L., McGrath J.P., Shepard A.M., Goncharoff D.K., Tait D.N., Fleming S.R., Vincent M.P., Steinhilb M.L. Implicating calpain in tau-mediated toxicity in vivo. PloS One 2011, 10.1371/journal.pone.0023865.
60. Roberson E.D., Scearce-Levie K., Palop J.J., Yan F., Cheng I.H., Wu T., Gerstein H., Yu G.-Q., Mucke L. Reducing endogenous tau ameliorates amyloid β-induced deficits in an Alzheimer's disease mouse model. Science 2007, 316:750-753.
61. Rohn T.T., Head E., Su J.H., Anderson A.J., Bahr B.A., Cotman C.W., Cribbs D.H. Correlation between caspase activation and neurofibrillary tangle formation in Alzheimer's disease. Am J Pathol 2001, 158:189-198.
62. Sartori S.B., Hauschild M., Bunck M., Gaburro S., Landgraf R., Singewald N. Enhanced fear expression in a psychopathological mouse model of trait anxiety: pharmacological interventions. PLoS One 2011, 6(2):e16849. 10.1371/journal.pone.0016849.
63. Shea T.B., Spencer M.J., Beermann M.L., Cressman C.M., Nixon R.A. Calcium influx into human neuroblastoma cells induces ALZ-50 immunoreactivity: involvement of calpain-mediated hydrolysis of protein kinase C. J Neurochem 1996, 66:1539-1549.
64. Simón A., Schiapparelli L., Salazar-Colocho P., Cuadrado-Tejedor M., Escribano L., López de Maturana R., Del Río J., Pérez-Mediavilla A., Frechilla D. Overexpression of wild-type human APP in mice causes cognitive deficits and pathological features unrelated to Aβ levels. Neurobiol Dis 2009, 33:369-378.
65. Singh C., Bortolato M., Bali N., Godar S.C., Scott A.L., Chen K., Thompson R.F., Shih J.C. Cognitive abnormalities and hippocampal alterations in monoamine oxidase A and B knockout mice. Proc Natl Acad Sci USA 2013, 110:12816-12821.
66. Sinjoanu R.C., Kleinschmidt S., Bitner R.S., Brioni J., Moeller A., Ferreira A. The novel calpain inhibitor A-705253 potently inhibits oligomeric beta-amyloid-induced dynamin 1 and tau cleavage in hippocampal neurons. Neurochem Intl 2008, 53:79-88.
67. Spires T.L., Hyman B.T. Transgenic models of Alzheimer's disease: learning from animals. J Am Soc Exp Neurother 2005, 2:423-437.
68. Su J.H., Zhao M., Anderson A.J., Srinivasan A., Cotman C.W. Activated caspase-3 expression in Alzheimer's and aged control brain: correlation with Alzheimer pathology. Brain Res 2001, 898:350-357.
69. Sze C.I., Troncoso J.C., Kawas C., Mouton P., Price D.L., Martin L.J. Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer's disease. J Neuropathol Exp Neurol 1997, 56:933-944.
70. Takashima A., Noguchi K., Sato K., Hoshino T., Imahori K. Tau protein kinase I is essential for amyloid beta-protein-induced neurotoxicity. Proc Natl Acad Sci USA 1993, 90:7789-7793.
71. Teri L., Ferretti L.E., Logsdon R.G., McCurry S.M., Kukull W.A., McCormick W.C., Bowen J.D., Larson E.B. Anxiety in Alzheimer's disease: prevalence and comorbidity. J Gerontol 1999, 54A:M348-M352.
72. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 1979, 76:4350-4354.
73. Watase K., Weeber E.J., Xu B., Antalffy B., Yuva Paylor L., Hashimoto K., Kano M., Atkinson R., Sun Y., Armstrong S.L., Sweatt J.D., Orr J.T., Paylor R., Zoghbi H.Y. A Long CAG repeat in the mouse Sca1 locus replicates SCA1 features and reveals the impact of protein solubility in selective neurodegeneration. Neuron 2002, 34:905-919.
74. Wood J.G., Mirra S.S., Pollock N.J., Binder L.I. Neurofibrillary tangles of Alzheimer disease share antigenic determinants with the axonal microtubule-associated protein tau (tau). Proc Natl Acad Sci USA 1986, 83:4040-4043.
75. Yakunin A.F., Hallenbeck P.C. A luminol/iodophenol chemiluminescent detection system for western immunoblots. Anal Biochem 1998, 258:146-149.
76. Yancopoulou D., Spillantini M.G. Tau protein in familial and sporadic diseases. Neuromol Med 2003, 4:37-48.
77. Yoshida H., Hastie C.J., McLauchlan H., Cohen P., Goedert M. Phosphorylation of microtubule-associated protein tau by isoforms of c-Jun N-terminal kinase (JNK). J Neurochem 2004, 90:352-358.