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Acknowledgements

This work was supported by NIH grant NS35060. The authors would like tothank Dr. P. Davies for the PHF1 antibody, Dr. L. Binder for the Tau-1 andTau5 antibodies, and Dr. P. Seubert for the 12E8 antibody. The UAB MassSpectrometry Shared Facility is supported in part by NIH grantP30-13148-27.

  • 1
    Ahuja H.S., Zhu Y., Zakeri Z. (1997) Association of cyclin-dependent kinase 5 and its activator p35 with apoptotic cell death.Dev. Genet. 21258267.
  • 2
    Alonso A.C., Zaidi T., Grundke-Iqbal I., Iqbal K. (1994) Role of abnormally phosphorylated tau in the breakdown of microtubules in Alzheimer disease.Proc. Natl. Acad. Sci. USA 9155625566.
  • 3
    Batistatou A. & Greene L.A. (1991) Aurintricarboxylic acid rescues PC12 cells and sympathetic neurons from cell death caused by nerve growth factor deprivation: correlation with suppression of endonuclease activity.J. Cell Biol. 115461471.
  • 4
    Biernat J., Gustke N., Drewes G., Mandelkow E.M., Mandelkow E. (1993) Phosphorylation of Ser262 strongly reduces binding of tau to microtubules: distinction between PHF-like immunoreactivity and microtubule binding.Neuron 11153163.
  • 5
    Binder L.I., Frankfurter A., Rebhun L.I. (1985) The distribution of tau in the mammalian central nervous system.J. Cell Biol. 10113711378.
  • 6
    Bramblett G.T., Goedert M., Jakes R., Merrick S.E., Trojanowski J.Q., Lee V.M. (1993) Abnormal tau phosphorylation at Ser396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding.Neuron 1010891099.
  • 7
    Brandt R., Leger J., Lee G. (1995) Interaction of tau with the neural plasma membrane mediated by tau's amino-terminal projection domain.J. Cell Biol. 13113271340.
  • 8
    Busser J., Geldmacher D.S., Herrup K. (1998) Ectopic cell cycle proteins predict the sites of neuronal cell death in Alzheimer's disease brain.J. Neurosci. 1828012807.
  • 9
    Couchie D., Mavilia C., Georgieff I.S., Liem R.K., Shelanski M.L., Nunez J. (1992) Primary structure of high molecular weight tau present in the peripheral nervous system.Proc. Natl. Acad. Sci. USA 8943784381.
  • 10
    Cross D.A., Alessi D.R., Cohen P., Andjelkovich M., Hemmings B.A. (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B.Nature 378785789.
  • 11
    Davis P.K. & Johnson G.V. (1999a) Energy metabolism and protein phosphorylation during apoptosis: a phosphorylation study of tau and high-molecular-weight tau in differentiated PC12 cells.Biochem. J. 3405158.
  • 12
    Davis P.K. & Johnson G.V. (1999b) The microtubule binding of tau and high molecular weight tau in apoptotic PC12 cells is impaired because of altered phosphorylation.J. Biol. Chem. 2743568635692.
  • 13
    Davis P.K., Dudek S.M., Johnson G.V. (1997) Select alterations in protein kinases and phosphatases during apoptosis of differentiated PC12 cells.J. Neurochem. 6823382347.
  • 14
    Drewes G., Ebneth A., Mandelkow E.M. (1998) MAPs, MARKs and microtubule dynamics.Trends Biochem. Sci. 23307311.
  • 15
    Dudek H., Datta S.R., Franke T.F., Birnbaum M.J., Yao R., Cooper G.M., Segal R.A., Kaplan D.R., Greenberg M.E. (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt [see comments].Science 275661665.
  • 16
    Gao C.Y. & Zelenka P.S. (1995) Induction of cyclin B and H1 kinase activity in apoptotic PC12 cells.Exp. Cell Res. 219612618.
  • 17
    Gervais F.G., Xu D., Robertson G.S., Vaillancourt J.P., Zhu Y., Huang J., LeBlanc A., Smith D., Rigby M., Shearman M.S., Clarke E.E., Zheng H., Van Der Ploeg L.H., Ruffolo S.C., Thornberry N.A., Xanthoudakis S., Zamboni R.J., Roy S., Nicholson D.W. (1999) Involvement of caspases in proteolytic cleavage of Alzheimer's amyloid-beta precursor protein and amyloidogenic A beta peptide formation.Cell 97395406.
  • 18
    Goedert M., Spillantini M.G., Jakes R., Rutherford D., Crowther R.A. (1989) Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease.Neuron 3519526.
  • 19
    Goedert M., Spillantini M.G., Crowther R.A. (1992) Cloning of a big tau microtubule-associated protein characteristic of the peripheral nervous system.Proc. Natl. Acad. Sci. USA 8919831987.
  • 20
    Greene L.A. (1978) Nerve growth factor prevents the death and stimulates the neuronal differentiation of clonal PC12 pheochromocytoma cells in serum-free medium.J. Cell Biol. 78747755.
  • 21
    Greene L.A. & Tischler A.S. (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor.Proc. Natl. Acad. Sci. USA 7324242428.
  • 22
    Guenal I., Risler Y., Mignotte B. (1997) Down-regulation of actin genes precedes microfilament network disruption and actin cleavage during p53-mediated apoptosis.J. Cell Sci. 110489495.
  • 23
    Gustke N., Steiner B., Mandelkow E.M., Biernat J., Meyer H.E., Goedert M., Mandelkow E. (1992) The Alzheimer-like phosphorylation of tau protein reduces microtubule binding and involves Ser-Pro and Thr-Pro motifs.FEBS Lett. 307199205.
  • 24
    Hanger D.P., Betts J.C., Loviny T.L., Blackstock W.P., Anderton B.H. (1998) New phosphorylation sites identified in hyperphosphorylated tau (paired helical filament-tau) from Alzheimer's disease brain using nanoelectrospray mass spectrometry.J. Neurochem. 7124652476.
  • 25
    Heintz N. (1993) Cell death and the cell cycle: a relationship between transformation and neurodegeneration?Trends Biochem. Sci. 18157159.
  • 26
    Henchcliffe C. & Burke R.E. (1997) Increased expression of cyclindependent kinase 5 in induced apoptotic neuron death in rat substantia nigra.Neurosci. Lett. 2304144.
  • 27
    Hughes K., Nikolakaki E., Plyte S.E., Totty N.F., Woodgett J.R. (1993) Modulation of the glycogen synthase kinase-3 family by tyrosine phosphorylation.EMBO J. 12803808.
  • 28
    Huot J., Houle F., Rousseau S., Deschesnes R.G., Shah G.M., Landry J. (1998) SAPK2/p38-dependent F-actin reorganization regulates early membrane blebbing during stress-induced apoptosis.J. Cell Biol. 14313611373.
  • 29
    Illenberger S., Zheng-Fischhofer Q., Preuss U., Stamer K., Baumann K., Trinczek B., Biernat J., Godemann R., Mandelkow E.M., Mandelkow E. (1998) The endogenous and cell cycle-dependent phosphorylation of tau protein in living cells: implications for Alzheimer's disease.Mol. Biol. Cell 914951512.
  • 30
    Imahori K., Hoshi M., Ishiguro K., Sato K., Takahashi M., Shiurba R., Yamaguchi H., Takashima A., Uchida T. (1998) Possible role of tau protein kinases in pathogenesis of Alzheimer's disease.Neurobiol. Aging 19S93S98.
  • 31
    Ishiguro K., Takamatsu M., Tomizawa K., Omori A., Takahashi M., Arioka M., Uchida T., Imahori K. (1992) Tau protein kinase I converts normal tau protein into A68-like component of paired helical filaments.J. Biol. Chem. 2671089710901.
  • 32
    Jicha G.A., Weaver C., Lane E., Vianna C., Kress Y., Rockwood J., Davies P. (1999) cAMP-dependent protein kinase phosphorylations on tau in Alzheimer's disease.J. Neurosci. 1974867494.
  • 33
    Johnson G.V. & Hartigan J.A. (1999) Tau protein in normal and Alzheimer's disease brain. an update.J. Alzheimer's Dis. 1329351.
  • 34
    Johnson G. V. and Jenkins S. M. (1996) Tau protein in normal and Alzheimer's disease brain. Alzheimer's Dis. Rev. 1,3854. http://www.coa.uky.edu/ADReview/
  • 35
    Johnson G.V., Jope R.S., Binder L.I. (1989) Proteolysis of tau by calpain.Biochem. Biophys. Res. Commun. 16315051511.
  • 36
    Joshi H.C. (1998) Microtubule dynamics in living cells.Curr. Opin. Cell Biol. 103544.
  • 37
    Kosik K.S., Orecchio L.D., Bakalis S., Neve R.L. (1989) Developmentally regulated expression of specific tau sequences.Neuron 213891397.
  • 38
    Kuret J., Johnson G.S., Cha D., Christenson E.R., DeMaggio A.J., Hoekstra M.F. (1997) Casein kinase 1 is tightly associated with paired-helical filaments isolated from Alzheimer's disease brain.J. Neurochem. 6925062515.
  • 39
    Kusakawa G., Saito T., Onuki R., Ishiguro K., Kishimoto T., Hisanaga S. (2000) Calpain-dependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator to p25.J. Biol. Chem. 2751716617172.
  • 40
    Ledesma M.D., Correas I., Avila J., Diaz-Nido J. (1992) Implication of brain cdc2 and MAP2 kinases in the phosphorylation of tau protein in Alzheimer's disease.FEBS Lett. 308218224.
  • 41
    Lee G., Cowan N., Kirschner M. (1988) The primary structure and heterogeneity of tau protein from mouse brain.Science 239285288.
  • 42
    Lee M.S., Kwon Y.T., Li M., Peng J., Friedlander R.M., Tsai L.H. (2000) Neurotoxicity induces cleavage of p35 to p25 by calpain.Nature 405360364.
  • 43
    Lee V.M. (1995) Disruption of the cytoskeleton in Alzheimer's disease.Curr. Opin. Neurobiol. 5663668.
  • 44
    Levee M.G., Dabrowska M.I., Lelli J.L.J, Hinshaw D.B. (1996) Actin polymerization and depolymerization during apoptosis in HL-60 cells.Am. J. Physiol. 271C1981C1992.
  • 45
    Levine A.J. (1997) p53, the cellular gatekeeper for growth and division.Cell 88323331.
  • 46
    Lindwall G. & Cole R.D. (1984) Phosphorylation affects the ability of tau protein to promote microtubule assembly.J. Biol. Chem. 25953015305.
  • 47
    Mandelkow E.M. & Mandelkow E. (1998) Tau in Alzheimer's disease.Trends Cell Biol. 8425427.
  • 48
    Michel G., Mercken M., Murayama M., Noguchi K., Ishiguro K., Imahori K., Takashima A. (1998) Characterization of tau phosphorylation in glycogen synthase kinase-3beta and cyclin dependent kinase-5 activator (p23) transfected cells.Biochim. Biophys. Acta 1380177182.
  • 49
    Mills J.C., Lee V.M., Pittman R.N. (1998) Activation of a PP2A-like phosphatase and dephosphorylation of tau protein characterize onset of the execution phase of apoptosis.J. Cell Sci. 111625636.
  • 50
    Mills J.C., Stone N.L., Pittman R.N. (1999) Extranuclear apoptosis. The role of the cytoplasm in the execution phase.J. Cell Biol. 146703708.
  • 51
    Morishima-Kawashima M., Hasegawa M., Takio K., Suzuki M., Yoshida H., Titani K., Ihara Y. (1995) Proline-directed and non—proline-directed phosphorylation of PHF-tau. J. Biol. Chem. 270823829.
  • 52
    Nuydens R., Dispersyn G., De Jong M., Van Den Kieboom G., Borgers M., Geerts H. (1997) Aberrant tau phosphorylation and neurite retraction during NGF deprivation in PC12 cells.Biochem. Biophys. Res. Commun. 240687691.
  • 53
    O'Farrell P.Z., Goodman H.M., O'Farrell P.H. (1977) High resolution two-dimensional electrophoresis of basic as well as acidic proteins.Cell 1211331141.
  • 54
    Otvos L.J, Feiner L., Lang E., Szendrei G.I., Goedert M., Lee V.M. (1994) Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residues 396 and 404.J. Neurosci. Res. 39669673.
  • 55
    Patrick G.N., Zukerberg L., Nikolic M., De La Monte S., Dikkes P., Tsai L.H. (1999) Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration [see comments].Nature 402615622.
  • 56
    Pei J.J., Grundke-Iqbal I., Iqbal K., Bogdanovic N., Winblad B., Cowburn R.F. (1998) Accumulation of cyclin-dependent kinase 5 (cdk5) in neurons with early stages of Alzheimer's disease neurofibrillary degeneration.Brain Res. 797267277.
  • 57
    Pittman R.N., Wang S., DiBenedetto A.J., Mills J.C. (1993) A system for characterizing cellular and molecular events in programmed neuronal cell death.J. Neurosci. 1336693680.
  • 58
    Seubert P., Mawal-Dewan M., Barbour R., Jakes R., Goedert M., Johnson G.V., Litersky J.M., Schenk D., Lieberburg I., Trojanowski J.Q., et al. (1995) Detection of phosphorylated Ser262 in fetal tau, adult tau, and paired helical filament tau.J. Biol. Chem. 2701891718922.
  • 59
    Sobue K., Agarwal-Mawal A., Li W., Sun W., Miura Y., Paudel H.K. (2000) Interaction of neuronal Cdc2-like protein kinase with microtubule-associated protein tau.J. Biol. Chem. 2751667316680.
  • 60
    Song Z. & Steller H. (1999) Death by design: mechanism and control of apoptosis.Trends Cell Biol. 9M49M52.
  • 61
    Stadelmann C., Deckwerth T.L., Srinivasan A., Bancher C., Bruck W., Jellinger K., Lassmann H. (1999) Activation of caspase-3 in single neurons and autophagic granules of granulovacuolar degeneration in Alzheimer's disease. Evidence for apoptotic cell death.Am. J. Pathol. 15514591466.
  • 62
    Steinberg R.A., O'Farrell P.H., Friedrich U., Coffino P. (1977) Mutations causing charge alterations in regulatory subunits of the cAMP-dependent protein kinase of cultured S49 lymphoma cells.Cell 10381391.
  • 63
    Szendrei G.I., Lee V.M., Otvos L.Jr. (1993) Recognition of the minimal epitope of monoclonal antibody Tau-1 depends upon the presence of a phosphate group but not its location.J. Neurosci. Res. 34243249.
  • 64
    Tang D. & Wang J.H. (1996) Cyclin-dependent kinase 5 (Cdk5) and neuron-specific Cdk5 activators.Prog. Cell Cycle Res. 2205216.
  • 65
    Trinczek B., Biernat J., Baumann K., Mandelkow E.M., Mandelkow E. (1995) Domains of tau protein, differential phosphorylation, and dynamic instability of microtubules.Mol. Biol. Cell 618871902.
  • 66
    Tsai L.H., Delalle I., Caviness V.S.J, Chae T., Harlow E. (1994) p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5.Nature 371419423.
  • 67
    Van Engeland M., Kuijpers H.J., Ramaekers F.C., Reutelingsperger C.P., Schutte B. (1997) Plasma membrane alterations and cytoskeletal changes in apoptosis.Exp. Cell Res. 235421430.
  • 68
    Vaux D.L. & Korsmeyer S.J. (1999) Cell death in development.Cell 96245254.
  • 69
    Vincent I., Rosado M., Davies P. (1996) Mitotic mechanisms in Alzheimer's disease?J. Cell Biol. 132413425.
  • 70
    Vincent I., Jicha G., Rosado M., Dickson D.W. (1997) Aberrant expression of mitotic cdc2/cyclin B1 kinase in degenerating neurons of Alzheimer's disease brain.J. Neurosci. 1735883598.
  • 71
    Vulliet R., Halloran S.M., Braun R.K., Smith A.J., Lee G. (1992) Proline-directed phosphorylation of human Tau protein.J. Biol. Chem. 2672257022574.
  • 72
    Weingarten M.D., Lockwood A.H., Hwo S.Y., Kirschner M.W. (1975) A protein factor essential for microtubule assembly.Proc. Natl. Acad. Sci. USA 7218581862.
  • 73
    Welsh G.I., Miyamoto S., Price N.T., Safer B., Proud C.G. (1996) T-cell activation leads to rapid stimulation of translation initiation factor eIF2B and inactivation of glycogen synthase kinase-3.J. Biol. Chem. 2711141011413.
  • 74
    Yoshida H. & Ihara Y. (1993) Tau in paired helical filaments is functionally distinct from fetal tau: assembly incompetence of paired helical filament-tau.J. Neurochem. 6111831186.
  • 75
    Zhang J., Sanchez R.J., Wang S., Guarnaccia C., Tossi A., Zahariev S., Pongor S. (1994) Substrate specificity of CDC2 kinase from human HeLa cells as determined with synthetic peptides and molecular modeling.Arch. Biochem. Biophys. 315415424.
  • 76
    Zhang Q., Ahuja H.S., Zakeri Z.F., Wolgemuth D.J. (1997) Cyclin-dependent kinase 5 is associated with apoptotic cell death during development and tissue remodeling.Dev. Biol. 183222233.
  • 77
    Zhou H., Summers S.A., Birnbaum M.J., Pittman R.N. (1998) Inhibition of Akt kinase by cell-permeable ceramide and its implications for ceramide-induced apoptosis.J. Biol. Chem. 2731656816575.