Insulin-like growth factor-1 and insulin mediate transient site-selective increases in tau phosphorylation in primary cortical neurons

Neuroscience

Volumn 99, Issue 2, 2000, Pages 305-316

  Lesort, M ^a   Johnson, G V W ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Glycogen synthase kinase 3 ; IGF 1; Lithium; Phosphorylation; Primary cortical neuron; Tau

Indexed keywords

INSULIN; SOMATOMEDIN C; TAU PROTEIN;

ANIMAL CELL; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; HORMONE ACTION; IMMUNOCYTOCHEMISTRY; NERVE FIBER GROWTH; NEUROENDOCRINOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; EMBRYO; GROWTH CONES; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN-LIKE GROWTH FACTOR I; NEURITES; PHOSPHORYLATION; RATS; TAU PROTEINS;

EID: 0034638270     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(00)00200-1     Document Type: Article

References (44)

1. Alessi D.R., Cuenda A., Cohen P., Dudley D.T., Saltiel A.R. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. biol. Chem. 270:1995;27489-27494.
2. Beck K.D., Powell-Braxton L., Widmer H.R., Valverde J., Hefti F. Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron. 14:1995;717-730.
3. Binder L.I., Frankfurter A., Rebhun L.I. The distribution of tau in the mammalian central nervous system. J. Cell Biol. 101:1985;1371-1378.
4. Bixby J.L., Jhabvala P. Tyrosine phosphorylation in early embryonic growth cones. J. Neurosci. 13:1993;3421-3432.
5. Black M.M., Slaughter T., Moshiach S., Obrocka M., Fischer I. Tau is enriched on dynamic microtubules in the distal region of growing axons. J. Neurosci. 16:1996;3601-3619.
6. Brion J.P., Guilleminot J., Couchie D., Flament-Durand J., Nunez J. Both adult and juvenile tau microtubule-associated proteins are axon specific in the developing and adult rat cerebellum. Neuroscience. 25:1988;139-146.
7. Brion J.P., Smith C., Couck A.M., Gallo J.M., Anderton B.H. Developmental changes in tau phosphorylation: fetal tau is transiently phosphorylated in a manner similar to paired helical filament-tau characteristic of Alzheimer's disease. J. Neurochem. 61:1993;2071-2080.
8. Caceres A., Kosik K.S. Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature. 343:1990;461-463.
9. Carmel G., Mager E.M., Binder L.I., Kuret J. The structural basis of monoclonal antibody Alz50's selectivity for Alzheimer's disease pathology. J. biol. Chem. 271:1996;32789-32795.
10. Challacombe J.F., Snow D.M., Letourneau P.C. Dynamic microtubule ends are required for growth cone turning to avoid an inhibitory guidance cue. J. Neurosci. 17:1997;3085-3095.
11. Connor B., Dragunow M. The role of neuronal growth factors in neurodegenerative disorders of the human brain. Brain Res. Rev. 27:1998;1-39.
12. Dotti C.G., Sullivan C.A., Banker G.A. The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8:1988;1454-1468.
13. Drubin D.G., Feinstein S.C., Shooter E.M., Kirschner M.W. Nerve growth factor-induced neurite outgrowth in PC12 cells involves the coordinate induction of microtubule assembly and assembly-promoting factors. J. Cell Biol. 101:1985;1799-1807.
14. Ekinci F.J., Shea T.B. Hyperactivation of mitogen-activated protein kinase increases phospho-tau immunoreactivity within human neuroblastoma: additive and synergistic influence of alteration of additional kinase activities. Cell. molec. Neurobiol. 19:1999;249-260.
15. Esmaeli-Azad B., McCarty J.H., Feinstein S.C. Sense and antisense transfection analysis of tau function: tau influences net microtubule assembly, neurite outgrowth and neuritic stability. J. Cell Sci. 107:1994;869-879.
16. Feldman E.L., Sullivan K.A., Kim B., Russell J.W. Insulin-like growth factors regulate neuronal differentiation and survival. Neurobiol. Dis. 4:1997;201-214.
17. 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. Devl Brain Res. 49:1989;215-228.
18. Goedert M., Spillantini M.G., Potier M.C., Ulrich J., Crowther R.A. Cloning and sequencing of the cDNA encoding an isoform of microtubule-associated protein tau containing four tandem repeats: differential expression of tau protein mRNAs in human brain. Eur. molec. Biol. Org. J. 8:1989;393-399.
19. Hong M., Lee V.M. Insulin and insulin-like growth factor-1 regulate tau phosphorylation in cultured human neurons. J. biol. Chem. 272:1997;19547-19553.
20. Hughes K., Nikolakaki E., Plyte S.E., Totty N.F., Woodgett J.R. Modulation of the glycogen synthase kinase-3 family by tyrosine phosphorylation. Eur. molec. Biol. Org. J. 12:1993;803-808.
21. Illenberger S., Zheng-Fischhofer Q., Preuss U., Stamer K., Baumann K., Trinczek B., Biernat J., Godemann R., Mandelkow E.M., Mandelkow E. The endogenous and cell cycle-dependent phosphorylation of tau protein in living cells: implications for Alzheimer's disease. Molec. Cell Biol. 9:1998;1495-1512.
22. Johnson G.V.W., Hartigan J.A. Tau Protein in Normal and Alzheimer's Disease Brain: An Update. Alz. Dis. Rev. 3:1998;125-141 http://www. coa. uky. edu/ADReview/.
23. Kempf M., Clement A., Faissner A., Lee G., Brandt R. Tau binds to the distal axon early in development of polarity in a microtubule- and microfilament-dependent manner. J. Neurosci. 16:1996;5583-5592.
24. Kim B., Feldman E.L. Differential regulation of focal adhesion kinase and mitogen-activated protein kinase tyrosine phosphorylation during insulin-like growth factor-I-mediated cytoskeletal reorganization. J. Neurochem. 71:1998;1333-1336.
25. Kim B., Leventhal P.S., Saltiel A.R., Feldman E.L. Insulin-like growth factor-I-mediated neurite outgrowth in vitro requires mitogen-activated protein kinase activation. J. biol. Chem. 272:1997;21,268-21,273.
26. Lesort M., Jope R.S., Johnson G.V. Insulin transiently increases tau phosphorylation: involvement of glycogen synthase kinase-3 beta and Fyn tyrosine kinase. J. Neurochem. 72:1999;576-584.
27. Lesort M., Terro F., Esclaire F., Hugon J. Neuronal APP accumulates in toxic membrane blebbings. J. Neural Trans. 104:1997;497-513.
28. Leventhal P.S., Shelden E.A., Kim B., Feldman E.L. Tyrosine phosphorylation of paxillin and focal adhesion kinase during insulin-like growth factor-I-stimulated lamellipodial advance. J. biol. Chem. 272:1997;5214-5218.
29. Mandell J.W., Banker G.A. The microtubule cytoskeleton and the development of neuronal polarity. Neurobiol. Aging. 16:1995;229-237.
30. Mandell J.W., Banker G.A. A spatial gradient of tau protein phosphorylation in nascent axons. J. Neurosci. 16:1996;5727-5740.
31. Pope W., Enam S.A., Bawa N., Miller B.E., Ghanbari H.A., Klein W.L. Phosphorylated tau epitope of Alzheimer's disease is coupled to axon development in the avian central nervous system. Expl Neurol. 120:1993;106-113.
32. Recio-Pinto E., Lang F.F., Ishii D.N. Insulin and insulin-like growth factor II permit nerve growth factor binding and the neurite formation response in cultured human neuroblastoma cells. Proc. natn. Acad. Sci. USA. 81:1984;2562-2566.
33. Recio-Pinto E., Rechler M.M., Ishii D.N. Effects of insulin, insulin-like growth factor-II, and nerve growth factor on neurite formation and survival in cultured sympathetic and sensory neurons. J. Neurosci. 6:1986;1211-1219.
34. Russell J.W., Windebank A.J., Schenone A., Feldman E.L. Insulin-like growth factor-I prevents apoptosis in neurons after nerve growth factor withdrawal. J. Neurobiol. 36:1998;455-467.
35. Stambolic V., Ruel L., Woodgett J.R. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signaling in intact cells. Curr. Biol. 6:1996;1664-1668.
36. Takahashi M., Tomizawa K., Kato R., Sato K., Uchida T., Fujita S.C., Imahori K. Localization and developmental changes of tau protein kinase I/glycogen synthase kinase-3 beta in rat brain. J. Neurochem. 63:1994;245-255.
37. Tatebayashi Y., Iqbal K., Grundke-Iqbal I. Dynamic regulation of expression and phosphorylation of tau by fibroblast growth factor-2 in neural progenitor cells from adult rat hippocampus. J. Neurosci. 19:1999;5245-5254.
38. Tint I., Slaughter T., Fischer I., Black M.M. Acute inactivation of tau has no effect on dynamics of microtubules in growing axons of cultured sympathetic neurons. J. Neurosci. 18:1998;8660-8673.
39. Villa-Moruzzi E. Stimulation of FA and phosphatase-1 activities by insulin in 3T3-L1 cells. Fedn Eur. biochem. Socs Lett. 258:1989;208-210.
40. Vlahos C.J., Matter W.F., Hui K.Y., Brown R.F. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. biol. Chem. 269:1994;5241-5248.
41. Xie H., Litersky J.M., Hartigan J.A., Jope R.S., Johnson G.V. The interrelationship between selective tau phosphorylation and microtubule association. Brain Res. 798:1998;173-183.
42. Yang S.D., Chou C.K., Huang M., Song J.S., Chen H.C. Epidermal growth factor induces activation of protein kinase FA and ATP. Mg-dependent protein phosphatase in A431 cells. J. biol. Chem. 264:1989;5407-5411.
43. Yang S.D., Ho L.T., Fung T.J., Yu J.S. Insulin induces activation of kinase FA in membranes and thereby promotes activation of ATP. Mg-dependent phosphatase in adipocytes. Biochem. biophys. Res. Commun. 158:1989;762-768.
44. Zakharenko S., Popov S. Dynamics of axonal microtubules regulate the topology of new membrane insertion into the growing neurites. J. Cell Biol. 143:1998;1077-1086.