Tau binds to the distal axon early in development of polarity in a microtubule- and microfilament-dependent manner

Journal of Neuroscience

Volumn 16, Issue 18, 1996, Pages 5583-5592

  Kempf, Martina ^a   Clement, Albrecht ^a   Faissner, Andreas ^a   Lee, Gloria ^b   Brandt, Roland ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

axon; hippocampal neuron; microtubule associated protein; plasma membrane; polarity; tau

Indexed keywords

COLCHICINE; CYTOCHALASIN B; MICROTUBULE ASSOCIATED PROTEIN 2; TAU PROTEIN;

ANIMAL CELL; ARTICLE; CELL POLARITY; CONTROLLED STUDY; DEPOLYMERIZATION; HIPPOCAMPUS; MICROFILAMENT; MICROTUBULE; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; RAT;

EID: 0029812945     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-18-05583.1996     Document Type: Article

References (55)

1. Baas PW, Sinclair GI, Heidemann SR (1987) Role of microtubules in the cytoplasmic compartmentation of neurons. Brain Res 420:73-81.
2. Baas PW, MM Black, Banker GA (1989) Changes in microtubule polarity orientation during the development of hippocampal neurons in culture. J Cell Biol 109:3085-3094.
3. Baas PW, Pienkowski TP, Cimbalnik KA, Toyama K, Bakalis S, Ahmad FJ, Kosik KS (1994) Tau confers drug stability but not cold stability to microtubules in living cells. J Cell Sci 107:135-143.
4. Bamburg JR, Bray D, Chapman K (1986) Assembly of microtubules at the tip of growing axons. Nature 321:788-790.
5. Banker G, Waxman A (1988) Hippocampal neurons generate natural shapes in cell culture. In: Intrinsic determinants of neuronal form (Lasek R, Black MB, eds). New York: Liss.
6. Bernhardt R, Matus A (1984) Light and electron microscopic studies of the distribution of microtubule-associated protein 2 in rat brain: a difference between dendritic and axonal cytoskeletons. J Comp Neurol 226:203-221.
7. Binder LI, Frankfurter A, Rebhun LI (1985) The distribution of tau in the mammalian central nervous system. J Cell Biol 101:1371-1378.
8. Bottenstein JE, Sato GH (1979) Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc Natl Acad Sci USA 76:514-519.
9. Brandt R, Lee G (1993) Functional organization of microtubule-associated protein tau. Identification of regions which affect microtubule growth, nucleation, and bundle formation in vitro. J Biol Chem 268:3414-3419.
10. Brandt R, Léger J, Lee G (1995) Interaction of tau with the neural plasma membrane mediated by tau's amino-terminal projection domain. J Cell Biol 131:1327-1340.
11. Brion JP, Guilleminot J, Couchie D, Flament DJ, Nunez J (1988) Both adult and juvenile tau microtubule-associated proteins are axon specific in the developing and adult rat cerebellum. Neuroscience 25:139-146.
12. Butner KA, Kirschner MW (1991) Tau protein binds to microtubules through a flexible array of distributed weak sites. J Cell Biol 115:717-730.
13. Cáceres A, Kosik KS (1990) Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343:461-463.
14. Cáceres A, Binder LI, Payne M, Bender P, Rebhun L, Steward O (1984) Differential subcellular localization of tubulin and the microtubule-associated protein MAP-2 in brain tissue as revealed by immunocytochemistry with hybridoma monoclonal antibodies. J Neurosci 4:394-410.
15. Cooper JA (1987) Effects of cytochalasin and phalloidin on actin. J Cell Biol 105:1473-1478.
16. Craig AM, Banker G (1994) Neuronal polarity. Annu Rev Neurosci 17:267-310.
17. Craig AM, Wyborski RJ, Banker G (1995) Preferential addition of newly synthesized membrane protein at axonal growth cones. Nature 375:592-594.
18. Dai J, Sheetz MP (1995) Axon membrane flows from the growth cone to the cell body. Cell 83:693-701.
19. DeCamilli P, Miller PE, Navone F, Theurkauf WE, Vallee RB (1984) Distribution of microtubule-associated protein 2 in the nervous system of the rat studied by immunofluorescence. Neuroscience 11:817-846.
20. DeHoop MJ, Dotti CG (1993) Membrane traffic in polarized neurons in culture. J Cell Sci Suppl 17:85-92.
21. Deitch JS, Banker GA (1993) An electron microscopic analysis of hippocampal neurons developing in culture: early stages in the emergence of polarity. J Neurosci 13:4301-4315.
22. DiTeMa M, Feiguin F, Morfini G, Cáceres A (1994) Microfilament-associated growth cone component depends upon tau for its intracellular localization. Cell Motil Cytoskeleton 29:117-130.
23. Dotti CG, Banker GA, Binder LI (1987) The expression and distribution of the microtubule-associated protein tau and microtubule-associated protein 2 in hippocampal neurons in the rat in situ and in cell culture. Neuroscience 23:121-130.
24. Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8:1454-1468.
25. Drubin DG, Kirschner MW (1986) Tau protein function in living cells. J Ceil Biol 103:2739-2746.
26. Drubin DG, Feinstein SC, Shooter EM, Kirschner MW (1985) Nerve growth factor-induced neurite outgrowth in PC12 cells involves the coordinate induction of microtubule assembly and assembly-promoting factors. J Cell Biol 101:1799-1807.
27. Esmaeli-Azad B, McCarty JH, Feinstem SC (1994) Sense and antisense transfection analysis of tau function - tau influences net microtubule assembly, neurite outgrowth, and neuritic stability. J Cell Sci 107:869-879.
28. Ferreira A, Busciglio J, Cáceres A (1989) 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 49:215-228.
29. Ferreira A, Kincaid R, Kosik KS (1993) Calcineurin is associated with the cytoskeleton of cultured neurons and has a role in the acquisition of polarity. Mol Biol Cell 4:1225-1238.
30. Garner CC, Tucker RP, Matus A (1988) Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites. Nature 336:674-677.
31. Goedert M, Crowther RA, Garner CC (1991) Molecular characterization of microtubule-associated proteins tau and MAP2. Trends Neurosci 14:193-199.
32. Goslin K, Banker G (1990) Rapid changes in the distribution of GAP-43 correlate with the expression of neuronal polarity during normal development and under experimental conditions. J Cell Biol 110:1319-1331.
33. Goslin K, Banker G (1991) Rat hippocampal neurons in low-density culture. In: Culturing nerve cells (Banker G, Goslin K, eds), pp 251-281. Cambridge, MA: MIT.
34. Gustke N, Trinczek B, Biernat J, Mandelkow E-M, Mandelkow E (1994) Domains of tau protein and interactions with microtubules. Biochemistry 33:9511-9522.
35. Hanemaaijer R, Ginzburg I (1991) Involvement of mature tau isoforms in the stabilization of neurites in PC12 cells. J Neurosci Res 30:163-171.
36. Kanai Y, Hirokawa N (1995) Sorting mechanisms of tau and MAP2 in neurons: suppressed axonal transit of MAP2 and locally regulated microtubule binding. Neuron 14:421-432.
37. Knops J, Kosik KS, Lee G, Pardee JD, Cohen GL, McConlogue L (1991) Overexpression of tau in a non-neuronal cell induces long cellular processes. J Cell Biol 114:725-733.
38. Kosik KS, Finch EA (1987) MAP2 and tau segregate into dendritic and axonal domains after the elaboration of morphologically distinct neurites: an immunocytochemical study of cultured rat cerebrum. J Neurosci 7:3142-3153.
39. Kosik KS, Orecchio LD, Binder L, Trojanowski JQ, Lee VM, Lee G (1988) Epitopes that span the tau molecule are shared with paired helical filaments. Neuron 1:817-825.
40. Kowall NW, Kosik KS (1987) Axonal disruption and aberrant localization of tau protein characterize the neuropil pathology of Alzheimer's disease. Ann Neurol 22:639-643.
41. Lee G, Rook SL (1992) Expression of tau protein in non-neuronal cells: microtubule binding and stabilization. J Cell Sci 102:227-237.
42. Lee G, Neve RL, Kosik KS (1989) The microtubule binding domain of tau protein. Neuron 2:1615-1624.
43. Litman P, Barg J, Rindzoonski L, Ginzburg I (1993) Subcellular localization of tau mRNA in differentiating neuronal cell culture: implications for neuronal polarity. Neuron 10:627-638.
44. Nakata T, Hirokawa N (1987) Cytoskeletal reorganization of human platelets after stimulation revealed by the quick-freeze deep-etch technique. J Cell Biol 105:1771-1780.
45. Okabe S, Hirokawa N (1989) Rapid turnover of microtubule-associated protein MAP2 in the axon revealed by microinjection of biotinylated MAP2 into cultured neurons. Proc Natl Acad Sci USA 86:4127-4131.
46. Peng I, Binder LI, Black MM (1986) Biochemical and immunological analyses of cytoskeletal domains of neurons. J Cell Biol 102:252-262.
47. Pennypacker K, Fischer I, Levin P (1991) Early in vitro genesis and differentiation of axons and dendrites by hippocampal neurons analyzed quantilatively with neurofilament-H and microtubule-associated protein 2 antibodies. Exp Neurol 111:25-35.
48. Pfeffer SR, Drubin DG, Kelley RB (1983) Identification of three coated vesicle components as α- and β-tubulin linked to a phosphorylated 50,000-dalton polypeptide. J Cell Biol 97:40-47.
49. Pleasure SJ, Page C, Lee VMY (1992) Pure, postmitotic, polarized human neurons derived from NTera 2 cells provide a system for expressing exogenous proteins in terminally differentiated neurons. J Neurosci 12:1802-1815.
50. Sharp DJ, Yu WQ, Baas PW (1995) Transport of dendritic microtubules establishes their nonuniform polarity. J Cell Biol 130:93-103.
51. Shea TB, Beermann ML, Nixon RA, Fischer I (1992) Microtubule-associated protein tau is required for axonal neurite elaboration by neuroblastoma cells. J Neurosci Res 32:363-374.
52. Trojanowski JQ, Schuck T, Schmidt ML, Lee VM (1989) Distribution of tau proteins in the normal human central and peripheral nervous system. J Histochem Cytochem 37:209-215.
53. Webster D, Gundersem G, Bulinski J, Borisy G (1987) Differential turnover of tyrosinated and detyrosinated microtubules. Proc Natl Acad Sci USA 84:9040-9044.
54. Wilson L, Bryan J (1974) Biochemical and pharmacological properties of microtubules. Adv Cell Mol Biol 3:22-72.
55. Winckler B, Poo M (1996) No diffusion barrier at axon hillock. Nature 379:213.