Swimming against the tide: Mobility of the microtubule-associated protein tau in neurons

Journal of Neuroscience

Volumn 27, Issue 37, 2007, Pages 9916-9927

  Konzack, Sven ^a,b   Thies, Edda ^a   Marx, Alexander ^a   Mandelkow, Eva Maria ^a   Mandelkow, Eckhard ^a  

^a MAX PLANCK UNIT FOR STRUCTURAL MOLECULAR BIOLOGY   (Germany)

^b Olympus Life and Material Science Europa GmbH   (Germany)

Author keywords

Alzheimer's disease; Axonal transport; Microtubules; Mitochondria; Synapse; Tau

Indexed keywords

CYAN FLUORESCENT PROTEIN; TAU PROTEIN;

ANIMAL CELL; ARTICLE; BRAIN CELL; CONTROLLED STUDY; DIFFUSION COEFFICIENT; EMBRYO; FLUORESCENCE MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RAT;

ANIMALS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NEURONS; PROTEIN TRANSPORT; RATS; TAU PROTEINS; VERO CELLS;

EID: 34548620157     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0927-07.2007     Document Type: Article

References (45)

1. Ahmad FJ, Baas PW (1995) Microtubules released from the neuronal centrosome are transported into the axon. J Cell Sci 108:2761-2769.
2. Andreadis A (2005) Tau gene alternative splicing: expression patterns, regulation and modulation of function in normal brain and neurodegenerative diseases. Biochim Biophys Acta 1739:91-103.
3. Aronov S, Aranda G, Behar L, Ginzburg I (2002) Visualization of translated tau protein in the axons of neuronal P19 cells and characterization of tau RNP granules. J Cell Sci 115:3817-3827.
4. Baas PW, Buster DW (2004) Slow axonal transport and the genesis of neuronal morphology. J Neurobiol 58:3-17.
5. Banker G, Goslin K (1988) Developments in neuronal cell culture. Nature 336:185-186.
6. Barghorn S, Zheng-Fischhofer Q, Ackmann M, Biernat J, von Bergen M, Mandelkow EM, Mandelkow E (2000) Structure, microtubule interactions, and paired helical filament aggregation by tau mutants of frontotemporal dementias. Biochemistry 39:11714-11721.
7. Biernat J, Gustke N, Drewes G, Mandelkow EM, Mandelkow E (1993) Phosphorylation of Ser262 strongly reduces binding of tau to microtubules: distinction between PHF-like immunoreactivity and microtubule binding. Neuron 11:153-163.
8. Bulinski JC, Odde DJ, Howell BJ, Salmon TD, Waterman-Storer CM (2001) Rapid dynamics of the microtubule binding of ensconsin in vivo. J Cell Sci 114:3885-3897.
9. Butner KA, Kirschner MW (1991) Tau protein binds to microtubules through a flexible array of distributed weak sites. J Cell Biol 115:717-730.
10. Chang S, Svitkina TM, Borisy GG, Popov SV (1999) Speckle microscopic evaluation of microtubule transport in growing nerve processes. Nat Cell Biol 1:399-403.
11. Chen J, Kanai Y, Cowan NJ, Hirokawa N (1992) Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons. Nature 360:674-677.
12. Drewes G, Ebneth A, Preuss U, Mandelkow EM, Mandelkow E (1997) MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell 89:297-308.
13. Drubin DG, Kirschner MW (1986) Tau protein function in living cells. J Cell Biol 103:2739-2746.
14. Garcia ML, Cleveland DW (2001) Going new places using an old MAP: tau, microtubules and human neurodegenerative disease. Curr Opin Cell Biol 13:41-48.
15. Goedert M, Jakes R (2005) Mutations causing neurodegenerative tauopathies. Biochim Biophys Acta 1739:240-250.
16. Gustke N, Trinczek B, Biernat J, Mandelkow EM, Mandelkow E (1994) Domains of tau protein and interactions with microtubules. Biochemistry 33:9511-9522.
17. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B (1998) A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 95:2509-2514.
18. He Y, Francis F, Myers KA, Yu W, Black MM, Baas PW (2005) Role of cytoplasmic dynein in the axonal transport of microtubules and neurofilaments. J Cell Biol 168:697-703.
19. Hirokawa N, Takemura R (2005) Molecular motors and mechanisms of directional transport in neurons. Nat Rev Neurosci 6:201-214.
20. Hirokawa N, Funakoshi T, Sato-Harada R, Kanai Y (1996) Selective stabilization of tau in axons and microtubule-associated protein 2C in cell bodies and dendrites contributes to polarized localization of cytoskeletal proteins in mature neurons. J Cell Biol 132:667-679.
21. Hollenbeck PJ, Saxton W (2005) The axonal transport of mitochondria. J Cell Sci 118:5411-5419.
22. Hong M, Zhukareva V, Vogelsberg-Ragaglia V, Wszolek Z, Reed L, Miller BI, Geschwind DH, Bird TD, McKeel D, Goate A, Morris JC, Wilhelmsen KC, Schellenberg GD, Trojanowski JQ, Lee VM (1998) Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 282:1914-1917.
23. 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.
24. 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.
25. Lee VM, Goedert M, Trojanowski JQ (2001) Neurodegenerative tauopathies. Annu Rev Neurosci 24:1121-1159.
26. Lim SS, Sammak PJ, Borisy GG (1989) Progressive and spatially differentiated stability of microtubules in developing neuronal cells. J Cell Biol 109:253-263.
27. Lu M, Kosik KS (2001) Competition for microtubule-binding with dual expression of tau missense and splice isoforms. Mol Biol Cell 12:171-184.
28. Ma Y, Shakiryanova D, Vardya I, Popov SV (2004) Quantitative analysis of microtubule transport in growing nerve processes. Curr Biol 14:725-730.
29. Mandelkow EM, Thies E, Trinczek B, Biernat J, Mandelkow E (2004) MARK/PAR1 kinase is a regulator of microtubule-dependent transport in axons. J Cell Biol 167:99-110.
30. Mercken M, Fischer I, Kosik KS, Nixon RA (1995) Three distinct axonal transport rates for tau, tubulin, and other microtubule-associated proteins: evidence for dynamic interactions of tau with microtubules in vivo. J Neurosci 15:8259-8267.
31. Miller KE, Sheetz MP (2006) Direct evidence for coherent low velocity axonal transport of mitochondria. J Cell Biol 173:373-381.
32. Olmsted JB, Stemple DL, Saxton W, Neighbors B, McIntosh JR (1989) Cell cycle-dependent changes in the dynamics of MAP 2 and MAP 4 in cultured cells. J Cell Biol 109:211-223.
33. Roy S, Coffee P, Smith G, Liem RK, Brady ST, Black MM (2000) Neurofilaments are transported rapidly but intermittently in axons: implications for slow axonal transport. J Neurosci 20:6849-6861.
34. Sabry J, O'Connor TP, Kirschner MW (1995) Axonal transport of tubulin in Ti1 pioneer neurons in situ. Neuron 14:1247-1256.
35. Samsonov A, Yu JZ, Rasenick M, Popov SV (2004) Tau interaction with microtubules in vivo. J Cell Sci 117:6129-6141.
36. Sontag E, Nunbhakdi-Craig V, Lee G, Brandt R, Kamibayashi C, Kuret J, White III CL, Mumby MC, Bloom GS (1999) Molecular interactions among protein phosphatase 2A, tau, and microtubules. Implications for the regulation of tau phosphorylation and the development of tauopathies. J Biol Chem 274:25490-25498.
37. Stamer K, Vogel R, Thies E, Mandelkow E, Mandelkow EM (2002) Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J Cell Biol 156:1051-1063.
38. Stoothoff WH, Johnson GV (2005) Tau phosphorylation: physiological and pathological consequences. Biochim Biophys Acta 1739:280-297.
39. Trinczek B, Ebneth A, Mandelkow EM, Mandelkow E (1999) Tau regulates the attachment/detachment but not the speed of motors in microtubule-dependent transport of single vesicles and organelles. J Cell Sci 112:2355-2367.
40. Utton MA, Connell J, Asuni AA, van Slegtenhorst M, Hutton M, de Silva R, Lees AJ, Miller CC, Anderton BH (2002) The slow axonal transport of the microtubule-associated protein tau and the transport rates of different isoforms and mutants in cultured neurons. J Neurosci 22:6394-6400.
41. Utton MA, Noble WJ, Hill JE, Anderton BH, Hanger DP (2005) Molecular motors implicated in the axonal transport of tau and alpha-synuclein. J Cell Sci 118:4645-4654.
42. Vershinin M, Carter B, Razafsky D, King SJ, Gross SP (2006) Multiple-motor based transport and its regulation by Tau. Proc Natl Acad Sci USA 104:87-92.
43. Wang L, Brown A (2002) Rapid movement of microtubules in axons. Curr Biol 12:1496-1501.
44. Wang L, Ho CL, Sun D, Liem RK, Brown A (2000) Rapid movement of axonal neurofilaments interrupted by prolonged pauses. Nat Cell Biol 2:137-141.
45. Waterman-Storer CM, Desai A, Bulinski JC, Salmon ED (1998) Fluorescent speckle microscopy, a method to visualize the dynamics of protein assemblies in living cells. Curr Biol 8:1227-1230.