Tau binding to microtubules does not directly affect microtubule-based vesicle motility

Journal of Neuroscience Research

Volumn 85, Issue 12, 2007, Pages 2620-2630

  Morfini, Gerardo ^a,b   Pigino, Gustavo ^a,b   Mizuno, Naoko ^c   Kikkawa, Masahide ^c   Brady, Scott T ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b MARINE BIOLOGICAL LABORATORY   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Microtubules; Tau binding; Vesicle motility

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN; KINESIN 1; TAU PROTEIN; UNCLASSIFIED DRUG;

AXOPLASM; CONFERENCE PAPER; CYTOPLASM; IN VITRO STUDY; MEMBRANE VESICLE; MICROTUBULE; NERVE FIBER TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING;

ANALYSIS OF VARIANCE; ANIMALS; AXONAL TRANSPORT; AXONS; CYTOPLASM; DECAPODIFORMES; HUMANS; MICROSCOPY, ELECTRON, SCANNING; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MOVEMENT; MUTATION; OPTIC LOBE, NONMAMMALIAN; TAU PROTEINS; TIME FACTORS; TRANSPORT VESICLES;

EID: 34250317264     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21154     Document Type: Conference Paper

References (82)

1. Amadoro G, Serafino AL, Barbato C, Ciotti MT, Sacco A, Calissano P, Canu N. 2004. Role of N-terminal tau domain integrity on the survival of cerebellar granule neurons. Cell Death Differ 11:217-230.
2. Amos LA. 1977. Arrangement of high molecular weight associated proteins on purified mammalian brain microtubules. J Cell Biol 72:642-654.
3. 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.
4. Baas PW, Qiang L. 2005. Neuronal microtubules: when the MAP is the roadblock. Trends Cell Biol 15:183-187.
5. Baas PW, Pienkowski TP, Kosik KS. 1991. Processes induced by tau expression in Sf9 cells have an axon-like microtubule organization. J Cell Biol 115:1333-1344.
6. Biernat J, Mandelkow EM. 1999. The development of cell processes induced by tau protein requires phosphorylation of serine 262 and 356 in the repeat domain and is inhibited by phosphorylation in the proline-rich domains. Mol Biol Cell 10:727-740.
7. Binder LI, Guillozet-Bongaarts AL, Garcia-Sierra F, Berry RW. 2005. Tau, tangles, and Alzheimer's disease. Biochim Biophys Acta 1739:216-223.
8. Brady ST, Lasek RJ, Allen RD. 1983. Fast axonal transport in extruded axoplasm from squid giant axon. Cell Motil3 [video supplement].
9. Brady ST, Lasek RJ, Allen RD. 1985. Video microscopy of fast axonal transport in isolated axoplasm: a new model for study of molecular mechanisms. Cell Motil 5:81-101.
10. Brady ST, Pfister KK, Leopold PL, Bloom GS. 1990. Fast Axonal Transport in Isolated Axoplasm. Cell Motil Cytoskeleton 17:22 [video supplement 2].
11. Brady ST, Richards BW, Leopold PL. 1993. Assay of vesicle motility in squid axoplasm. Methods Cell Biol 39:191-202.
12. 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.
13. 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 131:1327-1340.
14. Caceres A, Kosik KS. 1990. Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343:461-462.
15. Caceres A, Potrebic S, Kosik KS. 1991. The effect of tau antisense oligonucleotides on neurite formation of cultured cerebellar macroneurons. J Neurosci 11:1515-1523.
16. Charriere-Bertrand C, Nunez J. 1992. Regulation of tubulin, tau and microtubule associated protein 2 expression during mouse brain development. Neurochem Int 21:535-541.
17. Cho JH, Johnson GV. 2003. Glycogen synthase kinase 3beta phosphorylates tau at both primed and unprimed sites. Differential impact on microtubule binding. J Biol Chem 278:187-193.
18. Cleveland DW, Hwo SY, Kirschner MW. 1977. Purification of tau, a microtubule-associated protein that induces assembly of microtubules from purified tubulin. J Mol Biol 116:207-225.
19. Cyr JL, Brady ST. 1992. Molecular motors in axonal transport: cellular and molecular biology of kinesin. Mol Neurobiol 6:137-156.
20. Drechsel DN, Hyman AA, Cobb MH, Kirschner MW. 1992. Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol Biol Cell 3:1141-1154.
21. 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.
22. Drubin D, Kobayashi S, Kirschner M. 1986. Association of tau protein with microtubules in living cells. Ann N Y Acad Sci 466:257-268.
23. Drubin D, Kobayashi S, Kellogg D, Kirschner M. 1988. Regulation of microtubule protein levels during cellular morphogenesis in nerve growth factor-treated PC12 cells. J Cell Biol 106:1583-1591.
24. Ebneth A, Godemann R, Stamer K, Illenberger S, Trinczek B, Mandelkow E. 1998. Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J Cell Biol 143:777-794.
25. Esmaeli-Azad B, McCarty JH, Feinstein 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.
26. Felgner H, Frank R, Biernat J, Mandelkow EM, Mandelkow E, Ludin B, Matus A, Schliwa M. 1997. Domains of neuronal microtubule-associated proteins and flexural rigidity of microtubules. J Cell Biol 138:1067-1075.
27. Ferreira A, Busciglio J, Caceres A. 1987. An immunocytochemical analysis of the ontogeny of the microtubule-associated proteins MAP-2 and tau in the nervous system of the rat. Brain Res 431:9-31.
28. Ferreira A, Busciglio J, Caceres 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, Niclas J, Vale RD, Banker G, Kosik KS. 1992. Suppression of kinesin expression in cultured hippocampal neurons using antisense oligonucleotides. J Cell Biol 117:595-606.
30. Flaherty DB, Soria JP, Tomasiewicz HG, Wood JG. 2000. Phosphorylation of human tau protein by microtubule-associated kinases: GSK3beta and cdk5 are key participants. J Neurosci Res 62:463-472.
31. Grant P, Diggins M, Pant HC. 1999. Topographic regulation of cytoskeletal protein phosphorylation by multimeric complexes in the squid giant fiber system. J Neurobiol 40:89-102.
32. Gustke N, Trinczek B, Biernat J, Mandelkow EM, Mandelkow E. 1994. Domains of tau protein and interactions with microtubules. Biochemistry 33:9511-9522.
33. Hirokawa N. 1994a. Microtubule organization and dynamics dependent on microtubule-associated proteins. Curr Opin Cell Biol 6:74-81.
34. Hirokawa N. 1994b. The neuronal cytoskeleton: roles in neuronal morphogenesis and organelle transport. Prog Clin Biol Res 390:117-143.
35. Hirokawa N, Hisanaga S, Shiomura Y. 1988. MAP2 is a component of crossbridges between microtubules and neurofilaments in the neuronal cytoskeleton: quick-freeze, deep-etch immunoelectron microscopy and reconstitution studies. J Neurosci 8:2769-2779.
36. Jancsik V, Filliol D, Rendon A. 1996. Tau proteins bind to kinesin and modulate its activation by microtubules. Neurobiology 4:417-429.
37. Kanai Y, Takemura R, Oshima T, Mori H, Ihara Y, Yanigasawa M, Masaki T, Hirokawa N. 1989. Expression of multiple tau isoforms and microtubule bundle formation in fibroblasts transfected with a single tau cDNA. J Cell Biol 109:1173-1184.
38. Khatoon S, Grundke-Iqbal I, Iqbal K. 1992. Brain levels of microtubule-associated protein tau are elevated in Alzheimer's disease: a radioimmuno-slot-blot assay for nanograms of the protein. J Neurochem 59:750-753.
39. Knops J, Kosik KS, Lee G, Pardee JD, Cohen-Gould L, McConlogue L. 1991. Overexpression of tau in a nonneuronal cell induces long cellular processes. J Cell Biol 114:725-733.
40. Lasek RJ, Brady ST. 1985. Attachment of transported vesicles to microtubules in axoplasm is facilitated by AMP-PNP. Nature 316:645-647.
41. Lee G. 1993. Non-motor microtubule-associated proteins. Curr Opin Cell Biol 5:88-94.
42. Lee G, Newman ST, Gard DL, Band H, Panchamoorthy G. 1998. Tau interacts with src-family non-receptor tyrosine kinases. J Cell Sci 111:3167-3177.
43. Leger JG, Brandt R, Lee G. 1994. Identification of tau protein regions required for process formation in PC12 cells. J Cell Sci 107:3403-3412.
44. Leopold PL, Snyder R, Bloom GS, Brady ST. 1990. Nucleotide specificity for the bidirectional transport of membrane-bounded organelles in isolated axoplasm. Cell Motil Cytoskeleton 15:210-219.
45. Liao H, Li Y, Brautigan DL, Gundersen GG. 1998. Protein phosphatase 1 is targeted to microtubules by the microtubule-associated protein tau. J Biol Chem 273:21901-21908.
46. Lim RW, Halpain S. 2000. Regulated association of microtubule-associated protein 2 (MAP2) with Src and Grb2: evidence for MAP2 as a scaffolding protein. J Biol Chem 275:20578-20587.
47. Mandelkow EM, Biernat J, Drewes G, Gustke N, Trinczek B, Mandelkow E. 1995. Tau domains, phosphorylation, and interactions with microtubules. Neurobiol Aging 16:355-362.
48. Mandelkow EM, Schweers O, Drewes G, Biernat J, Gustke N, Trinczek B, Mandelkow E. 1996. Structure, microtubule interactions, and phosphorylation of tau protein. Ann N Y Acad Sci 777:96-106.
49. Mandelkow EM, Stamer K, Vogel R, Thies E, Mandelkow E. 2003. Clogging of axons by tau, inhibition of axonal traffic and starvation of synapses. Neurobiol Aging 24:1079-1085.
50. Marx A, Muller J, Mandelkow E. 2005. The structure of microtubule motor proteins. Adv Protein Chem 71:299-344.
51. Matus A. 1988. Microtubule-associated proteins: their potential role in determining neuronal morphology. Annu Rev Neurosci 11:29-44.
52. Mesngon MT, Tarricone C, Hebbar S, Guillotte AM, Schmitt EW, Lanier L, Musacchio A, King SJ, Smith DS. 2006. Regulation of cytoplasmic dynein ATPase by Lis1. J Neurosci 26:2132-2139.
53. Miller RH, Lasek RJ, Katz MJ. 1987. Preferred microtubules for vesicle transport in lobster axons. Science 235:220-222.
54. Mizuno N, Toba S, Edamatsu M, Watai-Nishii J, Hirokawa N, Toyoshima YY, Kikkawa M. 2004. Dynein and kinesin share an overlapping microtubule-binding site. EMBO J 23:2459-2467.
55. Morfini G, Tsai M, Szebenyi G, Brady ST. 2000. Approaches to study interactions between kinesin motors and membranes. In: Vernos I, editor. Kinesin protocols. Totowa, NJ: Humana Press. p 147-162.
56. Morfini G, Szebenyi G, Richards B, Brady ST. 2001. Regulation of kinesin: implications for neuronal development. Dev Neurosci 23:364-376.
57. Morfini G, Pigino G, Beffert U, Busciglio J, Brady ST. 2002a. Fast axonal transport misregulation and Alzheimer's disease. Neuromol Med 2:89-99.
58. Morfini G, Szebenyi G, Elluru R, Ratner N, Brady ST. 2002b. Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin-based motility. EMBO J 23:281-293.
59. Morfini G, Szebenyi G, Brown H, Pant HC, Pigino G, DeBoer S, Beffert U, Brady ST. 2004. A novel CDK5-dependent pathway for regulating GSK3 activity and kinesin-driven motility in neurons. EMBO J 23:2235-2245.
60. Morfini G, Pigino G, Brady ST. 2005a. Polyglutamine expansion diseases: failing to deliver. Trends Mol Med 11:64-70.
61. Morfini G, Stenoien DL, Brady ST. 2005b. Axonal transport. In: Siegel RWA, Brady ST, Price D, editors. Basic Neurochemistry. Boston, MA: Elsevier Academic Press. p 485-502.
62. Morfini G, Pigino G, Szebenyi G, You Y, Pollema S, Brady ST. 2006. JNK mediates pathogenic effects of polyglutamine-expanded androgen receptor on fast axonal transport. Nat Neurosci (in press).
63. Morris J, Lasek RJ. 1984. Monomer-polymer equilibria in the axon: direct measurement of tubulin and actin as polymer and monomer in axoplasm. J Cell Biol 98:2064-2076.
64. Murphy DB, Borisy GG. 1975. Association of high-molecular-weight proteins with microtubules and their role in microtubule assembly in vitro. Proc Natl Acad Sci U S A 72:2696-2700.
65. Oyama F, Kotliarova S, Harada A, Ito M, Miyazaki H, Ueyama Y, Hirokawa N, Nukina N, Ihara Y. 2004. Gem GTPase and tau: morphological changes induced by gem GTPase in cho cells are antagonized by tau. J Biol Chem 279:27272-27277.
66. Paglini G, Peris L, Mascotti F, Quiroga S, Caceres A. 2000. Tau protein function in axonal formation. Neurochem Res 25:37-42.
67. Papasozomenos SC, Binder LI. 1987. Phosphorylation determined two distinct species of tau in the central nervous system. Cell Motil Cytoskeleton 8:210-226.
68. Preuss U, Biernat J, Mandelkow EM, Mandelkow E. 1997. The "jaws" model of tau-microtubule interaction examined in CHO cells. J Cell Sci 110:789-800.
69. Ratner N, Bloom GS, Brady ST. 1998. A role for Cdk5 kinase in fast anterograde axonal transport: novel effects of olomoucine and the APC tumor suppressor protein. J Neurosci 18:7717-7726.
70. Samsonov A, Yu JZ, Rasenick M, Popov SV. 2004. Tau interaction with microtubules in vivo. J Cell Sci 117:6129-6141.
71. Santarella RA, Skiniotis G, Goldie KN, Tittmann P, Gross H, Mandelkow EM, Mandelkow E, Hoenger A. 2004. Surface-decoration of microtubules by human tau. J Mol Biol 339:539-553.
72. Seitz A, Kojima H, Oiwa K, Mandelkow EM, Song YH, Mandelkow E. 2002. Single-molecule investigation of the interference between kinesin, tau and MAP2c. EMBO J 21:4896-4905.
73. Shiomura Y, Hirokawa N. 1987. Colocalization of microtubule-associated protein 1A and microtubule-associated protein 2 on neuronal microtubules in situ revealed with double-label immunoelectron microscopy. J Cell Biol 104:1575-1578.
74. Sloboda RD, Rosenbaum JL. 1979. Decoration and stabilization of intact, smooth-walled microtubules with microtubule-associated proteins. Biochemistry 18:48-55.
75. Sontag E, Nunbhakdi-Craig V, Lee G, Brandt R, Kamibayashi C, Kuret J, White CL 3rd, 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.
76. 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.
77. Sun W, Qureshi HY, Cafferty PW, Sobue K, Agarwal-Mawal A, Neufield KD, Paudel HK. 2002. Glycogen synthase kinase-3beta is complexed with tau protein in brain microtubules. J Biol Chem 277: 11933-11940.
78. Szebenyi G, Smith GM, Li P, Brady ST. 2002. Overexpression of neurofilament H disrupts normal cell structure and function. J Neurosci Res 68:185-198.
79. Trinczek B, Biernat J, Baumann K, Mandelkow EM, Mandelkow E. 1995. Domains of tau protein, differential phosphorylation, and dynamic instability of microtubules. Mol Biol Cell 6:1887-1902.
80. 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.
81. Tsukane M, Yamauchi T. 2006. Increase in apoptosis with neural differentiation and shortening of the lifespan of P19 cells overexpressing tau. Neurochem Int 48:243-254.
82. Yoshizaki C, Tsukane M, Yamauchi T. 2004. Overexpression of tau leads to the stimulation of neurite outgrowth, the activation of caspase 3 activity, and accumulation and phosphorylation of tau in neuroblastoma cells on cAMP treatment. Neurosci Res 49:363-371.