Tau interacts with golgi membranes and mediates their association with microtubules

Cell Motility and the Cytoskeleton

Volumn 63, Issue 11, 2006, Pages 710-724

  Farah, Carole Abi ^a,b   Perreault, Sébastien ^a   Liazoghli, Dalinda ^a,b   Desjardins, Mylène ^a   Anton, Angela ^a   Lauzon, Michel ^a   Paiement, Jacques ^a   Leclerc, Nicole ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Golgi membranes; Immunogold; In vitro reconstitution assay; Microtubules; Subcellular fractionation; Tau membranous association

Indexed keywords

ANTIBODY; BIOLOGICAL MARKER; ISOPROTEIN; MANNOSIDASE; MANNOSIDASE II; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN MG160; PROTEIN TGN38; TAU PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CELL FRACTIONATION; ELECTRON MICROSCOPE; EMBRYO; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HIPPOCAMPUS; IMMUNOGOLD LABELING; IN VITRO STUDY; ISOLATION PROCEDURE; MEMBRANE VESICLE; MICROTUBULE; MORPHOMETRICS; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; BRAIN; CELLS, CULTURED; GOLGI APPARATUS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR MEMBRANES; MICE; MICROSCOPY, ELECTRON; MICROTUBULES; NEURONS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SUBCELLULAR FRACTIONS; TAU PROTEINS;

EID: 33750553861     PISSN: 08861544     EISSN: 10970169     Source Type: Journal    
DOI: 10.1002/cm.20157     Document Type: Article

References (51)

1. Banker G, Goslin K. 1998. Culturing Nerve Cells: A Bradford Book. Cambridge, MA: MIT Press. 666 p.
2. Baudhuin P, Evrard P, Berthet J. 1967. Electron microscopic examination of subcellular fractions. I. The preparation of representative samples from suspensions of particles. J Cell Biol 32(1):181-191.
3. Bloom GS, Brashear TA. 1989. A novel 58-kDa protein associates with the Golgi apparatus and microtubules. J Biol Chem 264(27):16083-16092.
4. Boyd A, Bolton W, Brinkley B. 1982. Microtubules and β cell function: Effect of colchicine on microtubules and insulin secretion in vitro by mouse β cells. J Cell Biol 92:425-434.
5. Brandt R, Léger J, Lee G. 1995. Interaction of τ with the neural plasma membrane mediated by τ's amino-terminal projection domain. J Cell Biol 131:1327-1340.
6. Buée L, Bussiere T, Buee Scherrer V, Delacourte A, Hof PR. 2000. τ protein isoforms, phosphorylation, and role in neurodegenerative disorders. Brain Res Brain Res Rev 33(1):95-130.
7. Caceres A, Potrebic S, Kosik K. 1991. The effect of τ antisense oligonucleotides on neurite formation of cultured cerebellar macroneurons. J Neurosci 11(6):1515-1523.
8. Caceres A, Mautino J, Kosik K. 1992. Suppression of MAP2 in cultured cerebellar macroneurons inhibits minor neurite formation. Neuron 9(4):607-618.
9. Cole N, Sciaky N, Marotta A, Song J, Lippincott-Schwartz J. 1996. Golgi dispersal during microtubule disruption: regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites. Mol Biol Cell 7:631-650.
10. Dawson H, Ferreira A, Eyster M, Ghoshal N, Binder L, Vitek M. 2001. Inhibition of neuronal maturation in primary hippocampal neurons from τ deficient mice. J Cell Sci 114(6):1179-1187.
11. Drewes G, Ebneth A, Mandelkow E. 1998. MAPs, MARKs, and microtubule dynamics. Trends Biochem Sci 23(8):307-311.
12. Farah C, Nguyen M, Julien J, Leclerc N. 2003. Altered levels and distribution of microtubule-associated proteins before disease onset in a mouse model of amyotrophic lateral sclerosis. J Neurochem 84(1):77-86.
13. Farah C, Liazoghli D, Perreault S, Desjardins M, Guimont A, Anton A, Lauzon M, Kreibich G, Paiement J, Leclerc N. 2005. Interaction of microtubule-associated protein-2 and p63: A new link between microtubules and rough endoplasmic reticulum membranes in neurons. J Biol Chem 280(10):9439-9449.
14. Garcia ML, Cleveland DW. 2001. Going new places using an old MAP: τ, microtubules and human neurodegenerative disease. Curr Opin Cell Biol 13(1):41-48.
15. Gleeson P, Lock J, Luke M, Stow J. 2004. Domains of the TGN: Coats, tethers and G proteins. Traffic 5:315-326.
16. Gonatas J, Chen Y, Stieber A, Mourelatos Z, Gonatas N. 1998. Truncations of the C-terminal cytoplasmic domain of MG160, a medial Golgi sialoglycoprotein, result in its partial transport to the plasma membrane and filopodia. J Cell Sci 111:249-260.
17. Heidary G, Fortini M. 2001. Identification and characterization of the Drosophila τ homolog. Mech Dev 108:171-178.
18. Heins S, Song Y, Wille H, Mandelkow E, Mandelkow E. 1991. Effect of MAP2, MAP2c and τ on kinesin-dependent microtubule motility. J Cell Sci Suppl 14:121-124.
19. Jicha G, Weaver C, Lane E, Vianna C, Kress Y, Rockwood J, Davies P. 1999. cAMP-dependent protein kinase phosphorylations on τ in Alzheimer's disease. J Neurosci 19(17):7486-7494.
20. Jung D, Filliol D, Miehe M, Rendon A. 1993. Interaction of brain mitochondria with microtubules reconstituted from brain tubulin and MAP2 or τ. Cell Motil Cytoskeleton 24(4):245-255.
21. Kawarabayashi T, Shoji M, Youkin L, Wen-Lang L, Dickson D, Murakami T, Matsubara E, Abe K, Ashe K, Younkin S. 2004. Dimeric amyloid B protein rapidly accumulates in lipid rafts followed by apoliprotein E and phosphorylated τ accumulation in the Tg2576 mouse model of Alzheimer' s disease. J Neurosci 24(15):3801-3809.
22. Lallemand-Breitenbach V, Quensnoit M, Braun V, El Marjou A, Pous C, Goud B, Perez F. 2004. CLIPR-59 is a lipid raft-associated protein containing a cytoskeleton-associated protein glycine-rich domain (CAP-Gly) that perturbs microtubule dynamics. J Biol Chem 279(39):41168-41178.
23. Lavoie C, Lanoix J, Kan FW, Paiement J. 1996. Cell-free assembly of rough and smooth endoplasmic reticulum. J Cell Sci 109 (Part 6):1415-1425.
24. Lee G, Newman S, Gard D, Band H, Panchamoorthy G. 1998. τ interacts with src-family non-receptor tyrosine kinases. J Cell Sci 111 (Part 21):3167-3177.
25. Lee V, Goedert M, Trojanowski J. 2001. Neurodegenerative tauopathies. Annu Rev Neurosci 24:1121-1159.
26. Liazoghli D, Perreault S, Micheva K, Desjardins M, Leclerc N. 2005. Fragmentation of the Golgi apparatus induced by the overexpression of wild-type and mutant human τ forms in neurons. Am J Pathol 166(5):1499-1514.
27. Lin W, Lewis J, Yen S, Hutton M, Dickson D. 2003. Ultrastructural neuronal pathology in transgenic mice expressing mutant (P301L) human tau. J Neurocytol 32:1091-1105.
28. Lucocq J, Pryde JG, Berger EG, Warren G. 1987. A mitotic form of the Golgi apparatus in Hela cells. J Cell Biol 104(4):865-874.
29. Lucocq J, Warren G. 1987. Fragmentation and partitioning of the Golgi apparatus during mitosis in Hela cells. EMBO J 6(11):3239-3246.
30. Lutjens R, Igarashi M, Pellier V, Blasey H, Di Paolo G, Ruchti E, Pfulg C, Staple J, Catsicas S, Grenningloh G. 2000. Localization and targeting of SCG10 to the trans-Golgi apparatus and growth cone vesicles. Eur J Neurosci 12:2224-2234.
31. Maas T, Eidenmller J, Brandt R. 2000. Interaction of τ with the neural membrane cortex is regulated by phosphorylation at sites that are modified in paired helical filaments. J Biol Chem 275(21):15733-15740.
32. Mandell J, Banker G. 1996. Microtubule-associated proteins, phosphorylation gradients, and the establishment of neuronal polarity. Perspect Dev Neurobiol 4(2/3):125-135.
33. Marsh B, Mastonarde D, Buttle K, Howell K, McIntosh R. 2001. Organellar relationships in the Golgi region of the pancreatic β cell line, HIT-115, visualized by high resolution electron tomography. Proc Natl Acad Sci USA 98:2399-2406.
34. Micheva K, Vallée A, Beaulieu C, Herman I, Leclerc N. 1998. βActin is confined to structures having high capacity of remodelling in developing and adult rat cerebellum. Eur J Neurosci 10(12): 3785-3798.
35. Mogelsvang S, Marsh B, Ladeinsky M, Howell K. 2004. Predicting function from structure: 3D structure studies of the mammalian Golgi complex. Traffic 5:338-345.
36. Papasozomenos S, Binder L. 1987. Phosphorylation determines two distinct species of τ in the central nervous system. Cell Motil Cytoskeleton 8:210-226.
37. Pernet-Gallay K, Antony C, Johannes L, Bornens M, Goud B, Rios R. 2002. The overexpression of GMAP-210 blocks anterograde and retrograde transport between the ER and the Golgi apparatus. Traffic 3:822-832.
38. Peters A, Palay S, Webster H. 1976. The Fine Structure of the Nervous System: The Neurons and Supporting Cells. Philadelphia: Saunders. 406 p.
39. Rambourg A, Clermont Y. 1990. Three-dimensional electron microscopy: Structure of the Golgi apparatus. Eur J Cell Biol 51:189-200.
40. Rios R, Sanchis A, Tassin A, Fedriani C, Bornens M. 2004. GMAP-210 recruits γ-tubulin complexes to cis-Golgi membranes and is required for Golgi ribbon formation. Cell 118:323-335.
41. Sampo B, Kaech S, Kunz S, Banker G. 2003. Two distinct mechanisms target membrane proteins to the axonal surface. Neuron 37:611-624.
42. Stamer K, et al. 2002. τ blocks traffic of organelles, neurofilaments and APP vesicles in neurons and enhances oxidative stress. J Cell Biol 156(6):1051-1063.
43. Sytnyk V, Leshchyns'ka I, Ditayatev A, Schachner M. 2004. Trans-Golgi network delivery of synaptic proteins in synaptogenesis. J Cell Sci 117:381-88.
44. Taguchi T, Pypaert M, Warren G. 2003. Biochemical sub-fractionation of the mammalian Golgi apparatus. Traffic 4:344-352.
45. Torre E, Steward O. 1996. Protein synthesis within dendrites: Glycosylation of newly synthesized proteins in dendrites of hippocampal neurons in culture. J Neurosci 16:5967-5978.
46. Van Vliet C, et al. 2003. Intracellular sorting and transport of proteins. Prog Biophys Mol Biol 83(1):1-45.
47. Velasco A, Hendricks L, Moremen K, Tulsani D, Touster O, Farquhar M. 1993. Cell type-dependent variations in the subcellular distribution of α-mannosidase I and II. J Cell Biol 122(1): 39-51.
48. Walenta J, Didier A, Liu X, Kramer H. 2001. The Golgi-associated Hook3 protein is a member of a novel family of microtubule-associated proteins. J Cell Biol 152:923-934.
49. Wiedenmann B, Lawley K, Grund C, Branton D. 1985. Solubilization of proteins from bovine brain coated vesicles by protein perturbants and triton X-100. J Cell Biol 101:12-18.
50. Yamaguchi N, Fukada M. 1995. Golgi retention mechanism of β-1-4-galactosyltransferase. Membrane-spanning domain-dependent homodimerization and association with α- and β-tubulins. J Biol Chem 270:12170-12176.
51. Yoshiyama Y, Zhang B, Bruce J, Trojanowski J, Lee V. 2003. Reduction of detyrosinated microtubules and Golgi fragmentation are linked to τ-induced degeneration in astrocytes. J Neurosci 23:10662-10671.