Reduction of Detyrosinated Microtubules and Golgi Fragmentation Are Linked to Tau-Induced Degeneration in Astrocytes

Journal of Neuroscience

Volumn 23, Issue 33, 2003, Pages 10662-10671

  Yoshiyama, Yasumasa ^a   Zhang, Bin ^a   Bruce, Jennifer ^a   Trojanowski, John Q ^a   Lee, Virginia M Y ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Alzheimer; Astrocyte; Astroglial; Degeneration; Golgi; Microtubule; Tau

Indexed keywords

ALPHA TUBULIN; BETA TUBULIN; GLUTAMIC ACID; KINESIN; TAU PROTEIN; TUBULIN;

ACETYLATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ATROPHY; BIOSYNTHESIS; CELL CULTURE; CELL DEATH; CELL DEGENERATION; CELL DISRUPTION; CELL ORGANELLE; CONTROLLED STUDY; DEGENERATIVE DISEASE; DISEASE ASSOCIATION; GENE TRANSFER; GLIA CELL; GOLGI COMPLEX; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; RAT;

EID: 0344874553     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-33-10662.2003     Document Type: Article

References (52)

1. Binder LI, Frankfurter A, Rebhun LI (1985) The distribution of tau in the mammalian central nervous system. J Cell Biol 101:1371-1378.
2. Botez G, Probst A, Ipsen S, Tolnay M (1999) Astrocytes expressing hyperphosphorylated tau protein without glial fibrillary tangles in argyophilic grain disease. Acta Neuropathol 98:231-236.
3. Braak H, Braak E (1987) Argyrophilic grains: characteristic pathology of cerebral cortex in cases of adult onset dementia without Alzheimer changes. Neurosci Lett 76:124-127.
4. Carmignoto G (2000) Reciprocal communication systems between astrocytes and neurones. Prog Neurobiol 62:561-581.
5. Cleveland DW, Lopata MA, Sherline P, Kirschner MW (1981) Unpolymerized tubulin modulates the level of tubulin mRNAs. Cell 25:537-546.
6. Contin MA, Sironi JJ, Barra HS, Arce CA (1999) Association of tubulin carboxypeptidase with microtubules in living cells. Biochem J 339:463-471.
7. 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.
8. Feany MB, Dickson DW (1995) Widespread cytoskeletal pathology characterizes corticobasal degeneration. Am J Pathol 146:1388-1396.
9. Finkel E (2001) The mitochondrion: is it central to apoptosis? Science 292:624-626.
10. Forman MS, Zhukareva V, Bergeron C, Chin SS-M, Grossman M, Clark C, Lee VM-Y, Trojanowski JQ (2002) Signature tau neuropathology in gray and white matter of corticobasal degeneration. Am J Pathol 160:2045-2053.
11. Goedert M, Spillantini MG, Crowther RA, Chen SG, Parchi P, Tabaton M, Lanska DJ, Markesbery WR, Wilhelmsen KC, Dickson DW, Petersen RB, Gambetti P (1999) Tau gene mutation in familial progressive subcortical gliosis. Nat Med 5:454-457.
12. Gonatas JO, Mezitis SG, Stieber A, Fleischer B, Gonatas NK (1989) MG-160. A novel sialoglycoprotein of the medial cisternae of the Golgi. J Biol Chem 264:646-653.
13. Gonatas NK, Stieber A, Mourelatos Z, Chen Y, Gonatas JO, Appel SH, Hays AP, Hickey WF, Hauw JJ (1992) Fragmentation of the Golgi apparatus of motor neurons in amyotrophic lateral sclerosis. Am J Pathol 140:731-737.
14. Gundersen GG, Kalnoski MH, Bulinski JC (1984) Distinct populations of microtubules: tyrosinated and nontyrosinated alpha tubulin are distributed differently in vivo. Cell 38:779-789.
15. Gundersen GG, Khawaja S, Bulinski JC (1987) Postpolymerization detyrosinatin of alpha-tubulin: a mechanism for subcellular differentiation of microtubules. J Cell Biol 106:141-149.
16. Gurland G, Gundersen GG (1995) Stable detyrosinated microtubules function to localize vimentin intermediate filaments in fibroblast. J Cell Biol 131:1275-1290.
17. Gyoeva FK, Gelfand VI (1991) Coalignment of vimentin intermediate filaments with microtubules depends on kinesin. Nature 353:445-448.
18. Hagiwara H, Yorifuji H, Sato-Yoshitake R, Hirokawa N (1994) Competition between motor molecules (kinesin and cytoplasmic dynein) and fibrous microtubule-associated proteins in binding to microtubules. J Biol Chem 269:3581-3589.
19. Hall GF, Chu B, Lee G, Yao J (2000) Human tau filaments induce microtubules and synapse loss in an in vivo model of neurofibrillary degenerative disease. J Cell Sci 113:1373-1387.
20. Hauw JJ, Verny M, Delacre P, He Y, Duyckaerts C (1990) Constant neurofibrillary changes in the neocortex in progressive supranuclear palsy: basic differences with Alzheimer disease and aging. Neurosci Lett 119:182-186.
21. Higuchi M, Ishihara T, Zhang B, Hong M, Andreadis A, Trojanowski JQ, Lee VM-Y. (2002) Transgenic mouse model of tauopathies with glia pathology and nervous system degeneration. Neuron 35:433-446.
22. Hirokawa N, Shiomura Y, Okabe S (1988) Tau proteins: the molecular structure and mode of binding on microtubules. J Cell Biol 107:1449-1459.
23. Hirokawa N, Sato-Yoshitake R, Kobayashi N, Pfister KK, Bloom GS, Brady ST (1991) Kinesin associates with anterogradely transported membranous organelles in vivo. J Cell Biol 114:295-302.
24. Infante C, Ramos-Morales F, Fedriani C, Bornens M, Rios RM (1999) GMAP-210, A cis-Golgi network-associated protein, is a minus end microtubule-binding protein. J Cell Biol 145:83-98.
25. Ishihara T, Hong M, Zhang B, Nakagawa Y, Lee MK, Trojanowski JQ, Lee VM-Y. (1999) Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron 24:751-762.
26. Kosik KS, Orecchio LD, Binder L, Trojanowski JQ, Lee VM-Y, Lee G (1988) Epitopes that span the tau molecule are shared with paired helical filaments. Neuron 1:817-825.
27. Kreis TE (1987) Microtubules containing detyrosinated tubulin are less dynamic. EMBO J 6:2597-2606.
28. Kreitzer G, Liao G, Gundersen GG (1999) Detyrosination of tubulin regulates the interaction of intermediate filaments with microtubules in vivo via a kinesin-dependent mechanism. Mol Biol Cell 10:1105-1118.
29. Larcher JC, Boucher D, Lazereg S, Gros F, Denoulet P (1996) Interaction of kinesin motor domains with α- and β-tubulin subunits at a tau-independent binding site. Regulation by polyglutamylation. J Biol Chem 271:22117-22124.
30. Lee VM-Y, Goedert M, Trojanowski JQ (2001) Neurodegenerative tauopathies. Annu Rev Neurosci 24:1121-1159.
31. Liao G, Gundersen GG (1998) Kinesin is a candidate for cross-bridging microtubules and intermediate filaments. Selective binding of kinesin to detyrosinated tubulin and vimentin. J Biol Chem 273:9797-9803.
32. MacRae TH (1997) Tubulin post-translational modifications-enzymes and their mechanisms of action. Eur J Biochem 244:265-278.
33. Manthorpe M, Rudge JS, Varon S (1986) Astroclial cell contributions to neuronal survival and neuritic growth. In: Astrocytes (Fedoroff S, Vernadakis A, eds). Orlando, FL: Academic.
34. Marya PK, Syed Z, Fraylich PE, Eagles PA (1994) Kinesin and tau bind to distinct sites on microtubules. J Cell Sci 107:339-344.
35. McCarthy KD, de Vellis J (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902.
36. Merrick SE, Trojanowski JQ, Lee VM-Y (1997) Selective destruction of stable microtubules and axons by inhibitors of protein serine/threonine phosphatases in cultured human neurons (NT2N cells). J Neurosci 17:5726-5737.
37. Mourelatos Z, Yachnis A, Rorke L, Mikol L, Gonatas NK (1993) The Golgi apparatus of motor neurons in amyotrophic lateral sclerosis. Ann Neurol 33:608-615.
38. Mourelatos Z, Gonatas NK, Stieber A, Gurney ME, Dal Canto MC (1996) The Golgi apparatus of spinal cord motor neurons in transgenic mice expressing mutant Cu, Zn superoxide dismutase becomes fragmented in early, preclinical stages of the disease. Proc Natl Acad Sci USA 93:5472-5477.
39. Pfister KK, Wagner MC, Stenoien DL, Brady ST, Bloom GS (1989) Monoclonal antibodies to kinesin heavy and light chains stain vesicle-like structures, but not microtubules, in cultured cells. J Cell Biol 108:1453-1463.
40. Prahlad V, Yoon M, Moir RD, Vale RD, Goldman RD (1998) Rapid movements of vimentin on microtubule tracks: kinesin-dependent assembly of intermediate filament networks. J Cell Biol 143:159-170.
41. Rapoport M, Dawson HN, Binder LI, Vitek MP, Ferreira A (2002) Tau is essential to β-amyloid-induced neurotoxicity. Proc Natl Acad Sci USA 99:6364-6369.
42. Sakurai A, Okamoto K, Fujita Y, Nakazato Y, Wakabayashi K, Takahashi H, Gonatas NK (2000) Fragmentation of the Golgi apparatus of the ballooned neurons in patients with corticobasal degeneration and Creutzfeldt-Jakob disease. Acta Neuropathol 100:270-274.
43. Seubert P, Mawal-Dewan M, Barbour R, Jakes R, Goedert M, Johnson GV, Litersky JM, Schenk D, Lieberburg I, Trojanowski JQ, Lee V.M.-Y (1995) Detection of phosphorylated Ser262 in fetal tau, adult tau, and paired helical filament tau. J Biol Chem 270:18917-18922.
44. Shin RW, Iwaki T, Kitamoto T, Tateishi J (1991) Hydrated autoclave pretreatment enhances tau immunoreactivity in formalin-fixed normal and Alzheimer's disease brain tissue. Lab Invest 64:693-702.
45. Spillantini MG, Goedert M (1998) Tau protein pathology in neurodegenerative diseases. Trends Neurosci 21:428-433.
46. 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.
47. Stieber A, Mourelatos Z, Gonatas NK (1996) In Alzheimer's disease the Golgi apparatus of a population of neurons without neurofibrillary tangles is fragmented and atrophic. Am J Pathol 148:415-426.
48. Tanemura K, Murayama M, Akagi T, Hashikawa T, Tominaga T, Ichikawa M, Yamaguchi H, Takashima A (2002) Neurodegeneration with tau accumulation in a transgenic mouse expressing V337M human tau. J Neurosci 22:133-141.
49. 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.
50. Vogelsberg-Ragaglia V, Bruce J, Richter-Landsberg C, Zhang B, Hong M, Trojanowski JQ, Lee VM-Y (2000) Distinct FTDP-17 missense mutations in tau produce tau aggregates and other pathological phenotypes in transfected CHO cells. Mol Biol Cell 11:4093-4104.
51. Yamada T, McGeer PL, McGeer EG (1992) Appearance of paired nucleated, tau-positive glia in patients with progressive supranuclear palsy brain tissue. Neurosci Lett 135:99-102.
52. Yen TJ, Gay DA, Pachter JS, Cleveland DW (1988) Autoregulated changes in stability of polyribosome-bound beta-tubulin mRNAs are specified by the first 13 translated nucleotides. Mol Cell Biol 8:1224-1235.