Regulation of mitochondrial transport and inter-microtubule spacing by tau phosphorylation at the sites hyperphosphorylated in Alzheimer's disease

Journal of Neuroscience

Volumn 32, Issue 7, 2012, Pages 2430-2441

  Shahpasand, Kourosh ^a   Uemura, Isao ^a   Saito, Taro ^a   Asano, Tsunaki ^a   Hata, Kenji ^a   Shibata, Keitaro ^b   Toyoshima, Yoko ^b   Hasegawa, Masato ^c   Hisanaga, Shin Ichi ^a  

^a TOKYO METROPOLITAN UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ASPARTIC ACID; SERINE; TAU PROTEIN; THREONINE;

ACTIN FILAMENT; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; FEMALE; HUMAN; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; MICROTUBULE; MITOCHONDRION; MOUSE; MUTATION; NERVE FIBER; NEURITE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; TIME LAPSE IMAGING;

ALANINE; ALZHEIMER DISEASE; ANIMALS; ASPARTIC ACID; BIOLOGICAL TRANSPORT; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; FEMALE; HUMANS; MALE; MICE; MICROTUBULES; MITOCHONDRIA; MUTATION; PC12 CELLS; PHOSPHORYLATION; PROTEIN BINDING; RATS; TAU PROTEINS;

EID: 84857073309     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5927-11.2012     Document Type: Article

References (66)

1. Bereiter-Hahn J, Jendrach M (2010) Mitochondrial dynamics. Int Rev Cell Mol Biol 284:1-65.
2. Bershadsky AD, Gelfand VI, Svitkina TM, Tint IS (1978) Microtubules in mouse embryo fibroblasts extracted with Triton X-100. Cell Biol Int Rep 2:425-432.
3. 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.
4. Darios F, Muriel MP, Khondiker ME, Brice A, Ruberg M (2005) Neurotoxic calcium transfer from endoplasmic reticulum to mitochondria is regulated by cyclin-dependent kinase 5-dependent phosphorylation of tau. J Neurosci 25:4159-4168.
5. Dixit R, Ross JL, Goldman YE, Holzbaur EL (2008) Differential regulation of dynein and kinesin motor proteins by tau. Science 319:1086-1089.
6. Dubey M, Chaudhury P, Kabiru H, Shea TB (2008) Tau inhibits anterograde axonal transport and perturbs stability in growing axonal neurites in part by displacing kinesin cargo: neurofilaments attenuate taumediated neurite instability. Cell Motil Cytoskeleton 65:89-99.
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. Endo R, Saito T, Asada A, Kawahara H, Ohshima T, Hisanaga S (2009) Commitment of 1-methyl-4-phenylpyrinidinium ion-induced neuronal cell death by proteasome-mediated degradation of p35 cyclin-dependent kinase 5 activator. J Biol Chem 284:26029-26039.
9. Frappier TF, Georgieff IS, Brown K, Shelanski ML (1994) Tau Regulation of microtubule-microtubule spacing and bundling. J Neurochem 63:2288-2294.
10. Furuta K, Edamatsu M, Maeda Y, Toyoshima YY (2008) Diffusion and directed movement: in vitro motile properties of fission yeast kinesin-14 Pkl1. J Biol Chem 283:36465-36473.
11. Goedert M, Jakes R, Vanmechelen E (1995) Monoclonal antibody AT8 recognises tau protein phosphorylated at both serine 202 and threonine 205. Neurosci Lett 189:167-169.
12. 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.
13. Hanger DP, Anderton BH, Noble W (2009) Tau phosphorylation: the therapeutic challenge for neurodegenerative disease. Trends Mol Med 15:112-119.
14. Hisanaga S, Hirokawa N (1989) The effects of dephosphorylation on the structure of the projections of neurofilament. J Neurosci 9:959-966.
15. Hollenbeck PJ, Saxton WM (2005) The axonal transport of mitochondria. J Cell Sci 118:5411-5419.
16. Hosokawa T, Saito T, Asada A, Fukunaga K, Hisanaga S (2010) Quantitative measurement of in vivo phosphorylation states of Cdk5 activator p35 by Phos-tag SDS-PAGE. Mol Cell Proteomics 9:1133-1143.
17. Ishiguro K, Takamatsu M, Tomizawa K, Omori A, Takahashi M, Arioka M, Uchida T, Imahori K (1992) Tau protein kinase I converts normal tau protein into A68-like component of paired helical filaments. J Biol Chem 267:10897-10901.
18. Jeganathan S, von Bergen M, Brutlach H, Steinhoff HJ, Mandelkow E (2006) Global hairpin folding of tau in solution. Biochemistry 45:2283-2293.
19. Jeganathan S, Hascher A, Chinnathambi S, Biernat J, Mandelkow EM, Mandelkow E (2008) Proline-directed pseudo-phosphorylation at AT8 and PHF1 epitopes induces a compaction of the paperclip folding of tau and generates a pathological (MC-1) conformation. J Biol Chem 283:32066-32076.
20. Jicha GA, Bowser R, Kazam IG, Davies P (1997) Alz-50 and MC-1, a new monoclonal antibody raised to paired helical filaments, recognize conformational epitopes on recombinant tau. J Neurosci Res 48:128-132.
21. Jicha GA, Berenfeld B, Davies P (1999) Sequence requirements for formation of conformational variants of tau similar to those found in Alzheimer's disease. J Neurosci Res 55:713-723.
22. Kaminosono S, Saito T, Oyama F, Ohshima T, Asada A, Nagai Y, Nukina N, Hisanaga S (2008) Suppression of mutant Huntingtin aggregate formation by Cdk5/p35 through the effect on microtubule stability. J Neurosci 28:8747-8755.
23. Kanai Y, Takemura R, Oshima T, Mori H, Ihara Y, Yanagisawa 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.
24. Kanungo J, Zheng Y, Rudrabhatla P, Amin N, Mishra B, Pant H (2011) Deregulation of cytoskeletal protein phosphorylation and neurodegeneration. In: Advances in neurobiology: cytoskeleton of the nervous system (Nixon RA and Yuan A, eds), pp 297-324. New York: Springer.
25. Kimura T, Yamashita S, Fukuda T, Park JM, Murayama M, Mizoroki T, Yoshiike Y, Sahara N, Takashima A (2007) Hyperphosphorylated tau in parahippocampal cortex impairs place learning in aged mice expressing wild-type human tau. EMBO J 26:5143-5152.
26. Kinoshita E, Kinoshita-Kikuta E, Takiyama K, Koike T (2006) Phosphatebinding tag, a new tool to visualize phosphorylated proteins. Mol Cell Proteomics 5:749-757.
27. Knowles R, LeClerc N, Kosik KS (1994) Organization of actin and microtubules during process formation in tau-expressing Sf9 cells. Cell Motil Cytoskeleton 28:256-264.
28. Kumar S, Yin X, Trapp BD, Hoh JH, Paulaitis ME (2002) Relating interactions between neurofilaments to the structure of axonal neurofilament distributions through polymer brush models. Biophys J 82:2360-2372.
29. Lippens G, Sillen A, Landrieu I, Amniai L, Sibille N, Barbier P, Leroy A, Hanoulle X, Wieruszeski JM (2007) Tau aggregation in Alzheimer's disease: what role for phosphorylation? Prion 1:21-25.
30. Liu F, Li B, Tung EJ, Grundke-Iqbal I, Iqbal K, Gong CX (2007) Site-specific effects of tau phosphorylation on its microtubule assembly activity and self-aggregation. Eur J Neurosci 26:3429-3436.
31. 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.
32. Marx A, Pless J, Mandelkow EM, Mandelkow E (2000) On the rigidity of the cytoskeleton: are MAPs cross-linkers or spacers of microtubules? Cell Mol Biol 46:949-965.
33. Marx A, Müller J, Mandelkow EM, Hoenger A, Mandelkow E (2006) Interaction of kinesin motors, microtubules, and MAPs. J Muscle Res Cell Motil 27:125-137.
34. Morel, M, Authelet M, Dedecker R, Brion JP (2010) Glycogen synthase kinase-3 and the P25 activator of cyclin dependent kinase 5 increase pausing of mitochondria in neurons. Neuroscience 167:1044-1056.
35. Morishima-Kawashima M, Hasegawa M, Takio K, Suzuki M, Yoshida H, Titani K, Ihara Y (1995) Proline-directed and non-proline-directed phosphorylation of PHF-tau. J Biol Chem 270:823-829.
36. Mukhopadhyay R, Hoh JH (2001) AFM force measurements on microtubuleassociated proteins: the projection domain exerts a long-range repulsive force. FEBS Lett 505:374-378.
37. Planel E, Sun X, Takashima A (2002) Role of GSK-3β in Alzheimer's disease pathology. Drug Dev Res 56:491-510.
38. Plattner F, Angelo M, Giese KP (2006) The roles of cyclin-dependent kinase 5 and glycogen synthase kinase 3 in tau hyperphosphorylation. J Biol Chem 281:25457-25465.
39. Rankin CA, Sun Q, Gamblin TC (2005) Pseudo-phosphorylation of tau at Ser202 and Thr205 affects tau filament formation. Mol Brain Res 138:84-93.
40. Rochlin MW, Wickline KM, Bridgman PC (1996) Microtubule stability decreases axon elongation but not axoplasm production. J Neurosci 16:3236-3246.
41. Rudrabhatla P, Grant P, Jaffe H, Strong MJ, Pant HC (2010) Quantitative phosphoproteomic analysis of neuronal intermediate filament proteins (NF-M/H) in Alzheimer's disease by iTRAQ. FASEB J 24:4396-4407.
42. Saito T, Onuki R, Fujita Y, Kusakawa G, Ishiguro K, Bibb JA, Kishimoto T, Hisanaga S (2003) Developmental regulation of the proteolysis of the p35 cyclin-dependent kinase 5 activator by phosphorylation. J Neurosci 23:1189-1197.
43. Sakaue F, Saito T, Sato Y, Asada A, Ishiguro K, Hasegawa M, Hisanaga S (2005) Phosphorylation of FTDP-17 mutant tau by cyclin-dependent kinase 5 complexed with p35, p25, or p39. J Biol Chem 280:31522-31529.
44. Seeger MA, Rice SE (2010) Microtubule-associated protein-like binding of the kinesin-1 tail to microtubules. J Biol Chem 285:8155-8162.
45. Shahpasand K, Ahmadian S, Riazi GH (2008) A possible mechanism for controlling processive transport by microtubule-associated proteins. Neurosci Res 61:347-350.
46. Shemesh OA, Erez H, Ginzburg I, Spira ME (2008) Tau-induced traffic jams reflect organelles accumulation at points of microtubule polar mismatching. Traffic 9:458-471.
47. 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.
48. Stokin GB, Lillo C, Falzone TL, Brusch RG, Rockenstein E, Mount SL, Raman R, Davies P, Masliah E, Williams DS, Goldstein LS (2005) Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 307:1282-1288.
49. Stoothoff WH, Johnson GV (2005) Tau phosphorylation: physiological and pathological consequences. Biochim Biophys Acta 1739:280-297.
50. Stoothoff W, Jones PB, Spires-Jones TL, Joyner D, Chhabra E, Bercury K, Fan Z, Xie H, Bacskai B, Edd J, Irimia D, Hyman BT (2009) Differential effect of three-repeat and four-repeat tau on mitochondrial axonal transport. J Neurochem 111:417-427.
51. Su B, Wang X, Zheng L, Perry G, Smith MA, Zhu X (2010) Abnormal mitochondrial dynamics and neurodegenerative diseases. Biochim Biophys Acta 1802:135-142.
52. Sudo H, Baas PW (2010) Acetylation of microtubules influences their sensitivity to severing by katanin in neurons and fibroblasts. J Neurosci 30:7215-7226.
53. Takahashi S, Saito T, Hisanaga S, Pant HC, Kulkarni AB (2003) Tau phosphorylation by cyclin-dependent kinase 5/p39 during brain development reduces its affinity for microtubules. J Biol Chem 278:10506-10515.
54. Tatebayashi Y, Haque N, Tung YC, Iqbal K, Grundke-Iqbal I (2004) Role of tau phosphorylation by glycogen synthase kinase-3W in the regulation of organelle transport. J Cell Sci 117:1653-1663.
55. Thies E, Mandelkow EM (2007) Missorting of tau in neurons causes degeneration of synapses that can be rescued by MARK2/Par-1. J Neurosci 27:2896-2907.
56. Tokuoka H, Saito T, Yorifuji H, Wei F, Kishimoto T, Hisanaga S (2000) Brain-derived neurotrophic factor-induced phosphorylation of neurofilament- H subunit in primary cultures of embryo rat cortical neurons. J Cell Sci 113:1059-1068.
57. Trinczek B, Ebneth A, Mandelkow EM, Mandelkow E (1999) Tau regulates the attachment/detachment but not the speed of motors in microtubuledependent transport of single vesicles and organelles. J Cell Sci 112:2355-2367.
58. Uchida A, Tashiro T, Komiya Y, Yorifuji H, Kishimoto T, Hisanaga S (2004) Morphological and biochemical changes of neurofilaments in aged rat sciatic nerve axons. J Neurochem 88:735-745.
59. Vershinin M, Carter BC, Razafsky DS, King SJ, Gross SP (2007) Multiple motor based transport and its regulation by Tau. Proc Natl Acad SciU S A 104:87-92.
60. Vershinin M, Xu J, Razafsky DS, King SJ, Gross SP (2008) Tuning microtubule-based transport through flamentous MAPs: the problem of dynein. Traffic 9:882-892.
61. Verwer RW, Sluiter AA, Balesar RA, Baayen JC, Noske DP, Dirven CM, Wouda J, van Dam AM, Lucassen PJ, Swaab DF (2007) Mature astrocytes in the adult human neocortex express the early neuronal marker doublecortin. Brain 130:3321-3335.
62. Vossel KA, Zhang K, Brodbeck J, Daub AC, Sharma P, Finkbeiner S, Cui B, Mucke L (2010) Tau reduction prevents Abeta-induced defects in axonal transport. Science 330:198.
63. Wada Y, Ishiguro K, Itoh TJ, Uchida T, Hotani H, Saito T, Kishimoto T, Hisanaga S (1998) Microtubule-stimulated phosphorylation of tau at Ser202 and Thr205 by cdk5 decreases its microtubule nucleation activity. J Biochem 124:738-746.
64. Wang ZF, Li HL, Li XC, Zhang Q, Tian Q, Wang Q, Xu H, Wang JZ (2006) Effects of endogenous beta-amyloid overproduction on tau phosphorylation in cell culture. J Neurochem 98:1167-1175.
65. Watanabe A, Hasegawa M, Suzuki M, Takio K, Morishima-Kawashima M, Titani K, Arai T, Kosik KS, Ihara Y (1993) In vivo phosphorylation sites in fetal and adult rat tau. J Biol Chem 268:25712-25717.
66. Yu W, Baas PW (1994) Changes in microtubule number and lenghh during axon differentiation. J Neurosci 14:2818-2829.