Selective clearance of aberrant tau proteins and rescue of neurotoxicity by transcription factor EB

EMBO Molecular Medicine

Volumn 6, Issue 9, 2014, Pages 1142-1160

  Polito, Vinicia A ^a   Li, Hongmei ^a   Martini Stoica, Heidi ^a   Wang, Baiping ^a   Yang, Li ^a   Xu, Yin ^a   Swartzlander, Daniel B ^a   Palmieri, Michela ^a,b   Di Ronza, Alberto ^a,b   Lee, Virginia M Y ^c   Sardiello, Marco ^a,b   Ballabio, Andrea ^a,b,d   Zheng, Hui ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b TEXAS CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Alzheimer's disease; Autophagy lysosomal pathway; PTEN; Tauopathy; TFEB

Indexed keywords

AMYLOID BETA PROTEIN; PARVOVIRUS VECTOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; TAU PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EB; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; MAPT PROTEIN, MOUSE; PTEN PROTEIN, MOUSE; TCFEB PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; DRUG TARGETING; HUMAN; HUMAN CELL; IN VIVO GENE TRANSFER; MOUSE; NERVE CELL PLASTICITY; NERVE DEGENERATION; NEUROFIBRILLARY TANGLE; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN PHOSPHORYLATION; SYNAPTIC TRANSMISSION; TAUOPATHY; ALZHEIMER DISEASE; ANIMAL; C57BL MOUSE; GENE EXPRESSION REGULATION; GENETICS; LYSOSOME; METABOLISM; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; ANIMALS; AUTOPHAGY; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; LYSOSOMES; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE DEGENERATION; NEUROFIBRILLARY TANGLES; PTEN PHOSPHOHYDROLASE; TAU PROTEINS; TAUOPATHIES;

EID: 84916928995     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201303671     Document Type: Article

References (61)

1. Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Holko M et al (2013) NCBI GEO: archive for functional genomics data sets-update. Nucleic Acids Res 41: D991-D995
2. Brunden KR, Trojanowski JQ, Lee VM (2009) Advances in tau-focused drug discovery for Alzheimer's disease and related tauopathies. Nat Rev Drug Discov 8: 783-793
3. Caccamo A, Magri A, Medina DX, Wisely EV, Lopez-Aranda MF, Silva AJ, Oddo S (2013) mTor regulates tau phosphorylation and degradation: implications for alzheimer's disease and other tauopathies. Aging Cell 12: 370-380
4. Cruz-Orive LM (1999) Precision of Cavalieri sections and slices with local errors. J Microsc 193: 182-198
5. Cuervo AM (2011) Cell biology. Autophagy's top chef. Science 332: 1392-1393
6. Decressac M, Mattsson B, Weikop P, Lundblad M, Jakobsson J, Bjorklund A (2013) TFEB-mediated autophagy rescues midbrain dopamine neurons from alpha-synuclein toxicity. Proc Natl Acad Sci USA 110: E1817-E1826
7. Dickey CA, Kamal A, Lundgren K, Klosak N, Bailey RM, Dunmore J, Ash P, Shoraka S, Zlatkovic J, Eckman CB et al (2007) The high-affinity HSP90-CHIP complex recognizes and selectively degrades phosphorylated tau client proteins. J Clin Investig 117: 648-658
8. Dickey CA, Koren J, Zhang YJ, Xu YF, Jinwal UK, Birnbaum MJ, Monks B, Sun M, Cheng JQ, Patterson C et al (2008) Akt and CHIP coregulate tau degradation through coordinated interactions. Proc Natl Acad Sci USA 105: 3622-3627
9. Franklin KBJ, Paxinos G (2001) The Mouse Brain in Stereotaxic Coordinates, 2nd edn. San Diego: Academic Press
10. Gendron TF, Petrucelli L (2009) The role of tau in neurodegeneration. Mol Neurodegener 4: 13
11. Giannakopoulos P, Herrmann FR, Bussiere T, Bouras C, Kovari E, Perl DP, Morrison JH, Gold G, Hof PR (2003) Tangle and neuron numbers, but not amyloid load, predict cognitive status in Alzheimer's disease. Neurology 60: 1495-1500
12. Haq R, Fisher DE (2011) Biology and clinical relevance of the micropthalmia family of transcription factors in human cancer. J Clin Oncol 29: 3474-3482
13. Hardy J (2006) A hundred years of Alzheimer's disease research. Neuron 52: 3-13
14. Harris H, Rubinsztein DC (2012) Control of autophagy as a therapy for neurodegenerative disease. Nat Rev Neurol 8: 108-117
15. da Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57
16. Inoue K, Rispoli J, Kaphzan H, Klann E, Chen EI, Kim J, Komatsu M, Abeliovich A (2012) Macroautophagy deficiency mediates age-dependent neurodegeneration through a phospho-tau pathway. Mol Neurodegener 7: 48
17. Kerr F, Rickle A, Nayeem N, Brandner S, Cowburn RF, Lovestone S (2006) PTEN, a negative regulator of PI3 kinase signalling, alters tau phosphorylation in cells by mechanisms independent of GSK-3. FEBS Lett 580: 3121-3128
18. Kimura S, Noda T, Yoshimori T (2007) Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3: 452-460
19. Kopeikina KJ, Hyman BT, Spires-Jones TL (2012) Soluble forms of tau are toxic in Alzheimer's disease. Transl Neurosci 3: 223-233
20. Kruger U, Wang Y, Kumar S, Mandelkow EM (2012) Autophagic degradation of tau in primary neurons and its enhancement by trehalose. Neurobiol Aging 33: 2291-2305
21. Kwon CH, Luikart BW, Powell CM, Zhou J, Matheny SA, Zhang W, Li Y, Baker SJ, Parada LF (2006) Pten regulates neuronal arborization and social interaction in mice. Neuron 50: 377-388
22. Kwon CH, Zhu X, Zhang J, Baker SJ (2003) mTor is required for hypertrophy of Pten-deficient neuronal soma in vivo. Proc Natl Acad Sci USA 100: 12923-12928
23. Kwon CH, Zhu X, Zhang J, Knoop LL, Tharp R, Smeyne RJ, Eberhart CG, Burger PC, Baker SJ (2001) Pten regulates neuronal soma size: a mouse model of Lhermitte-Duclos disease. Nat Genet 29: 404-411
24. Lin WL, Lewis J, Yen SH, Hutton M, Dickson DW (2003) Ultrastructural neuronal pathology in transgenic mice expressing mutant (P301L) human tau. J Neurocytol 32: 1091-1105
25. Lopes CT, Franz M, Kazi F, Donaldson SL, Morris Q, Bader GD (2010) Cytoscape Web: an interactive web-based network browser. Bioinformatics 26: 2347-2348
26. Mandelkow EM, Mandelkow E (2012) Biochemistry and cell biology of tau protein in neurofibrillary degeneration. Cold Spring Harb Perspect Med 2: a006247
27. Medina DL, Fraldi A, Bouche V, Annunziata F, Mansueto G, Spampanato C, Puri C, Pignata A, Martina JA, Sardiello M et al (2011) Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev Cell 21: 421-430
28. Mueller-Steiner S, Zhou Y, Arai H, Roberson ED, Sun B, Chen J, Wang X, Yu G, Esposito L, Mucke L et al (2006) Antiamyloidogenic and neuroprotective functions of cathepsin B: implications for Alzheimer's disease. Neuron 51: 703-714
29. Mullard A (2012) Sting of Alzheimer's failures offset by upcoming prevention trials. Nat Rev Drug Discov 11: 657-660
30. Nixon RA (2007) Autophagy, amyloidogenesis and Alzheimer disease. J Cell Sci 120: 4081-4091
31. Nixon RA, Wegiel J, Kumar A, Yu WH, Peterhoff C, Cataldo A, Cuervo AM (2005) Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J Neuropathol Exp Neurol 64: 113-122
32. Nixon RA, Yang DS (2011) Autophagy failure in Alzheimer's disease-locating the primary defect. Neurobiol Dis 43: 38-45
33. Oakley H, Cole SL, Logan S, Maus E, Shao P, Craft J, Guillozet-Bongaarts A, Ohno M, Disterhoft J, Van Eldik L et al (2006) Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J Neurosci 26: 10129-10140
34. Ozcelik S, Fraser G, Castets P, Schaeffer V, Skachokova Z, Breu K, Clavaguera F, Sinnreich M, Kappos L, Goedert M et al (2013) Rapamycin Attenuates the Progression of Tau Pathology in P301S Tau Transgenic Mice. PLoS ONE 8: e62459
35. Palmieri M, Impey S, Kang H, di Ronza A, Pelz C, Sardiello M, Ballabio A (2011) Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways. Hum Mol Genet 20: 3852-3866
36. Peethumnongsin E, Yang L, Kallhoff-Munoz V, Hu L, Takashima A, Pautler RG, Zheng H (2010) Convergence of presenilin- and tau-mediated pathways on axonal trafficking and neuronal function. J Neurosci 30: 13409-13418
37. Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, Small S, Spencer B, Rockenstein E, Levine B et al (2008) The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Invest 118: 2190-2199
38. Ramsden M, Kotilinek L, Forster C, Paulson J, McGowan E, SantaCruz K, Guimaraes A, Yue M, Lewis J, Carlson G et al (2005) Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J Neurosci 25: 10637-10647
39. Roczniak-Ferguson A, Petit CS, Froehlich F, Qian S, Ky J, Angarola B, Walther TC, Ferguson SM (2012) The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci Signal 5: ra42
40. Rohn TT, Wirawan E, Brown RJ, Harris JR, Masliah E, Vandenabeele P (2011) Depletion of Beclin-1 due to proteolytic cleavage by caspases in the Alzheimer's disease brain. Neurobiol Dis 43: 68-78
41. Santacruz K, Lewis J, Spires T, Paulson J, Kotilinek L, Ingelsson M, Guimaraes A, DeTure M, Ramsden M, McGowan E et al (2005) Tau suppression in a neurodegenerative mouse model improves memory function. Science 309: 476-481
42. Sardiello M, Palmieri M, di Ronza A, Medina DL, Valenza M, Gennarino VA, Di Malta C, Donaudy F, Embrione V, Polishchuk RS et al (2009) A gene network regulating lysosomal biogenesis and function. Science 325: 473-477
43. Schaeffer V, Lavenir I, Ozcelik S, Tolnay M, Winkler DT, Goedert M (2012) Stimulation of autophagy reduces neurodegeneration in a mouse model of human tauopathy. Brain 135: 2169-2177
44. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676-682
45. Settembre C, Di Malta C, Polito VA, Garcia Arencibia M, Vetrini F, Erdin S, Erdin SU, Huynh T, Medina D, Colella P et al (2011) TFEB links autophagy to lysosomal biogenesis. Science 332: 1429-1433
46. Settembre C, Zoncu R, Medina DL, Vetrini F, Erdin S, Huynh T, Ferron M, Karsenty G, Vellard MC, Facchinetti V et al (2012) A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J 31: 1095-1108
47. Song MS, Salmena L, Pandolfi PP (2012) The functions and regulation of the PTEN tumour suppressor. Nat Rev Mol Cell Biol 13: 283-296
48. Song W, Wang F, Savini M, Ake A, di Ronza A, Sardiello M, Segatori L (2013) TFEB regulates lysosomal proteostasis. Hum Mol Genet 22: 1994-2009
49. Sperow M, Berry RB, Bayazitov IT, Zhu G, Baker SJ, Zakharenko SS (2011) Phosphatase and tensin homologue (PTEN) regulates synaptic plasticity independently of its effect on neuronal morphology and migration. J Physiol 590: 777-792
50. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES et al (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102: 15545-15550
51. Takeuchi K, Gertner MJ, Zhou J, Parada LF, Bennett MV, Zukin RS (2013) Dysregulation of synaptic plasticity precedes appearance of morphological defects in a Pten conditional knockout mouse model of autism. Proc Natl Acad Sci USA 110: 4738-4743
52. Teresi RE, Planchon SM, Waite KA, Eng C (2008) Regulation of the PTEN promoter by statins and SREBP. Hum Mol Genet 17: 919-928
53. The Gene Ontology Consortium (2012) Gene Ontology annotations and resources. Nucleic Acids Res 41: D530-D535
54. Wang X, Trotman LC, Koppie T, Alimonti A, Chen Z, Gao Z, Wang J, Erdjument-Bromage H, Tempst P, Cordon-Cardo C et al (2007) NEDD4-1 is a proto-oncogenic ubiquitin ligase for PTEN. Cell 128: 129-139
55. Wang Y, Martinez-Vicente M, Kruger U, Kaushik S, Wong E, Mandelkow EM, Cuervo AM, Mandelkow E (2009) Tau fragmentation, aggregation and clearance: the dual role of lysosomal processing. Hum Mol Genet 18: 4153-4170
56. Wang Y, Martinez-Vicente M, Kruger U, Kaushik S, Wong E, Mandelkow EM, Cuervo AM, Mandelkow E (2010) Synergy and antagonism of macroautophagy and chaperone-mediated autophagy in a cell model of pathological tau aggregation. Autophagy 6: 182-183
57. West MJ, Gundersen HJ (1990) Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 296: 1-22
58. Yang DS, Stavrides P, Mohan PS, Kaushik S, Kumar A, Ohno M, Schmidt SD, Wesson D, Bandyopadhyay U, Jiang Y et al (2011) Reversal of autophagy dysfunction in the TgCRND8 mouse model of Alzheimer's disease ameliorates amyloid pathologies and memory deficits. Brain 134: 258-277
59. Zhang X, Li F, Bulloj A, Zhang YW, Tong G, Zhang Z, Liao FF, Xu H (2006a) Tumor-suppressor PTEN affects tau phosphorylation, aggregation, and binding to microtubules. FASEB J 20: 1272-1274
60. Zhang X, Zhang YW, Liu S, Bulloj A, Tong GG, Zhang Z, Liao FF, Xu H (2006b) Tumor suppressor PTEN affects tau phosphorylation: deficiency in the phosphatase activity of PTEN increases aggregation of an FTDP-17 mutant Tau. Mol Neurodegener 1: 7
61. Zhou J, Blundell J, Ogawa S, Kwon CH, Zhang W, Sinton C, Powell CM, Parada LF (2009) Pharmacological inhibition of mTORC1 suppresses anatomical, cellular, and behavioral abnormalities in neural-specific Pten knock-out mice. J Neurosci 29: 1773-1783