Lost after translation: Missorting of Tau protein and consequences for Alzheimer disease

Trends in Neurosciences

Volumn 37, Issue 12, 2014, Pages 721-732

  Zempel, Hans ^a   Mandelkow, Eckhard ^a,b,c  

^a GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^b CENTER OF ADVANCED EUROPEAN STUDIES AND RESEARCH CAESAR   (Germany)

^c DESY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; PRION PROTEIN; SPASTIN; TAU PROTEIN;

ALZHEIMER DISEASE; CELLULAR DISTRIBUTION; CYTOSKELETON; DENDRITIC SPINE; GENE OVEREXPRESSION; HUMAN; MICROTUBULE; NERVE CELL; NERVE DEGENERATION; NONHUMAN; OLIGOMERIZATION; PATHOLOGY; PATHOPHYSIOLOGY; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; TAUOPATHY; WILD TYPE; ANIMAL; DISEASE MODEL; GENETICS; METABOLISM; NERVE FIBER;

ALZHEIMER DISEASE; ANIMALS; AXONS; CYTOSKELETON; DISEASE MODELS, ANIMAL; HUMANS; NEURONS; TAU PROTEINS;

EID: 84919466585     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2014.08.004     Document Type: Review

References (131)

1. Serrano-Pozo A., et al. Neuropathological alterations in Alzheimer disease. Cold Spring Harb. Perspect. Med. 2011, 1:a006189.
2. Braak H., Del Tredici K. Alzheimer's disease: intraneuronal alterations precede insoluble amyloid-beta formation. Neurobiol. Aging 2004, 25:713-718. 743-716 discussion.
3. Roberson E.D., et al. Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model. Science 2007, 316:750-754.
4. Ittner L.M., et al. Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 2010, 142:387-397.
5. Weingarten M.D., et al. A protein factor essential for microtubule assembly. Proc. Natl. Acad. Sci. U.S.A. 1975, 72:1858-1862.
6. Cleveland D.W., et al. Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly. J. Mol. Biol. 1977, 116:227-247.
7. Drubin D.G., Kirschner M.W. Tau protein function in living cells. J. Cell Biol. 1986, 103:2739-2746.
8. Binder L.I., et al. Differential localization of MAP-2 and tau in mammalian neurons in situ. Ann. N. Y. Acad. Sci. 1986, 466:145-166.
9. Neve R.L., et al. Identification of cDNA clones for the human microtubule-associated protein tau and chromosomal localization of the genes for tau and microtubule-associated protein 2. Brain Res. 1986, 387:271-280.
10. Goedert M., et al. Cloning and sequencing of the cDNA encoding an isoform of microtubule-associated protein tau containing four tandem repeats: differential expression of tau protein mRNAs in human brain. EMBO J. 1989, 8:393-399.
11. Andreadis A. Tau splicing and the intricacies of dementia. J. Cell. Physiol. 2012, 227:1220-1225.
12. Mukrasch M.D., et al. Structural polymorphism of 441-residue tau at single residue resolution. PLoS Biol. 2009, 7:e34.
13. Drubin D.G., et al. Studies on the expression of the microtubule-associated protein, tau, during mouse brain development, with newly isolated complementary DNA probes. J. Cell Biol. 1984, 98:1090-1097.
14. Bullmann T., et al. Pattern of tau isoforms expression during development in vivo. Int. J. Dev. Neurosci. 2009, 27:591-597.
15. Ferreira A., et al. Selective phosphorylation of adult tau isoforms in mature hippocampal neurons exposed to fibrillar A beta. Mol. Cell. Neurosci. 1997, 9:220-234.
16. Mandell J.W., Banker G.A. The microtubule cytoskeleton and the development of neuronal polarity. Neurobiol. Aging 1995, 16:229-237.
17. Hanger D.P., et al. Tau phosphorylation: the therapeutic challenge for neurodegenerative disease. Trends Mol. Med. 2009, 15:112-119.
18. Stieler J.T., et al. The physiological link between metabolic rate depression and tau phosphorylation in mammalian hibernation. PLoS ONE 2011, 6:e14530.
19. Arendt T., et al. Reversible paired helical filament-like phosphorylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals. J. Neurosci. 2003, 23:6972-6981.
20. Magarinos A.M., et al. Rapid and reversible changes in intrahippocampal connectivity during the course of hibernation in European hamsters. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:18775-18780.
21. Planel E., et al. Anesthesia leads to tau hyperphosphorylation through inhibition of phosphatase activity by hypothermia. J. Neurosci. 2007, 27:3090-3097.
22. Aronov S., et al. Axonal tau mRNA localization coincides with tau protein in living neuronal cells and depends on axonal targeting signal. J. Neurosci. 2001, 21:6577-6587.
23. Morita T., Sobue K. Specification of neuronal polarity regulated by local translation of CRMP2 and Tau via the mTOR-p70S6K pathway. J. Biol. Chem. 2009, 284:27734-27745.
24. Hirokawa N., et al. Selective stabilization of tau in axons and microtubule-associated protein 2C in cell bodies and dendrites contributes to polarized localization of cytoskeletal proteins in mature neurons. J. Cell Biol. 1996, 132:667-679.
25. Lee M.J., et al. Tau degradation: the ubiquitin-proteasome system versus the autophagy-lysosome system. Prog. Neurobiol. 2013, 105:49-59.
26. Wang Y., Mandelkow E. Degradation of tau protein by autophagy and proteasomal pathways. Biochem. Soc. Trans. 2012, 40:644-652.
27. Kosik K.S., Shimura H. Phosphorylated tau and the neurodegenerative foldopathies. Biochim. Biophys. Acta 2005, 1739:298-310.
28. Dickey C.A., et al. Deletion of the ubiquitin ligase CHIP leads to the accumulation, but not the aggregation, of both endogenous phospho- and caspase-3-cleaved tau species. J. Neurosci. 2006, 26:6985-6996.
29. Kanai Y., Hirokawa N. Sorting mechanisms of tau and MAP2 in neurons: suppressed axonal transit of MAP2 and locally regulated microtubule binding. Neuron 1995, 14:421-432.
30. Hoogenraad C.C., Bradke F. Control of neuronal polarity and plasticity - a renaissance for microtubules?. Trends Cell Biol. 2009, 19:669-676.
31. Schneider A., et al. Phosphorylation that detaches tau protein from microtubules (Ser262, Ser214) also protects it against aggregation into Alzheimer paired helical filaments. Biochemistry 1999, 38:3549-3558.
32. Li X., et al. Novel diffusion barrier for axonal retention of Tau in neurons and its failure in neurodegeneration. EMBO J. 2011, 30:4825-4837.
33. Rasband M.N. The axon initial segment and the maintenance of neuronal polarity. Nat. Rev. Neurosci. 2010, 11:552-562.
34. Konzack S., et al. Swimming against the tide: mobility of the microtubule-associated protein tau in neurons. J. Neurosci. 2007, 27:9916-9927.
35. Mercken M., et al. Three distinct axonal transport rates for tau, tubulin, and other microtubule-associated proteins: evidence for dynamic interactions of tau with microtubules in vivo. J. Neurosci. 1995, 15:8259-8267.
36. Utton M.A., et al. The slow axonal transport of the microtubule-associated protein tau and the transport rates of different isoforms and mutants in cultured neurons. J. Neurosci. 2002, 22:6394-6400.
37. Harada A., et al. Altered microtubule organization in small-calibre axons of mice lacking tau protein. Nature 1994, 369:488-491.
38. Takei Y., et al. Defects in axonal elongation and neuronal migration in mice with disrupted tau and map1b genes. J. Cell Biol. 2000, 150:989-1000.
39. Halpain S., Dehmelt L. The MAP1 family of microtubule-associated proteins. Genome Biol. 2006, 7:224.
40. Riederer B.M. Microtubule-associated protein 1B, a growth-associated and phosphorylated scaffold protein. Brain Res. Bull. 2007, 71:541-558.
41. Bosc C., et al. STOP proteins. Biochemistry 2003, 42:12125-12132.
42. Braak H., et al. Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol. 2006, 112:389-404.
43. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991, 82:239-259.
44. McKhann G.M., et al. Clinical and pathological diagnosis of frontotemporal dementia: report of the Work Group on Frontotemporal Dementia and Pick's Disease. Arch. Neurol. 2001, 58:1803-1809.
45. Wider C., Wszolek Z.K. Etiology and pathophysiology of frontotemporal dementia, Parkinson disease and Alzheimer disease: lessons from genetic studies. Neurodegener. Dis. 2008, 5:122-125.
46. van Swieten J., Spillantini M.G. Hereditary frontotemporal dementia caused by Tau gene mutations. Brain Pathol. 2007, 17:63-73.
47. Goedert M., et al. Frontotemporal dementia: implications for understanding Alzheimer disease. Cold Spring Harb. Perspect. Med. 2012, 2:a006254.
48. Dickson D.W., et al. Neuropathology of frontotemporal lobar degeneration-tau (FTLD-tau). J. Mol. Neurosci. 2011, 45:384-389.
49. Buee L., Delacourte A. Comparative biochemistry of tau in progressive supranuclear palsy, corticobasal degeneration, FTDP-17 and Pick's disease. Brain Pathol. 1999, 9:681-693.
50. Hogg M., et al. The L266V tau mutation is associated with frontotemporal dementia and Pick-like 3R and 4R tauopathy. Acta Neuropathol. 2003, 106:323-336.
51. Dickson D.W., et al. Office of Rare Diseases neuropathologic criteria for corticobasal degeneration. J. Neuropathol. Exp. Neurol. 2002, 61:935-946.
52. Richter-Landsberg C. The cytoskeleton in oligodendrocytes. Microtubule dynamics in health and disease. J. Mol. Neurosci. 2008, 35:55-63.
53. Belkadi A., LoPresti P. Truncated Tau with the Fyn-binding domain and without the microtubule-binding domain hinders the myelinating capacity of an oligodendrocyte cell line. J. Neurochem. 2008, 107:351-360.
54. Blennow K., et al. The neuropathology and neurobiology of traumatic brain injury. Neuron 2012, 76:886-899.
55. Magnoni S., et al. Tau elevations in the brain extracellular space correlate with reduced amyloid-beta levels and predict adverse clinical outcomes after severe traumatic brain injury. Brain 2012, 135:1268-1280.
56. Tran H.T., et al. Controlled cortical impact traumatic brain injury in 3×Tg-AD mice causes acute intra-axonal amyloid-beta accumulation and independently accelerates the development of tau abnormalities. J. Neurosci. 2011, 31:9513-9525.
57. Gotz J., et al. Somatodendritic localization and hyperphosphorylation of tau protein in transgenic mice expressing the longest human brain tau isoform. EMBO J. 1995, 14:1304-1313.
58. Kimura T., et al. Hyperphosphorylated tau in parahippocampal cortex impairs place learning in aged mice expressing wild-type human tau. EMBO J. 2007, 26:5143-5152.
59. Terwel D., et al. Changed conformation of mutant Tau-P301L underlies the moribund tauopathy, absent in progressive, nonlethal axonopathy of Tau-4R/2N transgenic mice. J. Biol. Chem. 2005, 280:3963-3973.
60. Gilley J., et al. Age-dependent axonal transport and locomotor changes and tau hypophosphorylation in a 'P301L' tau knockin mouse. Neurobiol. Aging 2012, 33:621.e1-621.e15. http://www.neurobiologyofaging.org/article/S0197-4580(11)00043-1/pdf.
61. Rosenmann H., et al. A novel transgenic mouse expressing double mutant tau driven by its natural promoter exhibits tauopathy characteristics. Exp. Neurol. 2008, 212:71-84.
62. Polydoro M., et al. Age-dependent impairment of cognitive and synaptic function in the htau mouse model of tau pathology. J. Neurosci. 2009, 29:10741-10749.
63. Adams S.J., et al. Overexpression of wild-type murine tau results in progressive tauopathy and neurodegeneration. Am. J. Pathol. 2009, 175:1598-1609.
64. LaFerla F.M., Green K.N. Animal models of Alzheimer disease. Cold Spring Harb. Perspect. Med. 2012, 2:a006320.
65. Thies E., Mandelkow E.M. Missorting of tau in neurons causes degeneration of synapses that can be rescued by the kinase MARK2/Par-1. J. Neurosci. 2007, 27:2896-2907.
66. Mandelkow E.M., et al. MARK/PAR1 kinase is a regulator of microtubule-dependent transport in axons. J. Cell Biol. 2004, 167:99-110.
67. Park S.Y., Ferreira A. The generation of a 17 kDa neurotoxic fragment: an alternative mechanism by which tau mediates beta-amyloid-induced neurodegeneration. J. Neurosci. 2005, 25:5365-5375.
68. Garg S., et al. Cleavage of Tau by calpain in Alzheimer's disease: the quest for the toxic 17kD fragment. Neurobiol. Aging 2011, 32:1-14.
69. Khlistunova I., et al. Inducible expression of Tau repeat domain in cell models of tauopathy: aggregation is toxic to cells but can be reversed by inhibitor drugs. J. Biol. Chem. 2006, 281:1205-1214.
70. Sydow A., et al. Tau-induced defects in synaptic plasticity, learning, and memory are reversible in transgenic mice after switching off the toxic Tau mutant. J. Neurosci. 2011, 31:2511-2525.
71. King M.E., et al. Tau-dependent microtubule disassembly initiated by prefibrillar beta-amyloid. J. Cell Biol. 2006, 175:541-546.
72. Weissmann C., et al. Microtubule binding and trapping at the tip of neurites regulate tau motion in living neurons. Traffic 2009, 10:1655-1668.
73. Hoover B.R., et al. Tau mislocalization to dendritic spines mediates synaptic dysfunction independently of neurodegeneration. Neuron 2010, 68:1067-1081.
74. 2+ elevation, missorting of endogenous Tau into dendrites, Tau phosphorylation, and destruction of microtubules and spines. J. Neurosci. 2010, 30:11938-11950.
75. Roberson E.D., et al. Amyloid-β/Fyn-induced synaptic, network, and cognitive impairments depend on tau levels in multiple mouse models of Alzheimer's disease. J. Neurosci. 2011, 31:700-711.
76. Kremer A., et al. Early improved and late defective cognition is reflected by dendritic spines in Tau.P301L mice. J. Neurosci. 2011, 31:18036-18047.
77. Zempel H., et al. Amyloid-beta oligomers induce synaptic damage via Tau-dependent microtubule severing by TTLL6 and spastin. EMBO J. 2013, 32:2920-2937.
78. Sarasa M., Pesini P. Natural non-transgenic animal models for research in Alzheimer's disease. Curr. Alzheimer Res. 2009, 6:171-178.
79. Mattson M.P. Degenerative and protective signaling mechanisms in the neurofibrillary pathology of AD. Neurobiol. Aging 1995, 16:447-457.
80. Busciglio J., et al. Beta-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 1995, 14:879-888.
81. Carroll J.C., et al. Chronic stress exacerbates tau pathology, neurodegeneration, and cognitive performance through a corticotropin-releasing factor receptor-dependent mechanism in a transgenic mouse model of tauopathy. J. Neurosci. 2011, 31:14436-14449.
82. Higuchi M., et al. Axonal degeneration induced by targeted expression of mutant human tau in oligodendrocytes of transgenic mice that model glial tauopathies. J. Neurosci. 2005, 25:9434-9443.
83. Forman M.S., et al. Transgenic mouse model of tau pathology in astrocytes leading to nervous system degeneration. J. Neurosci. 2005, 25:3539-3550.
84. Yoshiyama Y., et al. Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 2007, 53:337-351.
85. Yamada K., et al. In vivo microdialysis reveals age-dependent decrease of brain interstitial fluid tau levels in P301S human tau transgenic mice. J. Neurosci. 2011, 31:13110-13117.
86. Gorlovoy P., et al. Accumulation of tau induced in neurites by microglial proinflammatory mediators. FASEB J. 2009, 23:2502-2513.
87. Brundin P., et al. Research in motion: the enigma of Parkinson's disease pathology spread. Nat. Rev. Neurosci. 2008, 9:741-745.
88. Clavaguera F., et al. Transmission and spreading of tauopathy in transgenic mouse brain. Nat. Cell Biol. 2009, 11:909-913.
89. Frost B., Diamond M.I. Prion-like mechanisms in neurodegenerative diseases. Nat. Rev. Neurosci. 2010, 11:155-159.
90. Braak H., Del Tredici K. Alzheimer's pathogenesis: is there neuron-to-neuron propagation?. Acta Neuropathol. 2011, 121:589-595.
91. de Calignon A., et al. Propagation of tau pathology in a model of early Alzheimer's disease. Neuron 2012, 73:685-697.
92. Liu L., et al. Trans-synaptic spread of tau pathology in vivo. PLoS ONE 2012, 7:e31302.
93. Pooler A.M., et al. Physiological release of endogenous tau is stimulated by neuronal activity. EMBO Rep. 2013, 14:389-394.
94. Bateman R.J., et al. Clinical and biomarker changes in dominantly inherited Alzheimer's disease. N. Engl. J. Med. 2012, 367:795-804.
95. Yanamandra K., et al. Anti-Tau antibodies that block Tau aggregate seeding in vitro markedly decrease pathology and improve cognition in vivo. Neuron 2013, 80:402-414.
96. Bi M., et al. Tau-targeted immunization impedes progression of neurofibrillary histopathology in aged P301L Tau transgenic mice. PLoS ONE 2011, 6:e26860.
97. Walls K.C., et al. p-Tau immunotherapy reduces soluble and insoluble tau in aged 3×Tg-AD mice. Neurosci. Lett. 2014, 575C:96-100.
98. Kishi M., et al. Mammalian SAD kinases are required for neuronal polarization. Science 2005, 307:929-932.
99. Kaech S., Banker G. Culturing hippocampal neurons. Nat. Protoc. 2006, 1:2406-2415.
100. Qian W., et al. PP2A regulates tau phosphorylation directly and also indirectly via activating GSK-3beta. J. Alzheimers Dis. 2010, 19:1221-1229.
101. Martin L., et al. Tau protein phosphatases in Alzheimer's disease: the leading role of PP2A. Ageing Res. Rev. 2013, 12:39-49.
102. Zhu L.Q., et al. Protein phosphatase 2A facilitates axonogenesis by dephosphorylating CRMP2. J. Neurosci. 2010, 30:3839-3848.
103. Hayashi K., et al. Maintenance of dendritic spine morphology by partitioning-defective 1b through regulation of microtubule growth. J. Neurosci. 2011, 31:12094-12103.
104. Matenia D., Mandelkow E.M. The tau of MARK: a polarized view of the cytoskeleton. Trends Biochem. Sci. 2009, 34:332-342.
105. Timm T., et al. Microtubule affinity regulating kinase activity in living neurons was examined by a genetically encoded fluorescence resonance energy transfer/fluorescence lifetime imaging-based biosensor: inhibitors with therapeutic potential. J. Biol. Chem. 2011, 286:41711-41722.
106. Whiteman I.T., et al. Rapid changes in phospho-MAP/tau epitopes during neuronal stress: cofilin-actin rods primarily recruit microtubule binding domain epitopes. PLoS ONE 2011, 6:e20878.
107. Dawson H.N., et al. Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J. Cell Sci. 2001, 114:1179-1187.
108. Zhang B., et al. The microtubule-stabilizing agent, epothilone D, reduces axonal dysfunction, neurotoxicity, cognitive deficits, and Alzheimer-like pathology in an interventional study with aged tau transgenic mice. J. Neurosci. 2012, 32:3601-3611.
109. Cash A.D., et al. Microtubule reduction in Alzheimer's disease and aging is independent of tau filament formation. Am. J. Pathol. 2003, 162:1623-1627.
110. Lacroix B., et al. Tubulin polyglutamylation stimulates spastin-mediated microtubule severing. J. Cell Biol. 2010, 189:945-954.
111. Van der Jeugd A., et al. Cognitive defects are reversible in inducible mice expressing pro-aggregant full-length human Tau. Acta Neuropathol. 2012, 123:787-805.
112. Gotz J., Ittner L.M. Animal models of Alzheimer's disease and frontotemporal dementia. Nat. Rev. Neurosci. 2008, 9:532-544.
113. Santacruz K., et al. Tau suppression in a neurodegenerative mouse model improves memory function. Science 2005, 309:476-481.
114. Kuchibhotla K.V., et al. Neurofibrillary tangle-bearing neurons are functionally integrated in cortical circuits in vivo. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:510-514.
115. Oddo S., et al. Reduction of soluble Abeta and tau, but not soluble Abeta alone, ameliorates cognitive decline in transgenic mice with plaques and tangles. J. Biol. Chem. 2006, 281:39413-39423.
116. Nishimura I., et al. PAR-1 kinase plays an initiator role in a temporally ordered phosphorylation process that confers tau toxicity in Drosophila. Cell 2004, 116:671-682.
117. Sofola O., et al. Inhibition of GSK-3 ameliorates Abeta pathology in an adult-onset Drosophila model of Alzheimer's disease. PLoS Genet. 2010, 6:e1001087.
118. Morris M., et al. The many faces of tau. Neuron 2011, 70:410-426.
119. Ikegami S., et al. Muscle weakness, hyperactivity, and impairment in fear conditioning in tau-deficient mice. Neurosci. Lett. 2000, 279:129-132.
120. Dawson H.N., et al. Loss of tau elicits axonal degeneration in a mouse model of Alzheimer's disease. Neuroscience 2010, 169:516-531.
121. Lei P., et al. Tau deficiency induces parkinsonism with dementia by impairing APP-mediated iron export. Nat. Med. 2012, 18:291-295.
122. Sudo H., Baas P.W. Strategies for diminishing katanin-based loss of microtubules in tauopathic neurodegenerative diseases. Hum. Mol. Genet. 2010, 20:763-778.
123. Sultan A., et al. Nuclear tau, a key player in neuronal DNA protection. J. Biol. Chem. 2011, 286:4566-4575.
124. Janke C., Kneussel M. Tubulin post-translational modifications: encoding functions on the neuronal microtubule cytoskeleton. Trends Neurosci. 2010, 33:362-372.
125. Walker L.C., et al. Mechanisms of protein seeding in neurodegenerative diseases. JAMA Neurol. 2013, 70:304-310.
126. Mandelkow E.M., Mandelkow E. Biochemistry and cell biology of tau protein in neurofibrillary degeneration. Cold Spring Harb. Perspect. Med. 2012, 2:a006247.
127. Niblock M., Gallo J.M. Tau alternative splicing in familial and sporadic tauopathies. Biochem. Soc. Trans. 2012, 40:677-680.
128. Hutton M., et al. Association of missense and 5'-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 1998, 393:702-705.
129. Orozco D., et al. Loss of fused in sarcoma (FUS) promotes pathological Tau splicing. EMBO Rep. 2012, 13:759-764.
130. Liu C., Gotz J. Profiling murine Tau with 0N, 1N and 2N isoform-specific antibodies in brain and peripheral organs reveals distinct subcellular localization, with the 1N isoform being enriched in the nucleus. PLoS ONE 2013, 8:e84849.
131. Lasagna-Reeves C.A., et al. Alzheimer brain-derived tau oligomers propagate pathology from endogenous tau. Sci. Rep. 2012, 2:700.