Tauopathies with parkinsonism: Clinical spectrum, neuropathologic basis, biological markers, and treatment options

European Journal of Neurology

Volumn 16, Issue 3, 2009, Pages 297-309

  Ludolph, A C ^a   Kassubek, J ^a   Landwehrmeyer, B G ^a   Mandelkow, E ^b   Mandelkow, E M ^b   Burn, D J ^c   Caparros Lefebvre, D ^d   Frey, K A ^e   De Yebenes, J G ^f   Gasser, T ^g   Heutink, P ^h   Hoglinger G ⁱ   Jamrozik, Z ^j   Jellinger, K A ^k   Kazantsev, A ^l   Kretzschmar, H ^m   Lang, A E ⁿ   Litvan, I ^o   Lucas, J J ^p   McGeer, P L ^q   Melquist, S ^r   Oertel, W ⁱ   Otto, M ^a   Paviour, D ^s   Reum, T ^t   Saint Raymond, A ^u   Steele, J C ^v   Tolnay, M ^w   Tumani, H ^a   Van Swieten, J C ^x   Vanier, M T ^y   Vonsattel, J P ^z   Wagner, S ^aa   Wszolek, Z K ^ab   more..

^a UNIVERSITY OF ULM   (Germany)

^b MAX PLANCK UNIT FOR STRUCTURAL MOLECULAR BIOLOGY   (Germany)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d CENTRE HOSPITALIER DE VALENCIENNES   (France)

^e UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^f HOSPITAL RAMÓN Y CAJAL   (Spain)

^g UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^h VU UNIVERSITY MEDICAL CENTER   (Netherlands)

ⁱ PHILIPPS UNIVERSITY MARBURG   (Germany)

^j MEDICAL UNIVERSITY OF WARSAW   (Poland)

^k INSTITUTE OF CLINICAL NEUROBIOLOGY   (Austria)

^l MASSACHUSETTS GENERAL HOSPITAL   (United States)

^m Institut für Neuropathologie   (Germany)

ⁿ TORONTO WESTERN HOSPITAL   (Canada)

^o University of Louisville School of Medicine   (United States)

^p CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^q UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^r MAYO GRADUATE SCHOOL   (United States)

^s NATIONAL HOSPITAL FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

^t Wissenschaftlicher Service Klinische Prüfungen   (Germany)

^u EUROPEAN MEDICINES AGENCY   (United Kingdom)

^v Guam Memorial Hospital   (Guam)

^w UNIVERSITY HOSPITAL BASEL   (Switzerland)

^x ERASMUS MEDICAL CENTER   (Netherlands)

^y INSERM   (France)

^z Och Spine at New York Presbyterian Hospitals   (United States)

^aa C/o S Wagner   (Germany)

^ab MAYO CLINIC   (United States)

more..

Author keywords

Corticobasal degeneration; Frontotemporal dementia with parkinsonism linked to chromosome 17; Microtubule associated protein tau; Multiple system atrophy; Parkinson disease; Parkinsonism; Progressive supranuclear palsy; Tauopathies

Indexed keywords

ANTHRAQUINONE DERIVATIVE; BENZOTHIAZOLE DERIVATIVE; BIOLOGICAL MARKER; LITHIUM; PHENOTHIAZINE DERIVATIVE; POLYPHENOL DERIVATIVE; TAU PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; CHROMOSOME 17; CLINICAL FEATURE; CORTICOBASAL DEGENERATION; DIFFERENTIAL DIAGNOSIS; DRUG MECHANISM; FRONTOTEMPORAL DEMENTIA; GENETICS; HISTORY; HUMAN; NEUROIMAGING; NEUROPATHOLOGY; NIEMANN PICK DISEASE; NONHUMAN; PARKINSONISM; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; PROTEOMICS; RATING SCALE; REVIEW; TARGET CELL; TAUOPATHY; TREATMENT PLANNING;

ANIMALS; BIOLOGICAL MARKERS; DEMENTIA; DRUG DESIGN; GEOGRAPHY; HUMANS; MODELS, BIOLOGICAL; MUTATION; NIEMANN-PICK DISEASE, TYPE C; PARKINSON DISEASE, POSTENCEPHALITIC; PARKINSONIAN DISORDERS; PICK DISEASE OF THE BRAIN; PROTEIN-SERINE-THREONINE KINASES; SUPRANUCLEAR PALSY, PROGRESSIVE; TAU PROTEINS; TAUOPATHIES;

EID: 60049091402     PISSN: 13515101     EISSN: 14681331     Source Type: Journal    
DOI: 10.1111/j.1468-1331.2008.02513.x     Document Type: Review

References (84)

1. Litvan I, Agid Y, Calne D, et al. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 1996 47 : 1 9.
2. Santacruz P, Uttl B, Litvan I, Grafman J. Progressive supranuclear palsy: a survey of the disease course. Neurology 1998 50 : 1637 1647.
3. Lopez OL, Litvan I, Catt KE, et al. Accuracy of four clinical diagnostic criteria for the diagnosis of neurodegenerative dementias. Neurology 1999 53 : 1292 1299.
4. Nath U, Ben-Shlomo Y, Thomson RG, Lees AJ, Burn DJ. Clinical features and natural history of progressive supranuclear palsy: a clinical cohort study. Neurology 2003 60 : 910 916.
5. Williams DR, de Silva R, Paviour DC, et al. Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson's syndrome and PSP-parkinsonism. Brain 2005 128 (Pt 6 1247 1258.
6. Steele JC, Richardson JC, Olszewski J. Progressive supranuclear palsy: a heterogeneous degeneration involving the brain stem, basal ganglia and cerebellum with vertical gaze and pseudobulbar palsy, nuchal dystonia and dementia. Archives of Neurology 1964 10 : 333 359.
7. Litvan I, Hauw JJ, Bartko JJ, et al. Validity and reliability of the preliminary NINDS neuropathologic criteria for progressive supranuclear palsy and related disorders. Journal of Neuropathology and Experimental Neurology 1996 55 : 97 105.
8. Boeve BF, Lang AE, Litvan I. Corticobasal degeneration and its relationship to progressive supranuclear palsy and frontotemporal dementia. Annals of Neurology 2003 54 (Suppl 5 S15 S19.
9. van Swieten J, Spillantini MG. Hereditary frontotemporal dementia caused by Tau gene mutations. Brain Pathology 2007 17 : 63 73.
10. Baker M, Mackenzie IR, Pickering-Brown SM, et al. Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 2006 442 : 916 919.
11. Vanier MT, Millat G. Niemann-Pick disease type C. Clinical Genetics 2003 64 : 269 281.
12. Steele JC. Parkinsonism-dementia complex of Guam. Movement Disorders 2005 20 (Suppl 12 S99 S107.
13. Caparros-Lefebvre D, Steele J, Kotake Y, Ohta S. Geographic isolates of atypical Parkinsonism and tauopathy in the tropics: possible synergy of neurotoxins. Movement Disorders 2006 21 : 1769 1771.
14. Steele JC, McGeer PL. The ALS/PDC syndrome of Guam and the cycad hypothesis. Neurology 2008 70 : 1984 1990.
15. Caparros-Lefebvre D, Elbaz A, Caribbean Parkinsonism Study Group. Possible relation of atypical parkinsonism in the French West Indies with consumption of tropical plants: a case-control study. Lancet 1999 354 : 281 286.
16. Caparros-Lefebvre D, Sergeant N, Lees A, et al. Guadeloupean parkinsonism: a cluster of progressive supranuclear palsy-like tauopathy. Brain 2002 125 (Pt 4 801 811.
17. Lannuzel A, Hoglinger GU, Verhaeghe S, et al. Atypical parkinsonism in Guadeloupe: a common risk factor for two closely related phenotypes? Brain 2007 130 (Pt 3 816 827.
18. Escobar-Khondiker M, Hollerhage M, Muriel MP, et al. Annonacin, a natural mitochondrial complex I inhibitor, causes tau pathology in cultured neurons. Journal of Neuroscience 2007 27 : 7827 7837.
19. Hutton M, Lendon CL, Rizzu P, et al. Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 1998 393 : 702 705.
20. Spillantini MG, Murrell JR, Goedert M, Farlow MR, Klug A, Ghetti B. Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proceedings of the National Academy of Sciences of the United States of America 1998 95 : 7737 7741.
21. de Yebenes JG, Sarasa JL, Daniel SE, Lees AJ. Familial progressive supranuclear palsy: description of a pedigree and review of the literature. Brain 1995 118 (Pt 5 1095 1103.
22. Wszolek ZK, Pfeiffer RF, Tsuboi Y, et al. Autosomal dominant parkinsonism associated with variable synuclein and tau pathology. Neurology 2004 62 : 1619 1622.
23. Miklossy J, Arai T, Guo JP, et al. LRRK2 expression in normal and pathologic human brain and in human cell lines. Journal of Neuropathology and Experimental Neurology 2006 65 : 953 963.
24. Baker M, Litvan I, Houlden H, et al. Association of an extended haplotype in the tau gene with progressive supranuclear palsy. Human Molecular Genetics 1999 8 : 711 715.
25. Melquist S, Craig DW, Huentelman MJ, et al. Identification of a novel risk locus for progressive supranuclear palsy by a pooled genomewide scan of 500,288 single-nucleotide polymorphisms. American Journal of Human Genetics 2007 80 : 769 778.
26. Ros R, Ampuero I, García de Yébenes J. Parkin polymorphisms in progressive supranuclear palsy. Journal of the Neurological Sciences 2008 268 : 176 178.
27. Paviour DC, Price SL, Jahanshahi M, Lees AJ, Fox NC. Longitudinal MRI in progressive supranuclear palsy and multiple system atrophy: rates and regions of atrophy. Brain 2006 129 (Pt 4 1040 1049.
28. Paviour DC, Price SL, Lees AJ, Fox NC. MRI derived brain atrophy in PSP and MSA-P: determining sample size to detect treatment effects. Journal of Neurology 2007 254 : 478 481.
29. Eckert T, Barnes A, Dhawan V, et al. FDG PET in the differential diagnosis of parkinsonian disorders. Neuroimage 2005 26 : 912 921.
30. Piccini P, de Yebenez J, Lees AJ, et al. Familial progressive supranuclear palsy: detection of subclinical cases using 18F-dopa and 18fluorodeoxyglucose positron emission tomography. Archives of Neurology 2001 58 : 1846 1851.
31. Mollenhauer B, Bibl M, Esselmann H, et al. Tauopathies and synucleinopathies: do cerebrospinal fluid beta-amyloid peptides reflect disease-specific pathogenesis? Journal of Neural Transmission 2007 114 : 919 927.
32. Brettschneider J, Petzold A, Sussmuth SD, et al. Neurofilament heavy-chain NfH(SMI35) in cerebrospinal fluid supports the differential diagnosis of Parkinsonian syndromes. Movement Disorders 2006 21 : 2224 2227.
33. Mandelkow EM, Drewes G, Biernat J, et al. Glycogen synthase kinase-3 and the Alzheimer-like state of microtubule-associated protein tau. FEBS Letters 1992 314 : 315 321.
34. Pei JJ, Braak E, Braak H, et al. Distribution of active glycogen synthase kinase 3β (GSK-3β) in brains staged for Alzheimer disease neurofibrillary changes. Journal of Neuropathology and Experimental Neurology 1999 58 : 1010 1019.
35. Ferrer I, Barrachina M, Puig B. Glycogen synthase kinase-3 is associated with neuronal and glial hyperphosphorylated tau deposits in Alzheimer's disease, Pick's disease, progressive supranuclear palsy and corticobasal degeneration. Acta Neuropathologica 2002 104 : 583 591.
36. Lucas JJ, Hernandez F, Gomez-Ramos P, Moran MA, Hen R, Avila J. Decreased nuclear β-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3β conditional transgenic mice. EMBO Journal 2001 20 : 27 39.
37. Hernandez F, Borrell J, Guaza C, Avila J, Lucas JJ. Spatial learning deficit in transgenic mice that conditionally over-express GSK-3β in the brain but do not form tau filaments. Journal of Neurochemistry 2002 83 : 1529 1533.
38. Engel T, Hernandez F, Avila J, Lucas JJ. Full reversal of Alzheimer's disease-like phenotype in a mouse model with conditional overexpression of glycogen synthase kinase-3. Journal of Neuroscience 2006 26 : 5083 5090.
39. Engel T, Goni-Oliver P, Lucas JJ, Avila J, Hernandez F. Chronic lithium administration to FTDP-17 tau and GSK-3β overexpressing mice prevents tau hyperphosphorylation and neurofibrillary tangle formation, but pre-formed neurofibrillary tangles do not revert. Journal of Neurochemistry 2006 99 : 1445 1455.
40. Duff K, Planel E. Untangling memory deficits. Nature Medicine 2005 11 : 826 827.
41. Lannuzel A, Michel PP, Caparros-Lefebvre D, Abaul J, Hocquemiller R, Ruberg M. Toxicity of Annonaceae for dopaminergic neurons: potential role in atypical parkinsonism in Guadeloupe. Movement Disorders 2002 17 : 84 90.
42. Lannuzel A, Michel PP, Hoglinger GU, et al. The mitochondrial complex I inhibitor annonacin is toxic to mesencephalic dopaminergic neurons by impairment of energy metabolism. Neuroscience 2003 121 : 287 296.
43. Champy P, Hoglinger GU, Féger J, et al. Annonacin, a lipophilic inhibitor of mitochondrial complex I, induces nigral and striatal neurodegeneration in rats: possible relevance for atypical parkinsonism in Guadeloupe. Journal of Neurochemistry 2004 88 : 63 69.
44. Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, Greenamyre JT. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nature Neuroscience 2000 3 : 1301 1306.
45. Hoglinger GU, Lannuzel A, Khondiker ME, et al. The mitochondrial complex I inhibitor rotenone triggers a cerebral tauopathy. Journal of Neurochemistry 2005 95 : 930 939.
46. Albers DS, Swerdlow RH, Manfredi G, et al. Further evidence for mitochondrial dysfunction in progressive supranuclear palsy. Experimental Neurology 2001 168 : 196 198.
47. McGeer PL, McGeer EG. The inflammatory response system of brain: implications for therapy of Alzheimer and other neurodegenerative diseases. Brain Research. Brain Research Reviews 1995 21 : 195 218.
48. Chen H, Zhang SM, Hernan MA, et al. Nonsteroidal anti-inflammatory drugs and the risk of Parkinson disease. Archives of Neurology 2003 60 : 1059 1064.
49. McGeer PL, McGeer E, Rogers J, Sibley J. Anti-inflammatory drugs and Alzheimer disease. Lancet 1990 335 : 1037.
50. Zhang B, Maiti A, Shively S, et al. Microtubule-binding drugs offset tau sequestration by stabilizing microtubules and reversing fast axonal transport deficits in a tauopathy model. Proceedings of the National Academy of Sciences of the United States of America 2005 102 : 227 231.
51. Le Corre S, Klafki HW, Plesnila N, et al. An inhibitor of tau hyperphosphorylation prevents severe motor impairments in tau transgenic mice. Proceedings of the National Academy of Sciences of the United States of America 2006 103 : 9673 9678.
52. Noble W, Planel E, Zehr C, et al. Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo. Proceedings of the National Academy of Sciences of the United States of America 2005 102 : 6990 6995.
53. Liou YC, Sun A, Ryo A, et al. Role of the prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration. Nature 2003 424 : 556 561.
54. Wang YP, Biernat J, Pickhardt M, Mandelkow E, Mandelkow EM. Stepwise proteolysis liberates tau fragments that nucleate the Alzheimer-like aggregation of full-length tau in a neuronal cell model. Proceedings of the National Academy of Sciences of the United States of America 2007 104 : 10252 10257.
55. Gamblin TC, Chen F, Zambrano A, et al. Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proceedings of the National Academy of Sciences of the United States of America 2003 100 : 10032 10037.
56. Pickhardt M, Gazova Z, von Bergen M, et al. Anthraquinones inhibit tau aggregation and dissolve Alzheimer's paired helical filaments in vitro and in cells. Journal of Biological Chemistry 2005 280 : 3628 3635.
57. Asuni AA, Boutajangout A, Quartermain D, Sigurdsson EM. Immunotherapy targeting pathological tau conformers in a tangle mouse model reduces brain pathology with associated functional improvements. Journal of Neuroscience 2007 27 : 9115 9129.
58. Rosenmann H, Grigoriadis N, Karussis D, et al. Tauopathy-like abnormalities and neurologic deficits in mice immunized with neuronal tau protein. Archives of Neurology 2006 63 : 1459 1467.
59. Lewis J, McGowan E, Rockwood J, et al. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nature Genetics 2000 25 : 402 405 (Erratum in: Nat Genet 2000 Sep;26(1):127).
60. Santacruz K, Lewis J, Spires T, et al. Tau suppression in a neurodegenerative mouse model improves memory function. Science 2005 309 : 476 481.
61. Duff K, Knight H, Refolo LM, et al. Characterization of pathology in transgenic mice over-expressing human genomic and cDNA tau transgenes. Neurobiology of Disease 2000 7 : 87 98.
62. Ishihara T, Hong M, Zhang B, et al. Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron 1999 24 : 751 762.
63. Gotz J, Chen F, Barmettler R, Nitsch RM. Tau filament formation in transgenic mice expressing P301L tau. Journal of Biological Chemistry 2001 276 : 529 534.
64. Gotz J, Probst A, Spillantini MG, et al. Somatodendritic localization and hyperphosphorylation of tau protein in transgenic mice expressing the longest human brain tau isoform. EMBO Journal 1995 14 : 1304 1313.
65. Probst A, Gotz J, Wiederhold KH, et al. Axonopathy and amyotrophy in mice transgenic for human four-repeat tau protein. Acta Neuropathologica 2000 99 : 469 481.
66. Tanemura K, Akagi T, Murayama M, et al. Formation of filamentous tau aggregations in transgenic mice expressing V337M human tau. Neurobiology of Disease 2001 8 : 1036 1045.
67. Tatebayashi Y, Miyasaka T, Chui DH, et al. Tau filament formation and associative memory deficit in aged mice expressing mutant (R406W) human tau. Proceedings of the National Academy of Sciences of the United States of America 2002 99 : 13896 13901.
68. Dawson HN, Cantillana V, Chen L, Vitek MP. The tau N279K exon 10 splicing mutation recapitulates frontotemporal dementia and parkinsonism linked to chromosome 17 tauopathy in a mouse model. Journal of Neuroscience 2007 27 : 9155 9168.
69. Allen B, Ingram E, Takao M, et al. Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein. Journal of Neuroscience 2002 22 : 9340 9351.
70. Yoshiyama Y, Higuchi M, Zhang B, et al. Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 2007 53 : 337 351 (Erratum in: Neuron. 2007 Apr 19;54:343-344).
71. Spittaels K, Van den Haute C, Van Dorpe J, et al. Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein. American Journal of Pathology 1999 155 : 2153 2165.
72. Forman MS, Lal D, Zhang B, et al. Transgenic mouse model of tau pathology in astrocytes leading to nervous system degeneration. Journal of Neuroscience 2005 25 : 3539 3550.
73. Ittner LM, Fath T, Ke YD, et al. Parkinsonism and impaired axonal transport in a mouse model of frontotemporal dementia. Proceedings of the National Academy of Sciences of the United States of America 2008 105 : 15997 16002.
74. Higuchi M, Zhang B, Forman MS, Yoshiyama Y, Trojanowski JQ, Lee VM. Axonal degeneration induced by targeted expression of mutant human tau in oligodendrocytes of transgenic mice that model glial tauopathies. Journal of Neuroscience 2005 25 : 9434 9443.
75. Mocanu MM, Nissen A, Eckermann K, et al. The potential for beta-structure in the repeat domain of tau protein determines aggregation, synaptic decay, neuronal loss, and coassembly with endogenous Tau in inducible mouse models of tauopathy. Journal of Neuroscience 2008 28 : 737 748.
76. Oddo S, Caccamo A, Shepherd JD, et al. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 2003 39 : 409 421.
77. Schindowski K, Bretteville A, Leroy K, et al. Alzheimer's disease-like tau neuropathology leads to memory deficits and loss of functional synapses in a novel mutated tau transgenic mouse without any motor deficits. American Journal of Pathology 2006 169 : 599 616.
78. Jackson GR, Wiedau-Pazos M, Sang TK, et al. Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila. Neuron 2002 34 : 509 519.
79. Wittmann CW, Wszolek MF, Shulman JM, et al. Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science 2001 293 : 711 714.
80. Kraemer BC, Zhang B, Leverenz JB, Thomas JH, Trojanowski JQ, Schellenberg GD. Neurodegeneration and defective neurotransmission in a Caenorhabditis elegans model of tauopathy. Proceedings of the National Academy of Sciences of the United States of America 2003 100 : 9980 9985.
81. Bai Q, Garver JA, Hukriede NA, Burton EA. Generation of a transgenic zebrafish model of Tauopathy using a novel promoter element derived from the zebrafish eno2 gene. Nucleic Acids Research 2007 35 : 6501 6516.
82. Golbe LI, Ohman-Strickland PA. A clinical rating scale for progressive supranuclear palsy. Brain 2007 130 (Pt 6 1552 1565.
83. van Balken I, Litvan I. Current and future treatments in progressive supranuclear palsy. Current Treatment Options in Neurology 2006 8 : 211 223.
84. Ludolph AC, Bendotti C, Blaugrund E, et al. Guidelines for the preclinical in vivo evaluation of pharmacological active drugs for ALS/MND: report on the 142nd ENMC international workshop. Amyotrophic Lateral Sclerosis 2007 8 : 217 223.