Clinical trials: Past, current, and future for atypical parkinsonian syndromes

Seminars in Neurology

Volumn 34, Issue 2, 2014, Pages 225-234

  Tsai, Richard M ^a   Boxer, Adam L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

clinical trials; corticobasal degeneration; dementia with Lewy bodies; multiple system atrophy; progressive supranuclear palsy; treatment

Indexed keywords

DAVUNETIDE; DONEPEZIL; EPOTHILONE D; GABAPENTIN; LITHIUM CHLORIDE; MEMANTINE; MINOCYCLINE; NICOTINIC ACID; PACLITAXEL; PHYSOSTIGMINE; PLACEBO; PYRUVIC ACID; QUETIAPINE; RIVASTIGMINE; THREO 3,4 DIHYDROXYPHENYLSERINE; TIDEGLUSIB; ZOLPIDEM;

ALZHEIMER DISEASE; ARTICLE; ATYPICAL PARKINSONIAN SYNDROME; CLINICAL TRIAL (TOPIC); CORTICOBASAL DEGENERATION; DIFFUSE LEWY BODY DISEASE; DISEASE COURSE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HUMAN; NEUROPATHOLOGY; NONHUMAN; PARKINSONISM; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; RANDOMIZED CONTROLLED TRIAL (TOPIC); SHY DRAGER SYNDROME; TAUOPATHY; MULTIPLE SYSTEM ATROPHY; PARKINSONIAN DISORDERS; SUPRANUCLEAR PALSY, PROGRESSIVE; TRENDS; UNITED STATES;

CLINICAL TRIALS AS TOPIC; HUMANS; MULTIPLE SYSTEM ATROPHY; PARKINSONIAN DISORDERS; SUPRANUCLEAR PALSY, PROGRESSIVE; UNITED STATES;

EID: 84903270208     PISSN: 02718235     EISSN: 10989021     Source Type: Journal    
DOI: 10.1055/s-0034-1381739     Document Type: Article

References (89)

1. Wenning G. K., Litvan I., Tolosa E. Milestones in atypical and secondary parkinsonisms. Mov Disord: 2011; 26 6 1083 1095
2. Steele J. C., Richardson J. C., Olszewski J. Progressive supranuclear palsy. A heterogeneous degeneration involving the brainstem, basal ganglia and cerebellum with vertical gaze and pseudobulbar palsy, nuchal dystonia and dementia. Arch Neurol: 1964; 10 333 359
3. Williams D. R., de Silva R., Paviour D. C., 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
4. Williams D. R., Lees A. J. Progressive supranuclear palsy: clinicopathological concepts and diagnostic challenges. Lancet Neurol: 2009; 8 3 270 279
5. Lang A. E. Treatment of progressive supranuclear palsy and corticobasal degeneration. Mov Disord: 2005; 20 12 S83 S91
6. Klawans H. L. Jr, Ringel S. P. Observations on the efficacy of L-dopa in progressive supranuclear palsy. Eur Neurol: 1971; 5 2 115 129
7. Kompoliti K., Goetz C. G., Litvan I., Jellinger K., Verny M. Pharmacological therapy in progressive supranuclear palsy. Arch Neurol: 1998; 55 8 1099 1102
8. Birdi S., Rajput A. H., Fenton M., et al. Progressive supranuclear palsy diagnosis and confounding features: report on 16 autopsied cases. Mov Disord: 2002; 17 6 1255 1264
9. Ruberg M., Javoy-Agid F., Hirsch E., et al. Dopaminergic and cholinergic lesions in progressive supranuclear palsy. Ann Neurol: 1985; 18 5 523 529
10. Javoy-Agid F. Cholinergic and peptidergic systems in PSP. J Neural Transm Suppl: 1994; 42 205 218
11. Levy R., Ruberg M., Herrero M. T., et al. Alterations of GABAergic neurons in the basal ganglia of patients with progressive supranuclear palsy: an in situ hybridization study of GAD67 messenger RNA. Neurology: 1995; 45 1 127 134
12. Litvan I., Gomez C., Atack J. R., et al. Physostigmine treatment of progressive supranuclear palsy. Ann Neurol: 1989; 26 3 404 407
13. Fabbrini G., Barbanti P., Bonifati V., et al. Donepezil in the treatment of progressive supranuclear palsy. Acta Neurol Scand: 2001; 103 2 123 125
14. Litvan I., Phipps M., Pharr V. L., Hallett M., Grafman J., Salazar A. Randomized placebo-controlled trial of donepezil in patients with progressive supranuclear palsy. Neurology: 2001; 57 3 467 473
15. Liepelt I., Gaenslen A., Godau J., et al. Rivastigmine for the treatment of dementia in patients with progressive supranuclear palsy: clinical observations as a basis for power calculations and safety analysis. Alzheimers Dement: 2010; 6 1 70 74
16. Daniele A., Moro E., Bentivoglio A. R. Zolpidem in progressive supranuclear palsy. N Engl J Med: 1999; 341 7 543 544
17. Poujois A., Vidailhet M., Trocello J. M., Bourdain F., Gaymard B., Rivaud-Péchoux S. Effect of gabapentin on oculomotor control and parkinsonism in patients with progressive supranuclear palsy. Eur J Neurol: 2007; 14 9 1060 1062
18. Rebeiz J. J., Kolodny E. H., Richardson E. P. Jr. Corticodentatonigral degeneration with neuronal achromasia: a progressive disorder of late adult life. Trans Am Neurol Assoc: 1967; 92 23 26
19. Lee S. E., Rabinovici G. D., Mayo M. C., et al. Clinicopathological correlations in corticobasal degeneration. Ann Neurol: 2011; 70 2 327 340
20. Ling H., O'Sullivan S. S., Holton J. L., et al. Does corticobasal degeneration exist? A clinicopathological re-evaluation. Brain: 2010; 133 Pt 7 2045 2057
21. Hughes A. J., Daniel S. E., Ben-Shlomo Y., Lees A. J. The accuracy of diagnosis of parkinsonian syndromes in a specialist movement disorder service. Brain: 2002; 125 Pt 4 861 870
22. Mathew R., Bak T. H., Hodges J. R. Diagnostic criteria for corticobasal syndrome: a comparative study. J Neurol Neurosurg Psychiatry: 2012; 83 4 405 410
23. Armstrong M. J., Litvan I., Lang A. E., et al. Criteria for the diagnosis of corticobasal degeneration. Neurology: 2013; 29 80 498 503
24. Maruyama M., Shimada H., Suhara T., et al. Imaging of tau pathology in a tauopathy mouse model and in Alzheimer patients compared to normal controls. Neuron: 2013; 79 6 1094 1108
25. Xia C. F., Arteaga J., Chen G., et al. [(18)F]T807, a novel tau positron emission tomography imaging agent for Alzheimer's disease. Alzheimers Dement: 2013; 9 6 666 676
26. Drechsel D. N., Hyman A. A., Cobb M. H., Kirschner M. W. Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol Biol Cell: 1992; 3 10 1141 1154
27. Khlistunova I., Biernat J., Wang Y., 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 2 1205 1214
28. Van der Jeugd A., Hochgräfe K., Ahmed T., et al. Cognitive defects are reversible in inducible mice expressing pro-aggregant full-length human tau. Acta Neuropathol: 2012; 123 6 787 805
29. Bramblett G. T., Goedert M., Jakes R., Merrick S. E., Trojanowski J. Q., Lee V. M. Abnormal tau phosphorylation at Ser396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron: 1993; 10 6 1089 1099
30. Brunden K. R., Trojanowski J. Q., Lee V. M. Advances in tau-focused drug discovery for Alzheimer's disease and related tauopathies. Nat Rev Drug Discov: 2009; 8 10 783 793
31. Roberson E. D., Scearce-Levie K., Palop J. J., et al. Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model. Science: 2007; 316 5825 750 754
32. Abbondante S., Baglietto-Vargas D., Rodriguez-Ortiz C. J., Estrada-Hernandez T., Medeiros R., Laferla F. M. Genetic ablation of tau mitigates cognitive impairment induced by type 1 diabetes. Am J Pathol: 2014; 184 3 819 826
33. Morris M., Hamto P., Adame A., Devidze N., Masliah E., Mucke L. Age-appropriate cognition and subtle dopamine-independent motor deficits in aged tau knockout mice. Neurobiol Aging: 2013; 34 6 1523 1529
34. Wischik C. M., Harrington C. R., Storey J. M. Tau-aggregation inhibitor therapy for Alzheimer's disease. Biochem Pharmacol: 2014; 88 4 529 539
35. US National Institute of Health Clinical Trials Registry. 2010. Available at: http://clinicaltrials.gov/show/NCT00703677. Accessed February 21, 2014
36. Höglinger G. U., Huppertz H. J., Wagenpfeil S., et al. TAUROS MRI Investigators. Tideglusib reduces progression of brain atrophy in progressive supranuclear palsy in a randomized trial. Mov Disord: 2014; 29 4 479 487
37. Tolosa E., Litvan I., Höglinger G. U., et al. TAUROS Investigators. A phase 2 trial of the GSK-3 inhibitor tideglusib in progressive supranuclear palsy. Mov Disord: 2014; 29 4 470 478
38. Min S. W., Cho S. H., Zhou Y., et al. Acetylation of tau inhibits its degradation and contributes to tauopathy. Neuron: 2010; 67 6 953 966
39. DeVos S. L., Goncharoff D. K., Chen G., et al. Antisense reduction of tau in adult mice protects against seizures. J Neurosci: 2013; 33 31 12887 12897
40. Pride M., Seubert P., Grundman M., Hagen M., Eldridge J., Black R. S. Progress in the active immunotherapeutic approach to Alzheimer's disease: clinical investigations into AN1792-associated meningoencephalitis. Neurodegener Dis: 2008; 5 3-4 194 196
41. Boimel M., Grigoriadis N., Lourbopoulos A., Haber E., Abramsky O., Rosenmann H. Efficacy and safety of immunization with phosphorylated tau against neurofibrillary tangles in mice. Exp Neurol: 2010; 224 2 472 485
42. Asuni A. A., Boutajangout A., Quartermain D., Sigurdsson E. M. Immunotherapy targeting pathological tau conformers in a tangle mouse model reduces brain pathology with associated functional improvements. J Neurosci: 2007; 27 34 9115 9129
43. Boutajangout A., Quartermain D., Sigurdsson E. M. Immunotherapy targeting pathological tau prevents cognitive decline in a new tangle mouse model. J Neurosci: 2010; 30 49 16559 16566
44. FierceBiotech AC Immune begins first trial of a tau-targeting Alzheimer's vaccine. 2014. Available at: http://www.fiercevaccines.com/story/ac-immune- begins-first-trial-tau-targeting-alzheimers-vaccine/2014-01-13. Accessed February 21, 2014
45. Chai X., Wu S., Murray T. K., et al. Passive immunization with anti-tau antibodies in two transgenic models: reduction of tau pathology and delay of disease progression. J Biol Chem: 2011; 286 39 34457 34467
46. Boutajangout A., Ingadottir J., Davies P., Sigurdsson E. M. Passive immunization targeting pathological phospho-tau protein in a mouse model reduces functional decline and clears tau aggregates from the brain. J Neurochem: 2011; 118 4 658 667
47. Yanamandra K., Kfoury N., Jiang H., et al. Anti-tau antibodies that block tau aggregate seeding in vitro markedly decrease pathology and improve cognition in vivo. Neuron: 2013; 80 2 402 414
48. Higuchi M., Lee V. M., Trojanowski J. Q. Tau and axonopathy in neurodegenerative disorders. Neuromolecular Med: 2002; 2 2 131 150
49. Brunden K. R., Ballatore C., Lee V. M., Smith A. B. III, Trojanowski J. Q. Brain-penetrant microtubule-stabilizing compounds as potential therapeutic agents for tauopathies. Biochem Soc Trans: 2012; 40 4 661 666
50. Barten D. M., Fanara P., Andorfer C., et al. Hyperdynamic microtubules, cognitive deficits, and pathology are improved in tau transgenic mice with low doses of the microtubule-stabilizing agent BMS-241027. J Neurosci: 2012; 32 21 7137 7145
51. US National Institute of Health Clinical Trials Registry. 2014. Available at: http://clinicaltrials.gov/ct2/show/NCT01966666?term=tpi+287&rank. Accessed February 21, 2014
52. Stamelou M., de Silva R., Arias-Carrión O., et al. Rational therapeutic approaches to progressive supranuclear palsy. Brain: 2010; 133 Pt 6 1578 1590
53. Stamelou M., Pilatus U., Reuss A., et al. In vivo evidence for cerebral depletion in high-energy phosphates in progressive supranuclear palsy. J Cereb Blood Flow Metab: 2009; 29 4 861 870
54. Swerdlow R. H., Golbe L. I., Parks J. K., et al. Mitochondrial dysfunction in cybrid lines expressing mitochondrial genes from patients with progressive supranuclear palsy. J Neurochem: 2000; 75 4 1681 1684
55. Albers D. S., Swerdlow R. H., Manfredi G., et al. Further evidence for mitochondrial dysfunction in progressive supranuclear palsy. Exp Neurol: 2001; 168 1 196 198
56. Chirichigno J. W., Manfredi G., Beal M. F., Albers D. S. Stress-induced mitochondrial depolarization and oxidative damage in PSP cybrids. Brain Res: 2002; 951 1 31 35
57. 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 9175 281 286
58. Abdin A. A., Hamouda H. E. Mechanism of the neuroprotective role of coenzyme Q10 with or without L-dopa in rotenone-induced parkinsonism. Neuropharmacology: 2008; 55 8 1340 1346
59. Stamelou M., Reuss A., Pilatus U., et al. Short-term effects of coenzyme Q10 in progressive supranuclear palsy: a randomized, placebo-controlled trial. Mov Disord: 2008; 23 7 942 949
60. US National Institute of Health Clinical Trials Registry. 2013. Available at: http://clinicaltrials.gov/show/NCT00382824. Accessed February 21, 2014
61. US National Institute of Health Clinical Trials Registry. 2009. http://clinicaltrials.gov/show/NCT00605930. Accessed February 21, 2014
62. McKeith I. G., Dickson D. W., Lowe J., et al. Consortium on DLB. Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology: 2005; 65 12 1863 1872
63. Piggott M. A., Marshall E. F., Thomas N., et al. Striatal dopaminergic markers in dementia with Lewy bodies, Alzheimer's and Parkinson's diseases: rostrocaudal distribution. Brain: 1999; 122 Pt 8 1449 1468
64. Klein J. C., Eggers C., Kalbe E., et al. Neurotransmitter changes in dementia with Lewy bodies and Parkinson disease dementia in vivo. Neurology: 2010; 74 11 885 892
65. Tiraboschi P., Hansen L. A., Alford M., et al. Early and widespread cholinergic losses differentiate dementia with Lewy bodies from Alzheimer disease. Arch Gen Psychiatry: 2002; 59 10 946 951
66. Lippa C. F., Duda J. E., Grossman M., et al. DLB/PDD Working Group. DLB and PDD boundary issues: diagnosis, treatment, molecular pathology, and biomarkers. Neurology: 2007; 68 11 812 819
67. Guo J. L., Lee V. M. Cell-to-cell transmission of pathogenic proteins in neurodegenerative diseases. Nat Med: 2014; 20 2 130 138
68. Masliah E., Rockenstein E., Mante M., et al. Passive immunization reduces behavioral and neuropathological deficits in an alpha-synuclein transgenic model of Lewy body disease. PLoS ONE: 2011; 6 4 e19338
69. Halliday G. M., Holton J. L., Revesz T., Dickson D. W. Neuropathology underlying clinical variability in patients with synucleinopathies. Acta Neuropathol: 2011; 122 2 187 204
70. McKeith I., Del Ser T., Spano P., et al. Efficacy of rivastigmine in dementia with Lewy bodies: a randomised, double-blind, placebo-controlled international study. Lancet: 2000; 356 9247 2031 2036
71. Wesnes K. A., McKeith I. G., Ferrara R., et al. Effects of rivastigmine on cognitive function in dementia with Lewy bodies: a randomised placebo-controlled international study using the cognitive drug research computerised assessment system. Dement Geriatr Cogn Disord: 2002; 13 3 183 192
72. Beversdorf D. Q., Warner J. L., Davis R. A., Sharma U. K., Nagaraja H. N., Scharre D. W. Donepezil in the treatment of dementia with lewy bodies. Am J Geriatr Psychiatry: 2004; 12 5 542 544
73. Mori E., Ikeda M., Kosaka K.; Donepezil-DLB Study Investigators. Donepezil for dementia with Lewy bodies: a randomized, placebo-controlled trial. Ann Neurol: 2012; 72 1 41 52
74. Tariot P. N., Farlow M. R., Grossberg G. T., Graham S. M., McDonald S., Gergel I.; Memantine Study Group. Memantine treatment in patients with moderate to severe Alzheimer disease already receiving donepezil: a randomized controlled trial. JAMA: 2004; 291 3 317 324
75. Reisberg B., Doody R., Stöffler A., Schmitt F., Ferris S., Möbius H. J.; Memantine Study Group. Memantine in moderate-to-severe Alzheimer's disease. N Engl J Med: 2003; 348 14 1333 1341
76. Aarsland D., Ballard C., Walker Z., et al. Memantine in patients with Parkinson's disease dementia or dementia with Lewy bodies: a double-blind, placebo-controlled, multicentre trial. Lancet Neurol: 2009; 8 7 613 618
77. Emre M., Tsolaki M., Bonuccelli U., et al. 11018 Study Investigators. Memantine for patients with Parkinson's disease dementia or dementia with Lewy bodies: a randomised, double-blind, placebo-controlled trial. Lancet Neurol: 2010; 9 10 969 977
78. Cummings J. L., Street J., Masterman D., Clark W. S. Efficacy of olanzapine in the treatment of psychosis in dementia with Lewy bodies. Dement Geriatr Cogn Disord: 2002; 13 2 67 73
79. Kurlan R., Cummings J., Raman R., Thal L.; Alzheimer's Disease Cooperative Study Group. Quetiapine for agitation or psychosis in patients with dementia and parkinsonism. Neurology: 2007; 68 17 1356 1363
80. Cummings J., Isaacson S., Mills R., et al. Pimavanserin for patients with Parkinson's disease psychosis: a randomised, placebo-controlled phase 3 trial. Lancet: 2014; 383 9916 533 540
81. Stefanova N., Bücke P., Duerr S., Wenning G. K. Multiple system atrophy: an update. Lancet Neurol: 2009; 8 12 1172 1178
82. Freeman R., Landsberg L., Young J. The treatment of neurogenic orthostatic hypotension with 3,4-DL-threodihydroxyphenylserine: a randomized, placebo controlled crossover trial. Neurology: 1999; 53 2151 2157
83. US National Institute of Health Clinical Trials Registry. 2013. Available at: http://clinicaltrials.gov/show/NCT00782340. Accessed February 21, 2014
84. MedScape FDA Clears Droxidopa for Neurogenic Orthostatic Hypotension. 2014. Available at: http://www.medscape.com/viewarticle/820786. Accessed February 21, 2014
85. Bensimon G., Ludolph A., Agid Y., Vidailhet M., Payan C., Leigh P. N.; NNIPPS Study Group. Riluzole treatment, survival and diagnostic criteria in Parkinson plus disorders: the NNIPPS study. Brain: 2009; 132 Pt 1 156 171
86. Dodel R., Spottke A., Gerhard A., et al. Minocycline 1-year therapy in multiple-system-atrophy: effect on clinical symptoms and [(11)C] (R)-PK11195 PET (MEMSA-trial). Mov Disord: 2010; 25 1 97 107
87. Schwid S. R., Cutter G. R. Futility studies: spending a little to save a lot. Neurology: 2006; 66 5 626 627
88. Schoenfeld D. A., Cudkowicz M. Design of phase II ALS clinical trials. Amyotroph Lateral Scler: 2008; 9 1 16 23
89. Collins B., Constant J., Kaba S., Barclay C. L., Mohr E. Dementia with Lewy bodies: implications for clinical trials. Clin Neuropharmacol: 2004; 27 6 281 292