Emerging drugs for progressive supranuclear palsy

References

• Boxer AL, Yu JT, Golbe LI, et al. Advances in progressive supranuclear palsy: new diagnostic criteria, biomarkers, and therapeutic approaches. Lancet Neurol. 2017;16:552–563.
   PubMed Web of Science ®Google Scholar
• Steele J, Richardson J, 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. Arch Neurol. 1964;10:333–359.
   PubMed Web of Science ®Google Scholar
• Respondek G, Stamelou M, Kurz C, et al. The phenotypic spectrum of progressive supranuclear palsy: a retrospective multicenter study of 100 definite cases. Mov Disord. 2014;29:1758–1766.
   PubMed Web of Science ®Google Scholar
• Respondek G, Kurz C, Arzberger T, et al. Which ante mortem clinical features predict progressive supranuclear palsy pathology? Mov Disord. 2017;32:995–1005.
   PubMed Web of Science ®Google Scholar
• Höglinger GU, Respondek G, Stamelou M, et al. Clinical diagnosis of progressive supranuclear palsy: the movement disorder society criteria. Mov Disord. 2017;32:853–864.
   PubMed Web of Science ®Google Scholar
• Golbe LI, Davis PH, Schoenberg BS, et al. Prevalence and natural history of progressive supranuclear palsy. Neurology. 1988;38:1031–1034.
   PubMed Web of Science ®Google Scholar
• Nath U, Ben-Shlomo Y, Thomson RG, et al. The prevalence of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome) in the UK. Brain. 2001;124:1438–1449.
   PubMed Web of Science ®Google Scholar
• Schrag A, Ben-Shlomo Y, Quinn N. Prevalence of progressive supranuclear palsy and multiple system atrophy: a cross-sectional study. Lancet. 1999;354:1771–1775.
   PubMed Web of Science ®Google Scholar
• Takigawa H, Kitayama M, Wada-Isoe K, et al. Prevalence of progressive supranuclear palsy in Yonago: change throughout a decade. Brain Behav. 2016;6:4–8.
   Web of Science ®Google Scholar
• Fleury V, Brindel P, Nicastro N, et al. Descriptive epidemiology of parkinsonism in the canton of Geneva, Switzerland. Park Relat Disord. 2018;54:30–39.
   PubMed Web of Science ®Google Scholar
• Kovacs GG. Invited review: neuropathology of tauopathies: principles and practice. Neuropathol Appl Neurobiol. 2015;41:3–23.
   PubMed Web of Science ®Google Scholar
• Dickson DW, Ahmed Z, Algom AA, et al. Neuropathology of variants of progressive supranuclear palsy. Curr Opin Neurol. 2010;23:394–400.
   PubMed Web of Science ®Google Scholar
• Arena JE, Weigand SD, Whitwell JL, et al. Progressive supranuclear palsy: progression and survival. J Neurol. 2016;263:380–389.
   PubMed Web of Science ®Google Scholar
• Owens E, Josephs KA, Savica R, et al. The clinical spectrum and natural history of pure akinesia with gait freezing. J Neurol. 2016;263:2419–2423.
   PubMed Web of Science ®Google Scholar
• Jecmenica-Lukic M, Petrovic IN, Pekmezovic T, et al. Clinical outcomes of two main variants of progressive supranuclear palsy and multiple system atrophy: a prospective natural history study. J Neurol. 2014;261:1575–1583.
   PubMed Web of Science ®Google Scholar
• Litvan I, Kong M. Rate of decline in progressive supranuclear palsy. Mov Disord. 2014;29:463–468.
   PubMed Web of Science ®Google Scholar
• Schmotz C, Richinger C, Lorenzl S. High burden and depression among late-stage idiopathic parkinson disease and progressive supranuclear palsy caregivers. J Geriatr Psychiatry Neurol. 2017;30:267–272.
   PubMed Web of Science ®Google Scholar
• Uttl B, Santacruz P, Litvan I, et al. Caregiving in progressive supranuclear palsy. Neurology. 1998;51:1303–1309.
   PubMed Web of Science ®Google Scholar
• McCrone P, Payan CAM, Knapp M, et al. The economic costs of progressive supranuclear palsy and multiple system atrophy in France, Germany and the United Kingdom. Uversky VN, editor. PLoS One. 2011;6:e24369.
   PubMed Web of Science ®Google Scholar
• Winter Y, Stamelou M, Cabanel N, et al. Cost-of-illness in multiple system atrophy and progressive supranuclear palsy. J Neurol. 2011;258:1827–1834.
   PubMed Web of Science ®Google Scholar
• Giagkou N, Stamelou M. Therapeutic management of the overlapping syndromes of atypical parkinsonism. CNS Drugs. 2018;32:827–837.
   PubMed Web of Science ®Google Scholar
• Stamelou M, Höglinger G. A review of treatment options for progressive supranuclear palsy. CNS Drugs. 2016;30:629–636.
   PubMed Web of Science ®Google Scholar
• Clerici I, Ferrazzoli D, Maestri R, et al. Rehabilitation in progressive supranuclear palsy: effectiveness of two multidisciplinary treatments. Fasano A, editor. PLoS One. 2017;12:e0170927.
   PubMed Web of Science ®Google Scholar
• Rittman T, Coyle-Gilchrist IT, Rowe JB. Managing cognition in progressive supranuclear palsy. Neurodegener Dis Manag. 2016;6:499–508.
   PubMed Web of Science ®Google Scholar
• Bhatia KP, Stamelou M. Nonmotor features in atypical parkinsonism. Int Rev Neurobiol. 2017;134:1285–1301.
   PubMed Web of Science ®Google Scholar
• Litvan I, Phipps M, Pharr VL, et al. Randomized placebo-controlled trial of donepezil in patients with progressive supranuclear palsy. Neurology. 2001;57:467–473.
   PubMed Web of Science ®Google Scholar
• Lamb R, Rohrer JD, Lees AJ, et al. Progressive supranuclear palsy and corticobasal degeneration: pathophysiology and treatment options. Curr Treat Options Neurol. 2016;18:42.
   PubMed Web of Science ®Google Scholar
• Eschlböck S, Krismer F, Wenning GK. Interventional trials in atypical parkinsonism. Parkinsonism Relat Disord. 2016;22:S82–S92.
   PubMed Web of Science ®Google Scholar
• Stamelou M, Reuss A, Pilatus U, et al. Short-term effects of coenzyme Q 10 in progressive supranuclear palsy: a randomized, placebo-controlled trial. Mov Disord. 2008;23:942–949.
   PubMed Web of Science ®Google Scholar
• Apetauerova D, Scala SA, Hamill RW, et al. CoQ10 in progressive supranuclear palsy: a randomized, placebo-controlled, double-blind trial. Neurol Neuroimmunol Neuroinflammation. 2016;3:e266.
   PubMed Web of Science ®Google Scholar
• Bensimon G, Ludolph A, Agid Y, et al. Riluzole treatment, survival and diagnostic criteria in parkinson plus disorders: the NNIPPS Study. Brain. 2009;132:156–171.
   PubMed Web of Science ®Google Scholar
• Nuebling G, Hensler M, Paul S, et al. PROSPERA: a randomized, controlled trial evaluating rasagiline in progressive supranuclear palsy. J Neurol. 2016;263:1565–1574.
   PubMed Web of Science ®Google Scholar
• Tolosa E, Litvan I, Höglinger GU, et al. A phase 2 trial of the GSK-3 inhibitor tideglusib in progressive supranuclear palsy. Mov Disord. 2014;29:470–478.
   PubMed Web of Science ®Google Scholar
• Höglinger GU, Huppertz HJ, Wagenpfeil S, et al. Tideglusib reduces progression of brain atrophy in progressive supranuclear palsy in a randomized trial. Mov Disord. 2014;29:479–487.
   PubMed Web of Science ®Google Scholar
• Boxer AL, Lang AE, Grossman M, et al. Davunetide in patients with progressive supranuclear palsy: a randomised, double-blind, placebo-controlled phase 2/3 trial. Lancet Neurol. 2014;13:676–685.
   PubMed Web of Science ®Google Scholar
• Boxer AL, Gold M, Huey E, et al. The advantages of frontotemporal degeneration drug development (part 2 of frontotemporal degeneration: the next therapeutic frontier). Alzheimer’s Dement. 2013;9:189–198.
   PubMed Web of Science ®Google Scholar
• Shoeibi A, Olfati N, Litvan I. Preclinical, phase I, and phase II investigational clinical trials for treatment of progressive supranuclear palsy. Expert Opin Investig Drugs. 2018;27:349–361.
   PubMed Web of Science ®Google Scholar
• Golbe LI, Ohman-Strickland PA. A clinical rating scale for progressive supranuclear palsy. Brain. 2007;130:1552–1565.
   PubMed Web of Science ®Google Scholar
• Hewer S, Varley S, Boxer AL, et al. Minimal clinically important worsening on the progressive supranuclear palsy rating scale. Mov Disord. 2016;31:1574–1577.
   PubMedGoogle Scholar
• Hall DA, Forjaz MJ, Golbe LI, et al. Scales to assess clinical features of progressive supranuclear palsy: MDS task force report. Mov Disord Clin Pract. 2015;2:127–134.
   PubMed Web of Science ®Google Scholar
• Höglinger GU, Schöpe J, Stamelou M, et al. Longitudinal magnetic resonance imaging in progressive supranuclear palsy: a new combined score for clinical trials. Mov Disord. 2017;32:842–852.
   PubMed Web of Science ®Google Scholar
• Hammes J, Drzezga A, Van Eimeren T. The role of tau imaging in parkinsonian disorders. Curr Neurol Neurosci Rep. 2018;18:86.
   PubMed Web of Science ®Google Scholar
• Rojas JC, Bang J, Lobach IV, et al. CSF neurofilament light chain and phosphorylated tau 181 predict disease progression in PSP. Neurology. 2018;90:e273-e281.
   PubMed Web of Science ®Google Scholar
• Stamelou M, Boxer AL. Disease-modifying treatments for progressive supranuclear palsy. Mov Disord Clin Pract. 2015;2:3–5.
   PubMed Web of Science ®Google Scholar
• Congdon EE, Sigurdsson EM. Tau-targeting therapies for alzheimer disease. Nat Rev Neurol. 2018;14:399–415.
   PubMed Web of Science ®Google Scholar
• Goedert M, Masuda-Suzukake M, Falcon B. Like prions: the propagation of aggregated tau and α-synuclein in neurodegeneration. Brain. 2017;140:266–278.
   PubMed Web of Science ®Google Scholar
• Clavaguera F, Bolmont T, Crowther RA, et al. Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Bio. 2009;11:909–913.
   PubMed Web of Science ®Google Scholar
• Clavaguera F, Akatsu H, Fraser G, et al. Brain homogenates from human tauopathies induce tau inclusions in mouse brain. Proc Natl Acad Sci. 2013;110:9535–9540.
   PubMed Web of Science ®Google Scholar
• Falcon B, Cavallini A, Angers R, et al. Conformation determines the seeding potencies of native and recombinant tau aggregates. J Biol Chem. 2015;290:1049–1065.
   PubMed Web of Science ®Google Scholar
• Wagshal D, Sankaranarayanan S, Guss V, et al. Divergent CSF τ alterations in two common tauopathies: alzheimer’s disease and progressive supranuclear palsy. J Neurol Neurosurg Psychiatry. 2015;86:244–250.
   PubMed Web of Science ®Google Scholar
• Meredith JE, Sankaranarayanan S, Guss V, et al. Characterization of novel CSF tau and ptau biomarkers for alzheimer’s disease. PLoS One. 2013;8:e76523.
   PubMed Web of Science ®Google Scholar
• Sato C, Barthélemy NR, Mawuenyega KG, et al. Tau kinetics in neurons and the human central nervous system. Neuron. 2018;97:1284–1298.e7.
   PubMed Web of Science ®Google Scholar
• 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;80:402–414.
   PubMed Web of Science ®Google Scholar
• Yanamandra K, Jiang H, Mahan TE, et al. Anti-tau antibody reduces insoluble tau and decreases brain atrophy. Ann Clin Transl Neurol. 2015;2:278–288.
   PubMed Web of Science ®Google Scholar
• West T, Hu Y, Verghese PB, et al. Preclinical and clinical development of ABBV-8E12, a humanized anti-tau antibody, for treatment of alzheimer’s disease and other tauopathies. J Prev Alzheimers Dis. 2017;44:236–241.
   Google Scholar
• Boxer A, Qureshi I, Grundman M, et al. Multiple ascending dose study of the tau-directed monoclonal antibody BIIB092 in patients with progressive supranuclear palsy (S27.004). Neurology. 2018; 90.
   Google Scholar
• Bright J, Hussain S, Dang V, et al. Human secreted tau increases amyloid-beta production. Neurobiol Aging. 2015;36:693–709.
   PubMed Web of Science ®Google Scholar
• Dam T, Boxer A, Golbe LI, et al. Efficacy and safety of BIIB092 in patients with progressive supranuclear palsy: PASSPORT phase 2 study design (P6.073). Neurology. 2018;90.
   Google Scholar
• Silberman S, Hwang JH, Marshall JL, et al. A phase I study of TPI 287, a novel taxane, administered weekly in patients with advanced cancer. J Clin Oncol. 2008;26: 2536–2536.
   Google Scholar
• Hauser TH, Salastekar N, Schaefer EJ, et al. Effect of targeting inflammation with salsalate. JAMA Cardiol. 2016;1:413.
   PubMedGoogle Scholar
• Castellano JM, Kirby ED, Wyss-Coray T. Blood-borne revitalization of the aged brain. JAMA Neurol. 2015;72:1191.
   PubMed Web of Science ®Google Scholar
• Kerchner GA, Ayalon G, Brunstein F, et al. A Phase I study to evaluate the safety and tolerability of RO7105705 in healthy volunteers and patients with mild-to-moderateAD. Alzheimer’s Dement. 2017;13:P601.
   Google Scholar
• Alam R, Driver D, Wu S, et al. Preclinical characterization of an antibody [LY3303560] targeting aggregated tau. Alzheimer’s Dement. 2017;13:P592–P593.
   PubMedGoogle Scholar
• Novak P, Schmidt R, Kontsekova E, et al. Safety and immunogenicity of the tau vaccine AADvac1 in patients with alzheimer’s disease: a randomised, double-blind, placebo-controlled, phase 1 trial. Lancet Neurol. 2017;16:123–134.
   PubMed Web of Science ®Google Scholar
• Kontsekova E, Zilka N, Kovacech B, et al. First-in-man tau vaccine targeting structural determinants essential for pathological tau-tau interaction reduces tau oligomerisation and neurofibrillary degeneration in an alzheimer’s disease model. Alzheimers Res Ther. 2014;6:44.
   PubMed Web of Science ®Google Scholar
• Gauthier S, Feldman HH, Schneider LS, et al. Efficacy and safety of tau-aggregation inhibitor therapy in patients with mild or moderate Alzheimer’s disease: a randomised, controlled, double-blind, parallel-arm, phase 3 trial. Lancet. 2016;388:2873–2884.
   PubMed Web of Science ®Google Scholar
• Wilcock GK, Gauthier S, Frisoni GB, et al. Potential of low dose leuco-methylthioninium Bis(Hydromethanesulphonate) (LMTM) monotherapy for treatment of mild alzheimer’s disease: cohort analysis as modified primary outcome in a phase iii clinical trial. J Alzheimer’s Dis. 2018;61:435–457.
   PubMed Web of Science ®Google Scholar
• Pagan F, Hebron M, Valadez EH, et al. Nilotinib effects in parkinson’s disease and dementia with lewy bodies. J Parkinsons Dis. 2016;6:503–517.
   PubMedGoogle Scholar
• Hebron ML, Javidnia M, Moussa CEH. Tau clearance improves astrocytic function and brain glutamate-glutamine cycle. J Neurol Sci. 2018;391:90–99.
   PubMed Web of Science ®Google Scholar
• Wyse RK, Brundin P, Sherer TB. Nilotinib – differentiating the hope from the hype. J Parkinsons Dis. 2016;6:519–522.
   PubMedGoogle Scholar
• Fricker RA, Green EL, Jenkins SI, et al. The influence of nicotinamide on health and disease in the central nervous system. Int J Tryptophan Res. 2018;11:1178646918776658.
   Web of Science ®Google Scholar
• Mignon L, Kordasiewicz H, Lane R, et al. Design of the first-in-human study of IONIS-MAPTRx, a Tau-lowering antisense oligonucleotide, in patients with alzheimer disease (S2.006). Neurology. 2018;90.
   Web of Science ®Google Scholar
• DeVos SL, Miller RL, Schoch KM, et al. Tau reduction prevents neuronal loss and reverses pathological tau deposition and seeding in mice with tauopathy. Sci Transl Med. 2017;9.
   PubMed Web of Science ®Google Scholar
• Rossor AM, Reilly MM, Sleigh JN. Antisense oligonucleotides and other genetic therapies made simple. Pract Neurol. 2018;18:126–131.
   PubMedGoogle Scholar
• Tabrizi S, Leavitt B, Kordasiewicz H, et al. Effects of IONIS-HTTRx in patients with early huntington’s disease, results of the first HTT-lowering drug trial (CT.002). Neurology. 2018;90.
   Web of Science ®Google Scholar
• Drugs@FDA: FDA approved drug products [Internet]. Silver Spring (MD): U.S. Food and Drug Administration; 2007. [cited 2018 Oct 10]. Available from: https://www.accessdata.fda.gov/scripts/cder/daf/
   Google Scholar
• Tegsedi [Internet]. London: European Medicines Agency; 2018. [cited 2018 Oct 13]. Available from: https://www.ema.europa.eu/medicines/human/EPAR/tegsedi
   Google Scholar
• Wisniewski T, Goñi F. Immunotherapeutic approaches for alzheimer’s disease. Neuron. 2015;85:1162–1176.
   PubMed Web of Science ®Google Scholar
• Qosa H, Volpe DA. The development of biological therapies for neurological diseases: moving on from previous failures. Expert Opin Drug Discov. 2018;13:283–293.
   PubMed Web of Science ®Google Scholar
• Register of designated orphan medicinal products (alphabetical) [Internet]. [cited 2018 Oct 10]. Available from: http://ec.europa.eu/health/documents/community-register/html/alforphreg.htm
   Google Scholar
• The Lancet Neurology. Treating rare disorders: time to act on unfair prices. Lancet Neurol. 2017;16:761.
   PubMed Web of Science ®Google Scholar
• Antoñanzas F, Juárez-Castelló CA, Rodríguez-Ibeas R. EMA Priority Medicines scheme (PRIME): will more paying-for-performance agreements be needed due to immature data? Eur. J Heal Econ. 2018;19:905–907.
   Web of Science ®Google Scholar
• Pariser AR, Robb M, Sherman RE. Expedited programs for drug development and approval. Expert Opin Orphan Drugs. 2013;1:507–510.
   Web of Science ®Google Scholar
• Gellad WF, Kesselheim AS. Accelerated approval and expensive drugs – a challenging combination. N Engl J Med. 2017;376:2001–2004.
   PubMed Web of Science ®Google Scholar
• Mitsumoto J, Dorsey ER, Beck CA, et al. Pivotal studies of orphan drugs approved for neurological diseases. Ann Neurol. 2009;66:184–190.
   PubMed Web of Science ®Google Scholar
• Kesselheim AS, Myers JA, Avorn J. Characteristics of clinical trials to support approval of orphan vs nonorphan drugs for cancer. JAMA. 2011;305:2320–2326.
   PubMed Web of Science ®Google Scholar