Effects of oxidized and reduced forms of methylthioninium in two transgenic mouse tauopathy models

Behavioural Pharmacology

Volumn 26, Issue 4, 2015, Pages 353-368

  Melis, Valeria ^a   Magbagbeolu, Mandy ^c   Rickard, Janet E ^a   Horsley, David ^a   Davidson, Kathleen ^a   Harrington, Kathleen A ^a   Goatman, Keith ^a   Goatman, Elizabeth A ^a   Deiana, Serena ^a   Close, Steve P ^a   Zabke, Claudia ^c   Stamer, Karsten ^c   Dietze, Silke ^c   Schwab, Karima ^c   Storey, John M D ^b   Harrington, Charles R ^a   Wischik, Claude M ^a   Theuring, Franz ^c   Riedel, Gernot ^b  

^a Section of Translational Medical Sciences   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Keywords: animal models; learning and memory; leucomethylthioninium; methylene blue; rat; RotaRod; tauopathies; water maze

Indexed keywords

LEUCOMETHYLTHIONINIUM; METHYLENE BLUE; UNCLASSIFIED DRUG; NEUROPROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COMPARATIVE EFFECTIVENESS; CONTROLLED STUDY; ENTORHINAL CORTEX; FOOD INTAKE; GENOTYPE; HIPPOCAMPUS; HISTOPATHOLOGY; LEARNING; LEARNING DISORDER; MAZE TEST; MOTOR PERFORMANCE; MOUSE; NONHUMAN; PHENOTYPE; PROBLEM SOLVING; ROTAROD TEST; SPATIAL LEARNING; TAUOPATHY; TRANSGENIC MOUSE; ANIMAL; BRAIN; CHEMISTRY; COHORT ANALYSIS; COMPARATIVE STUDY; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; FEMALE; LEARNING DISORDERS; METABOLISM; MOTOR ACTIVITY; NERVE CELL; OXIDATION REDUCTION REACTION; PATHOLOGY; PATHOPHYSIOLOGY; RANDOMIZATION; TAUOPATHIES;

ANIMALS; BRAIN; COHORT STUDIES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; LEARNING DISORDERS; MAZE LEARNING; METHYLENE BLUE; MICE, TRANSGENIC; MOTOR ACTIVITY; NEURONS; NEUROPROTECTIVE AGENTS; OXIDATION-REDUCTION; PROBLEM SOLVING; RANDOM ALLOCATION; TAUOPATHIES;

EID: 84928393250     PISSN: 09558810     EISSN: 14735849     Source Type: Journal    
DOI: 10.1097/FBP.0000000000000133     Document Type: Article

References (37)

1. Alzheimer A (1907). Uber eine eigenartige Erkrankung der Hirnrinde [article in German]. Allg Z Psych Psych-gerich Med 64:146-148.
2. Baddeley TC, McCaffrey J, Storey JM, Cheung JK, Melis V, Horsley D, et al. (2015). Complex disposition of methylthioninium redox forms: partial dissociation of cognitive and hematological activity. J Pharmacol Exp Ther 352:110-118.
3. Braak H, Braak E (1991). Neuropathological staging of Alzheimer-related changes. Acta Neuropathol 82:239-259.
4. Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, Probst A, et al. (2009). Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 11:909-913.
5. Congdon EE, Wu JW, Myeku N, Figueroa YH, Herman M, Marinec PS, et al. (2012). Methylthioninium chloride (methylene blue) induces autophagy and attenuates tauopathy in vitro and in vivo.. Autophagy 8:609-622.
6. Deiana S, Harrington CR, Wischik CM, Riedel G (2009). Methylthioninium chloride reverses cognitive deficits induced by scopolamine: comparison with rivastigmine. Psychopharmacology (Berl) 202:53-65.
7. Duyckaerts C (2011). Tau pathology in children and young adults: can you still be unconditionally baptist? Acta Neuropathol 121:145-147.
8. Franklin KBJ, Paxinos G (2008). The mouse brain in stereotaxic coordinates Compact, 3rd ed.. New York: Academic Press.
9. Frost B, Jacks RL, Diamond MI (2009). Propagation of tau misfolding from the outside to the inside of a cell. J Biol Chem 284:12845-12852.
10. Goedert M, Spillantini MG, Cairns NJ, Crowther RA (1992). Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron 8:159-168.
11. Harrington CR, Mukaetova-Ladinska EB, Hills R, Edwards PC, Montejo de Garcini E, Novak M, Wischik CM (1991). Measurement of distinct immunochemical presentations of tau protein in Alzheimer disease. Proc Natl Acad Sci USA 88:5842-5846.
12. Harrington CR, Storey JMD, Clunas S, Harrington KA, Horsley D, Ishaq A, et al. (2015). Cellular models of aggregation-dependent template-directed proteolysis to characterize tau aggregation inhibitors for treatment of Alzheimer's disease. DOI: 10.1074/jbc.M114.616029. [Epub ahead of print].
13. Hosokawa M, Arai T, Masuda-Suzukake M, Nonaka T, Yamashita M, Akiyama H, Hasegawa M (2012). Methylene blue reduced abnormal tau accumulation in P301L tau transgenic mice. PLOS ONE 7:e52389.
14. Jakes R, Novak M, Davison M,Wischik CM (1991). Identification of 3-And 4-repeat tau isoforms within the PHF in Alzheimer's disease. EMBO J 10:2725-2729.
15. May JM, Qu ZC, Cobb CE (2004). Reduction and uptake of methylene blue by human erythrocytes. Am J Physiol Cell Physiol 286:C1390-C1398.
16. Medina DX, Caccamo A, Oddo S (2011). Methylene blue reduces A? levels and rescues early cognitive deficit by increasing proteasome activity. Brain Pathol 21:140-149.
17. Melis V, Zabke C, Stamer K, Magbagbeolu M, Schwab K, Marschall P, et al. (2015). Different pathways of molecular pathophysiology underlie cognitive and motor tauopathy phenotypes in transgenic models for Alzheimer's disease and frontotemporal lobar degeneration. Cell Mol Life Sci [Epub ahead of print]. doi: 10.1007/s00018-014-1804-z.
18. Mukaetova-Ladinska EB, Garcia-Siera F, Hurt J, Gertz HJ, Xuereb JH, Hills R, et al. (2000). Staging of cytoskeletal and beta-Amyloid changes in human isocortex reveals biphasic synaptic protein response during progression of Alzheimer's disease. Am J Pathol 157:623-636.
19. Novak M, Kabat J, Wischik CM (1993). Molecular characterization of the minimal protease resistant tau unit of the Alzheimer's disease paired helical filament. EMBO J 12:365-370.
20. Ohm TG, Müller H, Braak H, Bohl J (1995). Close-meshed prevalence rates of different stages as a tool to uncover the rate of Alzheimer's disease-related neurofibrillary changes. Neuroscience 64:209-217.
21. O'Leary JC 3rd, Li Q, Marinec P, Blair LJ, Congdon EE, Johnson AG, et al. (2010). Phenothiazine-mediated rescue of cognition in tau transgenic mice requires neuroprotection and reduced soluble tau burden. Mol Neurodegener 5:45.
22. Oz M, Lorke DE, Yang KHS, Petroianu G (2013). On the interaction of ?-Amyloid peptides and ?7-nicotinic acetylcholine receptors in Alzheimer's disease. Curr Alzheimer Res 10:618-630.
23. Peter C, Hongwan D, Küpfer A, Lauterburg BH (2000). Pharmacokinetics and organ distribution of intravenous and oral methylene blue. Eur J Clin Pharmacol 56:247-250.
24. Ramsay RR, Dunford C, Gillman PK (2007). Methylene blue and serotonin toxicity: inhibition of monoamine oxidase A (MAO A) confirms a theoretical prediction. Br J Pharmacol 152:946-951.
25. Ramsden M, Kotilinek L, Forster C, Paulson J, McGowan E, SantaCruz K, 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.
26. R Development Core Team (2004). R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available at: http://www.r-project.org [Accessed 20 February 2015].
27. Schirmer RH, Adler H, Pickhardt M, Mandelkow E (2011). "Lest we forget you-methylene blue...". Neurobiol Aging 32:2325.e7-16.
28. Spires-Jones TL, Friedman T, Pitstick R, Polydoro M, Roe A, Carlson GA, Hyman BT (2014). Methylene blue does not reverse existing neurofibrillary tangle pathology in the rTg4510 mouse model of tauopathy. Neurosci Lett 562:63-68.
29. Stack C, Jainuddin S, Elipenahli C, Gerges M, Starkova N, Starkov AA, et al. (2014). Methylene blue upregulates Nrf2/ARE genes and prevents tau-related neurotoxicity. Hum Mol Genet 23:3716-3732.
30. Traykov L, Raoux N, Latour F, Gallo L, Hanon O, Baudic S, et al. (2007). Executive functions deficit in mild cognitive impairment. Cogn Behav Neurol 20:219-224.
31. Visarius TM, Stucki JW, Lauterburg BH (1997). Stimulation of respiration by methylene blue in rat liver mitochondria. FEBS Lett 412:157-160.
32. Walker LC, Diamond MI, Duff KE, Hyman BT (2013). Mechanisms of protein seeding in neurodegenerative diseases. JAMA Neurol 70: 304-310.
33. Weiler M, Fukuda A, Massabki LH, Lopes TM, Franco AR, Damasceno BP, et al. (2014). Default mode, executive function, and language functional connectivity networks are compromised in mild Alzheimer's disease. Curr Alzheimer Res 11:274-282.
34. Wischik CM, Novak M, Thøgersen HC, Edwards PC, Runswick MJ, Jakes R, et al. (1988). Isolation of a fragment of tau derived from the core of the paired helical filament of Alzheimer disease. Proc Natl Acad Sci USA 85:4506-4510.
35. Wischik CM, Edwards PC, Lai RYK, Roth M, Harrington CR (1996). Selective inhibition of Alzheimer disease-like tau aggregation by phenothiazines. Proc Natl Acad Sci USA 93:11213-11218.
36. Wischik CM, Harrington CR, Storey JMD (2014). Tau-Aggregation inhibitor therapy for Alzheimer's disease. Biochem Pharmacol 88:529-539.
37. Wischik CM, Staff R,Wischik DJ, Bentham P, Murray A, Storey JMD, et al. (2015). Tau aggregation inhibitor therapy: an exploratory Phase 2 study in mild or moderate Alzheimer's disease. J Alzheimer's Dis 44:705-720.