Monoamine oxidase B is elevated in Alzheimer disease neurons, is associated with γ-secretase and regulates neuronal amyloid β-peptide levels

Alzheimer's Research and Therapy

Volumn 9, Issue 1, 2017, Pages

  Schedin Weiss, Sophia ^a   Inoue, Mitsuhiro ^a,b   Hromadkova, Lenka ^c,d   Teranishi, Yasuhiro ^a,b   Yamamoto, Natsuko Goto ^a,b   Wiehager, Birgitta ^a   Bogdanovic, Nenad ^e   Winblad, Bengt ^a   Sandebring Matton, Anna ^a   Frykman, Susanne ^a   Tjernberg, Lars O ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b DAINIPPON SUMITOMO PHARMA CO LTD   (Japan)

^c NATIONAL INSTITUTE OF MENTAL HEALTH   (Czech Republic)

^d CHARLES UNIVERSITY   (Czech Republic)

^e UNIVERSITY OF OSLO   (Norway)

Author keywords

Alzheimer disease; Alzheimer disease pathogenesis; Amyloid peptide; Intraneuronal amyloid peptide; Monoamine oxidase B; Secretase

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME B; AMYLOID BETA PROTEIN; GAMMA SECRETASE; NOTCH RECEPTOR; AMINE OXIDASE (FLAVIN CONTAINING); N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NR2B NMDA RECEPTOR; PRESENILIN 1; SECRETASE; SMALL INTERFERING RNA;

ADULT; AGED; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CELL CULTURE; BRAIN HOMOGENATE; BRAIN NERVE CELL; CELL LEVEL; CONFOCAL MICROSCOPY; ENTORHINAL CORTEX; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; FRONTAL CORTEX; GENE OVEREXPRESSION; GENE SILENCING; GLIA CELL; HIPPOCAMPAL CA1 REGION; HUMAN; HUMAN TISSUE; IMAGE ANALYSIS; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MALE; MASS SPECTROMETRY; MIDDLE AGED; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PYRAMIDAL NERVE CELL; QUANTITATIVE ANALYSIS; SINGLE CELL ANALYSIS; STAINING; VERY ELDERLY; WESTERN BLOTTING; ANIMAL; AXON; BRAIN; DENDRITE; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; MOLECULAR MODEL; NERVE CELL; PATHOLOGY; RAT; SYNAPSE; TRANSFORMED CELL LINE; ULTRASTRUCTURE;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; AXONS; BRAIN; CELL LINE, TRANSFORMED; DENDRITES; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MALE; MICE; MIDDLE AGED; MODELS, MOLECULAR; MONOAMINE OXIDASE; NEURONS; PRESENILIN-1; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, SMALL INTERFERING; SYNAPSES; TRANSFECTION;

EID: 85026547521     PISSN: None     EISSN: 17589193     Source Type: Journal    
DOI: 10.1186/s13195-017-0279-1     Document Type: Article

References (40)

1. Winblad B, Amouyel P, Andrieu S, Ballard C, Brayne C, Brodaty H, Cedazo-Minguez A, Dubois B, Edvardsson D, Feldman H, et al. Defeating Alzheimer's disease and other dementias: a priority for European science and society. Lancet Neurol. 2016;15(5):455-532.
2. Steiner H, Fluhrer R, Haass C. Intramembrane proteolysis by gamma-secretase. J Biol Chem. 2008;283(44):29627-31.
3. Willem M, Lammich S, Haass C. Function, regulation and therapeutic properties of beta-secretase (BACE1). Semin Cell Dev Biol. 2009;20(2):175-82.
4. Bai XC, Yan C, Yang G, Lu P, Ma D, Sun L, Zhou R, Scheres SH, Shi Y. An atomic structure of human gamma-secretase. Nature. 2015;525(7568):212-7.
5. Jan A, Hartley DM, Lashuel HA. Preparation and characterization of toxic Abeta aggregates for structural and functional studies in Alzheimer's disease research. Nat Protoc. 2010;5(6):1186-209.
6. Söderberg L, Bogdanovic N, Axelsson B, Winblad B, Naslund J, Tjernberg LO. Analysis of single Alzheimer solid plaque cores by laser capture microscopy and nanoelectrospray/tandem mass spectrometry. Biochemistry. 2006;45(32):9849-56.
7. Kretner B, Trambauer J, Fukumori A, Mielke J, Kuhn PH, Kremmer E, Giese A, Lichtenthaler SF, Haass C, Arzberger T, et al. Generation and deposition of Abeta43 by the virtually inactive presenilin-1 L435F mutant contradicts the presenilin loss-of-function hypothesis of Alzheimer's disease. EMBO Mol Med. 2016;8(5):458-65.
8. Aoki M, Volkmann I, Tjernberg LO, Winblad B, Bogdanovic N. Amyloid beta-peptide levels in laser capture microdissected cornu ammonis 1 pyramidal neurons of Alzheimer's brain. Neuroreport. 2008;19(11):1085-9.
9. Hashimoto M, Bogdanovic N, Volkmann I, Aoki M, Winblad B, Tjernberg LO. Analysis of microdissected human neurons by a sensitive ELISA reveals a correlation between elevated intracellular concentrations of Abeta42 and Alzheimer's disease neuropathology. Acta Neuropathol. 2010;119(5):543-54.
10. Jack Jr CR, Knopman DS, Jagust WJ, Petersen RC, Weiner MW, Aisen PS, Shaw LM, Vemuri P, Wiste HJ, Weigand SD, et al. Tracking pathophysiological processes in Alzheimer's disease: an updated hypothetical model of dynamic biomarkers. Lancet Neurol. 2013;12(2):207-16.
11. Scheltens P, Blennow K, Breteler MM, de Strooper B, Frisoni GB, Salloway S, Van der Flier WM. Alzheimer's disease. Lancet. 2016;388(10043):505-17.
12. De Strooper B, Annaert W, Cupers P, Saftig P, Craessaerts K, Mumm JS, Schroeter EH, Schrijvers V, Wolfe MS, Ray WJ, et al. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature. 1999;398(6727):518-22.
13. De Kloe GE, De Strooper B. Small molecules that inhibit Notch signaling. Methods Mol Biol. 2014;1187:311-22.
14. Winblad B, Gottfries CG, Oreland L, Wiberg A. Monoamine oxidase in platelets and brains of non-psychiatric and non-neurological geriatric patients. Med Biol. 1979;57(2):129-32.
15. Adolfsson R, Gottfries CG, Oreland L, Wiberg A, Winblad B. Increased activity of brain and platelet monoamine oxidase in dementia of Alzheimer type. Life Sci. 1980;27(12):1029-34.
16. Rodriguez-Vieitez E, Saint-Aubert L, Carter SF, Almkvist O, Farid K, Scholl M, Chiotis K, Thordardottir S, Graff C, Wall A, et al. Diverging longitudinal changes in astrocytosis and amyloid PET in autosomal dominant Alzheimer's disease. Brain. 2016;139(Pt 3):922-36.
17. Frykman S, Teranishi Y, Hur JY, Sandebring A, Yamamoto NG, Tjernberg LO. Identification of two novel synaptic gamma-secretase associated proteins that affect amyloid beta-peptide levels without altering Notch processing. Neurochem Int. 2012;61(1):108-18.
18. Teranishi Y, Hur JY, Welander H, Franberg J, Aoki M, Tjernberg LO. Affinity pulldown of gamma-secretase and associated proteins from human and rat brain. J Cell Mol Med. 2010;14(11):2675-86.
19. Hur JY, Teranishi Y, Kihara T, Yamamoto NG, Inoue M, Tjernberg LO. Identification of novel gamma-secretase-associated proteins in detergent-resistant membranes from brain. J Biol Chem. 2012;287(15):11991-2005.
20. Teranishi Y, Inoue M, Yamamoto NG, Kihara T, Wiehager B, Ishikawa T, Winblad B, Schedin-Weiss S, Frykman S, Tjernberg LO. Proton myo-inositol cotransporter is a novel gamma-secretase associated protein that regulates Abeta production without affecting Notch cleavage. FEBS J. 2015;282(17):3438-51.
21. Fath T, Ke YD, Gunning P, Gotz J, Ittner LM. Primary support cultures of hippocampal and substantia nigra neurons. Nat Protoc. 2009;4(1):78-85.
22. Schedin-Weiss S, Inoue M, Teranishi Y, Yamamoto NG, Karlstrom H, Tjernberg LO. Visualizing active enzyme complexes using a photoreactive inhibitor for proximity ligation - application on gamma-secretase. PLoS One. 2013;8(5), e63962.
23. Soderberg O, Gullberg M, Jarvius M, Ridderstrale K, Leuchowius KJ, Landegren U. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods. 2006;3(12):995-1000.
24. Schedin-Weiss S, Caesar I, Winblad B, Blom H, Tjernberg LO. Super-resolution microscopy reveals gamma-secretase at both sides of the neuronal synapse. Acta Neuropathol Commun. 2016;4:29.
25. Inoue M, Hur JY, Kihara T, Teranishi Y, Yamamoto NG, Ishikawa T, Wiehager B, Winblad B, Tjernberg LO, Schedin-Weiss S. Human brain proteins showing neuron-specific interactions with gamma-secretase. FEBS J. 2015;282(14):2587-99.
26. Donoviel DB, Hadjantonakis AK, Ikeda M, Zheng H, Hyslop PS, Bernstein A. Mice lacking both presenilin genes exhibit early embryonic patterning defects. Genes Dev. 1999;13(21):2801-10.
27. Dani A, Huang B, Bergan J, Dulac C, Zhuang X. Superresolution imaging of chemical synapses in the brain. Neuron. 2010;68(5):843-56.
28. Saura J, Luque JM, Cesura AM, Da Prada M, Chan-Palay V, Huber G, Loffler J, Richards JG. Increased monoamine oxidase B activity in plaque-associated astrocytes of Alzheimer brains revealed by quantitative enzyme radioautography. Neuroscience. 1994;62(1):15-30.
29. Mousseau DD, Baker GB. Recent developments in the regulation of monoamine oxidase form and function: is the current model restricting our understanding of the breadth of contribution of monoamine oxidase to brain [dys]function? Curr Top Med Chem. 2012;12(20):2163-76.
30. Haass C, Kaether C, Thinakaran G, Sisodia S. Trafficking and proteolytic processing of APP. Cold Spring Harbor Perspect Med. 2012;2(5):a006270.
31. Area-Gomez E, Schon EA. Mitochondria-associated ER membranes and Alzheimer disease. Curr Opin Genet Dev. 2016;38:90-6.
32. Schreiner B, Hedskog L, Wiehager B, Ankarcrona M. Amyloid-beta peptides are generated in mitochondria-associated endoplasmic reticulum membranes. J Alzheimers Dis. 2015;43(2):369-74.
33. Binda C, Mattevi A, Edmondson DE. Structural properties of human monoamine oxidases A and B. Int Rev Neurobiol. 2011;100:1-11.
34. Bar-Am O, Amit T, Weinreb O, Youdim MB, Mandel S. Propargylamine containing compounds as modulators of proteolytic cleavage of amyloid-beta protein precursor: involvement of MAPK and PKC activation. J Alzheimers Dis. 2010;21(2):361-71.
35. Bar-Am O, Yogev-Falach M, Amit T, Sagi Y, Youdim MB. Regulation of protein kinase C by the anti-Parkinson drug, MAO-B inhibitor, rasagiline and its derivatives, in vivo. J Neurochem. 2004;89(5):1119-25.
36. Lingor P, Michel U, Scholl U, Bahr M, Kugler S. Transfection of "naked" siRNA results in endosomal uptake and metabolic impairment in cultured neurons. Biochem Biophys Res Commun. 2004;315(4):1126-33.
37. Carter SF, Scholl M, Almkvist O, Wall A, Engler H, Langstrom B, Nordberg A. Evidence for astrocytosis in prodromal Alzheimer disease provided by 11C-deuterium-L-deprenyl: a multitracer PET paradigm combining 11C-Pittsburgh compound B and 18 F-FDG. J Nucl Med. 2012;53(1):37-46.
38. Scholl M, Carter SF, Westman E, Rodriguez-Vieitez E, Almkvist O, Thordardottir S, Wall A, Graff C, Langstrom B, Nordberg A. Early astrocytosis in autosomal dominant Alzheimer's disease measured in vivo by multi-tracer positron emission tomography. Sci Rep. 2015;5:16404.
39. Sano M, Ernesto C, Thomas RG, Klauber MR, Schafer K, Grundman M, Woodbury P, Growdon J, Cotman CW, Pfeiffer E, et al. A controlled trial of selegiline, alpha-tocopherol, or both as treatment for Alzheimer's disease. The Alzheimer's Disease Cooperative Study. N Engl J Med. 1997;336(17):1216-22.
40. Naoi M, Maruyama W. Monoamine oxidase inhibitors as neuroprotective agents in age-dependent neurodegenerative disorders. Curr Pharm Des. 2010;16(25):2799-817.