nach oben

Journal of Neural Transmission

Erschienen in:

29.08.2019 | Psychiatry and Preclinical Psychiatric Studies - Original Article

Trehalose as glucose surrogate in proliferation and cellular mobility of adult neural progenitor cells derived from mouse hippocampus

verfasst von: Alexandra Bertl, Victor Brantl, Norbert Scherbaum, Dan Rujescu, Jens Benninghoff

Erschienen in: Journal of Neural Transmission | Ausgabe 11/2019

Einloggen, um Zugang zu erhalten

Abstract

The disaccharide trehalose (TRE) represents a natural energy supply for distinct non-mammalian species. Evidence has shown that TRE impacts on various properties including the stabilization of protein structure and cell membranes, which are important neuroprotective features against neurodegeneration. In this study, we tested the specific effect of TRE on cell proliferation and mobilization using an established experimental paradigm of adult neural progenitor cells (NPCs) derived from murine hippocampus. NPC proliferation, both measured by growth curve analysis over 25 days and by bromodeoxyuridine (BrdU) incorporation, was not altered by adding TRE instead of GLC to the culture media. Using Boyden chamber experiments, the mobility in regular glucose-containing media did not differ from glucose-free TRE-supplemented media. Our observation suggests that TRE has the capacity to replace glucose (GLC) as energy source in neural cells in our experimental paradigm.

Aguib Y, Heiseke A, Gilch S, Riemer C, Baier M, Schatzl HM, Ertmer A (2009) Autophagy induction by trehalose counteracts cellular prion infection. Autophagy 5(3):361–369CrossRefPubMed

Alvarez EO, Beauquis J, Revsin Y, Banzan AM, Roig P, De Nicola AF, Saravia F (2009) Cognitive dysfunction and hippocampal changes in experimental type 1 diabetes. Behav Brain Res 198(1):224–230. https://doi.org/10.1016/j.bbr.2008.11.001 CrossRefPubMed

Arai C, Kohguchi M, Akamatsu S, Arai N, Yoshizane C, Hasegawa N, Hanaya T, Arai S, Ikeda M, Kurimoto M (2001) Trehalose suppresses lipopolysaccharide-induced osteoclastogenesis bone marrow in mice. Nutr Res 21(7):993–999CrossRefPubMed

Beal MF (2005) Oxidative damage as an early marker of Alzheimer’s disease and mild cognitive impairment. Neurobiol Aging 26(5):585–586. https://doi.org/10.1016/j.neurobiolaging.2004.09.022 CrossRefPubMed

Benninghoff J, Gritti A, Rizzi M, Lamorte G, Schloesser RJ, Schmitt A, Robel S, Genius J, Moessner R, Riederer P, Manji HK, Grunze H, Rujescu D, Moeller HJ, Lesch KP, Vescovi AL (2010) Serotonin depletion hampers survival and proliferation in neurospheres derived from adult neural stem cells. Neuropsychopharmacology 35(4):893–903. https://doi.org/10.1038/npp.2009.181 CrossRefPubMed

Beranger F, Crozet C, Goldsborough A, Lehmann S (2008) Trehalose impairs aggregation of PrPSc molecules and protects prion-infected cells against oxidative damage. Biochem Biophys Res Commun 374(1):44–48. https://doi.org/10.1016/j.bbrc.2008.06.094 CrossRefPubMed

Butterfield DA (2002) Amyloid beta-peptide (1–42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer’s disease brain. A review. Free Radic Res 36(12):1307–1313CrossRefPubMed

Collins J, Robinson C, Danhof H, Knetsch CW, van Leeuwen HC, Lawley TD, Auchtung JM, Britton RA (2018) Dietary trehalose enhances virulence of epidemic Clostridium difficile. Nature 553(7688):291–294. https://doi.org/10.1038/nature25178 CrossRefPubMedPubMedCentral

DeBosch BJ, Heitmeier MR, Mayer AL, Higgins CB, Crowley JR, Kraft TE, Chi M, Newberry EP, Chen Z, Finck BN, Davidson NO, Yarasheski KE, Hruz PW, Moley KH (2016) Trehalose inhibits solute carrier 2A (SLC2A) proteins to induce autophagy and prevent hepatic steatosis. Sci Signal 9(416):ra21. https://doi.org/10.1126/scisignal.aac5472 CrossRefPubMedPubMedCentral

Elbein AD (1974) The metabolism of alpha, alpha-trehalose. Adv Carbohydr Chem Biochem 30:227–256CrossRefPubMed

Feinkohl I, Price JF, Strachan MW, Frier BM (2015) The impact of diabetes on cognitive decline: potential vascular, metabolic, and psychosocial risk factors. Alzheimers Res Ther 7(1):46. https://doi.org/10.1186/s13195-015-0130-5 CrossRefPubMedPubMedCentral

Ferrari D, Binda E, De Filippis L, Vescovi AL (2010) Isolation of neural stem cells from neural tissues using the neurosphere technique. Curr Protoc Stem Cell Biol Chapter 2(Unit2D):6. https://doi.org/10.1002/9780470151808.sc02d06s15 CrossRefPubMed

Galli R, Gritti A, Vescovi AL (2008) Adult neural stem cells. Methods Mol Biol 438:67–84. https://doi.org/10.1007/978-1-59745-133-8_7 CrossRefPubMed

Halbe L, Rami A (2019) Trehalase localization in the cerebral cortex, hippocampus and cerebellum of mouse brains. J Adv Res 18:71–79. https://doi.org/10.1016/j.jare.2019.01.009 CrossRefPubMedPubMedCentral

Iturriaga G, Suarez R, Nova-Franco B (2009) Trehalose metabolism: from osmoprotection to signaling. Int J Mol Sci 10(9):3793–3810. https://doi.org/10.3390/ijms10093793 CrossRefPubMedPubMedCentral

Jacobson AM, Musen G, Ryan CM, Silvers N, Cleary P, Waberski B, Burwood A, Weinger K, Bayless M, Dahms W, Harth J (2007) Long-term effect of diabetes and its treatment on cognitive function. N Engl J Med 356(18):1842–1852. https://doi.org/10.1056/NEJMoa066397 CrossRefPubMed

Jain NK, Roy I (2008) Role of trehalose in moisture-induced aggregation of bovine serum albumin. Eur J Pharm Biopharm 69(3):824–834. https://doi.org/10.1016/j.ejpb.2008.01.032 CrossRefPubMed

Jessberger S, Gage FH (2014) Adult neurogenesis: bridging the gap between mice and humans. Trends Cell Biol 24(10):558–563. https://doi.org/10.1016/j.tcb.2014.07.003 CrossRefPubMed

Jonsson KI (2007) Tardigrades as a potential model organism in space research. Astrobiology 7(5):757–766. https://doi.org/10.1089/ast.2006.0088 CrossRefPubMed

Kara NZ, Toker L, Agam G, Anderson GW, Belmaker RH, Einat H (2013) Trehalose induced antidepressant-like effects and autophagy enhancement in mice. Psychopharmacology 229(2):367–375. https://doi.org/10.1007/s00213-013-3119-4 CrossRefPubMed

Kempermann G, Kronenberg G (2003) Depressed new neurons–adult hippocampal neurogenesis and a cellular plasticity hypothesis of major depression. Biol Psychiatry 54(5):499–503CrossRefPubMed

Kruger U, Wang Y, Kumar S, Mandelkow EM (2012) Autophagic degradation of tau in primary neurons and its enhancement by trehalose. Neurobiol Aging 33(10):2291–2305. https://doi.org/10.1016/j.neurobiolaging.2011.11.009 CrossRefPubMed

Lazarov O, Marr RA (2010) Neurogenesis and Alzheimer’s disease: at the crossroads. Exp Neurol 223(2):267–281. https://doi.org/10.1016/j.expneurol.2009.08.009 CrossRefPubMed

Liu R, Barkhordarian H, Emadi S, Park CB, Sierks MR (2005) Trehalose differentially inhibits aggregation and neurotoxicity of beta-amyloid 40 and 42. Neurobiol Dis 20(1):74–81. https://doi.org/10.1016/j.nbd.2005.02.003 CrossRefPubMed

Mardones P, Rubinsztein DC, Hetz C (2016) Mystery solved: trehalose kickstarts autophagy by blocking glucose transport. Sci Signal 9(416):fs2. https://doi.org/10.1126/scisignal.aaf1937 CrossRefPubMed

Martano G, Gerosa L, Prada I, Garrone G, Krogh V, Verderio C, Passafaro M (2017) Biosynthesis of astrocytic trehalose regulates neuronal arborization in hippocampal neurons. ACS Chem Neurosci 8(9):1865–1872. https://doi.org/10.1021/acschemneuro.7b00177 CrossRefPubMed

Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223–250. https://doi.org/10.1146/annurev.neuro.28.051804.101459 CrossRefPubMed

Oesterreicher TJ, Markesich DC, Henning SJ (2001) Cloning, characterization and mapping of the mouse trehalase (Treh) gene. Gene 270(1–2):211–220CrossRefPubMed

Pereira CS, Lins RD, Chandrasekhar I, Freitas LC, Hunenberger PH (2004) Interaction of the disaccharide trehalose with a phospholipid bilayer: a molecular dynamics study. Biophys J 86(4):2273–2285. https://doi.org/10.1016/S0006-3495(04)74285-X CrossRefPubMedPubMedCentral

Richards AB, Krakowka S, Dexter LB, Schmid H, Wolterbeek AP, Waalkens-Berendsen DH, Shigoyuki A, Kurimoto M (2002) Trehalose: a review of properties, history of use and human tolerance, and results of multiple safety studies. Food Chem Toxicol 40(7):871–898CrossRefPubMed

Riederer P, Korczyn AD, Ali SS, Bajenaru O, Choi MS, Chopp M, Dermanovic-Dobrota V, Grunblatt E, Jellinger KA, Kamal MA, Kamal W, Leszek J, Sheldrick-Michel TM, Mushtaq G, Meglic B, Natovich R, Pirtosek Z, Rakusa M, Salkovic-Petrisic M, Schmidt R, Schmitt A, Sridhar GR, Vecsei L, Wojszel ZB, Yaman H, Zhang ZG, Cukierman-Yaffe T (2017) The diabetic brain and cognition. J Neural Transm (Vienna) 124(11):1431–1454. https://doi.org/10.1007/s00702-017-1763-2 CrossRef

Rodriguez-Navarro JA, Rodriguez L, Casarejos MJ, Solano RM, Gomez A, Perucho J, Cuervo AM, Garcia de Yebenes J, Mena MA (2010) Trehalose ameliorates dopaminergic and tau pathology in parkin deleted/tau overexpressing mice through autophagy activation. Neurobiol Dis 39(3):423–438. https://doi.org/10.1016/j.nbd.2010.05.014 CrossRefPubMed

Sacktor B, Berger SJ (1969) Formation of trehalose from glucose in the renal cortex. Biochem Biophys Res Commun 35(6):796–800CrossRefPubMed

Samuels BA, Mendez-David I, Faye C, David SA, Pierz KA, Gardier AM, Hen R, David DJ (2016) Serotonin 1A and serotonin 4 receptors: essential mediators of the neurogenic and behavioral actions of antidepressants. Neuroscientist 22(1):26–45. https://doi.org/10.1177/1073858414561303 CrossRefPubMed

Sarkar S, Davies JE, Huang Z, Tunnacliffe A, Rubinsztein DC (2007) Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and alpha-synuclein. J Biol Chem 282(8):5641–5652. https://doi.org/10.1074/jbc.M609532200 CrossRefPubMed

Snyder JS (2019) Recalibrating the relevance of adult neurogenesis. Trends Neurosci 42(3):164–178. https://doi.org/10.1016/j.tins.2018.12.001 CrossRefPubMed

Tanaka M, Machida Y, Niu S, Ikeda T, Jana NR, Doi H, Kurosawa M, Nekooki M, Nukina N (2004) Trehalose alleviates polyglutamine-mediated pathology in a mouse model of Huntington disease. Nat Med 10(2):148–154. https://doi.org/10.1038/nm985 CrossRefPubMed

van der Ven AT, Pape JC, Hermann D, Schloesser R, Genius J, Fischer N, Mossner R, Scherbaum N, Wiltfang J, Rujescu D, Benninghoff J (2017) Methylene blue (tetramethylthionine chloride) influences the mobility of adult neural stem cells: a potentially novel therapeutic mechanism of a therapeutic approach in the treatment of Alzheimer’s disease. J Alzheimers Dis 57(2):531–540. https://doi.org/10.3233/JAD-160755 CrossRefPubMed

Venables MC, Brouns F, Jeukendrup AE (2008) Oxidation of maltose and trehalose during prolonged moderate-intensity exercise. Med Sci Sports Exerc 40(9):1653–1659. https://doi.org/10.1249/MSS.0b013e318175716c CrossRefPubMed

Willette AA, Johnson SC, Birdsill AC, Sager MA, Christian B, Baker LD, Craft S, Oh J, Statz E, Hermann BP, Jonaitis EM, Koscik RL, La Rue A, Asthana S, Bendlin BB (2015a) Insulin resistance predicts brain amyloid deposition in late middle-aged adults. Alzheimers Dement 11(5):504–510e501. https://doi.org/10.1016/j.jalz.2014.03.011 CrossRefPubMed

Willette AA, Modanlo N, Kapogiannis D, Alzheimer’s Disease Neuroimaging I (2015b) Insulin resistance predicts medial temporal hypermetabolism in mild cognitive impairment conversion to Alzheimer disease. Diabetes 64(6):1933–1940. https://doi.org/10.2337/db14-1507 CrossRefPubMedPubMedCentral

Wolkers WF, Walker NJ, Tablin F, Crowe JH (2001) Human platelets loaded with trehalose survive freeze-drying. Cryobiology 42(2):79–87. https://doi.org/10.1006/cryo.2001.2306 CrossRefPubMed

Yang CR, Yu RK (2009) Intracerebral transplantation of neural stem cells combined with trehalose ingestion alleviates pathology in a mouse model of Huntington’s disease. J Neurosci Res 87(1):26–33. https://doi.org/10.1002/jnr.21817 CrossRefPubMedPubMedCentral

Yoshizane C, Mizote A, Yamada M, Arai N, Arai S, Maruta K, Mitsuzumi H, Ariyasu T, Ushio S, Fukuda S (2017) Glycemic, insulinemic and incretin responses after oral trehalose ingestion in healthy subjects. Nutr J 16(1):9. https://doi.org/10.1186/s12937-017-0233-x CrossRefPubMedPubMedCentral

Titel: Trehalose as glucose surrogate in proliferation and cellular mobility of adult neural progenitor cells derived from mouse hippocampus
verfasst von: Alexandra Bertl
Victor Brantl
Norbert Scherbaum
Dan Rujescu
Jens Benninghoff
Publikationsdatum: 29.08.2019
Verlag: Springer Vienna
Erschienen in: Journal of Neural Transmission / Ausgabe 11/2019
Print ISSN: 0300-9564
Elektronische ISSN: 1435-1463
DOI: https://doi.org/10.1007/s00702-019-02070-4

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

23.04.2024 | Demenz | Nachrichten

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Trehalose as glucose surrogate in proliferation and cellular mobility of adult neural progenitor cells derived from mouse hippocampus

Abstract

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Demenzkranke durch Antipsychotika vielfach gefährdet

Parkinson-Therapie im Wandel – aktuelle Leitlinie im Fokus

Auf diese Krankheiten bei Geflüchteten sollten Sie vorbereitet sein

Hustenstiller lindert Agitation bei Alzheimer

Update Neurologie

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 11/2019

FGF2 and dual agonist of NCAM and FGF receptor 1, Enreptin, rescue neurite outgrowth loss in hippocampal neurons expressing mutated huntingtin proteins

Motor and non-motor function predictors of mortality in Parkinson’s disease

Early detection of cognitive impairment in Parkinson’s disease with the use of the Wisconsin Card Sorting Test: correlations with Montreal Cognitive Assessment and smell identification test

“New methods of assessing autonomic disorders in Parkinson disease patients: skin-galvanic reaction”

Animal models of major depression: drawbacks and challenges

Characteristics and progression of cognitive deficits in progressive supranuclear palsy vs. multiple system atrophy and Parkinson’s disease

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Demenzkranke durch Antipsychotika vielfach gefährdet

Parkinson-Therapie im Wandel – aktuelle Leitlinie im Fokus

Auf diese Krankheiten bei Geflüchteten sollten Sie vorbereitet sein

Hustenstiller lindert Agitation bei Alzheimer

Update Neurologie