Cholesterol-rich naked mole-rat brain lipid membranes are susceptible to amyloid beta-induced damage


Journal

Aging
ISSN: 1945-4589
Titre abrégé: Aging (Albany NY)
Pays: United States
ID NLM: 101508617

Informations de publication

Date de publication:
04 11 2020
Historique:
received: 03 08 2020
accepted: 03 10 2020
pubmed: 5 11 2020
medline: 24 4 2021
entrez: 4 11 2020
Statut: ppublish

Résumé

Naked mole-rats are extraordinarily long-lived rodents that offer unique opportunities to study the molecular origins of age-related neurodegenerative diseases. Remarkably, they do not accumulate amyloid plaques, even though their brains contain high concentrations of amyloid beta (Aβ) peptide from a young age. Therefore, they represent a particularly favourable organism to study the mechanisms of resistance against Aβ neurotoxicity. Here we examine the composition, phase behaviour, and Aβ interactions of naked mole-rat brain lipids. Relative to mouse, naked mole-rat brain lipids are rich in cholesterol and contain sphingomyelin in lower amounts and of shorter chain lengths. Proteins associated with the metabolism of ceramides, sphingomyelins and sphingosine-1-phosphate receptor 1 were also found to be decreased in naked mole-rat brain lysates. Correspondingly, we find that naked mole-rat brain lipid membranes exhibit a high degree of phase separation, with the liquid ordered phase extending to 80% of the supported lipid bilayer. These observations are consistent with the 'membrane pacemaker' hypothesis of ageing, according to which long-living species have lipid membranes particularly resistant to oxidative damage. We also found that exposure to Aβ disrupts naked mole-rat brain lipid membranes significantly, breaking the membrane into pieces while mouse brain derived lipids remain largely intact upon Aβ exposure.

Identifiants

pubmed: 33147569
pii: 202138
doi: 10.18632/aging.202138
pmc: PMC7695401
doi:

Substances chimiques

Amyloid beta-Peptides 0
Lipid Bilayers 0
Peptide Fragments 0
amyloid beta-protein (1-42) 0
Cholesterol 97C5T2UQ7J

Types de publication

Comparative Study Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

22266-22290

Subventions

Organisme : Cancer Research UK
ID : C56829/A22053
Pays : United Kingdom

Références

Neuroscience. 2019 Apr 15;404:165-174
pubmed: 30817953
Langmuir. 2014 Nov 25;30(46):13934-41
pubmed: 25360827
J Gerontol A Biol Sci Med Sci. 2006 Oct;61(10):1009-18
pubmed: 17077193
Langmuir. 2011 Feb 15;27(4):1308-13
pubmed: 21090659
Physiology (Bethesda). 2020 Mar 1;35(2):96-111
pubmed: 32024425
Front Neurosci. 2016 Nov 08;10:504
pubmed: 27877105
Nat Rev Neurosci. 2020 Jan;21(1):21-35
pubmed: 31780819
Proteomics. 2019 May;19(9):e1800432
pubmed: 30888112
Acta Neurol Scand Suppl. 2006;185:50-7
pubmed: 16866911
Physiol Rev. 2017 Apr;97(2):699-720
pubmed: 28202600
FEBS J. 2011 Oct;278(20):3905-17
pubmed: 21722314
Biomacromolecules. 2015 Mar 9;16(3):944-50
pubmed: 25689632
Nutr Neurosci. 2019 Jul;22(7):453-463
pubmed: 29325505
Elife. 2018 Jan 24;7:
pubmed: 29364116
Nanoscale. 2019 Nov 21;11(43):20857-20867
pubmed: 31657431
Exp Gerontol. 2007 Nov;42(11):1053-62
pubmed: 18029129
Biochim Biophys Acta. 2006 Dec;1763(12):1511-26
pubmed: 17027098
Biophys J. 2006 Mar 15;90(6):2086-92
pubmed: 16387761
J Biol Chem. 2017 Jan 27;292(4):1404-1413
pubmed: 27927987
Neurobiol Aging. 2013 Oct;34(10):2352-60
pubmed: 23618870
Biochim Biophys Acta. 2012 Sep;1822(9):1442-52
pubmed: 22627108
Biochim Biophys Acta Biomembr. 2018 Sep;1860(9):1652-1662
pubmed: 29526709
J Comp Physiol B. 2008 May;178(4):439-45
pubmed: 18180931
Biochim Biophys Acta. 2010 Apr;1798(4):741-9
pubmed: 20044974
Neurochem Res. 2001 Jul;26(7):771-82
pubmed: 11565608
Biochim Biophys Acta Biomembr. 2019 Sep 1;1861(9):1523-1532
pubmed: 31295476
Z Naturforsch C J Biosci. 2005 Jan-Feb;60(1-2):143-51
pubmed: 15787260
Nat Chem. 2018 Jun;10(6):673-683
pubmed: 29736006
Nano Lett. 2018 May 9;18(5):3271-3281
pubmed: 29644863
J Theor Biol. 2005 May 21;234(2):277-88
pubmed: 15757684
Neurobiol Pain. 2020 May 11;8:100047
pubmed: 32478202
Lab Invest. 2019 Jul;99(7):958-970
pubmed: 30760863
Biochim Biophys Acta. 2016 Dec;1858(12):3041-3049
pubmed: 27616046
Curr Neuropharmacol. 2009 Mar;7(1):65-74
pubmed: 19721819

Auteurs

Daniel Frankel (D)

School of Engineering, Newcastle University, Newcastle Upon Tyne NE1 7RU, UK.

Matthew Davies (M)

School of Engineering, Newcastle University, Newcastle Upon Tyne NE1 7RU, UK.

Bharat Bhushan (B)

School of Engineering, Newcastle University, Newcastle Upon Tyne NE1 7RU, UK.

Yavuz Kulaberoglu (Y)

Department of Pharmacology, University of Cambridge, Cambridge, CB2 1PD, UK.

Paulina Urriola-Munoz (P)

Department of Pharmacology, University of Cambridge, Cambridge, CB2 1PD, UK.

Justine Bertrand-Michel (J)

MetaToulLipidomics Facility, INSERM UMR1048, Toulouse, France.

Melissa R Pergande (MR)

Department of Chemistry, University of Illinois at Chicago, Chicago, IL 60607, USA.

Andrew A Smith (AA)

Centre for Misfolding Diseases, Department of Chemistry, University of Cambridge, Cambridge, CB2 1EW, UK.

Swapan Preet (S)

Centre for Misfolding Diseases, Department of Chemistry, University of Cambridge, Cambridge, CB2 1EW, UK.

Thomas J Park (TJ)

Department of Biological Sciences, University of Illinois at Chicago, Chicago, IL 60607, USA.

Michele Vendruscolo (M)

Centre for Misfolding Diseases, Department of Chemistry, University of Cambridge, Cambridge, CB2 1EW, UK.

Kenneth S Rankin (KS)

Translational and Clinical Research Institute, Newcastle University, Paul O'Gorman Building, Framlington Place, Newcastle upon Tyne, NE2 4HH, UK.

Stephanie M Cologna (SM)

Department of Chemistry, University of Illinois at Chicago, Chicago, IL 60607, USA.

Janet R Kumita (JR)

Department of Pharmacology, University of Cambridge, Cambridge, CB2 1PD, UK.
Centre for Misfolding Diseases, Department of Chemistry, University of Cambridge, Cambridge, CB2 1EW, UK.

Nicolas Cenac (N)

IRSD, INSERM, INRA, INP-ENVT, Toulouse University 3 Paul Sabatier, Toulouse, France.

Ewan St John Smith (E)

Department of Pharmacology, University of Cambridge, Cambridge, CB2 1PD, UK.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH