Cyclized NDGA modifies dynamic α-synuclein monomers preventing aggregation and toxicity.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
27 02 2019
Historique:
received: 22 10 2018
accepted: 04 01 2019
entrez: 1 3 2019
pubmed: 1 3 2019
medline: 17 9 2020
Statut: epublish

Résumé

Growing evidence implicates α-synuclein aggregation as a key driver of neurodegeneration in Parkinson's disease (PD) and other neurodegenerative disorders. Herein, the molecular and structural mechanisms of inhibiting α-synuclein aggregation by novel analogs of nordihydroguaiaretic acid (NDGA), a phenolic dibenzenediol lignan, were explored using an array of biochemical and biophysical methodologies. NDGA analogs induced modest, progressive compaction of monomeric α-synuclein, preventing aggregation into amyloid-like fibrils. This conformational remodeling preserved the dynamic adoption of α-helical conformations, which are essential for physiological membrane interactions. Oxidation-dependent NDGA cyclization was required for the interaction with monomeric α-synuclein. NDGA analog-pretreated α-synuclein did not aggregate even without NDGA-analogs in the aggregation mixture. Strikingly, NDGA-pretreated α-synuclein suppressed aggregation of naïve untreated aggregation-competent monomeric α-synuclein. Further, cyclized NDGA reduced α-synuclein-driven neurodegeneration in Caenorhabditis elegans. The cyclized NDGA analogs may serve as a platform for the development of small molecules that stabilize aggregation-resistant α-synuclein monomers without interfering with functional conformations yielding potential therapies for PD and related disorders.

Identifiants

pubmed: 30814575
doi: 10.1038/s41598-019-39480-z
pii: 10.1038/s41598-019-39480-z
pmc: PMC6393491
doi:

Substances chimiques

Amyloid 0
Phospholipids 0
alpha-Synuclein 0
Masoprocol 7BO8G1BYQU

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

2937

Subventions

Organisme : NINDS NIH HHS
ID : R01 NS081033
Pays : United States
Organisme : NINDS NIH HHS
ID : R56 NS081033
Pays : United States
Organisme : NIA NIH HHS
ID : T32 AG000255
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM008076
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS079955
Pays : United States

Références

Acta Neuropathol. 2018 Jan;135(1):65-83
pubmed: 29209768
Proc Natl Acad Sci U S A. 2014 Oct 7;111(40):E4274-83
pubmed: 25246573
J Am Soc Mass Spectrom. 2017 Jan;28(1):21-28
pubmed: 27730522
Neuroscience. 2015 Feb 12;286:383-92
pubmed: 25498223
Science. 1997 Jun 27;276(5321):2045-7
pubmed: 9197268
Curr Opin Genet Dev. 2017 Jun;44:102-109
pubmed: 28242493
Biophys J. 2018 Jan 9;114(1):53-64
pubmed: 29320696
Neurotherapeutics. 2012 Apr;9(2):464-76
pubmed: 22373667
Proc Natl Acad Sci U S A. 2011 Mar 8;108(10):4194-9
pubmed: 21325059
Cell Mol Life Sci. 2000 Dec;57(13-14):1894-908
pubmed: 11215516
Acta Neuropathol. 2013 Jun;125(6):795-813
pubmed: 23604588
Hum Mol Genet. 2017 Sep 15;26(18):3466-3481
pubmed: 28911198
J Am Chem Soc. 2006 Aug 2;128(30):9893-901
pubmed: 16866548
Protein Expr Purif. 2005 Jul;42(1):173-7
pubmed: 15939304
Biochemistry. 2004 Mar 30;43(12):3704-15
pubmed: 15035641
Adv Exp Med Biol. 2015;870:49-122
pubmed: 26387100
Neuroreport. 2000 Jan 17;11(1):211-3
pubmed: 10683860
J Biol Chem. 2014 Aug 1;289(31):21299-310
pubmed: 24907278
Science. 2003 Oct 31;302(5646):841
pubmed: 14593171
Nat Commun. 2014 Dec 19;5:5857
pubmed: 25524885
Biophys J. 2006 Jun 15;90(12):4692-700
pubmed: 16581836
Free Radic Biol Med. 2012 Mar 1;52(5):850-9
pubmed: 22226831
Neurosci Lett. 1997 Dec 12;239(1):45-8
pubmed: 9547168
Brain Res. 2016 Nov 15;1651:17-26
pubmed: 27639810
J Neurosci. 2010 Sep 15;30(37):12535-44
pubmed: 20844148
Science. 2012 Nov 16;338(6109):949-53
pubmed: 23161999
Proc Natl Acad Sci U S A. 2010 Nov 9;107(45):19573-8
pubmed: 20974939
Ann Neurol. 2014 Mar;75(3):351-62
pubmed: 24243558
J Am Chem Soc. 2009 Jun 3;131(21):7390-401
pubmed: 19432426
J Biol Chem. 2005 Dec 30;280(52):43179-87
pubmed: 16166095
Food Chem Toxicol. 2010 Jan;48(1):409-16
pubmed: 19883714
J Biol Chem. 2003 May 9;278(19):16873-7
pubmed: 12621030
Nat Commun. 2015 Jun 16;6:7314
pubmed: 26076669
Neuron. 2005 Jun 16;46(6):857-68
pubmed: 15953415
J Neurosci. 2006 Nov 15;26(46):11915-22
pubmed: 17108165
J Neurosci. 2007 Aug 22;27(34):9220-32
pubmed: 17715357
Lancet. 1998 Aug 15;352(9127):547-8
pubmed: 9716068
Nat Genet. 1998 Feb;18(2):106-8
pubmed: 9462735
Lancet. 2004 Sep 25-Oct 1;364(9440):1167-9
pubmed: 15451224
J Clin Invest. 2015 Jul 1;125(7):2721-35
pubmed: 26075822
Neurology. 2013 Mar 12;80(11):1062-4
pubmed: 23427326
Biochemistry. 2013 Oct 8;52(40):6925-7
pubmed: 24047453
Proc Natl Acad Sci U S A. 1998 May 26;95(11):6469-73
pubmed: 9600990
Biochem J. 2017 Jun 6;474(12):2039-2049
pubmed: 28495859
Cell Death Differ. 1998 Oct;5(10):832-7
pubmed: 10203692
Proc Natl Acad Sci U S A. 2008 Jan 15;105(2):728-33
pubmed: 18182484
J Neural Transm (Vienna). 2016 Apr;123(4):439-45
pubmed: 26809243
Proc Natl Acad Sci U S A. 2010 Apr 27;107(17):7710-5
pubmed: 20385841
Nature. 2016 Feb 4;530(7588):45-50
pubmed: 26808899
Nature. 1997 Aug 28;388(6645):839-40
pubmed: 9278044
J Biol Chem. 2010 May 14;285(20):14941-54
pubmed: 20150427
Neurosci Lett. 1998 Jun 19;249(2-3):180-2
pubmed: 9682846
Sci Rep. 2017 Dec 20;7(1):17945
pubmed: 29263416
Neurobiol Dis. 2017 Oct;106:191-204
pubmed: 28711409
Nat Struct Mol Biol. 2008 Jun;15(6):558-66
pubmed: 18511942
Neuron. 2000 Jan;25(1):239-52
pubmed: 10707987
Proc Natl Acad Sci U S A. 2018 Jan 23;115(4):798-803
pubmed: 29311330
Am J Pathol. 1998 Feb;152(2):367-72
pubmed: 9466562
Brain. 2016 Dec;139(Pt 12):3217-3236
pubmed: 27679481
J Neurosci. 2014 Sep 10;34(37):12368-78
pubmed: 25209277
Anal Chem. 2016 Sep 6;88(17):8468-75
pubmed: 27467405
Neuron. 2002 May 16;34(4):521-33
pubmed: 12062037
Dalton Trans. 2006 Nov 14;(42):5068-76
pubmed: 17060993
Neuron. 2010 Jan 14;65(1):66-79
pubmed: 20152114
J Biol Chem. 2005 Jun 3;280(22):21212-9
pubmed: 15817478
Nat Neurosci. 2017 Nov;20(11):1560-1568
pubmed: 28920936
FEBS Lett. 2011 Apr 20;585(8):1113-20
pubmed: 21443877
Science. 2010 Sep 24;329(5999):1663-7
pubmed: 20798282
Proc Natl Acad Sci U S A. 2005 Mar 22;102(12):4294-9
pubmed: 15767574
Nat Med. 2008 May;14(5):501-3
pubmed: 18391963
Biochim Biophys Acta. 2015 Sep;1850(9):1884-90
pubmed: 26028294
J Neurosci. 2000 May 1;20(9):3214-20
pubmed: 10777786
Oncogene. 2003 Sep 18;22(40):6151-9
pubmed: 13679853
FASEB J. 2011 Jan;25(1):326-36
pubmed: 20876215
PLoS One. 2011 Jan 31;6(1):e16706
pubmed: 21304957
J Biol Chem. 2014 Apr 11;289(15):10727-37
pubmed: 24567327
J Neurosci. 2006 Sep 27;26(39):10068-78
pubmed: 17005870
Science. 2001 Nov 9;294(5545):1346-9
pubmed: 11701929
Mov Disord. 2013 Jun;28(6):811-3
pubmed: 23457019
Proc Natl Acad Sci U S A. 2017 Feb 7;114(6):E1009-E1017
pubmed: 28096355
ACS Chem Neurosci. 2017 Aug 16;8(8):1704-1712
pubmed: 28425704
J Neurochem. 2006 Apr;97(1):105-15
pubmed: 16524383
Neurology. 1998 Sep;51(3):887-9
pubmed: 9748051
J Neurosci. 2004 Feb 25;24(8):1888-96
pubmed: 14985429
J Biomol NMR. 2011 Jan;49(1):9-15
pubmed: 21190063
PLoS One. 2011 Apr 29;6(4):e19338
pubmed: 21559417
Neuron. 1995 Aug;15(2):361-72
pubmed: 7646890
J Vis Exp. 2008 Aug 15;(18):
pubmed: 19066505
Am J Pathol. 1998 Apr;152(4):879-84
pubmed: 9546347
Curr Opin Chem Biol. 2010 Aug;14(4):481-8
pubmed: 20598937
Mol Cancer Ther. 2007 Sep;6(9):2399-408
pubmed: 17876039
Acta Neuropathol Commun. 2017 Feb 2;5(1):12
pubmed: 28148299
J Biol Chem. 1998 Apr 17;273(16):9443-9
pubmed: 9545270
Biochemistry. 2009 Sep 1;48(34):8206-24
pubmed: 19634918
Parkinsons Dis. 2010 Jan 28;2010:650794
pubmed: 20976092
Anal Chem. 2016 Feb 16;88(4):2399-405
pubmed: 26813311
Biophys J. 2010 Oct 6;99(7):2279-88
pubmed: 20923663
Curr Opin Pharmacol. 2010 Dec;10(6):782-8
pubmed: 20889377
Neurodegener Dis. 2010;7(4):219-31
pubmed: 20197647
Bioorg Med Chem. 2015 Nov 1;23(21):7007-14
pubmed: 26439661
Science. 2017 Sep 22;357(6357):1255-1261
pubmed: 28882997
J Biol Chem. 2015 Nov 13;290(46):27582-93
pubmed: 26396193
Chem Biol. 2004 Nov;11(11):1513-21
pubmed: 15556002
Biochemistry. 2006 May 16;45(19):6085-94
pubmed: 16681381
J Neurosci. 2015 May 27;35(21):8345-58
pubmed: 26019347
J Neurosci. 2012 Jul 25;32(30):10129-35
pubmed: 22836248
Nat Neurosci. 2000 Dec;3(12):1301-6
pubmed: 11100151

Auteurs

Malcolm J Daniels (MJ)

Pharmacology Graduate Group, Raymond and Ruth Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.

J Brucker Nourse (JB)

Department of Biological Sciences, University of Alabama, Tuscaloosa, AL, 35487, USA.

Hanna Kim (H)

Department of Biological Sciences, University of Alabama, Tuscaloosa, AL, 35487, USA.

Valerio Sainati (V)

CERM and Department of Chemistry "Ugo Schiff", University of Florence, Sesto Fiorentino, Florence, 50019, Italy.

Marco Schiavina (M)

CERM and Department of Chemistry "Ugo Schiff", University of Florence, Sesto Fiorentino, Florence, 50019, Italy.

Maria Grazia Murrali (MG)

CERM and Department of Chemistry "Ugo Schiff", University of Florence, Sesto Fiorentino, Florence, 50019, Italy.

Buyan Pan (B)

Department of Chemistry, University of Pennsylvania, Philadelphia, PA, 19104, USA.

John J Ferrie (JJ)

Department of Chemistry, University of Pennsylvania, Philadelphia, PA, 19104, USA.

Conor M Haney (CM)

Department of Chemistry, University of Pennsylvania, Philadelphia, PA, 19104, USA.

Rani Moons (R)

Department of Chemistry, University of Antwerp, Antwerp, Belgium.

Neal S Gould (NS)

Department of Pediatrics, Children's Hospital of Philadelphia Research Institute, Philadelphia, PA, 19104, USA.

Antonino Natalello (A)

Department of Biotechnology and Biosciences, University of Milan-Bicocca, Milan, Italy.

Rita Grandori (R)

Department of Biotechnology and Biosciences, University of Milan-Bicocca, Milan, Italy.

Frank Sobott (F)

Biomolecular & Analytical Mass Spectrometry, Antwerp University, Antwerp, Belgium.
Astbury Centre for Structural Molecular Biology, University of Leeds, Leeds, United Kingdom.
School of Molecular and Cellular Biology, University of Leeds, Leeds, United Kingdom.

E James Petersson (EJ)

Department of Chemistry, University of Pennsylvania, Philadelphia, PA, 19104, USA.

Elizabeth Rhoades (E)

Department of Chemistry, University of Pennsylvania, Philadelphia, PA, 19104, USA.

Roberta Pierattelli (R)

CERM and Department of Chemistry "Ugo Schiff", University of Florence, Sesto Fiorentino, Florence, 50019, Italy.

Isabella Felli (I)

CERM and Department of Chemistry "Ugo Schiff", University of Florence, Sesto Fiorentino, Florence, 50019, Italy.

Vladimir N Uversky (VN)

Department of Molecular Medicine and Byrd Alzheimer's Research Institute, Morsani College of Medicine, University of South Florida, Tampa, FL, 33612, USA.
Institute for Biological Instrumentation, Russian Academy of Sciences, Pushchino, Moscow Region, 142292, Russian Federation.

Kim A Caldwell (KA)

Department of Biological Sciences, University of Alabama, Tuscaloosa, AL, 35487, USA.

Guy A Caldwell (GA)

Department of Biological Sciences, University of Alabama, Tuscaloosa, AL, 35487, USA.

Edward S Krol (ES)

College of Pharmacy & Nutrition, University of Saskatchewan, Saskatoon, Saskatchewan, Canada.

Harry Ischiropoulos (H)

Pharmacology Graduate Group, Raymond and Ruth Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA. ischirop@pennmedicine.upenn.edu.
Department of Pediatrics, Children's Hospital of Philadelphia Research Institute, Philadelphia, PA, 19104, USA. ischirop@pennmedicine.upenn.edu.
Children's Hospital of Philadelphia Research Institute and Systems Pharmacology and Translational Therapeutics, the Raymond and Ruth Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA. ischirop@pennmedicine.upenn.edu.

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