Aberrant protein S-nitrosylation contributes to hyperexcitability-induced synaptic damage in Alzheimer's disease: Mechanistic insights and potential therapies.
Alzheimer’s disease
NMDA receptors
NitroSynapsin
S-nitrosylation
glutamate excitotoxicity
hyperexcitability
Journal
Frontiers in neural circuits
ISSN: 1662-5110
Titre abrégé: Front Neural Circuits
Pays: Switzerland
ID NLM: 101477940
Informations de publication
Date de publication:
2023
2023
Historique:
received:
15
11
2022
accepted:
18
01
2023
entrez:
23
2
2023
pubmed:
24
2
2023
medline:
3
3
2023
Statut:
epublish
Résumé
Alzheimer's disease (AD) is arguably the most common cause of dementia in the elderly and is marked by progressive synaptic degeneration, which in turn leads to cognitive decline. Studies in patients and in various AD models have shown that one of the early signatures of AD is neuronal hyperactivity. This excessive electrical activity contributes to dysregulated neural network function and synaptic damage. Mechanistically, evidence suggests that hyperexcitability accelerates production of reactive oxygen species (ROS) and reactive nitrogen species (RNS) that contribute to neural network impairment and synapse loss. This review focuses on the pathways and molecular changes that cause hyperexcitability and how RNS-dependent posttranslational modifications, represented predominantly by protein S-nitrosylation, mediate, at least in part, the deleterious effects of hyperexcitability on single neurons and the neural network, resulting in synaptic loss in AD.
Identifiants
pubmed: 36817649
doi: 10.3389/fncir.2023.1099467
pmc: PMC9932935
doi:
Substances chimiques
Protein S
0
Reactive Nitrogen Species
0
Types de publication
Journal Article
Review
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
1099467Subventions
Organisme : NIA NIH HHS
ID : R01 AG061845
Pays : United States
Organisme : NIA NIH HHS
ID : R35 AG071734
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG078756
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG056259
Pays : United States
Organisme : NINDS NIH HHS
ID : RF1 NS123298
Pays : United States
Organisme : NIDA NIH HHS
ID : DP1 DA041722
Pays : United States
Organisme : NIA NIH HHS
ID : R56 AG065372
Pays : United States
Organisme : NINDS NIH HHS
ID : R61 NS122098
Pays : United States
Organisme : NIDA NIH HHS
ID : R01 DA048882
Pays : United States
Organisme : NIA NIH HHS
ID : RF1 AG057409
Pays : United States
Informations de copyright
Copyright © 2023 Ghatak, Nakamura and Lipton.
Déclaration de conflit d'intérêts
SL was an inventor on worldwide patents for the use of memantine and NitroSynapsin for neurodegenerative and neurodevelopmental disorders. Per Harvard University guidelines, SL participates in a royalty-sharing agreement with his former institution Boston Children’s Hospital/Harvard Medical School, which licensed the drug memantine (Namenda®) to Forest Laboratories, Inc./Actavis/Allergan/AbbVie. NitroSynapsin is licensed to the Boston-area biotechnology company EuMentis Therapeutics, Inc., for which SL was the scientific founder. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Références
Sci Adv. 2022 Dec 14;8(50):eade0764
pubmed: 36516243
J Mol Med (Berl). 2000;78(1):3-13
pubmed: 10759025
Nat Neurosci. 2002 May;5(5):405-14
pubmed: 11953750
Annu Rev Biochem. 1994;63:175-95
pubmed: 7526779
Trends Neurosci. 2002 Sep;25(9):474-80
pubmed: 12183209
Ann Neurol. 1991 Oct;30(4):572-80
pubmed: 1789684
Cell. 2011 Apr 15;145(2):284-99
pubmed: 21496646
Nat Rev Neurosci. 2010 Oct;11(10):682-96
pubmed: 20842175
J Alzheimers Dis. 2017;57(4):1041-1048
pubmed: 27662322
Nature. 1984 Feb 2-8;307(5950):462-5
pubmed: 6320006
Neuron. 2018 Apr 4;98(1):75-89.e5
pubmed: 29551491
J Biol Chem. 2010 Mar 5;285(10):7619-32
pubmed: 20032460
N Engl J Med. 1994 Mar 3;330(9):613-22
pubmed: 7905600
Proc Natl Acad Sci U S A. 2013 Jul 2;110(27):E2518-27
pubmed: 23776240
Mol Neurobiol. 2019 Aug;56(8):5568-5585
pubmed: 30652266
Cell Rep. 2020 Nov 3;33(5):108329
pubmed: 33147468
Nature. 2016 Dec 7;540(7632):230-235
pubmed: 27929004
Cell. 2013 Dec 5;155(6):1351-64
pubmed: 24290359
Arch Biochem Biophys. 1992 Nov 1;298(2):431-7
pubmed: 1416974
J Neurosci. 1999 Jun 1;19(11):4595-608
pubmed: 10341257
Neuron. 2014 Apr 16;82(2):279-93
pubmed: 24742457
Environ Int. 2021 Dec;157:106864
pubmed: 34537521
Science. 2019 Aug 9;365(6453):559-565
pubmed: 31395777
Science. 1992 Nov 27;258(5087):1498-501
pubmed: 1359647
Nat Rev Neurosci. 2011 Apr;12(4):204-16
pubmed: 21415847
Curr Alzheimer Res. 2006 Jul;3(3):201-4
pubmed: 16842096
Brain Pathol. 2021 Nov;31(6):e13005
pubmed: 34269494
Neurobiol Aging. 2011 Mar;32(3):553.e1-11
pubmed: 20416976
Neuron. 1992 Jun;8(6):1087-99
pubmed: 1376999
Brain Res Bull. 2018 Jan;136:3-16
pubmed: 28040508
Neuron. 2005 May 19;46(4):533-40
pubmed: 15944123
Nat Rev Drug Discov. 2004 Mar;3(3):205-14
pubmed: 15031734
Epilepsy Curr. 2012 Sep;12(5):178-83
pubmed: 23118602
Arch Neurol. 2009 Apr;66(4):435-40
pubmed: 19204149
Annu Rev Pharmacol Toxicol. 2021 Jan 6;61:701-721
pubmed: 32997602
Neuron. 2014 Dec 3;84(5):1023-33
pubmed: 25456500
Science. 2003 Feb 7;299(5608):896-9
pubmed: 12574632
J Neurosci. 1987 Feb;7(2):357-68
pubmed: 2880937
Front Pharmacol. 2013 Mar 13;4:24
pubmed: 23493925
Cell Death Differ. 2022 Nov;29(11):2137-2150
pubmed: 35462559
J Alzheimers Dis. 2007 Mar;11(1):97-116
pubmed: 17361039
J Neurol Sci. 2002 Aug 15;200(1-2):11-8
pubmed: 12127670
Philos Trans R Soc Lond B Biol Sci. 2014 Oct 19;369(1654):20130601
pubmed: 25225095
Nat Commun. 2021 May 10;12(1):2603
pubmed: 33972518
Hippocampus. 2019 Mar;29(3):184-238
pubmed: 29722465
Sci Transl Med. 2022 Jun;14(647):eabi8593
pubmed: 35648810
Nature. 1993 Jan 7;361(6407):31-9
pubmed: 8421494
Nat Neurosci. 2009 Dec;12(12):1567-76
pubmed: 19935655
Neurobiol Dis. 2005 Dec;20(3):685-93
pubmed: 15949941
Proc Natl Acad Sci U S A. 1988 Nov;85(21):7852-6
pubmed: 3186695
Curr Opin Neurobiol. 2018 Oct;52:182-187
pubmed: 30121451
Science. 2008 Sep 19;321(5896):1686-9
pubmed: 18802001
Nat Neurosci. 2016 Dec;19(12):1690-1696
pubmed: 27749827
Biochim Biophys Acta. 2014 Feb;1838(2):589-94
pubmed: 23535319
Neuron. 2002 Jan 31;33(3):325-40
pubmed: 11832222
Neuron. 2007 Jan 4;53(1):53-64
pubmed: 17196530
J Neurosci. 2010 May 26;30(21):7168-78
pubmed: 20505084
Nat Commun. 2017 Nov 14;8(1):1488
pubmed: 29133852
Nature. 2003 Aug 7;424(6949):677-81
pubmed: 12904794
ACS Pharmacol Transl Sci. 2020 Mar 12;3(2):334-344
pubmed: 32296772
J Physiol. 1997 Feb 15;499 ( Pt 1):27-46
pubmed: 9061638
PLoS One. 2010 Apr 28;5(4):e10390
pubmed: 20436928
Environ Int. 2023 Jan;171:107694
pubmed: 36521347
Science. 2015 Oct 23;350(6259):430-3
pubmed: 26494756
Cell Calcium. 2012 Feb;51(2):95-106
pubmed: 22177709
Philos Trans R Soc Lond B Biol Sci. 2016 Aug 5;371(1700):
pubmed: 27377723
Cell. 2001 Sep 21;106(6):675-83
pubmed: 11572774
Trends Cogn Sci. 2012 Dec;16(12):584-92
pubmed: 23142417
Cold Spring Harb Perspect Biol. 2012 Jun 01;4(6):
pubmed: 22510460
Neuron. 2004 Sep 30;44(1):181-93
pubmed: 15450169
Nature. 2002 Apr 4;416(6880):535-9
pubmed: 11932745
Neuropsychopharmacology. 2008 Jan;33(1):18-41
pubmed: 17728696
Nat Chem Biol. 2022 Sep 29;:
pubmed: 36175661
Curr Opin Chem Biol. 2012 Dec;16(5-6):498-506
pubmed: 23127359
J Alzheimers Dis. 2020;78(4):1345-1361
pubmed: 33325389
Neuron. 2007 Sep 6;55(5):697-711
pubmed: 17785178
Proc Natl Acad Sci U S A. 2009 Sep 22;106(38):16440-5
pubmed: 19805317
Epilepsy Behav. 2013 Mar;26(3):343-51
pubmed: 23321057
Nature. 1993 Aug 12;364(6438):626-32
pubmed: 8394509
Ann N Y Acad Sci. 2008;1129:119-29
pubmed: 18591474
Philos Trans R Soc Lond B Biol Sci. 2013 Dec 02;369(1633):20130129
pubmed: 24298133
J Physiol. 2015 Jan 1;593(1):39-48
pubmed: 25556786
J Neurosci. 2010 Aug 18;30(33):11246-50
pubmed: 20720132
Mol Cell. 2010 Jul 30;39(2):184-95
pubmed: 20670888
J Neurosci. 1999 Jul 1;19(13):5265-74
pubmed: 10377338
Front Psychiatry. 2018 Nov 06;9:561
pubmed: 30459657
Science. 1997 Jun 27;276(5321):2042-5
pubmed: 9197267
Neuron. 2006 Nov 9;52(3):475-84
pubmed: 17088213
J Neurosci. 1992 Nov;12(11):4427-36
pubmed: 1432103
Mol Psychiatry. 2021 Oct;26(10):5751-5765
pubmed: 32467645
Neuropsychopharmacology. 2017 Dec;42(13):2633-2639
pubmed: 28425497
Nat Neurosci. 2020 Oct;23(10):1183-1193
pubmed: 32778792
Neurobiol Dis. 2019 Jul;127:390-397
pubmed: 30928642
Front Syst Neurosci. 2019 Jan 08;12:64
pubmed: 30670952
Annu Rev Neurosci. 2002;25:103-26
pubmed: 12052905
Pharmacol Rev. 2010 Sep;62(3):405-96
pubmed: 20716669
Cell. 2003 Oct 17;115(2):139-50
pubmed: 14567912
Nat Neurosci. 2005 Jan;8(1):79-84
pubmed: 15608634
Epilepsia. 2004 Apr;45(4):314-21
pubmed: 15030493
Nat Med. 2017 Jun;23(6):678-680
pubmed: 28459436
Antioxid Redox Signal. 2013 Jan 20;18(3):239-49
pubmed: 22657837
Proc Natl Acad Sci U S A. 2001 Jan 16;98(2):676-82
pubmed: 11209064
Neuropharmacology. 2017 Feb;113(Pt A):293-300
pubmed: 27743932
J Biol Chem. 2009 Dec 18;284(51):35827-38
pubmed: 19840937
Nat Neurosci. 2018 Apr;21(4):463-473
pubmed: 29403035
J Alzheimers Dis. 2018;62(4):1789-1801
pubmed: 29614651
Elife. 2017 Feb 08;6:
pubmed: 28177283
J Biol Chem. 2002 Aug 30;277(35):32180-6
pubmed: 12070161
Neuron. 2019 Jun 5;102(5):929-943.e8
pubmed: 31076275
Nat Neurosci. 2010 Jul;13(7):812-8
pubmed: 20581818
Trends Endocrinol Metab. 2017 Dec;28(12):879-892
pubmed: 29097102
Alzheimers Res Ther. 2015 May 05;7(1):25
pubmed: 25945128
J Neurol Sci. 2001 Jan 1;182(2):151-9
pubmed: 11137521
Proc Natl Acad Sci U S A. 2018 Jun 26;115(26):6858-6863
pubmed: 29884650
Neuropharmacology. 2017 Jan;112(Pt A):221-227
pubmed: 27561971
Neuron. 2006 Oct 5;52(1):155-68
pubmed: 17015233
Nat Rev Neurosci. 2016 Dec;17(12):777-792
pubmed: 27829687
Elife. 2019 Nov 29;8:
pubmed: 31782729
Nature. 2006 May 25;441(7092):513-7
pubmed: 16724068
J Neurovirol. 2021 Jun;27(3):367-378
pubmed: 33876414
Neuron. 2013 Sep 4;79(5):887-902
pubmed: 24012003
J Neurosci. 2007 Mar 14;27(11):2866-75
pubmed: 17360908
Cell. 2012 Apr 27;149(3):708-21
pubmed: 22541439
Ann Neurol. 1990 May;27(5):457-64
pubmed: 2360787
Brain Res. 2005 Jun 7;1046(1-2):10-23
pubmed: 15890316
Neuron. 2011 Jul 14;71(1):131-41
pubmed: 21745643
J Neurosci. 2014 Apr 2;34(14):5023-8
pubmed: 24695719
Nat Rev Mol Cell Biol. 2005 Feb;6(2):150-66
pubmed: 15688001
Sci Rep. 2015 Oct 19;5:14781
pubmed: 26477507
Nat Neurosci. 2000 Jan;3(1):15-21
pubmed: 10607390
J Neurosci. 2010 Feb 17;30(7):2694-9
pubmed: 20164353
Neuron. 1991 Jul;7(1):111-8
pubmed: 1676893
Science. 1999 Jun 11;284(5421):1845-8
pubmed: 10364559
Science. 2009 Apr 3;324(5923):102-5
pubmed: 19342591
J Neurochem. 2004 Aug;90(4):913-9
pubmed: 15287897
Arch Biochem Biophys. 2017 Mar 1;617:137-144
pubmed: 27794428
Proc Natl Acad Sci U S A. 2013 Jan 15;110(3):1077-82
pubmed: 23277581
Nat Rev Neurosci. 2007 Oct;8(10):803-8
pubmed: 17882256
Future Neurol. 2012 Mar 1;7(2):177-192
pubmed: 22723738
Ann Neurol. 2016 Dec;80(6):858-870
pubmed: 27696483
J Neuropathol Exp Neurol. 1997 Aug;56(8):901-11
pubmed: 9258260
Cell Biosci. 2020 Mar 4;10:26
pubmed: 32158532
Neurochem Res. 2017 Jan;42(1):10-18
pubmed: 27696119
Science. 2021 Jan 15;371(6526):
pubmed: 33273062
JAMA Neurol. 2013 Sep 1;70(9):1158-66
pubmed: 23835471
Science. 1999 Apr 23;284(5414):651-4
pubmed: 10213689
Annu Rev Neurosci. 2012;35:203-25
pubmed: 22443509
Nat Neurosci. 2012 Oct;15(10):1422-9
pubmed: 22922786
Mol Neurodegener. 2014 Nov 14;9:48
pubmed: 25394486
Ann Neurol. 2010 Dec;68(6):865-75
pubmed: 21194156
Front Hum Neurosci. 2014 Mar 04;8:114
pubmed: 24624074
Aging Cell. 2022 May;21(5):e13593
pubmed: 35353937
J Neurosci. 2006 Oct 4;26(40):10222-31
pubmed: 17021177
Mol Pharmacol. 2013 Dec;84(6):935-47
pubmed: 24101301
Front Neural Circuits. 2021 Aug 17;15:711564
pubmed: 34483848
Cell Death Dis. 2022 Mar 19;13(3):253
pubmed: 35306512
Free Radic Biol Med. 2021 Aug 20;172:562-577
pubmed: 34224817
J Neurochem. 2001 Jul;78(1):175-82
pubmed: 11432984
Neuron. 2017 May 17;94(4):713-730
pubmed: 28521126
Acta Neurol Belg. 2020 Jun;120(3):531-544
pubmed: 32152997
Front Neurol. 2013 Feb 13;4:9
pubmed: 23407382
Science. 1936 Mar 13;83(2150):259-60
pubmed: 17757098
Proc Natl Acad Sci U S A. 2011 Aug 23;108(34):14330-5
pubmed: 21844361
Proc Natl Acad Sci U S A. 2009 Apr 28;106(17):7209-14
pubmed: 19357304
J Neurosci. 2004 Nov 10;24(45):10191-200
pubmed: 15537891
Ann Neurol. 1996 Nov;40(5):759-66
pubmed: 8957017
J Neurosci. 2001 Feb 15;21(4):1327-33
pubmed: 11160403
J Neurosci. 2011 Nov 30;31(48):17680-8
pubmed: 22131428
Antioxid Redox Signal. 2021 Sep 1;35(7):531-550
pubmed: 33957758
Science. 2016 Apr 29;352(6285):aad3873
pubmed: 26966189
J Alzheimers Dis. 2017;55(4):1683-1692
pubmed: 27911305
Adv Neurobiol. 2016;13:99-132
pubmed: 27885628
Lancet Neurol. 2017 Apr;16(4):311-322
pubmed: 28327340
J Neurochem. 1985 Jan;44(1):99-109
pubmed: 2856886
J Neurophysiol. 2004 Nov;92(5):2853-8
pubmed: 15212428
Neuron. 2009 Jun 25;62(6):788-801
pubmed: 19555648
Sci Signal. 2015 Jul 07;8(384):ra68
pubmed: 26152695
Neuron. 2000 Mar;25(3):649-62
pubmed: 10774732
Neuroscience. 2015 Dec 17;311:374-81
pubmed: 26541750
Cell Calcium. 2003 Oct-Nov;34(4-5):385-97
pubmed: 12909083
Neurosci Lett. 1997 Nov 7;236(3):139-42
pubmed: 9406756
Trends Neurosci. 2011 May;34(5):258-68
pubmed: 21420743
Nature. 1992 Dec 3;360(6403):471-4
pubmed: 1448171
Science. 2010 Apr 2;328(5974):106-9
pubmed: 20360111
Nat Med. 2014 Dec;20(12):1485-92
pubmed: 25384087
J Neurosci. 2022 Apr 6;42(14):3011-3024
pubmed: 35169022
Br J Pharmacol. 2012 Sep;167(2):324-52
pubmed: 22646481
Science. 1997 Jun 13;276(5319):1699-702
pubmed: 9180080
PLoS One. 2013 Nov 28;8(11):e81828
pubmed: 24312364
N Engl J Med. 2000 Aug 17;343(7):450-6
pubmed: 10944562
Neuron. 2013 May 22;78(4):596-614
pubmed: 23719160
Cell Rep. 2014 Jul 10;8(1):217-28
pubmed: 25001280
Front Cell Neurosci. 2018 Oct 11;12:362
pubmed: 30364226
Neurology. 2005 Aug 9;65(3):404-11
pubmed: 16087905
Cell. 2022 Aug 4;185(16):2853-2878
pubmed: 35931019
J Alzheimers Dis. 2014;39(1):89-101
pubmed: 24145381
Neurobiol Dis. 2016 Jan;85:111-121
pubmed: 26525100
Cell Calcium. 2010 Mar;47(3):264-72
pubmed: 20061018
Neuron. 2009 Jul 30;63(2):178-88
pubmed: 19640477
Neuron. 2017 Jun 7;94(5):993-1001
pubmed: 28595056
PLoS One. 2017 Feb 2;12(2):e0171489
pubmed: 28152104
J Neurosci. 1998 Nov 1;18(21):8751-7
pubmed: 9786982
J Neurosci. 2002 Feb 1;22(3):RC206
pubmed: 11826152
Nat Rev Drug Discov. 2006 Feb;5(2):160-70
pubmed: 16424917
Neuron. 2006 Dec 7;52(5):831-43
pubmed: 17145504