Cx43 hemichannels contribute to astrocyte-mediated toxicity in sporadic and familial ALS.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
29 03 2022
Historique:
entrez: 21 3 2022
pubmed: 22 3 2022
medline: 21 4 2022
Statut: ppublish

Résumé

Connexin 43 (Cx43) gap junctions and hemichannels mediate astrocyte intercellular communication in the central nervous system under normal conditions and contribute to astrocyte-mediated neurotoxicity in amyotrophic lateral sclerosis (ALS). Here, we show that astrocyte-specific knockout of Cx43 in a mouse model of ALS slows disease progression both spatially and temporally, provides motor neuron (MN) protection, and improves survival. In addition, Cx43 expression is up-regulated in human postmortem tissue and cerebrospinal fluid from ALS patients. Using human induced pluripotent stem cell–derived astrocytes (hiPSC-A) from both familial and sporadic ALS, we establish that Cx43 is up-regulated and that Cx43-hemichannels are enriched at the astrocyte membrane. We also demonstrate that the pharmacological blockade of Cx43-hemichannels in ALS astrocytes using GAP 19, a mimetic peptide blocker, and tonabersat, a clinically tested small molecule, provides neuroprotection of hiPSC-MN and reduces ALS astrocyte-mediated neuronal hyperexcitability. Extending the in vitro application of tonabersat with chronic administration to SOD1G93A mice results in MN protection with a reduction in reactive astrocytosis and microgliosis. Taking these data together, our studies identify Cx43 hemichannels as conduits of astrocyte-mediated disease progression and a pharmacological target for disease-modifying ALS therapies.

Identifiants

pubmed: 35312356
doi: 10.1073/pnas.2107391119
pmc: PMC9060483
doi:

Substances chimiques

Connexin 43 0
GJA1 protein, human 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2107391119

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM099490
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS117604
Pays : United States

Références

Neurosci Lett. 2006 Jan 9;392(1-2):52-7
pubmed: 16174551
JAMA Neurol. 2016 Apr;73(4):425-30
pubmed: 26903389
Exp Mol Med. 2009 Mar 31;41(3):140-50
pubmed: 19293633
Science. 2003 Oct 3;302(5642):113-7
pubmed: 14526083
Nat Cell Biol. 1999 Nov;1(7):457-9
pubmed: 10559992
Nat Neurosci. 2007 May;10(5):615-22
pubmed: 17435755
Exp Neurol. 2001 Dec;172(2):342-53
pubmed: 11716558
J Neurosci. 2006 May 17;26(20):5438-47
pubmed: 16707796
Antioxid Redox Signal. 2009 Feb;11(2):369-99
pubmed: 18816186
J Neurosci. 1991 May;11(5):1421-32
pubmed: 1851221
Neurotherapeutics. 2017 Oct;14(4):1148-1165
pubmed: 28560708
Sci Rep. 2017 Nov 2;7(1):14972
pubmed: 29097807
Proc Natl Acad Sci U S A. 2014 Jan 14;111(2):829-32
pubmed: 24379375
Neuron. 2014 Mar 5;81(5):1001-1008
pubmed: 24508385
Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):697-702
pubmed: 11805325
Sci Rep. 2016 Jan 27;6:19884
pubmed: 26814383
J Neurosci. 2012 Mar 7;32(10):3333-8
pubmed: 22399755
Neurology. 2014 Nov 4;83(19):1719-25
pubmed: 25298304
Life Sci. 2018 Sep 1;208:175-191
pubmed: 30031059
Exp Neurol. 2011 Mar;228(1):69-79
pubmed: 21168408
Nature. 2017 Jan 26;541(7638):481-487
pubmed: 28099414
Life Sci. 2019 Jan 1;216:59-66
pubmed: 30419280
Stem Cells Transl Med. 2019 Dec;8(12):1272-1285
pubmed: 31631575
Am J Physiol. 1992 Aug;263(2 Pt 1):C373-83
pubmed: 1325115
Biol Cell. 2002 Nov;94(7-8):457-75
pubmed: 12566220
Nat Biotechnol. 2011 Aug 10;29(9):824-8
pubmed: 21832997
Brain Res. 2015 May 14;1607:15-25
pubmed: 25223906
Prog Med Chem. 2000;37:177-200
pubmed: 10845250
Hippocampus. 1994 Jun;4(3):297-306
pubmed: 7842053
J Alzheimers Dis. 2009;18(1):177-89
pubmed: 19584439
Front Cell Neurosci. 2014 Oct 21;8:306
pubmed: 25374505
Cell Rep. 2017 May 30;19(9):1739-1749
pubmed: 28564594
Proc Natl Acad Sci U S A. 1989 Apr;86(8):2708-12
pubmed: 2784857
Nature. 1978 Apr 6;272(5653):501-6
pubmed: 211417
J Membr Biol. 2016 Jun;249(3):363-73
pubmed: 26873723
Nat Neurosci. 2007 May;10(5):608-14
pubmed: 17435754
Adv Exp Med Biol. 2016;949:93-108
pubmed: 27714686
Mol Brain. 2017 Jun 13;10(1):22
pubmed: 28610619
Brain. 2019 Mar 1;142(3):586-605
pubmed: 30698736
Neurosci Lett. 2019 Jan 10;689:1-4
pubmed: 30031035
Cell Rep. 2013 Sep 12;4(5):1035-1048
pubmed: 23994478
Nature. 2004 Sep 9;431(7005):195-9
pubmed: 15356633
Stem Cell Reports. 2017 Apr 11;8(4):843-855
pubmed: 28366455
Br J Pharmacol. 1997 Aug;121(8):1687-91
pubmed: 9283704
Nat Rev Neurol. 2018 Jun;14(6):351-362
pubmed: 29769699
PLoS One. 2012;7(3):e33090
pubmed: 22461890
Lancet Neurol. 2009 Aug;8(8):718-23
pubmed: 19570717
Br J Pharmacol. 1997 Aug;121(8):1679-86
pubmed: 9283703
Proc Natl Acad Sci U S A. 2006 Mar 21;103(12):4475-80
pubmed: 16537412
Science. 2008 Dec 5;322(5907):1551-5
pubmed: 19056987
EBioMedicine. 2019 Dec;50:274-289
pubmed: 31787569
Nat Med. 2016 Apr;22(4):397-403
pubmed: 26928464
J Neurosci. 1995 Mar;15(3 Pt 1):1835-53
pubmed: 7891138
Proc Natl Acad Sci U S A. 2011 Oct 25;108(43):17803-8
pubmed: 21969586
Cell Commun Adhes. 2001;8(4-6):315-20
pubmed: 12064610
J Neuropathol Exp Neurol. 2011 Aug;70(8):662-77
pubmed: 21760539
Methods Enzymol. 2021;654:271-293
pubmed: 34120717
Bioorg Med Chem Lett. 1999 Jan 18;9(2):285-90
pubmed: 10021946
Biochim Biophys Acta. 2013 Jan;1828(1):118-33
pubmed: 22244842
Front Mol Neurosci. 2019 Feb 06;12:23
pubmed: 30787868
Nature. 2016 May 18;533(7604):493-498
pubmed: 27225120
Cephalalgia. 2009 Jul;29(7):742-50
pubmed: 19222510
Nat Med. 2018 Jul;24(7):931-938
pubmed: 29892066
Glia. 2017 Oct;65(10):1607-1625
pubmed: 28703353
Cephalalgia. 2004 Oct;24(10):875-82
pubmed: 15377319
Proc Natl Acad Sci U S A. 2011 Nov 1;108(44):18126-31
pubmed: 22010221
Cephalalgia. 2009 Nov;29 Suppl 2:1-6
pubmed: 19723120
Cell Death Differ. 2016 Oct;23(10):1691-701
pubmed: 27391799
Glia. 1996 Mar;16(3):187-95
pubmed: 8833189
Mol Med Rep. 2013 Aug;8(2):585-90
pubmed: 23783886
Glia. 2016 Jul;64(7):1154-69
pubmed: 27083773
Brain Res Rev. 2010 May;63(1-2):160-76
pubmed: 19963007
Nature. 2010 Sep 16;467(7313):285-90
pubmed: 20644535
Epilepsy Res. 2013 Jan;103(1):2-30
pubmed: 23219031
J Neurochem. 2011 Sep;118(5):826-40
pubmed: 21294731
Neuroscience. 2016 May 26;323:207-21
pubmed: 25913636
Brain Res. 1996 Apr 22;717(1-2):173-8
pubmed: 8738268
Acta Neuropathol. 1996 Nov;92(5):528-33
pubmed: 8922067
J Neuroinflammation. 2014 Mar 06;11:42
pubmed: 24597481
Cell Stem Cell. 2014 Jun 5;14(6):781-95
pubmed: 24704492
Headache. 2009 Jan;49(1):5-20
pubmed: 19125874
Front Physiol. 2014 Feb 25;5:78
pubmed: 24611055
J Neurosci. 2001 Mar 15;21(6):1983-2000
pubmed: 11245683
Nat Neurosci. 2008 Mar;11(3):251-3
pubmed: 18246065
J Comp Neurol. 1996 Sep 30;373(4):619-31
pubmed: 8889947
Neural Dev. 2021 Jan 7;16(1):1
pubmed: 33413602
PLoS One. 2017 Apr 13;12(4):e0174925
pubmed: 28406915
Cell. 1993 Sep 24;74(6):1065-77
pubmed: 7691412

Auteurs

Akshata A Almad (AA)

Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205.

Arens Taga (A)

Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205.

Jessica Joseph (J)

Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205.

Sarah K Gross (SK)

Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205.

Connor Welsh (C)

Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205.

Aneesh Patankar (A)

Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205.

Jean-Philippe Richard (JP)

Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205.

Khalil Rust (K)

Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205.

Aayush Pokharel (A)

Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205.

Caroline Plott (C)

Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205.

Mauricio Lillo (M)

Department of Pharmacology, Physiology, & Neuroscience, New Jersey Medical School, Rutgers University, Newark, NJ 07101.

Raha Dastgheyb (R)

Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205.

Kevin Eggan (K)

Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138.

Norman Haughey (N)

Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205.

Jorge E Contreras (JE)

Department of Pharmacology, Physiology, & Neuroscience, New Jersey Medical School, Rutgers University, Newark, NJ 07101.
Department of Physiology and Membrane Biology, School of Medicine, University of California, Davis, CA 95616.

Nicholas J Maragakis (NJ)

Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205.

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