Overlapping transcriptional programs promote survival and axonal regeneration of injured retinal ganglion cells.

Animals Axons / metabolism Cell Survival / genetics Mammals Mice Nerve Regeneration / genetics Optic Nerve Injuries / genetics Retinal Ganglion Cells / physiology
CNTF Pten Socs3 Wt1 axonal regeneration single-cell RNA sequencing

Journal

Neuron
ISSN: 1097-4199
Titre abrégé: Neuron
Pays: United States
ID NLM: 8809320

Informations de publication

Date de publication:
17 08 2022
Historique:
received: 17 01 2022
revised: 08 04 2022
accepted: 03 06 2022
pubmed: 30 6 2022
medline: 23 8 2022
entrez: 29 6 2022
Statut: ppublish

Résumé

Injured neurons in the adult mammalian central nervous system often die and seldom regenerate axons. To uncover transcriptional pathways that could ameliorate these disappointing responses, we analyzed three interventions that increase survival and regeneration of mouse retinal ganglion cells (RGCs) following optic nerve crush (ONC) injury, albeit not to a clinically useful extent. We assessed gene expression in each of 46 RGC types by single-cell transcriptomics following ONC and treatment. We also compared RGCs that regenerated with those that survived but did not regenerate. Each intervention enhanced survival of most RGC types, but type-independent axon regeneration required manipulation of multiple pathways. Distinct computational methods converged on separate sets of genes selectively expressed by RGCs likely to be dying, surviving, or regenerating. Overexpression of genes associated with the regeneration program enhanced both survival and axon regeneration in vivo, indicating that mechanistic analysis can be used to identify novel therapeutic strategies.

Identifiants

DOI: 10.1016/j.neuron.2022.06.002 PMID: 35767994 PMC: PMC9391321
pubmed: 35767994
pii: S0896-6273(22)00540-2
doi: 10.1016/j.neuron.2022.06.002
pmc: PMC9391321
mid: NIHMS1819126
pii:
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

2625-2645.e7

Subventions

Organisme : NEI NIH HHS
ID : R01 EY021526
Pays : United States
Organisme : NEI NIH HHS
ID : R00 EY029360
Pays : United States
Organisme : NICHD NIH HHS
ID : P50 HD105351
Pays : United States
Organisme : NICHD NIH HHS
ID : P30 HD018655
Pays : United States
Organisme : NEI NIH HHS
ID : P30 EY012196
Pays : United States
Organisme : NINDS NIH HHS
ID : R21 NS104248
Pays : United States
Organisme : NEI NIH HHS
ID : R01 EY021342
Pays : United States
Organisme : NEI NIH HHS
ID : R01 EY026939
Pays : United States
Organisme : NEI NIH HHS
ID : R01 EY030204
Pays : United States
Organisme : NEI NIH HHS
ID : K99 EY029360
Pays : United States
Organisme : NEI NIH HHS
ID : K99 EY032181
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2022 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests J.R.S. is a consultant for Biogen. Z.H. is an advisor of SpineX, Life Biosciences, and Myro Therapeutics.

Références

J Immunol. 2018 Jun 15;200(12):4024-4035
pubmed: 29712772
J Biol Chem. 2014 Nov 21;289(47):32914-25
pubmed: 25296755
Neuron. 2016 Oct 19;92(2):419-434
pubmed: 27720483
Exp Neurol. 2008 Feb;209(2):321-32
pubmed: 17720160
Neuron. 2000 Oct;28(1):41-51
pubmed: 11086982
J Neurotrauma. 2011 Dec;28(12):2475-83
pubmed: 21861632
Neuron. 2022 Jan 5;110(1):51-69.e7
pubmed: 34706221
J Neurosci. 2000 Jun 1;20(11):4081-90
pubmed: 10818143
J Neurosci. 2014 Oct 29;34(44):14606-23
pubmed: 25355214
EMBO J. 2002 Mar 15;21(6):1398-405
pubmed: 11889045
Cell Cycle. 2006 Jun;5(12):1249-53
pubmed: 16760668
Front Oncol. 2019 Apr 17;9:289
pubmed: 31058089
Curr Biol. 2010 Jul 13;20(13):1154-64
pubmed: 20579880
PLoS Genet. 2021 Nov 4;17(11):e1009885
pubmed: 34735454
Nat Protoc. 2014 Jan;9(1):171-81
pubmed: 24385147
Exp Neurol. 2015 Apr;266:147-60
pubmed: 25704959
Annu Rev Vis Sci. 2020 Sep 15;6:195-213
pubmed: 32936739
Curr Opin Neurol. 2011 Dec;24(6):577-83
pubmed: 21968547
Cell. 2001 Apr 6;105(1):43-55
pubmed: 11301001
Mediators Inflamm. 2017;2017:9478542
pubmed: 28203046
J Comp Neurol. 2014 Apr 15;522(6):1411-43
pubmed: 24318667
Dev Med Child Neurol. 2012 Aug;54(8):765-9
pubmed: 22591407
Spinal Cord. 2010 Dec;48(12):850-6
pubmed: 20458328
J Neurosci. 2010 Feb 17;30(7):2623-35
pubmed: 20164347
Front Cell Neurosci. 2020 May 14;14:119
pubmed: 32477071
Invest Ophthalmol Vis Sci. 2020 Feb 7;61(2):31
pubmed: 32084268
Proc Natl Acad Sci U S A. 2021 Mar 2;118(9):
pubmed: 33627402
Neuron. 2019 Dec 18;104(6):1039-1055.e12
pubmed: 31784286
Nature. 2020 Nov;587(7835):613-618
pubmed: 33029008
OMICS. 2012 May;16(5):284-7
pubmed: 22455463
Brain Res. 2009 Feb 23;1256:43-54
pubmed: 19133245
Pharmacol Ther. 1994 Aug;63(2):187-98
pubmed: 7809179
Curr Opin Neurobiol. 2008 Jun;18(3):276-83
pubmed: 18655834
Proc Natl Acad Sci U S A. 2020 May 12;117(19):10339-10349
pubmed: 32341164
Exp Neurol. 2013 Sep;247:653-62
pubmed: 23510761
J Neurosci. 2011 May 18;31(20):7365-79
pubmed: 21593321
J Neurosci. 2002 Feb 15;22(4):1303-15
pubmed: 11850458
J Neurosci. 2015 Jul 01;35(26):9754-63
pubmed: 26134657
Cold Spring Harb Perspect Biol. 2022 Mar 1;14(3):
pubmed: 34518340
Nat Struct Mol Biol. 2013 Apr;20(4):469-76
pubmed: 23454976
Neuron. 2015 May 20;86(4):971-984
pubmed: 25959730
Nat Methods. 2017 Oct;14(10):979-982
pubmed: 28825705
Proc Natl Acad Sci U S A. 2016 Feb 16;113(7):1937-42
pubmed: 26831088
Neuron. 2016 Mar 2;89(5):956-70
pubmed: 26898779
Cell. 2021 Jun 24;184(13):3573-3587.e29
pubmed: 34062119
Int Rev Neurobiol. 2012;105:141-73
pubmed: 23206599
J Biol Chem. 2009 May 1;284(18):11755-9
pubmed: 19117948
Neuron. 2019 Jul 3;103(1):39-51.e5
pubmed: 31122676
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Cell Rep. 2020 Jan 28;30(4):1164-1177.e7
pubmed: 31995756
Nat Methods. 2017 Nov;14(11):1083-1086
pubmed: 28991892
Mol Neurobiol. 2006 Dec;34(3):205-19
pubmed: 17308353
J Cell Sci. 2008 Feb 1;121(Pt 3):249-53
pubmed: 18216329
Ophthalmic Res. 2021;64(3):345-355
pubmed: 33454713
Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11563-8
pubmed: 11016970
Neuron. 2022 Aug 17;110(16):2607-2624.e8
pubmed: 35767995
Development. 2017 Oct 1;144(19):3417-3429
pubmed: 28974639
Nature. 2011 Nov 06;480(7377):372-5
pubmed: 22056987
Invest Ophthalmol Vis Sci. 2016 Jun 1;57(7):3470-6
pubmed: 27367513
Neuron. 2020 Oct 14;108(1):128-144.e9
pubmed: 32810432
Mol Neurobiol. 1995 Apr-Jun;10(2-3):91-103
pubmed: 7576312
Genome Biol. 2004;5(10):R80
pubmed: 15461798
Invest Ophthalmol Vis Sci. 2013 Oct 23;54(10):6903-16
pubmed: 24154996
Cell. 2015 Jul 2;162(1):184-97
pubmed: 26095251
Neuron. 2012 Feb 9;73(3):445-52
pubmed: 22325198
Nat Biotechnol. 2018 Jun;36(5):421-427
pubmed: 29608177
Endocrinology. 2009 Jun;150(6):2758-66
pubmed: 19213842
Immunity. 2012 Feb 24;36(2):239-50
pubmed: 22342841
Leukemia. 2007 May;21(5):868-76
pubmed: 17361230
Neural Regen Res. 2022 Jun;17(6):1172-1182
pubmed: 34782551
Nature. 2020 May;581(7806):77-82
pubmed: 32376949
Nat Neurosci. 2016 Aug;19(8):1073-84
pubmed: 27399843
Science. 2008 Nov 7;322(5903):963-6
pubmed: 18988856
Neurobiol Dis. 2013 Mar;51:202-13
pubmed: 23194670
Neuron. 1999 May;23(1):83-91
pubmed: 10402195
Brain. 2020 Jul 1;143(7):2009-2026
pubmed: 32651949
Neuron. 2015 Mar 18;85(6):1244-56
pubmed: 25754821
Neuroscientist. 2014 Jan 6;20(4):343-358
pubmed: 24395337
Cell. 2007 Jun 29;129(7):1261-74
pubmed: 17604717
Neuron. 1999 Jan;22(1):89-101
pubmed: 10027292
Nat Protoc. 2020 Jul;15(7):2247-2276
pubmed: 32561888
J Cell Biochem. 2004 Oct 1;93(2):242-50
pubmed: 15368352
Nat Biotechnol. 2014 Apr;32(4):381-386
pubmed: 24658644
Brain. 2007 Dec;130(Pt 12):3308-20
pubmed: 17971355
J Neurosci. 2020 Jul 1;40(27):5177-5195
pubmed: 32457074
Nature. 2019 Feb;566(7745):496-502
pubmed: 30787437
Cell Rep. 2018 Aug 14;24(7):1865-1879.e9
pubmed: 30110642
Nat Rev Cancer. 2011 Feb;11(2):111-21
pubmed: 21248786
Mol Neurodegener. 2017 Oct 2;12(1):71
pubmed: 28969695
FASEB J. 1993 Jul;7(10):896-903
pubmed: 8393820
Curr Biol. 2014 Feb 3;24(3):310-5
pubmed: 24440397
Neuron. 2016 May 4;90(3):437-51
pubmed: 27151637
Exp Eye Res. 2005 Nov;81(5):551-60
pubmed: 15913606
Neuron. 2009 Dec 10;64(5):617-23
pubmed: 20005819
J Neurosci. 2015 Jan 21;35(3):943-59
pubmed: 25609613
Sci Rep. 2018 Aug 22;8(1):12565
pubmed: 30135567
Cell. 2014 Nov 6;159(4):896-910
pubmed: 25417164
Nature. 1984 Jun 28-Jul 4;309(5971):791-3
pubmed: 6204205
Nat Commun. 2017 Jan 16;8:14049
pubmed: 28091601
Neuron. 2019 Aug 21;103(4):642-657.e7
pubmed: 31255486
Life Sci Alliance. 2019 Jun 5;2(3):
pubmed: 31167803
Semin Cell Dev Biol. 2008 Aug;19(4):414-22
pubmed: 18708154
Genome Biol. 2006;7(10):R100
pubmed: 17076895
Mol Neurobiol. 2014 Dec;50(3):945-70
pubmed: 24752592

Auteurs

Anne Jacobi (A)

F.M. Kirby Neurobiology Center, Boston Children's Hospital, and Department of Neurology, Harvard Medical School, 300 Longwood Avenue, Boston, MA 02115, USA; Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, 52 Oxford Street, Cambridge, MA 02138, USA.

Nicholas M Tran (NM)

Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, 52 Oxford Street, Cambridge, MA 02138, USA; Department of Molecular and Human Genetics, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA.

Wenjun Yan (W)

Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, 52 Oxford Street, Cambridge, MA 02138, USA.

Inbal Benhar (I)

Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA.

Feng Tian (F)

F.M. Kirby Neurobiology Center, Boston Children's Hospital, and Department of Neurology, Harvard Medical School, 300 Longwood Avenue, Boston, MA 02115, USA.

Rebecca Schaffer (R)

Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, 52 Oxford Street, Cambridge, MA 02138, USA.

Zhigang He (Z)

F.M. Kirby Neurobiology Center, Boston Children's Hospital, and Department of Neurology, Harvard Medical School, 300 Longwood Avenue, Boston, MA 02115, USA. Electronic address: zhigang.he@childrens.harvard.edu.

Joshua R Sanes (JR)

Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, 52 Oxford Street, Cambridge, MA 02138, USA. Electronic address: sanesj@mcb.harvard.edu.

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Overlapping transcriptional programs promote...
questionsmedicales.fr › Cellules › Neurones › Neurofibres › Axones › Overlapping transcriptional programs promote...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Survie cellulaire › Overlapping transcriptional programs promote...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Overlapping transcriptional programs promote...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Overlapping transcriptional programs promote...
questionsmedicales.fr › Phénomènes biologiques › Régénération › Régénération nerveuse › Overlapping transcriptional programs promote...
questionsmedicales.fr › Plaies et blessures › Traumatismes du système nerveux › Traumatismes cranioencéphaliques › Lésions traumatiques des nerfs crâniens › Lésions traumatiques du nerf optique › Overlapping transcriptional programs promote...
questionsmedicales.fr › Cellules › Neurones › Neurones afférents › Neurones rétiniens › Cellules ganglionnaires rétiniennes › Overlapping transcriptional programs promote...