Recovery of Forearm and Fine Digit Function After Chronic Spinal Cord Injury by Simultaneous Blockade of Inhibitory Matrix Chondroitin Sulfate Proteoglycan Production and the Receptor PTPσ.
CSPGs
axon regeneration
axon sprouting
perineuronal net
receptor PTPσ
spinal cord injury
Journal
Journal of neurotrauma
ISSN: 1557-9042
Titre abrégé: J Neurotrauma
Pays: United States
ID NLM: 8811626
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
medline:
5
12
2023
pubmed:
22
8
2023
entrez:
22
8
2023
Statut:
ppublish
Résumé
Spinal cord injuries (SCI), for which there are limited effective treatments, result in enduring paralysis and hypoesthesia, in part because of the inhibitory microenvironment that develops and limits regeneration/sprouting, especially during chronic stages. Recently, we discovered that targeted enzymatic removal of the inhibitory chondroitin sulfate proteoglycan (CSPG) component of the extracellular and perineuronal net (PNN) matrix via Chondroitinase ABC (ChABC) rapidly restored robust respiratory function to the previously paralyzed hemi-diaphragm after remarkably long times post-injury (up to 1.5 years) following a cervical level 2 lateral hemi-transection. Importantly, ChABC treatment at cervical level 4 in this chronic model also elicited improvements in gross upper arm function. In the present study, we focused on arm and hand function, seeking to highlight and optimize crude as well as fine motor control of the forearm and digits at lengthy chronic stages post-injury. However, instead of using ChABC, we utilized a novel and more clinically relevant systemic combinatorial treatment strategy designed to simultaneously reduce and overcome inhibitory CSPGs. Following a 3-month upper cervical spinal hemi-lesion using adult female Sprague Dawley rats, we show that the combined treatment had a profound effect on functional recovery of the chronically paralyzed forelimb and paw, as well as on precision movements of the digits. The regenerative and immune system related events that we describe deepen our basic understanding of the crucial role of CSPG-mediated inhibition via the PTPσ receptor in constraining functional synaptic plasticity at lengthy time points following SCI, hopefully leading to clinically relevant translational benefits.
Identifiants
pubmed: 37606910
doi: 10.1089/neu.2023.0117
pmc: PMC10698859
doi:
Substances chimiques
Chondroitin ABC Lyase
EC 4.2.2.20
Chondroitin Sulfate Proteoglycans
0
Receptor-Like Protein Tyrosine Phosphatases, Class 2
EC 3.1.3.48
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2500-2521Références
Cell. 2018 Sep 6;174(6):1599
pubmed: 30193115
Bioact Mater. 2022 Jul 22;25:766-782
pubmed: 37056263
J Neurotrauma. 2004 Oct;21(10):1371-83
pubmed: 15672628
Dev Cell. 2022 Feb 28;57(4):440-450.e7
pubmed: 34986324
Mater Sci Eng C Mater Biol Appl. 2020 May;110:110656
pubmed: 32204084
Semin Cancer Biol. 2020 May;62:9-19
pubmed: 31319162
J Mol Histol. 2019 Jun;50(3):203-216
pubmed: 30903543
Cells. 2023 May 31;12(11):
pubmed: 37296640
J Neurosci. 2011 Jun 22;31(25):9332-44
pubmed: 21697383
J Neurosci Methods. 2014 Apr 15;226:124-131
pubmed: 24468219
Exp Neurol. 2022 Aug;354:114098
pubmed: 35504345
J Cell Biol. 1984 Feb;98(2):773-6
pubmed: 6537954
Adv Healthc Mater. 2022 Oct;11(19):e2200206
pubmed: 35882512
Front Cell Dev Biol. 2021 Jun 16;9:702179
pubmed: 34222264
Front Mol Neurosci. 2023 Jun 22;16:1206245
pubmed: 37426069
Biochim Biophys Acta. 2012 Jan;1824(1):68-88
pubmed: 22024571
Sci Adv. 2020 Aug 19;6(34):eabc6378
pubmed: 32875119
Exp Neurol. 2008 Aug;212(2):348-57
pubmed: 18534577
Brain. 2018 Aug 1;141(8):2362-2381
pubmed: 29912283
Br J Pharmacol. 2019 Sep;176(18):3611-3621
pubmed: 30924524
J Neuroinflammation. 2022 Aug 18;19(1):207
pubmed: 35982473
Neuroscientist. 2023 Oct;29(5):569-590
pubmed: 35872660
Front Cell Neurosci. 2023 May 24;17:1180825
pubmed: 37293626
Sci Transl Med. 2015 Aug 26;7(302):302ra134
pubmed: 26311729
Curr Opin Neurobiol. 2014 Aug;27:171-8
pubmed: 24762654
Exp Neurol. 2015 Dec;274(Pt B):115-25
pubmed: 26315937
Curr Opin Neurobiol. 2007 Feb;17(1):120-7
pubmed: 17223033
Exp Neurol. 2012 May;235(1):174-87
pubmed: 21952042
J Neuroinflammation. 2018 Mar 20;15(1):90
pubmed: 29558941
Front Neural Circuits. 2017 Oct 09;11:72
pubmed: 29062274
J Neurosci. 2004 Feb 11;24(6):1393-7
pubmed: 14960611
Cell Rep. 2013 Nov 14;5(3):573-81
pubmed: 24183669
Front Cell Neurosci. 2020 Aug 05;14:208
pubmed: 32848612
Nat Neurosci. 2004 Mar;7(3):269-77
pubmed: 14966523
Nat Commun. 2018 Oct 8;9(1):4126
pubmed: 30297691
Nature. 2011 Jul 13;475(7355):196-200
pubmed: 21753849
Cell Mol Neurobiol. 2023 Aug;43(6):2925-2937
pubmed: 36913114
Nat Neurosci. 2009 Sep;12(9):1145-51
pubmed: 19668200
J Comp Neurol. 2008 Dec 10;511(5):692-709
pubmed: 18924146
Stem Cells. 2015 Aug;33(8):2550-63
pubmed: 25703008
Lancet Neurol. 2014 Dec;13(12):1241-56
pubmed: 25453463
J Neurotrauma. 2020 Feb 1;37(3):572-579
pubmed: 31392919
Clin Neurophysiol. 2011 Apr;122(4):796-802
pubmed: 21075681
J Neurosurg. 2003 Sep;99(2 Suppl):188-97
pubmed: 12956462
Nat Neurosci. 2018 Apr;21(4):576-588
pubmed: 29556028
J Neurosci. 2004 Jul 21;24(29):6531-9
pubmed: 15269264
Brain Res Bull. 2022 Nov;190:179-194
pubmed: 36216273
Cell Mol Life Sci. 2000 Feb;57(2):276-89
pubmed: 10766023
J Neurosci. 2014 Apr 2;34(14):4822-36
pubmed: 24695702
Dev Neurobiol. 2011 Nov;71(11):1006-17
pubmed: 21898854
Dev Biol. 1990 Apr;138(2):359-76
pubmed: 1690673
Science. 1992 Feb 7;255(5045):733-6
pubmed: 1738848
Elife. 2018 May 15;7:
pubmed: 29762123
Exp Neurol. 2015 Jul;269:169-87
pubmed: 25900055
PLoS One. 2012;7(5):e37589
pubmed: 22629425
Nat Neurosci. 2016 Jun;19(6):784-7
pubmed: 27089020
Nat Rev Neurosci. 2004 Feb;5(2):146-56
pubmed: 14735117
Nature. 2015 Feb 19;518(7539):404-8
pubmed: 25470046
J Neurotrauma. 1995 Feb;12(1):1-21
pubmed: 7783230
Ann Biomed Eng. 2019 Mar;47(3):744-753
pubmed: 30627839
J Neurosci. 2018 Jun 6;38(23):5399-5414
pubmed: 29760175
Spine (Phila Pa 1976). 2001 Dec 15;26(24 Suppl):S2-12
pubmed: 11805601
J Physiol. 2021 Feb;599(4):1199-1224
pubmed: 33146892
J Neurosci. 2023 Mar 1;43(9):1492-1508
pubmed: 36653191
J Appl Physiol (1985). 2003 Feb;94(2):795-810
pubmed: 12531916
J Neurosci. 2006 Apr 19;26(16):4406-14
pubmed: 16624960
Trends Neurosci. 2008 Jan;31(1):44-52
pubmed: 18063497
J Neurotrauma. 2019 Jun 15;36(12):1985-1999
pubmed: 30565484
Annu Rev Cell Dev Biol. 2018 Oct 6;34:495-521
pubmed: 30044649
Adv Sci (Weinh). 2023 Jul;10(20):e2205804
pubmed: 37296073
J Neurosci. 2014 Sep 17;34(38):12690-700
pubmed: 25232107
J Cell Sci. 2008 Sep 15;121(Pt 18):3083-91
pubmed: 18768934
Sci Rep. 2015 Oct 14;5:14923
pubmed: 26464223
Proc Natl Acad Sci U S A. 2013 Mar 5;110(10):4057-62
pubmed: 23345436
Front Neurol. 2014 Jul 07;5:116
pubmed: 25071704
Sci Rep. 2023 Nov 6;13(1):19183
pubmed: 37932336
Exp Neurol. 2023 Aug;366:114444
pubmed: 37196696
Aging (Albany NY). 2017 Jun 28;9(6):1607-1622
pubmed: 28657900
J Neurosci. 2009 Sep 30;29(39):12145-58
pubmed: 19793972
Neuron. 2017 Apr 19;94(2):337-346.e6
pubmed: 28426967
Trends Neurosci. 2013 Sep;36(9):522-34
pubmed: 23835198
J Neurosci. 1998 Jul 15;18(14):5203-11
pubmed: 9651203
Neurosci Res. 2016 Dec;113:37-47
pubmed: 27497528
Exp Neurol. 2014 Nov;261:440-50
pubmed: 25086272
Proc Natl Acad Sci U S A. 2012 Mar 27;109(13):4768-73
pubmed: 22411830
Elife. 2020 Jan 27;9:
pubmed: 31985401
Exp Neurol. 2018 Nov;309:148-159
pubmed: 30118740
Nat Commun. 2015 Feb 02;6:6235
pubmed: 25639594
Neuroscientist. 2005 Apr;11(2):161-73
pubmed: 15746384
Exp Neurol. 2015 Apr;266:112-9
pubmed: 25666586
J Neurosci. 2008 Nov 12;28(46):11998-2009
pubmed: 19005065
Physiol Rev. 2018 Apr 1;98(2):881-917
pubmed: 29513146
Neuropsychopharmacology. 1999 Aug;21(2 Suppl):9S-15S
pubmed: 10432483
JACC Basic Transl Sci. 2022 Aug 24;7(9):915-930
pubmed: 36317132
J Neurosci. 2011 Apr 13;31(15):5605-16
pubmed: 21490201
Curr Opin Cell Biol. 2005 Oct;17(5):524-32
pubmed: 16112853
Cell Rep. 2022 Jul 26;40(4):111137
pubmed: 35905716
Neural Regen Res. 2021 Aug;16(8):1598-1605
pubmed: 33433490
Exp Neurol. 2005 May;193(1):19-28
pubmed: 15817261
Mol Cell Neurosci. 2009 Sep;42(1):1-10
pubmed: 19467332
Int J Mol Sci. 2021 Feb 28;22(5):
pubmed: 33670945
J Neurosci. 2011 Oct 5;31(40):14051-66
pubmed: 21976490
Prog Neurobiol. 2021 May;200:101983
pubmed: 33422662
Neurobiol Dis. 2021 Jan;147:105153
pubmed: 33127470
Trends Cell Biol. 2013 Oct;23(10):465-75
pubmed: 23916315
Small. 2023 Feb;19(6):e2205012
pubmed: 36398653
J Neurosci. 2008 Dec 24;28(52):14107-20
pubmed: 19109493
Exp Neurol. 1999 Nov;160(1):51-65
pubmed: 10630190
J Neurosci. 2010 Feb 3;30(5):1657-76
pubmed: 20130176
Proc Natl Acad Sci U S A. 2010 Feb 23;107(8):3340-5
pubmed: 19884507
World Neurosurg. 2018 May;113:e345-e363
pubmed: 29454115
Nat Commun. 2018 Nov 27;9(1):4843
pubmed: 30482901
Nat Chem Biol. 2019 Jul;15(7):699-709
pubmed: 31061498
Neuroscience. 1994 Jul;61(1):133-9
pubmed: 7969888
Science. 2009 Oct 23;326(5952):592-6
pubmed: 19833921
Front Behav Neurosci. 2023 Mar 14;17:1114789
pubmed: 36998537
Front Immunol. 2015 Mar 23;6:123
pubmed: 25852691
Brain Res. 2000 Mar 31;860(1-2):104-11
pubmed: 10727628
Nat Rev Neurosci. 2013 Oct;14(10):722-9
pubmed: 23985834
J Control Release. 2019 Mar 10;297:14-25
pubmed: 30690102
Learn Mem. 1999 Nov-Dec;6(6):542-71
pubmed: 10641762
Neurosci Res. 1986 Sep;3(6):617-27
pubmed: 3774241
Nat Neurosci. 2009 Apr;12(4):428-37
pubmed: 19252495
Sci Rep. 2019 Sep 26;9(1):13939
pubmed: 31558805
Exp Neurol. 2008 Feb;209(2):426-45
pubmed: 17540369
Matrix Biol. 2001 Feb;20(1):23-35
pubmed: 11246001
J Neurosci. 2019 Sep 11;39(37):7306-7320
pubmed: 31395620
J Physiol. 1895 Apr 6;17(6):455-85
pubmed: 16992199
Proc Natl Acad Sci U S A. 2001 Mar 13;98(6):3513-8
pubmed: 11248109
Proc Natl Acad Sci U S A. 2013 Jul 23;110(30):12456-61
pubmed: 23832785
Biochim Biophys Acta Gen Subj. 2017 Oct;1861(10):2435-2441
pubmed: 28596106
J Neurosci. 2010 Jun 9;30(23):7761-9
pubmed: 20534825
Respir Physiol Neurobiol. 2009 Nov 30;169(2):85-93
pubmed: 19539790
Am J Physiol. 1951 Aug;166(2):241-54
pubmed: 14857171
Glia. 2021 Jan;69(1):182-200
pubmed: 32865286