L-Arginine Depletion Improves Spinal Cord Injury via Immunomodulation and Nitric Oxide Reduction.

CNS trauma T cells arginase-1 neuroinflammation nitric oxide

Journal

Biomedicines
ISSN: 2227-9059
Titre abrégé: Biomedicines
Pays: Switzerland
ID NLM: 101691304

Informations de publication

Date de publication:
18 Jan 2022
Historique:
received: 01 10 2021
revised: 03 12 2021
accepted: 12 01 2022
entrez: 25 2 2022
pubmed: 26 2 2022
medline: 26 2 2022
Statut: epublish

Résumé

Spinal cord injury (SCI) elicits robust neuroinflammation that eventually exacerbates the initial damage to the spinal cord. L-arginine is critical for the responsiveness of T cells, which are important contributors to neuroinflammation after SCI. Furthermore, L-arginine is the substrate for nitric oxide (NO) production, which is a known inducer of secondary damage. To accomplish systemic L-arginine depletion, repetitive injections of recombinant arginase-1 (rArg-I) were performed. Functional recovery and histopathological parameters were analyzed. Splenic immune responses were evaluated by flow cytometry. Pro-inflammatory gene expression and nitrite concentrations were measured. We show for the first time that systemic L-arginine depletion improves locomotor recovery. Flow cytometry and immunohistological analysis showed that intraspinal T-cell infiltration was reduced by 65%, and peripheral numbers of Th1 and Th17 cells were suppressed. Moreover, rArg-I treatment reduced the intraspinal NO production by 40%. Histopathological analyses revealed a 37% and 36% decrease in the number of apoptotic neurons and neuron-macrophage/microglia contacts in the spinal cord, respectively. Targeting detrimental T-cell responses and NO-production via rArg-I led to a reduced neuronal cell death and an improved functional recovery. These findings indicate that L-arginine depletion holds promise as a therapeutic strategy after SCI.

Sections du résumé

BACKGROUND BACKGROUND
Spinal cord injury (SCI) elicits robust neuroinflammation that eventually exacerbates the initial damage to the spinal cord. L-arginine is critical for the responsiveness of T cells, which are important contributors to neuroinflammation after SCI. Furthermore, L-arginine is the substrate for nitric oxide (NO) production, which is a known inducer of secondary damage.
METHODS METHODS
To accomplish systemic L-arginine depletion, repetitive injections of recombinant arginase-1 (rArg-I) were performed. Functional recovery and histopathological parameters were analyzed. Splenic immune responses were evaluated by flow cytometry. Pro-inflammatory gene expression and nitrite concentrations were measured.
RESULTS RESULTS
We show for the first time that systemic L-arginine depletion improves locomotor recovery. Flow cytometry and immunohistological analysis showed that intraspinal T-cell infiltration was reduced by 65%, and peripheral numbers of Th1 and Th17 cells were suppressed. Moreover, rArg-I treatment reduced the intraspinal NO production by 40%. Histopathological analyses revealed a 37% and 36% decrease in the number of apoptotic neurons and neuron-macrophage/microglia contacts in the spinal cord, respectively.
CONCLUSIONS CONCLUSIONS
Targeting detrimental T-cell responses and NO-production via rArg-I led to a reduced neuronal cell death and an improved functional recovery. These findings indicate that L-arginine depletion holds promise as a therapeutic strategy after SCI.

Identifiants

pubmed: 35203413
pii: biomedicines10020205
doi: 10.3390/biomedicines10020205
pmc: PMC8869469
pii:
doi:

Types de publication

Journal Article

Langues

eng

Subventions

Organisme : Research Foundation - Flanders
ID : G067715N
Organisme : Research Foundation - Flanders
ID : G091518N
Organisme : Research Foundation - Flanders
ID : G0C2120N
Organisme : Stichting MS Research
ID : N.A.
Organisme : MS International Federation (MSIF) and MoveS
ID : N.A.

Références

Exp Neurol. 2012 Oct;237(2):274-85
pubmed: 22868200
Cell. 2016 Oct 20;167(3):829-842.e13
pubmed: 27745970
Blood. 2003 Jun 1;101(11):4260-6
pubmed: 12576317
J Clin Pathol. 2006 Nov;59(11):1151-9
pubmed: 17071802
Trends Immunol. 2003 Jun;24(6):302-6
pubmed: 12810105
Arq Neuropsiquiatr. 2017 Jun;75(6):387-393
pubmed: 28658409
Eur J Immunol. 2016 Jan;46(1):92-103
pubmed: 26449889
Ann Clin Biochem. 1989 Nov;26 ( Pt 6):547-53
pubmed: 2515788
Mediators Inflamm. 1998;7(4):239-55
pubmed: 9792334
Exp Neurol. 2014 Aug;258:78-90
pubmed: 25017889
Pediatr Res. 2015 Feb;77(2):290-7
pubmed: 25360828
Int J Mol Sci. 2021 May 26;22(11):
pubmed: 34073458
J Cell Sci. 2010 May 15;123(Pt 10):1652-62
pubmed: 20406886
Biochem J. 1998 Nov 15;336 ( Pt 1):1-17
pubmed: 9806879
J Neurotrauma. 2001 May;18(5):523-32
pubmed: 11393255
Brain. 2010 Feb;133(Pt 2):433-47
pubmed: 20085927
J Neurotrauma. 1996 Sep;13(9):537-48
pubmed: 8913970
J Immunol. 2014 Aug 15;193(4):1717-27
pubmed: 25015834
Exp Neurol. 1998 May;151(1):77-88
pubmed: 9582256
J Neuropathol Exp Neurol. 2003 Nov;62(11):1096-107
pubmed: 14656068
J Clin Neurosci. 2000 May;7(3):238-43
pubmed: 10833623
Scand J Immunol. 2015 May;81(5):284-90
pubmed: 25651871
J Neurosci. 2008 Sep 17;28(38):9330-41
pubmed: 18799667
Cell Death Dis. 2012 Aug 09;3:e363
pubmed: 22875000
Brain Behav Immun. 2019 Aug;80:129-145
pubmed: 30851378
J Neuroimmunol. 2007 Mar;184(1-2):100-12
pubmed: 17198734
J Comp Neurol. 2006 Feb 1;494(4):578-94
pubmed: 16374800
Spinal Cord. 2008 Feb;46(2):113-7
pubmed: 17420770
J Trauma. 2011 May;70(5):1198-202
pubmed: 20693923
J Endod. 2012 Apr;38(4):475-80
pubmed: 22414832
FASEB J. 2016 May;30(5):2040-57
pubmed: 26917739
J Clin Biochem Nutr. 2012 Jul;51(1):68-75
pubmed: 22798716
J Neurochem. 2000 Nov;75(5):2144-54
pubmed: 11032904
J Comp Neurol. 1997 Jan 20;377(3):443-64
pubmed: 8989657
J Biol Chem. 2002 Jun 14;277(24):21123-9
pubmed: 11950832
J Comp Neurol. 2003 Jul 21;462(2):223-40
pubmed: 12794745
Cancer Res. 2007 Jan 1;67(1):309-17
pubmed: 17210712
Naunyn Schmiedebergs Arch Pharmacol. 1997 Apr;355(4):447-51
pubmed: 9109359
Front Immunol. 2017 Jul 24;8:864
pubmed: 28791021
J Neurotrauma. 2010 Feb;27(2):411-21
pubmed: 19831737
Blood. 2007 Feb 15;109(4):1568-73
pubmed: 17023580
J Neuroimmunol. 2016 Jan 15;290:96-102
pubmed: 26711577
J Neurotrauma. 2006 May;23(5):635-59
pubmed: 16689667
Cell Immunol. 2004 Nov-Dec;232(1-2):21-31
pubmed: 15922712
Exp Neurol. 2016 Mar;277:190-201
pubmed: 26772636
J Neurosci. 2006 Aug 16;26(33):8512-6
pubmed: 16914676
Exp Neurol. 2013 Sep;247:226-40
pubmed: 23664962
J Vis Exp. 2012 Aug 15;(66):e3814
pubmed: 22929966
Eur J Immunol. 2009 Aug;39(8):2161-72
pubmed: 19637195
Eur J Neurosci. 1994 May 1;6(5):712-24
pubmed: 8075816
J Neurotrauma. 2006 May;23(5):660-73
pubmed: 16689668
Prog Brain Res. 2002;137:401-6
pubmed: 12440382
Nat Rev Immunol. 2007 Dec;7(12):964-74
pubmed: 18037898
Surgery. 1978 Aug;84(2):224-30
pubmed: 684614
Cancer Res. 2002 Oct 1;62(19):5443-50
pubmed: 12359751
Exp Neurol. 2003 Nov;184(1):456-63
pubmed: 14637115
Brain Res. 1993 Apr 23;609(1-2):293-7
pubmed: 8508311
Exp Neurobiol. 2018 Oct;27(5):437-452
pubmed: 30429652
J Neuroimmunol. 2013 Aug 15;261(1-2):7-20
pubmed: 23711349
J Neurosci. 2005 Jul 13;25(28):6576-83
pubmed: 16014718
Neuron. 2012 Jun 7;74(5):777-91
pubmed: 22681683
J Neurosci. 2004 Apr 14;24(15):3752-61
pubmed: 15084655
Eur Surg Res. 2005 Nov-Dec;37(6):323-9
pubmed: 16465055
Lancet. 2000 Jan 22;355(9200):286-7
pubmed: 10675079
J Neurosci Res. 2001 Jun 15;64(6):582-9
pubmed: 11398181
World Neurosurg. 2017 Jan;97:98-103
pubmed: 27717775
J Nutr. 2016 Dec;146(12):2579S-2586S
pubmed: 27934648

Auteurs

Céline Erens (C)

Department of Immunology and Infection, Biomedical Research Institute, Hasselt University, 3590 Diepenbeek, Belgium.

Jana Van Broeckhoven (J)

Department of Immunology and Infection, Biomedical Research Institute, Hasselt University, 3590 Diepenbeek, Belgium.

Cindy Hoeks (C)

Department of Immunology and Infection, Biomedical Research Institute, Hasselt University, 3590 Diepenbeek, Belgium.

Gernot Schabbauer (G)

Institute for Vascular Biology, Center for Physiology and Pharmacology, Medical University of Vienna, A-1090 Vienna, Austria.
Christian Doppler Laboratory for Arginine Metabolism in Rheumatoid Arthritis and Multiple Sclerosis, Centre of Physiology and Pharmacology, Medical University of Vienna, A-1090 Vienna, Austria.

Paul N Cheng (PN)

Department Research and Development, Bio-Cancer Treatment International Limited, Hong Kong 999077, China.

Li Chen (L)

Department Research and Development, Bio-Cancer Treatment International Limited, Hong Kong 999077, China.

Niels Hellings (N)

Department of Immunology and Infection, Biomedical Research Institute, Hasselt University, 3590 Diepenbeek, Belgium.

Bieke Broux (B)

Department of Immunology and Infection, Biomedical Research Institute, Hasselt University, 3590 Diepenbeek, Belgium.

Stefanie Lemmens (S)

Department of Immunology and Infection, Biomedical Research Institute, Hasselt University, 3590 Diepenbeek, Belgium.

Sven Hendrix (S)

Department of Immunology and Infection, Biomedical Research Institute, Hasselt University, 3590 Diepenbeek, Belgium.
Institute for Translational Medicine, Medical School Hamburg, 20457 Hamburg, Germany.

Classifications MeSH