Therapeutic Potential of B-1a Cells in Intestinal Ischemia-Reperfusion Injury.


Journal

The Journal of surgical research
ISSN: 1095-8673
Titre abrégé: J Surg Res
Pays: United States
ID NLM: 0376340

Informations de publication

Date de publication:
12 2021
Historique:
received: 22 02 2021
revised: 14 06 2021
accepted: 29 06 2021
pubmed: 17 8 2021
medline: 7 4 2022
entrez: 16 8 2021
Statut: ppublish

Résumé

Acute mesenteric ischemia is a common surgical emergency. Restoration of blood flow is a critical objective of treating this pathology. However, many patients suffer from ischemia-reperfusion (I/R) injuries at the time of revascularization, requiring prolonged hospitalizations. B-1a cells are a subtype of B lymphocytes with roles in regulating inflammation and tissue injury by spontaneous release of natural IgM and IL-10. We hypothesized that treatment with B-1a cells protects mice from intestinal I/R. Mesenteric ischemia was induced in mice by placing a vascular clip on the superior mesenteric artery for 60 minutes. At the time of reperfusion, B-1a cells or PBS control were instilled into the peritoneal cavity (PerC) of mice. PerC lavage, blood, intestine, and lungs were collected 4 h after reperfusion. Serum organ injury and inflammatory markers such as ALT, AST, LDH, lactate, IL-6, as well as lung and gut histology and myeloperoxidase (MPO) were assessed. In intestinal I/R, B-1a cell frequency and number in the PerC were significantly decreased compared to sham-operated mice. There was an increase in the serum levels of ALT, AST, LDH, lactate, and IL-6 when comparing the vehicle group with the sham group. These increases were significantly reduced in the B-1a cell treated group. B-1a cell treatment significantly decreased the intestine and lung injury scores as well as MPO content, compared to vehicle treated mice. B-1a cell treatment resulted in a reduction of apoptotic cells in these tissues. Serum IgM levels were decreased in intestinal I/R, while treatment with B-1a cells significantly increased their levels towards normal levels. B-1a cell treatment at the time of mesenteric reperfusion ameliorates end organ damage and reduces systemic inflammation through the improvement of serum IgM levels. Preserving B-1a cells pool could serve as a novel therapeutic avenue in intestinal I/R injury.

Sections du résumé

BACKGROUND
Acute mesenteric ischemia is a common surgical emergency. Restoration of blood flow is a critical objective of treating this pathology. However, many patients suffer from ischemia-reperfusion (I/R) injuries at the time of revascularization, requiring prolonged hospitalizations. B-1a cells are a subtype of B lymphocytes with roles in regulating inflammation and tissue injury by spontaneous release of natural IgM and IL-10. We hypothesized that treatment with B-1a cells protects mice from intestinal I/R.
METHODS
Mesenteric ischemia was induced in mice by placing a vascular clip on the superior mesenteric artery for 60 minutes. At the time of reperfusion, B-1a cells or PBS control were instilled into the peritoneal cavity (PerC) of mice. PerC lavage, blood, intestine, and lungs were collected 4 h after reperfusion. Serum organ injury and inflammatory markers such as ALT, AST, LDH, lactate, IL-6, as well as lung and gut histology and myeloperoxidase (MPO) were assessed.
RESULTS
In intestinal I/R, B-1a cell frequency and number in the PerC were significantly decreased compared to sham-operated mice. There was an increase in the serum levels of ALT, AST, LDH, lactate, and IL-6 when comparing the vehicle group with the sham group. These increases were significantly reduced in the B-1a cell treated group. B-1a cell treatment significantly decreased the intestine and lung injury scores as well as MPO content, compared to vehicle treated mice. B-1a cell treatment resulted in a reduction of apoptotic cells in these tissues. Serum IgM levels were decreased in intestinal I/R, while treatment with B-1a cells significantly increased their levels towards normal levels.
CONCLUSIONS
B-1a cell treatment at the time of mesenteric reperfusion ameliorates end organ damage and reduces systemic inflammation through the improvement of serum IgM levels. Preserving B-1a cells pool could serve as a novel therapeutic avenue in intestinal I/R injury.

Identifiants

pubmed: 34399355
pii: S0022-4804(21)00460-1
doi: 10.1016/j.jss.2021.06.070
pmc: PMC8678159
mid: NIHMS1727763
pii:
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

326-336

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM129633
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL076179
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM118337
Pays : United States

Informations de copyright

Copyright © 2021. Published by Elsevier Inc.

Références

Nat Rev Immunol. 2010 Nov;10(11):778-86
pubmed: 20948548
Surgery. 2017 Oct;162(4):917-927
pubmed: 28709648
Science. 2012 Feb 3;335(6068):597-601
pubmed: 22245738
Circ Res. 2019 Oct 25;125(10):e55-e70
pubmed: 31549940
Redox Biol. 2015 Dec;6:524-551
pubmed: 26484802
JCI Insight. 2020 Mar 12;5(5):
pubmed: 32027619
Shock. 2001 Jan;15(1):1-10
pubmed: 11198350
Arch Surg. 1999 Dec;134(12):1342-7
pubmed: 10593332
J Exp Med. 1998 Dec 21;188(12):2381-6
pubmed: 9858525
Int Immunol. 2008 Jun;20(6):729-37
pubmed: 18375938
Cell Rep. 2016 Mar 15;14(10):2348-61
pubmed: 26947073
Shock. 2020 Nov;54(5):586-594
pubmed: 32604223
JCI Insight. 2020 Mar 12;5(5):
pubmed: 32027618
J Exp Med. 2014 Jun 2;211(6):1243-56
pubmed: 24821911
Surgery. 2020 Sep;168(3):478-485
pubmed: 32439208
Immunity. 2005 Jul;23(1):7-18
pubmed: 16039575
Am J Respir Cell Mol Biol. 2011 May;44(5):725-38
pubmed: 21531958
Front Immunol. 2020 Sep 11;11:586685
pubmed: 33042165
Crit Care Clin. 2005 Apr;21(2):177-96
pubmed: 15781156
Front Immunol. 2012 Jan 11;2:96
pubmed: 22566885
Am J Pathol. 2011 Feb;178(2):735-43
pubmed: 21281806
J Pathol. 2000 Feb;190(3):255-66
pubmed: 10685060
Immunol Res. 2015 Dec;63(1-3):153-66
pubmed: 26427372
Virulence. 2014 Jan 1;5(1):12-9
pubmed: 24193307
J Leukoc Biol. 2019 Jul;106(1):133-146
pubmed: 30645013
Immunobiology. 2016 Jul;221(7):845-52
pubmed: 26898918
Immunity. 2005 Jul;23(1):1-2
pubmed: 16039572
Acute Med Surg. 2020 Apr 13;7(1):e501
pubmed: 32431842
Nat Rev Immunol. 2016 May 27;16(6):378-91
pubmed: 27231052
Cell Res. 2000 Dec;10(4):245-66
pubmed: 11191348
Methods Mol Biol. 2019;1904:53-81
pubmed: 30539466
J Korean Med Sci. 2012 Jan;27(1):27-35
pubmed: 22219610
J Immunol. 2016 May 15;196(10):4348-57
pubmed: 27183643
Front Immunol. 2012 Apr 04;3:66
pubmed: 22566947
Curr Top Microbiol Immunol. 1996;210:167-79
pubmed: 8565555
Am J Pathol. 2010 May;176(5):2283-91
pubmed: 20348235
J Exp Med. 2011 Jan 17;208(1):67-80
pubmed: 21220451
J Exp Med. 2006 Oct 30;203(11):2541-50
pubmed: 17060475
N Engl J Med. 2011 Feb 17;364(7):656-65
pubmed: 21323543
Nat Rev Immunol. 2010 Dec;10(12):826-37
pubmed: 21088683
Ann N Y Acad Sci. 2013 May;1285:97-114
pubmed: 23692567
Proc Natl Acad Sci U S A. 2004 Mar 16;101(11):3886-91
pubmed: 14999103
J Pediatr Surg. 2005 Mar;40(3):470-7
pubmed: 15793720
J Immunol. 2017 Jul 15;199(2):750-760
pubmed: 28630091
Compr Physiol. 2016 Dec 6;7(1):113-170
pubmed: 28135002
Immunity. 2014 Nov 20;41(5):694-707
pubmed: 25517612
Cell Death Differ. 2017 Apr;24(4):683-693
pubmed: 28157209
Arch Intern Med. 2004 May 24;164(10):1054-62
pubmed: 15159262
Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3320-4
pubmed: 1565622
Curr Opin Immunol. 2008 Apr;20(2):149-57
pubmed: 18434123
Am J Respir Crit Care Med. 2005 Oct 1;172(7):798-806
pubmed: 16020801
Mol Med. 2018 May 29;24(1):26
pubmed: 30134811
Int Rev Cell Mol Biol. 2012;298:229-317
pubmed: 22878108
J Immunol. 2012 Feb 1;188(3):939-45
pubmed: 22262757

Auteurs

William Royster (W)

Center for Immunology and Inflammation, The Feinstein Institutes for Medical Research, Manhasset, New York; Elmezzi Graduate School of Molecular Medicine, Manhasset, New York; Department of Surgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Manhasset, Manhasset, New York.

Mahendar Ochani (M)

Center for Immunology and Inflammation, The Feinstein Institutes for Medical Research, Manhasset, New York.

Monowar Aziz (M)

Center for Immunology and Inflammation, The Feinstein Institutes for Medical Research, Manhasset, New York; Elmezzi Graduate School of Molecular Medicine, Manhasset, New York; Department of Surgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Manhasset, Manhasset, New York.

Ping Wang (P)

Center for Immunology and Inflammation, The Feinstein Institutes for Medical Research, Manhasset, New York; Elmezzi Graduate School of Molecular Medicine, Manhasset, New York; Department of Surgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Manhasset, Manhasset, New York; Department of Molecular Medicine, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Manhasset, New York. Electronic address: pwang@northwell.edu.

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