دورية أكاديمية

Enteric glial cell network function is required for epithelial barrier restitution following intestinal ischemic injury in the early postnatal period.

التفاصيل البيبلوغرافية
العنوان: Enteric glial cell network function is required for epithelial barrier restitution following intestinal ischemic injury in the early postnatal period.
المؤلفون: Ziegler AL; Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, United States., Caldwell ML; Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, United States., Craig SE; Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, United States., Hellstrom EA; Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, United States., Sheridan AE; Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, United States., Touvron MS; Department of Molecular Biomedical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, United States., Pridgen TA; Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, United States., Magness ST; Joint Department of Biomedical Engineering, School of Medicine, University of North Carolina, Chapel Hill, North Carolina, United States., Odle J; Department of Animal Science, College of Agriculture and Life Sciences, North Carolina State University, Raleigh, North Carolina, United States., Van Landeghem L; Department of Molecular Biomedical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, United States., Blikslager AT; Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, United States.
المصدر: American journal of physiology. Gastrointestinal and liver physiology [Am J Physiol Gastrointest Liver Physiol] 2024 Mar 01; Vol. 326 (3), pp. G228-G246. Date of Electronic Publication: 2023 Dec 26.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: American Physiological Society Country of Publication: United States NLM ID: 100901227 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1522-1547 (Electronic) Linking ISSN: 01931857 NLM ISO Abbreviation: Am J Physiol Gastrointest Liver Physiol Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Bethesda, MD : American Physiological Society
مواضيع طبية MeSH: Neuroglia*/physiology , Intestine, Small*, Humans ; Animals ; Infant, Newborn ; Swine ; Intestines ; Intestinal Mucosa ; Jejunum ; Ischemia
مستخلص: Ischemic damage to the intestinal epithelial barrier, such as in necrotizing enterocolitis or small intestinal volvulus, is associated with higher mortality rates in younger patients. We have recently reported a powerful pig model to investigate these age-dependent outcomes in which mucosal barrier restitution is strikingly absent in neonates but can be rescued by direct application of homogenized mucosa from older, juvenile pigs by a yet-undefined mechanism. Within the mucosa, a postnatally developing network of enteric glial cells (EGCs) is gaining recognition as a key regulator of the mucosal barrier. Therefore, we hypothesized that the developing EGC network may play an important role in coordinating intestinal barrier repair in neonates. Neonatal and juvenile jejunal mucosa recovering from surgically induced intestinal ischemia was visualized by scanning electron microscopy and the transcriptomic phenotypes were assessed by bulk RNA sequencing. EGC network density and glial activity were examined by Gene Set Enrichment Analysis, three-dimensional (3-D) volume imaging, and Western blot and its function in regulating epithelial restitution was assessed ex vivo in Ussing chamber using the glia-specific inhibitor fluoroacetate (FA), and in vitro by coculture assay. Here we refine and elaborate our translational model, confirming a neonatal phenotype characterized by a complete lack of coordinated reparative signaling in the mucosal microenvironment. Furthermore, we report important evidence that the subepithelial EGC network changes significantly over the early postnatal period and demonstrate that the proximity of a specific functional population of EGC to wounded intestinal epithelium contributes to intestinal barrier restitution following ischemic injury. NEW & NOTEWORTHY This study refines a powerful translational pig model, defining an age-dependent relationship between enteric glia and the intestinal epithelium during intestinal ischemic injury and confirming an important role for enteric glial cell (EGC) activity in driving mucosal barrier restitution. This study suggests that targeting the enteric glial network could lead to novel interventions to improve recovery from intestinal injury in neonatal patients.
References: Physiology (Bethesda). 2018 Jul 1;33(4):269-280. (PMID: 29897300)
Cell Mol Gastroenterol Hepatol. 2016 Nov;2(6):716-724. (PMID: 28090566)
Am J Physiol Gastrointest Liver Physiol. 2017 Feb 1;312(2):G145-G152. (PMID: 28039160)
Neuron. 2015 Jan 21;85(2):289-95. (PMID: 25578362)
PLoS One. 2008;3(10):e3428. (PMID: 18927609)
Gastroenterology. 2007 Apr;132(4):1344-58. (PMID: 17408650)
EMBO Mol Med. 2021 Jan 11;13(1):e12724. (PMID: 33332729)
J Intern Med. 2008 Jun;263(6):577-83. (PMID: 18479256)
Int J Mol Sci. 2021 Feb 14;22(4):. (PMID: 33672854)
J Immunother Cancer. 2022 Apr;10(4):. (PMID: 35383115)
Am J Physiol Gastrointest Liver Physiol. 2003 Nov;285(5):G967-79. (PMID: 12801887)
EMBO J. 2017 Jan 4;36(1):5-24. (PMID: 27797821)
J Neurophysiol. 2017 Jan 1;117(1):365-375. (PMID: 27784805)
Nat Rev Gastroenterol Hepatol. 2021 Aug;18(8):571-587. (PMID: 33731961)
N Engl J Med. 2011 Jan 20;364(3):255-64. (PMID: 21247316)
PLoS One. 2018 Aug 23;13(8):e0200674. (PMID: 30138372)
Surg Infect (Larchmt). 2014 Aug;15(4):387-93. (PMID: 24828283)
Nucleic Acids Res. 2012 May;40(10):4288-97. (PMID: 22287627)
J Clin Invest. 2009 Jun;119(6):1420-8. (PMID: 19487818)
Am J Physiol Gastrointest Liver Physiol. 2016 Jun 1;310(11):G941-51. (PMID: 27056724)
Transl Res. 2015 Jul;166(1):12-27. (PMID: 25655839)
PLoS One. 2013 Jul 01;8(7):e69042. (PMID: 23840906)
J Biol Chem. 2013 May 24;288(21):15229-39. (PMID: 23558678)
Genome Biol. 2014;15(12):550. (PMID: 25516281)
Gastroenterology. 2016 Jan;150(1):168-80. (PMID: 26433161)
Nutr Res Rev. 2016 Jun;29(1):60-90. (PMID: 27176552)
Science. 2017 May 19;356(6339):722-726. (PMID: 28522527)
Nature. 2021 Nov;599(7883):125-130. (PMID: 34671159)
J Emerg Med. 2012 Jul;43(1):e49-51. (PMID: 22325550)
J Pediatr. 2011 Feb;158(2 Suppl):e25-8. (PMID: 21238702)
Mol Neurobiol. 2014 Oct;50(2):274-89. (PMID: 24878766)
Elife. 2015 Oct 08;4:e09652. (PMID: 26448485)
Gut. 2004 Feb;53(2):222-8. (PMID: 14724154)
Cell. 2018 Oct 4;175(2):372-386.e17. (PMID: 30270042)
J Anim Sci. 2013 Oct;91(10):4713-29. (PMID: 23942716)
Crit Care Med. 2003 Aug;31(8 Suppl):S532-7. (PMID: 12907883)
Front Immunol. 2013 Sep 11;4:272. (PMID: 24062740)
Proc Natl Acad Sci U S A. 2009 Jan 6;106(1):256-61. (PMID: 19109436)
BMC Genomics. 2009 Nov 02;10:507. (PMID: 19883504)
Am J Physiol Gastrointest Liver Physiol. 2007 Jan;292(1):G231-41. (PMID: 16423922)
Cells. 2020 Mar 31;9(4):. (PMID: 32244316)
Sci Rep. 2020 May 8;10(1):7737. (PMID: 32385412)
Dig Dis Sci. 2015 Sep;60(9):2677-89. (PMID: 25917048)
Gastroenterology. 2014 Dec;147(6):1230-7. (PMID: 25305504)
Am J Physiol Gastrointest Liver Physiol. 2011 Jun;300(6):G976-87. (PMID: 21350188)
EBioMedicine. 2019 Nov;49:172-188. (PMID: 31662289)
Surgery. 1997 May;121(5):526-34. (PMID: 9142151)
Int J Colorectal Dis. 2015 May;30(5):683-90. (PMID: 25694139)
J Cell Mol Med. 2009 Sep;13(9B):4061-76. (PMID: 19929946)
Front Immunol. 2022 Jan 20;12:826882. (PMID: 35126380)
Physiol Rev. 2007 Apr;87(2):545-64. (PMID: 17429041)
J Neuroinflammation. 2017 Apr 7;14(1):79. (PMID: 28388962)
Cell Stem Cell. 2022 Jan 6;29(1):86-100.e6. (PMID: 34727519)
Semin Pediatr Surg. 2013 May;22(2):83-7. (PMID: 23611611)
Glia. 2015 Feb;63(2):229-41. (PMID: 25161129)
Acta Histochem. 2019 Aug;121(6):665-679. (PMID: 31202513)
J Clin Invest. 2008 Mar;118(3):965-74. (PMID: 18246199)
Gastroenterology. 1993 Feb;104(2):440-7. (PMID: 8425686)
J Pediatr Surg. 1992 Oct;27(10):1343-5. (PMID: 1403518)
Int J Mol Sci. 2020 Feb 01;21(3):. (PMID: 32024112)
J Pediatr Surg. 2009 Jun;44(6):1072-5; discussion 1075-6. (PMID: 19524719)
Am J Physiol Gastrointest Liver Physiol. 2015 Jan 15;308(2):G63-75. (PMID: 25414098)
Trends Neurosci. 1994 Apr;17(4):138-42. (PMID: 7517589)
Vet Pathol. 2012 Mar;49(2):344-56. (PMID: 21441112)
Sci Rep. 2016 May 03;6:25203. (PMID: 27140063)
Commun Biol. 2022 Aug 12;5(1):811. (PMID: 35962064)
Gastroenterology. 2015 Aug;149(2):445-55.e3. (PMID: 25865048)
Neurogastroenterol Motil. 2011 Nov;23(11):e500-9. (PMID: 21410600)
Gut Microbes. 2015;6(6):398-403. (PMID: 26558327)
Sci Rep. 2019 Jan 24;9(1):665. (PMID: 30679569)
Gut. 2011 Apr;60(4):473-84. (PMID: 21139062)
J Physiol. 2017 Jun 1;595(11):3409-3424. (PMID: 28066889)
J Crohns Colitis. 2019 Mar 30;13(4):495-509. (PMID: 30395194)
Cell. 2014 Nov 6;159(4):896-910. (PMID: 25417164)
معلومات مُعتمدة: P30 DK034987 United States DK NIDDK NIH HHS; R01 HD095876 United States HD NICHD NIH HHS; T32 DK007737 United States DK NIDDK NIH HHS; L40 OD028437 United States OD NIH HHS; K01 OD028207 United States OD NIH HHS; L40 OD032118 United States OD NIH HHS
فهرسة مساهمة: Keywords: enteric glia; epithelial restitution; intestinal barrier; intestinal ischemia; restitution
تواريخ الأحداث: Date Created: 20231226 Date Completed: 20240214 Latest Revision: 20240629
رمز التحديث: 20240629
مُعرف محوري في PubMed: PMC11211042
DOI: 10.1152/ajpgi.00216.2022
PMID: 38147796
قاعدة البيانات: MEDLINE
الوصف
تدمد:1522-1547
DOI:10.1152/ajpgi.00216.2022