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Current Pediatric Reviews

Editor-in-Chief

ISSN (Print): 1573-3963
ISSN (Online): 1875-6336

Review Article

Enteric Nervous System in Neonatal Necrotizing Enterocolitis

Author(s): Pavithra Chandramowlishwaran, Shreya Raja, Akhil Maheshwari and Shanthi Srinivasan*

Volume 18, Issue 1, 2022

Published on: 21 December, 2021

Page: [9 - 24] Pages: 16

DOI: 10.2174/1573396317666210908162745

Price: $65

Abstract

Background: The pathophysiology of necrotizing enterocolitis (NEC) is not clear, but increasing information suggests that the risk and severity of NEC may be influenced by abnormalities in the enteric nervous system (ENS).

Objective: The purpose of this review was to scope and examine the research related to ENS-associated abnormalities that have either been identified in NEC or have been noted in other inflammatory bowel disorders (IBDs) with histopathological abnormalities similar to NEC. The aim was to summarize the research findings, identify research gaps in existing literature, and disseminate them to key knowledge end-users to collaborate and address the same in future studies.

Methods: Articles that met the objectives of the study were identified through an extensive literature search in the databases PubMed, EMBASE, and Scopus.

Results: The sources identified through the literature search revealed that: (1) ENS may be involved in NEC development and post-NEC complications, (2) NEC development is associated with changes in the ENS, and (3) NEC-associated changes could be modulated by the ENS.

Conclusion: The findings from this review identify the enteric nervous as a target in the development and progression of NEC. Thus, factors that can protect the ENS can potentially prevent and treat NEC and post-NEC complications. This review serves to summarize the existing literature and highlights a need for further research on the involvement of ENS in NEC.

Keywords: Necrotizing enterocolitis, neonates, premature, enteric nervous system, intestinal inflammation, gut dysbiosis.

Graphical Abstract
[1]
Gregory KE, Deforge CE, Natale KM, Phillips M, Van Marter LJ. Necrotizing enterocolitis in the premature infant: Neonatal nursing assessment, disease pathogenesis, and clinical presentation. Adv Neonatal Care 2011; 11(3): 155-64.
[http://dx.doi.org/10.1097/ANC.0b013e31821baaf4] [PMID: 21730907]
[2]
Schnabl KL, Van Aerde JE, Thomson AB, Clandinin MT. Necrotizing enterocolitis: A multifactorial disease with no cure. World J Gastroenterol 2008; 14(14): 2142-61.
[http://dx.doi.org/10.3748/wjg.14.2142] [PMID: 18407587]
[3]
Sharma R, Hudak ML. A clinical perspective of necrotizing enterocolitis: Past, present, and future. Clin Perinatol 2013; 40(1): 27-51.
[http://dx.doi.org/10.1016/j.clp.2012.12.012] [PMID: 23415262]
[4]
Fredriksson F, Engstrand Lilja H. Survival rates for surgically treated necrotising enterocolitis have improved over the last four decades. Acta Paediatr 2019; 108(9): 1603-8.
[http://dx.doi.org/10.1111/apa.14770] [PMID: 30825252]
[5]
Neu J. Necrotizing enterocolitis: The future. Neonatology 2020; 117(2): 240-4.
[http://dx.doi.org/10.1159/000506866] [PMID: 32155645]
[6]
Lin PW, Stoll BJ. Necrotising enterocolitis. Lancet 2006; 368(9543): 1271-83.
[http://dx.doi.org/10.1016/S0140-6736(06)69525-1] [PMID: 17027734]
[7]
Nezami BG, Srinivasan S. Enteric nervous system in the small intestine: Pathophysiology and clinical implications. Curr Gastroenterol Rep 2010; 12(5): 358-65.
[http://dx.doi.org/10.1007/s11894-010-0129-9] [PMID: 20725870]
[8]
Nagy N, Goldstein AM. Enteric nervous system development: A crest cell’s journey from neural tube to colon. Semin Cell Dev Biol 2017; 66: 94-106.
[http://dx.doi.org/10.1016/j.semcdb.2017.01.006] [PMID: 28087321]
[9]
Burns AJ, Roberts RR, Bornstein JC, Young HM. Development of the enteric nervous system and its role in intestinal motility during fetal and early postnatal stages. Semin Pediatr Surg 2009; 18(4): 196-205.
[http://dx.doi.org/10.1053/j.sempedsurg.2009.07.001] [PMID: 19782301]
[10]
Furness JB. The enteric nervous system and neurogastroenterology. Nat Rev Gastroenterol Hepatol 2012; 9(5): 286-94.
[http://dx.doi.org/10.1038/nrgastro.2012.32] [PMID: 22392290]
[11]
Zhou Y, Yang J, Watkins DJ, et al. Enteric nervous system abnormalities are present in human necrotizing enterocolitis: Potential neurotransplantation therapy. Stem Cell Res Ther 2013; 4(6): 157.
[http://dx.doi.org/10.1186/scrt387] [PMID: 24423414]
[12]
Tanner SM, Berryhill TF, Ellenburg JL, et al. Pathogenesis of necrotizing enterocolitis: Modeling the innate immune response. Am J Pathol 2015; 185(1): 4-16.
[http://dx.doi.org/10.1016/j.ajpath.2014.08.028] [PMID: 25447054]
[13]
Gephart SM, McGrath JM, Effken JA, Halpern MD. Necrotizing enterocolitis risk: State of the science. Adv Neonatal Care 2012; 12(2): 77-87.
[http://dx.doi.org/10.1097/ANC.0b013e31824cee94] [PMID: 22469959]
[14]
Berseth CL. Gestational evolution of small intestine motility in preterm and term infants. J Pediatr 1989; 115(4): 646-51.
[http://dx.doi.org/10.1016/S0022-3476(89)80302-6] [PMID: 2507768]
[15]
Berseth CL. Gastrointestinal motility in the neonate. Clin Perinatol 1996; 23(2): 179-90.
[http://dx.doi.org/10.1016/S0095-5108(18)30237-9] [PMID: 8780900]
[16]
Anderson RB, Newgreen DF, Young HM. Neural crest and the development of the enteric nervous system. Adv Exp Med Biol 2006; 589: 181-96.
[http://dx.doi.org/10.1007/978-0-387-46954-6_11] [PMID: 17076282]
[17]
Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF. The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature 1999; 399(6734): 366-70.
[http://dx.doi.org/10.1038/20700] [PMID: 10360575]
[18]
Sánchez-Mejías A, Watanabe Y, M Fernández R, et al. Involvement of SOX10 in the pathogenesis of Hirschsprung disease: Report of a truncating mutation in an isolated patient. J Mol Med (Berl) 2010; 88(5): 507-14.
[http://dx.doi.org/10.1007/s00109-010-0592-7] [PMID: 20130826]
[19]
Uesaka T, Nagashimada M, Enomoto H. GDNF signaling levels control migration and neuronal differentiation of enteric ganglion precursors. J Neurosci 2013; 33(41): 16372-82.
[http://dx.doi.org/10.1523/JNEUROSCI.2079-13.2013] [PMID: 24107967]
[20]
Ito Y, Wiese S, Funk N, et al. Sox10 regulates ciliary neurotrophic factor gene expression in Schwann cells. Proc Natl Acad Sci USA 2006; 103(20): 7871-6.
[http://dx.doi.org/10.1073/pnas.0602332103] [PMID: 16684879]
[21]
Hackam DJ, Sodhi CP. Toll-like receptor-mediated intestinal inflammatory imbalance in the pathogenesis of necrotizing enterocolitis. Cell Mol Gastroenterol Hepatol 2018; 6(2): 229-238.e1.
[http://dx.doi.org/10.1016/j.jcmgh.2018.04.001] [PMID: 30105286]
[22]
Chalazonitis A, Rothman TP, Chen J, Vinson EN, MacLennan AJ, Gershon MD. Promotion of the development of enteric neurons and glia by neuropoietic cytokines: Interactions with neurotrophin-3. Dev Biol 1998; 198(2): 343-65.
[http://dx.doi.org/10.1016/S0012-1606(98)80010-9] [PMID: 9659938]
[23]
Fichter M, Klotz M, Hirschberg DL, et al. Breast milk contains relevant neurotrophic factors and cytokines for enteric nervous system development. Mol Nutr Food Res 2011; 55(10): 1592-6.
[http://dx.doi.org/10.1002/mnfr.201100124] [PMID: 21809438]
[24]
Herrmann K, Carroll K. An exclusively human milk diet reduces necrotizing enterocolitis. Breastfeed Med 2014; 9(4): 184-90.
[http://dx.doi.org/10.1089/bfm.2013.0121] [PMID: 24588561]
[25]
Bergstrand O, Hellers G. Breast-feeding during infancy in patients who later develop Crohn’s disease. Scand J Gastroenterol 1983; 18(7): 903-6.
[http://dx.doi.org/10.3109/00365528309182113] [PMID: 6676923]
[26]
Klement E, Cohen RV, Boxman J, Joseph A, Reif S. Breastfeeding and risk of inflammatory bowel disease: A systematic review with meta-analysis. Am J Clin Nutr 2004; 80(5): 1342-52.
[http://dx.doi.org/10.1093/ajcn/80.5.1342] [PMID: 15531685]
[27]
Meng X, Dunsmore G, Koleva P, et al. The profile of human milk metabolome, cytokines, and antibodies in inflammatory bowel diseases versus healthy mothers, and potential impact on the newborn. J Crohn’s Colitis 2019; 13(4): 431-41.
[http://dx.doi.org/10.1093/ecco-jcc/jjy186] [PMID: 30418545]
[28]
Tang W, Su Y, Yuan C, et al. Prospective study reveals a microbiome signature that predicts the occurrence of post-operative enterocolitis in Hirschsprung disease (HSCR) patients. Gut Microbes 2020; 11(4): 842-54.
[http://dx.doi.org/10.1080/19490976.2020.1711685] [PMID: 31944159]
[29]
Cheng LS, Hotta R, Graham HK, Belkind-Gerson J, Nagy N, Goldstein AM. Postnatal human enteric neuronal progenitors can migrate, differentiate, and proliferate in embryonic and postnatal aganglionic gut environments. Pediatr Res 2017; 81(5): 838-46.
[http://dx.doi.org/10.1038/pr.2017.4] [PMID: 28060794]
[30]
Sigge W, Wedel T, Kühnel W, Krammer HJ. Morphologic alterations of the enteric nervous system and deficiency of non-adrenergic non-cholinergic inhibitory innervation in neonatal necrotizing enterocolitis. Eur J Pediatr Surg 1998; 8(2): 87-94.
[http://dx.doi.org/10.1055/s-2008-1071128] [PMID: 9617607]
[31]
Wedel T, Krammer HJ, Kühnel W, Sigge W. Alterations of the enteric nervous system in neonatal necrotizing enterocolitis revealed by whole-mount immunohistochemistry. Pediatr Pathol Lab Med 1998; 18(1): 57-70.
[http://dx.doi.org/10.1080/107710498174227] [PMID: 9566283]
[32]
Taguchi T, Ieiri S, Miyoshi K, et al. The incidence and outcome of allied disorders of Hirschsprung’s disease in Japan: Results from a nationwide survey. Asian J Surg 2017; 40(1): 29-34.
[http://dx.doi.org/10.1016/j.asjsur.2015.04.004] [PMID: 26216257]
[33]
Porter AJ, Wattchow DA, Brookes SJ, Costa M. Cholinergic and nitrergic interneurones in the myenteric plexus of the human colon. Gut 2002; 51(1): 70-5.
[http://dx.doi.org/10.1136/gut.51.1.70] [PMID: 12077095]
[34]
Rowland KJ, Choi PM, Warner BW. The role of growth factors in intestinal regeneration and repair in necrotizing enterocolitis. Semin Pediatr Surg 2013; 22(2): 101-11.
[http://dx.doi.org/10.1053/j.sempedsurg.2013.01.007] [PMID: 23611614]
[35]
Shelby RD, Cromeens B, Rager TM, Besner GE. Influence of growth factors on the development of necrotizing enterocolitis. Clin Perinatol 2019; 46(1): 51-64.
[http://dx.doi.org/10.1016/j.clp.2018.10.005] [PMID: 30771819]
[36]
Grisoni ER, Kalhan SC. Plasma vasoactive intestinal polypeptide in the newborn infant. J Pediatr Gastroenterol Nutr 1990; 10(2): 185-8.
[http://dx.doi.org/10.1097/00005176-199002000-00007] [PMID: 2303969]
[37]
Good M, Sodhi CP, Hackam DJ. Evidence-based feeding strategies before and after the development of necrotizing enterocolitis. Expert Rev Clin Immunol 2014; 10(7): 875-84.
[http://dx.doi.org/10.1586/1744666X.2014.913481] [PMID: 24898361]
[38]
Wei J, Zhou Y, Besner GE. Heparin-binding EGF-like growth factor and enteric neural stem cell transplantation in the prevention of experimental necrotizing enterocolitis in mice. Pediatr Res 2015; 78(1): 29-37.
[http://dx.doi.org/10.1038/pr.2015.63] [PMID: 25806717]
[39]
Abot A, Cani PD, Knauf C. Impact of intestinal peptides on the enteric nervous system: novel approaches to control glucose metabolism and food intake. Front Endocrinol (Lausanne) 2018; 9: 328.
[http://dx.doi.org/10.3389/fendo.2018.00328] [PMID: 29988396]
[40]
Seo S, Miyake H, Alganabi M, et al. Vasoactive intestinal peptide decreases inflammation and tight junction disruption in experimental necrotizing enterocolitis. J Pediatr Surg 2019; 54(12): 2520-3.
[http://dx.doi.org/10.1016/j.jpedsurg.2019.08.038] [PMID: 31668399]
[41]
Caputi V, Marsilio I, Cerantola S, et al. Toll-like receptor 4 modulates small intestine neuromuscular function through nitrergic and purinergic pathways. Front Pharmacol 2017; 8: 350.
[http://dx.doi.org/10.3389/fphar.2017.00350] [PMID: 28642706]
[42]
El-Nachef WN, Bronner ME. De novo enteric neurogenesis in post-embryonic zebrafish from Schwann cell precursors rather than resident cell types. Development 2020; 147(13): 147.
[PMID: 32541008]
[43]
Margolis KG, Li Z, Stevanovic K, et al. Serotonin transporter variant drives preventable gastrointestinal abnormalities in development and function. J Clin Invest 2016; 126(6): 2221-35.
[http://dx.doi.org/10.1172/JCI84877] [PMID: 27111230]
[44]
De Plaen IG. Inflammatory signaling in necrotizing enterocolitis. Clin Perinatol 2013; 40(1): 109-24.
[http://dx.doi.org/10.1016/j.clp.2012.12.008] [PMID: 23415267]
[45]
Furness JB, Stebbing MJ. The first brain: Species comparisons and evolutionary implications for the enteric and central nervous systems. Neurogastroenterol Motil 2018; 30(2): 30.
[http://dx.doi.org/10.1111/nmo.13234] [PMID: 29024273]
[46]
Fagbemi AO, Torrente F, Puleston J, Lakhoo K, James S, Murch SH. Enteric neural disruption in necrotizing enterocolitis occurs in association with myenteric glial cell CCL20 expression. J Pediatr Gastroenterol Nutr 2013; 57(6): 788-93.
[http://dx.doi.org/10.1097/MPG.0b013e3182a86fd4] [PMID: 24280992]
[47]
Epelman M, Daneman A, Navarro OM, et al. Necrotizing enterocolitis: Review of state-of-the-art imaging findings with pathologic correlation. Radiographics 2007; 27(2): 285-305.
[http://dx.doi.org/10.1148/rg.272055098] [PMID: 17374854]
[48]
Rabinowitz JG, Siegle RL. Changing clinical and roentgenographic patterns of necrotizing enterocolitis. AJR Am J Roentgenol 1976; 126(3): 560-6.
[http://dx.doi.org/10.2214/ajr.126.3.560] [PMID: 178203]
[49]
Rao M, Gershon MD. Enteric nervous system development: What could possibly go wrong? Nat Rev Neurosci 2018; 19(9): 552-65.
[http://dx.doi.org/10.1038/s41583-018-0041-0] [PMID: 30046054]
[50]
Vergnolle N, Cirillo C. Neurons and glia in the enteric nervous system and epithelial barrier function. Physiology (Bethesda) 2018; 33(4): 269-80.
[http://dx.doi.org/10.1152/physiol.00009.2018] [PMID: 29897300]
[51]
Claud EC. Neonatal necrotizing enterocolitis -inflammation and intestinal immaturity. Antiinflamm Antiallergy Agents Med Chem 2009; 8(3): 248-59.
[http://dx.doi.org/10.2174/187152309789152020] [PMID: 20498729]
[52]
Chassaing B, Kumar M, Baker MT, Singh V, Vijay-Kumar M. Mammalian gut immunity. Biomed J 2014; 37(5): 246-58.
[http://dx.doi.org/10.4103/2319-4170.130922] [PMID: 25163502]
[53]
Bassotti G, Villanacci V, Antonelli E, Morelli A, Salerni B. Enteric glial cells: New players in gastrointestinal motility? Lab Invest 2007; 87(7): 628-32.
[http://dx.doi.org/10.1038/labinvest.3700564] [PMID: 17483847]
[54]
von Boyen GB, Steinkamp M, Geerling I, et al. Proinflammatory cytokines induce neurotrophic factor expression in enteric glia: A key to the regulation of epithelial apoptosis in Crohn’s disease. Inflamm Bowel Dis 2006; 12(5): 346-54.
[http://dx.doi.org/10.1097/01.MIB.0000219350.72483.44] [PMID: 16670534]
[55]
Bush TG, Savidge TC, Freeman TC, et al. Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell 1998; 93(2): 189-201.
[http://dx.doi.org/10.1016/S0092-8674(00)81571-8] [PMID: 9568712]
[56]
Bassotti G, Battaglia E, Bellone G, et al. Interstitial cells of Cajal, enteric nerves, and glial cells in colonic diverticular disease. J Clin Pathol 2005; 58(9): 973-7.
[http://dx.doi.org/10.1136/jcp.2005.026112] [PMID: 16126881]
[57]
Forstermann U, Sessa WC. 2012; Nitric oxide synthases: Regulation and function. Eur Heart J 2012; 33: 829-37.
[http://dx.doi.org/10.1093/eurheartj/ehr304]
[58]
Lu H, Zhu B, Xue XD. Role of neuronal nitric oxide synthase and inducible nitric oxide synthase in intestinal injury in neonatal rats. World J Gastroenterol 2006; 12(27): 4364-8.
[http://dx.doi.org/10.3748/wjg.v12.i27.4364] [PMID: 16865779]
[59]
Ito J, Uchida H, Machida N, Ohtake K, Saito Y, Kobayashi J. Inducible and neuronal nitric oxide synthases exert contrasting effects during rat intestinal recovery following fasting. Exp Biol Med (Maywood) 2017; 242(7): 762-72.
[http://dx.doi.org/10.1177/1535370217694434] [PMID: 28195513]
[60]
Chang K, Lee SJ, Cheong I, et al. Nitric oxide suppresses inducible nitric oxide synthase expression by inhibiting post-translational modification of IkappaB. Exp Mol Med 2004; 36(4): 311-24.
[http://dx.doi.org/10.1038/emm.2004.42] [PMID: 15365250]
[61]
Di Lorenzo M, Krantis A. Altered nitric oxide production in the premature gut may increase susceptibility to intestinal damage in necrotizing enterocolitis. J Pediatr Surg 2001; 36(5): 700-5.
[http://dx.doi.org/10.1053/jpsu.2001.22940] [PMID: 11329569]
[62]
Caplan MS, Simon D, Jilling T. The role of PAF, TLR, and the inflammatory response in neonatal necrotizing enterocolitis. Semin Pediatr Surg 2005; 14(3): 145-51.
[http://dx.doi.org/10.1053/j.sempedsurg.2005.05.002] [PMID: 16084401]
[63]
Frost BL, Jilling T, Caplan MS. The importance of pro-inflammatory signaling in neonatal necrotizing enterocolitis. Semin Perinatol 2008; 32(2): 100-6.
[http://dx.doi.org/10.1053/j.semperi.2008.01.001] [PMID: 18346533]
[64]
Muguruma K, Gray PW, Tjoelker LW, Johnston JM. The central role of PAF in necrotizing enterocolitis development. Adv Exp Med Biol 1997; 407: 379-82.
[http://dx.doi.org/10.1007/978-1-4899-1813-0_56] [PMID: 9321979]
[65]
Wang GD, Wang XY, Hu HZ, et al. Platelet-activating factor in the enteric nervous system of the guinea pig small intestine. Am J Physiol Gastrointest Liver Physiol 2006; 291(5): G928-37.
[http://dx.doi.org/10.1152/ajpgi.00153.2006] [PMID: 17030900]
[66]
Amer MD, Hedlund E, Rochester J, Caplan MS. Platelet-activating factor concentration in the stool of human newborns: Effects of enteral feeding and neonatal necrotizing enterocolitis. Biol Neonate 2004; 85(3): 159-66.
[http://dx.doi.org/10.1159/000075306] [PMID: 14646336]
[67]
Gonzalez-Crussi F, Hsueh W. Experimental model of ischemic bowel necrosis. The role of platelet-activating factor and endotoxin. Am J Pathol 1983; 112(1): 127-35.
[PMID: 6859226]
[68]
Caplan MS, Hedlund E, Adler L, Lickerman M, Hsueh W. The platelet-activating factor receptor antagonist WEB 2170 prevents neonatal necrotizing enterocolitis in rats. J Pediatr Gastroenterol Nutr 1997; 24(3): 296-301.
[http://dx.doi.org/10.1097/00005176-199703000-00012] [PMID: 9138176]
[69]
Wang H, Tan X, Chang H, Gonzalez-Crussi F, Remick DG, Hsueh W. Regulation of platelet-activating factor receptor gene expression in vivo by endotoxin, platelet-activating factor and endogenous tumour necrosis factor. Biochem J 1997; 322(Pt 2): 603-8.
[http://dx.doi.org/10.1042/bj3220603] [PMID: 9065783]
[70]
Moya FR, Eguchi H, Zhao B, et al. Platelet-activating factor acetylhydrolase in term and preterm human milk: A preliminary report. J Pediatr Gastroenterol Nutr 1994; 19(2): 236-9.
[http://dx.doi.org/10.1097/00005176-199408000-00015] [PMID: 7815247]
[71]
Caplan MS, Lickerman M, Adler L, Dietsch GN, Yu A. The role of recombinant platelet-activating factor acetylhydrolase in a neonatal rat model of necrotizing enterocolitis. Pediatr Res 1997; 42(6): 779-83.
[http://dx.doi.org/10.1203/00006450-199712000-00010] [PMID: 9396557]
[72]
Rao M, Gershon MD. The bowel and beyond: The enteric nervous system in neurological disorders. Nat Rev Gastroenterol Hepatol 2016; 13(9): 517-28.
[http://dx.doi.org/10.1038/nrgastro.2016.107] [PMID: 27435372]
[73]
Tita AT, Andrews WW. Diagnosis and management of clinical chorioamnionitis. Clin Perinatol 2010; 37(2): 339-54.
[http://dx.doi.org/10.1016/j.clp.2010.02.003] [PMID: 20569811]
[74]
Been JV, Lievense S, Zimmermann LJ, Kramer BW, Wolfs TG. Chorioamnionitis as a risk factor for necrotizing enterocolitis: Asystematic review and meta-analysis. J Pediatr 2013; 162(2): 236-42.e2.
[http://dx.doi.org/10.1016/j.jpeds.2012.07.012] [PMID: 22920508]
[75]
Heymans C, de Lange IH, Lenaerts K, et al. Chorioamnionitis induces enteric nervous system injury: Effects of timing and inflammation in the ovine fetus. Mol Med 2020; 26(1): 82.
[http://dx.doi.org/10.1186/s10020-020-00206-x] [PMID: 32883198]
[76]
Heymans C, de Lange IH, Hütten MC, et al. Chronic intra-uterine Ureaplasma parvum infection induces injury of the enteric nervous system in ovine fetuses. Front Immunol 2020; 11: 189.
[http://dx.doi.org/10.3389/fimmu.2020.00189] [PMID: 32256485]
[77]
Gussenhoven R, Westerlaken RJJ, Ophelders DRMG, et al. Chorioamnionitis, neuroinflammation, and injury: Timing is key in the preterm ovine fetus. J Neuroinflammation 2018; 15(1): 113.
[http://dx.doi.org/10.1186/s12974-018-1149-x] [PMID: 29673373]
[78]
Cornet A, Savidge TC, Cabarrocas J, et al. Enterocolitis induced by autoimmune targeting of enteric glial cells: A possible mechanism in Crohn’s disease? Proc Natl Acad Sci USA 2001; 98(23): 13306-11.
[http://dx.doi.org/10.1073/pnas.231474098] [PMID: 11687633]
[79]
Fukui H. Increased intestinal permeability and decreased barrier function: does it really influence the risk of inflammation? Inflamm Intest Dis 2016; 1(3): 135-45.
[http://dx.doi.org/10.1159/000447252] [PMID: 29922669]
[80]
Jarret A, Jackson R, Duizer C, et al. Enteric nervous system-derived IL-18 orchestrates mucosal barrier immunity. Cell 2020; 180(1): 50-63.e12.
[http://dx.doi.org/10.1016/j.cell.2019.12.016] [PMID: 31923399]
[81]
Anitha M, Vijay-Kumar M, Sitaraman SV, Gewirtz AT, Srinivasan S. Gut microbial products regulate murine gastrointestinal motility via Toll-like receptor 4 signaling. Gastroenterology 2012; 143(4): 1006-16.e4.
[http://dx.doi.org/10.1053/j.gastro.2012.06.034] [PMID: 22732731]
[82]
Barajon I, Serrao G, Arnaboldi F, et al. Toll-like receptors 3, 4, and 7 are expressed in the enteric nervous system and dorsal root ganglia. J Histochem Cytochem 2009; 57(11): 1013-23.
[http://dx.doi.org/10.1369/jhc.2009.953539] [PMID: 19546475]
[83]
Leaphart CL, Cavallo J, Gribar SC, et al. A critical role for TLR4 in the pathogenesis of necrotizing enterocolitis by modulating intestinal injury and repair. J Immunol 2007; 179(7): 4808-20.
[http://dx.doi.org/10.4049/jimmunol.179.7.4808] [PMID: 17878380]
[84]
Lu P, Sodhi CP, Hackam DJ. Toll-like receptor regulation of intestinal development and inflammation in the pathogenesis of necrotizing enterocolitis. Pathophysiology 2014; 21(1): 81-93.
[http://dx.doi.org/10.1016/j.pathophys.2013.11.007] [PMID: 24365655]
[85]
Brun P, Giron MC, Qesari M, et al. Toll-like receptor 2 regulates intestinal inflammation by controlling integrity of the enteric nervous system. Gastroenterology 2013; 145(6): 1323-33.
[http://dx.doi.org/10.1053/j.gastro.2013.08.047] [PMID: 23994200]
[86]
Zamora R, Grishin A, Wong C, et al. High-mobility group box 1 protein is an inflammatory mediator in necrotizing enterocolitis: Protective effect of the macrophage deactivator semapimod. Am J Physiol Gastrointest Liver Physiol 2005; 289(4): G643-52.
[http://dx.doi.org/10.1152/ajpgi.00067.2005] [PMID: 15947118]
[87]
Gribar SC, Sodhi CP, Richardson WM, et al. Reciprocal expression and signaling of TLR4 and TLR9 in the pathogenesis and treatment of necrotizing enterocolitis. J Immunol 2009; 182(1): 636-46.
[http://dx.doi.org/10.4049/jimmunol.182.1.636] [PMID: 19109197]
[88]
Powley TL. Vagal input to the enteric nervous system. Gut 2000; 47(Suppl. 4): iv30-2.
[http://dx.doi.org/10.1136/gut.47.suppl_4.iv30] [PMID: 11076904]
[89]
Sri Paran T, Rolle U, Puri P. Developmental changes of the adrenergic network in the myenteric plexus of the porcine small bowel. Pediatr Surg Int 2007; 23(7): 659-63.
[http://dx.doi.org/10.1007/s00383-007-1924-8] [PMID: 17503058]
[90]
Meister AL, Doheny KK, Travagli RA. Necrotizing enterocolitis attenuates developmental heart rate variability increases in newborn rats. Neurogastroenterol Motil 2019; 31(3): e13484.
[http://dx.doi.org/10.1111/nmo.13484] [PMID: 30298607]
[91]
Pavlov VA, Wang H, Czura CJ, Friedman SG, Tracey KJ. The cholinergic anti-inflammatory pathway: A missing link in neuroimmunomodulation. Mol Med 2003; 9(5-8): 125-34.
[http://dx.doi.org/10.1007/BF03402177] [PMID: 14571320]
[92]
Liu HL, Garzoni L, Herry C, et al. Can monitoring fetal intestinal inflammation using heart rate variability analysis signal incipient necrotizing enterocolitis of the neonate? Pediatr Crit Care Med 2016; 17(4): e165-76.
[http://dx.doi.org/10.1097/PCC.0000000000000643] [PMID: 26914621]
[93]
Doheny KK, Palmer C, Browning KN, et al. Diminished vagal tone is a predictive biomarker of necrotizing enterocolitis-risk in preterm infants. Neurogastroenterol Motil 2014; 26(6): 832-40.
[http://dx.doi.org/10.1111/nmo.12337] [PMID: 24720579]
[94]
Passi R, Doheny KK, Gordin Y, Hinssen H, Palmer C. Electrical grounding improves vagal tone in preterm infants. Neonatology 2017; 112(2): 187-92.
[http://dx.doi.org/10.1159/000475744] [PMID: 28601861]
[95]
Lakhan SE, Kirchgessner A. Neuroinflammation in inflammatory bowel disease. J Neuroinflammation 2010; 7: 37.
[http://dx.doi.org/10.1186/1742-2094-7-37] [PMID: 20615234]
[96]
Chandrasekharan B, Nezami BG, Srinivasan S. Emerging neuropeptide targets in inflammation: NPY and VIP. Am J Physiol Gastrointest Liver Physiol 2013; 304(11): G949-57.
[http://dx.doi.org/10.1152/ajpgi.00493.2012] [PMID: 23538492]
[97]
Chiu IM, von Hehn CA, Woolf CJ. Neurogenic inflammation and the peripheral nervous system in host defense and immunopathology. Nat Neurosci 2012; 15(8): 1063-7.
[http://dx.doi.org/10.1038/nn.3144] [PMID: 22837035]
[98]
Bernardazzi C, Pêgo B, de Souza HS. Neuroimmunomodulation in the gut: focus on inflammatory bowel disease. Mediators Inflamm 2016; 2016: 1363818.
[http://dx.doi.org/10.1155/2016/1363818] [PMID: 27471349]
[99]
Bernstein CN, Robert ME, Eysselein VE. Rectal substance P concentrations are increased in ulcerative colitis but not in Crohn’s disease. Am J Gastroenterol 1993; 88(6): 908-13.
[PMID: 7684884]
[100]
Sébert M, Sola-Tapias N, Mas E, Barreau F, Ferrand A. Protease-activated receptors in the intestine: focus on inflammation and cancer. Front Endocrinol (Lausanne) 2019; 10: 717.
[http://dx.doi.org/10.3389/fendo.2019.00717] [PMID: 31708870]
[101]
Hu S, Zhao ZK, Liu R, et al. Electroacupuncture activates enteric glial cells and protects the gut barrier in hemorrhaged rats. World J Gastroenterol 2015; 21(5): 1468-78.
[http://dx.doi.org/10.3748/wjg.v21.i5.1468] [PMID: 25663766]
[102]
Beenken A, Mohammadi M. The FGF family: Biology, pathophysiology and therapy. Nat Rev Drug Discov 2009; 8(3): 235-53.
[http://dx.doi.org/10.1038/nrd2792] [PMID: 19247306]
[103]
Song X, Dai D, He X, et al. Growth factor FGF2 cooperates with interleukin-17 to repair intestinal epithelial damage. Immunity 2015; 43(3): 488-501.
[http://dx.doi.org/10.1016/j.immuni.2015.06.024] [PMID: 26320657]
[104]
Carver JD, Barness LA. Trophic factors for the gastrointestinal tract. Clin Perinatol 1996; 23(2): 265-85.
[http://dx.doi.org/10.1016/S0095-5108(18)30242-2] [PMID: 8780905]
[105]
Brun P, Zamuner A, Peretti A, et al. 3D synthetic peptide-based architectures for the engineering of the enteric nervous system. Sci Rep 2019; 9(1): 5583.
[http://dx.doi.org/10.1038/s41598-019-42071-7] [PMID: 30944410]
[106]
Conlin VS, Wu X, Nguyen C, et al. Vasoactive intestinal peptide ameliorates intestinal barrier disruption associated with Citrobacter rodentium-induced colitis. Am J Physiol Gastrointest Liver Physiol 2009; 297(4): G735-50.
[http://dx.doi.org/10.1152/ajpgi.90551.2008] [PMID: 19661153]
[107]
Soret R, Coquenlorge S, Cossais F, Meurette G, Rolli-Derkinderen M, Neunlist M. Characterization of human, mouse, and rat cultures of enteric glial cells and their effect on intestinal epithelial cells. Neurogastroenterol Motil 2013; 25(11): e755-64.
[http://dx.doi.org/10.1111/nmo.12200] [PMID: 23991747]
[108]
De Vadder F, Grasset E, Mannerås Holm L, et al. Gut microbiota regulates maturation of the adult enteric nervous system via enteric serotonin networks. Proc Natl Acad Sci USA 2018; 115(25): 6458-63.
[http://dx.doi.org/10.1073/pnas.1720017115] [PMID: 29866843]
[109]
Muller PA, Koscsó B, Rajani GM, et al. Crosstalk between muscularis macrophages and enteric neurons regulates gastrointestinal motility. Cell 2014; 158(2): 300-13.
[http://dx.doi.org/10.1016/j.cell.2014.04.050] [PMID: 25036630]
[110]
Yano JM, Yu K, Donaldson GP, et al. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 2015; 161(2): 264-76.
[http://dx.doi.org/10.1016/j.cell.2015.02.047] [PMID: 25860609]
[111]
Wall R, Ross RP, Ryan CA, et al. Role of gut microbiota in early infant development. Clin Med Pediatr 2009; 3: 45-54.
[http://dx.doi.org/10.4137/CMPed.S2008] [PMID: 23818794]
[112]
Yang I, Corwin EJ, Brennan PA, Jordan S, Murphy JR, Dunlop A. The infant microbiome: implications for infant health and neurocognitive development. Nurs Res 2016; 65(1): 76-88.
[http://dx.doi.org/10.1097/NNR.0000000000000133] [PMID: 26657483]
[113]
Wang Y, Hoenig JD, Malin KJ, et al. 16S rRNA gene-based analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis. ISME J 2009; 3(8): 944-54.
[http://dx.doi.org/10.1038/ismej.2009.37] [PMID: 19369970]
[114]
Li Y, Poroyko V, Yan Z, et al. Characterization of intestinal microbiomes of hirschsprung’s disease patients with or without enterocolitis using illumina-miseq high-throughput sequencing. PLoS One 2016; 11(9): e0162079.
[http://dx.doi.org/10.1371/journal.pone.0162079] [PMID: 27603009]
[115]
Bury RG, Tudehope D. Enteral antibiotics for preventing necrotizing enterocolitis in low birthweight or preterm infants. Cochrane Database Syst Rev 2001; (1): CD000405.
[http://dx.doi.org/10.1002/14651858.CD000405] [PMID: 11279690]
[116]
Zhu S, Jiang Y, Xu K, et al. The progress of gut microbiome research related to brain disorders. J Neuroinflammation 2020; 17(1): 25.
[http://dx.doi.org/10.1186/s12974-020-1705-z] [PMID: 31952509]
[117]
Mogensen TH. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 2009; 22(2): 240-73. [Table of Contents.].
[http://dx.doi.org/10.1128/CMR.00046-08] [PMID: 19366914]
[118]
McElroy SJ, Prince LS, Weitkamp JH, Reese J, Slaughter JC, Polk DB. Tumor necrosis factor receptor 1-dependent depletion of mucus in immature small intestine: A potential role in neonatal necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 2011; 301(4): G656-66.
[http://dx.doi.org/10.1152/ajpgi.00550.2010] [PMID: 21737776]
[119]
Burgueño JF, Barba A, Eyre E, Romero C, Neunlist M, Fernández E. TLR2 and TLR9 modulate enteric nervous system inflammatory responses to lipopolysaccharide. J Neuroinflammation 2016; 13(1): 187.
[http://dx.doi.org/10.1186/s12974-016-0653-0] [PMID: 27538577]
[120]
Sun J, Pan X, Christiansen LI, et al. Necrotizing enterocolitis is associated with acute brain responses in preterm pigs. J Neuroinflammation 2018; 15(1): 180.
[http://dx.doi.org/10.1186/s12974-018-1201-x] [PMID: 29885660]
[121]
Lara-Marquez ML, Mehta V, Michalsky MP, Fleming JB, Besner GE. Heparin-binding EGF-like growth factor down regulates proinflammatory cytokine-induced nitric oxide and inducible nitric oxide synthase production in intestinal epithelial cells. Nitric Oxide 2002; 6(2): 142-52.
[http://dx.doi.org/10.1006/niox.2001.0393] [PMID: 11890738]
[122]
Stringer MD, Brereton RJ, Drake DP, Kiely EM, Capps SN, Spitz L. Recurrent necrotizing enterocolitis. J Pediatr Surg 1993; 28(8): 979-81.
[http://dx.doi.org/10.1016/0022-3468(93)90496-8] [PMID: 8229602]
[123]
Christian VJ, Polzin E, Welak S. Nutrition management of necrotizing enterocolitis. Nutr Clin Pract 2018; 33(4): 476-82.
[http://dx.doi.org/10.1002/ncp.10115] [PMID: 29940075]
[124]
Cuna A, George L, Sampath V. Genetic predisposition to necrotizing enterocolitis in premature infants: Current knowledge, challenges, and future directions. Semin Fetal Neonatal Med 2018; 23(6): 387-93.
[http://dx.doi.org/10.1016/j.siny.2018.08.006] [PMID: 30292709]
[125]
Ting YJ, Chan KL, Wong SC, Chim S, Wong KY. Gastric pneumatosis in a premature neonate. AJP Rep 2011; 1(1): 11-4.
[http://dx.doi.org/10.1055/s-0030-1271218] [PMID: 23705077]
[126]
Nijenhuis CM, Horst PG, Berg LT, Wilffert B. Disturbed development of the enteric nervous system after in utero exposure of selective serotonin re-uptake inhibitors and tricyclic antidepressants. Part 1: Literature review. Br J Clin Pharmacol 2012; 73(1): 16-26.
[http://dx.doi.org/10.1111/j.1365-2125.2011.04075.x] [PMID: 21815911]
[127]
Yang G, Brisseau G, Yanchar NL. Infantile hypertrophic pyloric stenosis: An association in twins? Paediatr Child Health 2008; 13(5): 383-5.
[http://dx.doi.org/10.1093/pch/13.5.383] [PMID: 19412365]
[128]
Vanderwinden JM, Mailleux P, Schiffmann SN, Vanderhaeghen JJ, De Laet MH. Nitric oxide synthase activity in infantile hypertrophic pyloric stenosis. N Engl J Med 1992; 327(8): 511-5.
[http://dx.doi.org/10.1056/NEJM199208203270802] [PMID: 1378938]
[129]
D’Amelio M, Cavallucci V, Middei S, et al. Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer’s disease. Nat Neurosci 2011; 14(1): 69-76.
[http://dx.doi.org/10.1038/nn.2709] [PMID: 21151119]
[130]
Pozueta J, Lefort R, Ribe EM, Troy CM, Arancio O, Shelanski M. Caspase-2 is required for dendritic spine and behavioural alterations in J20 APP transgenic mice. Nat Commun 2013; 4: 1939.
[http://dx.doi.org/10.1038/ncomms2927] [PMID: 23748737]
[131]
Jaworski T, Lechat B, Demedts D, et al. Dendritic degeneration, neurovascular defects, and inflammation precede neuronal loss in a mouse model for tau-mediated neurodegeneration. Am J Pathol 2011; 179(4): 2001-15.
[http://dx.doi.org/10.1016/j.ajpath.2011.06.025] [PMID: 21839061]
[132]
Duyckaerts C, Delatour B, Potier MC. Classification and basic pathology of Alzheimer disease. Acta Neuropathol 2009; 118(1): 5-36.
[http://dx.doi.org/10.1007/s00401-009-0532-1] [PMID: 19381658]
[133]
Centonze D, Muzio L, Rossi S, Furlan R, Bernardi G, Martino G. The link between inflammation, synaptic transmission and neurodegeneration in multiple sclerosis. Cell Death Differ 2010; 17(7): 1083-91.
[http://dx.doi.org/10.1038/cdd.2009.179] [PMID: 19927157]
[134]
Tan AM, Stamboulian S, Chang YW, et al. Neuropathic pain memory is maintained by Rac1-regulated dendritic spine remodeling after spinal cord injury. J Neurosci 2008; 28(49): 13173-83.
[http://dx.doi.org/10.1523/JNEUROSCI.3142-08.2008] [PMID: 19052208]
[135]
Liberski PP, Brown DR, Sikorska B, Caughey B, Brown P. Cell death and autophagy in prion diseases (transmissible spongiform encephalopathies). Folia Neuropathol 2008; 46(1): 1-25.
[PMID: 18368623]
[136]
Mantyh CR, Pappas TN, Lapp JA, et al. Substance P activation of enteric neurons in response to intraluminal Clostridium difficile toxin A in the rat ileum. Gastroenterology 1996; 111(5): 1272-80.
[http://dx.doi.org/10.1053/gast.1996.v111.pm8898641] [PMID: 8898641]
[137]
White JA, Manelli AM, Holmberg KH, Van Eldik LJ, Ladu MJ. Differential effects of oligomeric and fibrillar amyloid-beta 1-42 on astrocyte-mediated inflammation. Neurobiol Dis 2005; 18(3): 459-65.
[http://dx.doi.org/10.1016/j.nbd.2004.12.013] [PMID: 15755672]
[138]
Lu X, Richardson PM. Inflammation near the nerve cell body enhances axonal regeneration. J Neurosci 1991; 11(4): 972-8.
[http://dx.doi.org/10.1523/JNEUROSCI.11-04-00972.1991] [PMID: 1901354]
[139]
Vercellino M, Masera S, Lorenzatti M, et al. Demyelination, inflammation, and neurodegeneration in multiple sclerosis deep gray matter. J Neuropathol Exp Neurol 2009; 68(5): 489-502.
[http://dx.doi.org/10.1097/NEN.0b013e3181a19a5a] [PMID: 19525897]
[140]
Leib SL, Kim YS, Chow LL, Sheldon RA, Täuber MG. Reactive oxygen intermediates contribute to necrotic and apoptotic neuronal injury in an infant rat model of bacterial meningitis due to group B streptococci. J Clin Invest 1996; 98(11): 2632-9.
[http://dx.doi.org/10.1172/JCI119084] [PMID: 8958228]
[141]
Sanovic S, Lamb DP, Blennerhassett MG. Damage to the enteric nervous system in experimental colitis. Am J Pathol 1999; 155(4): 1051-7.
[http://dx.doi.org/10.1016/S0002-9440(10)65207-8] [PMID: 10514387]
[142]
Linden DR, Couvrette JM, Ciolino A, et al. Indiscriminate loss of myenteric neurones in the TNBS-inflamed guinea-pig distal colon. Neurogastroenterol Motil 2005; 17(5): 751-60.
[http://dx.doi.org/10.1111/j.1365-2982.2005.00703.x] [PMID: 16185315]
[143]
Mawe GM. Colitis-induced neuroplasticity disrupts motility in the inflamed and post-inflamed colon. J Clin Invest 2015; 125(3): 949-55.
[http://dx.doi.org/10.1172/JCI76306] [PMID: 25729851]
[144]
Fu MH, Chen IC, Lee CH, et al. Anti-neuroinflammation ameliorates systemic inflammation-induced mitochondrial DNA impairment in the nucleus of the solitary tract and cardiovascular reflex dysfunction. J Neuroinflammation 2019; 16(1): 224.
[http://dx.doi.org/10.1186/s12974-019-1623-0] [PMID: 31729994]
[145]
Sharkey KA, Kroese AB. Consequences of intestinal inflammation on the enteric nervous system: Neuronal activation induced by inflammatory mediators. Anat Rec 2001; 262(1): 79-90.
[http://dx.doi.org/10.1002/1097-0185(20010101)262:1<79::AID-AR1013>3.0.CO;2-K] [PMID: 11146431]
[146]
Wood JD. Histamine, mast cells, and the enteric nervous system in the irritable bowel syndrome, enteritis, and food allergies. Gut 2006; 55(4): 445-7.
[http://dx.doi.org/10.1136/gut.2005.079046] [PMID: 16531524]
[147]
Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mörk S, Bö L. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 1998; 338(5): 278-85.
[http://dx.doi.org/10.1056/NEJM199801293380502] [PMID: 9445407]
[148]
Zemke AM, Boles LH, Gillespie M, Viljoen JM. Guillain-Barré syndrome hyponatremia: Is it SIADH or pseudohyponatremia? Oxf Med Case Rep 2018; 2018(7): omy042.
[http://dx.doi.org/10.1093/omcr/omy042] [PMID: 30090635]
[149]
Nikić I, Merkler D, Sorbara C, et al. A reversible form of axon damage in experimental autoimmune encephalomyelitis and multiple sclerosis. Nat Med 2011; 17(4): 495-9.
[http://dx.doi.org/10.1038/nm.2324] [PMID: 21441916]
[150]
Chalazonitis A, Rao M. Enteric nervous system manifestations of neurodegenerative disease. Brain Res 2018; 1693(Pt B): 207-13.
[http://dx.doi.org/10.1016/j.brainres.2018.01.011] [PMID: 29360466]
[151]
Popescu BF, Pirko I, Lucchinetti CF. Pathology of multiple sclerosis: Where do we stand? Continuum (Minneap Minn) 2013; 19(4 Multiple Sclerosis): 901-21.
[http://dx.doi.org/10.1212/01.CON.0000433291.23091.65] [PMID: 23917093]
[152]
Love S. Demyelinating diseases. J Clin Pathol 2006; 59(11): 1151-9.
[http://dx.doi.org/10.1136/jcp.2005.031195] [PMID: 17071802]
[153]
Hartlehnert M, Derksen A, Hagenacker T, et al. Schwann cells promote post-traumatic nerve inflammation and neuropathic pain through MHC class II. Sci Rep 2017; 7(1): 12518.
[http://dx.doi.org/10.1038/s41598-017-12744-2] [PMID: 28970572]
[154]
Gaudet AD, Popovich PG, Ramer MS. Wallerian degeneration: Gaining perspective on inflammatory events after peripheral nerve injury. J Neuroinflammation 2011; 8: 110.
[http://dx.doi.org/10.1186/1742-2094-8-110] [PMID: 21878126]
[155]
Rao M, Nelms BD, Dong L, et al. Enteric glia express proteolipid protein 1 and are a transcriptionally unique population of glia in the mammalian nervous system. Glia 2015; 63(11): 2040-57.
[http://dx.doi.org/10.1002/glia.22876] [PMID: 26119414]
[156]
Pochard C, Coquenlorge S, Freyssinet M, et al. The multiple faces of inflammatory enteric glial cells: Is Crohn’s disease a gliopathy? Am J Physiol Gastrointest Liver Physiol 2018; 315(1): G1-G11.
[http://dx.doi.org/10.1152/ajpgi.00016.2018] [PMID: 29517926]
[157]
Morales-Soto W, Gulbransen BD. Enteric Glia: A new player in abdominal pain. Cell Mol Gastroenterol Hepatol 2019; 7(2): 433-45.
[http://dx.doi.org/10.1016/j.jcmgh.2018.11.005] [PMID: 30739868]
[158]
Villanacci V, Bassotti G, Nascimbeni R, et al. Enteric nervous system abnormalities in inflammatory bowel diseases. Neurogastroenterol Motil 2008; 20(9): 1009-16.
[http://dx.doi.org/10.1111/j.1365-2982.2008.01146.x] [PMID: 18492026]
[159]
Kuhlmann T, Lingfeld G, Bitsch A, Schuchardt J, Brück W. Acute axonal damage in multiple sclerosis is most extensive in early disease stages and decreases over time. Brain 2002; 125(Pt 10): 2202-12.
[http://dx.doi.org/10.1093/brain/awf235] [PMID: 12244078]
[160]
Moreno B, Jukes JP, Vergara-Irigaray N, et al. Systemic inflammation induces axon injury during brain inflammation. Ann Neurol 2011; 70(6): 932-42.
[http://dx.doi.org/10.1002/ana.22550] [PMID: 22190366]
[161]
Lourenssen S, Wells RW, Blennerhassett MG. Differential responses of intrinsic and extrinsic innervation of smooth muscle cells in rat colitis. Exp Neurol 2005; 195(2): 497-507.
[http://dx.doi.org/10.1016/j.expneurol.2005.06.012] [PMID: 16098965]
[162]
Strobach RS, Ross AH, Markin RS, Zetterman RK, Linder J. Neural patterns in inflammatory bowel disease: An immunohistochemical survey. Mod Pathol 1990; 3(4): 488-93.
[PMID: 2217153]
[163]
Moynes DM, Lucas GH, Beyak MJ, Lomax AE. Effects of inflammation on the innervation of the colon. Toxicol Pathol 2014; 42(1): 111-7.
[http://dx.doi.org/10.1177/0192623313505929] [PMID: 24159054]
[164]
García-Cabo C, Morís G. Peripheral neuropathy: An underreported neurologic manifestation of inflammatory bowel disease. Eur J Intern Med 2015; 26(7): 468-75.
[http://dx.doi.org/10.1016/j.ejim.2015.07.013] [PMID: 26211733]
[165]
Wong J, Garcia-Carbonell R, Zelic M, et al. RIPK1 mediates TNF-induced intestinal crypt apoptosis during chronic NF-κB activation. Cell Mol Gastroenterol Hepatol 2020; 9(2): 295-312.
[http://dx.doi.org/10.1016/j.jcmgh.2019.10.002] [PMID: 31606566]
[166]
Werts AD, Fulton WB, Ladd MR, et al. A novel role for necroptosis in the pathogenesis of necrotizing enterocolitis. Cell Mol Gastroenterol Hepatol 2020; 9(3): 403-23.
[http://dx.doi.org/10.1016/j.jcmgh.2019.11.002] [PMID: 31756560]
[167]
Yi X, Chang X, Wang J, Yan C, Zhang B. Intestinal trefoil factor increased the Bcl-2 level in a necrotizingenterocolitis neonate rat model. Turk J Med Sci 2016; 46(3): 921-5.
[http://dx.doi.org/10.3906/sag-1501-65] [PMID: 27513274]
[168]
Chokshi NK, Guner YS, Hunter CJ, Upperman JS, Grishin A, Ford HR. The role of nitric oxide in intestinal epithelial injury and restitution in neonatal necrotizing enterocolitis. Semin Perinatol 2008; 32(2): 92-9.
[http://dx.doi.org/10.1053/j.semperi.2008.01.002] [PMID: 18346532]
[169]
Sayani FA, Keenan CM, Van Sickle MD, et al. The expression and role of Fas ligand in intestinal inflammation. Neurogastroenterol Motil 2004; 16(1): 61-74.
[http://dx.doi.org/10.1046/j.1365-2982.2003.00457.x] [PMID: 14764206]
[170]
Bach-Ngohou K, Mahé MM, Aubert P, et al. Enteric glia modulate epithelial cell proliferation and differentiation through 15-deoxy-12,14-prostaglandin J2. J Physiol 2010; 588(Pt 14): 2533-44.
[http://dx.doi.org/10.1113/jphysiol.2010.188409] [PMID: 20478974]
[171]
Verheijden S, De Schepper S, Boeckxstaens GE. Neuron-macrophage crosstalk in the intestine: A “microglia” perspective. Front Cell Neurosci 2015; 9: 403.
[http://dx.doi.org/10.3389/fncel.2015.00403] [PMID: 26528133]
[172]
Liu Y, Zhu L, Fatheree NY, et al. Changes in intestinal Toll-like receptors and cytokines precede histological injury in a rat model of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 2009; 297(3): G442-50.
[http://dx.doi.org/10.1152/ajpgi.00182.2009] [PMID: 19608731]
[173]
Richardson WM, Sodhi CP, Russo A, et al. 2010; Nucleotide-binding oligomerization domain-2 inhibits toll-like receptor-4 signaling in the intestinal epithelium. Gastroenterology 2010; 139: 904-17.
[http://dx.doi.org/10.1053/j.gastro.2010.05.038]
[174]
Freire P, Cardoso R, Figueiredo P, et al. NOD2 gene mutations in ulcerative colitis: Useless or misunderstood? Int J Colorectal Dis 2014; 29(6): 653-61.
[http://dx.doi.org/10.1007/s00384-014-1850-x] [PMID: 24651958]
[175]
Dziarski R, Gupta D. Role of MD-2 in TLR2- and TLR4-mediated recognition of Gram-negative and Gram-positive bacteria and activation of chemokine genes. J Endotoxin Res 2000; 6(5): 401-5.
[http://dx.doi.org/10.1177/09680519000060050101] [PMID: 11521063]
[176]
Chen Z, Zhang Y, Lin R, et al. Cronobacter sakazakii induces necrotizing enterocolitis by regulating NLRP3 inflammasome expression via TLR4. J Med Microbiol 2020; 69(5): 748-58.
[http://dx.doi.org/10.1099/jmm.0.001181] [PMID: 32209170]
[177]
Casanova JL, Abel L. Human Mannose-binding Lectin in Immunity: Friend, Foe, or Both? J Exp Med 2004; 199(10): 1295-9.
[http://dx.doi.org/10.1084/jem.20040537] [PMID: 15148331]
[178]
von Boyen GB, Steinkamp M, Reinshagen M, Schäfer KH, Adler G, Kirsch J. Proinflammatory cytokines increase glial fibrillary acidic protein expression in enteric glia. Gut 2004; 53(2): 222-8.
[http://dx.doi.org/10.1136/gut.2003.012625] [PMID: 14724154]
[179]
Denning TL, Bhatia AM, Kane AF, Patel RM, Denning PW. Pathogenesis of NEC: Role of the innate and adaptive immune response. Semin Perinatol 2017; 41(1): 15-28.
[http://dx.doi.org/10.1053/j.semperi.2016.09.014] [PMID: 27940091]
[180]
Lawrence SM, Ruoss JL, Wynn JL. IL-17 in neonatal health and disease. Am J Reprod Immunol 2018; 79(5): e12800.
[http://dx.doi.org/10.1111/aji.12800] [PMID: 29243317]

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