{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T10:51:07Z","timestamp":1790247067801,"version":"4.1.0"},"reference-count":75,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2019,4,24]],"date-time":"2019-04-24T00:00:00Z","timestamp":1556064000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Nitrergic enteric neurons are key players of the descending inhibitory reflex of intestinal peristalsis, therefore loss or damage of these neurons can contribute to developing gastrointestinal motility disturbances suffered by patients worldwide. There is accumulating evidence that the vulnerability of nitrergic enteric neurons to neuropathy is strictly region-specific and that the two main enteric plexuses display different nitrergic neuronal damage. Alterations both in the proportion of the nitrergic subpopulation and in the total number of enteric neurons suggest that modification of the neurochemical character or neuronal death occurs in the investigated gut segments. This review aims to summarize the gastrointestinal region and\/or plexus-dependent pathological changes in the number of nitric oxide synthase (NOS)-containing neurons, the NO release and the cellular and subcellular expression of different NOS isoforms. Additionally, some of the underlying mechanisms associated with the nitrergic pathway in the background of different diseases, e.g., type 1 diabetes, chronic alcoholism, intestinal inflammation or ischaemia, will be discussed.<\/jats:p>","DOI":"10.3390\/ijms20082003","type":"journal-article","created":{"date-parts":[[2019,4,25]],"date-time":"2019-04-25T03:02:59Z","timestamp":1556161379000},"page":"2003","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":54,"title":["Nitrergic Enteric Neurons in Health and Disease\u2014Focus on Animal Models"],"prefix":"10.3390","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9774-1387","authenticated-orcid":false,"given":"Nikolett","family":"B\u00f3di","sequence":"first","affiliation":[{"name":"Department of Physiology, Anatomy and Neuroscience, Faculty of Science and Informatics, University of Szeged, H-6726 Szeged, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zita","family":"Szalai","sequence":"additional","affiliation":[{"name":"Department of Physiology, Anatomy and Neuroscience, Faculty of Science and Informatics, University of Szeged, H-6726 Szeged, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3533-9461","authenticated-orcid":false,"given":"M\u00e1ria","family":"Bagy\u00e1nszki","sequence":"additional","affiliation":[{"name":"Department of Physiology, Anatomy and Neuroscience, Faculty of Science and Informatics, University of Szeged, H-6726 Szeged, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,4,24]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1093\/eurheartj\/ehr304","article-title":"Nitric oxide synthases: Regulation and function","volume":"33","author":"Forstermann","year":"2012","journal-title":"Eur. Heart J."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1111\/bph.14527","article-title":"Nitric oxide in the gastrointestinal tract: Opportunities for drug development","volume":"176","author":"Wallace","year":"2019","journal-title":"Br. J. Pharmacol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1556\/ABiol.60.2009.4.2","article-title":"Spatial pattern analysis of nitrergic neurons in the myenteric plexus of the duodenum of different mammalian species","volume":"60","author":"Bodi","year":"2009","journal-title":"Acta Biol. Hung."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1111\/bph.14459","article-title":"Nitric oxide and its role as a non-adrenergic, non-cholinergic inhibitory neurotransmitter in the gastrointestinal tract","volume":"176","author":"Sanders","year":"2019","journal-title":"Br. J. Pharmacol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"980","DOI":"10.1111\/j.1365-2982.2011.01780.x","article-title":"The involvement of nitric oxide synthase neurons in enteric neuropathies","volume":"23","author":"Rivera","year":"2011","journal-title":"Neurogastroenterol. Motil."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.autneu.2006.05.003","article-title":"The organisation of the autonomic nervous system: Peripheral connections","volume":"130","author":"Furness","year":"2006","journal-title":"Auton Neurosci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1038\/nrgastro.2012.32","article-title":"The enteric nervous system and neurogastroenterology","volume":"9","author":"Furness","year":"2012","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"250","DOI":"10.1016\/j.autneu.2006.02.015","article-title":"Effects of gastrointestinal inflammation on enteroendocrine cells and enteric neural reflex circuits","volume":"126\u2013127","author":"Lomax","year":"2006","journal-title":"Auton Neurosci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1007\/978-1-4939-0897-4_3","article-title":"The enteric nervous system and gastrointestinal innervation: Integrated local and central control","volume":"817","author":"Furness","year":"2014","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1186\/s12974-019-1434-3","article-title":"Impact of microbiota on central nervous system and neurological diseases: The gut-brain axis","volume":"16","author":"Ma","year":"2019","journal-title":"J. Neuroinflamm."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Wirth, R., Bodi, N., Maroti, G., Bagyanszki, M., Talapka, P., Fekete, E., Bagi, Z., and Kovacs, K.L. (2014). Regionally distinct alterations in the composition of the gut microbiota in rats with streptozotocin-induced diabetes. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0110440"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2989","DOI":"10.1113\/jphysiol.2014.273995","article-title":"The microbiota-gut-brain axis in gastrointestinal disorders: Stressed bugs, stressed brain or both?","volume":"592","author":"Collins","year":"2014","journal-title":"J. Physiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/S0165-1838(00)00127-2","article-title":"Types of neurons in the enteric nervous system","volume":"81","author":"Furness","year":"2000","journal-title":"J. Auton Nerv. Syst."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1007\/s00441-008-0684-7","article-title":"Immunohistochemical analysis of neuron types in the mouse small intestine","volume":"334","author":"Qu","year":"2008","journal-title":"Cell Tissue Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2359","DOI":"10.1002\/jcp.25518","article-title":"Neurotransmitters: The Critical Modulators Regulating Gut-Brain Axis","volume":"232","author":"Mittal","year":"2017","journal-title":"J. Cell Physiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"379","DOI":"10.3109\/07853899509002591","article-title":"Nitric oxide in the peripheral nervous system","volume":"27","author":"Lefebvre","year":"1995","journal-title":"Ann. Med."},{"key":"ref_17","first-page":"G275","article-title":"Nitrergic regulation of colonic transit in rats","volume":"277","author":"Mizuta","year":"1999","journal-title":"Am. J. Physiol."},{"key":"ref_18","first-page":"1547","article-title":"Gut region-specific rearrangement of the cellular and subcellular compartments of nitric oxide synthase isoforms after chronic ethanol consumption in rats","volume":"29","author":"Bodi","year":"2014","journal-title":"Histol. Histopathol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1016\/0896-6273(91)90374-9","article-title":"Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase","volume":"7","author":"Bredt","year":"1991","journal-title":"Neuron"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1053\/gast.1996.v111.pm8698225","article-title":"Colitis and interleukin 1beta up-regulate inducible nitric oxide synthase and superoxide dismutase in rat myenteric neurons","volume":"111","author":"Valentine","year":"1996","journal-title":"Gastroenterology"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/S0304-3940(02)00338-5","article-title":"Myenteric neurons and interstitial cells of Cajal of mouse colon express several nitric oxide synthase isoforms","volume":"326","author":"Vannucchi","year":"2002","journal-title":"Neurosci. Lett."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1026","DOI":"10.3748\/wjg.v17.i8.1026","article-title":"Subcellular distribution of nitric oxide synthase isoforms in the rat duodenum","volume":"17","author":"Talapka","year":"2011","journal-title":"World J. Gastroenterol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e237","DOI":"10.1111\/j.1365-2982.2011.01707.x","article-title":"Chronic alcohol consumption induces an overproduction of NO by nNOS- and iNOS-expressing myenteric neurons in the murine small intestine","volume":"23","author":"Bagyanszki","year":"2011","journal-title":"Neurogastroenterol. Motil."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1007\/s00441-009-0773-2","article-title":"Identification of neuron types in the submucosal ganglia of the mouse ileum","volume":"336","author":"Thacker","year":"2009","journal-title":"Cell Tissue Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"3387","DOI":"10.1002\/cne.22679","article-title":"Neurochemical phenotypes of myenteric neurons in the rhesus monkey","volume":"519","author":"Noorian","year":"2011","journal-title":"J. Comp. Neurol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"3683","DOI":"10.2174\/1381612043382792","article-title":"Point of NO return for nitrergic nerves in diabetes: A new insight into diabetic complications","volume":"10","author":"Cellek","year":"2004","journal-title":"Curr. Pharm. Des."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1016\/j.diabres.2007.12.013","article-title":"Immediate insulin treatment prevents gut motility alterations and loss of nitrergic neurons in the ileum and colon of rats with streptozotocin-induced diabetes","volume":"80","author":"Izbeki","year":"2008","journal-title":"Diabetes Res. Clin. Pract."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"161","DOI":"10.5056\/jnm.2013.19.2.161","article-title":"Gastrointestinal motility changes and myenteric plexus alterations in spontaneously diabetic biobreeding rats","volume":"19","author":"Demedts","year":"2013","journal-title":"J. Neurogastroenterol. Motil."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1172\/JCI8273C1","article-title":"Insulin restores neuronal nitric oxide synthase expression and function that is lost in diabetic gastropathy","volume":"106","author":"Watkins","year":"2000","journal-title":"J. Clin. Investig."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/j.autneu.2016.04.004","article-title":"Quantification of nitrergic neurons in the myenteric plexus of gastric antrum and ileum of healthy and diabetic dogs","volume":"197","author":"Giancola","year":"2016","journal-title":"Auton Neurosci."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1111\/j.1365-2982.2007.01040.x","article-title":"Distribution of interstitial cells of Cajal and nitrergic neurons in normal and diabetic human appendix","volume":"20","author":"Miller","year":"2008","journal-title":"Neurogastroenterol. Motil."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/j.ejphar.2019.02.033","article-title":"Diabetes-induced damage of gastric nitric oxide neurons mediated by P2\u00d77R in diabetic mice","volume":"851","author":"Zhang","year":"2019","journal-title":"Eur. J. Pharmacol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1016\/S1566-0702(01)00317-4","article-title":"Enhanced colonic peristalsis by impairment of nitrergic enteric neurons in spontaneously diabetic rats","volume":"92","author":"Yoneda","year":"2001","journal-title":"Auton Neurosci."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"967","DOI":"10.1111\/j.1530-0277.2006.00110.x","article-title":"Chronic ethanol exposure impairs neuronal nitric oxide synthase in the rat intestine","volume":"30","author":"Krecsmarik","year":"2006","journal-title":"Alcohol Clin. Exp. Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"7359","DOI":"10.3748\/wjg.v23.i41.7359","article-title":"Region-dependent effects of diabetes and insulin-replacement on neuronal nitric oxide synthase- and heme oxygenase-immunoreactive submucous neurons","volume":"23","author":"Bodi","year":"2017","journal-title":"World J. Gastroenterol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1111\/j.1549-8719.2012.00164.x","article-title":"Gut region-specific diabetic damage to the capillary endothelium adjacent to the myenteric plexus","volume":"19","author":"Bodi","year":"2012","journal-title":"Microcirculation"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"80","DOI":"10.4239\/wjd.v3.i5.80","article-title":"Diabetes-related alterations in the enteric nervous system and its microenvironment","volume":"3","author":"Bagyanszki","year":"2012","journal-title":"World J. Diabetes"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"G725","DOI":"10.1152\/ajpgi.00406.2006","article-title":"Diabetes induces sex-dependent changes in neuronal nitric oxide synthase dimerization and function in the rat gastric antrum","volume":"292","author":"Gangula","year":"2007","journal-title":"Am. J. Physiol. Gastrointest. Liver Physiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"G692","DOI":"10.1152\/ajpgi.00450.2009","article-title":"Tetrahydrobiopterin (BH4), a cofactor for nNOS, restores gastric emptying and nNOS expression in female diabetic rats","volume":"298","author":"Gangula","year":"2010","journal-title":"Am. J. Physiol. Gastrointest. Liver Physiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"2353","DOI":"10.2337\/diabetes.52.9.2353","article-title":"Two phases of nitrergic neuropathy in streptozotocin-induced diabetic rats","volume":"52","author":"Cellek","year":"2003","journal-title":"Diabetes"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1007\/s00125-003-1298-y","article-title":"Synergistic action of advanced glycation end products and endogenous nitric oxide leads to neuronal apoptosis in vitro: A new insight into selective nitrergic neuropathy in diabetes","volume":"47","author":"Cellek","year":"2004","journal-title":"Diabetologia"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1111\/j.1365-2982.2006.00774.x","article-title":"Suppression of nNOS expression in rat enteric neurones by the receptor for advanced glycation end-products","volume":"18","author":"Korenaga","year":"2006","journal-title":"Neurogastroenterol. Motil."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1111\/j.1365-2982.2007.01018.x","article-title":"Inhibitors of advanced glycation end-products prevent loss of enteric neuronal nitric oxide synthase in diabetic rats","volume":"20","author":"Jeyabal","year":"2008","journal-title":"Neurogastroenterol. Motil."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1890512","DOI":"10.1155\/2017\/1890512","article-title":"Diabetes-Related Induction of the Heme Oxygenase System and Enhanced Colocalization of Heme Oxygenase 1 and 2 with Neuronal Nitric Oxide Synthase in Myenteric Neurons of Different Intestinal Segments","volume":"2017","author":"Chandrakumar","year":"2017","journal-title":"Oxid. Med. Cell Longev."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/j.brainres.2005.11.057","article-title":"Diabetes only affects nitric oxide synthase-containing myenteric neurons that do not contain heme oxygenase 2","volume":"1068","author":"Shotton","year":"2006","journal-title":"Brain Res."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"51","DOI":"10.4291\/wjgp.v6.i3.51","article-title":"Gut region-dependent alterations of nitrergic myenteric neurons after chronic alcohol consumption","volume":"6","author":"Bagyanszki","year":"2015","journal-title":"World J. Gastrointest. Pathophysiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1536","DOI":"10.1002\/ar.21192","article-title":"Chronic alcohol consumption affects gastrointestinal motility and reduces the proportion of neuronal NOS-immunoreactive myenteric neurons in the murine jejunum","volume":"293","author":"Bagyanszki","year":"2010","journal-title":"Anat. Rec."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1080","DOI":"10.1016\/j.neuro.2008.08.007","article-title":"The protective effect of neuronal nitric oxide synthase (nNOS) against alcohol toxicity depends upon the NO-cGMP-PKG pathway and NF-kappaB","volume":"29","author":"Bonthius","year":"2008","journal-title":"Neurotoxicology"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1007\/s10571-015-0155-0","article-title":"The neuronal nitric oxide synthase (nNOS) gene and neuroprotection against alcohol toxicity","volume":"35","author":"Karacay","year":"2015","journal-title":"Cell Mol. Neurobiol"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"16690","DOI":"10.3748\/wjg.v20.i44.16690","article-title":"Alleviated mucosal and neuronal damage in a rat model of Crohn\u2019s disease","volume":"20","author":"Talapka","year":"2014","journal-title":"World J. Gastroenterol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1016\/j.yexmp.2005.04.006","article-title":"Deficient innervation characterizes intestinal strictures in a rat model of colitis","volume":"80","author":"Marlow","year":"2006","journal-title":"Exp. Mol. Pathol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/j.autneu.2007.03.001","article-title":"Differential responses of VIPergic and nitrergic neurons in paediatric patients with Crohn\u2019s disease","volume":"134","author":"Boyer","year":"2007","journal-title":"Auton Neurosci."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"G295","DOI":"10.1152\/ajpgi.00052.2013","article-title":"Paradoxical regulation of ChAT and nNOS expression in animal models of Crohn\u2019s colitis and ulcerative colitis","volume":"305","author":"Winston","year":"2013","journal-title":"Am. J. Physiol. Gastrointest. Liver Physiol"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"310","DOI":"10.5056\/jnm15082","article-title":"Changes in Enteric Neurons of Small Intestine in a Rat Model of Irritable Bowel Syndrome with Diarrhea","volume":"22","author":"Li","year":"2016","journal-title":"J. Neurogastroenterol. Motil."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1007\/s00441-015-2251-3","article-title":"Alterations in the distal colon innervation in Winnie mouse model of spontaneous chronic colitis","volume":"362","author":"Rahman","year":"2015","journal-title":"Cell Tissue Res."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1046\/j.1365-2982.2001.00265.x","article-title":"Neurotransmitter coding of enteric neurones in the submucous plexus is changed in non-inflamed rectum of patients with Crohn\u2019s disease","volume":"13","author":"Schneider","year":"2001","journal-title":"Neurogastroenterol. Motil."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1111\/nmo.12327","article-title":"The neurochemical changes in the innervation of human colonic mesenteric and submucosal blood vessels in ulcerative colitis and Crohn\u2019s disease","volume":"26","author":"Brookes","year":"2014","journal-title":"Neurogastroenterol. Motil."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1051","DOI":"10.1016\/S0002-9440(10)65207-8","article-title":"Damage to the enteric nervous system in experimental colitis","volume":"155","author":"Sanovic","year":"1999","journal-title":"Am. J. Pathol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1016\/j.nbd.2014.12.014","article-title":"Early inflammatory damage to intestinal neurons occurs via inducible nitric oxide synthase","volume":"75","author":"Venkataramana","year":"2015","journal-title":"Neurobiol. Dis."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1136\/gutjnl-2012-302090","article-title":"Enteroglial-derived S100B protein integrates bacteria-induced Toll-like receptor signalling in human enteric glial cells","volume":"63","author":"Turco","year":"2014","journal-title":"Gut"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.jcmgh.2015.08.007","article-title":"Enteric glia mediate neuron death in colitis through purinergic pathways that require connexin-43 and nitric oxide","volume":"2","author":"Brown","year":"2016","journal-title":"Cell Mol. Gastroenterol. Hepatol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"718","DOI":"10.1136\/gut.36.5.718","article-title":"Enhanced colonic nitric oxide generation and nitric oxide synthase activity in ulcerative colitis and Crohn\u2019s disease","volume":"36","author":"Rachmilewitz","year":"1995","journal-title":"Gut"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"3386","DOI":"10.3748\/wjg.v12.i21.3386","article-title":"Rectal nitric oxide as biomarker in the treatment of inflammatory bowel disease: Responders versus nonresponders","volume":"12","author":"Ljung","year":"2006","journal-title":"World J. Gastroenterol."},{"key":"ref_64","first-page":"129","article-title":"Inflammatory bowel disease affects density of nitrergic nerve fibers in the mucosal layer of the canine gastrointestinal tract","volume":"81","author":"Rychlik","year":"2017","journal-title":"Can. J. Vet. Res."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1080\/107710498174227","article-title":"Alterations of the enteric nervous system in neonatal necrotizing enterocolitis revealed by whole-mount immunohistochemistry","volume":"18","author":"Wedel","year":"1998","journal-title":"Pediatr. Pathol. Lab. Med."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1212","DOI":"10.1023\/B:DDAS.0000037815.63547.08","article-title":"Structural and neuronal changes in rat ileum after ischemia with reperfusion","volume":"49","author":"Lindestrom","year":"2004","journal-title":"Dig. Dis. Sci."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1007\/s00428-009-0739-5","article-title":"Apoptosis of interstitial cells of Cajal, smooth muscle cells, and enteric neurons induced by intestinal ischemia and reperfusion injury in adult guinea pigs","volume":"454","author":"Mei","year":"2009","journal-title":"Virchows Arch."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1007\/s00441-012-1451-3","article-title":"Knock out of neuronal nitric oxide synthase exacerbates intestinal ischemia\/reperfusion injury in mice","volume":"349","author":"Rivera","year":"2012","journal-title":"Cell Tissue Res."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1007\/s00401-009-0549-5","article-title":"The reactions of specific neuron types to intestinal ischemia in the guinea pig enteric nervous system","volume":"118","author":"Rivera","year":"2009","journal-title":"Acta Neuropathol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"3252","DOI":"10.1007\/s10620-015-3742-5","article-title":"Resveratrol Reduces Morphologic Changes in the Myenteric Plexus and Oxidative Stress in the Ileum in Rats with Ischemia\/Reperfusion Injury","volume":"60","author":"Borges","year":"2015","journal-title":"Dig. Dis. Sci."},{"key":"ref_71","first-page":"489","article-title":"Differential effects of intestinal ischemia and reperfusion in rat enteric neurons and glial cells expressing P2 \u00d7 2 receptors","volume":"30","author":"Marosti","year":"2015","journal-title":"Histol. Histopathol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1007\/s00441-010-1126-x","article-title":"Deleterious effects of intestinal ischemia\/reperfusion injury in the mouse enteric nervous system are associated with protein nitrosylation","volume":"344","author":"Rivera","year":"2011","journal-title":"Cell Tissue Res."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"9265","DOI":"10.1073\/pnas.84.24.9265","article-title":"Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide","volume":"84","author":"Ignarro","year":"1987","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"524","DOI":"10.1038\/327524a0","article-title":"Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor","volume":"327","author":"Palmer","year":"1987","journal-title":"Nature"},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Joca, S.R.L., Sartim, A.G., Roncalho, A.L., Diniz, C.F.A., and Wegener, G. (2019). Nitric oxide signalling and antidepressant action revisited. Cell Tissue Res.","DOI":"10.1007\/s00441-018-02987-4"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/20\/8\/2003\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T12:46:41Z","timestamp":1760186801000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/20\/8\/2003"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,4,24]]},"references-count":75,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2019,4]]}},"alternative-id":["ijms20082003"],"URL":"https:\/\/doi.org\/10.3390\/ijms20082003","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,4,24]]}}}