{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,12]],"date-time":"2025-10-12T06:12:12Z","timestamp":1760249532968,"version":"build-2065373602"},"reference-count":43,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2021,2,4]],"date-time":"2021-02-04T00:00:00Z","timestamp":1612396800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100007817","name":"Uniwersytet Rzeszowski","doi-asserted-by":"publisher","award":["UR"],"award-info":[{"award-number":["UR"]}],"id":[{"id":"10.13039\/501100007817","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>The enteric nervous system (ENS) is the part of the nervous system that is located in the wall of the gastrointestinal tract and regulates the majority of the functions of the stomach and intestine. Enteric neurons may contain various active substances that act as neuromediators and\/or neuromodulators. One of them is a gaseous substance, namely nitric oxide (NO). It is known that NO in the gastrointestinal (GI) tract may possess inhibitory functions; however, many of the aspects connected with the roles of this substance, especially during pathological states, remain not fully understood. An experiment is performed here with 15 pigs divided into 3 groups: C group (without any treatment), C1 group (\u201csham\u201d operated), and C2 group, in which experimental inflammation was induced. The aim of this study is to investigate the influence of inflammation on nitrergic nervous structures in the muscular layer of the porcine descending colon using an immunofluorescence method. The obtained results show that inflammation causes an increase in the percentage of nitric oxide synthase (nNOS)-positive neurons in the myenteric plexus of the ENS, as well as the number of nitrergic nerve fibers in the muscular layer of the descending colon. The obtained results suggest that NO is involved in the pathological condition of the large bowel and probably takes part in neuroprotective and\/or adaptive processes.<\/jats:p>","DOI":"10.3390\/ani11020394","type":"journal-article","created":{"date-parts":[[2021,2,4]],"date-time":"2021-02-04T03:15:28Z","timestamp":1612408528000},"page":"394","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Chemically-Induced Inflammation Changes the Number of Nitrergic Nervous Structures in the Muscular Layer of the Porcine Descending Colon"],"prefix":"10.3390","volume":"11","author":[{"given":"Liliana","family":"Rytel","sequence":"first","affiliation":[{"name":"Department of Internal Disease with Clinic, Faculty of Veterinary Medicine, University of Warmia and Mazury, Street Oczapowskiego 14, 10-719 Olsztyn, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ignacy","family":"Gonkowski","sequence":"additional","affiliation":[{"name":"Students\u2019 Scientific Club of Pathophysiologists, Department of Human Physiology and Pathophysiology, School of Medicine, University of Warmia and Mazury, 10-082 Olsztyn, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3522-1327","authenticated-orcid":false,"given":"Waldemar","family":"Grzegorzewski","sequence":"additional","affiliation":[{"name":"Interdisciplinary Center for Preclinical and Clinical Research, Department of Biotechnology, Institute of Biology and Biotechnology, College of Natural Sciences, University of Rzeszow, Pigonia 1 str., 35-310 Rzeszow, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0856-3644","authenticated-orcid":false,"given":"Joanna","family":"Wojtkiewicz","sequence":"additional","affiliation":[{"name":"Department of Human Physiology and Pathophysiology, School of Medicine, University of Warmia and Mazury, 10-082 Olsztyn, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,2,4]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1097\/01.mog.0000208459.46395.16","article-title":"Enteric nervous system","volume":"22","author":"Grundy","year":"2006","journal-title":"Curr. Opin. Gastroenterol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"S4","DOI":"10.1097\/01.scs.0000180285.51365.55","article-title":"Control of gastrointestinal motility by the \u201cgut brain\u201d\u2014The enteric nervous system","volume":"41","author":"Schemann","year":"2005","journal-title":"J. Pediatr. Gastroenterol. Nutr."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"e13234","DOI":"10.1111\/nmo.13234","article-title":"The first brain: Species comparisons and evolutionary implications for the enteric and central nervous systems","volume":"30","author":"Furness","year":"2018","journal-title":"Neurogastroenterol. Motil."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1034\/j.1600-0773.2003.t01-1-920301.x","article-title":"The enteric nervous system I: Organisation and classification","volume":"92","author":"Hansen","year":"2003","journal-title":"Pharmacol. Toxicol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1007\/s12640-016-9675-8","article-title":"T2 toxin-induced changes in cocaine- and amphetamine-regulated transcript (CART)-like immunoreactivity in the enteric nervous system within selected fragments of the porcine digestive tract","volume":"1","author":"Makowska","year":"2017","journal-title":"Neurotox. Res."},{"key":"ref_6","first-page":"219","article-title":"Immunolocalization of NOS, VIP, galanin and SP in the small intestine of suckling pigs treated with red kidney bean (Phaseolus vulgaris) lectin","volume":"3","author":"Arciszewski","year":"2013","journal-title":"Acta Histochem."},{"key":"ref_7","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_8","doi-asserted-by":"crossref","first-page":"1593","DOI":"10.1038\/ncomms15937","article-title":"Transplantation of enteric nervous system stem cells rescues nitric oxide synthase deficient mouse colon","volume":"8","author":"McCann","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1111\/j.1574-695X.2007.00329.x","article-title":"The role of nitric oxide in inflammatory reactions","volume":"51","author":"Tripathi","year":"2007","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"G627","DOI":"10.1152\/ajpgi.00519.2007","article-title":"Active and inactive pools of nNOS in the nerve terminals in mouse gut: Implications for nitrergic neurotransmission","volume":"294","author":"Rao","year":"2008","journal-title":"Am. J. Physiol. Gastrointest. Liver. Physiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/B978-0-12-800254-4.00005-2","article-title":"Nitric oxide in the nervous system: Biochemical, developmental, and neurobiological aspects","volume":"96","author":"Cossenza","year":"2014","journal-title":"Vitam. Horm."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"619","DOI":"10.2298\/VSP131025051S","article-title":"Multidisciplinary approach to nitric oxide signaling: Focus on the gastrointestinal and the central nervous system","volume":"72","author":"Djuric","year":"2015","journal-title":"Vojnosanit. Pregl."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/B978-0-12-800254-4.00006-4","article-title":"Hippocampus and nitric oxide","volume":"96","author":"Hu","year":"2014","journal-title":"Vitam. Horm."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1016\/j.coph.2014.07.009","article-title":"Importance of NO and its related compounds in enteric nervous system regulation of gut homeostasis and disease susceptibility","volume":"19","author":"Savidge","year":"2014","journal-title":"Curr. Opin. Pharmacol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"B\u00f3di, N., Szalai, Z., and Bagy\u00e1nszki, M. (2019). Nitrergic Enteric Neurons in Health and Disease-Focus on Animal Models. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20082003"},{"key":"ref_16","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_17","doi-asserted-by":"crossref","first-page":"31","DOI":"10.3923\/ijp.2011.31.39","article-title":"Nitric oxide and the gastrointestinal tract","volume":"7","author":"Kochar","year":"2011","journal-title":"Int. J. Pharmacol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1006\/gcen.2000.7568","article-title":"Ontogeny of neurohormonal peptides, serotonin, and nitric oxide synthase in the gastrointestinal neuroendocrine system of the axolotl (Ambystoma mexicanum): An immunohistochemical analysis","volume":"121","author":"Maake","year":"2001","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.pharmthera.2010.12.006","article-title":"Regulatory mechanism of duodenal bicarbonate secretion: Roles of endogenous prostaglandins and nitric oxide","volume":"130","author":"Takeuchi","year":"2011","journal-title":"Pharmacol. Ther."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1397","DOI":"10.1016\/S1567-5769(01)00086-8","article-title":"Nitric oxide in immunity and inflammation","volume":"8","author":"Coleman","year":"2001","journal-title":"Int. Immunopharmacol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.regpep.2008.09.005","article-title":"Autoinhibition of endothelial nitric oxide synthase (eNOS) in gut smooth muscle by nitric oxide","volume":"151","author":"Grider","year":"2008","journal-title":"Regul. Pept."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1078-e282","DOI":"10.1111\/j.1365-2982.2010.01532.x","article-title":"Tonic inhibition of human small intestinal motility by nitric oxide in children but not in adults","volume":"22","author":"Wittmeyer","year":"2010","journal-title":"Neurogastroenterol. Motil."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1007\/s00384-005-0744-3","article-title":"Nitric oxide synthase inhibition results in immediate postoperative recovery of gastric, small intestinal and colonic motility in awake rats","volume":"21","author":"Meile","year":"2006","journal-title":"Int. J. Colorectal. Dis."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.niox.2018.08.001","article-title":"Nitric oxide as an active substance in the enteric neurons of the porcine digestive tract in physiological conditions and under intoxication with bisphenol A (BPA)","volume":"80","author":"Szymanska","year":"2018","journal-title":"Nitric Oxide"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Makowska, K., and Gonkowski, S. (2019). Age and sex-dependent differences in the neurochemical characterization of calcitonin gene-related peptide-like immunoreactive (CGRP-LI) nervous structures in the porcine descending colon. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20051024"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Rychlik, A., Gonkowski, S., Kaczmar, E., Obremski, K., Calka, J., and Makowska, K. (2020). The T2 toxin produced by Fusarium spp. impacts porcine duodenal nitric oxide synthase (nNOS)-positive nervous structures-the preliminary study. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21145118"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1089\/dna.1994.13.839","article-title":"The neuronal marker protein gene product 9.5 (PGP 9.5) is phenotypically expressed in human breast epithelium, in milk, and in benign and malignant breast tumors","volume":"13","author":"Schumacher","year":"1994","journal-title":"DNA Cell Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1016\/j.pneurobio.2009.10.020","article-title":"UCHL1 (PGP 9.5): Neuronal biomarker and ubiquitin system protein","volume":"90","author":"Day","year":"2010","journal-title":"Prog. Neurobiol."},{"key":"ref_29","first-page":"521","article-title":"The immunolocalization of PGP 9.5 in normal human kidney and renal cell carcinoma","volume":"18","author":"Malinovsky","year":"1997","journal-title":"G Chir."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1046\/j.1523-1747.1998.00330.x","article-title":"Protein gene product 9.5 is expressed by fibroblasts in human cutaneous wounds","volume":"111","author":"Olerud","year":"1998","journal-title":"J. Invest. Dermatol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1007\/BF00572899","article-title":"Protein gene product 9.5 and ubiquitin immunoreactivities in rat epididymis epithelium","volume":"100","author":"Santamaria","year":"1993","journal-title":"Histochemistry"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Makowska, K., and Gonkowski, S. (2018). The influence of inflammation and nerve damage on the neurochemical characterization of calcitonin gene-related peptide-like immunoreactive (CGRP-LI) neurons in the enteric nervous system of the porcine descending colon. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19020548"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e13300","DOI":"10.1111\/nmo.13300","article-title":"Nitrergic signaling via interstitial cells of Cajal and smooth muscle cells influences circular smooth muscle contractility in murine colon","volume":"30","author":"Beck","year":"2018","journal-title":"Neurogastroenterol. Motil."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1111\/j.1439-0264.2006.00744.x","article-title":"The distribution and chemical coding of intramural neurons supplying the porcine stomach-the study on normal pigs and on animals suffering from swine dysentery","volume":"36","author":"Kaleczyc","year":"2007","journal-title":"Anat. Histol. Embryol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1016\/j.freeradbiomed.2011.04.041","article-title":"Nitric oxide counteracts the hyperoxia-induced proliferation and proinflammatory responses of mouse astrocytes","volume":"51","author":"Bruno","year":"2011","journal-title":"Free Radic. Biol. Med."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1157","DOI":"10.1189\/jlb.0310149","article-title":"The regulatory role of nitric oxide in proinflammatory cytokine expression during the induction and resolution of inflammation","volume":"88","author":"Kobayashi","year":"2010","journal-title":"J. Leukoc. Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.fct.2017.01.017","article-title":"Nitric oxide (NO)-mediated mitochondrial damage plays a critical role in T-2 toxin-induced apoptosis and growth hormone deficiency in rat anterior pituitary GH3 cells","volume":"102","author":"Liu","year":"2017","journal-title":"Food Chem. Toxicol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1186\/s40035-018-0108-x","article-title":"Hydrogen sulfide, nitric oxide, and neurodegenerative disorders","volume":"7","author":"Panthi","year":"2018","journal-title":"Transl. Neurodegener."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.neuroscience.2018.02.017","article-title":"Nitric oxide and mitochondrial function in neurological diseases","volume":"376","author":"Ghasemi","year":"2018","journal-title":"Neuroscience"},{"key":"ref_40","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":"Bonthius","year":"2015","journal-title":"Cell. Mol. Neurobiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"766","DOI":"10.1038\/nrn2214","article-title":"Nitric oxide in the central nervous system: Neuroprotection versus neurotoxicity","volume":"8","author":"Calabrese","year":"2007","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.niox.2018.01.011","article-title":"Nitrite potentiates the vasodilatory signaling of S-nitrosothiols","volume":"75","author":"Liu","year":"2018","journal-title":"Nitric Oxide"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1296","DOI":"10.1002\/glia.23603","article-title":"Nitric oxide as a messenger between neurons and satellite glial cells in dorsal root ganglia","volume":"67","author":"Belzer","year":"2019","journal-title":"Glia"}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/11\/2\/394\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:19:49Z","timestamp":1760159989000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/11\/2\/394"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,2,4]]},"references-count":43,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2021,2]]}},"alternative-id":["ani11020394"],"URL":"https:\/\/doi.org\/10.3390\/ani11020394","relation":{},"ISSN":["2076-2615"],"issn-type":[{"type":"electronic","value":"2076-2615"}],"subject":[],"published":{"date-parts":[[2021,2,4]]}}}