{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,14]],"date-time":"2025-10-14T00:52:26Z","timestamp":1760403146270,"version":"build-2065373602"},"reference-count":46,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2020,1,15]],"date-time":"2020-01-15T00:00:00Z","timestamp":1579046400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>Somatostatin (SOM) is the most common agent in the gastrointestinal (GI) tract that is involved in the regulation of several gastric functions, as well as in gastric disorders. Hyperglycemia, which develops as a consequence of improperly treated diabetes, can cause numerous disturbances in the appropriate functioning of the gastrointestinal tract. High glucose level is toxic to neurons. One of the lines of defense of neurons against this glucotoxicity are changes in their chemical coding. To better understood the role of SOM secreted by enteric neurons in neuronal response on elevated glucose level, pancreatic \u03b2 cells were destroyed using streptozotocin. Due to the close similarity of the pig to humans, especially the GI tract, the current study used pigs as an animal model. The results revealed that the number of enteric neurons immunoreactive to SOM (SOM-IR) in a physiological state clearly depend on the part of the GI tract studied. In turn, experimentally induced diabetes caused changes in the number of SOM-IR neurons. The least visible changes were observed in the stomach, where an increase in SOM-IR neurons was observed, only in the submucosal plexus in the corpus. However, diabetes led to an increase in the population of myenteric and submucosal neurons immunoreactive to SOM in all segments of the small intestine. The opposite situation occurred in the descending colon, where a decrease in the number of SOM-IR neurons was visible. This study underlines the significant role of SOM expressed in enteric nervous system neurons during diabetes.<\/jats:p>","DOI":"10.3390\/ani10010142","type":"journal-article","created":{"date-parts":[[2020,1,17]],"date-time":"2020-01-17T04:14:41Z","timestamp":1579234481000},"page":"142","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["The Influence of a Hyperglycemic Condition on the Population of Somatostatin Enteric Neurons in the Porcine Gastrointestinal Tract"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1402-5423","authenticated-orcid":false,"given":"Micha\u0142","family":"Bulc","sequence":"first","affiliation":[{"name":"Department of Clinical Physiology, Faculty of Veterinary Medicine, University of Warmia and Mazury, Oczapowskiego Str. 13, 10-719 Olsztyn, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7593-9552","authenticated-orcid":false,"given":"Katarzyna","family":"Palus","sequence":"additional","affiliation":[{"name":"Department of Clinical Physiology, Faculty of Veterinary Medicine, University of Warmia and Mazury, Oczapowskiego Str. 13, 10-719 Olsztyn, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jaros\u0142aw","family":"Ca\u0142ka","sequence":"additional","affiliation":[{"name":"Department of Clinical Physiology, Faculty of Veterinary Medicine, University of Warmia and Mazury, Oczapowskiego Str. 13, 10-719 Olsztyn, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2020,1,15]]},"reference":[{"key":"ref_1","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_2","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_3","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.autneu.2007.04.005","article-title":"Innervation of the gastrointestinal tract: Patterns of aging","volume":"136","author":"Philips","year":"2007","journal-title":"Auton. Neurosci."},{"key":"ref_4","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_5","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1440-1746.1990.tb01777.x","article-title":"The normal structure of gastrointestinal innervation","volume":"5","author":"Furness","year":"1990","journal-title":"J. Gastroenterol. Hepatol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1007\/s00418-009-0657-2","article-title":"Two submucosal nerve plexus in human intestines","volume":"133","author":"Brehmer","year":"2010","journal-title":"Histochem. Cell. Biol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1002\/cne.902360308","article-title":"Distribution of certain peptide-containing nerve fibres and endocrine cells in the gastrointestinal mucosa in five mammalian species","volume":"236","author":"Keast","year":"1985","journal-title":"J. Comp. Neurol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1093\/oxfordjournals.bmb.a071768","article-title":"Neuronal peptides in the intestine","volume":"38","author":"Costa","year":"1982","journal-title":"Br. Med. Bull."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/0166-2236(92)90029-8","article-title":"Roles of peptides in transmission in the enteric nervous system","volume":"15","author":"Furness","year":"1992","journal-title":"Trends Neurosci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1016\/j.yexmp.2010.01.011","article-title":"Changes in the somatostatin (SOM)-like immunoreactivity within nervous structures of the porcine descending colon under various pathological factors","volume":"88","author":"Gonkowski","year":"2010","journal-title":"Exp. Mol. Pathol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/0167-0115(83)90281-1","article-title":"Distribution and characterization of immunoreactive somatostatin in human gastrointestinal tract","volume":"7","author":"Penman","year":"1983","journal-title":"Regul. Pept."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/S0950-351X(05)80232-0","article-title":"Somatostatin: Physiology and clinical applications","volume":"8","author":"Shulkes","year":"1994","journal-title":"Baillieres Clin. Endocrinol. Metab."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/0304-3940(77)90021-0","article-title":"Evidence that some intrinsic neurons of the intestine contain somatostatin","volume":"6","author":"Costa","year":"1977","journal-title":"Neurosci. Lett."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1016\/0306-4522(80)90153-0","article-title":"An immunohistochemical study of the projections of somatostatin-containing neurons in the guinea-pig intestine","volume":"5","author":"Costa","year":"1980","journal-title":"Neuroscience"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"596","DOI":"10.1111\/j.1365-2982.2007.00931.x","article-title":"Effect of intestinal inflammation on the cell-specific expression of somatostatin receptor subtypes in the murine ileum","volume":"19","author":"Lantermann","year":"2007","journal-title":"Neurogastroenterol. Motil."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.yexmp.2010.11.004","article-title":"Axotomy induced changes in neuronal plasticity of sympathetic chain ganglia (SChG) neurons supplying descending colon in the pig","volume":"90","author":"Skobowiat","year":"2011","journal-title":"Exp. Mol. Pathol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"611","DOI":"10.1111\/nmo.12330","article-title":"Diabetic gastrointestinal motility disorders and the role of enteric nervous system: Current status and future directions","volume":"26","author":"Yarandi","year":"2014","journal-title":"Neurogastroenterol. Motil."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/j.cgh.2010.09.022","article-title":"Epidemiology, mechanisms, and management of diabetic gastroparesis","volume":"9","author":"Camilleri","year":"2011","journal-title":"Clin. Gastroenterol. Hepatol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3821","DOI":"10.3748\/wjg.v24.i34.3821","article-title":"Implication of neurohormonal-coupled mechanisms of gastric emptying and pancreatic secretory function in diabetic gastroparesis","volume":"24","author":"Mussa","year":"2018","journal-title":"World J. Gastroenterol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.jcpa.2007.09.003","article-title":"Distribution and chemical coding of intramural neurons in the porcine ileum during proliferative enteropathy","volume":"138","author":"Pidsudko","year":"2008","journal-title":"J. Comp. Pathol."},{"key":"ref_21","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\u2014The study on normal pigs and on animals suffering from swine dysentery","volume":"36","author":"Kaleczyc","year":"2007","journal-title":"Anat. Histol. Embryol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1016\/0006-8993(88)90478-7","article-title":"Effects of chronic experimental streptozotocin-induced diabetes on the noradrenergic and peptidergic innervation of the rat alimentary tract","volume":"458","author":"Schmidt","year":"1988","journal-title":"Brain Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1093\/ilar.47.4.358","article-title":"Preparation of swine for the laboratory","volume":"47","author":"Smith","year":"2006","journal-title":"ILAR J."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1159\/000200377","article-title":"Effect of diabetes in the BB Wistar rat on the peptidergic component of the enteric innervation","volume":"46","author":"Buchan","year":"1990","journal-title":"Digestion"},{"key":"ref_25","first-page":"11","article-title":"Comparative anatomy and physiology of the pig","volume":"25","author":"Swindle","year":"1998","journal-title":"Scand. J. Lab. Anim. Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"899","DOI":"10.1017\/S1751731110000200","article-title":"Porcine models for the metabolic syndrome, digestive and bone disorders: A general overview","volume":"4","author":"Corson","year":"2010","journal-title":"Animal"},{"key":"ref_27","first-page":"303","article-title":"Cholinergic, somatostatin-immunoreactive interneurons in the guinea pig intestine: Morphology, ultrastructure, connections and projections","volume":"187","author":"Portbury","year":"1995","journal-title":"J. Anat."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"6088","DOI":"10.3748\/wjg.v23.i33.6088","article-title":"Changes in expression of inhibitory substances in the intramural neurons of the stomach following streptozotocin- induced diabetes in the pig","volume":"23","author":"Bulc","year":"2017","journal-title":"World J. Gastroenterol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2018\/4735659","article-title":"Changes in Immunoreactivity of Sensory Substances within the Enteric Nervous System of the Porcine Stomach during Experimentally Induced Diabetes","volume":"2018","author":"Bulc","year":"2018","journal-title":"J. Diabetes Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"858","DOI":"10.1002\/ar.21365","article-title":"Calretinin and somatostatin immunoreactivities label different human submucosal neuron populations","volume":"294","author":"Kustermann","year":"2011","journal-title":"Anat. Rec."},{"key":"ref_31","first-page":"51","article-title":"An immunohistochemical study of the myenteric plexus of the colon in the rat and mouse","volume":"170","author":"Heinicke","year":"1990","journal-title":"J. Anat."},{"key":"ref_32","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_33","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/j.regpep.2006.11.024","article-title":"Survival and neurotransmitter plasticity in cultured rat colonic myenteric neurons","volume":"140","author":"Kristensson","year":"2007","journal-title":"Regul. Pept."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1002\/cne.903530202","article-title":"Neurochemical coding of enteric neurons in the guinea pig stomach","volume":"353","author":"Schemann","year":"1995","journal-title":"J. Comp. Neurol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1139\/y01-075","article-title":"The innervation of the human antro-pyloric region: Organization and composition","volume":"79","author":"Smith","year":"2001","journal-title":"Can. J. Physiol. Pharmacol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1007\/s11894-010-0129-9","article-title":"Enteric Nervous System in the Small Intestine: Pathophysiology and Clinical Implications","volume":"12","author":"Nezami","year":"2010","journal-title":"Curr. Gastroenterol. Rep."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"951","DOI":"10.1111\/j.1365-2982.2007.01023.x","article-title":"Diabetes and the enteric nervous system","volume":"19","author":"Chandrasekharan","year":"2007","journal-title":"Neurogastroenterol. Motil."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e13439","DOI":"10.1111\/nmo.13439","article-title":"Chemically induced inflammation and nerve damage aect the distribution of vasoactive intestinal polypeptide-like immunoreactive (VIP-LI) nervous structures in the descending colon of the domestic pig","volume":"30","author":"Makowska","year":"2018","journal-title":"Neurogastroenterol. Motil."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"9037476","DOI":"10.1155\/2017\/9037476","article-title":"Changes in somatostatin-like immunoreactivity in the sympathetic neurons projecting to the prepyloric area of the porcine stomach induced by selected pathological conditions","volume":"2017","author":"Palus","year":"2017","journal-title":"BioMed Res. Int."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1016\/0026-0495(78)90092-6","article-title":"Some thoughts on current research with somatostatin","volume":"27","author":"Guillemin","year":"1978","journal-title":"Metabolism"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/0014-2999(79)90434-5","article-title":"Actions of somatostatin on excitatory and inhibitory nerves in the intestine","volume":"56","author":"Furness","year":"1979","journal-title":"Eur. J. Pharmacol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1653","DOI":"10.1210\/endo-99-6-1653","article-title":"Somatostatin inhibits the release of acetylcholine induced electrically in the myenteric plexus","volume":"99","author":"Guillemin","year":"1976","journal-title":"Endocrinology"},{"key":"ref_43","first-page":"277","article-title":"Effects of somatostatin on intestinal circulation and oxygen consumption","volume":"74","author":"Pawlik","year":"1989","journal-title":"Acta Physiol. Hung."},{"key":"ref_44","first-page":"161","article-title":"Somatostatin and somatostatin receptors in the immune system: A review","volume":"11","author":"Hofland","year":"2000","journal-title":"Eur. Cytokine Netw."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/B978-0-444-53480-4.00006-0","article-title":"Diabetic autonomic neuropathy","volume":"126","author":"Freeman","year":"2014","journal-title":"Handb. Clin. Neurol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"481","DOI":"10.3109\/00365527809181925","article-title":"Eects of short-time somatostatin infusion on the gastric and intestinal propulsion in humans","volume":"13","author":"Johansson","year":"1978","journal-title":"Scand. J. Gastroenterol."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/10\/1\/142\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T14:26:31Z","timestamp":1760365591000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/10\/1\/142"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,1,15]]},"references-count":46,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2020,1]]}},"alternative-id":["ani10010142"],"URL":"https:\/\/doi.org\/10.3390\/ani10010142","relation":{},"ISSN":["2076-2615"],"issn-type":[{"type":"electronic","value":"2076-2615"}],"subject":[],"published":{"date-parts":[[2020,1,15]]}}}