Effect of Chemically-Induced Diabetes Mellitus on Phenotypic Variability of the Enteric Neurons in the Descending Colon in the Pig

Arciszewski M. B., Ekblad E. (2005). Effects of vasoactive intestinal peptide and galanin on survival of cultured porcine myenteric neurons. Regul. Pept., 125: 185–192.10.1016/j.regpep.2004.08.036Search in Google Scholar

Barada K. A., Saadé N. E., Atweh S. F., Khoury C. I., Nassar C. F. (2000). Calcitonin generelated peptide regulates amino acid absorption across rat jejunum. Regul. Pept., 90: 39–45.10.1016/S0167-0115(00)00103-8Search in Google Scholar

Barbiers M., Timmermans J. P., Scheuermann D. W., Adriaensen D., Mayer B., De Groodt Lasseel M. H. A. (1994). Nitric oxide synthase-containing neurons in the pig large intestine: Topography, morphology, and viscerofugal projections. Microsc. Res. Tech., 29: 72–78.10.1002/jemt.1070290203Search in Google Scholar

Belai A., Burnstock G. (1990). Changes in adrenergic and peptidergic nerves in the submucous plexus of streptozocin-diabetic rat ileum. Gastroenterology, 98: 1427–1436.10.1016/0016-5085(90)91072-ESearch in Google Scholar

Belai A., Lincoln J., Milner P., Crowe R., Loesch A., Burnstock G. (1985). Enteric nerves in diabetic rats: increase in vasoactive intestinal polypeptide but not substance P. Gastroenterology, 89: 967–976.10.1016/0016-5085(85)90195-7Search in Google Scholar

Belai A., Calcutt N. A., Carrington A. L., Diemel L. T., Tomlinson D. R., Burnstock G. (1996). Enteric neuropeptides in streptozotocindiabetic rats; effects of insulin and aldose reductase inhibition. Auton. Nerv. Syst., 58: 163–169.10.1016/0165-1838(95)00129-8Search in Google Scholar

Botella A., Delvaux M., Frexinos J., Bueno L. (1992). Comparative effects of galanin on isolated smooth muscle cells from ileum in five mammalian species. Life. Sci., 50: 1253–1261.10.1016/0024-3205(92)90325-JSearch in Google Scholar

Brehmer A., Schrodl F., Neuhuber W. (2006). Morphology of VIP/nNOS-immunoreactive myenteric neurons in the human gut. Histochem. Cell. Biol., 125: 557–565.10.1007/s00418-005-0107-8Search in Google Scholar

Brehmer A., Rupprecht H., Neuhuber W. (2010). Two submucosal nerve plexus in human intestines. Histochem. Cell. Biol. 133: 149–161.10.1007/s00418-009-0657-2Search in Google Scholar

Brenneman D. E., Hill J. M., Glazner G. W., Gozes I., Philips T. M. (1995). Interleukin-1α and vasoactive intestinal peptide: enigmatic regulation of neuronal survival. Int. J. Dev. Neurosci., 13: 187–200.10.1016/0736-5748(95)00014-8Search in Google Scholar

Brenneman D. E., Philips T. M., Hauser J., Hill J. M., Spong C., Gozes I. (2003). Complex array of cytokines released by vasoactive intestinal peptide. Neuropeptides, 37: 111–119.10.1016/S0143-4179(03)00022-2Search in Google Scholar

Bulc M., Gonkowski S., Całka J. (2015). Expression of cocaine and amphetamine regulated transcript (CART) in the porcine intramural neurons of stomach in the course of experimentally induced diabetes mellitus. J. Mol. Neurosci., 57: 376–385.10.1007/s12031-015-0618-2Search in Google Scholar

Bulc M., Palus K., Zielonka L., Gajecka M., Całka J. (2017), Changes in expression of inhibitory substances in the intramural neurons of the stomach following streptozotocin- induced diabetes in the pig. World. J. Gastroenterol., 23: 6088–6099.10.3748/wjg.v23.i33.6088559750028970724Search in Google Scholar

Bulc M., Palus K., Całka J., Zielonka L. (2018). Changes in immunoreactivity of sensory substances within the enteric nervous system of the porcine stomach during experimentally induced diabetes. J. Diabetes. Res., 2018: 1–18.10.1155/2018/4735659Search in Google Scholar

Bulc M., Palus K., Dąbrowski M., Całka J. (2019). Hyperglycaemia-induced downregulation in expression of nNOS intramural neurons of the small intestine in the pig. Int. J. Mol. Sci., 20: 1681.10.3390/ijms20071681Search in Google Scholar

Burleigh D. E., Banks M. R. (2007). Stimulation of intestinal secretion by vasoactive intestinal peptide and cholera toxin. Auton. Neurosci. Bas. Clin., 133: 64–75.10.1016/j.autneu.2006.08.004Search in Google Scholar

Chandrasekharan B., Srinivasan S. (2007). Diabetes and the enteric nervous system. Neurogastroenterol. Motil., 19: 951–960.10.1111/j.1365-2982.2007.01023.xSearch in Google Scholar

Clerc N., Furness J. B. (2004). Intrinsic primary afferent neurones of the digestive tract. Neurogastroenterol. Motil., 16: 24–27.10.1111/j.1743-3150.2004.00470.xSearch in Google Scholar

Costa M., Furness J. B. (1982). Neuronal peptides in the intestine. Br. Med. Bull., 38: 247–252.10.1093/oxfordjournals.bmb.a071768Search in Google Scholar

Demedts I., Masaoka T., Kindt S., De Hertogh G., Geboes K., Farré R., Vanden Berghe P., Tack J. (2013). Gastrointestinal motility changes and myenteric plexus alterations in spontaneously diabetic biobreeding rats. J. Neurogastroenterol. Motil., 19: 161–170.10.5056/jnm.2013.19.2.161Search in Google Scholar

Ekblad E. (2006). CART in the enteric nervous system. Peptides, 27: 2024–2030.10.1016/j.peptides.2005.12.015Search in Google Scholar

Ekblad E., Kuhar M., Wierup N., Sundler F. (2003). Cocaine- and amphetamine-regulated transcript: distribution and function in rat gastrointestinal tract. Neurogastroenterol. Motil., 15: 545–557.10.1046/j.1365-2982.2003.00437.xSearch in Google Scholar

Ellis L. M., Mawe G.M., (2003). Distribution and chemical coding of cocaine- and amphetamineregulated transcript peptide (CART)-immunoreactive neurons in the guinea pig bowel. Cell. Tissue. Res., 312: 265–274.10.1007/s00441-002-0678-9Search in Google Scholar

Evangelista S., Tramontana M. (1993). Involvement of calcitonin gene-related peptide in rat experimental colitis. J. Physiol., 87: 277–280.10.1016/0928-4257(93)90017-NSearch in Google Scholar

Feher E., Batbayar B., Ver A. (2006). Changes of the different neuropeptide-containing nerve fibres and immune cells in the diabetic rat’s alimentary tract. Ann. N.Y. Acad. Sci., 1084: 280–295.10.1196/annals.1372.023Search in Google Scholar

Foxt-Threlkeld J. E. T., Mc Donald T. J., Cipris S., Woskowska Z., Daniel E. E. (1991). Galanin inhibition of vasoactive intestinal polypeptide release and circular muscle motility in the isolated perfused canine ileum. Gastroenterology, 101: 1471–1476.10.1016/0016-5085(91)90381-TSearch in Google Scholar

Furness J. B. (2000). Types of neurons in the enteric nervous system. J. Auton. Nerv. Syst., 81: 87–96.10.1016/S0165-1838(00)00127-2Search in Google Scholar

Furness J. B. (2006). The organisation of the autonomic nervous system: peripheral connections. Auton. Neurosci., 130: 1–5.10.1016/j.autneu.2006.05.003Search in Google Scholar

Furness J. B. (2012). The enteric nervous system and neurogastroenterology. Nat. Rev. Gastroent. Hepatol., 5: 286–294.10.1038/nrgastro.2012.32Search in Google Scholar

Furness J. B., Callaghan B. P., Rivera L. R., Cho H. J. (2014). The enteric nervous system and gastrointestinal innervation: Integrated local and central control. Adv. Exp. Med. Biol., 817: 39–71.10.1007/978-1-4939-0897-4_3Search in Google Scholar

Gatopoulou A. N., Papanas E., Maltezos A. (2012). Diabetic gastrointestinal autonomic neuropathy: current status and new achievements for everyday clinical practice. Eur. J. Intern. Med., 6: 499–505.10.1016/j.ejim.2012.03.001Search in Google Scholar

Gonkowski S., Rytel L. (2019). Somatostatin as an active substance in the mammalian enteric nervous system. Int. J. Mol. Sci., 20: 4461.10.3390/ijms20184461Search in Google Scholar

Gonkowski S., Burliński P., Skobowiat C., Majewski M., Arciszewski M. B., Radziszewski P., Całka J. (2009). Distribution of cocaine- and amphetamine-regulated transcript-like immunoreactive (CART-LI) nerve structures in the porcine large intestine. Acta. Vet. Hung., 4: 509–520.10.1556/avet.57.2009.4.5Search in Google Scholar

Gonkowski S., Burliński P., Skobowiat C., Majewski M., Całka J. (2010). Inflammation-and axotomy-induced changes in galanin-like immunoreactive (GAL-LI) nerve structures in the porcine descending colon. Acta. Vet. Hung., 58: 91–103.10.1556/avet.58.2010.1.10Search in Google Scholar

Greenwood-Van Meerveld B., Johnson A. C., Grundy D. (2017). Gastrointestinal physiology and function. Handb. Exp. Pharmacol., 239: 1–16.10.1007/164_2016_118Search in Google Scholar

Grüssner R., Nakhleh R., Grüssner A., Tomadze G., Diem P., Sutherland D. (1993). Streptozotocin-induced diabetes mellitus in pigs. Horm. Metab. Res., 25: 199–203.10.1055/s-2007-1002076Search in Google Scholar

Jaworski J. N., Jones D. C. (2006). The role of CART in the reward/reinforcing properties of psychostimulants. Peptides, 27: 1993–2004.10.1016/j.peptides.2006.03.034Search in Google Scholar

Juranek J. K., Aleshin A., Rattigan E. M. (2010). Morphological changes and immunohistochemical expression of RAGE and its ligands in the sciatic nerve of hyperglycemic pig (Sus scrofa). Biochem. Insights., 2010: 47–59.10.4137/BCI.S5340Search in Google Scholar

Kaiser E. A., Rea B. J., Kuburas A., Kovacevich B. R., Garcia-Martinez L. F., Recober A., Russo A. F. (2017). Anti-CGRP antibodies block CGRP-induced diarrhea in mice. Neuropeptides, 64: 95–99.10.1016/j.npep.2016.11.004Search in Google Scholar

Kaleczyc J., Klimczuk M., Franke-Radowiecka A., Sienkiewicz W., Majewski M., Łakomy M. (2007). The distribution and chemical coding of intramural neurons supplying the porcine stomach – the study on normal pigs and on animals suffering from swine dysentery. Anat. Histol. Embryol., 36: 186–193.10.1111/j.1439-0264.2006.00744.xSearch in Google Scholar

Keast J. R., Furness J. B., Costa M. (1985). Distribution of certain peptide-containing nerve fibres and endocrine cells in the gastrointestinal mucosa in five mammalian species. J. Comp. Neurol., 236: 403–422.10.1002/cne.902360308Search in Google Scholar

Lambrecht N., Burchert M., Respondek M., Müller K. M., Peskar B. M. (1993). Role of calcitonin gene-related peptide and nitric oxide in the gastroprotective effect of capsaicin in the rat. Gastroenterology, 104: 1371–1380.10.1016/0016-5085(93)90345-DSearch in Google Scholar

Li F. J., Zou Y. Y., Cui Y., Yin Y., Guo G., Lu F. G. (2013). Calcitonin gene-related peptide is a promising marker in ulcerative colitis. Dig. Dis. Sci., 58: 686–693.10.1007/s10620-012-2406-ySearch in Google Scholar

Makowska K. (2018). Chemically induced inflammation and nerve damage affect the distribution of vasoactive intestinal polypeptide-like immunoreactive (VIP-LI) nervous structures in the descending colon of the domestic pig. Neurogastroenterol. Motil., 30: 13439.10.1111/nmo.13439Search in Google Scholar

Makowska K., 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: 548.10.3390/ijms19020548Search in Google Scholar

Makowska K., 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: 1024.10.3390/ijms20051024Search in Google Scholar

Makowska K., Gonkowski S., Zielonka L., Dabrowski M., Calka J. (2017). T2 toxininduced changes in cocaine- and amphetamine-regulated transcript (CART)-like immunoreactivity in the enteric nervous system within selected fragments of the porcine digestive tract. Neurotox. Res., 31: 136–147.10.1007/s12640-016-9675-8Search in Google Scholar

Nassar C. F., Abdallah L. E., Barada K. A., Atweh S. F., Saadé N. F. (1995). Effects of intravenous vasoactive intestinal peptide injection on jejunal alanine absorption and gastric acid secretion in rats. Regul. Pept., 55: 261–267.10.1016/0167-0115(94)00114-DSearch in Google Scholar

Nuki C., Kawasaki H., Kitamura K., Takenaga M., Kangawa K., Eto T. (1993). Vasodilator effect of adrenomedullin and calcitonin gene-related peptide receptors in rat mesenteric vascular beds. Biochem. Biophys. Res. Commun., 196: 245–251.10.1006/bbrc.1993.2241Search in Google Scholar

Ohno T., Hattori Y., Komine R., Ae T., Mizuguchi S., Arai K., Saeki T., Suzuki T., Hosono K., Hayashi I. (2008). Roles of calcitonin gene-related peptide in maintenance of gastric mucosal integrity and in enhancement of ulcer healing and angiogenesis. Gastroenterology, 134: 215–225.10.1053/j.gastro.2007.10.001Search in Google Scholar

Palus K., Bulc M., Całka J. (2018 a). Changes in VIP-, SP- and CGRP- like immunoreactivity in intramural neurons within the pig stomach following supplementation with low and high doses of acrylamide. Neurotoxicology, 69: 47–59.10.1016/j.neuro.2018.09.00230222996Search in Google Scholar

Palus K., Makowska K., Całka J. (2018 b). Acrylamide-induced alterations in the cocaine- and amphetamine-regulated peptide transcript (CART)-like immunoreactivity within the enteric nervous system of the porcine small intestines. Ann. Anat., 219: 94–101.10.1016/j.aanat.2018.06.00229944933Search in Google Scholar

Palus K., Makowska K., Całka J. (2019). Alterations in galanin-like immunoreactivity in the enteric nervous system of the porcine stomach following acrylamide supplementation. Int. J. Mol. Sci., 20: 3345.10.3390/ijms20133345Search in Google Scholar

Philips R. J., Powley T. L. (2007). Innervation of the gastrointestinal tract: Patterns of aging. Auton. Neurosci., 136: 1–19.10.1016/j.autneu.2007.04.005Search in Google Scholar

Rees D. A., Alcolado J. C. (2005). Animal models of diabetes mellitus. Diabet. Med., 22: 359–370.10.1111/j.1464-5491.2005.01499.xSearch in Google Scholar

Sanders K. M., Ward S. M. (1992). Nitric oxide as a mediator of nonadrenergic, noncholinergic neurotransmission. Am. J. Physiol., 262: G379–G392.10.1152/ajpgi.1992.262.3.G379Search in Google Scholar

Schleiffer R., Raul F. (1997). Nitric oxide and the digestive system in mammals and nonmammalian vertebrates. Comp. Biochem. Physiol., 118A: 965–974.10.1016/S0300-9629(97)00026-1Search in Google Scholar

Shah V., Lyford G., Gores G., Farrugia G. (2004). Nitric oxide in gastrointestinal health and disease. Gastroenterology, 126: 903–913.10.1053/j.gastro.2003.11.046Search in Google Scholar

Skobowiat C., Calka J., Majewski M. (2011). Axotomy induced changes in neuronal plasticity of sympathetic chain ganglia (SChG) neurons supplying descending colon in the pig. Exp. Mol. Pathol., 90: 13–18.10.1016/j.yexmp.2010.11.004Search in Google Scholar

Swindle M. M. (2012). The development of swine models in drug discovery and development. Future. Med. Chem., 4: 1771–1772.10.4155/fmc.12.113Search in Google Scholar

Swindle M. M., Smith A. C. (1998). Comparative anatomy and physiology of the pig. Scand. J. Lab. Anim. Sci., 25: 11–21.Search in Google Scholar

Szymanska K., Calka J., Gonkowski S. (2018). 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). Nitric. Oxide, 80: 1–11.10.1016/j.niox.2018.08.001Search in Google Scholar

Timmermans J. P., Scheuermann D. W., Stach W., Adriaensen D., de Groodt-Lesseal M. H. A. (1992 a). Functional morphology of the enteric nervous system with special reference to large mammals. Eur. J. Morphol., 30: 113–122.Search in Google Scholar

Timmermans J. P., Scheuermann D. W., Barbiers M., Adriaensen D., Stach W., Van Hee R., De Groodt-Lasseel M. H. A. (1992 b). Calcitonin gene-related peptide-like immunoreactivity in the human small intestine. Acta. Anat., 143: 48–53.10.1159/0001472271585788Search in Google Scholar

Vasina V., Barbara G., Talamonti L. (2006). Enteric neuroplasticity evoked by inflammation. Auton. Neurosci., 127: 264–272.10.1016/j.autneu.2006.02.025Search in Google Scholar

Vincent A. M., Russell J. W., Low P., Feldman E. L. (2004). Oxidative stress in the pathogenesis of diabetic neuropathy. Endocrin. Rev., 25: 612–628.10.1210/er.2003-0019Search in Google Scholar

Vinik A. I., Maser R. E., Mitchell B. D., Freeman R. (2003). Diabetic autonomic neuropathy Diabetes. Care, 5: 1553–1579.10.2337/diacare.26.5.1553Search in Google Scholar

Whittaker V. P. (1989). Vasoactive intestinal polypeptide (VIP) as a cholinergic co-transmitter: some recent results. Cell. Biol. Int. Rep., 13: 1039–1051.10.1016/0309-1651(89)90018-0Search in Google Scholar

Wolf M., Schrödl F., Neuhuber W., Brehmer A. (2007). Calcitonin gene-related peptide: A marker for putative primary afferent neurons in the pig small intestinal myenteric plexus? Anat. Rec., 290: 1273–1279.10.1002/ar.20577Search in Google Scholar

Yarandi S. S., Srinivasan S. (2014). Diabetic gastrointestinal motility disorders and the role of enteric nervous system: Current status and future directions. Neurogastroenterol. Motil., 26: 611–624.10.1111/nmo.12330Search in Google Scholar

Young H. M., Furness J. B., Shuttleworth C. W. R., Bredt D. S., Snyder S. H. (1992). Colocalization of nitric oxide synthase immunoreactivity and NADPH diaphorase staining in neurons of the guinea-pig intestine. Histochemistry, 97: 375–378.10.1007/BF00270041Search in Google Scholar