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Published in: Gut Pathogens 1/2017

Open Access 01-12-2017 | Research

Modulation of the main porcine enteric neuropeptides by a single low-dose of lipopolysaccharide (LPS) Salmonella Enteritidis

Authors: Anita Mikołajczyk, Sławomir Gonkowski, Dagmara Złotkowska

Published in: Gut Pathogens | Issue 1/2017

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Abstract

Background

The present research was conducted to investigate the influence of a low, single dose of LPS, which does not result in any clinical symptoms of intoxication on the expression of selected neuropeptides within the intestines of the domestic pig.

Methods

This experiment was conducted on immature female pigs of the Pitrain × Duroc breed (n = five per group). Seven days after the intravenous injection of 10 mL saline solution for control animals and 5 μg/kg b.w. (in 10 mL saline solution) LPS Salmonella Enteritidis for the experimental group, the excised segments of duodenum, jejunum, ileum, ileocecal valve, caecum, descending colon, transverse colon, ascending colon and rectum were prepared to extract the main enteric neuropeptides, including GAL, NPY, SOM, SP, VIP.

Results

The results of this research indicate that single low-dose LPS S. Enteritidis produced changes in the content of the selected neuropeptides of the porcine intestine. The most visible changes were observed in the transverse colon, where LPS induced the increase of GAL expression from 19.41 ± 7.121 to 92.92 ± 11.447 ng/g tissue.

Conclusion

The exact functions of the substances studied and mechanisms of responses to LPS action depend on the sections of the intestines. The mechanisms of observed changes are not fully understood, but fluctuations in neuronal active substance levels may be connected with neurodegenerative and/or pro-inflammatory activity of LPS.
Literature
11.
go back to reference Mohammadi Z. Endotoxin in endodontic infections: a review. J Calif Dent Assoc. 2011;39(3):153–61. Mohammadi Z. Endotoxin in endodontic infections: a review. J Calif Dent Assoc. 2011;39(3):153–61.
13.
go back to reference Mohammadi B, Schedel I, Graf K, Teiwes A, Heckeret H, et al. Role of endotoxin in the pathogenesis of critical illness polyneuropathy. J Neurol. 2008;255(2):265–72.CrossRefPubMed Mohammadi B, Schedel I, Graf K, Teiwes A, Heckeret H, et al. Role of endotoxin in the pathogenesis of critical illness polyneuropathy. J Neurol. 2008;255(2):265–72.CrossRefPubMed
14.
go back to reference Niehaus I. In vivo Radiodetoxification of Salmonella minnesota Lipopolysaccharides with radio-labeled leucine enkephalin cures sensory polyneuropathy: a Case report. TNHJ. 2010;10(1–2):26–33. Niehaus I. In vivo Radiodetoxification of Salmonella minnesota Lipopolysaccharides with radio-labeled leucine enkephalin cures sensory polyneuropathy: a Case report. TNHJ. 2010;10(1–2):26–33.
15.
go back to reference Webel DM, Finck BN, Baker DH, Johnson RW. Time course of increased plasma cytokines, cortisol, and urea nitrogen in pigs following intraperitoneal injection of lipopolysaccharide. J Anim Sci. 1997;75:1514–20.CrossRefPubMed Webel DM, Finck BN, Baker DH, Johnson RW. Time course of increased plasma cytokines, cortisol, and urea nitrogen in pigs following intraperitoneal injection of lipopolysaccharide. J Anim Sci. 1997;75:1514–20.CrossRefPubMed
19.
go back to reference Fox-Threlkeld JA, McDonald TJ, Cipris S, Woskowska Z, Daniel EE. Galanin inhibition of vasoactive intestinal polypeptide release and circular muscle motility in the isolated perfused canine ileum. Gastroenterology. 1991;101:1471–6.CrossRefPubMed Fox-Threlkeld JA, McDonald TJ, Cipris S, Woskowska Z, Daniel EE. Galanin inhibition of vasoactive intestinal polypeptide release and circular muscle motility in the isolated perfused canine ileum. Gastroenterology. 1991;101:1471–6.CrossRefPubMed
21.
go back to reference Sarnelli G, Vanden Berghe P, Raeymaekers P, Janssens J, Tack J. Inhibitory effects of galanin on evoked (Ca2+) responses in cultured myenteric neurons. Am J Physiol Gastrointest Liver Physiol. 2004;286:1009–14.CrossRef Sarnelli G, Vanden Berghe P, Raeymaekers P, Janssens J, Tack J. Inhibitory effects of galanin on evoked (Ca2+) responses in cultured myenteric neurons. Am J Physiol Gastrointest Liver Physiol. 2004;286:1009–14.CrossRef
22.
go back to reference Botella A, Delvaux M, Frexinos J, Bueno L. Comparative effects of galanin on isolated smooth muscle cells from ileum in five mammalian species. Life Sci. 1992;50:1253–61.CrossRefPubMed Botella A, Delvaux M, Frexinos J, Bueno L. Comparative effects of galanin on isolated smooth muscle cells from ileum in five mammalian species. Life Sci. 1992;50:1253–61.CrossRefPubMed
23.
go back to reference Shimizu Y, Matsuyama H, Shiina T, Takewaki T, Furness JB. Tachykinins and their functions in the gastrointestinal tract. Cell Mol Life Sci. 2008;65:295–311.CrossRefPubMed Shimizu Y, Matsuyama H, Shiina T, Takewaki T, Furness JB. Tachykinins and their functions in the gastrointestinal tract. Cell Mol Life Sci. 2008;65:295–311.CrossRefPubMed
25.
go back to reference Low MJ. The somatostatin neuroendocrine system: physiology and clinical relevance in gastrointestinal and pancreatic disorders. Best Pract Res Clin Endocrinol Metab. 2004;18:607–22.CrossRefPubMed Low MJ. The somatostatin neuroendocrine system: physiology and clinical relevance in gastrointestinal and pancreatic disorders. Best Pract Res Clin Endocrinol Metab. 2004;18:607–22.CrossRefPubMed
27.
go back to reference Kasparek MS, Fatima J, Iqbal CW, Duenes JA, Sarr MG. Role of VIP and substance P in NANC innervation in the longitudinal smooth muscle of the rat jejunum influence of extrinsic denervation. J Surg Res. 2007;141:22–30.CrossRefPubMed Kasparek MS, Fatima J, Iqbal CW, Duenes JA, Sarr MG. Role of VIP and substance P in NANC innervation in the longitudinal smooth muscle of the rat jejunum influence of extrinsic denervation. J Surg Res. 2007;141:22–30.CrossRefPubMed
28.
go back to reference Lamers CB. Clinical and pathophysiological aspects of somatostatin and the gastrointestinal tract. Acta Endocrinol Suppl (Copenh). 1987;286:19–25. Lamers CB. Clinical and pathophysiological aspects of somatostatin and the gastrointestinal tract. Acta Endocrinol Suppl (Copenh). 1987;286:19–25.
29.
32.
go back to reference Maes M, Kubera M, Leunis JC. The gut-brain barrier in major depression: intestinal mucosal dysfunction with an increased translocation of LPS from gram negative enterobacteria (leaky gut) plays a role in the inflammatory pathophysiology of depression. Neuro Endocrinol Lett. 2008;29(1):117–24.PubMed Maes M, Kubera M, Leunis JC. The gut-brain barrier in major depression: intestinal mucosal dysfunction with an increased translocation of LPS from gram negative enterobacteria (leaky gut) plays a role in the inflammatory pathophysiology of depression. Neuro Endocrinol Lett. 2008;29(1):117–24.PubMed
33.
go back to reference Giancola F, Torresan F, Repossi R, Bianco F, Latorre R, Ioannou A, Guarino M, Volta U, Clavenzani P, Mazzoni M, Chiocchetti R, Bazzoli F, Travagli RA, Sternini C, De Giorgio R. Downregulation of neuronal vasoactive intestinal polypeptide in Parkinson’s disease and chronic constipation. Neurogastroenterol Motil. 2016;29(5):1–9. https://doi.org/10.1111/nmo.12995. Giancola F, Torresan F, Repossi R, Bianco F, Latorre R, Ioannou A, Guarino M, Volta U, Clavenzani P, Mazzoni M, Chiocchetti R, Bazzoli F, Travagli RA, Sternini C, De Giorgio R. Downregulation of neuronal vasoactive intestinal polypeptide in Parkinson’s disease and chronic constipation. Neurogastroenterol Motil. 2016;29(5):1–9. https://​doi.​org/​10.​1111/​nmo.​12995.
41.
go back to reference Mikołajczyk A, Makowska K. Cocaine- and amphetamine-regulated transcript peptide (CART) in the nerve fibers of the porcine gallbladder wall under physiological conditions and after Salmonella Enteritidis lipopolysaccharides administration. Folia Morphol (Warsz). 2017. https://doi.org/10.5603/fm.a2017.0036. Mikołajczyk A, Makowska K. Cocaine- and amphetamine-regulated transcript peptide (CART) in the nerve fibers of the porcine gallbladder wall under physiological conditions and after Salmonella Enteritidis lipopolysaccharides administration. Folia Morphol (Warsz). 2017. https://​doi.​org/​10.​5603/​fm.​a2017.​0036.
42.
go back to reference Makowska K, Mikolajczyk A, Calka J, Gonkowski S. Neurochemical characterization of nerve fibers in the porcine gallbladder wall under physiological conditions and after the administration of Salmonella Enteritidis lipopolysaccharides (LPS). Toxicol Res. 2017. https://doi.org/10.1039/c7tx00211d. Makowska K, Mikolajczyk A, Calka J, Gonkowski S. Neurochemical characterization of nerve fibers in the porcine gallbladder wall under physiological conditions and after the administration of Salmonella Enteritidis lipopolysaccharides (LPS). Toxicol Res. 2017. https://​doi.​org/​10.​1039/​c7tx00211d.
45.
go back to reference Chowers Y, Cahalon L, Lahav M. Somatostatin through its specific receptor inhibits spontaneous and TNF-alpha and bacteria-induced IL-8 and IL-1 beta secretion from intestinal epithelial cells. J Immunol. 2000;165(6):2955–61.CrossRefPubMed Chowers Y, Cahalon L, Lahav M. Somatostatin through its specific receptor inhibits spontaneous and TNF-alpha and bacteria-induced IL-8 and IL-1 beta secretion from intestinal epithelial cells. J Immunol. 2000;165(6):2955–61.CrossRefPubMed
46.
48.
go back to reference Ibrahim H, Barrow P, Foster N. VIP as a potential therapeutic agent in gram negative sepsis. Endocr Metab Immune Disord Drug Targets. 2012;12(4):308–15.CrossRefPubMed Ibrahim H, Barrow P, Foster N. VIP as a potential therapeutic agent in gram negative sepsis. Endocr Metab Immune Disord Drug Targets. 2012;12(4):308–15.CrossRefPubMed
53.
go back to reference ter Veld F, Rose B, Mussmann R, Martin S, Herder C, Kempf K. Effects of somatostatin and octreotide on cytokine and chemokine production by lipopolysaccharide-activated peripheral blood mononuclear cells. J Endocrinol Invest. 2009;32(2):123–9.CrossRefPubMed ter Veld F, Rose B, Mussmann R, Martin S, Herder C, Kempf K. Effects of somatostatin and octreotide on cytokine and chemokine production by lipopolysaccharide-activated peripheral blood mononuclear cells. J Endocrinol Invest. 2009;32(2):123–9.CrossRefPubMed
54.
go back to reference Sergeyev V, Broberger C, Hökfelt T. Effect of LPS administration on the expression of POMC, NPY, galanin, CART and MCH mRNAs in the rat hypothalamus. Brain Res Mol Brain Res. 2001;90(2):93–100.CrossRefPubMed Sergeyev V, Broberger C, Hökfelt T. Effect of LPS administration on the expression of POMC, NPY, galanin, CART and MCH mRNAs in the rat hypothalamus. Brain Res Mol Brain Res. 2001;90(2):93–100.CrossRefPubMed
55.
go back to reference Lyudyno VI, Krasnova IN, Smirnova MP, Klimenko VM. Antipyretic effect of neuropeptide galanin in endotoxin-induced fever. Bull Exp Biol Med. 2001;131(1):60–3.CrossRefPubMed Lyudyno VI, Krasnova IN, Smirnova MP, Klimenko VM. Antipyretic effect of neuropeptide galanin in endotoxin-induced fever. Bull Exp Biol Med. 2001;131(1):60–3.CrossRefPubMed
59.
go back to reference Hauser GJ, Dayao EK, Zukowska-Grojec Z. Effect of neuropeptide Y on endotoxin-induced suppression of the response to various agonists in conscious rats. Life Sci. 1995;57(3):235–44.CrossRefPubMed Hauser GJ, Dayao EK, Zukowska-Grojec Z. Effect of neuropeptide Y on endotoxin-induced suppression of the response to various agonists in conscious rats. Life Sci. 1995;57(3):235–44.CrossRefPubMed
63.
go back to reference Meneses G, Bautista M, Florentino A, Díaz G, Acero G, Besedovsky H, Meneses D, Fleury A, Del Rey A, Gevorkian G, Fragoso G, Sciutto E. Electric stimulation of the vagus nerve reduced mouse neuroinflammation induced by lipopolysaccharide. J Inflamm. 2016;13(33):1–11. https://doi.org/10.1186/s12950-016-0140-5. Meneses G, Bautista M, Florentino A, Díaz G, Acero G, Besedovsky H, Meneses D, Fleury A, Del Rey A, Gevorkian G, Fragoso G, Sciutto E. Electric stimulation of the vagus nerve reduced mouse neuroinflammation induced by lipopolysaccharide. J Inflamm. 2016;13(33):1–11. https://​doi.​org/​10.​1186/​s12950-016-0140-5.
65.
go back to reference Garcia-Oscos F, Peña D, Housini M, Cheng D, Lopez D, Cuevas-Olguin R, Saderi N, Salgado Delgado R, Galindo Charles L, Salgado Burgos H, Rose-John S, Flores G, Kilgard MP, Atzori M. Activation of the anti-inflammatory reflex blocks lipopolysaccharide-induced decrease in synaptic inhibition in the temporal cortex of the rat. J Neurosci Res. 2015;93:859–65. https://doi.org/10.1002/jnr.23550.CrossRefPubMed Garcia-Oscos F, Peña D, Housini M, Cheng D, Lopez D, Cuevas-Olguin R, Saderi N, Salgado Delgado R, Galindo Charles L, Salgado Burgos H, Rose-John S, Flores G, Kilgard MP, Atzori M. Activation of the anti-inflammatory reflex blocks lipopolysaccharide-induced decrease in synaptic inhibition in the temporal cortex of the rat. J Neurosci Res. 2015;93:859–65. https://​doi.​org/​10.​1002/​jnr.​23550.CrossRefPubMed
66.
go back to reference Mikołajczyk A. Safe and effective anaesthesiological protocols in domestic pigs. Ann Warsaw Univ Life Sci SGGW Anim Sci. 2016;55(2):219–27. Mikołajczyk A. Safe and effective anaesthesiological protocols in domestic pigs. Ann Warsaw Univ Life Sci SGGW Anim Sci. 2016;55(2):219–27.
67.
go back to reference Llamas-Moya S, Boyle L, Arkins S, Lynch PB. Effects of husbandry and low-dose lipopolysaccharide challenge on the acute phase response of young pigs. End of Project Report no 5231, Teagsac. 2006; p. 1–38. http://hdl.handle.net/11019/982. Llamas-Moya S, Boyle L, Arkins S, Lynch PB. Effects of husbandry and low-dose lipopolysaccharide challenge on the acute phase response of young pigs. End of Project Report no 5231, Teagsac. 2006; p. 1–38. http://​hdl.​handle.​net/​11019/​982.
Metadata
Title
Modulation of the main porcine enteric neuropeptides by a single low-dose of lipopolysaccharide (LPS) Salmonella Enteritidis
Authors
Anita Mikołajczyk
Sławomir Gonkowski
Dagmara Złotkowska
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2017
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-017-0225-6

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