Enterocolic increase of cannabinoid receptor type 1 and type 2 and clinical improvement after probiotic administration in dogs with chronic signs of colonic dysmotility without mucosal inflammatory changes.
diarrhea
endocannabinoid system
enterocolitis
irritable bowel syndrome
probiotics
Journal
Neurogastroenterology and motility
ISSN: 1365-2982
Titre abrégé: Neurogastroenterol Motil
Pays: England
ID NLM: 9432572
Informations de publication
Date de publication:
01 2020
01 2020
Historique:
received:
19
03
2019
revised:
20
08
2019
accepted:
20
08
2019
pubmed:
10
9
2019
medline:
16
1
2021
entrez:
10
9
2019
Statut:
ppublish
Résumé
Colonic dysmotility in dogs can cause different GI signs. Sometimes, histology of enterocolic biopsies does not reveal inflammatory infiltrates or mucosal lesions that are typically associated with clinical disease activity. It is speculated that, similarly to humans, colonic dysmotility may be anxiety-based, although recent data demonstrate that irritable bowel syndrome (IBS) could result from acute infectious enteritis. Specific Lactobacillus spp. strains administered orally in humans induced the expression of μ-opioid and cannabinoid receptors in mucosal enterocytes, modulating intestinal morphine-like analgesic functions. We investigated the potential association of GI signs caused by colonic dysmotility and mucosal expression of cannabinoid receptors in intestinal epithelial cells and the number of mucosal mast cells. Ten to 15 endoscopic biopsies were collected from colonic mucosa of 20 dogs diagnosed with dysmotility disturbances before and after probiotic (Slab51 bacterial blend; Sivoy Decreased numbers of MCs (P < .0001) and increased CB1- and CB2-positive epithelial cells (P < .0001) in diseased dogs were positively associated with post-treatment CCECAI scores (P < .0001). Our results suggest that probiotic administration can reduce signs of colonic dysmotility, possibly due to microbiota modulation and epithelial cell receptor-mediated signaling in intestinal mucosa.
Sections du résumé
BACKGROUND
Colonic dysmotility in dogs can cause different GI signs. Sometimes, histology of enterocolic biopsies does not reveal inflammatory infiltrates or mucosal lesions that are typically associated with clinical disease activity. It is speculated that, similarly to humans, colonic dysmotility may be anxiety-based, although recent data demonstrate that irritable bowel syndrome (IBS) could result from acute infectious enteritis. Specific Lactobacillus spp. strains administered orally in humans induced the expression of μ-opioid and cannabinoid receptors in mucosal enterocytes, modulating intestinal morphine-like analgesic functions. We investigated the potential association of GI signs caused by colonic dysmotility and mucosal expression of cannabinoid receptors in intestinal epithelial cells and the number of mucosal mast cells.
METHODS
Ten to 15 endoscopic biopsies were collected from colonic mucosa of 20 dogs diagnosed with dysmotility disturbances before and after probiotic (Slab51 bacterial blend; Sivoy
KEY RESULTS
Decreased numbers of MCs (P < .0001) and increased CB1- and CB2-positive epithelial cells (P < .0001) in diseased dogs were positively associated with post-treatment CCECAI scores (P < .0001).
CONCLUSIONS AND INFERENCES
Our results suggest that probiotic administration can reduce signs of colonic dysmotility, possibly due to microbiota modulation and epithelial cell receptor-mediated signaling in intestinal mucosa.
Substances chimiques
Receptor, Cannabinoid, CB1
0
Receptor, Cannabinoid, CB2
0
Banques de données
GENBANK
['XM_532360', 'NM_001003142', 'AY_011618.1', 'NM_001284480']
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13717Informations de copyright
© 2019 John Wiley & Sons Ltd.
Références
Lacy BE, Mearin F, Chang L, et al. Bowel disorders. Gastroenterology. 2016;150:1393-1407.
Bashashati M, Moossavi S, Cremon C, et al. Colonic immune cells in irritable bowel syndrome: a systematic review and meta-analysis. Neurogastroenterol Motil. 2018;30:e13192.
Washabau RJ. Antispasmodic agents. In: Washabau RJ, Day MJ, eds. Canine and Feline Gastroenterology. St. Louis, MO: Elsevier Saunders; 2013:481-485.
Muelas MS, Ramirez P, Parrilla P, et al. Vagal system involvement in changes in small bowel motility during restraint stress: an experimental study in the dog. Br J Surg. 1993;80:479-483.
Chey WD, Kurlander J, Eswaran S. Irritable bowel syndrome: a clinical review. JAMA. 2015;313:949-958.
Leib MS. Treatment of chronic idiopathic large-bowel diarrhea in dogs with a highly digestible diet and soluble fiber: a retrospective review of 37 cases. J Vet Intern Med. 2000;14:27-32.
Cerquetella M, Spaterna A, Laus F, et al. Inflammatory bowel disease in the dog: differences and similarities with humans. World J Gastroenterol. 2010;16:1050-1056.
Cerquetella M, Rossi G, Spaterna A, et al. Is irritable bowel syndrome also present in dogs? Tierarztl Prax Ausg K. 2018;46(03):176-180.
Leib MS. Irritable bowel syndrome in dogs: fact or fiction? Compend Contin Educ Pract Vet. 2009;31(2 Suppl A):13-16.
Lecoindre P, Gaschen FP. Chronic idiopathic large bowel diarrhea in the dog. Vet Clin North Am Small Anim Pract. 2011;41:447-456.
Henroteaux M. Results of an endoscopical study of canine colonic diseases. Predominance of idiopathic colitis. Ann Méd Vét. 1990;134:389-392.
Qin H-Y, Wu J, Tong X-D, Sung J, Xu H-X, Bian Z-X. Systematic review of animal models of post-infectious/post-inflammatory irritable bowel syndrome. J Gastroenterol. 2011;46:164-174.
Sanson M, Bueno L, Fioramonti J. Involvement of cannabinoid receptors in inflammatory hypersensitivity to colonic distension in rats. Neurogastroenterol Motil. 2006;18:949-956.
Izzo AA, Mascolo N, Pinto L, Capasso R, Capasso F. The role of cannabinoid receptors in intestinal motility, defaecation and diarrhoea in rats. Eur J Pharmacol. 1999;384:37-42.
Esfandyari T, Camilleri M, Busciglio I, Burton D, Baxter K, Zinsmeister AR. Effects of a cannabinoid receptor agonist on colonic motor and sensory functions in humans: a randomized, placebo-controlled study. Am J Physiol Gastrointest Liver Physiol. 2007;293:G137-G145.
Esfandyari T, Camilleri M, Ferber I, Burton D, Baxter K, Zinsmeister AR. Effect of a cannabinoid agonist on gastrointestinal transit and postprandial satiation in healthy human subjects: a randomized, placebo-controlled study. Neurogastroenterol Motil. 2006;18:831838.
Facci L, Dal Toso R, Romanello S, Buriani A, Skaper SD, Leon A. Mast cells express a peripheral cannabinoid receptor with differential sensitivity to anandamide and palmitoylethanolamide. Proc Natl Acad Sci USA. 1995;92(8):3376-3380.
Granberg M, Fowler CJ, Jacobsson SO. Effects of the cannabimimetic fatty acid derivatives 2-arachidonoylglycerol, anandamide, palmitoylethanolamide and methanandamide upon IgE-dependent antigen-induced-αhexosaminidase, serotonin and TNFα release from rat RBL-2H3 basophilic leukaemic cells. Naunyn Schmiedebergs Arch Pharmacol. 2001;364(1):66-73.
Bisogno T, Maurelli S, Melck D, De Petrocellis L, Di Marzo V. Biosynthesis, uptake, and degradation of anandamide and palmitoylethanolamide in leukocytes. J Biol Chem. 1997;272(6):3315-3323.
Rousseaux C, Thuru X, Gelot A, et al. Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat Med. 2007;13(1):35-37.
Moayyedi P, Ford AC, Talley NJ, et al. The efficacy of probiotics in the treatment of irritable bowel syndrome: a systematic review. Gut. 2010;59(3):325-332.
Lemaire F. Do all types of human research need ethics committee approval? Am J Respir Crit Care Med. 2006;174(4):363-364.
Ford AC, Talley NJ. Mucosal inflammation as a potential etiological factor in irritable bowel syndrome: a systematic review. J Gastroenterol. 2011;46:421-431.
Allenspach K, Wieland B, Gröne A, Gaschen F. Chronic enteropathies in dogs: evaluation of risk factors for negative outcome. J Vet Int Med. 2007;21(4):700-708.
Irani AM, Schwartz LB. Mast cell heterogeneity. Clin Exp Allergy. 1989;19:143-155.
German AJ, Helps CR, Hall EJ, Day MJ. Cytokine mRNA expression in mucosal biopsies from German Shepherd dogs with small intestinal enteropathies. Dig Dis Sci. 2000;45:7-17.
Jergens AE, Schreiner CA, Frank DE, et al. A scoring index for disease activity in canine inflammatory bowel disease. J Vet Intern Med. 2003;17(3):291-297.
Day MJ, Bilzer T, Mansell J, et al. Histopathological standards for the diagnosis of gastrointestinal inflammation in endoscopic biopsy samples from the dog and cat: a report from the World Small Animal Veterinary Association Gastrointestinal Standardization Group. J Comp Pathol. 2008;138(Suppl 1):S1-43.
Kramer H, Windrum GM. The metachromatic staining reaction. J Histochem Cytochem. 1955;3(3):227-237.
Spicer SS. Histochemical properties of mucopolysaccharide and basic protein in mast cells. Ann NY Acad Sci. 1963;103:322-333.
Galiazzo G, Giancola F, Stanzani A, et al. Localization of cannabinoid receptors CB1, CB2, GPR55, and PPARα in the canine gastrointestinal tract. Histochem Cell Biol. 2018;150(2):187-205.
Campora L, Miragliotta V, Ricci E, et al. Cannabinoid receptor type 1 and 2 expression in the skin of healthy dogs and dogs with atopic dermatitis. Am J Vet Res. 2012;73(7):988-995.
Rossi G, Pengo G, Caldin M, et al. Comparison of microbiological, histological, and immunomodulatory parameters in response to treatment with either combination therapy with prednisone and metronidazole or probiotic VSL#3 strains in dogs with idiopathic inflammatory bowel disease. PLoS ONE. 2014;9(4):e94699.
Gioacchini G, Giorgini E, Olivotto I, Maradonna F, Merrifield DL, Carnevali O. The influence of probiotics on zebrafish danio rerio innate immunity and hepatic stress. Zebrafish. 2014;11(2):98-106.
Russo EB. Clinical endocannabinoid deficiency (CECD): can this concept explain therapeutic benefits of cannabis in migraine, fibromyalgia, irritable bowel syndrome and other treatment-resistant conditions? Neuroendocrinol Lett. 2004;25:31-39.
Burke NN, Finn DP, McGuire BE, Roche M. Psychological stress in early life as a predisposing factor for the development of chronic pain: Clinical and preclinical evidence and neurobiological mechanisms. J Neurosci Res. 2017;95:1257-1270.
Mechoulam R, Ben-Shabat S, Hanus L, et al. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol. 1995;50(1):83-90.
Pertwee RG. Cannabinoids and the gastrointestinal tract. Gut. 2001;48:859-867.
Hornby PJ, Prouty SM. Involvement of cannabinoid receptors in gut motility and visceral perception. Br J Pharmacol. 2004;141:1335-1345.
Pinto L, Capasso R, Di Carlo G, Izzo AA. Endocannabinoids and the gut. Prostaglandins Leukot Essent Fatty Acids. 2002;66(2-3):333-341.
Duncan M, Mouihate A, Mackie K, et al. Cannabinoid CB2 receptors in the enteric nervous system modulate gastrointestinal contractility in lipopolysaccharide-treated rats. Am J Physiol Gastrointest Liver Physiol. 2008;295(1):G78-G87.
Izzo AA, Mascolo N, Capasso F. The gastrointestinal pharmacology of cannabinoids. Curr Opin Pharmacol. 2001;1:597-603.
Ruilope LM, Després JP, Scheen A, et al. Effect of rimonabant on blood pressure in overweight/obese patients with/without co-morbidities: analysis of pooled RIO study results. J Hypertens. 2008;26(2):357-367.
Despres JP, Golay A, Sjostrom L. Effects of rimonabant on metabolic risk factors in overweight patients with dyslipidemia. N Engl J Med. 2005;353:2121-2134.
Addy C, Rothenberg P, Li S, et al. Multiple-dose pharmacokinetics, pharmacodynamics, and safety of taranabant, a novel selective cannabinoid-1 receptor inverse agonist, in healthy male volunteers. J Clin Pharmacol. 2008;48:734-744.
Singh UP, Singh NP, Singh B, Price RL, Nagarkatti M, Nagarkatti PS. Cannabinoid receptor-2 (CB2) agonist ameliorates colitis in IL-10(-/-) mice by attenuating the activation of T cells and promoting their apoptosis. Toxicol Appl Pharmacol. 2012;258(2):256-267.
Kikuchi A, Ohashi K, Sugie Y, Sugimoto H, Omura H. Pharmacological evaluation of a novel cannabinoid 2 (CB(2)) ligand, PF-03550096, in vitro and in vivo by using a rat model of visceral hypersensitivity. J Pharmacol Sci. 2008;106:219-224.
Verdú EF, Bercik P, Verma-Gandhu M, et al. Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice. Gut. 2006;55(2):182-190.
Ait-Belgnaoui A, Han W, Lamine F, et al. Lactobacillus farciminis treatment suppresses stress induced visceral hypersensitivity: a possible action through interaction with epithelial cell cytoskeleton contraction. Gut. 2006;55:1090-1094.
Gioacchini G, Rossi G, Carnevali O. Host-probiotic interaction: new insight into the role of the endocannabinoid system by in vivo and ex vivo approaches. Sci Rep. 2017;7(1):1261.
Storr MA, Yüce B, Andrews CN, Sharkey KA. The role of the endocannabinoid system in the pathophysiology and treatment of irritable bowel syndrome. Neurogastroenterol Motil. 2008;20:857-868.
Edwards JF, Fossum TW, Willard MD, Cohen ND, Patterson WB, Carey DP. Changes in the intestinal mucosal cell populations of German shepherd dogs fed diets containing different protein sources. Am J Vet Res. 1995;56:340-348.
Bischoff SC, Krämer S. Human mast cells, bacteria, and intestinal immunity. Immunol Rev. 2007;217:329-337.
O'Sullivan M, Clayton N, Breslin NP, et al. Increased mast cells in the irritable bowel syndrome. Neurogastroenterol Motil. 2000;12:449-457.
Guilarte M, Santos J, de Torres I, et al. Diarrhoea-predominant IBS patients show mast cell activation and hyperplasia in the jejunum. Gut. 2007;56(2):203-209.
Lee H, Park JH, Park DI, et al. Mucosal mast cell count is associated with intestinal permeability in patients with diarrhea predominant irritable bowel syndrome. J Neurogastroenterol Motil. 2013;19(2):244-250.
Martínez C, Vicario M, Ramos L, et al. The jejunum of diarrhea-predominant irritable bowel syndrome shows molecular alterations in the tight junction signaling pathway that are associated with mucosal pathobiology and clinical manifestations. Am J Gastroenterol. 2012;107:736-746.
Klooker TK, Braak B, Koopman KE, et al. The mast cell stabiliser ketotifen decreases visceral hypersensitivity and improves intestinal symptoms in patients with irritable bowel syndrome. Gut. 2010;59(9):1213-1221.
Santoni G, Cardinali C, Morelli MB, Santoni M, Nabissi M, Amantini C. Danger- and pathogen-associated molecular patterns recognition by pattern-recognition receptors and ion channels of the transient receptor potential family triggers the inflammasome activation in immune cells and sensory neurons. J Neuroinflammation. 2015;12:21.
Jeffery P, Zhu J. Mucin-producing elements and inflammatory cells. Novartis Found Symp. 2002;2(48):51-68.
Bischoff SC. Physiological and pathophysiological functions of intestinal mast cells. Semin Immunopathol. 2009;3(1):185-205.
Gionchetti P, Lammers KM, Rizzello F, Campieri M. VSL# 3: an analysis of basic and clinical contributions in probiotic therapeutics. Gastroenterol Clin North Am. 2005;34(3):499-513, ix-x.
Magerl M, Lammel V, Siebenhaar F, Zuberbier T, Metz M, Maurer M. Non-pathogenic commensal Escherichia coli bacteria can inhibit degranulation of mast cells. Exp Dermatol. 2008;17(5):427-435.
Ewaschuk JB, Walker JW, Diaz H, Madsen KL. Bioproduction of conjugated linoleic acid by probiotic bacteria occurs in vitro and in vivo in mice. J Nutr. 2006;136(6):1483-1487.
Clark RB. The role of PPARs in inflammation and immunity. J Leukoc Biol. 2002;71(3):388-400.
Petrof EO, Kojima K, Ropeleski MJ, et al. Probiotics inhibit nuclear factor-kappaB and induce heat shock proteins in colonic epithelial cells through proteasome inhibition. Gastroenterology. 2004;127(5):1474-1487.
Jijon H, Backer J, Diaz H, et al. DNA from probiotic bacteria modulates murine and human epithelial and immune function. Gastroenterology. 2004;126(5):1358-1373.
Sinagra E, Romano C, Cottone M. Psychopharmacological treatment and psychological interventions in irritable bowel syndrome. Gastroenterol Res Pract. 2012;2012:486067.
Lee YJ, Park KS. Irritable bowel syndrome: emerging paradigm in pathophysiology. World J Gastroenterol. 2014;20:2456-2469.