Mucosal immunity and gut microbiota in dogs with chronic enteropathy

Research in Veterinary Science - Tập 122 - Trang 156-164 - 2019
Nour Eissa1, Hatem Kittana2, João Carlos Gomes-Neto3, Hayam Hussein4
1Department of Immunology, University of Manitoba, Winnipeg, MB, Canada
2Department of Food Science and Technology, University of Nebraska-, Lincoln, NE, USA
3Nebraska Food for Health Center, Department of Food Science and Technology, University of Nebraska, Lincoln, NE, USA
4Department of Parasitology and Animal Diseases, Veterinary Research Division, National Research Centre, Giza, Egypt

Tài liệu tham khảo

Allenspach, 2011, Clinical immunology and immunopathology of the canine and feline intestine, Vet. Clin. N. Am. Small Anim. Pract., 41, 345, 10.1016/j.cvsm.2011.01.004 Allenspach, 2007, Chronic enteropathies in dogs: evaluation of risk factors for negative outcome, J. Vet. Intern. Med., 21, 700, 10.1111/j.1939-1676.2007.tb03011.x Allenspach, 2010, Evaluation of mucosal bacteria and histopathology, clinical disease activity and expression of Toll-like receptors in German shepherd dogs with chronic enteropathies, Vet. Microbiol., 146, 326, 10.1016/j.vetmic.2010.05.025 Allenspach, 2016, Long-term outcome in dogs with chronic enteropathies: 203 cases, Vet. Rec., 178, 368, 10.1136/vr.103557 Atreya, 2008, NF-κB in inflammatory bowel disease, J. Intern. Med., 263, 591, 10.1111/j.1365-2796.2008.01953.x Bain, 2013, Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6Chi monocyte precursors, Mucosal Immunol., 6, 498, 10.1038/mi.2012.89 Bastan, 2017, Assessment of eosinophil peroxidase as a potential diagnostic and prognostic marker in dogs with inflammatory bowel disease, Am. J. Vet. Res., 78, 36, 10.2460/ajvr.78.1.36 Baumgart, 2007, Inflammatory bowel disease: cause and immunobiology, Lancet, 369, 1627, 10.1016/S0140-6736(07)60750-8 Baumgart, 2007, Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn's disease involving the ileum, ISME J., 1, 403, 10.1038/ismej.2007.52 Belkaid, 2014, Role of the microbiota in immunity and inflammation, Cell, 157, 121, 10.1016/j.cell.2014.03.011 Boden, 2017 Bottero, 2017, Fecal microbiota transplantation (FMT) in 16 dogs with idiopatic IBD, Veterinaria (Cremona), 31, 31 Bron, 2012, Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa, Nat. Rev. Microbiol., 10, 66, 10.1038/nrmicro2690 Bunker, 2017, Natural polyreactive IgA antibodies coat the intestinal microbiota, Science, 358, 10.1126/science.aan6619 Canton, 2013, Scavenger receptors in homeostasis and immunity, Nat. Rev. Immunol., 13, 621, 10.1038/nri3515 Carvalho, 2012, Transient inability to manage proteobacteria promotes chronic gut inflammation in TLR5-deficient mice, Cell Host Microbe, 12, 139, 10.1016/j.chom.2012.07.004 Castigli, 2005, TACI and BAFF-R mediate isotype switching in B cells, J. Exp. Med., 201, 35, 10.1084/jem.20032000 Chaitman, 2016, Commentary on key aspects of fecal microbiota transplantation in small animal practice, Vet. Med., 7, 71 Chassaing, 2011, The commensal microbiota and enteropathogens in the pathogenesis of inflammatory bowel diseases, Gastroenterology, 140 Choy, 2017, An overview of the innate and adaptive immune system in inflammatory bowel disease, Inflamm. Bowel Dis., 23, 2, 10.1097/MIB.0000000000000955 Conte, 2014, Adherent-invasive Escherichia coli (AIEC) in pediatric Crohn's disease patients: phenotypic and genetic pathogenic features, BMC Res. Notes, 7, 748, 10.1186/1756-0500-7-748 Corthay, 2009, How do regulatory T cells work?, Scand. J. Immunol., 70, 326, 10.1111/j.1365-3083.2009.02308.x Cupi, 2014, Plasma cells in the mucosa of patients with inflammatory bowel disease produce granzyme B and possess cytotoxic activities, J. Immunol., 192, 6083, 10.4049/jimmunol.1302238 Dandrieux, 2008, Evaluation of lymphocyte apoptosis in dogs with inflammatory bowel disease, Am. J. Vet. Res., 69, 1279, 10.2460/ajvr.69.10.1279 Darfeuille-Michaud, 2004, High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease, Gastroenterology, 127, 412, 10.1053/j.gastro.2004.04.061 De Souza, 2016, Immunopathogenesis of IBD: current state of the art, Nat. Rev. Gastroenterol. Hepatol., 13, 13, 10.1038/nrgastro.2015.186 Eissa, 2015, Immunomodulatory effect of ghrelin in the intestinal mucosa, Neurogastroenterol. Motil., 27, 1519, 10.1111/nmo.12703 Eissa, 2017, Chromofungin (CHR: CHGA47-66) is downregulated in persons with active ulcerative colitis and suppresses pro-inflammatory macrophage function through the inhibition of NF-κB signaling, Biochem. Pharmacol., 145, 102, 10.1016/j.bcp.2017.08.013 Eissa, 2017, Chromofungin ameliorates the Progression of colitis by regulating alternatively activated Macrophages, Front. Immunol., 8, 1131, 10.3389/fimmu.2017.01131 Eissa, 2018, Chromogranin-A and its derived peptides and their pharmacological effects during intestinal inflammation, Biochem. Pharmacol., 152, 315, 10.1016/j.bcp.2018.04.009 Eissa, 2018, Chromogranin-A regulates macrophage function and the apoptotic pathway in murine DSS colitis, J. Mol. Med., 96, 183, 10.1007/s00109-017-1613-6 Elshaer, 2017, The role of barrier function, autophagy, and cytokines in maintaining intestinal homeostasis, Semin. Cell Dev. Biol., 51, 10.1016/j.semcdb.2016.08.018 Florey, 2017, Use of a granulocyte immunofluorescence assay designed for humans for detection of antineutrophil cytoplasmic antibodies in dogs with chronic enteropathies, J. Vet. Intern. Med., 31, 1062, 10.1111/jvim.14774 Foster, 2003, Serum IgE and IgG responses to food antigens in normal and atopic dogs, and dogs with gastrointestinal disease, Vet. Immunol. Immunopathol., 92, 113, 10.1016/S0165-2427(03)00033-3 Fries, 2011, Mucosal dendritic cell diversity in the gastrointestinal tract, Cell Tissue Res., 343, 33, 10.1007/s00441-010-1030-4 Gagliani, 2015, T H 17 cells transdifferentiate into regulatory T cells during resolution of inflammation, Nature, 523, 221, 10.1038/nature14452 Geremia, 2014, Innate and adaptive immunity in inflammatory bowel disease, Autoimmun. Rev., 13, 3, 10.1016/j.autrev.2013.06.004 German, 2000, An immunohistochemical study of histiocytic ulcerative colitis in boxer dogs, J. Comp. Pathol., 122, 163, 10.1053/jcpa.1999.0353 German, 2000, Cytokine mRNA expression in mucosal biopsies from German shepherd dogs with small intestinal enteropathies, Dig. Dis. Sci., 45, 7, 10.1023/A:1005436721798 German, 2001, Immune cell populations within the duodenal mucosa of dogs with enteropathies, J. Vet. Intern. Med., 15, 14, 10.1111/j.1939-1676.2001.tb02292.x German, 2003, Chronic intestinal inflammation and intestinal disease in dogs, J. Vet. Intern. Med., 17, 8, 10.1111/j.1939-1676.2003.tb01318.x Gill, 2012, Neutrophil elastase alters the murine gut microbiota resulting in enhanced Salmonella colonization, PLoS One, 7, e49646, 10.1371/journal.pone.0049646 Guard, 2015, Characterization of microbial dysbiosis and metabolomic changes in dogs with acute diarrhea, PLoS One, 10, 10.1371/journal.pone.0127259 Hammad, 2015, Barrier epithelial cells and the control of type 2 immunity, Immunity, 43, 29, 10.1016/j.immuni.2015.07.007 Han, 2017, The atopic march: current insights into skin barrier dysfunction and epithelial cell-derived cytokines, Immunol. Rev., 278, 116, 10.1111/imr.12546 Heilmann, 2016, Fecal S100A12 concentration predicts a lack of response to treatment in dogs affected with chronic enteropathy, Vet. J., 215, 96, 10.1016/j.tvjl.2016.03.001 Honneffer, 2014, Microbiota alterations in acute and chronic gastrointestinal inflammation of cats and dogs, World J. Gastroenterol., 20, 16489, 10.3748/wjg.v20.i44.16489 Igarashi, 2014, Expression profiling of pattern recognition receptors and selected cytokines in miniature dachshunds with inflammatory colorectal polyps, Vet. Immunol. Immunopathol., 159, 1, 10.1016/j.vetimm.2014.03.003 Igarashi, 2015, Functional analysis of pattern recognition receptors in miniature dachshunds with inflammatory colorectal polyps, J. Vet. Med. Sci., 77, 439, 10.1292/jvms.14-0505 Igarashi, 2015, Polymorphisms of nucleotide-binding oligomerization domain 2 (NOD2) gene in miniature dachshunds with inflammatory colorectal polyps, Vet. Immunol. Immunopathol., 164, 160, 10.1016/j.vetimm.2015.02.005 Jergens, 2009, Intestinal cytokine mRNA expression in canine inflammatory bowel disease: a meta-analysis with critical appraisal, Comp. Med., 59, 153 Jergens, 2010, Relationship of mucosal gene expression to microbiota composition in dogs with inflammatory bowel disease, J. Vet. Intern. Med., 24, 725 Junginger, 2012, Immunohistochemical investigation of Foxp3 expression in the intestine in healthy and diseased dogs, Vet. Res., 43, 23, 10.1186/1297-9716-43-23 Junginger, 2014, Canine gut dendritic cells in the steady state and in inflammatory bowel disease, Innate Immun., 20, 145, 10.1177/1753425913485475 Kainulainen, 2015, The canine isolate Lactobacillus acidophilus LAB20 adheres to intestinal epithelium and attenuates LPS-induced IL-8 secretion of enterocytes in vitro, BMC Microbiol., 15, 4, 10.1186/s12866-014-0337-9 Kalenyak, 2017, Comparison of the intestinal mucosal microbiota in dogs diagnosed with idiopathic inflammatory bowel disease and dogs with food-responsive diarrhea before and after treatment, FEMS Microbiol. Ecol., 94 Kao, 2017, Effect of oral capsule–vs colonoscopy-delivered fecal microbiota transplantation on recurrent clostridium difficile infection: a randomized clinical trial, JAMA, 318, 1985, 10.1001/jama.2017.17077 Kathrani, 2010, Polymorphisms in the TLR4 and TLR5 gene are significantly associated with inflammatory bowel disease in German shepherd dogs, PLoS One, 5, 10.1371/journal.pone.0015740 Kathrani, 2011, Breed-independent toll-like receptor 5 polymorphisms show association with canine inflammatory bowel disease, HLA, 78, 94 Kathrani, 2011, CD11c+ cells are significantly decreased in the duodenum, ileum and colon of dogs with inflammatory bowel disease, J. Comp. Pathol., 145, 359, 10.1016/j.jcpa.2011.03.010 Kathrani, 2012, TLR5 risk-associated haplotype for canine inflammatory bowel disease confers hyper-responsiveness to flagellin, PLoS One, 7, e30117, 10.1371/journal.pone.0030117 Kathrani, 2014, Association between nucleotide oligomerisation domain two (Nod2) gene polymorphisms and canine inflammatory bowel disease, Vet. Immunol. Immunopathol., 161, 32, 10.1016/j.vetimm.2014.06.003 Kinjo, 2017, Intestinal IL-17 expression in canine inflammatory bowel disease, Int. J. Vet. Health Sci. Res., 5, 171 Kleinschmidt, 2007, Characterization of mast cell numbers and subtypes in biopsies from the gastrointestinal tract of dogs with lymphocytic-plasmacytic or eosinophilic gastroenterocolitis, Vet. Immunol. Immunopathol., 120, 80, 10.1016/j.vetimm.2007.07.006 Köhler, 2007, Allograft inflammatory factor-1/Ionized calcium-binding adapter molecule 1 is specifically expressed by most subpopulations of macrophages and spermatids in testis, Cell Tissue Res., 330, 291, 10.1007/s00441-007-0474-7 Kolaczkowska, 2013, Neutrophil recruitment and function in health and inflammation, Nat. Rev. Immunol., 13, 159, 10.1038/nri3399 Kołodziejska-Sawerska, 2013, Cytokines in canine inflammatory bowel disease, Pol. J. Vet. Sci., 16, 165, 10.2478/pjvs-2013-0025 Krausgruber, 2016, T-bet is a key modulator of IL-23-driven pathogenic CD4+ T cell responses in the intestine, Nat. Commun., 7, 11627, 10.1038/ncomms11627 Kubinak, 2015, MyD88 signaling in T cells directs IgA-mediated control of the microbiota to promote health, Cell Host Microbe, 17, 153, 10.1016/j.chom.2014.12.009 Lecoindre, 2016, Focal intestinal lipogranulomatous lymphangitis in 10 dogs, J. Small Anim. Pract., 57, 465, 10.1111/jsap.12522 Locher, 2001, Quantitative assessment of mast cells and expression of IgE protein and mRNA for IgE and interleukin 4 in the gastrointestinal tract of healthy dogs and dogs with inflammatory bowel disease, Am. J. Vet. Res., 62, 211, 10.2460/ajvr.2001.62.211 Luckschander, 2006, Perinuclear antineutrophilic cytoplasmic antibody and response to treatment in diarrheic dogs with food responsive disease or inflammatory bowel disease, J. Vet. Intern. Med., 20, 221, 10.1111/j.1939-1676.2006.tb02849.x Luckschander, 2010, Activation of nuclear factor-κB in dogs with chronic enteropathies, Vet. Immunol. Immunopathol., 133, 228, 10.1016/j.vetimm.2009.08.014 Ma, 2017, Noninvasive fecal immunochemical testing and fecal calprotectin predict mucosal healing in inflammatory bowel disease: a prospective cohort study, Inflamm. Bowel Dis., 23, 1643, 10.1097/MIB.0000000000001173 Maeda, 2013, Decreased immunoglobulin A concentrations in feces, duodenum, and peripheral blood mononuclear cells of dogs with inflammatory bowel disease, J. Vet. Intern. Med., 27, 47, 10.1111/jvim.12023 Maeda, 2014, Methylation of TNFRSF13B and TNFRSF13C in duodenal mucosa in canine inflammatory bowel disease and its association with decreased mucosal IgA expression, Vet. Immunol. Immunopathol., 160, 97, 10.1016/j.vetimm.2014.04.005 Maeda, 2016, Changes in Foxp3-positive regulatory T cell number in the intestine of dogs with idiopathic inflammatory bowel disease and intestinal lymphoma, Vet. Pathol., 53, 102, 10.1177/0300985815591081 Mancho, 2010, Detection of perinuclear antineutrophil cytoplasmic antibodies and antinuclear antibodies in the diagnosis of canine inflammatory bowel disease, J. Vet. Diagn. Investig., 22, 553, 10.1177/104063871002200409 Martinez-Medina, 2014, Escherichia coli in chronic inflammatory bowel diseases: an update on adherent invasive Escherichia coli pathogenicity, World J. Gastrointest. Pathophysiol., 5, 213, 10.4291/wjgp.v5.i3.213 Martinez-Medina, 2011, Adherent-invasive Escherichia coli phenotype displayed by intestinal pathogenic E. coli strains from cats, dogs, and swine, Appl. Environ. Microbiol., 77, 5813, 10.1128/AEM.02614-10 McDaniel, 2016, Emerging roles for noncanonical NF-κB signaling in the modulation of inflammatory bowel disease pathobiology, Inflamm. Bowel Dis., 22, 2265, 10.1097/MIB.0000000000000858 McMahon, 2010, Expression of Toll-like receptor 2 in duodenal biopsies from dogs with inflammatory bowel disease is associated with severity of disease, Vet. Immunol. Immunopathol., 135, 158, 10.1016/j.vetimm.2009.11.012 Mills, 2017, Ruptured congenital jejunal diverticulum resulting in a mechanical gastrointestinal tract obstruction in a dog, Companion Anim., 22, 270, 10.12968/coan.2017.22.5.270 Minamoto, 2014, Prevalence of Clostridium perfringens, Clostridium perfringens enterotoxin and dysbiosis in fecal samples of dogs with diarrhea, Vet. Microbiol., 174, 463, 10.1016/j.vetmic.2014.10.005 Minamoto, 2015, Alteration of the fecal microbiota and serum metabolite profiles in dogs with idiopathic inflammatory bowel disease, Gut Microbes, 6, 33, 10.1080/19490976.2014.997612 Mito, 2010, IFNγ markedly cooperates with intratumoral dendritic cell vaccine in dog tumor models, Cancer Res., 70, 7093, 10.1158/0008-5472.CAN-10-0600 Mizoguchi, 2017, 111 Munyaka, 2015, Antepartum antibiotic treatment increases offspring susceptibility to experimental colitis: a role of the gut microbiota, PLoS One, 10, 10.1371/journal.pone.0142536 Nagaishi, 2017, 141 Nolte, 2017, Heterogeneity of macrophages in canine histiocytic ulcerative colitis, Innate Immun., 23, 228, 10.1177/1753425916686170 Ohta, 2013, Expression of CD4+ T cell cytokine genes in the colorectal mucosa of inflammatory colorectal polyps in miniature dachshunds, Vet. Immunol. Immunopathol., 155, 259, 10.1016/j.vetimm.2013.07.006 Ohta, 2014, CD4+ T cell cytokine gene and protein expression in duodenal mucosa of dogs with inflammatory bowel disease, J. Vet. Med. Sci., 76, 409, 10.1292/jvms.13-0008 Okanishi, 2013, NOD2 mRNA expression and NFkappaB activation in dogs with lymphocytic plasmacytic colitis, J. Vet. Intern. Med., 27, 439, 10.1111/jvim.12082 Okanishi, 2013, Activation of nuclear factor-kappa B and cell adhesion molecule mRNA expression in duodenal mucosa of dogs with lymphocytic-plasmacytic enteritis, Vet. Immunol. Immunopathol., 154, 145, 10.1016/j.vetimm.2013.05.013 Omori, 2017, Fecal microbiome in dogs with inflammatory bowel disease and intestinal lymphoma, J. Vet. Med. Sci., 79, 1840, 10.1292/jvms.17-0045 Osada, 2017, Expression of epithelial cell-derived cytokine genes in the duodenal and colonic mucosae of dogs with chronic enteropathy, J. Vet. Med. Sci., 79, 393, 10.1292/jvms.16-0451 Pai, 2011, Immunopathogenic behaviors of canine transmissible venereal tumor in dogs following an immunotherapy using dendritic/tumor cell hybrid, Vet. Immunol. Immunopathol., 139, 187, 10.1016/j.vetimm.2010.10.013 Peters, 2005, Cytokine mRNA quantification in duodenal mucosa from dogs with chronic enteropathies by real-time reverse transcriptase polymerase chain reaction, J. Vet. Intern. Med., 19, 644, 10.1111/j.1939-1676.2005.tb02742.x Peterson, 2014, Intestinal epithelial cells: regulators of barrier function and immune homeostasis, Nat. Rev. Immunol., 14, 141, 10.1038/nri3608 Pinto, 2017, Unusual small intestine inflammatory lesions in a dog with visceral leishmaniasis, Braz. J. Vet. Pathol., 6, 19 Planer, 2016, Development of the gut microbiota and mucosal IgA responses in twins and gnotobiotic mice, Nature, 534, 263, 10.1038/nature17940 Qeska, 2013, Species-specific properties and translational aspects of canine dendritic cells, Vet. Immunol. Immunopathol., 151, 181, 10.1016/j.vetimm.2012.12.003 Rabbi, 2017, Reactivation of intestinal inflammation is suppressed by catestatin in a murine model of colitis via M1 macrophages and not the gut microbiota, Front. Immunol., 8, 985, 10.3389/fimmu.2017.00985 Rabbi, 2017, Human catestatin alters gut microbiota composition in mice, Front. Microbiol., 7, 2151, 10.3389/fmicb.2016.02151 Ramsay, 2010, Mast cells in gastrointestinal disease, Gastroenterol. Hepatol., 6, 772 Reboldi, 2016, IgA production requires B cell interaction with subepithelial dendritic cells in Peyer's patches, Science, 352, 10.1126/science.aaf4822 Rescigno, 2009, Dendritic cells in intestinal homeostasis and disease, J. Clin. Invest., 119, 2441, 10.1172/JCI39134 Rivera-Chávez, 2016, Depletion of butyrate-producing Clostridia from the gut microbiota drives an aerobic luminal expansion of Salmonella, Cell Host Microbe, 19, 443, 10.1016/j.chom.2016.03.004 Rossi, 2014, 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, 9, e94699, 10.1371/journal.pone.0094699 Rychlik, 2013, The effectiveness of natural and synthetic immunomodulators in the treatment of inflammatory bowel disease in dogs, Acta Vet. Hung., 61, 297, 10.1556/AVet.2013.015 Sartor, 2008, Microbial influences in inflammatory bowel diseases, Gastroenterology, 134, 577, 10.1053/j.gastro.2007.11.059 Schmitz, 2016, Understanding the canine intestinal microbiota and its modification by pro-, pre-and synbiotics–what is the evidence?, Vet. Med. Sci., 2, 71, 10.1002/vms3.17 Schmitz, 2012, Gene expression of selected signature cytokines of T cell subsets in duodenal tissues of dogs with and without inflammatory bowel disease, Vet. Immunol. Immunopathol., 146, 87, 10.1016/j.vetimm.2012.01.013 Sekirov, 2010, Gut microbiota in health and disease, Physiol. Rev., 90, 859, 10.1152/physrev.00045.2009 da Silva, 2017, T lymphocytes and macrophages in the intestinal tissues of dogs infected with Leishmania infantum, Rev. Bras. Parasitol. Vet., 26, 159, 10.1590/s1984-29612017039 Simkin, 2017, Macrophages are necessary for epimorphic regeneration in African spiny mice, elife, 6, 10.7554/eLife.24623 Simpson, 2006, Adherent and invasive Escherichia coli is associated with granulomatous colitis in boxer dogs, Infect. Immun., 74, 4778, 10.1128/IAI.00067-06 Spees, 2013, Streptomycin-induced inflammation enhances Escherichia coli gut colonization through nitrate respiration, MBio, 4, 10.1128/mBio.00430-13 Steinbach, 2014, The role of macrophages and dendritic cells in the initiation of inflammation in IBD, Inflamm. Bowel Dis., 20, 166, 10.1097/MIB.0b013e3182a69dca Stokes, 2006, Mucosal defence along the gastrointestinal tract of cats and dogs, Vet. Res., 37, 281, 10.1051/vetres:2006015 Stonehewer, 1998, Evaluation of B and T lymphocytes and plasma cells in colonic mucosa from healthy dogs and from dogs with inflammatory bowel disease, Res. Vet. Sci., 65, 59, 10.1016/S0034-5288(98)90028-5 Strandmark, 2017, Eosinophils are required to suppress Th2 responses in Peyer's patches during intestinal infection by nematodes, Mucosal Immunol., 10, 661, 10.1038/mi.2016.93 Suchodolski, 2011, Companion animals symposium: microbes and gastrointestinal health of dogs and cats1, J. Anim. Sci., 89, 1520, 10.2527/jas.2010-3377 Suchodolski, 2011, Intestinal microbiota of dogs and cats: a bigger world than we thought, Vet. Clin. N. Am. Small Anim. Pract., 41, 261, 10.1016/j.cvsm.2010.12.006 Suchodolski, 2015, 183 Suchodolski, 2010, Molecular analysis of the bacterial microbiota in duodenal biopsies from dogs with idiopathic inflammatory bowel disease, Vet. Microbiol., 142, 394, 10.1016/j.vetmic.2009.11.002 Suchodolski, 2012, 16S rRNA gene pyrosequencing reveals bacterial dysbiosis in the duodenum of dogs with idiopathic inflammatory bowel disease, PLoS One, 7, e39333, 10.1371/journal.pone.0039333 Suzuki, 2007, Intestinal IgA synthesis: a primitive form of adaptive immunity that regulates microbial communities in the gut, Semin. Immunol., 127, 10.1016/j.smim.2006.10.001 Tamura, 2013, Markedly increased expression of interleukin-8 in the colorectal mucosa of inflammatory colorectal polyps in miniature dachshunds, Vet. Immunol. Immunopathol., 156, 32, 10.1016/j.vetimm.2013.09.017 Tamura, 2014, Evaluation of selected cytokine gene expression in colonic mucosa from dogs with idiopathic lymphocytic-plasmacytic colitis, J. Vet. Med. Sci., 76, 1407, 10.1292/jvms.13-0635 Vannella, 2017, Mechanisms of organ injury and repair by macrophages, Annu. Rev. Physiol., 79, 593, 10.1146/annurev-physiol-022516-034356 Vázquez-Baeza, 2016, Dog and human inflammatory bowel disease rely on overlapping yet distinct dysbiosis networks, Nat. Microbiol., 1, 16177, 10.1038/nmicrobiol.2016.177 Volkmann, 2013, Efficacy of AST-120 in dogs with chronic idiopathic enteropathies, J. Vet. Intern. Med., 27, 1637, 10.1111/jvim.12212 Weaver, 2007, IL-17 family cytokines and the expanding diversity of effector T cell lineages, Annu. Rev. Immunol., 25, 821, 10.1146/annurev.immunol.25.022106.141557 Wennogle, 2017, Histopathologic characteristics of intestinal biopsy samples from dogs with chronic inflammatory enteropathy with and without hypoalbuminemia, J. Vet. Intern. Med., 31, 371, 10.1111/jvim.14669 Wheat, 2017, Suppression of canine dendritic cell activation/maturation and inflammatory cytokine release by mesenchymal stem cells occurs through multiple distinct biochemical pathways, Stem Cells Dev., 26, 249, 10.1089/scd.2016.0199 Winter, 2013, Host-derived nitrate boosts growth of E. coli in the inflamed gut, Science, 339, 708, 10.1126/science.1232467 Woldemeskel, 2017, Ki-67 protein expression and tumor associated inflammatory cells (macrophages and mast cells) in canine colorectal carcinoma, BMC Vet. Res., 13, 111, 10.1186/s12917-017-1030-7 Xenoulis, 2008, Molecular-phylogenetic characterization of microbial communities imbalances in the small intestine of dogs with inflammatory bowel disease, FEMS Microbiol. Ecol., 66, 579, 10.1111/j.1574-6941.2008.00556.x Yi, 2012, Suppression of antigen-specific CD4+ T cell activation by SRA/CD204 through reducing the immunostimulatory capability of antigen-presenting cell, J. Mol. Med., 90, 413, 10.1007/s00109-011-0828-1 Yokoyama, 2017, Stimulation of colorectal biopsies from miniature dachshunds with inflammatory colorectal polyps with toll-like receptor ligands: a pilot study, Vet. Immunol. Immunopathol., 188, 78, 10.1016/j.vetimm.2017.05.006 Yokoyama, 2017, Localization of toll-like receptor (TLR) 2 and TLR4 mRNA in the colorectal mucosa of miniature dachshunds with inflammatory colorectal polyps, J. Comp. Pathol., 156, 183, 10.1016/j.jcpa.2016.10.010