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Research Paper

Interleukin 4 induces rapid mucin transport, increases mucus thickness and quality and decreases colitis and Citrobacter rodentium in contact with epithelial cells

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Pages 97-117 | Received 19 Oct 2018, Accepted 14 Jan 2019, Published online: 03 Feb 2019

References

  • Maiti AK, Sharba S, Navabi N, et al. IL-4 protects the mitochondria against TNFalpha and IFNgamma induced insult during clearance of infection with citrobacter rodentium and escherichia coli. Sci Rep. 2015;5:15434.
  • Johansson ME, Phillipson M, Petersson J, et al. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A. 2008;105(39):15064–15069.
  • Johansson ME, Gustafsson JK, Holmen-Larsson J, et al. Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut. 2013;63(2):281–291.
  • McGuckin MA, Linden SK, Sutton P, et al. Mucin dynamics and enteric pathogens. Nat Rev Microbiol. 2011;9(4):265–278.
  • Linden SK, Sutton P, Karlsson NG, et al. Mucins in the mucosal barrier to infection. Mucosal Immunol. 2008;1(3):183–197.
  • Hasnain SZ, Evans CM, Roy M, et al. Muc5ac: a critical component mediating the rejection of enteric nematodes. J Exp Med. 2011;208(5):893–900.
  • Cohn L, Homer RJ, Niu N, et al. T helper 1 cells and interferon gamma regulate allergic airway inflammation and mucus production. J Exp Med. 1999;190(9):1309–1318.
  • Cohn L, Whittaker L, Niu N, et al. Cytokine regulation of mucus production in a model of allergic asthma. Novartis Found Symp. 2002;248: 201–213. discussion 213-220, 277-282.
  • Jarry A, Muzeau F, Laboisse C. Cytokine effects in a human colonic goblet cell line. Cellular damage and its partial prevention by 5 aminosalicylic acid. Dig Dis Sci. 1992;37(8):1170–1178.
  • Gustafsson JK, Navabi N, Rodriguez-Pineiro AM, et al. Dynamic changes in mucus thickness and ion secretion during Citrobacter rodentium infection and clearance. PLoS One. 2013;8(12):e84430.
  • Bergstrom KS, Kissoon-Singh V, Gibson DL, et al. Muc2 protects against lethal infectious colitis by disassociating pathogenic and commensal bacteria from the colonic mucosa. PLoS Pathog. 2010;6(5):e1000902.
  • Wlodarska M, Thaiss CA, Nowarski R, et al. NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion. Cell. 2014;156(5):1045–1059.
  • Linden SK, Florin TH, McGuckin MA. Mucin dynamics in intestinal bacterial infection. PLoS One. 2008;3(12):e3952.
  • Maaser C, Housley MP, Iimura M, et al. Clearance of Citrobacter rodentium requires B cells but not secretory immunoglobulin A (IgA) or IgM antibodies. Infect Immun. 2004;72(6):3315–3324.
  • Kamada N, Sakamoto K, Seo SU, et al. Humoral immunity in the gut selectively targets phenotypically virulent attaching-and-effacing bacteria for intraluminal elimination. Cell Host Microbe. 2015;17(5):617–627.
  • Smirnova MG, Guo L, Birchall JP, Pearson JP. LPS up-regulates mucin and cytokine mRNA expression and stimulates mucin and cytokine secretion in goblet cells. Cell Immunol. 2003;221(1):42–49.
  • Enss ML, Cornberg M, Wagner S, et al. Proinflammatory cytokines trigger MUC gene expression and mucin release in the intestinal cancer cell line LS180. Inflammation Res. 2000;49(4):162–169.
  • Caballero-Franco C, Keller K, De Simone C, et al. The VSL#3 probiotic formula induces mucin gene expression and secretion in colonic epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2007;292(1):G315–G322.
  • Slomiany BL, Slomiany A. Cytosolic phospholipase A2 activation in Helicobacter pylori lipopolysaccharide-induced interference with gastric mucin synthesis. IUBMB Life. 2006;58(4):217–223.
  • Whittaker L, Niu N, Temann UA, et al. Interleukin-13 mediates a fundamental pathway for airway epithelial mucus induced by CD4 T cells and interleukin-9. Am J Respir Cell Mol Biol. 2002;27(5):593–602.
  • Dabbagh K, Takeyama K, Lee HM, et al. IL-4 induces mucin gene expression and goblet cell metaplasia in vitro and in vivo. J Iimmunol. 1999;162(10):6233–6237.
  • Navabi N, Johansson ME, Raghavan S, et al. Helicobacter pylori infection impairs the mucin production rate and turnover in the murine gastric mucosa. Infect Immun. 2013;81(3):829–837.
  • Dalton DK, Pitts-Meek S, Keshav S, et al. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science. 1993;259(5102):1739–1742.
  • Wu X, Feng X, He Y, et al. IL-4 administration exerts preventive effects via suppression of underlying inflammation and TNF-alpha-induced apoptosis in steroid-induced osteonecrosis. Osteoporos Int. 2016;27(5):1827–1837.
  • Proctor WR, Chakraborty M, Fullerton AM, et al. Thymic stromal lymphopoietin and interleukin-4 mediate the pathogenesis of halothane-induced liver injury in mice. Hepatology. 2014;60(5):1741–1752.
  • Chiba Y, Todoroki M, Nishida Y, et al. A novel STAT6 inhibitor AS1517499 ameliorates antigen-induced bronchial hypercontractility in mice. Am J Respir Cell Mol Biol. 2009;41(5):516–524.
  • Sun L, Ren X, Wang IC, et al. The FOXM1 inhibitor RCM-1 suppresses goblet cell metaplasia and prevents IL-13 and STAT6 signaling in allergen-exposed mice. Sci Signal. 2017;10(475).
  • Jensen LJ, Kuhn M, Stark M, et al. STRING 8–a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 2009;37(Database issue):D412–D416.
  • Gustafsson JK, Ermund A, Johansson ME, et al. An ex vivo method for studying mucus formation, properties, and thickness in human colonic biopsies and mouse small and large intestinal explants. Am J Physiol Gastrointest Liver Physiol. 2012;302(4):G430–G438.
  • Schroeder BO, Birchenough GMH, Ståhlman M, et al. Bifidobacteria or fiber protects against diet-induced microbiota-mediated colonic mucus deterioration. Cell Host Microbe. 2018;23(1):27–40.e27
  • Navabi N, McGuckin MA, Linden SK. Gastrointestinal cell lines form polarized epithelia with an adherent mucus layer when cultured in semi-wet interfaces with mechanical stimulation. PLoS One. 2013;8(7):e68761.
  • Quintana-Hayashi MP, Linden SK. Differentiation of gastrointestinal cell lines by culture in semi-wet interface. Methods Mol Biol. 2018;1817:41–46.
  • Zund G, Madara JL, Dzus AL, et al. Interleukin-4 and interleukin-13 differentially regulate epithelial chloride secretion. J Biol Chem. 1996;271(13):7460–7464.
  • Smirnova MG, Kiselev SL, Birchall JP, et al. Up-regulation of mucin secretion in HT29-MTX cells by the pro-inflammatory cytokines tumor necrosis factor-alpha and interleukin-6. Eur Cytokine Netw. 2001;12(1):119–125.
  • Hiscox S, Hallett MB, Puntis MC, et al. Inhibition of cancer cell motility and invasion by interleukin-12. Clin Exp Metastasis. 1995;13(5):396–404.
  • Adams RB, Planchon SM, Roche JK. IFN-gamma modulation of epithelial barrier function. Time course, reversibility, and site of cytokine binding. J Iimmunol. 1993;150(6):2356–2363.
  • Harrop CA, Gore RB, Evans CM, et al. TGF-beta(2) decreases baseline and IL-13-stimulated mucin production by primary human bronchial epithelial cells. Exp Lung Res. 2013;39(1):39–47.
  • Treede I, Braun A, Jeliaskova P, et al. TNF-alpha-induced up-regulation of pro-inflammatory cytokines is reduced by phosphatidylcholine in intestinal epithelial cells. BMC Gastroenterol. 2009;9:53.
  • Nicklasson M, Sjoling A, von Mentzer A, et al. Expression of colonization factor CS5 of enterotoxigenic escherichia coli (ETEC) is enhanced in vivo and by the bile component Na glycocholate hydrate. PloS one. 2012;7(4):e35827.
  • Westlund J, Livingston M, Fahlen-Yrlid L, et al. CD47-deficient mice have decreased production of intestinal IgA following oral immunization but a maintained capacity to induce oral tolerance. Immunology. 2012;135(3):236–244.
  • Gustafsson JK, Navabi N, Rodriguez-Piñeiro AM, et al. Pushpa Premaratne, Harvey R Fernandez et al. Dynamic changes in mucus thickness and ion secretion during Citrobacter rodentium infection and clearance. Plos One. 2013.
  • Quintana-Hayashi MP, Navabi N, Mahu M, et al. Neutrophil elastase and IL17 expressed in the pig colon during Brachyspira hyodysenteriae infection synergistically with the pathogen induce increased mucus transport speed and production via MAPK3. Infect Immun. 2017.
  • Hang HC, Yu C, Kato DL, et al. A metabolic labeling approach toward proteomic analysis of mucin-type O-linked glycosylation. Proc Natl Acad Sci U S A. 2003;100(25):14846–14851.
  • Johansson ME. Fast renewal of the distal colonic mucus layers by the surface goblet cells as measured by in vivo labeling of mucin glycoproteins. PloS one. 2012;7(7):e41009.
  • Malmberg EK, Noaksson KA, Phillipson M, et al. Increased levels of mucins in the cystic fibrosis mouse small intestine, and modulator effects of the Muc1 mucin expression. Am J Physiol Gastrointest Liver Physiol. 2006;291(2):G203–G210.
  • Parmley RR, Gendler SJ. Cystic fibrosis mice lacking Muc1 have reduced amounts of intestinal mucus. J Clin Invest. 1998;102(10):1798–1806.
  • McCauley HA, Guasch G. Three cheers for the goblet cell: maintaining homeostasis in mucosal epithelia. Trends Mol Med. 2015;21(8):492–503.
  • Chen G, Korfhagen TR, Xu Y, et al. SPDEF is required for mouse pulmonary goblet cell differentiation and regulates a network of genes associated with mucus production. J Clin Invest. 2009;119(10):2914–2924.
  • Wagner B, Perkins G, Babasyan S, et al. Neonatal immunization with a single IL-4/antigen dose induces increased antibody responses after challenge infection with equine herpesvirus type 1 (EHV-1) at weanling age. PLoS One. 2017;12(1):e0169072.
  • Serezani APM, Bozdogan G, Sehra S, et al. IL-4 impairs wound healing potential in the skin by repressing fibronectin expression. J Allergy Clin Immunol. 2017;139(1):142–151 e145.
  • Cosin-Roger J, Ortiz-Masia D, Calatayud S, et al. The activation of Wnt signaling by a STAT6-dependent macrophage phenotype promotes mucosal repair in murine IBD. Mucosal Immunol. 2016;9(4):986–998.
  • Navabi N, Johansson ME, Raghavan S, et al. Helicobacter pylori infection impair mucin production rate and turnover in the murine gastric mucosa. Infect Immun. 2012; 3;81(3):829-37.
  • Orsini B, Ottanelli B, Amedei A, et al. Helicobacter pylori cag pathogenicity island is associated with reduced expression of interleukin-4 (IL-4) mRNA and modulation of the IL-4delta2 mRNA isoform in human gastric mucosa. Infect Immun. 2003;71(11):6664–6667.
  • Cohn L, Homer RJ, Marinov A, et al. Induction of airway mucus production By T helper 2 (Th2) cells: a critical role for interleukin 4 in cell recruitment but not mucus production. J Exp Med. 1997;186(10):1737–1747.
  • Russell MA, Cooper AC, Dhayal S, et al. Differential effects of interleukin-13 and interleukin-6 on Jak/STAT signaling and cell viability in pancreatic beta-cells. Islets. 2013;5(2):95–105.
  • Rincon M, Anguita J, Nakamura T, et al. Interleukin (IL)-6 directs the differentiation of IL-4-producing CD4+ T cells. J Exp Med. 1997;185(3):461–469.
  • Huynh HQ, Couper RT, Tran CD, et al. N-acetylcysteine, a novel treatment for Helicobacter pylori infection. Dig Dis Sci. 2004;49(11–12):1853–1861.
  • Amrouche-Mekkioui I, Djerdjouri B. N-acetylcysteine improves redox status, mitochondrial dysfunction, mucin-depleted crypts and epithelial hyperplasia in dextran sulfate sodium-induced oxidative colitis in mice. Eur J Pharmacol. 2012;691(1–3):209–217.
  • Su CW, Cao Y, Zhang M, et al. Helminth infection impairs autophagy-mediated killing of bacterial enteropathogens by macrophages. J Immunol. 2012;189(3):1459–1466.
  • Kamada N, Kim YG, Sham HP, et al. Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science. 2012;336(6086):1325–1329.
  • Johansson ME, Jakobsson HE, Holmen-Larsson J, et al. Normalization of host intestinal mucus layers requires long-term microbial colonization. Cell Host Microbe. 2015;18(5):582–592.
  • Long KZ, Rosado JL, Santos JI, et al. Associations between mucosal innate and adaptive immune responses and resolution of diarrheal pathogen infections. Infect Immun. 2010;78(3):1221–1228.
  • Borenshtein D, Nambiar PR, Groff EB, et al. Development of fatal colitis in FVB mice infected with Citrobacter rodentium. Infect Immun. 2007;75(7):3271–3281.