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Dietary Indole-3-Carbinol Alleviated Spleen Enlargement, Enhanced Igg Response in C3H/Hen Mice Infected with Citrobacter Rodentium

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Dietary Indole-3-Carbinol Alleviated Spleen Enlargement, Enhanced Igg Response in C3H/Hen Mice Infected with Citrobacter Rodentium nutrients Article Dietary Indole-3-Carbinol Alleviated Spleen Enlargement, Enhanced IgG Response in C3H/HeN Mice Infected with Citrobacter rodentium Yanbei Wu 1,2,3,4, Jing Wang 1 , Qiang He 4, Liangli Yu 3 , Quynhchi Pham 2, Lumei Cheung 2, Zhi Zhang 3, Young S. Kim 5, Allen D. Smith 2,* and Thomas T. Y. Wang 2,* 1 China-Canada Joint Lab of Food Nutrition and Health (Beijing), Beijing Technology & Business University, Beijing 100048, China; [email protected] (Y.W.); [email protected] (J.W.) 2 Diet, Genomics, and Immunology Laboratory, Beltsville Human Nutrition Research Center, USDA-ARS, Beltsville, MD 20705, USA; [email protected] (Q.P.); [email protected] (L.C.) 3 Department of Nutrition and Food Science, University of Maryland, College Park, MD 20742, USA; [email protected] (L.Y.); [email protected] (Z.Z.) 4 College of Biomass Science and Engineering, Sichuan University, Chengdu 610065, China; [email protected] 5 Nutritional Science Research Group, Division of Cancer Prevention, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA; [email protected] * Correspondence: [email protected] (A.D.S.); [email protected] (T.T.Y.W.); Tel.: +(301)-504-8577 (A.D.S.); +(301)-504-8459 (T.T.Y.W.) Received: 6 September 2020; Accepted: 11 October 2020; Published: 15 October 2020 Abstract: Enteropathogenic and enterohemorrhagic Escherichia coli are important enteric pathogens that induce hemorrhagic colitis or even fatal hemolytic uremic syndrome. Emerging evidence shows that some bio-actives derived from fruits and vegetables may serve as alternatives to antibiotics for overcoming multidrug resistant E. coli infections. In this study, the Citrobacter rodentium (Cr) infection model was utilized to mimic E. coli-induced acute intestinal inflammation, and the effects of a cruciferous vegetable-derived cancer protective compound, indole-3-carbinol (I3C), on the immune responses of Cr-susceptible C3H/HeN mice were investigated. Dietary I3C significantly inhibited the loss of body weight and the increase in spleen size in Cr infected mice. In addition, I3C treatment reduced the inflammatory response to Cr infection by maintaining anti-inflammatory cytokine IL-22 mRNA levels while reducing expression of other pro-inflammatory cytokines including IL17A, IL6, IL1β, TNF-α, and IFN-γ. Moreover, the serum cytokine levels of IL17, TNF-α, IL12p70, and G-CSF also were down-regulated by I3C in Cr-infected mice. Additionally, dietary I3C specifically enhanced the Cr-specific IgG response to Cr infection. In general, dietary I3C reduced the Cr-induced pro-inflammatory response in susceptible C3H/HeN mice and alleviated the physiological changes and tissue damage induced by Cr infection but not Cr colonization. Keywords: indole-3-carbinol; C3H/HeN mice; Citrobacter rodentium; colitis; immunoregulation 1. Introduction Enteropathogenic and enterohemorrhagic Escherichia coli (EPEC and EHEC) are some of the most common pathogenic bacteria that contribute to clinical infections in both animals and humans [1]. EPEC/EHEC exist as normal microbes in the gastrointestinal tract of ruminant animals, such as cow and sheep, but are asymptomatic, while causing severe disease in humans [2]. The symptoms in humans include abdominal cramps, vomiting, and/or diarrhea, which may progress to hemorrhagic colitis [3,4]. About 30% of confirmed cases require hospitalization, and about 10% of cases develop into hemolytic uremic syndrome (HUS) that is characterized by anemia, kidney failure, and low platelet counts [5,6]. Nutrients 2020, 12, 3148; doi:10.3390/nu12103148 www.mdpi.com/journal/nutrients Nutrients 2020, 12, 3148 2 of 15 Nutrients 2020, 12, x FOR PEER REVIEW 2 of 16 Antibioticsinto hemolytic are commonly uremic prescribedsyndrome (HUS) for bacterial that is infectionscharacterized but theirby anemia, overuse kidney on farms failure, and and in hospitalslow has increasedplatelet counts the incidence[5,6]. Antibiotics of multidrug are commonly resistant prescribed (MDR) forE. bacterial coli infections, infections which but their have overuse become a significanton farms threat and in to hospitals human healthhas increased [7]. The the development incidence of multidrug of alternative resistant strategies (MDR) E. for coli controlling infections, the spreadwhich and have treatment become ofa significant EPEC and threat EHEC to human are necessary health [7]. to The protect development public of health alternative and minimizestrategies the economicfor controlling costs associated the spread with and outbreaks treatment ofof theseEPEC bacteria.and EHEC are necessary to protect public health Theand minimize study of the EPEC economic and EHECcosts associ is limitedated with by outbreaks the inability of these of bacteria. these bacteria to mimic human infectionsThe and study disease of EPEC when and using EHEC a rodentis limited model. by theCitrobacter inability of rodentiumthese bacteria(Cr) to is mimic a gram human negative infections and disease when using a rodent model. Citrobacter rodentium (Cr) is a gram negative microbe that naturally infects mice, causes diarrhea and shares 67% of its genes with EPEC and microbe that naturally infects mice, causes diarrhea and shares 67% of its genes with EPEC and EHEC, including genes associated with pathogenicity and virulence [1]. Cr infection in mice causes EHEC, including genes associated with pathogenicity and virulence [1]. Cr infection in mice causes attachingattaching and and effacing effacing (A /(A/E)E) lesions lesions and and a a potent potent TH1TH1/TH17/TH17 inflammatory inflammatory response response similar similar to those to those observedobserved in human in human EPEC EPEC/EHEC/EHEC infections. infections. Therefore,Therefore, it it has has become become a standard a standard small-animal small-animal model model to studyto study infectious infectious colitis colitis [8, 9[8,9].]. Cr Cr infection infection resultsresults in various various changes changes to tothe the colon colon of mice, of mice, including including epithelialepithelial cell proliferation,cell proliferation, crypt crypt hyperplasia, hyperplasia, an an uneven uneven apical apical enterocyte enterocyte surface,surface, cryptcrypt dilation, and mucosaland thickeningmucosal thickening [10]. Except [10]. in Except highly in susceptible highly susceptible mouse strains mouse suchstrains as C3Hsuch/ HeN,as C3H/HeN, colonization of Crcolonization is limited to of the Cr colon, is limited with to few the bacteria colon, with reaching few bacteria systemic reaching organs andsystemic the bloodstreamorgans and the [11 ,12]. Followingbloodstream oral administration, [11,12]. Following Cr oral initially administration, colonizes Cr the initially cecal patchcolonizes and the then cecal migrates patch and to thethen colon migrates to the colon by day 3 post-infection. Bacterial load in the distal colon peaks by day 7 and by day 3 post-infection. Bacterial load in the distal colon peaks by day 7 and remains at high levels remains at high levels through day 12, and is typically cleared by day 21 [13]. In general, Cr infection through day 12, and is typically cleared by day 21 [13]. In general, Cr infection can serve as a useful can serve as a useful model for studying compounds that may prevent or mitigate the effects of EPEC modelor forEHEC studying infections. compounds that may prevent or mitigate the effects of EPEC or EHEC infections. Indole-3-carbinolIndole-3-carbinol (I3C) (I3C) is is aa dietarydietary compound compound (Figure (Figure 1)1 )derived derived from from glucobrassicin, glucobrassicin, a a glucosinolateglucosinolate found found inin cruciferous vegetables vegetables cruciferous cruciferous vegetables vegetables such as such broccoli, as broccoli, cabbage and cabbage and cauliflower.cauliflower. The concentration concentration of ofI3C I3C from from cruciferous cruciferous vegetables vegetables can be can inferred be inferred from the from content the contentof of glucobrassicinglucobrassicin which which varies varies inin didifferentfferent kinds kinds of of cruciferous cruciferous vegetables, vegetables, ranging ranging from from 0.24 0.24μmol·g-1µmol g 1 · − DW toDW 6.2 toµ 6.2mol μmol·g-1g 1 DW DW [14 [14,15].,15]. I3C I3C and and itsits derivativesderivatives ha haveve attracted attracted increased increased attention attention due dueto their to their · − importantimportant role role as anti-inflammatory, as anti-inflammatory, anti-tumor anti-tumor andand immune modulating modulating agents agents [16,17]. [16,17 Substantial]. Substantial evidence indicates that the anti-inflammatory and anti-cancer effects of I3C and its metabolic evidence indicates that the anti-inflammatory and anti-cancer effects of I3C and its metabolic derivatives derivatives are attributed to their ability to modulate several nuclear transcriptional factors including are attributed to their ability to modulate several nuclear transcriptional factors including the estrogen the estrogen receptor (ER), nuclear factor-κB (NF-κB), and the aryl hydrocarbon receptor (AhR), receptorwhich (ER), contribute nuclear to factor- maintainingκB (NF- hormonalκB), and homeosta the aryl hydrocarbonsis, inhibiting receptorcell cycle (AhR),progression/apoptosis, which contribute to maintaininginducing hormonal DNA repair, homeostasis, and enhancing inhibiting carcinogen cell metabolism cycle progression [17,18]. Although/apoptosis, the inducing potential value DNA of repair, and enhancingI3C and its carcinogen derivativesmetabolism in cancer
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