We have recently shown that, within 1 week following peroral Campylobacter jejuni infection, conventional infant mice develop self-limiting enteritis. We here investigated the role of IL-23, IL-22, and IL-18 during C. jejuni strain 81-176 infection of infant mice. The pathogen efficiently colonized the intestines of IL-18−/− mice only, but did not translocate to extra-intestinal compartments. At day 13 postinfection (p.i.), IL-22−/− mice displayed lower colonic epithelial apoptotic cell numbers as compared to wildtype mice, whereas, conversely, colonic proliferating cells increased in infected IL-22−/− and IL-18−/− mice. At day 6 p.i., increases in neutrophils, T and B lymphocytes were less pronounced in gene-deficient mice, whereas regulatory T cell numbers were lower in IL-23p19−/− and IL-22−/− as compared to wildtype mice, which was accompanied by increased colonic IL-10 levels in the latter. Until then, colonic pro-inflammatory cytokines including TNF, IFN-γ, IL-6, and MCP-1 increased in IL-23p19−/− mice, whereas IL-18−/− mice exhibited decreased cytokine levels and lower colonic numbers of T and B cell as well as of neutrophils, macrophages, and monocytes as compared to wildtype controls. In conclusion, IL-23, IL-22, and IL-18 are differentially involved in mediating C. jejuni-induced immunopathology of conventional infant mice.
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-
1.
Young KT , Davis LM, Dirita VJ: Campylobacter jejuni: molecular biology and pathogenesis. Nat Rev Microbiol 5(9), 665–679 (2007)
-
2.
Dasti JI , Tareen AM, Lugert R, Zautner AE, Gross U: Campylobacter jejuni: a brief overview on pathogenicityassociated factors and disease-mediating mechanisms. Int J Med Microbiol: IJMM 300(4), 205–211 (2010)
-
3.
Lane JA , Mehra RK, Carrington SD, Hickey RM: The food glycome: a source of protection against pathogen colonization in the gastrointestinal tract. Int J Food Microbiol 142(1–2), 1–13 (2010)
-
4.
Guerry P , Szymanski CM: Campylobacter sugars sticking out. Trends Microbiol 16(9), 428–435 (2008)
-
5.
Wakerley BR , Uncini A, Yuki N, Group GBSC, Group GBSC: Guillain–Barre and Miller Fisher syndromes–new diagnostic classification. Nat Rev Neuro 10(9), 537–544 (2014)
-
6.
Masanta WO , Heimesaat MM, Bereswill S, Tareen AM, Lugert R, Gross U, Zautner AE: Modification of intestinal microbiota and its consequences for innate immune response in the pathogenesis of campylobacteriosis. Clin Dev Immunol 2013, 526860 (2013)
-
7.
van Spreeuwel JP, Duursma GC, Meijer CJ, Bax R, Rosekrans PC, Lindeman J: Campylobacter colitis: histological immunohistochemical and ultrastructural findings. Gut 26(9), 945–951 (1985)
-
8.
Walker RI , Caldwell MB, Lee EC, Guerry P, Trust TJ, Ruiz-Palacios GM: Pathophysiology of Campylobacter enteritis. Microbiol Rev 50(1), 81–94 (1986)
-
9.
Haag LM , Fischer A, Otto B, Plickert R, Kuhl AA, Gobel UB, Bereswill S, Heimesaat MM: Intestinal microbiota shifts towards elevated commensal Escherichia coli loads abrogate colonization resistance against Campylobacter jejuni in mice. PloS One 7(5), e35988 (2012)
-
10.
Haag LM , Fischer A, Otto B, Grundmann U, Kuhl AA, Gobel UB, Bereswill S, Heimesaat MM: Campylobacter jejuni infection of infant mice: acute enterocolitis is followed by asymptomatic intestinal and extra-intestinal immune responses. Eur J Microbiol Immunol (Bp) 2(1), 2–11 (2012)
-
11.
Heimesaat MM , Haag LM, Fischer A, Otto B, Kuhl AA, Gobel UB, Bereswill S: Survey of extra-intestinal immune responses in asymptomatic long-term Campylobacter jejuni-infected mice. Eur J Microbiol Immunol (Bp) 3(3), 174–182 (2013)
-
12.
Heimesaat MM , Fischer A, Alutis M, Grundmann U, Boehm M, Tegtmeyer N, Gobel UB, Kuhl AA, Bereswill S, Backert S: The impact of serine protease HtrA in apoptosis, intestinal immune responses and extra-intestinal histopathology during Campylobacter jejuni infection of infant mice. Gut Pathog 6, 16 (2014)
-
13.
Alutis ME , Grundmann U, Hagen U, Fischer A, Kuhl AA, Gobel UB, Bereswill S, Heimesaat MM: Matrix metalloproteinase-2 mediates intestinal immunopathogenesis in Campylobacter jejuni-infected infant mice. Eur J Microbiol Immunol (Bp) 5(3), 188–198 (2015)
-
14.
Heimesaat MM , Bereswill S: Murine infection models for the investigation of Campylobacter jejuni–host interactions and pathogenicity. Berl Muench Tierarztl Wochenschr 128(3–4), 98–103 (2015)
-
15.
Alutis ME , Grundmann U, Fischer A, Hagen U, Kuhl AA, Gobel UB, Bereswill S, Heimesaat MM: The role of gelatinases in Campylobacter jejuni infection of gnotobiotic mice. Eur J Microbiol Immunol (Bp) 5(4), 256–267 (2015)
-
16.
Malik A , Sharma D, St Charles J, Dybas LA, Mansfield LS: Contrasting immune responses mediate Campylobacter jejuni-induced colitis and autoimmunity. Mucosal Immunol 7(4), 802–817 (2014)
-
17.
Ouyang WJ , Rutz S, Crellin NK, Valdez PA, Hymowitz SG: Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu Rev Immunol 29, 71–109 (2011)
-
18.
Eidenschenk C , Rutz S, Liesenfeld O, Ouyang W: Role of IL-22 in microbial host defense. Curr Top Microbiol Immunol 380, 213–236 (2014)
-
19.
Munoz M , Heimesaat MM, Danker K, Struck D, Lohmann U, Plickert R, Bereswill S, Fischer A, Dunay IR, Wolk K, Loddenkemper C, Krell HW, Libert C, Lund LR, Frey O, Holscher C, Iwakura Y, Ghilardi N, Ouyang W, Kamradt T, Sabat R, Liesenfeld O: Interleukin (IL)-23 mediates Toxoplasma gondii-induced immunopathology in the gut via matrixmetalloproteinase-2 and IL-22 but independent of IL-17. J Exp Med 206(13), 3047–3059 (2009)
-
20.
Munoz M , Liesenfeld O, Heimesaat MM: Immunology of Toxoplasma gondii. Immunol Rev 240(1), 269–285 (2011)
-
21.
Munoz M , Eidenschenk C, Ota N, Wong K, Lohmann U, Kuhl AA, Wang X, Manzanillo P, Li Y, Rutz S, Zheng Y, Diehl L, Kayagaki N, van Lookeren-Campagne M, Liesenfeld O, Heimesaat M, Ouyang W: Interleukin-22 induces interleukin-18 expression from epithelial cells during intestinal infection. Immunity 42(2), 321–331 (2015)
-
22.
Bereswill S , Fischer A, Plickert R, Haag LM, Otto B, Kuhl AA, Dasti JI, Zautner AE, Munoz M, Loddenkemper C, Gross U, Gobel UB, Heimesaat MM: Novel murine infection models provide deep insights into the “menage a trois” of Campylobacter jejuni, microbiota and host innate immunity. PloS One 6(6), e20953 (2011)
-
23.
Haag LM , Fischer A, Otto B, Plickert R, Kuhl AA, Gobel UB, Bereswill S, Heimesaat MM: Campylobacter jejuni induces acute enterocolitis in gnotobiotic IL-10-/-mice via toll-like-receptor-2 and -4 signaling. PloS One 7(7), e40761 (2012)
-
24.
Alutis ME , Grundmann U, Fischer A, Kuhl AA, Bereswill S, Heimesaat MM: Selective gelatinase inhibition reduces apoptosis and pro-inflammatory immune cell responses in Campylobacter jejuni-infected gnotobiotic IL-10 deficient mice. Eur J Microbiol Immunol (Bp) 4(4), 213–222 (2014)
-
25.
Heimesaat MM , Lugert R, Fischer A, Alutis M, Kuhl AA, Zautner AE, Tareen AM, Gobel UB, Bereswill S: Impact of Campylobacter jejuni cj0268c knockout mutation on intestinal colonization, translocation, and induction of immunopathology in gnotobiotic IL-10 deficient mice. PloS One 9(2), e90148 (2014)
-
26.
Heimesaat MM , Alutis M, Grundmann U, Fischer A, Tegtmeyer N, Bohm M, Kuhl AA, Gobel UB, Backert S, Bereswill S: The role of serine protease HtrA in acute ulcerative enterocolitis and extra-intestinal immune responses during Campylobacter jejuni infection of gnotobiotic IL-10 deficient mice. Front Cell Infect Microbiol 4, 77 (2014)
-
27.
Paclik D , Berndt U, Guzy C, Dankof A, Danese S, Holzloehner P, Rosewicz S, Wiedenmann B, Wittig BM, Dignass AU, Sturm A: Galectin-2 induces apoptosis of lamina propria T lymphocytes and ameliorates acute and chronic experimental colitis in mice. J Mol Med 86(12), 1395–1406 (2008)
-
28.
Heimesaat MM , Bereswill S, Fischer A, Fuchs D, Struck D, Niebergall J, Jahn HK, Dunay IR, Moter A, Gescher DM, Schumann RR, Gobel UB, Liesenfeld O: Gram-negative bacteria aggravate murine small intestinal Th1-type immunopathology following oral infection with Toxoplasma gondii. J Immunol 177(12), 8785–8795 (2006)
-
29.
Scholzen T , Gerdes J: The Ki-67 protein: from the known and the unknown. J Cell Physiol 182(3), 311–322 (2000)
-
30.
Buonocore S , Ahern PP, Uhlig HH, Ivanov, II, Littman DR, Maloy KJ, Powrie F: Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature 464(7293), 1371–1375 (2010)
-
31.
Zilbauer M , Dorrell N, Boughan PK, Harris A, Wren BW, Klein NJ, Bajaj-Elliott M: Intestinal innate immunity to Campylobacter jejuni results in induction of bactericidal human beta-defensins 2 and 3. Infect Immun 73(11), 7281–7289 (2005)
-
32.
Edwards LA , Nistala K, Mills DC, Stephenson HN, Zilbauer M, Wren BW, Dorrell N, Lindley KJ, Wedderburn LR, Bajaj-Elliott M: Delineation of the innate and adaptive T-cell immune outcome in the human host in response to Campylobacter jejuni infection. PloS One 5(11), e15398 (2010)
-
33.
Mozaffari Namin B , Soltan Dallal MM, Ebrahimi Daryani N: The Effect of Campylobacter concisus on expression of IL-18, TNF-alpha and p53 in Barrett’s cell lines. Jundishapur J Microbiol 8(12), e26393 (2015)
-
34.
Kaakoush NO , Deshpande NP, Man SM, Burgos-Portugal JA, Khattak FA, Raftery MJ, Wilkins MR, Mitchell HM: Transcriptomic and proteomic analyses reveal key innate immune signatures in the host response to the gastrointestinal pathogen Campylobacter concisus. Infect Immun 83(2), 832–845 (2015)
-
35.
Heimesaat MM , Alter T, Bereswill S, Gölz G: Intestinal expression of genes encoding inflammatory mediators and gelatinases during Arcobacter butzleri infection of gnotobiotic IL-10 deficient mice. Eur J Microbiol Immunol (Bp) 6(1), 56–66 (2016)
-
36.
Bereswill S , Plickert R, Fischer A, Kuhl AA, Loddenkemper C, Batra A, Siegmund B, Gobel UB, Heimesaat MM: What you eat is what you get: Novel Campylobacter models in the quadrangle relationship between nutrition, obesity, microbiota and susceptibility to infection. Eur J Microbiol Immunol (Bp) 1(3), 237–248 (2011)
-
37.
Heimesaat MM , Plickert R, Fischer A, Gobel UB, Bereswill S: Can microbiota transplantation abrogate murine colonization resistance against Campylobacter jejuni? Eur J Microbiol Immunol (Bp) 3(1), 36–43 (2013)
-
38.
Otto B , Haag LM, Fischer A, Plickert R, Kuhl AA, Gobel UB, Heimesaat MM, Bereswill S: Campylobacter jejuni induces extra-intestinal immune responses via Toll-likereceptor-4 signaling in conventional IL-10 deficient mice with chronic colitis. Eur J Microbiol Immunol (Bp) 2(3), 210–219 (2012)
-
39.
Zenewicz LA , Yin X, Wang G, Elinav E, Hao L, Zhao L, Flavell RA: IL-22 deficiency alters colonic microbiota to be transmissible and colitogenic. J Immunol 190(10), 5306–5312 (2013)
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