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Germ‐free mice exhibit mast cells with impaired functionality and gut homing and do not develop food allergy

Schwarzer, Martin, Hermanova, Petra, Srutkova, Dagmar, Golias, Jaroslav, Hudcovic, Tomas, Zwicker, Christian, Sinkora, Marek, Akgün, Johnnie, Wiedermann, Ursula, Tuckova, Ludmila, Kozakova, Hana, Schabussova, Irma·2019·Frontiers in Immunology
DOI 10.3389/fimmu.2019.00205PMC PMC6379318

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Figure 1 Germ-free mice fail to develop symptoms of OVA-induced food allergy. (A) Experimental design: conventional (CV) and germ-free (GF) mice were sensitized twice within a two-week interval by intraperitoneal (i.p.) injection of 60 μg OVA in Al(OH)3 (alum) followed by intragastric gavage (i.g.) with 15 mg OVA in PBS 8 times within 17 days (OVA groups). Age-matched control mice were injected with PBS/alum and gavaged by PBS (ctrl groups). After the last i.g. exposure, rectal temperature was assessed and mice were sacrificed by cervical dislocation. Sera and small intestine samples were collected for further analysis. Graphic art was created in freely available professional vector graphics editor Inkscape 0.92 (https://inkscape.org/). (B) The occurrence of diarrhea was monitored for 60 min after each i.g. administration in control CV (gray squares), control GF (open squares), in OVA-treated CV (black circles), and OVA-treated GF (open circles) mice. (C) The diarrhea score was assessed according to the scoring method described in Material and Methods section. (D) Representative pictures of CV/OVA and GF/OVA mice after the last i.g. OVA exposure. (E) The rectal temperature was measured 30 min after the last i.g. exposure at day 44 of the experiment in CV/ctrl (gray bars), and GF/ctrl (dashed bars) control mice, and in CV/OVA (black bars) and GF/OVA (white bars) OVA-treated mice. Difference in the temperature before and after challenge is shown. Data are plotted as mean values ± SEM. Pooled values of at least two independent experiments (CV/ctrl n = 8, CV/OVA n = 14, GF/ctrl n = 9, GF/OVA n = 11 mice per group) are shown. **P ≤ 0.01, ****P ≤ 0.0001.
Figure 1 Germ-free mice fail to develop symptoms of OVA-induced food allergy. (A) Experimental design: conventional (CV) and germ-free (GF) mice were sensitized twice within a two-week interval by intraperitoneal (i.p.) injection of 60 μg OVA in Al(OH)3 (alum) followed by intragastric gavage (i.g.) with 15 mg OVA in PBS 8 times within 17 days (OVA groups). Age-matched control mice were injected with PBS/alum and gavaged by PBS (ctrl groups). After the last i.g. exposure, rectal temperature was assessed and mice were sacrificed by cervical dislocation. Sera and small intestine samples were collected for further analysis. Graphic art was created in freely available professional vector graphics editor Inkscape 0.92 (https://inkscape.org/). (B) The occurrence of diarrhea was monitored for 60 min after each i.g. administration in control CV (gray squares), control GF (open squares), in OVA-treated CV (black circles), and OVA-treated GF (open circles) mice. (C) The diarrhea score was assessed according to the scoring method described in Material and Methods section. (D) Representative pictures of CV/OVA and GF/OVA mice after the last i.g. OVA exposure. (E) The rectal temperature was measured 30 min after the last i.g. exposure at day 44 of the experiment in CV/ctrl (gray bars), and GF/ctrl (dashed bars) control mice, and in CV/OVA (black bars) and GF/OVA (white bars) OVA-treated mice. Difference in the temperature before and after challenge is shown. Data are plotted as mean values ± SEM. Pooled values of at least two independent experiments (CV/ctrl n = 8, CV/OVA n = 14, GF/ctrl n = 9, GF/OVA n = 11 mice per group) are shown. **P ≤ 0.01, ****P ≤ 0.0001.CC BY · PubMed Central
Figure 2 Impact of bacterial colonization on the levels of OVA-specific antibodies in sera and on OVA-induced cytokine production in splenocytes. Levels of OVA-specific antibodies were measured in sera of control CV (gray bars) and GF (dashed bars) mice, and sera of OVA-treated CV (black bars), and GF (white bars) mice. (A) Functional IgE in serum was measured by OVA-mediated β-hexosaminidase release from rat basophil leukemia cells (RBL). OVA-specific (B) IgE, (C), IgG1, (D), IgG2a, and (E), IgA were measured by ELISA and expressed as optical density (OD). Levels of (F), IFN-γ, (G), IL-4, (H), IL-5, (I), IL-13, and (J), IL-10 in splenocyte culture supernatants were measured by MILLIPLEX Cytokine panel. Cytokine levels are expressed after subtraction of base line levels of unstimulated splenocytes. Data are plotted as mean values ± SEM. Pooled values of at least two independent experiments (CV/ctrl n = 8, CV/OVA n = 14, GF/ctrl n = 9, GF/OVA n = 11 mice per group) are shown. *P ≤ 0.05, **P ≤ 0.01.
Figure 2 Impact of bacterial colonization on the levels of OVA-specific antibodies in sera and on OVA-induced cytokine production in splenocytes. Levels of OVA-specific antibodies were measured in sera of control CV (gray bars) and GF (dashed bars) mice, and sera of OVA-treated CV (black bars), and GF (white bars) mice. (A) Functional IgE in serum was measured by OVA-mediated β-hexosaminidase release from rat basophil leukemia cells (RBL). OVA-specific (B) IgE, (C), IgG1, (D), IgG2a, and (E), IgA were measured by ELISA and expressed as optical density (OD). Levels of (F), IFN-γ, (G), IL-4, (H), IL-5, (I), IL-13, and (J), IL-10 in splenocyte culture supernatants were measured by MILLIPLEX Cytokine panel. Cytokine levels are expressed after subtraction of base line levels of unstimulated splenocytes. Data are plotted as mean values ± SEM. Pooled values of at least two independent experiments (CV/ctrl n = 8, CV/OVA n = 14, GF/ctrl n = 9, GF/OVA n = 11 mice per group) are shown. *P ≤ 0.05, **P ≤ 0.01.CC BY · PubMed Central
Figure 3 Germ-free mice exhibit low numbers of intestinal mast cells, low expression of Cxcr2 and its ligands, and low levels of Mast cell protease-1 after OVA-sensitization and challenge. (A) Histological staining of jejunal sections for mastocytosis by hematoxylin/pararosaniline was performed on samples from control conventional (CV/ctrl) and germ-free (GF/ctrl), and from OVA-treated CV (CV/OVA) and germ-free (GF/OVA) mice (scale bars, 100 μm; inset scale bars, 25 μm) (B), Quantification of mast cells per villus in jejunal sections (CV/ctrl n = 3, CV/OVA n = 8, GF/ctrl n = 5, GF/OVA n = 5 mice per group). Messenger RNA expression of (C), Cxcr2 (D), Cxcl1, and (E), Cxcl2 (in the jejunal tissues was determined by real-time PCR. Relative expression to β-actin is shown (CV/ctrl n = 6, CV/OVA n = 7, GF/ctrl n = 6, GF/OVA n = 5 mice per group). Mast cell protease-1 (MCPT-1) levels were determined in (F), jejunal homogenates and in (G), sera of control conventional (CV; gray bars) and germ-free (GF; dashed bars) mice, and in OVA-treated CV (black bars), and GF (white bars) mice by ELISA. Data are plotted as mean values ± SEM. Pooled values of at least two independent experiments (CV/ctrl n = 8, CV/OVA n = 14, GF/ctrl n = 9, GF/OVA n = 11 mice per group) are shown. *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, ****P ≤ 0.0001.
Figure 3 Germ-free mice exhibit low numbers of intestinal mast cells, low expression of Cxcr2 and its ligands, and low levels of Mast cell protease-1 after OVA-sensitization and challenge. (A) Histological staining of jejunal sections for mastocytosis by hematoxylin/pararosaniline was performed on samples from control conventional (CV/ctrl) and germ-free (GF/ctrl), and from OVA-treated CV (CV/OVA) and germ-free (GF/OVA) mice (scale bars, 100 μm; inset scale bars, 25 μm) (B), Quantification of mast cells per villus in jejunal sections (CV/ctrl n = 3, CV/OVA n = 8, GF/ctrl n = 5, GF/OVA n = 5 mice per group). Messenger RNA expression of (C), Cxcr2 (D), Cxcl1, and (E), Cxcl2 (in the jejunal tissues was determined by real-time PCR. Relative expression to β-actin is shown (CV/ctrl n = 6, CV/OVA n = 7, GF/ctrl n = 6, GF/OVA n = 5 mice per group). Mast cell protease-1 (MCPT-1) levels were determined in (F), jejunal homogenates and in (G), sera of control conventional (CV; gray bars) and germ-free (GF; dashed bars) mice, and in OVA-treated CV (black bars), and GF (white bars) mice by ELISA. Data are plotted as mean values ± SEM. Pooled values of at least two independent experiments (CV/ctrl n = 8, CV/OVA n = 14, GF/ctrl n = 9, GF/OVA n = 11 mice per group) are shown. *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, ****P ≤ 0.0001.CC BY · PubMed Central
Figure 4 Germ-free mice have less mature mast cells and these cells are functionally impaired. (A) Messenger RNA expression of Stem cell factor (Scf) in the jejunal tissues was determined by real-time PCR. Relative expression to β-actin is shown. CV/ctrl (gray bars) n = 5, GF/ctrl (dashed bars) n = 6, CV/OVA (black bars) n = 5, GF/OVA (white bars) n = 5 mice per group. (B) Mean fluorescence intensity of CD117 was determined by flow cytometry on CD45+FcεRIα+ cells isolated from small intestine. CV (gray bars) n = 3, GF (dashed bars) n = 3 mice per group. (C) GF and CV mice were injected with degranulation-inducing compound 48/80 or PBS and edema was recorded. Data are presented as paw width after subtraction of baseline values, GF 48/80 (black circles) n = 6, CV 48/80 (open circles) n = 8, GF PBS (open squares) n = 5, CV PBS (gray squares) n = 8 mice per group. Data are plotted as mean values ± SEM. *P ≤ 0.05, **P ≤ 0.01, and ****P ≤ 0.0001.
Figure 4 Germ-free mice have less mature mast cells and these cells are functionally impaired. (A) Messenger RNA expression of Stem cell factor (Scf) in the jejunal tissues was determined by real-time PCR. Relative expression to β-actin is shown. CV/ctrl (gray bars) n = 5, GF/ctrl (dashed bars) n = 6, CV/OVA (black bars) n = 5, GF/OVA (white bars) n = 5 mice per group. (B) Mean fluorescence intensity of CD117 was determined by flow cytometry on CD45+FcεRIα+ cells isolated from small intestine. CV (gray bars) n = 3, GF (dashed bars) n = 3 mice per group. (C) GF and CV mice were injected with degranulation-inducing compound 48/80 or PBS and edema was recorded. Data are presented as paw width after subtraction of baseline values, GF 48/80 (black circles) n = 6, CV 48/80 (open circles) n = 8, GF PBS (open squares) n = 5, CV PBS (gray squares) n = 8 mice per group. Data are plotted as mean values ± SEM. *P ≤ 0.05, **P ≤ 0.01, and ****P ≤ 0.0001.CC BY · PubMed Central
Figure 5 Colonization of germ-free mice by the conventional microbiota but not by single bacterial strain Lactobacillus plantarum WCFS1 restores sensitivity to OVA-induced food allergy. Germ-free (GF) mice were colonized by co-housing with age-matched conventional (CV) animals (exGF group) or mono-associated with the strain L. plantarum WCFS1 (Lp group). At the age of 8 weeks, all groups were submitted to OVA-sensitization and challenge, as described in Figure 1. (A) The occurrence of diarrhea during OVA treatment. (B) The diarrhea score for each group was assessed according to the scoring described in section Materials and Methods section. (C) The rectal temperature was taken 30 min after the last i.g. exposure at day 44. Difference in the temperature before and after challenge is shown. Mast cell protease-1 (MCPT-1) levels were determined in jejunal homogenates (D), and in sera (E), by ELISA. Data are plotted as mean values ± SEM. CV/OVA (n = 8), GF/OVA (n = 5) and pooled values of two independent experiments for exGF/OVA (n = 9) and Lp/OVA (n = 13) colonized mice are shown. *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.01, ****P ≤ 0.0001.
Figure 5 Colonization of germ-free mice by the conventional microbiota but not by single bacterial strain Lactobacillus plantarum WCFS1 restores sensitivity to OVA-induced food allergy. Germ-free (GF) mice were colonized by co-housing with age-matched conventional (CV) animals (exGF group) or mono-associated with the strain L. plantarum WCFS1 (Lp group). At the age of 8 weeks, all groups were submitted to OVA-sensitization and challenge, as described in Figure 1. (A) The occurrence of diarrhea during OVA treatment. (B) The diarrhea score for each group was assessed according to the scoring described in section Materials and Methods section. (C) The rectal temperature was taken 30 min after the last i.g. exposure at day 44. Difference in the temperature before and after challenge is shown. Mast cell protease-1 (MCPT-1) levels were determined in jejunal homogenates (D), and in sera (E), by ELISA. Data are plotted as mean values ± SEM. CV/OVA (n = 8), GF/OVA (n = 5) and pooled values of two independent experiments for exGF/OVA (n = 9) and Lp/OVA (n = 13) colonized mice are shown. *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.01, ****P ≤ 0.0001.CC BY · PubMed Central

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Authors
Schwarzer, M., Hermanova, P., Srutkova, D., Golias, J., Hudcovic, T., Zwicker, C., Sinkora, M., Akgün, J., Wiedermann, U., Tuckova, L., Kozakova, H., & Schabussova, I.
Venue
Frontiers in Immunology
Publisher
Frontiers Media SA
Published
2019-02-12
Volume
10
ISSN
1664-3224
DOI
10.3389/fimmu.2019.00205
PMC
PMC6379318
Cited by
62
References
0
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
  • Grantová Agentura Ceské Republiky (17-09869S, 18-02993S, 18-07015Y)
  • Austrian Science Fund (SFB F46, MCCA)
  • OeAD-GmbH (CZ 16/2012, CZ 15/2015, CZ 16/2016)
  • Ministerstvo Školství, Mládeže a Telovýchovy (7AMB12AT020, 7AMB15AT025)

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