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Schistosoma japonicum-derived peptide SJMHE1 ameliorates allergic symptoms and responses in mice with allergic rhinitis

Gao, Xuerong, Mao, Chaoming, Zheng, Tingting, Xu, Xiaowei, Luo, Xinkai, Zhang, Shan, Liu, Jiameng, Wang, Xuefeng, Chen, Xiaojun, Dong, Liyang·2023·Frontiers in Cellular and Infection Microbiology
DOI 10.3389/fcimb.2023.1143950PMC PMC10279851
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Abstract

Helminth derived excretory/secretory molecules have shown efficacy in the treatment of allergic asthma in mice, but their roles in allergic rhinitis (AR) are little known. In this study, we aimed to determine the intervention effect of SJMHE1, a Schistosoma japonicum derived small molecular peptide, on ovalbumin (OVA)-induced AR mice and investigate its possible mechanism. AR was induced in BALB/c mice, following which the mice were treated with phosphate-buffered saline (PBS), OVA 323-339 and SJMHE1 respectively. SJMHE1 treatment improved clinical symptoms (rubbing and sneezing), suppressed infiltrates of inflammatory cells and eosinophils in nasal mucosa, modulated the production of type-2 (IL-4 and IL-13) and anti-inflammatory (IL-10) cytokines in the nasal lavage fluids (NLF), spleen, and serum. To investigate the underlying mechanism, fluorescein isothiocyanate (FITC)-labeled SJMHE1 was subcutaneously injected into AR mice, and we found that the FITC-SJMHE1 could accumulate in spleen, but not in nasal mucosa. FITC-SJMHE1 mainly bound to CD19 positive cells (B cells), and the SJMHE1 treatment significantly increased the proportion of regulatory B cells (Bregs) and B10 cells, along with the enhancement of PR domain containing protein 1 (Prdm1) protein levels. SJMHE1 may alleviate AR by upregulating Bregs, and has great potential as a new avenue for the AR treatment.

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Figure 1 Experimental protocol for the development of allergic rhinitis and treatment with SJMHE1. BALB/c mice were sensitized with OVA and aluminum hydroxide in PBS on days 0, 7 and 14 by intraperitoneal injection (i.p.). Subsequently, the sensitized mice were challenged intranasally with OVA daily from days 21 to 27 and 29 to 35. PBS, emulsified OVA323-339 or SJMHE1 with incomplete Freund’s adjuvant were subcutaneously (inner thigh) injected into mice on days 0, 14 and 28. The mice were sacrificed on day 36 and the samples were collected.
Figure 1 Experimental protocol for the development of allergic rhinitis and treatment with SJMHE1. BALB/c mice were sensitized with OVA and aluminum hydroxide in PBS on days 0, 7 and 14 by intraperitoneal injection (i.p.). Subsequently, the sensitized mice were challenged intranasally with OVA daily from days 21 to 27 and 29 to 35. PBS, emulsified OVA323-339 or SJMHE1 with incomplete Freund’s adjuvant were subcutaneously (inner thigh) injected into mice on days 0, 14 and 28. The mice were sacrificed on day 36 and the samples were collected.CC BY · PubMed Central
Figure 2 SJMHE1 treatment inhibits nasal rubbing and sneezes in allergic mice. The number of nasal rubbing (A) and sneezes movements (B) was counted for 20 min immediately after the last nasal challenge. Data are presented as mean ± SD (n = 11) from three independent experiments. Each dot represents data from one animal. (C) Representative image showing nasal external skin lesion induced by scratching. One-way analysis of variance (Tukey Kramer post hoc tests): **P<0.01, ***P<0.001.
Figure 2 SJMHE1 treatment inhibits nasal rubbing and sneezes in allergic mice. The number of nasal rubbing (A) and sneezes movements (B) was counted for 20 min immediately after the last nasal challenge. Data are presented as mean ± SD (n = 11) from three independent experiments. Each dot represents data from one animal. (C) Representative image showing nasal external skin lesion induced by scratching. One-way analysis of variance (Tukey Kramer post hoc tests): **P<0.01, ***P<0.001.CC BY · PubMed Central
Figure 3 SJMHE1 treatment inhibits the development of nasal mucosa inflammation in allergic mice. (A) Representative photographs of HE-stained nasal mucosa sections from each group. 20× magnification. (B) Histological analysis of nasal mucosa from mice by Wright-Giemsa staining. 100× magnification. Representative images are showed. (C) The number of eosinophils in nasal mucosa was measured microscopically. Data are presented as mean ± SD (n = 11) from three independent experiments. Each dot represents data from one animal. One-way analysis of variance (Tukey Kramer post hoc tests): ***P<0.001.
Figure 3 SJMHE1 treatment inhibits the development of nasal mucosa inflammation in allergic mice. (A) Representative photographs of HE-stained nasal mucosa sections from each group. 20× magnification. (B) Histological analysis of nasal mucosa from mice by Wright-Giemsa staining. 100× magnification. Representative images are showed. (C) The number of eosinophils in nasal mucosa was measured microscopically. Data are presented as mean ± SD (n = 11) from three independent experiments. Each dot represents data from one animal. One-way analysis of variance (Tukey Kramer post hoc tests): ***P<0.001.CC BY · PubMed Central
Figure 4 SJMHE1 treatment modulates the expression of cytokines in nasal lavage fluid (NLF) of allergic mice. On day 36, the mice were killed, and the NLF from each mouse was tested by ELISA. Statistical analysis of IL-4 (A), IL-13 (B) and IL-10 (C) levels in the NLF. Data are presented as mean ± SD (n = 9-11) from three independent experiments. Each dot represents data from one animal. One-way analysis of variance (Tukey Kramer post hoc tests): *P<0.05, **P<0.01, ***P<0.001.
Figure 4 SJMHE1 treatment modulates the expression of cytokines in nasal lavage fluid (NLF) of allergic mice. On day 36, the mice were killed, and the NLF from each mouse was tested by ELISA. Statistical analysis of IL-4 (A), IL-13 (B) and IL-10 (C) levels in the NLF. Data are presented as mean ± SD (n = 9-11) from three independent experiments. Each dot represents data from one animal. One-way analysis of variance (Tukey Kramer post hoc tests): *P<0.05, **P<0.01, ***P<0.001.CC BY · PubMed Central
Figure 5 SJMHE1 accumulates in spleen and regulates the systemic immune response in AR mice. (A) Immunofluorescence of FITC-SJMHE1 (green) in nasal mucosa and spleen of mice at day 3, 7, and 14 after FITC-SJMHE1 treatment. Quantitative analysis for relative IL-4 (B), IL-13 (C) and IL-10 (D) genes expression in the spleen of mice. Data are presented as mean ± SD (n = 11) from two independent experiments. Each dot represents data from one animal. (E–G) Statistical analysis of IL-4, IL-13 and IL-10 levels in the serum, respectively. Data are presented as mean ± SD (n = 11) from three independent experiments. Each dot represents data from one animal. (H) OVA-specific IgE level in serum of mice. Data are presented as mean ± SD (n = 11) from three independent experiments. Each dot represents data from one animal. One-way analysis of variance (Tukey Kramer post hoc tests): *P<0.05, **P<0.01, ***P<0.001.
Figure 5 SJMHE1 accumulates in spleen and regulates the systemic immune response in AR mice. (A) Immunofluorescence of FITC-SJMHE1 (green) in nasal mucosa and spleen of mice at day 3, 7, and 14 after FITC-SJMHE1 treatment. Quantitative analysis for relative IL-4 (B), IL-13 (C) and IL-10 (D) genes expression in the spleen of mice. Data are presented as mean ± SD (n = 11) from two independent experiments. Each dot represents data from one animal. (E–G) Statistical analysis of IL-4, IL-13 and IL-10 levels in the serum, respectively. Data are presented as mean ± SD (n = 11) from three independent experiments. Each dot represents data from one animal. (H) OVA-specific IgE level in serum of mice. Data are presented as mean ± SD (n = 11) from three independent experiments. Each dot represents data from one animal. One-way analysis of variance (Tukey Kramer post hoc tests): *P<0.05, **P<0.01, ***P<0.001.CC BY · PubMed Central
Figure 6 SJMHE1 binds to B cells in the spleen and upregulates the ratio of Bregs and B10 cells. (A) The percentages of CD4+FITC+ cells, CD19+FITC+ cells, CD11c+FITC+ cells and F4/80+FITC+ cells in spleen were analyzed by flow cytometry, and (B) percentage of CD19+ cells is shown (n = 3-5). (C) Splenocytes from mice were enriched for CD19+ cells using a flow cytometry sorter. (D) Gene expression profiles of the PBS and SJMHE1 groups were clustered in an unsupervised hierarchical manner. The heat map of differentially expressed genes identified by clustering analysis is shown in the figure. Each column represents a sample and each row represents a gene. Red and blue colors indicate genes with up- and down-regulated expression, respectively. (E) Dot plot shows 454 significantly differentially expressed (P < 0.05 and |log2FC| > 1) genes with 292 downregulated and 162 upregulated in the SJMHE1 group. FC: fold change. (F) Real-time PCR analysis of Hspa1a and Hspa1b mRNA levels in CD19+ B cells isolated from mouse splenocytes (n = 3). (G, H) Percentages of CD19+IL-10+ cells. Data are presented as mean ± SD (n = 9-11) from three independent experiments. Each dot represents data from one animal. (I, J) IL-10+ B-cell frequencies gated on CD1dhiCD5+ (n = 3-5). (K) Prmd1 expression in spleen of mice was detected by Western blotting (n = 2-3). One-way analysis of variance (Tukey Kramer post hoc tests) and Student’s t test: **P<0.01, ***P<0.001.
Figure 6 SJMHE1 binds to B cells in the spleen and upregulates the ratio of Bregs and B10 cells. (A) The percentages of CD4+FITC+ cells, CD19+FITC+ cells, CD11c+FITC+ cells and F4/80+FITC+ cells in spleen were analyzed by flow cytometry, and (B) percentage of CD19+ cells is shown (n = 3-5). (C) Splenocytes from mice were enriched for CD19+ cells using a flow cytometry sorter. (D) Gene expression profiles of the PBS and SJMHE1 groups were clustered in an unsupervised hierarchical manner. The heat map of differentially expressed genes identified by clustering analysis is shown in the figure. Each column represents a sample and each row represents a gene. Red and blue colors indicate genes with up- and down-regulated expression, respectively. (E) Dot plot shows 454 significantly differentially expressed (P < 0.05 and |log2FC| > 1) genes with 292 downregulated and 162 upregulated in the SJMHE1 group. FC: fold change. (F) Real-time PCR analysis of Hspa1a and Hspa1b mRNA levels in CD19+ B cells isolated from mouse splenocytes (n = 3). (G, H) Percentages of CD19+IL-10+ cells. Data are presented as mean ± SD (n = 9-11) from three independent experiments. Each dot represents data from one animal. (I, J) IL-10+ B-cell frequencies gated on CD1dhiCD5+ (n = 3-5). (K) Prmd1 expression in spleen of mice was detected by Western blotting (n = 2-3). One-way analysis of variance (Tukey Kramer post hoc tests) and Student’s t test: **P<0.01, ***P<0.001.CC BY · PubMed Central
Figure 7 Breg cells can be generated in vitro by direct interaction with SJMHE1. (A, B) Splenic B cells from naïve mice were cultured for 24 h with SJMHE1 (0.5 μg/ml), OVA323-339 (0.5 μg/ml), or medium. Intracellular IL-10 expression of total B cells after addition of PMA/ionomycin and monenisn to the last 4 hours of the culture was determined by flow cytometry. Data are presented as mean ± SD (n = 9) from three independent experiments. (C) Splenic B cells from naïve mice were cultured with SJMHE1 (0.5 μg/ml) for 24 hours, and the protein levels of IL-10 in the supernatant were detected by ELISA. Data are presented as mean ± SD (n = 6) from two independent experiments. One-way analysis of variance (Tukey Kramer post hoc tests): ***P<0.001.
Figure 7 Breg cells can be generated in vitro by direct interaction with SJMHE1. (A, B) Splenic B cells from naïve mice were cultured for 24 h with SJMHE1 (0.5 μg/ml), OVA323-339 (0.5 μg/ml), or medium. Intracellular IL-10 expression of total B cells after addition of PMA/ionomycin and monenisn to the last 4 hours of the culture was determined by flow cytometry. Data are presented as mean ± SD (n = 9) from three independent experiments. (C) Splenic B cells from naïve mice were cultured with SJMHE1 (0.5 μg/ml) for 24 hours, and the protein levels of IL-10 in the supernatant were detected by ELISA. Data are presented as mean ± SD (n = 6) from two independent experiments. One-way analysis of variance (Tukey Kramer post hoc tests): ***P<0.001.CC BY · PubMed Central
Figure 8 Biocompatibility evaluation of SJMHE1. (A) Schematic diagram for SJMHE1 treatment. (B) HE staining. (C) Body weight of mice. (D, E) The indicators reflecting the physiological functions of the liver (ALT and AST) and kidneys (CREA and UREA) were tested. Each dot represents data from one animal, and data are presented as mean ± SD (n = 10) from three independent experiments. Student’ s t test.
Figure 8 Biocompatibility evaluation of SJMHE1. (A) Schematic diagram for SJMHE1 treatment. (B) HE staining. (C) Body weight of mice. (D, E) The indicators reflecting the physiological functions of the liver (ALT and AST) and kidneys (CREA and UREA) were tested. Each dot represents data from one animal, and data are presented as mean ± SD (n = 10) from three independent experiments. Student’ s t test.CC BY · PubMed Central

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Authors
Gao, X., Mao, C., Zheng, T., Xu, X., Luo, X., Zhang, S., Liu, J., Wang, X., Chen, X., & Dong, L.
Venue
Frontiers in Cellular and Infection Microbiology
Publisher
Frontiers Media SA
Published
2023-06-06
Volume
13
ISSN
2235-2988
DOI
10.3389/fcimb.2023.1143950
PMC
PMC10279851
Cited by
10
References
3
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
National Natural Science Foundation of China

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CoChat. (2026). Citation check: Schistosoma japonicum-derived peptide SJMHE1 ameliorates allergic symptoms and responses in mice with allergic rhinitis. https://app.cochat.ai/papers/10.3389/fcimb.2023.1143950
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Gao, X., Mao, C., Zheng, T., Xu, X., Luo, X., Zhang, S., Liu, J., Wang, X., Chen, X., & Dong, L. (2023). Schistosoma japonicum-derived peptide SJMHE1 ameliorates allergic symptoms and responses in mice with allergic rhinitis. Frontiers in Cellular and Infection Microbiology. https://doi.org/10.3389/fcimb.2023.1143950