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Pediococcus pentosaceus MIANGUAN Enhances the Immune Response to Vaccination in Mice

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Abstract

Increasing evidence shows that some probiotics can improve vaccine responses as adjuvants. This study aimed to evaluate the effect of Pediococcus pentosaceus MIANGUAN (PPM) on SARS-CoV-2 vaccine-elicited immune response in mice. Six-week-old female ICR mice were primed and boosted with SARS-CoV-2 vaccine intramuscularly at weeks 0 and 4, respectively. Mice were gavaged with PPM (5 × 109 CFU/mouse) or PBS (control) for 3 days immediately after boosting vaccination. Compared to the control, oral PPM administration resulted in significantly higher levels of RBD-specific IgG binding antibodies (> 2.3-fold) and RBD-specific IgG1 binding antibodies (> 4-fold) in the serum. Additionally, PPM-treated mice had higher titers of RBD-specific IgG binding antibodies (> 2.29-fold) and neutralization antibodies (> 1.6-fold) in the lung compared to the control mice. The transcriptional analyses showed that the B cell receptor (BCR) signaling pathway was upregulated in both splenocytes and BAL cells in the PPM group vs. the control group. In addition, the number of IFN-γ-producing splenocytes (mainly in CD4 + T cells as determined by flow cytometry) in response to restimulation of RBD peptides was significantly increased in the PPM group. RNA sequencing showed that the genes associated with T cell activation and maturation and MHC class II pathway (CD4, H2-DMa, H2-DMb1, H2-Oa, Ctss) were upregulated, suggesting that oral administration of PPM may enhance CD4 + T cell responses through MHC class II pathway. Furthermore, PPM administration could downregulate the expression level of proinflammatory genes. To conclude, oral administration of PPM could boost SARS-CoV-2 vaccine efficacy through enhancing the specific humoral and cellular immunity response and decrease the expression of inflammation pathways.

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Data Availability

The original contributions presented in the study are publicly available. This data can be found in the NCBI SRA database (accession numbers: PRJNA953511).

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Acknowledgements

We thank the member of JGX and ZHR laboratory for advice and assistance during the study. We also thank Dr. Jianqing Xu and Dr. Kangli Cao from Zhongshan Hospital, Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University for SARS-CoV-2 vaccine (DNA-S and AdC68-Delta-S).

Funding

This work was supported by National Key R and D Program of China (2023YFC0871200) and Research Units of Discovery of Unknown Bacteria and Function (2018RU010) to J.G.X.

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Authors and Affiliations

  1. National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Beijing, 102206, China

    Yulu Chen, Zhijie Cao, Simin Lu, Zhihuan Wang, Caiyun Ma, Mengshan Chen, Jing Yang, Zhihong Ren & Jianguo Xu

  2. Research Unite for Unknown Microbe, Chinese Academy of Medical Sciences, Institute of Pathogen Biology, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing, 100730, China

    Simin Lu

  3. Department of Epidemiology, School of Public Health, Shanxi Medical University, Taiyuan, 030001, China

    Caiyun Ma

  4. Infection Management Office, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250021, China

    Gui Zhang

  5. Institute of Public Health, Nankai University, Tianjin, 300071, China

    Mengshan Chen & Jianguo Xu

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Contributions

JGX and ZHR conceived and designed the experiments. YLC conducted animal experiments and prepared the paper. ZJC constructed screening system of immunobiotics in vitro. SML, ZHW, and CYM assisted in animal study and ELISA. GZ isolated the PPM. MSC and JY analyzed data. All authors contributed to the article and approved the submitted version.

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Correspondence to Zhihong Ren or Jianguo Xu.

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The protocol for animal study was reviewed and approved by the Laboratory Animal Welfare and Ethics Committee of the National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Prevention and Control.

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Chen, Y., Cao, Z., Lu, S. et al. Pediococcus pentosaceus MIANGUAN Enhances the Immune Response to Vaccination in Mice. Probiotics & Antimicro. Prot. 16, 1117–1129 (2024). https://doi.org/10.1007/s12602-023-10205-z

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