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Anti-rotavirus Properties and Mechanisms of Selected Gram-Positive and Gram-Negative Probiotics on Polarized Human Colonic (HT-29) Cells

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Abstract

Probiotics have been investigated to improve the universal rotavirus (RV) vaccination as well as to ameliorate the RV infection. However, underlying mechanisms how probiotics mediate beneficial effects needs more investigation. Thus, in the present study, we used polarized HT-29 cells to assess the anti-RV properties of Gram-positive, (Lactobacillus acidophilus, Lacticaseibacillus rhamnosus GG, and Bifidobacterium subsp. Lactis Bb12) and Gram negative, (Escherichia coli Nissle 1917) probiotics and study their underlying mechanisms. Our results showed that pre-treatment of HT-29 cells for 4 h with probiotics, significantly reduced (p < 0.05) human RV replication and this effect was most pronounced for E. coli Nissle followed by L. acidophilus and L. rhamnosus GG. Strikingly, only pre-treatment with live bacteria or their supernatants demonstrated anti-RV properties. Except Gram negative E. coli Nissle, the Gram-positive probiotics tested did not bind to RV. Ingenuity pathway analysis of tight junction (TJ)- and innate immune-associated genes indicated that E. coli Nissle or E. coli Nissle + RV treatments improved cell–cell adhesion and cell contact, while L. acidophilus or L. acidophilus + RV treatments also activated cell–cell contact but inhibited cell movement functions. RV alone inhibited migration of cells event. Additionally, E. coli Nissle activated pathways such as the innate immune and inflammatory responses via production of TNF, while RV infection activated NK cells and inflammatory responses. In conclusion, E. coli Nissle’s ability to bind RV, modulate expression of TJ events, innate immune and inflammatory responses, via specific upstream regulators may explain superior anti-RV properties of E. coli Nissle. Therefore, prophylactic use of E. coli Nissle might help to reduce the RV disease burden in infants in endemic areas.

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All data generated or analyzed during this study are included in this published article (and in supplementary information files).

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Acknowledgements

Authors thank Dr. Sukumar Kandasamy and Tea Meulia for their technical assistance in performing rotavirus binding assay and electron microscopy imaging, respectively.

Funding

This work was supported by the Bill and Melinda Gates Foundation (OPP 1117467), the NIAID, NIH (R01 A1099451), federal and state funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University and from the NIH Office of Dietary Supplements (ODS) supplemental grant funds.

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  1. Center for Food Animal Health, Ohio Agricultural Research and Development Center, Department of Animal Sciences, Ohio State University, 1680 Madison Avenue, Wooster, OH, 44691, USA

    Anand Kumar, Yosra A. Helmy, Zachary Fritts, Anastasia Vlasova, Linda J. Saif & Gireesh Rajashekara

  2. Group B-10: Biosecurity and Public Health, Bioscience Division, Los Alamos National Lab, Los Alamos, NM, 87545, USA

    Anand Kumar

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Contributions

AK and GR conceptualize the study. AK, YH, and ZF performed the experiments and analyze the data. AK, YH, and ZF prepared the original draft of the manuscript. AK, YH, AV, LS, and GR reviewed and edited the manuscript. All authors have acknowledged the final version of the manuscript.

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Supplementary file1 Fig. S1 Total number of up/down regulated genes at different treatments in comparisons to HT-29 cells basal levels of expression. Fold change cut off value of ± 1.5 was used to count the total number of genes Fig. S2 Ingenuity Pathway Analysis (IPA) predicted TJ cellular functions that are consistently activated and inhibited on E. coli Nissle alone treatment. The networks of differentially expressed genes were algorithmically generated based on their connectivity such that the highly interconnected networks likely represent significant biological function. The Fischer’s exact test was used to calculate a P value for each biological function assigned to a particular network. The name and number of molecules involved are described in table Fig. S3 Ingenuity Pathway Analysis (IPA) predicted TJ cellular functions that are consistently activated and inhibited on L. acidophilus alone treatment. The networks of differentially expressed genes were algorithmically generated based on their connectivity such that the highly interconnected networks likely represent significant biological function. The Fischer’s exact test was used to calculate a P value for each biological function assigned to a particular network. The name and number of molecules involved are described in table Fig. S4 Total number of up/down regulated genes at different treatments in comparisons to HT-29 cells basal levels of expression. Fold change cut off value of ± 1.5 was used to count the total number of genes Fig. S5 Ingenuity Pathway Analysis (IPA) predicted innate cellular functions that are consistently activated and inhibited on E. coli Nissle alone treatment. The networks of differentially expressed genes were algorithmically generated based on their connectivity such that the highly interconnected networks likely represent significant biological function. The Fischer’s exact test was used to calculate a P value for each biological function assigned to a particular network. The name and number of molecules involved are described in table (PDF 4875 KB)

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Kumar, A., Helmy, Y.A., Fritts, Z. et al. Anti-rotavirus Properties and Mechanisms of Selected Gram-Positive and Gram-Negative Probiotics on Polarized Human Colonic (HT-29) Cells. Probiotics & Antimicro. Prot. 15, 107–128 (2023). https://doi.org/10.1007/s12602-021-09884-3

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