In vitro Modeling of the Effect of Lactobacillus Metabolites on the Systemic Response of the Body in Intestinal Viral Infection

Authors

DOI:

https://doi.org/10.20535/ibb.2024.8.2.306587

Keywords:

probiotic, lactobacillus, viral gastroenteritis, interferon, inflammatory factor, proliferation

Abstract

Background. Viral infectious diseases remain a significant cause of morbidity and mortality worldwide. The lack of effective antiviral drugs for the treatment of viral gastroenteritis emphasizes the relevance of various forms of combination therapy, including a balanced diet and the use of probiotics.

Objective. To verify in vitro the hypothesis about the effect of metabolites from probiotic strains of lactobacilli on the systemic response of the body in intestinal viral infection.

Methods. The objects of study were filtrates of culture fluids from probiotic lactobacillus strains L. delbrueckii subsp. lactis LE and L. rhamnosus LB3. HEp-2 and Namalwa cell cultures and vesicular stomatitis test virus were used as biological test objects. The study employed spectrophotometric and cytofluorometric analysis.

Results. The absence of a direct anti-inflammatory effect in the samples of lactobacillus culture fluid filtrates was revealed. It was found that the culture fluid filtrate of the lactobacillus strain L. delbrueckii subsp. lactis LE exhibited the most pronounced properties of an interferon coinducer. The proliferative index (PI) of HEp-2 cells was analyzed under different effects. Cells incubated with lactobacillus culture fluid filtrate (LE) showed an increase in PI for young cells, a decrease for mid-mature cells, and an increase for late-mature cells. The combined effect of TNF-a and lactobacillus LE culture filtrate was characterized by stimulation of PI for medium-mature cells and significant inhibition of PI of late-mature cells.

Conclusions. The synergistic effect of lactobacillus culture filtrates and inflammatory factors will contribute to the accelerated elimination of late-mature and affected cells from the intestine and stimulate the proliferation of young and medium-mature cells to replace them, thereby promoting the regeneration of the intestinal epithelium and accelerate recovery. At the same time, probiotic strains of lactobacilli can enhance the interferonogenic properties of gastroenteritis viruses, and ultimately stimulating the formation of specific immunity in these diseases.

References

Villena J, Shimosato T, Vizoso-Pinto MG, Kitazawa H. Editorial: nutrition, immunity and viral infections. Front Nutr. 2020;7:125. DOI: 10.3389/fnut.2020.00125

Lehtoranta L, Latvala S, Lehtinen MJ. Role of probiotics in stimulating the immune system in viral respiratory tract infections: a narrative review. Nutrients. 2020;12(10):3163. DOI: 10.3390/nu12103163

Betthäuser BA, Bach-Mortensen AM, Engzell P. A systematic review and meta-analysis of the evidence on learning during the COVID-19 pandemic. Nat Hum Behav. 2023;7(3):375-85. DOI: 10.1038/s41562-022-01506-4

Soloviov SO, Todosiichuk TS, Kovaliuk OV, Filippelli GM, Trokhymenko OP, Dziublyk IV, et al. Rotaviruses and noroviruses as etiological agents of acute intestinal diseases of ukrainian children. Int J Environ Res Public Health. 2022;19(8):4660. DOI: 10.3390/ijerph19084660

Dennehy PH. Viral gastroenteritis in children. Pediatr Infect Dis J. 2011;30(1):63-4. DOI: 10.1097/inf.0b013e3182059102

Bányai K, Estes MK, Martella V, Parashar UD. Viral gastroenteritis. Lancet. 2018;392(10142):175-86. DOI: 10.1016/s0140-6736(18)31128-0

Kanauchi O, Andoh A, AbuBakar S, Yamamoto N. Probiotics and paraprobiotics in viral infection: clinical application and effects on the innate and acquired immune systems. Curr Pharm Des. 2018;24(6):710-7. DOI: 10.2174/1381612824666180116163411

Lopez-Santamarina A, Miranda JM, Mondragon AD, Lamas A, Cardelle-Cobas A, Franco CM, et al. Potential use of marine seaweeds as prebiotics: a review. Molecules. 2020;25(4):1004. DOI: 10.3390/molecules25041004

Colbère-Garapin F, Martin-Latil S, Blondel B, Mousson L, Pelletier I, Autret A, et al. Prevention and treatment of enteric viral infections: possible benefits of probiotic bacteria. Microbes Infect. 2007;9(14-15):1623-31. DOI: 10.1016/j.micinf.2007.09.016

Libertucci J, Young VB. The role of the microbiota in infectious diseases. Nat Microbiol. 2019;4(1):35-45. DOI: 10.1038/s41564-018-0278-4

Probiotics in food: health and nutritional properties and guidelines for evaluation. Rome: World Health Organization, Food and Agriculture Organization of the United Nations; 2006. 56 p. Available at: https://www.fao.org/3/a0512e/a0512e.pdf

Ishizuka T, Kanmani P, Kobayashi H, Miyazaki A, Soma J, Suda Y, et al. Immunobiotic bifidobacteria strains modulate rotavirus immune response in porcine intestinal epitheliocytes via pattern recognition receptor signaling. Plos One. 2016;11(3):e0152416. DOI: 10.1371/journal.pone.0152416

Maragkoudakis PA, Chingwaru W, Gradisnik L, Tsakalidou E, Cencic A. Lactic acid bacteria efficiently protect human and animal intestinal epithelial and immune cells from enteric virus infection. Int J Food Microbiol. 2010;141 Suppl 1:91-7. DOI: 10.1016/j.ijfoodmicro.2009.12.024

Cristofori F, Dargenio VN, Dargenio C, Miniello VL, Barone M, Francavilla R. Anti-Inflammatory and immunomodulatory effects of probiotics in gut inflammation: a door to the body. Front Immunol. 2021;12:578386. DOI: 10.3389/fimmu.2021.578386

Grandy G, Medina M, Soria R, Terán CG, Araya M. Probiotics in the treatment of acute rotavirus diarrhoea. A randomized, double-blind, controlled trial using two different probiotic preparations in Bolivian children. BMC Infect Dis. 2010;10(1):253. DOI: 10.1186/1471-2334-10-253

Kotzampassi K, Giamarellos-Bourboulis EJ. Probiotics for infectious diseases: more drugs, less dietary supplementation. Int J Antimicrob Agents. 2012;40(4):288-96. DOI: 10.1016/j.ijantimicag.2012.06.006

Lee DK, Park JE, Kim MJ, Seo JG, Lee JH, Ha NJ. Probiotic bacteria, B. longum and L. acidophilus inhibit infection by rotavirus in vitro and decrease the duration of diarrhea in pediatric patients. Clin Res Hepatol Gastroenterol. 2015;39(2):237-44. DOI: 10.1016/j.clinre.2014.09.006

Olaya Galán NN, Ulloa Rubiano JC, Velez Reyes FA, Fernandez Duarte KP, Salas Cárdenas SP, Gutierrez Fernandez MF. In vitro antiviral activity of Lactobacillus casei and Bifidobacterium adolescentis against rotavirus infection monitored by NSP4 protein production. J Appl Microbiol. 2016;120(4):1041-51. DOI: 10.1111/jam.13069

In YW, Kim JJ, Kim HJ, Oh SW. Antimicrobial activities of acetic acid, citric acid and lactic acid against shigella species. J Food Saf. 2013;33(1):79-85. DOI: 10.1111/jfs.12025

Boskey ER, Telsch KM, Whaley KJ, Moench TR, Cone RA. Acid production by vaginal flora in vitro is consistent with the rate and extent of vaginal acidification. Infect Immun. 1999;67(10):5170-5. DOI: 10.1128/iai.67.10.5170-5175.1999

Kwon HJ, Kim HH, Ryu YB, Kim JH, Jeong HJ, Lee SW, et al. In vitro anti-rotavirus activity of polyphenol compounds isolated from the roots of Glycyrrhiza uralensis. Bioorganic Amp Med Chem. 2010;18(21):7668-74. DOI: 10.1016/j.bmc.2010.07.073

Clark KJ, Grant PG, Sarr AB, Belakere JR, Swaggerty CL, Phillips TD, et al. An in vitro study of theaflavins extracted from black tea to neutralize bovine rotavirus and bovine coronavirus infections. Vet Microbiol. 1998;63(2-4):147-57. DOI: 10.1016/s0378-1135(98)00242-9

van der Strate BW, Beljaars L, Molema G, Harmsen MC, Meijer DK. Antiviral activities of lactoferrin. Antivir Res. 2001;52(3):225-39. DOI: 10.1016/s0166-3542(01)00195-4

Superti F, Ammendolia MG, Valenti P, Seganti L. Antirotaviral activity of milk proteins: lactoferrin prevents rotavirus infection in the enterocyte-like cell line HT-29. Med Microbiol Immunol. 1997;186(2-3):83-91. DOI: 10.1007/s004300050049

Inagaki M, Muranishi H, Yamada K, Kakehi K, Uchida K, Suzuki T, et al. Bovine κ-casein inhibits human rotavirus (HRV) infection via direct binding of glycans to HRV. J Dairy Sci. 2014;97(5):2653-61. DOI: 10.3168/jds.2013-7792 24612801

Qureshi H, Saeed S, Ahmed S, Rasool SA. Coliphage hsa as a model for antiviral studies/spectrum by some indigenous bacteriocin like inhibitory substances (BLIS). Pak J Pharm Sci. 2006;19(3):182-5.

Saeed S, Rasool SA, Ahmad S, Zaidi SZ, Rehmani S. Antiviral activity of staphylococcin 188: A purified bacteriocin like inhibitory substance isolated from staphylococcus aureus AB188. Res J Microbiol. 2007;2(11):796-806. DOI: 10.3923/jm.2007.796.806

Todorov SD, Wachsman M, Tomé E, Dousset X, Destro MT, Dicks LM, et al. Characterisation of an antiviral pediocin-like bacteriocin produced by Enterococcus faecium. Food Microbiol. 2010;27(7):869-79. DOI: 10.1016/j.fm.2010.05.001

Brown AC, Valiere A. Probiotics and medical nutrition therapy. Nutr Clin Care. 2004;7(2):56-68.

Osunsanmi FO, Yotwana L, Mosa RA, Liu AL, Gao L, Du GH, et al. In vitro antiviral, antioxidant and in vivo antipyretic activity of three South Africa medicinal plants crude extracts. Boletin Latinoam Del Caribe Plantas Medicinales Aromat. 2022;21(5):620-30. DOI: 10.37360/blacpma.22.21.5.38

Fryer HJ, Davis GE, Manthorpe M, Varon S. Lowry protein assay using an automatic microtiter plate spectrophotometer. Anal Biochem. 1986;153(2):262-6. DOI: 10.1016/0003-2697(86)90090-4

Cell Proliferation Kit I (MTT) [Internet]. ROCHE – eLabDoc [cited 2024 Jan 9]. Available from: https://elabdoc-prod.roche.com/LifeScience/Document/319a443d-d6ed-e311-98a1-00215a9b0ba8

Terefe EM, Okalebo FA, Derese S, Muriuki J, Batiha GE. In vitro cytotoxicity and anti-hiv activity of crude extracts of croton macrostachyus, croton megalocarpus and croton dichogamus. J Exp Pharmacol. 2021;13:971-9. DOI: 10.2147/jep.s335104

Bulychev LE, Goncharova EP, Ryzhikov AB, Masycheva VI, P'iankova OG, Pliasunov IV, et al. Dynamics of interferon induction in albino mice by interferon inducer ridostin administered by various routes. Antibiot i Khimioterapiia. 1998;43(4):20-3.

Junior N. Lipoxygenase activity determination [Internet]. protocols.io; 2020 [cited 2024 Jan 9]. DOI: 10.17504/protocols.io.bhqmj5u6. Available from: https://dx.doi.org/10.17504/protocols.io.bhqmj5u6

Kim Y, Kim DM, Kim JY. Ginger extract suppresses inflammatory response and maintains barrier function in human colonic epithelial caco-2 cells exposed to inflammatory mediators. J Food Sci. 2017;82(5):1264-70. DOI: 10.1111/1750-3841.13695

Arjmand B, Goodarzi P, Aghayan HR, Payab M, Rahim F, Alavi-Moghadam S, et al. Co-transplantation of human fetal mesenchymal and hematopoietic stem cells in type 1 diabetic mice model. Front Endocrinol. 2019;10:761. DOI: 10.3389/fendo.2019.00761

Geiss G, Jin G, Guo J, Bumgarner R, Katze MG, Sen GC. A comprehensive view of regulation of gene expression by double-stranded RNA-mediated cell signaling. J Biol Chem. 2001;276(32):30178-82. DOI: 10.1074/jbc.c100137200

Lazar A, Reuveny S, Traub A, Minai M, Grosfeld H, Feinstein S, et al. Factors affecting the large scale production of human lymphoblastoid interferon. Dev Biol Stand. 1981;50:167-71.

Cho H, Kelsall BL. The role of type I interferons in intestinal infection, homeostasis, and inflammation. Immunol Rev. 2014;260(1):145-67. DOI: 10.1111/imr.12195

Wells JM. Immunomodulatory mechanisms of lactobacilli. Microb Cell Fact. 2011;10(Suppl 1):17. DOI: 10.1186/1475-2859-10-s1-s17

Kole A, He J, Rivollier A, Silveira DD, Kitamura K, Maloy KJ, et al. Type I IFNs regulate effector and regulatory T cell accumulation and anti-inflammatory cytokine production during T cell-mediated colitis. J Immunol. 2013;191(5):2771-9. DOI: 10.4049/jimmunol.1301093

Parameswaran N, Patial S. Tumor necrosis factor-α signaling in macrophages. Crit Rev Eukaryot Gene Expr. 2010;20(2):87-103. DOI: 10.1615/CritRevEukarGeneExpr.v20.i2.10

Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J, Parashar UD. 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect Dis. 2012;12(2):136-41. DOI: 10.1016/s1473-3099(11)70253-5

Hakim MS, Ding S, Chen S, Yin Y, Su J, van der Woude CJ, et al. TNF-α exerts potent anti-rotavirus effects via the activation of classical NF-κB pathway. Virus Res. 2018;253:28-37. DOI: 10.1016/j.virusres.2018.05.022

Yu TH, Tsai CN, Lai MW, Chen CC, Chao HC, Lin CW, et al. Antigenemia and cytokine expression in rotavirus gastroenteritis in children. J Microbiol Immunol Infect. 2012;45(4):265-70. DOI: 10.1016/j.jmii.2011.11.013

Published

2024-06-21

How to Cite

1.
Soloviov S, Trokhimenko O, Polishchuk V, Pits V, Vasylenko V, Vasylenko Y, Hol I, Symchuk A, Kostiuk O. In vitro Modeling of the Effect of Lactobacillus Metabolites on the Systemic Response of the Body in Intestinal Viral Infection. Innov Biosyst Bioeng [Internet]. 2024Jun.21 [cited 2024Dec.24];8(2):38-52. Available from: https://ibb.kpi.ua/article/view/306587

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