On probiotic integration in the management of inflammation and the maintenance of the intestinal epithelial barrier’s integrity

Submitted: February 6, 2024
Accepted: May 28, 2024
Published: August 8, 2024
Abstract Views: 144
PDF: 77
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

Inflammatory bowel disease epidemiology has grown dramatically in recent years, particularly in developed and developing Western countries. Many factors, including stress, diet, and medications, cause and exacerbate inflammatory conditions. Inflammation is closely related to the concept of intestinal barrier integrity. When integrity is compromised, toxins and pathogens can enter the bloodstream. In recent years, there has been a growing interest in using probiotic bacteria to prevent or treat a variety of pathologies, including inflammatory bowel disease. Some studies have looked at the effectiveness of multi-strain probiotic supplements in preventing intestinal barrier dysfunction in in vitro models of lipopolysaccharide-induced inflammation. To mimic the intestinal barrier, human colon adenocarcinoma cell lines were established in Transwell co-culture models. The epithelium permeability was assessed by measuring the transepithelial electrical resistance. The expression of individual proteins involved in barrier function was assessed. The immunomodulatory effects of probiotic formulations were studied in both human macrophage cell lines and ex vivo human peripheral blood mononuclear cell-derived macrophages. The intestinal epithelial layer was also interfaced with a human mast cell line. Selected probiotics have demonstrated high potential for use in maintaining intestinal barrier integrity and possessing anti-inflammatory properties.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

Citations

Kuenzig ME, Fung SG, Marderfeld L, et al. Twenty‐first century trends in the global epidemiology of pediatric‐onset inflammatory bowel disease: systematic review. Gastroenterology 2022;162:1147–59.e4. DOI: https://doi.org/10.1053/j.gastro.2021.12.282
Wang R, Li Z, Liu S, et al. Global, regional and national burden of inflammatory bowel disease in 204 countries and territories from 1990 to 2019: a systematic analysis based on the Global Burden of Disease Study 2019. BMJ Open 2023;13:e065186. DOI: https://doi.org/10.1136/bmjopen-2022-065186
Caviglia GP, Garrone A, Bertolino C, et al. Epidemiology of inflammatory bowel diseases: a population study in a healthcare district of north-west Italy. J Clin Med 2023;12:641. DOI: https://doi.org/10.3390/jcm12020641
Heyman MB, Kirschner BS, Gold BD, et al. Children with early-onset inflammatory bowel disease (IBD): analysis of a pediatric IBD consortium registry. J Pediatr 2005;146:35–40. DOI: https://doi.org/10.1016/j.jpeds.2004.08.043
Ghosh S, Whitley CB, Haribabu B, Jala VR. Regulation of intestinal barrier function by microbial metabolites. Cell Mol Gastroenter Hepatol 2021;11:1463-82. DOI: https://doi.org/10.1016/j.jcmgh.2021.02.007
Fucarino A, Burgio S, Paladino L, et al. The Microbiota is not an organ: introducing the muco-microbiotic layer as a novel morphofunctional structure. Anatomia 2022;1:186-203. DOI: https://doi.org/10.3390/anatomia1020019
Barbara G, Barbaro MR, Fuschi D, et al. Inflammatory and microbiota-related regulation of the intestinal epithelial barrier. Front Nutr 2021;8:718356. DOI: https://doi.org/10.3389/fnut.2021.718356
Talapko J, Vcev A, Meštrović T, et al. Homeostasis and dysbiosis of the intestinal microbiota: comparing hallmarks of a healthy state with changes in inflammatory bowel disease. Microorganisms 2022;10:2405. DOI: https://doi.org/10.3390/microorganisms10122405
Wang B, Yao M, Lv L, et al. The human microbiota in health and disease. Engineering 2017;3:71-82. DOI: https://doi.org/10.1016/J.ENG.2017.01.008
Holscher HD. Dietary fiber and prebiotics and the gastrointestinal microbiota. Gut Microbes 2017;8:172-84. DOI: https://doi.org/10.1080/19490976.2017.1290756
Yadav M, Verma MK, Chauhan NS. A review of metabolic potential of human gut microbiome in human nutrition. Arch Microbiol 2018;200:203-17. DOI: https://doi.org/10.1007/s00203-017-1459-x
Silva YP, Bernardi A, Frozza RL. The role of short-chain fatty acids from gut microbiota in gut-brain communication. Front Endocrinol 2020;11:25. DOI: https://doi.org/10.3389/fendo.2020.00025
Soderholm AT, Pedicord VA. Intestinal epithelial cells: at the interface of the microbiota and mucosal immunity. Immunology 2019;158:267-80. DOI: https://doi.org/10.1111/imm.13117
Zhao Q, Maynard CL. Mucus, commensals, and the immune system. Gut Microbes 2022;14:2041342. DOI: https://doi.org/10.1080/19490976.2022.2041342
Frossi B, Mion F, Sibilano R, et al. Is it time for a new classification of mast cells? what do we know about mast cell heterogeneity? Immunol Rev 2018;282:35-46. DOI: https://doi.org/10.1111/imr.12636
Traina G. Mast cells in gut and brain and their potential role as an emerging therapeutic target for neural diseases. Front Cell Neurosci 2019;13:345. DOI: https://doi.org/10.3389/fncel.2019.00345
Traina G. The role of mast cells in the gut and brain. J Integr Neurosci 2021;20:185–96. DOI: https://doi.org/10.31083/j.jin.2021.01.313
Belkaid Y, Hand T W. Role of the microbiota in immunity and inflammation. Cell 2014;157:121–41. DOI: https://doi.org/10.1016/j.cell.2014.03.011
Cammarota G, Ianiro G, Cianci R, et al. The involvement of gut microbiota in inflammatory bowel disease pathogenesis: potential for therapy. Pharmacol Ther 2015;149:191-212. DOI: https://doi.org/10.1016/j.pharmthera.2014.12.006
Sheehan D, Moran C, Shanahan F. The microbiota in inflammatory bowel disease. J Gastroenterol 2015;50:495-507. DOI: https://doi.org/10.1007/s00535-015-1064-1
Conte C, Sichetti M, Traina G. Gut–brain axis: focus on neurodegeneration and mast cells. Appl Sci 2020;10:1828. DOI: https://doi.org/10.3390/app10051828
Cocchi M, Mondo E, Romeo M, Traina G. The inflammatory conspiracy in multiple sclerosis: a crossroads of clues and insights through mast cells, platelets, inflammation, gut microbiota, mood disorders and stem cells. Int J Mol Sci 2022;23:3253. DOI: https://doi.org/10.3390/ijms23063253
Traina G, Cocchi M. Mast cells, astrocytes, arachidonic acid: do they play a role in depression? Appl Sci 2020;10:3455. DOI: https://doi.org/10.3390/app10103455
Foster JA, Rinaman L, Cryan JF Stress & the gut-brain axis: Regulation by the microbiome. Neurobiol stress 2017;7:124-36. DOI: https://doi.org/10.1016/j.ynstr.2017.03.001
Cocchi M, Traina G. Tryptophan and membrane mobility as conditioners and brokers of gut-brain axis in depression. Appl Sci 2020;10:4933. DOI: https://doi.org/10.3390/app10144933
Cussotto S, Sandhu KV, Dinan TG, Cryan JF. The neuroendocrinology of the microbiota-gut-brain axis: a behavioural perspective. Front Neuroendocrinol 2018;51:80-101. DOI: https://doi.org/10.1016/j.yfrne.2018.04.002
Johnson TB, Langin LM, Zhao J, et al. Changes in motor behavior, neuropathology, and gut microbiota of a Batten disease mouse model following administration of acidified drinking water. Sci Rep 2019;9:14962. DOI: https://doi.org/10.1038/s41598-019-51488-z
Traina G, Bernardi R, Cataldo E, et al. In the rat brain acetyl-L-carnitine treatment modulates the expression of genes involved in neuronal ceroid lipofuscinosis. Mol Neurobiol 2008;38:146-52. DOI: https://doi.org/10.1007/s12035-008-8038-8
Cavaliere G, Traina G. Neuroinflammation in the brain and role of intestinal microbiota: an overview of the players. J Integr Neurosci 2023;22:148. DOI: https://doi.org/10.31083/j.jin2206148
Carabotti M, Scirocco A, Maselli MA, Severi C. The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Ann Gastroenterol 2015;28:203-9.
Traina, G. The Connection between gut and lung microbiota, mast cells, platelets and SARS-CoV-2 in the elderly patient. Int J Mol Sci 2022;23:14898. DOI: https://doi.org/10.3390/ijms232314898
Seyedian SS, Nokhostin F, Malamir MD. A review of the diagnosis, prevention, and treatment methods of inflammatory bowel disease. J Med Life 2019;12:113-22. DOI: https://doi.org/10.25122/jml-2018-0075
Qiu P, Ishimoto T, Fu L, et al. The gut microbiota in inflammatory bowel disease. Front Cell Infect Microbiol 2022;12:733992. DOI: https://doi.org/10.3389/fcimb.2022.733992
Vich Vila A, Imhann F, Collij V, et al. Gut microbiota composition and functional changes in inflammatory bowel disease and irritable bowel syndrome. Sci Transl Med 2018;10:eaap8914. DOI: https://doi.org/10.1126/scitranslmed.aap8914
Maynard CL, Elson CO, Hatton RD, Weaver CT. Reciprocal interactions of the intestinal microbiota and immune system. Nature 2012;489:231-41. DOI: https://doi.org/10.1038/nature11551
Wasilewska E, Zlotkowska D, Wroblewska B. Yogurt starter cultures of Streptococcus thermophilus and Lactobacillus bulgaricus ameliorate symptoms and modulate the immune response in a mouse model of dextran sulfate sodium-induced colitis. J Dairy Sci 2019;102:37–53. DOI: https://doi.org/10.3168/jds.2018-14520
Food and Agricultural Organization of the United Nations and World Health Organization. Joint FAO/WHO working group report on drafting guidelines for the evaluation of probiotics in food. Food and Agricultural Organization of the United Nations, 2002.
Grispoldi L, Giglietti R, Traina G et al. How to assess in vitro probiotic viability and the correct use of neutralizing agents. Front Microbiol 2020;11:204. DOI: https://doi.org/10.3389/fmicb.2020.00204
Foligné B, Parayre S, Cheddani R, et al. Immunomodulation properties of multi-species fermented milks. Food Microbiol 2016;53:60–9. DOI: https://doi.org/10.1016/j.fm.2015.04.002
Sichetti M, De Marco S, Pagiotti R, et al. Anti-inflammatory effect of multistrain probiotic formulation (L. rhamnosus, B. lactis, and B. longum). Nutrition 2018;53:95–102. DOI: https://doi.org/10.1016/j.nut.2018.02.005
Chen C-Y, Tsen H-Y, Lin C-L, et al. Oral administration of a combination of select lactic acid bacteria strains to reduce the Salmonella invasion and inflammation of broiler chicks. Poult Sci 2012;91:2139–47. DOI: https://doi.org/10.3382/ps.2012-02237
Bellavia F, Rappa F, Lo Bello M, et al. Lactobacillus casei and Bifidobacterium lactis supplementation reduces tissue damage of intestinal mucosa and liver after 2,4,6-trinitrobenzenesulfonic acid treatment in mice. J Biol Regul Homeost Agents 2014;28:251-61.
De Marco S, Sichetti M, Muradyan D, et al. Probiotic cell-free supernatants exhibited anti-inflammatory and antioxidant activity on human gut epithelial cells and macrophages stimulated with LPS. Evid Based Complement Alternat Med 2018;2018:1756308. DOI: https://doi.org/10.1155/2018/1756308
Gou HZ, Zhang YL, Ren LF, et al. How do intestinal probiotics restore the intestinal barrier? Front Microbiol 2022;13:929346. DOI: https://doi.org/10.3389/fmicb.2022.929346
Monteagudo-Mera A, Rastall RA, Gibson GR, et al. Adhesion mechanisms mediated by probiotics and prebiotics and their potential impact on human health. Appl Microbiol Biotechnol 2019;103:6463–72. DOI: https://doi.org/10.1007/s00253-019-09978-7
Dominici L, Moretti M, Villarini M, et al. In vivo antigenotoxic properties of a commercial probiotic supplement containing Bifidobacteria. Int J Probiotics Prebiotics 2011;6:179–86.
Persichetti E, De Michele A, Codini M, Traina G. Antioxidative capacity of Lactobacillus fermentum LF31 evaluated in vitro by oxygen radical absorbance capacity assay. Nutrition 2014;30:936–8. DOI: https://doi.org/10.1016/j.nut.2013.12.009
Paladino L, Rappa F, Barone R, et al. NF-kB Regulation and the chaperone system mediate restorative effects of the probiotic Lactobacillus fermentum LF31 in the small intestine and cerebellum of mice with ethanol-induced damage. Biology 2023;12:1394. DOI: https://doi.org/10.3390/biology12111394
Khan S, Chousalkar KK. Short-term feeding of probiotics and synbiotics modulates caecal microbiota during Salmonella typhimurium infection but does not reduce shedding and invasion in chickens. Appl Microbiol Biotechnol 2020;104:319–34. DOI: https://doi.org/10.1007/s00253-019-10220-7
Douillard FP, Mora D, Eijlander RT, et al. Comparative genomic analysis of the multispecies probiotic-marketed product VSL# 3. PLoS ONE 2018;13:e0192452. DOI: https://doi.org/10.1371/journal.pone.0192452
Tien M-T, Girardin SE, Regnault B, et al. Anti-inflammatory effect of Lactobacillus casei on Shigella-infected human intestinal epithelial cells. J Immunol 2006;176:1228–37. DOI: https://doi.org/10.4049/jimmunol.176.2.1228
Rutherford ST, Bassler BL. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harbor Perspect Med 2012;2:705–9. DOI: https://doi.org/10.1101/cshperspect.a012427
Di Cagno R, De Angelis M, Limitone A, et al. Cell–cell communication in sourdough lactic acid bacteria: A proteomic study in Lactobacillus sanfranciscensis CB1. Proteomics 2007;7:2430–46. DOI: https://doi.org/10.1002/pmic.200700143
Kumar M, Kissoon-Singh V, Coria AL, et al. Probiotic mixture VSL#3 reduces colonic inflammation and improves intestinal barrier function in Muc2 mucin-deficient mice. Am J Physiol Gastrointest Liver Physiol 2017;312:G34-45. DOI: https://doi.org/10.1152/ajpgi.00298.2016
Traina G, Menchetti L, Rappa F, et al. Probiotic mixture supplementation in the preventive management of trinitrobenzenesulfonic acid-induced inflammation in a murine model. J Biol Regul Homeost Agents 2016;30:895–901.
di Vito R, Conte C, Traina G. A multi-strain probiotic formulation improves intestinal barrier function by the modulation of tight and adherent junction proteins. Cells 2022;11:2617. DOI: https://doi.org/10.3390/cells11162617
di Vito R, Di Mezza A, Conte C, Traina G. The crosstalk between intestinal epithelial cells and mast cells is modulated by the probiotic supplementation in co-culture models. Int J Mol Sci 2023;24:4157. DOI: https://doi.org/10.3390/ijms24044157
Lee SH. Intestinal permeability regulation by tight junction: implication on inflammatory bowel diseases. Intest Res 2015;13:11-8. DOI: https://doi.org/10.5217/ir.2015.13.1.11

How to Cite

Traina, G. (2024). On probiotic integration in the management of inflammation and the maintenance of the intestinal epithelial barrier’s integrity. Journal of Biological Research - Bollettino Della Società Italiana Di Biologia Sperimentale. https://doi.org/10.4081/jbr.2024.12362