Effect of microbiota on the physiology of blood-tissue barriers
Main Article Content
Keywords
Tight Junctions, Fatty Acids, Volatiles, Microbiota
Abstract
The tight-junction (TJ) is a highly complex structure that is located in the most apical portion of the basolateral membrane, and is composed of series of proteins, such as; claudins, occludins and proteins of the ZO family. The TJ restricts the passage of potentially harmful substances or microorganisms through the paracellular space and participates importantly in the mecanotransduction and intercellular signaling processes. Although the complex structure of the TJ, allowing it to function as a barrier in various tissues such as the brain-blood-barrier and testicular-blood-barrier, these barriers are prone to changes decreasing its permeability features. The contribution of microbiota in the formation, function and maintenance of TJs in various immunologically privileged niches such as, the gastrointestinal tract, the central nervous system and the testicles, has been recently studied. Nevertheless, it has been demonstrated that certain pathogenic microorganisms are able to disassemble or modify the permeability of the TJs in epithelial-blood barrier. Thereby, it is central to understand the physiological mechanisms of how microbiota could modify the function of the epithelial blood barriers in order to design new therapeutic strategies to ameliorate the harmful effects of many human diseases.
References
1. Vancamelbeke M, Vermeire S. The intestinal barrier:a fundamental role in health and disease. Expert Rev Gastroenterol Hepatol. 2017;11(9):821-34. doi:10.1080/17474124.2017.1343143
2. Hooper LV, Gordon GI. Commensal host-bacterial relationships in the gut. Science. 2001;292:1115-8.
3. Lin L, Zhang J. Role of intestinal microbiota and metabolites on gut homeostasis and human diseases. BMC Immunol. 2017;18(1):2. doi:10.1186/s12865-016-0187
4. Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Reddy DN. Role of the normal gut microbiota. World J Gastroenterol. 2015;21(29):8787-803. doi:10.3748/wjg.v21.i29.8787
5. Van Itallie CM, Anderson JM. Architecture of tight junctions and principles of molecular composition. Semin Cell Dev Biol. 2014;36:157-65. doi:10.1016/j.semcdb.2014.08.011
6. Shen L. Tight junctions on the move:molecular mechanisms for epithelial barrier regulation. Ann N Y Acad Sci. 2012;1258:9-18. doi:10.1111/j.1749-6632.2012.06613.x
7. González-Mariscal L, Betanzos A, Nava P, Jaramillo BE. Tight junction proteins. Prog Biophys Mol Biol. 2003;81(1):1-44.
8. Greenwood-Van Meerveld B, Johnson AC, Grundy D. Gastrointestinal physiology and function. Handb Exp Pharmacol. 2017;239:1-16. doi:10.1007/164_2016_118
9. Hand TW, Vujkovic-Cvijin I, Ridaura IC, Belkaid Y. Linking the microbiota, chronic disease, and the immune system. Trends Endocrinol Metab. 2016;27(12):831-43. doi:10.1016/j.TEM. 2016.08.003
10. Buckley A, Turner JR. Cell biology of tight junction barrier regulation and mucosal disease. Cold Spring Harb Perspect Biol. 2018;10(1):a029314. doi:10.1101/cshperspect.a029314
11. Takiishi T, Fenero CIM, Camera US. Intestinal barrier and gut microbiota:shaping our immune responses throughout life. Tissue Barriers. 2017;5(4):e1373208. doi:10.1080/21688370.2017.1373208
12. Shortt C, Hasselwander O, Meynier A, Nauta A, Fernández-Noriega E, Putz P, et al. Systematic review of the effects of the intestinal microbiota on selected nutrients and non-nutrients. Eur J Nutr. 2018;57(1):25-49. doi:10.1007/s00394-017-1546-4
13. He Y, Wen Q, Yao F, Xu D, Huang Y, Wang J. Gut-lung axis:the microbial contributions and clinical implications. Cry Rev Microbiol. 2017;43(1):81-95. doi:10.1080/1040841X.2016.1176988
14. Quigley EMM. Microbiota-brain-gut axis and neurodegenerative diseases. Curr Neurol Neurosci Rep. 2017;17(12):94.
15. Rowland I, Gibson G, Heinken A, Scott K, Swann J, Thiele I, et al. Gut microbiota functions:metabolism of nutrients and other food components. Eur J Nutr. 2018;57(1):1-24. doi:10.1007/s00394-017-1445-8
16. Zyrek AA, Cichon C, Helms S, Enders C, Sonnenborn U, Schmidt MA. Molecular mechanisms underlying the probiotic effects of Escherichia coli Nissle 1917 involve ZO-2 and PKCzeta redistribution resulting in tight junction and epithelial barrier repair. Cell Microbiol. 2007;9:804-16.
17. Ewaschuk JB, Diaz H, Meddings L, Diederichs B, Dmytrash A, Backer J, et al. Secreted bioactive factors from Bifidobacterium children enhance epithelial cell barrier function. Am J Physiol Gastrointest Liver Physiol. 2008;295:G1025-34.
18. Anderson RC, Cookson AL, McNabb WC, Park Z, McCann MJ, Kelly WJ, et al. Lactobacillus plantarum MB452 enhances the function of the intestinal barrier by increasing the expression levels of genes involved in tight junction formation. BMC Microbiol. 2010;10:316. doi:doi.org/10.1186/1471-2180-10-316
19. Karczewski J, Troost FJ, Konings I, Covers J, Kleerebezem M, Brummer RJ, et al. Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am J Physiol Gastrointest Liver Physiol. 2010;298:G851-9.
20. Qin H, Zhang Z, Hang X, Jiang Y. L. plantarum prevents enteroinvasive Escherichia coli-induced tight junction proteins changes in intestinal epithelial cells. BMC Microbiol. 2009;9:63.
21. Tan J, McKenzie C, Vuillermin PJ, Goverse G, Vinuesa CG, Mebius RE, et al. Dietary fiber and bacterial SCFA enhance oral tolerance and protect against food allergy through diverse cellular pathways. Cell Rep. 2016;15(12):2809-24. doi:10.1016/j.celrep.2016.05.047
22. Llewellyn A, Foey A. Probiotic modulation of innate cell pathogen sensing and signaling events. Nutrients. 2017;9(10):1156. doi:10.3390/nu9101156
23. Álvarez CS, Bay J, Bosch M, Giménez R, BaldomàL. Outer membrane vesicles and soluble factors released by probiotic Escherichia coli Nissle 1917 and commensal ECOR63 enhance barrier function by regulating expression of tight junction proteins in intestinal epithelial cells. Front Microbiol. 2016;7:1981. doi:10.3389/fmicb.2016.01981
24. Keaney J, Campbell M. The dynamic blood-brain barrier. FEBS J. 2015;282:4067-79.
25. Daneman R, Prat A. The blood-brain barrier. Cold Spring Harb Perspect Biol. 2015;7(1):a020412. doi:10.1101/cshperspect.a020412
26. Coureuil M, Lécuyer H, Bourdoulous S, Nassif X. A journey into the brain:insight into how bacterial pathogens cross blood-brain barriers. Nat Rev Microbiol. 2017;15(3):149-59. doi:10.1038/nrmicro.2016.178
27. Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Tóth M, et al. The gut microbiota influences blood-brain barrier permeability in mice. Sci Transl Med. 2014;6(263):263ra158. doi:10.1126/scitranslmed.3009759
28. Logsdon AF, Erickson MA, Rhea EM, Salameh TS, Banks WA. Gut reactions:how the blood-brain barrier connects the microbiome and the brain. Exp Biol Med (Maywood). 2018;243(2):159-65. doi:10.1177/153537 0217743766
29. Wen Q, Tang EI, Gao Y, Jesus TT, Chu DS, Lee WM, et al. Signaling pathways regulating blood-tissue barriers —lesson from the testis. Biochim Biophys Act Biomembr. 2018;1860(1):141-53. doi:10.1016/j.bbamem.2017.04.020
30. Curmudgeon DD, Cheng CY. The mammalian blood-testis barrier:its biology and regulation. Endocr Rev. 2015;36(5):564-91. doi:10.1210/er.2014-1101
31. Al-Asmakh M, Stukenborg JB, Reda A, Anuar F, Strand ML, Hedin L, et al. The gut microbiota and developmental programming of the testis in mice. PLoS One. 2014;9(8):e103809. doi:10.1371/journal.pone.0103809
32. Sánchez-Almaraz R, Martín-Fuentes M, Palma-Milla S, López-Plaza B, Bermejo-López LM, Gómez-Candela C. Fiber-type indication among different pathologies. Nutr Hosp. 2015;31(6):2372-83. doi:10.3305/NH.2015.31.6.9023
33. Fuller S, Beck E, Salman H, Tapsell L. New horizons for the study of dietary fiber and health:a review. Plant Foods Hum Nutr. 2016;71(1):1-12. doi:10.1007/s11130-016-0529-6
34. Kasubuchi M, Hasegawa S, Hiramatsu T, Ichimura A, Kimura I. Dietary gut microbial metabolites, short-chain fatty acids, and host metabolic regulation. Nutrients. 2015;7(4):2839-49. doi:10.3390/nu7042839
35. Yan H, Ajuwon KM. Butyrate modifies intestinal barrier function in IPEC-J2 cells through a selective upregulation of tight junction proteins and activation of the Act signaling pathway. PLoS One. 2017;12(6):0179586. doi:10.1371/journal.pone.0179586
Article Sidebar
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Authors retain their copyright and grant the Revista Médica del IMSS the right of first publication. Articles are distributed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which allows sharing as long as the author and the original source are properly credited.