Gut-liver axis: physeology through the prism of the microbiome
https://doi.org/10.29235/1814-6023-2022-19-4-413-423
Abstract
This paper presents a brief historical description of the evolution of views on the development of the concept of the gut liver axis functioning and its physiological aspects. The “new virtual human organ” physiological fundamentals and their role in the pathogenesis of chronic liver diseases, including late post-transplant period, are described and discussed.
Based on own experience, results of a new generation sequencing describing the characteristics of the microbiome palette in patients suffering from chronic liver diseases of various etiologies are presented. Personal study was based on 12 patients suffering chronic liver disease, who were examined before and after liver transplantation. The obtained results indicate the importance of the intestinal microbiome in the natural process of recovery after liver transplantation.
About the Authors
U. R. Salimov
Minsk Scientific Practical Center of Surgery, Transplantology and Hematology
Belarus
Belarus
Umid R. Salimov – Ph. D. (Med.), Doctoral student, Minsk Scientific and Practical Center of Surgery, Transplantology and Hematology.
8, Semashko Str., 220045, Minsk
I. O. Stoma
Gomel State Medical University
Belarus
Belarus
Igor O. Stoma – D. Sc. (Med.), Professor, Rector, Gomel State Medical University.
5, Lange Str., 246000, Gomel
A. A. Kovalev
Gomel State Medical University
Belarus
Belarus
Aliaksei A. Kovalev ‒ senior lecturer, Gomel State Medical University.
5, Lange Str., 246000, Gomel
A. E. Scherba
Minsk Scientific Practical Center of Surgery, Transplantology and Hematology
Belarus
Belarus
Aliaksei E. Shcherba – D. Sc. (Med.), Deputy Director, Minsk Scientific and Practical Center of Surgery, Transplantology and Hematology.
8, Semashko Str., 220045, Minsk
I. P. Shturich
Minsk Scientific Practical Center of Surgery, Transplantology and Hematology
Belarus
Belarus
Ivan P. Shturich ‒ Ph. D. (Med.), Associate Professor, Head of the Department, Minsk Scientific and Practical Center of Surgery, Transplantology and Hematology.
8, Semashko Str., 220045, Minsk
O. O. Rummo
Minsk Scientific Practical Center of Surgery, Transplantology and Hematology
Belarus
Belarus
Oleg O. Rummo ‒ Academician, D. Sc. (Med.), Professor, Director, Minsk Scientific and Practical Center of Surgery, Transplantology and Hematology.
8, Semashko Str., 220045, Minsk
References
1. Volta U., Bonazzi C., Bianchi F. B., Baldoni А. M., Zoli M., Pisi E. IgA antibodies to dietary antigens in liver cirrhosis. La Ricerca in Clinica e in Laboratorio, 1987, vol. 17, no. 3, pp. 235–242. https://doi.org/10.1007/BF02912537
2. Vajros P., Paolella G., Fasano A. Microbiota and gut-liver axis: their influences on obesity and obesity-related liver disease. Journal of Pediatric Gastroenterology and Nutrition, 2013, vol. 56, no. 5, pp. 461‒468. https://doi.org/10.1097/MPG.0b013e318284abb5
3. Ancona G., Alagna L., Lombardi A., Palomba E., Castelli V., Renisi G. [et al.]. The interplay between gut microbiota and the immune system in liver transplant recipients and its role in infections. Infection and Immunity, 2021, vol. 89, no. 11, p. e0037621. https://doi.org/10.1128/IAI.00376-21
4. Milosevic I., Vujovic A., Barac A., Djelic M., Korac M., Radovanovic Spurnic A. [et al.]. Gut microbiota, and its modulation in the management of liver diseases: a review of the literature. International Journal of Molecular Sciences, 2019, vol. 20, no. 2, p. 395. https://doi.org/10.3390/ijms20020395
5. Tilg H., Burcelin R., Tremaroli V. Liver tissue microbiome in NAFLD: next step in understanding the gut-liver axis? Gut, vol. 69, no. 8, pp. 1373‒1374. https://doi.org/10.1136/gutjnl-2019-320490
6. Solé C., Guilly S., Da Silva K., Llopis M., Le-Chatelier E., Huelin P. [et al.]. Alterations in gut microbiome in cirrhosis as assessed by quantitative metagenomics: relationship with acute-on-chronic liver failure and prognosis. Gastroenterology, vol. 160, no. 1, pp. 206‒218.e13. https://doi.org/10.1053/j.gastro.2020.08.054
7. Lee G.-H. Hepatic encephalopathy in acute-on-chronic liver failure. Hepatology International, vol. 9, no. 4, pp. 520‒526. https://doi.org/10.1007/s12072-015-9626-0
8. Stoma I. O., Karpov I. A. Human microbiome. Minsk, DoktorDizain Publ., 2018. 122 p. (in Russian).
9. Blesl A., Stadlbauer V. The gut-liver axis in cholestatic liver diseases. Nutrients, 2021, vol. 13, no. 3, art. 1018. https://doi.org/10.3390/nu13031018
10. Rey K., Manku S., Enns W., Van Rossum T., Bushell K., Morin R. D., Brinkman F. S. L., Choy J. C. Disruption of the gut microbiota with antibiotics exacerbates acute vascular rejection. Transplantation, 2018, vol. 102, no. 7, pp. 1085‒1095. https://doi.org/10.1097/TP.0000000000002169
11. Pirozzolo I., Li Z., Sepulveda M., Alegre M.-L. Influence of the microbiome on solid organ transplant survival. Journal of Heart and Lung Transplantation, vol. 40, no. 8, pp. 745‒753. https://doi.org/10.1016/j.healun.2021.04.004
12. Albillos A., de Gottardi A., Rescigno M. The gut-liver axis in liver disease: pathophysiological basis for therapy. Journal of Hepatology, 2020, vol. 72, no. 3, pp. 558‒577. https://doi.org/10.1016/j.jhep.2019.10.003
13. Kim S.-I. Bacterial infection after liver transplantation. World Journal of Gastroenterology, 2014, vol. 20, no. 20, pp. 6211‒6220. https://doi.org/10.3748/wjg.v20.i20.6211
14. Brandl K., Kumar V., Eckmann L. Gut-liver axis at the frontier of host-microbial interactions. American Journal of Physiology. Gastrointestinal and Liver Physiology, vol. 312, no. 5, pp. G413‒G419. https://doi.org/10.1152/ajpgi.00361.2016
15. Van der Sluis M., De Koning B. A., De Bruijn A. C., Velcich A., Meijerink J. P., Van Goudoever J. B. [et al.]. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology, 2006, vol. 131, no. 1, pp. 117–129. https://doi.org/10.1053/j.gastro.2006.04.020
16. Bergström J. H., Birchenough G. M. H., Katona G., Schroeder B. O., Schütte A., Ermund A., Johansson M. E. V., Hansson G. C. Gram-positive bacteria are held at a distance in the colon mucus by the lectin-like protein ZG16. Proceedings of the National Academy of Sciences of the United States of America, 2016, vol. 113, no. 48, pp. 13833‒13838. https://doi.org/10.1073/pnas.1611400113
17. Bel S., Pendse M., Wang Y., Li Y., Ruhn K. A., Hassell B., Leal T., Winter S. E., Xavier R. J., Hooper L. V. Paneth cells secrete lysozyme via secretory autophagy during bacterial infection of the intestine. Science, 2017, vol. 357, no. 6355, pp. 1047‒1052. https://doi.org/10.1126/science.aal4677
18. Velcich A., Yang W., Heyer J., Fragale A., Nicholas C., Viani S., Kucherlapati R., Lipkin M., Yang K., Augenlicht L. Colorectal cancer in mice genetically deficient in the mucin Muc2. Science, 2002, vol. 295, no. 5560, pp. 1726–1729. https://doi.org/10.1126/science.1069094
19. Spadoni I., Fornasa G., Rescigno M. Organ-specific protection mediated by cooperation between vascular and epithelial barriers. Nature Reviews Immunology, 2017, vol. 17, no. 12, pp. 761‒773. https://doi.org/10.1038/nri.2017.100
20. Vaishnava S., Yamamoto M., Severson K. M., Ruhn K. A., Yu X., Koren O., Ley R., Wakeland E. K., Hooper L. V. The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science, 2011, vol. 334, no. 6053, pp. 255‒258. https://doi.org/10.1126/science.1209791
21. Romanque U. P., Uribe M. M., Videla L. A. Molecular mechanisms in liver ischemic-reperfusion injury and ischemic preconditioning. Revista médica de Chile, vol. 133, no. 4, pp. 469‒476. https://doi.org/10.4067/s0034-98872005000400012
22. Suzuki T. Regulation of the intestinal barrier by nutrients: The role of tight junctions. Animal science journal = Nihon chikusan Gakkaihō, vol. 91, no. 1, p. e13357. https://doi.org/10.1111/asj.13357
23. Suzuki T. Regulation of intestinal epithelial permeability by tight junctions. Cellular and molecular life sciences: CMLS, vol. 70, no. 4, pp. 631‒659. https://doi.org/10.1007/s00018-012-1070-x
24. Dokladny K., Zuhl M. N., Moseley P. L. Intestinal epithelial barrier function and tight junction proteins with heat and exercise. Journal of Applied Physiology, 2016, vol. 120, no. 6, pp. 692‒701. https://doi.org/10.1152/japplphysiol.00536.2015
25. Allam-Ndoul B., Castonguay-Paradis S., Veilleux A. Gut microbiota and intestinal trans-epithelial permeability. International Journal of Molecular Sciences, vol. 21, no. 17, p. 6402. https://doi.org/10.3390/ijms21176402
26. Camus C. Complications infectieuses chez le transplanté hépatique. Réanimation, 2014, vol. 23, pp. 317‒326. https://doi.org/10.1007/s13546-014-0888-7
27. Peterson L. W., Artis D. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nature Reviews. Immunology, 2014, vol. 14, no. 3, pp. 141–153. https://doi.org/10.1038/nri3608
28. Moore W. E., Holdeman L. V. Human fecal flora: the normal flora of 20 Japanese-Hawaiians. Applied Microbiology, 1974, vol. 27, no. 5, pp. 961‒979. https://doi.org/10.1128/am.27.5.961-979.1974
29. Yang X., Lu D., Zhuo J., Lin Z., Yang M., Xu X. The gut-liver axis in immune remodeling: new insight into liver diseases. International Journal of Biology Sciences, 2020, vol. 16, no. 13, pp. 2357‒2366. https://doi.org/10.7150/ijbs.46405
30. Doré J., Corthier G. Le microbiote intestinal humain. Gastroentérologie Clinique et Biologique, 2010, vol. 34, suppl. 1, pp. S7‒S15 (in French). https://doi.org/10.1016/S0399-8320(10)70015-4
31. Holdeman L. V., Good I. J., Moore W. E. Human fecal flora: variation in bacterial composition within individuals and a possible effect of emotional stress. Applied and Environmental Microbiology, 1976, vol. 31, no. 3, pp. 359‒375. https://doi. org/10.1128/aem.31.3.359-375.1976
32. Yu L.-X., Schwabe R. F. The gut microbiome and liver cancer: mechanisms and clinical translation. Nature Reviews Gastroenterology and Hepatology, 2017, vol. 14, no. 9, pp. 527–539. https://doi.org/10.1038/nrgastro.2017.72
33. Kim C. H., Park J., Kim M. 2014. Gut microbiota-derived short-chain fatty acids, T cells, and inflammation. Immune Network, 2014, vol. 14, no. 6, pp. 277–288. https://doi.org/10.4110/in.2014.14.6.277
34. Acharya C., Sahingur S. E., Bajaj J. S. Microbiota, cirrhosis, and the emerging oral-gut-liver axis. JCI Insight, vol. 2, no. 19, p. e94416. https://doi.org/10.1172/jci.insight.94416
35. Merritt M. E., Donaldson J. R. Effect of bile salts on the DNA and membrane integrity of enteric bacteria. Journal of Medical Microbiology, 2009, vol. 58, pt. 12, pp. 1533–1541. https://doi.org/10.1099/jmm.0.014092-0
36. Mortha A., Chudnovskiy A., Hashimoto D., Bogunovic M., Spencer S. P., Belkaid Y., Merad M. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science, 2014, vol. 343, no. 6178, art. 1249288. https://doi.org/10.1126/science.1249288
37. Koh Y.-C., Yang G., Lai C.-S., Weerawatanakorn M., Pan M.-H. Chemopreventive effects of phytochemicals and medicines on M1/M2 polarized macrophage role in inflammation-related diseases. International Journal of Molecular Sciences, 2018, vol. 19, no. 8, art. 2208. https://doi.org/10.3390/ijms19082208
38. Llorente C., Schnabl B. Fast-track clearance of bacteria from the liver. Cell Host and Microbe, 2016, vol. 20, no. 1, pp. 1–2. https://doi.org/10.1016/j.chom.2016.06.012
39. Broadley S. P., Plaumann A., Coletti R., Lehmann C., Wanisch A., Seidlmeier A. [et al.]. Dual-track clearance of circulating bacteria balances rapid restoration of blood sterility with induction of adaptive immunity. Cell Host and Microbe, 2016, vol. 20, no. 1, pp. 36–48. https://doi.org/10.1016/j.chom.2016.05.023
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For citations:
Salimov U.R., Stoma I.O., Kovalev A.A., Scherba A.E., Shturich I.P., Rummo O.O. Gut-liver axis: physeology through the prism of the microbiome. Proceedings of the National Academy of Sciences of Belarus, Medical series. 2022;19(4):413-423. (In Russ.) https://doi.org/10.29235/1814-6023-2022-19-4-413-423
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