Журнал микробиологии, эпидемиологии и иммунобиологии. 2019; : 105-115
Аkkermansia muciniphila — новый универсальный пробиотик на основе живых комменсальных бактерий кишечника человека: действительность или легенда?
https://doi.org/10.36233/0372-9311-2019-4-105-115Аннотация
В обзоре представлены современные сведения о биологии Аkkermansia muciniphila, комменсального представителя анаэробной кишечной микробиоты, обладающего выраженной муколитической активностью и способного модулировать различные функции, метаболические и сигнальные реакция у здоровых и больных людей. Установленные зарубежными исследователями благоприятные и негативные эффекты связывают с наличием у этих грамотрицательных бактерий специфических поверхностных мембранных белков, продукцией определенных короткоцепочечных жирных кислот, деградацией муцина, изменением барьерной функции кишечника, продукцией эндотоксина, а также синтезом некоторых нейромедиаторов. Рассматриваются перспективы и сложности создания новых микробных нутрицевтиков и лекарственных препаратов на основе живых клеток A. muciniphila или их специфических низкомолекулярных компонентов и метаболитов.
Список литературы
1. Aguirre M. Fermentation of indigestible carbohydrates by the gut microbiota. Dissertation Degree of Doctor, Maastricht University. The Netherlands, 2016.
2. Bansil R., Turner D.S. The biology of mucus: Composition, synthesis and organization. Advanced Drug Delivery Reviews. 2018, 124: 3-15.
3. Burokas A., Arboleya S., Moloney R.D. et al. Targeting the Microbiota-Gut-Brain Axis: Prebiotics Have Anxiolytic and Antidepressant-like Effects and Reverse the Impact of Chronic Stress in Mice. Biol Psychiatry. 2017. Doi:10.1016/j.biopsych. 2016.12.031.
4. Candela M., Rampelli S., Turroni S. et al. Unbalance of intestinal microbiota in atopic children. BMC Microbiol. 2012, 12: 95. doi: 10.1186/1471-2180-12-95.
5. Cani P.D. Human gut microbiome: hopes, threats and promises. Gut, 2018: 1-10. Doi:10.1136/gutjnl-2018-316723.
6. Cani P.D., de Vos W.M. Next-Generation Beneficial Microbes: The Case of Akkermansia muciniphila. Frontiers in Microbiology, 2017,8,1765. http://journal.frontiersin.org/article/10.3389/fmicb.2017.01765/full.
7. Cekanaviciute E., Yoo B.B., Runia T.F. et al. Gut bacteria from multiple sclerosis patients modulate human T cells and exacerbate symptoms in mouse models. Proc. Natl. Acad. Sci USA. 2017, 114: 10713-10718.
8. de Vos W.M. Microbe Profile: Akkermansia muciniphila: a conserved intestinal symbiont that acts as the gatekeeper of our mucosa. Micobiology. 2017, 163: 646-648.
9. De la Cuesta-Zuluaga J., Mueller N.T., Corrales-Agudelo V. et al. Metformin is associated with higher relative abundance of mucin-degrading A. muciniphila and short-chain fatty acid producing microbiota in the gut. Diabetes Care. 2017, 40: 54-62.
10. Derrien M., Belzer C., de Vos W.M. Akkermansia muciniphila and its role in regulating host functions. Microbial Patjgenesis, 2016. http://dx.doi.org/10.1016/j.micpath.2016.02.005.
11. Derrien M., Van Baarlen P., Hooiveld G. et al. Modulation of mucosal immune response, tolerantce, and proliferation in mice colonized by the mucin-degrader Akkermansia muciniphila. Front. Microbiol. 2011, 2: 166. Doi: 10.3389/fmicb.2011.00166.
12. Derrien M., Vaughan E.E., Plugge C.M., de Vos W.M. Akkermansia muciniphila gen.nov., sp.nov., a human intestinal mucin-degrading bacterium. Int. J. Syst. Evol. Microbiol. 2004, 54(Pt 5): 1469-1476.
13. Everard A., Belzer C., Geurts L.et al. Crosstalk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. USA. 2013,110: 9066-9071.
14. Geerlings S.Y., Kostopoulos I., de Vos W.M., Belzer C. Akkermansia muciniphila in the Human Gastrointestinal Tract: When, Where, and How? Microorganisms. 2018, 6(3), 75. doi:10.3390/microorganisms6030075.
15. Gуmez-Gallego C., Pohl S., Salminen S. et al. Akkermansia muciniphila: a novel functional microbe with probiotic properties. Benef. Microbes. 2016; 7: 571-584.
16. Grander C., Adolph T.E., Wieser V. et al. Recovery of ethanol-induced Akkermansia muciniphila depletion ameliorates alcoholic liver disease. Gut. 2018, 67(5): 891-901.
17. Guo X., Li S., Zhang J.et al. Genome sequencing of 39 Akkermansia muciniphila isolates reveals its population structure, genomic and functional diverisity, and global distribution in mammalian gut microbiotas. BMC Genomics. 2017,18(1): 800. Doi: 10.1186/s12864-017-4195-3.
18. Hänninen A., Toivonen R., Pöysti S. et al. Akkermansia muciniphila induces gut microbiota remodelling and controls islet autoimmunity in NOD mice. Gut. 2017: gutjnl-2017-314508. Doi:10.1136/gutjnl-2017-314508.
19. Hansson G.C. Role of mucus layers in gut infection and inflammation. Curr. Opin. Microbiol. 2012; 15: 57-62.
20. Henning S.M., Summanen P.H., Lee R-R. et al. Pomegranate ellagitannins stimulate the growth of Akkermansia muciniphila in vivo. Anaerobe. 2017, 43: 56-60
21. Hur K.Y., Lee M.S. Gut Microbiota and Metabolic Disorders, Diabetes. Metab. J. 2015, 39: 198-203.
22. Kolmede C.A., de Vos W.M. Gut health and the personal microbiome. In: Nutrigenomics and Proteomics in Health and Disease. 2017, John Wiley & Sons, Ltd. 201-219.
23. Li S.S., Zhu A., Benes V. et al. Durable coexistence of donor and recipient strains after fecal microbiota transplantation. Science. 2016, 352: 586-589.
24. Li J., Zhao F., Wang Y. et al. Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome. 2017, 5:14. Doi: 10.1186/s40168-016-0222-x.
25. Mithieux G. Does Akkermansia muciniphila play a role in type 1 diabetes? Gut. 2018: gutjnl-2017-315732.
26. Naito Y., Uchiyama K., Takagi T. A next-generation beneficial microbe: Akkermansia muciniphila. J. Clin. Biochem. Nutr. 2018, 63(1): 33-35.
27. Ottman N., Davids M., Suarez-Diez M. et al. Genome-Scale Model and Omics Analysis of Metabolic Capacities of Akkermansia muciniphila Reveal a Preferential Mucin-Degrading Lifestyle. Appl. Environ. Microbiol. 2017, 83(18). pii: e01014-17. doi: 10.1128/AEM.01014-17.
28. Ottman N., Geerlings S.Y., Aalvink S. et al. C. Action and function of Akkermansia muciniphila in microbiome ecology, health and disease. Best Practice &Research Clinical Gastroenterology. 2017, 31: 637-642.
29. Ouwerkerk J.P., van der Ark R.C., Davids M. et al. Adaptation of Akkermansia muciniphila to the oxicanoxic interface of the mucus layer. Appl. Environ. Microbiol. 2016. doi:1o.1128/AEM.o1641-16k.
30. Parker E.P.K., Praharaj I., John J. et al. Changes in the intestinal microbiota following the administration of azithromycin in a randomized placebo-controlled trial among infants in south India. Scientific Reports. 2017; 7: 9168. DOI: 10.1038/s41598-017-06862-0.
31. Plovier H., Everard A., Druart C. et al. A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nature Med. 2017, 23: 107-113.
32. Qin J., Li Y., Cai Z. et al. Ametagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012, 490: 55-60.
33. Rajilic-Stojanovic M., de Vos W. M. The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiol. Rev. 2014, 38: 996-1047.
34. Rajilic-Stojanovic M., Guarner F., Shanahan F., de Vos W.M. Phylogenetic analysis of dysbiosis in ulcerative colitis during remission. Infiamm. Bowel. Dis. 2013,19: 481-488.
35. Ritari J., Salojarvi J., Lahti L., de Vos W.M. Improved taxonomic assignment of human intestinal 16S rRNA sequences by a dedicated reference database. BMC Genomics. 2015, 16: 1056. Doi: 10.1186/s12864-015-2265-y.
36. Romanн-Pérez M., Agusti A., Sanz Y. Innovation in microbiome-based strategies for promoting metabolic health. Curr. Opin. Clin. Nutr. Metab. Care. 2017, 20: 1-91.
37. Roopchand D.E., Carmody R.N., Kuhn P. et al. Dietary Polyphenols Promote Growth of the Gut Bacterium Akkermansia muciniphila and Attenuate High-Fat Diet-Induced Metabolic Syndrome, Diabetes. 2015, 64: 2847-2858.
38. Shin N.R., Lee J.C., Lee H.Y. et al. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut. 2014, 63:727-735.
39. Sommer F., Backhed F. The gut microbiota—masters of host development and physiology. Nat. Rev. Microbiol. 2013, 11(4): 227-238.
40. Sonoyama K., Ogasawara T., Goto H. et al. Comparison of gut microbiota and allergic reactions in BALB/c mice fed different cultivars of rice. Br. J. Nutr. 2010, 103: 218-226.
41. Swidsinski A., Dorffel Y., Loening-Baucke V. et al. Acute appendicitis is characterised by local invasion with Fusobacterium nucleatum/necrophorum. Gut. 2011, 60: 34-40.
42. Tailford L.E., Crost E.H., Kavanaugh D., Juge N. Mucin glycan foraging in the human gut microbiome. Front. Genet. 2015, 6: 81. Doi: 10.3389/fgene.2015.00081.
43. Tan L., Zhao S., Zhu W. et al. The Akkermansia muciniphila is a gut microbiota signature in psoriasis. Exp. Dermatol. 2018, 27(2): 144-114.
44. Van der Ark K.C.H. Metabolic characterization and viable delivery of Akkermansia muciniphila for its future application. PhD thesis, Wageningen University, Wageningen, the Netherlands. 2018. DOI: 10.18174/427507.
45. Van Passel M.W.J., Kant R., Zoetendal E. The Genome of Akkermansia muciniphila, a Dedicated Intestinal Mucin Degrader, and Its Use in Exploring Intestinal Metagenomes. PLoS ONE. 2011, 6(3): e16876. Doi: 10.1371/journal.pone.0016876.
46. Wang X., Wang J., Rao B., Deng L. Gut flora profiling and fecal metabolite composition of colorectal cancer patients and healthy individuals, Exp. Ther. Med. 2017, 3: 2848-2854.
47. Wang L., Christophersen C.T., Sorich M.J. et al. Low relative abundances of the mucolytic bacterium Akkermansia muciniphila and Bifidobacterium spp. in feces of children with autism. Appl. Environ. Microbiol. 2011, 77: 6718-6721.
48. Weir T.L., Manter D.K., Sheflin A.M. et al. Stool Microbiome and Metabolome Differences between Colorectal Cancer Patients and Healthy Adults. PLoS One. 2013, 8: e70803. https://doi.org/10.1371/journal.pone.0070803.
49. Zhang Y.J., Li S., Gan R.Y. et al. Impacts of gut bacteria on human health and diseases. Int. J. Mol. Sci. 2015, 16: 7493-7519.
50. Zhou K. Strategies to promote abundance of Akkermansia muciniphila, an emerging probiotics in the gut, evidence from dietary intervention studies. J. Functionl. Foods. 2017, 33: 194-201.
Journal of microbiology, epidemiology and immunobiology. 2019; : 105-115
Akkermansia muciniphila is a new universal probiotic on the basis of live human commensal gut bacteria: the reality or legend?
https://doi.org/10.36233/0372-9311-2019-4-105-115Abstract
Contemporary information on biology of Akkermansia muciniphila and the role of these gut mucolytic anaerobic bacteria in physiological functions, metabolic and signaling reactions in human health and diseases are presented in the review. Established by foreign researchers, favorable and negative effects are associated with the presence in these gram-negative bacteria specific surface membrane proteins, the production of certain short-chain fatty acids and endotoxin, as well as with the ability degrading mucin, changing intestinal barrier function and synthesizing some neurotransmitters. Prospects and difficulties of creation of new microbial nutraceuticals and drugs on the basis of living cells of A. muciniphila or their specific low-molecular components and metabolites are considered.
References
1. Aguirre M. Fermentation of indigestible carbohydrates by the gut microbiota. Dissertation Degree of Doctor, Maastricht University. The Netherlands, 2016.
2. Bansil R., Turner D.S. The biology of mucus: Composition, synthesis and organization. Advanced Drug Delivery Reviews. 2018, 124: 3-15.
3. Burokas A., Arboleya S., Moloney R.D. et al. Targeting the Microbiota-Gut-Brain Axis: Prebiotics Have Anxiolytic and Antidepressant-like Effects and Reverse the Impact of Chronic Stress in Mice. Biol Psychiatry. 2017. Doi:10.1016/j.biopsych. 2016.12.031.
4. Candela M., Rampelli S., Turroni S. et al. Unbalance of intestinal microbiota in atopic children. BMC Microbiol. 2012, 12: 95. doi: 10.1186/1471-2180-12-95.
5. Cani P.D. Human gut microbiome: hopes, threats and promises. Gut, 2018: 1-10. Doi:10.1136/gutjnl-2018-316723.
6. Cani P.D., de Vos W.M. Next-Generation Beneficial Microbes: The Case of Akkermansia muciniphila. Frontiers in Microbiology, 2017,8,1765. http://journal.frontiersin.org/article/10.3389/fmicb.2017.01765/full.
7. Cekanaviciute E., Yoo B.B., Runia T.F. et al. Gut bacteria from multiple sclerosis patients modulate human T cells and exacerbate symptoms in mouse models. Proc. Natl. Acad. Sci USA. 2017, 114: 10713-10718.
8. de Vos W.M. Microbe Profile: Akkermansia muciniphila: a conserved intestinal symbiont that acts as the gatekeeper of our mucosa. Micobiology. 2017, 163: 646-648.
9. De la Cuesta-Zuluaga J., Mueller N.T., Corrales-Agudelo V. et al. Metformin is associated with higher relative abundance of mucin-degrading A. muciniphila and short-chain fatty acid producing microbiota in the gut. Diabetes Care. 2017, 40: 54-62.
10. Derrien M., Belzer C., de Vos W.M. Akkermansia muciniphila and its role in regulating host functions. Microbial Patjgenesis, 2016. http://dx.doi.org/10.1016/j.micpath.2016.02.005.
11. Derrien M., Van Baarlen P., Hooiveld G. et al. Modulation of mucosal immune response, tolerantce, and proliferation in mice colonized by the mucin-degrader Akkermansia muciniphila. Front. Microbiol. 2011, 2: 166. Doi: 10.3389/fmicb.2011.00166.
12. Derrien M., Vaughan E.E., Plugge C.M., de Vos W.M. Akkermansia muciniphila gen.nov., sp.nov., a human intestinal mucin-degrading bacterium. Int. J. Syst. Evol. Microbiol. 2004, 54(Pt 5): 1469-1476.
13. Everard A., Belzer C., Geurts L.et al. Crosstalk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. USA. 2013,110: 9066-9071.
14. Geerlings S.Y., Kostopoulos I., de Vos W.M., Belzer C. Akkermansia muciniphila in the Human Gastrointestinal Tract: When, Where, and How? Microorganisms. 2018, 6(3), 75. doi:10.3390/microorganisms6030075.
15. Gumez-Gallego C., Pohl S., Salminen S. et al. Akkermansia muciniphila: a novel functional microbe with probiotic properties. Benef. Microbes. 2016; 7: 571-584.
16. Grander C., Adolph T.E., Wieser V. et al. Recovery of ethanol-induced Akkermansia muciniphila depletion ameliorates alcoholic liver disease. Gut. 2018, 67(5): 891-901.
17. Guo X., Li S., Zhang J.et al. Genome sequencing of 39 Akkermansia muciniphila isolates reveals its population structure, genomic and functional diverisity, and global distribution in mammalian gut microbiotas. BMC Genomics. 2017,18(1): 800. Doi: 10.1186/s12864-017-4195-3.
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21. Hur K.Y., Lee M.S. Gut Microbiota and Metabolic Disorders, Diabetes. Metab. J. 2015, 39: 198-203.
22. Kolmede C.A., de Vos W.M. Gut health and the personal microbiome. In: Nutrigenomics and Proteomics in Health and Disease. 2017, John Wiley & Sons, Ltd. 201-219.
23. Li S.S., Zhu A., Benes V. et al. Durable coexistence of donor and recipient strains after fecal microbiota transplantation. Science. 2016, 352: 586-589.
24. Li J., Zhao F., Wang Y. et al. Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome. 2017, 5:14. Doi: 10.1186/s40168-016-0222-x.
25. Mithieux G. Does Akkermansia muciniphila play a role in type 1 diabetes? Gut. 2018: gutjnl-2017-315732.
26. Naito Y., Uchiyama K., Takagi T. A next-generation beneficial microbe: Akkermansia muciniphila. J. Clin. Biochem. Nutr. 2018, 63(1): 33-35.
27. Ottman N., Davids M., Suarez-Diez M. et al. Genome-Scale Model and Omics Analysis of Metabolic Capacities of Akkermansia muciniphila Reveal a Preferential Mucin-Degrading Lifestyle. Appl. Environ. Microbiol. 2017, 83(18). pii: e01014-17. doi: 10.1128/AEM.01014-17.
28. Ottman N., Geerlings S.Y., Aalvink S. et al. C. Action and function of Akkermansia muciniphila in microbiome ecology, health and disease. Best Practice &Research Clinical Gastroenterology. 2017, 31: 637-642.
29. Ouwerkerk J.P., van der Ark R.C., Davids M. et al. Adaptation of Akkermansia muciniphila to the oxicanoxic interface of the mucus layer. Appl. Environ. Microbiol. 2016. doi:1o.1128/AEM.o1641-16k.
30. Parker E.P.K., Praharaj I., John J. et al. Changes in the intestinal microbiota following the administration of azithromycin in a randomized placebo-controlled trial among infants in south India. Scientific Reports. 2017; 7: 9168. DOI: 10.1038/s41598-017-06862-0.
31. Plovier H., Everard A., Druart C. et al. A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nature Med. 2017, 23: 107-113.
32. Qin J., Li Y., Cai Z. et al. Ametagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012, 490: 55-60.
33. Rajilic-Stojanovic M., de Vos W. M. The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiol. Rev. 2014, 38: 996-1047.
34. Rajilic-Stojanovic M., Guarner F., Shanahan F., de Vos W.M. Phylogenetic analysis of dysbiosis in ulcerative colitis during remission. Infiamm. Bowel. Dis. 2013,19: 481-488.
35. Ritari J., Salojarvi J., Lahti L., de Vos W.M. Improved taxonomic assignment of human intestinal 16S rRNA sequences by a dedicated reference database. BMC Genomics. 2015, 16: 1056. Doi: 10.1186/s12864-015-2265-y.
36. Romann-Pérez M., Agusti A., Sanz Y. Innovation in microbiome-based strategies for promoting metabolic health. Curr. Opin. Clin. Nutr. Metab. Care. 2017, 20: 1-91.
37. Roopchand D.E., Carmody R.N., Kuhn P. et al. Dietary Polyphenols Promote Growth of the Gut Bacterium Akkermansia muciniphila and Attenuate High-Fat Diet-Induced Metabolic Syndrome, Diabetes. 2015, 64: 2847-2858.
38. Shin N.R., Lee J.C., Lee H.Y. et al. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut. 2014, 63:727-735.
39. Sommer F., Backhed F. The gut microbiota—masters of host development and physiology. Nat. Rev. Microbiol. 2013, 11(4): 227-238.
40. Sonoyama K., Ogasawara T., Goto H. et al. Comparison of gut microbiota and allergic reactions in BALB/c mice fed different cultivars of rice. Br. J. Nutr. 2010, 103: 218-226.
41. Swidsinski A., Dorffel Y., Loening-Baucke V. et al. Acute appendicitis is characterised by local invasion with Fusobacterium nucleatum/necrophorum. Gut. 2011, 60: 34-40.
42. Tailford L.E., Crost E.H., Kavanaugh D., Juge N. Mucin glycan foraging in the human gut microbiome. Front. Genet. 2015, 6: 81. Doi: 10.3389/fgene.2015.00081.
43. Tan L., Zhao S., Zhu W. et al. The Akkermansia muciniphila is a gut microbiota signature in psoriasis. Exp. Dermatol. 2018, 27(2): 144-114.
44. Van der Ark K.C.H. Metabolic characterization and viable delivery of Akkermansia muciniphila for its future application. PhD thesis, Wageningen University, Wageningen, the Netherlands. 2018. DOI: 10.18174/427507.
45. Van Passel M.W.J., Kant R., Zoetendal E. The Genome of Akkermansia muciniphila, a Dedicated Intestinal Mucin Degrader, and Its Use in Exploring Intestinal Metagenomes. PLoS ONE. 2011, 6(3): e16876. Doi: 10.1371/journal.pone.0016876.
46. Wang X., Wang J., Rao B., Deng L. Gut flora profiling and fecal metabolite composition of colorectal cancer patients and healthy individuals, Exp. Ther. Med. 2017, 3: 2848-2854.
47. Wang L., Christophersen C.T., Sorich M.J. et al. Low relative abundances of the mucolytic bacterium Akkermansia muciniphila and Bifidobacterium spp. in feces of children with autism. Appl. Environ. Microbiol. 2011, 77: 6718-6721.
48. Weir T.L., Manter D.K., Sheflin A.M. et al. Stool Microbiome and Metabolome Differences between Colorectal Cancer Patients and Healthy Adults. PLoS One. 2013, 8: e70803. https://doi.org/10.1371/journal.pone.0070803.
49. Zhang Y.J., Li S., Gan R.Y. et al. Impacts of gut bacteria on human health and diseases. Int. J. Mol. Sci. 2015, 16: 7493-7519.
50. Zhou K. Strategies to promote abundance of Akkermansia muciniphila, an emerging probiotics in the gut, evidence from dietary intervention studies. J. Functionl. Foods. 2017, 33: 194-201.
