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Experimental and Clinical Gastroenterology

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Relationship of the mucin-degrading bacterium Akkermansia muciniphila with colorectal cancer

https://doi.org/10.31146/1682-8658-ecg-178-6-158-165

Abstract

Colorectal cancer is a disease that is far from the last place in the morbidity statistics in the Russian Federation and in the world. Along with well-known risk factors for the development of this pathology, some representatives of the intestinal microbiota are possible to participate in this process. Some studies suggest that Akkermansia muciniphila, a mucin-degrading bacterium, is associated with colorectal cancer development, but other studies cast doubt on this statement. In this review, we describe a series of studies devoted to determining the dependence of colorectal cancer on the amount of A. muciniphila, the relationship of this bacterium with inflammation development as a predictor of oncogenesis, the influence of other representatives of the intestinal microbiota on its function, and also describe one of the possible mechanisms linking the mucin-degraging ability of this bacterium with the development of oncogenesis.

About the Authors

A. M. Karamzin
I. M. Sechenov First Moscow State Medical University (Sechenov University)
Russian Federation

Cand. of Biol. Sci., Associate Professor of the Department of Microbiology, Virology and Immunology,

Moscow



A. V. Ropot
I. M. Sechenov First Moscow State Medical University (Sechenov University)
Russian Federation

student of the International school “Medicine of the Future”,

Moscow



R. E. Boshian
I. M. Sechenov First Moscow State Medical University (Sechenov University)
Russian Federation

Cand. of Med. Sci., Associate Professor of the Department of Microbiology, Virology and Immunology,

Moscow



References

1. Parkin D. M., Bray F., Ferlay J., Pisani P. Global cancer statistics // CA Cancer J Clin. – 2005. – Vol. 55, № 2. – P. 74–108.

2. Kaprin A. D., Starinsky V. V., Petrova G. V. Malignant neoplasms in Russia in 2018 (incidence and mortality). – Moscow: MNII them. P. A. Herzen, a branch of the Federal State Budgetary Institution Scientific Research Center for Radiology, Ministry of Health of Russia, 2019.

3. Chambers W. M., Warren B. F. Jewell D. P., Mortensen N. J. Cancer surveillance in ulcerative colitis // Br J Surg. – 2005. – Vol. 92, № 8. – P. 928–936.

4. Huxley R. R., Ansary–Moghaddam A., Clift on P. et al. The impact of dietary and lifestyle risk factors on risk of colorectal cancer: a quantitative overview of the epidemiological evidence // Int J Cancer. – 2009. – Vol. 125, № 1. – P. 171–180.

5. Larsson S. C., Rafter J., Holmberg L. et al. Red meat consumption and risk of cancers of the proximal colon, distal colon and rectum: the Swedish Mammography Cohort // Int J Cancer. – 2005. – Vol. 113, № 5. – P. 829–834.

6. Slattery M. L. Diet, lifestyle, and colon cancer // Semin Gastrointest Dis. – 2000. – Vol. 11, № 3. – P. 142–146.

7. Cheesman S. E., Neal J. T., Mittge E. et al. Epithelial cell proliferation in the developing zebrafi sh intestine is regulated by the Wnt pathway and microbial signaling via Myd88 // Proc Natl Acad Sci U S A. – 2011. – № 108, Suppl 1. – P. 4570–4577.

8. Dolara P., Caderni G., Salvadori M. et al. Fecal levels of short–chain fatty acids and bile acids as determinants of colonic mucosal cell proliferation in humans // Nutr Cancer. – 2002. – Vol. 42, № 2. – P. 186–190.

9. Stappenbeck T. S., Hooper L. V., Gordon, J. I. De ve lop mental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells // Proc Natl Acad Sci U S A. – 2002. – Vol. 99, № 24. – P. 15451–15455.

10. Rakoff –Nahoum S., Medzhitov R. Regulation of spontaneous intestinal tumorigenesis through the adaptor protein MyD88 // Science. – 2007. – Vol. 317, № 5834. – P. 124–127.

11. 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. – Vol. 54, № 5. – P. 1469–1476.

12. Collado M. C., Derrien M., Isolauri E. et al. Intestinal integrity and Akkermansia muciniphila, a mucin–degrading member of the intestinal microbiota present in infants, adults, and the elderly // Appl Environ Microbiol. – 2007. – Vol. 73, № 23. – P. 7767–7770.

13. Derrien M., Belzer C., de Vos W. M. Akkermansia muciniphila and its role in regulating host functions // Microb Pathog. – 2017. – № 106. – P. 171–181.

14. Ottman N., Geerlings S. Y., Aalvink S. et al. Action and function of Akkermansia muciniphila in microbiome ecology, health and disease // Best Pract Res Clin Gastroenterol. – 2017. – Vol. 31, № 6. – P. 637–642.

15. Weir T. L., Manter D. K., Shefl in A. M. et al. Stool microbiome and metabolome diff erences between colorectal cancer patients and healthy adults // PLoS One. – 2013. – Vol. 8, № 8. – P. e70803.

16. Byrd J. C., Bresalier R. S. Mucins and mucin binding proteins in colorectal cancer // Cancer Metastasis Rev. – 2004. – Vol. 23, № 1–2. – P. 77–99.

17. Lance P. Recent developments in colorectal cancer // J R Coll Physicians Lond. – 1997.–Vol. 31, № 5.–P. 483–487.

18. Sanapareddy N., Legge R. M., Jovov B. et al. Increased rectal microbial richness is associated with the presence of colorectal adenomas in humans // ISME J. – 2012.–Vol. 6, № 10. – P. 1858–1868.

19. Farhana L., Antaki F., Murshed F. et al. Gut microbiome profi ling and colorectal cancer in African Americans and Caucasian Americans // World J Gastrointest Pathophysiol. – 2018. – Vol. 9, № 2. – P. 47–58.

20. Ashktorab H., Kupfer S. S., Brim H., Carethers J. M. Racial Disparity in Gastrointestinal Cancer Risk // Gastroenterology. – 2017. – Vol. 153, № 4. – P. 910–923.

21. Howe C., Kim S. J., Mitchell J. et al. Diff erential expression of tumor–associated genes and altered gut microbiome with decreased Akkermansia muciniphila confer a tumor–preventive microenvironment in intestinal epithelial Pten–deficient mice // Biochim Biophys Acta Mol Basis Dis. – 2018. – Vol. 1864, № 12. – P. 3746–3758.

22. Hsu F., Mao Y. The structure of phosphoinositide phosphatases: Insights into substrate specificity and catalysis // Biochim Biophys Acta. – 2015. – Vol. 1851, № 6. – P. 698–710.

23. Lin P.C., Lin J. K., Lin H. H. et al. A comprehensive analysis of phosphatase and tensin homolog deleted on chromosome 10 (PTEN) loss in colorectal cancer // World J Surg Oncol. – 2015. – № 13. – P. 186.

24. Colakoglu T., Yildirim S., Kayaselcuk F. et al. Clinicopathological significance of PTEN loss and the phosphoinositide 3–kinase/Akt pathway in sporadic colorectal neoplasms: is PTEN loss predictor of local recurrence? // Am J Surg. – 2008. – Vol. 195, № 6. – P. 719–725.

25. Zhou X.P., Loukola A., Salovaara R. et al. PTEN mutational spectra, expression levels, and subcellular localization in microsatellite stable and unstable colorectal cancers // Am J Pathol. – 2002. – Vol. 161, № 2. – P. 439–447.

26. Bohn B.A., Mina S., Krohn A. et al. Altered PTEN function caused by deletion or gene disruption is associated with poor prognosis in rectal but not in colon cancer // Hum Pathol. – 2013. – Vol. 44, № 8. – P. 1524–1533.

27. Choi Y.J., Jung J., Chung H. K. et al. PTEN regulates TLR5–induced intestinal inflammation by controlling Mal/TIRAP recruitment // FASEB J. – 2013. – Vol. 27, № 1. – P. 243–254.

28. Im E., Jung J., Pothoulakis C., Rhee S. H. Disruption of Pten speeds onset and increases severity of spontaneous colitis in Il10(–/–) mice // Gastroenterology. – 2014.–Vol. 147, № 3. – P. 667–679.e10.

29. Langlois M.J., Roy S. A., Auclair B. A. et al. Epithelial phosphatase and tensin homolog regulates intestinal architecture and secretory cell commitment and acts as a modifier gene in neoplasia // FASEB J. – 2009. –Vol. 23, № 6. – P. 1835–1844.

30. Lee D.H., Anderson K. E., Harnack L. J. et al. Heme iron, zinc, alcohol consumption, and colon cancer: Iowa Women’s Health Study // J Natl Cancer Inst. – 2004. – Vol. 96, № 5. – P. 403–407.

31. Balder H.F., Vogel J., Jansen M. C. et al. Heme and chlorophyll intake and risk of colorectal cancer in the Netherlands cohort study // Cancer Epidemiol Biomarkers Prev. – 2006. – Vol. 15, № 4. – P. 717–725.

32. Sesink A.L., Termont D. S., Kleibeuker J. H., Van der Meer R. Red meat and colon cancer: the cytotoxic and hyperproliferative effects of dietary heme // Cancer Res. – 1999. – Vol. 59, № 22. – P. 5704–5709.

33. IJssennagger N., Rijnierse A., de Wit N. et al. Dietary haem stimulates epithelial cell turnover by downregulating feedback inhibitors of proliferation in murine colon // Gut. – 2012. – Vol. 61, № 7. – P. 1041–1049.

34. Kinzler K.W., Vogelstein B. Lessons from hereditary colorectal cancer // Cell. – 1996. –Vol. 87, № 2. –P. 159–170.

35. IJssennagger N., Derrien M., van Doorn G. M. et al. Dietary heme alters microbiota and mucosa of mouse colon without functional changes in host–microbe cross– talk // PLoS One. – 2012. – Vol. 7, № 12. – P. e49868.

36. Ijssennagger N., Rijnierse A., de Wit N. J. et al. Dietary heme induces acute oxidative stress, but delayed cytotoxicity and compensatory hyperproliferation in mouse colon // Carcinogenesis. – 2013. – Vol. 34, № 7. – P. 1628–1635.

37. Ijssennagger N., Belzer C., Hooiveld G. J. et al. Gut microbiota facilitates dietary heme–induced epithelial hyperproliferation by opening the mucus barrier in colon // Proc Natl Acad Sci U S A. – 2015. – Vol. 112, № 32. – P. 10038–10043.

38. Ullman T.A., Itzkowitz S. H. Intestinal inflammation and cancer // Gastroenterology. – 2011. – Vol. 140, № 6. – P. 1807–1816.

39. Eaden J.A., Abrams K. R., Mayberry J. F. The risk of colorectal cancer in ulcerative colitis: a meta–analysis // Gut. – 2001. – Vol. 48, № 4. – P. 526–535.

40. Canavan C., Abrams K. R., Mayberry J. Meta–analysis: colorectal and small bowel cancer risk in patients with Crohn’s disease // Aliment Pharmacol Th er. – 2006.–Vol. 23, № 8. – P. 1097–1104.

41. Earley H., Lennon G., Balfe Á. et al. The abundance of Akkermansia muciniphila and its relationship with sulphated colonic mucins in health and ulcerative colitis // Sci Rep. – 2019. – Vol. 9, № 1. – P. 15683.

42. Png C.W., Lindén S. K., Gilshenan K. S. et al. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria // Am J Gastroenterol. – 2010. – Vol. 105, № 11. – P. 2420–2428.

43. Zhou X., Chen C., Zhong Y. N. et al. Effect and mechanism of vitamin D on the development of colorectal cancer based on intestinal flora disorder // J Gastroenterol Hepatol. – 2019. – Опубликовано онлайн до печати.

44. Jenab M., Bueno–de–Mesquita H.B., Ferrari P. et al. Association between pre–diagnostic circulating vitamin D concentration and risk of colorectal cancer in European populations: a nested case–control study // BMJ. – 2010. – Vol. 340, № b5500.

45. De Robertis M., Massi E., Poeta M. L. et al. The AOM/ DSS murine model for the study of colon carcinogenesis: From pathways to diagnosis and therapy studies // J Carcinog. – 2011. – Vol. 10, № 9.

46. Baxter N.T., Zackular J. P., Chen G. Y., Schloss P. D. Structure of the gut microbiome following colonization with human feces determines colonic tumor burden // Microbiome. – 2014. – Vol. 2, № 20.

47. Dingemanse C., Belzer C., van Hijum S. A. et al. Akkermansia muciniphila and Helicobacter typhlonius modulate intestinal tumor development in mice // Carcinogenesis. – 2015. – Vol. 36, № 11. – P. 1388–1396.

48. Ganesh B.P., Klopfleisch R., Loh G., Blaut M. Commensal Akkermansia muciniphila exacerbates gut inflammation in Salmonella Typhimurium–infected gnotobiotic mice // PLoS One. – 2013. – Vol. 8, № 9. – P. e74963.

49. Shin NR, Lee JC, Lee HY, et al. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet–induced obese mice. Gut. 2014;63(5):727–735. doi:10.1136/gutjnl-2012-303839

50. Lee H., Ko G. Effect of metformin on metabolic improvement and gut microbiota // Appl Environ Microbiol. – 2014. – Vol. 80, № 19. – P. 5935–5943.

51. Kosciow K., Deppenmeier U. Characterization of a phospholipid–regulated β–galactosidase from Akkermansia muciniphila involved in mucin degradation // Microbiologyopen. – 2019. – Vol. 8, № 8. – P. e00796.

52. Ravichandran K. S. Find–me and eat–me signals in apoptotic cell clearance: progress and conundrums // J Exp Med. – 2010. – Vol. 207, № 9. – P. 1807–1817.

53. Piller F., Le Deist F., Weinberg K. I. Altered O-glycan synthesis in lymphocytes from patients with Wiskott– Aldrich syndrome // J Exp Med. – 1991. – Vol. 173, № 6. – P. 1501–1510.

54. Eda S., Yamanaka M., Beppu M. Carbohydrate–mediated phagocytic recognition of early apoptotic cells undergoing transient capping of CD43 glycoprotein // J Biol Chem. – 2004. – Vol. 279, № 7. – P. 5967–5974.

55. Stace C.L., Ktistakis N. T. Phosphatidic acid– and phosphatidylserine–binding proteins // Biochim Biophys Acta. – 2006. – Vol. 1761, № 8. – P. 913–926.

56. Yamaji–Hasegawa A., Tsujimoto M. Asymmetric distribution of phospholipids in biomembranes // Biol Pharm Bull. – 2006. – Vol. 29, № 8. – P. 1547–1553.

57. Fourcade O., Simon M. F., Viodé C. et al. Secretory phospholipase A2 generates the novel lipid mediator lysophosphatidic acid in membrane microvesicles shed from activated cells // Cell. – 1995.–Vol. 80, № 6.–С. 919–927.


Review

For citations:


Karamzin A.M., Ropot A.V., Boshian R.E. Relationship of the mucin-degrading bacterium Akkermansia muciniphila with colorectal cancer. Experimental and Clinical Gastroenterology. 2020;(6):158-165. (In Russ.) https://doi.org/10.31146/1682-8658-ecg-178-6-158-165

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