Akkermansia muciniphila adheres to enterocytes and strengthens the integrity of the epithelial cell layer

Applied and Environmental Microbiology

Volumn 81, Issue 11, 2015, Pages 3655-3662

  Reunanen, Justus ^a   Kainulainen, Veera ^a   Huuskonen, Laura ^a   Ottman, Noora ^b   Belzer, Clara ^b   Huhtinen, Heikki ^c   de Vos, Willem M ^a,b   Satokaria, Reetta ^a,d  

^a UNIVERSITY OF HELSINKI   (Finland)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c TURKU UNIVERSITY HOSPITAL   (Finland)

^d UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CELL CULTURE; CYTOLOGY; ESCHERICHIA COLI; MONOLAYERS;

CELL CONCENTRATIONS; DEGRADING BACTERIA; EXTRACELLULAR MATRIX PROTEIN; GASTROINTESTINAL TRACT; INTESTINAL EPITHELIUM; INTESTINAL HEALTHS; PROMOTING EFFECT; TRANSEPITHELIAL ELECTRICAL RESISTANCES;

CELLS;

ADHESION; CONCENTRATION (COMPOSITION); DIABETES; GERM CELL; METABOLISM; MICROBIAL ACTIVITY; PROTEIN;

AKKERMANSIA MUCINIPHILA; ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

INTERLEUKIN 8;

BACTERIUM ADHERENCE; CELL LINE; EPITHELIUM CELL; HUMAN; IMMUNOLOGY; INTESTINE CELL; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; VERRUCOMICROBIA;

BACTERIAL ADHESION; CELL LINE; ENTEROCYTES; EPITHELIAL CELLS; HUMANS; INTERLEUKIN-8; VERRUCOMICROBIA;

EID: 84930038638     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.04050-14     Document Type: Article

References (39)

1. Derrien M, Vaughan EE, Plugge CM, de Vos WM. 2004. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 54:1469-1476. http://dx.doi.org/10.1099/ijs.0.02873-0.
2. Collado MC, Derrien M, Isolauri E, de Vos WM, Salminen S. 2007. Intestinal integrity and Akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults, and the elderly. Appl Environ Microbiol 73:7767-7770. http://dx.doi.org/10.1128/AEM.01477-07.
3. Lyra A, Forssten S, Rolny P, Wettergren Y, Lahtinen SJ, Salli K, Cedgård L, Odin E, Gustavsson B, Ouwehand AC. 2012. Comparison of bacterial quantities in left and right colon biopsies and faeces. World J Gastroenterol 18:4404-4411. http://dx.doi.org/10.3748/wjg.v18.i32.4404.
4. van Passel MWJ, Kant R, Zoetendal EG, Plugge CM, Derrien M, Malfatti SA, Chain PSG, Woyke T, Palva A, de Vos WM, Smidt H. 2011. The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PLoS One 6(3): e16876. http://dx.doi.org/10.1371/journal.pone.0016876.
5. Png CW, Lindén SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, McGuckin MA, Florin TH. 2010. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol 105:2420-2428. http://dx.doi.org/10.1038/ajg.2010.281.
6. Rajilić-Stojanović M, Shanahan F, Guarner F, de Vos WM. 2013. Phylogenetic analysis of dysbiosis in ulcerative colitis during remission. Inflamm Bowel Dis 2013 19:481-488. http://dx.doi.org/10.1097/MIB .0b013e31827fec6d.
7. Swidsinski A, Dörffel Y, Loening-Baucke V, Theissig F, Rückert JC, Ismail M, Rau WA, Gaschler D, Weizenegger M, Kühn S, Schilling J, Dörffel WV. 2011. Acute appendicitis is characterised by local invasion with Fusobacterium nucleatum/necrophorum. Gut 60:34-40. http://dx.doi .org/10.1136/gut.2009.191320.
8. Hansen CH, Krych L, Nielsen DS, Vogensen FK, Hansen LH, Sørensen SJ, Buschard K, Hansen AK. 2012. Early life treatment with vancomycin propagates Akkermansia muciniphila and reduces diabetes incidence in the NOD mouse. Diabetologia 55:2285-2294. http://dx.doi.org/10.1007/s00125-012-2564-7.
9. Karlsson CL, Onnerfält J, Xu J, Molin G, Ahrné S, Thorngren-Jerneck K. 2012. The microbiota of the gut in preschool children with normal and excessive body weight. Obesity (Silver Spring) 20:2257-2261. http://dx .doi.org/10.1038/oby.2012.110.
10. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, Almeida M, Arumugam M, Batto JM, Kennedy S, Leonard P, Li J, Burgdorf K, Grarup N, Jørgensen T, Brandslund I, Nielsen HB, Juncker AS, Bertalan M, Levenez F, Pons N, Rasmussen S, Sunagawa S, Tap J, Tims S, Zoetendal EG, Brunak S, Clément K, Doré J, Kleerebezem M, Kristiansen K, Renault P, Sicheritz-Ponten T, de Vos WM, Zucker JD, Raes J, Hansen T, MetaHIT consortium, Bork P, Wang J, Ehrlich SD, Pedersen O. 2013. Richness of human gut microbiome correlates with metabolic markers. Nature 500:541-546. http://dx.doi.org/10.1038/nature12506.
11. Derrien M, Van Baarlen P, Hooiveld G, Norin E, Müller M, de Vos WM. 2011. Modulation of mucosal immune response, tolerance, and proliferation in mice colonized by the mucin-degrader Akkermansia muciniphila. Front Microbiol 2:166. http://dx.doi.org/10.3389/fmicb.2011.00166.
12. Lukovac S, Belzer C, Pellis L, Keijser BJ, de Vos WM, Montijn RC, Roeselers G. 2014. Differential modulation by Akkermansia muciniphila and Faecalibacterium prausnitzii of host peripheral lipid metabolism and histone acetylation in mouse gut organoids. mBio 5(4):e01438-14. http://dx.doi.org/10.1128/mBio.01438-14.
13. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, de Vos WM, Cani PD. 2013. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A 110: 9066-9071. http://dx.doi.org/10.1073/pnas.1219451110.
14. Johansson MEV, Ambort D, Pelaseyed T, Schütte A, Gustafsson JK, Ermund A, Subramani DB, Holmén-Larsson JM, Thomsson KA, Bergström JH, van der Post S, Rodriguez-Pinẽiro AM, Sjövall H, Bäckström M, Hansson GC. 2011. Composition and functional role of the mucus layers in the intestine. Cell Mol Life Sci 68:3635-3641. http://dx.doi.org/10.1007/s00018-011-0822-3.
15. Kainulainen V, Reunanen J, Hiippala K, Guglielmetti S, Vesterlund S, Palva A, Satokari R. 2013. BopA does not have a major role in the adhesion of Bifidobacterium bifidum to intestinal epithelial cells, extracellular matrix proteins, and mucus. Appl Environ Microbiol 79:6989-6997. http://dx.doi.org/10.1128/AEM.01993-13.
16. Vesterlund S, Paltta J, Karp M, Ouwehand AC. 2005. Measurement of bacterial adhesion-in vitro evaluation of different methods. J Microbiol Methods 60:225-233. http://dx.doi.org/10.1016/j.mimet.2004.09.013.
17. Reunanen J, von Ossowski I, Hendrickx APA, Palva A, de Vos WM. 2012. Characterization of the SpaCBA pilus fibers in the probiotic Lactobacillus rhamnosus GG. Appl Environ Microbiol 78:2337-2344. http://dx .doi.org/10.1128/AEM.07047-11.
18. Kankainen M, Paulin L, Tynkkynen S, von Ossowski I, Reunanen J, Partanen P, Satokari R, Vesterlund S, Hendrickx AP, Lebeer S, De Keersmaecker SC, Vanderleyden J, Hämäläinen T, Laukkanen S, Salovuori N, Ritari J, Alatalo E, Korpela R, Mattila-Sandholm T, Lassig A, Hatakka K, Kinnunen KT, Karjalainen H, Saxelin M, Laakso K, Surakka A, Palva A, Salusjärvi T, Auvinen P, de Vos WM. 2009. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proc Natl Acad Sci U S A 106:17193-17198. http://dx.doi.org/10.1073/pnas.0908876106.
19. Lebeer S, Claes I, Tytgat HL, Verhoeven TL, Marien E, von Ossowski I, Reunanen J, Palva A, de Vos WM, Keersmaecker SC, Vanderleyden J. 2012. Functional analysis of Lactobacillus rhamnosus GG pili in relation to adhesion and immunomodulatory interactions with intestinal epithelial cells. Appl Environ Microbiol 78:185-193. http://dx.doi.org/10.1128/AEM.06192-11.
20. Pinto M, Robine-Leon S, Appay M-D, Kedinger M, Triadou N, Dussaulx E, Lacroix B, Simon-Assmann P, Haffen K, Fogh J, Zweibaum A. 1983. Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture. Biol Cell 47:323-330.
21. Evers BM, Zhou Z, Celano P, Li J. 1995. The neurotensin gene is a downstream target for Ras activation. J Clin Invest 95:2822-2830. http://dx.doi.org/10.1172/JCI117987.
22. Blikslager AT, Adam J, Moeser AJ, Jody L, Gookin JL, Jones SL, Odle J. 2007. Restoration of barrier function in injured intestinal mucosa. Physiol Rev 87:545-564. http://dx.doi.org/10.1152/physrev.00012.2006.
23. Geens MM, Niewold TA. 2010. Preliminary characterization of the transcriptional response of the porcine intestinal cell line IPEC-J2 to enterotoxigenic Escherichia coli, Escherichia coli, and E. coli lipopolysaccharide. Comp Funct Genomics 2010:469583. http://dx.doi.org/10.1155/2010/469583.
24. Alhawi M, Stewart J, Erridge C, Patrick S, Poxton IR. 2009. Bacteroides fragilis signals through Toll-like receptor (TLR) 2 and not through TLR4. J Med Microbiol 58:1015-1022. http://dx.doi.org/10.1099/jmm.0.009936-0.
25. Patrick S, Houston S, Thacker Z, Blakely GW. 2009. Mutational analysis of genes implicated in LPS and capsular polysaccharide biosynthesis in the opportunistic pathogen Bacteroides fragilis. Microbiology 155:1039-1049. http://dx.doi.org/10.1099/mic.0.025361-0.
26. Mammen JM, Matthews JB. 2003. Mucosal repair in the gastrointestinal tract. Crit Care Med 31(Suppl):S532-S537. http://dx.doi.org/10.1097/01.CCM.0000081429.89277.AF.
27. Vereecke L, Beyaert R, van Loo G. 2011. Enterocyte death and intestinal barrier maintenance in homeostasis and disease. Trends Mol Med 17: 584-593. http://dx.doi.org/10.1016/j.molmed.2011.05.011.
28. Sambuy Y, De Angelis I, Ranaldi G, Scarino ML, Stammati A, Zucco F. 2005. The Caco-2 cell line as a model of the intestinal barrier: influence of cell and culture-related factors on Caco-2 cell functional characteristics. Cell Biol Toxicol 21:1-26. http://dx.doi.org/10.1007/s10565-005-0085-6.
29. García-Lorenzo A, Rodríguez-Piñeiro AM, Rodríguez-Berrocal FJ, Cadena MP, Martínez-Zorzano VS. 2012. Changes on the Caco-2 secretome through differentiation analyzed by 2-D differential in-gel electrophoresis (DIGE). Int J Mol Sci 13:14401-14420. http://dx.doi.org/10.3390/ijms131114401.
30. Coconnier MH, Bernet MF, Kerneis S, Chauviere G, Fourniat J, Servin AL. 1993. Inhibition of adhesion of enteroinvasive pathogens to human intestinal Caco-2 cells by Lactobacillus acidophilus strain LB decreases bacterial invasion. FEMS Microbiol Lett 110:299-305. http://dx.doi.org/10.1111/j.1574-6968.1993.tb06339.x.
31. Iizuka M, Konno S. 2011. Wound healing of intestinal epithelial cells. World J Gastroenterol 17:2161-2171. http://dx.doi.org/10.3748/wjg.v17.i17.2161.
32. Johansson MEV, Thomsson KA, Hansson GC. 2009. Proteomic analyses of the two mucus layers of the colon barrier reveal that their main component, the Muc2 mucin, is strongly bound to the Fcgbp protein. J Proteome Res 8:3549-3557. http://dx.doi.org/10.1021/pr9002504.
33. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmée E, Cousin B, Sulpice T, Chamontin B, Ferrières J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R. 2007. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56:1761-1772. http://dx .doi.org/10.2337/db06-1491.
34. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, Burcelin R. 2008. Changes in gut microbiota control metabolic endotoxemia- induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57:1470-1481. http://dx.doi.org/10.2337/db07-1403.
35. Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, Rottier O, Geurts L, Naslain D, Neyrinck A, Lambert DM, Muccioli GG, Delzenne NM. 2009. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58:1091-1103. http://dx.doi.org/10.1136/gut.2008.165886.
36. Tilg H, Moschen AR. 2006. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol 6:772-783. http://dx.doi.org/10.1038/nri1937.
37. Stenman LK, Holma R, Korpela R. 2012. High-fat-induced intestinal permeability dysfunction associated with altered fecal bile acids. World J Gastroenterol 18:923-929. http://dx.doi.org/10.3748/wjg.v18.i9.923.
38. Sun L, Yu Z, Ye X, Zou S, Li H, Yu D, Wu H, Chen Y, Dore J, Clément K, Hu FB, Lin X. 2010. A marker of endotoxemia is associated with obesity and related metabolic disorders in apparently healthy Chinese. Diabetes Care 33:1925-1932. http://dx.doi.org/10.2337/dc10-0340.
39. Baggiolini M, Clark-Lewis I. 1992. Interleukin-8, a chemotactic and inflammatory cytokine. FEBS Lett 307:97-101. http://dx.doi.org/10.1016/0014-5793(92)80909-Z.