Live Faecalibacterium prausnitzii does not enhance epithelial barrier integrity in an apical anaerobic co-culture model of the large intestine

Nutrients

Volumn 9, Issue 12, 2017, Pages

  Maier, Eva ^a,b   Anderson, Rachel C ^a,b   Roy, Nicole C ^a,b,c  

^a AGRESEARCH GRASSLANDS   (New Zealand)

^b MASSEY UNIVERSITY   (New Zealand)

^c National Science Challenge   (New Zealand)

Author keywords

Intestinal barrier maturation; Intestinal microbiota; Obligate anaerobic bacteria; Tight junctions

Indexed keywords

TOLL LIKE RECEPTOR 2;

ANAEROBIC BACTERIUM; ANAEROBIC METABOLISM; ARTICLE; BACTERIUM CULTURE; CACO-2 CELL LINE; CELL VIABILITY ASSAY; COCULTURE; COLONY FORMING UNIT; CONTROLLED STUDY; FAECALIBACTERIUM PRAUSNITZII; HUMAN; HUMAN CELL; INTESTINE FLORA; LARGE INTESTINE; NONHUMAN; RESPONSE VARIABLE; SURVIVAL ANALYSIS; TIGHT JUNCTION; TRANSEPITHELIAL ELECTRICAL RESISTANCE; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; IMMUNOSENESCENCE; INTESTINE MUCOSA; MICROBIOLOGY; PHYSIOLOGY; PROCEDURES;

BACTERIA, ANAEROBIC; CACO-2 CELLS; COCULTURE TECHNIQUES; FAECALIBACTERIUM PRAUSNITZII; HUMANS; IMMUNOSENESCENCE; INTESTINAL MUCOSA; INTESTINE, LARGE;

EID: 85038091684     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu9121349     Document Type: Article

References (45)

1. Duncan, S.H.; Hold, G.L.; Harmsen, H.J.M.; Stewart, C.S.; Flint, H.J. Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov. Int. J. Syst. Evol. Microbiol. 2002, 52, 2141–2146.
2. Hold, G.L.; Schwiertz, A.; Aminov, R.I.; Blaut, M.; Flint, H.J. Oligonucleotide probes that detect quantitatively significant groups of butyrate-producing bacteria in human feces. Appl. Environ. Microbiol. 2003, 69, 4320–4324.
3. Swidsinski, A.; Loening-Baucke, V.; Vaneechoutte, M.; Doerffel, Y. Active Crohn’s disease and ulcerative colitis can be specifically diagnosed and monitored based on the biostructure of the fecal flora. Inflamm. Bowel Dis. 2008, 14, 147–161.
4. Sokol, H.; Seksik, P.; Furet, J.P.; Firmesse, O.; Nion-Larmurier, I.; Beaugerie, L.; Cosnes, J.; Corthier, G.; Marteau, P.; Doraé, J. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm. Bowel Dis. 2009, 15, 1183–1189.
5. Mondot, S.; Kang, S.; Furet, J.P.; Aguirre De Carcer, D.; McSweeney, C.; Morrison, M.; Marteau, P.; Doré, J.; Leclerc, M. Highlighting new phylogenetic specificities of Crohn’s disease microbiota. Inflamm. Bowel Dis. 2011, 17, 185–192.
6. Kabeerdoss, J.; Sankaran, V.; Pugazhendhi, S.; Ramakrishna, B.S. Clostridium leptum group bacteria abundance and diversity in the fecal microbiota of patients with inflammatory bowel disease: A case-control study in India. BMC Gastroenterol. 2013, 13, 20.
7. Fujimoto, T.; Imaeda, H.; Takahashi, K.; Kasumi, E.; Bamba, S.; Fujiyama, Y.; Andoh, A. Decreased abundance of Faecalibacterium prausnitzii in the gut microbiota of Crohn’s disease. J. Gastroenterol. Hepatol. 2013, 28, 613–619.
8. Rajilic-Stojanovic, M.; Biagi, E.; Heilig, H.G.; Kajander, K.; Kekkonen, R.A.; Tims, S.; de Vos, W.M. Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome. Gastroenterology 2011, 141, 1792–1801.
9. Balamurugan, R.; Rajendiran, E.; George, S.; Samuel, G.V.; Ramakrishna, B.S. Real-time polymerase chain reaction quantification of specific butyrate-producing bacteria, Desulfovibrio and Enterococcus faecalis in the feces of patients with colorectal cancer. J. Gastroenterol. Hepatol. 2008, 23, 1298–1303.
10. De Palma, G.; Nadal, I.; Medina, M.; Donat, E.; Ribes-Koninckx, C.; Calabuig, M.; Sanz, Y. Intestinal dysbiosis and reduced immunoglobulin-coated bacteria associated with coeliac disease in children. BMC Microbiol. 2010, 10, 63.
11. Martín, R.; Miquel, S.; Benevides, L.; Bridonneau, C.; Robert, V.; Hudault, S.; Chain, F.; Berteau, O.; Azevedo, V.; Chatel, J.M., et al. Functional characterization of novel Faecalibacterium prausnitzii strains isolated from healthy volunteers: A step forward in the use of F. prausnitzii as a next-generation probiotic. Front. Microbiol. 2017, 8, 1226.
12. Blatchford, P.; Stoklosinski, H.; Walton, G.; Swann, J.; Gibson, G.; Gearry, R.; Ansell, J. Kiwifruit fermentation drives positive gut microbial and metabolic changes irrespective of initial microbiota composition. Bioact. Carbohydr. Diet. Fibre 2015, 6, 37–45.
13. Neu, J. Gastrointestinal maturation and implications for infant feeding. Early Hum. Dev. 2007, 83, 767–775.
14. Talarico, S.T.; Santos, F.E.; Brandt, K.G.; Martinez, M.B.; Taddei, C.R. Anaerobic bacteria in the intestinal microbiota of Brazilian children. Clinics (Sao Paulo) 2017, 72, 154–160.
15. Hopkins, M.J.; Macfarlane, G.T.; Furrie, E.; Fite, A.; Macfarlane, S. Characterisation of intestinal bacteria in infant stools using real-time PCR and northern hybridisation analyses. FEMS Microbiol. Ecol. 2005, 54, 77–85.
16. Pop, M.; Walker, A.W.; Paulson, J.; Lindsay, B.; Antonio, M.; Hossain, M.A.; Oundo, J.; Tamboura, B.; Mai, V.; Astrovskaya, I., et al. Diarrhea in young children from low-income countries leads to large-scale alterations in intestinal microbiota composition. Genome Biol. 2014, 15, R76.
17. Miquel, S.; Leclerc, M.; Martin, R.; Chain, F.; Lenoir, M.; Raguideau, S.; Hudault, S.; Bridonneau, C.; Northen, T.; Bowen, B., et al. Identification of metabolic signatures linked to anti-inflammatory effects of Faecalibacterium prausnitzii. MBio 2015, 6, e00300-15.
18. Wrzosek, L.; Miquel, S.; Noordine, M.-L.; Bouet, S.; Chevalier-Curt, M.J.; Robert, V.; Philippe, C.; Bridonneau, C.; Cherbuy, C.; Robbe-Masselot, C., et al. Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. BMC Biol. 2013, 11, 61.
19. Maier, E.; Anderson, R.C.; Altermann, E.; Roy, N.C. Live Faecalibacterium prausnitzii induces greater TLR2 and TLR2/6 activation than the dead bacterium in an apical anaerobic co-culture system. Cell. Microbiol. 2017, e12805.
20. Wells, J.M.; Loonen, L.M.; Karczewski, J.M. The role of innate signaling in the homeostasis of tolerance and immunity in the intestine. Int. J. Med. Microbiol. 2010, 300, 41–48.
21. Groschwitz, K.R.; Hogan, S.P. Intestinal barrier function: Molecular regulation and disease pathogenesis. J. Allergy Clin. Immunol. 2009, 124, 3–20.
22. Carlsson, A.H.; Yakymenko, O.; Olivier, I.; Håkansson, F.; Postma, E.; Keita, Å.V.; Söderholm, J.D. Faecalibacterium prausnitzii supernatant improves intestinal barrier function in mice DSS colitis. Scand. J. Gastroenterol. 2013, 48, 1136–1144.
23. Ulluwishewa, D.; Anderson, R.C.; Young, W.; McNabb, W.C.; van Baarlen, P.; Moughan, P.J.; Wells, J.M.; Roy, N.C. Live Faecalibacterium prausnitzii in an apical anaerobic model of the intestinal epithelial barrier. Cell. Microbiol. 2015, 17, 226–240.
24. Haller, D.; Bode, C.; Hammes, W.P. Cytokine secretion by stimulated monocytes depends on the growth phase and heat treatment of bacteria: A comparative study between lactic acid bacteria and invasive pathogens. Microbiol. Immunol. 1999, 43, 925–935.
25. Yu, Q.; Yuan, L.; Deng, J.; Yang, Q. Lactobacillus protects the integrity of intestinal epithelial barrier damaged by pathogenic bacteria. Front. Cell. Infect. Microbiol. 2015, 5, 26.
26. Anderson, R.C.; Young, W.; Clerens, S.; Cookson, A.L.; McCann, M.J.; Armstrong, K.M.; Roy, N.C. Human oral isolate Lactobacillus fermentum AGR1487 reduces intestinal barrier integrity by increasing the turnover of microtubules in Caco-2 cells. PLoS ONE 2013, 8, e78774.
27. Wilkins, T.D.; Chalgren, S. Medium for use in antibiotic susceptibility testing of anaerobic bacteria. Antimicrob. Agents Chemother. 1976, 10, 926–928.
28. Wandersman, C.; Delepelaire, P. Bacterial iron sources: Fromsiderophores to hemophores. Annu. Rev. Microbiol. 2004, 58, 611–647.
29. Bentley, R.; Meganathan, R. Biosynthesis of vitamin K (menaquinone) in bacteria. Microbiol. Rev. 1982, 46, 241–280.
30. Kurosu, M.; Begari, E. Vitamin K2 in electron transport system: Are enzymes involved in vitamin K2 biosynthesis promising drug targets? Molecules 2010, 15, 1531.
31. Nakagawa, K.; Hirota, Y.; Sawada, N.; Yuge, N.; Watanabe, M.; Uchino, Y.; Okuda, N.; Shimomura, Y.; Suhara, Y.; Okano, T. Identification of UBIAD1 as a novel human menaquinone-4 biosynthetic enzyme. Nature 2010, 468, 117–121.
32. Heinken, A.; Khan, M.T.; Paglia, G.; Rodionov, D.A.; Harmsen, H.J.M.; Thiele, I. Functional metabolic map of Faecalibacterium prausnitzii, a beneficial human gut microbe. J. Bacteriol. 2014, 196, 3289–3302.
33. Miyakawa, M.F.; Creydt, V.P.; Uzal, F.; McClane, B.; Ibarra, C. Clostridium perfringens enterotoxin damages the human intestine in vitro. Infect. Immun. 2005, 73, 8407–8410.
34. Soler, A.P.; Miller, R.D.; Laughlin, K.V.; Carp, N.Z.; Klurfeld, D.M.; Mullin, J.M. Increased tight junctional permeability is associated with the development of colon cancer. Carcinogenesis 1999, 20, 1425–1432.
35. Sadaghian Sadabad, M.; von Martels, J.Z.H.; Khan, M.T.; Blokzijl, T.; Paglia, G.; Dijkstra, G.; Harmsen, H.J.M.; Faber, K.N. A simple coculture system shows mutualism between anaerobic faecalibacteria and epithelial Caco-2 cells. Sci. Rep. 2015, 5, 17906.
36. Shekels, L.L.; Lyftogt, C.T.; Ho, S.B. Bile acid-induced alterations of mucin production in differentiated human colon cancer cell lines. Int. J. Biochem. Cell Biol. 1996, 28, 193–201.
37. Klinken, B.J.-W.; Oussoren, E.; Weenink, J.-J.; Strous, G.J.; Büller, H.A.; Dekker, J.; Einerhand, A.W.C. The human intestinal cell lines Caco-2 and LS174T as models to study cell-type specific mucin expression. Glycoconj. J. 1996, 13, 757–768.
38. Khan, M.T.; Duncan, S.H.; Stams, A.J.M.; van Dijl, J.M.; Flint, H.J.; Harmsen, H.J.M. The gut anaerobe Faecalibacterium prausnitzii uses an extracellular electron shuttle to grow at oxic-anoxic interphases. ISME J. 2012, 6, 1578–1585.
39. Khan, M.T.; Browne, W.R.; Van Dijl, J.M.; Harmsen, H.J.M. How can Faecalibacterium prausnitzii employ riboflavin for extracellular electron transfer? Antioxid. Redox Signal. 2012, 17, 1433–1440.
40. Ewaschuk, J.B.; Diaz, H.; Meddings, L.; Diederichs, B.; Dmytrash, A.; Backer, J.; Looijer-van Langen, M.; Madsen, K.L. Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 295, G1025–G1034.
41. Segawa, S.; Fujiya, M.; Konishi, H.; Ueno, N.; Kobayashi, N.; Shigyo, T.; Kohgo, Y. Probiotic-derived polyphosphate enhances the epithelial barrier function and maintains intestinal homeostasis through integrin–p38 MAPK pathway. PLoS ONE 2011, 6, e23278.
42. Otte, J.-M.; Podolsky, D.K. Functional modulation of enterocytes by gram-positive and gram-negative microorganisms. Am. J. Physiol. Gastrointest. Liver Physiol. 2004, 286, G613–G626.
43. Peng, L.; Li, Z.-R.; Green, R.S.; Holzman, I.R.; Lin, J. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J. Nutr. 2009, 139, 1619–1625.
44. Karczewski, J.; Troost, F.J.; Konings, I.; Dekker, J.; Kleerebezem, M.; Brummer, R.-J.M.; Wells, J.M. 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–G859.
45. Cario, E.; Gerken, G.; Podolsky, D.K. Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterology 2007, 132, 1359–1374.