Akkermansia muciniphila-derived extracellular vesicles influence gut permeability through the regulation of tight junctions

Experimental and Molecular Medicine

Volumn 50, Issue 2, 2018, Pages

  Chelakkot, Chaithanya ^a   Choi, Youngwoo ^a   Kim, Dae Kyum ^a   Park, Hyun T ^a   Ghim, Jaewang ^b   Kwon, Yonghoon ^a   Jeon, Jinseong ^a   Kim, Min Seon ^c   Jee, Young Koo ^d   Gho, Yong S ^a   Park, Hae Sim ^e   Kim, Yoon Keun ^f   Ryu, Sung H ^a  

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

^b NovaCell Technology Inc   (South Korea)

^c University of Ulsan College of Medicine   (South Korea)

^d Dankook University College of Medicine   (South Korea)

^e Ajou University School of Medicine   (South Korea)

^f MD Healthcare Inc   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

OCCLUDIN; BIOLOGICAL MARKER;

AKKERMANSIA MUCINIPHILA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT GAIN; CACO-2 CELL LINE; CANCER CELL CULTURE; CELL FUNCTION; CELL THERAPY; CONTROLLED STUDY; DIABETIC PATIENT; EPITHELIUM CELL; EXOSOME; FECES ANALYSIS; GLUCOSE TOLERANCE; HUMAN; HUMAN CELL; INTESTINE MUCOSA PERMEABILITY; LIPID DIET; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; TIGHT JUNCTION; ANIMAL; BIODIVERSITY; CELL MEMBRANE PERMEABILITY; FECES; INTESTINE FLORA; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; VERRUCOMICROBIA;

ANIMALS; BIODIVERSITY; BIOMARKERS; CACO-2 CELLS; CELL MEMBRANE PERMEABILITY; DIABETES MELLITUS, TYPE 2; DIET, HIGH-FAT; EXTRACELLULAR VESICLES; FECES; GASTROINTESTINAL MICROBIOME; HUMANS; INTESTINAL MUCOSA; MICE; TIGHT JUNCTIONS; VERRUCOMICROBIA;

EID: 85047009337     PISSN: 12263613     EISSN: 20926413     Source Type: Journal    
DOI: 10.1038/emm.2017.282     Document Type: Article

References (72)

1. Cani PD, Osto M, Geurts L, Everard A. Involvement of gut microbiota in the development of low-grade inflammation and type 2 diabetes associated with obesity. Gut Microbes 2012; 3: 279–288.
2. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007; 56: 1761–1772.
3. Osborn O, Olefsky JM. The cellular and signaling networks linking the immune system and metabolism in disease. Nat Med 2012; 18: 363–374.
4. Collado MC, Isolauri E, Laitinen K, Salminen S. Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am J Clin Nutr 2008; 88: 894–899.
5. Karlsson CL, Onnerfalt J, Xu J, Molin G, Ahrne S, Thorngren-Jerneck K. The microbiota of the gut in preschool children with normal and excessive body weight. Obesity (Silver Spring) 2012; 20: 2257–2261.
6. Belzer C, de Vos WM. Microbes inside–from diversity to function: the case of Akkermansia. ISME J 2012; 6: 1449–1458.
7. Derrien M, Vaughan EE, Plugge CM, de Vos WM. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 2004; 54: 1469–1476.
8. Collado MC, Derrien M, Isolauri E, de Vos WM, Salminen S. Intestinal integrity and Akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults, and the elderly. Appl Environ Microbiol 2007; 73: 7767–7770.
9. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci USA 2013; 110: 9066–9071.
10. Derrien M, Van Baarlen P, Hooiveld G, Norin E, Muller M, de Vos WM. Modulation of mucosal immune response, tolerance, and proliferation in mice colonized by the mucin-degrader Akkermansia muciniphila. Front Microbiol 2011; 2: 166.
11. Konig J, Wells J, Cani PD, Garcia-Rodenas CL, MacDonald T, Mercenier A et al. Human Intestinal Barrier Function in Health and Disease. Clin Transl Gastroenterol 2016; 7: e196.
12. Moreira AP, Texeira TF, Ferreira AB, Peluzio Mdo C, Alfenas Rde C. Influence of a high-fat diet on gut microbiota, intestinal permeability and metabolic endotoxaemia. Br J Nutr 2012; 108: 801–809.
13. Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, Rottier O et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 2009; 58: 1091–1103.
14. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 2008; 57: 1470–1481.
15. Ellis TN, Kuehn MJ. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol Mol Biol Rev 2010; 74: 81–94.
16. Lee EY, Choi DY, Kim DK, Kim JW, Park JO, Kim S et al. Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles. Proteomics 2009; 9: 5425–5436.
17. Lee EY, Bang JY, Park GW, Choi DS, Kang JS, Kim HJ et al. Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics 2007; 7: 3143–3153.
18. Horstman AL, Kuehn MJ. Bacterial surface association of heat-labile enterotoxin through lipopolysaccharide after secretion via the general secretory pathway. J Biol Chem 2002; 277: 32538–32545.
19. Hong SW, Kim MR, Lee EY, Kim JH, Kim YS, Jeon SG et al. Extracellular vesicles derived from Staphylococcus aureus induce atopic dermatitis-like skin inflammation. Allergy 2011; 66: 351–359.
20. Kim YS, Choi EJ, Lee WH, Choi SJ, Roh TY, Park J et al. Extracellular vesicles, especially derived from Gram-negative bacteria, in indoor dust induce neutrophilic pulmonary inflammation associated with both Th1 and Th17 cell responses. Clin Exp Allergy 2013; 43: 443–454.
21. Kuehn MJ, Kesty NC. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev 2005; 19: 2645–2655.
22. Choi Y, Kwon Y, Kim DK, Jeon J, Jang SC, Wang T et al. Gut microbe-derived extracellular vesicles induce insulin resistance, thereby impairing glucose metabolism in skeletal muscle. Sci Rep 2015; 5: 15878.
23. Kang CS, Ban M, Choi EJ, Moon HG, Jeon JS, Kim DK et al. Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis. PLoS ONE 2013; 8: e76520.
24. Ma TY, Hoa NT, Tran DD, Bui V, Pedram A, Mills S et al. Cytochalasin B modulation of Caco-2 tight junction barrier: role of myosin light chain kinase. Am J Physiol Gastrointest Liver Physiol 2000; 279: G875–G885.
25. Natoli M, Leoni BD, D'Agnano I, Zucco F, Felsani A. Good Caco-2 cell culture practices. Toxicol In Vitro 2012; 26: 1243–1246.
26. Chelakkot C, Ghim J, Rajasekaran N, Choi JS, Kim JH, Jang MH et al. Intestinal epithelial cell-specific deletion of PLD2 alleviates DSS-induced colitis by regulating occludin. Sci Rep 2017; 7: 1573.
27. Biganzoli E, Cavenaghi LA, Rossi R, Brunati MC, Nolli ML. Use of a Caco-2 cell culture model for the characterization of intestinal absorption of antibiotics. Farmaco 1999; 54: 594–599.
28. Yamashita S, Furubayashi T, Kataoka M, Sakane T, Sezaki H, Tokuda H. Optimized conditions for prediction of intestinal drug permeability using Caco-2 cells. Eur J Pharm Sci 2000; 10: 195–204.
29. Corr SC, Palsson-McDermott EM, Grishina I, Barry SP, Aviello G, Bernard NJ et al. MyD88 adaptor-like (Mal) functions in the epithelial barrier and contributes to intestinal integrity via protein kinase C. Mucosal Immunol 2014; 7: 57–67.
30. Wang Q, Pantzar N, Jeppsson B, Westrom BR, Karlsson BW. Increased intestinal marker absorption due to regional permeability changes and decreased intestinal transit during sepsis in the rat. Scand J Gastroenterol 1994; 29: 1001–1008.
31. Brandl K, Rutschmann S, Li X, Du X, Xiao N, Schnabl B et al. Enhanced sensitivity to DSS colitis caused by a hypomorphic Mbtps1 mutation disrupting the ATF6-driven unfolded protein response. Proc Natl Acad Sci USA 2009; 106: 3300–3305.
32. Hwang D, Rust AG, Ramsey S, Smith JJ, Leslie DM, Weston AD et al. A data integration methodology for systems biology. Proc Natl Acad Sci USA 2005; 102: 17296–17301.
33. Kim YS, Lee WH, Choi EJ, Choi JP, Heo YJ, Gho YS et al. Extracellular vesicles derived from Gram-negative bacteria, such as Escherichia coli, induce emphysema mainly via IL-17A-mediated neutrophilic inflammation. J Immunol 2015; 194: 3361–3368.
34. Park KS, Choi KH, Kim YS, Hong BS, Kim OY, Kim JH et al. Outer membrane vesicles derived from Escherichia coli induce systemic inflammatory response syndrome. PLoS ONE 2010; 5: e11334.
35. Mangell P, Nejdfors P, Wang M, Ahrne S, Westrom B, Thorlacius H et al. Lactobacillus plantarum 299v inhibits Escherichia coli-induced intestinal permeability. Dig Dis Sci 2002; 47: 511–516.
36. Feldman GJ, Mullin JM, Ryan MP. Occludin: structure, function and regulation. Adv Drug Deliv Rev 2005; 57: 883–917.
37. Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest 2005; 115: 1111–1119.
38. Mehta NN, McGillicuddy FC, Anderson PD, Hinkle CC, Shah R, Pruscino L et al. Experimental endotoxemia induces adipose inflammation and insulin resistance in humans. Diabetes 2010; 59: 172–181.
39. Hadad SM, Appleyard V, Thompson AM. Therapeutic metformin/AMPK activation promotes the angiogenic phenotype in the ERalpha negative MDA-MB-435 breast cancer model. Breast Cancer Res Treat 2009; 114: 391.
40. Zhang L, Jouret F, Rinehart J, Sfakianos J, Mellman I, Lifton RP et al. AMP-activated protein kinase (AMPK) activation and glycogen synthase kinase-3beta (GSK-3beta) inhibition induce Ca2+-independent deposition of tight junction components at the plasma membrane. J Biol Chem 2011; 286: 16879–16890.
41. Zheng B, Cantley LC. Regulation of epithelial tight junction assembly and disassembly by AMP-activated protein kinase. Proc Natl Acad Sci USA 2007; 104: 819–822.
42. Zhang L, Li J, Young LH, Caplan MJ. AMP-activated protein kinase regulates the assembly of epithelial tight junctions. Proc Natl Acad Sci USA 2006; 103: 17272–17277.
43. Wells JM, Brummer RJ, Derrien M, MacDonald TT, Troost F, Cani PD et al. Homeostasis of the gut barrier and potential biomarkers. Am J Physiol Gastrointest Liver Physiol 2017; 312: G171–G193.
44. Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 2009; 9: 799–809.
45. Peterson LW, Artis D. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 2014; 14: 141–153.
46. Shen L, Su L, Turner JR. Mechanisms and functional implications of intestinal barrier defects. Dig Dis 2009; 27: 443–449.
47. Fasano A, Shea-Donohue T. Mechanisms of disease: the role of intestinal barrier function in the pathogenesis of gastrointestinal autoimmune diseases. Nat Clin Pract Gastroenterol Hepatol 2005; 2: 416–422.
48. Piche T, Barbara G, Aubert P, Bruley des Varannes S, Dainese R, Nano JL et al. Impaired intestinal barrier integrity in the colon of patients with irritable bowel syndrome: involvement of soluble mediators. Gut 2009; 58: 196–201.
49. Maloy KJ, Powrie F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 2011; 474: 298–306.
50. Karl JP, Margolis LM, Madslien EH, Murphy NE, Castellani JW, Gundersen Y et al. Changes in intestinal microbiota composition and metabolism coincide with increased intestinal permeability in young adults under prolonged physiological stress. Am J Physiol Gastrointest Liver Physiol 2017; 312: G559–G571.
51. Miele L, Valenza V, La Torre G, Montalto M, Cammarota G, Ricci R et al. Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease. Hepatology 2009; 49: 1877–1887.
52. de Magistris L, Familiari V, Pascotto A, Sapone A, Frolli A, Iardino P et al. Alterations of the intestinal barrier in patients with autism spectrum disorders and in their first-degree relatives. J Pediatr Gastroenterol Nutr 2010; 51: 418–424.
53. White JF. Intestinal pathophysiology in autism. Exp Biol Med (Maywood) 2003; 228: 639–649.
54. Damms-Machado A, Louis S, Schnitzer A, Volynets V, Rings A, Basrai M et al. Gut permeability is related to body weight, fatty liver disease, and insulin resistance in obese individuals undergoing weight reduction. Am J Clin Nutr 2017; 105: 127–135.
55. Odenwald MA, Turner JR. Intestinal permeability defects: is it time to treat? Clin Gastroenterol Hepatol 2013; 11: 1075–1083.
56. Bischoff SC, Barbara G, Buurman W, Ockhuizen T, Schulzke JD, Serino M et al. Intestinal permeability–a new target for disease prevention and therapy. BMC Gastroenterol 2014; 14: 189.
57. Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, Keilbaugh SA, Hamady M, Chen YY et al. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 2009; 137: 1716–1724 e1711–e1712.
58. Backhed F, Manchester JK, Semenkovich CF, Gordon JI. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci USA 2007; 104: 979–984.
59. Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012; 490: 55–60.
60. Santacruz A, Collado MC, Garcia-Valdes L, Segura MT, Martin-Lagos JA, Anjos T et al. Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr 2010; 104: 83–92.
61. Derrien M, Collado MC, Ben-Amor K, Salminen S, de Vos WM. The Mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Appl Environ Microbiol 2008; 74: 1646–1648.
62. Plovier H, Everard A, Druart C, Depommier C, Van Hul M, Geurts L et al. A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nat Med 2017; 23: 107–113.
63. Anhe FF, Marette A. A microbial protein that alleviates metabolic syndrome. Nat Med 2017; 23: 11–12.
64. Galan JE, Collmer A. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 1999; 284: 1322–1328.
65. Thery C. Exosomes: secreted vesicles and intercellular communications. F1000 Biol Rep 2011; 3: 15.
66. Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 2006; 20: 1487–1495.
67. Gyorgy B, Szabo TG, Pasztoi M, Pal Z, Misjak P, Aradi B et al. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci 2011; 68: 2667–2688.
68. Unal CM, Schaar V, Riesbeck K. Bacterial outer membrane vesicles in disease and preventive medicine. Semin Immunopathol 2011; 33: 395–408.
69. Shen Y, Giardino Torchia ML, Lawson GW, Karp CL, Ashwell JD, Mazmanian SK. Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe 2012; 12: 509–520.
70. Dao MC, Everard A, Aron-Wisnewsky J, Sokolovska N, Prifti E, Verger EO et al. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut 2016; 65: 426–436.
71. Renelli M, Matias V, Lo RY, Beveridge TJ. DNA-containing membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential. Microbiology 2004; 150: 2161–2169.
72. Perez-Cruz C, Delgado L, Lopez-Iglesias C, Mercade E. Outer-inner membrane vesicles naturally secreted by Gram-negative pathogenic bacteria. PLoS ONE 2015; 10: e0116896.