Activation of immune and defense responses in the intestinal mucosa by outer membrane vesicles of commensal and probiotic Escherichia coli strains

Frontiers in Microbiology

Volumn 7, Issue MAY, 2016, Pages

  Fábrega, María José ^a   Aguilera, Laura ^a   Giménez, Rosa ^a   Varela, Encarna ^b   Cañas, María Alexandra ^a   Antolín, María ^b   Badía, Josefa ^a   Baldomà, Laura ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Caco 2 PBMC co culture; Gut microbes; Intestinal mucosa; Membrane vesicles; Microbiota host crosstalk; Nissle 1917; Probiotics

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 22; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; PATTERN RECOGNITION RECEPTOR; PROBIOTIC AGENT; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BACTERIAL SECRETION SYSTEM; CENTRIFUGATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; ESCHERICHIA COLI; FILTERS AND MEMBRANES; HUMAN; HUMAN CELL; IMMUNE SYSTEM; INTESTINE MUCOSA; KNOWLEDGE; MEMBRANE VESICLE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; STIMULATION; WESTERN BLOTTING;

EID: 84973534463     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00705     Document Type: Article

References (63)

1. Aguilera, L., Toloza, L., Giménez, R., Odena, A., Oliveira, E., Aguilar, J., et al. (2014). Proteomic analysis of outer membrane vesicles from the probiotic strain Escherichia coli Nissle 1917. Proteomics 14, 222-229. doi: 10.1002/pmic.201300328
2. Apostolopoulos, V., Stojanovska, L., and Gargosky, S. E. (2015). MUC1 (CD227): a multi-tasked molecule. Cell. Mol. Life Sci. 72, 4475-4500. doi: 10.1007/s00018-015-2014-z
3. Arribas, B., Rodríguez-Cabezas, M. E., Camuesco, D., Comalada, M., Bailón, E., Utrilla, P., et al. (2009). A probiotic strain of Escherichia coli, Nissle 1917, given orally exerts local and systemic anti-inflammatory effects in lipopolysaccharide-induced sepsis in mice. Br. J. Pharmacol. 157, 1024-1033. doi: 10.1111/j.1476-5381.2009.00270.x
4. Becker, S., Oelschlaeger, T. A., Wullaert, A., Vlantis, K., Pasparakis, M., Wehkamp, J., et al. (2013). Bacteria regulate intestinal epithelial cell differentiation factors both in vitro and in vivo. PLoS ONE 8:e55620. doi: 10.1371/journal.pone.0055620
5. Belkaid, Y., and Hand, T. W. (2014). Role of the microbiota in immunity and inflammation. Cell 157, 121-141. doi: 10.1016/j.cell.2014.03.011
6. Bergström, A., Kristensen, M. B., Bahl, M. I., Metzdorff, S. B., Fink, L. N., Frøkiaer. H., et al. (2012). Nature of bacterial colonization influences transcription of mucin genes in mice during the first week of life. BMC Res. Notes 5:402. doi: 10.1186/1756-0500-5-402
7. Bomberger, J. M., Maceachran, D. P., Coutermarsh, B. A., Ye, S., O'Toole, G. A., and Stanton, B. A. (2009). Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog. 5:e1000382. doi: 10.1371/journal.ppat.1000382
8. Borruel, N., Casellas, F., Antolin, M., Llopis, M., Carol, M., Espíin, E., et al. (2003). Effects of nonpathogenic bacteria on cytokine secretion by human intestinal mucosa. Am. J. Gastroenterol. 98, 865-870. doi: 10.1111/j.1572-0241.2003.07384.x
9. Caballero, S., and Pamer, E. G. (2015). Microbiota-mediated inflammation and antimicrobial defense in the intestine. Annu. Rev. Immunol. 33, 227-256. doi: 10.1146/annurev-immunol-032713-120238
10. Chatterjee, D., and Chaudhuri, K. (2013). Vibrio cholerae O395 outer membrane vesicles modulate intestinal epithelial cells in a NOD1 protein-dependent manner and induce dendrític cell-mediated Th2/Th17 cell responses. J. Biol. Chem. 288, 4299-4309. doi: 10.1074/jbc. M112.408302
11. Chibbar, R., and Dieleman, L. A. (2015). Probiotics in the management of ulcerative colitis. J. Clin. Gastroenterol. 49, S50-S55. doi: 10.1097/MCG.0000000000000368
12. Cobo, E. R., and Chadee, K. (2013). Antimicrobial human b-defensins in the colon and their role in infectious and non-infectious diseases. Pathogens 2, 177-192. doi: 10.3390/pathogens2010177
13. Egea, L., Aguilera, L., Giménez, R., Sorolla, M. A., Aguilar, J., Badía, J., et al. (2007). Role of secreted glyceraldehyde-3-phosphate dehydrogenase in the infection mechanism of enterohemorrhagic and enteropathogenic Escherichia coli: interaction of the extracellular enzyme with human plasminogen and fibrinogen. Int. J. Biochem. Cell Biol. 39, 1190-1203. doi: 10.1016/j.biocel.2007.03.008
14. Ellis, T. N., and Kuehn, M. J. (2010). Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol. Mol. Biol. Rev. 74, 81-94. doi: 10.1128/MMBR.00031-09
15. Fang, H. W., Fang, S. B., Chiang Chiau, J. S., Yeung, C. Y., Chan, W. T., Jiang, C. B., et al. (2010). Inhibitory effects of Lactobacillus casei subsp. rhamnosus on Salmonella lipopolysaccharide-induced inflammation and epithelial barrier dysfunction in a co-culture model using Caco-2/peripheral blood mononuclear cells. J. Med. Microbiol. 59, 573-579. doi: 10.1099/jmm.0.009662-0
16. Foxx-Orenstein, A. E., and Chey, W. D. (2012). Manipulation of the gut microbiota as a novel treatment strategy for gastrointestinal disorders. Am. J. Gastroenterol. Suppl. 1, 41-46. doi: 10.1038/ajgsup.2012.8
17. Garrett, W. S., Gordon, J. I., and Glimcher, L. H. (2010). Homeostasis and inflammation in the intestine. Cell 140, 859-870. doi: 10.1016/j.al.2010.01.02
18. Gipson, I. K., Spurr-Michaud, S., Tisdale, A., and Menon, B. B. (2014). Comparison of the transmembrane mucins MUC1 and MUC16 in epithelial barrier function. PLoS ONE 9:e100393. doi: 10.1371/journal.pone.0100393
19. Güttsches, A. K., Löseke, S., Zähringer, U., Sonnenborn, U., Enders, C., Gatermann, S., et al. (2012). Anti-inflammatory modulation of immune response by probiotic Escherichia Coli Nissle 1917 in human blood mononuclear cells. Innate Immun. 18, 204-216. doi: 10.1177/1753425910396251
20. Hafez, M., Hayes, K., Goldrick, M., Grencis, R. K., and Roberts, I. S. (2010). The K5 capsule of Escherichia coli strain Nissle 1917 is important in stimulating expression of Toll-like receptor 5, CD14, MyD88, and TRIF together with the induction of interleukin-8 expression via the mitogen-activated protein kinase pathway in epithelial cells. Infect. Immun. 78, 2153-2162. doi: 10.1128/IAI.01406-09
21. Haller, D., Bode, C., Hammes, W. P., Pfeifer, A. M., Schiffrin, E. J., and Blum, S. (2000). Non-pathogenic bacteria elicit a differential cytokine response by intestinal epithelial cell/leucocyte co-cultures. Gut 47, 79-87. doi: 10.1136/gut.47.1.79
22. Jacobs, J. P., and Braun, J. (2014). Immune and genetic gardening of the intestinal microbiome. FEBS Lett. 588, 4102-4111. doi: 10.1016/jfehslet.2014.02.052
23. Jia, W., Li, H., Zhao, L., and Nicholson, J. K. (2008). Gut microbiota: a potential new territory for drug targeting. Nat. Rev. Drug Discov. 7, 123-129. doi: 10.1038/nrd2505
24. Johansson, M. E, Phillipson, M., Petersson, J., Velcich, A., Holm, L., and Hansson, G. C. (2008). The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc. Natl. Acad. Sci. U.S.A. 105, 15064-15069. doi: 10.1073/pnas.0803124105
25. Kang, C. S., Ban, M., Choi, E. J., Moon, H. G., Jeon, J. S., Kim, D. K., et al. (2013). Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis. PLoS ONE 8:e76520. doi: 10.1371/journal.pone.0076520
26. Kaparakis-Liaskos, M., and Ferrero, R. L. (2015). Immune modulation by bacterial outer membrane vesicles. Nat. Rev. Immunol. 15, 375-387. doi: 10.1038/nri3837
27. Khanh do, T., Mekata, E., Mukaisho, K., Sugihara, H., Shimizu, T., Shiomi, H., et al. (2013). Transmembrane mucin MUC1 overexpression and its association with CD10+ myeloid cells, transforming growth factor-ß1 expression, and tumor budding grade in colorectal cancer. Cancer Sci. 104, 958-964. doi: 10.1111/cas.12170
28. Kim, J. H., Lee, J., Park, J., and Gho, Y. S. (2015). Gram-negative and Gram-positive bacterial extracellular vesicles. Semin. Cell Dev. Biol. 40, 97-104. doi: 10.1016/j.semcdb.2015.02.006
29. Krishnan, S., Alden, N., and Lee, K. (2015). Pathways and funcions of gut microbiota metabolism impacting host physiology. Curr. Opin. Biotechnol. 36, 137-145. doi: 10.1016/j.cell.2014.03.011
30. Kruis, W., Fric, P., Pokrotnieks, J., Lukás, M., Fixa, B., Kascák, M., et al. (2004). Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 53, 1617-1623. doi: 10.1136/gut.2003.037747
31. Kulp, A., and Kuehn, M. J. (2010). Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu. Rev. Microbiol. 64, 163-184. doi: 10.1146/annurev.micro.091208.073413
32. Le Chatelier, E., Nielsen, T., Qin, J., Prifti, E., Hildebrand, F., Falony, G., et al. (2013). Richness of human gut microbiome correlates with metabolic markers. Nature 500, 541-546. doi: 10.1038/nature12506
33. Liu, H. P., Cao, A. T., Feng, T., Li, Q., Zhang, W., Yao. S., et al. (2015). TGF-ß converts Th1 cells into Th17 cells trough stimulation of Runx1 expression. Eur. J. Immunol. 45, 1010-1018. doi: 10.1002/eji.201444726
34. Llopis, M., Antolin, M., Carol, M., Borruel, N., Casellas, F., Martinez, C., et al. (2009). Lactobacillus casei downregulates commensals' inflammatory signals in Crohn's disease mucosa. Inflamm. Bowel Dis. 15, 275-283. doi: 10.1002/ibd.20736
35. López, P., González-Rodríguez, I., Sánchez, B., Gueimonde, M., Margolles, A., and Suárez, A. (2012). Treg-inducing membrane vesicles from Bifidobacterium bifidum LMG13195 as potential adjuvants in immunotherapy. Vaccine 30, 825-829. doi: 10.1016/j.vaccine.2011.11.115
36. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-273.
37. Möndel, M., Schroeder, B. O., Zimmermann, K., Huber, H., Nuding, S., Beisner, J., et al. (2009). Probiotic E. coli treatment mediates antimicrobial human beta-defensin synthesis and fecal excretion in humans. Mucosal Immunol. 2, 166-172. doi: 10.1038/mi.2008.77
38. Nikoopour, E., Bellemore, S. M., and Singh, B. (2015). IL-22, cell regeneration and autoimmunity. Cytokine 74, 35-42. doi: 10.1016/j.cyto.2014.09.007
39. Nishida, A., Lau, C. W., Zhang, M., Andoh, A., Shi, H. N., Mizoguchi, E., et al. (2012). The membrane-bound mucin Muc1 regulates T helper 17-cell responses and colitis in mice. Gastroenterology 142, 865-874. doi: 10.1053/j.gastro.2011.12.036
40. O'Hara, A. M., and Shanahan, F. (2006). The gut flora as a forgotten organ. EMBO Rep. 7, 688-693. doi: 10.1038/sj.embor.7400731
41. Ochman, H., and Selander, R. K. (1984). Standard reference strains of Escherichia coli from natural populations. J. Bacteriol. 157, 690-693.
42. Olsen, I., and Amano, A. (2015). Outer membrane vesicles-offensive weapons or good Samaritans? J. Oral Microbiol. 7, 27468. doi: 10.3402/jom.v7.27468
43. Pozo-Rubio, T., Mujico, J. R., Marcos, A., Puertollano, E., Nadal, I., Sanz, Y., et al. (2011). Immunostimulatory effect of faecal Bifidobacterium species of breast-fed and formula-fed infants in a peripheral blood mononuclear cell/Caco-2 co-culture system. Br. J. Nutr. 106, 1216-1223. doi: 10.1017/S0007114511001656
44. Robles-Alonso, V., and Guarner, F. (2013). Linking the gut microbiota to human health. Br. J. Nutr. 2, S21-S26. doi: 10.1017/S0007114512005235
45. Sanjabi, S., Zenewicz, L. A., Kamanaka, M., and Flavell, R. A. (2009). Anti-inflammatory and pro-inflammatory roles of TGF-beta, IL-10, and IL-22 in immunity and autoimmunity. Curr. Opin. Pharmacol. 9, 447-453. doi: 10.1016/j.coph.2009.04.008
46. Schaar, V., de Vries, S. P., Perez Vidakovics, M. L., Bootsma, H. J., Larsson, L., Hermans, P. W., et al. (2011). Multicomponent Moraxella catarrhalis outer membrane vesicles induce an inflammatory response and are internalized by human epithelial cells. Cell. Microbiol. 13, 432-449. doi: 10.1111/j.1462-5822.2010.01546.x
47. Schertzer, J. W., and Whiteley, M. (2013). Bacterial outer membrane vesicles in trafficking, communication and the host-pathogen interaction. J. Mol. Microbiol. Biotechnol. 23, 118-130. doi: 10.1159/000346770
48. Schlee, M., Wehkamp, J., Altenhoefer, A., Oelschlaeger, T. A., Stange, E. F., and Fellermann, K. (2007). Induction of human beta-defensin 2 by the probiotic Escherichia coli Nissle 1917 is mediated through flagellin. Infect. Immun. 75, 2399-2407. doi: 10.1128/IAI.01563-06
49. Sears, C. L., and Garrett, W. S. (2014). Microbes, microbiota and colon cancer. Cell Host Microbe 15, 317-328. doi: 10.1016/j.chom.2014.02.007
50. Shanahan, F. (2011). The gut microbiota in 2011: translating the microbiota to medicine. Nat. Rev. Gastroenterol. Hepatol. 9, 72-74. doi: 10.1038/nrgastro.2011.250
51. Shen, Y., Giardino Torchia, M. L., Lawson, G. W., Karp, C. L., Ashwell, J. D., and Mazmanian, S. K. (2012). Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe 12, 509-520. doi: 10.1016/j.chrom.2012.08.004
52. Sivan, A., Corrales, L., Hubert, N., Williams, J. B., Aquino-Michaels, K., Earley, Z. M., et al. (2015). Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350, 1084-1089. doi: 10.1126/science.aac4255
53. Stefka, A. T., Feehley, T., Tripathi, P, Qiu, J., McCoy, K., Mazmanian, S. K., and et al. (2014). Commensal bacteria protect against food allergen sensitization. Proc. Natl. Acad. Sci. U.S.A. 111, 13145-13150. doi: 10.1073/pnas.1412008111
54. Stentz, R., Horn, N., Cross, K., Salt, L., Brearley, C., Livermore, D. M., et al. (2015). Cephalosporinases associated with outer membrane vesicles released by Bacteroides spp. protect gut pathogens and commensals against ß-lactam antibiotics. J. Antimicrob. Chemother. 70, 701-709. doi: 10.1093/jac/dku466
55. Sturm, A., Rilling, K., Baumgart, D. C., Gargas, K., Abou-Ghazalé, T., Raupach, B., et al. (2005). Escherichia coli Nissle 1917 distinctively modulates T-cell cycling and expansion via toll-like receptor 2 signaling. Infect. Immun. 73, 1452-1465. doi: 10.1128/IAI.73.3.1452-1465.2005
56. Thaiss, C. A., Levy, M., Suez, J., and Elinav, E. (2014). The interplay between the innate inmune system and the microbiota. Curr. Opin. Immunol. 26, 41-48. doi: 10.1016/jcoi.2013.10.016
57. Ukena, S. N., Singh, A., Dringenberg, U., Engelhardt, R., Seidler, U., Hansen, W., et al. (2007). Probiotic Escherichia coli Nissle 1917 inhibits leaky gut by enhancing mucosal integrity. PLoS ONE 2:e1308. doi: 10.1371/journal.pone.0001308
58. Vaishnava, S., Yamamoto, M., Severson, K. M., Ruhn, K. A., Yu, X., Koren, O., et al. (2011). The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science 334, 255-258. doi: 10.1126/science.1209791
59. Vétizou, M., Pitt, J. M., Daillère, R., Lepage, P., Waldschmitt, N., Flament, C., et al. (2015). Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350, 1079-1084. doi: 10.1126/science.aad1329
60. Viaud, S., Daillère, R., Boneca, I. G., Lepage, P., Langella, P., Chamaillard, M., et al. (2015). Gut microbiome and anticancer immune response: really hot Sh*t! Cell Death Differ. 22, 199-214. doi: 10.1038/cdd.2014.56
61. Wehkamp, J., Harder, J., Wehkamp, K., Wehkamp-von Meissner, B., Schlee, M., Enders, C., et al. (2004). NF-kappaB-and AP-1-mediated induction of human beta defensin-2 in intestinal epithelial cells by Escherichia coli Nissle 1917: a novel effect of a probiotic bacterium. Infect. Immun. 72, 5750-5758. doi: 10.1128/IAI.72.10.5750-5758.2004
62. Zoumpopoulou, G., Tsakalidou, E., Dewulf, J., Pot, B., and Grangette, C. (2009). Differential crosstalk between epithelial cells, dendritic cells and bacteria in a co-culture model. Int. J. Food Microbiol. 131, 40-51. doi: 10.1016/j.ijfoodmicro.2008.12.037
63. Zyrek, A. A., Cichon, C., Helms, S., Enders, C., Sonnenborn, U., and Schmidt, M. A. (2007). Molecular mechanisms underlying the probiotic effects of Escherichia coli Nissle 1917 involve ZO-2 and PKCzeta redistribution resulting in tight junction and epithelial barrier repair. Cell. Microbiol. 9, 804-816. doi: 10.1111/j.1462-5822.2006.00836.x