A transgenic probiotic secreting a parasite immunomodulator for site-directed treatment of gut inflammation

Molecular Therapy

Volumn 22, Issue 10, 2014, Pages 1730-1740

  Whelan, Rose A ^a   Rausch, Sebastian ^a   Ebner, Friederike ^a   Günzel, Dorothee ^b   Richter, Jan F ^b,c   Hering, Nina A ^b   Schulzke, Jörg Dieter ^b   Kühl, Anja A ^b   Keles, Ahmed ^b   Janczyk, Pawel ^d   Nöckler, Karsten ^d   Wieler, Lothar H ^a   Hartmann, Susanne ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^d FEDERAL INSTITUTE FOR RISK ASSESSMENT   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTATIN; INTERLEUKIN 17; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; PROBIOTIC AGENT; RANTES; CHEMOKINE; IMMUNOLOGIC FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG MEGADOSE; DRUG SAFETY; DRUG TOLERABILITY; ENTERITIS; ESCHERICHIA COLI; ESCHERICHIA COLI NISSLE 1917; FOXP3+ REGULATORY T LYMPHOCYTE; INTESTINE MUCOSA PERMEABILITY; MACROPHAGE ACTIVATION; MALE; MOUSE; NONHUMAN; PIGLET; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; ANIMAL; BIOSYNTHESIS; CHEMICALLY INDUCED; DISEASE MODEL; GASTROENTERITIS; GENE EXPRESSION; GENETICS; IMMUNOLOGY; INTESTINE MUCOSA; METABOLISM; PARASITOLOGY; PATHOLOGY; PIG;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI NISSLE 1917; MURINAE; SUIDAE; VERMES;

ANIMALS; CHEMOKINES; COLITIS; CYSTATINS; DISEASE MODELS, ANIMAL; ESCHERICHIA COLI; GASTROENTERITIS; GENE EXPRESSION; IMMUNOLOGIC FACTORS; INTESTINAL MUCOSA; MALE; MICE; PROBIOTICS; SWINE;

EID: 84926186891     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2014.125     Document Type: Article

References (49)

1. Whelan, RA, Hartmann, S and Rausch, S (2012). Nematode modulation of inflammatory bowel disease. Protoplasma 249: 871-886.
2. Summers, RW, Elliott, DE, Urban, JF Jr., Thompson, RA and Weinstock, JV (2005). Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128: 825-832.
3. McSorley, HJ, Hewitson, JP and Maizels, RM (2013). Immunomodulation by helminth parasites: defining mechanisms and mediators. Int J Parasitol 43: 301-310.
4. Klotz, C, Ziegler, T, Daniowicz-Luebert, E and Hartmann, S (2011). Cystatins of parasitic organisms. Adv Exp Med Biol 712: 208-221.
5. Schierack, P, Lucius, R, Sonnenburg, B, Schilling, K and Hartmann, S (2003). Parasitespecific immunomodulatory functions of filarial cystatin. Infect Immun 71: 2422-2429.
6. Schnoeller, C, Rausch, S, Pillai, S, Avagyan, A, Wittig, BM, Loddenkemper, C et al. (2008). A helminth immunomodulator reduces allergic and inflammatory responses by induction of IL-10-producing macrophages. J Immunol 180: 4265-4272.
7. Daniowicz-Luebert, E, Steinfelder, S, Kühl, AA, Drozdenko, G, Lucius, R, Worm, M et al. (2013). A nematode immunomodulator suppresses grass pollen-specific allergic responses by controlling excessive Th2 inflammation. Int J Parasitol 43: 201-210.
8. Klotz, C, Ziegler, T, Figueiredo, AS, Rausch, S, Hepworth, MR, Obsivac, N et al. (2011). A helminth immunomodulator exploits host signaling events to regulate cytokine production in macrophages. PLoS Pathog 7: e1001248.
9. Anderson, CA, Boucher, G, Lees, CW, Franke, A, D'Amato, M, Taylor, KD et al. (2011). Meta-Analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat Genet 43: 246-252.
10. Jacobi, CA and Malfertheiner, P (2011). Escherichia coli Nissle 1917 (Mutaflor): new insights into an old probiotic bacterium. Dig Dis 29: 600-607.
11. 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.
12. Garrido-Mesa, N, Utrilla, P, Comalada, M, Zorrilla, P, Garrido-Mesa, J, Zarzuelo, A et al. (2011). The association of minocycline and the probiotic Escherichia coli Nissle 1917 results in an additive beneficial effect in a DSS model of reactivated colitis in mice. Biochem Pharmacol 82: 1891-1900.
13. Altenhoefer, A, Oswald, S, Sonnenborn, U, Enders, C, Schulze, J, Hacker, J et al. (2004). The probiotic Escherichia coli strain Nissle 1917 interferes with invasion of human intestinal epithelial cells by different enteroinvasive bacterial pathogens. FEMS Immunol Med Microbiol 40: 223-229.
14. Schierack, P, Kleta, S, Tedin, K, Babila, JT, Oswald, S, Oelschlaeger, TA et al. (2011). E. coli Nissle 1917 Affects Salmonella adhesion to porcine intestinal epithelial cells. PLoS One 6: e14712.
15. Hering, NA, Richter, JF, Fromm, A, Wieser, A, Hartmann, S, Günzel, D et al. (2014). TcpC protein from E. coli Nissle improves epithelial barrier function involving PKC? and ERK1/2 signaling in HT-29/B6 cells. Mucosal Immunol 7: 369-378.
16. Ukena, SN, 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.
17. Sturm, A, Rilling, K, Baumgart, DC, 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.
18. Westendorf, AM, Gunzer, F, Deppenmeier, S, Tapadar, D, Hunger, JK, Schmidt, MA et al. (2005). Intestinal immunity of Escherichia coli NISSLE 1917: a safe carrier for therapeutic molecules. FEMS Immunol Med Microbiol 43: 373-384.
19. Waddell, A, Ahrens, R, Steinbrecher, K, Donovan, B, Rothenberg, ME, Munitz, A et al. (2011). Colonic eosinophilic inflammation in experimental colitis is mediated by Ly6C(high) CCR2(+) inflammatory monocyte/macrophage-derived CCL11. J Immunol 186: 5993-6003.
20. Izcue, A, Hue, S, Buonocore, S, Arancibia-Cárcamo, CV, Ahern, PP, Iwakura, Y et al. (2008). Interleukin-23 restrains regulatory T cell activity to drive T cell-dependent colitis. Immunity 28: 559-570.
21. Stritesky, GL, Yeh, N and Kaplan, MH (2008). IL-23 promotes maintenance but not commitment to the Th17 lineage. J Immunol 181: 5948-5955.
22. Meurens, F, Summerfield, A, Nauwynck, H, Saif, L and Gerdts, V (2012). The pig: a model for human infectious diseases. Trends Microbiol 20: 50-57.
23. Huang, Y, Gauvreau, H and Harding, J (2012). Diagnostic investigation of porcine periweaning failure-to-thrive syndrome: lack of compelling evidence linking to common porcine pathogens. J Vet Diagn Invest 24: 96-106.
24. Pié, S, Lallés, JP, Blazy, F, Laffitte, J, Séve, B and Oswald, IP (2004). Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. J Nutr 134: 641-647.
25. Pedersen, KS, Kristensen, CS and Nielsen, JP (2012). Demonstration of non-specific colitis and increased crypt depth in colon of weaned pigs with diarrhea. Vet Q 32: 45-49.
26. Veltman, K, Hummel, S, Cichon, C, Sonnenborn, U and Schmidt, MA (2012). Identification of specific miRNAs targeting proteins of the apical junctional complex that simulate the probiotic effect of E. coli Nissle 1917 on T84 epithelial cells. Int J Biochem Cell Biol 44: 341-349.
27. Zyrek, AA, Cichon, C, Helms, S, Enders, C, Sonnenborn, U and Schmidt, MA (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.
28. Matthes, H, Krummenerl, T, Giensch, M, Wolff, C and Schulze, J (2010). Clinical trial: probiotic treatment of acute distal ulcerative colitis with rectally administered Escherichia coli Nissle 1917 (EcN). BMC Complement Altern Med 10: 13.
29. Schultz, M, Strauch, UG, Linde, HJ, Watzl, S, Obermeier, F, Göttl, C et al. (2004). Preventive effects of Escherichia coli strain Nissle 1917 on acute and chronic intestinal inflammation in two different murine models of colitis. Clin Diagn Lab Immunol 11: 372-378.
30. Rollins, BJ (1997). Chemokines. Blood 90: 909-928.
31. Banks, C, Bateman, A, Payne, R, Johnson, P and Sheron, N (2003). Chemokine expression in IBD. Mucosal chemokine expression is unselectively increased in both ulcerative colitis and Crohn's disease. J Pathol 199: 28-35.
32. Mazzucchelli, L, Hauser, C, Zgraggen, K, Wagner, HE, Hess, MW, Laissue, JA et al. (1996). Differential in situ expression of the genes encoding the chemokines MCP-1 and RANTES in human inflammatory bowel disease. J Pathol 178: 201-206.
33. Ito, R, Kita, M, Shin-Ya, M, Kishida, T, Urano, A, Takada, R et al. (2008). Involvement of IL-17A in the pathogenesis of DSS-induced colitis in mice. Biochem Biophys Res Commun 377: 12-16.
34. Unutmaz, D and Pulendran, B (2009). The gut feeling of Treg cells: IL-10 is the silver lining during colitis. Nat Immunol 10: 1141-1143.
35. Korn, T, Bettelli, E, Oukka, M and Kuchroo, VK (2009). IL-17 and Th17 Cells. Annu Rev Immunol 27: 485-517.
36. Fina, D, Sarra, M, Fantini, MC, Rizzo, A, Caruso, R, Caprioli, F et al. (2008). Regulation of gut inflammation and th17 cell response by interleukin-21. Gastroenterology 134: 1038-1048.
37. Shaw, MH, Kamada, N, Kim, YG and Núñez, G (2012). Microbiota-induced IL-1?, but not IL-6, is critical for the development of steady-state TH17 cells in the intestine. J Exp Med 209: 251-258.
38. Mucida, D, Park, Y, Kim, G, Turovskaya, O, Scott, I, Kronenberg, M et al. (2007). Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317: 256-260.
39. Liu, H, Yao, S, Dann, SM, Qin, H, Elson, CO and Cong, Y (2013). ERK differentially regulates Th17-And Treg-cell development and contributes to the pathogenesis of colitis. Eur J Immunol 43: 1716-1726.
40. Huber, S, Gagliani, N, Esplugues, E, O'Connor, W Jr., Huber, FJ, Chaudhry, A et al. (2011). Th17 cells express interleukin-10 receptor and are controlled by Foxp3? and Foxp3+ regulatory CD4+ T cells in an interleukin-10-dependent manner. Immunity 34: 554-565.
41. Kleta, S, Steinrück, H, Breves, G, Duncker, S, Laturnus, C, Wieler, LH et al. (2006). Detection and distribution of probiotic Escherichia coli Nissle 1917 clones in swine herds in Germany. J Appl Microbiol 101: 1357-1366.
42. Hu, C, Song, J, Li, Y, Luan, Z and Zhu, K (2013). Diosmectite-zinc oxide composite improves intestinal barrier function, modulates expression of proinflammatory cytokines and tight junction protein in early weaned pigs. Br J Nutr 110: 681-688.
43. Watson, CJ, Hoare, CJ, Garrod, DR, Carlson, GL and Warhurst, G (2005). Interferon-gamma selectively increases epithelial permeability to large molecules by activating different populations of paracellular pores. J Cell Sci 118(Pt 22): 5221-5230.
44. Choi, HJ, Ahn, JH, Park, SH, Do, KH, Kim, J and Moon, Y (2012). Enhanced wound healing by recombinant Escherichia coli Nissle 1917 via human epidermal growth factor receptor in human intestinal epithelial cells: therapeutic implication using recombinant probiotics. Infect Immun 80: 1079-1087.
45. Yuvaraj, S, Peppelenbosch, MP and Bos, NA (2007). Transgenic probiotica as drug delivery systems: the golden bullet? Expert Opin Drug Deliv 4: 1-3.
46. Hold, GL, Smith, M, Grange, C, Watt, ER, El-Omar, EM and Mukhopadhya, I (2014). Role of the gut microbiota in inflammatory bowel disease pathogenesis: what have we learnt in the past 10 years? World J Gastroenterol 20: 1192-1210.
47. Tesseur, I, Zou, K, Berber, E, Zhang, H and Wyss-Coray, T (2006). Highly sensitive and specific bioassay for measuring bioactive TGF-beta. BMC Cell Biol 7: 15.
48. Pieper, R, Kröger, S, Richter, JF, Wang, J, Martin, L, Bindelle, J et al. (2012). Fermentable fiber ameliorates fermentable protein-induced changes in microbial ecology, but not the mucosal response, in the colon of piglets. J Nutr 142: 661-667.
49. Kreusel, KM, Fromm, M, Schulzke, JD and Hegel, U (1991). Cl-secretion in epithelial monolayers of mucus-forming human colon cells (HT-29/B6). Am J Physiol 261(4 Pt 1): C574-C582.