Paracellular entry of interleukin-10 producing Lactococcus lactis in inflamed intestinal mucosa in mice

Inflammatory Bowel Diseases

Volumn 14, Issue 4, 2008, Pages 471-479

  Waeytens, Anouk ^a   Ferdinande, Liesbeth ^a   Neirynck, Sabine ^b,d   Rottiers, Pieter ^a,d   De Vos, Martine ^c   Steidler, Lothar ^b,d   Cuvelier, Claude A ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c GHENT UNIVERSITY HOSPITAL   (Belgium)

^d ActoGeniX NV   (Belgium)

Author keywords

Inflammatory bowel disease; Interleukin 10 therapy; Intestinal mucosa; Lactococcus lactis

Indexed keywords

INTERLEUKIN 10;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL VIABILITY; COLITIS; CONTROLLED STUDY; IMMUNOBLOTTING; INTESTINE MUCOSA; LACTOCOCCUS LACTIS; MOUSE; MUCOSA INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; COLITIS; COLON; GENETIC ENGINEERING; ILEUM; INTERLEUKIN-10; INTESTINAL MUCOSA; LACTOCOCCUS LACTIS; MICE; MICE, INBRED BALB C; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION;

EID: 42449120971     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1002/ibd.20346     Document Type: Article

References (38)

1. Kucharzik T, Maaser C, Lugering A, et al. Recent understanding of IBD pathogenesis: implications for future therapies. Inflamm Bowel Dis. 2006;12:1068-1083.
2. Moore KW, de Waal MR, Coffman RL, et al. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol. 2001;19:683-765.
3. Kuhn R, Lohler J, Rennick D, et al. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993;75:263-274.
4. Powrie F, Leach MW, Mauze S, et al. Inhibition of Th1 responses prevents inflammatory bowel disease in scid mice reconstituted with CD45RBhi CD4+ T cells. Immunity. 1994;1:553-562.
5. Herfarth HH, Mohanty SP, Rath HC, et al. Interleukin 10 suppresses experimental chronic, granulomatous inflammation induced by bacterial cell wall polymers. Gut. 1996;39:836-845.
6. Barbara G, Xing Z, Hogaboam CM, et al. Interleukin 10 gene transfer prevents experimental colitis in rats. Gut. 2000;46:344-349.
7. Fedorak RN, Gangl A, Elson CO, et al. Recombinant human interleukin 10 in the treatment of patients with mild to moderately active Crohn's disease. The Interleukin 10 Inflammatory Bowel Disease Cooperative Study Group. Gastroenterology. 2000;119:1473-1482.
8. Schreiber S, Fedorak RN, Nielsen OH, et al. Safety and efficacy of recombinant human interleukin 10 in chronic active Crohn's disease. Crohn's Disease IL-10 Cooperative Study Group. Gastroenterology. 2000;119:1461-1472.
9. Steidler L. Hans W, Schotte L, et al. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science. 2000;289:1352-1355.
10. Braat H, Rottiers P, Hommes DW, et al. A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease. Clin Gastroenterol Hepatol. 2006;4:754-759.
11. Steidler L, Neirynck S, Huyghebaert N, et al. Biological containment of genetically modified Lactococcus lactis for intestinal delivery of human interleukin 10. Nat Biotechnol. 2003;21:785-789.
12. Okayasu I, Hatakeyama S, Yamada M, et al. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology. 1990;98:694-702.
13. Sellon RK, Tonkonogy S, Schultz M, et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun. 1998;66:5224-5231.
14. Rath HC, Schultz M, Freitag R, et al. Different subsets of enteric bacteria induce and perpetuate experimental colitis in rats and mice. Infect Immun. 2001;69:2277-2285.
15. Berg DJ, Davidson N, Kuhn R, et al. Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses. J Clin Invest. 1996;98:1010-1020.
16. Cruickshank SM, English NR, Felsburg PJ, et al. Characterization of colonic dendritic cells in normal and colitic mice. World J Gastroenterol. 2005;11:6338-6347.
17. Macpherson AJ, Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science. 2004;303:1662-1665.
18. Keita AV, Gullberg E, Ericson AC, et al. Characterization of antigen and bacterial transport in the follicle-associated epithelium of human ileum. Lab Invest. 2006;86:504-516.
19. Rescigno M, Urbano M, Valzasina B, et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol. 2001;2:361-367.
20. Rescigno M, Rotta G, Valzasina B, et al. Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology. 2001;204:572-581.
21. Vallon-Eberhard A, Landsman L, Yogev N, et al. Transepithelial pathogen uptake into the small intestinal lamina propria. Journal of Immunology. 2006;176:2465-2469.
22. McCormick DA, Horton LW, Mee AS. Mucin depletion in inflammatory bowel disease. J Clin Pathol. 1990;43:143-146.
23. Sartor RB. The influence of normal microbial flora on the development of chronic mucosal inflammation. Res Immunol. 1997;148:567-576.
24. Clayburgh DR, Shen L, Turner JR. A porous defense: the leaky epithelial barrier in intestinal disease. Laboratory Investigation. 2004;84:282-291.
25. Kleessen B, Kroesen AJ, Buhr HJ, et al. Mucosal and invading bacteria in patients with inflammatory bowel disease compared with controls. Scand J Gastroenterol. 2002;37:1034-1041.
26. Swidsinski A, Ladhoff A, Pernthaler A, et al. Mucosal flora in inflammatory bowel disease. Gastroenterology. 2002:122:44-54.
27. Swidsinski A, Loening-Baucke V, Lochs H, et al. Spatial organization of bacterial flora in normal and inflamed intestine: a fluorescence in situ hybridization study in mice. World J Gastroenterol. 2005;11:1131-1140.
28. van Deventer SJ, Elson CO, Fedorak RN. Multiple doses of intravenous interleukin 10 in steroid-refractory Crohn's disease. Crohn's Disease Study Group. Gastroenterology. 1997;113:383-389.
29. Colombel JF, Rutgeerts P, Malchow H, et al. Interleukin 10 (Tenovil) in the prevention of postoperative recurrence of Crohn's disease. Gut. 2001;49:42-46.
30. Lauw FN, Pajkrt D, Hack CE, et al. Proinflammatory effects of IL-10 during human endotoxemia. J Immunol. 2000;165:2783-2789.
31. Tilg H, Van Montfrans C, van den Ende A, et al. Treatment of Crohn's disease with recombinant human interleukin 10 induces the proinflammatory cytokine interferon gamma. Gut. 2002;50:191-195.
32. Lindsay JO, Ciesielski CJ, Scheinin T, et al. Local delivery of adenoviral vectors encoding murine interleukin 10 induces colonic interleukin 10 production and is therapeutic for murine colitis. Gut. 2003;52:981-987.
33. Van Montfrans C, Rodriguez Pena MS, et al. Prevention of colitis by interleukin 10-transduced T lymphocytes in the SCID mice transfer model. Gastroenterology. 2002;123:1865-1876.
34. Nakase H, Okazaki K, Tabata Y, et al. New cytokine delivery system using gelatin microspheres containing interleukin-10 for experimental inflammatory bowel disease. J Pharmacol Exp Ther. 2002;301:59-65.
35. Huyghebaert N, Vermeire A, Neirynck S, et al. Evaluation of extrusion/spheronisation, layering and compaction for the preparation of an oral, multi-particulate formulation of viable, hIL-10 producing Lactococcus lactis. Eur J Pharm Biopharm. 2005;59:9-15.
36. Huyghebaert N, Vermeire A, Neirynck S, et al. Development of an enteric-coated formulation containing freeze-dried, viable recombinant Lactococcus lactis for the ileal mucosal delivery of human interleukin-10. Eur J Pharm Biopharm. 2005;60:349-359.
37. Termont S, Vandenbroucke K, Iserentant D, et al. Intracellular accumulation of trehalose protects Lactococcus lactis from freeze-drying damage and bile toxicity and increases gastric acid resistance. Appl Environ Microbiol. 2006;72:7694-700.
38. Braat H, Steidler L, Neirynck S, et al. Turbo-probiotics as a tool for cell-based (mucosal) delivery of interleukin-10. Gastroenterology. 2005;128:A5.