Worm proteins of Schistosoma mansoni reduce the severity of experimental chronic colitis in mice by suppressing colonic proinflammatory immune responses

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Heylen, Marthe ^a   Ruyssers, Nathalie E ^a   De Man, Joris G ^a   Timmermans, Jean Pierre ^a   Pelckmans, Paul A ^a,b   Moreels, Tom G ^a,b   De Winter, Benedicte Y ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b ANTWERP UNIVERSITY HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFLAMMATORY AGENT; BIOLOGICAL PRODUCT; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; MESSENGER RNA; MYELOPEROXIDASE; SCHISTOSOMA MANSONI SOLUBLE WORM PROTEIN; UNCLASSIFIED DRUG; HELMINTH PROTEIN; INTERLEUKIN DERIVATIVE;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL TRANSFER; COLONOSCOPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE CLASSIFICATION; DISEASE SEVERITY; DOSE RESPONSE; DOWN REGULATION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL COLITIS; FEMALE; FLOW CYTOMETRY; IMMUNE RESPONSE; IMMUNOMODULATION; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SCHISTOSOMA MANSONI; T LYMPHOCYTE; TREATMENT RESPONSE; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CHRONIC DISEASE; COLITIS; COLON; GENE EXPRESSION; GENETICS; IMMUNOLOGY; INTESTINE MUCOSA; METABOLISM; PATHOLOGY; SCID MOUSE;

MUS; SCHISTOSOMA MANSONI;

ANIMALS; CHRONIC DISEASE; COLITIS; COLON; FEMALE; GENE EXPRESSION; HELMINTH PROTEINS; INTERLEUKINS; INTESTINAL MUCOSA; MICE, INBRED BALB C; MICE, SCID; SCHISTOSOMA MANSONI; T-LYMPHOCYTES;

EID: 84908006899     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110002     Document Type: Article

References (48)

1. Gyires K, Toth EV, Zadori SZ (2014) Gut inflammation: current update on pathophysiology, molecular mechanism and pharmacological treatment modalities. Curr Pharm Des 20: 1063-1081.
2. Speight RA, Mansfield JC (2013) Drug advances in inflammatory bowel disease. Clin Med 13: 378-382.
3. MacDonald TT, Monteleone I, Fantini MC, Monteleone G (2011) Regulation of homeostasis and inflammation in the intestine. Gastroenterology 140: 1768-1775.
4. Pastorelli L, De Salvo C, Mercado JR, Vecchi M, Pizarro TT (2013) Central role of the gut epithelial barrier in the pathogenesis of chronic intestinal inflammation: lessons learned from animal models and human genetics. Front Immunol 4: 280.
5. Knights D, Lassen KG, Xavier RJ (2013) Advances in inflammatory bowel disease pathogenesis: linking host genetics and the microbiome. Gut 62: 1505-1510.
6. Baumgart DC, Carding SR (2007) Inflammatory bowel disease: cause and immunobiology. Lancet 369: 1627-1640.
7. McGuckin MA, Eri R, Simms LA, Florin TH, Radford-Smith G (2009) Intestinal barrier dysfunction in inflammatory bowel diseases. Inflamm Bowel Dis 15: 100-113.
8. Cools N, Ponsaerts P, Van Tendeloo VF, Berneman ZN (2007) Regulatory T cells and human disease. Clin Dev Immunol 2007: 89195.
9. Elliott DE, Urban JJ, Argo CK, Weinstock JV (2000) Does the failure to acquire helminthic parasites predispose to Crohn's disease? Faseb J 14: 1848-1855.
10. Weinstock JV (2012) Autoimmunity: the worm returns. Nature 491: 183-185.
11. Heylen M, Ruyssers NE, Gielis EM, Vanhomwegen E, Pelckmans PA, et al. (2014) Of worms, mice and man: an overview of experimental and clinical helminth-based therapy for inflammatory bowel disease. Pharmacol Ther 143: 153-167.
12. Allen JE, Maizels RM (2011) Diversity and dialogue in immunity to helminths. Nat Rev Immunol 11: 375-388.
13. Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, et al. (2004) Helminth parasites-masters of regulation. Immunol Rev 201: 89-116.
14. Maizels RM, Hewitson JP, Smith KA (2012) Susceptibility and immunity to helminth parasites. Curr Opin Immunol 24: 459-466.
15. Khan AR, Fallon PG (2013) Helminth therapies: translating the unknown unknowns to known knowns. Int J Parasitol 43: 293-299.
16. Weinstock JV, Elliott DE (2013) Translatability of helminth therapy in inflammatory bowel diseases. Int J Parasitol 43: 245-251.
17. Elliott DE, Weinstock JV (2012) Where are we on worms? Curr Opin Gastroenterol 28: 551-556.
18. Summers RW, Elliott DE, Qadir K, Urban JF, Thompson R, et al. (2003) Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am J Gastroenterol 98: 2034-2041.
19. Summers RW, Elliott DE, Urban JF Jr, Thompson R, Weinstock JV (2005) Trichuris suis therapy in Crohn's disease. Gut 54: 87-90.
20. Summers RW, Elliott DE, Urban JF Jr, Thompson RA, Weinstock JV (2005) Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128: 825-832.
21. Sandborn WJ, Elliott DE, Weinstock J, Summers RW, Landry-Wheeler A, et al. (2013) Randomised clinical trial: the safety and tolerability of Trichuris suis ova in patients with Crohn's disease. Aliment Pharmacol Ther 38: 255-263.
22. McSorley HJ, Hewitson JP, Maizels RM (2013) Immunomodulation by helminth parasites: defining mechanisms and mediators. Int J Parasitol 43: 301-310.
23. Ruyssers NE, De Winter BY, De Man JG, Loukas A, Pearson MS, et al. (2009) Therapeutic potential of helminth soluble proteins in TNBS-induced colitis in mice. Inflamm Bowel Dis 15: 491-500.
24. McSorley HJ, Maizels RM (2012) Helminth infections and host immune regulation. Clin Microbiol Rev 25: 585-608.
25. Heylen M, Deleye S, De Man JG, Ruyssers NE, Vermeulen W, et al. (2013) Colonoscopy and microPET/CT are valid techniques to monitor inflammation in the adoptive transfer colitis model in mice. Inflamm Bowel Dis 19: 967-976.
26. Ratcliffe EC, Wilson RA (1991) The magnitude and kinetics of delayed-type hypersensitivity responses in mice vaccinated with irradiated cercariae of Schistosoma mansoni. Parasitology 103: 65-75.
27. Jones LJ, Haugland RP, Singer VL (2003) Development and characterization of the NanoOrange protein quantitation assay: a fluorescence-based assay of proteins in solution. Biotechniques 34: 850-854, 856, 858 passim.
28. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
29. Zaccone P, Fehervari Z, Jones FM, Sidobre S, Kronenberg M, et al. (2003) Schistosoma mansoni antigens modulate the activity of the innate immune response and prevent onset of type 1 diabetes. Eur J Immunol 33: 1439-1449.
30. Moreels TG, Nieuwendijk RJ, De Man JG, De Winter BY, Herman AG, et al. (2004) Concurrent infection with Schistosoma mansoni attenuates inflammation induced changes in colonic morphology, cytokine levels, and smooth muscle contractility of trinitrobenzene sulphonic acid induced colitis in rats. Gut 53: 99-107.
31. Ledeganck KJ, Boulet GA, Horvath CA, Vinckx M, Bogers JJ, et al. (2011) Expression of renal distal tubule transporters TRPM6 and NCC in a rat model of cyclosporine nephrotoxicity and effect of EGF treatment. Am J Physiol 301: F486-493.
32. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
33. Ostanin DV, Pavlick KP, Bharwani S, D'Souza D, Furr KL, et al. (2006) T cell-induced inflammation of the small and large intestine in immunodeficient mice. Am J Physiol 290: G109-119.
34. Bosma MJ, Carroll AM (1991) The SCID mouse mutant - definition, characterization and potential uses. Annu Rev Immunol 9: 323-350.
35. Leithauser F, Meinhardt-Krajina T, Fink K, Wotschke B, Moller P, et al. (2006) Foxp3-expressing CD103+ regulatory T cells accumulate in dendritic cell aggregates of the colonic mucosa in murine transfer colitis. Am J Pathol 168: 1898-1909.
36. Morrissey PJ, Charrier K, Braddy S, Liggitt D, Watson JD (1993) Cd4+ T-cells that express high-levels of Cd45rb induce wasting disease when transferred into congenic severe combined immunodeficient mice - disease development is prevented by cotransfer of purified Cd4+ T-cells. J Exp Med 178: 237-244.
37. Jurjus AR, Khoury NN, Reimund JM (2004) Animal models of inflammatory bowel disease. J Pharmacol Toxicol Methods 50: 81-92.
38. Hang L, Setiawan T, Blum AM, Urban J, Stoyanoff K, et al. (2010) Heligmosomoides polygyrus infection can inhibit colitis through direct interaction with innate immunity. J Immunol 185: 3184-3189.
39. Smith P, Mangan NE, Walsh CM, Fallon RE, McKenzie AN, et al. (2007) Infection with a helminth parasite prevents experimental colitis via a macrophage-mediated mechanism. J Immunol 178: 4557-4566.
40. Hunter MM, Wang A, Parhar KS, Johnston MJ, Van Rooijen N, et al. (2010) In vitro-derived alternatively activated macrophages reduce colonic inflammation in mice. Gastroenterology 138: 1395-1405.
41. Blum AM, Hang L, Setiawan T, Urban JP Jr, Stoyanoff KM, et al. (2012) Heligmosomoides polygyrus bakeri induces tolerogenic dendritic cells that block colitis and prevent antigen-specific gut T cell responses. J Immunol 189: 2512-2520.
42. Donskow-Lysoniewska K, Majewski P, Brodaczewska K, Jozwicka K, Doligalska M (2012) Heligmosmoides polygyrus fourth stages induce protection against DSS-induced colitis and change opioid expression in the intestine. Parasite Immunol 34: 536-546.
43. Schnoeller C, Rausch S, Pillai S, Avagyan A, Wittig BM, et al. (2008) A helminth immunomodulator reduces allergic and inflammatory responses by induction of IL-10-producing macrophages. J Immunol 180: 4265-4272.
44. Du L, Tang H, Ma Z, Xu J, Gao W, et al. (2011) The protective effect of the recombinant 53-kDa protein of Trichinella spiralis on experimental colitis in mice. Dig Dis Sci 56: 2810-2817.
45. Jang SW, Cho MK, Park MK, Kang SA, Na BK, et al. (2011) Parasitic helminth cystatin inhibits DSS-induced intestinal inflammation via IL-10(+)F4/80(+) macrophage recruitment. Korean J Parasitol 49: 245-254.
46. Ferreira I, Smyth D, Gaze S, Aziz A, Giacomin P, et al. (2013) Hookworm excretory/secretory products induce interleukin-4 (IL-4)+ IL-10+ CD4+ T cell responses and suppress pathology in a mouse model of colitis. Infect Immun 81: 2104-2111.
47. Broadhurst MJ, Ardeshir A, Kanwar B, Mirpuri J, Gundra UM, et al. (2012) Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon. PLoS Pathog 8: e1003000.
48. Boukli NM, Delgado B, Ricaurte M, Espino AM (2011) Fasciola hepatica and Schistosoma mansoni: identification of common proteins by comparative proteomic analysis. J Parasitol 97: 852-861.