Characterization of the immuno-regulatory response to the tapeworm Hymenolepis diminuta in the non-permissive mouse host

International Journal for Parasitology

Volumn 37, Issue 3-4, 2007, Pages 393-403

  Persaud, Robin ^a   Wang, Arthur ^a   Reardon, Colin ^a   McKay, Derek M ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Alternatively activated macrophages; CD4 cells; Colitis; Helminth rejection; Intestine; Regulatory T cells; TH2 cytokines

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 9;

ANTIPARASITE DEFENSE; DISEASE RESISTANCE; FLATWORM; HOST-PATHOGEN INTERACTION; IMMUNE RESPONSE; INFECTIOUS DISEASE; RODENT;

ARTICLE; CESTODE; HELPER CELL; HYMENOLEPIS DIMINUTA; IMMUNE RESPONSE; IMMUNOREGULATION; INFLAMMATION; JEJUNUM; LYMPH NODE; MESENTERY; NONHUMAN; SPLEEN; WILD TYPE;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; COLITIS; CYTOKINES; DINITROFLUOROBENZENE; DISEASE SUSCEPTIBILITY; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HOST-PARASITE RELATIONS; HYMENOLEPIASIS; HYMENOLEPIS DIMINUTA; INTERLEUKIN-10; INTESTINAL MUCOSA; ION TRANSPORT; JEJUNUM; MACROPHAGE ACTIVATION; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; RNA, MESSENGER; T-LYMPHOCYTES, REGULATORY;

HYMENOLEPIS DIMINUTA; MUS; VERMES;

EID: 33846808667     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2006.09.012     Document Type: Article

References (45)

1. Allez M., and Mayer L. Regulatory T cells: peace keepers in the gut. Inflamm. Bowel. Dis. 10 (2004) 666-676
2. Artis D. New weapons in the war on worms: identification of putative mechanisms of immune-mediated expulsion of gastrointestinal nematodes. Int. J. Parasitol. 36 (2006) 723-733
3. Balmer P., and Devaney E. NK T cells are a source of early interleukin-4 following infection with third-stage larvae of the filarial nematode Brugia pahangi. Infect. Immun. 70 (2002) 2215-2219
4. + Tregs. J. Clin. Invest. 115 (2005) 2904-2913
5. Castro G.A. Immunophysiology of enteric parasitism. Parasitol. Today 5 (1989) 11-19
6. Contigli C., Silva-Teixeira D.N., Del Prete G., D'Elios M.M., De Carli M., Manghetti M., Amedei A., Almerigogno F., Lambertucci J.R., and Goes A.M. Phenotype and cytokine profile of Schistosoma mansoni specific T cell lines and clones derived from schistosomiasis patients with distinct clinical forms. Clin. Immunol. 91 (1999) 338-344
7. Elliott D.E., Urban Jr. J.F., Argo C.K., and Weinstock J.V. Does failure to acquire helminthic parasites predispose to Crohn's disease?. FASEB J. 14 (2000) 1848-1855
8. Elliott D.E., Setiawan T., Metwali A., Blum A., Urban Jr. J.F., and Weinstock J.V. Heligmosomoides polygyrus inhibits established colitis in IL-10-deficient mice. Eur. J. Immunol. 34 (2004) 2690-2698
9. Elliott D.E., Summers R.W., and Weinstock J.V. Helminths and the modulation of mucosal inflammation. Curr. Opin. Gastroenterol. 21 (2005) 51-58
10. Fallon P.G., Ballantyne S.J., Mangan N.E., Dasvarma A., McIlgorm A., Jolin H.E., and McKenzie A.N. Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J. Exp. Med. 203 (2006) 1105-1116
11. + T cells. J. Immunol. 172 (2004) 5149-5153
12. Finkelman F.D., Shea-Donohue T., Goldhill J., Sullivan C.A., Morris S.C., Madden K.B., Gause W.C., and Urban Jr. J.F. Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Ann. Rev. Immunol. 15 (1997) 505-533
13. - secretion and parasite rejection in rat intestine. J. Immunol. 138 (1987) 1250-1255
14. Hayes K.S., Bancroft A.J., and Grencis R.K. Immune-mediated regulation of chronic intestinal nematode infection. Immunol. Rev. 201 (2004) 75-88
15. Hunter M.M., Wang A., Hirota C.L., and McKay D.M. Neutralizing anti-IL-10 antibody blocks the protective effect of tapeworm infection in a murine model of chemically-induced colitis. J. Immunol. 174 (2005) 7368-7375
16. Khan W.I., and Collins S.M. Immune-mediated alteration in gut physiology and its' role in host defense in nematode infection. Parasite Immunol. 26 (2004) 319-326
17. La Flamme A.C., Ruddenklau K., and Backstrom B.T. Schistosomiasis decreases central nervous system inflammation and alters the progression of experimental autoimmune encephalomyelitis. Infect. Immun. 71 (2003) 4996-5004
18. Little M.C., Bell L.V., Cliffe L.J., and Else K.J. The characterization of intraepithelial lymphocytes, lamina propria leukocytes, and isolated lymphoid follicles in the large intestine of mice infected with the intestinal nematode parasite Trichuris muris. J. Immunol. 175 (2005) 6713-6722
19. Maizels R.M., and Holland M.J. Parasite immunology: pathways for expelling intestinal helminths. Curr. Biol. 8 (1998) R711-R714
20. Maizels R.M., Balic A., Gomez-Escobar N., Nair M., Taylor M.D., and Allen J.E. Helminth parasites-masters of regulation. Immunol. Rev. 201 (2004) 89-116
21. Masson S.D., McKay D.M., Stead R.H., Agro A., Stanisz A., and Perdue M.H. Nippostrongylus brasiliensis infection causes neuronal abnormalities and altered neurally regulated ion secretion in rat jejunum. Parasitology 113 (1996) 173-182
22. McDermott J.R., Humphreys N.E., Forman S.P., Donaldson D.D., and Grencis R.K. Intraepithelial NK cell-derived IL-13 induces intestinal pathology associated with nematode infection. J. Immunol. 175 (2005) 3207-3213
23. McKay D.M. The beneficial helminth parasite?. Parasitology 132 (2006) 1-12
24. McKay D.M., and Fairweather I. A role for the enteric nervous system in the response to helminth infections. Parasitol. Today 13 (1997) 63-69
25. McKay D.M., and Khan W.I. STAT-6 is an absolute requirement for murine rejection of Hymenolepis diminuta. J. Parasitol. 89 (2003) 188-189
26. McKay D.M., Halton D.W., Johnston C.F., Fairweather I., and Shaw C. Hymenolepis diminuta: changes in intestinal morphology and the enterochromaffin cell population associated with infection in male C57 mice. Parasitology 101 (1990) 107-113
27. McKay D.M., Halton D.W., McCaigue M.D., Johnston C.F., Fairweather I., and Shaw C. Hymenolepis diminuta: intestinal goblet cell response in male C57 mice. Exp. Parasitol. 71 (1990) 9-20
28. McKay D.M., Halton D.W., Shaw C., Johnston C.F., Fairweather I., and Buchanan K.D. Hymenolepis diminuta: changes in the levels of certain intestinal regulatory peptides in infected C57 mice. Exp. Parasitol. 73 (1991) 15-26
29. McKay D.M., Benjamin M., Baca-Estrada M., D'Inca R., Croitoru K., and Perdue M.H. Role of T lymphocytes in secretory response to an enteric nematode parasite: studies in athymic rats. Dig. Dis. Sci. 40 (1995) 331-337
30. + T cells mediate superantigen-induced abnormalities in murine jejunal ion transport. Am. J. Physiol. (Gastrointest. Liver Physiol.) 275 (1998) G29-G38
31. + regulatory T cells in the intestine by Heligmosomoides polygyrus infection. Am. J. Physiol. (Gastrointest. Liver Physiol.) 291 (2006) G253-G259
32. Nair M.G., Gallagher I.J., Taylor M.D., Loke P., Coulson P.S., Wilson R.A., Maizels R.M., and Allen J.E. Chitinase and Fizz family members are a generalized feature of nematode infection with selective up-regulation of Ym1 and Fizz1 by antigen-presenting cells. Infect. Immun. 73 (2005) 385-394
33. Owang A.M., Zaph C., Wilson E.H., Guild K.J., McClanahan, Miller H.R., Cua D.J., Goldschmidt M., Hunter C.A., Kastelein R.A., and Artis D. Interleukin 25 regulates type 2 cytokine-dependent immunity and limits chronic inflammation in the gastrointestinal tract. J. Exp. Med. 203 (2006) 843-849
34. Palmas C., Bortoletti G., Gabriele F., Wakelin, and Conchedda M. Cytokine production during infection with Hymenolepis diminuta in Balb/c mice. Int. J. Parasitol. 27 (1997) 855-859
35. Reardon C., Sanchez A., Hogaboam C.M., and McKay D.M. Tapeworm infection reduces the ion transport abnormalities induced by dextran sulphate sodium (DSS) colitis. Infect. Immun. 69 (2001) 4417-4423
36. Rodriguez-Sosa M., Saavedra R., Tenorio E.P., Rosas L.E., Satoskar A.R., and Terrazas L.I. A STAT4-dependent Th1 response is required for resistance to the helminth parasite Taenia crassiceps. Infect. Immun. 72 (2004) 4552-4560
37. Russel D.A., and Castro G.A. Immunological regulation of colonic ion transport. Am. J. Physiol. 26 (1989) G396-G403
38. Shea-Donohue T., Sullivan C., Finkelman F.D., Madden F.D., Morris S.C., Goldhill J., Pineiro-Carrero V., and Urban Jr. J.F. The role of IL-4 in Heligosomoides polygyrus-induced alterations in murine intestinal epithelial cell function. J. Immunol. 167 (2001) 2234-2239
39. Smith P.D., Smythies L.E., Mosteller-Barnum M., Sibley D.A., Russell M.W., Merger M., Sellers M.T., Orenstein J.M., Shimada T., Graham M.F., and Kubagawa H. Intestinal macrophages lack CD14 and CD89 and consequently are down-regulated for LPS- and IgA-mediated activities. J. Immunol. 167 (2001) 2651-2656
40. Summers R.W., Elliott D.E., Urban Jr. J.F., Thompson R., and Weinstock J.V. Trichuris suis therapy in Crohn's disease. Gut 54 (2005) 87-90
41. Tyzanik A.J., Sun J.C., and Bevan M.J. The CD8 population in CD4-deficient mice is heavily contaminated with MHC class II-restricted T cells. J. Exp. Med. 16 (2004) 559-565
42. Velazquez P., Wei B., and Braun J. Surveillance B lymphocytes and mucosal immunoregulation. Springer Semin. Immunopathol. 26 (2005) 453-462
43. Walker M., Baz A., Dematteis S., Stettler M., Gottstein B., Schaller J., and Hemphill A. Isolation and characterization of a secretory component of Echinococcus multiocularis metacestodes potentially involved in modulating the host-parasite interface. Infect. Immun. 72 (2004) 527-536
44. Wilson M.S., Taylor M.D., Balic A., Finney C.A., Lamb J.R., and Maizels R.M. Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J. Exp. Med. 202 (2005) 1199-1212
45. Yazdanbakhsh M., van den Biggelaar A., and Maizels R.M. Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol. 22 (2001) 372-377