A time course study of immunological responses in Trichuris suis infected pigs demonstrates induction of a local type 2 response associated with worm burden

International Journal for Parasitology

Volumn 36, Issue 8, 2006, Pages 915-924

  Kringel, Helene ^a   Iburg, Tine ^a   Dawson, Harry ^b   Aasted, Bent ^a   Roepstorff, Allan ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b BELTSVILLE HUMAN NUTRITION RESEARCH CENTER   (United States)

Author keywords

Eosinophils; Immune response; Mast cells; Trichuris suis

Indexed keywords

ARGININE; B7 ANTIGEN; CD3 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; CHEMOKINE RECEPTOR CCR3; FC EPSILON 1 ALPHA RECEPTOR; FC RECEPTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 13 RECEPTOR ALPHA1; INTERLEUKIN 13 RECEPTOR ALPHA2; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR ALPHA; INTERLEUKIN 5; MUCIN 5AC; TUMOR NECROSIS FACTOR ALPHA;

GENE EXPRESSION; HOST-PARASITE INTERACTION; IMMUNE RESPONSE; NEMATODE; PIG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; ASCENDING COLON; AUTOPSY; COLON MUCOSA; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENTERITIS; FEMALE; GENETIC TRANSCRIPTION; GOBLET CELL; HISTOPATHOLOGY; HYPERTROPHY; IMMUNE FUNCTION TEST; IMMUNOMODULATION; IMMUNOREACTIVITY; INOCULATION; INTESTINE CRYPT; INTESTINE INFECTION; LYMPHOCYTIC INFILTRATION; MALE; MAST CELL; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; SPECIES COMPARISON; SWINE; TH1 CELL; TH2 CELL; TISSUE SECTION; TRICHURIASIS; TRICHURIS; TRICHURIS SUIS; WORM INFECTION;

ANIMALS; CYTOKINES; EOSINOPHILS; FEMALE; FLOW CYTOMETRY; HISTOCYTOCHEMISTRY; IMMUNOPHENOTYPING; INTESTINAL DISEASES, PARASITIC; INTESTINAL MUCOSA; MALE; MAST CELLS; RANDOM ALLOCATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; SWINE; SWINE DISEASES; TRICHURIASIS; TRICHURIS;

TRICHURIS SUIS; VERMES;

EID: 33748697948     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2006.04.008     Document Type: Article

References (86)

1. Abdallahi O.M., Bensalem H., Augier R., Diagana M., De Reggi M., and Gharib B. Arginase expression in peritoneal macrophages and increase in circulating polyamine levels in mice infected with Schistosoma mansoni. Cell Mol. Life Sci. 58 (2001) 1350-1357
2. Abner S.R., Hill D.E., Turner J.R., Black E.D., Bartlett P., Urban J.F., and Mansfield L.S. Response of intestinal epithelial cells to Trichuris suis excretory-secretory products and the influence on Campylobacter jejuni invasion under in vitro conditions. J. Parasitol. 88 (2002) 738-745
3. Armitage R.J., Fanslow W.C., Strockbine L., Sato T.A., Clifford K.N., Macduff B.M., Anderson D.M., Gimpel S.D., vis-Smith T., and Maliszewski C.R. Molecular and biological characterization of a murine ligand for CD40. Nature 357 (1992) 80-82
4. Artis D., Humphreys N.E., Bancroft A.J., Rothwell N.J., Potten C.S., and Grencis R.K. Tumor necrosis factor alpha is a critical component of interleukin 13-mediated protective T helper cell type 2 responses during helminth infection. J. Exp. Med. 190 (1999) 953-962
5. Artis D., Potten C.S., Else K.J., Finkelman F.D., and Grencis R.K. Trichuris muris: host intestinal epithelial cell hyperproliferation during chronic infection is regulated by interferon-gamma. Exp. Parasitol. 92 (1999) 144-153
6. Bancroft A.J., McKenzie A.N., and Grencis R.K. A critical role for IL-13 in resistance to intestinal nematode infection. J. Immunol. 160 (1998) 3453-3461
7. Bancroft A.J., Artis D., Donaldson D.D., Sypek J.P., and Grencis R.K. Gastrointestinal nematode expulsion in IL-4 knockout mice is IL-13 dependent. Eur. J. Immunol. 30 (2000) 2083-2091
8. Beer R.J. Studies on the biology of the life-cycle of Trichuris suis Schrank, 1788. Parasitology 67 (1973) 253-262
9. Beer R.J. The relationship between Trichuris trichiura (Linnaeus 1758) of man and Trichuris suis (Schrank 1788) of the pig. Res. Vet. Sci. 20 (1976) 47-54
10. Beer R.J., and Rutter J.M. Spirochaetal invasion of the colonic mucosa in a syndrome resembling swine dysentery following experimental Trichuris suis infection in weaned pigs. Res. Vet. Sci. 13 (1972) 593-595
11. Belkaid Y., Piccirillo C.A., Mendez S., Shevach E.M., and Sacks D.L. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 420 (2002) 502-507
12. Betts C.J., and Else K.J. Mast cells, eosinophils and antibody-mediated cellular cytotoxicity are not critical in resistance to Trichuris muris. Parasite Immunol. 21 (1999) 45-52
13. Bischoff S.C., Sellge G., Lorentz A., Sebald W., Raab R., and Manns M.P. IL-4 enhances proliferation and mediator release in mature human mast cells. Proc. Natl Acad. Sci. USA 96 (1999) 8080-8085
14. Boes J., and Helwigh A.B. Animal models of intestinal nematode infections of humans. Parasitology 121 Suppl. (2000) S97-S111
15. Bundy D.A. Epidemiological aspects of Trichuris and trichuriasis in Caribbean communities. Trans. R. Soc. Trop. Med. Hyg. 80 (1986) 706-718
16. Bundy D.A. Population ecology of intestinal helminth infections in human communities. Philos. Trans. R. Soc. Lond. B Biol. Sci. 321 (1988) 405-420
17. Bundy D.A., and Cooper E.S. Trichuris and trichuriasis in humans. Adv. Parasitol. 28 (1989) 107-173
18. Bundy D.A., Cooper E.S., Thompson D.E., Didier J.M., Anderson R.M., and Simmons I. Predisposition to Trichuris trichiura infection in humans. Epidemiol. Infect. 98 (1987) 65-71
19. Burden D.J., and Hammet N.C. A comparison of infectivity of Trichuris-Suis ova embryonated by 4 different methods. Vet. Parasitol. 2 (1976) 307-311
20. Chang C.I., Liao J.C., and Kuo L. Arginase modulates nitric oxide production in activated macrophages. Am. J. Physiol. 274 (1998) H342-H348
21. Cliffe L.J., Humphreys N.E., Lane T.E., Potten C.S., Booth C., and Grencis R.K. Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science 308 (2005) 1463-1465
22. Cooper E.S., Spencer J., Whyte-Alleng C.A., Cromwell O., Whitney P., Venugopal S., Bundy D.A., Haynes B., and MacDonald T.T. Immediate hypersensitivity in colon of children with chronic Trichuris trichiura dysentery. Lancet 338 (1991) 1104-1107
23. Corradin S.B., Buchmuller-Rouiller Y., and Mauel J. Phagocytosis enhances murine macrophage activation by interferon-gamma and tumor necrosis factor-alpha. Eur. J. Immunol. 21 (1991) 2553-2558
24. Crompton D.W. How much human helminthiasis is there in the world?. J. Parasitol. 85 (1999) 397-403
25. Dawson H.D., Beshah E., Nishi S., Solano-Aguilar G., Morimoto M., Zhao A., Madden K.B., Ledbetter T.K., Dubey J.P., Shea-Donohue T., Lunney J.K., and Urban Jr. J.F. Localized multigene expression patterns support an evolving Th1/Th2-like paradigm in response to infections with Toxoplasma gondii and Ascaris suum. Infect. Immun. 73 (2005) 1116-1128
26. deSchoolmeester M.L., and Else K.J. Cytokine and chemokine responses underlying acute and chronic Trichuris muris infection. Int. Rev. Immunol. 21 (2002) 439-467
27. deSchoolmeester M.L., Little M.C., Rollins B.J., and Else K.J. Absence of CC chemokine ligand 2 results in an altered Th1/Th2 cytokine balance and failure to expel Trichuris muris infection. J. Immunol. 170 (2003) 4693-4700
28. Else K.J., and deSchoolmeester M.L. Immunity to Trichuris muris in the laboratory mouse. J. Helminthol. 77 (2003) 95-98
29. Else K.J., Hultner L., and Grencis R.K. Modulation of cytokine production and response phenotypes in murine trichuriasis. Parasite Immunol. 14 (1992) 441-449
30. Else K.J., Finkelman F.D., Maliszewski C.R., and Grencis R.K. Cytokine-mediated regulation of chronic intestinal helminth infection. J. Exp. Med. 179 (1994) 347-351
31. Faulkner H., Turner J., Kamgno J., Pion S.D., Boussinesq M., and Bradley J.E. Age- and infection intensity-dependent cytokine and antibody production in human trichuriasis: the importance of IgE. J. Infect. Dis. 185 (2002) 665-672
32. Furesz S.E., Wilkie B.N., Mallard B.A., Rosendal S., and MacInnes J.I. Anti-haemolysin IgG1 to IgG2 ratios correlate with haemolysin neutralization titres and lung lesion scores in Actinobacillus pleuropneumoniae infected pigs. Vaccine 16 (1998) 1971-1975
33. Gerber B.O., Zanni M.P., Uguccioni M., Loetscher M., Mackay C.R., Pichler W.J., Yawalkar N., Baggiolini M., and Moser B. Functional expression of the eotaxin receptor CCR3 in T lymphocytes co-localizing with eosinophils. Curr. Biol. 7 (1997) 836-843
34. Gordon S. Alternative activation of macrophages. Nat. Rev. Immunol. 3 (2003) 23-35
35. Gordon J.R., Burd P.R., and Galli S.J. Mast cells as a source of multifunctional cytokines. Immunol. Today 11 (1990) 458-464
36. Guihot G., Guimbaud R., Bertrand V., Narcy-Lambare B., Couturier D., Duee P.H., Chaussade S., and Blachier F. Inducible nitric oxide synthase activity in colon biopsies from inflammatory areas: correlation with inflammation intensity in patients with ulcerative colitis but not with Crohn's disease. Amino. Acids 18 (2000) 229-237
37. Helmby H., and Grencis R.K. Essential role for TLR4 and MyD88 in the development of chronic intestinal nematode infection. Eur. J. Immunol. 33 (2003) 2974-2979
38. Hill D.E., Romanowski R.D., and Urban J.F. A Trichuris specific diagnostic antigen from culture fluids of Trichuris suis adult worms. Vet. Parasitol. 68 (1997) 91-102
39. Hogan S.P., Mishra A., Brandt E.B., Foster P.S., and Rothenberg M.E. A critical role for eotaxin in experimental oral antigen-induced eosinophilic gastrointestinal allergy. Proc. Natl Acad. Sci. USA 97 (2000) 6681-6686
40. Huang F.P., Niedbala W., Wei X.Q., Xu D., Feng G.J., Robinson J.H., Lam C., and Liew F.Y. Nitric oxide regulates Th1 cell development through the inhibition of IL-12 synthesis by macrophages. Eur. J. Immunol. 28 (1998) 4062-4070
41. Jackson J.A., Turner J.D., Rentoul L., Faulkner H., Behnke J.M., Hoyle M., Grencis R.K., Else K.J., Kamgno J., Boussinesq M., and Bradley J.E. T helper cell type 2 responsiveness predicts future susceptibility to gastrointestinal nematodes in humans. J. Infect. Dis. 190 (2004) 1804-1811
42. Jackson J.A., Turner J.D., Rentoul L., Faulkner H., Behnke J.M., Hoyle M., Grencis R.K., Else K.J., Kamgno J., Bradley J.E., and Boussinesq M. Cytokine response profiles predict species-specific infection patterns in human GI nematodes. Int. J. Parasitol. 34 (2004) 1237-1244
43. Jenkins T. A morphological and histochemical study of Trichuris suis (Schrank, 1788) with special reference to the host-parasite relationship. Parasitology 61 (1970) 357-374
44. Kaur G., Raj S.M., and Naing N.N. Trichuriasis: localized inflammatory responses in the colon. Southeast Asian J. Trop. Med. Public Health 33 (2002) 224-228
45. Kimura H., Miura S., Shigematsu T., Ohkubo N., Tsuzuki Y., Kurose I., Higuchi H., Akiba Y., Hokari R., Hirokawa M., Serizawa H., and Ishii H. Increased nitric oxide production and inducible nitric oxide synthase activity in colonic mucosa of patients with active ulcerative colitis and Crohn's disease. Dig. Dis. Sci. 42 (1997) 1047-1054
46. Kinet J.P. The high-affinity IgE receptor (Fc epsilon RI): from physiology to pathology. Annu. Rev. Immunol. 17 (1999) 931-972
47. Koyama K. Dendritic cell expansion occurs in mesenteric lymph nodes of B10.BR mice infected with the murine nematode parasite Trichuris muris. Parasitol. Res. 97 (2005) 186-190
48. Koyama K., and Ito Y. Mucosal mast cell responses are not required for protection against infection with the murine nematode parasite Trichuris muris. Parasite Immunol. 22 (2000) 13-20
49. Kringel, H., Roepstorff, A., 2006. Trichuris suis population dynamics following a primary experimental infection. Vet. Parasitol.
50. Kringel H., Roepstorff A., and Murrell K.D. A method for the recovery of immature Trichuris suis from pig intestine. Acta Vet. Scand. 43 (2002) 185-189
51. Kullberg M.C., Jankovic D., Gorelick P.L., Caspar P., Letterio J.J., Cheever A.W., and Sher A. Bacteria-triggered CD4(+) T regulatory cells suppress Helicobacter hepaticus-induced colitis. J. Exp. Med. 196 (2002) 505-515
52. Lee T.D., and Wakelin D. The use of host strain variation to assess the significance of mucosal mast cells in the spontaneous cure response of mice to the nematode Trichuris muris. Int. Arch. Allergy Appl. Immunol. 67 (1982) 302-305
53. Lillywhite J.E., Bundy D.A., Didier J.M., Cooper E.S., and Bianco A.E. Humoral immune responses in human infection with the whipworm Trichuris trichiura. Parasite Immunol. 13 (1991) 491-507
54. Lorentz A., Schwengberg S., Sellge G., Manns M.P., and Bischoff S.C. Human intestinal mast cells are capable of producing different cytokine profiles: role of IgE receptor cross-linking and IL-4. J. Immunol. 164 (2000) 43-48
55. Lugli S.M., Feng N., Heim M.H., Adam M., Schnyder B., Etter H., Yamage M., Eugster H.P., Lutz R.A., Zurawski G., and Moser R. Tumor necrosis factor alpha enhances the expression of the interleukin (IL)-4 receptor alpha-chain on endothelial cells increasing IL-4 or IL-13-induced Stat6 activation. J. Biol. Chem. 272 (1997) 5487-5494
56. Luna L.G. Luna's stain for eosinophils. In: Luna L.G. (Ed). Manual of Histologic staining methods of the Armed Forces Institute of Pathology (1968), McGraw-Hill Book Company, New York
57. MacDonald T.T., Spencer J., Murch S.H., Choy M.Y., Venugopal S., Bundy D.A., and Cooper E.S. Immunoepidemiology of intestinal helminthic infections. 3. Mucosal macrophages and cytokine production in the colon of children with Trichuris trichiura dysentery. Trans. R. Soc. Trop. Med. Hyg. 88 (1994) 265-268
58. Madden K.B., Yeung K.A., Zhao A., Gause W.C., Finkelman F.D., Katona I.M., Urban Jr. J.F., and Shea-Donohue T. Enteric nematodes induce stereotypic STAT6-dependent alterations in intestinal epithelial cell function. J. Immunol. 172 (2004) 5616-5621
59. 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
60. Mansfield L.S., and Urban J.F. The pathogenesis of necrotic proliferative colitis in swine is linked to whipworm induced suppression of mucosal immunity to resident bacteria. Vet. Immunol. Immunopathol. 50 (1996) 1-17
61. Miller E.R., and Ullrey D.E. The pig as a model for human nutrition. Annu. Rev. Nutr. 7 (1987) 361-382
62. Needham C.S., Lillywhite J.E., Didier J.M., Bianco A.E., and Bundy D.A. Temporal changes in Trichuris trichiura infection intensity and serum isotype responses in children. Parasitology 109 Pt 2 (1994) 197-200
63. Parthasarathy G., and Mansfield L.S. Trichuris suis excretory secretory products (ESP) elicit interleukin-6 (IL-6) and IL-10 secretion from intestinal epithelial cells (IPEC-1). Vet. Parasitol. 131 (2005) 317-324
64. Pedersen S., and Saeed I. Acquired immunity to Trichuris suis infection in pigs. Parasitology 123 (2001) 95-101
65. Pedersen S., and Saeed I. Host age influence on the intensity of experimental Trichuris suis infection in pigs. Parasite 9 (2002) 75-79
66. Ponath P.D., Qin S., Post T.W., Wang J., Wu L., Gerard N.P., Newman W., Gerard C., and Mackay C.R. Molecular cloning and characterization of a human eotaxin receptor expressed selectively on eosinophils. J. Exp. Med. 183 (1996) 2437-2448
67. Powers K.G., Todd A.C., and Mcnutt S.H. Experimental infections of swine with Trichuris-Suis. Am. J. Vet. Res. 21 (1960) 262-268
68. Ray R.M., Viar M.J., McCormack S.A., and Johnson L.R. Focal adhesion kinase signaling is decreased in polyamine-depleted IEC-6 cells. Am. J. Physiol. Cell Physiol. 281 (2001) C475-C485
69. Roepstorff A., and Murrell K.D. Transmission dynamics of helminth parasites of pigs on continuous pasture: Ascaris suum and Trichuris suis. Int. J. Parasitol. 27 (1997) 563-572
70. Romagnani P., de P.A., Beltrame C., Annunziato F., Dente V., Maggi E., Romagnani S., and Marone G. Tryptase-chymase double-positive human mast cells express the eotaxin receptor CCR3 and are attracted by CCR3-binding chemokines. Am. J. Pathol. 155 (1999) 1195-1204
71. Rossignol J.F., and Maisonneuve H. Benzimidazoles in the treatment of trichuriasis: a review. Ann. Trop. Med. Parasitol. 78 (1984) 135-144
72. Rutter J.M., and Beer R.J. Synergism between Trichuris suis and the microbial flora of the large intestine causing dysentery in pigs. Infect. Immun. 11 (1975) 395-404
73. Sallusto F., Mackay C.R., and Lanzavecchia A. Selective expression of the eotaxin receptor CCR3 by human T helper 2 cells. Science 277 (1997) 2005-2007
74. Scaglia M., Tinelli M., Revoltella R., Peracino A., Falagiani P., Jayakar S.D., Desmarais J.C., and Siccardi A.G. Relationship between serum IgE levels and intestinal parasite load in African populations. Int. Arch. Allergy Appl. Immunol. 59 (1979) 465-468
75. Schopf L.R., Hoffmann K.F., Cheever A.W., Urban Jr. J.F., and Wynn T.A. IL-10 is critical for host resistance and survival during gastrointestinal helminth infection. J. Immunol. 168 (2002) 2383-2392
76. Shaoul R., Okada Y., Cutz E., and Marcon M.A. Colonic expression of MUC2, MUC5AC, and TFF1 in inflammatory bowel disease in children. J. Pediatr. Gastroenterol. Nutr. 38 (2004) 488-493
77. Shea-Donohue T., Sullivan C., Finkelman F.D., Madden K.B., Morris S.C., Goldhill J., Pineiro-Carrero V., and Urban Jr. J.F. The role of IL-4 in Heligmosomoides polygyrus-induced alterations in murine intestinal epithelial cell function. J. Immunol. 167 (2001) 2234-2239
78. Stephenson L.S., Holland C.V., and Cooper E.S. The public health significance of Trichuris trichiura. Parasitology 121 (2000) S73-S95
79. Summers R.W., Elliott D.E., Qadir K., Urban J.F., Thompson R., and Weinstock J.V. Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am. J. Gastroenterol. 98 (2003) 2034-2041
80. Summers R.W., Elliot D., Urban J., Thompson R., and Weinstock J. Trichuris suis therapy in Crohn's disease. Gut 54 (2005) 87-90
81. Summers R.W., Elliott D.E., Urban Jr. J.F., Thompson R.A., and Weinstock J.V. Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128 (2005) 825-832
82. Takamoto M., Ovington K.S., Behm C.A., Sugane K., Young I.G., and Matthaei K.I. Eosinophilia, parasite burden and lung damage in Toxocara canis infection in C57Bl/6 mice genetically deficient in IL-5. Immunology 90 (1997) 511-517
83. Uguccioni M., Mackay C.R., Ochensberger B., Loetscher P., Rhis S., LaRosa G.J., Rao P., Ponath P.D., Baggiolini M., and Dahinden C.A. High expression of the chemokine receptor CCR3 in human blood basophils. Role in activation by eotaxin, MCP-4, and other chemokines. J. Clin. Invest. 100 (1997) 1137-1143
84. Urban J., Fang H., Liu Q., Ekkens M.J., Chen S.J., Nguyen D., Mitro V., Donaldson D.D., Byrd C., Peach R., Morris S.C., Finkelman F.D., Schopf L., and Gause W.C. IL-13-mediated worm expulsion is B7 independent and IFN-gamma sensitive. J. Immunol. 164 (2000) 4250-4256
85. Xu L.R., Carr M.M., Bland A.P., and Hall G.A. Histochemistry and morphology of porcine mast cells. Histochem. J. 25 (1993) 516-522
86. Yoshikawa M., Nakajima T., Tsukidate T., Matsumoto K., Iida M., Otori N., Haruna S., Moriyama H., and Saito H. TNF-alpha and IL-4 regulate expression of IL-13 receptor alpha2 on human fibroblasts. Biochem. Biophys. Res. Commun. 312 (2003) 1248-1255