Immunomodulation in trichinellosis: Does Trichinella Really escape the host immune system?

Endocrine, Metabolic and Immune Disorders - Drug Targets

Volumn 12, Issue 1, 2012, Pages 4-15

  Bruschi, Fabrizio ^a   Chiumiento, Lorena ^a  

^a UNIVERSITY OF PISA   (Italy)

Author keywords

Eosinophils; Escape mechanisms; IgE; Immunomodulation; Mast cells; T helper 1; T helper 2; Trichinellosis

Indexed keywords

ANTIBODY; CHYMASE; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; INTERLEUKIN 10; INTERLEUKIN 10 ANTIBODY; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 18; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 9; STEM CELL FACTOR RECEPTOR; STEM CELL FACTOR RECEPTOR ANTIBODY; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

APOPTOSIS; CD4+ T LYMPHOCYTE; CELL FUNCTION; CELL PROLIFERATION; CYTOKINE PRODUCTION; DENDRITIC CELL; DIARRHEA; EOSINOPHIL; EOSINOPHILIA; HOST PARASITE INTERACTION; HUMAN; HUMORAL IMMUNITY; HYPERGAMMAGLOBULINEMIA; IMMUNE RESPONSE; IMMUNITY; IMMUNOMODULATION; INNATE IMMUNITY; INTESTINE CONTRACTION; INTESTINE MUSCLE; LARVA; MAST CELL; MAST CELL DEGRANULATION; MASTOCYTOSIS; NEMATODE LIFE CYCLE STAGE; NEUTROPHIL; NONHUMAN; PARASITE LOAD; REVIEW; SPLEEN CELL; T LYMPHOCYTE; TH1 CELL; TH2 CELL; TRANSCRIPTION INITIATION; TRICHINELLA; TRICHINELLA SPIRALIS; TRICHINOSIS; WORM EXPULSION;

EID: 84857134533     PISSN: 18715303     EISSN: 22123873     Source Type: Journal    
DOI: 10.2174/187153012799279081     Document Type: Review

References (101)

1. Pozio, E. In: Guidelines for the surveillance, management, prevention and control of trichinellosis; J. Dupouy-Camet & K.D. Murrell, Ed; FAO/WHO/OIE: Paris, 2007, Vol., pp.1-36.
2. Bell, R.G. (1998) The generation and expression of immunity to Trichinella spiralis in laboratory rodents. Adv. Parasitol., 41, 149-217.
3. Viallet, J.; MacLean, J.D.; Goresky, L.A.; Staudt, M.; Gaetane, R. and Law, C. (1986) Arctic trichinosis presenting as prolonged diarrhea. Gastroenterology, 91, 938-946.
4. MacLean, J.P.; Viallet, J.; Law, C. and Stuart, M. (1989) Trichinosis in the Canadian Arctic: report of five outbreaks and a new clinical syndrome. J. Infect. Dis., 160, 513-520.
5. Grencis, R.K.; Riedlinger, J. and Wakelin, D. (1985) L3T4-positive T lymphoblasts are responsible for transfer of immunity to Trichinella spiralis in mice. Immunology, 56, 213-218.
6. Riedlinger, J.; Grencis, R.K. and Wakelin, D. (1986) Antigen-specific T-cell lines transfer protective immunity against Trichinella spiralis in vivo. Immunology, 58, 57-61.
7. - T-helper cells that are generated in the intestine. Immunology, 66, 588-594.
8. Bell, R.G. and Issekutz, T. (1993) Expression of a protective intestinal immune response can be inhibited at three distinct sites by treatment with anti-alpha 4 integrin. J. Immunol., 151, 4790-4802.
9. Zhu, D. and Bell, R.G. (1989) IL-2 production, IL-2 receptor expression, and IL-2 responsiveness of spleen and mesenteric lymph node cells from inbred mice infected with Trichinella spiralis. J. Immunol., 142, 3262-3267.
10. Mucida, D. and Cheroutre, H. (2010) The many face-lifts of CD4 T helper cells. Adv. Immunol., 107, 139-152.
11. Grencis, R.K.; Riedlinger, J. and Wakelin, D. (1987) Lymphokine production by T cells generated during infection with Trichinella spiralis. Int. Arch. Allergy Appl. Immunol., 83, 92-95.
12. Ramaswamy, K.; Negrao-Correa, D. and Bell, R.G. (1996) Local intestinal immune responses to infections with Trichinella spiralis. Real-time, continuous assay of cytokines in the intestinal (afferent) and efferent thoracic duct lymph of rats. J. Immunol., 156, 4328-4337.
13. Ishikawa, N.; Goyal, P.K.; Mahida, Y.R.; Li, K-F and Wakelin, D. (1998) Early cytokine responses during intestinal parasitic infections. Immunology, 93, 257-263.
14. Gomez-Morales, M.A.; Mele, R.; Sanchez, M.; Sacchini, D.; De Giacomo, M. and Pozio, E. (2002) Increased CD8+-T cell expression and a Type 2 cytokine pattern during the musculature phase of Trichinella infection in humans. Infect. Immunity, 70, 233-239.
15. McDermott, J.R.; Humphreys, N.E.; Forman, S.P.; Donaldson, D.D. and Grencis, R.K. (2005) Intraepithelial NK cell-derived IL-13 induces intestinal pathology associated with nematode infection. J. Immunol., 175, 3207-3213.
16. Lawrence, C.E.; Paterson, J.C.; Higgins, L.M.; MacDonald, T.T.; Kennedy, M.W. and Garside, P. (1998) IL-4-regulated enteropathy in an intestinal nematode infection. Eur. J. Immunol., 28, 2672-2684.
17. Urban, J.F.Jr.; Schopf, L.; Morris, S.C.; Orekhova, T.; Madden, K.B.; Betts, C.J.; Gamble, H.R.; Byrd, C.; Donaldson, D.; Else, K. and Finkelman, F.D. (2000) Stat6 signaling promotes protective immunity against Trichinella spiralis through a mast cell - and T cell-dependent mechanism. J. Immunol., 164, 2046-2052.
18. Finkelman, F.D.; Katona, I.M.; Urban, J.F.Jr.; Snapper, C.M.; Ohara, J. and Paul, W.E. (1986) Suppression of in vivo polyclonal IgE responses by monoclonal antibody to the lymphokine B-cell stimulatory factor 1. Proc. Natl. Acad. Sci. USA, 83, 9675-9388.
19. Ahmad, A.; Wang, C.H. and Bell, R.G. (1991) A role for IgE in intestinal immunity. Expression of rapid expulsion of Trichinella spiralis in rats transfused with IgE and thoracic duct lymphocytes. J. Immunol., 146, 3563-3570.
20. Ramaswamy, K.; Hakimi, J. and Bell, R.G. (1994) Evidence for an interleukin 4-inducible immunoglobulin E uptake and transport mechanism in the intestine. J. Exp. Med., 180, 1793-1803.
21. Khan, W.I.R.M.; Richard, H.; Akiho, P.A.; Blennerhasset, N.E.; Humphreys, R.K.; Grencis, J.; Van Snick, J. and Collins, S.M. (2003) Modulation of intestinal muscle contraction by interleukin-9 (IL-9) or IL-9 neutralization: correlation with worm expulsion in murine nematode infections. Infect. Immun., 71, 2430-2438.
22. Helmby, H. and Grencis, R.K. (2003a) Contrasting roles for IL-10 in protective immunity to different life cycle stages of intestinal nematode parasites. Eur. J. Immunol., 33, 2382-2390.
23. Helmby, H. and Grencis, R.K. (2003b) IFN-gamma-Independent Effects of IL-12 During Intestinal Nematode Infection. J. Immunol., 171, 3691-3696.
24. Fu, Y.; Wang, W.; Tong, J.; Pan, Q.; Long, Y.; Qian, W. and Hou, X. (2009) Th17: A New Participant in Gut Dysfunction in Mice Infected with Trichinella spiralis. Mediators Inflamm., 2009, 517052.
25. Helmby, H. and Grencis, R.K. (2002) IL-18 regulates intestinal mastocytosis and Th2 cytokine production independently of IFN- gamma during Trichinella spiralis infection. J. Immunol., 169, 2553-2560.
26. Scales, H.E.; Ierna, M.X. and Lawrence, C.E. (2007) The role of IL-4, IL-13 and IL-4Ralpha in the development of protective and pathological responses to Trichinella spiralis. Parasite Immunol., 29, 81-91.
27. Woodbury, R.G.; Miller, H.R.P.; Huntley, J.F.; Newlands, G.F.J.; Palliser, A.C. and Wakelin, D. (1984) Mucosal mast cells are functionally active during spontaneous expulsion of intestinal nematode infections in rat. Nature, 312, 450-452.
28. Miller, H.R. (1996) Mucosal mast cells and the allergic response against nematode parasites. Vet. Immunol. Immunopathol., 54, 331-336.
29. Gustowska, L.; Ruitenberg, E.J.; Elgersma, A. and Kociecka, W. (1983) Increase of mucosal mast cells in the jejunum of patients infected with Trichinella spiralis. Int. Arch. Allergy Appl. Immunol., 71, 304-308.
30. Suzuki, T.; Sasaki, T.; Takagi, H.; Sato, K. and Ueda, K. (2008) The effectors responsible for gastrointestinal nematode parasites, Trichinella spiralis, expulsion in rats. Parasitol. Res., 103, 1289-1295.
31. Garside, P.; Grencis, R.K. and Mowat, A.M. (1992) T lymphocyte dependent enteropathy in murine Trichinella spiralis infection. Parasite Immunol., 14, 217-225.
32. Ha, T.Y.; Reed, N.D. and Crowle P.K. (1983) Delayed expulsion of adult Trichinella spiralis by mast cell-deficient W/Wv mice. Infect. Immun., 41, 445-447.
33. Donaldson, L.E.; Schmitt, E.; Huntley, J.F.; Newlands, G.F.J. and Grencis, R.K. (1996) A critical role for stem cell factor and c-kit in host protective immunity to an intestinal helminth. Int. Immunol., 8, 559-567.
34. Faulkner, H.; Humphries, N.; Renauld, J.C.; van Snick, J. and Grencis, R. (1997) Interleukin-9 is involved in host protective immunity to intestinal nematode infection. Eur. J. Immunol., 27, 2536-2540.
35. Scudamore, C.L.; Pennington, A.M.; Thornton, E.M.; McMillan, L.; Newlands, G.F.J. and Miller, H.R.P. (1995) Release of the mucosal mast cell granule chymase, rat mast cell protease-II, during anaphylaxis is associated with the rapid development of paracellular permeability to macromolecules in rat jejunum. J. Exp. Med., 182, 1871-1881.
36. Scudamore, C.L.; Jepson, M.A.; Hirst, B.H. and Miller, H.R. (1998) The rat mucosal mast cell chymase, RMCP-II, alters epithelial cell monolayer permeability in association with altered distribution of the tight junction proteins ZO-1 and occludin. Eur. J. Cell Biol., 75, 321-330.
37. Knight, P.A.; Wright, S.H.; Lawrence, C.E.; Paterson, Y.Y.M. and Miller, H.R.P. (2000) Delayed expulsion of the nematode Trichinella spiralis in mice lacking the mucosal mast cell-specific granule chymase, mouse mast cell protease-1. J. Exp. Med., 192, 1849-1856.
38. Shin, K.; Watts, G.F.; Oettgen, H.C.; Friend, D.S.; Pemberton, A.D.; Gurish, M.F. and Lee, D.M. (2008) Mouse mast cell tryptase mMCP-6 is a critical link between adaptive and innate immunity in the chronic phase of Trichinella spiralis infection. J. Immunol., 180, 4885-4891.
39. Blum, L.K.; Thrasher, S.M.; Gagliardo, L.F.; Fabre, V. and Appleton, J.A. (2009) Expulsion of secondary Trichinella spiralis infection in rats occurs independently of mucosal mast cell release of mast cell protease II. J. Immunol., 183, 5816-5822.
40. th International Conference on Trichinellosis, CINVESTAV, Mexico, Ortega-Pierres, M.G.; Gamble, H.R. and Wakelin, D. Eds.; Mexico D.F., 1997, pp. 397-404.
41. Arizmendi, N.; Yepez-Mulia, L.; Cedillo-Rivera, R.; Ortega-Pierres, M.G.; Munoz, O.; Befus, D. and Enciso-Moreno, J.A. (2001) Interleukin mRNA changes in mast cells stimulated by TSL-1 antigens. Parasite, 8, S114-S116.
42. Yépez-Mulia, L.; Montaño-Escalona, C.; Fonseca-Liñán, R.; Muñoz-Cruz, S.: Arizmendi-Puga, N.; Boireau, P. and Ortega-Pierres, G. (2009) Differential activation of mast cells by antigens from Trichinella spiralis muscle larvae, adults, and newborn larvae. Vet. Parasitol., 159, 253-257.
43. Vallance, B.A.; Blennerhassett, P.A.; Deng, Y.; Matthaei, K.I.; Young, I.G. and Collins, S. (1999) IL-5 contributes to worm expulsion and muscle hypercontractility in a primary T. spiralis infection. Am. J. Physiol., 277, G400-G408.
44. Vallance, B.A.; Matthaei, K.I.; Sanovic, S.; Young, I.G. and Collins, S.M. (2000) Interleukin-5 deficient mice exhibit impaired host defence against challenge Trichinella spiralis infections. Parasite Immunol., 22, 487-492.
45. Lee, T.D. (1991) Helminthotoxic responses of intestinal eosinophils to Trichinella spiralis newborn larvae. Infect. Immun., 59, 4405-4411.
46. Man Warren, T.; Gagliardo, L.; Geyer, J.; McVay, C.; Pearce-Kelling, S. and Appleton, J. (1997) Invasion of intestinal epithelia in vitro by the parasitic nematode Trichinella spiralis. Infect. Immun., 65, 4806-4812.
47. McVay, C.S.; Bracken, P.; Gagliardo, L.F. and Appleton, J. (2000) Antibodies to tyvelose exhibit multiple modes of interference with the epithelial niche of Trichinella spiralis. Infect. Immun., 68, 1912-1918.
48. Li, C.F.K.; Seth, R.; Gray, T.; Bayston, R.; Mahida, R. and Wakelin D. (1998) Production of proinflammatory cytokines and inflammatory mediators in human intestinal epithelial cells after invasion by Trichinella spiralis. Infect. Immun., 66, 2200-2206.
49. Urban, J.F. Jr.; Noben-Trauth, N.; Schopf, L.; Madden, K.B. and Finkelman, F.D. (2001) Cutting edge: IL-4 receptor expression by non-bone marrow-derived cells is required to expel gastrointestinal nematode parasites. J. Immunol., 167, 6078-6081.
50. Ierna, M.X.; Scales, H.E.; Saunders, K.L. and Lawrence, C.E. (2008) Mast cell production of IL-4 and TNF may be required for protective and pathological responses in gastrointestinal helminth infection. Mucosal Immunol., 1, 147-155.
51. Michels, C.E.; Scales, H.E.; Saunders, K.A; McGowan, S.; Brombracher, F.; Alexander, J. and Lawrence, C.E. (2009) Neither interleukin-4 receptor alpha expression on CD4+ T cells, or macrophages and neutrophils is required for protective immunity to Trichinella spiralis. Immunology, 128, 385-394.
52. Lawrence, C.E.; Paterson, J.C.; Higgins, M.; McDonald, T.; Kennedy, M.W. and Garside, P. (1998) IL-4-regulated enteropathy in an intestinal nematode infection. Eur. J. Immunol., 28, 2672-2684.
53. Ierna, M.X.; Scales, H.E.; Mueller, C. and Lawrence C.E. (2009) Trans-membrane tumor necrosis factor alpha is required for. enteropathy and is sufficient to promote parasite expulsion in. gastrointestinal helminth infection. Infect. Immun., 77, 3879-3885.
54. James, S.L. (1995) Role of nitric oxide in parasitic infections. Microbiol. Rev., 59, 533-547.
55. Lawrence, C.E.; Paterson, J.C.; Wei, X.; Liew, F.Y.; Garside, P. and Kennedy, M.W. (2000) Nitric oxide mediates intestinal pathology but not immune expulsion during Trichinella spiralis infection in mice. J. Immunol., 164, 4229-4234.
56. Watanabe, N.; Bruschi, F. and Korenaga, M. (2005) IgE: a question of protective immunity in Trichinella spiralis infection. Trends Parasitol., 21, 175-178.
57. Gurish, M.F.; Bryce, P.J.; Tao, H.; Kisselgof, A.B.; Thornton, E.M.; Miller, H.R.; Friend, D.S. and Oettgen, H.C. (2004) IgE enhances parasite clearance and regulates mast cell responses in mice infected with Trichinella spiralis. J Immunol., 172, 1139-1145.
58. Bruschi, F.; Pozio, E.; Watanabe, N.; Gomez-Morales, M.A.; Ito, M.; Huang, Y. and Binaghi, R. (1999) Anaphylactic response to parasite antigens: IgE and IgG1 independently induce death in Trichinella-infected mice. Int. Arch. Allergy Appl. Immunol., 119, 291-296.
59. Venturiello, S.M.; Verzoletti, M.L.; Costantino, S.N.; Forestiero, M.A. and Roux, M.E. (2006) Early pulmonary response in rats infected with Trichinella spiralis. Parasitology, 134, 1-8.
60. Kamal, M.; Wakelin, D.; Ouellette, A.J.; Smith, A., Podolsky, D.K. and Mahida, Y.R. (2001) Mucosal T cells regulate Paneth and intermediate cell numbers in the small intestine of T. spiralis-infected mice. Clin. Exp. Immunol., 126, 117-125.
61. Bliss, S.K.; Bliss, S.P.; Beiting, D.P.; Alcaraz, A. and Appleton, J.A. (2007) IL-10 regulates movement of intestinally derived CD4+ T cells to the liver. J. Immunol., 178, 7974-7983.
62. Douglas, D.B.; Beiting, D.P.; Loftus, J.P.; Appleton, J.A. and Bliss, S.K. (2010) Combinatorial effects of interleukin 10 and interleukin 4 determine the progression of hepatic inflammation following murine enteric parasitic infection. Hepatology, 51, 2162-2171.
63. Beiting, D.P.; Bliss, S.K.; Schlafer, D.H.; Roberts, V.L. and Appleton, J.A. (2004) Interleukin-10 limits local and body cavity inflammation during infection with muscle-stage Trichinella spiralis. Infect. Immun., 72, 3129-3137.
64. Beiting, D.P.; Gagliardo, L.F.; Hesse, M.; Bliss, S.K.; Meskill, D. and Appleton J.A. (2007) Coordinated control of immunity to muscle stage Trichinella spiralis by IL-10, regulatory T cells, and TGF-beta. J. Immunol., 178, 1039-1047.
65. Bruschi, F.; Marucci, G.; Pozio, E. and Masetti, M. (2009) Evaluation of inflammatory responses against muscle larvae of different Trichinella species by an image analysis system. Vet. Parasitol., 159, 258-262.
66. Shupe, K. and Stewart, G.L. (1991) Stimulated chemotactic response in neutrophils from Trichinella pseudospiralis-infected mice and the neutrophilotactic potential of Trichinella extracts. Int. J. Parasitol., 21, 625-630.
67. Fabre, V.; Beiting, D.P.; Bliss, S.K.; Gebreselassie, N.G.; Gagliardo, L.F.; Lee, N.A.; Lee, J.J. and Appleton, J.A. (2009) Eosinophil deficiency compromises parasite survival in chronic nematode infection. J. Immunol., 182, 1577-1583.
68. Fabre, M.V.; Beiting, D.P.; Bliss, S.K. and Appleton, J.A. (2009) Immunity to Trichinella spiralis muscle infection. Vet. Parasitol., 159, 245-248.
69. Bruschi, F. and Chiumiento, L. (2011) Trichinella inflammatory myophaty: host or parasite strategy? Parasite & Vectors, 4, 42.
70. Stewart, G.L. (1995) Myopathogenesis and myoredifferentiation in trichinosis. Bas. Appl. Myol., 5, 213-222.
71. Li, C.K.F. and Ko, R.C. (2001) Inflammatory response during the muscle phase of Trichinella spiralis and Trichinella pseudospiralis infections. Parasitol. Res., 87, 708-714.
72. Ferraccioli, G.; Mercadanti, M.; Salaffi, F.; Bruschi, F.; Melissari, M. and Pozio, E. (1988) Prospective rheumatological study of muscle and joint symptoms during Trichinella nelsoni infection. Quart. J. Med., 69, 973-984.
73. Madden, K.B.; Murrell, K.D. and Lunney, J.K. (1990) Trichinella spiralis: major histocompatibility complex-associated elimination. of encysted muscle larvae in swine. Exp. Parasitol., 70, 443-451.
74. Madden, K.B,; Moeller, R.F. Jr.; Douglass, L.W.; Goldman, T. and Lunney, J.K. (1993) Trichinella spiralis: genetic basis and kinetics of the anti-encysted muscle larval response in miniature swine. Exp. Parasitol., 77, 23-35.
75. Bruschi, F.; Korenaga, M. and Watanabe, N. (2008) Eosinophils and Trichinella infection: toxic for the parasite and the host? Trends Parasitol., 24, 462-467.
76. Gon, S.; Saito, S.; Takeda, Y.; Miyata, H., Takatsu, K. and Sendo, F. (1997) Apoptosis and in vivo distribution and clearance of eosinophils in normal and Trichinella spiralis-infected rats. J. Leukoc. Biol., 62, 309-317.
77. Simon, H.U. and Blaser, K. (1995) Inhibition of programmed eosinophil death: a key pathogenic event for eosinophilia? Immunol. Today, 16, 53-55.
78. Gurish, M.F.; Humbles, A.; Tao, H.; Finkelstein, S.; Boyce, J.A.; Gerard, C.; Friend, D.S. and Austen, K.F. (2002) CCR3 is required for tissue eosinophilia and larval cytotoxicity after infection with Trichinella spiralis. J. Immunol., 168, 5730-5736.
79. Bruschi, F. (2004) Focus on immunology of trichinellosis. Med. Chem. Rev., 1, 179-185.
80. Jungery, M.; Clark, N.W.T. and Parkhouse, R.M.E. (1983) A major change in surface antigens during the maturation of newborn larvae of Trichinella spiralis. Mol. Biochem. Parasitol., 7, 101-109.
81. Gansmüller, A.; Anteunis, A.; Venturiello, S.M.; Bruschi, F. and Binaghi, R.A. (1987) Antibody-dependent in-vitro cytotoxicity of newborn Trichinella spiralis larvae: nature of the cells involved. Parasite Immunol., 9, 281-292.
82. Venturiello, S.M.; Giambartolomei, G.H. and Costantino, S.N. (1993) Immune killing of newborn Trichinella larvae by human leucocytes. Parasite Immunol., 15, 559-564.
83. Bruschi, F. (2002) The immune response to the parasitic nematode Trichinella and the ways to escape it. From experimental studies to implications for human infection. Curr. Drug Targets Immune Endocr. Metabol. Disord., 2, 269-280.
84. Leiro, J.; Santamarina, M.T.; Sernández, L.; Sanmartín, M.L. and Ubeira, F.M. (1988) Immunomodulation by Trichinella spiralis: primary versus secondary response to phosphorylcholine-containing antigens. Med. Microbiol. Immunol., 177, 161-167.
85. Ilic, N.; Colic, M.; Gruden-movsesijan, A.; Majstorovic, I.; Vasilev, S. and Sofronic-Milosavljevic, L. (2008) Characterization of rat bone marrow dendritic cells initially primed by Trichinella spiralis antigens. Parasite Immunol., 30, 491-495.
86. Langelaar, M.; Aranzamendi, C.; Franssen, F.; Van der Giessen, J.; Rutten, V.; van der Ley, P. and Pinelli, E. (2009) Suppression of dendritic cell maturation by Trichinella spiralis excretory/secretory products. Parasite Immunol., 31, 641-645.
87. Pennock, J.L.; Behnke, J.M.; Bickle, Q.D.; Devaney, E.; Grencis, R.K.; Isaac, R.E.; Joshua, G.W.P.; Selkirk, M.E.; Zhang, Y. and Meyer, D.J. (1998) Rapid purification and characterization of L- dopachrome-methyl ester tautomerase (macrophage-migrationinhibitory factor) from Trichinella spiralis, Trichuris muris and Brugia pahangi. Biochem. J., 335, 495-498.
88. Bruschi, F.; Carulli, G.; Azzara', A.; Homan, W.; Minnucci, S.; Rizzuti-Gullaci, A.; Sbrana S. and Angiolini, C. (2000) Inhibitory effects of human neutrophil functions by the 45-kD glycoprotein derived from the parasitic nematode Trichinella spiralis. Int. Arch. Allergy Appl. Immunol., 122, 58-65.
89. Bian K.; Harari, Y.; Zhong, M.; Lai, M.; Castro, G.; Weisbrodt, N.; and Murad F. (2001) Down-regulation of inducible nitric-oxide synthase (NOS-2) during parasite-induced gut inflammation: a path to identify a selective NOS-2 inhibitor. Mol Pharmacol., 59, 939-947.
90. Bian, K.; Zhong, M.; Harari, Y.; Lai, M.; Weisbrodt, N.; and Murad, F. (2005) Helminth regulation of host IL-4Ra &2044; Stat6 signaling: mechanism underlying NOS-2 inhibition by Trichinella spiralis. Proc. Natl. Acad. Sci. USA, 102, 3936-3941.
91. Näreaho, A.; Saari, S.; Meri, S. and Sukura, A. (2009) Complement membrane attack complex formation and infectivity of Trichinella spiralis and T. nativa in rats. Vet. Parasitol., 159, 263-267.
92. Belkaid, Y.; Sun, C.M. and Bouladoux, N. (2006) Parasites and immunoregulatory T cells. Curr. Opin. Immunol., 18, 406-412.
93. Khan, W.I.; Blennerhasset, P.A.; Varghese, A.K.; Chowdhury, S.K.; Omsted, P.; Deng, Y. and Collins, S.M. (2002) Intestinal nematode infection ameliorates experimental colitis in mice. Infect. Immun., 70, 5931-5937.
94. Domingues, H.S.; Mues, M.; Lassmann, H.; Wekerle, H. and Krishnamoorthy, G. (2010) Functional and pathogenic differences of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. PLoS One, 5, e15531.
95. Gruden-Movsesijan, A.; Ilic, N.; Mostarica-Stojkovic, M.; Stosic-Grujicic, S.; Milic, M. and Sofronic-Milosavljevic, L. (2008) Trichinella spiralis: modulation of experimental autoimmune encephalomyelitis in DA rats. Exp. Parasitol., 118, 641-647.
96. Gruden-Movsesijan, A.; Ilic, N.; Mostarica-Stojkovic, M; Stosic-Grujicic, S.; Milic, M. and Sofronic-Milosavljevic, L. (2010) Mechanisms of modulation of experimental autoimmune encephalomyelitis by chronic Trichinella spiralis infection in Dark Agouti rats. Parasite Immunol., 32, 450-459.
97. Wu, Z.; Nagano, I.; Asano K. and Takahashi, Y. (2010) Infection of non-encapsulated species of Trichinella ameliorates experimental autoimmune encephalomyelitis involving suppression of Th17 and Th1 response. Parasitol. Res., 107, 1173-1188.
98. Saunders, K.A.; Raine, T.; Cooke, A. and Lawrence, C.E. (2007) Inhibition of autoimmune type 1 diabetes by gastrointestinal helminth infection. Infect. Immun., 75, 397-407.
99. Furze, R.C.; Hussell T.; and Selkirk, M.E. (2006) Amelioration of influenza-induced pathology in mice by coinfection with Trichinella spiralis. Infect. Immun., 74, 1924-1932.
100. Park, H.K.; Cho, M.K.; Choi, S.H.; Kim, Y.S. and Yu HS. (2011) Trichinella spiralis: infection reduces airway allergic inflammation in mice. Exp. Parasitol., 127, 539-544.
101. Strachan, D. P. (1989) Hay fever, hygiene, and household size. Br. Med. J., 299, 1259-1260.