Parasitic helminths of veterinary concern:host immune response regulation and potential use for the treatment of inflammatory diseases

Carlos Ramón Bautista Garfias

2009, Number 3

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Vet Mex 2009; 40 (3)

Parasitic helminths of veterinary concern:host immune response regulation and potential use for the treatment of inflammatory diseases

Bautista GCR

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Language: English/Spanish
References: 149
Page: 283-291
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ABSTRACT

In recent years, a new alternative for the treatment of human inflammatory diseases, such as Crohn’s disease, by oral administration of eggs from the swine parasitic nematode Trichuris suis has attracted attention, based on the capacity of helminths to polarize T helper cells (Th) to Th2 type which inhibits inflammation. In the present review the mechanisms used by parasitic helminths to modify the host immune response are analyzed and their potential use for the treatment of a variety of inflammatory diseases is discussed.

REFERENCES

1.ANONYMOUS. Get the balance right. Nat Immunol 2005;6:1177.
2.HENSON PM. Dampening inflammation. Nat Immunol 2005;6:1179-1181.
3.ABBAS AK, LICHTMAN AH, PILLAI SP. Cellular and molecular immunology. 6th ed. Philadelphia: Saunders Elsevier, 2007.
4.NAIRN R, HELBERT M. Immunology for medical students. 2nd ed. Philadelphia: Mosby Elsevier, 2007.
5.GERSHWIN LJ. Veterinary autoimmunity: Autoimmune diseases in domestic animals. Ann NY Acad Sci 2007;1109:109-116.
6.ERB KJ. Helminths, allergic disorders and IgE-mediated immune responses: where do we stand? Eur J Immunol 2007;37:1170-1173.
7.SEDER RA, PAUL WE. Acquisition of lymphokine-prodas ducing phenotype by CD4+ T cells. Annu Rev Immunol 1994;12:635-673.
8.SANDERSON CJ, CAMPBELL HD, YOUNG IG. Molecular and cellular biology of eosinophil differentiation factor (interleukin-5) and its effects on human and Mouse B cells. Immunol Rev 1988;102:29-50.
9.COFFMAN RL, SEYMOUR BWP, HUDAK S, JACKSON J, RENNICK D. Antibody to interleukin-5 inhibits helminth-induced eosinophilia in mice. Science 1989;245:308-310.
10.BACELLAR O, DÓLIVEIRA A JR, JERONIMO S, CARVALHO EM. IL-10 and IL-12 are the main regulatory cytokines in visceral leishmaniasis. Cytokine 2000;12:1228-1231.
11.FINNEY CAM, TAYLOR MD, WILSON MS, MAIZELS RM. Expansion and activation of CD+CD25+ regulatory T cells in Heligmosomoides polygyrus infection. Eur J Immunol 2007;37:1874-1886.
12.O’NEILL SM, BRADY MT, CALLANAN JJ, MULCAHY G, JOYCE P, MILLS KH et al. Fasciola hepatica infection downregulates Th1 responses in mice. Parasite Immunol 2000;22:147-155.
13.PESCE JT, LIU Z, HAMED H, ALEM F, WHITMIRE J, LIN H et al. Neutrophils clear bacteria associated with parasitic nematodes augmenting the development of an effective Th2-type response. J Immunol 2008;180:464-474.
14.PATERSON S, BARBER R. Experimental evolution of parasite life-story traits in Strongyloides ratti (Nematoda). Proc Biol Soc 2007;274:1467-1474.
15.GIRONES N, VALERO MA, GARCIA-BODELON MA, CHICO-CALERO I, PUNZON C, FRESNO et al. Immune suppression in advanced chronic fascioliasis: an experimental study in a rat model. J Infec Dis 2007;195:1504-1512.
16.WEBB RA, HOQUE T, DIMAS S. Expulsion of the gastrointestinal cestode, Hymenolepis diminuta by tolerant rats: evidence for mediation by a Th2 type immune enhanced goblet cell hyperplasia, increased mucin production and secretion. Parasite Immunol 2007;29:11-21.
17.JITTIMANEE J, SERMSWAN RW, PUAPAIROJ A, MALEEWONG W, WONGRTANACHEEWIN S. Cytokine expression in hamsters experimentally infected with Opistorchis viverrini. Parasite Immunol 2007;29:159- 167.
18.MENDEZ S, VALENZUELA JG, WU W, HOTEZ PJ. Cytokine production, lymphoproliferation, and antibody responses during the course of Ancylostoma ceylanicum infection in the golden hamster. Infect Immun 2005;73:3402-3407.
19.DEGEN WG, DAAL N, ROTHWELL L, KAISER P, SCHIJNS VE. Th1/Th2 polarization by viral and helminth infection in birds. Vet Microbiol 2005; 105:163- 167.
20.TORINA A, CARACAPPA S, BARERA A, DIELI F, SIRECI G, GENCHI C et al. Toxocara canis infection induces antigen-specific IL-10 and IFNgamma production in pregnant dogs and their puppies. Vet Immunol Immunopathol 2005;108:247-251.
21.MORCHON R, LOPEZ-BELMONTE J, BAZZOCCHI C, GRANDI G, KRAMER L, SIMON F. Dogs with patent Dirofilaria immitis infection have higher expression of circulating IL-4, IL-10 and iNOS mRNA than those with occult infection. Vet Immunol Immunopathol 2007;115:184-188.
22.GILBERT S, HALLIWELL REW. The effects of endoparasitism on the immune response to orally administered antigen in cats. Vet Immunol Immunopathol 2005;106:113-120.
23.DAWSON HD, BESHAH E, NISHI S, SOLANOAGUILAR G, MORIMOTO M, ZHAO A et al. Localized multigene expression patterns support an evolving Th1/Th2-like paradigm in response to infections with Toxoplasma gondii and Ascaris suum. Infect Immun 2005;73:1116-1128.
24.KRINGEL H, IBURG T, DAWSON H, AASTED B, ROEPSTORFF A. A time course study of immunological responses in Trichuris suis infected pigs demonstrates induction of local type 2 response associated with worm burden. Int J Parasitol 2006:36:915-924.
25.TECHAU ME, JOHANSEN MV, AASTED B, LIND P, ORNBJERG N, OSWALD IP. Cytokine mRNA profiles in pigs exposed prenatally and postnatally to Schistosoma japonicum. Vet Res 2007;38:25-36.
26.LACROUX C, NGUYEN THC, ANDREOLETTI O, PREVOT F, GRISEZ C, BERGAUD JP et al. Haemonchus contortus (Nematoda:Trichostongylidae) infection in lambs elicits an unequivocal Th2 immune response. Vet Res 2006;37:607-622.
27.PERNTHANER A, COLE SA, MORRISON L, HEIN WR. Increased expression of interleukin-5 (IL-5), IL-13, and tumor necrosis factor alfa genes in intestinal lymph cells of sheep selected for enhanced resistance to nematodes during infection with Trichostrongylus colubriformis. Infect Immun 2005;73:2175-2183.
28.BROWN WC, DAVIES WC, DOBBELAERE DA, RICEFICHT AC. CD4+ T-cell clones obtained from cattle chronically infected with Fasciola hepatica and specific for adult Word antigen Express both unrestricted and Th2 cytokines profiles. Infect Immun 1994; 62:818-827.
29.FLYNNN RJ, MANNION C, GOLDEN O, HACARIZ O, MULCAHY G. Experimental Fasciola hepatica infection alters responses to tests used for diagnosis of bovine tuberculosis. Infect Immun 2007;75:1373-1381.
30.FLYNN RJ, MULCAHY G. Possible role of Toll-like receptors in interaction of Fasciola hepatica excretory/ secretory products with bovine macrophages. Infect Immun 2008;76:678-684.
31.JOHNSON DR, SALES J, MATTHEWS JB. Local cytokine responses in Dictiocaulus viviparous infection. Vet Parasitol 2005;128:309-318.
32.CLAEREBOUT E, VERCAUTEREN I, GELDHOF P, OLBRECHTS A, ZARLENGA DS, GODDEERIS BM et al. Cytokine responses in immunized and non-immunized calves after Ostertagia ostertagi infection. Parasite Immunol 2005;27:325-331
33.SWIDERSKI CE, KLEI TR, FOLSOM RW, POURCIAU SS, CHAPMAN A, CHAPMAN RR et al. Vaccination against Strongylus vulgaris in ponies: comparison of the humoral and cytokine responses of vaccinates and nonvaccinates. Adv Vet Med Vet Vacc Diagn 1999;41:389-404.
34.GOMEZ MORALES MA, MELE R, SANCHEZ M, SACCHINI D, DE GIACOMO M, POZIO E. Increased CD8+-T-cell expression and type 2 cytokine pattern during the muscular phase of Trichinella infection in humans. Infect Immun 2002;70:233-239.
35.MAIZELS RM, YAZDANBAKHSH M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol 2003;3:733-744.
36.WEINSTOCK JV. Helminths and mucosal immune modulation. Ann NY Acad Sci 2006;1072:356-364.
37.VAN RIET E, HARTGERS FC, YAZDANBAKHSH M. Chronic helminth infections induce immunomodulation: consequences and mechanisms. Immunobiology 2007; 212:475-490.
38.FALLON PG, MANGAN NE. Suppresion of TH2-type allergic reactions by helminth infection. Nat Rev Immunol 2007;7:220-230.
39.GORDON S. Alternative activation of macrophages. Nat Rev Immunol 2002;3:23-35.
40.ANTHONY RM, RUTITZKY LI, URBAN JR JF, STADECKER MJ, GAUSE WC. Protective immune mechanism in helminth infection. Nat Rev Immunol 2007;7:975-987.
1.ANONYMOUS. Get the balance right. Nat Immunol 2005;6:1177.
2.HENSON PM. Dampening inflammation. Nat Immunol 2005;6:1179-1181.
3.ABBAS AK, LICHTMAN AH, PILLAI SP. Cellular and molecular immunology. 6th ed. Philadelphia: Saunders Elsevier, 2007.
4.NAIRN R, HELBERT M. Immunology for medical students. 2nd ed. Philadelphia: Mosby Elsevier, 2007.
5.GERSHWIN LJ. Veterinary autoimmunity: Autoimmune diseases in domestic animals. Ann NY Acad Sci 2007;1109:109-116.
6.ERB KJ. Helminths, allergic disorders and IgE-mediated immune responses: where do we stand? Eur J Immunol 2007;37:1170-1173.
7.SEDER RA, PAUL WE. Acquisition of lymphokine-prodas ducing phenotype by CD4+ T cells. Annu Rev Immunol 1994;12:635-673.
8.SANDERSON CJ, CAMPBELL HD, YOUNG IG. Molecular and cellular biology of eosinophil differentiation factor (interleukin-5) and its effects on human and Mouse B cells. Immunol Rev 1988;102:29-50.
9.COFFMAN RL, SEYMOUR BWP, HUDAK S, JACKSON J, RENNICK D. Antibody to interleukin-5 inhibits helminth-induced eosinophilia in mice. Science 1989;245:308-310.
10.BACELLAR O, DÓLIVEIRA A JR, JERONIMO S, CARVALHO EM. IL-10 and IL-12 are the main regulatory cytokines in visceral leishmaniasis. Cytokine 2000;12:1228-1231.
11.FINNEY CAM, TAYLOR MD, WILSON MS, MAIZELS RM. Expansion and activation of CD+CD25+ regulatory T cells in Heligmosomoides polygyrus infection. Eur J Immunol 2007;37:1874-1886.
12.O’NEILL SM, BRADY MT, CALLANAN JJ, MULCAHY G, JOYCE P, MILLS KH et al. Fasciola hepatica infection downregulates Th1 responses in mice. Parasite Immunol 2000;22:147-155.
13.PESCE JT, LIU Z, HAMED H, ALEM F, WHITMIRE J, LIN H et al. Neutrophils clear bacteria associated with parasitic nematodes augmenting the development of an effective Th2-type response. J Immunol 2008;180:464-474.
14.PATERSON S, BARBER R. Experimental evolution of parasite life-story traits in Strongyloides ratti (Nematoda). Proc Biol Soc 2007;274:1467-1474.
15.GIRONES N, VALERO MA, GARCIA-BODELON MA, CHICO-CALERO I, PUNZON C, FRESNO et al. Immune suppression in advanced chronic fascioliasis: an experimental study in a rat model. J Infec Dis 2007;195:1504-1512.
16.WEBB RA, HOQUE T, DIMAS S. Expulsion of the gastrointestinal cestode, Hymenolepis diminuta by tolerant rats: evidence for mediation by a Th2 type immune enhanced goblet cell hyperplasia, increased mucin production and secretion. Parasite Immunol 2007;29:11-21.
17.JITTIMANEE J, SERMSWAN RW, PUAPAIROJ A, MALEEWONG W, WONGRTANACHEEWIN S. Cytokine expression in hamsters experimentally infected with Opistorchis viverrini. Parasite Immunol 2007;29:159- 167.
18.MENDEZ S, VALENZUELA JG, WU W, HOTEZ PJ. Cytokine production, lymphoproliferation, and antibody responses during the course of Ancylostoma ceylanicum infection in the golden hamster. Infect Immun 2005;73:3402-3407.
19.DEGEN WG, DAAL N, ROTHWELL L, KAISER P, SCHIJNS VE. Th1/Th2 polarization by viral and helminth infection in birds. Vet Microbiol 2005; 105:163- 167.
20.TORINA A, CARACAPPA S, BARERA A, DIELI F, SIRECI G, GENCHI C et al. Toxocara canis infection induces antigen-specific IL-10 and IFNgamma production in pregnant dogs and their puppies. Vet Immunol Immunopathol 2005;108:247-251.
21.MORCHON R, LOPEZ-BELMONTE J, BAZZOCCHI C, GRANDI G, KRAMER L, SIMON F. Dogs with patent Dirofilaria immitis infection have higher expression of circulating IL-4, IL-10 and iNOS mRNA than those with occult infection. Vet Immunol Immunopathol 2007;115:184-188.
22.GILBERT S, HALLIWELL REW. The effects of endoparasitism on the immune response to orally administered antigen in cats. Vet Immunol Immunopathol 2005;106:113-120.
23.DAWSON HD, BESHAH E, NISHI S, SOLANOAGUILAR G, MORIMOTO M, ZHAO A et al. Localized multigene expression patterns support an evolving Th1/Th2-like paradigm in response to infections with Toxoplasma gondii and Ascaris suum. Infect Immun 2005;73:1116-1128.
24.KRINGEL H, IBURG T, DAWSON H, AASTED B, ROEPSTORFF A. A time course study of immunological responses in Trichuris suis infected pigs demonstrates induction of local type 2 response associated with worm burden. Int J Parasitol 2006:36:915-924.
25.TECHAU ME, JOHANSEN MV, AASTED B, LIND P, ORNBJERG N, OSWALD IP. Cytokine mRNA profiles in pigs exposed prenatally and postnatally to Schistosoma japonicum. Vet Res 2007;38:25-36.
26.LACROUX C, NGUYEN THC, ANDREOLETTI O, PREVOT F, GRISEZ C, BERGAUD JP et al. Haemonchus contortus (Nematoda:Trichostongylidae) infection in lambs elicits an unequivocal Th2 immune response. Vet Res 2006;37:607-622.
27.PERNTHANER A, COLE SA, MORRISON L, HEIN WR. Increased expression of interleukin-5 (IL-5), IL-13, and tumor necrosis factor alfa genes in intestinal lymph cells of sheep selected for enhanced resistance to nematodes during infection with Trichostrongylus colubriformis. Infect Immun 2005;73:2175-2183.
28.BROWN WC, DAVIES WC, DOBBELAERE DA, RICEFICHT AC. CD4+ T-cell clones obtained from cattle chronically infected with Fasciola hepatica and specific for adult Word antigen Express both unrestricted and Th2 cytokines profiles. Infect Immun 1994; 62:818-827.
29.FLYNNN RJ, MANNION C, GOLDEN O, HACARIZ O, MULCAHY G. Experimental Fasciola hepatica infection alters responses to tests used for diagnosis of bovine tuberculosis. Infect Immun 2007;75:1373-1381.
30.FLYNN RJ, MULCAHY G. Possible role of Toll-like receptors in interaction of Fasciola hepatica excretory/ secretory products with bovine macrophages. Infect Immun 2008;76:678-684.
31.JOHNSON DR, SALES J, MATTHEWS JB. Local cytokine responses in Dictiocaulus viviparous infection. Vet Parasitol 2005;128:309-318.
32.CLAEREBOUT E, VERCAUTEREN I, GELDHOF P, OLBRECHTS A, ZARLENGA DS, GODDEERIS BM et al. Cytokine responses in immunized and non-immunized calves after Ostertagia ostertagi infection. Parasite Immunol 2005;27:325-331
33.SWIDERSKI CE, KLEI TR, FOLSOM RW, POURCIAU SS, CHAPMAN A, CHAPMAN RR et al. Vaccination against Strongylus vulgaris in ponies: comparison of the humoral and cytokine responses of vaccinates and nonvaccinates. Adv Vet Med Vet Vacc Diagn 1999;41:389-404.
34.GOMEZ MORALES MA, MELE R, SANCHEZ M, SACCHINI D, DE GIACOMO M, POZIO E. Increased CD8+-T-cell expression and type 2 cytokine pattern during the muscular phase of Trichinella infection in humans. Infect Immun 2002;70:233-239.
35.MAIZELS RM, YAZDANBAKHSH M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol 2003;3:733-744.
36.WEINSTOCK JV. Helminths and mucosal immune modulation. Ann NY Acad Sci 2006;1072:356-364.
37.VAN RIET E, HARTGERS FC, YAZDANBAKHSH M. Chronic helminth infections induce immunomodulation: consequences and mechanisms. Immunobiology 2007; 212:475-490.
38.FALLON PG, MANGAN NE. Suppresion of TH2-type allergic reactions by helminth infection. Nat Rev Immunol 2007;7:220-230.
39.GORDON S. Alternative activation of macrophages. Nat Rev Immunol 2002;3:23-35.
40.ANTHONY RM, RUTITZKY LI, URBAN JR JF, STADECKER MJ, GAUSE WC. Protective immune mechanism in helminth infection. Nat Rev Immunol 2007;7:975-987.
41.ELLIOT DE, SUMMERS RW, WEISNTOCK JV. Helminths and the modulation of mucosal inflammation. Curr Opin Gastroenterol 2005;21:51-58.
42.YAZDANBAKHSH M, KREMSNER PG, VAN REE R. Allergy, parasites, and the hygiene hypothesis. Science 2002;296:490-494.
43.KLAUS JE. Helminths, allergic disorders and IgEmediated immune responses: Where do we stand? Eur J Immunol 2007;37:1170-1173.
44.STANWELL-SMITH R, BLOOMFIELD S. The hygiene hypothesis and implications for home hygiene. A report commissioned by The International Scientific Forum on Home Hygiene (IFH). Milano, Italy: Arti Grafiche Bazzi, 2004.
45.FIASSE R, LATINNE D. Intestinal Helminths: a clue explaining the low incidence of inflammatory bowel diseases in Subsaharan Africa? Potential benefits and hazards of helminth therapy. Acta Gastroenterol Beld 2006;69:418-422.
46.LIMA C, PERINI A, GARCIA ML, MARTINS MA,TEIXEIRA MM, MACEDO MS. Eosinophilic inflammation and airway hyper-responsiveness are profoundly inhibited by a helminth (Ascaris suum) extract in a murine model of asthma. Clin Exp Allergy 2002;32:1659-1666.
47.MCCONCHIE BW, NORRIS HH, BUNDOC VG,TRIVEDI S, BOESEN A, URBAN JR JF et al. Ascaris suum-derived products suppres mucosal allergic inflammation in an interleukin-10-independent manner via interference with dendritic cell function. Infect Immun 2006;74:6632-6641.
48.SCHOPF L, LUCCIOLI S, BUNDOC V, JUSTICE P, CHAN CC, WETZEL B et al. Differential modulation of allergic eye disease by chronic and acute Ascaris infection. Investig Ophthalmol Vis Sci 2005;46:2772-2780.
49.IMAI S, TEZUKA H, FUJITA K. A factor of inducing IgE from filarial parasite prevents insulin-dependent diabetes mellitus in nonobese diabetic mice. Biochem Biophys Res Commun 2001;286:1051-1058.
50.ZACCONE P, FEHERVARI Z, PHILLIPS JM, DUNNE DW, COOKE A. Parasitic worms and inflammatory diseases. Parasite Immunol 2006;28:515-523.
51.SAUNDERS KA, RAINE T, COOKE A, LAWRENCE CE. Inhibition of autoimmune type 1 diabetes by gastrointestinal helminth infection. Infect Immun 2007;75:397-407.
52.COOKE A, TONOS P, JONES FM, O´SHEA H, HUTCHINGS P, FULFORD AJ et al. Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in non-obese diabetic mice. Parasite Immunol 1999;21:169-176.
53.MANGAN NE, VAN ROOIJEN N, MCKENZIE ANJ, FALLON PG. Helminth-modified pulmonary immune response protects mice from allergen-induced airway hyperresponsiveness. J Immunol 2006;176:138-147.
54.ELLIOT DE, SUMMERS RW, WEINSTOCK JV. Helminths as governors of immune-mediated inflammation. Int J Parasitol 2007;37:457-464.
55.SUMMERS RW, ELLIOT DE, QADIR K, URBAN JF JR, THOMPSON R, WEISTOCK JV. Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am J Gastroenterol 2003;98:2034-2041.
56.SUMMERS RW, ELLIOT DE, URBAN JF JR, THOMPSON RA, WEINSTOCK JV. Trichuris suis therapy for active ulcerative colitis: a randomixed controlled trial. Gastroenterology 2005:128:825-832.
57.SUMMERS RW, ELLIOT DE, QADIR K, URBAN JF JR, THOMPSON R, WEISTOCK JV. Trichuris suis therapy in Crohn´s disease. Gut 2005;54:87-90.
58.REDDY A, FRIED B. The use of Trichuris suis and other helminth therapies to treat Crohn´s disease. Parasitol Res 2007;100:1432-1955.
59.BAUTISTA GARFIAS CR, OROZCO M, MORALES E. Modulación de la respuesta de anticuerpos a eritrocitos de pollo en ovinos infectados experimentalmente con Fasciola hepatica. Rev Mex Parasitol 1988; 1:14-18.
60.BRADY MT, O´NEILL SM, DALTON JP, MILLS KHG.Fasciola hepatica suppresses a protective Th1 response against Bordetella pertussis. Infec Immun 1999; 67:5372- 5378.
61.URBAN JR JF, STEENHARD NR, SOLANO-AGUILAR GI, DAWSON HD, IWEALA OI, NAGLER CR et al. Infection with parasitic nematodes confounds vaccination efficacy. Vet Parasitol 2007;148:14-20.
62.FLYNN RJ, MANNION C, GOLDEN O, HACARIZ O, MULCAHY. Experimental Fasciola hepatica infection alters responses to tests used for diagnosis of bovine tuberculosis, Infect Immun 2007;75:1373-1381.
63.MACDONALDAS, ARAUJO MI, PEARCE EJ. Immunology of parasitic helminth infections. Infec Immun 2002;70:427-433.
64.BASHIR MEH, ANDERSEN P, FUSS IJ, SHI HN, NAGLER-ANDERSON C. An enteric helminth infection protects against an allergic response to dietary antigen. J Immunol 2002;169:3284-3292.
65.WEINSTOCK JV, SUMMERS RW, ELLIOTT DE. Helminths and harmony. Gut 2004;53:7-9.
66.ARTIS D. New weapons in the war on worms: identification of putative mechanisms of immune-mediated expulsion of gastrointestinal nematodes. Int J Parasitol 2006; 36:723-733.
67.ANTHONY RM, URBAN JR JF, ALEM F, HAMED HA, ROZO CT, BOUCHER JL et al. Memory Th2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat Med 2006;12:955-960.
68.GEIGER SM, CALDAS IR, MC GLONE BE, CAMPIAZEVEDO AC, DE OLIVEIRA LM, BROOKER S et al. Stage-specific immune responses in human Necator americanus infection. Parasite Immunol 2007;29:347-358.
69.HUMPHREYS NE, XU D, HEPWORTH MR, LIEW FY, GRENCIS RK. IL-33, a potent inducer of adaptive immunity to intestinal nematodes. J Immunol 2008;180:2443-2449.
70.POCHANKE V, KOLLER S, DAYER R, HATAK S, LUDEWIG B, ZINKERNAGEL RM et al. Identification and characterization of a novel antigen from the nema- tode Nippostrongylus brasiliensis recognized by specific IgE. Eur J Immunol 2007;37:1275-1284.
71.HUNTER MM, MCKAY DM. Review article: helminths as therapeutic agents for inflammatory bowel disease. Aliment Pharmacol Ther 2004;19:167-177.
72.PROUDFOOT L. Parasitic helminths tip the balance: potential anti-inflammatory therapies. Immunology 2004;113:438-440.
73.OWYANG AM, ZAPH C, WILSON EH, GUILD KJ, MCCLANAHAN T, MILLER HRP et al. Interleukin 25 regulates type 2 cytokine-dependent immunity and limits chronic inflammation in the gastrointestinal tract. J Exp Med 2006;4:843-849.
74.BAUTISTA-GARFIAS CR, FLORES-HERNANDEZ O, QUIROZ-ROMERO H. Non-specific resistance of sheep against Haemonchus contortus with Freund's complete adjuvant. Parasite Immunol 1991; 13: 565-569.
75.BAUTISTA GARFIAS CR, GÓMEZ ARROYO A, MORILLA GONZÁLEZ A, VERA MONTENEGRO Y, IBARRA VELARDE F. Inducción de resistencia inespecífica contra la infección por Fasciola hepatica en ovinos con adyuvante completo de Freund. Rev Méx Parasitol 1992;3: 1-3.
76.BAUTISTA GARFIAS CR, ZERON F, DE LA JARA F, FLORES R. Effect of three immunostimulants on the resistance against Trichinella spiralis infection in mice. (Preliminary Report). Arch Med Res 1995;26: 91-93.
77.BAUTISTA-GARFIAS CR, ORDUÑA M, IXTA O, MARTINEZ F, AGUILAR B, CORTES A. Enhancement of resistance in mice treated with Lactobacillus casei: Effect on Trichinella spiralis infection. Vet Parasitol 1999;80:251-260.
78.BAUTISTA-GARFIAS CR, IXTA-RODRIGUEZ O, MARTINEZ-GOMEZ F, LOPEZ MG, AGUILARFIGUEROA BR.. Effect of viable or dead Lactobacillus casei organisms administered orally to mice on resistance against Trichinella spiralis infection. Parasite 2001; 8: S226-S228.
79.BAUTISTA-GARFIAS CR, IXTA-RODRIGUEZ O, AGUILAR-FIGUEROA BR, MARTINEZ-GOMEZ F, MIRALRIO-FLORES L. Induction of resistance against Hymenolepis nana infection in NIH mice treated intraperitoneally with Lactobacillus casei. Proceedings of the 10th Internacional Congress of Parasitology-ICOPA X; 2002 August 4-9; Vancouver, Canada. Bologna, Italy: Monduzzi Editore S.p.A. –Medimond Inc. 2002–:.645-648.
80.BAUTISTA GARFIAS CR, POSADAS BELTRÁN A, IXTA RODRÍGUEZ O. Inmunización de ratones BALB/c con un antígeno de larvas musculares de Trichinella spiralis utilizando Lactobacillus casei como adyuvante. Vet Méx 2004; 35: 359-368.
81.MATSUZAKI T, YAMAZAKI R, HASHIMOTO S, YOKOKURA T. The effect of oral feeding of Lactobacillus casei strain shirota on immunoglobulin E production in mice. J Dairy Sci 1998;81:48-53.
82.KATO I, TANAKA K, YOKOKURA T. Lactic acid bacterium induces the production of interleukin-12 and interferon-gamma by mouse splenocytes. Int J Immunopharmacol 1999:21:121-131.
83.SHIBAKI A, KATZ SI. Induction of skewed Th1/Th2 T-cell differentiation via subcutaneous immunization with Freund’s adjuvant. Exp Dermatol 2002;11:126-134.
84.CERVI L, BORGONOVO J, EGEA M, CHIAPELLO L, MASIH D. Immunization of rats against Fasciola hepatica using crude antigens conjugated with Freund’s adjuvant or oligodeoxynucleotides. Vet Immunol Immunopathol 2004;97:97-104
85.AGRAWAL A, DILLON S, DENNING TL, PULENDRAN B. ERK1-/- mice exhibit Th1 polarization and increased susceptibility to experimental autoimmune encephalomyelitis. J Immunol 2006;176:5788-5796.
86.RIGANO R, BUTTARI B, PROFUMO E, ORTONA E, DELUNARDO F, MARGUTTI P et al. Equinococcus granulosus antigen B impairs human dendritic cell differentiation and polarize immature dendritic cell maturation towards a Th2 cell response. Infec Immun 2007; 75:1667-1678.