Helminth infections prevent autoimmune diseases through Th2-type immune response

Yonago Acta Medica

Volumn 52, Issue 3, 2009, Pages 95-104

  Fukumoto, Soji ^a   Iriko, Hideyuki ^a   Otsuki, Hitoshi ^b  

^a TOTTORI UNIVERSITY   (Japan)

^b EHIME UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Alternatively activated macrophage; Autoimmune disease; Helminth; T helper 2; Thymic stromal lymphopoietin

Indexed keywords

CD4 ANTIGEN; CYTOKINE; INTERLEUKIN 33; INTERLEUKIN 4; MESSENGER RNA; THYMIC STROMAL LYMPHOPOIETIN;

AUTOIMMUNE DISEASE; BASOPHIL; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CYTOKINE RELEASE; DENDRITIC CELL; ENTERITIS; HELMINTH; HELMINTHIASIS; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; INFLAMMATION; INNATE IMMUNITY; INSULIN DEPENDENT DIABETES MELLITUS; INTESTINE EPITHELIUM CELL; MACROPHAGE; MAST CELL; MOLECULAR RECOGNITION; NONHUMAN; PARASITE; PARASITOSIS; PHENOTYPE; PROTECTION; REVIEW; TH2 CELL; WORM EXPULSION; WOUND HEALING;

EID: 70450177672     PISSN: 05135710     EISSN: 13468049     Source Type: Journal    
DOI: None     Document Type: Review

References (90)

1. Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F. Interleukins 1β and 6 but not transforming growth factor-β are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol 2007;8:942-949. (Pubitemid 47300008)
2. Allakhverdi Z, Comeau MR, Jessup HK, Yoon BR, Brewer A, Chartier S, et al. Thymic stromal lymphopoietin is released by human epithelial cells in response to microbes, trauma, or inflammation and potently activates mast cells. J Exp Med 2007;204:253-258. (Pubitemid 46294541)
3. Anthony RM, Rutitzky LI, Urban JF Jr, Stadecker MJ, Gause WC. Protective immune mechanisms in helminth infection. Nat Rev Immunol 2007;7:975-987.
4. H2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat Med 2006;12:955-960.
5. Arinobu Y, Iwasaki H, Gurish MF, Mizuno S, Shigematsu H, Ozawa H, et al. Developmental checkpoints of the basophil/mast cell lineages in adult murine hematopoiesis. Proc Natl Acad Sci USA 2005;102:18105-18110. (Pubitemid 41798509)
6. Artis D, Kane CM, Fiore J, Zaph C, Shapira S, Joyce K, et al. Dendritic cell-intrinsic expression of NF- κB1 is required to promote optimal Th2 cell differentiation. J Immunol 2005;174:7154-7159. (Pubitemid 40705682)
7. Balic A, Harcus Y, Holland MJ, Maizels RM. Selective maturation of dendritic cells by Nippostrongylus brasiliensis- secreted proteins drives Th2 immune responses. Eur J Immunol 2004;34:3047-3059.
8. Blumberg RS, Strober W. Prospects for research in in- flammatory bowel disease. JAMA 2001; 285:643-647. (Pubitemid 32656339)
9. Bonecchi R, Sozzani S, Stine JT, Luini W, D'Amico G, Allavena P, et al. Divergent effects of interleukin-4 and interferon- on macrophage-derived chemokine production: an amplification circuit of polarized T helper 2 responses. Blood 1998;92:2668-2671. (Pubitemid 28469077)
10. Bouma G, Strober W. The immunological and genetic basis of inflammatory bowel disease. Nat Rev Immunol 2003;3:521-533. (Pubitemid 37328672)
11. Brunner M, Krenn C, Roth G, Moser B, Dworschak M, Jensen-Jarolim E, et al. Increased levels of soluble ST2 protein and IgG1 production in patients with sepsis and trauma. Intensive Care Med 2004;30:1468-1473. (Pubitemid 38951733)
12. Chappaz S, Flueck L, Farr AG, Rolink AG, Finke D. Increased TSLP availability restores T- and B-cell compartments in adult IL-7 deficient mice. Blood 2007;110:3862-3870. (Pubitemid 350248441)
13. Cooke A, Tonks 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.
14. Cooke A, Zaccone P, Raine T, Phillips J M, Dunne DW. Infection and autoimmunity: are we winning the war, only to lose the peace? Trends Parasitol 2004;20:316-321.
15. Croese J, O'neil J, Masson J, Cooke S, Melrose W, Pritchard D, et al. A proof of concept study establishing Necator americanus in Crohn's patients and reservoir donors. Gut 2006;55:136-137.
16. David T, Thomas C, Zaccone P, Dunne DW, Cooke A. The impact of infection on the incidence of autoimmune disease. Curr Top Med Chem 2004;4:521-529. (Pubitemid 38832735)
17. Donnelly S, O'Neill SM, Sekiya M, Mulcahy G, Dalton JP. Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages. Infect Immun 2005;73:166-173.
18. Donnelly S, Stack CM, O'Neill SM, Sayed AA, Williams DL, Dalton JP. Helminth 2-Cys peroxiredoxin drives Th2 responses through a mechanism involving alternatively activated macrophages. FASEB J 2008;22:4022-4032.
19. Dzik JM, Golos B, Jagielska E, Zielinski Z, Walajtys-Rode E. A non-classical type of alveolar macrophage response to Trichinella spiralis infection. Parasite Immunol 2004;26:197-205.
20. Elliott DE, Li J, Blum A, Metwali A, Qadir K, Urban JF Jr, et al. Exposure to schistosome eggs protects mice from TNBS-induced colitis. Am J Physiol Gastrointest Liver Physiol 2003;284:G385-G391. (Pubitemid 36227886)
21. Elliott DE, Setiawan T, Metwali A, Blum A, Urban JF Jr, Weinstock JV. Heligmosomoides polygyrus inhibits established colitis in IL-10-deficient mice. Eur J Immunol 2004;34:2690-2698.
22. Fallon PG, Ballantyne SJ, Mangan NE, Barlow JL, Dasvarma A, Hewett DR, et al. 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 2006;203:1105-1116.
23. Faveeuw C, Mallevaey T, Paschinger K, Wilson IB, Fontaine J, Mollicone R, et al. Schistosome N-glycans containing core 3-fucose and core β2-xylose epitopes are strong inducers of Th2 responses in mice. Eur J Immunol 2003;33:1271-1281. (Pubitemid 36609145)
24. Finkelman FD, Shea-Donohue T, Morris SC, Gildea L, Strait R, Madden KB, et al. Interleukin-4- and interleukin- 13-mediated host protection against intestinal nematode parasites. Immunol Rev 2004;201:139-155. (Pubitemid 39318449)
25. Florian S, Sonneck K, Czerny M, Hennersdorf F, Hauswirth AW, Bühring HJ, et al. Detection of novel leukocyte differentiation antigens on basophils and mast cells by HLDA8 antibodies. Allergy 2006;61:1054-1062. (Pubitemid 44175211)
26. Gale EA. The rise of childhood type 1 diabetes in the 20th century. Diabetes 2002; 51:3353-3361. (Pubitemid 35403436)
27. Gause WC, Urban JF Jr, Stadecker MJ. The immune response to parasitic helminths: insights from murine models. Trends Immunol 2003;24:269-277.
28. Goerdt S, Orfanos CE. Other functions, other genes: alternative activation of antigen-presenting cells. Immunity 1999;10:137-142. (Pubitemid 29115619)
29. Gordon S, Alternative activation of macrophages. Nat Rev Immunol 2003;3:23-35.
30. Gomez-Garcia L, Rivera-Montoya I, Rodriguez-Sosa M, Terrazas LI. Carbohydrate components of Taenia crassiceps metacestodes display Th2-adjuvant and antiinflammatory properties when co-injected with bystander antigen. Parasitol Res 2006;99:440-448.
31. Goodridge HS, Marshall FA, Else KJ Houston KM, Egan C, Al-Riyami L, et al. Immunomodulation via novel use of TLR4 by the filarial nematode phosphorylcholine- containing secreted product, ES-62. J Immunol 2005;174:284-293. (Pubitemid 40007415)
32. Helmby H, Grencis RK. Essential role for TLR4 and MyD88 in the development of chronic intestinal nematode infection. Eur J Immunol 2003;33:2974-2979. (Pubitemid 37428329)
33. Herber t DR, Holscher C, Mohrs M, Arendse B, Schwegmann A, Radwanska M, et al. Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 2004;20:623-635.
34. Holland MJ, Harcus YM, Riches PL, Maizels RM. Proteins secreted by the parasitic nematode Nippostrongylus brasiliensis act as adjuvants for Th2 responses. Eur J Immunol 2000;30:1977-1987.
35. 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.
36. Imai T, Nagira M, Takagi S, Kakizaki M, Nishimura M, Wang J, et al. Selective recruitment of CCR4-bearing Th2 cells toward antigen-presenting cells by the CC chemok ines thymus and activation-regulated chemokine and macrophage- derived chemokine. Int Immunol 1999;11:81-88. (Pubitemid 29037591)
37. Imai S, Tezuka H, Fujita K. A factor of inducing IgE from a filarial parasite prevents insulin-dependent diabetes mellitus in nonobese diabetic mice. Biochem Biophys Res Commun 2001;286:1051-1058. (Pubitemid 32924878)
38. Ito T, Wang YH, Duramad O, Hori T, Delespesse GJ, Watanabe N, et al. TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J Exp Med 2005;202:1213-1223. (Pubitemid 41586952)
39. Kane CM, Cervi L, Sun J, McKee AS, Masek KS, Shapira S, et al. Helminth antigens modulate TLR-initiated dendritic cell activation. J Immunol 2004;173:7454-7461. (Pubitemid 39628185)
40. Khan WI, Blennerhasset PA, Varghese AK, Chowdhury SK, Omsted P, Deng Y, et al. Intestinal nematode infection ameliorates experimental colitis in mice. Infect Immun 2002;70:5931-5937. (Pubitemid 35192680)
41. La Flamme AC, Ruddenklau K, Bäckström BT. Schistosomiasis decreases central nervous system inflammation and alters the progression of experimental autoimmune encephalomyelitis. Infect Immun 2003;71:4996-5004. (Pubitemid 37070742)
42. Layland LE, Wagner H, da Costa CU. Lack of antigenspecific Th1 response alters granuloma formation and composition in Schistosoma mansoni-infected MyD88-/- mice. Eur J Immunol 2005;35:3248-3257.
43. Lee HC, Ziegler SF. Inducible expression of the proallergic cytokine thymic stromal lymphopoietin in airway epithelial cells is controlled by NFkB. Proc Natl Acad Sci USA 2007;104:914-919. (Pubitemid 46154711)
44. Leech MD, Grencis RK. Induction of enhanced immunity to intestinal nematodes using IL-9-producing dendritic cells. J Immunol 2006;176:2505-2511.
45. Loke P, Nair MG, Parkinson J, Guiliano D, Blaxter M, Allen JE. IL-4 dependent alternatively-activated macrophages have a distinctive in vivo gene expression phenotype. BMC Immunol 2002;3:7-11. (Pubitemid 38692919)
46. Liu T, Dhanasekaran SM, Jin H, Hu B, Tomlins SA, Chinnaiyan AM, et al. FIZZ1 stimulation of myofibroblast differentiation. Am J Pathol 2004;164:1315-1326.
47. Liu YJ, Soumelis V, Watanabe N, Ito T, Wang YH, Malefyt Rde W, et al. TSLP: an epithelial cell cytokine that regulates T cell differentiation by conditioning dendritic cell maturation. Annu Rev Immunol 2007;25:193-219. (Pubitemid 46697907)
48. MacDonald AS, Straw AD, Bauman B, Pearce EJ. CD8- dendritic cell activation status plays an integral role in influencing Th2 response development. J Immunol 2001; 167:1982-1988. (Pubitemid 32747504)
49. Martin P, Leibovich SJ. Inflammatory cells during wound repair: the good, the bad and the ugly. Trends Cell Biol 2005;15:599-607. (Pubitemid 41619424)
50. Massacand JC, Stettler RC, Meier R, Humphreys NE, Grencis RK, Marsland BJ, et al. Helminth products bypass the need for TSLP in Th2 immune responses by directly modulating dendritic cell function. Proc Natl Acad Sci USA 2009;106:13968-13973.
51. McInnes IB, Leung BP, Harnett M, Gracie JA, Liew FY, Harnett W. A novel therapeutic approach targeting articular inflammation using the filarial nematode-derived phosphorylcholine-containing glycoprotein ES-62. J Immunol 2003;171 :2127-2133. (Pubitemid 36966497)
52. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature 2007;449:819-826. (Pubitemid 47598622)
53. Min B, Prout M, Hu-Li J, Zhu J, Jankovic D, Morgan ES, et al. Basophils produce IL-4 and accumulate in tissues after infection with a Th2-inducing parasite. J Exp Med 2004;200:507-517. (Pubitemid 39121907)
54. Motomura Y, Wang H, Deng Y, El-Sharkawy RT, Verdu EF, Khan WI. Helminth antigen-based strategy to ameliorate inflammation in an experimental model of colitis. Clin Exp Immunol 2008;155:88-95.
55. Nakanishi K, Yoshimoto T, Tsutsui H, Okamura H. Interleukin- 18 regulates both Th1 and Th2 responses. Annu Rev Immunol 2001;19:423-474. (Pubitemid 32368042)
56. Nair MG, Cochrane DW, Allen JE. Macrophages in chronic type 2 inflammation have a novel phenotype characterized by the abundant expression of Ym1 and Fizz1 that can be partly replicated in vitro. Immunol Lett 2003;85:173-180.
57. Nair MG, Gallagher IJ, Taylor MD, Loke P, Coulson PS, Wilson RA, et al. Chitinase and Fizz family members are a generalized feature of nematode infection with selective upregulation of Ym1 and Fizz1 by antigen-presenting cells. Infect Immun 2005;73:385-394. (Pubitemid 40041131)
58. Okano M, Satoskar AR, Nishizaki K, Harn DA Jr. Lacto- N-fucopentaose III found on Schistosoma mansoni egg antigens functions as adjuvant for proteins by inducing Th2-type response. J Immunol 2001;167:442-450.
59. Omori M, Ziegler S. Induction of IL-4 expression in CD4+ T cells by thymic stromal lymphopoietin. J Immunol 2007;178:1396-1404. (Pubitemid 46154610)
60. Oshikawa K, Kuroiwa K, Tago K, Iwahana H, Yanagisawa K, Ohno S. Elevated soluble ST2 protein levels in sera of patients with asthma with an acute exacerbation. Am J Respir Crit Care Med 2001;164:277-281. (Pubitemid 34001295)
61. Owhashi M, Arita H, Hayai N. Identification of a novel eosinophil chemotactic cytokine (ECF-L) as a chitinase family protein. J Biol Chem 2000;275:1279-1286. (Pubitemid 30051182)
62. Owyang AM, Zaph C, Wi lson EH, Gui ld KJ, McClanahan T, Miller HR, et al. Interleukin 25 regulates type 2 cytokine-dependent immunity and limits chronic inflammation in the gastrointestinal tract. J Exp Med 2006;203:843-849.
63. Raes G, De Baetselier P, Noel W, Beschin A, Brombacher F, Hassanzadeh Gh G. Differential expression of FIZZ1 and Ym1 in alternatively versus classically activated macrophages. J Leukoc Biol 2002;71:597-602.
64. Reardon C, Sanchez A, Hogaboam CM, McKay DM. Tapeworm infection reduces epithelial ion transport abnormalities in murine dextran sulfate sodium-induced colitis. Infect Immun 2001;69:4417-4423. (Pubitemid 32574440)
65. Reese TA, Liang HE, Tager AM, Luster AD, Van Rooijen N, Voehringer D, et al. Chitin induces accumulation in tissue of innate immune cells associated with allergy. Nature 2007;447:92-96. (Pubitemid 46685837)
66. Rimoldi M, Chieppa M, Salucci V, Avogadri F, Sonzogni A, Sampietro GM, et al. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat Immunol 2005;6:507-514. (Pubitemid 41716764)
67. Rodriguez-Sosa M, Satoskar AR, Calderon R, Gomez Garcia L, Saavedra R, Bojalil R, et al. Chronic helminth infection induces alternatively activated macrophages expressing high levels of CCR5 with low interleukin-12 production and Th2-biasing ability. Infect Immun 2002; 70:3656-3664. (Pubitemid 34666004)
68. Sandler NG, Mentink-Kane MM, Cheever AW, Wynn TA. Global gene expression profiles during acute pathogeninduced pulmonary inflammation reveal divergent roles for Th1 and Th2 responses in tissue repair. J Immunol 2003;171:3655-3667.
69. Saunders KA, Raine T, Cooke A, Lawrence CE. Inhibition of autoimmune type 1 diabetes by gastrointestinal helminth infection. Infect Immun 2007;75:397-407. (Pubitemid 46047916)
70. Sewell D, Qing Z, Reinke E, Elliot D, Weinstock J, Sandor M, et al. Immunomodulation of experimental autoimmune encephalomyelitis by helminth ova immunization. Int Immunol 2003;15:59-69. (Pubitemid 36163769)
71. Shinkai K, Mohrs M, Locksley RM. Helper T cells regulate type-2 innate immunity in vivo. Nature 2002;420: 825-829. (Pubitemid 36019631)
72. Smith P, Mangan NE, Walsh CM, Fallon RE, McKenzie AN, van Rooijen N, et al. Infection with a helminth parasite prevents experimental colitis via a macrophagemediated mechanism. J Immunol 2007;178:4557-4566. (Pubitemid 46492408)
73. Song E, Ouyang N, Hörbelt M, Antus B, Wang M, Exton MS. Influence of alternatively and classically activated macrophages on fibrogenic activities of human fibroblasts. Cell Immunol 2000;204:19-28. (Pubitemid 30766296)
74. Soumelis V, Reche PA, Kanzler H, Yuan W, Edward G, Homey B, et al. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat Immunol 2002;3:673-680. (Pubitemid 34752477)
75. Stein M, Keshav S, Harris N, Gordon S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med 1992;176:287-292.
76. Summers RW, Elliott DE, Qadir K, Urban JF Jr, Thompson R, Weinstock JV. Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am J Gastroenterol 2003;98:2034-2041.
77. Summers RW, Elliott DE, Urban JF Jr, Thompson R, Weinstock JV. Trichuris suis therapy in Crohn's disease. Gut 2005a;54:87-90.
78. Summers RW, Elliott DE, Urban JF Jr, Thompson RA, Weinstock JV. Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 2005b;128:825-832.
79. + T cell hyporesponsiveness at sites peripheral to filarial infection. J Immunol 2006;176:6918-6927.
80. Taylor BC, Zaph C, Troy AE, Du Y, Guild KJ, Comeau MR, et al. TSLP regulates intestinal immunity and inflammation in mouse models of helminth infection and colitis. J Exp Med 2009;206:655-667.
81. Thomas PG, Carter MR, Atochina O, Da'Dara AA, Piskorska D, McGuire E, et al. Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Tolllike receptor 4-dependent mechanism. J Immunol 2003;171:5837-5841. (Pubitemid 37467200)
82. Thomas PG, Carter MR, Da'dara AA, DeSimone TM, Harn DA. A helminth glycan induces APC maturation via alternative NF- κB activation independent of I B degradation. J Immunol 2005;175:2082-2090.
83. van der Kleij D, Latz E, Brouwers JF, Kruize YC, Schmitz M, Kurt-Jones EA, et al. A novel host-parasite lipid crosstalk. Schistosomal lyso-phosphatidylserine activates tolllike receptor 2 and affects immune polarization. J Biol Chem 2002;277:48122-48129. (Pubitemid 35470760)
84. van Vliet SJ, Garcia-Vallejo JJ, van Kooyk Y. Dendritic cells and C-type lectin receptors: coupling innate to adaptive immune responses. Immunol Cell Biol 2008;86:580-587.
85. Voehringer D, van Rooijen N, Locksley RM. Eosinophils develop in distinct stages and are recruited to peripheral sites by alternatively activated macrophages. J Leukoc Biol 2007;81:1434-1444. (Pubitemid 46827966)
86. Yoshimoto T, Nakanishi K. Roles of IL-18 in basophils and mast cells. Allergol Int 2006;55:105-113. (Pubitemid 43973882)
87. Zaccone P, Fehervari Z, Jones FM, Sidobre S, Kronenberg M, Dunne DW, et al. Schistosoma mansoni antigens modulate the activity of the innate immune response and prevent onset of type 1 diabetes. Eur J Immunol 2003;33:1439-1449.
88. Zeuthen LH, Fink LN, Frokiaer H. Epithelial cells prime the immune response to an array of gut-derived commensals towards a tolerogenic phenotype through distinct actions of thymic stromal lymphopoietin and transforming growth factor-β . Immunology 2008;123:197-208.
89. Zhu Z, Zheng T, Homer RJ, Kim YK, Chen NY, Cohn L, et al. Acidic mammalian chitinase in asthmatic Th2 inflammation and IL-13 pathway activation. Science 2004;304:1678-1682. (Pubitemid 38765861)
90. Ziegler SF, Liu YJ. Thymic stromal lymphopoietin in normal and pathogenic T cell development and function. Nat Immunol 2006;7:709-714. (Pubitemid 43905869)