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The Role of Antibody in Parasitic Helminth Infections

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How Helminths Alter Immunity to Infection

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 828))

Abstract

A wealth of data on the protective immune mechanisms induced following helminth infection exist, but how antibody responses protect against helminth infections is unclear and shows variation between species. Understanding antibody responses to different helminth species is important to support the future development of anti-helminth vaccines that will be robust enough to protect against/inhibit infection (acute or chronic). Both the biological similarities and diversity of helminths highlights the importance of understanding both broad anti-helminth and species-specific host antibody responses. Vaccine development requires knowledge of which molecules would stimulate the most protective antibody responses, and whether certain molecules would be cross-reactive between species to be used for protection against multiple helminth species. Such information may lead to a reduced cost of vaccine development, encouraging effective implementation. The aim of this chapter is to assimilate our current understanding of antibody responses to helminths in mice, livestock and humans, and to discuss their importance in the context of potential vaccine development.

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References

  1. Pearce EJ, Caspar P, Grzych JM, Lewis FA, Sher A (1991) Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J Exp Med 173(1):159–166 (PubMed PMID: 1824635. Pubmed Central PMCID: 2118762)

    Google Scholar 

  2. Horsnell WG, Darby MG, Hoving JC, Nieuwenhuizen NE, McSorley HJ, Ndlovu H et al (2013) IL-4Ralpha associated antigen processing by B cells promotes immunity in Nippostrongylus brasiliensis infection. PLoS Pathog 9(10):1–12

    Article  Google Scholar 

  3. Bancroft AJ, McKenzie AN, Grencis RK (1998) A critical role for IL-13 in resistance to intestinal nematode infection. J Immunol 160(7):3453–3461 (PubMed PMID: 9531306)

    Google Scholar 

  4. Bancroft AJ, Artis D, Donaldson DD, Sypek JP, Grencis RK (2000) Gastrointestinal nematode expulsion in IL-4 knockout mice is IL-13 dependent. Eur J Immunol 30(7):2083–2091 (PubMed PMID: 10940898)

    Google Scholar 

  5. Kuhn R, Rajewsky K, Muller W (1991) Generation and analysis of interleukin-4 deficient mice. Science 254(5032):707–710 (PubMed PMID: 1948049)

    Google Scholar 

  6. Lawrence RA, Gray CA, Osborne J, Maizels RM (1996) Nippostrongylus brasiliensis: cytokine responses and nematode expulsion in normal and IL-4-deficient mice. Exp Parasitol 84(1):65–73 (PubMed PMID: 8888733)

    Google Scholar 

  7. Barner M, Mohrs M, Brombacher F, Kopf M (1998) Differences between IL-4R alpha-deficient and IL-4-deficient mice reveal a role for IL-13 in the regulation of Th2 responses. Curr Biol 8(11):669–672 (PubMed PMID: 9635196)

    Google Scholar 

  8. McKenzie GJ, Bancroft A, Grencis RK, McKenzie AN (1998) A distinct role for interleukin-13 in Th2-cell-mediated immune responses. Curr Biol 8(6):339–342 (PubMed PMID: 9512421)

    Google Scholar 

  9. Urban JF Jr, Noben-Trauth N, Donaldson DD, Madden KB, Morris SC, Collins M et al (1998) IL-13, IL-4Ralpha, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity 8(2):255–264 (PubMed PMID: 9492006)

    Google Scholar 

  10. Curry AJ, Else KJ, Jones F, Bancroft A, Grencis RK, Dunne DW (1995) Evidence that cytokine-mediated immune interactions induced by Schistosoma mansoni alter disease outcome in mice concurrently infected with Trichuris muris. J Exp Med 181(2):769–774 (PubMed PMID: 7836929. Pubmed Central PMCID: 2191884)

    Google Scholar 

  11. Else KJ, Finkelman FD, Maliszewski CR, Grencis RK (1994) Cytokine-mediated regulation of chronic intestinal helminth infection. J Exp Med 179(1):347–351 (PubMed PMID: 8270879. Pubmed Central PMCID: 2191309)

    Google Scholar 

  12. Svetic A, Madden KB, Zhou XD, Lu P, Katona IM, Finkelman FD et al (1993) A primary intestinal helminthic infection rapidly induces a gut-associated elevation of Th2-associated cytokines and IL-3. J Immunol 150(8 Pt 1):3434–3441 (PubMed PMID: 8468481)

    Google Scholar 

  13. Cooper PJ, Chico ME, Sandoval C, Espinel I, Guevara A, Kennedy MW et al (2000) Human infection with Ascaris lumbricoides is associated with a polarized cytokine response. J Infect Dis 182(4):1207–1213 (PubMed PMID: 10979919)

    Google Scholar 

  14. Turner JD, Faulkner H, Kamgno J, Cormont F, Van Snick J, Else KJ et al (2003) Th2 cytokines are associated with reduced worm burdens in a human intestinal helminth infection. J Infect Dis 188(11):1768–1775 (PubMed PMID: 14639550)

    Google Scholar 

  15. Jackson JA, Turner JD, Rentoul L, Faulkner H, Behnke JM, Hoyle M et al (2004) T helper cell type 2 responsiveness predicts future susceptibility to gastrointestinal nematodes in humans. J Infect Dis 190(10):1804–1811 (PubMed PMID: 15499537)

    Google Scholar 

  16. Schmidt S, Hoving JC, Horsnell WG, Mearns H, Cutler AJ, Brombacher TM et al (2012) Nippostrongylus-induced intestinal hypercontractility requires IL-4 receptor alpha-responsiveness by T cells in mice. PloS One 7(12):e52211 (PubMed PMID: 23284939. Pubmed Central PMCID: 3527412)

    Google Scholar 

  17. Marillier RG, Brombacher TM, Dewals B, Leeto M, Barkhuizen M, Govender D et al (2010) IL-4R{alpha}-responsive smooth muscle cells increase intestinal hypercontractility and contribute to resistance during acute Schistosomiasis. Am J Physiol Gastrointestinal Liver Physiol 298(6):G943–G951 (PubMed PMID: 20360135)

    Google Scholar 

  18. Zhao A, Urban JF Jr, Anthony RM, Sun R, Stiltz J, van Rooijen N et al (2008) Th2 cytokine-induced alterations in intestinal smooth muscle function depend on alternatively activated macrophages. Gastroenterology 135(1):217–225.e1 (PubMed PMID: 18471439. Pubmed Central PMCID: 2954589)

    Google Scholar 

  19. Cliffe LJ, Humphreys NE, Lane TE, Potten CS, Booth C, Grencis RK (2005) Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science 308(5727):1463–1465 (PubMed PMID: 15933199)

    Google Scholar 

  20. Hasnain SZ, Wang H, Ghia JE, Haq N, Deng Y, Velcich A et al (2010) Mucin gene deficiency in mice impairs host resistance to an enteric parasitic infection. Gastroenterology 138(5):1763–1771 (PubMed PMID: 20138044. Pubmed Central PMCID: 3466424)

    Google Scholar 

  21. Hasnain SZ, Evans CM, Roy M, Gallagher AL, Kindrachuk KN, Barron L et al (2011) Muc5ac: a critical component mediating the rejection of enteric nematodes. J Exp Med 208(5):893–900 (PubMed PMID: 21502330. Pubmed Central PMCID: 3092342)

    Google Scholar 

  22. Paul WE, Ohara J (1987) B-cell stimulatory factor-1/interleukin 4. Annual Rev Immunol 5:429–459 (PubMed PMID: 3297106)

    Google Scholar 

  23. Coffman RL, Ohara J, Bond MW, Carty J, Zlotnik A, Paul WE (1986) B cell stimulatory factor-1 enhances the IgE response of lipopolysaccharide-activated B cells. J Immunol 136(12):4538–4541 (PubMed PMID: 3486902)

    Google Scholar 

  24. Lebman DA, Coffman RL (1988) Interleukin 4 causes isotype switching to IgE in T cell-stimulated clonal B cell cultures. J Exp Med 168(3):853–862 (PubMed PMID: 3049907. Pubmed Central PMCID: 2189023)

    Google Scholar 

  25. Kepron MR, Chen YW, Uhr JW, Vitetta ES (1989) IL-4 induces the specific rearrangement of gamma 1 genes on the expressed and unexpressed chromosomes of lipopolysaccharide-activated normal murine B cells. J Immunol 143(1):334–339 (PubMed PMID: 2786532)

    Google Scholar 

  26. Esser C, Radbruch A (1989) Rapid induction of transcription of unrearranged S gamma 1 switch regions in activated murine B cells by interleukin 4. EMBO J 8(2):483–488 (PubMed PMID: 2785916. Pubmed Central PMCID: 400830)

    Google Scholar 

  27. Rothman P, Lutzker S, Cook W, Coffman R, Alt FW (1988) Mitogen plus interleukin 4 induction of C epsilon transcripts in B lymphoid cells. J Exp Med 168(6):2385–2389 (PubMed PMID: 3264328. Pubmed Central PMCID: 2189140)

    Google Scholar 

  28. Gauchat JF, Lebman DA, Coffman RL, Gascan H, de Vries JE (1990) Structure and expression of germline epsilon transcripts in human B cells induced by interleukin 4 to switch to IgE production. J Exp Med 172(2):463–473 (PubMed PMID: 1695667. Pubmed Central PMCID: 2188335)

    Google Scholar 

  29. Mizoguchi C, Uehara S, Akira S, Takatsu K (1999) IL-5 induces IgG1 isotype switch recombination in mouse CD38-activated sIgD-positive B lymphocytes. J Immunol 162(5):2812–2819 (PubMed PMID: 10072528)

    Google Scholar 

  30. Kikuchi Y, Yasue T, Miyake K, Kimoto M, Takatsu K (1995) CD38 ligation induces tyrosine phosphorylation of Bruton tyrosine kinase and enhanced expression of interleukin 5-receptor alpha chain: synergistic effects with interleukin 5. Proc Natl Acad Sci U S A 92(25):11814–11818 (PubMed PMID: 8524855. Pubmed Central PMCID: 40493)

    Google Scholar 

  31. Shapira SK, Jabara HH, Thienes CP, Ahern DJ, Vercelli D, Gould HJ et al (1991) Deletional switch recombination occurs in interleukin-4-induced isotype switching to IgE expression by human B cells. Proc Natl Acad Sci U S A 88(17):7528–7532 (PubMed PMID: 1881893. Pubmed Central PMCID: 52334)

    Google Scholar 

  32. Tangye SG, Ferguson A, Avery DT, Ma CS, Hodgkin PD (2002) Isotype switching by human B cells is division-associated and regulated by cytokines. J Immunol 169(8):4298–4306 (PubMed PMID: 12370361)

    Google Scholar 

  33. Gascan H, Gauchat JF, Roncarolo MG, Yssel H, Spits H, de Vries JE (1991) Human B cell clones can be induced to proliferate and to switch to IgE and IgG4 synthesis by interleukin 4 and a signal provided by activated CD4+ T cell clones. J Exp Med 173(3):747–750 (PubMed PMID: 1997653. Pubmed Central PMCID: 2118815)

    Google Scholar 

  34. Punnonen J, Aversa G, Cocks BG, McKenzie AN, Menon S, Zurawski G et al (1993) Interleukin 13 induces interleukin 4-independent IgG4 and IgE synthesis and CD23 expression by human B cells. Proc Natl Acad Sci U S A 90(8):3730–3734 (PubMed PMID: 8097323. Pubmed Central PMCID: 46375)

    Google Scholar 

  35. Vallance BA, Galeazzi F, Collins SM, Snider DP (1999) CD4 T cells and major histocompatibility complex class II expression influence worm expulsion and increased intestinal muscle contraction during Trichinella spiralis infection. Infect Immun 67(11):6090–6097 (PubMed PMID: 10531271. Pubmed Central PMCID: 96997)

    Google Scholar 

  36. Holland MJ, Harcus YM, Balic A, Maizels RM (2005) Th2 induction by Nippostrongylus secreted antigens in mice deficient in B cells, eosinophils or MHC Class I-related receptors. Immunol Lett 96(1):93–101 (PubMed PMID: 15585312)

    Google Scholar 

  37. Hernandez HJ, Wang Y, Tzellas N, Stadecker MJ (1997) Expression of class II, but not class I, major histocompatibility complex molecules is required for granuloma formation in infection with Schistosoma mansoni. Eur J Immunol 27(5):1170–1176 (PubMed PMID: 9174607)

    Google Scholar 

  38. Linsley PS, Ledbetter JA (1993) The role of the CD28 receptor during T cell responses to antigen. Annual Rev Immunol 11:191–212 (PubMed PMID: 8386518)

    Google Scholar 

  39. Harris NL, Prout M, Peach RJ, Fazekas de St Groth B, Ronchese F (2001) CD80 costimulation is required for Th2 cell cytokine production but not for antigen-specific accumulation and migration into the lung. J Immunol 166(8):4908–4914 (PubMed PMID: 11290768)

    Google Scholar 

  40. Urban J, Fang H, Liu Q, Ekkens MJ, Chen SJ, Nguyen D et al (2000) IL-13-mediated worm expulsion is B7 independent and IFN-gamma sensitive. J Immunol 164(8):4250–4256 (PubMed PMID: 10754322)

    Google Scholar 

  41. Liu Z, Liu Q, Pesce J, Whitmire J, Ekkens MJ, Foster A et al (2002) Nippostrongylus brasiliensis can induce B7-independent antigen-specific development of IL-4-producing T cells from naive CD4 T cells in vivo. J Immunol 169(12):6959–6968 (PubMed PMID: 12471130)

    Google Scholar 

  42. Greenwald RJ, Lu P, Halvorson MJ, Zhou X, Chen S, Madden KB et al (1997) Effects of blocking B7-1 and B7-2 interactions during a type 2 in vivo immune response. J Immunol 158(9):4088–4096 (PubMed PMID: 9126967)

    Google Scholar 

  43. Ndlovu H, Darby M, Froelich M, Horsnell W, Lühder F, Hünig T, Brombacher F (2014) Inducible deletion of CD28 prior to secondary Nippostrongylus brasiliensis infection impairs worm expulsion and recall of protective memory CD4+ T cell responses. PLoS Pathog 10(2):e1003906 (PubMed PMID: 24516382)

    Google Scholar 

  44. Gause WC, Chen SJ, Greenwald RJ, Halvorson MJ, Lu P, Zhou XD et al (1997) CD28 dependence of T cell differentiation to IL-4 production varies with the particular type 2 immune response. J Immunol 158(9):4082–4087 (PubMed PMID: 9126966)

    Google Scholar 

  45. Gause WC, Lu P, Zhou XD, Chen SJ, Madden KB, Morris SC et al (1996) H. polygyrus: B7-independence of the secondary type 2 response. Exp Parasitol 84(2):264–273 (PubMed PMID: 8932776)

    Google Scholar 

  46. Horsnell WG, Vira A, Kirstein F, Mearns H, Hoving JC, Cutler AJ et al (2011) IL-4Ralpha-responsive smooth muscle cells contribute to initiation of TH2 immunity and pulmonary pathology in Nippostrongylus brasiliensis infections. Mucosal Immunol 4(1):83–92 (PubMed PMID: 20737001)

    Google Scholar 

  47. Urban JF Jr, Noben-Trauth N, Schopf L, Madden KB, Finkelman FD (2001) Cutting edge: IL-4 receptor expression by non-bone marrow-derived cells is required to expel gastrointestinal nematode parasites. J Immunol 167(11):6078–6081 (PubMed PMID: 11714764)

    Google Scholar 

  48. Dewals B, Hoving JC, Leeto M, Marillier RG, Govender U, Cutler AJ et al (2009) IL-4Ralpha responsiveness of non-CD4 T cells contributes to resistance in schistosoma mansoni infection in pan-T cell-specific IL-4Ralpha-deficient mice. Am J Pathol 175(2):706–716 (PubMed PMID: 19628763. Pubmed Central PMCID: 2716945)

    Google Scholar 

  49. Metwali A, Blum A, Elliott DE, Weinstock JV (2002) Interleukin-4 receptor alpha chain and STAT6 signaling inhibit gamma interferon but not Th2 cytokine expression within schistosome granulomas. Infect Immunity 70(10):5651–5658 (PubMed PMID: 12228294. Pubmed Central PMCID: 128339)

    Google Scholar 

  50. Urban JF Jr, Schopf L, Morris SC, Orekhova T, Madden KB, Betts CJ et al (2000) Stat6 signaling promotes protective immunity against Trichinella spiralis through a mast cell- and T cell-dependent mechanism. J Immunol 164(4):2046–2052 (PubMed PMID: 10657657)

    Google Scholar 

  51. Khan WI, Vallance BA, Blennerhassett PA, Deng Y, Verdu EF, Matthaei KI et al (2001) Critical role for signal transducer and activator of transcription factor 6 in mediating intestinal muscle hypercontractility and worm expulsion in Trichinella spiralis-infected mice. Infect Immunity 69(2):838–844 (PubMed PMID: 11159976. Pubmed Central PMCID: 97960)

    Google Scholar 

  52. Zhu J, Yamane H, Cote-Sierra J, Guo L, Paul WE (2006) GATA-3 promotes Th2 responses through three different mechanisms: induction of Th2 cytokine production, selective growth of Th2 cells and inhibition of Th1 cell-specific factors. Cell Res 16(1):3–10 (PubMed PMID: 16467870)

    Google Scholar 

  53. Zheng W, Flavell RA (1997) The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 89(4):587–596 (PubMed PMID: 9160750)

    Google Scholar 

  54. Zhu J, Min B, Hu-Li J, Watson CJ, Grinberg A, Wang Q et al (2004) Conditional deletion of Gata3 shows its essential function in T(H)1-T(H)2 responses. Nat Immunol 5(11):1157–1165 (PubMed PMID: 15475959)

    Google Scholar 

  55. Marillier RG, Michels C, Smith EM, Fick LC, Leeto M, Dewals B et al (2008) IL-4/IL-13 independent goblet cell hyperplasia in experimental helminth infections. BMC Immunol 9:11 (PubMed PMID: 18373844. Pubmed Central PMCID: 2329604)

    Google Scholar 

  56. Herbert DR, Holscher C, Mohrs M, Arendse B, Schwegmann A, Radwanska M et al (2004) Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 20(5):623–635 (PubMed PMID: 15142530)

    Google Scholar 

  57. Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK et al (2005) IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23(5):479–490 (PubMed PMID: 16286016)

    Google Scholar 

  58. Humphreys NE, Xu D, Hepworth MR, Liew FY, Grencis RK (2008) IL-33, a potent inducer of adaptive immunity to intestinal nematodes. J Immunol 180(4):2443–2449 (PubMed PMID: 18250453)

    Google Scholar 

  59. Marcet R, Diaz A, Arteaga E, Finlay CM, Sarracent J (2002) Passive protection against fasciolosis in mice by immunization with a monoclonal antibody (ES-78 MoAb). Parasite Immunol 24(2):103–108 (PubMed PMID: 11874565)

    Google Scholar 

  60. Dixon H, Little MC, Else KJ (2010) Characterisation of the protective immune response following subcutaneous vaccination of susceptible mice against Trichuris muris. Int J Parasitol 40(6):683–693 (PubMed PMID: 19968992. Pubmed Central PMCID: 2896472)

    Google Scholar 

  61. Attallah AM, Attia H, El-Nashar EM, Nawar A, Abdel Kader K, Ismail H et al (1999) Induction of resistance against Schistosoma mansoni infection by passive transfer of an IgG2a monoclonal antibody. Vaccine 17(18):2306–2310 (PubMed PMID: 10403599)

    Google Scholar 

  62. Ligas JA, Kerepesi LA, Galioto AM, Lustigman S, Nolan TJ, Schad GA et al (2003) Specificity and mechanism of immunoglobulin M (IgM)- and IgG-dependent protective immunity to larval Strongyloides stercoralis in mice. Infect Immunity 71(12):6835–6843 (PubMed PMID: 14638770. Pubmed Central PMCID: 308934)

    Google Scholar 

  63. Harris NL, Spoerri I, Schopfer JF, Nembrini C, Merky P, Massacand J et al (2006) Mechanisms of neonatal mucosal antibody protection. J Immunol 177(9):6256–6262 (PubMed PMID: 17056555)

    Google Scholar 

  64. Kerepesi LA, Nolan TJ, Schad GA, Lustigman S, Herbert DR, Keiser PB et al (2004) Human immunoglobulin G mediates protective immunity and identifies protective antigens against larval Strongyloides stercoralis in mice. J Infect Dis 189(7):1282–1290 (PubMed PMID: 15031798)

    Google Scholar 

  65. Hewitson JP, Filbey KJ, Grainger JR, Dowle AA, Pearson M, Murray J et al (2011) Heligmosomoides polygyrus elicits a dominant nonprotective antibody response directed against restricted glycan and peptide epitopes. J Immunol 187(9):4764–4777 (PubMed PMID: 21964031)

    Google Scholar 

  66. Gu Y, Wei J, Yang J, Huang J, Yang X, Zhu X (2013) Protective immunity against Trichinella spiralis infection induced by a multi-epitope vaccine in a Murine Model. PloS One 8(10):e77238 (PubMed PMID: 24130862. Pubmed Central PMCID: 3795051)

    Google Scholar 

  67. Cui J, Ren HJ, Liu RD, Wang L, Zhang ZF, Wang ZQ (2013) Phage-displayed specific polypeptide antigens induce significant protective immunity against Trichinella spiralis infection in BALB/c mice. Vaccine 31(8):1171–1177 (PubMed PMID: 23306358)

    Google Scholar 

  68. Blackwell NM, Else KJ (2001) B cells and antibodies are required for resistance to the parasitic gastrointestinal nematode Trichuris muris. Infect Immunity 69(6):3860–3868 (PubMed PMID: 11349052. Pubmed Central PMCID: 98409)

    Google Scholar 

  69. Martin C, Saeftel M, Vuong PN, Babayan S, Fischer K, Bain O et al (2001) B-cell deficiency suppresses vaccine-induced protection against murine filariasis but does not increase the recovery rate for primary infection. Infect Immunity 69(11):7067–7073 (PubMed PMID: 11598082. Pubmed Central PMCID: 100087)

    Google Scholar 

  70. Liu Q, Kreider T, Bowdridge S, Liu Z, Song Y, Gaydo AG et al (2010) B cells have distinct roles in host protection against different nematode parasites. J Immunol 184(9):5213–5223 (PubMed PMID: 20357259. Pubmed Central PMCID: 3729113)

    Google Scholar 

  71. El-Malky MA, Maruyama H, Al-Harthi SA, El-Beshbishi SN, Ohta N (2013) The role of B-cells in immunity against adult Strongyloides venezuelensis. Parasit Vectors 6:148 (PubMed PMID: 23705584. Pubmed Central PMCID: 3669613)

    Google Scholar 

  72. McCoy KD, Stoel M, Stettler R, Merky P, Fink K, Senn BM et al (2008) Polyclonal and specific antibodies mediate protective immunity against enteric helminth infection. Cell Host Microbe 4(4):362–373 (PubMed PMID: 18854240)

    Google Scholar 

  73. Rajan B, Ramalingam T, Rajan TV (2005) Critical role for IgM in host protection in experimental filarial infection. J Immunol 175(3):1827–1833 (PubMed PMID: 16034125)

    Google Scholar 

  74. Watanabe N, Katakura K, Kobayashi A, Okumura K, Ovary Z (1988) Protective immunity and eosinophilia in IgE-deficient SJA/9 mice infected with Nippostrongylus brasiliensis and Trichinella spiralis. Proc Natl Acad Sci U S A 85(12):4460–4462 (PubMed PMID: 3380800. Pubmed Central PMCID: 280449)

    Google Scholar 

  75. El Ridi R, Ozaki T, Kamiya H (1998) Schistosoma mansoni infection in IgE-producing and IgE-deficient mice. J Parasitol 84(1):171–174 (PubMed PMID: 9488359)

    Google Scholar 

  76. Gurish MF, Bryce PJ, Tao H, Kisselgof AB, Thornton EM, Miller HR et al (2004) IgE enhances parasite clearance and regulates mast cell responses in mice infected with Trichinella spiralis. J Immunol 172(2):1139–1145 (PubMed PMID: 14707089)

    Google Scholar 

  77. Anthony RM, Rutitzky LI, Urban JF Jr, Stadecker MJ, Gause WC (2007) Protective immune mechanisms in helminth infection. Nature Rev Immunol 7(12):975–987 (PubMed PMID: 18007680. Pubmed Central PMCID: 2258092)

    Google Scholar 

  78. Harris N, Gause WC (2011) To B or not to B: B cells and the Th2-type immune response to helminths. Trends Immunol 32(2):80–88 (PubMed PMID: 21159556. Pubmed Central PMCID: 3076625)

    Google Scholar 

  79. Herbst T, Esser J, Prati M, Kulagin M, Stettler R, Zaiss MM et al (2012) Antibodies and IL-3 support helminth-induced basophil expansion. Proc Natl Acad Sci U S A 109(37):14954–14959 (PubMed PMID: 22930820. Pubmed Central PMCID: 3443190)

    Google Scholar 

  80. Ohnmacht C, Schwartz C, Panzer M, Schiedewitz I, Naumann R, Voehringer D (2010) Basophils orchestrate chronic allergic dermatitis and protective immunity against helminths. Immunity 33(3):364–374 (PubMed PMID: 20817571)

    Google Scholar 

  81. Ohnmacht C, Voehringer D (2010) Basophils protect against reinfection with hookworms independently of mast cells and memory Th2 cells. J Immunol 184(1):344–350 (PubMed PMID: 19955520)

    Google Scholar 

  82. Perrigoue JG, Saenz SA, Siracusa MC, Allenspach EJ, Taylor BC, Giacomin PR et al (2009) MHC class II-dependent basophil-CD4+ T cell interactions promote T(H)2 cytokine-dependent immunity. Nature Immunol 10(7):697–705 (PubMed PMID: 19465906. Pubmed Central PMCID: 2711559)

    Google Scholar 

  83. Sullivan BM, Liang HE, Bando JK, Wu D, Cheng LE, McKerrow JK et al (2011) Genetic analysis of basophil function in vivo. Nature Immunol 12(6):527–535 (PubMed PMID: 21552267. Pubmed Central PMCID: 3271435)

    Google Scholar 

  84. Matsumoto M, Sasaki Y, Yasuda K, Takai T, Muramatsu M, Yoshimoto T et al (2013) IgG and IgE collaboratively accelerate expulsion of Strongyloides venezuelensis in a primary infection. Infect Immunity 81(7):2518–2527 (PubMed PMID: 23630966. Pubmed Central PMCID: 3697603)

    Google Scholar 

  85. Wojciechowski W, Harris DP, Sprague F, Mousseau B, Makris M, Kusser K et al (2009) Cytokine-producing effector B cells regulate type 2 immunity to H. polygyrus. Immunity 30(3):421–433 (PubMed PMID: 19249230. Pubmed Central PMCID: 2745290)

    Google Scholar 

  86. McVay CS, Tsung A, Appleton J (1998) Participation of parasite surface glycoproteins in antibody-mediated protection of epithelial cells against Trichinella spiralis. Infect Immunity 66(5):1941–1945 (PubMed PMID: 9573073. Pubmed Central PMCID: 108147)

    Google Scholar 

  87. McVay CS, Bracken P, Gagliardo LF, Appleton J (2000) Antibodies to tyvelose exhibit multiple modes of interference with the epithelial niche of Trichinella spiralis. Infect Immunity 68(4):1912–1918 (PubMed PMID: 10722582. Pubmed Central PMCID: 97366)

    Google Scholar 

  88. Nieuwenhuizen NE, Meter JM, Horsnell WG, Hoving JC, Fick L, Sharp MF et al (2013) A cross-reactive monoclonal antibody to nematode haemoglobin enhances protective immune responses to Nippostrongylus brasiliensis. PLoS Negl Trop Dis 7(8):e2395 (PubMed PMID: 24009787. Pubmed Central PMCID: 3757078)

    Google Scholar 

  89. Hagan P, Blumenthal UJ, Dunn D, Simpson AJ, Wilkins HA (1991) Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature 349(6306):243–245 (PubMed PMID: 1898985)

    Google Scholar 

  90. Jiz M, Friedman JF, Leenstra T, Jarilla B, Pablo A, Langdon G et al (2009) Immunoglobulin E (IgE) responses to paramyosin predict resistance to reinfection with Schistosoma japonicum and are attenuated by IgG4. Infect Immunity 77(5):2051–2058 (PubMed PMID: 19273558. Pubmed Central PMCID: 2681753)

    Google Scholar 

  91. Li Y, Sleigh AC, Ross AG, Li Y, Zhang X, Williams GM et al (2001) Human susceptibility to Schistosoma japonicum in China correlates with antibody isotypes to native antigens. Trans R Soc Trop Med Hyg 95(4):441–448 (PubMed PMID: 11579893)

    Google Scholar 

  92. Demeure CE, Rihet P, Abel L, Ouattara M, Bourgois A, Dessein AJ (1993) Resistance to Schistosoma mansoni in humans: influence of the IgE/IgG4 balance and IgG2 in immunity to reinfection after chemotherapy. J Infect Dis 168(4):1000–1008 (PubMed PMID: 7690821)

    Google Scholar 

  93. Pinot de Moira AJ, Mwatha JK et al (2013) Effects of treatment on IgE responses against parasite allergen-like proteins and immunity to reinfection in childhood schistosome and hookworm coinfections. Infect Immun 81(1):23–32 (PubMed PMID: 23071136. Pubmed Central PMCID: 3536155)

    Google Scholar 

  94. Dafa’alla TH, Ghalib HW, Abdelmageed A, Williams JF (1992) The profile of IgG and IgG subclasses of onchocerciasis patients. Clin Exp Immunol 88(2):258–263 (PubMed PMID: 1572089. Pubmed Central PMCID: 1554306)

    Google Scholar 

  95. Turner JD, Faulkner H, Kamgno J, Kennedy MW, Behnke J, Boussinesq M et al (2005) Allergen-specific IgE and IgG4 are markers of resistance and susceptibility in a human intestinal nematode infection. Microbes Infect 7(7–8):990–996 (PubMed PMID: 15961339)

    Google Scholar 

  96. Hagel I, Cabrera M, Buvat E, Gutierrez L, Santaella C, Borges R et al (2008) Antibody responses and resistance against Ascaris lumbricoides infection among Venezuelan rural children: the influence of ethnicity. J Trop Pediatr 54(5):354–356 (PubMed PMID: 18453627)

    Google Scholar 

  97. van Riet EW, Tielens AG et al (2006) Antibody responses to Ascaris-derived proteins and glycolipids: the role of phosphorylcholine. Parasite Immunol 28(8):363–371 (PubMed PMID: 16879308)

    Google Scholar 

  98. Figueiredo CA, Barreto ML, Rodrigues LC, Cooper PJ, Silva NB, Amorim LD et al (2010) Chronic intestinal helminth infections are associated with immune hyporesponsiveness and induction of a regulatory network. Infect Immun 78(7):3160–3167 (PubMed PMID: 20404082. Pubmed Central PMCID: 2897394)

    Google Scholar 

  99. Hussain R, Ottesen EA (1986) IgE responses in human filariasis. IV. Parallel antigen recognition by IgE and IgG4 subclass antibodies. J Immunol 136(5):1859–1863 (PubMed PMID: 3950405)

    Google Scholar 

  100. Hussain R, Poindexter RW, Ottesen EA (1992) Control of allergic reactivity in human filariasis. Predominant localization of blocking antibody to the IgG4 subclass. J Immunol 148(9):2731–2737 (PubMed PMID: 1573266)

    Google Scholar 

  101. van de Veen WS, Akdis DG et al (2013) IgG(4) production is confined to human IL-10-producing regulatory B cells that suppress antigen-specific immune responses. J Allergy Clin Immun 131(4):1204–1212 (PubMed PMID: WOS:000317187200031. English)

    Google Scholar 

  102. Schuurman J, Van Ree R, Perdok GJ, Van Doorn HR, Tan KY, Aalberse RC (1999) Normal human immunoglobulin G4 is bispecific: it has two different antigen-combining sites. Immunology 97(4):693–698 (PubMed PMID: 10457225. Pubmed Central PMCID: 2326875)

    Google Scholar 

  103. Karagiannis P, Gilbert AE, Josephs DH, Ali N, Dodev T, Saul L et al (2013) IgG4 subclass antibodies impair antitumor immunity in melanoma. J Clin Invest 123(4):1457–1474 (PubMed PMID: 23454746. Pubmed Central PMCID: 3613918)

    Google Scholar 

  104. Zack DJ, Stempniak M, Wong AL, Weisbart RH (1995) Localization of an Fc-binding reactivity to the constant region of human IgG4. Implications for the pathogenesis of rheumatoid arthritis. J Immunol 155(10):5057–5063 (PubMed PMID: 7594514)

    Google Scholar 

  105. Canals A, Zarlenga DS, Almeria S, Gasbarre LC (1997) Cytokine profile induced by a primary infection with Ostertagia ostertagi in cattle. Vet Immunol Immunopathol 58(1):63–75 (PubMed PMID: 9343340)

    Google Scholar 

  106. Canals A, Gasbarre LC (1990) Ostertagia ostertagi: isolation and partial characterization of somatic and metabolic antigens. Int J Parasitol 20(8):1047–1054 (PubMed PMID: 2074130)

    Google Scholar 

  107. Mansour MM, Dixon JB, Clarkson MJ, Carter SD, Rowan TG, Hammet NC (1990) Bovine immune recognition of Ostertagia ostertagi larval antigens. Vet Immunol Immunopathol 24(4):361–371 (PubMed PMID: 2339503)

    Google Scholar 

  108. Klesius PH, Washburn SM, Haynes TB (1986) Serum antibody response to soluble extract of the third-larval stage of Ostertagia ostertagi in cattle. Vet Parasitol 20(4):307–314 (PubMed PMID: 3716175)

    Google Scholar 

  109. Almeria S, Canals A, Gomez-Munoz MT, Zarlenga DS, Gasbarre LC (1998) Characterization of protective immune responses in local lymphoid tissues after drug-attenuated infections with Ostertagia ostertagi in calves. Vet Parasitol 80(1):53–64 (PubMed PMID: 9877071)

    Google Scholar 

  110. Geldhof P, Claerebout E, Knox D, Vercauteren I, Looszova A, Vercruysse J (2002) Vaccination of calves against Ostertagia ostertagi with cysteine proteinase enriched protein fractions. Parasite Immunol 24(5):263–270 (PubMed PMID: 12060320)

    Google Scholar 

  111. Laing R, Kikuchi T, Martinelli A, Tsai IJ, Beech RN, Redman E et al (2013) The genome and transcriptome of Haemonchus contortus, a key model parasite for drug and vaccine discovery. Genome Biol 14(8):R88 (PubMed PMID: 23985316)

    Google Scholar 

  112. Ortolani EL, Leal ML, Minervino AH, Aires AR, Coop RL, Jackson F et al (2013) Effects of parasitism on cellular immune response in sheep experimentally infected with Haemonchus contortus. Vet Parasitol 196(1–2):230–234 (PubMed PMID: 23522899)

    Google Scholar 

  113. Alba-Hurtado F, Munoz-Guzman MA (2013) Immune responses associated with resistance to haemonchosis in sheep. BioMed Res Int 2013:162158 (PubMed PMID: 23509684. Pubmed Central PMCID: 3591228)

    Google Scholar 

  114. Bowdridge S, MacKinnon K, McCann JC, Zajac AM, Notter DR (2013) Hair-type sheep generate an accelerated and longer-lived humoral immune response to Haemonchus contortus infection. Vet Parasitol 196(1–2):172–178 (PubMed PMID: 23414615)

    Google Scholar 

  115. De la Chevrotière C, Bambou JC, Arquet R, Jacquiet P, Mandonnet N (2012) Genetic analysis of the potential role of IgA and IgE responses against Haemonchus contortus in parasite resistance of Creole goats. Vet Parasitol 186(3–4):337–343

    Article  PubMed  Google Scholar 

  116. Sahoo S, Murugavel S, Devi KI, Vedamurthy GV, Gupta SC, Singh BP et al (2013) Glyceraldehyde 3 phosphate dehydrogenase of the parasitic nematode Haemonchus contortus binds to complement C3 and inhibits its activity. Parasite Immunol 35(12):457–467 (PubMed PMID: 23927077)

    Google Scholar 

  117. Echevarria F, Borba MFS, Pinheiro AC, Waller PJ, Hansen JW (1996) The prevalence of anthelmintic resistance in nematode parasites of sheep in Southern Latin America: Brazil. Vet Parasitol 62:199–206

    Article  PubMed  CAS  Google Scholar 

  118. Rialch A, Vatsya S, Kumar RR (2013) Detection of benzimidazole resistance in gastrointestinal nematodes of sheep and goats of sub-Himalyan region of northern India using different tests. Vet Parasitol 198(3–4):312–318 (PubMed PMID: 24126090)

    Google Scholar 

  119. Piedrafita DP, de Veer MJ, Sherrard J, Kraska T, Elhay M, Meeusen EN (2012) Field vaccination of sheep with a larval-specific antigen of the gastrointestinal nematode, Haemonchus contortus, confers significant protection against an experimental challenge infection. Vaccine 30(50):7199–7204 (PubMed PMID: 23107597)

    Google Scholar 

  120. Loukas A, Opdebeeck J, Croese J, Prociv P (1996) Immunoglobulin G subclass antibodies against excretory/secretory antigens of Ancylostoma caninum in human enteric infections. Am J Trop Med Hyg 54(6):672–676 (PubMed PMID: 8686791)

    Google Scholar 

  121. Loukas A, Croese J, Opdebeeck J, Prociv P (1992) Detection of antibodies to secretions of Ancylostoma caninum in human eosinophilic enteritis. Trans R Soc Trop Med Hyg 86(6):650–653 (PubMed PMID: 1287934)

    Google Scholar 

  122. Ghosh K, Hotez PJ (1999) Antibody-dependent reductions in mouse hookworm burden after vaccination with Ancylostoma caninum secreted protein 1. J Infect Dis 180(5):1674–1681 (PubMed PMID: 10515831)

    Google Scholar 

  123. Hotez PJ, Ashcom J, Zhan B, Bethony J, Loukas A, Hawdon J et al (2003) Effect of vaccination with a recombinant fusion protein encoding an astacinlike metalloprotease (MTP-1) secreted by host-stimulated Ancylostoma caninum third-stage infective larvae. J Parasitol 89(4):853–855 (PubMed PMID: 14533704)

    Google Scholar 

  124. Loukas A, Bethony JM, Mendez S, Fujiwara RT, Goud GN, Ranjit N et al (2005) Vaccination with recombinant aspartic hemoglobinase reduces parasite load and blood loss after hookworm infection in dogs. PLoS Med 2(10):e295 (PubMed PMID: 16231975. Pubmed Central PMCID: 1240050)

    Google Scholar 

  125. Urban JF Jr, Alizadeh H, Romanowski RD (1988) Ascaris suum: development of intestinal immunity to infective second-stage larvae in swine. Exp Parasitol 66(1):66–77 (PubMed PMID: 3366215)

    Google Scholar 

  126. Urban JF Jr, Romanowski RD (1985) Ascaris suum: protective immunity in pigs immunized with products from eggs and larvae. Exp Parasitol 60(2):245–254 (PubMed PMID: 4029352)

    Google Scholar 

  127. Knox DP, Kennedy MW (1988) Proteinases released by the parasitic larval stages of Ascaris suum, and their inhibition by antibody. Mol Biochem Parasitol 28(3):207–216 (PubMed PMID: 3290677)

    Google Scholar 

  128. Lima C, Perini A, Garcia ML, Martins MA, Teixeira MM, Macedo MS (2002) Eosinophilic inflammation and airway hyper-responsiveness are profoundly inhibited by a helminth (Ascaris suum) extract in a murine model of asthma. Clin Exp Allergy 32(11):1659–1666 (PubMed PMID: 12569989)

    Google Scholar 

  129. McConchie BW, Norris HH, Bundoc VG, Trivedi S, Boesen A, Urban JF Jr, et al (2006) Ascaris suum-derived products suppress mucosal allergic inflammation in an interleukin-10-independent manner via interference with dendritic cell function. Infect Immun 74(12):6632–6641 (PubMed PMID: 16966410. Pubmed Central PMCID: 1698059)

    Google Scholar 

  130. Pedersen S, Saeed I (2001) Acquired immunity to Trichuris suis infection in pigs. Parasitology 123(Pt 1):95–101 (PubMed PMID: 11467788)

    Google Scholar 

  131. Kringel H, Iburg T, Dawson H, Aasted B, Roepstorff A (2006) A time course study of immunological responses in Trichuris suis infected pigs demonstrates induction of a local type 2 response associated with worm burden. Int J Parasitol 36(8):915–924 (PubMed PMID: 16750534)

    Google Scholar 

  132. Kringel H, Roepstorff A (2007) Trichuris suis excretory/secretory antigen-specific antibodies in serum from single-inoculated pigs. Parasite Immunol 29(6):327–330 (PubMed PMID: 17518951)

    Google Scholar 

  133. Summers RW, Elliott DE, Qadir K, Urban JF Jr, Thompson R, Weinstock JV (2003) Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am J Gastroenterol 98(9):2034–2041 (PubMed PMID: 14499784)

    Google Scholar 

  134. Summers RW, Elliott DE, Urban JF Jr, Thompson R, Weinstock JV (2005) Trichuris suis therapy in Crohn’s disease. Gut 54(1):87–90 (PubMed PMID: 15591509. Pubmed Central PMCID: 1774382)

    Google Scholar 

  135. Bourke CD, Mutapi F, Nausch N, Photiou DM, Poulsen LK, Kristensen B et al (2012) Trichuris suis ova therapy for allergic rhinitis does not affect allergen-specific cytokine responses despite a parasite-specific cytokine response. Clin Exp Allergy 42(11):1582–1595 (PubMed PMID: 23106658)

    Google Scholar 

  136. Fridman WH (1991) Fc receptors and immunoglobulin binding factors. FASEB J 5(12):2684–2690 (PubMed PMID: 1916092)

    Google Scholar 

  137. Pleass RJ, Woof JM (2001) Fc receptors and immunity to parasites. Trends Parasitol 17(11):545–551 (PubMed PMID: 11872400)

    Google Scholar 

  138. Anderson CL, Shen L, Eicher DM, Wewers MD, Gill JK (1990) Phagocytosis mediated by three distinct Fc gamma receptor classes on human leukocytes. J Exp Med 171(4):1333–1345 (PubMed PMID: 2139103. Pubmed Central PMCID: 2187839)

    Google Scholar 

  139. Young JD, Ko SS, Cohn ZA (1984) The increase in intracellular free calcium associated with IgG gamma 2b/gamma 1 Fc receptor-ligand interactions: role in phagocytosis. Proc Natl Acad Sci U S A 81(17):5430–5434 (PubMed PMID: 6236462. Pubmed Central PMCID: 391718)

    Google Scholar 

  140. Fanger MW, Graziano RF, Shen L, Guyre PM (1989) Fc gamma R in cytotoxicity exerted by mononuclear cells. Chem Immunol 47:214–253 (PubMed PMID: 2532893)

    Google Scholar 

  141. Titus JA, Perez P, Kaubisch A, Garrido MA, Segal DM (1987) Human K/natural killer cells targeted with hetero-cross-linked antibodies specifically lyse tumor cells in vitro and prevent tumor growth in vivo. J Immunol 139(9):3153–3158 (PubMed PMID: 2959724)

    Google Scholar 

  142. Phillips NE, Parker DC (1983) Fc-dependent inhibition of mouse B cell activation by whole anti-mu antibodies. J Immunol 130(2):602–606 (PubMed PMID: 6401302)

    Google Scholar 

  143. Muta T, Kurosaki T, Misulovin Z, Sanchez M, Nussenzweig MC, Ravetch JV (1994) A 13-amino-acid motif in the cytoplasmic domain of Fc gamma RIIB modulates B-cell receptor signalling. Nature 368(6466):70–73 (PubMed PMID: 8107887)

    Google Scholar 

  144. Ravetch JV, Bolland S (2001) IgG Fc receptors. Annu Rev Immunol 19:275–290 (PubMed PMID: 11244038)

    Google Scholar 

  145. Plaut M, Pierce JH, Watson CJ, Hanley-Hyde J, Nordan RP, Paul WE (1989) Mast cell lines produce lymphokines in response to cross-linkage of Fc epsilon RI or to calcium ionophores. Nature 339(6219):64–67 (PubMed PMID: 2469965)

    Google Scholar 

  146. Jankovic D, Cheever AW, Kullberg MC, Wynn TA, Yap G, Caspar P et al (1998) CD4+ T cell-mediated granulomatous pathology in schistosomiasis is downregulated by a B cell-dependent mechanism requiring Fc receptor signaling. J Exp Med 187(4):619–629 (PubMed PMID: 9463412. Pubmed Central PMCID: 2212140)

    Google Scholar 

  147. Jankovic D, Kullberg MC, Dombrowicz D, Barbieri S, Caspar P, Wynn TA et al (1997) Fc epsilonRI-deficient mice infected with Schistosoma mansoni mount normal Th2-type responses while displaying enhanced liver pathology. J Immunol 159(4):1868–1875 (PubMed PMID: 9257851)

    Google Scholar 

  148. Griffith QK, Liang Y, Onguru DO, Mwinzi PN, Ganley-Leal LM (2011) CD23-bound IgE augments and dominates recall responses through human naive B cells. J Immunol 186(2):1060–1067 (PubMed PMID: 21160045)

    Google Scholar 

  149. Onguru D, Liang Y, Elliot J, Mwinzi P, Ganley-Leal L (2011) CD23b isoform expression in human schistosomiasis identifies a novel subset of activated B cells. Infect Immun 79(9):3770–3777 (PubMed PMID: 21708991. Pubmed Central PMCID: 3165463)

    Google Scholar 

  150. Onah DN, Uchiyama F, Nagakui Y, Ono M, Takai T, Nawa Y (2000) Mucosal defense against gastrointestinal nematodes: responses of mucosal mast cells and mouse mast cell protease 1 during primary strongyloides venezuelensis infection in FcRgamma-knockout mice. Infect Immun 68(9):4968–4971 (PubMed PMID: 10948112. Pubmed Central PMCID: 101712)

    Google Scholar 

  151. Jones RE, Finkelman FD, Hester RB, Kayes SG (1994) Toxocara canis: failure to find IgE receptors (Fc epsilon R) on eosinophils from infected mice suggests that murine eosinophils do not kill helminth larvae by an IgE-dependent mechanism. Exp Parasitol 78(1):64–75 (PubMed PMID: 8299761)

    Google Scholar 

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  1. Division of Immunology/IIDM, University of Cape Town, Lovers Walk Street, Rondebosch, Cape Town, 7701, South Africa

    William G. Horsnell

  2. Clinical and Laboratory Sciences, Division of Immunology, Health Sciences Faculty, University of Cape Town, Anzio Road, Cape Town, Western Cape, 7925, South Africa

    Erin Logan

  3. Clinical Laboratory Science, University of Cape Town, Williams Street, Observatory, Cape Town, Western Province, 7701, South Africa

    Alisha Chetty

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    William Horsnell

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Logan, E., Chetty, A., Horsnell, W. (2014). The Role of Antibody in Parasitic Helminth Infections. In: Horsnell, W. (eds) How Helminths Alter Immunity to Infection. Advances in Experimental Medicine and Biology, vol 828. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1489-0_1

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