Role of eosinophils in protective immunity against secondary nematode infections

References

• World Health Organization. Research priorities for helminth infections technical report of the TDR disease reference group on helminth infections introduction. WHO technical report series; 972. Geneva, Switzerland: WHO; 2012.
   Google Scholar
• De Neve J-W, Andriantavison RL, Croke K, et al. Health, financial, and education gains of investing in preventive chemotherapy for schistosomiasis, soil-transmitted helminthiases, and lymphatic filariasis in Madagascar: a modeling study. PLoS Negl Trop Dis. 2018;12(12):e0007002.
   Web of Science ®Google Scholar
• Mitchell GF, Hogarth-Scott RS, Edwards RD, et al. Studies on immune responses to parasite antigens in mice. III. Nippostrongylus brasiliensis infections in hypothymic nu/nu mice. Int Arch Allergy Immunol. 1976;52(1-4):95–104.
   Web of Science ®Google Scholar
• Prowse SJ, Mitchell GF, Ey PL, et al. Nematospiroides dubius: susceptibility to infection and the development of resistance in hypothymic (nude) BALB/c mice. Aust J Exp Biol Med Sci. 1978;56(5):561–570.
   Google Scholar
• Ruitenberg EJ, Elgersma A, Kruizinga W, et al. Trichinella spiralis infection in congenitally athymic (nude) mice. Parasitological, serological and haematological studies with observations on intestinal pathology. Immunology. 1977;33(4):581–587.
   Web of Science ®Google Scholar
• Kemp M, Kurtzhals JA, Kharazmi A, et al. Interferon-gamma and interleukin-4 in human Leishmania donovani infections. Immunol Cell Biol. 1993;71 (6):583–587.
   Google Scholar
• Urban JF, Madden KB, Svetica A, et al. The importance of Th2 cytokines in protective immunity to nematodes. Immunol Rev. 1992;127(1):205–220.
   Google Scholar
• Finkelman FD, Shea-Donohue T, Morris SC, et al. Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol Rev. 2004;201(1):139–155.
   Google Scholar
• Grencis RK. Immunity to helminths: resistance, regulation, and susceptibility to gastrointestinal nematodes. Annu Rev Immunol. 2015;33(1):201–225.
   Google Scholar
• Yasuda K, Nakanishi K. Host responses to intestinal nematodes. Int Immunol. 2018;30(3):93–102.
   Web of Science ®Google Scholar
• Else KJ, Finkelman FD, Maliszewski CR, et al. Cytokine-mediated regulation of chronic intestinal helminth infection. J Exp Med. 1994;179(1):347–351.
   PubMed Web of Science ®Google Scholar
• Bouchery T, Kyle R, Ronchese F, et al. The differentiation of CD4(+) T-helper cell subsets in the context of helminth parasite infection. Front Immunol. 2014;5:487.
   PubMed Web of Science ®Google Scholar
• White RR, Artavanis-Tsakonas K. How helminths use excretory secretory fractions to modulate dendritic cells. Virulence. 2012;3(7):668–677.
   PubMed Web of Science ®Google Scholar
• Laan LC, Williams AR, Stavenhagen K, et al. The whipworm (Trichuris suis) secretes prostaglandin E2 to suppress proinflammatory properties in human dendritic cells. Faseb J. 2017;31(2):719–731.
   PubMed Web of Science ®Google Scholar
• Hammad H, Lambrecht BN. Barrier epithelial cells and the control of Type 2 immunity. Immunity. 2015;43(1):29–40.
   PubMed Web of Science ®Google Scholar
• Neill DR, Wong SH, Bellosi A, et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature. 2010;464(7293):1367–1370.
   PubMed Web of Science ®Google Scholar
• Roediger B, Weninger W. Group 2 innate lymphoid cells in the regulation of immune responses. Adv Immunol. 2015;125:111–154.
   PubMed Web of Science ®Google Scholar
• Moro K, Kabata H, Tanabe M, et al. Interferon and IL-27 antagonize the function of group 2 innate lymphoid cells and type 2 innate immune responses. Nat Immunol. 2016;17(1):76–86.
   PubMed Web of Science ®Google Scholar
• Paul WE. History of interleukin-4. Cytokine. 2015;75(1):3–7.
   PubMed Web of Science ®Google Scholar
• Bao K, Reinhardt RL. The differential expression of IL-4 and IL-13 and its impact on type-2 immunity. Cytokine. 2015;75(1):25–37.
   PubMed Web of Science ®Google Scholar
• LaPorte SL, Juo ZS, Vaclavikova J, et al. Molecular and structural basis of cytokine receptor pleiotropy in the interleukin-4/13 system. Cell. 2008;132(2):259–272.
   PubMed Web of Science ®Google Scholar
• Grünig G, Warnock M, Wakil AE, et al. Requirement for IL-13 independently of IL-4 in experimental asthma. Science. 1998;282(5397):2261–2263.
   PubMed Web of Science ®Google Scholar
• Cliffe LJ, et al. Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science. 2005;308(5727):1463–1465.
   PubMed Web of Science ®Google Scholar
• Artis D, Wang ML, Keilbaugh SA, et al. RELMbeta/FIZZ2 is a goblet cell-specific immune-effector molecule in the gastrointestinal tract. Proc Natl Acad Sci USA. 2004;101(37):13596–13600.
   Web of Science ®Google Scholar
• Stockinger S, Albers T, Duerr CU, et al. Interleukin-13-mediated paneth cell degranulation and antimicrobial peptide release. J Innate Immun. 2014;6(4):530–541.
   Web of Science ®Google Scholar
• Gerbe F, Sidot E, Smyth DJ, et al. Intestinal epithelial tuft cells initiate type 2 mucosal immunity to helminth parasites. Nature. 2016;529(7585):226–230.
   PubMed Web of Science ®Google Scholar
• Howitt MR, Lavoie S, Michaud M, et al. Tuft cells, taste-chemosensory cells, orchestrate parasite type 2 immunity in the gut. Science. 2016;351(6279):1329–1333.
   PubMed Web of Science ®Google Scholar
• von Moltke J, Ji M, Liang HE, et al. Tuft-cell-derived IL-25 regulates an intestinal ILC2-epithelial response circuit. Nature. 2016;529(7585):221–225.
   PubMed Web of Science ®Google Scholar
• Akiho H, Blennerhassett P, Deng Y, et al. Role of IL-4, IL-13, and STAT6 in inflammation-induced hypercontractility of murine smooth muscle cells. Am J Physiol Gastrointest Liver Physiol. 2002;282(2):G226–232.
   Web of Science ®Google Scholar
• Li L, Xia Y, Nguyen A, et al. Effects of Th2 cytokines on chemokine expression in the lung: IL-13 potently induces eotaxin expression by airway epithelial cells. J Immunol. 1999;162(5):2477–2487.
   Web of Science ®Google Scholar
• Zhu Z, Ma B, Zheng T, et al. IL-13-induced chemokine responses in the lung: role of CCR2 in the pathogenesis of IL-13-induced inflammation and remodeling. J Immunol. 2002;168(6):2953–2962.
   Web of Science ®Google Scholar
• Van Dyken SJ, Locksley RM. Interleukin-4- and interleukin-13-mediated alternatively activated macrophages: roles in homeostasis and disease. Annu Rev Immunol. 2013;31(1):317–343.
   PubMed Web of Science ®Google Scholar
• Coffman RL, Savelkoul HF, Lebman DA. Cytokine regulation of immunoglobulin isotype switching and expression. Semin Immunol. 1989;1(1):55–63.
   Google Scholar
• Goswami R, Kaplan MH. A brief history of IL-9. J Immunol. 2011;186(6):3283–3288.
   PubMed Web of Science ®Google Scholar
• Dougan M, Dranoff G, Dougan SK. GM-CSF, IL-3, and IL-5 family of cytokines: regulators of inflammation. Immunity. 2019;50(4):796–811.
   PubMed Web of Science ®Google Scholar
• Fulkerson PC, Fischetti CA, McBride ML, et al. A central regulatory role for eosinophils and the eotaxin/CCR3 axis in chronic experimental allergic airway inflammation. Proc Natl Acad Sci USA. 2006;103(44):16418–16423.
   PubMed Web of Science ®Google Scholar
• Schmitz J, Owyang A, Oldham E, et al. 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. 2005;23(5):479–490.
   PubMed Web of Science ®Google Scholar
• Yasuda K, Muto T, Kawagoe T, et al. Contribution of IL-33-activated type II innate lymphoid cells to pulmonary eosinophilia in intestinal nematode-infected mice. Proc Natl Acad Sci USA. 2012;109(9):3451–3456.
   PubMed Web of Science ®Google Scholar
• Cayrol C, Girard JP. IL-33: an alarmin cytokine with crucial roles in innate immunity, inflammation and allergy. Curr Opin Immunol. 2014;31:31–37.
   PubMed Web of Science ®Google Scholar
• Dahlgren MW, Jones SW, Cautivo KM, et al. Adventitial stromal cells define group 2 innate lymphoid cell tissue niches. Immunity. 2019;50(3):707–722.e706.
   Web of Science ®Google Scholar
• Matsuba-Kitamura S, Yoshimoto T, Yasuda K, et al. Contribution of IL-33 to induction and augmentation of experimental allergic conjunctivitis. Int Immunol. 2010;22(6):479–489.
   Web of Science ®Google Scholar
• Huang L, Appleton JA. Eosinophils in helminth infection: defenders and dupes. Trends Parasitol. 2016;32(10):798–807.
   PubMed Web of Science ®Google Scholar
• Weller PF, Spencer LA. Functions of tissue-resident eosinophils. Nat Rev Immunol. 2017;17(12):746–760.
   PubMed Web of Science ®Google Scholar
• Travers J, Rothenberg ME. Eosinophils in mucosal immune responses. Mucosal Immunol. 2015;8(3):464–475.
   PubMed Web of Science ®Google Scholar
• Giacomin PR, Gordon DL, Botto M, et al. The role of complement in innate, adaptive and eosinophil-dependent immunity to the nematode Nippostrongylus brasiliensis. Mol Immunol. 2008;45(2):446–455.
   Web of Science ®Google Scholar
• Ramalho-Pinto FJ, McLaren DJ, Smithers SR. Complement-mediated killing of schistosomula of Schistosoma mansoni by rat eosinophils in vitro. J Exp Med. 1978;147(1):147–156.
   Web of Science ®Google Scholar
• Gounni AS, Lamkhioued B, Ochiai K, et al. High-affinity IgE receptor on eosinophils is involved in defence against parasites. Nature. 1994;367(6459):183–186.
   Web of Science ®Google Scholar
• Khalife J, Dunne DW, Richardson BA, et al. Functional role of human IgG subclasses in eosinophil-mediated killing of schistosomula of Schistosoma mansoni. J Immunol. 1989;142(12):4422–4427.
   Web of Science ®Google Scholar
• Shamri R, Xenakis JJ, Spencer LA. Eosinophils in innate immunity: an evolving story. Cell Tissue Res. 2011;343(1):57–83.
   PubMed Web of Science ®Google Scholar
• Löffler W. Flüchtige Lungeninfiltrate mit Eosinophilie. Klin Wochenschr. 1935;14(9):297–299.
   Google Scholar
• Tindall NR, Wilson PA. An extended proof of migration routes of immature parasites inside hosts: pathways of Nippostrongylus brasiliensis and Strongyloides ratti in the rat are mutually exclusive. Parasitology. 1990;100(2):281–288.
   Google Scholar
• Takamure A. Migration route of Strongyloides venezuelensis in rodents. Int J Parasitol. 1995;25(8):907–911.
   Web of Science ®Google Scholar
• Cardoso V, Chesné J, Ribeiro H, et al. Neuronal regulation of type 2 innate lymphoid cells via neuromedin U. Nature. 2017;549(7671):277–281.
   Web of Science ®Google Scholar
• Kopf M, Brombacher F, Hodgkin PD, et al. IL-5-deficient mice have a developmental defect in CD5+ B-1 cells and lack eosinophilia but have normal antibody and cytotoxic T cell responses. Immunity. 1996;4(1):15–24.
   Web of Science ®Google Scholar
• Klion AD, Nutman TB. The role of eosinophils in host defense against helminth parasites. J Allergy Clin Immunol. 2004;113(1):30–37.
   PubMed Web of Science ®Google Scholar
• Coffman RL, Seymour BW, Hudak S, et al. Antibody to interleukin-5 inhibits helminth-induced eosinophilia in mice. Science. 1989;245(4915):308–310.
   Web of Science ®Google Scholar
• Swartz JM, Dyer KD, Cheever AW, et al. Schistosoma mansoni infection in eosinophil lineage-ablated mice. Blood. 2006;108(7):2420–2427.
   PubMed Web of Science ®Google Scholar
• Capron M, Bazin H, Joseph M, et al. Evidence for IgE-dependent cytotoxicity by rat eosinophils. J Immunol. 1981;126(5):1764–1768.
   Web of Science ®Google Scholar
• de Andres B, Rakasz E, Hagen M, et al. Lack of Fc-epsilon receptors on murine eosinophils: implications for the functional significance of elevated IgE and eosinophils in parasitic infections. Blood. 1997;89(10):3826–3836.
   Web of Science ®Google Scholar
• Pearce EJ, Caspar P, Grzych JM, et al. Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J Exp Med. 1991;173(1):159–166.
   PubMed Web of Science ®Google Scholar
• Svensson M, Bell L, Little MC, et al. Accumulation of eosinophils in intestine-draining mesenteric lymph nodes occurs after Trichuris muris infection. Parasite Immunol. 2011;33(1):1–11.
   Web of Science ®Google Scholar
• Hurst RJ, Else KJ. Trichuris muris research revisited: a journey through time. Parasitology. 2013;140(11):1325–1339.
   Web of Science ®Google Scholar
• Fabre V, Beiting DP, Bliss SK, et al. Eosinophil deficiency compromises parasite survival in chronic nematode infection. J Immunol. 2009;182(3):1577–1583.
   Web of Science ®Google Scholar
• Huang L, Gebreselassie NG, Gagliardo LF, et al. Eosinophil-derived IL-10 supports chronic nematode infection. Ji . 2014;193(8):4178–4187.
   Google Scholar
• Gebreselassie NG, Moorhead AR, Fabre V, et al. Eosinophils preserve parasitic nematode larvae by regulating local immunity. J Immunol. 2012;188(1):417–425.
   PubMed Web of Science ®Google Scholar
• Herndon FJ, Kayes SG. Depletion of eosinophils by anti-IL-5 monoclonal antibody treatment of mice infected with Trichinella spiralis does not alter parasite burden or immunologic resistance to reinfection. J Immunol. 1992;149(11):3642–3647.
   Web of Science ®Google Scholar
• Vallance BA, Matthaei KI, Sanovic S, et al. Interleukin-5 deficient mice exhibit impaired host defence against challenge Trichinella spiralis infections. Parasite Immunol. 2000;22(10):487–492.
   Web of Science ®Google Scholar
• Martin C, Al-Qaoud KM, Ungeheuer M-N, et al. IL-5 is essential for vaccine-induced protection and for resolution of primary infection in murine filariasis. Med Microbiol Immunol. 2000;189(2):67–74.
   Web of Science ®Google Scholar
• Le Goff L, Loke P, Ali HF, et al. J. E. Interleukin-5 is essential for vaccine-mediated immunity but not innate resistance to a filarial parasite. Infect Immun. 2000;68(5):2513–2517.
   Web of Science ®Google Scholar
• Mesnil C, Raulier S, Paulissen G, et al. Lung-resident eosinophils represent a distinct regulatory eosinophil subset. J Clin Invest. 2016;126(9):3279–3295.
   PubMed Web of Science ®Google Scholar
• Obata-Ninomiya K, Ishiwata K, Tsutsui H, et al. The skin is an important bulwark of acquired immunity against intestinal helminths. J Exp Med. 2013;210(12):2583–2595.
   Web of Science ®Google Scholar
• Knott ML, Matthaei KI, Giacomin PR, et al. Impaired resistance in early secondary Nippostrongylus brasiliensis infections in mice with defective eosinophilopoeisis. Int J Parasitol. 2007;37(12):1367–1378.
   Web of Science ®Google Scholar
• Huang L, Gebreselassie NG, Gagliardo LF, et al. Eosinophils mediate protective immunity against secondary nematode infection. J Immunol. 2015;194(1):283–290.
   Web of Science ®Google Scholar
• Bass DA, Szejda P. Eosinophils versus neutrophils in host defense. Killing of newborn larvae of Trichinella spiralis by human granulocytes in vitro. J Clin Invest. 1979;64(5):1415–1422.
   Web of Science ®Google Scholar
• Schwartz C, Turqueti-Neves A, Hartmann S, et al. Basophil-mediated protection against gastrointestinal helminths requires IgE-induced cytokine secretion. Proc Natl Acad Sci USA. 2014;111(48):E5169–5177.
   Web of Science ®Google Scholar
• Mukai K, Karasuyama H, Kabashima K, et al. Differences in the importance of mast cells, basophils, IgE, and IgG versus that of CD4+ T cells and ILC2 cells in primary and secondary immunity to Strongyloides venezuelensis. Infect Immun. 2017;85(5):pii: e00053-17.
   Web of Science ®Google Scholar
• Yasuda K, Adachi T, Koida A, et al. Nematode-infected mice acquire resistance to subsequent infection with unrelated nematode by inducing highly responsive group 2 innate lymphoid cells in the lung. Front Immunol. 2018;9:2132.
   Web of Science ®Google Scholar
• Martinez-Gonzalez I, Mathä L, Steer CA, et al. Allergen-experienced group 2 innate lymphoid cells acquire memory-like properties and enhance allergic lung inflammation. Immunity. 2016;45(1):198–208.
   PubMed Web of Science ®Google Scholar
• Guo L, Huang Y, Chen X, et al. Innate immunological function of TH2 cells in vivo. Nat Immunol. 2015;16(10):1051–1059.
   Web of Science ®Google Scholar
• Gazzinelli-Guimaraes PH, et al. Allergen presensitization drives an eosinophil-dependent arrest in lung-specific helminth development. J Clin Invest. 2019;130:3686–3701.
   Google Scholar
• Filbey KJ, Camberis M, Chandler J, et al. Intestinal helminth infection promotes IL-5- and CD4. Mucosal Immunol. 2019;12(2):352–362.
   Web of Science ®Google Scholar
• Gazzinelli-Guimaraes PH, Nutman TB. Helminth parasites and immune regulation. F1000Res. 2018;7:1685.
   Google Scholar
• Smallwood TB, Giacomin PR, Loukas A, et al. Helminth immunomodulation in autoimmune disease. Front Immunol. 2017;8:453.
   PubMed Web of Science ®Google Scholar
• Varyani F, Fleming JO, Maizels RM. Helminths in the gastrointestinal tract as modulators of immunity and pathology. Am J Physiol Gastrointest Liver Physiol. 2017;312(6):G537–G549.
   PubMed Web of Science ®Google Scholar