{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,6]],"date-time":"2026-09-06T23:50:50Z","timestamp":1788738650370,"version":"build-2803163510"},"reference-count":128,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2023,1,23]],"date-time":"2023-01-23T00:00:00Z","timestamp":1674432000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Nematode infection is a major threat to the health of humans, domestic animals and wildlife. Nematodes vary in their effect on the host and in the mechanisms underlying immunity but the general features are becoming clear. There is considerable variation among individuals in resistance to infection and much of this variation is due to genetic variation in the immune response. The major histocompatibility complex has a strong influence on resistance to infection but other genes are collectively more important. Resistant individuals produce more IgA, eosinophils, IgE and mast cells than susceptible individuals and this is a consequence of stronger type 2 (Th2) immune responses. A variety of factors promote Th2 responses including genetic background, diet, molecules produced by the parasite and the location of the infection. A variety of cells and molecules including proteins, glycolipids and RNA act in concert to promote responses and to regulate the response. Nematodes themselves also modulate the host response and over 20 parasite-derived immunomodulatory molecules have been identified. Different species of nematodes modulate the immune response in different ways and probably use multiple molecules. The reasons for this are unclear and the interactions among immunomodulators have still to be investigated.<\/jats:p>","DOI":"10.3390\/ijms24032283","type":"journal-article","created":{"date-parts":[[2023,1,24]],"date-time":"2023-01-24T01:29:45Z","timestamp":1674523785000},"page":"2283","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":27,"title":["The Immune Response to Nematode Infection"],"prefix":"10.3390","volume":"24","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5054-1348","authenticated-orcid":false,"given":"Michael","family":"Stear","sequence":"first","affiliation":[{"name":"Department of Animal, Plant and Soil Sciences, AgriBio, La Trobe University, Bundoora, VIC 3086, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah","family":"Preston","sequence":"additional","affiliation":[{"name":"School of Science, Psychology and Sport, Federation University Australia, Mt Helen, VIC 3350, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"Piedrafita","sequence":"additional","affiliation":[{"name":"School of Science, Psychology and Sport, Federation University Australia, Mt Helen, VIC 3350, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katarzyna","family":"Donskow-\u0141ysoniewska","sequence":"additional","affiliation":[{"name":"Department of Experimental Immunotherapy, Faculty of Medicine, Lazarski University, ul. \u015awieradowska 43, 02-662 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,1,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1016\/j.immuni.2018.10.016","article-title":"Modulation of Host Immunity by Helminths: The Expanding Repertoire of Parasite Effector Molecules","volume":"49","author":"Maizels","year":"2018","journal-title":"Immunity"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"484","DOI":"10.3390\/agriculture3030484","article-title":"Global Change and Helminth Infections in Grazing Ruminants in Europe: Impacts, Trends and Sustainable Solutions","volume":"3","author":"Morgan","year":"2013","journal-title":"Agriculture"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1079\/ASC41010023","article-title":"Costs of the major endemic diseases of sheep in Great Britain and the potential benefits of reduction in disease impact","volume":"81","author":"Nieuwhof","year":"2005","journal-title":"Anim. Sci."},{"key":"ref_4","unstructured":"Lane, J., Jubb, T., Shephard, R., Webb-Ware, J., and Fordyce, G. (2015). Priority List of Endemic Diseases for the Red Meat Industries, Meat & Livestock Australia Limited."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1038\/nature03276","article-title":"Parasites and climate synchronize red grouse populations","volume":"433","author":"Cattadori","year":"2006","journal-title":"Nature"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1017\/S0021859600041782","article-title":"The effect of three levels of Ostertagia circumcincta larvae on growth rate, food intake and body composition of growing lambs","volume":"98","author":"Coop","year":"1982","journal-title":"J. Agric. Sci. (Camb.)"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1079\/AHRR200351","article-title":"A Key Mechanism of Pathogenesis in Sheep Infected with the Nematode Teladorsagia circumcincta","volume":"4","author":"Stear","year":"2003","journal-title":"Anim. Health Res. Rev."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1017\/S0031182006000618","article-title":"Gastrointestinal nematode species burdens and host mortality in a feral sheep population","volume":"133","author":"Craig","year":"2006","journal-title":"Parasitology"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1016\/j.ijpara.2016.07.001","article-title":"Haemonchus contortus: The then and now, and where to from here?","volume":"46","author":"Emery","year":"2016","journal-title":"Int. J. Parasitol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1017\/S0031182006001557","article-title":"Alternatives to anthelmintics for the control of nematodes in livestock","volume":"134","author":"Stear","year":"2007","journal-title":"Parasitology"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1046\/j.1365-3024.1997.d01-202.x","article-title":"Heterogeneity in the recognition of Ostertagia circumcincta antigens by serum antibody from mature, infected sheep","volume":"19","author":"McCririe","year":"1997","journal-title":"Parasite Immunol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1017\/S0022149X11000058","article-title":"An evolutionary perspective on gastrointestinal nematodes of sheep","volume":"85","author":"Stear","year":"2011","journal-title":"J. Helminthol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1016\/j.ijpara.2013.03.003","article-title":"Genetic and phenotypic relationships between carbohydrate larval antigen (CarLA) IgA, parasite resistance and productivity in serial samples taken from lambs after weaning","volume":"43","author":"Shaw","year":"2013","journal-title":"Int. J. Parasitol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/j.vetpar.2011.11.051","article-title":"Salivary IgA: A suitable measure of immunity to gastrointestinal nematodes in sheep","volume":"186","author":"Shaw","year":"2012","journal-title":"Vet. Parasitol."},{"key":"ref_15","unstructured":"Sompayrac, L. (2016). How the Immune System Works, Blackwell."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1038\/mi.2017.113","article-title":"Immunity to gastrointestinal nematode infections","volume":"11","author":"Sorobetea","year":"2018","journal-title":"Mucosal Immunol."},{"key":"ref_17","unstructured":"Day, M.J., and Schultz, R.D. (2019). Veterinary Immunology: Principles and Practice, CRC Press."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"995","DOI":"10.1016\/0092-8674(91)90323-Q","article-title":"Somatic generation of diversity in a mammalian primary lymphoid organ: The sheep ileal Peyer\u2019s patches","volume":"64","author":"Reynaud","year":"1991","journal-title":"Cell"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1186\/1297-9716-42-46","article-title":"The dynamic influence of the DRB1*1101 allele on the resistance of sheep to experimental Teladorsagia circumcincta infection","volume":"42","author":"Hassan","year":"2011","journal-title":"Vet. Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1111\/pim.12347","article-title":"Immunogenomics of gastrointestinal nematode infection in ruminants\u2013breeding for resistance to produce food sustainably and safely","volume":"38","author":"Sweeney","year":"2016","journal-title":"Parasite Immunol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1017\/S0031182005007778","article-title":"Major histocompatibility complex DRB1 gene: Its role in nematode resistance in Suffolk and Texel sheep breeds","volume":"131","author":"Sayers","year":"2005","journal-title":"Parasitology"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1016\/0020-7519(94)00216-B","article-title":"An ovine Major histocompatibility complex DRB1 allele is associated with low faecal egg counts following natural, predominantly Ostertagia circumcincta infection","volume":"25","author":"Schwaiger","year":"1995","journal-title":"Int. J. Parasitol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1016\/j.ijpara.2019.05.003","article-title":"Identification of the amino acids in the Major Histocompatibility Complex class II region of Scottish Blackface sheep that are associated with resistance to nematode infection","volume":"49","author":"Stear","year":"2019","journal-title":"Int. J. Parasitol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"e12626","DOI":"10.1111\/pim.12626","article-title":"Association of MHC class II haplotypes with reduced faecal nematode egg count and IgA activity in British Texel sheep","volume":"41","author":"Ali","year":"2019","journal-title":"Parasite Immunol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1534\/genetics.119.302022","article-title":"Divergent Allele Advantage Provides a Quantitative Model for Maintaining Alleles with a Wide Range of Intrinsic Merits","volume":"212","author":"Stefan","year":"2019","journal-title":"Genetics"},{"key":"ref_26","first-page":"11","article-title":"Association between MHC class II alleles and resistance to the parasitic nematode Ostertagia circumcincta","volume":"42","author":"Buitkamp","year":"1999","journal-title":"Arch. F\u00fcr Tierz."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1017\/S0031182000080173","article-title":"The effects of H-2 and non H-2 genes on the expulsion of the nematode Trichuris muris from inbred and congenic mice","volume":"96","author":"Else","year":"1988","journal-title":"Parasitology"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/0304-4017(90)90077-O","article-title":"The relationships among ecto- and endoparasite levels, class I antigens of the bovine major histocompatibility system, immunoglobulin E levels and weight gain","volume":"34","author":"Stear","year":"1990","journal-title":"Vet. Parasitol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1016\/j.immuni.2013.08.029","article-title":"CD301b(+) dermal dendritic cells drive T helper 2 cell-mediated immunity","volume":"39","author":"Kumamoto","year":"2013","journal-title":"Immunity"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1038\/nri.2017.118","article-title":"TH2 cell development and function","volume":"18","author":"Walker","year":"2018","journal-title":"Nat. Rev. Immunol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2990","DOI":"10.1038\/ncomms3990","article-title":"Transcription factor IRF4 drives dendritic cells to promote Th2 differentiation","volume":"4","author":"Williams","year":"2013","journal-title":"Nat. Commun."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"722","DOI":"10.1016\/j.immuni.2013.08.028","article-title":"Control of T helper 2 responses by transcription factor IRF4-dependent dendritic cells","volume":"39","author":"Gao","year":"2013","journal-title":"Immunity"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1016\/j.immuni.2015.04.017","article-title":"Klf4 expression in conventional dendritic cells is required for T helper 2 cell responses","volume":"42","author":"Tussiwand","year":"2015","journal-title":"Immunity"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/bs.ai.2020.10.003","article-title":"IgE and mast cells: The endogenous adjuvant","volume":"148","author":"Kanagaratham","year":"2020","journal-title":"Adv. Immunol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"664","DOI":"10.3389\/fimmu.2018.00664","article-title":"Helminth Infections: Recognition and Modulation of the Immune Response by Innate Immune Cells","volume":"9","author":"Motran","year":"2018","journal-title":"Front. Immunol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1146\/annurev-immunol-042718-041717","article-title":"Regulatory T Cells and Human Disease","volume":"38","author":"Sakaguchi","year":"2020","journal-title":"Annu. Rev. Immunol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1007\/s00281-012-0347-3","article-title":"Immunity to the model intestinal helminth parasite Heligmosomoides polygyrus","volume":"34","author":"Reynolds","year":"2012","journal-title":"Semin. Immunopathol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/0304-4017(94)90089-2","article-title":"Genetic resistance to parasitic disease: Particularly of resistance in ruminants to gastrointestinal nematodes","volume":"54","author":"Stear","year":"1994","journal-title":"Vet. Parasitol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1053\/rvsc.2001.0496","article-title":"The sustainability, feasibility and desirability of breeding livestock for disease resistance","volume":"71","author":"Stear","year":"2001","journal-title":"Res. Vet. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1038\/37895","article-title":"How hosts control worms","volume":"389","author":"Stear","year":"1997","journal-title":"Nature"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1017\/S0031182002001580","article-title":"Eosinophilia as a marker of resistance to Teladorsagia circumcincta in Scottish Blackface lambs","volume":"124","author":"Stear","year":"2002","journal-title":"Parasitology"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1017\/S0031182002001531","article-title":"The genetic control of IgA activity against Teladorsagia circumcincta and its association with parasite resistance in naturally infected sheep","volume":"124","author":"Strain","year":"2002","journal-title":"Parasitology"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1084\/jem.20100793","article-title":"Dectin-2 mediates Th2 immunity through the generation of cysteinyl leukotrienes","volume":"208","author":"Barrett","year":"2011","journal-title":"J. Exp. Med."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1753","DOI":"10.1084\/jem.20111381","article-title":"Schistosome-derived omega-1 drives Th2 polarization by suppressing protein synthesis following internalization by the mannose receptor","volume":"209","author":"Everts","year":"2012","journal-title":"J. Exp. Med."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1038\/nm.3444","article-title":"Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis","volume":"20","author":"Trompette","year":"2014","journal-title":"Nat. Med."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1017\/S0031182097001947","article-title":"The influence of dietary supplementation with urea on resilience and resistance to infection with Haemonchus contortus","volume":"116","author":"Wallace","year":"1998","journal-title":"Parasitology"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1017\/S1357729800051031","article-title":"The influence of increased feeding on the susceptibility of sheep to infection with Haemonchus contortus","volume":"69","author":"Wallace","year":"1999","journal-title":"Anim. Sci."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1016\/0034-5288(95)90108-6","article-title":"Influence of supplementation with dietary soyabean meal on resistance to haemonchosis in Hampshire down lambs","volume":"58","author":"Wallace","year":"1995","journal-title":"Res. Vet. Sci."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1016\/S0034-5288(96)90008-9","article-title":"Influence of soyabean meal supplementation on the resistance of Scottish Blackface lambs to haemonchosis","volume":"60","author":"Wallace","year":"1996","journal-title":"Res. Vet. Sci."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1038\/mi.2009.134","article-title":"The influence of TSLP on the allergic response","volume":"3","author":"Comeau","year":"2010","journal-title":"Mucosal Immunol."},{"key":"ref_51","first-page":"24","article-title":"Role of thymic stromal lymphopoietin in allergy and beyond","volume":"23","author":"Leonard","year":"2022","journal-title":"Nat. Rev. Immunol."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Zaiss, M.M., Maslowski, K.M., Mosconi, I., Guenat, N., Marsland, B.J., and Harris, N.L. (2013). IL-1beta suppresses innate IL-25 and IL-33 production and maintains helminth chronicity. PLoS Pathog., 9.","DOI":"10.1371\/journal.ppat.1003531"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"E3081","DOI":"10.1073\/pnas.1406322111","article-title":"Transcriptomics identified a critical role for Th2 cell-intrinsic miR-155 in mediating allergy and antihelminth immunity","volume":"111","author":"Okoye","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"753","DOI":"10.1038\/nri2400","article-title":"The alliance of sphingosine-1-phosphate and its receptors in immunity","volume":"8","author":"Rivera","year":"2008","journal-title":"Nat. Rev. Immunol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"821","DOI":"10.1016\/j.immuni.2016.01.003","article-title":"MicroRNAs 24 and 27 Suppress Allergic Inflammation and Target a Network of Regulators of T Helper 2 Cell-Associated Cytokine Production","volume":"44","author":"Pua","year":"2016","journal-title":"Immunity"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1084\/jem.20150990","article-title":"miR-23\u223c27\u223c24 clusters control effector T cell differentiation and function","volume":"213","author":"Cho","year":"2016","journal-title":"J. Exp. Med."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1111\/imm.12601","article-title":"Immune polarization by hookworms: Taking cues from T helper type 2, type 2 innate lymphoid cells and alternatively activated macrophages","volume":"148","author":"Nair","year":"2016","journal-title":"Immunology"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1016\/0021-9975(84)90063-X","article-title":"Manifestations of resistance to ovine ostertagiasis associated with immunological responses in the gastric lymph","volume":"94","author":"Smith","year":"1984","journal-title":"J. Comp. Pathol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1016\/0169-4758(96)10069-7","article-title":"The key components of resistance to Ostertagia circumcincta in lambs","volume":"12","author":"Stear","year":"1996","journal-title":"Parasitol. Today"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1111\/j.1365-3024.1995.tb01010.x","article-title":"Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta","volume":"17","author":"Stear","year":"1995","journal-title":"Parasite Immunol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1046\/j.1365-3024.2001.00375.x","article-title":"Cross-protection studies with gut membrane glycoprotein antigens from Haemonchus contortus and Teladorsagia circumcincta","volume":"23","author":"Smith","year":"2001","journal-title":"Parasite Immunol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1084\/jem.20102057","article-title":"Muc5ac: A critical component mediating the rejection of enteric nematodes","volume":"208","author":"Hasnain","year":"2011","journal-title":"J. Exp. Med."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"348","DOI":"10.1186\/s13071-022-05483-5","article-title":"Whipworm secretions and their roles in host-parasite interactions","volume":"15","author":"Shears","year":"2022","journal-title":"Parasit Vectors"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1016\/S0020-7519(98)00040-X","article-title":"Attempts to generate immunity against Trichostrongylus colubriformis and Haemonchus contortus in young lambs by vaccination with viable parasites","volume":"28","author":"McClure","year":"1998","journal-title":"Int. J. Parasitol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/S0020-7519(98)00179-9","article-title":"Mechanisms underlying resistance to nematode infection","volume":"29","author":"Stear","year":"1999","journal-title":"Int. J. Parasitol."},{"key":"ref_66","first-page":"E9849","article-title":"CXCR6(+)ST2(+) memory T helper 2 cells induced the expression of major basic protein in eosinophils to reduce the fecundity of helminth","volume":"115","author":"Ishiwata","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1111\/imm.13190","article-title":"Regulatory T-cells in helminth infection: Induction, function and therapeutic potential","volume":"160","author":"White","year":"2020","journal-title":"Immunology"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"3100","DOI":"10.3389\/fimmu.2019.03100","article-title":"Treg Heterogeneity, Function, and Homeostasis","volume":"10","author":"Shevyrev","year":"2019","journal-title":"Front. Immunol."},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Machcinska, M., Kierasinska, M., Michniowska, M., Maruszewska-Cheruiyot, M., Szewczak, L., Rola, R., Karlinska, A., Stear, M., and Donskow-Lysoniewska, K. (2022). Reduced Expression of PD-1 in Circulating CD4+ and CD8+ Tregs Is an Early Feature of RRMS. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23063185"},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Timperi, E., and Barnaba, V. (2021). CD39 Regulation and Functions in T Cells. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22158068"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1016\/j.diagmicrobio.2008.06.015","article-title":"Ascaris lumbricoides-induced suppression of total and specific IgE responses in atopic subjects is interleukin 10-independent and associated with an increase of CD25(+) cells","volume":"62","author":"Matera","year":"2008","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Ricci, N.D., Fiuza, J.A., Bueno, L.L., Cancado, G.G., Gazzinelli-Guimaraes, P.H., Martins, V.G., Matoso, L.F., de Miranda, R.R., Geiger, S.M., and Correa-Oliveira, R. (2011). Induction of CD4(+)CD25(+)FOXP3(+) regulatory T cells during human hookworm infection modulates antigen-mediated lymphocyte proliferation. PLoS Negl. Trop. Dis., 5.","DOI":"10.1371\/journal.pntd.0001383"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"5375","DOI":"10.4049\/jimmunol.0904067","article-title":"At homeostasis filarial infections have expanded adaptive T regulatory but not classical Th2 cells","volume":"184","author":"Metenou","year":"2010","journal-title":"J. Immunol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1002\/eji.200838727","article-title":"Early recruitment of natural CD4+ Foxp3+ Treg cells by infective larvae determines the outcome of filarial infection","volume":"39","author":"Taylor","year":"2009","journal-title":"Eur. J. Immunol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1874","DOI":"10.1002\/eji.200636751","article-title":"Expansion and activation of CD4(+)CD25(+) regulatory T cells in Heligmosomoides polygyrus infection","volume":"37","author":"Finney","year":"2007","journal-title":"Eur. J. Immunol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1017\/S0031182021000883","article-title":"Trichuris muris and comorbidities\u2014Within a mouse model context","volume":"148","author":"Hayes","year":"2021","journal-title":"Parasitology"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"2904","DOI":"10.4049\/jimmunol.1202502","article-title":"Regulatory T cells limit induction of protective immunity and promote immune pathology following intestinal helminth infection","volume":"192","author":"Sawant","year":"2014","journal-title":"J. Immunol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1051\/parasite\/2014051","article-title":"Immune modulation by helminth parasites of ruminants: Implications for vaccine development and host immune competence","volume":"21","author":"McNeilly","year":"2014","journal-title":"Parasite"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"648","DOI":"10.1017\/S003118202100007X","article-title":"The interaction of host and nematode galectins influences the outcome of gastrointestinal nematode infections","volume":"148","author":"Stear","year":"2021","journal-title":"Parasitology"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1111\/imm.12049","article-title":"Modulation of dendritic cell function and immune response by cysteine protease inhibitor from murine nematode parasite Heligmosomoides polygyrus","volume":"138","author":"Sun","year":"2013","journal-title":"Immunology"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"109807","DOI":"10.1016\/j.vetpar.2022.109807","article-title":"Nematode galectin binds IgE and modulates mast cell activity","volume":"311","author":"Gonzalez","year":"2022","journal-title":"Vet. Parasitol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1741","DOI":"10.1038\/s41467-017-01886-6","article-title":"A structurally distinct TGF-beta mimic from an intestinal helminth parasite potently induces regulatory T cells","volume":"8","author":"Johnston","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"666","DOI":"10.1016\/j.jaci.2016.07.007","article-title":"Regulation of the host immune system by helminth parasites","volume":"138","author":"Maizels","year":"2016","journal-title":"J. Allergy Clin. Immunol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1038\/32160","article-title":"A molecular evolutionary framework for the phylum Nematoda","volume":"392","author":"Blaxter","year":"1998","journal-title":"Nature"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1042\/bj3570373","article-title":"Macrophage migration inhibitory factor of the parasitic nematode Trichinella spiralis","volume":"357","author":"Tan","year":"2001","journal-title":"Biochem. J."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1096\/fj.201600841R","article-title":"The whipworm (Trichuris suis) secretes prostaglandin E2 to suppress proinflammatory properties in human dendritic cells","volume":"31","author":"Laan","year":"2017","journal-title":"FASEB J."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"15921","DOI":"10.1038\/s41598-018-34174-4","article-title":"Analysis of the Trichuris suis excretory\/secretory proteins as a function of life cycle stage and their immunomodulatory properties","volume":"8","author":"Leroux","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"6234836","DOI":"10.1155\/2021\/6234836","article-title":"A Helminth-Derived Chitinase Structurally Similar to Mammalian Chitinase Displays Immunomodulatory Properties in Inflammatory Lung Disease","volume":"2021","author":"Ebner","year":"2021","journal-title":"J. Immunol. Res."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"e12131","DOI":"10.1002\/jev2.12131","article-title":"Parasite worm antigens instruct macrophages to release immunoregulatory extracellular vesicles","volume":"10","author":"Zakeri","year":"2021","journal-title":"J. Extracell Vesicles"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"155919","DOI":"10.1016\/j.cyto.2022.155919","article-title":"Antigens from the parasitic nematode Trichuris suis induce metabolic reprogramming and trained immunity to constrain inflammatory responses in macrophages","volume":"156","author":"Zakeri","year":"2022","journal-title":"Cytokine"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"44261","DOI":"10.1074\/jbc.M204655200","article-title":"Homologues of human macrophage migration inhibitory factor from a parasitic nematode: Gene cloning, protein activity, and crystal structure","volume":"277","author":"Zang","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"5955","DOI":"10.1128\/IAI.66.12.5955-5963.1998","article-title":"Filarial nematode parasites secrete a homologue of the human cytokine macrophage migration inhibitory factor","volume":"66","author":"Pastrana","year":"1998","journal-title":"Infect. Immun."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"6402","DOI":"10.1128\/IAI.68.11.6402-6410.2000","article-title":"Identification of tgh-2, a filarial nematode homolog of Caenorhabditis elegans daf-7 and human transforming growth factor \u03b2, expressed in microfilarial and adult stages of Brugia malayi","volume":"68","author":"Gregory","year":"2000","journal-title":"Infect. Immun."},{"key":"ref_94","doi-asserted-by":"crossref","unstructured":"Gomez-Escobar, N., Bennett, C., Prieto-Lafuente, L., Aebischer, T., Blackburn, C.C., and Maizels, R.M. (2005). Heterologous expression of the filarial nematode alt gene products reveals their potential to inhibit immune function. BMC Biol., 3.","DOI":"10.1186\/1741-7007-3-8"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1128\/CVI.00594-12","article-title":"Nematode asparaginyl-tRNA synthetase resolves intestinal inflammation in mice with T-cell transfer colitis","volume":"20","author":"Kron","year":"2013","journal-title":"Clin. Vaccine Immunol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"3952","DOI":"10.1096\/fj.14-251967","article-title":"Kv1.3 channel-blocking immunomodulatory peptides from parasitic worms: Implications for autoimmune diseases","volume":"28","author":"Chhabra","year":"2014","journal-title":"FASEB J."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1016\/S0960-9822(01)00118-X","article-title":"Bm-CPI-2, a cystatin homolog secreted by the filarial parasite Brugia malayi, inhibits class II MHC-restricted antigen processing","volume":"11","author":"Manoury","year":"2001","journal-title":"Curr. Biol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"520","DOI":"10.4269\/ajtmh.1992.46.520","article-title":"Release of prostaglandin E2 by microfilariae of Wuchereria bancrofti and Brugia malayi","volume":"46","author":"Liu","year":"1992","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_99","doi-asserted-by":"crossref","unstructured":"Kaisar, M.M.M., Ritter, M., Del Fresno, C., Jonasdottir, H.S., van der Ham, A.J., Pelgrom, L.R., Schramm, G., Layland, L.E., Sancho, D., and Prazeres da Costa, C. (2018). Dectin-1\/2-induced autocrine PGE2 signaling licenses dendritic cells to prime Th2 responses. PLoS Biol., 16.","DOI":"10.1371\/journal.pbio.2005504"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"953053","DOI":"10.3389\/fimmu.2022.953053","article-title":"The parasitic worm product ES-62 protects the osteoimmunology axis in a mouse model of obesity-accelerated ageing","volume":"13","author":"Harnett","year":"2022","journal-title":"Front. Immunol."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"694","DOI":"10.1016\/j.pt.2017.05.007","article-title":"Can parasitic worms cure the modern world\u2019s ills?","volume":"33","author":"Harnett","year":"2017","journal-title":"Trends Parasitol."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1017\/S0022149X14000200","article-title":"Immunosuppressive PAS-1 is an excretory\/secretory protein released by larval and adult worms of the ascarid nematode Ascaris suum","volume":"89","author":"Antunes","year":"2015","journal-title":"J. Helminthol."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1017\/S0031182099005363","article-title":"The ABA-1 allergen of Ascaris lumbricoides: Sequence polymorphism, stage and tissue-specific expression, lipid binding function, and protein biophysical properties","volume":"120","author":"Xia","year":"2000","journal-title":"Parasitology"},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1016\/j.immuni.2017.09.015","article-title":"HpARI Protein Secreted by a Helminth Parasite Suppresses Interleukin-33","volume":"47","author":"Osbourn","year":"2017","journal-title":"Immunity"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1016\/j.molimm.2021.06.017","article-title":"Helminth extracellular vesicles: Interactions with the host immune system","volume":"137","author":"Drurey","year":"2021","journal-title":"Mol. Immunol."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"1545","DOI":"10.1016\/j.celrep.2017.05.001","article-title":"Extracellular Vesicles from a Helminth Parasite Suppress Macrophage Activation and Constitute an Effective Vaccine for Protective Immunity","volume":"19","author":"Coakley","year":"2017","journal-title":"Cell Rep."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"5488","DOI":"10.1038\/ncomms6488","article-title":"Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity","volume":"5","author":"Buck","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_108","doi-asserted-by":"crossref","unstructured":"Mukundan, A., Byeon, C.-H., Hinck, C.S., Smyth, D.J., Maizels, R., and Hinck, A.P.M. (2020). Structure-based mapping of the T\u03b2RI and T\u03b2RII receptor binding sites of the parasitic TGF-\u03b2 mimic, Hp-TGM. BioRxiv.","DOI":"10.1101\/2020.12.08.416701"},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1038\/nri.2016.95","article-title":"Interleukin-33 in health and disease","volume":"16","author":"Liew","year":"2016","journal-title":"Nat. Rev. Immunol."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"1871","DOI":"10.1084\/jem.182.6.1871","article-title":"Release of the mucosal mast cell granule chymase, rat mast cell protease II during anaphylaxis is associated with the rapid development of paracellular permeability to macromolecules in rat jejunum","volume":"182","author":"Scudamore","year":"1995","journal-title":"J. Exp. Med."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"7761","DOI":"10.1073\/pnas.1231488100","article-title":"Mast cells disrupt epithelial barrier function during enteric nematode infection","volume":"100","author":"McDermott","year":"2003","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"710","DOI":"10.1016\/j.immuni.2017.09.013","article-title":"Epidermal Growth Factor Receptor Expression Licenses Type-2 Helper T Cells to Function in a T Cell Receptor-Independent Fashion","volume":"47","author":"Minutti","year":"2017","journal-title":"Immunity"},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"1746","DOI":"10.1126\/science.1133715","article-title":"Amphiregulin, a TH2 cytokine enhancing resistance to nematodes","volume":"314","author":"Zaiss","year":"2006","journal-title":"Science"},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/j.immuni.2012.09.023","article-title":"Amphiregulin enhances regulatory T cell-suppressive function via the epidermal growth factor receptor","volume":"38","author":"Zaiss","year":"2013","journal-title":"Immunity"},{"key":"ref_115","unstructured":"Taylor, M.A., Coop, R.L., and Wall, R.L. (2007). Veterinary Parasitology, Wiley-Blackwell. [3rd ed.]."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1111\/j.1365-3024.2007.00995.x","article-title":"Identification of a 55 kDa Haemonchus contortus excretory\/secretory glycoprotein as a neutrophil inhibitory factor","volume":"30","author":"Anbu","year":"2008","journal-title":"Parasite Immunol."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"10008","DOI":"10.1016\/S0021-9258(17)36982-X","article-title":"A hookworm glycoprotein that inhibits neutrophil function is a ligand of the integrin CD11b\/CD18","volume":"269","author":"Moyle","year":"1994","journal-title":"J. Biol. Chem."},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1016\/j.vetpar.2006.01.055","article-title":"Identification of a 66kDa Haemonchus contortus excretory\/secretory antigen that inhibits host monocytes","volume":"138","author":"Rathore","year":"2006","journal-title":"Vet. Parasitol."},{"key":"ref_119","first-page":"952104","article-title":"Secreted filarial nematode galectins modulate host immune cells","volume":"11","author":"Loghry","year":"2022","journal-title":"BioRxiv"},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"1177","DOI":"10.1093\/molbev\/msh082","article-title":"Phylogenetic analysis of the vertebrate galectin family","volume":"21","author":"Houzelstein","year":"2004","journal-title":"Mol. Biol. Evol."},{"key":"ref_121","first-page":"41","article-title":"Inactivation of platelet-activating factor by a putative acetylhydrolase from the gastrointestinal nematode parasite Nippostrongylus brasiliensis","volume":"75","author":"Blackburn","year":"1992","journal-title":"Immunology"},{"key":"ref_122","doi-asserted-by":"crossref","unstructured":"Vaux, R., Schnoeller, C., Berkachy, R., Roberts, L.B., Hagen, J., Gounaris, K., and Selkirk, M.E. (2016). Modulation of the Immune Response by Nematode Secreted Acetylcholinesterase Revealed by Heterologous Expression in Trypanosoma musculi. PLoS Pathog., 12.","DOI":"10.1371\/journal.ppat.1005998"},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1016\/j.exppara.2013.01.006","article-title":"Molecular cloning and characterisation of in vitro immune response against astacin-like metalloprotease Ace-MTP-2 from Ancylostoma ceylanicum","volume":"133","author":"Zygner","year":"2013","journal-title":"Exp. Parasitol."},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"e157","DOI":"10.1038\/cti.2017.42","article-title":"Suppression of inflammation and tissue damage by a hookworm recombinant protein in experimental colitis","volume":"6","author":"Ferreira","year":"2017","journal-title":"Clin. Transl. Immunol."},{"key":"ref_125","doi-asserted-by":"crossref","first-page":"362ra143","DOI":"10.1126\/scitranslmed.aaf8807","article-title":"Hookworm recombinant protein promotes regulatory T cell responses that suppress experimental asthma","volume":"8","author":"Navarro","year":"2016","journal-title":"Sci. Transl. Med."},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"6447","DOI":"10.4049\/jimmunol.165.11.6447","article-title":"Eotaxin is specifically cleaved by hookworm metalloproteases preventing its action in vitro and in vivo","volume":"165","author":"Culley","year":"2000","journal-title":"J. Immunol."},{"key":"ref_127","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1093\/infdis\/jiu451","article-title":"Probing of a human proteome microarray with a recombinant pathogen protein reveals a novel mechanism by which hookworms suppress B-cell receptor signaling","volume":"211","author":"Tribolet","year":"2015","journal-title":"J. Infect. Dis."},{"key":"ref_128","doi-asserted-by":"crossref","first-page":"863","DOI":"10.1016\/j.immuni.2017.04.017","article-title":"Mast Cells Are Crucial for Induction of Group 2 Innate Lymphoid Cells and Clearance of Helminth Infections","volume":"46","author":"Shimokawa","year":"2017","journal-title":"Immunity"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/3\/2283\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:14:27Z","timestamp":1760120067000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/3\/2283"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,1,23]]},"references-count":128,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2023,2]]}},"alternative-id":["ijms24032283"],"URL":"https:\/\/doi.org\/10.3390\/ijms24032283","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,1,23]]}}}