Immune and other factors modulating host resistance against gastrointestinal nematode parasites in sheep

PDF
Published: Jan 29, 2018
DOI: https://doi.org/10.12681/jhvms.15597
Keywords:
Sheep gastrointestinal nematodes resistance immunity genes
K. ARSENOPOULOS
Laboratory of Parasitology and Parasitic Diseases, School of Veterinary Medicine, Faculty of Health Sciences, Aristotle University of Thessaloniki
I. SYMEONIDOU
Laboratory of Parasitology and Parasitic Diseases, School of Veterinary Medicine, Faculty of Health Sciences, Aristotle University of Thessaloniki
E. PAPADOPOULOS
Laboratory of Parasitology and Parasitic Diseases, School of Veterinary Medicine, Faculty of Health Sciences, Aristotle University of Thessaloniki
Abstract

Infection of small ruminants with gastrointestinal nematode (GIN) parasites is a significant problem with crucial impact on meat and milk production. The strategy of administrating anthelminthic drugs has been implemented for many years and has resulted in the development of resistant strains of parasites. Meanwhile, consumers demand for free of drugs products have led to the adoption of alternative control methods, which involve the selective breeding of animals, which are resistant to parasitism. The development of immunity and therefore, resistance against gastrointestinal parasites is based on the activation of specific host genes. Gene analysis has revealed areas (QTLs), which affect resistance or susceptibility of sheep to gastrointestinal infestations between animals of different breeds and between individuals of the same breed. The role of cytokines and T helper cells has been enhanced as research, strongly, supports the connection of Th2 cells with resistance and Th1 cells with susceptibility against GIN. Latest data implicates T regulatory cells and a specific cell type, Th17, in immune response mechanisms. Specific adhesion molecules (integrins, lectins, cadherins) are produced in the gut lumen in sufficient amounts and appear to boost immunity and reduce clinical signs in sheep. Additionally, the immunoglobulins IgA and IgE have been positively correlated with increased resistance against GIN. In several cases of GIN, where an increased number of eosinophils and mast cells in the intestinal epithelium have been recorded, the animals had a reduced number of parasite eggs in their feces. The genes of the Major Histocompatibility Complex have been referred to as potential resistance or susceptibility markers. Other enzymes, like chitinases, enhance the resilience of animals and protect them effectively. Animal’s nutritional status is another determinant factor of immune capability against GIN in sheep, both systemic, as well as locally. Regarding the effect of reactive oxygen and nitrogen species, some researchers support their direct effect against GIN, resulting in a natural reduction of their number, while others claim the indirect action in the intestinal epithelium by reducing local immunity. Consequently, the detection of genes associated with resistance or susceptibility to gastrointestinal infestations is promising and in line with modern requirements.

Article Details
  • Section
  • Review Articles
Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

Authors who publish with this journal agree to the following terms:

· Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution Non-Commercial License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.

· Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.

· Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.

Downloads
Download data is not yet available.
References
Ahern PP, Schiering C, Buonocore S, McGeachy MJ, Cua DJ, Maloy KJ, Powrie F (2010) Interleukin-23 drives intestinal inflammation through direct activity on T cells. Immunity 33:279-288.
Anthony RM, Rutitzky LI, Urban JF, Stadecker MJ, Gause WC (2007) Protective immune mechanisms in helminth infection. Nat Rev Immunol 7:975–987.
Artis D, Grencis RK (2008) The intestinal epithelium: sensors to effectors in nematode infection. Muc Immunol 1:252–264.
Artis D, Wang ML, Keilbaugh SA, He W, Brenes M, Swain GP, Knight PA Donaldson DD, Lazar MA, Miller HR, Schad GA, Scott P, Wu GD (2004) RELMbeta/FIZZ2 is a goblet cell-specific immuneeffector molecule in the gastrointestinal tract. Proc Nat Acad Sci USA 101: 13596–13600.
Athanasiadou S, Jones LA, Burgess ST, Kyriazakis I, Pemberton AD, Houdijk JG, Huntley JF (2011) Genome-wide transcriptomic analysis of intestinal tissue to assess the impact of nutrition and a secondary nematode challenge in lactating rats. PLoS One 6 e20771.
Athanasiadou S, Pemberton A, Jackson F, Inglis N, Miller HR, Thιvenod F, Mackellar A, Huntley JF (2008) Proteomic approach to identify candidate effector molecules during the in vitro immune exclusion of infective Teladorsagia circumcincta in the abomasum of sheep. Vet Res 39:58.
Balic A, Bowles VM, Meeusen EN (2000) Cellular profiles in the abomasal mucosa and lymph node during primary infection with Haemonchus contortus in sheep. Vet Immunol Immunopathol 75:109–120.
Balic A, Bowles VM, Meeusen EN (2002) Mechanisms of immunity to Haemonchus contortus infection in sheep. Parasite Immunol 24:39–46.
Balic A, Cunningham CP, Meeusen EN (2006) Eosinophil interactions with Haemonchus contortus larvae in the ovine gastrointestinal tract. Parasite Immunol 28:107–115.
Belkaid Y, Rouse BT (2005) Natural regulatory T cells in infectious disease. Nat Immunol 6:353–360.
Belkaid Y, Tarbell K (2009) Regulatory T cells in the control of host microorganism interactions. Annu Rev Immunol 27:551–589.
Bell LV, Else KJ (2008) Mechanisms of leucocyte recruitment to the inflamed large intestine: redundancy in integrin and addressin usage. Parasite Immunol 30:163–170.
Benavides MV, Weimer TA, Borba MFS, Berne MEA, Sacco AMS (2002) Association between microsatellite markers of sheep chromosome 5 and faecal egg counts. Small Ruminant Research 46:97–105.
Beraldi D, Craig BH, Bishop SC, Hopkins J, Pemberton JM (2008) Phenotypic analysis of host-parasite interactions in lambs infected with Teladorsagia circumcincta. Int J Parasitol 38:1567–1577.
Bishop SC, Morris CA (2007) Genetics of disease resistance in sheep and goats. Small Rum Res 70:48–59.
Buitkamp J, Filmether P, Stear MJ, Epplen JT (1996) Class I and class II major histocompatibility complex alleles are associated with faecal egg counts following natural, predominantly Ostertagia circumcincta infection. Parasitol Res 82:693–696.
Colasanti M, Gradoni L, Mattu M, Persichini T, Salvati L, Venturini G, Ascenzi P (2002) Molecular bases for the anti-parasitic effect of NO. Int J Mol Med 9:131–134.
Colditz IG (2008) Six costs of immunity to gastrointestinal nematode infections. Parasite Immunol 30:63–70.
Coop RL, Kyriazakis I (1999) Nutrition–parasite interaction. Vet Parasitol 84:187–204.
Cooper DW, Van Oorschot RAH, Piper LR, Le Jambre LF (1989) No association between the ovine leukocyte antigen (OLA) system in the Australian Merino and susceptibility to Haemonchus contortus infestation. Int J Parasitol 15:101–109.
Craig NM, Miller HR, Smith WD, Knight PA (2007) Cytokine expression in naive and previously infected lambs after challenge with Teladorsagia circumcincta. Vet Immunol Immunopathol 120:47–54.
Crawford AM, McEwan JC, Dodds KG, Wright CS, Bisset SA, Macdonald PA, Knowler KJ, Greer GJ, Green RS, Shaw RJ, Paterson KA, Cuthbertson RP, Vlassoff A, Squire DR, West CJ, Phua SH (1997) In: Proceedings of the 12th Conference on Resistance to Nematode Parasites in Sheep: How Important are the MHC Genes? Part 1 Dubbo, NSW, Australia, pp.58–62.
Cresswell P (1994) Assembly, transport, and function of MHC class-II molecules. Annu Rev Immunol 12:259–293.
Dawkins HJ, Windon RG, Eagleson GK (1989) Eosinophil responses in sheep selected for high and low responsiveness to Trichostrongylus colubriformis. Int J Parasitol 19:199–205.
Dawson HD, Solano-Aguilar G, Beal M, Beshah E, Vangimalla V, Jones E, Botero S, Urban JF (2009) Localized Th1, Th2, T regulatory cell and inflammation associated hepatic and pulmonary immune responses in Ascaris suum-infected swine are increased by retinoic acid. Infect Immun 77:2576–2587.
Dunphy JL, Balic A, Barcham GJ, Horvath AJ, Nash AD, Meeusen EN (2000) Isolation and characterization of a novel inducible mammalian galectin. J Biol Chem 275:32106–32113.
Dzik JM, Zielinski Z, Golos B, Walajtys-Rode E (2006) Trichinella spiralis infection affects p47(phox) protein expression in guineapig alveolar macrophages. Exp Parasitol 112:158–163.
Dzik JM (2006) Molecules released by helminth parasites in host colonization. Acta Biochim Pol 53:33–64.
Ennen S, Hamann H, Distl O, Hickford J, Zhou H, Ganter M (2009) A field trial to control ovine footrot via vaccination and genetic markers. Small Rumin Res 86:22–25.
Familton AS, McAnulty RW (1997) Life cycles and development of nematode parasites of ruminants in sustainable control of internal parasites in ruminants. Animal Industries Workshop 67–80.
Finkelman FD, Urban JF (2001) The other side of the coin: the protective role of the TH2 cytokines. J Allergy Clin Immunol 107:772–780.
Finney CA, Taylor MD, Wilson MS, Maizels RM (2007) Expansion and activation of CD4(+)CD25(+) regulatory T cells in Heligmosomoides polygyrus infection. Eur J Immunol 37:1874–1886.
Fontenot JD, Rasmussen JP, Williams LM, Dooley JL, Farr AG, Rudensky AY (2005) Regulatory T cell lineage specification by the forkhead transcription factor FoxP3. Immunity 22:329–341.
French AT, Bethune JA, Knight PA, McNeilly TN, Wattegedera S, Rhind S, Miller HR, Pemberton AD (2007) The expression of intelectin in sheep goblet cells and upregulation by interleukin 4. Vet Immunol Immunopathol 120:41–46.
French AT, Knight PA, Smith WD, Brown JK, Craig NM, Pate JA, Miller HR, Pemberton AD (2008) Up-regulation of intelectin in sheep after infection with Teladorsagia circumcincta. Int J Parasitol 38:467–475.
French AT, Knight PA, Smith WD, Pate JA, Miller HR, Pemberton AD (2009) Expression of three intelectins in sheep and response to a Th2 environment. Vet Res 40:53.
Galioto AM, Hess JA, Nolan TJ, Schad GA, Lee JJ, Abraham D (2006) Role of eosinophils and neutrophils in innate and adaptive protective immunity to larval Strongyloides stercoralis in mice. Infect Immun 74:5730–5738.
Gasbarre LC, Smith LL, Lichtenfels JR, Pilitt PA (2009) The identification of cattle nematode parasites resistant to multiple classes of anthelmintics in a commercial cattle population in the US. Vet Parasitol 166: 281–5.
Gossner A, Wilkie H, Joshi A, Hopkins J (2013) Exploring the abomasal lymph node transcriptome for genes associated with resistance to the sheep nematode Teladorsagia circumcincta. Vet Res 44(1):68.
Gossner AG, Venturina VM, Peers A, Watkins CA, Hopkins J (2012b) Expression of sheep interleukin 23 (IL23A, alpha subunit p19) in two distinct gastrointestinal diseases. Vet Immunol Immunopathol 150:118–122.
Gossner AG, Venturina VM, Shaw DJ, Pemberton JM, Hopkins J (2012a) Relationship between susceptibility of Blackface sheep to Teladorsagia circumcincta infection and an inflammatory mucosal T cell response. Vet Res 43:26.
Greer AW, Huntley JF, MacKellar A, McAnulty RW, Jay NP, Green RS, Stankiewicz M, Sykes AR (2008) The effect of corticosteroid treatment on local immune responses, intake and performance in lambs infected with Teladorsagia circumcincta. Int J Parasitol 38:1717–1728.
Halliday AM, Routledge CM, Smith SK, Matthews JB, Smith WD (2007) Parasite loss and inhibited development of Teladorsagia circumcincta in relation to the kinetics of the local IgA response in sheep. Parasite Immunol 29:425–434.
Harper RW, Xu C, Eiserich JP, Chen Y, Kao CY, Thai P, Setiadi H, Wu R (2005) Differential regulation of dual NADPH oxidases/peroxidases Duox2 and Duox2, by Th1 and Th2 cytokines in respiratory tract epithelium. FEBS Lett 579:11–17.
Hasnain SZ, Evans CM, Roy M, Gallagher AL, Kindrachuk KN, Barron L, Dickey BF, Wilson MS, Wynn TA, Grencis RK, Thornton DJ (2011) Muc5ac: a critical component mediating the rejection of enteric nematodes. J Exp Med 208:893–900.
Hassan M, Good B, Hanrahan J, Campion D, Sayers G, Mulcahy G, Sweeney T (2011) The dynamic influence of the DRB1*1101 allele on the resistance of sheep to experimental Teladorsagia circumcincta infection. Vet Res 42:46.
Henderson NG, Stear MJ (2006) Eosinophil and IgA responses in sheep infected with Teladorsagia circumcincta. Vet Immunol Immunopathol 112:62–66.
Hickford J, Forrest R, Zhou H, Fang Q, Frampton C (2011) Association between variation in faecal egg count for a mixed field-challenge of nematode parasites and ovine MHC-DQA2 polymorphism. Vet Immunol Immunopathol 144:312–320.
Hori S, Nomura T, Sakaguchi S (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science 299:1057–1061.
Hoste H, Torres-Acosta JF (2011) Non chemical control of helminthes in ruminants: adapting solutions for changing worms in a changing world. Vet Parasitol 180:144–154.
Hunter AR, MacKenzie G (1982) The pathogenesis of a single challenge dose of Haemonchus contortus in lambs under six months of age. J Helminthol 56:135–144.
Ingham A, Reverter A, Windon R, Hunt P, Menzies M (2008) Gastrointestinal nematode challenge induces some conserved gene expression changes in the gut mucosa of genetically resistant sheep. Int J Parasitol 38:431–442.
Kim ES, Sonstegard TS, Vinicius M, Silva GB, Gasbarre LC, Van Tassell CP (2013) Identification of quantitative trait loci affecting gastrointestinal parasite resistance in an experimental Angus population. Animal Genetics 45:117–121.
Kimura A, Kishimoto T (2010) IL-6: regulator of Treg/Th17 balance. Eur J Immunol 40:1830–1835.
Knight PA, Pate J, Smith WD, Miller HR (2007) An ovine chitinaselike molecule, chitinase-3 like-1 (YKL-40), is upregulated in the abomasum in response to challenge with the gastrointestinal nematode, Teladorsagia circumcincta. Vet Immunol Immunopathol 120(1–2):55–60.
Korn T, Bettelli E, Oukka M, Kuchroo VK (2009) IL-17 and Th17 Cells. Annu Rev Immunol 27:485–517.
Korten S, Badusche M, Buettner DW, Hoerauf A, Brattig N, Fleischer B (2008) Natural death of adult Onchocerca volvulus and filaricidal effects of doxycycline induce local FOXP3+/CD4 + regulatory T cells and granzyme expression. Microbes Infect 10:313–324.
Kotze AC (2003) Catalase induction protects Haemonchus contortus against hydrogen peroxide in vitro. Int J Parasitol 33:393–400.
Lasky LA (1991) Lectin cell adhesion molecules (LEC-CAMs): a new family of cell adhesion proteins involved with inflammation. J Cell Biochem 45:139–146.
Lee CG, Da Silva CA, Dela Cruz CS, Ahangari F, Ma B, Kang M-J, He C-H, Takyar S, Elias JA (2011) Role of chitin and chitinase/chitinase-like proteins in inflammation, tissue remodeling, and injury. Annu Rev Physiol 73(1):479–501.
Lees MS, Robinson MA, Inghama AB, Kotzea AC, Piedrafit DM (2011) Dual oxidase 2 and glutathione peroxidase gene expression are elevated in hyperimmunised sheep challenged with Haemonchus contortus. Vet Parasitol 179:113–122.
Li RW, Choudhary RK, Capuco AV, Urban Jr JF (2012) Exploring the host transcriptome for mechanisms underlying protective immunity and resistance to nematode infections in ruminants Vet Parasitol 190:1-11.
Li RW, Gasbarre LC (2009) A temporal shift in regulatory networks and pathways in the bovine small intestine during Cooperia oncophora infection. Int. J. Parasitol 39:813–824.
Li RW, Gasbarre LC (2010) Gene expression in the bovine gastrointestinal tract during nematode infection. Vet Parasitol 157–178.
Li RW, Hou Y, Li C, Gasbarre LC (2010) Localized complement activation in the development of protective immunity against Ostertagia ostertagi infections in cattle. Vet Parasitol 174:247–256.
Li RW, Sonstegard TS, Van Tassell CP, Gasbarre LC (2007) Local inflammation as a possible mechanism of resistance to gastrointestinal nematodes in Angus heifers. Vet Parasitol 145:100–107.
Macpherson AJ, McCoy KD, Johansen FE, Brandtzaeg P (2008) The immune geography of IgA induction and function. Mucosal Immunol 1:11–22.
Maizels RM, Yazdanbakhsh M (2003) Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol 3:733–744.
Marshall K, Maddox JF, Lee SH, Zhang Y, Kahn L (2009) Genetic mapping of quantitative trait loci for resistance to Haemonchus contortus in sheep. Anim Genet 40:262–72.
Marshall K, Mugambi JM, Nagda S, Sonstegard TS, Van Tassell SP, Baker RL, Gibson JP (2012) Quantitative trait loci for resistance to Haemonchus contortus artificial challenge in Red Maasai and Dorper sheep of East Africa. Anim Genetics 44:285-295.
McDermott JR, Leslie FC, D‘Amato M, Thompson DG, Grencis RG, McLaughlin JT (2006) Immune control of food intake: enteroendocrine cells are regulated by CD4+ T lymphocytes during small intestinal inflammation. Gut 55:492–497.
McRae K, McEwan JC, Dodds KG, Gemmell NJ (2014) Signatures of selection in sheep bred for resistance or susceptibility to gastrointestinal nematodes. Genomics 15:637.
Meeusen EN, Balic A, Bowles V (2005) Cells, cytokines and other molecules associated with rejection of gastrointestinal nematode parasites. Vet Immunol Immunopathol 108:121–125.
Miller CM, Waghorn TS, Leathwick DM, Candy PM, Oliver AMB, Watson TG (2012) The production cost of anthelmintic resistance in lambs. Vet Parasitol 186(3–4):376–381.
Miller JE, Bishop SC, Cockett NE, McGraw RA (2006) Segregation of natural and experimental gastrointestinal nematode infection in F2 progeny of susceptible Suffolk and resistant Gulf Coast Native sheep and its usefulness in assessment of genetic variation. Vet Parasit 140:83–89.
Morris CA, Vlassoff A, Bisset S, Baker R, Watson TG, West CJ, Wheeler M (2000) Continued selection of Romney sheep for resistance or susceptibility to nematode infection: estimates of direct and correlated responses. Anim Sci 70:17–27.
Morris CA, Wheeler M, Watson TG, Hosking BC, Leathwick DM (2005) Direct and correlated responses to selection for high or low faecal nematode egg count in Perendale sheep. N Z J Agric Res 48:1–10.
Murphy L, Eckersall PD, Bishop SC, Pettit JJ, Huntley JF, Burchmore R, Stear MJ (2010) Genetic variation among lambs in peripheral IgE activity against the larval stages of Teladorsagia circumcincta. Parasitol 137:1249–1260.
Nair MG, Guild KJ, Du Y, Zaph C, Yancopoulos GD, Valenzuela DM, Murphy A, Stevens S, Karow M, Artis D (2008) Goblet cell-derived resistin-like molecule beta augments CD4+ T cell production of IFNgamma and infection-induced intestinal inflammation. J Immunol 181:4709–4715.
Nakamura Y, Syouji T, Onodera T, Kawashima K, Inumaru S, Yokomizo Y (2002) Effects of recombinant bovine interferon gamma on Strongyloides papillosus infection in calves. J Helminthol 76:59–64.
Outteridge PM, Windon RG, Dineen JK (1985) An association between a lymphocyte antigen in sheep and the response to vaccination against the parasite Trichostrongylus colubriformis. Int J Parasitol 15:121–127.
Outteridge PM, Windon RG, Dineen JK, Smith EF (1986) The relationship between ovine lymphocyte antigens and faecal egg count of sheep selected for responsiveness to vaccination against Trichostrongylus colubriformis. Int J Parasitol 16:369–374.
Ouyang W, Rutz S, Crellin NK, Valdez PA, Hymowitz SG (2011) Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu Rev Immunol 29(29):71–109.
Paludan SR (1998) Interleukin-4 and interferon-gamma: the quintessence of a mutual antagonistic relationship. Scand J Immunol 48:459–468.
Patel N, Kreider T, Urban JF, Gause WC (2009) Characterisation of effector mechanisms at the host parasite interface during the immune response to tissue-dwelling intestinal nematode parasites. Int J Parasitol 39:13–21.
Paterson S, Wilson K, Pemberton JM (1998) Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Proc Natl Acad Sci 95:3714–3719.
Peck A, Mellins ED (2009) Breaking old paradigms: Th17 cells in autoimmune arthritis. Clin Immunol 132:295–304.
Pennock JL, Grencis RK (2006) The mast cell and gut nematodes: damage and defence. Chem Immunol Allergy 90:128–140.
Periasamy K, Pichler R, Poli M, Cristel S, Cetra B, Medus D, Basar M, Thiruvenkadan A.K, Ramasamy S, Ellahi M.B, Mohammed F, Teneva A, Shamsuddin M, Podesta MG, Diallo A (2014) Candidate Gene Approach for Parasite Resistance in Sheep–Variation in Immune Pathway Genes and Association with Fecal Egg Count. PLoS ONE 9(2):e88337. doi:10.1371/journal.pone.0088337.
Pernthaner A, Cole SA, Morrison L, Hein WR (2005) Increased expression of interleukin-5 (IL-5), IL-13 and tumor necrosis factor alpha genes in intestinal lymph cells of sheep selected for enhanced resistance to nematodes during infection with Trichostrongylus colubriformis. Infect Immun 73:2175–2183.
Pernthaner A, Vlassoff A, Douch PGC, Maas D (1997) Cytokine mRNA expression and IFN-production in nematode resistant and susceptible line lambs artificially infected with gastrointestinal nematodes. Acta Parasitol 42:55–61.
Perry BD, Randolph TF (1999) Improving the assessment of the economic impact of parasitic diseases and of their control in production animals. Vet Parasitol 84(3–4):145–168.
Pesce JT, Liu Z, Hamed H, Alem F, Whitmire J, Lin H, Liu Q, Urban Jr JF, Gause WC (2008) Neutrophils clear bacteria associated with parasitic nematodes augmenting the development of an effective Th2- type response. J Immunol 180:464–474.
Pochanke V, Koller S, Dayer R, Hatak S, Ludewig B, Zinkernagel RM, Hengartner H, McCoy KD (2007) Identification and characterization of a novel antigen from the nematode Nippostrongylus brasiliensis recognized by specific IgE. Eur J Immunol 37:1275–1284.
Pulendran B (2004) Modulating Th1/Th2 responses with microbes, dendritic cells and pathogen recognition receptors. Immunol Res 29:187–196.
Rainbird MA, Macmillan D, Meeusen EN (1998) Eosinophil-mediated killing of Haemonchus contortus larvae: effect of eosinophil activation and role of antibody, complement and interleukin-5. Parasite Immunol 20:93–103.
Robinson N, Piedrafita D, Snibson K, Harrison P, Meeusen EN (2010) Immune cell kinetics in the ovine abomasal mucosa following hyperimmunization and challenge with Haemonchus contortus. Vet Res 41.
Rowe A, Gondro C, Emery D, Sangster N (2009) Sequential microarray to identify timing of molecular responses to Haemonchus contortus infection in sheep. Vet Parasitol 161:76–87.
Salle P, Jacquiet L, Gruner J, Cortet C, Sauve F, Prevot C, Grisez JP, Bergeaud LA (2012) Genome scan for QTL affecting resistance to Haemonchus contortus in sheep. J Anim Sci 90:4690-4705.
Sargison ND (2012) Pharmaceutical treatments of gastrointestinal nematode infections of sheep-Future of anthelmintic drugs. Vet Parasitol 189(1):79–84.
Sayers G, Good B, Hanrahan JP, Ryan M, Sweeney T (2005b) Intron 1 of the interferon gamma gene: its role in nematode resistance in Suffolk and Texel sheep breeds. Res Vet Sci 79:191–196.
Sayre BL, Harris GC (2012) Systems genetics approach reveals candidate genes for parasite resistance from quantitative trait loci studies in agricultural species. Anim Genet 43:190–8.
Schallig HDFH (2000) Immunological responses of sheep to Haemonchus contortus. Parasitol 120:S63–S72.
Schwaiger FW, Gostomski D, Stear MJ, Duncan JL, McKellar QA, Epplen JT, Buitkamp J (1995) An ovine major histocompatibility complex DRB1 allele is associated with low faecal egg counts following natural, predominantly Ostertagia circumcincta infection. Int J Parasitol 25:815–822.
Shakya KP, Miller JE, Lomax LG, Burnett DD (2011) Evaluation of immune response to artificial infections of Haemonchus contortus in Gulf Coast Native compared with Suffolk lambs. Vet Parasitol 181 239–247.
Shaw R, Morris C, Wheeler M, Tate M, Sutherland I (2012) Salivary IgA: a suitable measure of immunity to gastrointestinal nematodes in sheep. Vet Parasitol 186:109–117.
Silva MVB, Sonstegard TS, Hanotte O (2012) Identification of quantitative trait loci affecting resistance to gastrointestinal parasites in a double backcross population of Red Maasai and Dorper sheep. Anim Genet 43:63–71.
Singh-Dang T, Walker M, Ford D, Valentine RA (2014) Nutrigenomics: the role of the nutrients in gene expression, Periodontology 2000 64:154-160.
Smith A, Madden KB, Yeung KJA, Zhao A, Elfrey J, Finkelman F, Levander O, Shea-Donohue T, Urban JF (2005) Deficiencies in selenium and/or vitamin E lower the resistance of mice to Heligmosomoides polygyrus infections. J Nutr 135:830–836.
Sonstegard TS, Van Tassell CP, Matukumalli LK, Harhay GP, Bosak S, Rubenfield M, Gasbarre LC (2004) Production of EST from Cdna libraries derived from immunologically activated bovine gut. In Germplasm Release.
Stear MJ, Bairden K, Innocent GT, Mitchell S, Strain S, Bishop SC (2004) The relationship between IgA activity against 4th-stage larvae and density-dependent effects on the number of 4th-stage larvae of Teladorsagia circumcincta in naturally infected sheep. Parasitol 129:363–369.
Stear MJ, Bishop SC, Henderson NG, Scott I (2003) A key mechanism of pathogenesis in sheep infected with the nematode Teladorsagia circumcincta. Anim Health Res Rev 4:45–52.
Sykes AR (2008) Manipulating host immunity to improve nematode parasite control. Parasite Immunol 30:71–77.
Taylor MD, LeGoff L, Harris A, Malone E, Allen JE, Maizels RM (2005) Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J Immunol 174:4924–4933.
Terefe G, Yacob HT, Grisez C, Prevot F, Dumas E, Bergeaud JP, Dorchies P, Hoste H, Jacquiet P (2005) Haemonchus contortus egg excretion and female length reduction in sheep previously infected with Oestrus ovis (Diptera: Oestridae) larvae. Vet Parasitol 128:271–283.
Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B (2006) TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24:179–189.
Venturina MV, Gossner AG, Hopkins J (2013) The immunology and genetics of resistance of sheep to Teladorsagia circumcincta. Vet Res Commun 37:171–181.
Wagland BM, Steel JW, Windon RG, Dineen JK (1984) The response of lambs to vaccination and challenge with Trichostrongylus colubriformis: effect of plane of nutrition on, and the interrelationship between, immunological responsiveness and resistance. Int J Parasitol 14:39-44.
Weaver CT, Hatton RD, Mangan PR, Harrington LE (2007) IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol 25:821–852.
Zhao A, Urban Jr JF, Anthony RM, Sun R, Stiltz J, Van RN, Wynn TA, Gause WC, Shea-Donohue T (2008) Th2 cytokine-induced alterations in intestinal smooth muscle function depend on alternatively activated macrophages. Gastroenterology 135:217–225.
Zhu Z, Zheng T, Homer RJ, Kim Y-K, Chen NY, Cohn L, Hamid Q, Elias JA (2004) Acidic mammalian chitinase in asthmatic Th2 inflammation and IL-13 pathway activation. Science 304 (5677):1678–1682.
Most read articles by the same author(s)