Skip to main content
Log in

Characterization of interferon gamma gene in relation to immunological responses in Haemonchus contortus resistant and susceptible Garole sheep

  • Research
  • Published:
Veterinary Research Communications Aims and scope Submit manuscript

Abstract

Garole sheep exhibits within-breed difference in resistance to natural gastrointestinal nematode infection predominated by Haemonchus contortus. In the present study, interferon gamma gene (IFN-γ) was characterized in relation to parasitological, haematological, and immune response against H. contortus in resistant and susceptible Garole sheep. Resistant and susceptible Garole sheep were selected from the field based on consistent low faecal egg counts (FEC) for one year and single nucleotide polymorphisms (SNPs) in the IFN-γ gene. The partial amplification of IFN-γ gene (1282 bp) revealed 4 SNPs exclusively in resistant sheep and 3 SNPs were shared between resistant and susceptible Garole sheep. The selected resistant and susceptible Garole sheep were challenged with H. contortus infection. The parasitological, haematological, immunological responses, and expression of IFN-γ gene were compared between the resistant and susceptible Garole sheep. The FEC of resistant sheep was significantly (P < 0.05) lower than the susceptible sheep infected with H. contortus. There was spontaneous elimination of H. contortus from 28 to 33 days post infection (DPI) in resistant sheep. Haemoglobin and packed cell volume were significantly (P < 0.05) higher in resistant sheep than the susceptible sheep. The serum concentration of immunoglobulin (Ig)G1 and IgA and cytokine IFN-γ activity and also the expression of IFN-γ gene were significantly (P < 0.05) higher in the infected resistant sheep from 14 to 28 DPI compared to the susceptible sheep. In resistant sheep, IgA and IgG1 and cytokine IFN-γ positively correlated with expression of IFN-γ gene, and the SNPs recorded in the resistant sheep only might play an important role in conferring resistance against H. contortus. Further studies are required to elucidate the role of IFN-γ gene in H. contortus resistance in Garole sheep.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Code or data availability

The datasets generated in this study are included in this article (and its supplementary information files) and are also available from the corresponding author on a reasonable request.

References

  • Aguerrea S, Jacquiet P, Brodier H, Bournazel JP, Grisez C, Prévot F, Michot L, Fidelle F, Astruc JM, Morenoa CR (2018) Resistance to gastrointestinal nematodes in dairy sheep: Genetic variability and relevance of artificial infection of nucleus rams to select for resistant ewes on farms. Vet Parasitol 256:16–23

    Article  Google Scholar 

  • Albuquerque AA, Bassetto CC, Almeida FA, Hildersley KA, McNeilly TN, Britton C, Amarante AFT (2019) Differences in immune responses to Haemonchus contortus infection in the susceptible Ile de France and the resistant Santa Ines sheep under different anthelmintic treatments regimens. Vet Res 50:104 https://doi.org/10.1186/s13567-019-0722-3

  • Amarante AFT (2014) Sustainable worm control practices in South America. Small Rumin Res 118:56–62

    Article  Google Scholar 

  • Amarante AFT, Bricarello PA, Huntley JF, Mazzolinb LP, Gomes JC (2005) Relationship of abomasal histology and parasite-specific immunoglobulin A with the resistance to Haemonchus contortus infection in three breeds of sheep. Vet Parasitol 128:99–107

    Article  CAS  PubMed  Google Scholar 

  • Andronicos N, Hunt P, Windon R (2010) Expression of genes in gastrointestinal and lymphatic tissues during parasite infection in sheep genetically resistant or susceptible to Trichostrongyluscolubriformis and Haemonchus contortus. Int J Parasitol 40(4):417–429

    Article  CAS  PubMed  Google Scholar 

  • Arsenopoulos KV, Fthenakis GC, Katsarou EI, Papadopoulos E (2021) Haemonchosis: A challenging parasitic infection of sheep and goats. Animals 11(2):363. https://doi.org/10.3390/ani11020363

    Article  PubMed  PubMed Central  Google Scholar 

  • Arsenopoulos S, Papadopoulos E (2017) Immune and other factors modulating host resistance against gastrointestinal nematode parasites in sheep. J Hellenic Vet Med Soc 68:131–144

    Article  Google Scholar 

  • Baker R, Audho J, Aduda E, Thorpe W (2017) Genetic resistance to gastro-intestinal nematode parasties in Galla and Small East African goats in the sub-humid tropics. Anim Sci 73:61–70. https://doi.org/10.1017/S1357729800058057

    Article  Google Scholar 

  • Banerjee D, Upadhyay CR, Chaudhary UB, Kumar R, Singh S, Ashutosh JMG, Polley S, Mukherjee A, Das TK, De S (2014) Seasonal variation in expression pattern of genes under HSP70 family in heat- and cold-adapted goats (Capra hircus). Cell Stress Chaperones 19:401-408 https://doi.org/10.1007/s12192-013-0469-0

  • Banerjee R, Mandal PK, Pal UK, Roy K (2010) Productivity and general potential of Garole sheep of India - A review. Asian J Anim Sci 4:170–189

    Article  Google Scholar 

  • Bassetto CC, Almeida FA, Newlands GFJ, Smith WD, Castilhos AM, Fernandes S, Siqueira ER, Amarante AFT (2018) Trials with the Haemonchus vaccine, Barbervax®, in ewes and lambs in a tropical environment: Nutrient supplementation improves protection in periparturient ewes. Vet Parasitol 264:52–57. https://doi.org/10.1016/j.vetpar.2018.11.006

    Article  CAS  PubMed  Google Scholar 

  • Becker GM, Burke JM, Lewis RM, Miller JE, Morgan JLM, Notter DR, Murdoch BM (2020) Genome-wide association study to identify genetic loci associated with gastrointestinal nematode resistance in Katahdin sheep. Anim Genet 51(2):330–335. https://doi.org/10.1111/age.12895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bendixen T, Windon RG, Huntley JF, Mac Kellar A, Davey RJ, McClure SJ, Emery DL (2004) Development of a new monoclonal antibody to ovine chimeric IgE and its detection of systemic and local IgE antibody responses to the intestinal nematode Trichostrongylus colubriformis. Vet Immunol Immunopathol 97:11–24

    Article  Google Scholar 

  • Beraldi D, McRae AF, Gratten J, Pilkington JG, Slate J, Visscher PM, Pemberton JM (2007) Quantitative trait loci (QTL) mapping of resistance to strongyles and coccidia in the free-living Soay sheep (Ovis aries). Int J Parasitol 37:121–129

    Article  CAS  PubMed  Google Scholar 

  • Benavides M, Sonstegard T, Van Tassel C (2016) Genomic regions associated with sheep resistance to gastrointestinal nematodes. Trends Parasitol 32(6). https://doi.org/10.1016/j.pt.2016.03.007

  • Bordoloi G, Jas R, Ghosh JD (2012) Parasitological and haemato-biochemical response to Haemonchus contortus infection in Garole sheep. Indian J Anim Sci 82(4):359–362

    Google Scholar 

  • Bouyum A (1968) Isolation of mononuclear cells and granulocytes from human blood. Isolation of mononuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 G. Scand J Clin Lab Invest Suppl 97:77–89

    Google Scholar 

  • Bowdridge SA, Zajac AM, Notter DR (2015) St. Croix sheep produce a rapid and greater cellular immune response contributing to reduced establishment of Haemonchus contortus. Vet Parasitol 208(3–4):204–210 https://doi.org/10.1016/j.vetpar.2015.01.019

  • Braga FR, de Araújo JV (2014) Nematophagous fungi for biological control of gastrointestinal nematodes in domestic animals. Appl Microbiol Biotechnol 98(1):71–82. https://doi.org/10.1007/s00253-013-5366-z

    Article  CAS  PubMed  Google Scholar 

  • Brahma A, De T, Jas R, Baidya S, Pandit S, Mandal SC, Kumar D, Rai S (2022) Within Breed Resistance to Naturally Occurring Gastrointestinal Nematodoses in Garole Sheep of West Bengal. Indian J Anim Res, India. https://doi.org/10.18805/IJAR.B-4936

    Book  Google Scholar 

  • Brown DJ, Fogarty NM (2017) Genetic relationships between internal parasite resistance and production traits in Merino sheep. Anim Prod Sci 57:209–215

    Article  Google Scholar 

  • Bungiro RD, Sun T, Harrison LM, Shoemaker CB, Cappello M (2008) Mucosal antibody responses in experimental hookworm infection. Parasite Immunol 30:293–303

    Article  CAS  PubMed  Google Scholar 

  • Chauhan KK, Rout PK, Singh PK, Mandal A (2003) Genetic resistance of Barbari and Jamunapari kids to natural infection with gastrointestinal nematodes. Trop Anim Health Prod 35(5):397–408

    Article  CAS  PubMed  Google Scholar 

  • Ciappesoni G, Goldberg V, Gimeno D (2013) Estimates of genetic parameters for worm resistance, wool and growth traits in Merino sheep of Uruguay. Livest Sci 157(1):65–74

    Article  Google Scholar 

  • Cintra MCR, Teixeira VN, Nascimento LV, Sotomaior CS (2016) Lack of efficacy of monepantel against Trichostrongylus colubriformis in sheep in Brazil. Vet Parasitol 216:4–6. https://doi.org/10.1016/j.vetpar.2015.11.013

    Article  CAS  PubMed  Google Scholar 

  • Coltman DW, Wilson K, Pilkington JG, Stear MJ, Pemberton JM (2001) A microsatellite polymorphism in the gamma interferon gene is associated with resistance to gastrointestinal nematodes in a naturally parasitized population of Soay sheep. Parasitology 122:571–582

    Article  CAS  PubMed  Google Scholar 

  • Craig NM, Miller HRP, Smith WD, Knight PA (2007) Cytokine expression in naïve and previously infected lambs after challenge with Teladorsagia circumcincta. Vet Immunol Immunopathol 120:47–54

    Article  CAS  PubMed  Google Scholar 

  • Crawford AM, McEwan JC (1999) Determining resistance or susceptibility of farmed animals to nematode parasites. UK Patent GB2337587

  • Daş G, Klauser S, Stehr M, Tuchscherer A, Metges CC (2020) Accuracy and precision of McMaster and Mini-FLOTAC egg counting techniques using egg-spiked faeces of chickens and two different flotation fluids. Vet Parasitol. https://doi.org/10.1016/j.vetpar.2020.109158

    Article  PubMed  Google Scholar 

  • Davies G, Stear MJ, Benothman M, Abuagob O, Kerr A, Mitchell S, Bishop SC (2006) Quantitative trait loci associated with parasitic infection in Scottish Blackface sheep. Heredity 96:252–258

    Article  CAS  PubMed  Google Scholar 

  • 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 186:337–343

    Article  PubMed  Google Scholar 

  • Dervishi E, Uriarte J, Valderrabano J, Calvo JH (2011) Structural and functional characterization of the ovine interferon gamma (IFN-γ) gene: Its role in nematode resistance in Rasa Aragonesa ewes. Vet Immunol Immunopathol 141:100–108

    Article  CAS  PubMed  Google Scholar 

  • Dominik S (2005) Quantitative trait loci for internal nematode resistance in sheep: a review. Genet Sel Evol 37:83–96

    Article  Google Scholar 

  • Emery DL, Hunt PW, Jambre LFLe (2016) Haemonchus contortus: the then and now, and where to from here? Int J Parasitol 46(12):755–769

  • Falzon LC, Menzies PI, Shakya KP, Jones-Bitton A, Vanleeuwen J, Avula J, Stewart H, Jansen JT, Taylor MA, Learmount J, Peregrine AS (2013) Anthelmintic resistance in sheep flocks in Ontario, Canada. Vet Parasitol 193(1–3):150–162

    Article  CAS  PubMed  Google Scholar 

  • Ghosh JD, Jas R, Bordoloi G (2012) Exploration of resistance/resilience against gastrointestinal nematode infection in Garole sheep. Indian J Anim Sci 82(8):818–821

    Google Scholar 

  • Gill HS, Altmann K, Cross ML, Husband AJ (2000) Induction of T helper -1 and T helper-2 immune responses during Haemonchus contortus infection in sheep. Immunology 99:458–463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gowane GR, Swarnkar CP, Misra SS, Kumar R, Kumar A, Prince LLL (2019) Genetic parameter estimates for faecal egg counts and their relationship with growth in Avikalin and Malpura sheep. Animal 13:1788–1796. https://doi.org/10.1017/S1751731118003749

    Article  CAS  PubMed  Google Scholar 

  • Gruner J, Cortet C, Sauve C, Hoste H (2004) Regulation of Teladorsagia circumcincta and Trichostrongylus colubriformis worm populations by grazing sheep with differing resistance status. Vet Res 35:91–101

  • Haehling MB, Toscano JHB, Giraldelo LA, Santos IB, Esteves SN, Benavides MV, Tholon P, Chagas ACS (2021) Is selection for resistance and resilience to Haemonchus contortus possible in Morada Nova sheep? Small Rumin Res 201https://doi.org/10.1016/j.smallrumres.2021.106447

  • Han T, Wang M, Zhang G, Han D, Li X, Liu G, Li X, Wang Z (2017) Gastrointestinal nematode infections and anthelmintic resistance in grazing sheep in the Eastern Inner Mangolia in China. Acta Parasitol 62:815–822. https://doi.org/10.1515/ap-2017-0098

    Article  CAS  PubMed  Google Scholar 

  • Harrison GBL, Pulford HD, Doolin EE, Pernthaner A, Shoemaker CB, Hein WR (2008) Antibodies to surface epitopes of the carbohydrate larval antigen CarLA are associated with passive protection in strongylid nematode challenge infections. Parasite Immunol 30:577–584

    CAS  PubMed  Google Scholar 

  • Harrison GBL, Pulford HD, Hein WR, Barber TK, Shaw RJ, McNeill M, Wakefield St J, Shoemaker CB (2003) Immune rejection of Trichostrongylus colubriformis in sheep; a possible role for intestinal mucus antibody against an L3-specific surface antigen. Parasite Immunol 25(1):45–53

    Article  CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.1186/1297-9716-42-46

    Article  PubMed  PubMed Central  Google Scholar 

  • Huntley JF, Redmond J, Welfare W, Brennan G, Jackson F, Kooyman F, Vervelde L (2001) Studies on the immunoglobulin E responses to Teladorsagia circumcincta in sheep: purification of a major high molecular weight allergen. Parasite Immunol 23:227–235

    Article  CAS  PubMed  Google Scholar 

  • Jackson F, Miller J (2006) Alternative approaches to control –Quo vadit? Vet Parasitol 139:371–384

    Article  PubMed  Google Scholar 

  • Jas R, Bordoloi G, Das S, Brahma A, Kumar D, Baidya S, Ghosh JD (2016) Comparative parasitological and immunological response of resistant Garole and sustainable Sahabadi sheep to experimentally induced haemonchosis. Int J Parasitol Res 8(3):187–190

    Google Scholar 

  • Karrow NA, Goliboski K, Stonos N, Schenkel F, Peregrine A (2014) Review: Genetics of helminth resistance in sheep. Can J Anim Sci 94(1):1–9

    Article  CAS  Google Scholar 

  • Kemper KE, Palmer DG, Liu SM, Greeff JC, Bishop SC, Karlsson LJ (2010) Reduction of faecal worm egg count, worm numbers and worm fecundity in sheep selected for worm resistance following artificial infection with Teladorsagia circumcincta and Trichostrongylus colubriformis. Vet Parasitol 171(3–4):238–246. https://doi.org/10.1016/j.vetpar.2010.04.005

  • Lacroux C, Nguyen TH, Andreoletti O, Prevot F, Grisez C, Bergeaud JP, Gruner L, Brunel JC, Francois D, Dorchies P, Jacquiet P (2006) Haemonchus contortus (Nematoda: Trichostrongylidae) infection in lambs elicits an unequivocal Th2 immune response. Vet Res 37:607–622

    Article  CAS  PubMed  Google Scholar 

  • Leathwick DM, Besier RB (2014) The management of anthelmintic resistance in grazing ruminants in Australia – Strategies and experiences. Vet Parasitol 204:44–54

    Article  CAS  PubMed  Google Scholar 

  • Li RW, Meyer MJ, Van Tassell CP, Sonstegard TS, Conner EE, Van Amburgh ME, Boisclair YR, Capuco AV (2006) Identification of estrogen responsive genes in the parenchyma and fat pad of the bovine mammary gland by microarray analysis. Physiol Genomics 27:42–53

    Article  CAS  PubMed  Google Scholar 

  • MAFF (1971) Manual of Veterinary Parasitological Laboratory Techniques, Technical Bulletin No. 18, Her Majesty's Stationery Office, Ministry of Agriculture, Fisheries and Food, London, U.K.

  • Mandal A, Yadav NK, Sharma DK, Rout PK, Roy R (2008) Transformation methods for analysis of data on faecal egg counts in sheep. Indian J Anim Sci 78:364–366

    Google Scholar 

  • Mandonnet N, Menendez-Buxadera A, Arquet R, Mahieu M, Bachand M, Aumont G (2006) Genetic variability in resistance to gastrointestinal Strongyles during early lactation in Creole goats. Anim Sci 82:283–287

    Article  Google Scholar 

  • Marshall K, Mugambi JM, Nagda S, Sonstegard TS, Van Tassell CP, 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 Genet 44:285–295. https://doi.org/10.1111/j.1365-2052.2012.02401.x

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Valladares M, Vara-Del Río MP, Cruz-Rojo MA, Rojo-Vázquez FA (2005) Genetic resistance to Teladorsagia circumcincta: IgA and parameters at slaughter in Churra sheep. Parasite Immunol 27(6):213–218

    Article  PubMed  Google Scholar 

  • Martins AC, Bergamasco PLF, Felippelli G, Tebaldi JH, Moraes MFD, Testi AJP, Lapera IM, Hoppe EGL (2017) Haemonchus contortus resistance to monepantel in sheep: fecal egg count reduction tests and randomized controlled trials. Semina Ciências Agrárias Londorina 38(1):231–238

  • McRae KM, McEwan JC, Dodds KG, Gemmell NJ (2014) Signatures of selection in sheep bred for resistance or susceptibility to gastrointestinal nematodes. BMC Genomics 15:637. https://doi.org/10.1186/1471-2164-15-637

    Article  PubMed  PubMed Central  Google Scholar 

  • Mendes JB, Cintra MCR, Nascimento LV, de Jesus RMM, Maia D, Ostrensky A, Teixeira VN, Sotomaior CS (2018) Effects of protein supplementation on resistance and resilience of lambs naturally infected with gastrointestinal parasites. Semina Ciências Agrárias 39(2):643–655 https://doi.org/10.5433/1679-0359.2018v39n2p643

  • Michael L, Bordoloi G, Pandit S, Baidya S, Joardar SN, Patra AK, Jas R (2020) Parasitological and immunological response to Haemonchus contortus infection: Comparison between resistant Garole and susceptible Sahabadi sheep. Vet Parasitol Regional Studies and Reports https://doi.org/10.1016/j.vprsr.2020.100477

  • Miller JE, Horohov DW (2006) Immunological aspects of nematode parasite control in sheep. J Anim Sci 84:124–132

    Article  Google Scholar 

  • Mphahlele M, Tsotetsi-Khambule AM, Moerane R, Komape D, Thekisoe O (2021) Anthelmintic resistance and prevalence of gastrointestinal nematodes infecting sheep in Limpop Province, South Africa. Vet World 14:302–313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muchiut SM, Fernández AS, Steffan PE, Riva E, Fiel CA (2018) Anthelmintic resistance: Management of parasite refugia for Haemonchus contortus through the replacement of resistant with susceptible populations. Vet Parasitol 254:43–48

    Article  PubMed  Google Scholar 

  • Muñoz-Guzmán MA, Cuéllar-Ordaz JA, Valdivia-Anda AG, Buendía-Jiménez JA, Alba-Hurtado F (2006) Correlation of parasitological and immunological parameters in sheep with high and low resistance to haemonchosis. Can J Anim Sci 86(3):363–371

    Article  Google Scholar 

  • Nguyen TM, Binh DV, Orskov ER (2005) Effect of foliages containing condensed tannins and on gastroin- testinal parasites. Anim Feed Sci Technol 121:77–87

    Article  CAS  Google Scholar 

  • Nimbkar C, Ghalasi PM, Swan AA, Walkden-Brown SW, Kahn LP (2003) Evaluation of growth rates and resistance to nematodes of Deccani and Bannur lambs and their crosses with Garole. Anim Sci 76:503–515

    Article  Google Scholar 

  • Onzima RB, Mukiibi R, Ampaire A, Benda KK, Kanis E (2017) Between-breed variations in resistance/resilience to gastrointestinal nematodes among indigenous goat breeds in Uganda. Trop Anim Health Prod 49(8):1763–1769. https://doi.org/10.1007/s11250-017-1390-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papadolous E, Gallidis E, Ptochos S (2012) Anthelmintic resistance in sheep in Europe: a selected review. Vet Parasitol 189(1):85–92

    Article  Google Scholar 

  • Patra G, Jas R, Ghosh JD, Borthakur SK, Paul A (2016) Single nucleotide polymorphism and expression studies of the interferon gamma gene against Haemonchus contortus in Garole and Sahabadi sheep. Asian Pac J Trop Dis 6(2):106–112

    Article  Google Scholar 

  • Peña MT, Miller JE, Horohov DW (2004) Effect of dexamethasone treatment on the immune response of Gulf Coast Native lambs to Haemonchus contortus infection. Vet Parasitol 119:223–235

    Article  PubMed  Google Scholar 

  • Periasamy K, Pichler R, Poli M, Cristel S, Cetrá B, Medus D, Basar M, Thiruvenkadan AK, Ramasamy S, Ellahi MB, 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. https://doi.org/10.1371/journal.pone.0088337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pettit JJ, Jackson F, Rocchi M, Huntley JF (2005) The relationship between responsiveness against gastrointestinal nematodes in lambs and the numbers of circulating IgE-bearing cells. Vet Parasitol 134:131–139

  • Pernthaner A, Cole SA, Morrison L, Green R, Shaw RJ, Hein WR (2006) Cytokine and antibody subclass responses in the intestinal lymph of sheep during repeated experimental infections with the nematode parasite Trichostrongylus colubriformis. Vet Immunol Immunopathol 114:135–148

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29(9):e45. https://doi.org/10.1093/nar/29.9.e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rocha RA, Bricarello PA, Silva MB, Houdijk JGM, Almeida FA, Cardia DFF, Amarante AFT (2011) Influence of protein supplementation during late pregnancy and lactation on the resistance of Santa Ines and Ile de France ewes to Haemonchus contortus. Vet Parasitol 181:229–238

    Article  CAS  PubMed  Google Scholar 

  • Saddiqi HA, Iqbal Z, Khan MN, Muhammad G (2010) Comparative resistance of sheep breeds to Haemonchus contortus in a natural pasture infection. Int J Agric Biol 12:739–773

    Google Scholar 

  • SAS (2001) SAS/STAT User’s Guide, Version 8.02. SAS Institute Inc., Cary, NC, US

  • Sayers G, Good B, Hanrahan JP, Ryan M, Sweeney T (2005) Intron 1 of the interferon gamma gene: its role in nematode resistance in Suffolk and Texel sheep breeds. Res Vet Sci 79:191–196

    Article  CAS  PubMed  Google Scholar 

  • Schalm OW, Jain NC, Carroll EJ (1986) Veterinary Haematology, 4th edn. Lea and Febiger, Philadephia

    Google Scholar 

  • 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(2–4):239–247

    Article  CAS  PubMed  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva MVB, Sonstegard TS, Hanotte O, Mugambi JM, Garcia JF, Nagda S, Gibson JP, Iraqi FA, McClintock AE, Kemp SJ, Boettcher PJ, Malek M, Van Tassell CP, Bakeret RL (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(1):63–71

    Article  CAS  PubMed  Google Scholar 

  • Soulsby EJL (1982) Helminths, arthropods and protozoa of domesticated animals. Seventh edition. The English Language Book Society and Bailliere. Tindall, London, pp 232–252

  • 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. Parasitology 129:363–369

    Article  CAS  PubMed  Google Scholar 

  • Stear MJ, Boag B, Cattadori I, Murphy L (2009) Genetic variation in resistance to mixed, predominantly Teladorsagia circumcincta nematode infections of sheep: from heritabilities to gene identification. Parasite Immunol 31:274–282

    Article  CAS  PubMed  Google Scholar 

  • Swarnkar CP, Singh D, Kumar S, Mishra AK, Arora AL (2009) Study on Malpura sheep selected for resistance to Haemonchus contortus. Indian J Anim Sci 79(6):577–581

    Google Scholar 

  • Terefe G, Lacroux C, Andreoletti O, Grisez C, Prevot F, Bergeaud JP, Penicaud J, Rouillon V, Gruner L, Brunel JC, Francois D, Bouix J, Dorchies J, Jacquiet P (2007) Immune response and resistance to Haemonchus contortus in sheep Immune response to Haemonchus contortus infection in susceptible (INRA 401) and resistant (Barbados Black Belly) breeds of lambs. Parasite Immunol 29:415–424 https://doi.org/10.1111/j.1365-3024.2007.00958.x

  • Torres-Acosta JFJ, Mendoza-de-Gives P, Aguilar-Caballero AJ, Cuellar-Ordaz JA (2012) Anthelmintic resistance in sheep farms: update of the situation in the American continent. Vet Parasitol 189(1):89–96

    Article  CAS  PubMed  Google Scholar 

  • Urquhart GM, Armour J, Duncan JL, Dunn AM, Jennings FW (1996) Veterinary Parasitology. Cambridge, Mass. Blackwell Science, United Kingdom.

  • Vanimisetti HB, Andre SL, Zajac AM, Notter DR (2004) Inheritance of fecal egg count and packed cell volume and their relationship with production traits in sheep infected with Haemonchus contortus. J Anim Sci 82:1602–1611

    Article  CAS  PubMed  Google Scholar 

  • Váradyová Z, Mravčáková D, Babják M, Bryszak M, Grešáková L, Čobanová K, Kišidayová S, Plachá I, Königová A, Cieslak A, Slusarczyk S, Pecio L, Kowalczyk M, Várady M (2018) Effects of herbal nutraceuticals and/or zinc against Haemonchus contortus in lambs experimentally infected. BMC Vet Res 14:78. https://doi.org/10.1186/s12917-018-1405-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waller PJ, Thamsborg SM (2004) Nematode control in ‘green’ ruminant production systems. Trends Parasitol 20(10):493–497

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thankfully acknowledge Late Prof. J. D. Ghosh.

Funding

The financial assistance of the Indian Council of Agricultural Research, New Delhi in conducting this study under the research project entitled “All India Network Programme on Gastrointestinal Parasitism.”

Author information

Authors and Affiliations

Authors

Contributions

Anupam Brahma: Methodology, Data curation, Investigation; Ruma Jas: Conceptualization, Project administration, Funding acquisition, Writing – original draft; Amlan Kumar Patra: Data analysis, Formal analysis, Writing – review & editing; Surajit Baidya: Resource; Soumitra Pandit: Data curation; Subhas Chandra Mandal: Visualization; Dipak Banerjee: Formal analysis, Data Curation; Kinsuk Das: Methodology, Investigation. All authors approved the final version of this manuscript.

Corresponding author

Correspondence to Ruma Jas.

Ethics declarations

Ethical approval

The entire experimental design and protocol for the present work for animal caring were approved by the Institutional Animal Ethical Committee of the West Bengal University of Animal and Fishery Sciences, Kolkata (763/GO/Re/SL/03/CPCSEA) approved by the Committee for the Purpose of Control and Supervision of Experiments on Animals (CPCSEA) under the Ministry of Fisheries, Animal Husbandry and Dairying; Government of India.

Competing interest

Authors declare that there are no competing financial interests and personal relationships that could inappropriately influence the present research work.

Consent for publication

Not applicable.

Consent to participate

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 710 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brahma, A., Jas, R., Patra, A.K. et al. Characterization of interferon gamma gene in relation to immunological responses in Haemonchus contortus resistant and susceptible Garole sheep. Vet Res Commun 47, 599–614 (2023). https://doi.org/10.1007/s11259-022-10015-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11259-022-10015-8

Keywords

Navigation