Skip to main content
Log in

Polymorphism detection of promoter region of IFN-\(\gamma \) and IL-2 genes and their association with productive traits in Mazandaran native breeder fowls

  • Research Article
  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

To identify polymorphism in interferon gamma (IFN-\(\upgamma \)) and interleukin-2 (IL-2) genes, blood samples were collected from 380 breeder hens of the Mazandaran native fowls breeding station. DNA extraction was performed through a modified salting-out method and fragments of 670 and 659 bp from the promoter regions of IFN-\(\upgamma \) and IL-2 genes were amplified by using specific primers, respectively. Following genotyping in the IFN-\(\upgamma \) gene using the Tsp509I restriction enzyme, two alleles of A and G with the frequencies of 0.55 and 0.45 and three genotypes of AA, AG and GG were observed with the frequencies of 0.32, 0.46 and 0.22, respectively. For the IL-2 gene, two alleles of A and G were also detected using the MnlI restriction enzyme with the frequencies of 0.58 and 0.42 and three genotypes of AA, AG and GG with the frequencies of 0.33, 0.50 and 0.17, respectively. Statistical analysis revealed significant associations between IL-2 gene single-nucleotide polymorphism and productive traits including the average egg weight (EW) at 345–375 days of age, egg number (EN) at 345–375 days of age and body weight (BW) at 8 weeks of age traits (\(P{<}0.05\)). Further, in a mean comparison analysis, there were also significant differences between different genotypes of the IL-2 gene in average EW at 28 and 30 weeks of age, in which AG genotypes showed higher performance. Additionally, for the IFN-\(\upgamma \) gene, a significant difference was found between the genotypes in average EW at 28 weeks of age trait. Therefore, it can be concluded that the above-mentioned polymorphisms could be considered as the pivotal genetic makers to improve Mazandaran native fowl breeding programmes to achieve the optimum performance in productive traits more efficiently.

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

Similar content being viewed by others

References

  • Ahmed A. 2010 Associations of polymorphisms in four immune-related genes with antibody kinetics and body weight in chickens. Asian-Australas. J. Anim. Sci. 23, 1089–1095.

    Article  CAS  Google Scholar 

  • Alluwaimi A., Leutenegger C., Farver T., Rossitto P., Smith W. and Cullor J. 2003 The cytokine markers in Staphylococcus aureus mastitis of bovine mammary gland. J. Vet. Med. B Infect. Dis. Vet. Public Health 50, 105–111.

    Article  CAS  PubMed  Google Scholar 

  • Barua A. and Yoshimura Y. 1999 Effects of aging and sex steroids on the localization of T cell subsets in the ovary of chicken, Gallus domesticus. Gen. Comp. Endocrinol. 114, 28–35.

    Article  CAS  PubMed  Google Scholar 

  • Benyo D., Haibel G., Laufman H. P. and Pate J. L. 1991 Expression of major histocompatibility complex antigens on the bovine corpus luteum during the estrous cycle, luteolysis and early pregnancy. Biol. Reprod. 45, 229–234.

    Article  CAS  PubMed  Google Scholar 

  • Burchill M. A., Yang J., Vang K. B. and Farrar M. A. 2007 Interleukin-2 receptor signaling in regulatory T cell development and homeostasis. Immunol. Lett. 114, 1–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheema M., Qureshi M. and Havenstein G. 2003 A comparison of the immune response of a 2001 commercial broiler with a 1957 random bred broiler strain when fed representative 1957 and 2001 broiler diets. Poult. Sci. 82, 1519–1529.

    Article  CAS  PubMed  Google Scholar 

  • Choi K. D. and Lillehoj H. S. 2000 Role of chicken IL-2 on \(\upgamma \delta \) T-cells and Eimeria acervulina-induced changes in intestinal IL-2 mRNA expression and \(\upgamma \delta \) T-cells. Vet. Immunol. Immunopathol. 73, 309–321.

    Article  CAS  PubMed  Google Scholar 

  • Clarkson R. W., Wayland M. T., Lee J., Freeman T. and Watson C. J. 2003 Gene expression profiling of mammary gland development reveals putative roles for death receptors and immune mediators in post-lactational regression. Breast Cancer Res. 6, R92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coussens P. M., Verman N., Coussens M. A., Elftman M. D. and McNulty A. M. 2004 Cytokine gene expression in peripheral blood mononuclear cells and tissues of cattle infected with Mycobacterium avium subsp. paratuberculosis: evidence for an inherent proinflammatory gene expression pattern. Infect. Immun. 72, 1409–1422.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhama K., Saminathan M., Jacob S. S., Singh M., Karthik K., Tiwari R. et al. 2015 Effect of immunomodulation and immunomodulatory agents on health with some bioactive principles, modes of action and potent biomedical applications. Int. J. Pharmacol. 11, 253–290.

    Article  CAS  Google Scholar 

  • Dimitriadis E., White C., Jones R. and Salamonsen L. 2005 Cytokines, chemokines and growth factors in endometrium related to implantation. Hum. Reprod. Update 11, 613–630.

    Article  CAS  PubMed  Google Scholar 

  • Donadoni F., Tizioto P., Meirelles S., Malago Junior W., Giglioti R., Ibelli A. et al. 2011 Identification of a SNP in the gene IL2 and its association with resistance against gastrointestinal infection by nematodes in goat. J. Anim. Sci. 89(e-suppl.); J. Dairy Sci. 94(e-suppl. 1), 280, 2011. Abstract T45. Abstracts of ADSA-ASAS Joint Annual Meeting, July 2011, New Orleans.

  • Erfaniasl Z., Hashemi A., Zarringhabaie G. E. and Farhadian M. 2015 Association of the interleukin-2 gene polymorphism with egg performance in a native Turkey population. Genetika 47, 417–424.

    Article  Google Scholar 

  • Felten S., Madden K., Bellinger D., Kruszewska B., Moynihan J. and Felten D. 1997 The role of the sympathetic nervous system in the modulation of immune responses. Adv. Pharmacol. 42, 583–587.

    Article  Google Scholar 

  • Goldsby R., Kindt T., Osborne B. and Kuby J. 2003 Immunology, 5th edition. Freeman, New York.

    Google Scholar 

  • Hales D. B. 2000 Cytokines and testicular function. Cytokines Hum. Reprod. 17–42, ISBN 0-471-35242-X.

  • Heinrich J.-M., Bernheiden M., Minigo G., Yang K. K., Schütt C., Männel D. N. et al. 2001 The essential role of lipopolysaccharide-binding protein in protection of mice against a peritoneal Salmonella infection involves the rapid induction of an inflammatory response. J. Immunol. 167, 1624–1628.

    Article  CAS  PubMed  Google Scholar 

  • Hellberg P., Thomsen P., Olof Janson P. and Brännström M. 1991 Leukocyte supplementation increases the luteinizing hormone-induced ovulation rate in the in vitro-perfused rat ovary. Biol. Reprod. 44, 791–797.

    Article  CAS  PubMed  Google Scholar 

  • Hu H., Wang H., Yuan B., Zhou S., Li X., Huang Y. et al. 2006 Immunoenhancement of eukaryotic expression plasmids with chicken IL-2 or IL-15 genes on H5 subtype avian influenza vaccine. Vet. Sci. China 10, 805–810.

    Google Scholar 

  • Janss L. and Bolder N. 2000 Heritabilities of and genetic relationships between salmonella resistance traits in broilers. J. Anim. Sci. 78, 2287–2291.

    Article  CAS  PubMed  Google Scholar 

  • Ji B., Sun T., Ma Z., Lu Q., Hu W., Jian Z. et al. 2015 Possible association of IFN-g Gene -316A/G SNP with humoral immune response to killed H5N1 HPAI vaccine in a red jungle fowl population. J. Interferon Cytokine Res. 11, 844–849.

    Article  CAS  Google Scholar 

  • Kaiser P. and Mariani P. 1999 Promoter sequence, exon: intron structure, and synteny of genetic location show that a chicken cytokine with T-cell proliferative activity is IL2 and not IL15. Immunogenetics 49, 26–35.

    Article  CAS  PubMed  Google Scholar 

  • Kaiser P., Wain H. M. and Rothwell L. 1998 Structure of the chicken interferon-\(\upgamma \) gene, and comparison to mammalian homologues. Gene 207, 25–32.

    Article  CAS  PubMed  Google Scholar 

  • Kaiser P., Howell J., Fife M., Sadeyen J., Salmon N., Rothwell L. et al. 2008 Integrated immunogenomics in the chicken: deciphering the immune response to identify disease resistance genes. Dev. Biol. 132, 57–66.

    CAS  Google Scholar 

  • Kayisli U. A., Mahutte N. G. and Arici A. 2002 Uterine chemokines in reproductive physiology and pathology. Am. J. Reprod. Immunol. 47, 213–221.

    Article  PubMed  Google Scholar 

  • Knight P. G. and Glister C. 2003 Local roles of TGF-\(\upbeta \) superfamily members in the control of ovarian follicle development. Anim. Reprod. Sci. 78, 165–183.

    Article  CAS  PubMed  Google Scholar 

  • Kogut M., Rothwell L. and Kaiser P. 2002 Differential effects of age on chicken heterophile functional activation by recombinant chicken interleukin-2. Dev. Comp. Immunol. 26, 817–830.

    Article  CAS  PubMed  Google Scholar 

  • Kogut M. H., Rothwell L. and Kaiser P. 2003 Priming by recombinant chicken interleukin-2 induces selective expression of IL-8 and IL-18 mRNA in chicken heterophils during receptor-mediated phagocytosis of opsonized and nonopsonized Salmonella enterica serovar enteritidis. Mol. Immunol. 40, 603–610.

    Article  CAS  PubMed  Google Scholar 

  • Lambrecht B., Gonze M., Meulemans G. and van denBerg T. P. 2004 Assessment of the cell-mediated immune response in chickens by detection of chicken interferon-\(\upgamma \) in response to mitogen and recall Newcastle disease viral antigen stimulation. Avian Pathol. 33, 343–350.

    Article  CAS  PubMed  Google Scholar 

  • Lamont S., Kaiser M. and Liu W. 2002 Candidate genes for resistance to Salmonella enteritidis colonization in chickens as detected in a novel genetic cross. Vet. Immunol. Immunopathol. 87, 423–428.

    Article  CAS  PubMed  Google Scholar 

  • Li G., Lillehoj E. P. and Lillehoj H. S. 2002 Interleukin-2 production in SC and TK chickens infected with Eimeria tenella. Avian Dis. 46, 2–9.

    Article  PubMed  Google Scholar 

  • Lühken G., Stamm I., Menge C. and Erhardt G. 2005 Functional analysis of a single nucleotide polymorphism in a potential binding site for GATA transcription factors in the ovine interleukin 2 gene. Vet. Immunol. Immunopathol. 107, 51–56.

    Article  CAS  PubMed  Google Scholar 

  • Lühken G., Gauly M., Kaufmann F. and Erhardt G. 2011 Association study in naturally infected helminth layers shows evidence for influence of interferon-gamma gene variants on Ascaridia galli worm burden. Vet. Res. 42, 84.

    Article  PubMed  PubMed Central  Google Scholar 

  • Miyamoto T., Min W. and Lillehoj H. S. 2002 Kinetics of interleukin-2 production in chickens infected with Eimeria tenella. Comp. Immunol. Microbiol. Infect. Dis. 25, 149–158.

    Article  PubMed  Google Scholar 

  • Nagarajan U. M., Sikes J., Prantner D., Andrews C. W., Frazer L., Goodwin A. et al. 2011 MyD88 deficiency leads to decreased NK cell gamma interferon production and T cell recruitment during Chlamydia muridarum genital tract infection, but a predominant Th1 response and enhanced monocytic inflammation are associated with infection resolution. Infect. Immun. 79, 486–498.

    Article  CAS  PubMed  Google Scholar 

  • Neuvians T., Schams D., Berisha B. and Pfaffl M. 2004 Involvement of pro-inflammatory cytokines, mediators of inflammation, and basic fibroblast growth factor in prostaglandin F2\(\upalpha \)-induced luteolysis in bovine corpus luteum. Biol. Reprod. 70, 473–480.

    Article  CAS  PubMed  Google Scholar 

  • Nishimura R., Bowolaksono A., Acosta T. J., Murakami S., Piotrowska K., Skarzynski D. J. et al. 2004 Possible role of interleukin-1 in the regulation of bovine corpus luteum throughout the luteal phase. Biol. Reprod. 71, 1688–1693.

    Article  CAS  PubMed  Google Scholar 

  • Parish C. R. and O’neill E. R. 1997 Dependence of the adaptive immune response on innate immunity: some questions answered but new paradoxes emerge. Immunol. Cell Biol. 75, 543–552.

    Article  Google Scholar 

  • Park J. H., Sung H. W., Yoon B. I. and Kwon H. M. 2009 Protection of chicken against very virulent IBDV provided by in ovo priming with DNA vaccine and boosting with killed vaccine and the adjuvant effects of plasmid-encoded chicken interleukin-2 and interferon-\(\upgamma \). J. Vet. Sci. 10, 131–139.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pasanen S., Ylikomi T., Palojoki E., Syvälä H., Pelto-Huikko M. and Tuohimaa P. 1998 Progesterone receptor in chicken bursa of Fabricius and thymus: evidence for expression in B-lymphocytes. Mol. Cell. Endocrinol. 141, 119–128.

    Article  CAS  PubMed  Google Scholar 

  • Patra G., Jas R., Ghosh J., Borthakur S. K. and Paul A. 2016 Single nucleotide polymorphism and expression studies of the interferon gamma gene and its role against Haemonchus contortus in Garole and Sahabadi sheep. Asian Pac. J. Trop. Dis. 6, 106–112.

    Article  CAS  Google Scholar 

  • Pintarič M., Gerner W. and Saalmüller A. 2008 Synergistic effects of IL-2, IL-12 and IL-18 on cytolytic activity, perforin expression and IFN-\(\upgamma \) production of porcine natural killer cells. Vet. Immunol. Immunopathol. 121, 68–82.

    Article  CAS  PubMed  Google Scholar 

  • Prakash V., Bhattacharya T. K. and Pandey O. 2010 Genetic polymorphism study of promoter region of interleukin-2 gene and its association with certain milk associated traits in Indian crossbred cattle. J. Mol. Genet. 2, 15–19.

    Article  Google Scholar 

  • Rahman A., Snibson K. J., Lee C. S. and Meeusen E. N. 2004 Effects of implantation and early pregnancy on the expression of cytokines and vascular surface molecules in the sheep endometrium. J. Reprod. Immunol. 64, 45–58.

    Article  CAS  PubMed  Google Scholar 

  • Reemers S. S., Van Haarlem D. A., Sijts A. J., Vervelde L. and Jansen C. A. 2012 Identification of novel avian influenza virus derived CD8+ T-cell epitopes. PLoS One 7, e31953.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roussan D., Haddad R. and Khawaldeh G. 2008 Molecular survey of avian respiratory pathogens in commercial broiler chicken flocks with respiratory diseases in Jordan. Poult. Sci. 87, 444–448.

    Article  CAS  PubMed  Google Scholar 

  • Savan R., Ravichandran S., Collins J. R., Sakai M. and Young H. A. 2009 Structural conservation of interferon gamma among vertebrates. Cytokine Growth Factor Rev. 20, 115–124.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sebastiani G., Blais V., Sancho V., Vogel S. N., Stevenson M. M., Gros P. et al. 2002 Host immune response to Salmonella enterica serovar Typhimurium infection in mice derived from wild strains. Infect. Immun. 70, 1997–2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shah M. A. A., Song X., Xu L., Yan R., Song H., Ruirui Z. et al. 2010 The DNA-induced protective immunity with chicken interferon gamma against poultry coccidiosis. Parasitol. Res. 107, 747–750.

    Article  PubMed  Google Scholar 

  • Sharma R. K. and Gandhi E. 2011 Effect of interleukin-2 on steroidogenesis of goat ovary. J. Immunol. Immunopathol. 13, 20–24.

    Google Scholar 

  • Singh S., Pei J. and Collisson E. 2014 Viral specific CD8 + T lymphocyte immunity provides protection against heterotypic stains of avian influenza viruses and avian coronaviruses. Int. Trends. Immun. 2, 36–46.

    CAS  Google Scholar 

  • Soboloff J., Desilets M. and Tsang K. 1995 Influence of tumor necrosis factor alpha on intracellular \(\text{ Ca }^{2+}\) in hen granulosa cells in vitro during follicular development. Biol. Reprod. 53, 546–552.

    Article  CAS  PubMed  Google Scholar 

  • Soller M. and Andersson L. 1998 Genomic approaches to the improvement of disease resistance in farm animals. Rev. Sci. Tech. 17, 329–345.

    Article  CAS  PubMed  Google Scholar 

  • Sundaresan N., Anish D., Sastry K., Saxena V., Mohan J. and Ahmed K. 2007 Cytokines in reproductive remodeling of molting White Leghorn hens. J. Reprod. Immunol. 73, 39–50.

    Article  CAS  PubMed  Google Scholar 

  • Swaggerty C. L., Kogut M. H., Ferro P. J., Rothwell L., Pevzner I. Y. and Kaiser P. 2004 Differential cytokine mRNA expression in heterophils isolated from Salmonella-resistant and-susceptible chickens. Immunology 113, 139–148.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tohidi R., Idris I. B., Panandam J. M. and Bejo M. H. 2012 The effects of polymorphisms in IL-2, IFN-\(\upgamma \), TGF-\(\upbeta \)2, IgL, TLR-4, MD-2, and iNOS genes on resistance to Salmonella Enteritidis in indigenous chickens. Avian Pathol. 41, 605–612.

    Article  CAS  PubMed  Google Scholar 

  • Van der Poel J. and Parmentier H. 2003 Genetic bases for resistance and immunity to Avian Disease. S. l.: S. n. (Annual Report, contributing project to NE-1016) - 4 p, (https://www.nimss.org/projects/view/SAES/3474).

  • Vervelde L., Matthijs M., Van Haarlem D., de Wit J. and Jansen C. 2013 Rapid NK-cell activation in chicken after infection with infectious bronchitis virus M41. Vet. Immunol. Immunopathol. 151, 337–341.

    Article  CAS  PubMed  Google Scholar 

  • Vetrivel S. and Chandrakumarmangalam S. 2013 The role of poultry industry in Indian Economy. Rev. Bras. Cienc. Avic. 15, 287–293.

    Article  Google Scholar 

  • Withanage G., Sasai K., Fukata T., Miyamoto T., Lillehoj H. and Baba E. 2003 Increased lymphocyte subpopulations and macrophages in the ovaries and oviducts of laying hens infected with Salmonella enterica serovar Enteritidis. Avian Pathol. 32, 583–590.

    Article  CAS  PubMed  Google Scholar 

  • Withanage G., Kaiser P., Wigley P., Powers C., Mastroeni P., Brooks H. et al. 2004 Rapid expression of chemokines and proinflammatory cytokines in newly hatched chickens infected with Salmonella enterica serovar Typhimurium. Infect. Immun. 72, 2152–2159.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Q., Song X., Xu L., Yan R., Shah M. A. A. and Li X. 2008 Vaccination of chickens with a chimeric DNA vaccine encoding Eimeria tenella TA4 and chicken IL-2 induces protective immunity against coccidiosis. Vet. Parasitol. 156, 319–323.

    Article  CAS  PubMed  Google Scholar 

  • Yakubu A., Salako A., Donato M., Takeet M., Peters S., Wheto M. et al. 2016 Interleukin-2 (IL-2) gene polymorphism and association with heat tolerance in Nigerian goats. Small Rumin. Res. 141, 127–134.

    Article  Google Scholar 

  • Ye X., Avendano S., Dekkers J. and Lamont S. 2006 Association of twelve immune-related genes with performance of three broiler lines in two different hygiene environments. Poult. Sci. 85, 1555–1569.

    Article  CAS  PubMed  Google Scholar 

  • Zettergren L. D. and Cutlan R. T. 1992 Immunoglobulin-containing cells in chick embryo urogenital tissues: a new site for early B lineage cells in endothermic vertebrates. J. Exp. Zool. Part A 262, 458–461.

    Article  CAS  Google Scholar 

  • Zhang D., Zhao H., Luo Y. and Han J. 2011 Characterization of haplotype diversity defined by discontinuous insertions/deletions within the intron 2 of interleukin 2 in different domestic chicken populations. J. Biol. Sci. 11, 261–267.

    Article  CAS  Google Scholar 

  • Zhao K., He W., Gao W., Lu H., Han T., Li J. et al. 2011 Orf virus DNA vaccines expressing ORFV 011 and ORFV 059 chimeric protein enhances immunogenicity. J. Virol. 8, 562.

    Article  CAS  Google Scholar 

  • Zhou H., Buitenhuis A., Weigend S. and Lamont S. 2001 Candidate gene promoter polymorphisms and antibody response kinetics in chickens: interferon-\(\upgamma \), interleukin-2, and immunoglobulin light chain. Poult. Sci. 80, 1679–1689.

    Article  CAS  PubMed  Google Scholar 

  • Zhou H., Lillehoj H. S. and Lamont S. J. 2002 Associations of interferon-\(\upgamma \) genotype and protein level with antibody response kinetics in chickens. Avian Dis. 46, 869–876.

    Article  CAS  PubMed  Google Scholar 

  • Zhou H., Li H. and Lamont S. 2003 Genetic markers associated with antibody response kinetics in adult chickens. Poult. Sci. 82, 699–708.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mojtaba Najafi.

Additional information

Corresponding editor: Silvia Garagna

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kazemi, H., Najafi, M., Ghasemian, E. et al. Polymorphism detection of promoter region of IFN-\(\gamma \) and IL-2 genes and their association with productive traits in Mazandaran native breeder fowls. J Genet 97, 843–851 (2018). https://doi.org/10.1007/s12041-018-0981-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12041-018-0981-1

Keywords

Navigation