Skip to main content

Advertisement

SpringerLink
Log in

Cytokine responses of Holstein and Sahiwal zebu derived monocytes after mycobacterial infection

  • Original Research
  • Published:
Tropical Animal Health and Production Aims and scope Submit manuscript

Abstract

Recently, we found that Holstein cattle (Bos taurus taurus) displayed higher skin test prevalence and disease severity compared to zebu (Bos taurus indicus) herd-mates kept under identical husbandry conditions in Ethiopia. To determine whether these susceptibility differences were patent at the level of the innate immune system, we infected monocytes from naïve Holstein or Sahiwal zebu cattle with either live virulent Mycobacterium tuberculosis or Mycobacterium bovis. The cytokine profile following infection was compared between the two breeds by measuring IL-1α, IL-6, IL-10, IL-12 and TNF-α as well as nitric oxide in culture supernatants. Our results suggested subtle differences in the cytokine profile because only infection-induced IL-6 production was significantly increased in monocytes from the more susceptible Holstein cattle.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aldwell, F.E., Wedlock, D.N., Buddle, B.M.. 1996. Bacterial metabolism, cytokine mRNA transcription and viability of bovine alveolar macrophages infected with Mycobacterium bovis BCG or virulent M. bovis. Immunology and Cell Biology 74, 45–51.

    Article  PubMed  CAS  Google Scholar 

  • Ameni, G., Aseffa, A., Engers, H., Young, D., Gordon, S., Hewinson, G., Vordermeier, M. 2007. High prevalence and increased severity of pathology of bovine tuberculosis in Holsteins compared to zebu breeds under field cattle husbandry in central Ethiopia. Clinical and Vaccine Immunolology, 14, 1356–1361.

    Article  CAS  Google Scholar 

  • Ameni, G., Hewinson, G., Aseffa, A., Young, D., Vordermeier, M. 2008. Appraisal of interpretation criteria for the comparative intradermal tuberculin test for diagnosis of tuberculosis in cattle in central Ethiopia. Clinical and Vaccine Immunolology, 15, 1272–1276.

    Article  CAS  Google Scholar 

  • Amirzargar, A.A., Naroueynejad, M., Khosravi, F., Dianat, S., Rezaei, N., Mytilineos, J., Nikbin, B. 2008. Cytokine single nucleotide polymorphisms in Iranian populations. European Cytokine Network, 19, 104–112.

    PubMed  CAS  Google Scholar 

  • Bakheit, M.A., Latif, A.A. 2002. The innate resistance of Kenana cattle to tropical theileriosis (Theileria annulata infection) in the Sudan. Annals of the New York Academy of Science, 969, 159–163.

    Article  CAS  Google Scholar 

  • Berg, S., Firdessa, R., Habtamu, M., Gadisa, E., Mengistu, A., Yamuah, L., Ameni, G., Vordermeier, M., Robertson, B.D., Smith, N.H., Engers, H., Young, D., Hewinson, R.G., Aseffa, A., Gordon, S.V. 2009. The burden of mycobacterial disease in Ethiopian cattle: implications for public health. PLoS ONE 4, e5068.

    Article  PubMed  Google Scholar 

  • Carmichael, J. 1939. Bovine tuberculosis in the tropics, with special reference to Uganda, part 1. Journal of Comparative Pathology and Therapy, 52, 322–335.

    Google Scholar 

  • Coad, M., Clifford, D., Rhodes, S.G., Hewinson, R.G., Vordermeier, H.M., Whelan, A.O. 2010. Repeat tuberculin skin testing leads to desensitisation in naturally infected tuberculous cattle which is associated with elevated interleukin-10 and decreased interleukin-1 beta responses. Veterinary Research 41, 14.

    Article  PubMed  Google Scholar 

  • Correia, J.W., Freitas, M.V., Queiroz, J.A., PereiraPerrin, M., Cavadas, B. 2009. Interleukin-6 blood levels in sensitive and multiresistant tuberculosis. Infection 37, 138–141.

    Article  PubMed  CAS  Google Scholar 

  • de Jong, E., Suddason, T., Lord, G.M. 2010. Translational mini-review series on Th17 cells: development of mouse and human T helper 17 cells. Clinical and Experimental Immunology, 159, 148–158.

    Article  PubMed  Google Scholar 

  • Djoba Siawaya, J.F., Beyers, N., van Helden, P., Walzl, G. 2009. Differential cytokine secretion and early treatment response in patients with pulmonary tuberculosis. Clinical and Experimental Immunology, 156, 69–77.

    Article  PubMed  CAS  Google Scholar 

  • Glass, E.J., Jensen, K. 2007. Resistance and susceptibility to a protozoan parasite of cattle—gene expression differences in macrophages from different breeds of cattle. Veterinary Immunology and Immunopatholology, 120, 20–30.

    Article  CAS  Google Scholar 

  • Hall, L.J., Clare, S., Dougan, G. 2010. NK cells influence both innate and adaptive immune responses after mucosal immunization with antigen and mucosal adjuvant. Journal of Immunology, 184, 4327–4337.

    Article  CAS  Google Scholar 

  • Jensen, K., Paxton, E., Waddington, D., Talbot, R., Darghouth, M.A., Glass, E.J. 2008. Differences in the transcriptional responses induced by Theileria annulata infection in bovine monocytes derived from resistant and susceptible cattle breeds. International Journal of Parasitology, 38, 313–325.

    Article  PubMed  CAS  Google Scholar 

  • Khader, S.A., Bell, G.K., Pearl, J.E., Fountain, J.J., Rangel-Moreno, J., Cilley, G.E., Shen, F., Eaton, S.M., Gaffen, S.L., Swain, S.L., Locksley, R.M., Haynes, L., Randall, T.D., Cooper, A.M. 2007. IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nature Immunolology, 8, 369–377.

    Article  CAS  Google Scholar 

  • Ladel, C.H., Blum, C., Dreher, A., Reifenberg, K., Kopf, M., Kaufmann, S.H. 1997. Lethal tuberculosis in interleukin-6-deficient mutant mice. Infection and Immunity, 65, 4843–4849.

    PubMed  CAS  Google Scholar 

  • Larcombe, L.A., Orr, P.H., Lodge, A.M., Brown, J.S., Dembinski, I.J., Milligan, L.C., Larcombe, E.A., Martin, B.D., Nickerson, P.W. 2008. Functional gene polymorphisms in Canadian aboriginal populations with high rates of tuberculosis. Journal of Infectious Disease, 198, 1175–1179.

    Article  Google Scholar 

  • Liston, W.G., Soparkar, M.B. 1917. The susceptibility of Indian Milch cows to tuberculosis. Indian Journal of Medical Research, 5, 19–71.

    Google Scholar 

  • Naessens, J., Teale, A.J., Sileghem, M. 2002. Identification of mechanisms of natural resistance to African trypanosomiasis in cattle. Veterinary Immunology and Immunopathology, 87, 187–194.

    Article  PubMed  CAS  Google Scholar 

  • Pokkali, S., Das, S.D. 2009. Augmented chemokine levels and chemokine receptor expression on immune cells during pulmonary tuberculosis. Human Immunology, 70, 110–115.

    Article  PubMed  CAS  Google Scholar 

  • Radaeva, T.V., Kondratieva, E.V., Sosunov, V.V., Majorov, K.B., Apt, A. 2008. A human-like TB in genetically susceptible mice followed by the true dormancy in a Cornell-like model. Tuberculosis (Edinb), 88, 576–585.

    Article  CAS  Google Scholar 

  • Reed, S.G., Coler, R.N., Dalemans, W., Tan, E.V., DeLa Cruz, E.C., Basaraba, R.J., Orme, I.M., Skeiky, Y.A., Alderson, M.R., Cowgill, K.D., Prieels, J.P., Abalos, R.M., Dubois, M.C., Cohen, J., Mettens, P., Lobet, Y. 2009. Defined tuberculosis vaccine, Mtb72F/AS02A, evidence of protection in cynomolgus monkeys. Proceedings of the National Academy of Science USA, 106, 2301–2306.

    Article  CAS  Google Scholar 

  • Rhodes, S.G., Sawyer, J., Whelan, A.O., Dean, G.S., Coad, M., Ewer, K.J., Waldvogel, A.S., Zakher, A., Clifford, D.J., Hewinson, R.G., Vordermeier, H.M. 2007. Is interleukin-4delta3 splice variant expression in bovine tuberculosis a marker of protective immunity? Infection and Immunity, 75, 3006–3013.

    Article  PubMed  CAS  Google Scholar 

  • Sharma, A.K., Vanaayya, P.R., Parihar, N.S. 1985. Tuberculosis in cattle: a retrospective study based on necroscopy. Indian Journal of Veterinary Pathology, 9, 17–18.

    Google Scholar 

  • Soparkar, M.B. 1927. The relative susceptibility of Indian Milch cattle of various breeds to tuberculosis. Indian Journal of Medical Research, 8, 755–779.

    Google Scholar 

  • Stern, J.N., Keskin, D.B., Romero, V., Zuniga, J., Encinales, L., Li, C., Awad, C., Yunis, E.J. 2009. Molecular signatures distinguishing active from latent tuberculosis in peripheral blood mononuclear cells, after in vitro antigenic stimulation with purified protein derivative of tuberculin (PPD) or Candida: a preliminary report. ImmunologyResearch, 45, 1–12.

    CAS  Google Scholar 

  • Tsikas, D. 2007. Analysis of nitrite and nitrate in biological fluids by assays based on the Griess reaction: appraisal of the Griess reaction in the L-arginine/nitric oxide area of research. Journal of Chromatography B, 851, 51–70

    Article  CAS  Google Scholar 

  • Vordermeier, H.M., Villarreal-Ramos, B., Cockle, P.J., McAulay, M., Rhodes, S.G., Thacker, T., Gilbert, S.C., McShane, H., Hill, A.V., Xing, Z., Hewinson, R.G. 2009. Viral booster vaccines improve Mycobacterium bovis BCG-induced protection against bovine tuberculosis. Infection and Immunity, 77, 3364–3373.

    Article  PubMed  CAS  Google Scholar 

  • Welsh, K.J., Abbott, A.N., Hwang, S.A., Indrigo, J., Armitige, L.Y., Blackburn, M.R., Hunter, R.L., Jr., Actor, J.K. 2008. A role for tumour necrosis factor-alpha, complement C5 and interleukin-6 in the initiation and development of the mycobacterial cord factor trehalose 6,6′-dimycolate induced granulomatous response. Microbiology, 154, 1813–1824.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr C. Garcia-Pelayo (VLA Weybridge) for providing mycobacterial stocks for the infection experiments. The work was supported by the Wellcome Trust. We also like to thank Dr Jayne Hope (Institute for Animal Health, Compton, UK) for the supply of bovine cytokines. Dr. Glass received financial support from the Biotechnology and Biological Sciences Research Council (BBSRC) through Institute Strategic Grant funding as well as Grant number 215/S15354, and the Wellcome Trust ‘Animal Health in the Developing World Initiative’ grant. [Grant number 075820/A/04/Z].

Author information

Authors and Affiliations

  1. TB Research Group, Animal Health and Veterinary Laboratories Agency, New Haw, Addlestone, Surrey, KT15 3NB, UK

    Martin Vordermeier

  2. Institute for Pathobiology, Addis Ababa University, Addis Ababa, Ethiopia

    Gobena Ameni

  3. The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Roslin, Midlothian, EH25 9RG, UK

    Elizabeth J. Glass

Authors
  1. Martin Vordermeier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gobena Ameni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elizabeth J. Glass
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Vordermeier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vordermeier, M., Ameni, G. & Glass, E.J. Cytokine responses of Holstein and Sahiwal zebu derived monocytes after mycobacterial infection. Trop Anim Health Prod 44, 651–655 (2012). https://doi.org/10.1007/s11250-011-9950-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11250-011-9950-x

Keywords

Search

Navigation