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Research article

References

  1. Zekarias B, Ter Huurne AA, Landman WJ, Rebel JM, Pol JM, Gruys E. 2002. Immunological basis of differences in disease resistance in the chicken. Vet. Res. 33: 109-125.
    Pubmed CrossRef
  2. Adams LG, Schutta C. 2010. Natural resistance against brucellosis: a review. Open Vet. Sci. J. 4: 61-71.
    CrossRef
  3. Chen P, Shakhnovich E. 2010. Thermal adaptation of viruses and bacteria. Biophys. J. 98: 1109-1118.
    Pubmed PMC CrossRef
  4. Butcher G, Miles R. 1991. The avian immune system. VM74. Available from http://edis.ifas.ufl.edu/pdffiles/VM/VM01600.pdf. Accessed 2015.
  5. Gray D, Marais M, Maloney S. 2013. A review of the physiology of fever in birds. J. Comp. Physiol. B 183: 297-312.
    Pubmed CrossRef
  6. Qureshi N, Perera PY, Shen J, Zhang G, Lenschat A, Splitter G, et al. 2003. The proteasome as a lipopolysaccharide-binding protein in macrophages: differential effects of proteasome inhibition on lipopolysaccharide-induced signaling events. J. Immunol. 171: 1515-1525.
    Pubmed CrossRef
  7. Cullum A, Bennet A, Lenski R. 2001. Evolutionary adaptation to temperature. IX. Preadaptation to novel stressful environments of Escherichia coli adapted to high temperature. Evolution 55: 2194-2202.
    Pubmed CrossRef
  8. Travisano M, Lenski R. 1996. Long term experimental evolution in E. coli. IV. Targets of selection and specificity of adaptation. Genetics 143: 15-26.
    Pubmed PMC
  9. Beug H, Kirchbach A, Döderlein G, Conscience JF, Graf T. 1979. Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation. Cell 18: 375-390.
    CrossRef
  10. Lee JJ, Kim DH, Lee HJ, Min W, Rhee M, Kim S, et al. 2013. Phellinus baumii extract influences pathogenesis of Brucella abortus by disrupting the phagocytic and intracellular trafficking pathway. J. Appl. Microbiol. 114: 329-338.
    Pubmed CrossRef
  11. Higa F, Kusano N, Tateyama M. 1998. Simplified quantitative assay system for measuring activities of drugs against intracellular Legionella pneumophila. J. Clin. Microbiol. 36:1392-1398.
    Pubmed PMC
  12. Lee JJ, Kim DH, Kim DG, Lee HJ, Min W, Rhee MH, et al. 2013. Toll-like receptor 4-linked Janus kinase 2 signaling contributes to internalization of Brucella abortus by macrophages. Infect. Immun. 81: 2448-2458.
    Pubmed PMC CrossRef
  13. Braukmann M, Methner U, Berndt A. 2015. Immune reaction and survivability of Salmonella Typhimurium and Salmonella Infantis i s after infection of p rimary a vian m acroph ages. PLoS One 10: e0122540.
    Pubmed PMC CrossRef
  14. Hong YH, Lillehoj HS, Lee SH, Dalloul RA, Lillehoj EP. 2006. Analysis of chicken cytokine and chemokine gene expression following Eimeria acervulina and Eimeria tenella infections. Vet. Immunol. Immunopathol. 114: 209-223.
    Pubmed CrossRef
  15. Kapczynski D, Jiang HJ, Kogut MH. 2014. Characterization of cytokine expression induced by avian influenza virus infection with real-time RT-PCR. Methods Mol. Biol. 1161:217-233.
    Pubmed CrossRef
  16. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data u sing r eal-time q uantitative PCR a nd t h e 2-ΔΔCt method. Methods 25: 402-408.
    Pubmed CrossRef
  17. Adamu NB, Adamu SG, Jajere MS. 2014. Serological survey of brucellosis in slaughtered local chickens, guinea fowls, ducks and turkey in North-Eastern Nigeria. Int. J. Poult. Sci. 13: 340-342.
    CrossRef
  18. Detilleux DG, Cheville NF, Deyoe BL. 1997. Pathogenesis of Brucella abortus in chicken embryos. Vet. Pathol. 25: 138-146.
    Pubmed CrossRef
  19. Abbas B, Talei A. 2010. Isolation, identification and biotyping of Brucella spp. from milk product of Basrah Province. Bas. J. Vet. Res. 9: 152-162.
  20. Zeldovich KB, Chen P, Shakhnovich E. 2007. Protein stability imposes limits on organism complexicity and speed of molecular evolution. Proc. Natl. Acad. Sci. USA 104: 1615216157.
    Pubmed PMC CrossRef
  21. Dyson HJ, Wright PE. 2005. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol 6: 197-208.
    Pubmed CrossRef
  22. Uversky VN. 2002. Natively unfolded proteins: a point where biology waits for physics. Protein Sci. 11: 739-756.
    Pubmed PMC CrossRef
  23. Bloom JD, Raval A, Wilke CO. 2007. Thermodynamics of neutral protein evolution. Genetics 175: 255-266.
    Pubmed PMC CrossRef
  24. Taverna DM, Goldstein RA. 2002. Why are proteins marginally stable? Proteins 46: 105-109.
    Pubmed CrossRef
  25. Leuenberger P, Ganscha S, Kahraman A, Cappelletti V, Boersema PJ, von Mering C, et al. 2017. Cell-wide analysis of protein thermal unfolding reveals determinants of thermostability. Science 355: eaai7825.
  26. Kim W, Jeong J, Park A, Kim S, Min W, Kim D, et al. 2014. Downregulation of chicken interleukin-17 receptor A during Eimeria infection. Infect. Immun. 82: 3845-3854.
    Pubmed PMC CrossRef
  27. Reyes AW, Arayan LT, Simborio HL, Hop HT, Min W, Lee HJ, et al. 2016. Dextran sulfate sodium upregulates MAPK signaling for the uptake and subsequent intracellular survival of Brucella abortus in murine macrophages. Microb. Pathog. 91: 68-73.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(10): 1837-1843

Published online October 28, 2017 https://doi.org/10.4014/jmb.1705.05061

Copyright © The Korean Society for Microbiology and Biotechnology.

The Bactericidal Effect of High Temperature Is an Essential Resistance Mechanism of Chicken Macrophage against Brucella abortus Infection

Lauren Togonon Arayan 1, Alisha Wehdnesday Bernardo Reyes 1, Huynh Tan Hop 1, Huy Tran Xuan 1, Eun Jin Baek 1, Wongi Min 1 and Suk Kim 1*

Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University, Jinju 52828, Republic of Korea

Received: May 23, 2017; Accepted: August 16, 2017

Abstract

Knowledge of avian host responses to brucellosis is critical to understanding how birds resist
this infection; however, this mechanism is not well established. On the other hand,
temperature has a major involvement in the physiology of living organisms, and cell death
induced by heat is attributed to protein denaturation. This study demonstrates the direct
bactericidal effect of a high temperature (41ºC) on Brucella abortus that resulted in the gradual
reduction of intracellular bacteria and inhibited bacterial growth within avian macrophage
HD11 in an increasing period of time. On the other hand, this study also revealed that high
temperature does not affect the rate of bacterial uptake, as confirmed by the bacterial
adherence assay. No significant difference was observed in the expression of target genes
between infected and uninfected cells for both temperatures. This study suggests the
susceptibility of B. abortus to bacterial death under a high temperature with an increased
period of incubation, leading to suppression of bacterial growth.

Keywords: B. abortus, avian macrophage, bactericidal effect, body temperature

References

  1. Zekarias B, Ter Huurne AA, Landman WJ, Rebel JM, Pol JM, Gruys E. 2002. Immunological basis of differences in disease resistance in the chicken. Vet. Res. 33: 109-125.
    Pubmed CrossRef
  2. Adams LG, Schutta C. 2010. Natural resistance against brucellosis: a review. Open Vet. Sci. J. 4: 61-71.
    CrossRef
  3. Chen P, Shakhnovich E. 2010. Thermal adaptation of viruses and bacteria. Biophys. J. 98: 1109-1118.
    Pubmed KoreaMed CrossRef
  4. Butcher G, Miles R. 1991. The avian immune system. VM74. Available from http://edis.ifas.ufl.edu/pdffiles/VM/VM01600.pdf. Accessed 2015.
  5. Gray D, Marais M, Maloney S. 2013. A review of the physiology of fever in birds. J. Comp. Physiol. B 183: 297-312.
    Pubmed CrossRef
  6. Qureshi N, Perera PY, Shen J, Zhang G, Lenschat A, Splitter G, et al. 2003. The proteasome as a lipopolysaccharide-binding protein in macrophages: differential effects of proteasome inhibition on lipopolysaccharide-induced signaling events. J. Immunol. 171: 1515-1525.
    Pubmed CrossRef
  7. Cullum A, Bennet A, Lenski R. 2001. Evolutionary adaptation to temperature. IX. Preadaptation to novel stressful environments of Escherichia coli adapted to high temperature. Evolution 55: 2194-2202.
    Pubmed CrossRef
  8. Travisano M, Lenski R. 1996. Long term experimental evolution in E. coli. IV. Targets of selection and specificity of adaptation. Genetics 143: 15-26.
    Pubmed KoreaMed
  9. Beug H, Kirchbach A, Döderlein G, Conscience JF, Graf T. 1979. Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation. Cell 18: 375-390.
    CrossRef
  10. Lee JJ, Kim DH, Lee HJ, Min W, Rhee M, Kim S, et al. 2013. Phellinus baumii extract influences pathogenesis of Brucella abortus by disrupting the phagocytic and intracellular trafficking pathway. J. Appl. Microbiol. 114: 329-338.
    Pubmed CrossRef
  11. Higa F, Kusano N, Tateyama M. 1998. Simplified quantitative assay system for measuring activities of drugs against intracellular Legionella pneumophila. J. Clin. Microbiol. 36:1392-1398.
    Pubmed KoreaMed
  12. Lee JJ, Kim DH, Kim DG, Lee HJ, Min W, Rhee MH, et al. 2013. Toll-like receptor 4-linked Janus kinase 2 signaling contributes to internalization of Brucella abortus by macrophages. Infect. Immun. 81: 2448-2458.
    Pubmed KoreaMed CrossRef
  13. Braukmann M, Methner U, Berndt A. 2015. Immune reaction and survivability of Salmonella Typhimurium and Salmonella Infantis i s after infection of p rimary a vian m acroph ages. PLoS One 10: e0122540.
    Pubmed KoreaMed CrossRef
  14. Hong YH, Lillehoj HS, Lee SH, Dalloul RA, Lillehoj EP. 2006. Analysis of chicken cytokine and chemokine gene expression following Eimeria acervulina and Eimeria tenella infections. Vet. Immunol. Immunopathol. 114: 209-223.
    Pubmed CrossRef
  15. Kapczynski D, Jiang HJ, Kogut MH. 2014. Characterization of cytokine expression induced by avian influenza virus infection with real-time RT-PCR. Methods Mol. Biol. 1161:217-233.
    Pubmed CrossRef
  16. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data u sing r eal-time q uantitative PCR a nd t h e 2-ΔΔCt method. Methods 25: 402-408.
    Pubmed CrossRef
  17. Adamu NB, Adamu SG, Jajere MS. 2014. Serological survey of brucellosis in slaughtered local chickens, guinea fowls, ducks and turkey in North-Eastern Nigeria. Int. J. Poult. Sci. 13: 340-342.
    CrossRef
  18. Detilleux DG, Cheville NF, Deyoe BL. 1997. Pathogenesis of Brucella abortus in chicken embryos. Vet. Pathol. 25: 138-146.
    Pubmed CrossRef
  19. Abbas B, Talei A. 2010. Isolation, identification and biotyping of Brucella spp. from milk product of Basrah Province. Bas. J. Vet. Res. 9: 152-162.
  20. Zeldovich KB, Chen P, Shakhnovich E. 2007. Protein stability imposes limits on organism complexicity and speed of molecular evolution. Proc. Natl. Acad. Sci. USA 104: 1615216157.
    Pubmed KoreaMed CrossRef
  21. Dyson HJ, Wright PE. 2005. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol 6: 197-208.
    Pubmed CrossRef
  22. Uversky VN. 2002. Natively unfolded proteins: a point where biology waits for physics. Protein Sci. 11: 739-756.
    Pubmed KoreaMed CrossRef
  23. Bloom JD, Raval A, Wilke CO. 2007. Thermodynamics of neutral protein evolution. Genetics 175: 255-266.
    Pubmed KoreaMed CrossRef
  24. Taverna DM, Goldstein RA. 2002. Why are proteins marginally stable? Proteins 46: 105-109.
    Pubmed CrossRef
  25. Leuenberger P, Ganscha S, Kahraman A, Cappelletti V, Boersema PJ, von Mering C, et al. 2017. Cell-wide analysis of protein thermal unfolding reveals determinants of thermostability. Science 355: eaai7825.
  26. Kim W, Jeong J, Park A, Kim S, Min W, Kim D, et al. 2014. Downregulation of chicken interleukin-17 receptor A during Eimeria infection. Infect. Immun. 82: 3845-3854.
    Pubmed KoreaMed CrossRef
  27. Reyes AW, Arayan LT, Simborio HL, Hop HT, Min W, Lee HJ, et al. 2016. Dextran sulfate sodium upregulates MAPK signaling for the uptake and subsequent intracellular survival of Brucella abortus in murine macrophages. Microb. Pathog. 91: 68-73.
    Pubmed CrossRef