Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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The Bactericidal Effect of High Temperature Is an Essential Resistance Mechanism of Chicken Macrophage against Brucella abortus Infection

  • Arayan, Lauren Togonon (Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University) ;
  • Reyes, Alisha Wehdnesday Bernardo (Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University) ;
  • Hop, Huynh Tan (Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University) ;
  • Xuan, Huy Tran (Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University) ;
  • Baek, Eun Jin (Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University) ;
  • Min, Wongi (Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University) ;
  • Kim, Suk (Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University)
  • Received : 2017.05.23
  • Accepted : 2017.08.16
  • Published : 2017.10.28
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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 ($41^{\circ}C$) 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

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. https://doi.org/10.1051/vetres:2002001
  2. Adams LG, Schutta C. 2010. Natural resistance against brucellosis: a review. Open Vet. Sci. J. 4: 61-71. https://doi.org/10.2174/1874318801004010061
  3. Chen P, Shakhnovich E. 2010. Thermal adaptation of viruses and bacteria. Biophys. J. 98: 1109-1118. https://doi.org/10.1016/j.bpj.2009.11.048
  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. https://doi.org/10.1007/s00360-012-0718-z
  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. https://doi.org/10.4049/jimmunol.171.3.1515
  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. https://doi.org/10.1111/j.0014-3820.2001.tb00735.x
  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.
  9. Beug H, Kirchbach A, Doderlein 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. https://doi.org/10.1016/0092-8674(79)90057-6
  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. https://doi.org/10.1111/jam.12072
  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.
  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. https://doi.org/10.1128/IAI.00403-13
  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. https://doi.org/10.1371/journal.pone.0122540
  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. https://doi.org/10.1016/j.vetimm.2006.07.007
  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.
  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 $2^{-{\Delta}{\Delta}Ct}$ method. Methods 25: 402-408. https://doi.org/10.1006/meth.2001.1262
  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. https://doi.org/10.3923/ijps.2014.340.342
  18. Detilleux DG, Cheville NF, Deyoe BL. 1997. Pathogenesis of Brucella abortus in chicken embryos. Vet. Pathol. 25: 138-146.
  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: 16152-16157. https://doi.org/10.1073/pnas.0705366104
  21. Dyson HJ, Wright PE. 2005. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol 6: 197-208. https://doi.org/10.1038/nrm1589
  22. Uversky VN. 2002. Natively unfolded proteins: a point where biology waits for physics. Protein Sci. 11: 739-756. https://doi.org/10.1110/ps.4210102
  23. Bloom JD, Raval A, Wilke CO. 2007. Thermodynamics of neutral protein evolution. Genetics 175: 255-266.
  24. Taverna DM, Goldstein RA. 2002. Why are proteins marginally stable? Proteins 46: 105-109. https://doi.org/10.1002/prot.10016
  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. https://doi.org/10.1126/science.aai7825
  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. https://doi.org/10.1128/IAI.02141-14
  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. https://doi.org/10.1016/j.micpath.2015.10.024

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