전체메뉴
검색
Article Search

JMB Journal of Microbiolog and Biotechnology

QR Code QR Code

Articles Service

Supplementary
Share this article on :
Metrics

Related articles in JMB

More Related Articles

Research article

Molecular and Cellular Microbiology (MCM)  |  Pathogenesis and Host-Microbial interactions

Modulatory Effect of Linoleic Acid During Brucella abortus 544 Infection in Murine Macrophage RAW264.7 Cells and Murine Model BALB/c Mice

Alisha Wehdnesday Bernardo Reyes 1, Son Hai Vu 1, Tran Xuan Ngoc Huy 1, Wongi Min 1, Hu Jang Lee 1, Hong Hee Chang 1, John Hwa Lee 2 and Suk Kim 1*

1Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University, Jinju, 52828, Republic of Korea
2College of Veterinary Medicine, Chonbuk National University, Iksan, 54596, Republic of Korea

Received: November 18, 2019; Accepted: January 29, 2020

J. Microbiol. Biotechnol. 2020; 30(5): 642-648

Published May 28, 2020 https://doi.org/10.4014/jmb.1911.11037

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

In this study, we investigated the effects of linoleic acid (LA) treatment on Brucella abortus infection in professional phagocyte RAW264.7 cells, particularly during the pathogen’s invasion and intracellular growth in these cells, as well as in murine model BALB/c mice focusing on bacterial splenic proliferation and immunoregulatory activities. LA inhibited the growth of Brucella in a doseand time-dependent manner. The ability of the pathogen to enter the phagocytes was inhibited as was its survival within these cells. This was accompanied by increased nitrite accumulation in these cells at 24 h post-infection. The concentration of LA used in the present study did not affect the total body weight or liver function of the mice. During Brucella infection, the total splenic weight of these animals was not changed; rather, resistance to bacterial proliferation was enhanced in the spleen. Furthermore, mice treated with LA displayed elevated levels of IL-12 and IFN-γ but reduced levels of IL-10 during infection. The findings in this study showed the regulatory role of LA against B. abortus infection suggesting its potential use in designing intervention strategy for brucellosis.

Keywords

Brucella abortus, cytokines, invasion, linoleic acid, spleen weight

Graphical Abstract

References

  1. Negron ME, Kharod GA, Bower WA, Walke H. 2019. Notes from the field: human Brucella abortus RB51 infections caused by consumption of unpasteurized domestic dairy products - United States, 2017-2019. MMWR Morb. Mortal. Wkly. Rep. 68: 185.
    Pubmed PMC
  2. Guimarães ES, Gomes MTR, Campos PC, Mansur DS, dos Santos AA, Harms J, et al. 2019. Brucella abortus cyclic dinucleotides trigger STING-dependent unfolded protein response that favors bacterial replication. J. Immunol. 202: 2671-2681.
    Pubmed PMC
  3. de Figueiedo P, Ficht TA, Rice-Ficht A, Rossetti CA, Adams LG. 2015. Pathogenesis and immunobiology of brucellosis. Am. J. Pathol. 185: 1505-1517.
    Pubmed PMC
  4. Barquero-Calvo E, Mora-Cartin R, Arce-Gorvel V, de Diego JL, Chacon-Diaz C, Chaves-Olarte E, et al. 2015. Brucella abortus induces the premature death of human neutrophils through the action of its lipopolysaccharide. PLoS Pathog. 11: e1004853.
    Pubmed PMC
  5. Bosilkovski M. 2019. Brucellosis: Microbiology, Epidemiology, and Pathogenesis. Available from https://www.uptodate.com/contents/brucellosis-microbiology-epidemiology-and-pathogenesis. Accessed May 31, 2019.
  6. Yang X, Skyberg JA, Cao L, Clapp B, Thornburg T, Pascual DW. 2013. Progress in Brucella vaccine development. Front. Biol. (Beijing) 8: 60-77.
    Pubmed PMC
  7. Dorneles EMS, Sriranganathan N, Lage AP. 2015. Recent advances in Brucella abortus vaccines. Vet. Res. 46: 76.
    Pubmed PMC
  8. Khan MZ, Zahoor M. 2018. An overview of brucellosis in cattle and humans, and its serological and molecular diagnosis in control strategies. Trop. Med. Infect. Dis. 14: 65.
    Pubmed PMC
  9. Das UN. 2018. Arachidonic acid and other unsaturated fatty acids and some of their metabolites function as endogenous antimicrobial molecules: a review. J. Adv. Res. 11: 57-66.
    Pubmed PMC
  10. Zheng CJ, Yoo JS, Lee TG, Cho HY, Kim YH, Kim WG. 2005. Fatty acid synthesis is a target for antibacterial activity of unsaturated fatty acids. FEBS Lett. 579: 5157-5162.
    Pubmed
  11. Correia M, Michel V, Matos AA, Carvalho P, Oliveira MJ, Ferreira R, et al. 2012. Docosahexaenoic acid inhibits Helicobacter pylori growth in vitro and mice gastric mucosa colonization. PLoS One. 7: E35072.
    Pubmed PMC
  12. Sanders TAB. 2016. Functional Dietary Lipids: Food Formulation, Consumer Issues and Innovation for Health, pp. 1-20. 1st Ed. Woodhead Publishing, Cambridge.
  13. Lankinen MA, Fauland A, Shimizu B, Agren J, Wheelock CE, Laakso M, et al. 2019. Inflammatory response to dietary linoleic acid depends on FADS1 genotype. Am. J. Clin. Nutr. 108: 1-11.
    Pubmed
  14. Reyes AWB, Hop HT, Arayan LT, Huy TXN, Park SJ, Kim KD, et al. 2017. The host immune enhancing agent Korean red ginseng oil successfully attenuates Brucella abortus infection in a murine model. J. Ethnopharmacol. 198: 5-14.
    Pubmed
  15. Grillo MJ, Blasco JM, Gorvel JP, Moriyon I, Moreno E. 2012. What have we learned from brucellosis in the mouse model? Vet. Res. 43: 29.
    Pubmed PMC
  16. Dilika F, Bremner PD, Meyer JJ. 2000. Antibacterial activity of linoleic and oleic acids isolated from Helichrysum pedunculatum: a plant used during circumcision rites. Fitoterapia 71: 450-452.
  17. Peng M, Tabashsum Z, Patel P, Bernhardt C, Biswas D. 2018. Linoleic acids overproducing Lactobacillus casei limits growth, survival, and virulence of Salmonella Typhimurium and enterohaemorrhagic Escherichia coli. Front. Microbiol. 9: 2663.
    Pubmed PMC
  18. Gutierrez-Jimenez C, Mora-Cartin R, Altamirano-Silva P, Chacon-Diaz C, Chaves-Olarte E, Moreno E, Barquero-Calvo E. 2019. Neutrophils as trojan horse vehicles for Brucella abortus macrophage infection. Front. Immunol. 10: 1012.
    Pubmed PMC
  19. Hop HT, Arayan LT, Reyes AWB, Huy TXN, Baek EJ, Min WG, et al. 2017. Inhibitory effect of the ethanol extract of a rice bran mixture comprising Angelica gigas, Cnidium officinale, Artemisia princeps, and Camellia sinensis on Brucella abortus uptake by professional and nonprofessional phagocytes. J. Microbiol. Biotechnol. 27: 1885-1891.
    Pubmed
  20. Gross A, Spiesser S, Terraza A, Rouot B, Caron E, Dornand J. 1998. Expression and bactericidal activity of nitric oxide synthase in Brucella suis-infected murine macrophages. Infect. Immun. 66: 1309-1316.
    Pubmed PMC
  21. Wang M, Qureshi N, Soeurt N, Splitter G. 2001. High levels of nitric oxide production decrease early but increase late survival of Brucella abortus in macrophages. Microb. Pathog. 31: 221-230.
    Pubmed
  22. Liang JF, Akaike T. 1998. Protective effect of linoleic acid on IFN-γ-induced cellular injury in primary culture hepatocytes. J. Biochem. 123: 213-218.
    Pubmed
  23. Babu U, Wiesenfeld P, Gaines D, Raybourne RB. 2009. Effect of long chain fatty acids on Salmonella killing, superoxide and nitric oxide production by chicken macrophages. Int. J. Food Microbiol. 132: 67-72.
    Pubmed
  24. Changhua L, Yindong Y, Defa L, Lidan Z, Shiyan Q, Jianjun X. 2005. Conjugated linoleic acid attenuates the production and gene expression of proinflammatory cytokines in weaned pigs challenged with lipopolysaccharide. J. Nutr. 135: 239-244.
    Pubmed
  25. He X, Zhang H, Yang X, Zhang S, Dai Q, Xiao W, et al. 2007. Modulation of immune function by conjugated linoleic acid in chickens. Food Agr. Immunol. 18: 169-178.
  26. Dornand J, Gross A, Lafont V, Liautard J, Oliaro J, Liautard JP. 2002. The innate immune response against Brucella in humans. Vet. Microbiol. 90: 383-394.
  27. Zhan Y, Cheers C. 1995. Endogenous interleukin-12 is involved in resistance to Brucella abortus infection. Infect. Immun. 63, 1387-1390.
    Pubmed PMC
  28. Macedo GC, Magnani DM, Carvalho NB, Bruna-Romero O, Gazzinelli RT, Oliveira SC. 2008. Central role of MyD88-dependent dendritic cell maturation and proinflammatory cytokine production to control Brucella abortus infection. J. Immunol. 180: 1080-1087.
    Pubmed
  29. Malovrh T, Kompan L, Juntes P, Wraber B, Spindler-Vesel A, Kompan D. 2009. Influence of conjugated linoleic acid on the porcine immune response and morbidity: a randomized controlled trial. Lipids Health Dis. 8: 22.
    Pubmed PMC
  30. Murphy EA, Sathiyaseelan J, Parent MA, Zou B, Baldwin CL. 2001. Interferon-g is crucial for surviving a Brucella abortus infection in both resistant C57BL/6 and susceptible BALB/c mice. Immunol. 103: 511-518.
    Pubmed PMC
  31. Corsetti PP, de Almeida LA, Carvalho NB, Azevedo V, Silva TMA, Teixeira HC, et al. 2013. Lack of endogenous IL-10 enhances production of proinflammatory cytokines and leads to Brucella abortus clearance in mice. PLoS One 8: e74729.
    Pubmed PMC
  32. Fernandes DM, Baldwin CL. 1995. Interleukin-10 downregulates protective immunity to Brucella abortus. Infect. Immun. 63, 1130-1133.
    Pubmed PMC
  33. Sammon AM. 1999. Dietary linoleic acid, immune inhibition and disease. Postgrad. Med. J. 75: 129-132.
    Pubmed PMC