Journal of Veterinary Clinics (한국임상수의학회지)

The Korean Society of Veterinary Clinics (한국임상수의학회)
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Zinc Enhances Neutrophil Extracellular Trap Formation of Porcine Peripheral Blood Polymorphonuclear Cells through Tumor Necrosis Factor-Alpha from Peripheral Blood Mononuclear Cells

  • Heo, Ju-Haeng (Department of Veterinary Medicine, Veterinary Medical Center and College of Veterinary Medicine, Chungbuk National University) ;
  • Kim, Hakhyun (Department of Veterinary Medicine, Veterinary Medical Center and College of Veterinary Medicine, Chungbuk National University) ;
  • Kang, Byeong-Teck (Department of Veterinary Medicine, Veterinary Medical Center and College of Veterinary Medicine, Chungbuk National University) ;
  • Yang, Mhan-Pyo (Department of Veterinary Medicine, Veterinary Medical Center and College of Veterinary Medicine, Chungbuk National University)
  • Received : 2020.07.28
  • Accepted : 2020.10.08
  • Published : 2020.10.30
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Abstract

Neutrophil extracellular trap (NET) formation is an immune response for the invasion of microbes. The purpose of this study is to examine the effect of zinc on NET formation of porcine peripheral blood polymorphonuclear cells (PMNs). The NET formation of PMNs was measured by fluorescence microplate reader. The production of tumor necrosis factor (TNF)-α in the culture supernatants from zinc-treated peripheral blood mononuclear cells (PBMCs) was measured by enzyme-linked immunosorbent assay (ELISA). Zinc itself did not have no effect on NET formation. However, the NET formation of PMNs was increased by culture supernatants from PBMCs treated with zinc. Also, the NET formation of PMNs was increased by recombinant porcine (rp) TNF-α. The production of TNF-α in PBMCs culture supernatants was shown to increase upon zinc treatments. These NET formations of PMNs increased by either culture supernatant from PBMCs treated with zinc or rpTNF-α were inhibited by treatment of anti-rpTNF-α polyclonal antibody (pAb). These results suggested that zinc has an immunostimulating effect on the NET formation of PMNs, which is mediated by TNF-α released from zinc-treated PBMCs. Therefore, zinc may play an important role for NET formation in the defense of porcine inflammatory diseases.

Keywords

References

  1. Allen JI, Perri RT, McClain CJ, Kay NE. Alterations in human natural killer cell activity and monocyte cytotoxicity induced by zinc deficiency. J Lab Clin Med 1983; 102: 577-589.
  2. Benna JE, Hayem G, Dang PMC, Fay M, Chollet-Martin S, Elbim C, Meyer O, Gougerot-Pocidalo MA. NADPH oxidase priming and p47phox phosphorylation in neutrophils from synovial fluid of patients with rheumatoid arthritis and spondylarthropathy. Inflammation 2002; 26: 273-278. https://doi.org/10.1023/A:1021460517468
  3. Bianchi M, Hakkim A, Brinkmann V, Siler U, Seger RA, Zychlinsky A, Reichenbach J. Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 2009; 114: 2619-2622.
  4. Borregaard N. Neutrophils, from marrow to microbes. Immunity 2010; 33: 657-670. https://doi.org/10.1016/j.immuni.2010.11.011
  5. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science 2004; 303: 1532-1535. https://doi.org/10.1126/science.1092385
  6. Driessen C, Hirv K, Rink L, Kirchner H. Induction of cytokines by zinc ions in human peripheral bold mononuclear cells and separated monocytes. Lymphokine Cytokine Res 1994; 13: 15-20.
  7. Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, Weinrauch Y, Brinkmann V, Zychlinsky A. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 2007; 176: 231-241. https://doi.org/10.1083/jcb.200606027
  8. Gray RD, Lucas CD, MacKellar A, Li F, Hiersemenzel K, Haslett C, Davidson DJ, Rossi AG. Activation of conventional protein kinase C (PKC) is critical in the generation of human neutrophil extracellular traps. J Inflamm 2013; 10: 12. doi:10.1186/1476-9255-10-12.
  9. Grimble RF. Dietary lipids and the inflammatory response. Proc Nutr Soc 1998; 57: 535-542. https://doi.org/10.1079/PNS19980078
  10. Gupta AK, Joshi MB, Philippova M, Erne P, Hasler P, Hahn S, Resink TJ. Activated endothelial cells induce neutrophil extracellular traps and are susceptible to netosis-mediated cell death. FEBS Lett 2010; 584: 3193-3197. https://doi.org/10.1016/j.febslet.2010.06.006
  11. Haase H, Rink L. Signal transduction in monocytes: the role of zinc ions. Biometals 2007; 20: 579-585. https://doi.org/10.1007/s10534-006-9029-8
  12. Hasan R, Rink L, Haase H. Zinc signals in neutrophil granulocytes are required for the formation of neutrophil extracellular traps. Innate Immun 2013; 19: 253-264. https://doi.org/10.1177/1753425912458815
  13. Jeffery U, Kimura K, Gray R, Lueth P, Bellaire B, LeVine D. Dogs cast NETs too: canine neutrophil extracellular traps in health and immune-mediated hemolytic anemia. Vet Immunol Immunopathol 2015; 168: 262-268. https://doi.org/10.1016/j.vetimm.2015.10.014
  14. Jeon CJ, Kim SH, Kim SS, Kang JH, Yang MP. Fucoidan upregulates chemotactic activity of canine peripheral blood polymorphonuclear cells through interleukin-8 from peripheral blood mononuclear cells in vitro. J Vet Clin 2012; 29: 207-212.
  15. Jin JO, Yu Q. Fucoidan delays apoptosis and induces proinflammatory cytokine production in human neutrophils. Int J Biol Macromol 2015; 73; 65-71. https://doi.org/10.1016/j.ijbiomac.2014.10.059
  16. Kaplan MJ, Radic M. Neutrophil extracellular traps: doubleedged swords of innate immunity. J Immunol 2012; 189: 2689-2695. https://doi.org/10.4049/jimmunol.1201719
  17. Keshari RS, Jyoti A, Dubey M, Kothari N, Kohli M, Bogra J, Barthwal MK, Dikshit M. Cytokines induced neutrophil extracellular traps formation: implication for the inflammatory disease condition. PLoS ONE 2012; 7: e48111. https://doi.org/10.1371/journal.pone.0048111
  18. Keshari RS, Jyoti A, Kumar S, Dubey M, Verma A, Srinag BS, Krishnamurthy H, Barthwal MK, Dikshit M. Neutrophil extracellular traps contain mitochondrial as well as nuclear DNA and exhibit inflammatory potential. Cytometry A 2012; 81: 238-247.
  19. Kim HM, Ahn C, Kang BT, Kang JH, Jeung EB, Yang MP. Fucoidan suppresses excessive phagocytic capacity of porcine peripheral blood polymorphonuclear cells by modulating production of tumor necrosis factor-alpha by lipopolysaccharidestimulated peripheral blood mononuclear cells. Res Vet Sci 2018; 118: 413-418. https://doi.org/10.1016/j.rvsc.2018.04.007
  20. Kim SH, Kang JH, Yang MP. Fucoidan increases phagocytic capacity and oxidative burst activity of canine peripheral blood polymorphonuclear cells through TNF-${\alpha}$ from peripheral blood mononuclear cells. J Vet Clin 2011; 28: 183-189.
  21. Kim YJ, Kang JH, Yang MP. Zinc increase the phagocytic capacity of canine peripheral blood phagocytes in vitro. Vet Res Commun 2009; 33: 251-261. https://doi.org/10.1007/s11259-008-9173-4
  22. Medina E. Neutrophil extracellular traps: a strategic tactic to defeat pathogens with potential consequences for the host. J Innate Immun 2009; 1: 176-180. https://doi.org/10.1159/000203699
  23. Mitroulis I, Kambas K, Chrysanthopoulou A, Skendros P, Apostolidou E, Kourtzelis I, Drosos GI, Boumpas DT, Ritis K. Neutrophil extracellular trap formation is associated with IL-$1{\beta}$ and autophagy-related signaling in gout. PLoS ONE 2011; 6: e29318. https://doi.org/10.1371/journal.pone.0029318
  24. Mullen PG, Windsor AC, Walsh CJ, Fowler 3rd AA, Sugerman HJ. Tumor necrosis factor-alpha and interleukin-6 selectively regulate neutrophil function in vitro. J Surg Res 1995; 58: 124-130. https://doi.org/10.1006/jsre.1995.1020
  25. Papayannopoulos V, Metzler KD, Hakkim A, Zychlinsky A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J Cell Biol 2010; 191: 677-691. https://doi.org/10.1083/jcb.201006052
  26. Patel S, Kumar S, Jyoti A, Srinag BS, Keshari RS, Saluja R, Verma A, Mitra K, Barthwal MK, Krishnamurthy H, Bajpai VK, Dikshit M. Nitric oxide donors release extracellular traps from human neutrophils by augmenting free radical generation. Nitric Oxide 2010; 22: 226-234. https://doi.org/10.1016/j.niox.2010.01.001
  27. Remijsen Q, Berghe TV, Wirawan E, Asselbergh B, Parthoens E, Rycke RD, Noppen S, Delforge M, Willems J, Vandenabeele P. Neutrophil extracellular trap cell death requires both autophagy and superoxide generation. Cell Res 2011; 21: 290-304. https://doi.org/10.1038/cr.2010.150
  28. Seo DH, Kang BT, Kang JH, Yang MP. Zinc increases chemotactic activity of porcine peripheral blood polymorphonuclear cells. J Vet Clin 2018; 35: 195-199. https://doi.org/10.17555/jvc.2018.10.35.5.195
  29. Vallee BL, Falchuk KH. The biochemical basis of zinc physiology. Physiol Rev 1993; 73: 79-118. https://doi.org/10.1152/physrev.1993.73.1.79
  30. Wang Y, Li M, Stadler S, Correll S, Li P, Wang D, Hayama R, Leonelli L, Han H, Grigoryev SA, Allis CD, Coonrod SA. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol 2009; 184: 205-213. https://doi.org/10.1083/jcb.200806072
  31. Zawrotniak M, Rapala-Kozik M. Neutrophil extracellular traps (NETs)-formation and implications. Acta Biochim Pol 2013; 60: 277-284.