DOI QR코드

DOI QR Code

Kinetics of IL-23 and IL-12 Secretion in Response to Toxoplasma gondii Antigens from THP-1 Monocytic Cells

  • Quan, Juan-Hua (Department of Infection Biology and Research Institute for Medical Sciences, Chungnam National University School of Medicine) ;
  • Zhou, Wei (Department of Infection Biology and Research Institute for Medical Sciences, Chungnam National University School of Medicine) ;
  • Cha, Guang-Ho (Department of Infection Biology and Research Institute for Medical Sciences, Chungnam National University School of Medicine) ;
  • Choi, In-Wook (Department of Infection Biology and Research Institute for Medical Sciences, Chungnam National University School of Medicine) ;
  • Shin, Dae-Whan (Department of Infection Biology and Research Institute for Medical Sciences, Chungnam National University School of Medicine) ;
  • Lee, Young-Ha (Department of Infection Biology and Research Institute for Medical Sciences, Chungnam National University School of Medicine)
  • Received : 2012.11.23
  • Accepted : 2013.01.15
  • Published : 2013.03.15

Abstract

IL-23 and IL-12 are structurally similar and critical for the generation of efficient cellular immune responses. Toxoplasma gondii induces a strong cell-mediated immune response. However, little is known about IL-23 secretion profiles in T. gondii-infected immune cells in connection with IL-12. We compared the patterns of IL-23 and IL-12 production by THP-1 human monocytic cells in response to stimulation with live or heat-killed T. gondii tachyzoites, or with equivalent quantities of either T. gondii excretory/secretory proteins (ESP) or soluble tachyzoite antigen (STAg). IL-23 and IL-12 were significantly increased from 6 hr after stimulation with T. gondii antigens, and their secretions were increased with parasite dose-dependent manner. IL-23 concentrations were significantly higher than those of IL-12 at the same multiplicity of infection. IL-23 secretion induced by live parasites was significantly higher than that by heat-killed parasites, ESP, or STAg, whereas IL-12 secretion by live parasite was similar to those of ESP or STAg. However, the lowest levels of both cytokines were at stimulation with heat-killed parasites. These data indicate that IL-23 secretion patterns by stimulation with various kinds of T. gondii antigens at THP-1 monocytic cells are similar to those of IL-12, even though the levels of IL-23 induction were significantly higher than those of IL-12. The detailed kinetics induced by each T. gondii antigen were different from each other.

Keywords

References

  1. Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Int J Parasitol 2000; 30: 1217-1258. https://doi.org/10.1016/S0020-7519(00)00124-7
  2. Miller CM, Boulter NR, Ikin RJ, Smith NC. The immunobiology of the innate response to Toxoplasma gondii. Int J Parasitol 2009; 39: 23-39. https://doi.org/10.1016/j.ijpara.2008.08.002
  3. Langrish CL, McKenzie BS, Wilson NJ, de Waal Malefyt R, Kastelein RA, Cua DJ. IL-12 and IL-23: master regulators of innate and adaptive immunity. Immunol Rev 2004; 202: 96-105. https://doi.org/10.1111/j.0105-2896.2004.00214.x
  4. Bliss SK, Marshall AJ, Zhang Y, Denkers EY. Human polymorphonuclear leukocytes produce IL-12, TNF-${\alpha}$, and the chemokines macrophage-inflammatory protein-$1{\alpha}$ and -$1{\beta}$ in response to Toxoplasma gondii antigens. J Immunol 1999; 162: 7369-7375.
  5. Robben PM, Mordue DG, Truscott SM, Takeda K, Akira S, Sibley LD. Production of IL-12 by macrophages infected with Toxoplasma gondii depends on the parasite genotype. J Immunol 2004; 172: 3686-3694.
  6. Lieberman LA, Cardillo F, Owyang AM, Rennick DM, Cua DJ, Kastelein RA, Hunter CA. IL-23 provides a limited mechanism of resistance to acute toxoplasmosis in the absence of IL-12. J Immunol 2004; 173: 1887-1893.
  7. Aldebert D, Durand F, Mercier C, Brenier-Pinchart MP, Cesbron-Delauw MF, Pelloux H. Toxoplasma gondii triggers secretion of interleukin-12 but low level of interleukin-10 from the THP-1 human monocytic cell line. Cytokine 2007; 37: 206-211. https://doi.org/10.1016/j.cyto.2007.03.012
  8. Son ES, Nam HW. Detection and characterization of excretory/secretory proteins from Toxoplasma gondii by monoclonal antibodies. Korean J Parasitol 2001; 39: 49-56. https://doi.org/10.3347/kjp.2001.39.1.49
  9. Munoz M, Heimesaat MM, Danker K, Struck D, Lohmann U, Plickert R, Bereswill S, Fischer A, Dunay IR, Wolk K, Loddenkemper C, Krell HW, Libert C, Lund LR, Frey O, Holscher C, Iwakura Y, Ghilardi N, Ouyang W, Kamradt T, Sabat R, Liesenfeld O. Interleukin (IL)-23 mediates Toxoplasma gondii-induced immunopathology in the gut via matrix metalloproteinase-2 and IL-22 but independent of IL-17. J Exp Med 2009; 206: 3047-3059. https://doi.org/10.1084/jem.20090900
  10. Subauste CS, Wessendarp M. Human dendritic cells discriminate between viable and killed Toxoplasma gondii tachyzoites: dendritic cell activation after infection with viable parasites results in CD28 and CD40 ligand signaling that controls IL-12-dependent and -independent T cell production of IFN-gamma. J Immunol 2000; 165: 1498-1505.
  11. He R, Shepard LW, Chen J, Pan ZK, Ye RD. Serum amyloid A is an endogenous ligand that differentially induces IL-12 and IL-23. J Immunol 2006; 177: 4072-4079.
  12. Khayrullina T, Yen JH, Jing H, Ganea D. In vitro differentiation of dendritic cells in the presence of prostaglandin $E_2$ alters the IL-12/IL-23 balance and promotes differentiation of Th17 cells. J Immunol 2008; 181: 721-735.
  13. Liu CH, Fan YT, Dias A, Esper L, Corn RA, Bafica A, Machado FS, Aliberti J. Cutting edge: dendritic cells are essential for in vivo IL-12 production and development of resistance against Toxoplasma gondii infection in mice. J Immunol 2006; 177: 31-35.
  14. Reis e Sousa C, Hieny S, Scharton-Kersten T, Jankovic D, Charest H, Germain RN, Sher A. In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas. J Exp Med 1997; 186: 1819-1829. https://doi.org/10.1084/jem.186.11.1819
  15. Park AY, Scott P. IL-12: keeping cell-mediated immunity alive. Scand J Immunol 2001; 53: 529-532. https://doi.org/10.1046/j.1365-3083.2001.00917.x
  16. Boniface K, Blom B, Liu YJ, Waal Malefyt R. From interleukin-23 to T-helper 17 cells: human T-helper cell differentiation revisited. Immunol Rev 2008, 132-146.
  17. Ahern PP, Izcue A, Maloy KJ, Powrie F. The interleukin-23 axis in intestinal inflammation. Immunol Rev 2008; 226: 147-159. https://doi.org/10.1111/j.1600-065X.2008.00705.x

Cited by

  1. Besnoitia besnoiti tachyzoites induce monocyte extracellular trap formation vol.113, pp.11, 2014, https://doi.org/10.1007/s00436-014-4094-3
  2. Levels of Transforming Growth Factor-Beta After Immunization of Mice With in vivo prepared Toxoplasma gondii Excretory/Secretory Proteins vol.8, pp.5, 2013, https://doi.org/10.5812/jjm.8(5)2015.17802
  3. Intracellular Networks of the PI3K/AKT and MAPK Pathways for Regulating Toxoplasma gondii -Induced IL-23 and IL-12 Production in Human THP-1 Cells vol.10, pp.11, 2013, https://doi.org/10.1371/journal.pone.0141550
  4. Far beyond Phagocytosis: Phagocyte-Derived Extracellular Traps Act Efficiently against Protozoan Parasites In Vitro and In Vivo vol.2016, pp.None, 2013, https://doi.org/10.1155/2016/5898074
  5. Secretion of Rhoptry and Dense Granule Effector Proteins by Nonreplicating Toxoplasma gondii Uracil Auxotrophs Controls the Development of Antitumor Immunity vol.12, pp.7, 2016, https://doi.org/10.1371/journal.pgen.1006189
  6. Cytokine response of human THP-1 macrophages to Trichomonas tenax vol.169, pp.None, 2013, https://doi.org/10.1016/j.exppara.2016.07.011
  7. IL-12 and IL-23 Production in Toxoplasma gondii- or LPS-Treated Jurkat T Cells via PI3K and MAPK Signaling Pathways vol.55, pp.6, 2013, https://doi.org/10.3347/kjp.2017.55.6.613