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Alteration of Cytokine Production during Visceral Larva Migrans by Toxascaris leonina in Mice

  • Kang, Shin Ae (Department of Parasitology, School of Medicine, Pusan National University, and Immunoregulatory Therapeutics Group in Brain Busan 21 Project) ;
  • Park, Mi-Kyung (Department of Parasitology, School of Medicine, Pusan National University, and Immunoregulatory Therapeutics Group in Brain Busan 21 Project) ;
  • Cho, Min Kyoung (Department of Parasitology, School of Medicine, Pusan National University, and Immunoregulatory Therapeutics Group in Brain Busan 21 Project) ;
  • Yu, Hak Sun (Department of Parasitology, School of Medicine, Pusan National University, and Immunoregulatory Therapeutics Group in Brain Busan 21 Project)
  • Received : 2013.05.31
  • Accepted : 2013.08.09
  • Published : 2013.10.31

Abstract

To determine alteration of immune responses during visceral larva migrans (VLM) caused by Toxascaris leonina at several time points, we experimentally infected mice with embryonated eggs of T. leonina and measured T-helper (Th) cell-related serial cytokine production after infection. At day 5 post infection (PI), most larvae were detected from the lungs, spleen, intestine, and muscle. Expression of thymic stromal lymphopoietin (TSLP) and CCL11 (eotaxin) showed a significant increase in most infected organs, except the intestine. However, expression of the CXCL1 (Gro-${\alpha}$) gene was most highly enhanced in the intestine at day 14 PI. Th1-related cytokine secretion of splenocytes showed increases at day 28 PI, and the level showed a decrease at day 42 PI. Th2-related cytokine secretion of splenocytes also showed an increase after infection; in particular, IL-5 level showed a significant increase at day 14 PI, and the level showed a decrease at day 28 PI. However, levels of Th17-related cytokines, IL-6 and IL-17A, showed gradual increases until day 42 PI. In conclusion, Th1, Th2, and Th17-related cytokine production might be important in immune responses against T. leonina VLM in experimental mice.

References

  1. Lee KH, Park HK, Jeong HJ, Park SK, Lee SJ, Choi SH, Cho MK, Ock MS, Hong YC, Yu HS. Immunization of proteins from Toxascaris leonina adult worm inhibits allergic specific Th2 response. Vet Parasitol 2008; 156: 216-225. https://doi.org/10.1016/j.vetpar.2008.06.016
  2. Roberts LS, Schmidt GD, Janovy J. Foundations of Parasitology. New York, USA. McGraw-Hill. 2009.
  3. Nagy D, Bede O, Danka J, Szenasi Z, Sipka S. Analysis of serum cytokine levels in children with chronic cough associated with Toxocara canis infection. Parasite Immunol 2012; 34: 581-588. https://doi.org/10.1111/pim.12010
  4. Nagy D, Bede O, Danka J, Szenasi Z, Sipka S. Analysis of serum cytokine levels in children with chronic cough associated with Toxocara canis infection. Parasite Immunol; 34: 581-588.
  5. Takamoto M, Wang ZX, Watanabe N, Matsuzawa A, Nariuchi H, Sugane K. Eosinophilia, IgE production, and cytokine production by lung T cells in surface CD4-deficient mutant mice infected with Toxocara canis. Immunology 1998; 95: 97-104. https://doi.org/10.1046/j.1365-2567.1998.00575.x
  6. Torina A, Caracappa S, Barera A, Dieli F, Sireci G, Genchi C, Deplazes P, Salerno A. Toxocara canis infection induces antigen-specific IL-10 and IFN-gamma production in pregnant dogs and their puppies. Vet Immunol Immunopathol 2005; 108: 247-251. https://doi.org/10.1016/j.vetimm.2005.08.006
  7. Park HK, Cho MK, Park MK, Kang SA, Kim YS, Kim KU, Lee MK, Ock MS, Cha HJ, Yu HS. A 24 kDa excretory-secretory protein of Anisakis simplex larvae could elicit allergic airway inflammation in mice. Korean J Parasitol 2011; 49: 373-380. https://doi.org/10.3347/kjp.2011.49.4.373
  8. Park MK, Cho MK, Kang SA, Park HK, Kim YS, Kim KU, Ahn SC, Kim DH, Yu HS. Protease-activated receptor 2 is involved in Th2 responses against Trichinella spiralis infection. Korean J Parasitol 2011; 49: 235-243. https://doi.org/10.3347/kjp.2011.49.3.235
  9. Canto GJ, Garcia MP, Garcia A, Guerrero MJ, Mosqueda J. The prevalence and abundance of helminth parasites in stray dogs from the city of Queretaro in central Mexico. J Helminthol 2011: 1-7.
  10. Kim YH, Huh S. Prevalence of Toxocara canis, Toxascaris leonina, and Dirofilaria immitis in dogs in Chuncheon, Korea (2004). Korean J Parasitol 2005; 43: 65-67. https://doi.org/10.3347/kjp.2005.43.2.65
  11. Prokopic J, Figallova V. The migration of larvae of Toxascaris leonina (Linstow, 1909) in experimentally infected white mice. Folia Parasitol (Praha) 1982; 29: 233-238.
  12. Maizels RM, Hewitson JP, Smith KA. Susceptibility and immunity to helminth parasites. Curr Opin Immunol 2012; 24: 459-466. https://doi.org/10.1016/j.coi.2012.06.003
  13. Mathew A, MacLean JA, DeHaan E, Tager AM, Green FH, Luster AD. Signal transducer and activator of transcription 6 controls chemokine production and T helper cell type 2 cell trafficking in allergic pulmonary inflammation. J Exp Med 2001; 193: 1087-1096. https://doi.org/10.1084/jem.193.9.1087
  14. Sallusto F. The role of chemokines and chemokine receptors in T cell priming and Th1/Th2-mediated responses. Haematologica 1999; 84(suppl EHA-4): 28-31.
  15. Okoshi S, Usui M. Experimental studies on Toxascaris leonina. VI. Experimental infection of mice, chickens and earthworms with Toxascaris leonina, Toxocara canis and Toxocara cati. Nippon Juigaku Zasshi 1968; 30: 151-166. https://doi.org/10.1292/jvms1939.30.151
  16. Bettelli E, Korn T, Oukka M, Kuchroo VK. Induction and effector functions of T(H)17 cells. Nature 2008; 453: 1051-1057. https://doi.org/10.1038/nature07036
  17. Yao R, Ma YL, Liang W, Li HH, Ma ZJ, Yu X, Liao YH. MicroRNA- 155 modulates Treg and Th17 cell differentiation and Th17 cell function by targeting SOCS1. PLoS One 2012; 7: e46082. https://doi.org/10.1371/journal.pone.0046082
  18. Kang SA, Cho MK, Park MK, Kim DH, Hong YC, Lee YS, Cha HJ, Ock MS, Yu HS. Alteration of helper T-cell related cytokine production in splenocytes during Trichinella spiralis infection. Vet Parasitol 2012; 186: 319-327. https://doi.org/10.1016/j.vetpar.2011.12.002
  19. Bazzone LE, Smith PM, Rutitzky LI, Shainheit MG, Urban JF, Setiawan T, Blum AM, Weinstock JV, Stadecker MJ. Coinfection with the intestinal nematode Heligmosomoides polygyrus markedly reduces hepatic egg-induced immunopathology and proinflammatory cytokines in mouse models of severe schistosomiasis. Infect Immun 2008; 76: 5164-5172. https://doi.org/10.1128/IAI.00673-08
  20. Reece JJ, Siracusa MC, Southard TL, Brayton CF, Urban JF Jr., Scott AL. Hookworm-induced persistent changes to the immunological environment of the lung. Infect Immun 2008; 76: 3511-3524. https://doi.org/10.1128/IAI.00192-08
  21. Cheung PF, Wong CK, Lam CW. Molecular mechanisms of cytokine and chemokine release from eosinophils activated by IL- 17A, IL-17F, and IL-23: implication for Th17 lymphocytes-mediated allergic inflammation. J Immunol 2008; 180: 5625-5635. https://doi.org/10.4049/jimmunol.180.8.5625
  22. Akbari O, DeKruyff RH, Umetsu DT. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat Immunol 2001; 2: 725-731. https://doi.org/10.1038/90667
  23. Presser K, Schwinge D, Wegmann M, Huber S, Schmitt S, Quaas A, Maxeiner JH, Finotto S, Lohse AW, Blessing M, Schramm C. Coexpression of TGF-beta1 and IL-10 enables regulatory T cells to completely suppress airway hyperreactivity. J Immunol 2008; 181: 7751-7758. https://doi.org/10.4049/jimmunol.181.11.7751