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Acta Parasitologica

, Volume 64, Issue 3, pp 520–527 | Cite as

Vaccaria n-Butanol Extract Lower the Production of Proinflammatory Cytokines and the Infection Risk of T. spiralis In Vivo

  • Fei Xu
  • Bao Hou
  • Xuexue Zhu
  • Yixiao Liu
  • Xuelin Shi
  • Shuangshuang Li
  • Zhongjie Li
  • Weiwei Cai
  • Yuetao Zhou
  • Liying QiuEmail author
Original Paper
  • 41 Downloads

Abstract

Introduction

Trichinellosis is a severe zoonosis involving the activation of inflammatory cells, accompanied by the prominent expressions of proinflammatory cytokines in the host. Semen vaccariae, the seeds of Vaccaria segetalis (Neck.) Garcke. ex Asch. (Caryophyllaceae), is a famous traditional herb that is rich in vaccaria n-butanol extract (VNE). Vaccarin is one major active component of VNE, and it is reported in the treatment of stranguria disease. Hypaphorine is another main active component of VNE and has good anti-inflammatory effect, whereas the potential bioactivity of VNE in trichinellosis treatment is still unknown.

Materials and methods

This study was designed to evaluate the potential anthelmintic and anti-inflammatory activity of VNE toward T. spiralis infection. ICR mice were used to assess the effect of VNE on repression larvae and adult worms in vivo. Immunohistochemistry analysis was performed to evaluate the expression levels of IL-1β, IL-6, TNF-α, and COX-2.

Results

Our results showed that VNE could effectively depress the expressions of proinflammatory cytokines, including IL-1β, IL-6, TNF-α, and COX-2. The adult worms were decreased by 79.53%, while the muscle larvae were diminished by 77.70% as compared to the control.

Conclusion

These results demonstrated that VNE may be a promising therapeutic agent against the inflammation and diseases caused by T. spiralis infection.

Keywords

Zoonosis Trichinellosis Vaccariae semen Hypaphorine Vaccarin Proinflammatory cytokines 

Notes

Acknowledgements

The authors acknowledge the funding from Wuxi Science and Technology Development Fund 2018 (Grant no. WX0302B010507180101 PB) and Jiangnan University Youth Fund 2018 (Grant no. K2050205). This work was also supported by the National First-Class Discipline Program of Food Science and Technology (JUFSTR20180101).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical standards

All experiments on human subjects published in this article were in accordance with the Helsinki Declaration of 1975.

Consent for publication

All animal procedures and protocols of this project were conformed to Good Publishing Practice in Acta Parasitologica. The study was approved by the Animal Care Committee of Jiangnan University.

References

  1. 1.
    Abou Rayia DM et al (2017) Implication of artemisinin nematocidal activity on experimental trichinellosis: in vitro and in vivo studies. Parasitol Int 66:56–63.  https://doi.org/10.1016/j.parint.2016.11.012 CrossRefPubMedGoogle Scholar
  2. 2.
    Attia RA et al (2015) Effect of myrrh and thyme on Trichinella spiralis enteral and parenteral phases with inducible nitric oxide expression in mice. Mem Inst Oswaldo Cruz 110:1035–1041.  https://doi.org/10.1590/0074-02760150295 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Bruschi F (2012) Trichinellosis in developing countries: is it neglected? J Infect Dev Ctries 6:216–222CrossRefGoogle Scholar
  4. 4.
    Bruschi F, Chiumiento L (2011) Trichinella inflammatory myopathy: host or parasite strategy? Parasites Vectors 4:42.  https://doi.org/10.1186/1756-3305-4-42 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Bruschi F et al (2016) Matrix metalloproteinase (MMP)-9: a reliable marker for inflammation in early human trichinellosis. Vet Parasitol 231:132–136.  https://doi.org/10.1016/j.vetpar.2016.04.011 CrossRefPubMedGoogle Scholar
  6. 6.
    Caner A et al (2008) Comparison of the effects of Artemisia vulgaris and Artemisia absinthium growing in western Anatolia against trichinellosis (Trichinella spiralis) in rats. Exp Parasitol 119:173–179.  https://doi.org/10.1016/j.exppara.2008.01.012 CrossRefPubMedGoogle Scholar
  7. 7.
    Cannon CP, Cannon PJ (2012) COX-2 inhibitors and cardiovascular risk. Science 336:1386–1387.  https://doi.org/10.1126/science.1224398 CrossRefPubMedGoogle Scholar
  8. 8.
    Denham DA (1965) Studies with methyridine and Trichinella spiralis. I. Effect upon the intestinal phase in mice. Exp Parasitol 17:10–14CrossRefGoogle Scholar
  9. 9.
    Dong Y, Liao J (2017) Application of traditional Chinese medicine in treatment of atrial fibrillation. Hum Fertil 2017:1381732.  https://doi.org/10.1155/2017/1381732 CrossRefGoogle Scholar
  10. 10.
    Dunn IJ, Wright KA (1985) Cell injury caused by Trichinella spiralis in the mucosal epithelium of B10A mice. J Parasitol 71:757–766CrossRefGoogle Scholar
  11. 11.
    Falduto GH et al (2016) Regulatory parameters of the lung immune response during the early phase of experimental trichinellosis. Vet Parasitol 231:47–52.  https://doi.org/10.1016/j.vetpar.2016.05.009 CrossRefPubMedGoogle Scholar
  12. 12.
    Gottstein B et al (2009) Epidemiology, diagnosis, treatment, and control of trichinellosis. Clin Microbiol Rev 22:127–145.  https://doi.org/10.1128/cmr.00026-08 (Table of contents) CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Horiuchi T et al (2010) Transmembrane TNF-alpha: structure, function and interaction with anti-TNF agents. Rheumatology 49:1215–1228.  https://doi.org/10.1093/rheumatology/keq031 CrossRefPubMedGoogle Scholar
  14. 14.
    Huang SW et al (2017) P2X7 receptor-dependent tuning of gut epithelial responses to infection. Immunol Cell Biol 95:178–188.  https://doi.org/10.1038/icb.2016.75 CrossRefPubMedGoogle Scholar
  15. 15.
    Im SS et al (2011) Linking lipid metabolism to the innate immune response in macrophages through sterol regulatory element binding protein-1a. Cell Metab 13:540–549.  https://doi.org/10.1016/j.cmet.2011.04.001 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Imaizumi T et al (2010) IFN-gamma and TNF-alpha synergistically induce microRNA-155 which regulates TAB 2/IP-10 expression in human mesangial cells. Am J Nephrol 32:462–468.  https://doi.org/10.1159/000321365 CrossRefPubMedGoogle Scholar
  17. 17.
    Keating C et al (2011) P2X7 receptor-dependent intestinal afferent hypersensitivity in a mouse model of postinfectious irritable bowel syndrome. J Immunol 187:1467–1474.  https://doi.org/10.4049/jimmunol.1100423 CrossRefPubMedGoogle Scholar
  18. 18.
    Li Z et al (2016) Celastrol nanomicelles attenuate cytokine secretion in macrophages and inhibit macrophage-induced corneal neovascularization in rats. Int J Nanomedicine 11:6135–6148.  https://doi.org/10.2147/ijn.s117425 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Long SR, Tian XY, Wang ZQ, Liu RD, Liu LN et al (2015) Serodiagnosis of trichinellosis by ELISA using recombinant nudix hydrolase of Trichinella spiralis. Trop Biomed 32:669–675Google Scholar
  20. 20.
    Mariathasan S et al (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440:228–232.  https://doi.org/10.1038/nature04515 CrossRefGoogle Scholar
  21. 21.
    Ming L et al (2016) Invasion by Trichinella spiralis infective larvae affects the levels of inflammatory cytokines in intestinal epithelial cells in vitro. Exp Parasitol 170:220–226.  https://doi.org/10.1016/j.exppara.2016.10.003 CrossRefPubMedGoogle Scholar
  22. 22.
    Munoz-Carrillo JL et al (2017) Resiniferatoxin lowers TNF-alpha, NO and PGE2 in the intestinal phase and the parasite burden in the muscular phase of Trichinella spiralis infection. Parasites Immunol.  https://doi.org/10.1111/pim.12393 CrossRefGoogle Scholar
  23. 23.
    Oliver KM et al (2009) Hypoxia. Regulation of NFkappaB signalling during inflammation: the role of hydroxylases. Arthritis Res Ther 11:215.  https://doi.org/10.1186/ar2575 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Othman AA et al (2016) Atorvastatin and metformin administration modulates experimental Trichinella spiralis infection. Parasitol Int 65:105–112.  https://doi.org/10.1016/j.parint.2015.11.001 CrossRefPubMedGoogle Scholar
  25. 25.
    Park MK et al (2018) Effect of muscle strength by Trichinella spiralis infection during chronic phase. Int J Med Sci 15:802–807.  https://doi.org/10.7150/ijms.23497 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Puljiz I et al (2005) Electrocardiographic changes and myocarditis in trichinellosis: a retrospective study of 154 patients. Ann Trop Med Parasitol 99:403–411.  https://doi.org/10.1179/136485905X36307 CrossRefPubMedGoogle Scholar
  27. 27.
    Ranganathan PV et al (2013) Netrin-1 regulates the inflammatory response of neutrophils and macrophages, and suppresses ischemic acute kidney injury by inhibiting COX-2-mediated PGE2 production. Kidney Int 83:1087–1098.  https://doi.org/10.1038/ki.2012.423 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Rostami A et al (2017) Meat sources of infection for outbreaks of human trichinellosis. Food Microbiol 64:65–71.  https://doi.org/10.1016/j.fm.2016.12.012 CrossRefPubMedGoogle Scholar
  29. 29.
    Schultz HS et al (2016) OSCAR-collagen signaling in monocytes plays a proinflammatory role and may contribute to the pathogenesis of rheumatoid arthritis. Eur J Immunol 46:952–963.  https://doi.org/10.1002/eji.201545986 CrossRefPubMedGoogle Scholar
  30. 30.
    Shalaby MA et al (2010) Effect of methanolic extract of Balanites aegyptiaca fruits on enteral and parenteral stages of Trichinella spiralis in rats. Parasitol Res 107:17–25.  https://doi.org/10.1007/s00436-010-1827-9 CrossRefPubMedGoogle Scholar
  31. 31.
    Soliman GA et al (2011) Therapeutic efficacy of doramectin, ivermectin and levamisole against different stages of Trichinella spiralis in rats. Turk Parazitol Derg 35:86–91.  https://doi.org/10.5152/tpd.2011.22 CrossRefGoogle Scholar
  32. 32.
    Su XD et al (2019) Anti-inflammatory potential of saponins from Aster tataricus via NF-kappaB/MAPK activation. J Nat Prod.  https://doi.org/10.1021/acs.jnatprod.8b00856 CrossRefPubMedGoogle Scholar
  33. 33.
    Turiac IA et al (2017) Trichinellosis outbreak due to wild boar meat consumption in southern Italy. Parasites Vectors 10:107.  https://doi.org/10.1186/s13071-017-2052-5 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Wang SW et al (2011) Protein change of intestinal epithelial cells induced in vitro by Trichinella spiralis infective larvae. Parasitol Res 108:593–599.  https://doi.org/10.1007/s00436-010-2102-9 CrossRefPubMedGoogle Scholar
  35. 35.
    Xie F et al (2015) Vaccarin attenuates the human EA.hy926 endothelial cell oxidative stress injury through inhibition of Notch signaling. Int J Mol Med 35:135–142.  https://doi.org/10.3892/ijmm.2014.1977 CrossRefPubMedGoogle Scholar
  36. 36.
    Xie PS, Leung AY (2009) Understanding the traditional aspect of Chinese medicine in order to achieve meaningful quality control of Chinese materia medica. J Chromatogr A 1216:1933–1940.  https://doi.org/10.1016/j.chroma.2008.08.045 CrossRefPubMedGoogle Scholar
  37. 37.
    Yadav AK, Temjenmongla (2012) Efficacy of Lasia spinosa leaf extract in treating mice infected with Trichinella spiralis. Parasitol Res 110:493–498.  https://doi.org/10.1007/s00436-011-2551-9 CrossRefPubMedGoogle Scholar
  38. 38.
    Zhao X, Pang J (2017) Application of spontaneous photon emission in the growth ages and varieties screening of fresh Chinese herbal medicines. Evid Based Complement Altern Med 2017:2058120.  https://doi.org/10.1155/2017/2058120 CrossRefGoogle Scholar

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2019

Authors and Affiliations

  1. 1.Department of Basic Medicine, Wuxi School of MedicineJiangnan UniversityWuxiPeople’s Republic of China

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