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Vitamin A Deficiency Promotes Inflammation by Induction of Type 2 Cytokines in Experimental Ovalbumin-Induced Asthma Murine Model

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Abstract

Vitamin A (VA) deficiency is one of the most common malnutrition conditions. Recent reports showed that VA plays an important role in the immune balance; lack of VA could result in enhanced type 2 immune response characterized by increased type 2 cytokine production and type 2 innate lymphoid cell infiltration and activation. Type 2 immune response plays protective role in anti-infection but plays pathological role in asthmatic disease. In order to investigate the role of VA in the asthmatic disease, we used ovalbumin-induced asthma murine model and observed the pathological changes between mouse-received VA-deficient and VA-sufficient diets. We also measured the type 2 cytokine expressions to reveal the potential mechanism. Our results showed that VA deficiency exacerbates ovalbumin-induced lung inflammation and type 2 cytokine productions. Thus, VA deficiency, or malnutrition in further extent, may contribute to the increasing prevalence of asthma.

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References

  1. Braman, S.S. 2006. The global burden of asthma. Chest 130: 4S–12S.

    Article  PubMed  Google Scholar 

  2. Platts-Mills, T.A. 2015. The allergy epidemics: 1870-2010. Journal of Allergy and Clinical Immunology 136: 3–13.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Galli, S.J. 2016. The mast cell-IgE paradox: from homeostasis to anaphylaxis. American Journal of Pathology 186: 212–224.

    Article  CAS  PubMed  Google Scholar 

  4. Urb, M., and D.C. Sheppard. 2012. The role of mast cells in the defence against pathogens. PLoS Pathogens 8: e1002619.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Zissler UM, Esser-von Bieren J, Jakwerth CA, Chaker AM, Schmidt-Weber CB. Current and future biomarkers in allergic asthma. Allergy. 2015

  6. Eberl, G., J.P. Di Santo, and E. Vivier. 2015. The brave new world of innate lymphoid cells. Nature Immunology 16: 1–5.

    Article  CAS  PubMed  Google Scholar 

  7. Kim, H.Y., D.T. Umetsu, and R.H. Dekruyff. 2016. Innate lymphoid cells in asthma: will they take your breath away? European Journal of Immunology 46(4): 795–806.

    Article  CAS  PubMed  Google Scholar 

  8. Chung, K.F. 2015. Targeting the interleukin pathway in the treatment of asthma. Lancet 386: 1086–1096.

    Article  CAS  PubMed  Google Scholar 

  9. Schaible, U.E., and S.H. Kaufmann. 2007. Malnutrition and infection: complex mechanisms and global impacts. PLoS Medicine 4: e115.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Zeng, H., and H. Chi. 2015. Metabolic control of regulatory T cell development and function. Trends in Immunology 36: 3–12.

    Article  CAS  PubMed  Google Scholar 

  11. Spencer, S.P., C. Wilhelm, Q. Yang, J.A. Hall, N. Bouladoux, A. Boyd, T.B. Nutman, J.F. Urban Jr., J. Wang, T.R. Ramalingam, et al. 2014. Adaptation of innate lymphoid cells to a micronutrient deficiency promotes type 2 barrier immunity. Science 343: 432–437.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Julia, V., L. Macia, and D. Dombrowicz. 2015. The impact of diet on asthma and allergic diseases. Nature Reviews Immunology 15: 308–322.

    Article  CAS  PubMed  Google Scholar 

  13. Li, D., R. Guabiraba, A.G. Besnard, M. Komai-Koma, M.S. Jabir, L. Zhang, G.J. Graham, M. Kurowska-Stolarska, F.Y. Liew, C. McSharry, and D. Xu. 2014. IL-33 promotes ST2-dependent lung fibrosis by the induction of alternatively activated macrophages and innate lymphoid cells in mice. Journal of Allergy and Clinical Immunology 134: 1422–1432. e1411.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Hall, J.A., J.R. Grainger, S.P. Spencer, and Y. Belkaid. 2011. The role of retinoic acid in tolerance and immunity. Immunity 35: 13–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Nurmatov, U., G. Devereux, and A. Sheikh. 2011. Nutrients and foods for the primary prevention of asthma and allergy: systematic review and meta-analysis. Journal of Allergy and Clinical Immunology 127: 724–733 e721-730.

    Article  PubMed  Google Scholar 

  16. Luo, Z.X., E.M. Liu, J. Luo, F.R. Li, S.B. Li, F.Q. Zeng, P. Qu, Z. Fu, and T.Y. Li. 2010. Vitamin A deficiency and wheezing. World Journal of Pediatrics 6: 81–84.

    Article  CAS  PubMed  Google Scholar 

  17. Al Senaidy, A.M. 2009. Serum vitamin A and beta-carotene levels in children with asthma. Journal of Asthma 46: 699–702.

    Article  CAS  PubMed  Google Scholar 

  18. Checkley, W., K.P. West Jr., R.A. Wise, L. Wu, S.C. LeClerq, S. Khatry, J. Katz, P. Christian, J.M. Tielsch, and A. Sommer. 2011. Supplementation with vitamin A early in life and subsequent risk of asthma. European Respiratory Journal 38: 1310–1319.

    Article  CAS  PubMed  Google Scholar 

  19. Arora, P., V. Kumar, and S. Batra. 2002. Vitamin A status in children with asthma. Pediatric Allergy and Immunology 13: 223–226.

    Article  PubMed  Google Scholar 

  20. Pushparaj, P.N., D. Li, M. Komai-Koma, R. Guabiraba, J. Alexander, C. McSharry, and D. Xu. 2013. Interleukin-33 exacerbates acute colitis via interleukin-4 in mice. Immunology 140: 70–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Kurowska-Stolarska, M., B. Stolarski, P. Kewin, G. Murphy, C.J. Corrigan, S. Ying, N. Pitman, A. Mirchandani, B. Rana, N. van Rooijen, et al. 2009. IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation. Journal of Immunology 183: 6469–6477.

    Article  CAS  Google Scholar 

  22. Stolarski, B., M. Kurowska-Stolarska, P. Kewin, D. Xu, and F.Y. Liew. 2010. IL-33 exacerbates eosinophil-mediated airway inflammation. Journal of Immunology 185: 3472–3480.

    Article  CAS  Google Scholar 

  23. Johnston, R.A., M. Zhu, Y.M. Rivera-Sanchez, F.L. Lu, T.A. Theman, L. Flynt, and S.A. Shore. 2007. Allergic airway responses in obese mice. American Journal of Respiratory and Critical Care Medicine 176: 650–658.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Grieger, J.A., L.G. Wood, and V.L. Clifton. 2013. Improving asthma during pregnancy with dietary antioxidants: the current evidence. Nutrients 5: 3212–3234.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Ertesvag, A., N. Engedal, S. Naderi, and H.K. Blomhoff. 2002. Retinoic acid stimulates the cell cycle machinery in normal T cells: involvement of retinoic acid receptor-mediated IL-2 secretion. Journal of Immunology 169: 5555–5563.

    Article  CAS  Google Scholar 

  26. Dennert, G., and R. Lotan. 1978. Effects of retinoic acid on the immune system: stimulation of T killer cell induction. European Journal of Immunology 8: 23–29.

    Article  CAS  PubMed  Google Scholar 

  27. Kim, M.H., E.J. Taparowsky, and C.H. Kim. 2015. Retinoic acid differentially regulates the migration of innate lymphoid cell subsets to the gut. Immunity 43: 107–119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Mari, N., M. Hercor, S. Denanglaire, O. Leo, and F. Andris. 2013. The capacity of Th2 lymphocytes to deliver B-cell help requires expression of the transcription factor STAT3. European Journal of Immunology 43: 1489–1498.

    Article  CAS  PubMed  Google Scholar 

  29. Kurowska-Stolarska, M., P. Kewin, G. Murphy, R.C. Russo, B. Stolarski, C.C. Garcia, M. Komai-Koma, N. Pitman, Y. Li, W. Niedbala, et al. 2008. IL-33 induces antigen-specific IL-5+ T cells and promotes allergic-induced airway inflammation independent of IL-4. Journal of Immunology 181: 4780–4790.

    Article  CAS  Google Scholar 

  30. Mora, J.R., M. Iwata, and U.H. von Andrian. 2008. Vitamin effects on the immune system: vitamins A and D take centre stage. Nature Reviews Immunology 8: 685–698.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 81501423) and Norman Bethune Program of Jilin University (No. 2015223).

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Correspondence to Xun Zhu or Dong Li.

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The authors declare that they have no conflict of interest.

Key Findings:

1. Vitamin A deficiency exacerbates inflammations in an asthmatic setting.

2. Vitamin A deficiency promotes the production of type 2 cytokines like IL-4, IL-5, and IL-13.

Additional information

Weiwei Cui and Peng Zhang contributed equally to this work.

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Cui, W., Zhang, P., Gu, J. et al. Vitamin A Deficiency Promotes Inflammation by Induction of Type 2 Cytokines in Experimental Ovalbumin-Induced Asthma Murine Model. Inflammation 39, 1798–1804 (2016). https://doi.org/10.1007/s10753-016-0415-2

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