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Anti-allergic effects of Rosae multiflorae fructus via inhibition of T cell proliferation and the mast cell function

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Abstract

Anti-allergic effects of the hot water extract of Rosae multiflorae fructus (Rosae extract), which has long been used in oriental medicine for treatment of various diseases, were explored with a chicken ovalbumin (cOVA)-induced mouse model of food allergy. Compared to the sham mice to show severe allergic symptoms (i.e., anaphylaxis, diarrhea and decrease in the body temperature) following oral cOVA challenge, the Rosae extract-treated mice showed a marked improvement in those symptoms. Histology data demonstrated that Rosae extract treatment resulted in a amelioration in the intestinal inflammatory lesion and a reduction in the numbers of mast cells and eosinophils in the small intestine. Studies using DO11.10 TCR transgenic T cells indicated that Rosae extract had an activity to subdue the antigen-specific T cell activation/proliferation in vivo and thereby to lower the level of Th2 cytokine production by T cells during the antigen-specific immune response. Moreover, passive systemic anaphylaxis study showed that the extract also had an activity to inhibit the mast cells function in vivo, i.e., release of granules triggered by specific IgE-antigen interaction. Altogether, the results from this study not only imply a potential clinical application of Rosae extract in prevention and treatment of food allergy but also clearly elucidate the immunoregulatory mechanisms of Rosae extract underlying its anti-allergic effect.

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References

  1. Sicherer SH, Sampson HA (2009) Food allergy: recent advances in pathophysiology and treatment. Ann Rev Med 60:261–277

    Article  CAS  Google Scholar 

  2. Flokstra-de Blok BM, Dubois AE, Vlieg-Boerstra BJ, Oude Elberink JN, Raat H, DunnGalvin A, Hourihane JO, Duiverman EJ (2010) Health-related quality of life of food allergic patients: comparison with the general population and other diseases. Allergy 65:238–244

    Article  CAS  Google Scholar 

  3. Gupta RS, Springston EE, Warrier MR, Smith B, Kumar R, Pongracic J, Holl JL (2011) The prevalence, severity, and distribution of childhood food allergy in the United States. Pediatrics 128:e9–17

    Article  Google Scholar 

  4. Prescott SL, Pawankar R, Allen K, Campbell DE, Sinn JKH, Fiocchi A, Ebisawa M, Sampson HA, Beyer K, Lee BW (2013) A global survey of changing patterns of food allergy burden in children. World Allergy Organ J 6:21

    Article  Google Scholar 

  5. Devereux G (2006) The increase in the prevalence of asthma and allergy: food for thought. Nat Rev Immunol 6:869–874

    Article  CAS  Google Scholar 

  6. Berin MC, Sampson HA (2013) Mucosal immunology of food allergy. Curr Biol CB 23:R389–R400

    Article  CAS  Google Scholar 

  7. Bischoff SC, Mayer JH, Manns MP (2000) Allergy and the gut. Int Arch Allergy Immunol 121:270–283

    Article  CAS  Google Scholar 

  8. Cianferoni A, Spergel JM (2009) Food allergy: review, classification and diagnosis. Allergol Int Off J Jpn Soc Allergol 58:457–466

    Article  CAS  Google Scholar 

  9. Bischoff SC (2007) Role of mast cells in allergic and non-allergic immune responses: comparison of human and murine data. Nat Rev Immunol 7:93–104

    Article  CAS  Google Scholar 

  10. Galli SJ (2000) Mast cells and basophils. Curr Opin Hematol 7:32–39

    Article  CAS  Google Scholar 

  11. Liang HE, Reinhardt RL, Bando JK, Sullivan BM, Ho IC, Locksley RM (2012) Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity. Nat Immunol 13:58–66

    Article  CAS  Google Scholar 

  12. Wynn TA (2015) Type 2 cytokines: mechanisms and therapeutic strategies. Nat Rev Immunol 15:271–282

    Article  CAS  Google Scholar 

  13. Cheng A (2011) Emergency treatment of anaphylaxis in infants and children. Paediatr Child Health 16:35–40

    CAS  Google Scholar 

  14. Syed A, Kohli A, Nadeau KC (2013) Food allergy diagnosis and therapy: where are we now? Immunotherapy 5:931–944

    Article  CAS  Google Scholar 

  15. Berin MC, Mayer L (2013) Can we produce true tolerance in patients with food allergy? J Allergy Clin Immunol 131:14–22

    Article  CAS  Google Scholar 

  16. Buchanan AD, Green TD, Jones SM, Scurlock AM, Christie L, Althage KA, Steele PH, Pons L, Helm RM, Lee LA, Burks AW (2007) Egg oral immunotherapy in nonanaphylactic children with egg allergy. J Allergy Clin Immunol 119:199–205

    Article  CAS  Google Scholar 

  17. Dan B (1993) Gamble A: Chinese Herbal Medicine. In Materia Medica Revised ed Seattle: Eastland Press

  18. Burns JJ, Zhao L, Taylor EW, Spelman K (2010) The influence of traditional herbal formulas on cytokine activity. Toxicology 278:140–159

    Article  CAS  Google Scholar 

  19. Chung MY, Shin HS, Choi DW, Shon DH (2016) Citrus tachibana leaf extract mitigates symptoms of food allergy by inhibiting Th2-Associated responses. J Food Sci 81:H1537–H1545

    Article  CAS  Google Scholar 

  20. Song Y, Qu C, Srivastava K, Yang N, Busse P, Zhao W, Li XM (2010) Food allergy herbal formula 2 protection against peanut anaphylactic reaction is via inhibition of mast cells and basophils. J Allergy Clin Immunol 126(1208–1217):e1203

    Google Scholar 

  21. Joon H (2012) Donguibogam; The Principles and Practice of Eastern Medicine

  22. Li X (2002) Chinese materia medica: combinations and applications, 1st edn. Elsevier, Amsterdam

    Google Scholar 

  23. Jo Y-Y (2011) Agricultural and marine products that are allowed to be used other than food. http://www.mfdsgokr/seoul/indexdo?mid=58&pageNo=17&seq=12315&cmd=v

  24. Cheng BC, Ma XQ, Kwan HY, Tse KW, Cao HH, Su T, Shu X, Wu ZZ, Yu ZL (2014) A herbal formula consisting of Rosae Multiflorae Fructus and Lonicerae Japonicae Flos inhibits inflammatory mediators in LPS-stimulated RAW 264.7 macrophages. J Ethnopharmacol 153:922–927

    Article  Google Scholar 

  25. Cheng BC, Yu H, Guo H, Su T, Fu XQ, Li T, Cao HH, Tse AK, Wu ZZ, Kwan HY, Yu ZL (2016) A herbal formula comprising Rosae Multiflorae Fructus and Lonicerae Japonicae Flos, attenuates collagen-induced arthritis and inhibits TLR4 signalling in rats. Sci Rep 6:20042

    Article  CAS  Google Scholar 

  26. Plaza M, Turner C (2015) Pressurized hot water extraction of bioactives. TrAC Trends Anal Chem 71:39–54

    Article  CAS  Google Scholar 

  27. Brandt EB, Strait RT, Hershko D, Wang Q, Muntel EE, Scribner TA, Zimmermann N, Finkelman FD, Rothenberg ME (2003) Mast cells are required for experimental oral allergen-induced diarrhea. J Clin Investig 112:1666–1677

    Article  CAS  Google Scholar 

  28. Meyerholz DK, Griffin MA, Castilow EM, Varga SM (2009) Comparison of histochemical methods for murine eosinophil detection in a RSV vaccine-enhanced inflammation model. Toxicol Pathol 37:249–255

    Article  Google Scholar 

  29. Sridharan G, Shankar AA (2012) Toluidine blue: a review of its chemistry and clinical utility. J Oral Maxillofac Pathol 16:251–255

    Article  Google Scholar 

  30. Ovary Z (1958) Passive cutaneous anaphylaxis in the mouse. J Immunol 81:355–357

    CAS  Google Scholar 

  31. Wex E, Thaler E, Blum S, Lamb D (2014) A novel model of IgE-mediated passive pulmonary anaphylaxis in rats. PLoS One 9:e116166

    Article  Google Scholar 

  32. Kearney ER, Pape KA, Loh DY, Jenkins MK (1994) Visualization of peptide-specific T cell immunity and peripheral tolerance induction in vivo. Immunity 1:327–339

    Article  CAS  Google Scholar 

  33. Shepherd DM, Dearstyne EA, Kerkvliet NI (2000) The effects of TCDD on the activation of ovalbumin (OVA)-specific DO11.10 transgenic CD4(+) T cells in adoptively transferred mice. Toxicol Sci Off J Soc Toxicol 56:340–350

    Article  CAS  Google Scholar 

  34. Venetianer A, Aranyi P, Bosze ZS, Fachet J (1978) Sensitivity to glucocorticoids of lymph node cells stimulated in vivo by oxazolone. Scand J Immunol 8:355–362

    Article  CAS  Google Scholar 

  35. McKay LI, Cidlowski JA (2003) Physiologic and Pharmacologic Effects of Corticosteroids. 6th edn

  36. Burton OT, Darling AR, Zhou JS, Noval-Rivas M, Jones TG, Gurish MF, Chatila TA, Oettgen HC (2013) Direct effects of IL-4 on mast cells drive their intestinal expansion and increase susceptibility to anaphylaxis in a murine model of food allergy. Mucosal Immunol 6:740–750

    Article  CAS  Google Scholar 

  37. Stone KD, Prussin C, Metcalfe DD (2010) IgE, mast cells, basophils, and eosinophils. J Allergy Clin Immunol 125:S73–S80

    Article  Google Scholar 

  38. Martin LB, Kita H, Leiferman KM, Gleich GJ (1996) Eosinophils in allergy: role in disease, degranulation, and cytokines. Int Arch Allergy Immunol 109:207–215

    Article  CAS  Google Scholar 

  39. Oka T, Rios EJ, Tsai M, Kalesnikoff J, Galli SJ (2013) Rapid desensitization induces internalization of antigen-specific IgE on mouse mast cells. J Allergy Clin Immunol 132(922–932):e16

    Google Scholar 

  40. Huang K (1999) The pharmacology of Chinese herbs, 2nd edn. CRC Press, Boca Raton, pp 118–120

    Google Scholar 

  41. Cheng BCY, Yu H, Su T, Fu XQ, Guo H, Li T, Cao HH, Tse AKW, Kwan HY, Yu ZL (2015) A herbal formula comprising Rosae Multiflorae Fructus and Lonicerae Japonicae Flos inhibits the production of inflammatory mediators and the IRAK-1/TAK1 and TBK1/IRF3 pathways in RAW 264.7 and THP-1 cells. J Ethnopharmacol 174:195–199

    Article  CAS  Google Scholar 

  42. Song CH, Bui TT, Piao CH, Shin HS, Shon DH, Han EH, Kim HT, Chai OH (2016) Rosae multiflorae fructus hot water extract inhibits a murine allergic asthma via the suppression of Th2 cytokine production and histamine release from mast cells. J Med Food 19:853–859

    Article  CAS  Google Scholar 

  43. Tixier E, Lalanne F, Just I, Galmiche JP, Neunlist M (2005) Human mucosa/submucosa interactions during intestinal inflammation: involvement of the enteric nervous system in interleukin-8 secretion. Cell Microbiol 7:1798–1810

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Linying Li and Sojin Choi in College of Pharmacy, Chungnam National University, for technical supports and discussions. We also thank Daewoon Choi and Hyejeong Shi in Korea Food Research Institute for preparation of Rosae extract. This work was supported by CNU Research Grant (2015-1858-01), a grant for Institute of Drug Research and Development in College of Pharmacy (CNU) (Natonal Research Foundation of Korea), grants from National Research Foundation of Korea (NRF-2015R1D1A1A02062348 and NRF-2014K1A4A3069114) and a grant from Korea Food Research Institute (E0121304-05). Nguyen Thi Minh Nguyet and Maria Lomunova are supported by BK21 Plus program by National Research Foundation of Korea.

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Authors and Affiliations

  1. College of Pharmacy, Chungnam National University, 99 Daehak-ro Yuseong-gu, Daejeon, 305-764, Republic of Korea

    Thi Minh Nguyet Nguyen, Maria Lomunova, Young Ho Kim & Inkyu Hwang

  2. Division of Nutrition and Functionality Research, Korea Food Research Institute, Seongnam, Gyeonggi-do, Republic of Korea

    Hee Soon Shin

  3. Division of Functional Food Research, Korea Food Research Institute, Seongnam, Gyeonggi-do, Republic of Korea

    Dong-Hwa Shon

  4. Division of Food Biotechnology, University of Science and Technology, Seongnam, Gyeonggi-do, Republic of Korea

    Hee Soon Shin & Dong-Hwa Shon

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  1. Thi Minh Nguyet Nguyen
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  2. Maria Lomunova
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Correspondence to Inkyu Hwang.

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Nguyen, T.M.N., Lomunova, M., Shin, H.S. et al. Anti-allergic effects of Rosae multiflorae fructus via inhibition of T cell proliferation and the mast cell function. Appl Biol Chem 60, 391–402 (2017). https://doi.org/10.1007/s13765-017-0292-x

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