Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
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Alisol B 23-Acetate Ameliorates Ovalbumin-Induced Allergic Asthma during Sensitization and Challenge Periods

  • Ki-Hyuk Nam (Department of Pharmaceutical Sciences, College of Pharmacy, Kyung Hee University) ;
  • Dong-Soon Im (Department of Fundamental Pharmaceutical Sciences, Graduate School, Kyung Hee University)
  • Received : 2023.02.18
  • Accepted : 2023.04.17
  • Published : 2023.11.01
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Abstract

Rhizome of Alisma orientale has been used as a traditional medicine for treating kidney diseases in East Asian countries. Its inhibitory effects on hypersensitivity responses have been reported for methanol extracts, with alisol B 23-acetate (AB23Ac) being the most active constituent among six terpenes in inhibiting the direct passive Arthus reaction. However, whether AB23Ac has efficacy against allergic asthma has not been tested to date. The in vivo efficacy of AB23Ac in an ovalbumin (OVA)-induced allergic asthma mouse model was evaluated by administrating AB23Ac before OVA sensitization or OVA challenge in BALB/c mice. AB23Ac suppressed antigen-induced degranulation of RBL-2H3 mast cells in a concentration-dependent manner. The administration of AB23Ac both before OVA sensitization and OVA challenge greatly lowered pulmonary resistance and the increase in immune cell counts and inflammatory responses around the peribronchial and perivascular regions. In addition, the inflammatory cytokine levels of Th1/Th2/Th17 cells in the bronchoalveolar lavage fluid decreased in the AB23Ac-treated groups. AB23Ac reduced the number of PAS-stained cells in the lungs. Furthermore, a computer modeling study indicated that AB23Ac can bind tightly to spleen tyrosine kinase (Syk). These results suggest that AB23Ac may ameliorate allergic asthma by suppressing immune responses in dendritic cells during sensitization and in mast cells during challenge periods.

Keywords

Acknowledgement

This research was supported by the Basic Research Laboratory Program (BRL) and the Basic Science Research Program of the Korean National Research Foundation funded by the Korean Ministry of Science, ICT, and Future Planning (NRF-2020R1A4A1016142, NRF-2023R1A2C2002380, and NRF-2019R1A2C1005523).

References

  1. Akdis, C. A., Arkwright, P. D., Bruggen, M.-C., Busse, W., Gadina, M., Guttman-Yassky, E., Kabashima, K., Mitamura, Y., Vian, L., Wu, J. and Palomares, O. (2020) Type 2 immunity in the skin and lungs. Allergy 75, 1582-1605. https://doi.org/10.1111/all.14318
  2. Bhatiaa, M., Chaudharya, J., Jaina, A. and Pareekb, B. (2022) Pathophysiology and management of asthma. In Contemporary Aadvances in Science & Technology Volume-IV (R. Singh, Ed.), pp. 17-42. Notion Press, New Delhi.
  3. Duman, B., Borekci, S., Akdeniz, N., Gazioglu, S. B., Deniz, G. and Gemicioglu, B. (2022) Inhaled corticosteroids' effects on biomarkers in exhaled breath condensate and blood in patients newly diagnosed with asthma who smoke. J. Asthma 59, 1613-1620. https://doi.org/10.1080/02770903.2021.1962341
  4. Hesse, L., Elberink, J. O., van Oosterhout, A. J. and Nawijn, M. C. (2022) Allergen immunotherapy for allergic airway diseases: use lessons from the past to design a brighter future. Pharmacol. Ther. 237, 108115.
  5. Kao, S. T., Wang, S. D., Lin, C. C. and Lin, L. J. (2018) Jin Gui Shen Qi Wan, a traditional Chinese medicine, alleviated allergic airway hypersensitivity and inflammatory cell infiltration in a chronic asthma mouse model. J. Ethnopharmacol. 227, 181-190. https://doi.org/10.1016/j.jep.2018.08.028
  6. Kim, G. Y., Song, C. W., Yang, Y.-S., Lee, N.-R., Yoo, H.-S., Son, S. H., Lee, S. J., Park, J. S., Lee, J. K., Inn, K.-S. and Kim, N. J. (2021) Chemical degradation of androgen receptor (AR) using bicalutamide analog-thalidomide PROTACs. Molecules 26, 2525.
  7. Kubo, M., Matsuda, H., Tomohiro, N. and Yoshikawa, M. (1997) Studies on Alismatis rhizoma. I. Anti-allergic effects of methanol extract and six terpene components from Alismatis rhizoma (dried rhizome of Alisma orientale). Biol. Pharm. Bull. 20, 511-516. https://doi.org/10.1248/bpb.20.511
  8. Lee, J.-H. and Im, D.-S. (2021a) 4-CMTB ameliorates ovalbumininduced allergic asthma through FFA2 activation in mice. Biomol. Ther. (Seoul) 29, 427-433. https://doi.org/10.4062/biomolther.2020.176
  9. Lee, J.-H., Son, S.-H., Kim, N.-J. and Im, D.-S. (2023) NJK14047 suppression of the p38 MAPK ameliorates OVA-induced allergic asthma during sensitization and challenge periods. Biomol. Ther. (Seoul) 31, 183-192. https://doi.org/10.4062/biomolther.2022.078
  10. Lee, J. E. and Im, D. S. (2021b) Suppressive effect of carnosol on ovalbumin- induced allergic asthma. Biomol. Ther. (Seoul) 29, 58-63. https://doi.org/10.4062/biomolther.2020.050
  11. Lee, J. H., Kwon, O. S., Jin, H. G., Woo, E. R., Kim, Y. S. and Kim, H. P. (2012) The rhizomes of Alisma orientale and alisol derivatives inhibit allergic response and experimental atopic dermatitis. Biol. Pharm. Bull. 35, 1581-1587. https://doi.org/10.1248/bpb.b110689
  12. Lee, Y.-J. and Im, D.-S. (2022) Efficacy comparison of LPA2 antagonist H2L5186303 and agonist GRI977143 on ovalbumin-induced allergic asthma in BALB/c mice. Int. J. Mol. Sci. 23, 9745.
  13. Matsubara, S., Koya, T., Takeda, K., Joetham, A., Miyahara, N., Pine, P., Masuda, E. S., Swasey, C. H. and Gelfand, E. W. (2006a) Syk activation in dendritic cells is essential for airway hyperresponsiveness and inflammation. Am. J. Respir. Cell Mol. Biol. 34, 426-433. https://doi.org/10.1165/rcmb.2005-0298OC
  14. Matsubara, S., Li, G., Takeda, K., Loader, J. E., Pine, P., Masuda, E. S., Miyahara, N., Miyahara, S., Lucas, J. J., Dakhama, A. and Gelfand, E. W. (2006b) Inhibition of spleen tyrosine kinase prevents mast cell activation and airway hyperresponsiveness. Am. J. Respir. Crit. Care Med. 173, 56-63. https://doi.org/10.1164/rccm.200503-361OC
  15. Matsuda, H., Tomohiro, N., Yoshikawa, M. and Kubo, M. (1998) Studies on Alismatis Rhizoma. II. Anti-complementary activities of methanol extract and terpene components from Alismatis Rhizoma (dried rhizome of Alisma orientale). Biol. Pharm. Bull. 21, 1317-1321. https://doi.org/10.1248/bpb.21.1317
  16. Meng, Q., Chen, X., Wang, C., Liu, Q., Sun, H., Sun, P., Peng, J. and Liu, K. (2014) Alisol B 23-acetate promotes liver regeneration in mice after partial hepatectomy via activating farnesoid X receptor. Biochem. Pharmacol. 92, 289-298. https://doi.org/10.1016/j.bcp.2014.09.009
  17. Nakashima, K., Kokubo, T., Shichijo, M., Li, Y. F., Yura, T. and Yamamoto, N. (2004) A novel Syk kinase-selective inhibitor blocks antigen presentation of immune complexes in dendritic cells. Eur. J. Pharmacol. 505, 223-228. https://doi.org/10.1016/j.ejphar.2004.10.024
  18. Scarlata, S. and Incalzi, R. A. (2022) Chronic obstructive pulmonary disease and asthma. In Pathy's Principles and Practice of Geriatric Medicine, pp. 542-554.
  19. Sedlik, C., Orbach, D., Veron, P., Schweighoffer, E., Colucci, F., Gamberale, R., Ioan-Facsinay, A., Verbeek, S., Ricciardi-Castagnoli, P., Bonnerot, C., Tybulewicz, V. L., Di Santo, J. and Amigorena, S. (2003) A critical role for Syk protein tyrosine kinase in Fc receptormediated antigen presentation and induction of dendritic cell maturation. J. Immunol. 170, 846-852. https://doi.org/10.4049/jimmunol.170.2.846
  20. Shao, C., Fu, B., Ji, N., Pan, S., Zhao, X., Zhang, Z., Qiu, Y., Wang, R., Jin, M., Wen, K. and Kong, D. (2018) Alisol B 23-acetate inhibits IgE/Ag-mediated mast cell activation and allergic reaction. Int. J. Mol. Sci. 19, 4092.
  21. Shichijo, M., Yamamoto, N., Tsujishita, H., Kimata, M., Nagai, H. and Kokubo, T. (2003) Inhibition of syk activity and degranulation of human mast cells by flavonoids. Biol. Pharm. Bull. 26, 1685-1690. https://doi.org/10.1248/bpb.26.1685
  22. Son, S.-E., Koh, J.-M. and Im, D.-S. (2022) Activation of free fatty acid receptor 4 (FFA4) ameliorates ovalbumin-induced allergic asthma by suppressing activation of dendritic and mast cells in mice. Int. J. Mol. Sci. 23, 5270.
  23. Sun, Y., Long, J., Chen, W., Sun, Y., Zhou, L., Zhang, L., Zeng, H. and Yuan, D. (2021) Alisol B 23-acetate, a new promoter for cholesterol efflux from dendritic cells, alleviates dyslipidemia and inflammation in advanced atherosclerotic mice. Int. Immunopharmacol. 99, 107956.
  24. Sung, W.-S., Jeon, S.-R., Hong, Y.-J., Kim, T.-H., Shin, S., Lee, H.-J., Seo, B.-K., Park, Y.-C., Kim, E.-J. and Nam, D.-W. (2019) Efficacy, safety, and cost-effectiveness analysis of adjuvant herbal medicine treatment, Palmijihwang-hwan, for chronic low back pain: a study protocol for randomized, controlled, assessor-blinded, multicenter clinical trial. Trials 20, 778.