Antimicrobial Acylphloroglucinol Meroterpenoids and Acylphloroglucinols from Dryopteris crassirhizoma

Ping Hai; Yunqing He; Ruirui Wang; Jian Yang; Yuan Gao; Xudong Wu; Nie Chen; Li Ye; Rongtao Li

doi:10.1055/a-1917-7910

Planta Medica, Table of Contents

Planta Med 2023; 89(03): 295-307
DOI: 10.1055/a-1917-7910

Biological and Pharmacological Activity

Original Papers

Antimicrobial Acylphloroglucinol Meroterpenoids and Acylphloroglucinols from Dryopteris crassirhizoma

Ping Hai

¹Faculty of Life Science and Technology, Kunming University of Science and Technology, Kunming, China

,

Yunqing He

²Faculty of Materials and Chemical Engineering, Yibin University, Yibin, China

,

Ruirui Wang

³School of Pharmaceutical Sciences, Yunnan University of Chinese Medicine, Kunming, China

,

Jian Yang

⁴State Key Laboratory Breeding Base of Dao-di Herbs, National Resource Center for Chinese Materia Medical, China Academy of Chinese Medical Sciences, Beijing, China

,

Yuan Gao

²Faculty of Materials and Chemical Engineering, Yibin University, Yibin, China

,

Xudong Wu

²Faculty of Materials and Chemical Engineering, Yibin University, Yibin, China

,

Nie Chen

²Faculty of Materials and Chemical Engineering, Yibin University, Yibin, China

,

Li Ye

²Faculty of Materials and Chemical Engineering, Yibin University, Yibin, China

,

Rongtao Li

¹Faculty of Life Science and Technology, Kunming University of Science and Technology, Kunming, China

› Author Affiliations

Abstract

Ten novel meroterpenoids, dryoptins/11″-epi-dryoptins A~E (1~10) with an unprecedented skeleton consisting of dimeric or trimeric acylphloroglucinols and dehydrotheonelline, two undescribed acylphloroglucinol-nerolidol meroterpenoids (11~12), and ten known acylphloroglucinol derivatives (13~22), were isolated from D. crassirhizoma. The novel structures including absolute configurations were established by comprehensive spectroscopic analyses and quantum chemical electronic circular dichroism (ECD) calculations. A biosynthetic pathway of 1~10 was assumed. The trimeric acylphloroglucinol meroterpenoids 7/8 showed significant antifungal activity against standard Candida albicans with a MIC₅₀ value of 1.61 µg/mL [fluconazole (FLC): 3.41 µg/mL], and when combined with FLC, the principal components 20 and 21 exhibited strong antifungal activities against FLC-resistant C. albicans with MIC₅₀ values of 8.39 and 7.16 µg/mL (FLC: > 100 µg/mL), respectively. Moreover, compounds 2, 5/6, 18, 19, and 21 exhibited inhibitory effects against several pathogenic fungi and bacteria, with MIC₅₀ values of 6.25 ~ 50 µg/mL.

Key words

Dryopteridaceae - Dryopteris crassirhizoma - acylphloroglucinol-meroterpenoid - acylphloroglucinol - Candida albicans - antifungal activity

Full Text

References

References
1 Zhang LB. Flora of China. Beijing: Science Press; 2013: 5714
2 Lian YQ, Wang XN, Chen ZC, Liu BD. Studies on the using of Dryopteris crassirhizoma Nakai. Zhongguo yesheng zhiwu ziyuan 2005; 24: 29-32
3 Chen X, Wu Y, Chen C, Gu Y, Zhu C, Wang S, Chen J, Zhang L, Lv L, Zhang G, Yuan Y, Chai Y, Zhu M, Wu C. Identifying potential anti-COVID-19 pharmacological components of traditional Chinese medicine Lianhuaqingwen capsule based on human exposure and ACE2 biochromatography screening. Acta Pharm Sin B 2021; 11: 222-236
4 Yu BF, Zheng X, Ni YF. Observation on the curative effect of Kang gan ke li in the treatment of 62 children with acute upper respiratory tract infection. West China J Pharm Sciences 2008; 23: 732
5 Chen N, Wu Z, Li W, Li Y, Luo D, Chen L, Zhang X, Zhang Y, Guocai W, Li Y. Acylphloroglucinols-based meroterpenoid enantiomers with antiviral activities from Dryopteris crassirhizoma . Ind Crop Prod 2020; 150: 112415
6 Ban SH, Kim JE, Pandit S, Jeon JG. Influences of Dryopteris crassirhizoma extract on the viability, growth and virulence properties of Streptococcus mutans . Molecules 2012; 17: 9231-9244
7 Wang J, Yan YT, Fu SZ, Peng B, Bao LL, Zhang YL, Hu JH, Zeng ZP, Geng DH, Gao ZP. Anti-influenza virus (H5N1) activity screening on the phloroglucinols from rhizomes of Dryopteris crassirhizoma . Molecules 2017; 22: 431
8 Hou B, Liu Z, Yang XB, Zhu WF, Li JY, Yang L, Reng FC, Lv YF, Hu JM, Liao GY, Zhou J. Total synthesis of dryocrassin ABBA and its analogues with potential inhibitory activity against drug-resistant neuraminidases. Bioorg Med Chem 2019; 27: 3846-3852
9 Yim NH, Lee JJ, Lee B, Li W, Ma JY. Antiplatelet activity of acylphloroglucinol derivatives isolated from Dryopteris crassirhizoma . Molecules 2019; 24: 2212-2222
10 Hai P, Rao K, Jiang N, Liu D, Wang R, Gao Y, Liu X, Deng S, Zhou Y, Chen X, Li X, Li R. Structure elucidation, biogenesis, and bioactivities of acylphloroglucinol-derived meroterpenoid enantiomers from Dryopteris crassirhizoma . Bioorg Chem 2022; 119: 105567
11 Chen N, Li W, Zhang J, Xu W, Wu Z, Li Y, Zhang Y, Zhang Q, Wang G. Isolation and structural elucidation of β-tocopherol derivatives from Dryopteris crassirhizoma . Ind Crop Prod 2021; 172: 114010
12 Ng KP, Kuan CS, Kaur H, Na SL, Atiya N, Velayuthan RD. Candida species epidemiology 2000–2013: a laboratory-based report. Trop Med Int Health 2015; 20: 1447-1453
13 Pu D, Li X, Lin J, Zhang R, Luo T, Wang Y, Gao J, Zeb MA, Zhang X, Li X, Wang R, Xiao W. Triterpenoids from Ganoderma gibbosum: a class of sensitizers of FLC-resistant Candida albicans to fluconazole. J Nat Prod 2019; 82: 2067-2077
14 Nidhi P, Rolta R, Kumar V, Dev K, Sourirajan A. Synergistic potential of Citrus aurantium L. essential oil with antibiotics against Candida albicans . J Ethnopharmacol 2020; 262: 113135
15 Ito H, Muranaka T, Mori K, Jin ZX, Tokuda H, Nishino H, Yoshida T. Ichthyotoxic phloroglucinol derivatives from Dryopteris fragrans and their anti-tumor promoting activity. Chem Pharm Bull (Tokyo) 2000; 48: 1190-1195
16 Ccana-Ccapatinta GV, Correa de Barros FM, Bridi H. Dimeric acylphloroglucinols in Hypericum species from sections Brathys and Trigynobrathys . Phytochem Rev 2014; 14: 25-50
17 Na M, Jang J, Min BS, Lee SJ, Lee MS, Kim BY, Oh WK, Ahn JS. Fatty acid synthase inhibitory activity of acylphloroglucinols isolated from Dryopteris crassirhizoma . Bioorg Med Chem Lett 2006; 16: 4738-4742
18 Patama TT, Widen CJ. Phloroglucinol derivatives from Dryopteris fusco-atra and D. hawaiiensis . Phytochemistry 1991; 30: 3305-3310
19 Jia XZ, Li XX, Yuan LB, Yin YQ, Yang XH, Shen ZB. Study on the three kinds of phloroglucinol derivatives of Dryopteris crassirhizoma Nakai and their antifungal activity. J Guangdong Pharm Univ 2016; 32: 582-585
20 Zhao DD, Zhao QS, Liu L, Chen ZQ, Zeng WM, Lei H, Zhang YL. Compounds from Dryopteris fragrans (L.) Schott with cytotoxic activity. Molecules 2014; 19: 3345-3355
21 Tanaka N, Maehashi H, Saito S, Murakami T, Saiki Y, Chen G, Iitaka Y. Chemical and chemotaxonomical studies of ferns. XXXI. Chemical studies on the constituents of Arachinoides standishii Ohwi. Chem Pharm Bull 1980; 28: 3070-3077
22 Ito H, Midori T, Mori K, Jin ZX, Yoshida T. Dryofragin and aspidin PB, piscicidal components from Dryopteris fragrans . Chem Pharm Bull 1997; 45: 1720-1722
23 Zdero C, Lehmann L, Bohlmann F. Chemotaxonomy of Athanasia and related genera. Phytochemistry 1991; 30: 1161-1163
24 Gao ZP, Ali Z, Zhao JP, Qiao L, Lei HM, Lu YR, Ikhlas AK. Phytochemical investigation of the rhizomes of Dryopteris crassirhizoma . Phytochem Lett 2008; 1: 188-190
25 Bifulco G, Dambruoso P, Gomez-Paloma L, Riccio R. Determination of relative configuration in organic compounds by NMR spectroscopy and computational methods. Chem Rev 2007; 107: 3744-3779
26 Gao ZP, Li RF, Wang BH, Lu RW. Progress in chemical constituents of genus Dryopteris. Chin. J Experimental Traditional Med Formulae 2003; 9: 50-55
27 Van De Water RW, Pettus TRR. o-Quinone methides: intermediates underdeveloped and underutilized in organic synthesis. Tetrahedron 2002; 58: 5367-5405
28 Lam HC, Spence JT, George JH. Biomimetic total synthesis of hyperjapones A–E and hyperjaponols A and C. Angew Chem Int Ed Engl 2016; 55: 10368-10371
29 CLSI. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard – Third Edition. CLSI document M27-A3. Wayne, PA: Clinical and Laboratory Standards Institute; 2008
30 Liu Y, Ren H, Wang D, Zhang M, Sun S, Zhao Y. The synergistic antifungal effects of gypenosides combined with fluconazole against resistant Candida albicans via inhibiting the drug efflux and biofilm formation. Biomed Pharmacother 2020; 130: 110580
31 Zhao W, Xu LL, Zhang X, Gong XW, Zhu DL, Xu XH, Wang F, Yang XL. Three new phenanthrenes with antimicrobial activities from the aerial parts of Juncus effuses . Fitoterapia 2018; 130: 247-250

Supplementary Material

Supporting Information