Antiviral and anti-inflammatory activities of chemical constituents from twigs of Mosla chinensis Maxim

doi:10.1007/s13659-024-00448-w

Abstract

Abstract: Seven undescribed compounds, including three flavones (1–3), one phenylpropanoid (19), three monoaromatic hydrocarbons (27–29), were isolated from the twigs of Mosla chinensis Maxim together with twenty-eight known compounds. The structures were characterized by HRESIMS, 1D and 2D NMR, and ECD spectroscopic techniques. Compound 20 displayed the most significant activity against A/WSN/33/2009 (H1N1) virus ( IC₅₀ = 20.47 μM) compared to the positive control oseltamivir ( IC₅₀ = 6.85 μM). Further research on the anti-influenza mechanism showed that compound 20 could bind to H1N1 virus surface antigen HA1 and inhibit the early attachment stage of the virus. Furthermore, compounds 9, 22, 23, and 25 displayed moderate inhibitory effects on the NO expression in LPS inducing Raw 264.7 cells with IC₅₀ values of 22.78, 20.47, 27.66, and 30.14 μM, respectively.

Key words: Mosla chinensis Maxim, Flavonoids, Phenolic structure, Anti-H1N1 virus activity, Anti-inflammatory activity

摘要： Seven undescribed compounds, including three flavones (1–3), one phenylpropanoid (19), three monoaromatic hydrocarbons (27–29), were isolated from the twigs of Mosla chinensis Maxim together with twenty-eight known compounds. The structures were characterized by HRESIMS, 1D and 2D NMR, and ECD spectroscopic techniques. Compound 20 displayed the most significant activity against A/WSN/33/2009 (H1N1) virus ( IC₅₀ = 20.47 μM) compared to the positive control oseltamivir ( IC₅₀ = 6.85 μM). Further research on the anti-influenza mechanism showed that compound 20 could bind to H1N1 virus surface antigen HA1 and inhibit the early attachment stage of the virus. Furthermore, compounds 9, 22, 23, and 25 displayed moderate inhibitory effects on the NO expression in LPS inducing Raw 264.7 cells with IC₅₀ values of 22.78, 20.47, 27.66, and 30.14 μM, respectively.

关键词: Mosla chinensis Maxim, Flavonoids, Phenolic structure, Anti-H1N1 virus activity, Anti-inflammatory activity

Shi-Yan Feng, Na Jiang, Jia-Ying Yang, Lin-Yao Yang, Jiang-Chao Du, Xuan-Qin Chen, Dan Liu, Rong-Tao Li, Jin-Dong Zhong. Antiviral and anti-inflammatory activities of chemical constituents from twigs of Mosla chinensis Maxim[J]. Natural Products and Bioprospecting, 2024, 14(3): 26-26.

References

1. Heo JY, Song JY, Noh JY, Choi MJ, Yoon JG, Lee SN, Cheong HJ, Kim WJ. Effects of influenza immunization on pneumonia in the elderly. Hum Vacc Immunother. 2018;14:744–9.
2. Schanzer DL, Langley JM, Tam TWS. Hospitalization attributable to influenza and other viral respiratory illnesses in Canadian children. Pediatr Infect Dis J. 2006;25:795–800.
3. Li Z, Wang H, Wang FX, Li HY, Cao F, Luo DQ, Zhang Q, Chen FL. Isolation of essential oil from Mosla chinensis Maxim by surfactant-enzyme pretreatment in high-solid system and evaluation of its biological activity. Ind Crop Prod. 2022;189: 115871.
4. National Pharmacopoeia Committee. Pharmacopoeia of People’s Republic of China. Part 1. Medical Science and Technology Press: Beijing, 2015; 259–60.
5. Cao L, Si JY, Liu Y, Sun H, Jin W, Li Z, Zhao XH, Pan RL. Essential oil composition, antimicrobial and antioxidant properties of Mosla chinensis Maxim. Food Chem. 2009;115:801–5.
6. Liu MT, Luo FY, Zeng JG. Composition analysis of essential oil of Mosla chinensis Maxim and its antibacterial and antioxidant activity. Chin Tradit Patent Med. 2020;42:3091–5.
7. Lin CL, Cai JZ, Lin GY. Chemical constituent study of volatile oils from the Mosla chinensis Maxim in Zhejiang Province. Chin Arch Tradit Chin Med. 2012;30:197–8.
8. Feng Y, Liu J. Effects of volatile oil from Mosla chinensis Maxim on bacteriostasis and immune response. Amino Acids Biotic Resour. 2009;31:30–2.
9. Ge B, Lu XY, Jiang HM. Study on antibacterial effect of volatile oil of Mosla chinensis Maxim in vitro. Chin J Tradit Veterinary Sci. 2005;2:8–10.
10. Zhang XX, Wu QF, Yan YL, Zhang FL. Inhibitory effects and related molecular mechanisms of total flavonoids in Mosla chinensis Maxim against H1N1 influenza virus. Inflamm Res. 2018;67:179–89.
11. Zhang L, Yang LY, Li RT, Yu F, Zhong JD. A new prenylated 3-benzoxepin derivative with anti-influenza A virus activity from Elsholtzia penduliflora. Nat Prod Res. 2022;36:719–25.
12. Yang LY, Du JC, Li RT, Yu F, Zhong JD. Bodiniosides S-Y, seven new triterpenoid saponins from Elsholtzia bodinieri and their anti-Influenza activities. Molecules. 2021;26:6535.
13. Qiao Y, Sun WW, Wang JF, Zhang JD. Flavonoids from Podocarpus macrophyllus and their cardioprotective activities. J Asian Nat Prod Res. 2014;16:222–9.
14. Sugimoto S, Yamano Y, Desoukey SY, Katakawa K, Matsunami K. Isolation of sesquiterpene–amino acid conjugates, onopornoids A-D, and a flavonoid glucoside from Onopordum alexandrinum. J Nat Prod. 2019;82:1471–7.
15. Sinha NK, Seth KK, Pandey VB, Dasgupta B, Shah AH. Flavonoids from the flowers of Clerodendron infortunatum. Planta Med. 1981;42:296–8.
16. Seo YH, Trinh TA, Ryu SM, Kim HS, Lee J. Chemical constituents from the aerial parts of Elsholtzia ciliata and their protective activities on glutamate-induced HT22 Cell Death. J Nat Prod. 2020;83(10):3149–55.
17. Perry NB, Foster LM. Antiviral and antifungal flavonoids, plus a triterpene, from Hebe cupressoides. Planta Med. 1994;60(5):491–2.
18. Hori K, Satake T, Saiki Y, Tanaka N, Murakami T, Chen CM. Chemical and chemotaxonomical studies of Filices. LXXIV. The novel flavanone glycosides of Pyrrosia linearfolia (HOOK.) Ching. J Pharm Soc Jpn. 1988;108(5):417–21.
19. Zhang XL, Guo YS, Wang CH, Li GQ, Xu JJ, Chung HY, Ye WC, Li YL, Wang GC. Phenolic compounds from Origanum vulgare and their antioxidant and antiviral activities. Food Chem. 2014;152:300–6.
20. Lai GF, Zhu XD, Luo SD, Wang YF. Chemical constituents from Elsholtzia rugulos. Chin Tradit Herb Drugs. 2008;5(39):661–4.
21. Oyama KI, Kondo T. Total synthesis of apigenin 7,4 prime-di-O-β-glucopyranoside, a component of blue flower pigment of Salvia patens, and seven chiral analogues. Tetrahedeon. 2004;60(9):2025–34.
22. Besson E, Chopin J. Sugar ring isomerization in C-arabinosyl flavones. Phytochemistry. 1983;22(9):2051–6.
23. Wang XF, Li H, Jiang K, Wang QQ, Zheng YH, Wei T, Tan CH. Anti-inflammatory constituents from Perilla frutescens on lipopolysaccharide-stimulated RAW 264.7 cells. Fitoterapia. 2018;130:61–5.
24. Formisano C, Rigano D, Senatore F, Bancheva S, Maggio A, Rosselli S, Bruno M. Flavonoids in subtribe centaureinae (Cass.) Dumort. (Tribe Cardueae, Asteraceae): distribution and 13C-NMR spectral data. Chem Biodiversity. 2012;9(10):2096–158.
25. Kong CH, Xu XH, Hu F, Chen XH, Ling B, Tan ZW. Using specific secondary metabolites as markers to evaluate allelopathic potentials of rice varieties and individual plants. Chin Sci Bull. 2002;47(10):839–43.
26. Zhang Q, Guilhon CC, Fernandes PD, Boylan F. Antinociceptive and anti-inflammatory activities of Elsholtzia ciliata (Thunb.) Hyl. (Lamiaceae) extracts. Planta Med. 2014;80(16):1406–1406.
27. Chen XF, Ma GX, Huang Z, Wu TY, Xu XD, Zhong XM. Identification of water-soluble phenolic acids from Clerodendranthus spicatus. Chin Tradit Herb Drugs. 2017;48(13):2614–8.
28. Tsai SF, Lee SS. Neolignans as xanthine oxidase inhibitors from Hyptis rhomboides. Phytochemistry. 2014;101:121–7.
29. Lee C, Kim J, Lee H, Lee S, Kho Y. Two new constituents from Isodon excisus and their evaluation in an apoptosis inhibitioni assay. J Nat Prod. 2001;64(5):659–60.
30. Su D, Tang W, Hu Y, Liu Y, Yu S, Ma S, Qu J, Yu D. Lignan glycosides from Neoalsomitra integrifoliola. J Nat Prod. 2008;71(5):784–8.
31. Gu QC, Yin ZK, Feng ZM, Jiang JS, Zhang X, Zhang PC, Yang YN. Three 11,12-seco-tanshinone derivatives from the rhizomes of Salvia miltiorrhiza. J Asian Nat Prod Res. 2020;22(10):935–40.
32. Kato H, Li W, Koike M, Wang Y, Koike K. Phenolic glycosides from Agrimonia pilosa. Phytochemistry. 2010;71(16):1925–9.
33. Dhingra MS, Dhingra S, Kumria R, Chadha R, Singh T, Kumar A, Karan M. Effect of trimethylgallic acid esters against chronic stress-induced anxiety-like behavior and oxidative stress in mice. Pharmacol Rep. 2014;66(4):606–12.
34. Takeda Y, Tomonari M, Arimoto S, Masuda T, Otsuka H, Matsunami K, Honda G, Ito M, Takaishi Y, Kiuchi F, Khodzhimatov OK, Ashurmetov OA. A new phenolic glucoside from an Uzbek medicinal plant, Origanum tyttanthum. J Nat Med. 2008;62(1):71–4.
35. Bravo JA, Sauvain M, Gimenez A, Munoz V, Callapa J, Le L, Massiot G, Lavaud C. Bioactive phenolic glycosides from Amburana cearensis. Phytochemistry. 1999;50(1):71–4.
36. Koike K, Li W, Liu LJ, Hata E, Nikaido T. New phenolic glycosides from the seeds of Cucurbita moschata. Chem Pharma Bull. 2005;53(2):225–8.
37. Guetchueng ST, Nahar L, Ritchie KJ, Ismail FMD, Dempster NM, Nnanga EN, Sarker SD. Phenolic compounds from the leaves and stem bark of Pseudospondias microcarpa (A. Rich.) Engl. (Anacardiaceae). Biochem Syst Ecol. 2020;91:104078.
38. Tagousop CN, Ngnokam D, Harakat D. Three new flavonoid glycosides from the aerial parts of Graptophyllum grandulosum Turril (Acanthaceae). Phytochem Lett. 2017;19:172–5.
39. Xu JZ, Zhang SS, Qu HB. Chemical constituents from Viola yedoensis. Chin Tradit Herb Drugs. 2010;41(9):1423–5.
40. Miyazawa M, Hisama M. Antimutagenic activity of flavonoids from Chrysanthemum morifolium. Biosci Biotechnol Biochem. 2003;67(10):2091–9.
41. Murata T, Sasaki K, Sato K, Yoshizaki F, Yamada H, Mutoh H, Umehara K, Miyase T, Warashina T, Aoshima H. Matrix metalloproteinase-2 inhibitors from Clinopodium chinense var. parviflorum. J Nat Prod. 2009;72(8):1379–84.
42. Zhong M, Sun G, Zhang X, Sun G, Xu X, Yu S. A New prenylated naphthoquinoid from the aerial parts of Clinopodium chinense (Benth.) O. Kuntze. Molecules. 2012;17(12):13910–6.
43. Hiipakka RA, Zhang HZ, Dai W, Dai Q, Liao S. Structure-activity relationships for inhibition of human 5alpha-reductases by polyphenols. Biochem Pharmacol. 2002;63(6):1165–76.
44. Liu F, Zhong J, Zhou Y, Gao Z, Walsh PJ, Wang X, Ma S, Hou S, Liu S, Wang M, Wang M, Bian Q. Cobalt-catalyzed enantioselective negishi cross-coupling of racemic α-Bromo esters with arylzincs. Chemistry. 2018;24(9):2059–64.
45. Mair CM, Ludwig K, Herrmann A, Sieben C. Receptor binding and pH stability—how influenza A virus hemagglutinin affects host-specific virus infection. Bba-Biomembranes. 2014;1838(4):1153–68.
46. Tavares LP, Teixeira MM, Garcia CC. The inflammatory response triggered by influenza virus: a two edged sword. Inflamm Res. 2017;66(4):283–302.
47. Wu ST, Li F, Wang YX, Yu BH, Ma CL, Qiu HQ, Wang GS. Phenylpropanoids from Brachybotrys paridiformis Maxim. Ex Oliv. and their anti-HBV activities. Phytochemistry. 2022;197:113114.
48. Fujihara T, Obora Y, Tokunaga M, Sato H, Tsuji Y. Dendrimer N-heterocyclic carbene complexes with rhodium(I) at the core. Chem Commun. 2005;8(36):4526–8.
49. Li JC, Dai WF, Liu D, Jiang MY, Zhang ZJ, Chen XQ, Chen CH, Li RT, Li HM. Bioactive ent-isopimarane diterpenoids from Euphorbia neriifolia. Phytochemistry. 2020;175: 112373.
50. Chen X, Cao YG, Ren YJ, Liu YL, Fan XL, He C, Li XD, Ma XY, Zheng XK, Feng WS. Ionones and lignans from the fresh roots of Rehmannia glutinosa. Phytochemistry. 2022;203: 113423.
51. Wang P, Liu F, Yang X, Liang Y, Li S, Su G, Jin DQ, Ohizumi Y, Xu J, Guo Y. Clerodane diterpenoids from Scutellaria formosana with inhibitory effects on NO production and interactions with iNOS protein. Phytochemistry. 2017;144:141–50.
52. Dang Z, Jung K, Zhu L, Lai W, Xie H, Lee KH, Huang L, Chen CH. Identification and synthesis of quinolizidines with anti-influenza a virus activity. ACS Med Chem Lett. 2014;5(8):942–6.
53. Vanderlinden E, Göktas F, Cesur Z, Froeyen M, Reed ML, Russell CJ, Cesur N, Naesens L. Novel inhibitors of influenza virus fusion: structureactivity relationship and interaction with the viral hemagglutinin. J Virol. 2010;84(9):4277–88.
54. Jones JC, Turpin EA, Bultmann H, Brandt CR. Inhibition of influenza virus infection by a novel antiviral peptide that targets viral attachment to cells. J Virol. 2006;80(24):11960–7.
55. Zhang YZ, Naguro I, Herr AE. In situ single-cell western blot on adherent cell culture. Angew Chem Int Ed Engl. 2019;58(39):13929–34.
56. Liang XX, Zhang XJ, Zhao YX, Feng J, Zeng JC, Shi QQ, Kaunda JS, Li XL, Wang WG, Xiao WL. Aspulvins A-H, aspulvinone analogues with SARS-CoV-2 M(pro) inhibitory and anti-inflammatory activities from an Endophytic Cladosporium sp. J Nat Prod. 2022;85(4):878–87.
57. Zhang T, Lo CY, Xiao M, Cheng L, Pun Mok CK, Shaw PC. Anti-influenza virus phytochemicals from Radix Paeoniae Alba and characterization of their neuraminidase inhibitory activities. J Ethnopharmacol. 2020;253: 112671.
58. Shi WZ, Jiang LZ, Song GP, Wang S, Xiong P, Ke CW. Study on the antiviral activities and hemagglutinin-based molecular mechanism of novel chlorogenin 3-O-β-chacotrioside derivatives against H5N1 subtype viruses. Viruses. 2020;12(3):304.
59. Ye M, Liao Y, Wu L, Qi W, Choudhry N, Liu Y, Chen W, Song G, Chen J. An oleanolic acid derivative inhibits hemagglutinin-mediated entry of influenza A virus. Viruses. 2020;12(2):225.
60. Lee JW, Jin Q, Jang H, Lee D, Han SB, Kim Y, Hong JT, Lee MK, Hwang BY. Jatrophane and ingenane-type diterpenoids from Euphorbia kansui inhibit the LPS-induced NO production in RAW 264.7 cells. Bioorg Med Chem Lett. 2016;26(14):3351–4.
61. Cao L, Li RT, Chen XQ, Xue Y, Liu D. Neougonin A inhibits lipopolysaccharide-induced inflammatory responses via downregulation of the NF-kB signaling pathway in RAW 264.7 macrophages. Inflammation. 2016;39:1939–48.

[1]	Hongyan Wen, Sheng Li, Yu Zhang. Phthalide mono- and dimers from the rhizomes of Angelica sinensis and their anti-inflammatory activities [J]. Natural Products and Bioprospecting, 2025, 15(3): 26-26.
[2]	Shi-Hui Qin, Zhi-Lan Li, Liu Yang, Jiang-Miao Hu. Gastrodinol derivatives and prenylated flavones from the flower branch of Gastrodia elata [J]. Natural Products and Bioprospecting, 2024, 14(3): 22-22.
[3]	Thua-Phong Lam, Ngoc-Vi Nguyen Tran, Long-Hung Dinh Pham, Nghia Vo-Trong Lai, Bao-Tran Ngoc Dang, Ngoc-Lam Nguyen Truong, Song-Ky Nguyen-Vo, Thuy-Linh Hoang, Tan Thanh Mai, Thanh-Dao Tran. Flavonoids as dual-target inhibitors against α-glucosidase and α-amylase: a systematic review of in vitro studies [J]. Natural Products and Bioprospecting, 2024, 14(1): 4-4.
[4]	Xun Wei, Jia-Luo Huang, Hua-Hua Gao, Fang-Yu Yuan, Gui-Hua Tang, Sheng Yin. New halimane and clerodane diterpenoids from Croton cnidophyllus [J]. Natural Products and Bioprospecting, 2023, 13(3): 21-21.
[5]	Prabhakar Semwal, Abdur Rauf, Ahmed Olatunde, Pooja Singh, Mohamed Y. Zaky, Md. Mozahidul Islam, Anees Ahmed Khalil, Abdullah S. M. Aljohani, Waleed Al Abdulmonem, Giovanni Ribaudo. The medicinal chemistry of Urtica dioica L.: from preliminary evidence to clinical studies supporting its neuroprotective activity [J]. Natural Products and Bioprospecting, 2023, 13(3): 16-16.
[6]	Sitian Zhang, Shuyuan Mo, Fengli Li, Yaxin Zhang, Jianping Wang, Zhengxi Hu, Yonghui Zhang. Drimane sesquiterpenoids from a wetland soil-derived fungus Aspergillus calidoustus TJ403-EL05 [J]. Natural Products and Bioprospecting, 2022, 12(4): 27-27.
[7]	Wenting Liu, Weikang Zheng, Liping Cheng, Ming Li, Jie Huang, Shuzheng Bao, Qiang Xu, Zhaocheng Ma. Citrus fruits are rich in flavonoids for immunoregulation and potential targeting ACE2 [J]. Natural Products and Bioprospecting, 2022, 12(1): 1-10.
[8]	Ning-Ning Wang, Chun-Yu Liu, Tian Wang, Yue-Lan Li, Ke Xu, Hong-Xiang Lou. Two New Quinazoline Derivatives from the Moss Endophytic Fungus Aspergillus sp. and Their Anti-inflammatory Activity [J]. Natural Products and Bioprospecting, 2021, 11(1): 105-110.
[9]	Mohammad Sanad Abu-Darwish, Célia Cabral, Zulfigar Ali, Mei Wang, Shabana I. Khan, Melissa R. Jacob, Surendra K. Jain, Babu L. Tekwani, Fazila Zulfiqar, Ikhlas A. Khan, Hatem Taifour, Lígia Salgueiro, Thomas Efferth. Salvia ceratophylla L. from South of Jordan: new insights on chemical composition and biological activities [J]. Natural Products and Bioprospecting, 2020, 10(5): 307-316.
[10]	Lin Wang, Junke Song, Ailin Liu, Bin Xiao, Sha Li, Zhang Wen, Yang Lu, Guanhua Du. Research Progress of the Antiviral Bioactivities of Natural Flavonoids [J]. Natural Products and Bioprospecting, 2020, 10(5): 271-283.
[11]	Nay Lin Tun, Dong-Bao Hu, Meng-Yuan Xia, Dong-Dong Zhang, Jun Yang, Thaung Naing Oo, Yue-Hu Wang, Xue-Fei Yang. Chemical Constituents from Ethanoic Extracts of the Aerial Parts of Leea aequata L., a Traditional Folk Medicine of Myanmar [J]. Natural Products and Bioprospecting, 2019, 9(3): 243-249.
[12]	Yin-E Zhi, Xu-Jie Qin, Hui Liu, Yuan Zeng, Wei Ni, Li He, Zu-Ding Wang, Hai-Yang Liu. Structurally Diverse Polymethylated Phloroglucinol Meroterpenoids from Baeckea frutescens [J]. Natural Products and Bioprospecting, 2018, 8(6): 431-439.
[13]	Lai-Bin Zhang, Chun Lei, Li-Xin Gao, Jing-Ya Li, Jia Li, Ai-Jun Hou. Isoprenylated Flavonoids with PTP1B Inhibition from Macaranga denticulata [J]. Natural Products and Bioprospecting, 2016, 6(1): 25-30.
[14]	Da-Song Yang, Shuang-Mei Wang, Wei-Bing Peng, Yong-Ping Yang, Ke-Chun Liu, Xiao-Li Li, Wei-Lie Xiao. Minor Prenylated Flavonoids from the Twigs of Macaranga adenantha and Their Cytotoxic Activity [J]. Natural Products and Bioprospecting, 2015, 5(2): 105-109.