盛智麗, 劉俊梅, 高潔, 楊寶

無花果亞屬植物異戊烯基類黃酮及其生物活性研究進展

盛智麗1,2, 劉俊梅2, 高潔3, 楊寶1*

(1.中國科學院華南植物園，廣東省應用植物學重點實驗室，廣州 510650；2. 吉林農(nóng)業(yè)大學食品科學與工程學院，長春 130118；3. 華南理工大學食品科學與工程學院，廣州 510641)

無花果亞屬隸屬于桑科，既是重要的水果資源，也是優(yōu)良的中藥資源，廣泛種植于熱帶、亞熱帶地區(qū)，因含有豐富的生物活性成分和保健功效，經(jīng)濟價值突出。無花果亞屬植物中異戊烯基類黃酮含量豐富，結構多樣，已報道有37種異黃酮、2種黃烷酮、7種黃酮和1種查爾酮。無花果異戊烯基類黃酮具有突出的抗氧化活性，能夠緩解更年期癥狀，保護骨骼、預防炎癥、預防癌癥等。從化學結構和生物活性兩方面對無花果亞屬植物的異戊烯基黃酮類化合物的研究概況進行總結，以期為該屬植物的開發(fā)和利用提供參考。

異戊烯基類黃酮；生物活性；?？疲粺o花果亞屬；綜述

無花果亞屬(subgenus)是榕屬(genus)中最大的開花植物屬，包含700余種植物[1]。原產(chǎn)于西南亞和地中海地區(qū)，現(xiàn)已在熱帶、亞熱帶及溫帶地區(qū)廣泛種植[2]。無花果亞屬植物具有重要的食用和藥用價值[3–4], 其果實在很多國家可食用,根和葉則被應用于傳統(tǒng)醫(yī)藥。在越南，地果()廣泛用于治療水腫、痢疾、膿皰等病癥[5]，因其提取物具有顯著的抗菌活性[6]，常被用來提取精油。在印度，對葉榕()常用于治療皮膚、呼吸系統(tǒng)和泌尿系統(tǒng)等的疾病[7]。作為無花果亞屬中最具商業(yè)價值的水果，無花果()既是口感甜美的水果食品，同時也具有祛痰、疏肝、消炎、抗癌功效并用于治療肝脾疾病等[8–9]。查閱近年來國內(nèi)外對無花果亞屬植物化學成分和生物活性的報道, 該亞屬植物富含類黃酮[10]、三萜、香豆素等活性成分[11–12]。其中，一些香豆素類成分，如馬豆素、補骨脂素、香檸檬烯等可減少氧化應激，防止胰島細胞損傷，表現(xiàn)出降血糖活性[13]。部分萜類成分,如鮑爾烯醇、羽扇豆醇、齊墩果酸等具有抗氧化、抗炎、保肝等功效[11]。此外，異戊烯基黃酮類物質(zhì)是該類植物的特征性物質(zhì)，已成為近年來學者們關注的熱點，具有重要的藥用價值。本文對無花果亞屬中異戊烯基黃酮類化合物進行綜述。

1 結構類型

無花果亞屬植物中，已報道47個異戊烯基黃酮類化合物。異戊烯基主要存在形式有13種(圖1)，其中二甲基烯丙基是主要的結構類型。取代位點發(fā)生在類黃酮A環(huán)或B環(huán)，以A-異戊烯基化為主, 最常見的取代位點為A-6位和A-8位；部分取代發(fā)生在B環(huán)上，主要取代位點為B-2?和B-4?處。除異戊烯基取代外，黃酮母核上通常還連有羥基和甲氧基。無花果亞屬植物異戊烯基黃酮的類黃酮骨架類型主要以異黃酮為主，還包含少量的黃烷酮、黃酮、查爾酮(圖2, 3)。

2 異戊烯基黃酮類成分和生物活性

黃酮類化合物是重要天然活性物質(zhì)，安全性好，具有抗腫瘤、抗病毒、抗炎、抗菌等活性。已有化學及生物活性研究結果表明，大多數(shù)情況下,異戊烯基基團的引入會增加類黃酮的親脂性，改善對生物膜的親和性，顯著提高生物活性[14–15]。表1列出了已報道的無花果亞屬植物異戊烯基類黃酮的生物活性。

2.1 雌激素受體調(diào)節(jié)活性

異戊烯基異黃酮是無花果異戊烯基類黃酮的主要結構形式，在結構上與雌激素相似[16]，可以與雌激素、受體結合，并具有選擇性。通過發(fā)揮雌激素受體調(diào)節(jié)活性，異戊烯基異黃酮可緩解更年期癥狀，保護骨骼，預防乳腺癌[17]等疾病。在已經(jīng)報道的47種異戊烯基類黃酮中，37種為異戊烯基異黃酮。因此，無花果亞屬植物是豐富的異戊烯基異黃酮資源，可用于功能食品或藥物開發(fā)。

圖1 異戊烯基結構

圖2 無花果亞屬植物異戊烯基類黃酮成分結構(1～29)

2.2 抗氧化

氧化損傷是引發(fā)癌癥、心血管疾病、動脈粥樣硬化等多種慢性病的重要因素[18]，常常伴隨炎癥的產(chǎn)生。通過抑制或延遲氧化反應來預防和治療疾病十分重要[19]。作為膳食抗氧化劑，食源性黃酮類成分在減緩氧化損傷中具有重要作用。已有研究表明[5,7,11,20–21]，無花果中大部分異戊烯基類黃酮成分(化合物17、18、21、22、29、35、37、42、45、46、47)表現(xiàn)出優(yōu)良的清除DPPH自由基活性?？寡趸钚詮娙鹾彤愇煜┗慄S酮的母核結構、官能團排列、酚羥基數(shù)目直接相關。B環(huán)羥基與2,3-烯基的存在是影響抗氧化活性的重要因素[22]。此外, Popoola等[23]的研究表明，化合物26還可以抑制酪氨酸酶活性，減少體內(nèi)自由基的積累，進而預防皮膚衰老。

2.3 預防炎癥

炎癥，通常是機體對抗外界感染而產(chǎn)生的防御性免疫反應[24]。炎癥失衡可引發(fā)哮喘、糖尿病等多種急、慢性并發(fā)癥[15]。在無花果異戊烯基類黃酮中，17種成分通過調(diào)節(jié)促炎分子合成和炎癥相關細胞因子分泌而表現(xiàn)出抗炎活性。其中，化合物1～15通過抑制NO的產(chǎn)生而緩解炎癥反應[25]?；衔?7對抑制單核細胞/巨噬細胞活化具有重要作用[26]。在這些具有抗炎活性的化合物中，9～11、13表現(xiàn)出強抗炎活性(IC50值<2mol/L)[25]。這幾個物質(zhì)的類黃酮骨架結構與異戊烯基結構特征是影響其抗炎活性的關鍵因素。

2.4 預防癌癥

抗炎治療是治療早期腫瘤進展和惡性轉(zhuǎn)化的一種有效的治療方法。無花果異戊烯基類黃酮在發(fā)抗炎活性的同時，也具有抗癌細胞增殖作用[27]。

圖3 無花果亞屬植物異戊烯基類黃酮成分結構(30～47)

此外，異戊烯基類黃酮通過調(diào)節(jié)不同分子靶點發(fā)揮癌癥預防作用。主要機制包括誘導細胞凋亡、抑制血管生成、調(diào)控遺傳因子、轉(zhuǎn)錄因子等[28]。如化合物16可通過誘導細胞中ROS和ERK抑制癌細胞增殖[29]；化合物44可抑制A549和NCI-292細胞的增殖[30]?；衔?8通過誘導肺細胞、食管鱗狀細胞、腎細胞凋亡抗癌[21]；化合物20對TPA誘導的Raji細胞中EBV-EA活化的抑制作用明顯[31];化合物35可抑制前列腺癌細胞系(DU-145)和靜脈內(nèi)皮細胞系(HUVEC)實現(xiàn)抗腫瘤和抗血管生成作用[32]；化合物42通過MAPK和AKT信號傳導途徑誘導HeLa細胞凋亡預防癌癥[33]。

2.5 抗菌活性

不同于常規(guī)藥物，植物類黃酮在發(fā)揮抗菌活性的同時具有較好的安全性，可以選擇性地靶向細菌細胞，抑制毒性因子和微生物威脅的同時，不會引發(fā)抗生素耐藥性等問題[53]，已成為目前最受歡迎的生物抗菌劑之一。無花果異戊烯基類黃酮物質(zhì)中, 化合物18和30對金黃色葡萄球菌，大腸桿菌、李斯特菌具有抑制作用[30–31]。化合物17可抑制結核分岐桿菌[38], 表現(xiàn)出抗結核作用，可用于開發(fā)肺部感染的抗菌藥物。Lopes等[28,33]的研究表明，化合物2和4具有明顯抗真菌活性，可能是由于羥基化程度的增加導致對微生物的抑制能力提升。此外，化合物21和22也表現(xiàn)出抗菌活性[11]，其抗菌機理還需進一步研究。

2.6 其他活性

Sakat等[7]報道，化合物31～34和38可通過抑制-葡萄糖苷酶活性預防糖尿病。與目前在T2D的治療中使用的-葡萄糖苷酶抑制劑(如阿卡波糖)相比，不產(chǎn)生胃腸道副作用，有希望成為新型和更安全的治療藥物。Jung-Hae等[43]報道，化合物28可通過抑制血小板來預防血栓。Matsuda等[42]的研究表明，化合物24可抑制d-半乳糖胺誘導的小鼠原代肝細胞的細胞毒性，具有保肝作用。Williams等[35]的研究表明，化合物3、25和33可通過抑制BACE1活性預防阿爾茲海默癥。

表1 無花果亞屬植物異戊烯基類黃酮

續(xù)表(Continued)

①: 抗炎; ②: 抗細胞增殖; ③: 抗皮膚炎癥; ④: 預防阿爾茲海默癥; ⑤: 抗真菌; ⑥: 抗菌; ⑦: 預防癌癥; ⑧: 保肝作用; ⑨: 預防糖尿病; ⑩: 預防血栓; ?: 促進骨細胞增殖; ?: 抗氧化。

①: Anti-inflammatory; ②: Cell proliferation-inhibitory; ③: Anti-dermatitis; ④: Alzheimer’s disease prevention; ⑤: Antifungal activity; ⑥: Antibacterial; ⑦: Cancer prevention; ⑧: Hepatoprotective activity; ⑨: Anti-diabetic; ⑩: Thromboprophylaxis; ?: Proliferation-promote of osteoblast; ?: Antioxidant.

3 展望

因為富含結構多樣、活性突出的異戊烯基類黃酮物質(zhì)，無花果亞屬植物已成為功能食品、天然藥物領域的重要原料來源。在未來研究中，仍需加強對無花果亞屬植物的化學成分發(fā)掘，深入闡明其生物活性作用機理以及構效關系。相關研究結果對于該亞屬植物的綜合開發(fā)與利用具有重要意義。

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Prenylated Flavonoids insubgenus: Chemistry and Bioactivities

SHENG Zhili1,2, LIU Junmei2, GAO Jie3, YANG Bao1*

(1. Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of Sciences,Guangzhou 510650, China; 2. College of Food Science and Engineering, Jilin Agricultural University, Changchun 130118, China; 3. College of Food Science and Engineering, South China University of Technology,Guangzhou 510641, China)

Subgenusbelongs to Moraceae, which is an important resource of fruit and herbal medicine.subgenus is widely planted in tropical and subtropical areas. It has outstanding economic value because of abundant bioactive compounds and multiple health benefits. Prenylated flavonoids are the characteristic bioactive compounds ofsubgenus, including 37 isoflavones, 2 flavanones, 7 flavones, and 1 chalcone. Numerous biological activities have been reported for these prenylated flavonoids, such as menopause relief, bone protection, anti-inflammation, anti-oxidation, cancer prevention and anti-bacteria activities. The updated information regarding the prenylated flavonoids insubgenus was summarized, and also their chemical structures and biological activities. The information is helpful for the development and utilization of this subgenus.

Prenylated flavonoid; Biological activity; Moraceae;subgenus; Review

10.11926/jtsb.4496

2021-08-16

2021-10-08

國家自然科學基金項目(31871851)資助

This work was supported by the National Natural Science Foundation of China (Grant No. 31871851).

盛智麗, 女，碩士研究生。E-mail: shengzl@scbg.ac.cn

E-mail: yangbao@scbg.ac.cn