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Inhibition of Viral Proteases by Zingiberaceae Extracts and Flavones Isolated from Kaempferia Parviflora

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Inhibition of Viral Proteases by Zingiberaceae Extracts and Flavones Isolated from Kaempferia Parviflora ORIGINAL ARTICLES Research Centre for Bioorganic Chemistry1, Department of Chemistry, Faculty of Science, Chulalongkorn University, Bang- kok, Thailand and Department of Biochemistry2, Uppsala University, Uppsala, Sweden Inhibition of viral proteases by Zingiberaceae extracts and flavones isolated from Kaempferia parviflora K. Sookkongwaree1, M. Geitmann2, S. Roengsumran1, A. Petsom1, U. H. Danielson2 Received May 23, 2005, accepted November 9, 2005 Prof. U. Helena Danielson, Department of Biochemistry, Uppsala University, Box 576, SE-751 23 Uppsala, Sweden [email protected] Pharmazie 61: 717–721 (2006) In order to identify novel lead compounds with antiviral effect, methanol and aqueous extracts of eight medicinal plants in the Zingiberaceae family were screened for inhibition of proteases from human immunodeficiency virus type 1 (HIV-1), hepatitis C virus (HCV) and human cytomegalovirus (HCMV). In general, the methanol extracts inhibited the enzymes more effectively than the aqueous extracts. HIV-1 protease was strongly inhibited by the methanol extract of Alpinia galanga. This extract also inhibited HCV and HCMV proteases, but to a lower degree. HCV protease was most efficiently inhib- ited by the extracts from Zingiber officinale, with little difference between the aqueous and the metha- nol extracts. Many of the methanol extracts inhibited HCMV protease, but the aqueous extracts showed weak inhibition. In a first endeavor to identify the active constituents, eight flavones were isolated from the black rhizomes of Kaempferia parviflora. The most effective inhibitors, 5-hydroxy-7- methoxyflavone and 5,7-dimethoxyflavone, inhibited HIV-1 protease with IC50 values of 19 mM. More- over, 5-hydroxy-3,7-dimethoxyflavone inhibited HCV protease and HCMV protease with IC50 values of 190 and 250 mM, respectively. 1. Introduction In the present study, proteases involved in AIDS, hepatitis C (HCV) and human cytomegalovirus (HCMV) infections The success in developing drugs against AIDS that target were selected as targets for the antiviral compounds. HIV-1 protease has resulted in a major interest in pro- These proteases are all crucial for the life cycle of the teases as drug targets. Modern discovery of drugs is typi- virus from which they originate, making them all attrac- cally based on mechanistic and structural information tive targets for antiviral drug therapy. They are structurally about the enzyme of interest and on organic synthesis of and mechanistically distinct and only distantly related to transition state analogues. Another strategy is based on the endogenous human proteases. Human immunodeficiency analysis of effects of natural products on diseases or tar- type 1 (HIV-1) protease is an aspartic protease consisting gets directly. Natural products have historically been the of two identical subunits, a type only present in retro- most important sources of drugs for mankind and still viruses. In contrast, the HCV non-structural protein 3 serve as important original starting points for synthesis (NS3) protease is a serine protease structurally related to new drugs (Newman et al. 2003). chymotrypsin type proteases, but is in HCV linked to the Therefore our laboratory has been interested in searching viral helicase and activated by a viral peptide cofactor. for antiviral compounds from natural sources. In this pa- Although, HCMV protease is also a serine protease, it per, we investigated Thai herbs of the Zingiberaceae fa- represents a unique type of serine protease, occurring only mily for potential antiviral protease activity. The medicinal in herpes viruses. By using different proteases it was pos- plants in this family have not only been used for spicy sible to use the extracts efficiently and the specificity of cooking but also as health-promoting herbs (Sirirugsa inhibition could be evaluated at an early stage. 1999). The rhizomes of Zingiberaceae have been shown to contain different bioactive compounds, such as curcumi- noids (Lechtenberg et al. 2004), sesquiterpenes (Hong 2. Investigations and results et al. 2001) and flavones (Yenjai et al. 2004). One of the 2.1. Inhibitory effect of crude extracts plants we found to contain inhibitory compounds of all three enzymes, Kaempferia parviflora, has been known in Methanol and aqueous crude extracts were prepared from Thailand as a health-promoting herb, and used for treat- eight medicinal plants in the Zingiberaceae family. The ment of colic disorder, peptic and duodenal ulcer (Yenjai fresh rhizome was used, but for one of the plants (K. ga- et al. 2004). It was therefore used as a starting point for langa) the dried rhizome was used instead. The effect of identification of the active ingredients. each extract on the activity of HIV-1, HCV and HCMV Pharmazie 61 (2006) 8 717 ORIGINAL ARTICLES Table 1: Inhibition of HIV-1, HCV and HCMV proteases by methanol extracts from Zingiberaceae medicinal herbs Name Used part % Inhibition HIV-1 protease HCV protease HCMV protease 20 mg/ml 200 mg/ml 20 mg/ml 200 mg/ml 20 mg/ml 200 mg/ml Kaempferia galanga Dried rhizome 1.5 Æ 0.8 4.9 Æ 1.4 3.5 Æ 2.7 20.9 Æ 6.4 22.3 Æ 0.8 45.6 Æ 1.7 Curcuma zedoaria Fresh rhizome 18.6 Æ 2.7 97.8 Æ 1.5 68.9 Æ 2.4 84.7 Æ 6.2 32.1 Æ 1.6 94.8 Æ 2.8 Curcuma longa Fresh rhizome 67.8 Æ 5.6 92.9 Æ 0.9 44.6 Æ 6.1 84.9 Æ 2.8 68.6 Æ 1.2 97.3 Æ 2.4 Kaempferia parviflora Fresh rhizome 37.1 Æ 0.4 81.5 Æ 0.8 17.7 Æ 2.8 71.9 Æ 2.3 29.6 Æ 4.0 74.7 Æ 3.5 Boesenbergia pandurata Fresh rhizome 22.1 Æ 2.1 64.6 Æ 2.0 33.9 Æ 3.5 82.0 Æ 1.2 47.9 Æ 3.6 96.2 Æ 0.6 Zingiber zerumbet Fresh rhizome 9.9 Æ 2.8 17.8 Æ 1.4 47.2 Æ 3.5 85.4 Æ 5.5 20.5 Æ 2.4 39.0 Æ 0.3 Zingiber officinale Fresh rhizome 14.8 Æ 2.7 46.0 Æ 8.6 53.6 Æ 0.8 96.0 Æ 1.4 4.0 Æ 1.5 57.2 Æ 5.8 Alpinia galanga Fresh rhizome 97.5 Æ 0.4 98.2 Æ 1.0 58.7 Æ 1.8 82.8 Æ 0.9 77.1 Æ 0.3 96.6 Æ 0.3 Extracts of the specified part were tested at 20 and 200 mg/ml, values are means Æ SD, n ¼ 3 Table 2: Inhibition of HIV-1, HCV and HCMV proteases by aqueous extracts from Zingiberaceae medicinal herbs Name Used part % Inhibition HIV protease HCV protease HCMV protease 20 mg/ml 200 mg/ml 20 mg/ml 200 mg/ml 20 mg/ml 200 mg/ml Kaempferia galanga Dried rhizome 0.7 Æ 0.7 22.1 Æ 1.2 8.3 Æ 0.1 29.4 Æ 3.9 6.7 Æ 1.7 22.9 Æ 0.4 Curcuma zedoaria Fresh rhizome 26.5 Æ 3.4 89.8 Æ 1.2 50.6 Æ 9.9 81.3 Æ 1.3 13.1 Æ 4.7 57.5 Æ 0.2 Curcuma longa Fresh rhizome 35.3 Æ 3.5 97.0 Æ 1.9 65.1 Æ 5.8 84.5 Æ 5.9 1.8 Æ 0.9 54.1 Æ 3.2 Kaempferia parviflora Fresh rhizome 15.2 Æ 0.6 48.3 Æ 7.8 56.7 Æ 2.3 87.2 Æ 2.6 11.3 Æ 6.5 33.8 Æ 7.3 Boesenbergia pandurata Fresh rhizome 35.7 Æ 1.7 57.9 Æ 2.0 54.0 Æ 0.9 84.8 Æ 2.1 13.1 Æ 3.0 19.2 Æ 3.9 Zingiber zerumbet Fresh rhizome 5.0 Æ 0.6 8.5 Æ 0.5 7.9 Æ 4.4 71.8 Æ 5.5 0.9 Æ 0.4 5.5 Æ 4.3 Zingiber officinale Fresh rhizome 17.6 Æ 0.6 26.8 Æ 0.7 43.0 Æ 9.7 93.1 Æ 2.2 5.8 Æ 0.4 11.9 Æ 8.2 Alpinia galanga Fresh rhizome 16.5 Æ 0.1 37.9 Æ 1.0 12.3 Æ 0.8 75.7 Æ 5.2 5.2 Æ 3.0 10.7 Æ 3.9 Extracts from the specified parts were tested at 20 and 200 mg/ml, values are means Æ SD, n ¼ 3 proteases was tested at a concentration of 20 mg/ml and extracts, most of the examined herbal aqueous extracts, 200 mg/ml. The methanol extracts (Table 1) were overall except Kaempferia galanga, showed more than 70% inhi- more inhibitory than the aqueous extracts (Table 2). Only bition of HCV protease at a concentration of 200 mg/ml two aqueous extracts resulted in more than 90% inhibi- (Table 2). At a concentration of 20 mg/ml, the aqueous ex- tion, while nine methanol extracts exhibited at least 90% tracts of Curcuma zedoaria, Curcuma longa, Kaempferia inhibition of the proteases studied. Furthermore, none of parviflora and Boesenbergia pandurata showed more than the aqueous extracts were inhibitory to this degree at the 50% inhibition. lower concentration tested, while two of the methanol ex- tracts were. The methanol extracts that corresponded to 2.1.3. Inhibition of HCMV protease the two aqueous extracts that showed at least 90% inhibi- tion, were also inhibitory to this degree. The methanol crude extract of Curcuma zedoaria, Curcu- ma longa, Kaempferia parviflora, Boesenbergia pandurata and Alpinia galanga inhibited HCMV protease by more 2.1.1 Inhibition of HIV-1 protease than 70% at high concentration (200 mg/ml) (Table 1).
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