The Styracaceae

Styracaceae

REVISÃO

The Styracaceae

Styracaceae

Patrícia M. Pauletti; Helder L. Teles; Dulce H.S. Silva; Ângela R. Araújo; Vanderlan S. Bolzani^*

NuBBE- Núcleo de Bioensaios, Biossíntese e Ecofisiologia de Produtos Naturais, Instituto de Química, Universidade Estadual Paulista, UNESP, CP 355, 14801-970, Araraquara, SP, Brazil

ABSTRACT

The Styracaceae contains 11 genera and approximately 160 species consisting of small trees and shrubs, mostly native to tropical and subtropical regions. This family is well-known by the genus Styrax, which is notorious due to the production of resinous material, a pathological product, harvested by making incisions into the tree’s bark. The gum is used in perfumes, as antiseptic, expectorant, incense, and fumigating material. This paper reviews the phytochemical and biological studies carried out on 11 species of this family. A total of 92 papers were consulted, and 130 compounds were described, thus these data indicate that Styrax is by far the largest genus in the family, and the only which has been extensively investigated.

Keywords: Styracaceae, Styrax, lignans, tritepenes, review.

RESUMO

Styracaceae possui 11 gêneros e aproximadamente 160 espécies, sendo árvores e arbustos, distribuídos nas regiões tropicais e subtropicais. Esta família é conhecida principalmente devido ao gênero Styrax, que é notório pela produção de um material resinoso, produto patológico, coletado a partir de incisões realizadas no caule. Esta goma é usada em perfumes, como anti-séptico, expectorante, incenso e material fumegante. Este artigo reúne os estudos fitoquímicos e biológicos realizados em 11 espécies desta família. Foram consultados 92 artigos e levantadas 130 substâncias, que indicaram que Styrax é o maior gênero desta família e o único que foi extensivamente investigado.

Unitermos: Styracaceae, Styrax, lignanas, tritepenenos, revisão.

INTRODUCTION

The Styracaceae contains approximately 160 species grouped in 11 genera: Styrax L., Halesia J. Ellis ex L. (three species), Alniphyllum Matsum. (three species), Bruinsmia Boer. & Koord. (two species), Huodendron Rehder (four species), Parastyrax W. W. Sm. (two species), Pterostyrax Siebold & Zucc. (four species), Rehderodendron Hu (five species), Changiostyrax C. T. Chen (one specie), Melliodendron Hand. –Mazz. (one specie), and Sinojackia Hu (five species) (Fritsch et al., 2001). Traditionally, the Styracaceae has been placed with some or all of the following families: Ebenaceae, Lissocarpaceae, Sapotaceae, and Symplocaceae at the ordinal level Ebenales (Cronquist, 1981). Styrax is, by far, the largest genus in the family, consisting of about 130 species, which comprises 80 % of the total number of species in Styracaceae. This genus has a widespread but disjunctive distribution, occurring in the Americas, eastern Asia, and the Mediterranean region, with over half the species presented in South America (Fritsch, 2001). Styrax distinguishes among other genera of this family due to the production of resinous material, commonly referred to as benzoin resin, usually secreted when sharp objects injure the bark. This resin has been used in many parts of the world in perfumery, cosmetics, and folk medicine as expectorant and in inhalation (Costa, 1996; Corrêa, 1926). The tincture of benzoin (a mixture of 10% Benzoin, 2% Aloe, 8% Storax, 4% Tolu Balsam and alcohol) has a long history of use and can be traced back to at least the 15th century in the medical uses, and Egyptian and Greek times as a balsam (Lovell, 1993). It has both fungicidal and bacteriostatic properties, and it also adheres well to skin and mucous membranes (Hjorth, 1961). It has been used added to water and glycerine in preparing steam inhalations for bronchitis, asthma and other respiratory disorders (Steiner; Leifer, 1949). Allergy for tincture of Benzoin was firstly reported in 1874 with a patient who developed a purpuric eruption after inhaling its vapors. On the other hand, there have been few reports of contact allergy to Benzoin tincture suggesting that it is in fact not a strong sensitizer (Scardamaglia et al., 2003). In this review the biological activities and phytochemistry of Styrax are considered, since this genus is the only studied extensively.

MATERIAL AND METHODS

The keywords used for this review were Styracaceae, Styrax, Halesia, Alniphyllum, Bruinsmia, Huodendron, Parastyrax, Pterostyrax, Rehderodendron, Changiostyrax, Melliodendron , and Sinojackia , and the search was realized using Chemical Abstracts, Web of Science and PubMed.

RESULTS AND DISCUSSION

Consultation of the references found in our search resulted in the elaboration of a list of species studied. Table 1 and 2 describe the biological activities of crude extracts and fractions and the distribution of the compounds isolated by species, respectively. The compounds structures are presented in Figures 1-5, and the references correspond to the first report on that compound or the one in which the most relevant spectroscopic data were presented.

Bioactivity of crude extracts and fractions

The resin gum benzoin from S. benzoin inhibited LDL (low-density lipoproteins) oxidation lower than 2% (Teissedre; Waterhouse, 2000), and the insaponifiable fraction, obtained from the balsamic resin, showed immune stimulant activity, stimulating the phagocytic activity of reticulum endothelial system in mice inoculated with Escherichia coli (Delaveau et al., 1980).

Oral administration of dry 70 % ethanolic extract from the stems of S. camporum Pohl , known in Brazil as "estoraque do campo" or "cuia do brejo", to rats during 15 days decreased the ulceration size, gastric secretion volume, and increased collagen fibre number of chronic ulcer induced by acetic acid. It was established that the ethyl acetate fraction was responsible for the antiulcer activity. This study supported the use of S. camporum hydroalcoholic extract in folk medicine as antiulcer drug (Bacchi; Sertié, 1994, Bacchi et al., 1995).

The crude extract of the leaves of S. ferrugineus showed antibacterial and antifungal activities against Staphylococcus aureus, Candida albicans , and Cladosporium sphaerospermum , and the MIC (minimum inhibition concentration) was established as 200 µg/mL, 800 µg/mL, and 750 µg, respectively (Pauletti et al., 2000).

The 70% aqueous acetone extract of S. formosanum was evaluated by various antioxidant assays, including the free radical scavenging ability using 1,1-diphenyl-2-picrylhydrazyl (DPPH), hydroxyl radicals, and reducing power assays. This extract showed IC₅₀ of 31.5 µg/mL and 0.3 µg/mL in the DPPH and hydroxyl radicals assays, respectively. The total phenolic content was determined as 2.7 mg of gallic acid/g of dried extract determined according to a Folin-Ciocalteu method. In the reducing power assay the activity was moderated, and the results obtained in the different antioxidant assays, did not show significant correlations (Hou et al., 2003).

In Japan, pericarps of S. japonica found use as washing soap, cough medicine and as a piscicidal agent (Takanashi, 1991). The propan-2-one extract of S. japonica and the water insoluble fraction showed insecticidal action against Culex pipiens larvae (Yamaguchi et al. 1950), and the essential oil exhibited strong growth inhibitory effects on Bacillus cereus, Salmonella typhimurium and S. aureus (Kim; Shin, 2004; Kim et al., 2004c). The hexane and dichloromethane soluble fractions obtained from the methanolic extract of the seeds exhibited strong cytotoxic activities in brine shrimp lethality test (Kwon; Kim, 2002). A methylene chloride soluble fraction from the methanolic extract of the stem bark showed significant cell cytotoxicity in vitro by SRB method against five human tumor cell lines A549 (non small cell lungcarcinoma), SK-OV-3 (adenocarcinoma, ovary malignant ascites), SK-MEL-2 (malignant melanoma, metastasis to skin of thigh), MES-AS (uterine sarcoma), and HCT-15 (colon adenocarcinoma) (Kim et al., 2004b), and exhibited significant MMP-1 expression inhibition in vitro (Moon et al., 2005b). In addition, total saponins extract increased plasma ACTH (adrenocorticotropic hormone), corticosterone and glucose after the intraperitoneal administration in rats ( Yokoyama et al., 1982).

The methanolic extract of S. obassia was found to inhibit production of inflammatory mediators, such as prostaglandins and leukotrienes, in vitro assay system (Jung et al., 2003).

Gummy exudates of S. officinalis could be applied as a suspending agent for the formulation of antiacid preparations (Shahjahan; Islan, 1998), and pericarps have been used as fish poison, furthermore it has been claimed that saponins appeared to be responsible for the ichthyotoxic action, also they were highly haemolytic (Segal et al., 1964, 1966). As well, the aqueous ethanolic extract from the aerial parts showed antitumoral activity against 3PS test systems (141 % in 10 mg/kg doses), but were toxic in high doses (Ulubelen; Gören, 1973). Proestos and coworkers studied extracts by HPLC/UV and distinguished, identified, to quantify phenolic compounds. They also determined the antioxidant capacity with the Rancimat test using sun flower oil as substrate, and the total phenolic content in the extracts applying the Folin-Ciocalteu assay. Among the plants investigated was the leaves of S. officinalis that showed total phenolic concentration of 18.4 ± 0.3 mg of gallic acid/g of dry extract, and the antioxidant protection factor was equal to 1.8 to the ground material and 1.7 to the methanolic extract. Additionally, the methanolic extract showed slight antimicrobial activity against E. coli, B. cereus and Pseudomonas putida , the susceptibility of the test organisms to the extract was determined by employing the standard disk diffusion technique (Proestos et al. 2006).

Essential oil from the wood of S. tonkinensis was investigated by disk diffusion assay and the broth dilution method against Aspergillus niger and A. flavus. It showed relatively small inhibition zones of 4 mm and 5 mm at 25 mg/disk, respectively. The MIC was 0.78 mg/mL for both species of Aspergillus (Shin, 2003). Additionally, the balsamic resin and its insaponifiable fraction stimulated the phagocytic activity of reticulum endothelial system in mice inoculated with E. coli (Delaveau et al., 1980). The importance of this plant promoted its inclusion in Brazilian Pharmacopoeia (Brandão et al., 2006).

Bioactivity of metabolites

The saponins, jegosaponin A-D (1-4) led to complete suppression of the sensation of sweetness induced by 0.2 M sucrose, but did not suppress the sweetness of 0.4 M sucrose at 1 mM solution (Yoshikawa et al., 2000).

Saponin A-B (5 -6) showed fungistatic activity against Rhizoctonia solani, Pytium aphanidermatum, Rhizopus mucco, A. niger, Fusarium oxyporumlycopersici and Trichoderma viride. For the first two fungi, no mycelial growth inhibition was detected for 5 at concentrations lower than 80 µg/mL. The dose response for 50 % inhibition (ID₅₀) for 5 was determined for T. viride, R. mucco, F. oxysporum , and A. niger as 3.4 µg/mL, 25 µg/mL, 11.7 µg/mL, and 12 µg/mL, respectively. Saponin 6 had no fungistatic activity at lower than 80 µg/mL except on T. viride. The mechanism of action of saponins was related to their hemolytic activity (Zehavi et al., 1986; Segal et al., 1966).

Egonol (7), homoegonol (8), egonol-b-glucoside (9), homoegonol-b-glucoside (10), and dihydrodehydrodiconiferyl alcohol (11) showed antibacterial and antifungal activities against S. aureus and C. albicans with MIC in the range 10 - 20 µg/mL, respectively. However, only 7 and 8 were active in the range of 5 - 10 µg to C. sphaerospermum (Pauletti et al., 2000).

Egonol (7), homoegonol (8), and syringaresinol (12) were evaluated for their cytotoxicity by the MTT method in three cell lines: Hep-2 (larynx epidermoid carcinoma), HeLa (human cervix carcinoma) and C6 (rat glioma). Moderate activities had been observed for 7 against C6 (10.5 µM/mL), and Hep-2 (11.8 µM/mL), also for 8 against HeLa (16.5 µM/mL). Nevertheless, 12 was less active showing a range 27.9- 82.6 µM/mL (Teles et al., 2005). Additionally, the egonol derivatives attracted the attention of synthetic chemists due to its activity against human leukemic HL-60 cells (Hirano et al., 1994).

A lignan, pinoresinol (13), is useful as an antioxidant for thermoplastic resins, foods, pharmaceuticals, and cosmetics, and also as an antihypertensive (Kakie et al., 1994).

The compounds styraxlignolide B-F (14-18), taraxerol (19), syringin (20), and pinoresinol glucoside (21) were tested in vitro for antioxidant activity against DPPH. Compounds 15 , 16 , 17 and 21 exhibited weak radical-scavenging activity, with IC₅₀ values of 380, 278, 194, and 260 µM, respectively. In contrast, 14 , 18 , 19 e 20 which do not have free phenolic groups at all showed IC₅₀ > 500 µM (Min et al., 2004a).

Compounds egonol-b-glucoside (9), styraxjaponoside A-B (22-23), matairesinoside (24), and dihydrodehydrodiconiferyl alcohol-9’-O -glucoside (25) showed no cytotoxicity against the human dermal fibroblasts in the test dose 0.1 – 10 µM, when compared to the control. Therefore the effect of compounds on the expression of type I procollagen, and the MMP-1 proteins (matrix metalloproteinases) in cultured human dermal fibroblasts was examined, and 23 increased the type I procollagen protein expression level by 518.9 ± 18.0%, and decreased the MMP-1 protein expression level significantly by an average of 62.1 ± 8.3 % at 10 µM, compared with the vehicle-treated controls cells. The UV induced MMP-1 protein expression level was significantly inhibited by 63.5 ± 17.6 %, at the same concentration by a pretreatment with 23 in the cultured human dermal fibroblasts. Compound 23 exhibited almost equivalent effects on type I procolagen and MMP-1 expression to that of epigallocatechin-3-gallate, which is used as a positive control. These results indicated that 23 can be used for the treatment and prevention of the skin aging processes (Kim et al., 2004a).

Compounds egonol (7), styraxlignolide A (26), styraxoside A-B (27-28), and masutakeside (29) were tested for anti-complement activity of the complement system; the modulation of complementary activity should be beneficial in the therapy of inflammatory diseases. Compounds 7 , 26 , 28 , and 29 inhibited the hemolytic activity of the complement system with IC₅₀ values of 33, 123, 65, and 166 µM, respectively. In addition to, compound 27 was unable to inhibiting complement activity. The hydrolytic analogues of 26 and 28 were inactive showing that sugar moiety is necessary to enhance the anti-complementary activity of human serum against erythrocytes. On the other hand, the methylenedioxy group seems to be important to the inhibition (Min et al., 2004b).

The benzofurans 5-(3''-hydroxypropyl)-7-hydroxy-2-(3',4'-methylenedioxyphenyl)benzofuran (30), and trans -5-(3'''-hydroxypropyl)-7-methoxy-2[2',3'-dihydro-3'-hydroxymethyl-7'-methoxy-2'-(3''-methoxy-4''-hydroxyphenyl)-benzofuran-5'-yl]benzofuran (31) exhibited cytotoxic activity in vitro using two breast cancer cell lines MCF-7 and MDA-MB-231 (Li et al., 2005).

The triterpenes, oleanolic aldehyde acetate (32), erythrodiol-3-acetate (33), euphorginol (34), and anhydrosophoradiol-3-acetate (35) were evaluated for their cytotoxicity against tumor cells lines. Compounds 32 and 35 exhibited potent cytotoxicity against A549, SK-OV-3, SK-MEL-2, MES-AS, and HCT-15, which IC₅₀ were in the range 5.07 - 9.86 µg/mL, and 3.42 - 7.81 µg/mL, respectively (Kim et al., 2004b). Additionally, the compounds 32 and 35 exhibited potent cytotoxicity against human dermal fibroblasts (IC₅₀ 0.84 µM and 1.12 µM, respectively), and compounds 33 and 34 did not showed cytotoxicity against human dermal fibroblasts in the test dose 0.01-1 µM. Thus the effect on the expression of metaloproteinases (MMP-1) and type I procollagem of 33 and 34 were examined in cultured human skin fibroblasts, given that the regulation mechanisms of MMPs activities are closely related to chronic skin diseases, such as melanona as well as photoaging, which showed higher MMP protein expression, and are caused by long term and repeated exposure of ultraviolet light. Thus 34 did not showed activity on the MMP-1 and type I procollagen synthesis, and 33 reduced the expression of MMP-1 but not MMP-2, at the mRNA and protein levels in a dose-dependent manner by UV irradiation, so it suggests that 33 plays an important role in the reduction of MMP-1 induction by UV irradiation and induced of type I procollagen (Moon et al., 2005a, b).

The triterpenoids, 3b-hydroxy-12-oxo-13Ha-olean-28,19b-olide (36), 6b-hydroxy-3-oxo-11a,12a-epoxyolean-28,13b-olide (37), 3b,6b-dihydroxy-11-oxo-olean-12-en-28-oic acid (38), 3b,6b-dihydroxy-11a,12a-epoxyolean-28,13b-olide (39), 19a-hydroxy-3-oxo-olean-12-en-28-oic acid (40), 6b-hydroxy-3-oxo-olean-12-en-28-oic acid (41), sumaresinolic acid (42), siaresinolic acid (43), and oleanolic acid (44) inhibited HL-60 cell growth with IG₅₀ values ranging from 8.9 to 99.4 µM. Oleanolic acid (44) was the most effective antiproliferative agent, with an IG₅₀ value of 8.9 µM, while (39) exhibited the least effective growth inhibition among these triterpenoids, it induced HL-60 cells to undergo differentiation as measured by an NBT reduction assay (Wang et al., 2006a).

Nerol (45) showed growth inhibitory effect in cooked rice package in the range of 0.5 - 1.5 log CFU/g, the result suggested that this compound could be used as potential agent to extend shelf life of cooked rice (Kim et al., 2004c).

Phytochemistry

Styrax has attracted considerable interest mainly due to the water insoluble resin that has been used in folk medicine and perfumery. Early works focused on the analyses of resin quality and possible adulterations. This resin, known as Benzoin gum, consists of several unique aromatic compounds. Among the resins preparation, the most important are the Siam Benzoin, which is produced from the barks of S. tonkinense and S. benzoin , and Sumatra Benzoin, obtained from S. paralleloneurum (Pastorova et al., 1997).

The phytochemistry investigation on this genus increased in 1915, when Okada isolated egonol (7) for the first time, as an unsaponifiable constituent of the seed oil of S. japonica and its structure was determined by Kawai and Sugiyama (Okada, 1915; Kawai; Sugiyama, 1939).

Other important classes of compounds, the saponins and sapogenin have been studied since 1899, when Keimatsu isolated jegosaponin from the fruits of S. japonica. Since then, the elucidation of the chemical structure of this saponin has been the subject of a number of investigations (Asahina; Momoya, 1914a, b, Sone, 1934, 1936, Tobinaga, 1958). However, in spite of these intensive studies, no structure could be proposed for this saponin until the years 1967 and 1969 (Nakano et al., 1967, 1969). The earlier workers (Asahina; Momoya, 1914a, b; Sone, 1934, 1936; Tobinaga, 1958) reported that the acid hydrolysis of jegosaponin yielded 2 equivalents each of glucuronic acid and glucose (Matsunami, 1927) as well as a sapogenin which, on digestion with alkali, was hydrolyzed to tiglic acid and jegosapogenol (46) (Nakano et al., 1967). Actually, the jegosaponin isolated from S. japonica comprises several saponins, in which, the aglycones are the acylated (acetyl, tigloyl, or 2’-cis -hexenoyl) derivatives of 46 , and jegosapogenin is the major acid-hydrolysis product (Hayashi et al., 1967).

Besides, only one paper reported a comparative study between Styrax and Halesia. The seed, kernel or fruit oils of S. japonicum and H. carolina were analyzed for fatty acid composition, in Halesia , linoleic acid predominates over oleic acid, whereas in Styrax , equal amounts of these two acids are found (Breuer et al., 1987).

CONCLUSION

These data reveal predominately the occurrence of shikimate derivatives such as lignans derivatives of 3,7-dioxabicyclo [3.3.0], butanolide, and tetrahydrofuran, neolignans derivatives of dihydrobenzofuran, norlignans derivatives of benzofuran, phenylpropanoids, and phenolic acids, as well as the presence of acetate derivatives pentacyclic saponins and triterpenes in Styrax species. Some of saponins exhibited antisweet activity (1 -4), fungistatic activity (5 -6), and anti-inflammatory activity (28). The shikimate derivatives showed a variety of activities such as antibacterial and antifungal (7 -11), cytotoxicity against tumor cell lines (7 , 8 , 12 , 30 , 31), antioxidant activity (13 , 15 -17 , 21) antihypertensive (13), antiinflamatory (7 , 26 , 28 , 29), and prevention of skin aging process (23). The triterpenes showed cytotoxicity against tumor cell lines (32-44) and protection against UV irradiation (33). Our contribution was principally in relation to the isolation of pentacyclic triterpenes, and biological activity studies. Nevertheless, only some genera have been studied chemically, and the chemotaxonomic aspects of Styracaceae are far from being established. Otherwise it seems that Styrax accumulates norlignans derivatives as benzofuran, and it is important to point out that this particular class of norlignan occurs widely in Styrax. Thus benzofuran derivatives should be considered chemosystematic markers of Styrax. Additionally, it seems that Styrax being these derivatives leads chemistry. On the other hand, some extracts showed important activities and they might be useful as phytomedicines. Styrax has proven to be a very valuable genus to the discovery and utilization of medicinal natural products, and to drug discorery particularly lignans, norlignans, saponins and pentacyclic triterpenes.

ACKNOWLEDGMENT

PMP, VdaSB, HLT, and DHSS acknowledge CNPq and FAPESP for financial support. This work was funded by grants of the State of São Paulo Research Foundation (FAPESP) within the Biota-FAPESP (www.biotasp.org.br); Grant # 03/02176-7 awarded to Dr. Bolzani, principal investigator.

Received 07/31/06. Accepted 10/24/06

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Publication Dates

• Publication in this collection
  17 May 2007
• Date of issue
  Dec 2006

History

• Accepted
  24 Oct 2006
• Received
  31 July 2006