Mini Review | Volume: 10, Issue: 7, July, 2020

Bioactive compounds of Boesenbergia sp. and their anti-inflammatory mechanism: A review

Aziiz Mardanarian Rosdianto Irma Melyani Puspitasari Ronny Lesmana Jutti Levita   

Open Access   

Published:  Jul 04, 2020

DOI: 10.7324/JAPS.2020.10715
Abstract

Boesenbergia sp. (Zingiberaceae) has been empirically used in Indonesia, to treat rheumatism. The rhizome of Boesenbergia rotunda contains essential oils (nerol, camphor, cineole, fenchene, hemanthidine, and limonene), flavonoids (alpinetin, boesenbergin, cardamonin, pinostrobin, pinocembrin, geraniol, panduratin, and silybin), and polyphenols (caffeic acid, coumaric acid, chlorogenic acid, hesperidin, kaempferol, naringin, and quercetin), which explain its many interesting pharmacological activities (antifungal, anti-inflammatory, antimicrobial, antibacterial, anticancer, antimutagenic, antiparasitic, antiulcer, antileukemia, hepatoprotective, and antiviral). This review focuses on the bioactive compounds in Boesenbergia sp. and their molecular mechanism in reducing inflammation. Of all bioactive compounds, panduratin A and 4-hydroxypanduratin A have proven their activity in inhibiting the production of nitric oxide and PGE2 as well as on tumor necrosis factor-alpha. Moreover, this paper also provides other uses of this plant species as well as future study aspects.


Keyword:     B. rotunda flavonoid kaempferol panduratin A quercetin Zingiberaceae.


Citation:

Rosdianto AM, Puspitasari IM, Lesmana R, Levita J. Bioactive compounds of Boesenbergia sp. and their anti-inflammatory mechanism: A review. J Appl Pharm Sci, 2020; 10(07):116-126.

Copyright: © The Author(s). This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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INTRODUCTION

Inflammation is the body’s response in combatting pathogens or destructing chemicals (cytokines and histamines). The cascade of inflammatory-related mediators frames the acute inflammatory response, which is activated by recruiting granular white blood cells and frequently resolves the outcome recovery. Understanding how the inflammatory process is triggered might be beneficial for developing the strategies to inhibit the inflammatory responses (Ward and Lentsch, 1999).

Various therapeutics are being used to stop or reduce the inflammation process, such as nonsteroidal anti-inflammatory drugs and corticosteroids. Unfortunately, these drugs have been reported, case by case, for their unfavorable effects, for example, the increase of blood pressure, peptic ulceration, acute kidney dysfunction, and other serious conditions (Attiq et al., 2017).

The plants of Zingiberaceae family, for example, Boesenbergia rotunda (L.) Mansf. (Eng-Chong et al., 2011; Jing et al., 2010; Yusuf et al., 2013), Renealmia alpinia (Nunez et al., 2004), and Zingiber zerumbet (Taha et al., 2010), have been extensively investigated for their potential phytoconstituents and molecular mechanism.

Boesenbergia rotunda contains various phytoconstituents, classified into two major groups – namely, flavonoids and chalcone derivatives (pinocembrin, pinostrombin, alpinetin, panduratin, cardamonin, quercetin, and kaempferol) (Eng-Chong et al., 2012; Rosdianto et al., 2020), which might indicate a great benefit for drug discovery (Jing et al., 2010; Yusuf et al., 2013). Since this plant serves as the wide range of traditional medicine applications, many thorough studies were carried out to assess its pharmacology activities, such as antiulceration (Abdelwahab et al., 2011), hepatoprotective (Mahmood et al., 2010; Salama et al., 2013), Helicobacter pylori inhibitor (Bhamarapravati et al., 2006), anti-inflammatory (Isa et al., 2012), anticancer (Cheah et al., 2011; Isa et al., 2013), antiallergic (Madaka & Tewtrakul, 2011), antibacterial (Udomthanadech et al., 2015; Zainin et al., 2013), antileptospiral (Chander et al., 2016), antioxidant (Chiang et al., 2017), anti-dengue viral (Chee et al., 2010; Kiat et al., 2006), antiherpes viral (Wu et al., 2011), wound-healing (Mahmood et al., 2010), antimutagenic, antibacterial, antifungal, analgesic, antipyretic, antispasmodic, insecticidal, larvicidal, and pupicidal (Ching et al., 2007; Jaiptech et al., 2010; Phukerd et al., 2013) activities.

This review focuses on the bioactive compounds in Boesenbergia sp. and their mechanism as anti-inflammatory agents. Moreover, this paper also provides other utilities of Boesenbergia sp. as well as its future study aspects (Table 1). The required pieces of information were obtained by searching keywords which include Boesenbergia, Zingiberaceae, flavonoids, kaempferol, panduratin, and quercetin, among published articles until March 2020 in authentic scientific databases.

Methods

The literature search was performed on PubMed database using the following keywords: “Boesenbergia sp.” [Medical Subject Headings (MEeSH) terms] or “Zingiberaceae” [all fields] and “B. rotunda” [Subheading] or “Zingiberaceae” [all fields] or “bioactive compounds” [all fields] or “bioactive compounds” [all fields] or “pharmacological activity of B. rotunda” [MeSH terms] or “pharmacological activity of B. rotunda” [all fields] or “anti-inflammatory activity of B. rotunda” [MeSH terms] or “anti-inflammatory activity of Boesenbergia sp.” [all fields]. A search on other scientific databases using the same keywords was done for additional data.

Ethnobotany Facts

Zingiberaceae, a family of lasting herbs, are aromatic, with fleshy tuberous or nontuberous rhizomes. Zingiberaceae plants are widely distributed throughout the tropics, especially in Indonesia, and comprise 150 species of ginger (Habsah et al., 2000; Ibrahim et al., 2010). Ginger plants are extensively utilized to enhance food taste, cure diseases, beverages, perfume, and so forth (Abdelwahab et al., 2010; Taha et al., 2010). Recent molecular studies such as chloroplast DNA, nuclear internal transcribed spacer, random amplified polymorphic DNA, plastid regions, pollen-based classifications, amplified fragment length polymorphism, and single-strand conformation polymorphism have been employed to taxonomically classify Boesenbergia species (Chen and Xia, 2011; Kress et al., 2002; Techaprasan et al., 2006; Techaprasan et al., 2008; Vanijajiva et al., 2005).

Phytoconstituents

The active phytoconstituents of B. rotunda are (1) flavonoids including alpinetin, boesenbergin, cardamonin, pinostrobin, pinocembrin, geraniol, panduratin, and silybin (Fig. 1) (Ching et al., 2007; Morikawa et al., 2008; Yusuf et al., 2013); (2) essential oils including camphor, cineole, fenchene, hemanthidine, and limonene (Fig. 2) (Baharudin et al., 2015); and (3) polyphenols including caffeic acid, coumaric acid, chlorogenic acid, hesperidin, kaempferol, naringin, and quercetin (Fig. 3) (Jing et al., 2010; Rosdianto et al., 2020).

Anti-Inflammatory Mechanism of Boesenbergia sp.

Table 1 shows all the pharmacological activities of B. rotunda; however, this review study will only focus on the anti-inflammatory mechanism of this plant.

In the Asia region, particularly in Indonesia, B. rotunda has been empirically utilized to treat various types of inflammation. Its flavonoids (panduratin A, 4-hydroxypanduratin A, cardamonin, 2′,4′,6′-trihydroxychalcone, uvangoletin, panduratin C, boesenbergin A, 2′,6′-dihydroxy-4′-methoxychalcone, hydroxypanduratin A, (−)-isopanduratin A, (+)-krachaizin B, (−)-krachaizin B, quercetin, and kaempferol) extracted from the tuberous root of B. pandurata had been studied for their anti-inflammatory activity (Chahyadi et al., 2014; Isa et al., 2012; Rho et al., 2011; Tewtrakul et al., 2009; Tuchinda et al., 2002; Yun et al., 2003).

Panduratin A and Hydroxypanduratin A inhibit TNF-α and the production of nitric oxide

Nitric oxide (NO) plays a key role in maintaining vascular function. The overproduction of NO could damage the tissue and is related to acute and chronic inflammation. An anti-inflammatory study in Thailand reported that phytoconstituents isolated from the extract of B. rotunda strongly inhibit NO production, for example, panduratin A, hydroxypanduratin A, and cardamonin. Moreover, a medium strength of inhibitory activity on tumor necrosis factor-alpha (TNF-α) was observed for both panduratin A and hydroxypanduratin A (Tewtrakul et al., 2009). The NO inhibitors are favorable because NO regulates cerebral blood flow and nociception in migraine-induced animal models (Wong and Lerner, 2015).

Panduratin A and Hydroxypanduratin A inhibit PGE2 production

Prostaglandin synthase catalyzes two separate reactions: (1) the addition of O2 to oxygenate the arachidonic acid molecule until an unstable prostaglandin G2 (PGG2) is produced and (2) PGG2 then migrates to the peroxidase site where it reacts with the hemin group to generate prostaglandin H2 (PGH2) (Levita et al., 2009). PGH2 is subsequently converted into the active PGE2, PGI2, PGD2, PGF, and thromboxane A2 (Nørregaard et al., 2015). Both panduratin A and hydroxypanduratin A strongly inhibit PGE2 production (Tewtrakul et al., 2009). The inhibition of PGE2 production could lessen inflammatory symptoms and pain (Sugita et al., 2016).

Boesenbergia rotunda inhibits the infiltration of inflammatory cells in the hepatic bile ducts

The extract of B. rotunda reduces the inflammation caused by Opisthorchis viverrini and induced by N-nitrosodimethylamine administration in rats. This study proved that there was a decrease in the number of inflammatory cells infiltrated into the hepatic bile ducts as well as the serum alanine transaminase and direct bilirubin level (Boonjaraspinyo et al., 2010).

Boesenbergia rotunda accelerates wound healing in rats

A wound recovery is a dynamic process of repairing cellular structures in damaged tissue. Wound abridgment occurs throughout the recovery process commencing in the fibroblastic stage followed by the proliferative stage (Midwood et al., 2004). Flavonoids have been proven to promote the wound-healing process due to their antimicrobial activities, which is responsible for wound contraction and increased the rate of epithelialization. Flavonoids could inhibit lipid peroxidation by preventing the onset of cell necrosis and improving vascularity. Therefore, any compound that reduces lipid peroxidation is predicted, which might be able to enhance the viability of collagen fibers, increase blood circulation, halt the cell damage, and stimulate the DNA synthesis (Getie et al., 2002).

Table 1. Pharmacology activity of B. rotunda.



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Figure 1. 2D structure of flavonoids in B. rotunda (downloaded from http://www.chemspider.com/).

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The ethanolic extract of B. rotunda rhizome could accelerate wound healing in rats (Mahmood et al., 2010). This plant extract, which contains various types of free radical scavenging molecules – for example, flavonoids and polyphenols, has exhibited antioxidant activity (Shindo et al., 2006). Antioxidants significantly play an important role in the wound-healing process and block the oxidative damage (Martin, 1996).

Boesenbergia rotunda and pinostrobin reduce ulcer inflammation

Boesenbergia rotunda has been utilized empirically to cure ulcers by the people in Thailand and Indonesia. The antiulcer activity of the methanol extract of B. rotunda and its phytoconstituent pinostrobin has been studied by Abdelwahab et al. It was reported that B. rotunda extract and pinostrobin revealed the cytoprotective effects on ulcer-induced rats. This plant extract also significantly decreased submucosal edema and leukocyte infiltration (Abdelwahab et al., 2011).

Boesenbergia rotunda and panduratin A as anticancer

Kirana et al. (2003) assayed through eleven species of Zingiberaceae and discovered that B. rotunda and Zingiber aromaticum indicated the highest inhibition toward the growth of MCF-7 breast cancer and human HT-29 colon cancer cells (Kirana et al., 2003). An additional study of panduratin A on the same cell lines has also proven similar potent inhibitory properties and a nontoxic result to the rats (Kirana et al., 2007).

B. rotunda volatile oils revealed cytotoxic activities against MCF-7 (IC50  31.7 ± 5.4 μg/ml) and LS174T cell lines (Zaeoung et al., 2005). In a separate study, Jing et al. (2011) demonstrated that B. rotunda possessed a moderate inhibitory activity against CaOV3 ovarian cancer, breast cancer malone dialdehyde-MB-231, MCF-7, HeLa cervical cancer, and HT-29 colon cancer cell growth as compared to three other Boesenbergia species: B. pulchella var. attenuate and B. armeniaca (Jing et al., 2011).

In 2006, Yun et al. demonstrated that panduratin A could prevent the growth of prostate cancer cell lines (PC3 and DU145) in a time- and dose-dependent manner. An immunofluorescence assay revealed that panduratin A activated the induction of apoptosis in both cell lines by inhibiting apoptotic-related procaspases 3, 6, 8, and 9 (Yun et al., 2006). Panduratin A also exhibited inhibitory activities against the growth of A549 human non-small cell lung cancer cells (Cheah et al., 2011).

Figure 2. 2D structure of essential oils in B. rotunda (downloaded from http://www.chemspider.com/).

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Figure 3. 2D 2D structure of polyphenols in B. rotunda (downloaded from http://www.chemspider.com/).

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The antileukemia activity of B. rotunda rhizome extracts has been investigated and revealed that the chloroform extract and boesenbergin A could inhibit the growth of HL-60 cell line (Sukari et al., 2007).

Panduratin A inhibits NF-kappaB translocation to the nucleus

Panduratin A could inhibit the translocation of NF-kappaB from the cytoplasm to nuclei (Cheah et al., 2011).

Toxicity Study

The toxicity of the B. rotunda extract was studied in normal healthy rats by exposing the animals to high doses of the rhizome extract (2  and 5 g/kg of BW) (Mahmood et al., 2010; Manosroi et al., 2017; Salama et al., 2012). An in vivo study indicated that the ethanol extract of B. rotunda was not toxic as there were no significant changes in the body weight of the rats. Moreover, all hematological and histopathological parameters did not show any adverse changes (Lim, 2016; Saraithong et al., 2010). Meanwhile, pinostrobin and pinocembrin revealed no mutagenic effect or toxicity toward Wistar rats, which confirmed the safety of these compounds (Charoensin et al., 2010).


CONCLUSION

The traditional utilities of B. rotunda rationalize that this plant could be upgraded to the next level of drug discovery study. Nonetheless, the molecular mechanism of panduratin A and 4-hydroxypanduratin A of B. rotunda has described their activity in inhibiting the production of nitric oxide and PGE2 as well as on TNF-α. Panduratin A also inhibits the translocation of NF-kappaB to the nucleus, which might contribute to this plant’s anti-inflammatory activity. Furthermore, the ethanolic extract of B. rotunda was considered not toxic as it did not alter the body weight and hematological parameters of rats.


ACKNOWLEDGMENT

The publication fee is funded by Doctoral Dissertation Grant 2019 of the Ministry of Research and Technology and Higher Education, the Republic of Indonesia (10/E1/KP.PTNBH/2019).


CONFLICTS OF INTEREST

There are no conflicts of interest related to the publication of this paper.


FUNDING

None.


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Techaprasan J, Ngamriabsakul C, Klinbunga S, Chusacultanachai S, Jenjittikul T. Genetic variation and species identification of Thai Boesenbergia (Zingiberaceae) analyzed by chloroplast DNA polymorphism. J Biochem Mol Biol, 2006; 39(4):361–70. CrossRef

Teethaisong Y, Pimchan T, Srisawat R, Hobbs G, Eumkeb G. Boesenbergia rotunda (L.) Mansf. extract potentiates the antibacterial activity of some β-lactams against β-lactam-resistant staphylococci. J Glob Antimicrob Resist, 2018; 12:207–13. CrossRef

Tewtrakul S, Subhadhirasakul S, Kummee S. HIV-1 protease inhibitory effects of medicinal plants used as self medication by AIDS patients. Songklanakarin J Sci Technol, 2003; 25(2):239–43. CrossRef

Tewtrakul S, Subhadhirasakul S, Karalai C, Ponglimanont C, Cheenpracha S. Anti-inflammatory effects of compounds from Kaempferia parviflora and Boesenbergia pandurata. Food Chem, 2009; 115(2):534–538. Available via http://dx.doi.org/10.1016/j.foodchem.2008.12.057

Trakoontivakorn G, Nakahara K, Shinmoto H, Takenaka M, Onishi-Kameyama M, Ono H, Yoshida M, Nagata T, Tsushida T. Structural analysis of a novel antimutagenic compound, 4-hydroxypanduratin A, and the antimutagenic activity of flavonoids in a Thai spice, fingerroot (Boesenbergia pandurata Schult.) against mutagenic heterocyclic amines. J Agric Food Chem, 2001; 49(6):3046–50. CrossRef

Tuchinda P, Reutrakul V, Claeson P, Pongprayoon U, Sematong T, Santisuk T, Taylor WC. Anti-inflammatory cyclohexenyl chalcone derivatives in Boesenbergia pandurata. Phytochem, 2002; 59(2):169–73. CrossRef

Udomthanadech K, Vajrodaya S, Paisooksantivatana Y. Antibacterial properties of the extracts from some Zingibereous species in Thailand against bacteria causing diarrhea and food poisoning in human. Int Trans J Eng Manage Appl Sci Technol, 2015; 6:203–13.

Vanijajiva O, Sirirugsa P, Suvachittanont W. Confirmation of relationships among Boesenbergia (Zingiberaceae) and related genera by RAPD. Biochem Syst Ecol. 2005; 33(2):159–70. CrossRef

Voravuthikunchai SP, Phongpaichit S, Subhadirasakul S. Evaluation of antibacterial activity of medicinal plants widely used among AIDS patients in Thailand. Pharm Biol, 2005; 43:701–6. CrossRef

Ward PA, Lentsch AB. The acute inflammatory response and its regulation. Arch Surg, 1999; 134(6):666–9. CrossRef

Wong V, Lerner E. Nitric oxide inhibition strategies. Future Sci OA, 2015; 1(1):FSO35. CrossRef

Wu N, Kong Y, Zu Y, Fu Y, Liu Z, Meng R, Liu X, Efferth T. Activity investigation of pinostrobin towards herpes simplex virus-1 as determined by atomic force microscopy. Phytomedicine, 2011; 18:110–8. CrossRef

Yu JM, Kwon H, Hwang JK. In vitro anti-inflammatory activity of panduratin A isolated from Kaempferia pandurata in RAW264.7 cells. Planta Med, 2003; 69:1102–8. CrossRef

Yun JM, Kwaeon MH, Kwon H, Hwang JK, Mukhtar H. Induction of apoptosis and cell cycle arrest by a chalcone panduratin A isolated from Kaempferia pandurata in androgen-independent human prostate cancer cells PC3 and DU145. Carcinogenesis, 2006; 27(7):1455–64. CrossRef

Yusuf N, Annuar M, Khalid N. Existence of bioactive flavonoids in rhizomes and plant cell cultures of Boesenbergia rotunda (L.). Mansf. Kulturpfl. Aust J Crop Sci, 2013; 7:730–4. Available via https://www.researchgate.net/publication/288138724_ Existence_of_bioactive_ flavonoids_in_rhizomes_and_plant_cell_cultures_ of_boesenbergia_rotunda_L_Mansf_Kulturpfl

Zaeoung S, Plubrukarn A, Keawpradub N. Cytotoxic and free radical scavenging activities of Zingiberaceous rhizomes. Songklanakarin J Sci Technol, 2005; 27(4):799–812. Available via http://rdo.psu.ac.th/sjstweb/journal/27-4/11-Zingiberaceous-rhizomes.pdf

Zainin N, Lau K, Zakaria M, Son R, Abdull RA, Rukayadi Y. Antibacterial activity of Boesenbergia rotunda (L.). Mansf. A. extract against Escherichia coli. Internat Food Res J, 2013; 20:3319–23. Available via http://www.ifrj.upm.edu.my/ 20%20(06)%202013/50%20I FRJ%2020%20(06)%202013%20Rohman%20Yaya%20422.pdf

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Udomthanadech K, Vajrodaya S, Paisooksantivatana Y. Antibacterial properties of the extracts from some Zingibereous species in Thailand against bacteria causing diarrhea and food poisoning in human. Int Trans J Eng Manage Appl Sci Technol, 2015; 6:203-13.

Vanijajiva O, Sirirugsa P, Suvachittanont W. Confirmation of relationships among Boesenbergia (Zingiberaceae) and related genera by RAPD. Biochem Syst Ecol. 2005; 33(2):159-70. https://doi.org/10.1016/j.bse.2004.06.012

Voravuthikunchai SP, Phongpaichit S, Subhadirasakul S. Evaluation of antibacterial activity of medicinal plants widely used among AIDS patients in Thailand. Pharm Biol, 2005; 43:701-6. https://doi.org/10.1080/13880200500385194

Ward PA, Lentsch AB. The acute inflammatory response and its regulation. Arch Surg, 1999; 134(6):666-9. https://doi.org/10.1001/archsurg.134.6.666

Wong V, Lerner E. Nitric oxide inhibition strategies. Future Sci OA, 2015; 1(1):FSO35. https://doi.org/10.4155/fso.15.35

Wu N, Kong Y, Zu Y, Fu Y, Liu Z, Meng R, Liu X, Efferth T. Activity investigation of pinostrobin towards herpes simplex virus-1 as determined by atomic force microscopy. Phytomedicine, 2011; 18:110-8. https://doi.org/10.1016/j.phymed.2010.07.001

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Yun JM, Kwaeon MH, Kwon H, Hwang JK, Mukhtar H. Induction of apoptosis and cell cycle arrest by a chalcone panduratin A isolated from Kaempferia pandurata in androgen-independent human prostate cancer cells PC3 and DU145. Carcinogenesis, 2006; 27(7):1455- 64. https://doi.org/10.1093/carcin/bgi348

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