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Bioassay-guided isolation of a sesquiterpene lactone of deoxyelephantopin from Elephantopus scaber Linn, active on Trypanosome brucei rhodesience.


Methanolic extracts of 70 Malaysia plants were screened for their in vitro antitrypanosomal activity using Trypanosome brucei rhodesience, strain STIB 900 and mouse skeletal cell (L-6) in cytotoxicity activity assay. Results indicated that methanol extract from Elephantopus scaber Linn. (E. scaber) possessed the highest value of antitrypanosomal activity with good selectivity index (antitrypanosomal [IC.sub.50] of 0.22 [+ or -] 0.02 [micro]g/ml, Si value of 204.55). Based on these results, E. scaber was chosen for further study by applying bioassay guided fractionation to isolate its antiprotozoal principle. The antiprotozoal principle was isolated from the ethyl acetate partition through solvent fractionation and crystallization process. The isolated active compound 1 was identified as deoxyelephantopin on the basis of its spectral analysis (FTIR.MS, ID and 2D NMR).


Elephantopus scaber



Trypanosome brucei rhodesience

Bioassay-guided isolation;


Sleeping sickness or known as Human African Trypamosomiasis (HAT) is a disease that has affects 36 countries of sub-Saharan Africa, annually reported as 17,500 new cases (Sykes and Avery 2009). This disease was considered to be the first or second greatest cause of mortality, compared to HIV/AIDS, in those communities (WHO 2006). The treatment of this disease is few and limited due to age, toxicity, difficulty to administer, cost, and/or compromised by the development of resistance (Hoet et al. 2004a). The identification of new potential of antitrypanosomal drug candidates should be an urgent priority (Watkins 2003).

The disease is caused by infection of protozoan parasite genus of Trypanosome: Trypanosoma brucei rhodosiense (in East and Southern Africa) and Trypanosoma bruceigambiense (in west and central Africa) (Salem and Werbovetz 2006). Tsetse fly (Clossina sp.) is the vector of this disease. Infection is transmitted through bloodsucking male and female flies (Salem and Werbovetz 2006). The protozoan parasites will then live and multiply extracellular in blood and tissue fluids of their mammalian that had been transmitted (Steverding 2008). The life cycle of T. brucei subspecies begun in human infected with metacyclic forms then differentiate into bloodstream, subcutaneous tissues and lymph (Sternberg 2004).

Research had been carried out in discovering drugs to treat the disease since 1950s (Salem and Werbovetz 2006). Pentamidine and Suramine were used to treat initial phase but do not cross blood-brain barrier (Khan 2007; Nok 2003). Melarsoprol was used to treat late stage of the disease (Gull 2002; Nok 2003). However, it could caused fatal reactive encephalopathy in 5-10% of cases treated and 10-50% patients died (Gull 2002). Another drug, Elfornithine was used for late stage of T. brucei gambiense infection but it is ineffective against T. brucei rhodesiense and must be administered in high doses over a long course of treatment (Salem and Werbovetz 2006).

Medicinal plants are one of unique parts in this megabiodiversity, without no doubt possess active principles that can cure many diseases. Therefore, it is not surprising that some natural products of plant origin display trypanocidal activities (Adewunmi et al. 2001; Bala et al. 2011; Cotinguiba et al. 2009; Freiburghaus et al. 1996; Ogbunugafor et al. 2008; Hoet et al. 2004a; Mbaya et al. 2007; Mesia et al. 2008; Wurochekke and Nok 2005).

Over the last decade, several natural compounds including alkaloids, quinones and terpenes have been identified to inhibit the growth of trypanosomes in vitro (Hoet et al. 2004b). Sesquiterpene lactones isolated from Sausseria costus have been shown to inhibit the growth of T. brucei rhodesiense (Julianti et al. 2011). Another interesting compound, ascofuranone, isolated from phytopathogenic fungus Aschochyta visiae was found to inhibit the trypanosomal alternative oxidase, a unique mitochondrial electron transport system of T. brucei rhodesiense (Yabu et al. 2003). Our group has been engaged in the intense search for new natural products for treatment of HAT from plants and other biodiversity resources. We have screened 70 plant extracts on trypanosome parasite, T. brucei rhodesiense (STIB900) and isolated an active compound from medicinal plant, Elephantopus scaber by using bioassay guided approached.

Materials and methods

General experiment procedure

Optical rotation was recorded with a Jasco DIP-370 Digital Polarimeter. Melting point was measured on a Leica Gallen III Kofler micro melting point apparatus and was uncorrected. Infrared spectrum was obtained using a Nicolet 6700 FT-IR spectrophotometer equipped with an attenuated total reflectance (ATR) accessory. [sup.1H] NMR (400MHz) and [sup.13]C NMR (100MHz) spectra were recorded on a Bruker Avance 400 spectrometer, with CD[Cl.sub.3] as a solvent and tetramethylsilane (TMS) as internal standard. COSY, DEPT, HMQC and HMBC NMR experiments were performed in the same spectrometer. ESIMS was recorded on TSQ Quantum Ultra Triple Quadrupole spectrometer. Thin layer chromatography (TLC) was performed on 0.20 mm precoated silica gel aluminum sheets (Merck Kieselgel 6O[F.sub.254]).Spots were visualized with UV light (254 nm) and sprayed with vanillin sulphuric acid. Gravity column chromatography (CC) was carried out by using Merck silica gel 60 (70-230 mesh).

Plant material

Leaves of E. scaber were collected from Taman Pertanian, Relau, Penang, Malaysia in 2009. The taxonomic identification of the plant was identified by a botanist of Forest Biodiversity Division, Forest Research Institute Malaysia, Malaysia. Voucher specimen is deposited in the herbarium of INaC Library (IPharm Natural Compound Library) with coding of IPharm/HerbOl. Plants were dried in the drying oven for 3 days at 50[degrees]C.

Preparation of the crude plant extract

The dried powder of E. scaber(300 g) was soaked with methanol (1.51) for three days. Then, the extracts were concentrated by using rotary vacuum evaporator (Brand: Eyela) at 40[degrees]C under reduced pressure to dryness to give 24g (8%) of methanol extract. The methanolic extract was kept at 4[degrees]C.

Fractionation of the methanolic extract of E. scaber

24g of methanolic extract was dissolved in 500 ml of 80% methanol. The methanolic extract was then partitioned by using ethyl acetate (3x400 ml), n-hexane (3 x 400 ml) and n-butanol (3 x 400 ml), subsequently. The n-hexane extract formed was designated as fraction A (6.05 g), ethyl acetate extract as fraction B (4.47 g) and n-butanol extract as fraction C (0.13 g).

Isolation of compound 1

Fraction B (2g) was further fractionated by open silica gel column chromatography (silica gel 60F, 70-230 mesh, 0.040-0.063 mm, Merck) and eluted with mixture of increasing polarity n-hexane-ethyl acetate-methanol (100:0:0, 80:20:0, 70:30:0, 60:40:0, 50:50:0, 0:100:0, 0:50:50, 0:0:100). The eluent size used was 400 ml for each of eluent system to obtain 320 fractions. Based on the TLC pattern of these fractions, 14 fractions were finally obtained. Fr. 13 exhibited the most potent antitrypanocidal activity. Upon crystallization of Fr. 13 with n-hexane and methanol afforded pure antitrypanosomal compound 1 (66 mg) (Fig. 1).

Trypanosome parasite and cell line

T. brucei rhodesience (strain STIB 900) was imported from Swiss Tropical Institute, Basel Switzerland in 2007. The parasites were grown and maintained as reported previously (Freiburghaus et al. 1998). Mouse skeletal cell (L-6) was purchased from ATCC. Cells were cultured and maintained as reported previously (Ioset et al. 2009).

Antitrypanosomal activity and cytotoxicity of samples

T. brucei rhodesience (strain STIB 900) parasite and mouse skeletal (L-6) cell were used in the in vitro antitrypanosomal assay and cytotoxicity assay as reported previously (Bakunov et al. 2009). 1% of DMSO solution of samples (100 pl/well, concentration of the sample range of 90-0.123 [micro]g/ml) was added to both assays at 37[degrees]C under 5% C[O.sub.2] atmosphere. The incubation period was 72 hours and 70 hours on antitrypanosomal assay and cytotoxicity assay, respectively. The survival of both parasites and cells were assessed using the fluorescence reduction of the resazurin by the viable parasites and viable cells in accordance with the procedure of Raz et al. (1997) with small modifications.

Results and discussion

In present study, 70 methanolic extracts were tested for their in vitro antitrypanosomal activity against T. brucei rhodesience strain STIB 900. The active extracts were then tested on their cytotoxicity activity against mouse skeletal cell (L-6) to determine their selectivity index value. The methanolic extract was tested at concentration range of 0.123-90 [micro]g/ml for both assays. Out of 70 methanolic extracts, E. scaber potently reduced T. brucei. rhodesience parasites with [IC.sub.50] 0.22 [+ or -] 0.02 [micro]g/ml. Mouse skeletal cell (L-6) viability was high with selectivity index (SI) of 204.55. From the result of the present screening, it is expected that E. scaber contains antitrypanosomal parasites ingredients. Subsequently, the methanolic extract of E. scaber was chosen in this study to isolate the active antitrypanosomal compound.

E, scaber comes from Compositae (Astaraceae) family with small herb and grow mild throughout the warm part. It is also popularly known as Prickley leaved elephant (English), Gobhi (Hindi), Gojivha (Sanskrit), Eddumalikechettu (Telugu) and Nayi naliga (Kannada) (Singh et al. 2005). There are many constituents in E. scaber including flavanoids, triterpenoids, flavanoids esters and sesquertepene lactone (Xu et al. 2006). Sesquertepene lactones such as scabotopin, isoscarbotepin, deoxyelephantopin and iso-deoxyelephantopin are the most important constituents as they have good activity in antitumor (Xu et al. 2006).

Table 1 showed the results on antitrypanosomal activity and cytotoxicity activity tested on extract, partitions, fractions and compound on study of bioassay guided isolation in search of antitrypanosomal substance from E. scaber. In addition, the [IC.sub.50] value of standard drugs used in the study i.e. melarsoprol and pentamidine were also included in Table 1. Based on the results, ethyl acetate fraction (Fr. B) of the methanolic extract of E. scaber revealed the highest antitrypanosomal activity (0.21 [+ or -] 0.04 [micro]g/ml) with a lower cytotoxicity (6.25 [+ or -] 0.77 [micro]g/ml). This fraction was further purified on a silica gel column by subjecting to bioassay-guided fractionation and as a result, a known sesquiterpene lactone deoxyelephantopin (compound 1) (Fig. 1) was isolated as the antitrypanosomal compound. Compound 1 agrees in every respect (mp, UV, 1R, NMR and MS) with those of the literatures (But et al. 1997; Than et al. 2005)

With an [IC.sub.50] value of 0.024 [+ or -] 0.005 [micro]g/ml, compound 1 showed a potent trypanocidal activity. However the activity of compound 1 is lower than the activity of suramine and pentamidine, drugs used for treatment of sleeping sickness.

The in vitro antitrypanosomal activity of the germacranolide dilactone of compound 1 could be due to the presence the [alpha]-methylene-[gamma]-lactone moiety. Several sesquiterpene lactones having an [alpha]-methylene-[gamma]-lactone moiety such as parthenolide, eupatoriopicrin, costunolide (Julianti et al. 2011), 15-deoxygoyazensolide (Chiari et al. 1991), dehydrozaluzanin C (Fournet et al. 1993), lychnopholide (de Oliveira et al. 1996), naematolin (Inchausti et al. 1997) and dehydroleucodine (Brengio et al. 2009) have been reported to show trypanocidal activity. The presence of [alpha]-methylene-[gamma]-lactone moiety in 1 could form the basis for the study of the mechanism of action of this active compound. The bond formation of [alpha]-methylene-[gamma]-lactone moiety of compound 1 with the -SH groups of panothione (1,8-bis-glutathionyl spermidine) of the trypanosome could inactivate the defence system and exposing the parasite to oxidative damage (Daunes and D'Silva 2002).

Although compound 1 has been previously isolated from the plant of E. scaber, this is the first report on the antitrypanocidal activity for this compound. Further studies will be required to determine mechanism action of this active compound with the presence of [alpha]-methylene-[gamma]-lactone moiety and to evaluate therapeutic value of this kind of natural products for trypanosomiasis infection.


Article history:

Received 30 May 2013

Received in revised form 8 August 2013

Accepted 19 September 2013


This project was financially supported by Research Grant No: 09-05-IFN-BPH-003, Ministry of Science, Technology and Innovation Malaysia.

The authors would like to acknowledge: Team of Drug for Neglected Diseases Initiative (DNDi), Professor Reto Brun and Tanja Wenzler from the Swiss Tropical and Public Health Institute for guidance in the bioassay transfer and for providing the Trypanosoma brucei rhodesiense strain ST1B900.


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Zuriati Zahari (a), Nor Akmalazura Jani (b), Azimah Amanah (a), Mohd Naffidi Abdul Latif (a), Mohamed Isa Abdul Majid (c), Mohd Ilham Adenan (a,d) *

(a) Malaysian Institute of Pharmaceuticals and Nutraceuticals, Ministry of Science, Technology and Innovation, Malaysia

(b) Universiti Teknologi MARA Negeri Sembilan, Kampus Kuala Pilah, Beting, 72000 Kuala Pilah, Negeri Sembilan, Malaysia

(c) Universiti Sains Malaysia, Penang, Malaysia

(d) Forest Research Institute Malaysia. 52109 Kepong, Selangor, Malaysia

* Corresponding author at: Forest Research Institute Malaysia. 52109 Kepong, Selangor, Malaysia. Tel.: +603 62797000.

E-mail address: (M.I. Adenan).

Table 1
Antitrypanosomal activity against Trypanosome brucei rhodesience STIB
900 and cytotoxicity in L-6 cell of Elephantopus scaber extract,
fractions and compound 1 and two commonly used antitrypanosomal drugs.

Samples                        [IC.sub.50] ([micro]g/ml)

                          Antitrypanosomal       Cytotoxicity L-6
                          activity ST1B 900

(a) Crude methanol         0.22 [+ or -] 0.02     45.00 [+ or -] 2.50

(b) Partition extracts

  n-Hexane (Fraction A)    6.97 [+ or -] 2.26      >90 [+ or -] 0
  ethyl acetate            0.21 [+ or -] 0.04     6.25 [+ or -] 0.77
    (Fraction B)
  n-Butanol               16.35 [+ or -] 2.03    77.99 [+ or -] 7.79
    (Fraction C)

(c) Fractions (from
  active ethyl acetate

  Fr 1                    69.06 [+ or -] 5.04      >90 [+ or -] 0.0
  Fr 2                    31.33 [+ or -] 14.77     >90 [+ or -] 0.0
  Fr 3                    68.36 [+ or -] 2.76      >90 [+ or -] 0.0
  Fr 4                    15.94 [+ or -] 4.77    68.48 [+ or -] 12.44
  Fr 5                     6.57 [+ or -] 0.35    54.63 [+ or -] 1.01
  Fr 6                    17.41 [+ or -] 1.59    83.55 [+ or -] 2.14
  Fr 7                    17.08 [+ or -] 1.67    69.64 [+ or -] 0.24
  Fr 8                     6.06 [+ or -] 0.67    54.29 [+ or -] 1.60
  Fr 9                     5.84 [+ or -] 0.47    56.89 [+ or -] 3.15
  Fr 10                    6.38 [+ or -] 0.50    67.91 [+ or -] 10.68
  Fr 11                    2.22 [+ or -] 0.28    46.06 [+ or -] 1.06
  Fr 12                    2.29 [+ or -] 0.08    79.43 [+ or -] 9.53
  Fr 13                    0.76 [+ or -] 0.05    16.88 [+ or -] 2.11
  Fr 14                   44.63 [+ or -] 0.91      >90 [+ or -] 0

(d) Compound 1            0.024 [+ or -] 0.005    1.41 [+ or -] 0.16
  (derived from Fr. 13)

(e) Commonly used
  antitrypanosomal drug

  Melarsoprol              1.61 [+ or -] 0.50     >100
  Pentamidine              0.50 [+ or -] 0.12     >100

Samples                   (a) Selectivity index (SI)

                          L-6/STIB 900

(a) Crude methanol        204.55

(b) Partition extracts

  n-Hexane (Fraction A)   >12.91
  ethyl acetate           29.76
    (Fraction B)
  n-Butanol               4.77
    (Fraction C)

(c) Fractions (from
  active ethyl acetate

  Fr 1                    >1.30
  Fr 2                    >2.87
  Fr 3                    >1.32
  Fr 4                    4.30
  Fr 5                    8.32
  Fr 6                    4.80
  Fr 7                    4.08
  Fr 8                    8.96
  Fr 9                    9.73
  Fr 10                   10.64
  Fr 11                   20.77
  Fr 12                   34.64
  Fr 13                   22.24
  Fr 14                   >2.02

(d) Compound 1            64.5
  (derived from Fr. 13)

(e) Commonly used
  antitrypanosomal drug

  Melarsoprol             >62.11
  Pentamidine             >200

 (a) Selectivity index (SI) trypanosome = [IC.sub.50] cytotoxicity
activity/[IC.sub.50] anti-trypanosomal activity (Otoguro et al. 2011).
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Title Annotation:Short communication
Author:Zahari, Zuriati; Jani, Nor Akmalazura; Amanah, Azimah; Latif, Mohd Naffidi Abdul; Majid, Mohamed Isa
Publication:Phytomedicine: International Journal of Phytotherapy & Phytopharmacology
Article Type:Report
Geographic Code:9MALA
Date:Feb 15, 2014
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