Structure and activities of a steroidal saponin from Chlorophytum nimonii (Grah) Dalz

Article abstract of DOI:10.1080/14786410902986597

A new steroidal saponin, chloragin (1), was isolated and characterised from the aerial part of Chlorophytum nimonii. The structure of chloragin (1) was established as tigogenin-3-O-α-L-rhamnopyranosyl-(1 → 4)-β-D-glucopyranosyl-(1 → 3)-β-D-xylopyranosyl-(

Full text of DOI:10.1080/14786410902986597

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Structure and activities of a steroidal
saponin from Chlorophytum nimonii
(Grah) Dalz
Vijai Lakshmi a , Rajesh Kumar a , Kartikey Pandey a ,
Bhawani Shanker Joshi a , Raja Roy a , Kunnath Padamnabham
Madhusudanan a , Priti Tiwari a & Arvind Kumar Srivastava a
a Medicinal and Process Chemistry Division , Central Drug Research
Institute , Chattar Manzil Palace, Lucknow-226001, India
Published online: 29 Oct 2009.
To cite this article: Vijai Lakshmi , Rajesh Kumar , Kartikey Pandey , Bhawani Shanker Joshi ,
Raja Roy , Kunnath Padamnabham Madhusudanan , Priti Tiwari & Arvind Kumar Srivastava
(2009) Structure and activities of a steroidal saponin from Chlorophytum nimonii (Grah)
Dalz, Natural Product Research: Formerly Natural Product Letters, 23:10, 963-972, DOI:
10.1080/14786410902986597
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Natural Product Research
Vol. 23, No. 10, 10 July 2009, 963–972
Structure and activities of a steroidal saponin from Chlorophytum nimonii
(Grah) Dalz
*
Vijai Lakshmi , Rajesh Kumar, Kartikey Pandey, Bhawani Shanker Joshi, Raja Roy,
Kunnath Padamnabham Madhusudanan, Priti Tiwari and Arvind Kumar Srivastava
Medicinal and Process Chemistry Division, Central Drug Research Institute, Chattar Manzil Palace
Lucknow-226001, India
(Received 23 March 2007; final version received 16 August 2007)
A new steroidal saponin, chloragin (1), was isolated and characterised from the
aerial part of Chlorophytum nimonii. The structure of chloragin (1) was
established as tigogenin-3-O-ꢀ-L-rhamnopyranosyl-(1 ! 4)-ꢁ-D-glucopyranosyl-
(1 ! 3)-ꢁ-D-xylopyranosyl-(1 ! 4)-ꢁ-D-glucopyranosyl-(1 ! 4)-ꢁ-D-xyloopyrano-
side on the basis of detailed chemical and spectral evidence. The saponin showed
potent antihyperglycaemic and antidyslipidaemic activities in albino rats.
Keywords: Chlorophytum nimonii; Antheraceae; steroidal saponin (chloragin (1));
antihyperglycaemic and antihyperlipidaemic activities in albino rats
1. Introduction
The genus Chlorophytum (family Antheraceae) consists of at least 200 species distributed
mainly in tropical and subtropical countries (Chopra, Nayar, & Chopra, 1956; Phondke,
1992); about 15 species are found in India, mainly in peninsular India. Most of the
species are herbs with short stalk-fasciled roots, which are often thick, fleshy and
tuberous. As a part of our continuing search for bioactive molecules from natural
sources, this plant exhibited a high order of antihyperglycaemic and antihyperlipidaemic
activities. The literature indicated that no chemical or biological work has been done on
this species; while other species indicated the presence of spiroketal steroidal saponins,
sapogenins, phenolic glycosides and fatty acids (Li, Wang, & Yang, 1990; Mimaki et al.,
1996; Tandon & Shukla, 1992a, 1992b, 1992c, 1993, 1996). In our continued interest in
biologically active saponins, we have undertaken the chemical investigation of
Chlorophytum nimonii, which is a species indigenous to India. The present communi-
cation deals with the isolation and characterisation of a novel spiroketal saponin with
antidyslipidaemic activity from the aerial part of the plant, designated as chloragin (1)
(Figures 1 and 2).
*Corresponding author. Email: vijlakshmius@yahoo.com
ISSN 1478–6419 print/ISSN 1029–2349 online
ß 2009 Taylor & Francis
DOI: 10.1080/14786410902986597
http://www.informaworld.com

964
V. Lakshmi et al.
O
O
H
OH
H
H
O
HO
O
O
OH
O
H
O
O
HO
HO
HO
O
OH
O
HO
O
OH
O
HO
OH
OH
OH
Figure 1. Chemical structure of chloragin (1).
O
H
H
H
C
O
NOESY
HMBC
H
H
OH
H
H
H
H
O
HO
O
O
H
O
H
OH
H
H
O
O
HO
H
OH
O
H
H
O
O
O
OH
O
HO
HO
OH
HO
H
H
OH
OH
H
H
Figure 2. Selected HMBC and NOESY correlations observed in chloragin (1).
2. Material and methods
2.1. Plant material
The aerial part of C. nimonii was collected from Kerala, India, in May 1995 by the botany
division of the Central Drug Research Institute, and a voucher specimen has been
preserved in the Herbarium of the Institute as a Botany Serial No. 6949.
2.2. Extraction and isolation
Air dried and powdered aerial parts (1.0 kg) of the plant were percolated in 80% aqueous
ethanol for 24 h and boiled for 10 h. The aqueous ethanol extract was filtered when it was
hot and was concentrated under reduced pressure to obtain a residue. The crude aqueous
ethanol extract so obtained was fractionated into four fractions by successive maceration
with hexane, chloroform and n-butanol, and were concentrated individually under reduced
pressure. Further, out of these fractions, activity was shown only in the n-butanol soluble
fraction and therefore chemical investigation of only this fraction was done to isolate the
active principle. Repeated chromatography of the n-butanol soluble fraction over a
column of silica gel using eluent CHCl3 : MeOH : H2O (8 : 2 : 0.2 to 7 : 3 : 0.5, v/v) and
HPLC using acetonitrile : water (30 : 70, v/v) gave a saponin designated as chloragin (1)
(200 mg). It was obtained as white crystals in methanol. The other minor constituents
present in the fraction were not purified (Figure 3).

Natural Product Research
965
Air-dried powdered plant (aerial parts, 1.0 kg)
Extracted with 80% aqueous
ethanol,
filtered and concentrated
under reduced pressure
Residual plant
(rejected)
80% ethanol
extract
(25.0 g)
(20.0 g)
Fractionated by maceration with hexane, chloroform
and n-butanol successively and concentrated separately
Hexane fraction
(1.2 g)
Chloroform fraction
(1.8 g)
n-Butanol fraction
n-Butanol insoluble fraction
(10.6 g)
(7.4 g)
Chromatography
and rechromatography
Chloragin (1)
(200 mg)
Figure 3. Extraction, fractionation and isolation.
2.3. Antihyperglycaemic activity in streptozotocin-induced antidiabetic rat model
Male Sprague Dawley strain albino rats of average body weight 140 ꢀ 20 g, having
blood glucose profiles between 60 and 80 mg dLꢁ1, were selected and were made
diabetic by intraperitoneal administration of streptozotocin at a dose level of
45 mg kgꢁ1 body weight. Streptozotocin (Sigma, USA) was dissolved in 100 mM citrate
buffer (pH 4.5), and a calculated amount of freshly prepared solution of streptozotocin
was injected to overnight-fasted rats. Blood glucose profile was again checked after 48 h
by glucostrips (Boehringer Mannheim), and animals showing blood glucose values
between 150 and 450 mg dLꢁ1 were included in the experiments and termed diabetic.
The diabetic animals were divided into groups consisting of five animals in each group.
Rats of experimental groups were administered a suspension of the desired test sample
prepared in 1% gum acacia at 100 mg kgꢁ1 dose level. Animals of control group were
given an equal amount of 1% gum acacia. Blood glucose profile of animals of all
groups was again checked at 1, 2, 3, 4, 5, 6, 7 and 24 h post-administration of test
sample. Animals not found to be diabetic after 48 h post-treatment of the test sample
were not considered, were omitted from the calculations, and termed as non-
responders. Food, but not water, was withheld from the cages during the
experimentation. The percentage of antihyperglycaemic activity was determined by
comparing the AUC of experimental and control groups. Statistical comparison was
made by Dunnett’s test.

966
V. Lakshmi et al.
2.4. Antidyslipidaemic activity in triton model
The antidyslipidaemic activity of chloragin (1) was evaluated in triton-induced
hyperglycaemic rats. However, lipid as well as glucose lowering action of chloragin (1)
was assessed in dyslipidaemic rat model. Male Charles Foster rats weighing 200–225 g
were divided into control, hyperlipidaemic and hyperlipidaemic plus drug-treated groups
containing six animals in each group. Hyperlipidaemia was induced by the administration
of triton WR-1339 [200 mg kgꢁ1, i.p.]. All the animals were maintained on a standard
pellet diet and water ad libitum. Chloragin (1) and standard drug ‘Guggal lipid’ were
macerated with 2% aqueous gum acacia suspension separately. The suspension was fed
orally, the dose of 100 mg kgꢁ1 simultaneously with triton in the drug-treated group. The
animals of the control group received the same amount of gum acacia suspension. At the
end of the experiment, after 18 h, blood was withdrawn from the retro-orbital plexus and
plasma was used for the assay of the total cholesterol (enzymatic determination of blood
cholesterol – by diagnostic code No. 1489232 (CHOD-PAP) supplied by Boehringer
Mannheim GmbH, Germany), phospholipid (Phosphorous-lipid Assay Kit Code No.
124574 supplied by Boehringer Mannheim GmbH, Germany) and triglyceride (Plasma
Triglyceride Assay Kit Engymatic determination code No. 701904, GOP-PAP, supplied by
Boehringer Mannhein GmbH, Germany). The results are tabulated in Table 1.
2.5. Antidyslipidaemic activity in hamster model
Male golden Syrian Hamsters weighing 120–130 g were used and were divided into
dyslipidaemic and dyslipidaemic plus drug-treated groups of eight animals in each group.
Dyslipidaemia was produced by feeding with high-fat diet (HFD) (supplied by NOVO –
NORDISK, Denmark, Cat. No. 99122211). Dyslipidaemic hamsters had free access to
HFD and water ad libitum throughout the experiment for 10 days. The test sample was fed
orally a dose of 250 mg kgꢁ1 from day 4 to day 10 (7 days) in the HFD hamsters. Normal
hamsters fed with HFD and given drug vehicle served as control animals. The body weight
of each animal and diet intake of each animal group was recorded daily to check the effect
of the drug on food intake and body weight of the animals. At the end of the experiment,
Table 1. Antihyperglycaemic effect of extract per fraction and chloragin (1) in streptozotocin-
induced diabetic rats.
% Antihyperglycaemic activity
Sl. No.
Compound
Dose (mg kgꢁ1
)
7 h
24 h
1.
2.
3.
4.
5.
6.
80% Aqueous ethanol extract
Hexane soluble fraction
Chloroform soluble fraction
n-Butanol soluble fraction
Butanol insoluble fraction
Chloragin (1)
250
100
100
100
100
100
100
100
100
16.1**
3.61
3.14
14.8**
4.88
16.7**
12.2*
26.4 **
23.6**
25.6**
5.10
2.41
18.7**
3.53
15.7**
13.9**
35.8***
41.2***
7.
Metformin (positive control)
Glybenclamide (positive control)
Note: Significance: ***p 5 0.001 except marked with asterisk, **p 5 0.01, *p 5 0.05.

Natural Product Research
967
i.e. on the tenth day, the blood of non-fasted animals were withdrawn in two sets of tubes,
in which one set contains 120 mL NaF (4.5 mg mLꢁ1) and after 15 min plasma was
separated in cold. Biochemical analysis of plasma without NaF was performed on the
same day for triglycerides (TG), total cholesterol (TC) and HDL-cholesterol, using
enzymatic diagnostic kits. Similarly, the plasma containing NaF glucose was assayed for
glucose, glycerol and free fatty acids (FFA) on a Synchron CX-5, Clinical System
Beckmann Coulter Instrument. The data was analysed for its significance on Prism
Software.
1
Chloragin (1): Melting point: 250ꢂC (dec) and ½ꢀꢃD ꢁ38.89 (MeOH, c 0.052), H and 13C
NMR (DMSO-d6), see Tables 2 and 3. Positive FABMS showed molecular ion at m/z 1173
[M þ Na]þ, 1041 [M þ Na-132]þ, 879 [M þ Na-132-162]þ, 747 [M þ Na-2 ꢄ 132-162]þ, 585
[M þ Na-2 ꢄ 132-2 ꢄ 162]þ and 438 [M þ Na-2 ꢄ 132-162-147]þ.
26
Table 2. 1H and 13C data of the sugar moieties of chloragin (1).
ꢂH multiplicityb
(J values in Hz)
Carbons per sugar unit
ꢂca
Rh-1
-2
99.9
70.6
70.6
80.2
68.1
17.7
5.12 d (3.6)
3.66 m
3.39 dd (8.8, 3.0)
3.18 dd (8.8, 3.0)
3.95 dq (9.6, 6.2)
1.70 d (6.2)
-3
-4
-5
-6
Glc-1
-2
104.0
71.4
85.7
69.0
75.8
59.9
4.60 d (7.8)
3.31 dd (7.6, 8.3)
3.60 dd (8.3, 9.0)
3.09 m
3.22 m
3.71 m, 3.35 m
-3
-4
-5
-6
Xyl-1
-2
103.5
69.5
70.6
74.4
63.9
4.48 d (7.9)
3.03 dd (7.9, 9.1)
3.11 m
3.49 m
3.09 dd (11.0, 5.4)
3.76 dd (11.0, 11.1)
-3
-4
-5
Glc-1
-2
98.4
72.6
73.5
79.5
75.8
61.5
4.29 d (7.6)
3.31 dd (7.6, 8.5)
3.33 m
3.76 m
3.34 m
3.70 m, 3.34 m
-3
-4
-5
-6
Xyl-1
-2
103.6
73.5
76.6
74.4
63.9
4.36 d (7.4)
3.03 dd (7.4, 9.2)
3.39 m
3.50 m
3.90 dd (11.2, 5.6)
3.40 dd (11.2, 11.1)
-3
-4
-5
a
Notes: Recorded at 75.0 MHz in DMSO-d6; multiplicity by DEPT experiments.
bRecorded at 300 MHz in DMSO-d6.

968
V. Lakshmi et al.
Table 3. 1H and 13C NMR for aglycon moiety of chloragin (1).
ꢂH multiplicityb
(J values in Hz)
Carbon Nos.
ꢂca
C-1
C-2
C-3
C-4
C-5
C-6
C-7
C-8
36.6
29.4
76.6
33.3
44.0
29.1
31.9
34.7
53.8
35.4
20.7
39.6
40.3
55.7
31.8
80.4
61.8
16.0
12.0
41.6
14.5
109.0
30.8
28.9
30.6
65.9
0.88 m; 1.25 m
1.65 m; 1.81 m
3.89 m
1.62 m; 1.89 m
0.90 m
1.20 m; 0.88 m
1.65 m; 8.85 m
0.85 m
C-9
1.01 m
C-10
C-11
C-12
C-13
C-14
C-15
C-16
C-17
C-18
C-19
C-20
C-21
C-22
C-23
C-24
C-25
C-26
–
1.28 m
1.35 m
–
2.00 m
1.58 m; 2.05 m
4.38 m
2.26 m
0.86 s
0.82 s
2.24 m
1.14 d 6.7
–
1.28 m; 1.60 m
1.58 m; 1.62 m
1.56 m
3.51 dd (10.2, 10.3)
3.62 dd (10.3, 3.2)
0.70 d (6.1)
C-27
17.2
Notes: aRecorded at 75.0 MHz in DMSO-d6. bRecorded at 300 MHz in
DMSO-d6.
2.6. Acid hydrolysis of chloragin (1)
A solution of chloragin (1) (50 mg) in H2O (1.0 mL) and 2N aqueous HCl (5 mL) was
refluxed at 100ꢂC for 2 h. The reaction mixture was diluted with water (10 mL) and
extracted with CH2Cl2 (3 ꢄ 10 mL). The combined CH2Cl2 extract was washed with
water, dried over anhydrous sodium sulphate and concentrated under reduced pressure
to afford the aglycon. It was identified as tigogenin by comparing spectral data with
those reported in the literature (Agarwal, Jain, Gupta, & Thakur, 1985) and co-TLC
with the authentic sample. The aqueous layer was evaporated under reduced pressure to
complete dryness. It was dissolved in 2 mL of pyridine and 10 mg of NH4OH ꢅ HCl was
added, heated at 100ꢂC for 1h, cooled and 5 mL of acetic anhydride was added, then
again refluxed at 100ꢂC for 2 h. The reaction mixture was worked-up as usual and the
resulting aldonitrile per acetate was analysed by GC-MS using standard aldonitrile
peracetate as standard reference samples. Xylose, rhamnose and glucose were identified
in chloragin (1) in the ratio of 2 : 1 : 2.

Natural Product Research
969
3. Results and discussion
Chloragin (1) showed a molecular ion peak at m/z 1173 [M þ Na]þ corresponding to the
molecular formula C55H90O25 in its FABMS. It showed the losses of one pentostyl, one
pentosyl plus one hexosyl, two pentosyl plus one hexosyl and two pentosyl plus one
hexosyl plus one methyl pentosyl moieties. The fragment ion at m/z 438 [M þ Na]þ
corresponded to the molecular ion of the aglycone (tigogenin). The proton NMR spectrum
of the compound in DMSO-d6 showed signals for four steroidal methyls, two of them as
tertiary methyls showing signals at ꢂ 0.82 and 0.86 (3H each, s), and rest of the secondary
methyls at ꢂ 0.70 (3H, d, J, 6.1 Hz) and 1.14 (3H, d, J, 6.7 Hz) along with methyl pentose
1
secondary methyl at ꢂ 1.70 (3H, d, J, 6.2 Hz). Further, H NMR spectrum displayed five
anomeric protons at ꢂ 5.12, 4.60, 4.48, 4.36 and 4.29, respectively. This corresponded with
13C NMR cross peaks, which were observed at ꢂ 99.9, 104.0, 103.5, 103.6 and 98.4,
respectively, in the HMQC spectrum, confirming that chloragin (1) contains five sugar
units. Acid hydrolysis of 1 with 2N HCl in 80% aqueous ethanol at 100ꢂC for 2 h afforded
D-glucose, L-rhamnose and D-xylose in the ratio of 2 : 1 : 2, and the aglycone was identified
as tigogenin by comparing spectral data with those given in the literature (Agarwal et al.,
1985) and the co-TLC with an authentic sample. The proton and carbon assignment of
each sugar unit was unambiguously assigned, starting by the combined use of COSY,
TOCSY and NOESY, NMR spectra (Table 3), which was further confirmed by HMQC
and HMBC NMR spectra. The sequences of the sugar chains were determined by HMBC
and NOESY spectra. Cross peak correlations observed in the HMBC spectrum between
signals at ꢂH 5.12 and ꢂc 76.6 (aglycone-3) showed that the L-rhamnosyl moiety is linked at
C-3 of the aglycon (tigogenin). This was confirmed by the NOESY correlation observed
between signals at ꢂ 5.12 (1H, d, J 7.1 Hz) and ꢂH 3.89 (aglycon-3). The glucosyl-1 H-1 at ꢂ
4.60 and rhamnosyl C-4 at ꢂ 75.9, xylosyl-1 at ꢂ 4.48 and glucosyl-1 C-3 at ꢂ 85.7; glucosyl-
2 H-1 at ꢂ 4.29 and xylosyl-1 C-4 at ꢂ 75.9 and xylosyl-2, H-1 at ꢂ 4.36 and glucosyl-2,
C-4 at 79.5 correlated in the HMBC spectrum confirmed that the structure of chloragin (1)
is tigogenin-3-O-ꢀ-L-rhamnopyranosyl-(1 ! 4)-ꢁ-D-glucopyranosyl-(1 ! 3)-ꢁ-D-xylopy-
ranosyl-(1 ! 4)-ꢁ-D-glucopyranosyl-(1 ! 4)-ꢁ-D-xylopyranoside.
3.1. Antihyperglycaemic activity
The crude extract showed promising antihyperglycaemic activity in the streptozotocin-
induced diabetic rat model on further fractionation of the crude extract into four fractions;
the activity was found to be localised in only the n-butanol soluble fraction. Therefore,
only the n-butanol soluble fraction was taken up for detail chemical investigations. The
major pure compound chloragin (1) was isolated and characterised, which is a new
structure and also showed promising antihyperglycaemic effect in the streptozotocin-
induced diabetic rat model. The results are summarised in Table 1.
3.2. Antihyperlipidaemic activity
The antihyperlipidaemic activity of chloragin (1) in triton and hamster models was
evaluated. The results are summarised in Tables 4–6. Values expressed as mg dLꢁ1 are
the mean ꢀ SD of six hamsters. Values in parentheses are percentage change as
compared to HFD group. Data in Table 4 showed that administration of triton

970
V. Lakshmi et al.
Table 4. Hypolipidaemic effect of chloragin (1) in triton-treated rats.
Treatment (Dose mg kgꢁ1
)
Total cholesterol
Phospholipid
Triglyceride
Control
Triton
87.5 ꢀ 13
76.8 ꢀ 14
90.0 ꢀ 13
466.9 ꢀ 90
318.5 ꢀ 21
268.0 ꢀ 20
Triton þ chloragin (1) (100 mg kgꢁ1
)
345.7 ꢀ 27* (26)
239.9 ꢀ 40* (25)
208.5 ꢀ 31* (22)
Triton þ guggul lipid (100 mg kgꢁ1
)
307.9 ꢀ 88 (34)
201.8 ꢀ 32 (37)
177.5 ꢀ 29 (34)
Notes: Values expressed as mg dLꢁ1 are the mean ꢀ SD of six rats. Values in the parentheses are
percent decrease in triton and drug-treated group compared to triton-treated group.
Significance: p 5 0.001 except marked with asterisk *p 5 0.01.
Table 5. Effect of chloragin (1) on plasma lipid profiles of dyslipidaemic hamsters.
Treatment
Total cholesterol
Triglycerides
Glucose
Control
HFD
126.4 ꢀ 12
64.6 ꢀ 4
86.0 ꢀ 12
112.5 ꢀ 12
96.5 ꢀ 10 (14)
109.2 ꢀ 16
310.1 ꢀ 8
278.7 ꢀ 3
HFD þ chloragin (1) (345 mg kgꢁ1
)
237.7 ꢀ 7 (23)
220.6 ꢀ 5 (5)
HFD þ guggul lipid (250 mg kgꢁ1
)
218.5 ꢀ 5 (30)
204.5 ꢀ 5 (27)
Notes: Values expressed as mg dLꢁ1 are the mean ꢀ SD of six hamsters. Values in parentheses are the
percent decrease from compound to HFD group.
WR-1337 in rats caused increase in their plasma Tc, PL and Tg levels by 5.33, 4.14
and 2.91 folds, respectively. Treatment with chloragin (1) caused significant lowering
in plasma lipid levels of triton plus drug-treated group; however, these effects were of
lower order than guggul lipid. Feeding hamsters with HFD caused dyslipidaemia,
which was reflected in increased levels of plasma Tc (2.45 fold), Tg (4.3 fold) and
glucose (30%), respectively. Treatment with chloragin (1) caused lowering in plasma
levels of Tc, Tg and glucose by 23, 21 and 14%, respectively. At the same time the
standard lipid lowering drug; guggul lipid exerted more lipid lowering action but did
not effect the increased level of glucose in dyslipidaemic hamsters (Table 5).
Investigations on the effect of chloragin (1) were also made on the dyslipidaemia
induced in hamster fed with HFD-D-99122211 supplied by Novo-Nordisk, Denmark.
Feeding with HFD caused marked increase in the level of blood glucose. Feeding of
HFD D-9912211 to hamsters caused marked increase in plasma Tg, Tc and FFA
levels by 3.7, 4.3 and 3.1 folds, respectively, accompanied by increase in HDL, glucose
and glycerol by 25, 30 and 31%, respectively. Treatment with chloragin (1) at a dose
of 345 mg kgꢁ1 p.o.ꢁ1 significantly reversed the plasma levels of Tg, Tc, glu, glycerol
and FFA by 52, 63, 42, 30 and 33%, respectively, in dyslipidaemic plus drug-treated
animals without causing any adverse effect on plasma HDL (Table 6). In conclusion,
chloragin (1) has potent antidyslipidaemic activity together with the activity in
validated animal models. This compound also has favourable effects on HDL-
cholesterol levels in animals.

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V. Lakshmi et al.
Acknowledgement
The authors are grateful to the Director Central Drug Research Institute, Lucknow, India for
providing necessary research facilities to carry out this work.
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steroidal sapogenins and saponins. Phytochemistry, 24, 2479–2496.
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