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Introduction
Diabetes is a group of metabolic diseases plants with their various biological constituents
characterized by hyperglycemia resulting from have been used effectively by the communities
defects in insulin secretion or insulin action, or since long time to treat diabetes. Several natural
both [1]. Broad research on diabetes leads to a products such as alkaloids, flavonoids,
number of synthetic oral hypoglycemic agents terpenoids, saponins, polysaccharides and
like biguanides, sulphonylureas and glycosides are isolated from medicinal plants and
thiozolidinediones being used to treat diabetes. are being reported to possess anti-diabetic
But all have side effects associated with their activities [3]. In addition, herbal drugs are
uses [2]. On other hand, traditional medicinal extensively used to treat various diseases due to
doi:10.5138/ijpm.2010.0975.0185.02004
©arjournals.org, All rights reserved.
Dineshkumar et al: International Journal of Phytomedicine 2 (2010) 22-30
their effectiveness, minimal side effects and were grounded into fine powder using a domestic
relatively low cost [4]. Therefore, it is important electric grinder (Product: GX 21, Bajaj
to isolate the lead molecules from traditional anti- appliances, Mumbai, India) and used for
diabetic plants. extraction.
Murraya koenigii (Rutaceae) commonly known
as “Curry Patta” (Hindi) is widely used as a spice
and condiment in India and other tropical
countries. Various parts of Murraya koenigii have
been used in traditional or folk medicine for the
treatment of rheumatism, traumatic injury and
snake bite and it has been reported to have
antioxidant, anti-diabetic and anti-dysenteric
activities [5,6]. Mahanimbine is a carbazole
alkaloid and present in leaves, stem bark and root
of Murraya koenigii. Most of the carbazole
alkaloids have been isolated from
taxanonomically related plants of the genus
Murraya, Glycosmic and Clausena from the Figure 1: Structure of Mahanimbine
family Rutaceae [7]. The Murraya species has
richest source of carbazole alkaloids. Further, Extraction and isolation
Carbazole alkaloids has been reported for their The dried plant powder of Murraya koenigii
various pharmacological activities such as anti- leaves were extracted with petroleum ether (60-
tumor, anti-viral, anti-inflammatory, anti- 80ºC) in a Soxhlet apparatus for 72 h. at room
convulsant, diuretic and anti-oxidant activities temperature. The total extract was concentrated
[8]. Therefore, the present study was undertaken under reduced pressure and kept at room
to evaluate anti-diabetic and anti-hyperlipidemic temperature. A greenish solid (3.6%) was
effects of mahanimbine (carbazole alkaloid) in separated out. This was dissolved in petroleum
streptozotocin-induced diabetic rats. ether (60-80ºC) and chromatographed using silica
gel (60-120 mesh) column and eluted
Materials and methods successively with petroleum ether and chloroform
Plant materials mixture. The fractions obtained with 50%
Murraya koenigii leaves (Rutaceae) were petroleum ether (60-80ºC) in chloroform afforded
collected from the locality of IIT Kharagpur compound-I (mahanimbine). The compound-I
campus, West Bengal, India in the month of was subjected to preparative TLC gave pure
September and October 2007. The leaves were mahanimbine (0.4%).
inspected to be healthy and botanically identified
and authenticated by M. Senthilkumar, Plant General experiments procedure
Biotechnologist, Prathyusha Institute of Melting point was determined in open capillary
Technology and Management, Chennai. The tube in SUNBIM melting point apparatus.
herbarium Murraya koenigii leaves was deposited HPTLC (CAMAG, Switzerland) analysis was
in the Prathyusha Institute of Technology and performed using silica gel 60 F254 TLC plate.
Management (PITAM) against voucher no. Mahanimbine was spotted (10µl) on a silica gel
PITAM/CH/00009/2007. Murraya koenigii 60 F254 (Merck, Darmstadt, Germany) TLC
leaves after collection were dried at room plate. The plate was air dried and then developed
temperature (27-30ºC) for 25-30 days. After using the solvent system petroleum ether and
complete drying (inspection), the dried materials chloroform (7:3) in a CAMAG- twin-trough glass
23
Dineshkumar et al: International Journal of Phytomedicine 2 (2010) 22-30
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Dineshkumar et al: International Journal of Phytomedicine 2 (2010) 22-30
density lipoprotein (VLDL) levels and high- mahanimbine required to inhibit 50% of alpha
density lipoprotein (HDL) level in blood serum amylase activity under the conditions was defined
were measured spectrophotometrically (Semi- as the IC50 value. The experiments were repeated
Autoanalyzer, Microlab 300, Merck) by using thrice with the same protocol. The α-amylase
diagnostic kits and reagents obtained from inhibitory activity was calculated as follows:
Merck, India. The α-amylase inhibitory activity = (Ac+) – (Ac-) –
(As-Ab) / (Ac+) – (Ac-) × 100
Where, Ac+, Ac-, As, Ab are defined as the
absorbance of 100% enzyme activity (only
solvent with enzyme), 0% enzyme activity (only
solvent without enzyme), a test sample (with
enzyme) and a blank (a test sample without
enzyme) respectively.
25
Dineshkumar et al: International Journal of Phytomedicine 2 (2010) 22-30
para-nitrophenol released from pNPG. The assay 104.22, 116.67, 118.40 and 123.98 were due to
was performed in triplicate. The concentration of presence of C1, C12, C11 and C3 respectively. The
mahanimbine required to inhibit 50% of alpha signals at δ 110.39, 117.56, 119.47, 121.90 and
glucosidase activity under the conditions was 124.21 showed presence of C8, C6, C4, C5 and C7
defined as the IC50 value. The experiments were respectively. The signals δ 25.64, 25.87, 40.85,
repeated thrice with same protocol. 119.28 and 131.64 indicated presence of an iso-
prenyl chain attached to one of the gem dimethyl
Statistical analysis of the 2, 2 dimethyl chromene unit. The
All values were expressed mean ± standard remaining tweleve signals unequivocally
deviation. Statistical analysis of in vivo results confirmed the presence of carbazole nucleus.
were performed by one-way analysis of variance ESI-MS (m/z, % intensity): m/z 354 [M-H]-.
(ANOVA) followed by Student’s t-test. P < 0.05 The body weight was slightly increased in
was considered statistically significant. In vitro normal control rats compared to initial body
inhibitory assay statistical difference and linear weight whereas streptozotocin-induced diabetic
regression analysis were performed using rats showed loss of body weight (173.1 ± 0.57g)
Graphpad prism 5 statistical software. after 30 days as compared with initially weight of
diabetic rats (198.3 ± 0.64g). However, body
Results weight of diabetic rats was restored by treating
Mahanimbine was isolated from Murraya with glibenclamide (0.5 mg/kg) and
koenigii leaves. Mahanimbine (Figure 1): white mahanimbine (at a dose of 50 mg/kg and 100
solid, C23H25NO, m.p 87-90ºC. In HPTLC mg/kg, i.p) once a week for 30 days (Table 1).
analysis indicated the retention factor (Rf) values
of mahanimbine was 0.34 (Figure 2). Table 1: Body weights of streptozotocin-
Confirmative test for mahanimbine showed induced diabetic rats after treatment with
purple colour spot (carbazole alkaloid). IR (KBr Mahanimbine
disc): 3440 (N-H), 2920, 1642 (C=C), 1456,
1378, 1312 (C-N), 1211 (C-O), 1164, 741 cm-1 Group Initial body Final body
weight weight
(Figure 3). In 1H NMR (CDCl3): data showed Normal 195.5 ± 0.49 203.8 ± 1.31
presence of aromatic methyl group at δ 2.34, gem control
dimethyl on a double bond at δ 1.58 and 1.66. A Diabetic 198. 3 ± 0.64 173.1 ± 0.57*
tertiary methyl adjacent to oxygen at a sharp control
singlet δ 1.45 and a triplet at δ 5.12 (1H). A 50 mg/kg 194.2 ± 0.63 188.3 ± 0.71*
mahanimbine
multiplet at δ 2.12-2.17 along with gem dimethyl 100 mg/kg 192.1 ± 0.74 186.2 ± 0.69*
signals showed presence of iso-prenyl side chain. mahanimbine
A triplet at δ 1.77 (2H) and two doublets at δ 5.67 0.5 mg/kg of 187.0 ± 0.53 179.1 ± 0.69*
(1H) and 6.67 (1H) along with tertitary methyl glibenclamide
signal, showed presence of a 2, 2 dimethyl
Values are expressed as mean ± S.D. * P <0.05, treated
chromene ring linked by an iso-prenyl side chain.
diabetic groups Vs diabetic control group.
The signals at δ 7.38 (d, 1H), 7.17 (t, 1H), 7.30 (t,
1H) and 7.93 (d, 1H) indicated showed presence Streptozotocin treatment resulted in elevation of
of other ring protons. The signal at 7.89 showed fasting blood glucose, triglycerides, total
due to presence of N-H proton. In 13C NMR cholesterol, low density lipoprotein and very low
(CDCl3): data showed signal at δ16.04 due to density lipoprotein and reduction in high density-
presence of aromatic methyl signal on C3. Signals lipoprotein levels as compared to the normal
at δ 78.19, 128.48, 124.25, 22.78 and 17.57 control rats as noted at end of the study (Table 2).
showed presences of 2, 2 dimethyl chromene When diabetic rats treated with mahanimbine (at
rings on C1 and C2 in carbazole moiety. Signals at
26
Dineshkumar et al: International Journal of Phytomedicine 2 (2010) 22-30
a dose of 50mg/kg and 100 mg/kg, i.p) once a significant (P < 0.05) reduction in triglycerides,
week for 30 days showed significant (P < 0.05) total cholesterol, low density lipoprotein and very
reduction in fasting blood sugar levels (217.0 ± low density lipoprotein levels of diabetic rats
0.61 mg/dl and 198.0 ± 0.84 mg/dl respectively). treated with mahanimbine (50 and 100mg/kg, i.p)
However, the standard drug glibenclamide as comparable to diabetic control. However, there
(0.5mg/kg, i.p) exhibited potent anti-diabetic was a significant (P < 0.05) elevation of HDL
activity with maximum reduction of fasting blood level in mahanimbine (50 and 100mg/kg, i.p)
sugar level (175.4 ± 0.77 mg/dl) on 30 days as treated diabetic rats on 30 days as compared to
compared to the diabetic control. There was a the diabetic control group.
Table 2: Effect of Mahanimbine on FBS, TC, TG, HDL, LDL and VLDL in normal and diabetic rats
for 30 days
Values are expressed as mean ± S.D. n=6/group. Group-I served as normal control. Group-II served as diabetic control. Group
III received 50 mg/kg (i.p) of mahanimbine. Group IV received 100 mg/kg (i.p) of mahanimbine. Group V received 0.5 mg/kg
(i.p) of glibenclamide (positive control). BBP-Biochemical parameters, FBS-fasting blood sugar, TC-total cholesterol, TG-
triglycerides, LDL-low-density lipoprotein, VLDL-very low-density lipoprotein, HDL-high-density lipoprotein. # P <0.05,
Group 1 vs. Group 2. * P <0.05, treated diabetic groups vs. diabetic control group.
Mahanimbine showed appreciable alpha amylase Murraya koenigii leaves) on blood glucose and
inhibitory effects (IC50 value of 83.72 ± serum lipid profiles on streptozotocin-induced
1.4µg/ml) and a weak alpha glucosidase (IC50 diabetic rats. When compared FTIR, ESI-MS, 1H
value of 99.89 ± 1.2µg/ml) as compared with NMR and 13C NMR spectra of isolated
acarbose (IC50 value of 83.33 ± 1.8µg/ml) (Figure mahanimbine with the previously reported
4). mahanimbine showed significant similarity [13,
14].
Discussion Intra-peritoneal administration of 50mg/kg and
The present study was designed to explore the 100 mg/kg of mahanimbine once a week for 30
effect of mahanimbine (carbazole alkaloid from days showed anti-diabetic and hypolipidemic
27
Dineshkumar et al: International Journal of Phytomedicine 2 (2010) 22-30
effects in diabetic rats. Since, lipid abnormalities bark of Murraya koenigii showed antimicrobial
accompanying with atherosclerosis is the major activity [26]. Some of the isolated carbazole
cause of cardiovascular disease in diabetes. alkaloids and their derivative from Murraya
Therefore ideal treatment of diabetes, in addition koenigii leaves showed anti-trichomonal activity
to glycemic control, should have a favorable [27]. Three carbaozole alkaloids (namely,
effect on lipid profiles. High level of TC and Mahanine, Pyrayafoline-D and Murrayafoline –I)
LDL are major coronary risk factors [15]. were isolated from Murraya koenigii leaves and
Further, several studies suggested that TG itself is reported that these alkaloids could be used for
indendently related to coronary heart disease [16, treatment of cancer as chemopreventive agents
17]. The abnormalities in lipid metabolism lead [28]. Murraya koenigii leaves extract showed the
to elevation in the levels of serum lipid and therapeutic protective nature in diabetes by
lipoprotein that in turn play an important role in decreasing oxidative stress and pancreatic beta
occurrence of premature and severe cell damage [29]. Different doses of curry leaves
atherosclerosis, which affects patients with (5, 10 and 15%) were given to normal rats, mild
diabetes [18]. Hence, measurements of and moderate diabetic rats for 7 days. The results
biochemical parameters are necessary to prevent showed that Murraya koenigii could be useful for
cardiac complications in diabetes condition. management of pre-diabetic state or mild diabetes
In the present study, an increase in blood sugar [30]. The carbazole alkaloids (koenimbine and
levels in diabetic rats was observed after the kurryam) were isolated from Murraya koenigii
induction of diabetes by streptozotocin. This was seed and oral administration of 50 mg/kg of
prevented by treating diabetic rats with koenimbine and kurryam exhibited significant
mahanimbine (at a dose 50 and 100 mg/kg, i.p) ant-diarrhoeal effects in castor oil-induced
once in a week for 30 days. The standard drug diarrhoea rats [31].
glibenclamide has been used to treat diabetes, In this study, treatment with mahanimbine (at a
which stimulate insulin secretion from pancreatic dose 50 and 100 mg/kg, i.p) once a week for 30
beta cells, it may be suggested that the days caused significant reduction in fasting blood
mechanism of action of mahanimbine is similar glucose level of diabetic rats. This is an
to glibenclamide. Several alkaloids had been interesting, as the treatment with dose of 50 and
reported to possess similar anti-diabetic effects of 100 mg/kg mahanimbine will not result in
glibenclamide [19-20]. The possible mechanism hypoglycemic shock in diabetic rats. Treatment
by which the mahanimbine decreases blood sugar with mahanimbine (at a dose 50 and 100 mg/kg,
level may be by potentiating of insulin effect i.p) for 30 days significantly reduced total
either by increasing the pancreatic secretion of cholesterol, triglycerides, low density lipoprotein
insulin from beta cells of islets of langerhans or and very low density lipoprotein associated with
by increasing the peripheral glucose uptake. The significant increase in HDL levels in diabetic
mahanimbine (at a dose 50 and 100 mg/kg, i.p) rats. Since HDL is responsible for the
treated diabetic rats showed a significant transportation of cholesterol from peripheral
reduction in both fasting blood sugar levels and tissues to the liver for metabolism. The weight
serum lipid profiles (TC, TG, LDL, and VLDL). loss in diabetic rats may be associated with lipid
There are several studies regarding the biological lowering activity of mahanimbine or due to its
activity of carbazole alkaloids. Many carbazole influence on various lipid regulation systems.
alkaloids such as mukonicine, isomurrayazoline, Hence, treatment with mahanimbine (at a dose
koenoline, isomahanine, murrayanol and 50mg/kg and 100 mg/kg body weight) in diabetic
mahanimbine were isolated from different parts rats has potential role to prevent formation of
(leaves, stem bark, seed) of Murraya Koenigii atherosclerosis and coronary heart disease.
[21-25]. Carbazole alkaloid and Therefore, our in vivo study clearly indicated that
benzoisofuranone derivative isolated from stem intra-peritoneal administration of mahanimbine
28
Dineshkumar et al: International Journal of Phytomedicine 2 (2010) 22-30
(carbazole alkaloid from Murraya koenigii and Management (PITAM), Chennai for his
leaves) at a dose 50 and 100 mg/kg exhibited valuable support in this research work.
anti-diabetic and hypolipidemic effects in
streptozotocin-induced diabetic rats. References
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