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Antidiabetic potential of mangrove plants: areview

Swagat Kumar Das, Dibyajyoti Samantaray, Jayanta Kumar Patra, LunaSamanta & Hrudayanath Thatoi

To cite this article: Swagat Kumar Das, Dibyajyoti Samantaray, Jayanta Kumar Patra, LunaSamanta & Hrudayanath Thatoi (2016) Antidiabetic potential of mangrove plants: a review,

Frontiers in Life Science, 9:1, 75-88, DOI: 10.1080/21553769.2015.1091386

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Frontiers in Life Science , 2016Vol. 9, No. 1, 7588, http: // dx.doi.org / 10.1080 / 21553769.2015.1091386

Antidiabetic potential of mangrove plants: a review

Swagat Kumar Dasa, Dibyajyoti Samantaray

a, Jayanta Kumar Patra

b, Luna Samanta

cand Hrudayanath Thato i

d

a Department of Biotechnology, College of Engineering and Technology, Biju Patnaik University of Technology, Bhubaneswar 751003,Odisha, India; b School of Biotechnology, Yeungnam University, Gyeongsan 712749, Republic of Korea; c Department of Zoology,

Ravenshaw University, Cuttack 753003, Odisha, India; d Department of Biotechnology, North Orissa University, Baripada 757003,Odisha, India

( Received 7 May 2015; accepted 3 September 2015 )

Diabetes mellitus is a heterogeneous group of metabolic disorders characterized by persistent hyperglycaemia and becominga serious threat to mankind health in all parts of the world. Production of reactive oxygen species and disturbed capacityof antioxidant defence have been reported for enhanced production of free radicals in diabetic subjects. As oxidative stressis found to be a central event in the development of diabetic complications, hence antioxidants may play an importantrole in the improvement of diabetes and its associated complications. Currently there has been an increased interest glob-ally to identify antioxidant compounds that are pharmacologically potent and have low or no side effects. Phytochemicalsand metabolites from mangrove plants are reported to exhibit strong antioxidant properties in terms of both enzymatic and

non-enzymatic activities. Recent researches have also revealed that a number of mangrove plants have shown antidiabeticactivities attributed to their unique metabolites such as avonoids, triterpenoids, limonoids and polysaccharides. Thus, man-grove plants can be of great use in tackling diabetic and its associated oxidative stress mediated complications. The presentreview highlights a relation between oxidative stress and diabetes and the role of mangrove plants in alleviating diabetes, ingeneral, and oxidative stress mediated diabetic complications, in particular.

Keywords: mangroves; antidiabetic; antioxidant; oxidative stress

1. Introduction

Diabetes is a chronic metabolic disorder characterized byabsolute or relative deciencies in insulin secretion or insulin action associated with chronic hyperglycaemia and disturbances of carbohydrate, lipid and protein metabolism

(Bastaki 2005 ). There are three types of diabetes melli-tus recognized by the World Health Organization (WHO)such as (i) type 1 diabetes (insulin-dependent) (ii) type2 diabetes (non-insulin-dependent) and (iii) gestationaldiabetes. The -cells in the pancreas are the key play-ers in glycaemic homeostasis. Glucotoxicity, lipotoxicity,inammatory mediators and incretin were reported to mod-ulate function and survival of -cell (Leahy et al. 2010 ).Besides, oxidative stress is thought to be a major risk factor on the onset and progression of diabetes (Rains &Jain 2011 ). Both type-1 and type-2 diabetes are associated with increased formation of free radicals and decreased antioxidant potential (Maritim et al. 2003 ).

Diabetes is a common disease in the developed and developing countries. According to a WHO report in2011, approximately 360 million people globally suffer from diabetes. Diabetes epidemic is more pronounced indeveloping countries such as India. As per reports of theWHO, 32 million people of India had diabetes in the

*Corresponding author. Email: [email protected]

year 2002 and it is expected that more people in Indiawill be affected by diabetes in the near future. Therefore,management of diabetes in recent times possesses a bigchallenge. Apart from insulin, several types of glucose-lowering drugs (including insulin secretagogues, insulin

sensitizers, -glucosidase inhibitors, peptide analogues, di- peptidyl peptidase-4 inhibitors and glucagon like peptide-1) have been developed. However, these synthetic oralhypoglycaemic agents have characteristic proles of seri-ous side effects, which include hypoglycaemia, weightgain, gastrointestinal discomfort, nausea, diarrhoea, liver,heart failure, etc. (Joshi & Joshi 2009 ). Thus, alternativetherapy is the need of hour.

Since centuries, many plants are considered to be a richsource of potent antidiabetic drugs and these herbal prepa-rations are considered to be devoid of any side effects. Ithas been estimated that more than 400 plants and their secondary metabolites such as glycosides, alkaloids, terpenoids, avonoids, carotenoids, tannins and polyphenolicderivatives are being used for the management of diabetesmellitus across the globe (Bailey & Day 1989 ). Currentlythere has been an increased interest globally to identifyantioxidant compounds that are pharmacologically potentand have low side effects for use in antidiabetic therapy.

2015 Taylor & Francis
http://-/?-mailto:[email protected]:[email protected]://-/?-


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76 S.K. Das et al.

The mangroves (unique plant communities growing atthe interface between the land and sea in tropical and sub-tropical regions of the world) are capable of thriving under stress conditions exemplied by high salinity, extremetides, strong winds, high temperatures and muddy anaer-obic soils (Kathiresan & Ramanathan 1997 ). They havehighly developed morphological and physiological adap-tations to the extreme conditions of their environment and possess metabolites of unique biological activity that arerich in medicinal potential. Traditionally, mangrove plantsare being used in folklore medicine for treatment of var-ious ailments including diabetes (Bandaranayake 2002 ).However, the antidiabetic potentials of these plants and itscorrelation with antioxidant potential are yet to be estab-lished. Hence, the present review highlights a relation between oxidative stress and diabetes and the potential

role of mangrove plants in management of diabetes and itsoxidative-stress-associated complications.

2. Pathological pathways involved in diabetes

There are four key metabolic pathways playing major role in hyperglycaemia-induced cell damage and diabetesassociated complications such as (a) increased polyol path-way ux; (b) increased advanced glycation end prod-uct (AGE) formation; (c) activation of protein kinaseC and (d) increased hexosamine pathway ux (Robert-son 2004 ) (Figure 1). In diabetes, cell damages aremanifested through damage to proteins, lipids and carbohydrates, while the diabetic-associated complicationsinclude diabetic nephropathy, retinopathy, neuropathy,etc.

Figure 1. Hyperglycaemia-induced reactive oxygen species (ROS) generation and diabetic-associated pathological complications. :Stimulate. : Inhibit.


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Frontiers in Life Science 77

3. Inuence of oxidative stress on insulin signalling

The normal insulin signalling pathway (which is a tightlyregulated process) is found to be impaired during oxidativestress conditions, resulting in development of insulin resis-tance (Evans et al. 2002 ). Several mechanisms have been proposed for the causal link between oxidative stress and

impairment of insulin signalling pathways, which include(i) activation of stress kinases, (ii) decreasing GLUT-4gene transcription, (iii) alteration in mitochondrial activityand (iv) free fatty acids (FFA) mediated apoptosis.

Studies have shown that oxidative stress can activate anumber of stress kinases along with activation of stress sig-nalling pathways such as NF- . The NF- pathway isactivated by phosphorylation of a serine kinase IkB kinasewhich has shown a negative effect on normal insulin sig-nalling pathway. The activation of other stress signalling pathways such as p38, MAPK and JNK/SAPK also inter-fere in the insulin signalling by dephosphorylating the IRS,leading to deactivation of signalling cascades resulting in

insulin resistance (Baldwin 2001 ; Ogihara et al. 2004 )(Figure 2).

The facilitated diffusion of glucose into the cell is medi-ated by a number of glucose transporters, of which theGLUT1 and GLUT4 play an important role in insulinsignalling. The oxidative stress has been shown to down-regulate the expression of GLUT4, which in turn decreases

Figure 2. Effects of oxidative stress on the insulin signalling pathway. : Stimulate. : Inhibit.

Figure 3. Proposed pathway linking FFA and hyperglycaemiain the pathogenesis of diabetes. : Stimulate. : Inhibit.

the glucose uptake, resulting in development of insulin

resistance (Bloch-Damti & Bashan 2005 ).Mitochondria also play an important role in the releaseof insulin from -cells in response to blood glucose lev-els (Rains & Jain 2011 ). The mitochondrial dysfunction byoxidative stress is reported to be involved in insulin resis-tance and may be an underlying cause in the developmentof diabetes (Szendroedi et al. 2009 ).

The hyperglycaemia and FFA also elevate ROS and reactive nitrogen species production levels and activatestress signalling pathways causing -cell dysfunction and insulin resistance (Evans et al. 2003 ) (Figure 3).

4. Antidiabetic potential of phytochemicals; amangrove plant perspective

Metabolites with some novel chemical structures and diversied chemical classes have been characterized inmangroves and mangal associates. Aliphatic alcohols,acids, amino acids, alkaloids, carbohydrates, carotenoids,hydrocarbons, FFA (including polyunsaturated fattyacids), lipids, pheromones, phorbol esters, steroids, triterpenes and their glycosides, tannins, terpenes, phenolics and related compounds are among these classes that have estab-lished pharmacological bioactivity (Bandaranayake 2002 ).


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Table 1. Major phytoconstituents of mangrove plants exhibiting hypoglycaemic activities.

Class of compound

Hypoglycaemicactivity

Mangrovespecies

Major phytoconstituents References

Alkaloids Inhibit alpha-glucosidase Glucose transport

through the intestinal

epithelium.

Bruguiera sp., X. granatum

Brugine, tropine and tropineesters of acetic, iosbutyric, ios-valeric, propionic, n-butyric,

4-hydroxybenzoic acid, ethyl3,4-dihydroxybenzoate

Cheng et al.(2009 )

Polysaccharides Levels of serum insulin Blood glucose levels Improve tolerance of glu-

cose

S. alba Complex polysaccharide Morada et al.(2011 )

Flavonoids Suppressed the glucoselevel

Plasma cholesterol and triglycerides signicantly

Hepatic glucokinaseactivity

A. ilicifolius, Bruguierasp., X. granatum

Rutin, quercetin, kaempferol,catechin, epicatechin

Li et al. ( 2009 )

Saponins Stimulates the release of insulin

B. gymnor-rhiza,B. sexangula

-Sitosterol, -amyrin, ursolicacid, -amyrin, stigmasterol

Nebula et al.(2013 )

Phenoliccompounds

The levels of seruminsulin,

The sensitivity of tissuesto insulin action

B. racemosa, Rhizophorasp.

Methyl 3,4,5-trihydroxy benzoate; 3 ,4,5-trimethoxy phenol 1- O- -D-(6-galloyl)-glucopyranoside, gallicacid

Kabir et al.(2013 ) and Liet al. (2009 )

The phytochemicals from mangrove plants with potentialhypoglycaemic activity are summarized in Table 1.

4.1. Alkaloids

Alkaloids produce antihyperglycaemic action by potenti-ating pancreatic secretion of insulin from -cell of islets

or by enhancing transport of blood glucose to peripheraltissue (Gulfraz et al. 2011 ). Alkaloids such as xylograna-tinin, granatoin, acanthicifoline and trigonellin are reported in mangrove plants such as Xylocarpus granatum and Acanthus sp. (Li et al. 2009 ).

4.2. Polysaccharides

The antihyperglycaemic effect of polysaccharides is due tothe increased level of serum insulin, reduced blood glu-cose level and enhanced tolerance to glucose (Bhushanet al. 2010 ). Morada et al. (2011 ) have also reported thatthe hypoglycaemic property in mangrove plant Sonneratia

alba is due to the presence of a complex polysaccharidemolecule.

4.3. Flavonoids

Flavonoids might prove to be important for alternativediabetic treatment, as it helps in preventing -cell apop-tosis, promoting -cell proliferation and insulin secretion,and enhancing insulin activity. Mangrove plants such as Avicennia marina , X. granatum and Bruguiera sexangulaare reported to be rich in avonoids (such as quercetin,

kaempferol, catechin, epicatechin and rutin) that exhibithypoglycaemic activities (Cheng et al. 2009 ; Zhu et al.2009 ; Nebula et al. 2013).

4.4. Saponins: triterpenoid and steroidal glycosides

Triterpenoid and steroidal glycosides are collectively

referred to as saponins. These compounds are known to possess potent hypoglycaemic activity (Rao & Gurnkel2000 ). Mahera et al. (2013 ) reported that the presenceof stigmasterol-3- O- -D-galactopyranoside and -amyrinin mangrove plant of A. marina is responsible for itsantidiabetic activity. Similarly, bartogenic acid in another mangrove plant Barringtonia racemosa was also found to possess -glucosidase inhibition activity (Gowri et al.2007 ). Pentacyclictriterpenoids such as oleanolic acid,ursolic acid and lupeol found in mangrove plants suchas A. marina and Sonneratia caseolaris also exhibited antidiabetic activities (Tiwari et al. 2010 ; Mahera et al.2013 ).

4.5. Phenolic compounds

The phenolic compounds may exhibit their hypoglycaemicactivities by increasing the levels of serum insulin, increas-ing the sensitivity of tissues to insulin action, stimulatingthe activity of enzymes of glucose utilization and inhibit-ing the activity of -amylase (Arif et al. 2014 ). Mangrove plants such as B. racemosa possess phenolic compound (such as gallic acid) that have antidiabetic activities (Kabir et al. 2013 ).


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Figure 4. Possible role of mangrove plants in the management of diabetes and its associated oxidative-stress-mediated complications. : Stimulate. : Inhibit.

4.6. Tannins

Tannins also play an important role in preventing diabeticcomplications by reducing the formation of AGEs and oxidative stress (Soman et al. 2013 ). Members of the fam-ilies Avicenniaceae, Rhizophoraceae and Sonneratiaceaeare rich source of tannins (Bandaranayake 1995). Man-groves such as Xylocarpus moluccensis are reported to richin non-hydrolysable tannins such as procyanidindecamer and procyanidinundecamer (Wangensteen et al. 2009 ).

4.7. Other compounds

Some macyrocylic polydisulde such as gymnorrhizolfrom mangrove plant Bruguiera gymnorrhiza and poly-acetylenes from Aegiceras corniculatum are also reported to possess antidiabetic activity (Sun & Guo 2004 ; Wanget al. 2006 ).

5. Progress of antidiabetic research in mangroveplants

Mangrove plants living in an ecological hostile condi-tion enumerated by different stress conditions such as

salinity, high temperature, water logging, low oxygen and light are reported to be rich in antioxidant compounds.These compounds include phytochemicals such as cin-namic acids, coumarins, diterpenes, avonoids, lignans,monoterpenes, phenylpropanoids, tannins and triterpenes(Bandaranayake 2002 ; Thatoi et al. 2014). The searchfor antidiabetic phytoconstituents from mangrove plantshaving enriched antioxidant property has taken a pacein recent times. Traditionally more than 100 numbers of mangroves and mangrove-associated plant used for treat-ment of diabetes have been reported; however, only afew have been evaluated and reported scientically (Ban-daranayake 2002 ). Based upon the antidiabetic researchcarried upon mangrove plants, it has been suggested thatthese plants can exhibit their antidiabetic action by severalways such as (i) insulin mimetic activity, (ii) decreas-ing intestinal glucose absorption, (iii) decreasing AGEsand (iv) by exerting antioxidative effect (thereby decreas-ing oxidative-stress-associated diabetic complications(Figure 4).

Some of the important mangrove plants along withtheir phytoconstituents (Figure 5) and mode of antidiabeticaction are summarized in Table 2.


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80 S.K. Das et al.

Figure 5. Hypoglycaemic compounds from mangrove plants.

5.1. A. corniculatum

A. corniculatum L. (black mangrove) belongs to the fam-ily Myrsinaceae. The different parts of the plant have beentraditionally used for treatment of rheumatism, arthritis,inammation, antioxidant, free radical scavenging and

hepatoprotective action (Roome et al. 2008). Ethanolicextract of A. corniculatum leaves regulate blood glucoselevel in alloxan-induced diabetic rats at a dose of 100mg/kg. Improvement in body weight in diabetic-induced rat was observed along with decrease in the activities


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Table 2. Mangrove plants with reported antioxidant and antidiabetic activities.

Mangrovespecies Family Phytoconstituents

Antioxidantactivities

studied (A)Antidiabetic

mechanism (D) References

A. corniculatum Myrsinaceae Flavonoids, tannins,saponins,

Phenolic content;reducing ability

Utilization of glucose;either by direct

stimulation of glucoseuptake or via themediation of enhanced insulin secretion;

(A) Roome et al.(2008 );

polyphenols (D) Gurudeeban et al.(2012 )

Elevated glucoseand glycosylated haemoglobin levels.

A. ilicifolius Acanthaceae Flavonoids OH radical,DPPH, ABTSscavenging

Regeneration of -cells of pancreas

(A) Firdaus et al.(2013 )

(D) Venkataiah et al.(2013 )

A. marina Avicenniaceae Saponins Catalase Stimulation of -cells torelease more insulin

(A) Takemura et al.(2002 )

Antiglycation activity (D) Babuselvam et al.(2013 );

Mahera et al. (2011 ) B. cylindrica Rhizophoraceae avonoids, phenolicacids, sterols/triterpenoid,alkaloids, tanninsanthocyanins

OH radical,DPPH, ABTSscavenging

Stimulation of -cells torelease more insulin

(A) Krishnamoorthyet al. (2011 )

(D) Shyam and Kadalmani ( 2014 )

B. racemosa Lecythidaceae Flavonoids, tannins,saponins

DPPH scavenging,superoxidescavenging,FRAP

-Glucosidase and -amylase inhibitory property

(A) Kong et al. ( 2012 )(D) Gowri et al. ( 2007 )

B. gymnorrhiza Rhizosphoraeae Flavonoids, tan-nins, saponins, polyphenols,glycosides

SOD, DPPH,ABTS,scavenging

Presence of antidiabetic principles

(A) Agoramoorthyet al. ( 2008 )

(D) Karimulla and Kumar (2011 )

C. decandra Rhizosphoraeae Flavonoids, tan-nins, saponins, polyphenols,glycosides

DPPH radicalscavenging Stimulation -cells torelease more insulin;The increased hexokinase

activity may result inincreased glycolysisand increased utilizationof glucose for energy production.

(A) Agoramoorthyet al. (2008 )(D) Nabeel et al.

(2010 )

C. tagal Rhizosphoraeae Flavonoids, tannins,saponins, polyphe-nols, glycosides,terpenoids

DPPH scavenging,anti-lipid peroxidation

Inhibition against PTPaseenzyme activity, which plays an importantrole in the negativeregulation of the insulinsignalling pathway;

Stimulation of glucoseuptake; -Glucosidaseinhibitory property

(A) Bunyapraphatsaraet al. (2003 )

(D) Tiwari et al.(2008 ); Tamrakar et al. ( 2008 ); Lawaget al. (2012 )

E. agallocha Euphorbiaceae Flavonoids, tan-nins, saponins, polyphenols phorbol

DPPH radicalscavenging,reducing power, H 2O2scavengingassay, nitricoxide (NO)

Pancreatic secretion of insulin; Uptake of glucose.

(A) Patra et al. (2009 )(D) Rahman et al.

(2010 ); Thiru-murugan et al.(2009 )

(Continued ).


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82 S.K. Das et al.

Table 2. Continued

Mangrovespecies Family Phytoconstituents

Antioxidantactivities

studied (A)Antidiabetic

mechanism (D) References

H. fomes Sterculiaceae Tanins, terpenoids, DPPH radicalscavenging

assay and 1,5-lipoxygenaseinhibiting activities

Enhancement of pancreatic secretion of

insulin; The glucose uptake;Inhibition in glucose

absorption in gut

(A) Wangensteen,Dang et al. ( 2009 )

(D) Ali et al. ( 2011 )

avonoids

R. mucronata Rhizosphoraeae Alkaloids, tannins,saponins, phenolic

compunds

SOD, LPO, NO and DPPH assays

Improved level of insulinsecretion and its action;

Insulin mimetic activity; -Glucosidase inhibitory

Banerjee et al. ( 2008 );Agoramoorthyet al. (2008 );Bunyapraphatsaraet al. (2003 )

(D) Lawag et al.(2012 ); Nabeel et al.(2012 ); Gaffar et al.(2011 ); Haque et al.(2013 )

R. apiculata Rhizosphoraeae Tannin, steroids,

triterpenes, phenoliccompounds

SOD, LPO, NO,

reducing power,superoxide, OH . and DPPH assays

Improved level of insulin

secretion and its action;Insulin mimetic activity -Cell protection

(A) Agoramoorthy

et al. (2008 ); Sur et al. (2015 )(D) Lakshmi et al.

(2006 ); Sur et al.(2004 ), (2015 ); Nabeel et al. ( 2012 )

R. annamalayana Rhizosphoraeae Alkaloids, tanins,steroids

DPPH scaveng-ing, anti-lipid peroxidation

Improved level of insulinsecretion and its action ;

Insulin mimetic activity


(D) Ali et al. ( 2011 ); Nabeel et al. ( 2012 )

N. fruticans Arecaceaea Alkaloids, glycosides,tannins, sterols

Free radicalscavenging

Utilization of glucose,either by directstimulation of glucoseuptake or via themediation of enhanced

insulin secretion

(A) Prasad et al. (2013 )(D) Reza et al. (2011 )

S. caseolaris Lythraceae Steroids, glycosides DPPH scaveng-ing, anti-lipid peroxidation

Intestinal -glucosidaseinhibitory activity;

Potentiation pancreaticsecretion of insulin;

Glucose uptake fromserum;

Glucose absorptionfrom gut.

(A) Kaewpiboon et al.(2012 )

(D) Tiwari et al.(2010 ); Rahmatullahet al. (2012 ); Hasanet al. (2013 )

S. apetala Lythraceae Triterpenes, steroids,avonoids,alkaloids, diterpenes

DPPH assay, NOscavenging assay,ferrous ion chelatingassay, totalantioxidant capacityassay

Enhanced insulin releasingactivity;

Insulin mimetic activity;Modifying glucose

utilization;Stimulating the regen-

eration of islets of langerhans in pancreas;

Enhance transport of blood glucose to the peripheral tissue.

(A) Banerjee et al.(2008 ); Vadlapudiand Naidu ( 2009 )

(D) Hossain et al.(2013 ); Patra et al.(2014 )

S. alba Lythraceae Tanins, phenoliccompunds

DPPH scaveng-ing, anti-lipid peroxidation

Modifying glucoseutilization


(D) Morada et al.(2011 )

(Continued ).


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Table 2. Continued

X. granatum Meliaceae Alkaloids, steroids,tannins, triterpenes,

Limonoids

DPPH assay, NOscavenging assay,ferrous ion chelatingassay, totalantioxidant capacityassay

Stimulation on -cells and help in the release of insulin;

Elevation in insulinsensitivity to glucose;

Protein tyrosine phosphatase activitymay be helping ininsulin action

(A) Vadlapudi and Naidu ( 2009 )

(D) Srivastava et al.(2011 )

X. moluccensis Meliaceae Alkaloids, steroids, DPPH scaveng-ing, anti-lipid peroxidation

Insulin mimetic or insulinsecretagogue activityInsulin resistancereversal activity -Glucosidase inhibitoryactivity

(A) Bunyapraphatsaraet al. (2003 );

(D) Srivastava et al.(2014 )

tannins, triterpenes, proanthocyanidins

Note: (A) References cited for antioxidant studies in mangrove plants; (D) references cited for antidiabetic studies in mangrove plants.

of glucose-6-phosphatase, fructose 1,6-bisphosphatase and

glycosylated haemoglobin. Besides, increased activity of liver hexokinase was also observed (Gurudeeban et al.2012 ).

5.2. Acanthus ilicifolius

A. ilicifolius (sea holly) belongs to the family of Acan-thaceae . Studies have reported that oral administration of ethanolic root extract of A. ilicifolius at a dose of 200 and 400 mg/kg body weight signicantly reduced the blood sugar level in normal, glucose-fed hyperglycaemic and alloxan-induced diabetic rats. Regeneration of -cells hasalso been reported in the diabetic rats (Venkataiah et al.

2013 ). The presence of avonoids, alkaloids, terpenoids,tannins and steroids in the root extracts of this plant may play important role in their hypogycaemic activities.

5.3. A. marina

A. marina belongs to the family Avicenniaceae. Theethanolic leaf extracts of A. marina has been shown to pos-sess antihyperglycaemic activity in alloxan-induced diabetic rats. The ethanolic leaf extracts (250 and 500 mg/kg)upon treatment on the diabetic rats for 15 days signif-icantly reduced the blood glucose levels along with anincrease in total haemoglobin (Hb), total protein and serum

insulin level. The A. marina leaf extract can reduce thelevel of serum urea that conrms the capacity to protectvital tissues, for example, kidney, liver and pancreas. It alsoimproved the biochemical parameters such as serum phos- phorous, albumin and globulin. The possible mechanismunderlying the antihyperglycaemic action of A. marinais attributed to stimulation of surviving -cells releasingmore insulin (Babuselvam et al. 2013 ). Methanolic extractof pnuematophores (aerial roots) of A. marina exhibitsantihyperglycaemic effect, which might be due to inhibition of AGEs. Studies have reported that triterpenoids

such as stigmasterol-3- O- -D-glucopyranoside may be the

hypoglycaemic components present in this plant whichcould be responsible for its antiglycation activity (Maheraet al. 2011 ).

5.4. B. racemosa

B. racemosa is an evergreen mangrove plant, belongingto the family Lecythidaceae. The bark and leaves have been traditionally used for anticancer, analgesic, antibacte-rial, anticolic and antifungal activities (Khan et al. 2001 ;Thomas et al. 2002 ). The bark and the roots of the plant have been reported to possess different compoundssuch as 3,3 -dimethoxy ellagic acid, dihydromyticetin, gal-

lic acid, bartogenic acid, stigmasterol, olean-18-en-3- -O-ecoumaroylester and olean-18-en-3- -O-Z-coumaroylesters along with germanicol, germanicone, betulinicacid, lupeol, taraxerol, neo-clerodane type diterpenoids,nasimalun A and nasimalun B (Sun et al. 2006 ; Yang et al.2006 ). The hexane, ethanol, methanol extracts of seedsof B. racemosa reported to possess -glucosidase and -amylase inhibition activities (Gowri et al. 2007 ). Gowrietal. ( 2009 ) also reported the presence of pentacyclic triterpenoid bartogenic acid in the methanol extracts of this plant responsible for its antidiabetic activity.

5.5. B. gymnorrhizaThe genus Bruguiera has six species and belongs tothe family Rhizophoraceae. The ethanolic bark extractof B. gymnorrhiza displayed antihyperglycaemic effectin streptozotocin (STZ)-induced diabetic rats. The potentantidiabetic compounds of this plant include phytocon-stituents such as bruguierol, -sitosterol, -amyrin, -amyrin, lupeol, oleanolic acid, ursolic acid, taraxerol, gym-norhizol and ellagic acid. The treatment with ethanolic bark extracts (400 mg/kg) for 21 days reported signicantreduction in blood glucose level in the STZ-induced dia-


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84 S.K. Das et al.

betic rats, which was comparable to that of a standard drugglibenclamide (0.5 mg/kg). Further, a decreased level of total cholesterol, triglycerides, very low density lipopro-tein, low density lipoprotein along with increased highdensity lipoprotein level in the diabetic rats was observed (Karimulla & Kumar 2011 ).

5.6. Ceriops sp.

The genus of Ceriops has two species namely Ceriopsdecandra , Ceriops tagal and belongs to the family Rhi-zosphoraceae. The ethanolic leaf extract of C. decan-dra (120 mg/kg) showed a signicant serum-glucose-lowering property in alloxan-induced diabetic mice uponoral administration, which was comparable to those of glibenclamide (0.1 mg/kg bw) (Nabeel et al. 2010 ). Thetreatment of diabetic rats with ethanolic leaf extractsresulted in an increase in insulin secretion, body weight,Hb levels and decrease in HbA1c levels. It was alsofound to regulate the key enzymes involved in the glucosemetabolism such as hexokinase, glucose-6-phosphataseand fructose 1,6-bisphosphatase. The activity of bothglucose-6-phosphatase and fructose 1,6-bisphosphatasewas found to be near-normal levels upon administrationof ethanolic leaf extracts to the diabetic rat. Increased hex-okinase enzyme activity was also reported in the diabeticrats. The possible mechanism underlying the antihypergly-caemic action of C. decandra may be due to the stimulationof surviving -cells to release more insulin (Nabeel et al.2010 ). Tiwari et al. (2008 ) reported that the ethanolicleaf extract of C. tagal improved the glucose toleranceof the normoglycaemic rats post sucrose load and also

lowered the blood glucose levels in STZ-induced diabetic rats after oral administration at a 250 mg/kg dose.The hexane sub-fraction of ethanolic leaf extract of C.tagal (100 mg/kg bw) was found to be most effectivefor the antihyperglycaemic activity in normal healthy rats post sucrose load, which was comparable to the effectof metformin. The compounds isolated from the hexanefraction of the C. tagal also showed signicant inhibi-tion against PTPase enzyme activity, which help in insulinaction (Tiwari et al. 2008 ). Similarly n-hexane soluble frac-tion of ethanolic leaf extracts of C. tagal was reported to stimulate the glucose uptake in L6 muscle cells in adose-dependent manner, which is comparable to the stan-

dard drug metformin (Tamrakar et al. 2008 ). In another study, the hydroalcoholic bark extracts of C. tagal showed antihyperglycaemic activity, which was attributed to its -glucosiadase inhibition potential (Lawag et al. 2012).

5.7. Excoecaria agallocha

E. agallocha , a mangrove species, belongs to the genus Excoecaria of the family Euphorbiaceae. Rahman et al.(2010 ) showed that the methanol stem extract of E. agal-locha reduces the serum glucose levels at doses of 200

and 400 mg/kg, which was signicantly lower than thelevel observed with glibenclamide (10 mg/kg bw). E. agal-locha has been reported to contain b-amyrin acetate, whichmay be responsible for its antidiabetic activity (Tian et al.2008 ). Thirumurugan et al. (2009 ) also reported that theethanolic leaf extracts of E. agallocha showed signi-cant hypoglycaemic activity. The antidiabetic potential isattributed to the presence of bioactive principles such asavonoids, triterpenoids, alkaloids and phenolics.

5.8. Heritiera fomes

H. fomes belongs to the family Sterculiaceae. The crudemethanol extract of H. fomes bark showed dose-dependentreductions in concentrations of serum glucose in mice. At60 min following glucose administration, the bark extractsignicantly lowered serum glucose levels by 49.2% at adose of 250 mg extract/kg body weight in comparison to43.5% by glibenclamide. Further it was investigated and reported that the crude methanolic extract of the bark has along-term action in its glucose-lowering effect and is better than glibenclamide (Ali et al. 2011 ).

5.9. Rhizophora sp.

The mangrove genus Rhizophora belongs to the fam-ily Rhizosphoraceae. Of the ten species of genus Rhi- zophora, the antidiabetic activity has been reported in threespecies: Rhizophora apiculata , Rhizophora annamalayanaand Rhizophora mucronata. The ethanolic root extracts of R. apiculata showed promising antihyperglycaemic activ-ity at 250 mg/kg in experimental rats. The chloroform and

aqueous sub-fractions of ethanolic root extract of the plantis rich in phytochemicals responsible antihyperglycaemicactivity. Further purication led to the isolation of seven pure compounds: lupeol, oleanolic acid, -sitosterol, palmitic acid, -sitosterol- -D-glucoside, inositol and pinitol. Among these compounds, inositol and pinitolshowed promising activity in the STZ model at 100mg/kg dose level (Lakshmi et al. 2006 ). The ethano-lic leaf extracts of R. apiculata showed hypoglycaemicand antihyperglycaemic effect in normal, glucose-fed and STZ diabetic rats (Sur et al. 2004 , 2015 ). The hypogly-caemic action of R. apiculata is attributed to the pres-ence of avonoids along with other bioactive compounds.

The antidiabetic properties of the hydro-methanolic leaf extracts of this plant can be attributed to its radical scav-enging and -cell protection properties.

Nabeel et al. ( 2012 ) have reported the antidiabetic potential of three mangrove plants: R. mucronata , R. apic-ulata and R. annamalayana . Oral administration of 60mg/kg aqueous extract of leaf modulated the parameterssuch as blood glucose, plasma insulin, body weight, totalhaemoglobin, glycosylated haemoglobin, liver glycogen, plasma and tissue lipids, cholesterol, triglycerides, FFAand phospholipids to normal levels in the alloxan-induced


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diabetic rats. The antidiabetic activity of R. apiculatawas more pronounced than that of the other mangroveextracts. The presence of an insulin-like protein in themangrove extracts was detected by sodium dodecyl sulfate polyacrylamide gel electrophoresis analysis and conrmed through enzyme linked immunosorbent assay. The antidi-abetic activity of the mangrove plants may be due to theimproved level of insulin secretion and its action (Nabeelet al. 2012 ). Gaffar et al. (2011 ) investigated the antidiabetic effect of R. mucronata , which is due to its capacityto inhibit carbohydrate digestion and absorption. Haqueet al. ( 2013 ) reported that the aqueous bark extracts of R. mucronata possess signicant hypoglycaemic and anti-hyperglycaemic activities. The bark extracts of this plantshowed dose-dependent antidiabetic effects, which signi-cantly suppressed postprandial hyperglycaemia. The glu-cose absorption inhibition could have been the possiblemechanism behind its hypoglycaemic effect. In another study, the hydroalcoholic bark extracts of R. mucronata

showed antihyperglycaemic activity, which was attributed to its -glucosiadase inhibition potential (Lawag et al.2012 ).

5.10. Nypa fruticans

N. fruticans (Arecaceae) is a mangrove palm well knownfor its traditional uses by the local practitioners againstdifferent ailments in southern regions of Bangladesh. Themethanolic leaf and stem extracts of this plant (500 mg/kg)has been shown to exert signicant antihyperglycaemiceffect in diabetic mice (Reza et al. 2011 ).

5.11. Sonneratia sp.

The mangrove genus Sonneratia belongs to the familyLythraceae. Of the twenty identied species of genusSonneratia , the antidiabetic activity has been reported inthree species such as S. alba , Sonneratia apetala and S.caseolaris. Fruits of S. caseolaris have many therapeuticapplications in folklore medicine (Bandaranayake 2002 ).Compounds such as oleanolic acid, -sistosterol- -D-glucopyranoside and luteolin isolated from the methanolicextract of its fruits have shown inhibition of -glucosidaseenzyme in a dose-dependent manner (Tiwari et al. 2010 ).Further, the methanolic fruit extracts of this plant sig-

nicantly reduced the serum glucose concentrations inglucose-loaded mice in a dose-dependent manner (Rah-matullah et al. 2012 ; Hasan et al. 2013 ). The antihyper-glycaemic activities of this plant may be due to a number of factors such as decreased intestinal glucose absorp-tion, increase in pancreatic secretions, glucose uptake,insulin secretion and better glyceamic control. Moradaet al. (2011 ) reported the antidiabetic potential of methano-lic leaf extracts of S. alba using in vivo mice model.The tremendous blood-glucose-attenuating activity of theextract was attributed to complex polysaccharide molecule

obtained from S. alba leaf extracts. Signicant reductionin sugar level was observed during the rst 6 (19.2%) and 12 h (66.9%) after the administration of the extracts to thediabetic mice. Similarly, the antihyperglycaemic activity of seeds and pericarps of S. apetala fruits were reported inSTZ-induced diabetic mice (Hossain et al. 2013 ). The anti-hyperglycaemic activity of this plant may be due to insulinmimetic activity, better glucose utilization, regeneration of islets of langerhans in pancreas and enhanced transport of blood glucose to the peripheral tissue.

5.12. Xylocarpus sp.

The genus Xylocarpus belongs to the family Meliaceaeand consists of three species such as X. granatum , Xylo-carpus mekongensis and X. moluccensis . The antidiabeticactivities have been reported in X. granatum and X. moluc-censis . X. granatum (which is commonly known as cannon ball tree and found in the coastal region of India, Aus-tralia, South East Asia and East Africa) was reported to possess antidiabetic activity (Srivastava et al. 2011 ).The ethanolic extract of epicarp of X. granatum showed improvement of oral glucose tolerance post sucrose load inSTZ-induced diabetic rats. It also showed blood-glucose-lowering effect and improvement in insulin resistance. Thecommon biochemical markers of diabetes (that is, glucose-6-phosphatase, phosphorfructokinase, phosphoenolpyru-vate carboxy kinase, pyruvate kinase, lactate dehydroge-nase and glycogen phosphorylase of liver and kidney inSTZ-treated rats) were also found towards normalizationafter the oral treatment of the extracts at 250 mg/kg dose

for three weeks. The antidiabetic effects may be due toincrease insulin release and inhibition of -glucosidaseenzymes.

The ethyl acetate soluble fraction of epicarp of X. moluccensis (EAXm) showed both antidiabetic and antidyslipidemic effects in diabetic-induced rats. Thetreatment with EAXm led to a signicant fall in theelevated blood glucose level in the STZ-induced rats,which was found to be comparable to standard drug met-formin. The extracts signicantly increased both seruminsulin and HDL-C levels. The extract also displayed enormous ability to improve the liver and renal func-tions as evident by decline AST, ALT, urea, uric acid

and creatinine levels in the serum. Treatment with EAXmalso restored the altered activities of few key regula-tory enzymes involved in carbohydrate metabolism suchas glucokinase, phospho-fructokinase, pyruvate kinase,glucose-6-phosphatase, fructose-1,6-bisphosphatase and glycogen phosphorylase in liver, muscle and renal tis-sues of STZ-induced diabetic rats. The EAXm also displayed an in increase glucose uptake and inhibition of alpha-glucosidase enzyme as evident by various in vitrostudies. The mechanism of antihyperglycaemic activity of this plant extract may be due to insulin mimetic, insulin


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86 S.K. Das et al.

secretagogue and insulin resistance reversal activity (Sri-vastava et al. 2014 ).

6. Epilogue

The modulation of cellular signal transduction pathways by naturally occurring phytochemicals has recently beenextended to elucidate the molecular basis of diseases, ingeneral, and diabetes, in particular. Many of the agentswhich are a mainstay of pharmacotherapy in diabetes have been shown to have antioxidant properties in addition totheir primary pharmacological actions. Therefore, strate-gies to block the formation of reactive radicals or scav-enging the reactive free radical may provide a targeted and casual approach for the treatment of diabetes. Discussionsvide supra clearly points towards the therapeutic potentialsof diabetes by mangrove plant extracts as they have shownsubstantial hypoglycaemic and insulin mimetic potentialwith pronounced antioxidant activity. The mangrove plants

survive in an ecologically hostile condition where no other plants could survive; therefore they are supposed to berich in antioxidant compounds which can be exploited therapeutically. This review has covered only 18 poten-tial mangrove plants that could be used in the treatmentof diabetes. However, some of the other mangrove plantsthat have not yet been fully explored may have therapeuticapplications in diabetes. The development of new antidi-abetic moieties from bioactive compounds is necessaryin order to nd more effective and less toxic antidiabeticdrugs. Therefore, extensive study on the potential of man-grove plants with isolated active compounds that haveshown antidiabetic activity should go through additional

in vitro and in vivo animal testing followed by toxicity and clinical tests. This may provide a promising compound to be optimized and suitable for application in the productionof new antidiabetic compounds.

Disclosure statementThe authors declare that they have no conicts of interest todisclose.

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