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A review on a mangrove species from the Sunderbans, Bangladesh: Bruguiera gymnorrhiza (L.) Lam.

INTRODUCTION

Bruguiera gymnorrhiza is a small tree that can grow up to 10 meters high. The tree can be found on the seaward side of mangrove swamps in the Sunderbans forest of Bangladesh. The tree develops short prop-roots. Fruits are spindle-shaped and drop in an upright position, in which position they are embedded in the soil and develop roots.

Kingdom: Plantae

Phylum: Streptophyta

Order: Malpighiales

Family: Rhizophoraceae

Genus: Bruguiera

Species: gymnorrhiza (L.) Lam. (also spelled as gymnorhiza)

The genus Bruguiera, besides gymnorhiza, includes other species such as Bruguiera cylindrica, Bruguiera hainesii, Bruguiera parviflora and Bruguiera sexangula.

Scientific synonyms:

Rhizophora gymnorrhiza L.

Bruguiera conjugata Merr.

Bruguiera cylindrica (non Blume) Hance

Bruguiera rheedii Bl.

Bruguiera rumphii Bl.

Other names:

Kankra (Bangladesh), black mangrove, large-leafed mangrove, orange mangrove (Northern Australia); oriental mangrove; thuddu ponna or uredi (Andhra Pradesh, India), malkadol or srikanda (Sri Lanka); muia or mkoko wimbi (Kenya, Tanzania, Zanzibar, Mozambique); prasak tooch or Burma mangrove (Cambodia); bakauan (Tagalog, the Phillipines); putut (Sumatra, Indonesia); bakau besar (Peninsular malay); mangoro (Pidgin Papua New Guinea); tumu merah (Singapore); pang ka ha sum (Thailand); vet den (Vietnam).

Distribution:

Black mangrove is one of the most widely distributed trees in the tropics, and occurs in the tropical South and East Africa, Madagascar, Seychelles, Sri Lanka, Southeastern Asia (throughout Malaysia to Philippines), Ryukyu Islands; Australia, Micronesia, and Polynesia. It grows on the seaward side of estuaries in mud, in places that are well watered and frost free [76]. In Bangladesh, the tree can be found in the Sunderbans forest, which covers part of Khulna Division. The Sunderbans forest is considered the largest mangrove forest in the whole world.

Botanical features:

Bruguiera gymnorrhiza is an evergreen tree 8-35 m high, with straight trunk 40-90 cm in diameter, buttressed at base, and with many upright pneumatophores rising to 45 cm from long horizontal roots. The bark is pale-brown to gray, smooth to roughly fissured, thick and the inner bark is reddish. The leaves are opposite, crowded at the ends of branches, roughly elliptical, 60-120 x 20-60 mm, hairless, glossy apple green when young, becoming yellow with age. The flowers are red and remain attached to the propagule when it falls. The propagules are green and cigar-shaped, between 10 and 20 cm long and can be found throughout the year. Fruit is a fleshy berry up to 25 mm long, germinating on the tree (viviparous) [13,41].

Chemical constituents:

From flowers:

Dammarane triterpenes, namely bruguierins A-C [52].

A new cyclic 4-hydroxy-dithiosulfonate, bruguiesulfurol, 4-hydroxydithiolane 1-oxides, brugierol and isobrugierol [53].

From stem:

Pimaren diterpenoids such as ent-8(14)-pimarene-15R, 16-diol; ent-8(14)-pimarene-1alpha, 15R, 16-triol; (5R, 9S, 10R, 13S, 15S)-ent-8(14)-pimarene-1-oxo-15R, 16-diol; isopimar-7-ene-15S,16-diol; (-)-1[beta], 15(R)-ent-pimar-8(14)-en1,15,16-triol [49].

Aromatic compounds such as bruguierols A-C; 1-(3-hydroxyphenyl)- 2, 5-hexanediol and 3, 4-dihydro-3-(3-hydroxybutyl)-1, 1-dimethyl 1H-2-benzopyran-6,8-diol [50]. ent-Kaurane diterpenoids such as (4alpha, 8beta, 13beta)- 13-(hydroxymethyl)-16-oxo 17-norkauran-18-al; (4alpha, 16alpha)-17-chloro-13, 16-dihydroxy- kauran-18-al; (4alpha)-13, 16,17-trihydroxykaur-9(11)-en-18-oic acid; (4alpha)- 16, 17-dihydroxy- kaur-9(11)-en-18-al; ent-Kaurenol; ent-Kaur-16-ene-13, 19-diol; (-)-Kauran-17, 19-diol; (-)-17-Hydroxy-16alpha-kauran-19-oic acid; (4[alpha])- 16, 17-dihydroxy- Kauran-18-al; (-)-ent-Kaur-16-en-13-hydroxy-19-al; 16, 17-Dihydroxy-9(11)-kauren-18-oic acid [48].

Whole plant:

Gymnorrhizol, an unusual novel macrocyclic polydisulfide [129].

Gibberellin A3, A4 and A7 [40].

Tannins containing catechin-3-O-rhamnoside chain extender units in polymeric procyanidins [2].

Leaves:

Sterols such as cholesterol, campesterol, stigmasterol, and 28-isofucosterol; triacyl glycerols, wax ester and sterol ester (mainly lupeol based) [88, 95].

Gramrione (4',5',7-trihydroxy-3',5-dimethoxy flavone), a new flavone [111].

Beta-amyrin palmitate, lupeol stearate, lupenone, lupeol, [??]-amyrin, taraxerol, and beta-sitosterol [112].

Roots:

Diterpenoids such as steviol (see [endnotes.sup.3]); ent-kaur-16-en-13-hydroxy-19-al, 15(S)-isopimar-7-en-15,16-diol); ent-kaur-16-en-13, 19-diol; methyl-ent-kaur-9(11)-en-13, 17-epoxy-16-hydroxy-19-oate and 1[beta],15(R)-ent-pimar-8(14)-en-1, 15, 16-triol [48].

Apiculol (1-hydroxy-epimanoyl oxide), a diterpene of labdene series [117].

Ethnomedicinal uses of Bruguiera gymnorrhiza and related species:

The bark is used as an abortifacient and for treating burns in the Solomon Islands. The bark is reported to be have astringent property and is used for malaria and diarrhea in Cambodia and in Indonesia and China respectively, and cure fish poisoning (Marshall Islands) [14, 52, 106]. Elsewhere the fruit is used to treat eye problems, and scrapped skin of the fruit to stop bleeding. The fruit can be chewed as a betel nut substitute. The leaves are used in India to control blood pressure [www.naturia.per.sg/buloh/plants/bruguiera%20gymnorhizo.htm].

Pounded twig tips of the plant along with coconut oil and leaves of Ocimum sanctum L. are rubbed on the body after hard physical work to reduce fatigue by the Nicobarese of Car Nicobar Islands, India [142]. Leaves are considered tumor inhibitors by the inhabitants of Pichavaram forest on the east coast of Tamil Nadu, India. The whole plant boiled in water is given twice daily after meals to relieve constipation [114]. A similar use of the plant has been reported for the villagers of Coringa wildlife sanctuary, East Godavari district, Andhra Pradesh, India [80].

A related species, Bruguiera cylindrica is used for treatment of hepatitis by the village people surrounding the Pitchavaram mangrove forest in Tamil Nadu, India [110]. Other ethnomedicinal uses of various species belonging to the Bruguiera genera have been reviewed [10]. The bark and leaves of Bruguiera caryophylloides are used for treatment of ulcers. The bark of Bruguiera exaristata, Bruguiera parviflora and Bruguiera sexangula is used as an anti-tumor agent, while the fruits of Bruguiera gymnorrhiza are used for treatment of eye diseases. The leaves of Bruguiera rumphii are used ethnomedicinally for treatment of diabetes.

Other uses:

All portions of the live tree are used for timber; in addition to making boats, poles are used to make fish traps and the frames of huts. The heavy wood (specific gravity 0.87-1.08) is durable and is used for construction, furniture, houseposts, and pilings [76]. In Malaysia, the wood is chipped for the manufacture of pulp and rayon, and fragments of wood are made into charcoal in many places. The bark is high in tannins, and so has been used for tanning. Fruits (propagules) are eaten occasionally when anything better is unavailable. More often, they are chewed as astringent with the betel quid. Chinese in Java make a sweetmeat there from. Dutch Indians use the bark to flavor raw fish. The leaves and peeled propagules are eaten in the Moluccas after soaking and boiling [54]. The pigment derived from the bark is used in China and Malaya for black dye [14]. In Hawaii, the flowers are used for making lei (flower necklaces, mostly these days draped around arriving tourists). In South Africa, the tree has been planted to stabilize dunes and in fresh water swamps.

[http://www. hort.purdue.edu/newcrop/duke_energy/B ruguiera_gymnorrhiza. html]

Reported biological activities and properties of phytochemical constituents:

Beta-Amyrin (12-oleanex-3beta-ol) is found in a wide variety of plants, some of which are given below. The compound has been isolated from germinating seeds (along with beta-sitosterol) of Pisum sativum [9], root of Byrsonima intermedia [27], with ellagic acid from Couroupita amazonica [122], from light petroleum extract of the stem bark (with iguesterin, pristimerin, tingenone, beta-sitosterol and maytenonic acid) and root bark (with pristimerin, tingenone and beta-sitosterol) of Gymnosporia montana [61], with beta-sitosterol, stigmasterol, campesterol, cholesterol, alpha-amyrin (12-ursen-3beta-ol), taraxasterol and pseudo-taraxasterol from Tanacetum vulgare [16] and Achillea millefolium [17], with beta-methyl oleanate, beta-sitosterol, stigmasterol and trichodesmine from Trichodesma africanum [100], with three guaianolide sesquiterpenes-montacephalin, tomencephalin, and 5-hydroxytomencephalin as well as beta-amyrin acetate, stigmasterol, stigmasterol-3-beta-D-glucoside, (-)-kaur-16-en-19-oic acid and monoginoic acid from the leaves of Montanoa tomentosa [137], from Zanthoxylum planispinum [22], with epinodosinol, lasiodonin and alpha-amyrin from the leaves and stems of Isodon parvifolia [43], with the coumarins- toddaculin, coumurrayin, toddanone, 8-(3,3-dimethylallyl)-6,7-dimethoxycoumarin, isopimpinellin, 6-(3-chloro-2-hydroxy-3-methylbutyl)-5, 7-dimethoxycoumarin, 6-formyllimettin, 5,7,8-trimethoxycoumarin, toddasin, (+)-toddanol, 6-(2-hydroxy-3-methoxy-3-methylbutyl)-5, 7-dimethoxycoumarin, toddalolactone, toddalenol, toddalosin, 5-methoxysuberenon, toddalenone, and 8-formyllimettin, benzo[c]phenanthridine alkaloids-[des-N-methylchelerythrine, oxychelerythrine, arnottianamide, oxyavicine, avicine, chelerythrine and chelerythrine-psi-cyanide, four quinoline alkaloids- N-methylflindersine, 4-methoxy-1-methyl-2-quinolone, skimmianine and integriquinolone from the root bark of Toddalia asiatica [56], as beta-amyrin acetate along with glyceride-1, 3-dipalmito-2-sorbate, thesoideaside, lupeol acetate (lup-20(29)-en-3beta-yl acetate), alpha-amyrin caprylate, tamarixetin and tamarixetin-3-O-beta-D-galacto-pyranoside from Cynanchum thesioides [151], with 3-epi-ursolic acid, methyl maslinate, 3beta-acetoxy-delta-7-cholest-7-ene, protocatechuic acid, ethyl n-hexacosanoate and ethyl n-tetracosanoate from the radix of Vaccinium scopulorum [119], as beta-amyrin palmitate from Lobelia inflata [125], with beta-sitosterol, stigmasterol, alpha-amyrin, friedelin, naringenin, quercetin and eudesmane derivatives from the aerial parts of Artemisia argyi [131], as beta-amyrin acetate along with O-acetyl-pachymic acid, 3beta-hydroxy-lanosta-7,9(11), 24-trien-21-oic acid and 3beta-hydroxy-16alpha-acetoxy-lanosta-7,9(11),24-trien-21-oic acid from ethereal extracts of Poria cocos [143], with the coumarins schinicoumarin, acetoxyaurapten, epoxycollinin, schininallylol, schinilenol, schinindiol, aurapten, collinin, epoxyaurapten, hydrangetin, umbelliferone, acetoxycollinin and aesculetin dimethyl ether, three alkaloids- norchelerythrine, dictamnine and skimmianine as well as the triterpenoid- friedelin from the chloroform soluble part of the bark of Zanthoxylum schinifolium [21], with betulin, vanillic acid, ethyl gallate, kaempferol, 3,5-dimethoxy-4-hydroxybenzoic acid, aromadendrol and resveratrol from the roots of Ampelopsis brevipedunculata [149], with n-hexacosanol, germanicol, isobaurenol, lupeol (lup-20(29)-en-3beta-ol), hopenol-a, hopeol, cholesterol, campesterol, stigmasterol, sitosterol, and dihydrositosterol from petroleum ether extract of Festuca argentina [15], with beta-sitosterol, daucosterol, spinasterol, stigmasterol, dammara-20,24-dien-3beta-ol and epifriedlinol from Aster poliothamnus [153], with beta-sitosterol, daucosterol, stigmasterol, stigmasterol-3-O-beta-D-glucopyranoside and 4',5',7-trihydroxy-flavone-6-O-beta-D-glucopyranoside from Begonia evansiana [154], with australone A, 3beta-[(m-methoxybenzoyl)oxy]urs-12-en-28-ioc acid, morusin, kuwanon C, betulinic acid, quercetin, and ursolic acid from the root bark of Morus australis [65], with lupeol and germanicol from Vernonia brasiliana [7], as beta-amyrin acetate along with (22-E)-stigmasta-5, 22-dien-3beta-ol, ent-kaur-16-en-19-oic acid, ent-kaur-9(11), 16(17)-dien-19-oic acid and 3alpha-angeloiloxy-ent-kaur-16-en-19-oic acid from ethanolic extract of the aerial parts of Wedelia paludosa [12], as beta-amyrin acetate along with alpha-amyrin acetate, glochidone, betulinic acid and isoquercitrin from Ipomoea pes-caprae [67], with alpha-amyrin, lupeol, germanicol, chamaedrydiol, castanopsol, 2alpha-hydroxylupeol and epigermanidiol from hexane extract of Marsypianthes chamaedrys [32], with alpha-amyrin and friedelin from hexane extracts of leaves and stems of Anchietia salutaris [34], with olean-12-ene-3beta, 11alpha-diol, lupeol, oleanolic acid, globuxanthone, subelliptenone H, subelliptenone B, 12[??]-hydroxy-des-D-garcigerrin, 1-O-methylglobuxanthone and symphoxanthone from hexane extract of the bark of Garcinia vilersiana [92], as beta-amyrin acetate with olean-12-en-21beta-yl acetate, olean-12-en-3alpha-yl acetate, 16(17)-seco-urs-12,20(30)-dien-18alpha H-3beta-yl acetate, urs-20(30)-en-18beta H-3beta-yl acetate, 16(17)-seco-urs-12, 20(30)dien-18alpha H-3beta-ol, and lup-1, 12-dien-3-on-21-ol from the roots of Hemidesmus indicus [115], with beta-sitosterol, stigmasterol, friedelan-3beta-ol (epifriedelenol), cycloartenone, beta-amyrin acetate, friedelin and epifriedenyl acetate from the hexane extract of Heliotropium marifolium [121], with 14beta-15alpha-dihydroxy-delta4pregnene-3, 20-dione, 3beta-14beta,15alpha-16alpha-hydroxy-20-oxo-delta5pregnene-tetra-ol, alpha-amyrin and beta-sitosterol from the leaves of Solenostemma argel [51], with alpha-amyrin, maniladiol, brein, 3beta, 24-dihydroxy-urs-12-ene, 3-oxo-20S-hydroxytaraxastane and 3beta,20S-dihydroxytaraxastane from the resin of Protium heptaphyllum [130], with the dihydroagarofuran alkaloid 1beta-acetoxy-9alpha-benzoyloxy-2beta, 6alpha-dinicotinoyloxy-beta-dihydroagarofuran, maytenfolic acid, 3alpha-hydroxy-2-oxofriedelane-20alpha-carboxylic acid, lup-20(29)-ene-1beta, 3beta-diol, (-)-4'methylepigallocatechin and (-)-epicatechin from ethanol extracts of Maytenus heterophylla [101], with (-)-epicatechin and (-)-4'methylepigallocatechin from Maytenus arbutifolia [101], with friedelin, epifriedelinol, beta-sitosterol, beta-sitosterol 3beta-D-glucopyranoside and naringin from the dried rhizome of Drynaria quercifolia [113], with makisterone A, 2,3-dimethoxy-9,10-dihydroxy-N-methyltetrahydroproto-berberine quaternary salt (haitinosporine), palmatine and docosyl ferulate from the vine stalk of Tinospora hainanesis (Guo et al, 1998), as beta-amyrin palmitate and beta-amyrin acetate along with alpha-amyrin palmitate, lupeyl acetate, lupeol, kairatenyl palmitate and hopenyl palmitate from a C[H.sub.2][Cl.sub.2]/MeOH extract of small twigs of Brachylaena ramiflora var. ramiflora [20], with two steroidal lactones of the withanolide type-5beta, 6alpha,14alpha,17beta,20beta-pentahydroxy-1-oxo-20S, 22R-witha-2,24-dienolide and 6alpha,7alpha-epoxy-5alpha,14alpha,17alpha, 23beta-tetrahydroxy-1-oxo-22R-witha-2,24-dienolide, as well as scopoletin, aesculetin, stigmasterol and sitosterol from the fruit of Withania somnifera [1], as beta-amyrin acetate along with isobauerenyl acetate, 24-methylenecycloartenone, octacosyl ferulate and 2,4-dihydroxy-6-methoxy-3-methylacetophenone from ethanol extract of dried roots of Euphorbia fischeriana [78], with fridelin, 1-octadecanol, beta-sitosterol, daucosterol and gallic acid from Quercus mongolica [152], with alpha-amyrin, lupeol and lupeol acetate from the seeds of Caesalpinia bonducella [116], with luteolin 5-O-beta-d-glucopyranoside, luteolin, luteolin 7-methyl ether, luteolin 5-O-beta-d-glucuronide, 5-O-beta-d-glucopyranosyl-luteolin 7-methyl ether, rosmarinic acid, rosmarinic acid methyl ester, daucosterol and alpha-amyrin from EtOH extract of Coleus parvifolius [135], with salireposide, benzoylsalireposide, oleonolic acid, beta-sitosterol and beta-sitosterol glycoside from Symplocos racemosa [4], with a bisabolene- 6-hydroxy-2-methyl-5-(5'-hydroxy-1'(R), 5'-dimethylhex-3'-enyl)-phenol, dammarane triterpenes-3beta, 16beta,20(S),25-tetrahydroxydammar-23-ene and 3beta-acetoxy-16beta,20(S),25-trihydroxydammar-23-ene as well as 2-methyl-5-(4'(S)-hydroxy-1'(R), 5'-dimethylhex-5'-enyl)-phenol, 2-acetoxyfuranodienone, 2-methoxyfuranodienone, 3beta,16beta,20(R)-trihydroxydammar-24-ene and its acetate derivative, 3beta-acetoxy-16beta,20(R)-dihydroxy dammar-24-ene and beta-amyrin acetate from the resin of Commiphora kua [82], with dammarane triterpenes- (20S)-3beta-acetoxy-12beta,16beta-trihydroxydammar-24-ene, (20S)-12beta,16beta-trihydroxy dammar-24-ene-3beta-Obeta-glucopyranoside, (20S)-3beta-acetoxy-12beta,16beta,25-tetrahydroxydammar-23-ene, (20S)-3beta,12beta,16beta,25-pentahydroxydammar-23-ene, (20R)-3beta-acetoxy-16beta-dihydroxydammar-24-ene, (20R)-3beta,16beta-trihydroxydammar-24-ene, 3beta-acetoxy-16betahydroxydammar-24-ene, 3beta-hydroxydammar-24ene, and 3beta-acetoxydammar-24-ene along with 3beta-amyrinacetate, 2-methoxyfuranodienone, 2-acetoxyfuranodienone, and beta-sistosterol from the resin of Commiphora confusa [83], with triacontanoic acid, palmitic acid, stigmasterol, oleanolic acid and soya-cerebroside I from Lysimachia davurica [136], as beta-amyrin palmitate with taraxastery acetate, luteolin-7-O-alpha-L-rhamanopyranosyl-(1 -->2)-beta-D-glucopyranoside, luteolin-7-O-beta-D-glucopyranoside, triacontanic acid, beta-sitosterol, stigmasterol and stigmast-7-en-3-beta-ol from Carduus crispus [156], with pterodontriol A, pterodontriol B, pterodonta acid, ilicic acid, costic acid and an eudesmane derivative-4alpha, 5alpha-dihydroxyeudesma-11(13)-en-12-oic acid from Laggera pterodonta [148], with cedashnine, cedphiline, cedmiline, scoparone and sitosteryl glucoside from hexane extract of stem bark of Cedrelopsis grevei [89], with ursolic acid, oleanoic acid, alpha-amyrin, lupeol and beta-sitosterol from methylene chloride and hexane extracts of Miconia rubiginosa [123], with alpha-amyrin, beta-sitosterol, 5,6,7-trimethoxycoumarin and 6-methoxy-7,8-methylenedioxycoumarin from non-polar fraction of Artemisia apiacea [73], as beta-amyrin acetate with trans-phytol, ent-germacra-4(15),5,10(14)-trien-1beta-ol, beta-dictyopterol, oleanolic acid, kaempferol, kaempferol-3-Orutinoside, methyl 3,5-di-O-caffeoyl quinate and 3,5-di-O-caffeoyl quinic acid from the aerial parts of Solidago virga-aurea var. gigantea [22], with oleanolic acid, beta-sitosterol and clerodane-type diterpenoids- ballotenic acid and ballodiolic acid from Ballota limbata [5], with alpha-amyrin and baurenol from the leaves of Carmona retusa [142], with anadanthoflavone, alnusenol, lupenone, lupeol, betulinic acid, alpha-amyrin, beta-sitosterol, stigmasterol, apigenin, 4-hydroxybenzoic acid and cinnamic acid from the aerial parts of Anadenanthera colubrina [47], with 3-O-fatty acid esters of triterpene alcohols- arnidiol, maniladiol and 16beta-hydroxylupeol along with alpha-amyrin, beta-sitosterol, 3,4-O-dicaffeoyl quinic acid, cinnamic acid, pinoresinol-beta-D-glucoside and rutin from the aerial parts of Achillea alexandri-regis [69], as beta-amyrin juarezate [3-[5-phenyl-(2E,4E)-penta-2,4-dienoyloxy]-olean-12-ene] and the pentacyclic triterpene esters, peltastina A [3beta-[5-phenyl-(2E,4E)-penta-2,4-dienoyloxy]-urs-12-ene] and peltastine B [3beta-[5-phenyl-(2E,4E)-penta-2,4-dienoyloxy]-lup-20(29)-ene] from the stem of Peltastes peltatus [55], as beta-amyrin acetate with isolariciresinol 9-O-beta-D-glucopyranoside, cycloartenol, beta-sitosterol and daucosterol from Ervatamia hainanensis [132], with methyl gallate, gallic acid, laricetrin, laricetrin 3-glucoside, laricetrin 3-galactoside, laricetrin 5-galloyl-3beta-D-xylopyranoside, beta-sitosterol, lupenone, beta-amyrinone, alpha-amyrinone, lupeol, alpha-amyrin and alpha-tocopherol from ethyl acetate and hexane extracts of leaves of Moldenhawera nutans [35], with oleanolic acid, beta-amyrin acetate, rutin, narcissin, 3-glucoside of isorhamnetin, quercetin, isoquercitrin, vanillic acid, caffeic acid, chlorogenic acid, protokatechuic acid, p-coumaric acid and syringic acid from Calendulae officinalis flos [86], with alpha-amyrin, stigmast-5-en-3-ol, squalene, tetracosan, phytol, hexadecanoic acid and octadecanoic acid from lipophilic extracts of foliage of Betula alleghaniensis [72], with oleonolic acid, beta-sitosterol and three sesquiterpene hemiacetals named achilleanone, vermiculone and vermicularone from Achillea vermicularis [6], with ursolic acid, oleanolic acid and alpha-amyrin from leaves and callus of Vaccinium corymbosum [87], with lupeol, betulin, delta1-lupenone, 3-hydroxy-2-methoxy-8,8,10-trimethyl-8H-antracen-1,4,5-trione, 3,7-dihydroxy-2-methoxy-8,8,10-trimethyl-7,8-dihydro6H-antracen-1,4,5-trione, (2[S.sup.*],10a[R.sup.*])-2,8-dihydroxy-6-methoxy-1,1,7-trimethyl-2,3,10,10a-tetrahydro-1H-fenantren-9-one and (2S,3S)-3'hydroxy-4',5,7-trimethoxy-flavan-3-ol from the wood of Byrsonima microphylla (Aguiar et al, 2005), with moretenol, stigmast-6-en-3beta-ol and veridiflorol from Achillea ligustica [25], with daucosterol, beta-sitosterol, campesterol and alpha-amyrin from Nepeta cataria var. citriodora [63], with (6R)-2-chloro-6-[(1S)-1,5-dimethylhex-4-en-1yl]-3-methylcyclohex-2-en-1-one, (6R)-6-[(1S)-1,5-dimethylhex-4-en-1-yl]-3-methylcyclohex-2-en-1-one, bauerenol acetate, lupenone, alpha-amyrenone, beta-sitosterol, stigmasterol, ursolic acid, betulinic acid and scopolin from the roots of Euphorbia chrysocoma [120], as beta-amyrin acetate with caudatin, metaplexigenin, cynauricuoside, succinic acid, azelaic acid, wilforibiose, sucrose, 1-O-hexadecanolenin, cynanchone A, acetylquinol, beta-sitosterol and daucosterol from Cynanchum auriculatum [155], as beta-amyrin acetate with friedelin, betulinic acid and lupeol from EtOAc extract of the stem bark of Syzygium jambos [68], with beta-sitosterol, gallic acid, luteolin, quercetin, 2,4-dimethyl-heptene, ethylbenzene, O-xylene, styrene, hexadecanoic acid etylester, 9,12-octodecadienoic acid ethyl ester, diisooctyl phthalate and alpha-amyrin from the hypogeal part of Limonium bicolor [145], as beta-amyrin acetate with balanophorin A, balanophorin B, monogynol A, lupeone, caffeic acid ethyl ester, catechin, and 1-O(E)-caffeoyl-3-O-galloyl-beta-D-glucopyranose from Balanophora spicata [26], with alpha-amyrin, ursolic acid, corosolic acid, euscaphic acid, pomolic acid, tormentic acid, 2alpha,3alpha-dihydroxyurs-12-en-28-oic acid, 2beta,3beta,19alpha-trihydroxyurs-12-en-28-oic acid, asiatic acid, 24-hydroxy tormentic acid, myrianthic acid, oleanolic acid, maslinic acid and 2alpha,3alpha,dihydroxyolean-12-en-28-oic acid from Potentilla chinesis [77], as beta-amyrin acetate and beta-amyrin palmitate with (23Z)-feruloylhederagenin and (23E)-feruloylhederagenin from Ludwigia octovalvis [18], and as beta-amyrin acetate with 3beta,24-dihydroxytaraxer-14-ene, cleomiscosin A, cleomiscosin C and beta-sitosterol glucoside-3'-O-hexacosanoicate from leaf and twig of Acer okamotoanum [59].

The crude methanolic extract from the leaves of Lobelia inflata containing beta-amyrin palmitate reportedly exhibited antidepressant activity in mice [125]. In studies on forced swimming method in mice, it has been shown that beta-amyrin palmitate caused a release of [3H]norepinephrine in mouse brain synaptosomes, suggesting that the compound might activate noradrenergic activity and this activity is responsible for the antidepressant effect [126].

It has been suggested that beta-amyrin palmitate has similar properties in some respects to mianserin (an antidepressant drug) and might possess a sedative action. In forced swimming test, beta-amyrin palmitate has been shown to reduce the duration of immobility of mice significantly in a dose-dependent manner (5, 10 and 20 mg/kg body weight). The compound also elicited a dose-related reduction in locomotor activity of mice and antagonized locomotor stimulation induced by methamphetamine [127]. Beta-amyrin palmitate enhanced hypoactivity of mice treated with clonidine and antagonized hyperactivity produced by phenylephrine; the inhibitory action of beta-amyrin palmitate was not affected by yohimbine, but was potentiated by prazosin. When combined with a dopaminergic agonist, apomorphine, beta-amyrin palmitate did not affect locomotor stimulation produced by apomorphine, suggesting that beta-amyrin palmitate might inhibit alpha1-adrenoceptors [128]. The anxiolytic and antidepressant effects of a mixture of alpha- and beta-amyrins has been demonstrated by the open-field, elevated-plus-maze, rota rod, forced swimming and pentobarbital-induced sleeping time tests. The authors concluded that the sedative and anxiolytic actions of alpha- and beta-amyrins might involve an action on benzodiazepine-type receptors, while the antidepressant effect might involve noradrenergic mechanisms [3].

A mixture of alpha- and beta-amyrins isolated from the resin of a medicinal plant Protium heptaphyllum demonstrated antipruritic effect in mice against scratching behavior induced by dextran T40 and compound 48/80. The observed results indicated that the effect may be related to a stabilizing action on mast cell membrane, since ex vivo, compound 48/80-induced degranulation of rat peritoneal mast cells was markedly reduced in animals pre-treated with a mixture of alpha- and beta-amyrins [96].

A mixture of alpha- and beta-amyrins obtained from Protium heptaphyllum also protected mice against gastric mucosal damage induced by intragastric ethanol. Activation of capsaicin-sensitive primary afferent neurons has been implicated in the gastro-protective mechanism of alpha- and beta-amyrins [97]. The triterpene mixture of alpha- and beta-amyrins, isolated from the trunk wood resin of Protium heptaphyllum also protected mice against liver injury-induced by acetaminophen. Pretreatment of mice with the triterpenes attenuated the acetaminophen-induced acute increase in serum ALT and AST activities, replenished the depleted hepatic GSH, and considerably reduced the histopathological alterations in a manner similar to N-acetycysteine. The acetaminophen-associated mortality was completely suppressed by treatment with the triterpenes. Additionally, alpha- and beta-amyrins potentiated pentobarbital sleeping time, suggesting the possible suppression of liver cytochrome-P450. It has been suggested that alpha- and beta-amyrins cause a dimunition in oxidative stress and toxic metabolite formation leading to its hepatoprotective activity [96].

A mixture of alpha- and beta-amyrins, isolated from the resin of Protium kleinii and given by intraperitoneal (i.p.) or oral (p.o.) routes, dose-relatedly exhibited significant antinociception against visceral pain in mice produced by i.p. injection of acetic acid. Moreover, i.p., p.o., intracerebroventricular (i.c.v.) or intrathecal (i.t.) administration of alpha- and beta-amyrins inhibited both neurogenic and inflammatory phases of the overt nociception caused by intraplanar (i.p.l.) injection of formalin. alpha- and beta-Amyrins, similarly, when given by i.p., p.o., i.t., or i.c.v. routes inhibited the neurogenic nociception induced by capsaicin. I.P. treatment with alpha- and beta-amyrins reduced the nociception produced by 8-bromo-cAMP (8-Br-cAMP) and by 12-O-tetradecanoylphorbol-13-acetate (TPA) or the hyperalgesia caused by glutamate. The i.p. administration of alpha- and beta-amyrins reduced the mechanical hyperalgesia produced by i.p.l. injection of carrageenan, capsaicin, bradykinin, substance P, prostaglandin E2, 8-Br-cAMP, and TPA in rats. It has been concluded that the mixture of alpha- and beta-amyrins produced consistent peripheral, spinal, and supraspinal antinociception in rodents, especially in inflammatory models of pain and this seems to involve inhibition of protein kinase a (PKA)- and protein kinase C (PKC)-sensitive pathways [103]. The triterpinic mixture of [alpha] and [beta]-amyrins, isolated from Protium heptaphyllum resin also has been observed to suppress capsiacin-evoked nociception in mice, when administered orally at doses of 3-100 mg/kg body weight. The authors concluded from their studies that the mixture of [alpha]- and [beta]-amyrins had an analgesia-inducing effect, possibly involving vanilloid receptor (TRPV1) and an opioid mechanism [97]. However, in a further study it has been concluded that alpha- and beta-amyrin-attenuation of cyclophosphamide-induced bladder pain in mice or intracolonic mustard oil-induced nociceptive behaviors possibly involved opioid and TRPV1 receptor mechanisms [75].

Amyrins and ursolic acid and their synthesized lipophilic 3-O-fatty acid ester chains (C12-C18)- the major metabolites from the plant Diopsyros melanoxylon exhibited potent activity against the Gram negative bacteria, Pseudomonas syringae (ATCC #13457) and fairly good activity against the Gram positive bacteria, Bacillus sphaericus (ATCC #14577) and Bacillus subtilis (ATCC #6051) [81].

Bruguierin A, brugierol and isobrugierol inhibited phorbol ester-induced NFkappaB luciferase activation with [IC.sub.50] values of 1.4, 85 and 14.5 microM, respectively [52,53].

Bruguierin and brugierol selectively inhibited cyclooxygenase-2 (COX-2) activity with [IC.sub.50] value of 0.37 and 6.1 microM, respectively [52,53].

With stably-transfected HepG2 cells, bruguierin A-C, bruguiesulfurol, brugierol and isobrugierol activated antioxidant response element (ARE) luciferase activation with ([EC.sub.50]) values of 7.8, 9.4, 15.7, 56.7, 3.7 and 1.8 microM, respectively [52,53].

Bruguierols C showed moderate activity against gram-positive and gram-negative bacteria including mycobacteria and resistant strains (MICs 12.5 microg/mL) [50].

There is a recent patent regarding the invention, which provides 78 novel Bruguiera gymnorrhiza-derived gene fragments capable of furnishing salt tolerance to plants at a cellular level. These genes can improve salt tolerance of plants by themselves, and therefore, can easily confer the trait of salt tolerance to plant species [62].

Gibberellins (chemically diterpenoids), some of which have been isolated from B. gymnorrhiza, are quite well-known phytohormones regulating many aspects of plant physiology such as stimulating growth in stem and leaves, triggering germination of seeds, breaking the bud dormancy, sex expression, delaying senescence, vernalization and last but not the least, stimulating fruit production along with auxin. GA3 (also known as Gibberellic acid) is the most prominent of all members [Plant physiology online: http://3e.plantphys.net/chapter.php?ch=20].

Steviol (13-hydroxy-ent-kaurenoic acid) is the metabolic aglycone product of stevioside, a common constituent in the plant Stevia rebaudiana. Stevioside is commonly used as a noncaloric sugar substitute in Japan and Brazil. Since steviol and not stevioside, has been reported from Bruguiera gymnorhiza, this review shall deal exclusively with steviol. In rat models, steviol absorption is rapid, a peak plasma concentration can be observed within 15 min of oral administration of steviol. Oxidative metabolites of steviol (monohydroxy and dihydroxy) have been observed in following incibation of steviol with both rat and human liver microsomes [66].

Application of steviol to mouse skin 1h before or after application of TPA reportedly resulted in considerable reduction in the induction of ornithine decarboxylase (ODC) activity [94]. On the other hand, steviol was found to be highly mutagenic when evaluated in the presence of a 9000 X g supernatant fraction derived from the livers of Aroclor 1254-pretreated rats. The expression of mutagenic activity was also dependent on addition of NADPH [107]. Other studies have confirmed that steviol is mutagenic toward Salmonella typhimurium strain TM677 in the presence of a metabolic activating system derived from the liver of Aroclor 1254-pretreated rats. The required activating component was found to be localized in the microsomal fraction of rat liver, suggesting a cytochrome P-450-mediated reaction. The 13-hydroxy group of steviol was required for the expression of mutagenicity [108,134]. Steviol proved to be non-mutagenic in reverse mutation assays (Ames test) using Salmonella typhimurium TA100, TA98, TA102 and TA97 [84]. The genetic toxicity of steviol has further been assessed with seven mutagenicity tests using bacteria (reverse mutation assay, forward mutation assay, umu test and rec assay), cultured mammalian cells (chromosomal aberration test and gene mutation assay) and mice (micronucleus test). Steviol produced dose-related positive responses in some mutagenicity tests like the forward mutation assay using Salmonella typhimurium TM677, the chromosomal aberration test using Chinese hamster lung fibroblast cell line (CHL) and the gene mutation assay using CHL. Metabolic activation systems containing 9000g supernatant fraction (S9) of liver homogenates prepared from polychlorinated biphenyl or phenobarbital plus 5,6-benzoflavonepretreated rats were required for mutagenesis and clastogenesis. Steviol was weakly positive in the umu test using Salmonella typhimurium TA1535/pSK1002 with or without the metabolic system and was negative in other assays (even in the presence of the S9 activation system) using Salmonella typhimurium TA97, TA98, TA100, TA102, TA104, TA1535, TA1537 and Escherichia coli WP2 uvrA/pKM101 and the rec-assay using Bacillus subtilis and in the mouse micronucleus test [85]. Using Salmonella typhimurium tester strains TA98 and TA100, either in the presence or absence of metabolic activating system derived from sodium phenobarbital and 5,6-benzoflavone pretreated liver S9 fractions from rat, mouse, hamster and guinea pig, steviol, at concentrations up to 2 mg per plate demonstrated no mutagenic effects [64]. Steviol, even at a dose of 4g/kg body weight for hamsters and 8g/kg body weight for rats and mice did not show any effect on the frequencies of micronucleus formation in bone marrow erythrocytes of both male and female animals. However, at the given doses, steviol caused significant reduction of polychromatic erythrocytes: normochromatic erythrocytes (PCE:NCE) ratio of female hamsters at 72h, and rats and mice at 48 and 72h [133].

Steviol did not show any genotoxicity at doses of 62.5, 125, 250 and 500 microg/ml, i.e. did not damage nuclear DNA of TK6 and WTK1 cells in the presence and absence of S9 mix. Mice, sacrificed after 3 and 24h following oral administration of steviol at 250, 500, 1000 and 2000 mg/kg did not demonstrate any damage to DNA of stomach, colon, liver, kidney and testis. In vivo studies using the comet assay also demonstrated that mice sacrificed 3 and 24h following oral administration of steviol at the above-mentioned doses did not have any stomach, colon and liver DNA damages [118].

In rat renal cortical tubules, steviol was found to decrease glucose production and inhibited oxygen uptake [150]. In vitro experiments with hamster jejunum showed inhibition of glucose absorption by steviol with the site of inhibitory action at the mucosal side and/or at the intracellular organelles of intestinal absorptive cells [138]. A further study concluded that steviol-induced inhibition of glucose absorption in hamster jejunum is due to the reduction in mucosal ATP and an alteration of the morphology of the intestinal absorptive cells [139].

The acute toxicity of steviol has been studied in hamster, rat and mouse. When animals were treated intragastrically with steviol, hamsters showed greater susceptibility than rats or mice ([LD.sub.50] values for male and female hamsters were, respectively 5.2 and 6.1g/kg body weight versus higher than 15g/kg body weight in both sexes of rats and mice). Histopathological examination of hamster kidneys revealed severe degeneration of the proximal tubular cells, along with an increase in serum blood urea nitrogen and creatinine, suggesting that acute renal failure is the cause of hamster mortality [140]. In isolated rabbit renal proximal tubules, steviol inhibited transepithelial transport of para-aminohippurate (PAH) by interfering with organic anion transport system. In S2 cells expressing human organic anion transporters (OATs), substrate uptake was inhibited in all S2hOAT cells and steviol had low [IC.sub.50] for both hOAT1 and hOAT3, suggesting that the inhibition of OAT-mediated transport by steviol could alter renal drug clearance. In mouse renal cortical slices, steviol was a potent inhibitor of PAH and estrone sulfate (ES) transport [124].

Steviol at doses of 0.75 and 1g/kg body weight/day, when intubated into pregnant hamsters were highly toxic to both dams and fetuses. There was a decrease in maternal body weight and increase in maternal mortality. The number of live fetuses per litter and mean fetal weight also significantly decreased in the steviol-treated animals. However, there was no maternal toxicity or embryotoxicity of steviol at an oral dose of 0.25g/kg body weight/day [144].

The bioactive profile of lupeol has been reviewed previously [38], in which review the anticancer, antprotozoal, anti-inflammatory, and chempreventive effects of the compounds have been emphasized. Recent reports on lupeol have been given in an accompanying paper on another mangrove species plant, Barringtonia racemosa. In this review, the antidiabetic, anti-inflammatory, and analgesic effects of lupeol will be discussed briefly.

The antidiabetic effect of Sambucus nigra L. and its ethnomedicinal use as an antidiabetic plant has been known for long. Aqueous extract of the plant has been shown to exhibit insulin-like and insulin-releasing actions in vitro, which effects have been attributed to presence of lupeol and beta-sitosterol, among other constituents, in the extract [42]. Notably, both compounds are present in Bruguiera gymnorrhiza, marking the plant as a potential agent for antidiabetic use. The methanolic extract of Tournefortia hartwegiana Steud. has been reported to show alpha-glucosidase inhibitory activity; lupeol and beta-sitosterol has been identified in the extract [102]. Lupeol and beta-sitosterol has also been identified as possible bioactive components in ethanolic extract of the roots of Rhizophora apiculata Blume, which reportedly showed antihyperglycemic activity in streptozotocin-induced diabetic rat models [70].

Inhibition of protein tyrosine phosphatase 1B can play a beneficial role in Type 2 diabetic patients. The methanol extract of stem barks of Sorbus commixta Hedl. Has been shown to exhibit strong protein tyrosine phosphatase 1B inhibitory activity; lupeol and lupenone has been isolated from the extract [90]. Lupeol has been shown as one of the constituent in root bark of Euclea undulata Thunb. var. myrtina, which showed hypoglycemic activity [33]. Aqueous and ethanolic extracts of Moringa peregrina (Forssk.) Fiori. has been shown to exhibit potent antihyperglycemic activity in rats; lupeol acetate, beta-sitosterol, alpha-amyrin, and beta-amyrin were present in the fractions [36]. Lupeol, isolated from Solanum xanthocarpum Schrad and Wendl., reportedly suppressed the progression of diabetes in experimental hyperglycemia, as manifested by decrease in glycated hemoglobin, serum glucose and nitric oxide, levels of thiobarbituric caid-reactive oxygen species, and increases in serum insulin levels [46].

The hypoglycemic and beta-cells regenerative effects of Aegle marmelos (L.) Corr. bark extract have been demonstrated in streptozotocin-induced diabetic rats. Lupeol has been identified as one of the bioactive constituents behind the observed antidiabetic effect [39]. The stem bark extract of Cenostigma macrophyllum Tul. var. acuminata Teles Freire reportedly attenuated tactile allodynia in streptozotocin-induced diabetic rats [109]. Thus lupeol (a component of the stem bark), besides, antidiabetic properties, has also been shown to exert antinociceptive effects.

Lupeol has been implicated as at least one of the bioactive constituents in various plants extracts exerting anti-inflammatory and analgesic effects. Some of these include anti-inflammatory activity of Calendula officinalis L. flowers [28]; anti-inflammatory and analgesic activities of latex of Himatanthus sucuuba (Spruce ex Mull.Arg.) Woodson [29]; anti-inflammatory effect of Pimenta racemosa var. ozua (Urb. & Ekman) Landrum [37]; analgesic activity of Miconia rubiginosa (Bonpl.) DC. extract [123]; anti-inflammatory and analgesic effects of extracts from Zanthoxylum riedelianum Engl. leaves and stem bark [74]; antinociceptive properties of Matayba elaeagnoides Radlk. bark [31]; anti-inflammatory activity of stem bark of Allanblackia monticola Staner L.C. [91]; analgesic and anti-inflammatory effects of Cassia siamea stem bark extracts [93]; antinociceptive effect of Zanthoxylum rhoifolium Lam. in models of acute pain in rodents [105]; anti-inflammatory effect of Himatanthus drasticus (Mart.) Plumel [79]; anti-inflammatory properties of Ligustrum species (Ligustrum lucidum Ait., Ligustrum pricei Hayata and Ligustrum sinensis Lour.) leaves [146]; anti-inflammatory and analgesic property of Ligustrum morrisonense Kaneh. & Sasaki leaves in rodents [147]; anti-inflammatory effect of stem bark of Pterodon emarginatus Vogel [30]; anti-inflammatory activity of Pueraria lobata (Willd.) Ohwi roots [60]; and analgesic and anti-inflammatory activities of Cissus repens in mice [19].

The antidiabetic effect of beta-sitosterol and stigmasterol, two compounds present in Bruguiera gymnorrhiza, has been reported. Beta-sitosterol-3-beta-D-glucoside and beta-sitosterol has been shown to have insulin-secretion effect in vivo and in vitro models [57,58]. The antidiabetic and antioxidant potential of beta-sitosterol has also been demonstrated in streptozotocin-induced experimental hyperglycemia [45]. The hypoglycemic effect of stigmasterol isolated from Butea monosperma has also been demonstrated [104].

Drug discovery potential:

Bruguierin A can provide a scaffold for developing novel cancer chemopreventive drug. Lupeol and beta-sitosterol can prove as novel antidiabetic and anticancer agents.

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Sk. Mizanur Rahman, Md. Zahirul Kabir, Prashanta Kumer Paul, Md. Rashedul Islam, Shahnaz Rahman, Rownak Jahan, Mohammed Rahmatullah

Faculty of Life Sciences, University of Development Alternative, Dhanmondi, Dhaka-1209, Bangladesh.

Received: November 03, 2013; Revised: January 13, 2014; Accepted: January 16, 2014

Corresponding Author: Dr. Mohammed Rahmatullah, Pro-Vice Chancellor University of Development Alternative House No. 78, Road No. 11A (new) Dhanmondi R/A, Dhaka-1209 Bangladesh Phone: 88-01715032621; Fax: 88-02-8157339; E-mail: rahamatm@hotmail.com
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Title Annotation:Research Article
Author:Rahman, Mizanur; Kabir, Zahirul; Paul, Prashanta Kumer; Islam, Rashedul; Rahman, Shahnaz; Jahan, Row
Publication:American-Eurasian Journal of Sustainable Agriculture
Article Type:Report
Geographic Code:9BANG
Date:Dec 1, 2013
Words:10554
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