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Natural Product Communications

EDITOR-IN-CHIEF DR. PAWAN K AGRAWAL Natural Product Inc. 7963, Anderson Park Lane, Westerville, Ohio 43081, USA

[email protected] EDITORS PROFESSOR ALEJANDRO F. BARRERO Department of Organic Chemistry, University of Granada, Campus de Fuente Nueva, s/n, 18071, Granada, Spain [email protected] PROFESSOR ALESSANDRA BRACA Dipartimento di Chimica Bioorganicae Biofarmacia, Universita di Pisa, via Bonanno 33, 56126 Pisa, Italy [email protected] PROFESSOR DEAN GUO State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking University, Beijing 100083, China [email protected] PROFESSOR YOSHIHIRO MIMAKI School of Pharmacy, Tokyo University of Pharmacy and Life Sciences, Horinouchi 1432-1, Hachioji, Tokyo 192-0392, Japan [email protected] PROFESSOR STEPHEN G. PYNE Department of Chemistry University of Wollongong Wollongong, New South Wales, 2522, Australia [email protected] PROFESSOR MANFRED G. REINECKE Department of Chemistry, Texas Christian University, Forts Worth, TX 76129, USA [email protected] PROFESSOR WILLIAM N. SETZER Department of Chemistry The University of Alabama in Huntsville Huntsville, AL 35809, USA [email protected] PROFESSOR YASUHIRO TEZUKA Institute of Natural Medicine Institute of Natural Medicine, University of Toyama, 2630-Sugitani, Toyama 930-0194, Japan [email protected] PROFESSOR DAVID E. THURSTON Department of Pharmaceutical and Biological Chemistry, The School of Pharmacy, University of London, 29-39 Brunswick Square, London WC1N 1AX, UK [email protected]

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Prof. Karsten Krohn Paderborn, Germany Prof. Chiaki Kuroda Tokyo, Japan Prof. Hartmut Laatsch Gottingen, Germany Prof. Marie Lacaille-Dubois Dijon, France Prof. Shoei-Sheng Lee Taipei, Taiwan Prof. Francisco Macias Cadiz, Spain Prof. Imre Mathe Szeged, Hungary Prof. Ermino Murano Trieste, Italy Prof. M. Soledade C. Pedras Saskatoon, Canada Prof. Luc Pieters Antwerp, Belgium Prof. Peter Proksch Düsseldorf, Germany Prof. Phila Raharivelomanana Tahiti, French Polynesia Prof. Luca Rastrelli Fisciano, Italy Prof. Monique Simmonds Richmond, UK Dr. Bikram Singh Palampur, India Prof. John L. Sorensen Manitoba, Canada Prof. Valentin Stonik Vladivostok, Russia Prof. Winston F. Tinto Barbados, West Indies Prof. Sylvia Urban Melbourne, Australia Prof. Karen Valant-Vetschera Vienna, Austria

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NPC

Natural Product Communications

Natural Products from Marine Algae of the Genus Osmundaria (Rhodophyceae, Ceramiales)

2013 Vol. 8 No. 4 533 - 538

Kelvin Osakoa and Valéria Laneuville Teixeiraa,b a

Programa de Pós-Graduação em Ciências e Biotecnologia, Instituto de Biologia, Universidade Federal Fluminense, Niterói/Rio de Janeiro, Brazil 24210-130 b Departamento de Biologia Marinha, Instituto de Biologia, Universidade Federal Fluminense, Niterói/Rio de Janeiro, Brazil, 24001-970 [email protected] Received: February 10th, 2013; Accepted: March 1st, 2013

The present work is a review of the natural products isolated from red marine algae of the genus Osmundaria (including Vidalia), which intends to encompass their occurrence in the species of this genus, the possible synonymies, their geographic distribution, their structural variety and their biological potential as prototypes for the pharmaceutical industry and as active principles of cosmetics. At the end, we provide a table with these natural products and their biological activities. Keywords: Seaweed, Rhodophyceae, Osmundaria, Marine red algae, Natural products, Biological activities.

Natural products represent the greatest source of chemical diversity and have been lead compounds in pharmacological studies since the past century [1]. These products and their semisynthetic derivatives have provided a unique source of therapeutic agents used in the treatment of infectious diseases [2]. In addition, their use as food additives and in the production of toiletries has been widely discussed since their effectiveness and the risks they may represent to human health are being evaluated [3-5]. With regard to natural products, numerous compounds with biological activity have been isolated from marine organisms, such as sponges, corals, echinoderms, tunicates, bacteria and fungi [3, 6]. The main motivation of studies involving marine natural products is their antibacterial, anticoagulant, antifungal, anti-inflammatory, antimalarial and antiviral action [7]. Some of these products are already in various stages of clinical study, for example, bryostatin, an anticancer substance isolated initially from the bryozoan Bugula neritina [8]. Several substances on the other hand are currently commercialized, such as Yondelis®, with anticancer action, isolated from a tunicate; Prialt®, which has analgesic activity and is isolated from a mollusc; and two substances isolated from sponges, ViraA®, an antiviral product, and Cytosar-U, an anticancer agent [9]. The macroalgae are rich in fibers, proteins, minerals, vitamins, antioxidants, phytochemicals and low calorie polyunsaturated fatty acids [10]. Moreover, some natural marine products are utilized in the food industry as additives due to their gelling and thickening properties, such as carrageenan, for instance. It is important to mention the ulvans present in Chlorophyceae, and alginates, laminarins and fucans present in Phaeophyceae [11]. Marine algae, notably Rhodophyceae, are the most abundant source of sulfated polysaccharides consisting of carrageenans and agarans. Not only are these polysaccharides known for their rheological properties, but also for other biological activities, such as anticoagulant, antiviral, anticancer and immunomodulatory [12]. A variety of compounds, mainly bromophenols, has been reported for the algal genus Osmundaria [13].

The genus Osmundaria J.V. Lamouroux (Order Ceramiales, family Rhodomelaceae), known for occurring only in the southern region of the Australian coast, has been studied in relation to its possible taxonomic synonymy with the genus Vidalia J.V. Lamouroux ex J. Agardh (Order Ceramiales, Family Rhodomelaceae), established by Norris in 1991 [14]. The majority of authors do not accept the separation of the two genera, considering all the former species of Vidalia as belonging to Osmundaria. However, several articles published after this study continued to use Vidalia, a wellestablished generic name in phycology [15-31]. There are 13 species of Osmundaria cited in the literature, although only 9 are currently accepted [32]. Based on the reproductive structures of the algae, Norris [14] suggested that O. fimbriata (Lamouroux) R.E. Norris, O. obtusiloba (C. Agardh) R.E. Norris, O. volubilis (Linnaeus) R.E. Norris, O. oliveae R.E. Norris and O. prolifera J. V. Lamouroux (type species) be considered the most primitive, followed by O. papenfussii R.E. Norris, O. serrata (Suhr) R.E. Norris, O. melvillii (J. Agardh) R.E. Norris, O. spiralis var. cliftonii (Harvey) R.E. Norris and, finally, O. colensoi (J.D. Hooker & Harvey) R.E. Norris, the most advanced in terms of reproductive character. O. intermedia (J. Agardh) De Toni (taxonomic synonym of O. prolifera), O. smithiae (Hooker & Harvey) Kuntze (taxonomic synonym of Epiglossum smithiae) and O. spiralis (Lamouroux) R.E. Norris were omitted from this list. In accordance with the hypothesis formulated by Norris [14], the present review will follow this order to present the natural products of this genus. Osmundaria fimbriata The motivation for the first studies came when researchers found stalks of O. fimbriata free from epiphytes that colonize other algae in the region of the Antarctic Peninsula [33], which led to the isolation of some acetoxyfimbrolides. These compounds, found in the dichloromethane extract of the lyophilized alga collected near Sydney, presented antimicrobial and antifungal activity [34]. As well as acetoxyfimbrolides, the same authors isolated other halogenated lactones and defined their names according to their polarity in ascending order: fimbrolides (e.g. 1),

534 Natural Product Communications Vol. 8 (4) 2013

hydroxyfimbrolides (e.g. 2), and acetoxyfimbrolides (e.g. 3) [34]. Later, the first syntheses of fimbrolides [35] and other halogenated ketones with antifungal activity were achieved [36]. R

Br H

O

O

Br

R H OH OAc

1 2 3

R1 OH OH OAc OAc OAc OAc

4 5 6 7 8 9 R1

O

R2 CH2I OCH3 CH3 OCH3 CHBr2 OCH3

R3 OCH3 CH2I OCH3 CH3 OCH3 CHBr2

Br R2

O

R3

10 11 12 13 14 15 16

R1 H H OH OH OAc OAc OH

R2 Br H H Br H Br H

R3 Br Br Br H Br H I

17 18 19 20 21 22

R1 OH OAc OH OAc OH OH

R2 I H Br Br H Cl

Osako & Teixeira

to the size of population of bacteria [39], such as Escherichia coli [3] and Pseudomonas aeruginosa [40]. The furanone, N-acetyl-γhydroxyvaline (30), isolated from a streptomycete found in marine sediment from Brazil [41], has also been studied for its role in quorum sensing. When analyzing sterols present in V. fimbriata collected in Inhaca Island, Mozambique, it was possible to observe that C27 sterols were predominant. Cholesterol and 22dehydrocholesterol were, respectively, the major and minor components [42]. Osmundaria obtusiloba The first report concerning isolated compounds from O. obtusiloba came in 1991 [42] when the bromophenols vidalol A (31) and B (32), with anti-inflammatory activity, were isolated from the alga collected in the Caribbean Sea. One of the hypotheses for the mechanism of action of their anti-inflammatory activity is the inhibition of the enzyme phospholipase A2 in the arachidonic acid metabolic pathway [16, 22, 43].

R3 H I Br Br Cl H 31

New polyhalogenated furanones were isolated from O. fimbriata (as Delisea pulchra) collected in Cape Banks, New South Wales, in Australia. They were then structurally elucidated by spectroscopic (1D- and 2D-NMR, UV, and IR) and mass spectrometric data [38]. The halogenated lactones previously isolated [33-34, 36] were found again and for the first time complete ¹H and ¹³C NMR data were reported for several of these compounds (4-22).

OH O N H 33

In 1997, the isolation of compounds 23-26 from O. fimbriata (as D. fimbriata) collected in South Shetland, Antarctica, was performed [38].This isolation was considered unprecedented because, since then, only halogenated ketones have been isolated [33-34, 26-37]. Moreover, the isolated compounds have shown biogenetic potential [38] given that the authors considered compound 27 the probable precursor of the majority of the metabolites with a skeleton of eight carbon atoms from members of the Bonnemaisoniaceae family. Nonetheless, new studies of the alga, currently known as O. fimbriata and a member of the Rhodomelaceae family [32], are necessary, in order to evaluate the hypothesis suggested by Cueto and collaborators [38].

23 R =H 24 R = OH

28

25 R = H 26 R = Cl

29

27

30

In reviews of organobromide compounds produced naturally [17], and on volatile halogenated metabolites produced by marine red algae [19], the authors listed the compounds isolated from the algae D. pulchra and D. fimbriata (28-29). A good portion of these compounds has been studied because of their action as blockers of bacterial quorum sensing [39]. Quorum sensing is a process that consists of the control of the expression of target genes in response

32

OH O

34

35

36

37

38 R=Me; R1=H 38a R=R1= H 38b R=R1=Me

39

In 1996, during an investigation of neuroexcitatory amino acids in 46 species of marine algae occurring in islands of south-eastern Japan, kainic acid and domoic acid were found in O. obtusiloba [28]. Other marine algae and freshwater cyanobacteria also produce domoic acid [44]. Domoic acid (33) and kainic acid (34) are analogues and may contaminate an entire trophic chain [44]. In 1987, in Canada, the first episode of poisoning by domoic acid in humans happened and the clinical condition was known as Amnesia Shellfish Poisoning [21]. Additionally, domoic acid may go through a pregnant women’s placenta, damaging the development of the foetus, and causing temporal lobe epilepsy [44].

Natural products from red marine algae of the genus Osmundaria

Carvalho & Roque published a review on the halogenated and/or sulfated phenols found in marine macroalgae, including O. obtusiloba. On the other hand, seven substances were identified in Brazilian O. obtusiloba [16a,16b], three sulfated bromophenols (35-37), four bromophenols (31-32, 38-39), one sterol and one glyceride. In 2012 [46], the structure of the sulfoquinovosyldiacylglycerol isolated from a specimen collected in Rio de Janeiro, Brazil, was characterized for the first time. Glycolipids mono- and digalactosyldiacylglycerol were also found in the alga and characterized. The use of this alga as food was studied by Ramos and colleagues [26], in which the protein content (18 ± 1.7%), the dry weight (23.4 ± 2.0%), the composition, and the ratio of amino acids of the alga collected from the coast of Ceará, north-eastern Brazil were evaluated. Methionine was the primary limiting amino acid for the majority of the species studied, including O. obtusiloba. In addition, the alga is rich in phenylalanine/tyrosine, when compared with other algae. In another study on the nutritive and non-nutritive composition of a miscellany of algae from Ceará, Brazil, including O. obtusiloba [24], lectins and other toxic compounds that inhibit trypsin and αamylase were found. Also, a lectin from a specimen collected from the coast of Ceará, Brazil, was purified and partially characterized [23]. The authors observed a predominance of Asp/Asn, Glu/Gln and Leu, which corresponds to the amino acid composition encountered by Ramos and collaborators [26]. Extracts from 4 marine algae collected in Rio de Janeiro, Brazil, were analyzed to determine their inhibitory effect on the formation of HTLV-1-induced syncytium [27]. At a concentration of 5% of O. obtusiloba, it was possible to observe a 76% inhibition, which is lower than the inhibition rates of extracts of Ulva fasciata, Sargassum vulgare and Laminaria abyssalis at the same concentration. The last of these species presented 100% inhibition at a concentration of 2.5%. However, it was clear that the extract of O. obtusiloba presented significant antiviral activity. The antiviral activity and cytotoxicity of acetone and methanol extracts were investigated in Vero cells (cells from African green monkey) [46]. The glycolipids of O. obtusiloba collected in Rio de Janeiro, Brazil, presented potent antiviral activity against HSV-1ACVs (Herpes Simplex Type 1 Acyclovir-sensitive virus) and HSV-1-ACVr (Herpes Simplex Type 1 Acyclovir-resistant). At the maximum non-toxic concentrations of the extract in acetone (50 µg/mL) and methanol (100µg/mL), the inhibition rates were respectively 82.2% and 99.5% against HSV-1-ACVs, and 99.7% and 99.9% against HSV-1-ACVr. It was thought by then that the active glycolipids responsible for the antiviral activity were sulfoglycolipids and glycosyldiacylglycerols [6, 46]. Later, the fraction of sulfoglycolipids from O. obtusiloba was purified and its antiviral activity tested against HSV-1 (Herpes Simplex Virus type 1) and HSV-2 (Herpes Simplex Virus type 2). Inhibition of 75% and 96% was achieved by the purified fraction against HSV-1 and HSV-2, respectively. The authors [45] attributed this reduction of antiviral activity in relation to HSV-1 to the absence of other polar lipids in the purified fraction, such as glycoglycerolipids, which may have a synergistic effect. The cytotoxicity was also tested in Vero cells and the maximum nontoxic concentration was 50 µg/mL. The antifouling activity of the crude extract of the alga collected in Rio de Janeiro, Brazil, was tested against the mollusc Perna perna

Natural Product Communications Vol. 8 (4) 2013 535

[47]. When algae had suffered previous damage by herbivory, their extracts presented approximately 10% inhibitory action. However, the extracts of the algae that had not suffered damage did not present antifouling activity. A study on the difference in biomass of algae according to the variation in depth (10, 15 and 20 m) in rhodolith beds was conducted in north-eastern Brazil [48]. The greatest biomass observed for O. obtusiloba was at 15 m depth, with 3.08 ± 1.11g/0.25m², the second greatest observed of the 66 species studied, 37 of them Rhodophyceae. The general conclusion was that the number of species and abundance of macroalgae diminish as depth increases and transparency decreases. Osmundaria volubilis Contrary to the theory that red algae do not perform C24 alkylation [49], O. volubilis collected mostly in the region of Sicily [25, 32, 50-51] presented 24-methylenecholesterol as the main sterol [50]. A study of the composition of fatty acids in the trophic ecology of the sea urchin Spatangus purpureus in the Balearic Islands, western Mediterranean [52], measured the composition of fatty acids present in O. volubilis. High levels of polyunsaturated fatty acids, such as docasahexaenoic acid (DHA, C22:6n-3), were found, which is indicative of quality food. However, since the most well-known source of this acid is animal, the authors attribute its presence to epiphyte organisms of the algal fauna [52]. Two Dragendorff-positive compounds, N,N,N-trimethyltaurine and 4-dimethylsulfonio-2-methoxybutyrate, were isolated and may be used as indicators in taxonomic studies [51]. (-)-(S)-4Dimethylsulfonio-2-methoxybutanoate (DMMB), (+)-(S)-Nmethylaspartic acid (MAsp) and a betaine, 2-amino-5trimethylammoniopentanoate (ATMP), were isolated as well [25]. Similar to N,N,N-trimethyltaurine and 4-dimethylsulphonio-2methoxybutyrate, it was shown that they had an important role in the biosynthesis of methylated metabolites of marine algae [25, 51]. The alga presented other sulfated substances, for instance 1’,4potassium disulfate, 2,3-dibromo-1,4,5-trihydroxybenzyl and 2,3dibromo-5-hydroxybenzyl-1’,4-disulfate [15a]. It is important to highlight that the last of these presented activity in vitro at 400 ppm against strains of Proteus, Klebsiella pneumoniae, Streptococcus pyogenes, Pasteurella and Salmonella typhimurium [19]. Osmundaria prolifera As in the case of O. fimbriata, C27 sterols predominate in O. prolifera. Cholesterol and 22-dehydrocholesterol are, respectively, its major and minor compounds [42]. The authors concluded that the sterols present in this alga could not be used as taxonomic markers because of their heterogeneity. Indeed, O. prolifera has been collected as O. prolifera in Venus Bay, South Australia, and as V. gregaria in Eucla, Western Australia [42]. Osmundaria serrata Studies on the growth of fungi and marine and terrestrial bacteria have shown that the crude extract of O. serrata presents good antimicrobial activity, indicating the presence of an active compound [53]. The extract provoked deformities and altered the production of chlamydospores of the fungi Verticillium sp. and Rhizoctonia solani [53]. In addition, extracts of algae collected from Palm and Trafalgar Beaches, KwaZulu-Natal, South Africa, were tested against terrestrial and marine bacteria, as well as against fungi of medical and/or economic importance. These studies also


led to the first isolation of lanosol ethyl ether (40) from O. serrata. The results indicated that this compound is more effective as a bacteriostatic and fungistatic, with minimum inhibitory concentrations (MIC) of 0.27 ± 0.07 mg mL-1 , than as a bactericide and fungicide, with MIC values of 0.69 ± 0.15 mg mL-1 [16,22,5354].

40

41

42

CH2 OH

Br HO 44

upper limit of susceptibility to enzymatic digestion [60]. Its nutritional composition was also analyzed [59]. A study was made of the population of the mollusc Perna canaliculus in the north of New Zealand associated with the colonization of O. colensoi, as well as other Rhodophyceae, such as Plocamium costatum and Corallina officinalis [61]. Perna canaliculus is the basis of a US$150 million economy in New Zealand [62]. An obstacle to the expansion of this industry is the low occurrence of natural seed necessary for the growth of P. canaliculus [63]. However, it was shown that the apolar extract of O. colensoi caused an increase in the colonization of the mollusc, while the polar extract reduced it. This study also evaluated the significance of the type of substratum to which the molluscs are attached and studied the effect of natural products on it. The conclusion was that hilly surfaces facilitate colonization more than flat ones regardless of the presence of extracts [63]. Table 1: Natural products isolated from Osmundaria species, with their biological activities.

Br OH

43

Osako & Teixeira

45

Except for old parts, biofilm coverage was observed over the entire alga, including meristematic regions [53]. Afterwards, the authors treated samples of O. serrata with osmium tetroxide (OsO4) in order to evaluate if this treatment, followed by fixation in glutaraldehyde, could preserve the biofilm [55]. This hypothesis was confirmed with the observation of stabilized lipids in the extracellular polymeric substance of the biofilm, indicating that these lipids may have a role in the cohesion and integrity of the biofilm. Vidalia spiralis 3,4-Dibromo-5-methylenecyclopent-3-ene-1,2-diol (41) was isolated from specimens of Vidalia spiralis collected in Western Australia [17, 19, 56]. Although the crude extract of the alga in dichloromethane has shown hypotensive activity, and the extract in methanol, a stimulating activity on the central nervous system, the previously unpublished dibromodihydrofulvene is not responsible for the hypotensive activity of the crude extract [56]. Osmundaria colensoi The kinetics of assimilation of ammonium was investigated using O. colensoi collected in north eastern New Zealand, along with the green alga Enteromorpha sp. [57]. The utilization of ammonium by marine algae comprises three essential components: capture of ammonium amino acids in the environment, assimilation of the ammonium present in amino acids, and incorporation of amino acids in proteins and other macromolecules [58]. O. colensoi and Enteromorpha sp. presented Michaelis-Menten assimilation kinetics, a model originally designed to measure enzymatic activity rates with maximum assimilation rates (Vmax) of 12 and 27 µmol.(g dry weight)-1.hour-1 and a Michaelis constant (Km) of 41 and 18 µM, respectively [57]. Although not considered part of the fish diet in New Zealand [59], the lysis of algal cells caused by gastric acids observed in the digestion of herbivorous marine fish was investigated. O. colensoi collected from the north-eastern coast of New Zealand was included [60]. Spectrophotometric analyses showed peaks of absorbance for O. colensoi at 230 nm and 287 nm. Effects caused by reduction in pH during enzymatic hydrolysis of starch were not observed. The authors concluded that the differences in effects caused by pH are related to the algal morphology: the more delicate, the greater the

Product colensolide A domoic acid kainic acid lanosol

Alga (References) O. colensoi [13] O. obtusiloba [28] O. obtusiloba [28] O. serrata; O. colensoi; O. obtusiloba; O. sp. [13, 15, 31, 53]

lanosol 1,4-disulfate

O. serrata [53]

lanosol ethyl ether

O. serrata [55]

lectin

O. colensoi, O. serrata [13,53] O. obtusiloba [23]

vidalol A

O. obtusiloba [43]

vidalol B

O. obtusiloba [43]

lanosol methyl ether

Biological activity Cytotoxic and bactericidal activity Neuroexcitatory activity Neuroexcitatory activity Cytotoxic; fungicidal and bactericidal activity; reduces herbivory against abalones Antimicrobial activity; reduction of herbivory against abalones Bacteriostatic and fungistatic activity; reduction of herbivory against abalones Antimicrobial activity;reduction of herbivory against abalones Hemagglutinating activity Reduces herbivory; bactericidal and anti-inflammatory activity Reduces herbivory; bactericidal and anti-inflammatory activity

In addition to the compounds isolated from other species of Osmundaria [15a, 53], the nitrogenated bromophenol colensolide A (42) was also obtained from the methanol extract of O. colensoi collected in New Zealand [13]. The anticancer activity of lanosol butenone (43) isolated from O. colensoi was investigated and presented cytotoxicity to human leukemia cells with an IC50 value of 8.0µM. The antimicrobial activity of this compound was also tested, along with lanosol methyl ether (44) and rhodomelol (45). All of them presented antibacterial activity against strain MC155 of Mycobacterium smegmatis with IC50 values of 7.8, 26.2 and 28.1µM for lanosol methyl ether (44), lanosol butenone (43) and rhodomelol (45), respectively [13, 22]. 2-O-Methyl-3,6-anhydro-α-L-galactopyranosyl, found in Bostrychia montagnei, a member of the Rhodomelaceae, was also found in O. colensoi. Nevertheless, the agarans of B. montagnei collected in the tropical Atlantic did not present the gelling properties of O. colensoi [64]. Table 1 present the natural products isolated from Osmundaria species and their biological activities. Osmundaria oliveae, O. papenfussii and O. melvillii These algae have no published work on their natural products. Acknowledgments - We are grateful to CAPES for providing a MSc fellowship and CNPq and FAPERJ for financial support and Productivity and Cientista do Nosso Estado Fellowship to VLT.

Natural products from red marine algae of the genus Osmundaria

Natural Product Communications Vol. 8 (4) 2013 537

References [1] [2] [3] [4] [5] [6] [7] [8] [9] [10] [11] [12] [13] [14] [15] [16] [17] [18] [19] [20] [21] [22] [23] [24] [25] [26] [27] [28] [29] [30] [31] [32] [33] [34] [35] [36] [37] [38]

Mishra BB, Tiwari VK. (2011) Natural products: An evolving role in future drug discovery. European Journal of Medicinal Chemistry, 46, 47694807. Roemer T, Xu D, Singh SB, Parish CA, Harris G, Wang H, Davies JE, Bills GF. (2011) Confronting the challenges of natural product-based antifungal discovery. Chemistry & Biology, 18, 148-164. Imhoff JF, Labes A, Wiese J. (2011) Bio-mining the microbial treasures of the ocean: New natural products. Biotechnology Advances, 29, 468-482. Nohynek G, Antigna E, Re T, Toutain H. (2010) Safety assessment of personal care products/cosmetics and their ingredients. Toxicology and Applied Pharmacology, 243, 239-259. Vivó-Sesé I, Pla MD. (2007) Bioactive ingredients in cosmetics. In Analysis of Cosmetic Products. Salvador A, Chisvert A. (Eds). Elsevier, Amsterdam, 380-389. Vo TS, Ngo DH, Ta QV, Kim SW. (2011) Marine organisms as a therapeutic source against herpes simplex virus infection. European Journal of Pharmaceutical Sciences, 44, 11-20. Mayer AMS, Rodríguez AD, Berlinck RGS, Fusetani N. (2011) Marine pharmacology in 2007-8: Marine compounds with antibacterial, anticoagulant, antifungal, anti-inflammatory, antimalarial, antiprotozoal, antituberculosis, and antiviral activities; affecting the immune and nervous system, and other miscellaneous mechanisms. Comparative Biochemistry and Physiology, Part C, 153, 191-222. Pettit GR, Tan R, Cichacz ZA. (1982) Isolation and structure of bryostatin-1. Journal of the American Chemical Society, 104, 6846–6848. Mayer AMS, Glaser KB, Cuevas C, Jacobs RS, Kem W, Little RD, McIntosh JM, Newman DJ, Potts BC, Shuster DE. (2010) The odyssey of marine pharmaceuticals: a current pipeline perspective. Trends in Pharmacological Sciences, 31, 255-265. Mohamed S, Hashim SN, Rahman HA. (2012) Seaweeds: A sustainable functional food for complementary and alternative therapy. Trends in Food Science & Technology, 23, 83-96. Jiao G, Yu G, Zhang J, Ewart HS. (2011) Chemical structures and bioactivities of sulfated polysaccharides from marine algae. Marine Drugs, 9, 196-223. Wijesekara I, Pangestuti R, Kim SK. (2011) Biological activities and potential health benefits of sulfated polysaccharides derived from marine algae. Carbohydrate Polymers, 84, 14-21. Popplewell WL, Northcote PT. (2009) Colensolide A: a new nitrogenous bromophenol from the New Zealand marine red alga Osmundaria colensoi. Tetrahedron Letters, 50, 6814-6817. Norris RE. (1991) The structure, reproduction and taxonomy of Vidalia and Osmundaria (Rhodophyta, Rhodomelaceae). Botanical Journal of the Linnean Society, 106, 1-40. Carvalho LR, Roque NF. (2000). Fenóis halogenados e/ou sulfatados de macroalgas marinhas. Quimica Nova, 23, 757-764. Carvalho LR, Guimarães SMPB, Roque NF. (2006) Sulphated bromophenols from Osmundaria obtusiloba (C. Adardh) R.E. Norris (Rhodophyta, Ceramiales). Revista Brasileira de Botanica, 29, 453-459. El Gamal AA. (2010) Biological importance of marine algae. Saudi Pharmaceutical Journal, 18, 1-25. Gribble GW. (2000) The natural production of organobromine compounds. Environmental Science and Pollution Research International, 7, 37-47. Guimaraens MA, Coutinho R. (1996) Spatial and temporal variation of benthic marine algae at the Cabo Frio upwelling region, Rio de Janeiro, Brazil. Aquatic Botany, 52, 283-299. Kladi M, Vagias C, Roussis V. (2004) Volatile halogenated metabolites from marine red algae. Phytochemistry Reviews, 3, 337-366. Klisch M, Häder DP. (2008) Mycosporine-like amino acids and marine toxins--the common and the different. Marine Drugs, 6, 147-163. Lefebvre KA, Robertson A. (2009) Domoic acid and human exposure risks: A review. Toxicon, 56, 218-230. Liu M, Hansen PE, Lin X. (2011) Bromophenols in marine algae and their bioactivities. Marine Drugs, 9, 1273-1292. Melo FR, Benevides NMB, Pereira MG, Holanda ML, Mendes FNP, Oliveira SRM, Freitas ALP, Silva LMCM. (2004) Purification and partial characterisation of a lectin from the red marine alga Vidalia obtusiloba C. Agardh. Revista Brasileira de Botânica, 27, 263-269. Oliveira MN, Freitas ALP, Carvalho AFU, Sampaio TMT, Farias DF, Teixeira DIA, Gouveia ST, Pereira JG, Sena MMCC. (2009) Nutritive and non-nutritive attributes of washed-up seaweeds from the coast of Ceará, Brazil. Food Chemistry, 115, 254-259. Patti A, Morrone R. (1992) Biosynthetic relationship between sulfonium and N-methylated compounds in the red alga Vidalia volubilis. Journal of Natural Products, 55, 53-57. Ramos MV, Monteiro ACO, Moreira RA, Carvalho AFFU (2000) Amino acid composition of some Brazilian seaweed species. Journal of Food Biochemistry, 24, 33-39. Romanos MV, Andrada-Serpa MJ, Santos MGM, Ribeiro ACF, Yoneshigue-Valentin Y, Costa SS, Wigg MD. (2002) Inhibitory effect of extracts of Brazilian marine algae on human T-cell lymphotropic virus type 1 (HTLV-1)-induced syncytium formation in vitro. Cancer Investigation, 20, 46-54. Sato M, Nakano T, Takeuchi M, Kanno N, Nagahisa E, Sato Y. (1996) Distribution of neuroexcitatory amino acids in marine algae. Phytochemistry, 42, 1595-1597. Smit AJ. (2004) Medicinal and pharmaceutical uses of seaweed natural products: A review. Journal of Applied Phycology, 16, 245-262. Suyama TL, Cao Z, Murray TF, Gerwick WH. (2010) Ichthyotoxic brominated diphenyl ethers from a mixed assemblage of a red alga and cyanobacterium: structure clarification and biological properties. Toxicon, 55, 204-210. Yoo HD, Ketchum SO, France D, Bair K, Gerwick WH. (2002) Vidalenolone, a novel phenolic metabolite from the tropical red alga Vidalia sp. Journal of Natural Products, 65, 51-53. Guiry MD, Guiry GM. (2012) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org, searched on 22 January 2012. Pettus Jr. JA, Wing RM, Sims JJ. (1977) Marine Natural Products XII. Isolation of a family of multihalogenated gamma-methylene lactones from the red seaweed Delisea fimbriata. Tetrahedron Letters, 18, 41-44. Kazlauskas R, Murphy PT, Quinn RJ, Wells RJ. (1977) A new class of halogenated lactones from the red alga Delisea fimbriata (Bonnemaisoniaceae). Tetrahedron Letters, 18, 37-40. Beechan CM, Sims JJ. (1979) The first synthesis of fimbrolides, a novel class of halogenated lactones naturally occurring in the red seaweed Delisea fimbriata (Bonnemaisoniaceae). Tetrahedron Letters, 18, 1649-1652. Rose AF, Pettus Jr, JA, Sims JJ. (1977). Marine Natural Products XIII. Isolation and synthesis of some halogenated ketones from the red seaweed Delisea fimbriata. Tetrahedron Letters, 18, 1847-1850. Nys R, Wright AD, König GM, Sticher O. (1993) New halogenated furanones from the marine alga Delisea pulchra (cf . fimbriata). Tetrahedron, 49, 11213-11220. Cueto M, Darias J, San-Martín A, Rovirosa J. (1997) New acetyl derivatives from Antarctic Delisea fimbriata. Journal of Natural Products, 60, 279-281.


[39] [40] [41] [42] [43] [44] [45] [46] [47] [48] [49] [50] [51] [52] [53] [54] [55] [56] [57] [58] [59] [60] [61] [62] [63] [64]

Osako & Teixeira

Koch B, Liljefors T, Persson T, Nielsen J, Kjelleberg S, Givskov M. (2005) The LuxR receptor: the sites of interaction with quorum-sensing signals and inhibitors. Microbiology, 151, 3589-3602. Berlinck RGS, Hadju E, Rocha RM, Oliveira JHHL, Hernández ILC, Seleghim MHR, Granato AC, Almeida EVR, Nuñez C, Muricy G, Peixinho S, Pessoa C, Moraes MO, Cavalcanti BC, Nascimento GGF, Thiemann O, Silva M, Souza AO, Silva CL, Minarini PRR. (2004) Challenges and rewards of research in marine natural products chemistry in Brazil. Journal of Natural Products, 67, 510-522. Hernandez ILC, Godinho MJL, Schefer AB, Ferreira AG, Berlinck RGS. (2000) N-acetyl-gamma-hydroxyvaline lactone, an unusual amino acid derivative from a marine streptomycete. Journal of Natural Products, 63, 664-665. Combaut G, Saenger P. (1984) Sterols of the Amansieae (Rhodomelaceae: Rhodophyta). Phytochemistry, 23, 781-782. Wiemer DF, Idler DD, Fenical W. (1991) Vidalols A and B, new anti-inflammatory bromophenols from the Caribbean marine red alga Vidalia obtusaloba. Experientia, 47, 851-853. Stewart I. (2010) Environmental risk factors for temporal lobe epilepsy - is prenatal exposure to the marine algal neurotoxin domoic acid a potentially preventable cause? Medical Hypotheses, 74, 466-481. Souza LM, Sassaki GL, Romanos MTV, Barreto-Bergter E. (2012) Structural characterization and anti-HSV-1 and HSV-2 activity of glycolipids from the marine algae Osmundaria obtusiloba isolated from southeastern Brazilian coast. Marine Drugs, 10, 918-931. Mattos BB, Romanos MTV, Souza LM, Sassaki G, Barreto-Bergter E. (2011) Glycolipids from macroalgae: potential biomolecules for marine biotechnology? Revista Brasileira de Farmacognosia, 21, 244-247. Gama BAP, Carvalho AGV, Weidner K, Soares AR, Coutinho R, Fleury BG, Teixeira VL, Pereira RC. (2008) Antifouling activity of natural products from Brazilian seaweeds. Botanica Marina, 51, 191-201. Riul P, Lacouth P, Pagliosa PR, Christoffersen ML, Horta PA. (2009) Rhodolith beds at the easternmost extreme of South America: Community structure of an endangered environment. Aquatic Botany, 90, 315-320. Combaut G, Codomier L, Teste J, Pedersen M. (1981) The occurrence of C28 sterols in red algae. Phytochemistry, 20, 1748. Fattorusso E, Magno S, Santacroce C, Sica D, Impellizzeri G, Mangiafico S, Piattelli M, Sciuto S. (1976) Sterols of Mediterranean Florideophyceae. Biochemical Systematics and Ecology, 4, 135-138. Sciuto S, Chillemi R, Morrone R, Patti A, Piattelli M. (1989) Dragendorff-positive compounds in some Mediterranean red algae. Biochemical Systematics and Ecology, 17, 5-10. Barberá C, Fernández-Jover D, López-Jiménez JA, González-Silvera D, Hinz H, Moranta J. (2011) Trophic ecology of the sea urchin Spatangus purpureus elucidated from gonad fatty acids composition analysis. Marine Environmental Research, 71, 235-246. Barreto M, Meyer J. (2006) Isolation and antimicrobial activity of a lanosol derivative from Osmundaria serrata (Rhodophyta) and a visual exploration of its biofilm covering. South African Journal of Botany, 72, 521-528. Vuuren SF. (2008) Antimicrobial activity of South African medicinal plants. Journal of Ethnopharmacology, 119, 462-72. Barreto M, Meyer JJM. (2007) The preservation of biofilms on macroalgae by osmium vapour. South African Journal of Botany, 73, 64-69. Kazlauskas R, Murphy PT, Wells RJ. (1982) A brominated metabolite from the red alga Vidalia spiralis. Australian Journal of Chemistry, 35, 219-220. Taylor MW, Rees TAV. (1999) Kinetics of ammonium assimilation in two seaweeds, Enteromorpha sp. (Chlorophyceae) and Osmundaria colensoi (Rhodophyceae). Journal of Phycology, 35, 740-746. Fujita RM, Wheeler PA, Edwards RL. (1988) Metabolic regulation of ammonium uptake by Ulva rigida (Chlorophyta): a compartmental analysis of the rate-limiting step for uptake. Journal of Phycology, 24, 560–566. Zemke-White WL, Clements KD. (1999) Chlorophyte and rhodophyte starches as factors in diet choice by marine herbivorous fish. Journal of Experimental Marine Biology and Ecology, 240, 137-149. Zemke-White WL, Clements KD, Harris PJ. (1999) Acid lysis of macroalgae by marine herbivorous fishes: myth or digestive mechanism? Journal of Experimental Marine Biology and Ecology, 233, 95-113. Alfaro AC. (2006) Population dynamics of the green-lipped mussel, Perna canaliculus, at various spatial and temporal scales in northern New Zealand. Journal of Experimental Marine Biology and Ecology, 334, 294-315. Dunphy BJ, MilletMA, Jeffs AG. (2011) Elemental signatures in the shells of early juvenile green-lipped mussels (Perna canaliculus) and their potential use for larval tracking. Aquaculture, 311, 187-192. Gribben PE, Jeffs AG, Nys R, Steinberg PD. (2011) Relative importance of natural cues and substrate morphology for settlement of the New Zealand Greenshelltm mussel, Perna canaliculus. Aquaculture, 319, 240-246. Duarte MER, Noseda MD, Cardoso MA, Tulio S, Cerezo AS. (2002) The structure of a galactan sulfate from the red seaweed Bostrychia montagnei. Carbohydrate Research, 337, 1137-1144.

Natural Product Communications Vol. 8 (4) 2013 Published online (www.naturalproduct.us)

Volatile Composition of Six Horsetails: Prospects and Perspectives Françoise Fons, Didier Froissard, Jean-Marie Bessière, Alain Fruchier, Bruno Buatois and Sylvie Rapior Chemical Compositions of the Rhizome, Leaf and Stem Oils from Malaysian Hornstedtia leonurus Nor Akmalazura Jani, Hasnah Mohd. Sirat, NorAzah Mohamad Ali and Azrina Aziz Effect on Emotional Behavior and Stress by Inhalation of the Essential oil from Chamaecyparis obtusa Hikaru Kasuya, Erika Hata, Tadaaki Satou, Masaki Yoshikawa, Shinichiro Hayashi, Yoshinori Masuo and Kazuo Koike Chemical Composition and Antibacterial Activity of Rhizome Oils from Five Hedychium Species Ratchuporn Suksathan, Siriwoot Sookkhee, Somboon Anuntalabhochai and Sunee Chansakaow Chemical Composition and Antimicrobial Activity of Three Essential Oils from Curcuma wenyujin Jingjing Zhu, Agnieszka D. Lower-Nedza, Meng Hong, Song Jiec, Zhimin Wang, Dong Yingmao, Christine Tschiggerl, Franz Bucar and Adelheid H. Brantner Essential Oil Composition and Antimicrobial Activity of Aerial Parts and Ripe Fruits of Echinophora spinosa (Apiaceae) from Italy Daniele Fraternale, Salvatore Genovese and Donata Ricci Composition and in vitro Anticancer Activities of the Leaf Essential Oil of Neolitsea variabillima from Taiwan Yu-Chang Su, Kuan-Ping Hsu, Eugene I-Chen Wang and Chen-Lung Ho

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Review/Account Natural Products from Marine Algae of the Genus Osmundaria (Rhodophyceae, Ceramiales) Kelvin Osako and Valéria Laneuville Teixeira Phenols, Alkaloids and Terpenes from Medicinal Plants with Antihypertensive and Vasorelaxant Activities. A Review of Natural Products as Leads to Potential Therapeutic Agents Francesco Maione, Carla Cicala, Giulia Musciacco, Vincenzo De Feo, Anibal G. Amat, Armando Ialenti and Nicola Mascolo Diosmin – Isolation Techniques, Determination in Plant Material and Pharmaceutical Formulations, and Clinical Use Anna Bogucka – Kocka, Michał Woźniak, Marcin Feldo, Janusz Kocki and Katarzyna Szewczyk

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Natural Product Communications 2013 Volume 8, Number 4 Contents Original Paper Anti-melanogenesis Constituents from the Seaweed Dictyota coriacea Ryeo Kyeong Ko, Min-Chul Kang, Sang Suk Kim, Tae Heon Oh, Gi-Ok Kim, Chang-Gu Hyun, Jin Won Hyun and Nam Ho Lee Methyl Carnosate, an Antibacterial Diterpene Isolated from Salvia officinalis Leaves Elisa Climati, Fabio Mastrogiovanni, Maria Valeri, Laura Salvini, Claudia Bonechi, Nilufar Zokirzhonovna Mamadalieva, Dilfuza Egamberdieva, Anna Rita Taddei and Antonio Tiezzi Cytotoxicity of Meroterpenoids from Sargassum siliquastrum against Human Cancer Cells Jung Im Lee, Myoung K. Kwak, Hee Y. Park and Youngwan Seo Isolation of Methyl 27-caffeoyloxyoleanolate – A New Oleanane Triterpenoid from the Roots of Hibiscus vitifolius Duraisamy Ramasamy and Ariamuthu Saraswathy Synthesis and Cytotoxic Activity of New Betulin and Betulinic Acid Esters with Conjugated Linoleic Acid (CLA) Barbara Tubek, Paweł Mituła, Natalia Niezgoda, Katarzyna Kempińska, Joanna Wietrzyk and Czesław Wawrzeńczyk Analysis of Pyrrolizidine Alkaloids and Evaluation of Some Biological Activities of Algerian Senecio delphinifolius (Asteraceae) Soukaina Tidjani, Philippe N. Okusa, Amar Zellagui, Laetitia Moreno Y Banuls, Caroline Stévigny, Pierre Duez and Salah Rhouati Berbanine: a New Isoquinoline-isoquinolone Alkaloid from Berberis vulgaris (Berberidaceae) Anna Hošťálková, Zdeněk Novák, Milan Pour, Anna Jirošová, Lubomír Opletal, Jiří Kuneš and Lucie Cahlíková Dicentrine Production in Callus and Cell Suspension Cultures of Stephania venosa Tharita Kitisripanya, Jukrapun Komaikul, Nirachara Tawinkan, Chuennapha Atsawinkowit and Waraporn Putalun New Flavan and Alkyl α,β-Lactones from the Stem Bark of Horsfieldia superba Nabil Ali Al-Mekhlafi, Khozirah Shaari, Faridah Abas, Ethyl Jeyaseela Jeyaraj, Johnson Stanslas, Shaik Ibrahim Khalivulla and Nordin H. Lajis New Flavonol Triglycosides from the Leaves of Soybean Cultivars Yoshinori Murai, Ryoji Takahashi, Felipe Rojas Rodas, Junichi Kitajima and Tsukasa Iwashina Melitidin: A Flavanone Glycoside from Citrus grandis ‘Tomentosa’ Wei Zou, Yonggang Wang, Haibin Liu, Yulong Luo, Si Chen and Weiwei Su Two New Chalcones from the Flowers of Clerodendrum inerme Shaik Khadar Shahabuddin, Rachakunta Munikishore, Golakoti Trimurtulu, Duvvuru Gunasekar, Alexandre Deville and Bernard Bodo A Novel Phenolic Compound from Phyllanthus emblica Gaimei She, Ruiyang Cheng, Lei Sha, Yixia Xu, Renbin Shi, Lanzhen Zhang and Yajian Guo Anti-austeric Activity of Phenolic Constituents of Seeds of Arctium lappa Yasuhiro Tezuka, Keiichi Yamamoto, Suresh Awale, Feng Li, Satoshi Yomoda and Shigetoshi Kadota Bioactive Lignans from the Leaves and Stems of Schisandra wilsoniana Guang-Yu Yang, Rui-Rui Wang, Zhong-Hua Gao, Yin-Ke Li, Liu-Meng Yang, Xiao-Nian Li, Shan-Zhai Shang, Yong-Tang Zheng, Wei-Lie Xiao and Han-Dong Sun Antioxidative / Acetylcholinesterase Inhibitory Activity of Some Asteraceae Plants Ivana Generalić Mekinić, Franko Burčul, Ivica Blažević, Danijela Skroza, Daniela Kerum and Višnja Katalinić Antioxidant and Antimicrobial Activities, and Phenolic Compounds of Selected Inula species from Turkey Alper Gökbulut, Onural Özhan, Basri Satılmış, Kadir Batçıoğlu, Selami Günal and Engin Şarer Two New Dihydrostilbenoid Glycosides Isolated from the Leaves of Litsea coreana and their Anti-inflammatory Activity Wenjian Tang, Weili Lu, Xiaoqing Cao, Yilong Zhang, Hong Zhang, Xiongwen Lv and Jun Li Inhibitory Activity of Benzophenones from Anemarrhena asphodeloides on Pancreatic Lipase Yang Hee Jo, Seon Beom Kim, Jong Hoon Ahn, Qing Liu, Bang Yeon Hwang and Mi Kyeong Lee Identification and Quantification of Furanocoumarins in Stem Bark and Wood of Eight Algerian Varieties of Ficus carica by RP-HPLC-DAD and RP-HPLC-DAD-MS Samia Rouaiguia-Bouakkaz, Habiba Amira-Guebailia, Céline Rivière, Jean-Claude Delaunay, Pierre Waffo-Téguo and Jean-Michel Mérillon UPLC-Q-TOF/MS Coupled with Multivariate Statistical Analysis as a Powerful Technique for Rapidly Exploring Potential Chemical Markers to Differentiate Between Radix Paeoniae Alba and Radix Paeoniae Rubra Nian-cui Luo, Wen Ding, Jing Wu, Da-wei Qian, Zhen-hao Li, Ye-fei Qian, Jian-ming Guo and Jin-ao Duan Antimicrobial Activity of Crude Methanolic Extract from Phyllanthus niruri Darah Ibrahim, Lim Sheh Hong and Ninthianantham Kuppan Cellulose Contents of Some Abundant Indian Seaweed Species Arup K. Siddhanta, Sanjay Kumar, Gaurav K. Mehta, Mahesh U. Chhatbar, Mihir D. Oza, Naresh D. Sanandiya, Dharmesh R. Chejara, Chirag B. Godiya and Stalin Kondaveeti Anti-inflammatory Potential of Silk Sericin Pornanong Aramwit, Pasarapa Towiwat and Teerapol Srichana Composition of Essential Oil from Aerial and Underground Parts of Geum rivale and G. urbanum Growing in Poland Aleksandra Owczarek, Jan Gudej and Agnieszka Kice Continued Inside backcover

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