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Bioactive Secondary Metabolites from the Marine Sponge Genus Agelas

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Bioactive Secondary Metabolites from the Marine Sponge Genus Agelas marine drugs Review Bioactive Secondary Metabolites from the Marine Sponge Genus Agelas Huawei Zhang 1,* ID , Menglian Dong 1, Jianwei Chen 1, Hong Wang 1, Karen Tenney 2 and Phillip Crews 2 ID 1 Department of Pharmaceutical Sciences, Zhejiang University of Technology, Hangzhou 310014, China; [email protected] (M.D.); [email protected] (J.C.); [email protected] (H.W.) 2 Department of Chemistry & Biochemistry, University of California Santa Cruz, Santa Cruz 95064, CA, USA; [email protected] (K.T.); [email protected] (P.C.) * Correspondence: [email protected]; Tel.: +86-571-8832-0613 Received: 19 September 2017; Accepted: 3 November 2017; Published: 8 November 2017 Abstract: The marine sponge genus Agelas comprises a rich reservoir of species and natural products with diverse chemical structures and biological properties with potential application in new drug development. This review for the first time summarized secondary metabolites from Agelas sponges discovered in the past 47 years together with their bioactive effects. Keywords: marine sponge; Agelas; secondary metabolite; natural product; bioactivity 1. Introduction The search for natural drug candidates from marine organisms is the eternal impetus to pharmaceutical scientists. For the past six decades, marine sponges have been a prolific and chemically diverse source of natural compounds with potential therapeutic application [1,2]. The marine sponge Agelas (Porifera, Demospongiae, Agelasida, Agelasidae) is widely distributed in the marine eco-system and includes at least 19 species (Figure1): A. axifera, A. cerebrum, A. ceylonica, A. citrina, A. clathrodes, A. conifera, A. dendromorpha, A. dispar, A. gracilis, A. linnaei, A. longissima, A. mauritiana, A. nakamurai, A. nemoechinata, A. oroides, A. sceptrum, A. schmidtii, A. sventres, and A. wiedenmayeri. Since the beginning of the 1970s, many research groups around the world have carried out chemical investigation on Agelas spp., resulting in fruitful achievements. Their studies revealed that Agelas sponges harbor many bioactive secondary metabolites, including alkaloids (especially bromopyrrole derivatives), terpenoids, glycosphingolipids, carotenoids, fatty acids and meroterpenoids [3]. These natural products are an attractive resource for drug candidates due to their rich chemodiversity and interesting biological activities. Mar. Drugs 2017, 15, 351; doi:10.3390/md15110351 www.mdpi.com/journal/marinedrugs Mar. Drugs 2017, 15, 351 2 of 29 Mar. Drugs 2017, 15, 351 2 of 29 Agelas clathrodes Agelas conifera Agelas dispar Agelas inequalis Agelas mauritiana Agelas sceptrum Agelas wiendermayeri Agelas sp. Figure 1. Photos of Agelas sponges provided by professor Crews. Figure 1. Photos of Agelas sponges provided by professor Crews. 2. Natural Products from Agelas Genus 2. Natural Products from Agelas Genus The chemical diversity of natural products is determined by the biological diversity of organisms. ToThe date, chemical 291 secondary diversity metabolites of natural ( products1–291) have isdetermined been isolated by and the biologicalcharacterized diversity from the of organisms.marine Tosponge date, 291 Agelas secondary spp. (Table metabolites 1). These chemicals (1–291) have were been introduced isolated and and assorted characterized as follows from according the marine to spongetheir biologicalAgelas spp. sources. (Table 1). These chemicals were introduced and assorted as follows according to their biological sources. Mar. Drugs 2017, 15, 351 3 of 29 Mar. Drugs 2017, 15, 351 3 of 29 Mar. Drugs 2017, 15, 351 3 of 29 Mar. Drugs 2017, 15, 351 3 of 29 2.1.2.1. Agelas Agelas axifera axifera 2.1. Agelas axifera 2.1. Agelas axifera ThreeThree newnew alkaloids,alkaloids, namednamed axistatinsaxistatins 11 (1(1),), 22 (2(2),), andand 33 (3(3)) (Figure(Figure2 ),2), were were isolated isolated and and Three new alkaloids, named axistatins 1 (1), 2 (2), and 3 (3) (Figure 2), were isolated and characterizedcharacterizedThree new fromfrom alkaloids,Agelas Agelas axiferanamedaxiferacollected collectedaxistatinsin in the1 the (1 Republic ),Republic 2 (2), andof of Palau Palau3 (3) and and(Figure found found 2), to towere exhibit exhibit isolated inhibitory inhibitory and characterized from Agelas axifera collected in the Republic of Palau and found to exhibit inhibitory characterizedeffectseffects on on cancer cancer from cell cell Agelas lines, lines, axifera including including collected P388, P388, BXPC-3, inBXPC-3, the Republic MCF-7,MCF-7, of SF-268,SF-268, Palau NCI-H460, NCI-H460,and foundKM20L2 KM20L2to exhibit andand inhibitory DU-145.DU-145. effects on cancer cell lines, including P388, BXPC-3, MCF-7, SF-268, NCI-H460, KM20L2 and DU-145. effectsTheThe exquisitely exquisitely on cancer sensitive cellsensitive lines, Gram-negative Gram-negativeincluding P388, pathogen pathogen BXPC-3, NeisseriaMCF-7, Neisseria SF-268, gonorrheae gonorrheae NCI-H460,and and the the KM20L2 opportunistic opportunistic and DU-145. fungus fungus The exquisitely sensitive Gram-negative pathogen Neisseria gonorrheae and the opportunistic fungus TheCryptococcusCryptococcus exquisitely neoformansneoformans sensitive wereGram-negative inhibited inhibited by pathogen by 1–13– 3withwith Neisseria MIC MIC values valuesgonorrheae of 1–8, of 1–8,and 2–4, the 2–4, and opportunistic and8 μg/mL, 8 µg/mL, and fungus 1–4, and 2, Cryptococcus neoformans were inhibited by 1–3 with MIC values of 1–8, 2–4, and 8 μg/mL, and 1–4, 2, 1–4,Cryptococcusand 2,8–16 and μ 8–16 g/mL,neoformansµg/mL, respectively. were respectively. inhibited Furthermore, by Furthermore, 1–3 withthese MIC compounds these values compounds of had1–8, antimicrobial2–4, had and antimicrobial 8 μg/mL, effect and on effect 1–4,Gram- on 2, and 8–16 μg/mL, respectively. Furthermore, these compounds had antimicrobial effect on Gram- andGram-positivepositive 8–16 bacteria,μg/mL, bacteria, respectively.including including Staphylococcus Furthermore,Staphylococcus aureus these aureus, Streptococcuscompounds, Streptococcus hadpneumoniae pneumoniaeantimicrobial, Enterococcus, Enterococcus effect onfaecalis Gram- faecalis and positive bacteria, including Staphylococcus aureus, Streptococcus pneumoniae, Enterococcus faecalis and positiveandMicrococcusMicrococcus bacteria, luteus luteus including [4]. [4]. Staphylococcus aureus, Streptococcus pneumoniae, Enterococcus faecalis and Micrococcus luteus [4]. Micrococcus luteus [4]. 1 2 3 1 2 3 1 2 3 Figure 2. Chemical structures of compounds 1–3. Figure 2. Chemical structures of compounds 1–3. Figure 2. Chemical structures of compounds 1–3. 2.2. Agelas cerebrum 2.2. Agelas cerebrum 2.2. Agelas cerebrum Marine sponge Agelas cerebrum was classified as a new species in 2001 [5]. Chemical investigation Marine spongespongeAgelas Agelas cerebrumcerebrumwas was classified classified as as a a new new species species in in 2001 2001 [5 [5].]. Chemical Chemical investigation investigation of of CaribbeanMarine sponge specimen Agelas A. cerebrumcerebrum led was to classified the isolation as a of new three species brom ininated 2001 compounds, [5]. Chemical 5-bromopyrrole- investigation Caribbeanof Caribbean specimen specimenA. A. cerebrum cerebrumled led to to the the isolation isolation of of three three brominated brominated compounds, compounds, 5-bromopyrrole-2- 5-bromopyrrole- of2-carboxylic Caribbean specimenacid (4), 4-bromopyrrole-2-carboxylicA. cerebrum led to the isolation acid of three (5) and brom 3,4-bromopyrroleinated compounds,-2-carboxylic 5-bromopyrrole- acid (6) carboxylic2-carboxylic acid acid ( 4(),4), 4-bromopyrrole-2-carboxylic 4-bromopyrrole-2-carboxylic acidacid ((55)) andand 3,4-bromopyrrole-2-carboxylic3,4-bromopyrrole-2-carboxylic acid ( 6)) 2-carboxylic(Figure 3) [6]. acid Biological (4), 4-bromopyrrole-2-carboxylic tests indicated that these isolatesacid (5 )had and strong 3,4-bromopyrrole cytotoxic activities-2-carboxylic in vitro acid against (6) (Figure3 3)) [[6].6]. Biological tests indicated that these isolates had had strong strong cytotoxic cytotoxic activities activities inin vitro vitro against (Figurehuman 3) tumor [6]. Biological cell lines tests at ≥ 1indicated mg/mL, thatincluding these isolates A549, HT29 had strong and MDA-MB-231. cytotoxic activities in vitro against human tumor cellcell lineslines atat≥ ≥1 mg/mL, including including A549, A549, HT29 and MDA-MB-231. human tumor cell lines at ≥1 mg/mL, including A549, HT29 and MDA-MB-231. 4: R1 = H, R2 =H, R3 = Br 4: R1 = H, R2 =H, R3 = Br 4:5: R R11= = H, H, R R22=H, = Br, R 3R=3 Br= H 5: R1 = H, R2 = Br, R3 = H 5:6: R R11 = = H, Br, R R2 2= = Br, Br, R R3 3= = H H. 6: R1 = Br, R2 = Br, R3 = H. 6: R1 = Br, R2 = Br, R3 = H. Figure 3. Chemical structures of compounds 4–6. Figure 3. Chemical structures of compounds 4–6. Figure 3. Chemical structures of compounds 4–6. 2.3. Agelas ceylonica 2.3. Agelas ceylonica 2.3. Agelas ceylonica Only one case of chemical study on Agelas ceylonica has been reported [7]. The specimen of A. Only one case of chemical study on Agelas ceylonica has been reported [7]. The specimen of A. ceylonicaOnly collectedone one case case fromof of chemical chemical India Mandapam study study on on Agelas Agelascoast ceylonicawas ceylonica found hashas to been produce been reported reported one methyl[7]. [7 ].The Theester specimen specimen hanishin of A. of(7 ) ceylonica collected from India Mandapam coast was found to produce one methyl ester hanishin (7) ceylonicaA.(Figure ceylonica 4),collected collectedwhich fromhas from been India India previously
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