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Cytotoxic Heterocycles from an Australian Marine Sponge, Trachycladus Laevispirulifer†

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Cytotoxic Heterocycles from an Australian Marine Sponge, Trachycladus Laevispirulifer† PAPER www.rsc.org/obc | Organic & Biomolecular Chemistry Trachycladindoles A–G: cytotoxic heterocycles from an Australian marine sponge, Trachycladus laevispirulifer† Robert J. Capon,*a Chongsheng Pengb and Cedric Doomsa Received 28th February 2008, Accepted 8th May 2008 First published as an Advance Article on the web 29th May 2008 DOI: 10.1039/b803455a A southern Australian marine sponge, Trachycladus laevispirulifer, yielded the cytotoxic agents trachycladindoles A–G (1–7) as a selection of novel indole-2-carboxylic acids bearing a 2-amino-4,5-dihydroimidazole moiety. The trachycladindoles displayed promising selective cytotoxicity against a panel of human cancer cell lines and their structures were assigned on the basis of detailed spectroscopic analysis. Preliminary structure activity relationship (SAR) investigations by co-metabolite defined structural features key to the trachycladindole pharmacophore, highlighting an unusual bioactive molecular motif deserving of future investigation. Introduction lines to reveal 110 marine specimens with promising cytotoxicity profiles. Of these target specimens, 81 localized the cytotoxic During an investigation into anticancer agents from marine activity exclusively in the n-BuOH partition, 23 exclusively in organisms, we examined a collection of invertebrates and algae the H2O partition, and 6 in both n-BuOH and H2O partitions. acquired over a period of more than two decades from various This pool of targeted marine specimens formed the basis of southern Australian and Antarctic locations, ranging from inter- our chemical investigations aimed at discovering new anticancer tidal to deep water, and utilizing collection methods from hand agents. In this report, we describe the discovery of novel cytotoxic (SCUBA) to commercial and scientific trawling. Solvent extracts metabolites, trachycladindoles A–G (1–7) produced by a specimen prepared from these samples were screened for their growth of Trachycladus laevispirulifer collected in 2001 during commercial inhibitory and cytotoxic activity against a panel of human trawling operations (Orange Roughy bycatch) in the Great Aus- cancer cell lines, leading to the identification of a number of tralian Bight. A portion of the aqueous EtOH extract obtained noteworthy bioactive extracts. Detailed chemical analysis of one from a southern Australian specimen of T.laevispirulifer displaying of these extracts led to the identification of a novel family of cytotoxicity against human cancer cell lines was concentrated in cytotoxic indole-2-carboxylic acid heterocycles, trachycladindoles vacuo and the residue (1.8 g) partitioned into n-BuOH (331 mg) A–G (1–7). This report describes the isolation, characterization and H2O (1298 mg) solubles. The cytotoxic n-BuOH solubles were and structure elucidation of the trachycladindoles, together with sequentially triturated with hexane, CH2Cl2 and MeOH, followed preliminary structure activity relationship investigations. by reverse phase HPLC, to yield novel heterocyclic indole-2- carboxylic acids, trachycladindoles A–G (1–7). Results and discussion High resolution ESI(+)MS analysis of trachycladindole A (1) revealed a pseudo molecular ion (M + H) consistent with Several thousand marine specimens from multiple field collection a molecular formula (C13H13BrN4O2, Dmmu 1.4) incorporating sites were transferred frozen to the laboratory where they were nine double bond equivalents (DBE). Analysis of the 13CNMR ◦ catalogued, diced and steeped in aqueous EtOH at −30 Cfor 2 (CD3OD) data for 1 (see Table 1) revealed eight sp carbons (dC prolonged storage. To facilitate handling and biological screening, 112.5 to 135.1) attributed to four carbon–carbon double bonds, a portion (7 mL) of each extract was decanted, concentrated and a further two deshielded resonances (dC 168.6 and 160.4) in vacuo, weighed and partitioned in situ between n-BuOH (2 mL) consistent with sp2 carbonyl/iminyl carbons. These observations and H2O (2 mL). Aliquots (1 mL) of both the n-BuOH and accounted for six DBE and required that 1 be tricyclic. Further H2O partitions were transferred to deep 96 well plates and stored analysis of the 1H and COSY NMR (CD OD) data revealed − ◦ 3 at 30 C ahead of being sub-sampled to support biological resonances and correlations consistent with three isolated spin screening. systems; (a) a 1,2,4-trisubstituted aromatic ring (dH 7.30, dd, J = Screening aliquots (5–10 lL) of n-BuOH and H2O partitions 8.7 and 1.8 Hz, H-6; 7.39, dd, J = 8.7 and 0.5 Hz, H-7; and (2 × 2624 samples) were assayed against a selection of cancer cell 7.60, brs, H-4); (b) an N-methyl (dH 2.74, s, N12-Me); and (c) a deshielded methine–methylene pair (dH 6.38, brs, H-8; 3.69, brm, = 13 aInstitute for Molecular Bioscience, The University of Queensland, St Lucia, H-9b; and 4.06, dd, J 10.2 and 10.2 Hz, H-9a). Deshielded C Queensland, 4072, Australia. E-mail: [email protected]; Fax: 617 3346 NMR (CD3OD) chemical shifts for C-8 (dC 58.9) and C-9 (dC 48.8), 2090; Tel: 617 3346 2979 together with gHMBC correlations from H-9b and N12-Me to a bSchool of Pharmacy, Shanghai Jiaotong University, Shanghai, 200249, common C-11 guanidino carbon (dC 160.4) and C-8, supported P. R. China assignment of the 2-amino-4,5-dihydroimidazole heterocycle as † Electronic supplementary information (ESI) available: Tabulated 1D and 2D NMR data, and 1H NMR spectra for trachycladindoles A–G (1–7). shown. Such heterocycles are rare among published natural prod- See DOI: 10.1039/b803455a ucts with a noteworthy marine occurrence being discodermindole This journal is © The Royal Society of Chemistry 2008 Org. Biomol. Chem., 2008, 6, 2765–2771 | 2765 c c c c c c c Table 1 NMR (600 MHz, CD3OD) data for trachycladindole A (1) b C d 1 169.2 112.6 126.5 120.4 113.8 b 1 13 # dH/m dC COSY gHMBC ( H- C) a N1-H d d 2 a a /Hz C2-CO2H 168.6 J 3 112.5 /m 3a 128.1 H 3.75 (dd, 8.8, 8.8) d 7.46 (d, 8.4) 4.06 (dd, 10.0, 10.0) 48.4 4 7.60 (brs) 122.8 H-6 5 114.3 ca ca c c c c c 6 7.30 (dd) 127.4 H-7, H-4 C-7a, C-5, C-4 b d C d 7 7.39 (dd) 115.5 H-6 C-6, C-5, C-4, C-3a 137.5 168.9 110.9 120.9 106.9 7.05 (bdd, 7.5, 7.6)137.4 121.2 137.1 7a 135.1 8 6.38 (brs) 58.9 e 9a 4.06 (dd) 48.8 H-9b C-11, C-8, C-3 /Hz 9b 3.69 (brm) H-9a J N10-H a /m H 11 160.4 d 7.25 (brs) 123.3 N12-Me 2.74 (s) 29.7 C-11, C-8 ca c c c a b 13 Not observed. C NMR assignments supported by DEPT and HSQC b C d experiments. c 8.7, 1.8. d 8.7, 0.5. e 10.2, 10.2. 168.2 a 114.4 135.0 (8), reported in 1991 by Sun et al.1 from a deep-water collection /Hz of the sponge Discodermia polydiscus. A second example of this J structure class, 6-hydroxydiscodermindole (9), was reported by /m H ) Gunasekera et al.2 during a 2004 re-investigation of this same d a aa 7.29 (dd, 8.7, 1.7) 127.4 153.4 7.21 (bdd, 7.5, 7.6) 124.7 2–7 D. polydiscus specimen. A significant difference in the NMR (d6- DMSO) data for the 2-amino-4,5-dihydroimidazole heterocycle in c c c trachycladindole A (1) compared to discodermindole (8)wasthe b C d pronounced deshielding of H-8 (DdH −1.21) and C-8 (DdC −5.3). 169.0 This deshielding was attributed to the ability of 1 to form an internal salt with restricted conformational freedom (see below). Further spectroscopic comparison to 8 permitted incorporation Overlapping resonances. of the 1,2,4-trisubstituted aromatic structure fragment in 1 into d /Hz the indole ring system as shown. Placement of the 2-amino-4,5- J dihydroimidazole substituent at C-3 (as indicated) was supported /m H d a by gHMBC (CD3OD) correlations (see Table 1) from H-9a to an 2 ca a sp carbon resonance attributed to C-3 (d 112.6), and further OD) data from trachycladindoles B–G ( C 3 b confirmed by a suite of diagnostic NOESY (CD3OD) correlations C d 135.2 169.2 between H-9a, H-9b and N12-Me, to H-4 (dH 7.60). These NOESY Assignment tentative. correlations together with further NMR comparisons to 8, also c confirmed placement of a C-5 bromo substituent as indicated. The structure arguments as presented above for 1 account for all but the identity of the C-2 substituent and the elements of CO2H. As /Hz a result, the complete planar structure for trachycladindole A (1) J C NMR (150 MHz, CD /m 13 was proposed as shown (in an internal salt form—see below). H d a High resolution ESI(+)MS analysis of trachycladindole B (2) revealed a pseudo molecular ion (M + Na) consistent with a b C OD) and d a 168.5 3 molecular formula (C14H15BrN4O2, Dmmu −0.3) for a methyl homologue of trachycladindole A (1). Comparison of the NMR (CD3OD) data between 1 and 2 (see Tables 1, 2) revealed the only significant difference to be an additional N-methyl resonance /Hz (dH 3.11 and dC 32.5) in 2 compared to 1. Further analysis of J C NMR assignments supported by HSQC.
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