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Aaptamine Derivatives with Antifungal and Anti-HIV-1 Activities from the South China Sea Sponge Aaptos Aaptos

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Aaptamine Derivatives with Antifungal and Anti-HIV-1 Activities from the South China Sea Sponge Aaptos Aaptos Mar. Drugs 2014, 12, 6003-6013; doi:10.3390/md12126003 OPEN ACCESS marine drugs ISSN 1660-3397 www.mdpi.com/journal/marinedrugs Article Aaptamine Derivatives with Antifungal and Anti-HIV-1 Activities from the South China Sea Sponge Aaptos aaptos Hao-Bing Yu 1,2,†, Fan Yang 2,†, Fan Sun 2,†, Jing Li 2, Wei-Hua Jiao 2, Jian-Hong Gan 1, Wen-Zhen Hu 2 and Hou-Wen Lin 1,2,* 1 Laboratory of Marine Drugs, Department of Pharmacy, Changzheng Hospital, Second Military Medical University, Shanghai 200003, China; E-Mails: [email protected] (H.-B.Y.); [email protected] (J.-H.G.) 2 Marine Drugs Research Center, Department of Pharmacy, State Key Laboratory of Oncogenes and Related Genes, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai 200127, China; E-Mails: [email protected] (F.Y.); [email protected] (F.S.); [email protected] (J.L.); [email protected] (W.-H.J.); [email protected] (W.-Z.H.) † These authors contributed equally to this work. * Author to whom correspondence should be addressed; E-Mail: [email protected]; Tel.: +86-21-6838-3346; Fax: +86-21-5873-2594. External Editor: Keith B. Glaser Received: 15 October 2014; in revised form: 3 November 2014 / Accepted: 2 December 2014 / Published: 16 December 2014 Abstract: Five new alkaloids of aaptamine family, compounds (1–5) and three known derivatives (6–8), have been isolated from the South China Sea sponge Aaptos aaptos. The structures of all compounds were unambiguously elucidated by spectroscopic analyses, as well as by comparison with the literature data. Compounds 1–2 are characterized with triazapyrene lactam skeleton, whereas compounds 4–5 share an imidazole-fused aaptamine moiety. These compounds were evaluated in antifungal and anti-HIV-1 assays. Compounds 3, 7, and 8 showed antifungal activity against six fungi, with MIC values in the range of 4 to 64 μg/mL. Compounds 7–8 exhibited anti-HIV-1 activity, with inhibitory rates of 88.0% and 72.3%, respectively, at a concentration of 10 μM. Mar. Drugs 2014, 12 6004 Keywords: Aaptos aaptos; aaptamine; antifungal; anti-HIV-1 activity 1. Introduction Marine invertebrates such as sponges are well-known sources of a wide variety of natural alkaloids [1]. The aaptamines are an intriguing group of biologically active marine alkaloids sharing a rare 1H-benzo[de]-1,6-naphthyridine skeleton [2]. Since the first and most prominent member of this family, aaptamine, was obtained from the marine sponge Aaptos aaptos by Nakamura et al. in 1982 [2], various aaptamine derivatives have been isolated from marine sponges belonging to the genera Aaptos, Suberites, Luffariella, Hymeniacidon, Suberea, and Xestospongia [3]. Because of their various biological activities, such as α-adrenoceptor blocking [4], anti-HIV-1 [5], antimicrobial [6], antiherpes [7], sortase A inhibitory [8], and cytotoxic activities [9,10], these alkaloids has become an interesting focus for synthesis, structure-activity relationship and bioactivity studies [3,11]. In particular, the genus Aaptos continues to be an abundant source of aaptamine alkaloids [12,13], which still spurs interest in finding new bioactive metabolites. Our previous chemical investigation of the sponge A. aaptos, collected from the Xisha islands in the South China Sea, led to the isolation of a series of cytotoxic aaptamine derivatives [14]. As a continuation of our studies on aaptamine alkaloids, we carried out further chromatographic purification on the extracts of A. aaptos, and five new alkaloids 1–5 related to aaptamines, in addition to three known aaptamines 6–8 were isolated. Herein, we described the isolation, the structure determination of these compounds, as well as the evaluation of their antifungal and anti-HIV-1 activities. 2. Results and Discussion Compound 1 obtained as an amorphous yellow solid, revealed an [M + Na]+ peak at m/z 330.1220, suggesting a molecular formula of C18H17N3O2 and 12 degrees of unsaturation. The IR spectrum showed bands due to lactam carbonyl functions (1663 cm−1) [15], while the UV absorptions at 208, 224, 273, 282, 412, and 434 nm suggested the presence of triazapyrene lactam core in the molecule [13]. The 1H NMR spectrum displayed the characteristic signals for one isolated methoxy protons 8-OCH3 (δH 4.12, 3H, s), two sets of coupled protons at H-2 (δH 8.73, d, J = 8.0 Hz) and H-3 (δH 7.48, d, J = 8.0 Hz), and H-5 (δH 7.76, d, J = 5.5 Hz) and H-6 (δH 8.70, d, J = 5.5 Hz), and the isolated proton H-7 (δH 7.39, 1H, s), which can be found in most of aaptamine structures [13]. Unlike the other aaptamine analogs reported in the literature [2,14], the absence of proton 1-NH and methoxy protons 9-OCH3 in 1 indicated the substitutions of both N-1 and C-9. In addition, key HMBC correlations from H-2 to C-3a (δC 148.2) and C-9a (δC 126.7), from H-3 to C-2 (δC 126.5) and C-9b (δC 112.8), from H-5 to C-6 (δC 116.9) and C-6a (δC 137.1), from H-6 to C-5 (δC 147.4), C-7 (δC 99.2), and C-9b, from H-7 to C-6, C-8 (δC 157.3), C-9 (δC 119.5), and C-9b, and from 8-OCH3 to C-8 (Figure 1 and Supplementary Figure S5), confirmed that 1 was an aaptamine congener [13]. Moreover, the quaternary carbons at C-11 (δC 153.9) and C-12 (δC 150.7) were confirmed to be a sp2 quaternary carbon and a lactam carbonyl, respectively, by comparison the 13C NMR data with the reported aaptamine derivatives [13]. The quaternary carbon C-11 was further linked to C-9 via a nitrogen atom on consideration of its chemical shifts. Apart from these signals, one Mar. Drugs 2014, 12 6005 methine carbon (δC 26.7), one methylene carbon (δC 42.4), and two overlapped methyl carbons (δC 22.6, 22.6) remained unassigned. These signals were revealed to be an isobutyl group, supported by COSY correlations of H2-13 (δH 2.91)/H-14 (δH 2.34), H-14/H3-15 (δH 0.99), and H-14/H3-16 (δH 0.99). The isobutyl group was tethered to C-12 via C-11, based on the HMBC correlations from H2-13 to C-11 and C-12. Since all the above resonances accounted for 11 out of the 12 degrees of unsaturation, the remaining one degree of unsaturation was assumed to the presence of a tetracyclic system in 1. Finally, a directly bridge between N-1 and C-12 could be rationalized the remaining one degree of unsaturation and the molecular formula. Therefore, the structure of compound 1 was unambiguously assigned as depicted in Figure 2. Figure 1. COSY, HMBC and selected NOESY correlations of compounds 1, 3, and 4. Figure 2. Structures of compounds 1–8. Compound 2 was also obtained as a yellow solid. The molecular formula of C18H17N3O2 was deduced from its HRESIMS data (m/z 308.1400 [M + H]+) in combination with extensive NMR analyses. The NMR data for 2 indicated an overall structure similar to 1, with the only difference at the side chain substituted to C-11 (Tables 1 and 2). The 1H NMR data for 2 lacked two overlapped methyl doublets at δH 0.99, and instead one methyl doublet at δH 1.31 and one methyl triplet at δH 0.91 were evident. These Mar. Drugs 2014, 12 6006 data suggested that the isobutyl group in 1 was replaced by a sec-butyl group in 2, which was supported by the COSY correlations of H2-14 (δH 1.65/1.94)/H3-15 (δH 0.91) and H-13 (δH 3.51)/H3-16 (δH 1.31), as well as the HMBC correlations from H2-14 and H3-15 to C-13 (δC 37.7), and from H-13, H2-14, and H3-16 to C-11 (δC 157.8). Table 1. 13C NMR Data for Compounds 1–5. Carbon 1 a 2 a 3 b 4 b 5 b 2 126.5 126.6 147.6 125.7 125.3 3 118.6 116.9 122.5 114.6 115.5 3a 148.2 148.3 149.6 145.6 146.2 5 147.4 147.5 156.1 144.8 144.4 6 116.9 116.9 117.8 116.2 116.2 6a 137.1 137.2 139.3 134.8 134.8 7 99.2 99.3 99.6 97.4 97.2 8 157.3 157.3 162.3 156.8 156.4 9 119.5 120.9 96.3 126.2 126.2 9a 126.7 126.5 155.7 129.4 129.4 9b 112.8 112.9 116.8 112.3 112.4 8-OCH3 56.3 56.4 56.1 56.6 56.5 9-OCH3 52.0 10 60.0 11 153.9 157.8 15.3 151.8 146.7 12 150.7 150.3 34.3 36.2 13 42.4 37.7 29.2 28.8 14 26.7 27.3 12.1 22.7 15 22.6 11.9 19.2 22.7 16 22.6 17.9 a b Measured at 125 MHz in DMSO-d6; Measured at 150 MHz in CDCl3. Compound 3 was obtained as a yellow solid. The molecular formula was determined as C15H16N2O3 by an HRESIMS ion peak at m/z 295.1058 [M + Na]+. The 1H NMR spectrum revealed the resonances for two sets of coupled protons at δH 8.93 (d, J = 5.4 Hz) and 7.87 (d, J = 5.4 Hz), as well as 8.91 (d, J = 4.8 Hz) and 7.14 (d, J = 4.8 Hz), one singlet at δH 6.14, and two methoxy groups at δH 3.96 and 3.22, indicating the characteristic patterns for aaptamine congener [16].
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