Cyclic Cystine-Bridged Peptides from the Marine. Sponge Clathria basilana Induce Apoptosis in. Tumor Cells and Depolarize the Bacterial
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- Φιλύρη Λαμπρόπουλος
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1 Supporting information Cyclic Cystine-Bridged Peptides from the Marine Sponge Clathria basilana Induce Apoptosis in Tumor Cells and Depolarize the Bacterial Cytoplasmic Membrane Amin Mokhlesi,, Fabian Stuhldreier, Katharina W. Wex, Anne Berscheid, Rudolf Hartmann, Nidja Rehberg, Parichat Sureechatchaiyan, Chaidir Chaidir, O Matthias U. Kassack, Rainer Kalscheuer, Heike Brötz-Oesterhelt, Sebastian Wesselborg, Björn Stork, Georgios Daletos,*, and Peter Proksch*, Institute of Pharmaceutical Biology and Biotechnology, Heinrich Heine University, Universitätsstraße 1, D Düsseldorf, Germany. Department of Marine Biology, Faculty of Marine Sciences, Tarbiat Modares University, Noor, Iran. Institute of Molecular Medicine I, Medical Faculty, Heinrich Heine University, Universitätsstraße 1, D Düsseldorf, Germany. Department of Microbial Bioactive Compounds, Interfaculty Institute of Microbiology and Infection Medicine, University of Tübingen, Auf der Morgenstelle 28/E8, Tübingen, Germany. Institute of Complex Systems: Strukturbiochemie, Forschungszentrum Jülich, Wilhelm- Johnenstrasse, Jülich, Germany. 1
2 Institute of Pharmaceutical and Medicinal Chemistry, Heinrich Heine University, Universitätsstraße 1, D Düsseldorf, Germany. O Center for Pharmaceutical and Medical Technology, Agency for the Assessment and Application Technology, Jakarta, Indonesia. * Corresponding authors. Tel: proksch@uni-duesseldorf.de, georgios.daletos@uni-duesseldorf.de 2
3 Contents S1. Microcionamide C (1)... 6 S H NMR (DMSO-d 6, 600 MHz) spectrum of S1-2. HMBC NMR (DMSO-d 6, 600 MHz) spectrum of S1-3. ROESY NMR (DMSO-d 6, 600 MHz) spectrum of S1-4. HSQC NMR (DMSO-d 6, 600 MHz) spectrum of S1-5. TOCSY NMR (DMSO-d 6, 600 MHz) spectrum of S1-6. HRESIMS spectrum of S1-7. HRESIMS/MS spectrum of S2. Microcionamide D (2) S2-1. Table of 1 H (600 MHz), 13 C (150 MHz), HMBC, and ROESY NMR Data (DMSO-d 6, δ in ppm) of Microcionamide D (2) S H NMR (DMSO-d 6, 600 MHz) spectrum of S2-3. HMBC NMR (DMSO-d 6, 600 MHz) spectrum of S2-4. ROESY NMR (DMSO-d 6, 600 MHz) spectrum of S2-5. HSQC NMR (DMSO-d 6, 600 MHz) spectrum of S2-6. TOCSY NMR (DMSO-d 6, 600 MHz) spectrum of S2-7. COSY NMR (DMSO-d 6, 600 MHz) spectrum of S2-8. HRESIMS spectrum of S2-9. HRESIMS/MS spectrum of S3. Microcionamide A (3) S H NMR (MeOH-d 4, 600 MHz) spectrum of S4. Gombamide B (4) S H NMR (DMSO-d 6, 600 MHz) spectrum of S C NMR (DMSO-d 6, 600 MHz) spectrum of S4-3. HMBC NMR (DMSO-d 6, 600 MHz) spectrum of S4-4. ROESY NMR (DMSO-d 6, 600 MHz) spectrum of S4-5. HSQC NMR (DMSO-d 6, 600 MHz) spectrum of S4-6. TOCSY NMR (DMSO-d 6, 600 MHz) spectrum of
4 S4-7. COSY NMR (DMSO-d 6, 600 MHz) spectrum of S4-8. HRESIMS spectrum of S4-9. HRESIMS/MS spectrum of S5. Gombamide C (5) S5-1. Table of 1 H (600 MHz), 13 C (150 MHz), and HMBC NMR Data (DMSO-d 6, δ in ppm) of Gombamide C (5) S H NMR (DMSO-d 6, 600 MHz) spectrum of S5-3. HMBC NMR (DMSO-d 6, 600 MHz) spectrum of S5-4. HSQC NMR (DMSO-d 6, 600 MHz) spectrum of S5-5. TOCSY NMR (DMSO-d 6, 600 MHz) spectrum of S5-6. HRESIMS spectrum of S5-7. HRESIMS/MS spectrum of S6. Gombamide D (6) S H NMR (DMSO-d 6, 600 MHz) spectrum of S C NMR (DMSO-d 6, 150 MHz) spectrum of S6-3. HMBC NMR (DMSO-d 6, 600 MHz) spectrum of S6-4. ROESY NMR (DMSO-d 6, 600 MHz) spectrum of S6-5. HSQC NMR (DMSO-d 6, 600 MHz) spectrum of S6-6. COSY NMR (DMSO-d 6, 600 MHz) spectrum of S6-7. HRESIMS spectrum of S6-8. HRESIMS/MS spectrum of S7. (E)-2-amino-3-methyl-N-styrylbutanamide (7) S H NMR (MeOH-d4, 600 MHz) spectrum of S C NMR (MeOH-d4, 600 MHz) spectrum of S7-3. HMBC NMR (MeOH-d4, 600 MHz) spectrum of S7-4. COSY NMR (MeOH-d4, 600 MHz) spectrum of S7-5. HRESIMS spectrum of S8. Marfey s analysis S8-1. Table of HPLC (C 18 ) retention times of acid hydrolysates of 1 7 using Marfey s method
5 S8-2. Table of HPLC (C 4 ) retention times for L-Ile and L-allo-Ile of 1 5 using Marfey s method S HPLC chromatogram of derivatized L- and D-allo-Ile standards S HPLC chromatogram of derivatized D-allo-Ile, L-allo-Ile, and L-Ile standards S9. Structures of known compounds S10. Bioactivity results S10-1. Cytotoxicity effects of 1 3 on human lymphoma and leukemia cell lines S10-2. Table of antibacterial activity of new 1 7 and known (8 17) compounds reported as minimal inhibitory concentration (MIC) a
6 S1. Microcionamide C (1) S H NMR (DMSO-d 6, 600 MHz) spectrum of 1 6
7 S1-2. HMBC NMR (DMSO-d 6, 600 MHz) spectrum of 1 7
8 S1-3. ROESY NMR (DMSO-d 6, 600 MHz) spectrum of 1 8
9 S1-4. HSQC NMR (DMSO-d 6, 600 MHz) spectrum of 1 9
10 S1-5. TOCSY NMR (DMSO-d 6, 600 MHz) spectrum of 1 10
11 S1-6. HRESIMS spectrum of 1 11
12 S1-7. HRESIMS/MS spectrum of 1 12
13 S2. Microcionamide D (2) S2-1. Table of 1 H (600 MHz), 13 C (150 MHz), HMBC, and ROESY NMR Data (DMSO-d 6, δ in ppm) of Microcionamide D (2) Unit Position δ c, a type δ H (J in Hz) HMBC ROESY b Z-PEA NH 9.46, d (10.5) Cys 1 -CO Cys 1 -α, Cys 1 -NH α 121.1, CH 6.72, d (10.0) Cys 1 -CO, Z-PEA-β, Z-PEA-1 β 110.8, CH 5.74, d (10.0) Z-PEA-α, Z-PEA-1, Z-PEA- 2/6 aromatic 1: 134.7, C 2: 127.9, CH 7.35 c Z-PEA-β, Z-PEA-1, Z-PEA- 6, Z-PEA-4 3: 128.3, CH 7.35 c Z-PEA-1, Z-PEA-5, Z-PEA-4 4: 126.4, CH 7.24, m Z-PEA-2/6 5: 128.3, CH 7.35 c Z-PEA-1, Z-PEA-3, Z-PEA-4 6: 127.9, CH 7.35 c Z-PEA-β, Z-PEA-1, Z-PEA- 2, Z-PEA-4 Cys 1 NH 8.24, br s Z-PEA- NH, Ile 2 -α CO 168.0, C α 51.7, CH 4.62 c Cys 1 -CO, Ile 2 -CO, Cys 1 -β Z-PEA-NH β 40.9, CH , br t (11.0); 3.28 c Cys 1 -α, Cys 1 -CO Ile 2 NH 7.77, br s CO 170.9, C α 57.2, CH 4.01, br t (8.5) Ile 2 -CO, Ile 3 -CO, Ile 2 -β, Ile 2 - γ, Ile 2 -γ Cys 1 -NH β 34.3, CH 1.77, m Ile 2 -α γ 24.3, CH , m; 1.48, m Ile 2 -α γ 15.1, CH c Ile 2 -α 13
14 δ 11.0, CH c,d Ile 3 NH n.d. e CO α n.d. e 4.08 c β 36.4, CH 1.79, m γ 24.4, CH , m; 1.51, m γ 15.2, CH c δ 11.0, CH c,d Ile 4 NH 7.39 c CO n.d. e α 57.0, CH 4.31, br s Ile 5 -β β 35.9, CH 2.08, br s γ 23.5, CH , m; 1.33, m γ 15.6, CH c δ 11.1, CH c,d Ile 5 NH 8.59, d (9.3) Cys 6 -CO Cys 6 -α CO 170.4, C α 58.0, CH 4.17, dd (9.7, 7.5) Ile 5 -CO, Cys 6 -CO, Ile 5 -β, Ile 5 -γ, Ile 5 -γ Cys 6 -α β 36.4, CH 1.80, m Ile 5 -α Ile 4 -α, Cys 6 -NH, Cys 6 -α γ 24.3, CH , m; 1.41, m Ile 5 -α γ 15.2, CH c Ile 5 -α δ 10.9, CH c,d Cys 6 NH 8.82, br d (7.0) Ile 7 -CO Ile 7 -α, Ile 7 - β, Ile 7 -γ, Ile 5 -β CO 168.6, C 14
15 α 52.5, CH 4.61 c Ile 7 -CO Ile 5 -NH, Ile 7 -α, Ile 5 - α β 40.2, CH , m; 3.35, m Ile 7 NH , br s CO 167.8, C α 56.1, CH 3.66, br t (5.0) Ile 7 -CO, Ile 7 -β, Ile 7 -γ, Ile 7 -γ Cys 6 -α, Cys 6 -NH β 36.2, CH 1.79, m Ile 7 -α Cys 6 -NH γ 23.4, CH , m; 1.46, m Ile 7 -α Cys 6 -NH γ 14.2, CH c Ile 7 -α δ 10.8, CH c.d a Data extracted from HSQC and HMBC spectra. b Sequential NOEs. c Signal overlap prevents determination of couplings. d Assignments within the same column may be interchanged. e n.d. : not detected 15
16 S H NMR (DMSO-d 6, 600 MHz) spectrum of 2 16
17 S2-3. HMBC NMR (DMSO-d 6, 600 MHz) spectrum of 2 17
18 S2-4. ROESY NMR (DMSO-d 6, 600 MHz) spectrum of 2 18
19 S2-5. HSQC NMR (DMSO-d 6, 600 MHz) spectrum of 2 19
20 S2-6. TOCSY NMR (DMSO-d 6, 600 MHz) spectrum of 2 20
21 S2-7. COSY NMR (DMSO-d 6, 600 MHz) spectrum of 2 21
22 S2-8. HRESIMS spectrum of 2 22
23 S2-9. HRESIMS/MS spectrum of 2 23
24 S3. Microcionamide A (3) S H NMR (MeOH-d 4, 600 MHz) spectrum of 3 24
25 S4. Gombamide B (4) S H NMR (DMSO-d 6, 600 MHz) spectrum of 4 25
26 S C NMR (DMSO-d 6, 600 MHz) spectrum of 4 26
27 S4-3. HMBC NMR (DMSO-d 6, 600 MHz) spectrum of 4 27
28 S4-4. ROESY NMR (DMSO-d 6, 600 MHz) spectrum of 4 28
29 S4-5. HSQC NMR (DMSO-d 6, 600 MHz) spectrum of 4 29
30 S4-6. TOCSY NMR (DMSO-d 6, 600 MHz) spectrum of 4 30
31 S4-7. COSY NMR (DMSO-d 6, 600 MHz) spectrum of 4 31
32 S4-8. HRESIMS spectrum of 4 32
33 S4-9. HRESIMS/MS spectrum of 4 33
34 S5. Gombamide C (5) S5-1. Table of 1 H (600 MHz), 13 C (150 MHz), and HMBC NMR Data (DMSO-d 6, δ in ppm) of Gombamide C (5) Unit Position δ c, a type δ H (J in Hz) HMBC Cys 1 NH 7.89, br d (8.6) Phe-CO CO 168.4, C α 51.5, CH 4.76 b β 41.7, CH , dd (14.4, 12.4); 3.14, dd (14.4, 3.4) Z-PEA NH 9.72, br d (10.1) Cys 1 -CO α 121.3, CH 6.71, dd (10.1, 9.7) Cys 1 -CO, Z-PEA-β β 111.6, CH 5.79, d (9.7) Z-PEA-α, Z-PEA-2/6, Z-PEA-1 aromatic 1: 135.2, C 2: 128.1, CH 7.38 b 3: 128.4, CH 7.38 b 4: 126.6, CH 7.38 b 5: 128.4, CH 7.38 b 6: 128.1, CH 7.38 b Phe NH 9.00, br d (8.8) CO 170.5, C α 53.4, CH 4.75 b Phe-CO, Phe-β, Pro 3 -CO β 34.1, CH , m Phe-α, Phe-1, Phe-2/6 aromatic 1: 138.0, C 2: 129.1, CH 7.40, br d (7.5) Phe-β, Phe-6, Phe-4 3: 128.0, CH 7.28, br t (7.5) Phe-1, Phe-5 4: 126.1, CH 7.19, br t (7.5) Phe-2/6 5: 128.0, CH 7.28, br t (7.5) Phe-1, Phe-3 6: 129.1, CH 7.40, br d (7.5) Phe-β, Phe-6, Phe-4 34
35 Pro 3 CO 171.2, C α 60.7, CH 4.34, d (8.0) Pro 3 -CO, Pro 4 -CO, Pro 3 -β, Pro 3 -γ, Pro 3 -δ β 31.1, CH , m; 1.87, m γ 20.0, CH , m; 0.58, m δ 45.9, CH , m Pro 4 CO 169.2, C α 59.0, CH 4.80, dd (8.8, 3.0) Pro 4 -γ β 30.1, CH , m; 2.22, m γ 21.6, CH , m δ 46.7, CH , m; 3.47, m Cys 5 NH 8.00, br d (10.0) Leu-CO CO 167.9, C α 48.1, CH 4.55, td (10.0, 5.1) Leu-CO, Cys 5 -CO, Cys 5 -β β 37.9, CH , dd (13.0, 10.0); 3.20, dd (13.0, 5.1) Cys 5 -α, Cys 5 -CO Leu NH 8.04, br d (9.9) CO 170.3, C α 50.3, CH 4.47, ddd (9.9, 8.6, 6.1) Leu-CO, Leu-β, Ile-CO β 41.0, CH , m Leu-α, Leu-δ, Leu-δ, Leu-CO γ 23.8, CH 1.62, m δ 21.2, CH , d (6.5) Leu-β, Leu-δ δ' 23.2, CH , d (6.6) Leu-β, Leu-δ Ile NH 8.06, br d (8.7) CO 170.5, C α 56.8, CH 4.15, t (8.5) Glp-CO, Ile-CO, Ile-β, Ile-γ, Ile-γ β 35.4, CH 1.72, m Ile-α, Ile-δ γ 24.0, CH , m; 1.42, m Ile-α, Ile-δ 35
36 γ 15.2, CH , d (6.8) Ile-α δ 10.2, CH , t (7.4) Ile-β, Ile-γ Glp NH 7.80, s Glp-CO, Glp-α, Glp-β, Glp-γ CO CO 172.2, C 177.4, C α 55.0, CH 4.09, dd (8.7, 3.6) Glp-CO, Glp-β, Glp-γ β 25.2, CH , m; 2.22, m Glp-CO, Glp-α γ 28.8, CH , m; 2.09, m Glp-α a Data extracted from HSQC and HMBC spectra. b Signal overlap prevents determination of couplings. 36
37 S H NMR (DMSO-d 6, 600 MHz) spectrum of 5 37
38 S5-3. HMBC NMR (DMSO-d 6, 600 MHz) spectrum of 5 38
39 S5-4. HSQC NMR (DMSO-d 6, 600 MHz) spectrum of 5 39
40 S5-5. TOCSY NMR (DMSO-d 6, 600 MHz) spectrum of 5 40
41 S5-6. HRESIMS spectrum of 5 41
42 S5-7. HRESIMS/MS spectrum of 5 42
43 S6. Gombamide D (6) S H NMR (DMSO-d 6, 600 MHz) spectrum of 6 43
44 S C NMR (DMSO-d 6, 150 MHz) spectrum of 6 44
45 S6-3. HMBC NMR (DMSO-d 6, 600 MHz) spectrum of 6 45
46 S6-4. ROESY NMR (DMSO-d 6, 600 MHz) spectrum of 6 46
47 S6-5. HSQC NMR (DMSO-d 6, 600 MHz) spectrum of 6 47
48 S6-6. COSY NMR (DMSO-d 6, 600 MHz) spectrum of 6 48
49 S6-7. HRESIMS spectrum of 6 49
50 S6-8. HRESIMS/MS spectrum of 6 50
51 S7. (E)-2-amino-3-methyl-N-styrylbutanamide (7) S H NMR (MeOH-d4, 600 MHz) spectrum of 7 51
52 S C NMR (MeOH-d4, 600 MHz) spectrum of 7 52
53 S7-3. HMBC NMR (MeOH-d4, 600 MHz) spectrum of 7 53
54 S7-4. COSY NMR (MeOH-d4, 600 MHz) spectrum of 7 54
55 S7-5. HRESIMS spectrum of 7 55
56 S8. Marfey s analysis S8-1. Table of HPLC (C 18 ) retention times of acid hydrolysates of 1 7 using Marfey s method Amino acid Standard L-Cys D-Cys 21.2 L-Ile D-Ile 24.2 L-Leu D-Leu 24.3 L-Val 14.5 D-Val L-Pro D-Pro 11.4 L-Glu D-Glu 14.2 L-Phe D-Phe
57 S8-2. Table of HPLC (C 4 ) retention times for L-Ile and L-allo-Ile of 1 5 using Marfey s method Amino acid Standard L-Ile L-allo-Ile Marfey 160min 25C #4 Marfey 160min DLallo UV_VIS_1 mau WVL:235 nm L-allo-Ile D-allo-Ile min 20,0 30,0 40,0 50,0 60,0 70,0 80,0 S HPLC chromatogram of derivatized L- and D-allo-Ile standards Marfey 160min 25C #3 Marfey 160min DLallo+LIle 2 UV_VIS_1 mau WVL:235 nm L-allo-Ile/L-Ile D-allo-Ile 0-60 min 20,0 30,0 40,0 50,0 60,0 70,0 80,0 S HPLC chromatogram of derivatized D-allo-Ile, L-allo-Ile, and L-Ile standards 57
58 S9. Structures of known compounds S9-1. Structures of known compounds, including 1H-indole-3-carbaldehyde (8), 1H-indole-3-carboxylic acid (9), 6-bromo-1H-indole-3-carbaldehyde (10), 6-bromo-1H-indole-3-carboxylic acid (11), methyl 6- bromo-1h-indole-3-carboxylate (12), ethyl 6-bromo-1H-indole-3-carboxylate (13), 7-bromo-4(1H)- quinolinone (14), (3-(2-(4-hydroxyphenyl)-2-oxoethyl)-5,6-dihydropyridin-2(1H)-one) (15), 2- deoxythymidine (16), and 4-hydroxybenzoic acid (17). 58
59 S10. Bioactivity results S10-1. Cytotoxicity effects of 1 3 on human lymphoma and leukemia cell lines, measured by MTT assay. (A) Ramos (Burkitt s lymphoma), (B) Jurkat J16 (acute T cell leukemia), (C) Nomo-1 (acute myeloid leukemia) and (D) HL-60 (acute promyelocytic leukemia) cells were seeded at a density of cells/ml and incubated with increasing concentrations of 1, 2 and 3, respectively. Cells treated with DMSO (0.1% v/v) for 24 h were used as the negative control. After an incubation period of 24 h cell viability was monitored using the MTT assay as described in methods. Relative viability in DMSOtreated control cells was set to 100%. Data points shown are the mean of triplicates, error bars = SD. Viability and IC 50 values (IC 50 = half maximal inhibitory concentration) were calculated using Prism 6 (GraphPad Software). 59
60 S10-2. Table of antibacterial activity of new 1 7 and known (8 17) compounds reported as minimal inhibitory concentration (MIC) a Compound Staphylococcus aureus ATCC Enterococcus faecium BM Escherichia coli ATCC Klebsiella pneumoniae ATCC Enterobacter aerogenes ATCC Pseudomonas aeruginosa ATCC Acinetobacter baumannii Mycobacterium tuberculosis H37Rv > 100 > 100 > 100 > 100 > n.i. b n.i. n.i. n.i. n.i. n.i. n.i. n.i c 12.5 > 100 > 100 > 100 > 100 > > 50 > 50 > 100 > 100 > 100 > 100 > 100 > n.i. n.i. n.i. n.i. n.i. n.i. n.i. n.i > 50 > 50 > 100 > 100 > 100 > 100 > 100 n.i. ciprofloxacin n.i. doxycycline n.i. n.i. n.i. vancomycin 1 4 > 64 > 64 > 64 > 64 > 64 n.i. a MIC values are reported for test compounds in µm and for reference antibiotics in µg/ml and indicate the lowest concentration fully inhibiting visible bacterial growth. b n.i. : not investigated. c Growth reduction was already observed at 3.1 µm 60
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