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Acetylcholine-like and trimethylglycine-like PTA (1,3,5-triaza-7-phosphaadamantane) derivatives for the development of innovative Ru- and Pt-based therapeutic agents.

PMID: 24801393
Article pubs.acs.org/IC Acetylcholine-like and Trimethylglycine-like PTA (1,3,5-Triaza-7phosphaadamantane) Derivatives for the Development of Innovative Ru- and Pt-Based Therapeutic Agents Valeria Ferretti,† Marco Fogagnolo,† Andrea Marchi,† Lorenza Marvelli,† Fabio Sforza,‡ and Paola Bergamini*,† † Dipartimento di Scienze Chimiche e Farmaceutiche, Università degli Studi di Ferrara, Via Fossato di Mortara 17, 44121 Ferrara, Italy Dipartimento di Biochimica e Biologia Molecolare, Sezione di Biologia Molecolare, Università degli Studi di Ferrara, Via Fossato di Mortara 74, 44121 Ferrara, Italy ‡ S Supporting Information * ABSTRACT: The PTA N-alkyl derivatives (PTAC2H4OCOMe)X (1X: 1a, X = Br; 1b, X = I; 1c, X = PF6; 1d, X = BPh4), (PTACH2COOEt)X (2X: 2a, X = Br; 2b, X = Cl; 2c, X = PF6), and (PTACH2CH2COOEt)X (3X: 3a, X = Br; 3c, X = PF6), presenting all the functional groups of the natural cationic compounds acetylcholine or trimethylglycine combined with a P-donor site suitable for metal ion coordination, were prepared and characterized by NMR, ESI-MS, and elemental analysis. The X-ray crystal structures of 1d and 2c were determined. Ligands 1c, 2b, and 3c were coordinated to Pt(II) and Ru(II) to give the cationic complexes cis[PtCl2(L)2]X2 and [RuCpCl(PPh3)(L)]X (L = 1, 2, 3, X = Cl or PF6) designed with a structure targeted for anticancer activity. The X-ray crystal structure of [CpRu(PPh3)(PTAC2H4OCOMe)Cl]PF6 (1cRu) was determined. The antiproliferative activity of the ligands and the complexes was evaluated on three human cancer cell lines. ■ INTRODUCTION attracted by molecules bearing a quaternary ammonium group, for the following reasons: • When inserted in a metal complex, they should favor the antiproliferative effect on cancer cells because of the electrostatic attraction between N+ and the polyanionic DNA. • They could exploit OCTs (organic cation transporters) expressed in the brain−blood barrier (BBB) to pass from the blood to CNS, thus acting as Trojan horses for metal ions.6 We describe here our work on synthetic analogues of two model molecules containing a quaternary ammonium group, acetylcholine and trimethylglycine. We designed a structural modification of their structure in order to synthesize derivatives preserving all the functional groups of the natural molecule, associated with a suitable coordination site for metals. The work previously reported by us and others7 about Nalkylation of PTA (1,3,5-triaza-7-phosphaadamantane) suggested that 1X, 2X, and 3X could represent appropriate, readily available candidates for our purposes. In Scheme 1 the structural analogies with the natural molecules are highlighted. There is still a great interest in medical applications of metal complexes. The present challenges of inorganic medicinal chemistry are (a) to improve the therapeutic performance of classic platinum anticancer drugs, based on over 30 years of research and successful clinical use,1 and (b) to open a new scenario by investigating the potential activity of metal drugs for the diagnosis and therapy of other pathologies, mainly neurodegenerative diseases, where an aberrant biochemistry of endogenous metals seems to have a relevant role.2 The design and synthesis of metal compounds capable of reaching the central nervous system (CNS), overcoming the physiological protecting barriers, meet both purposes. In fact traditional platinum-containing anticancer drugs do not reach therapeutic concentrations in the CNS and therefore cannot be used against brain cancer;3 for the same reason the possibility of a positive interference of exogenous metal complexes with biochemical mechanisms causing neurodegenerative diseases has just started to get attention.4 Following the consolidated idea that endogenous molecules with appropriate character could bind therapeutics and drag them into specific biological cycles,5 we looked for natural molecules suited to be introduced as ligands in Pt and Ru complexes, hopefully improving their performance related to the above-described aims. Our attention has been recently © 2014 American Chemical Society Received: December 3, 2013 Published: May 6, 2014 4881 dx.doi.org/10.1021/ic402953s | Inorg. Chem. 2014, 53, 4881−4890 Inorganic Chemistry Article N+CH2P), 56.0 (1C, N+CH2CH2CO), 60.0 (1C, N+CH2CH2CO), 70.5 (1C, NCH2N), 79.1 (2C, NCH2N+), 169.9 (1C, CO). ESI-MS: observed m/z 244, calculated 244 for C10H19N3O2P [M − Br]+. S25 °C (H2O): 700 g L−1. Synthesis of (PTAC2H4OCOMe)I, 1b. Step (i): Synthesis of IC2H4OCOMe. IC2H4OCOCH3 was obtained as a pale yellow oil through the same procedure above-described for BrC2H4OCOMe, using 2-iodoethanol (1.0 g, 5.8 × 10−3 mol) and acetic anhydride (1.2 g, 1.2 × 10−2 mol, 2 equiv). 1H NMR (400 MHz, CDCl3) δ (ppm): 2.09 (s, 3H, CH3), 3.30 (t, 3JHH = 6.0 Hz, 2H, ICH2), 4.33 (t, 3JHH = 6.0 Hz, 2H, −CH2OCOMe) ppm. Step (ii): PTA Alkylation with IC2H4OCOMe. PTA (0.062 g, 4 × 10−4 mol) was dissolved in acetone (30 mL), and the mixture was gently warmed; an excess of IC2H4OCOMe (0.17 g, 8 × 10−4 mol) was then added to the solution, and the mixture was refluxed for 15 min. The pale yellow solid (PTAC2H4OCOCH3)I was filtered off, washed with diethyl ether, and dried under vacuum. (0.06 g, 2.47 × 10−4 mol, yield 62%). Anal. Calcd for C10H19I N3O2P (MW 371): C 32.4, H 5.2, N 11.3. Found: C 32.5, H 5.4, N 11.1. IR: CO 1746 cm−1. 31 1 P{ H} NMR (121.5 MHz, d6-dmso) δ (ppm): −83.67. 1H NMR (300 MHz, d6-dmso) δ (ppm): 2.05 (s, 3H, OCOCH3), 3.15 (m, 2H, N+CH2CH2OCOCH3), 3.85 (m, 4H, NCH2P), 4.40 (m, 2H, PCH2N+ + 2H, CH2OCOCH3), δ 4.47 (d, 2H, CH2, NCH2N), 4.90 (m, 2H, CH2, NCH2N+), 5.10 (m, 2H, N+CH2N). S25 °C (H2O): 270 g L−1. Synthesis of (PTAC2H4OCOMe)PF6, 1c. A methanolic solution of KPF6 (0.17 g, 0.93 × 10−3 mol, 1.5 equiv) in 1 mL of MeOH was added dropwise to a solution of (PTAC2H4OCOMe)Br (0.2 g, 0.62 × 10 −3 mol) in the same solvent (40 mL). The solvent was slowly evaporated in a stream of nitrogen, and microcrystals of the PF6− salt were filtered off, rapidly washed with methanol, and finally dried under vacuum (1.43 g, 0.37 × 10−3 mol, yield 60%). Anal. Calcd for C10H19F6N3O2P2 (MW 389): C 30.8, H 4.9, N 10.8. Found: C 30.5, H 5.2, N 10.5. IR: CO 1746 cm−1. 31P{1H} NMR (121.5 MHz, D2O) δ (ppm): −83.33 (s), −142.7 (sept, 1JFP = 707 Hz). 1H NMR (300 MHz, D2O) δ (ppm): 1.99 (s, 3H, OCOCH3), 3.18 (m, 2H, N+CH2CH2OCOCH3), 3.80 (m, 4H, NCH2P), 4.40 (m, 2H NCH2N +2H N+CH2P + 2H N+CH2CH2OCOCH3), 4.98 (m, 4H, N+CH2N). 13 C{1H} NMR (100.57 MHz, d6-dmso) δ (ppm): 21.1 (CH3), 45.2 (d, 1 JPC = 20 Hz, 2C, NCH2P), 51.8 (d, 1JPC = 32.0 Hz, 1C, N+CH2P), 56.0 (1C, N+CH2CH2CO), 60.1 (1C, N+CH2CH2CO), 70.7 (1C, NCH2N), 79.0 (2C, NCH2N+), 170.0 (1C, CO). S25 °C (H2O): 0.74 g L−1. Synthesis of (PTAC2H4OCOMe)BPh4, 1d. A solution of NaBPh4 (0.3 g, 3.3 × 10−4 mol, 1.1 equiv) in MeOH (3 mL) was added to a solution of (PTAC2H4OCOMe)Br (0.1 g, 3 × 10−4 mol) in 20 mL of MeOH. 1d precipitated as white microcrystals, which were filtered off and washed with diethyl ether (0.09 g, 1.52 × 10−4 mol, yield 51%). The crude product was recrystallized at room temperature from acetone and diethyl ether, giving crystals suitable for X-ray analysis (see Figure 1 and Table 2). 31P{1H} NMR (121.5 MHz, d6-dmso) δ (ppm): −84.66 (s). 1H NMR (300 MHz, d6-dmso) δ (ppm): 2.00 (s, 3H, OCOCH3), 3.21 (m, 2H, N+CH2CH2OCOCH3), 3.79 (m, 4H, NCH 2 P), 4.40 (m, 2H, NCH 2 N + 2H, N + CH 2 P + 2H, N+CH2CH2OCOCH3), 5.00 (m, 4H, N+CH2N) ppm, 6.5−7.5 (m, 20H, Ph). S25 °C (H2O): 1.6 × 10−2 g L−1. Synthesis of cis-[(PTAC2H4OCOMe)2PtCl2](PF6)2, 1cPt. A solution of (PTAC2H4OCOMe)PF6 (0.11 g, 2.83 × 10−4 mol) in H2O (10 mL) was added to an aqueous solution of K2PtCl4 (0.058 g, 1.4 × 10−4 mol; 1 mL of H2O) under stirring. An off-white solid immediately started to precipitate. After 4 h, the cream-white solid was collected on a sintered glass-frit, washed with water, and dried over P2O5 (0.06 g, 5.7 × 10−5 mol, yield 40%). Anal. Calcd for C20H38Cl2F12N6O4P4Pt (MW 1044): C 23.0, H 3.7, N 8.0. Found: C 22.5, H 3.8, N 7.8. IR: CO 1745 cm−1. 31P{1H} NMR (121.5 MHz, d6-dmso) δ (ppm): −41.74 (s, 1JPtP 3495 Hz), −142.7 (sept, PF6−, 1JFP = 707 Hz). 1H NMR (300 MHz, d6-dmso) δ (ppm): 2.0 (s, 3H, OCOCH3), 2.7 (m, 2H, −N+CH2CH2OCOMe), 4.5 (bm, 10H), 5.0− 5.2 (m, 4H, N+CH2N). ESI-MS: observed m/z 377, calculated 377 for C20H38Cl2N6O4P2Pt [M − 2PF6]2+. S25 °C (H2O): 0.01 g L−1. Scheme 1 PTA and its derivatives are attracting increasing attention for medicinal applications because of their favorable properties such as stability to oxidation, small dimensions, and solubility in water.8 A group of Ru-PTA complexes called RAPTA type are particularly promising species, mainly because of their peculiar antimetastatic activity, never observed before in other metal anticancer drugs.9 ■ EXPERIMENTAL SECTION General Procedures. All the reactions were routinely performed under a dry nitrogen atmosphere. The compound PTA10 and the metal complex precursors cis-[PtBr2(PTA)2],11 [CpRu(PPh3)2Cl], and [CpRu(PPh3)(PTA)Cl]12 were prepared as described in the literature. All chemicals and solvents were used as purchased (reagent grade). NMR spectra were recorded at 25 °C on a Varian Gemini 300 MHz spectrometer (1H at 300 MHz, 13C at 75.43 MHz, 31P at 121.50 MHz) and a Varian 400 MHz (1H at 400 MHz, 13C at 100.57 MHz, 31P at 161.92 MHz). The 13C and 31P spectra were run with proton decoupling, and 31P spectra are reported in ppm relative to an external 85% H3PO4 standard, with positive shifts downfield. 13C NMR spectra are reported in ppm relative to external tetramethylsilane (TMS), with positive shifts downfield. The ESI mass spectra were acquired with a Micromass LCQDuo Finningan. Elemental analyses (C, H, N) were performed using a Carlo Erba instrument model EA1110. FT-IR spectra were recorded on a Bruker Vertex 70 FT-IR instrument (4000−400 cm−1). Synthesis of (PTAC2H4OCOMe)Br, 1a. Step (i): Synthesis of BrC2H4OCOMe. A flask containing acetic anhydride (1.6 g, 1.5 × 10−2 mol) and a drop of 98% H2SO4 was cooled in an ice-bath; previously precooled 2-bromoethanol (1.0 g, 8 × 10−3 mol) was added in the same flask at 0 °C. The mixture was left at room temperature for 20 h and subsequently transferred into a separating funnel with 30 mL of diethyl ether. The organic phase was treated with a saturated aqueous solution of NaHCO3 and a saturated aqueous solution of NaCl and finally was dried over anhydrous sodium sulfate. The final solution was concentrated under vacuum to a small volume, and the product was isolated as a pale yellow oil (1.2 g, 7.2 × 10−3 mol, yield 90%). 1H NMR (400 MHz, CDCl3) δ (ppm): 2.09 (s, 3H, CH3), 3.50 (t, 2H, 3 JHH = 6.2 Hz, BrCH2‑), 4.37 (t, 2H, 3JHH = 6.2 Hz,−CH2OCOMe). Step (ii): PTA Alkylation with BrC2H4OCOMe. PTA (0.3 g, 1.91 × 10−3 mol) was dissolved in acetone (30 mL), and the mixture was gently warmed; an excess of BrC2H4OCOMe (1.59 g, 5 equiv) was added to the solution, and the mixture was stirred under reflux for 3 h. 1a precipitated as an off-white solid. The warm mixture was filtered, and the isolated solid product was dried under vacuum (0.48 g, 1.48 × 10−3 mol, yield 78%). Anal. Calcd for C10H19BrN3O2P (MW 324): C 37.0, H 5.9, N 13.0. Found: C 37.1, H 5.9, N 12.7. IR: CO 1746 cm−1. 31 1 P{ H} NMR (121.5 MHz, d6-dmso) δ (ppm): −84.77 (s). 1H NMR (300 MHz, d6-dmso) δ (ppm): 2.05 (s, 3H, OCOCH3), 3.20 (m, 2H, N+CH2CH2OCOCH3), 3.91 (m, 4H, NCH2P), 4.41 (m, 2H, N+CH2CH2OCOCH3), 4.49 (m, 2H, NCH2N), 4.74 (m, 2H, N+CH2P), 4.98 (m, 2H, N+CH2N), 5.10 (m, 2H, N+CH2N). 13 C{1H} NMR (100.57 MHz, d6-dmso) δ (ppm): 20.8 (CH3), 45.2 (d, 1JPC = 19.9 Hz, 2C, NCH2P), 52.1 (d, 1JPC = 32.1 Hz, 1C, 4882 dx.doi.org/10.1021/ic402953s | Inorg. Chem. 2014, 53, 4881−4890 Inorganic Chemistry Article Table 2. Selected Bond Distances and Angles and Geometrical Parameters for C−H···O and C−H···π Intermolecular Interactions in 1d (Å, deg) bond distances P1−C3 P1−C5 P1−C6 O1−C8 O1−C9 O2−C9 bond angles 1.695(6) 1.698(6) 1.708(5) 1.443(6) 1.338(6) 1.176(6) C3−P1−C5 C3−P1−C6 C5−P1−C6 97.9(2) 97.5(3) 100.9(3) intermolecular interactionsa D−H i C2−H2A···O2 C5−H5A···(C29−C34)i a Figure 1. ORTEP view and atom-numbering scheme for 1d. Thermal ellipsoids are drawn at the 40% probability level. 0.97 0.97 D···A 3.370(6) 3.23 H···A D−H···A 2.46 2.92 154 162 Centroid; symmetry code (i): x+1/2, 3/2−y, −z. C{1H} NMR (100.57 MHz, d6-dmso) δ (ppm): 20.7 (CH3), 49.5 (d, JPC 19.9 Hz, 2C, NCH2P), 51.6 (d, 1JPC 32.1 Hz, 1C, N+CH2P), 56.1 (1C, N+CH2CH2 CO), 59.9 (1C, N+CH2 CH2CO), 64.5 (1C, NCH2N), 79.4 (5C, Cp), 80.9 (2C, NCH2N+), 128−138 (18C, Ph), 169.9 (1C, CO). ESI-MS: observed m/z 708, calculated 708 for C33H39ClN3O2P2Ru (M − PF6)+. S25 °C (H2O): 0.05 g L−1. Synthesis of (PTACH2COOEt)Br, 2a. A solution of PTA (0.220 g, 1.4 × 10−3 mol) in 30 mL of acetone was treated with ethyl bromoacetate (0.37 g, 2.2 × 10−3 mol, 1.6 equiv) and stirred at room temperature for 3 h. The white precipitate was filtered off and washed with acetone (0.354 g, 1.1 × 10−3 mol, yield 78%).31P{1H} NMR (121.5 MHz, d6-dmso) δ (ppm): −84.05 (s). 1H NMR (300 MHz, d6dmso) δ (ppm): 1.20 (t, 3JHH = 5 Hz, 3H, CH2CH3), 3.92 (m, 2H, N+CH2COOEt + 4H, NCH2P), 4.22 (q, 3JHH = 5 Hz, 2H, CH2CH3), 4.41 (d, 2JHH = 10 Hz, 1H, NCH2N), 4.52 (m, 1H, NCH2N + 2H, N+CH2P), 4.90 (d, 2JHH = 9 Hz, 2H, N+CH2N), 5.20 (d, 2JHH = 9 Hz, 2H, N+CH2N). S25 °C (H2O): 625 g L−1. Synthesis of (PTACH2COOEt)Cl, 2b. PTA (0.4 g, 2.6 0.10−3 mol) was dissolved in warm acetone (50 mL), and the solution was treated with 800 μL of ethyl chloroacetate (0.932 g, 7.6 × 10−3 mol, 3 equiv); the mixture was stirred at room temperature for 18 h. An off-white solid was then filtered off and washed with acetone and diethyl ether (0.44 g, 1.6 × 10−3 mol, yield 61%). Anal. Calcd for C10H19ClN3O2P (MW 280): C 42.9, H 6.8, N 15.0. Found: C 43.0, H 7.1, N 14.8. IR: CO 1745 cm−1. 31P{1H} NMR (121.5 MHz, CD3OD) δ (ppm): −81.03 (s). 1H NMR (300 MHz, CD3OD) δ (ppm): 1.32 (t, 3JHH = 5 Hz, 3H, CH2CH3), 3.95 (m, 4H, NCH2P + 2H N+CH2CO), 4.32 (q, 3 JHH = 5 Hz, 2H, CH2CH3), 4.50 (d, 2JHH = 11 Hz, 1 H, NCH2N), 13 1 Synthesis of [CpRu(PPh3)(PTAC2H4OCOMe)Cl]Br, 1aRu. To a solution of [CpRu(PPh3)(PTA)Cl] (0.1 g, 1.6 × 10−4 mol) in 25 mL of acetone was added dropwise a large excess of 2-bromoethyl acetate (10 equiv). After 24 h under stirring, 1aRu was recovered as a yellow solid, filtered off, and washed with ethyl ether (0.04 g, 4.8 × 10−4 mol, yield 30%). 31P{1H} NMR (121.5 MHz, d6-dmso) δ (ppm): 46.45 (d, PPh3, 2JPP = 43.7 Hz), −14.32 (d, 2JPP = 43.7 Hz). 1H NMR (300 MHz, d6-dmso) δ (ppm): 2.07 (s, 3H, OCOCH3), 2.70 (m, 2H, −N+CH2CH2OCOMe), 3.21 (m, 4H, NCH2P), 3.45 (m, 2H, −N+CH2CH2OCOMe), 4.42 (m, 4H, NCH2N + N+CH2P), 4.56 (s, Cp, 5H), 4.7−5.0 (m, 4H, N+CH2N), 7.35−7.50 (15H, PPh3). Synthesis of [CpRu(PPh3)(PTAC2H4OCOMe)Cl]PF6, 1cRu. A slight excess of solid 1c (0.08 g, 0.2 × 10−3 mol, 1.5 equiv) was added under stirring to a solution of [CpRu(PPh3)2Cl], (0.1 g, 0.14 × 10−3 mol) in acetone (30 mL). The mixture was refluxed for 3 h. The evaporation of the solvent to a small volume and the slow addition of diethyl ether gave a light yellow precipitate, which was filtered off and dried in air (0.095 g, 0.11 × 10−3 mol, yield 80%). Anal. Calcd for C33H39ClF6N3O2P3Ru (MW 853): C 46.5, H 4.6, N 4.9. Found: C 46.1, H 4.9, N 4.5. IR: CO 1748 cm−1. 31P{1H} NMR (121.5 MHz, d6dmso) δ (ppm): 46.50 (d, PPh3, 2JPP = 43.7 Hz), −14.49 (d, 1c, 2JPP = 43.7 Hz), −143.25 (PF6−, 1JFP = 707 Hz). 1H NMR (300 MHz, d6dmso) δ (ppm): 2.05 (s, 3H, OCOCH 3 ), 2.72 (m, 2H, −N+CH2CH2OCOMe), 3.21 (m, 4H, NCH2P), 3.43 (m, 2H, −N+CH2CH2OCOMe), 4.40 (m, 4H, NCH2N + N+CH2P), 4.56 (s, Cp, 5H), 4.8−5.0 (m, 4H, N+CH2N), 7.35−7.50 (15H, PPh3). Table 1. Crystal Data and Details of Data Collection for 1d, 1cRu, and 2c chemical formula Mr cryst syst, space group a, b, c (Å) α, β, γ (deg) V (Å3) Z μ (mm−1) cryst size (mm) no. of measd, indep, and obsd [I > 2σ(I)] reflns Rint R[F2 > 2σ(F2)], wR(F2), S no. of reflns no. of params no. of restraints Δρmax, Δρmin (e Å−3) 1d 1cRu 2c (C10H19N3O2P)+(C24H20B)− 563.46 orthorhombic, P212121 9.8011(1), 10.2689(1), 29.9161(5) (C33H39ClN3O2P2Ru)+(PF6)− 853.10 triclinic, P1̅ 9.3552(3), 14.1403(5), 14.8980(6) 68.377(2), 75.999(1), 75.979(3) 1751.87(11) 2 0.73 0.19 × 0.12 × 0.04 12 060, 6386, 5030 0.037 0.051, 0.154, 1.06 6386 443 0 0.91, −0.80 (C10H19N3O2P)+(PF6)− 389.22 monoclinic, P21/n 9.4394(2), 10.9595(2), 16.1133(3) 103.1990(7) 1622.88(5) 4 0.34 0.44 × 0.29 × 0.19 6654, 3511, 2979 0.013 0.076, 0.248, 1.13 3511 208 0 0.64, −0.47 3010.95(7) 4 0.13 0.39 × 0.26 × 0.15 5839, 5839, 4189 0.040 0.074, 0.245, 0.99 5839 370 6 0.35, −0.59 4883 dx.doi.org/10.1021/ic402953s | Inorg. Chem. 2014, 53, 4881−4890 Inorganic Chemistry Article 4.65 (d, 2JHH = 11 Hz, 1H, NCH2N), 4.67 (d, 2H, 2JHP = 7 Hz, N+CH2P), 5.10 (d, 2H, 2JHH = 9 Hz, N+CH2N), 5.39 (d, 2H, 2JHH = 9 Hz, N+CH2N). 13C{1H} NMR (100.57 MHz, d6-dmso) δ (ppm): 13.8 (CH3), 45.4 (d, 1JPC = 20.1 Hz, 2C, NCH2P), 52.7 (d, 1JPC = 33.7 Hz, 1C, N+CH2P), 59.2 (1C, N+CH2CO), 62.1 (1C, CH2CH3), 69.1 (1C, NCH2N), 79.6 (2C, NCH2N+), 162.2 (1C, COOEt). S25 °C (H2O): 910 g L−1. Synthesis of (PTACH2COOEt)PF6, 2c. (PTACH2COOEt)PF6 was obtained by adding a solution of KPF6 (0.2 g, 1.4 × 10−3 mol, 2 equiv) in 1 mL of methanol to a solution of 2a (0.23 g, 7.2 × 10−4 mol) in 20 mL of methanol. The solution was stirred at room temperature for 10 min and then slowly concentrated under nitrogen (over about 20 h) to give white microcrystals, which were filtered off and washed with methanol (0.17 g, 4.3 × 10−4 mol, yield 60%). The crude product 2c, recrystallized at room temperature from MeOH and Et2O, gave crystals suitable for Xray analysis (Figure 3, Table 4). Anal. Calcd for C10H19F6N3O2P2 Table 3. Selected Bond Distances and Angles and Geometrical Parameters for C−H···Halide Intermolecular Interactions in 1cRu (Å, deg) bond distances Ru1−C1 Ru1−P1 Ru1−P2 Ru1−Cp(centroid) Ru−C (mean) P1−C (mean) P2−C (mean) bond angles 2.455(2) 2.269(1) 2.309(1) 1.856 2.20(2) 1.846(5) 1.832(7) Cl1−Ru1−P1 Cl1−Ru1−P2 P1−Ru1−P2 Cl1−Ru−Cp(centroid) P1−Ru−Cp(centroid) P2−Ry−Cp(centroid) 89.63(4) 91.56(4) 98.20(4) 122.7 121.3 124.7 intermolecular interactionsa D−H C3−H···F4 C5−H···F1 C10−H···F6i C5−H···F1ii C6−H···F1ii C6−H C1−H···Cl1iii 0.97 0.97 0.96 0.97 0.97 0.97 0.97 D···A 3.51(1) 3.33(1) 3.25(2) 3.41(1) 3.424(8) 3.708(6) 3.805(5) H···A D−H···A 2.62 2.45 2.45 2.53 2.55 2.78 2.92 152 152 141 150 150 159 152 Symmetry code: (i) 1−x, −y, 2−z, (ii) 2−x, −y, 2−z, (iii) 1−x, 1−y, 2−z. a Table 4. Selected Bond Distances and Angles and Geometrical Parameters for C−H···X Intermolecular Interactions in 2c (Å, deg) bond distances P1−C1 P1−C4 P1−C6 O1−C8 O2−C8 O2−C9 Figure 2. ORTEP view and atom-numbering scheme for 1cRu. Thermal ellipsoids are drawn at the 40% probability level. The PF6 anion has been omitted for clarity. bond angles 1.835(3) 1.821(4) 1.834(5) 1.180(4) 1.327(4) 1.464(6) C1−P1−C4 C1−P1−C6 C4−P1−C6 95.6(1) 96.8(2) 97.4(2) intermolecular interactionsa C1−H···F3 C3−H···F2 C6−H···F4 C2−H···O1i C3−H···F1ii C6−H···F1iii C5−H···F3iii C4−H···F5iv D−H D···A H···A D-H···A 0.97 0.97 0.97 0.97 0.97 0.97 0.97 0.97 3.429(5) 3.598(6) 3.569(6) 3.233(5) 3.146(4) 3.438(5) 3.524(7) 3.515(5) 2.50 2.65 2.66 2.44 2.33 2.57 2.57 2.56 160 164 156 138 141 148 169 167 a Symmetry code: (i) 1−x, −y, 1−z., (ii) −x, 1−y, 1−z, (iii) x+1/2, 1/ 2−y, z+1/2, (iv) −x, −y, 1−z. (CH3), 47.5 (d, 1JPC = 20.6 Hz, 2C, NCH2P), 55.2 (d, 1JPC = 34.4 Hz, 1C, N+CH2P), 60.7 (1C, N+CH2CO), 63.8 (1C, CH2CH3), 71.3 (1C, NCH2N), 82.1 (2C, NCH2N+), 165.4 (1C, COOEt). ESI-MS: observed m/z 244, calculated 244 per C10H19N3O2P [M − PF6]+. S25 °C (H2O): 1.9 g L−1. Synthesis of cis-[(PTACH 2 COOEt) 2 PtBr 2 ]Br 2 , 2aPt. cis[PtBr2(PTA)2] (0.15 g, 2.24 × 10−4 mol) was suspended in MeOH (30 mL), and a large excess of BrCH2COOEt (500 μL = 0.75 g, 4.48 × 10−3 mol, 20 equiv) was added. The mixture was stirred overnight at room temperature and then taken to dryness, leaving a white residue, which was washed with MeOH (0.119 g, 1.43 × 10−4 mol, yield 64%). 31 1 P{ H}NMR (121.5 MHz, CD3OD): δ −42.12 ppm (br s, 1JPtP 3364 Hz). 1H NMR (300 MHz, CD3OD) δ (ppm): 1.35 (t, 3JHH = 5 Hz, 3H, CH2CH3), 4.20 (s, 2H, N+CH2CO), 4.32 (q, 3JHH = 5 Hz, 2H, CH2), 4.50 (d, 2JHH = 11 Hz, 1H, NCH2N), 4.67 (d, 2JHH = 11 Hz, 1H, Figure 3. ORTEP view and atom-numbering scheme for 2c. Thermal ellipsoids are drawn at the 40% probability level. (MW 389): C 30.8, H 4.9, N 10.8. Found: C 30.8, H 4.6, N 11.0. IR: CO 1745 cm−1. 31P{1H} NMR (121.5 MHz, d6-dmso) δ (ppm): −83.46 s, −142.7 sept (1JFP 707 Hz). 1H NMR (300 MHz, CD3OD) δ (ppm): 1.32 (t, 3JHH = 5 Hz, 3H, CH3), 3.9 (m, 4H, NCH2P+ 2H, N+CH2CO), 4.35 (q, 3JHH = 5 Hz, 2H, CH2), 4.50 (d, 2JHH = 11 Hz, 1H, NCH2N), 4.60 (d, 1H, NCH2N), 4.67 (d, 2JHP = 4 Hz, 2H, N+CH2P), 5.05 (d, 2JHH = 9 Hz, 2H, N+CH2N), 5.35 (d, 2JHH = 9 Hz, 2H, N+CH2N). 13C{1H} NMR (100.57 MHz, CD3OD) δ (ppm): 14.2 4884 dx.doi.org/10.1021/ic402953s | Inorg. Chem. 2014, 53, 4881−4890 Inorganic Chemistry Article (1JFP 707 Hz). 1H NMR (300 MHz, d6-dmso) δ (ppm): 1.20 (t, 3JHH = 9 Hz, 3H, CH3), 2.90 (t, 2H, N+CH2CH2CO), 3.07 (t, 2H, N+CH2CH2CO), 3.82 (m, 4H, NCH2P), 4.10 (q, 3JHH = 9 Hz, 2H, Et) 4.31 (m, 2H, N+CH2P + 1 H, NCH2N), 4.48 (d, 2JHH = 11 Hz, 1H, NCH2N), 4.80 (d, 2JHH = 11 Hz, 2H, N+CH2N), 4.95 (d, 2JHH = 11 Hz, 2H, N+CH2N). 13C{1H} NMR (100.57 MHz, CD3OD) δ (ppm): 14.4 (CH3), 26.1 (CH2CH2N+), 47.4 (d, 1JPC 21.4 Hz, 2C, NCH2 P), 54.1 (d, 1JPC 34.5 Hz, 1C, N+CH2P), 58.6 (1C, CH2CH2CO), 62.5 (1C, CH2CH3), 71.2 (1C, NCH2N), 82.2 (2C, NCH2N+), 171.3 (1C, COOEt). ESI-MS: observed m/z 258, calculated 258 for C11H21N3O2P [M − PF6]+. S25 °C (H2O): 1.6 g L−1. Synthesis of cis-[(PTACH2CH2COOEt)2PtCl2](PF6)2, 3cPt. The ligand (PTACH2CH2COOEt)PF6, 3c (0.080 g, 2. 10−4 mol, 2 equiv), was dissolved in 2 mL of water, and this solution was added to a second one obtained by dissolving K2PtCl4 (0.041 g, 1 × 10−4 mol, 1 equiv) in 1 mL of water. The milky suspension was stirred for 18 h, and then a white solid was separated by centrifugation, washed with water (2 × 2 mL), and dried under vacuum over P2O5 (0.061 g, 0.5 × 10−4 mol, yield 57%). Anal. Calcd for C22H42Cl2F12N6O4P4Pt.H2O (MW 1090): C 24.6, H 3.9, N 7.8. Found: C 24.2, H 4.0, N 7.7. IR: CO 1748 cm−1. 31P{1H} NMR (121.5 MHz, d6-dmso) δ (ppm): −41.69 (s, 1JPtP = 3425 Hz), −143.25 (PF6−, 1JFP = 707 Hz). 1H NMR (300 MHz, d6-dmso) δ (ppm): 1.20 (t, 3JHH = 9 Hz, 3H, CH3), 2.95 (m, 2H, N+CH2CH2CO), 3.4 (m, 6H, NCH2P + N+CH2CH2CO), 4.10 (q, 3JHH = 9 Hz, 2H, CH2CH3), 4.5 (m, 4H, N+CH2P + NCH2N), 5.0 (m, 4H, N+CH2N). S25 °C (H2O): 0.02 g L−1. Synthesis of [CpRu(PPh3)(PTACH2CH2COOEt)Cl]PF6, 3cRu. A slight excess of solid 3c (0.061 g, 0.15 × 10−3 mol, 1.1 equiv) was added under stirring to a solution of [CpRu(PPh3)2Cl], (0.10 g, 0.14 × 10−3 mol) in acetone (25 mL), and the mixture was refluxed for 4 h. The solvent was then removed in vacuo, leaving an orange solid, which was washed with diethyl ether, then filtered and dried in air (0.11 g, 0.12 × 10−3 mol, yield 88%). Anal. Calcd for C34H41ClF6N3O2P3Ru (MW 866.7): C 47.1, H 4.8, N 4.9. Found: C 45.1, H 4.6, N 4.9. IR: CO 1750 cm−1. 31P{1H} NMR (121.5 MHz, CD3OD) δ (ppm): 45.55 (d, PPh3, 2JPP = 43.7 Hz), −14.55 (d, 3c, 2JPP = 43.7 Hz), −143.25 (PF6−, 1JFP = 707 Hz). 1H NMR (300 MHz, CD3OD) δ (ppm): 1.29 (t, 3 J H H = 11 Hz, 3H, OCH 2 CH 3 ), 2.63 (br s, 2H, N+CH2CH2COOEt), 3.2−4.0 (br m, 6H), 4.18 (q, 3JHH = 11 Hz, 2H, OCH2CH3), 4.35 (m, 4H), 4.55 (s, Cp, 5H), 4.6−4.8 (m, 4H, N+CH2N), 7.35−7.50 (15H, PPh3). 13C{1H} NMR (300 MHz, CD3OD) δ (ppm): 14.0 (s, OCH2CH3), 42.5 (d, NCH2P, 1JPC = 20.0 Hz), 52.0 (d, N+CH2P, 1JPC = 32.0 Hz), 56.1 (s, N+CH2CH2CO2Et), 59.9 (s, N+CH2CH2CO2Et), 60.6 (s, OCH2CH3), 64.5 (s, NCH2N), 80.1 (s, Cp), 80.8 (s, N+CH2N), 137−127 (aromatics), 170.03 (s, CO). ESI-MS: observed m/z 722, calculated 722 for C34H41ClN3O2P2Ru [M − PF6]+. Crystallography. The crystallographic data for 1d, 1cRu, and 2c were collected on a Nonius Kappa CCD diffractometer at room temperature using graphite-monochromated Mo Kα radiation (λ = 0.71073 Å). Data sets were corrected for Lorentz−polarization effects; data for 1cRu were corrected also for absorption effects.13 The crystal parameters and other experimental details of the data collections are summarized in Table 1. The structures were solved by direct methods (SIR97)14 and refined by full-matrix least-squares methods with all non-hydrogen atoms anisotropic. Hydrogens were included on calculated positions, riding on their carrier atoms. In 1d, a case of substitutional disorder, i.e., a situation in which the same site in two unit cells is occupied by different types of atoms, was present, involving atoms P1 and N3. The positions of the two atoms were assigned on the basis of the highest SOF. All calculations were performed using SHELXL-9715 implemented in the WINGX system of programs.16 Selected bond distances and angles and geometrical parameters for C−H···X and C−H···π interactions for 1d, 1cRu, and 2c are given in Tables 2, 3, and 4. We have considered only contacts where C−H···X angles are greater than 130° and H···X distances are shorter than the sum of the van der Waals radii. NCH2N), 4.80−5.00 (m, 4H, N+CH2P + NCH2P), 5.15 (d, 2H, 2JHH = 9 Hz) 5.45 (d, 2H, 2JHH = 9 Hz, N+CH2N). Synthesis of cis-[(PTACH2COOEt)2PtCl2]Cl2, 2bPt. The ligand (PTACH2COOEt)Cl (0.112 g, 4 × 10−4 mol, 2 equiv) was dissolved in 1.5 mL of water, and this solution was added to a second one obtained by dissolving K2PtCl4 (0.083 g, 2 × 10−4 mol, 1 equiv) in 0.7 mL of water. A white precipitate was formed immediately. After 30 min under stirring, the solid was separated by centrifugation, washed with water (2 × 2 mL), and dried under vacuum over P2O5 (0.135 g, 1.6. 10−4 mol, yield 80%). Anal. Calcd for C20H38Cl4N6O4P2Pt (MW 825): C 29.1, H 4.6, N 10.2. Found: C 28.7, H 4.9, N 9.7. IR: CO 1746 cm−1. 31P{1H} NMR (121.5 MHz, d6-dmso) δ (ppm): −38.87 (s, 1JPtP 3489 Hz). 1H NMR (300 MHz, d6-dmso) δ (ppm): 1.22 (t, 3 JHH = 5 Hz, 3H, −CH2CH3), 4.20 (m, 4H, NCH2P + 2H N+CH2CO), 4.32 (q, 3JHH = 5 Hz, 2H, −CH2CH3), 4.40−4.70 (m, 4H), 5.00−5.30 (m, 4H). S25 °C (H2O): 0.7 g L−1. The aqueous supernatant was examined by 31P{1H} NMR, and the singlet with satellites of Pt complex (−38.9 s, 1JPtP = 3511 Hz) was the only observed signal. Synthesis of [CpRu(PPh3)(PTACH2COOEt)Cl]Cl, 2bRu. Method 1. To a solution of [CpRu(PPh3)(PTA)Cl] (0.1 g, 0.16 × 10−3 mol) in 20 mL of acetone was added dropwise a 5-fold excess of ethyl chloroacetate (0.099 g, 0.8 × 10−3 mol). The complete conversion into the final product required 20 h at room temperature. The volume was reduced to 1 mL, and the addition of diethyl ether gave a yellow precipitate of 2bRu, which was filtered and washed with ether (0.1 g, 0.13 × 10−3 mol, yield 81%). Method 2. A slight excess of solid (PTACH2COOEt)Cl (2b) (0.06 g, 0.2 × 10−3 mol, 1.5 equiv) was added under stirring to a solution of [CpRu(PPh3)2Cl] (0.1 g, 0.14 × 10−3 mol) in 30 mL of acetone. The mixture was refluxed for 6 h. The evaporation of the solvent to a small volume and the slow addition of diethyl ether gave a yellow precipitate of 2bRu, which was filtered and dried in air (0.05 g, 0.75 × 10−3 mol, yield 54%). Anal. Calcd for C33H39Cl2N3O2P3Ru (MW 743): C 53.3, H 5.3, N 5.6. Found: C 54.3, H 4.9, N 5.0. IR: CO 1750 cm−1. 31P{1H} NMR (121.5 MHz, CDCl3) δ (ppm): 46.32 (d, PPh3, 2JPP = 43.7 Hz), −14.38 (d, 2, 2JPP = 43.7 Hz). 1H NMR (300 MHz, d6-dmso): 1.35 (t, 3H, OCH2CH3, 2JHH = 11 Hz), 2.70 (m, 2H, −NCH2COOEt), 3.2− 4.0 (br m, 4H, cage), 4.18 (q, 2H, OCH2CH3, 2JHH = 11 Hz), 4.35 (m, 4H, cage), 4.56 (s, 5H, Cp), 4.8−5.0 (m, 4H, N+CH2N), 7.35−7.45 (15H, PPh3). 13C{1H} NMR (300 MHz, CDCl3) δ (ppm): 14.1 (s, CH3), 49.5 (d, NCH2P, 1JPC = 20.1 Hz), 51.6 (d, N+CH2P, 1JPC = 32.0 Hz), 57.2 (s N+CH2COOEt), 60.0 (s OCH2CH3), 65.5 (s, NCH2N), 79.4 (s, Cp), 79.8 (s, N+CH2N), 137−128 (18H, aromatic), 169.0 (s, 1C, CO). ESI-MS: observed m/z 708, calculated 708 for C33H39ClN3O2P2Ru [M − Cl]+. S25 °C (H2O): 21.5 g L−1. Synthesis of (PTACH2CH2COOEt)Br, 3a. A solution of PTA (0.200 g, 1.3 ·10−3 mol) in 30 mL of acetone was treated with ethyl 3bromopropionate (400 μL, 0.56 g, 3.1 × 10−3 mol, 2.4 equiv) and stirred at room temperature for 48 h. The white precipitate was filtered off and washed with acetone (2 × 2 mL) (0.27 g, 8 × 10−4 mol, 63%). Anal. Calcd for C11H21BrN3O2P (MW 338): C 39.1, H 6.2, N 12.4. Found: C 40.3, H 6.2, N 11.9. 31P{1H} NMR (121.5 MHz, CD3OD) δ (ppm): −82.67 (s). 1H NMR (300 MHz, CD3OD) δ (ppm): 1.25 (t, 3 JHH = 8 Hz, 3H, CH3), 2.95 (t, 2H, N+CH2CH2CO), 3.22 (t, 2H, N+CH2CH2CO), 3.9 (m, 4H, NCH2P), 4.2 (q, 3JHH = 8 Hz, 2H, Et + d, 3JHP = 5.6 Hz 2H, N+CH2P), 4.45 (d, 2JHH = 12 Hz 1 H, NCH2N), 4.6 (d, 2JHH = 12 Hz, 1H, NCH2N), 4.90 (d, 2JHH = 11 Hz, 2H, N+CH2N), 5.10 (d, 2JHH = 11 Hz, 2H, N+CH2N). ESI-MS: observed m/z 258, calculated 258 for C11H21N3O2P [M − Br]+. S25 °C (H2O): 173 g L−1. Synthesis of (PTACH2CH2COOEt)PF6, 3c. (PTACH2CH2COOEt)PF6 was obtained by adding a solution of KPF6 (0.28 g, 1.5 × 10−3 mol) in 1 mL of methanol to a solution of (PTACH2CH2COOEt)Br (0.52 g, 1.5 × 10−3 mol) in 20 mL of methanol. The solution was stirred at room temperature for 10 min and then slowly concentrated under nitrogen, giving a white solid, which was filtered off and washed with methanol (0.27 g, 7 × 10−4 mol, yield 47%). Anal. Calcd for C11H21F6N3O2P2 (MW 403): C 32.8, H 5.2, N 10.4. Found: C 33.2, H 5.4, N 10.2. IR: CO 1746 cm−1. 31 1 P{ H} NMR (121.5 MHz, d6-dmso) δ (ppm): −85.08 s, −143.2 sept 4885 dx.doi.org/10.1021/ic402953s | Inorg. Chem. 2014, 53, 4881−4890 Inorganic Chemistry Article ORTEP III17 views of 1d, 1cRu, and 2c are given in Figures 1, 2, and 3. Growth Inhibition Assays. Cell growth inhibition assays were carried out using the leukemia cell line K562 and two human ovarian cancer cell lines, A2780 and SKOV3; A2780 cells are cisplatinsensitive, and SKOV3 cells are cisplatin-resistant. Cell lines were obtained from ATCC (Manassas, VA, USA) and maintained in RPMI 1640, supplemented with 10% fetal bovine serum (FBS), penicillin (100 U mL−1), streptomycin (100 U mL−1), and glutamine (2 mM); the pH of the medium was 7.2 and incubation was performed at 37 °C in a 5% CO2 atmosphere. Cells were routinely passaged every 3 days at 70% confluence; for the adherent cell lines, 0.05% trypsin-EDTA (Lonza) was used. The antiproliferative activity of compounds was tested with the MTT assay. The cells were seeded in triplicate in 96well trays at a density of 5 × 103 in 50 μL of complete medium. Stock solutions (20 mM) of each compound were made in dmso and diluted in complete medium to give final concentrations of 0.1, 1, 10, 50, and 100 μM. Cisplatin was employed as a control for the cisplatin-sensitive A2780 cell line and for the cisplatin-resistant SKOV3. Untreated cells were placed in every plate as a negative control. The cells were exposed to the compounds, in 100 μL total volume, for 72 h, and then 25 μL of a 12 mM solution of 3-(4,5-dimethylthiozol-2-yl)-2,5diphenyltetrazolium bromide solution (MTT) was added. After 2 h of incubation, 100 μL of lysing buffer (50% DMF + 20% SDS, pH 4.7) was added to convert the MTT solution into a violet-colored formazan. After an additional 18 h the solution absorbance, proportional to the number of live cells, was measured by spectrophotometer at 570 nm and converted into % of growth inhibition.18 ppm (1b), close to the values previously reported for other NalkylPTA derivatives.19−21 In 1H NMR, the conversion of PTA into an alkyl derivative is typically characterized by an increased number of signals due to the loss of symmetry of the phosphaadamantane cage. Some signals of 1a and 1b appear complicated by the geminal coupling between the two diastereotopic protons of each CH2 group and, for P-bonded CH2, also by the coupling to that nucleus. The [M − Br]+ peak of 1a is observed by ESI-MS at the expected value of 244. In view of the coordination of ligand 1X to metal ions, noncoordinating anions are preferred in order to avoid exchange with metal ligands (e.g., metal-bonded chloride), so the bromide of 1a was exchanged with PF6− and with BPh4−, giving 1c and 1d, respectively. The solubility in water at 25 °C, remarkable for 1a (700 g/ L), decreases with the increase in the anion size (1a = 700 g/L and 1b = 270 g/L, 1c = 0.74 g/L and 1d = 1.56 × 10−2 g/L). The tetraphenylborate 1d, recrystallized with acetone and diethyl ether, gave crystals suitable for X-ray determination of crystal structure (Figure 1 and Table 2). The asymmetric unit of 1d consists of PTAC2H4OCOMe+ and BPh4− ions; the substitutional disorder, described in the experimental paragraph, makes the P1−C distances abnormally short (Table 2) and the N3−C quite long (N−C mean distance = 1.59[6] Å). Besides electrostatic forces between anions and cations, in this structure, given the absence of “good” proton donors, the different units interact with each other through weak C−H···O hydrogen bonds and through C−H··· π interactions (see Table 2). The reaction of 1c with K2PtCl4 (molar ratio 2:1) in water (Scheme 3) gave a single complex, cis- ■ RESULTS AND DISCUSSION The new ligands, as halides salts 1X (1a, X = Br and 1b, X = I), 2X (2a, X = Br and 2b, X = Cl), and 3X (3a, X = Br), can be easily prepared in a pure form because the N-alkylation of PTA is a selective process giving exclusively monoalkylated cationic derivatives, as previously reported for many PTA derivatives including MePTA19 and larger and more functionalized products.20 In general, the N-alkylation of PTA can be performed with either alkyl bromides or alkyl iodides, but the reaction is faster with iodide. When the alkylating agent bears the halide on an activated carbon atom (benzylic, allylic, or α to a carbonylic group), the reaction is faster and takes place also with chloro derivatives.21 The alkylation of PTA is generally carried out in acetone and occurs with product precipitation, which probably drives the process nearly to completeness giving fairly pure products. Synthesis and Characterization of 1a−d and Coordination to Pt(II) and Ru(II). The ligand 1a was obtained in two steps starting from 2-bromoethanol, which was first acetylated with acetic anhydride, and the resulting bromoester was then used as an alkylating agent for PTA. The iodide 1b was obtained in the same way from 2-iodoethanol (Scheme 2). The alkylation step is faster with the alkyl iodide, but the 31P NMR observation of the solution shows the formation of P-oxidated impurities, which reduce the yield of 1b. The 31P NMR signal, observed at −100 ppm for free PTA in dmso, in the products is shifted to −84.77 ppm (1a) or −83.67 Scheme 3 [PtCl2(PTAC2H4OCOMe)2](PF6)2 (1cPt), as a precipitate with low solubility in water (S25 °C(H2O) = 0.01 g L−1). It was identified by 31P NMR (−41.74 broad singlet, 1JPtP 3495 Hz, in dmso), where the observed shift of the Pt complex signal at −41.74 ppm is about 40 ppm downfield with respect to the free ligand 1c (−83.33 ppm) and about 10 ppm downfield with respect to the neutral PTA complex cis-[PtCl2(PTA)2] (31P −51.85 ppm 1JPtP 3285 Hz). These data comply with those found for other Pt complexes of N-alkylPTA ligands, e.g., cis[PtCl2(MePTA)2](PF6)2 (31P −43.51 ppm, 1JPtP 3384 Hz)7b compared with MePTAPF6 (31P −84.2 ppm). The broadness observed for the 31P NMR signal of 1cPt has been reported in many cases for metal complexes of PTA or PTA derivatives by us7b and others.7c−e,8a We did some additional NMR experiments on 1cPt in DMSO, and we found that the line broadening is not effected by concentration (the line width does not change by reducing the concentration to 1/ 10) or temperature (from 25 to 120 °C). Also, on replacing DMSO with DMF the signal does not become sharp. Scheme 2 4886 dx.doi.org/10.1021/ic402953s | Inorg. Chem. 2014, 53, 4881−4890 Inorganic Chemistry Article Scheme 4 ature led to several unidentified side products. In particular, the MePTA complex [RuCpCl(MePTA)(PPh3)]PF6 (d, 16.06, d, 46.31, 2JPP = 43.7 Hz in dmso) was occasionally observed as a side-product when reaction mixtures were refluxed, probably due to the presence of traces of water. It was previously observed that MePTA is formed by Cα−Cβ bond breaking of N-alkylPTA derivatives in the presence of water.7c We attempted to prepare also Pt complexes of 1a and 1b by alkylation of Pt-coordinated PTA, but the product signal was not observed by 31P NMR over 3 days. After prolonged reaction time, signals of P-containing oxidative degradation products started to appear in the 31P NMR. The 31P NMR spectrum of [RuCpCl(PTAC2H4OCOMe)(PPh3)]X (1cRu, X = PF6; 1aRu, X = Br) shows two doublets at about 46.5 ppm (Ru-coordinated PPh3) and −14.5 ppm (Rucoordinated ligand 1) reciprocally coupled with 2JPP = 43.7 Hz. These signals are clearly distinguishable from the corresponding ones of the reagent complexes [RuCpCl(PPh3)2] for route (i) (38.8 ppm)26 and [RuCpCl(PTA)(PPh3)]12 for route (ii) (48.16 and −34.96 ppm, 2JPP = 34.7 Hz). The solubility in water of 1c (S25 °C 0.74 g L−1) decreases upon coordination to Pt (1cPt, S25 °C 0.01 g L−1) and to Ru (1cRu, S25 °C 0.05 g L−1). Complex 1cRu was separated in a pure form by recrystallization with acetone and Et2O, which gave crystals suitable for X-ray diffraction (Figure 2, Table 3). The asymmetric unit is formed by one Ru complex and one PF6 anion (not shown in Figure 2). The ruthenium atom is in an octahedral environment since it is bound to a cyclopentadienyl ring (formally three fac positions), two phosphorus atoms, one from a triphenylphosphine and one from ligand 1, and a chloride ion. The coordination geometry of the complex is that of a three-legged “piano stool”. For comparative reasons, five structures27,12 strictly related to the present Ru complex, in which the metal ion is surrounded by PTA, Cl, TriP, and Cp ligands, were retrieved from the Cambridge Crystallographic Database.28 In these structures the Ru−P(PTA), Ru−P(TriP), Ru-Cp(centroid), and Ru−Cl distances vary in the ranges 2.280−2.314, 2.270−2.309, 1.837−1.890, and 2.449−2.466 Å, respectively, perfectly in line with the structural parameters listed in Table 3. In the crystal anions and cations are linked not only via electrostatic forces but also by a number of weak C−H···Halide interactions, listed in Table 3. Synthesis and Characterization of 2a−c and Coordination to Pt(II) and Ru(II). Ligand 2 was prepared as the ethyl esters 2X (2a, X = Br and 2b, X = Cl) by treating PTA with commercial XCH2COOEt in acetone. A similar synthesis for the methyl esters (PTACH2COOMe)X (X = Br and X = Cl) has been reported by Laguna.21,29 The signal broadening in complex 1cPt (and analogues) could be the consequence of a restricted conformational freedom around P−Pt bonds due to the presence of two ligands bearing two positive charges, which tend to keep as far as possible one from each other in order to minimize the electrostatic repulsion. The steric hindrance of the alkyl substituents on two spatially close nitrogen atoms could also limit the rotation. To support this hypothesis, it is useful to verify if in the 31P NMR of a Pt complex bearing only one 1c ligand the signal is sharp; so we did the following NMR experiment: the known complex [terpyPt(H2O)]2+ was dissolved in DMSO and 1 equiv of ligand 1c was added to give [terpyPt(1c)]2+. After 18 h the observed 31P NMR spectrum was indeed a sharp singlet with satellites at −50.8 with 1JPtP = 3599 Hz. The isotopic pattern for the [M − 2PF6]2+ ion of 1cPt, observed by ESI-MS at 377 m/z, compared with the calculated one, confirmed the composition of the Pt complex, while the value of the PtP coupling constant (3495 Hz) indicates the cis geometry. The Ru(II) coordination of ligand 1c was also successfully achieved. This result is particularly relevant because the development of Ru-based drugs is one of the most promising frontiers of research in inorganic medicinal chemistry.1a,22 For example, the peculiar pharmacological activity of [RuCl2(η6arene)(PTA)] (arene = p-cymene, toluene, benzene, benzo-15crown-5, 1-ethylbenzene-2,3-dimethylimidazolium tetrafluoroborate, ethyl benzoate, hexamethylbenzene) complexes, abbreviated RAPTA, was evaluated in mice, and it was observed that they can reduce the growth of lung metastases without action on the primary tumor growth.23 Since in our previous work on Ru-containing complexes we found that the combination of PTA and PPh3 in the same complex seems to improve the antiproliferative activity with respect to single-phosphine analogues,24 the mixed phosphine complexes [RuCpCl(PTAC2H4OCOMe)(PPh3)]X (X = Br, 1aRu; X = PF6−, 1cRu) looked like the best candidates for achieving anticancer activity. Complex 1cRu was prepared by replacing one PPh3 of [RuCpCl(PPh3)2] with ligand 1c (Scheme 4, route (i)), while the bromide 1aRu was obtained by alkylation of the Rucoordinated PTA in [RuCpCl(PTA)(PPh3)]25 (Scheme 4, route (ii)). The first route gives the pure product 1cRu as a yellow precipitate with a good yield (80%) after 3 h of reflux in acetone. The second requires 24 h at room temperature, and the yield is low (ca. 30%). In general, the alkylation of metal-bonded PTA seems to occur as a slow process (24 h) when PTA is coordinated to Ru. Attempts to accelerate the reaction by increasing the temper4887 dx.doi.org/10.1021/ic402953s | Inorg. Chem. 2014, 53, 4881−4890 Inorganic Chemistry Article series of molecules where the distance between the carbonyl carbon and the quaternary nitrogen N+ is four bonds (1X), three bonds (3X), and two bonds (2X) (Scheme 7). The availability of the three compounds will be useful for investigating the interactions of ligands and their metal complexes with acetylcholine receptors or cation transporters and establishing a structure−activity relationship. In fact it has been proposed that the affinity of a chemical species with acetylcholine receptors is related to its length.30 The reaction between 3-bromoethylpropionate and PTA in acetone produced 3a, which was collected as a white solid after 20 h. The NMR in CD3OD confirmed the structure, showing a 31 P signal at −82.67 ppm and, in 1H NMR, two signals at 2.95 and 3.22 ppm due to the alkyl chain CH2 groups besides the typical signals of the alkylated PTA cage. The PF6− salt 3c was obtained from the bromide by anion exchange with KPF6 in methanol (Scheme 8). Scheme 5 By exchange with KPF6 in methanol, the bromide 2a was converted in the PF6− salt 2c, whose X-ray crystal structure was determined (Figure 3, Table 4). The crystal structures of the analogue methyl ester bromide21 and triflate29 were previously reported. In 2c the asymmetric unit contains the PTA derivative and its counterion; the different units interact with each other through weak C−H···O/F hydrogen bonds. The reaction of the chloride 2b with K2PtCl4 in water gave the Pt complex cis-[PtCl2(PTACH2COOEt)2]Cl2, 2bPt, characterized by a 31P NMR single signal at −38.87 ppm with 1JPtP = 3489 Hz, confirming the cis geometry. The bromide analogue of this complex, cis[PtBr2(PTACH2COOEt)2]Br2, 2aPt, can be obtained by alkylation of Pt-coordinated PTA in cis-[PtBr2(PTA)2] with BrCH2COOEt (Scheme 6). The alkylation of PTA bonded to Pt has not been observed before, and it does not occur with the corresponding chloride ClCH2COOEt. Scheme 8 The reaction of 3c with K2PtCl4 in water gave the complex cis-[PtCl2(PTACH2CH2COOEt)2](PF6)2, 3cPt, characterized in 31P NMR data by a singlet at −41.69 ppm with a 1JPtP = 3425 Hz. The Ru complex 3cRu was also obtained with a good yield from the reaction of [CpRu(PPh3)2Cl] with a slight excess of solid 3c in refluxing acetone. Its 31P NMR in CD3OD shows two doublets at 45.55 ppm due to coordinated PPh3 and −14.55 ppm due to Ru-bonded 3c, reciprocally coupled with 2 JPP= 43.7 Hz. Antiproliferative Activity of 1c, 2b, 2c, 3c, 1cPt, 1cRu, 2bPt, 2cRu, and 3cPt. The antiproliferative activity of ligands 1c, 2b, 2c, and 3c and complexes 1cPt, 1cRu, 2bPt, 2cRu, and 3cPt was tested on two human ovarian cancer cell lines, A2780 and SKOV3, and on the leukemic line K562, in comparison with cisplatin, and the results are reported in Table 5. The complexes to test were designed and chosen in order to get the highest activity on the basis of previously reported characteristics, e.g., cis geometry for Pt complexes, Ru state of oxidation = 2, and chloride as metal-bonded halide (rather than bromide and iodide). Moreover all complexes tested have Cl− or PF6− as counterions so as to avoid ligand exchanges. These figures indicated that the organic free ligands 1c, 2b, 2c, and 3c do not show appreciable activity on all three lines, while their metal complexes do in some cases. The platinum complexes 1cPt, 2bPt, and 3cPt show low activity on cisplatin-resistant SKOV3 and an appreciable activity on cisplatin-sensitive A2780. These data allow us to hypothesize a cisplatin-like action for Pt complexes. Scheme 6 The ruthenium complex [CpRu(PPh3)(PTACH2COOEt)Cl]Cl, 2bRu, was prepared either by alkylation of Rucoordinated PTA in [CpRu(PPh3)(PTA)Cl] or by substitution of PPh3 with 2b in [CpRu(PPh3)2Cl], as above-mentioned for the Ru complexes of ligand 1a and 1c. As previously observed for ligand 1X, the water solubility of 2X changes with the anion X and the trend is Cl− > Br− > PF6−: 2b (S25 °C 910 g L−1) > 2a (S25 °C 625g L−1) >2c (S25 °C 1.9 g L−1). Although in general we found that the water solubility of these ligands greatly decreases upon coordination, complexes 2bPt (S25 °C 0.7 g L−1) and 2bRu (S25 °C 21.5 g L−1), where X = Cl−, maintain some aqueous solubility. Synthesis and Characterization of 3a and 3c and Coordination to Pt(II) and Ru(II). Ligand 3X, the superior homologue of 2X, was also prepared, in order to complete a Scheme 7 4888 dx.doi.org/10.1021/ic402953s | Inorg. Chem. 2014, 53, 4881−4890 Inorganic Chemistry Article Interuniversitario di Ricerca in Chimica dei Metalli nei Sistemi Biologici) for support. Table 5. Estimated IC50 (μM) of 1c, 2b, 2c, 3c, 1cPt, 1cRu, 2bPt, 2cRu, and 3cPt on A2780, SKOV3, and K562 Cell Linesa compound A2780 SKOV3 K562 1c 2b 2c 3c 1cPt 1cRu 2bPt 2bRu 3cPt cisplatin 49 ± 1 46 ± 3 47 ± 5 56 ± 4 18 ± 3 4.7 ± 1 36 ± 4 5.8 ± 0.5 17 ± 4 0.91 ± 0.08 >100 >100 >100 >100 42 ± 11 6.0 ± 0.5 47 ± 2 8.3 ± 0.8 63 ± 2 7.9 ± 3 >100 >100 >100 >100 40 ± 2 5.1 ± 0.3 66 ± 3 5.5 ± 0.2 59 ± 2 7.4 ± 1 ■ (1) (a) Barry, N. P. E.; Sadler, P. J. Chem. Commun. 2013, 49, 5106− 5131. (b) Harper, B. W.; Krause-Heuer, A. M.; Grant, M. P.; Manohar, M.; Garbutcheon-Singh, K. B.; Aldrich-Wright, J. R. Chem.Eur. J. 2010, 16, 7064−7077. (c) Wheate, N. J.; Walker, S.; Craig, G. E.; Oun, R. Dalton Trans. 2010, 39, 8113−8127. (2) Breydo, L.; Uversky, V. N. Metallomics 2011, 3 (11), 1163−1180. (3) (a) Jacobs, S.; McCully, C. L.; Murphy, R. F.; Bacher, J.; Balis, E. F. M.; Fox, E. E. Cancer Chemother. Pharmacol. 2010, 65, 817−824. (b) Bernocchi, G.; Bottone, M. G.; Piccolini, V. 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All ligands and their Pt and Ru complexes, as chloride or PF6− salts, were tested for antiproliferative activity on three human cancer cell lines, and the best performance was obtained by Ru complexes. The X-ray crystal structure of complex 1cRu was determined. These results encourage us to investigate the behavior of all these compounds as neuroactive species: the nontoxic salts 1c, 2c, 3c, and 2b could interfere with the cholinergic cascade involved in Alzheimer disease, while, after appropriate coordination, they could act as carriers for metal ions through the blood−brain barrier, allowing them to act as metallotherapeutics in the central nervous system. ■ ASSOCIATED CONTENT S Supporting Information * Crystallographic data in cif format. This material is available free of charge via the Internet at http://pubs.acs.org. Crystallographic data for the structural analysis of 1d, 2c, and 1cRu have been deposited at the Cambridge Crystallographic Data Center, 12 Union Road, Cambridge, CB2 1EZ, UK, and are available free of charge from the Director on request quoting the deposition number CCDC 960858, 960859, and 960860 for 1d, 2c, and 1cRu, respectively. ■ REFERENCES AUTHOR INFORMATION Corresponding Author *E-mail: p.bergamini@unife.it. Tel: +39 0532 455129. Fax: +39 0532 455167. Notes The authors declare no competing financial interest. ■ ACKNOWLEDGMENTS We thank Dr. T. Bernardi, Dr. E. Bianchini, and Mr. P. Formaglio for technical assistance and CIRCMSB (Consorzio 4889 dx.doi.org/10.1021/ic402953s | Inorg. Chem. 2014, 53, 4881−4890 Inorganic Chemistry Article (15) Sheldrick, G. M. SHELXL97, Program for Crystal Structure Refinement; University of Göttingen: Göttingen, Germany, 1997. (16) Farrugia, L. J. J. Appl. Crystallogr. 1999, 32, 837−838. (17) Burnett, M.N.; Johnson, C.K. 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