Soluble Cytotoxic Ruthenium(II) Complexes with 2-Hydrazinopyridine

Article abstract of DOI:10.1134/S0036023619060020

New water soluble Ru(II) binary complex [Ru(C₅H₇N₃)(X)(H₂O)₂] with 2-hydrazinopyridine and its ternary complexes with X = dichloride, oxalate, malonate or pyrophosphate ligands have been synthesized. The complexes have been characterized using elemental analyses, mass, IR, and UV-Vis. spectroscopies, cyclic voltammetry, magnetic susceptibility, and thermal analysis. The complexes are diamagnetic and the electronic spectral data showed that peaks are due to low spin octahedral Ru(II) complexes. The optimized structures of the complexes 1–4 indicate distorted octahedral geometry with bond angles around the ruthenium atom ranged from 80.44° to 99.64°. The values of the electronic energies (?635 to ?1145 a.u.), the highest occupied molecular orbital energies (?0.181 to 0.073 a.u.) and lowest unoccupied molecular orbital energies (?0.056 to 0.167 a.u.) indicate the stability of the complexes. The complexes are polarized as indicated from the dipole moment values (9.39–14.27 Debye). The complexes have noticeable cytotoxicity with IC₅₀ (μM): 0.011–0.062 (HepG-2), 0.015–0.080 (MCF-7), 0.015–0.116 (HCT-116), and PC-3 (0.034–0.125).

Full text of DOI:10.1134/S0036023619060020

ISSN 0036-0236, Russian Journal of Inorganic Chemistry, 2019, Vol. 64, No. 6, pp. 742–754. © Pleiades Publishing, Ltd., 2019.
COORDINATION
COMPOUNDS
Soluble Cytotoxic Ruthenium(II) Complexes
with 2-Hydrazinopyridine
A. A. Solimana, *, F. A. Attabya, O. I. Alajrawyb, S. R. Majeeda, C. Sahinc, and C. Varliklid
aDepartment of Chemistry, Faculty of Science, Cairo University, Giza, 12613 Egypt
bDepartment of Applied Chemistry, College of Applied Science, University of Fallujah, Fallujah, Anbar, Iraq
cDepartment of Chemistry, Art and Science Faculty, Pamukkale University, Denizli, Turkey
dDepartment of Photonics, Izmir Institute of Technology, Urla-Izmir, 35430 Turkey
*e-mail: ahmedsoliman61@gmail.com
Received June 4, 2018; revised August 21, 2018; accepted November 27, 2018
Abstract– New water soluble Ru(II) binary complex [Ru(C5H7N3)(X)(H2O)2] with 2-hydrazinopyridine and
its ternary complexes with X = dichloride, oxalate, malonate or pyrophosphate ligands have been synthesized.
The complexes have been characterized using elemental analyses, mass, IR, and UV-Vis. spectroscopies,
cyclic voltammetry, magnetic susceptibility, and thermal analysis. The complexes are diamagnetic and the
electronic spectral data showed that peaks are due to low spin octahedral Ru(II) complexes. The optimized
structures of the complexes 1‒4 indicate distorted octahedral geometry with bond angles around the ruthe-
nium atom ranged from 80.44° to 99.64°. The values of the electronic energies (‒635 to ‒1145 a.u.), the high-
est occupied molecular orbital energies (‒0.181 to 0.073 a.u.) and lowest unoccupied molecular orbital ener-
gies (‒0.056 to 0.167 a.u.) indicate the stability of the complexes. The complexes are polarized as indicated
from the dipole moment values (9.39‒14.27 Debye). The complexes have noticeable cytotoxicity with IC50
(μM): 0.011‒0.062 (HepG-2), 0.015‒0.080 (MCF-7), 0.015‒0.116 (HCT-116), and PC-3 (0.034‒0.125).
Keywords: Ru(II) complexes, 2-hydrazinopyridine, antitumor complexes, Cytotoxicity, DFT calculations
DOI: 10.1134/S0036023619060020
INTRODUCTION
pounds were the ruthenium polypyridyl which showed
attractive antitumor cytotoxicity. These complexes
were inducing the apoptosis of the cancer cells [18].
The toxic side effects of cisplatin and the limitation
of activity against wide spectrum of cell lines with its
second generation (oxaliplatin) and third generation
(carboplatin) motivate the researchers to design and
prepare innovative metal-based anticancer drugs
[1‒2]. The most important point is improving the
strategy of the targeting by designing metal-based
complexes with ligands to increase cellular uptake and
selectivity of the drugs against the cancer cells [3‒5].
The main reason encouraging the chemists to design
and prepare ruthenium complexes as a chemothera-
peutic agent is the high selectivity for cancer cells [6].
In addition, ruthenium has unique properties, namely:
The important ruthenium complex, RAPTA-C
[Ru(η6-p-cymene)Cl2(1,3,5-triaza-7-phosphaadaman-
tane)] has been shown to possess interesting clinical
properties when the complex is applied in combina-
tion with other drugs and gives good inhibition of
tumor growth without side effects and very low doses.
The complex RDC11 [Ru(phenanthroline)(κ-C,N-
(2-phenyl-pyridine)(NCMe)2]PF6 showed similar
tumor reduction compared to cisplatin on the tumor
volume when tested against xenografted A2780 ovar-
ian cancer cells and U87 glioblastoma cells. The com-
mimic to iron can bind to serum transferrin and albu- plex [Ru(η6-arene)(ethylenediamine)Cl]+ showed
min, considered as pro-drug by reduction from the promising anticancer properties in different in vivo
inert oxidation state Ru(III) to more active oxidation models [8, 19, 20]. The kinetics of ligand exchange of
state Ru(II) in tumor tissue and this gives selective tox- metal complexes is the crucial step of hydrolysis in
icity, slow ligand exchange kinetics and the ability to aqueous solution, hence, of complexes cytotoxicity.
bind to DNA [7, 8]. Because of the octahedral geom- The hydrolysis of ruthenium complexes is very close to
etry, ruthenium has been used to build effective che- the value of platinum complexes [21]. Several ruthe-
motherapeutic agents which have lower side effects nium complexes have been prepared and used as alter-
and more selective than platinum complexes; they natives for platinum complexes in chemotherapy.
have been examined as DNA topoisomerase inhibitors Ruthenium bipyridyl complexes don’t accumulate in
[9‒17]. The most extensively studied ruthenium com- the nucleus and their cellular uptake occurs either by
742

SOLUBLE CYTOTOXIC RUTHENIUM(II) COMPLEXES
endocytosis or by active transport depending on the EXPERIMENTAL
743
structure of the complex. For example, [Ru(2,2'-
bipyridine)2Cl2] is inactive, whereas [Ru(2,2',6',2''-
terpyridine)Cl3] has good cytotoxicity against the
murine and human cancer cell lines [21]. In Continu-
ation to our work on antitumor metal complexes
[22‒24], we report here four Ru(II) complexes with 2-
hydrazinopyridine ligand as the diamine moiety and
either chloride, oxalate, malate or pyrophosphate
Materials. The chemicals used are highly pure.
Ruthenium(III) chloride monohydrate RuCl3 ⋅ H2O,
2-hydrazinopyridine hydrochloride C5H7N3, potas-
sium oxalate monohydrate K2C2O4 ⋅ H2O, malonic
acid CH2(COOH)2, and sodium pyrophosphate deca-
hydrate Na4P2O7 ⋅ 10H2O were supplied by Aldrich;
tetrabutyl ammonium hexafluorophosphate TBAPF6
ligands as the labile group. The structures of ligands was purchased from Fluka. All solvents were of analyt-
used in this study are shown in Scheme 1.
ical grade.
C3H2O42– malonate
P2O47– pyrophosphate
Scheme 1. Structures of the ligands used in this study.
Measurements. The elemental analysis for carbon, to pH 3.5 and refluxed at 90°C for 4 h under constant
hydrogen, and nitrogen was carried out at the micro- stirring to get complex 1. Complex 2 has been prepared
analytical laboratory of Cairo University, Egypt. Elec- by the addition of potassium oxalate monohydrate
trochemical data were obtained by using a CH Instru- K2C2O4 · H2O (0.18 g, 1.0 mmol) to a solution of 2-hydra-
ment 660 B Model Electrochemical Workstation. IR
measurements of the solid complexes were carried out
as KBr pellets using Jasco FTIR-460 plus and Jasco
FTIR-4000 (range 400–4000 cm–1); mass-spectral
measurements were conducted using a GCMS-QP
1000EX Shimadzu device. UV-Vis spectra were
recorded in a 1 cm path length quartz cell by using an
Optizen UV-Vis spectrophotometer. The magnetic
susceptibility measurements of the solid complexes
were carried out using a Sherwood Scientific, Cam-
bridge Science Park Cambridge-England magnetic
susceptibility balance. Thermal analysis was carried
out using a Shimadzu thermo-gravimetric analyzer
TGA-60H; under a nitrogen atmosphere (20 mL/min)
with a heating rate of 10 K/min over a temperature
range from room temperature up to 1000°C.
zinopyridine ligand and ruthenium salt while stirring.
Similarly, complexes 3 and 4 have been prepared by the
addition of malonic acid H2C3H2O4 (0.10 g, 1.0 mmol)
and sodium pyrophosphate decahydrate Na4P2O7 ·
10H2O (0.45 g, 1.0 mmol), respectively. The com-
plexes were obtained as deep-violet precipitates. Yield,
76.3 (1), 73.2 (2), 77.6 (3), and 71.4% (4).
For 1 (C5H11Cl2N3O2Ru) anal. calcd. (%): C,
18.94; H, 3.50; N, 13.25. Found (%): C, 18.87; H,
3.38; N, 13.16; mp > 300°C;
For 2 (C7H11N3O6Ru) anal. calcd. (%): C, 25.15;
H, 3.32; N, 12.57. Found (%): C, 24.99; H, 3.27; N,
12.84; mp > 300°C.
For 3 (C8H13N3O6Ru) anal. calcd. (%): C, 27.59;
H, 3.76; N, 12.07. Found (%): C, 27.42; H, 3.58; N,
11.89; mp > 300°C.
For 4 (C5H13N3O9P2Ru) anal. calcd. (%): 14.22; H,
3.10; N, 9.95. Found (%): C, 14.17; H, 3.05; N, 9.78;
mp > 300°C.
MO calculations were carried out using the
GAUSSIAN 09W software. The geometries of the sin-
glet ground state of complexes were fully optimized in
the gas phase at the B3LYP/LanL2DZ basis set.
Preparation of complexes 1–4. 2-Hydrazinopyri-
dine (0.11 g, 1.0 mmol) was dissolved separately in 10 mL
of ethanol and slightly added to RuCl3.H2O (0.21 g,
In vitro antitumor activity. The cytotoxicity tests
were carried out using the rapid colorimetric assay for
1.0 mmol) in water (10 mL). The mixture was adjusted cellular growth and survival [25]. The human tumor
RUSSIAN JOURNAL OF INORGANIC CHEMISTRY Vol. 64 No. 6 2019

744
SOLIMAN et al.
Table 1. Analytical and spectral data of the Ru(II) complexes prepared
Ʌ ,
m
m/z (P+)
Complex
Molar mass
317.14
UV-V is absorption peaks, nm
Ω
‒1 cm2 mol‒1
[Ru(C5H7N3)Cl2(H2O)2] (1)
318
1.43
310
380
π → π*
n → π*
LMCT
470‒560
[Ru(C5H7N3)(C2O4)(H2O)2] (2)
[Ru(C5H7N3)(C3H2O4)(H2O)2] (3)
[Ru(C5H7N3)(H2P2O7)(H2O)2] (4)
334.24
348.28
422.20
334
349
424
3.31
2.65
4.20
300
360
460‒580
π → π*
n → π*
LMCT
310
370
460‒560
π → π*
n → π
LMCT
300
360
460‒580
π → π*
n → π*
LMCT
* LMCT: ν (πL → Meg(σ*)), ν (σL → Meg(σ*)).
2
4
cells used are hepatocellular cancer cell line (HepG-2), the ligand spectrum has been appeared in the spectra
breast cancer cell line (MCF-7), colon carcinoma cell
line (HCT-116), and prostate carcinoma cell line (PC-3)
to test the cytotoxicity of the complexes under study.
The tumor cells were cultured in Dulbecco’s modified
Eagle’s medium (DMEM) or RPMI-1640 depending
on the type of cell line supplemented with 10% heat-
inactivated fetal bovine serum, 1% L-glutamine,
HEPES buffer and 50 μg/mL gentamycin. The cells
were incubated at 37°C in a humidified atmosphere
with 5% CO2 and were subcultured two times a week
along the experimentation. Each experiment has been
carried out in triplicate. The cytotoxicity test was car-
ried out in the Regional Centre for Mycology and Bio-
technology Al-Azhar University, Cairo, Egypt.
of all complexes as merged broad bands being shifted
to the range 3427‒3431 cm‒1 indicating the NH2
groups to participate in coordination [31]. The coordi-
nation of the NH2 groups has been also confirmed by
the shift of the bending vibrations found at 1159‒1250,
1075‒1154, and 768‒776 cm‒1 assigned for the
stretching vibrations (ρtNH2), (ρwNH2), and
(ρrNH2), respectively. The spectra of complexes 2 and
3 showed new additional bands at 1642 and 1626 cm‒1,
respectively, which assigned for the stretching vibra-
tions ν(C=O). The asymmetric and the symmetric
COO stretching vibrations have been found at
1511‒1528 and 1301‒1320 cm‒1, respectively [32, 33].
The difference (∆ν) of the asymmetric and symmetric
carbonyl stretching frequencies is larger than 200 cm‒1,
which indicates that the two carboxylate groups of the
oxalate and malonate are coordinated to ruthe-
nium(II) in cis-form [34‒36]. The IR spectrum of
complex 4 showed bands at 1187 and 1075 cm‒1
assigned to the asymmetric and symmetric stretching
vibration of the terminal ν(PO3), respectively. The
existence of ν(PO3) in the complex spectrum indicates
that [P2O7]4− ring adopts a bent configuration [18,
34‒36]. The experimental and calculated IR spectra
of the ligand and complexes 1–4 are shown in
Figs. S1–S5 in SI. There is agreement between the
experimental and calculated spectra as shown in Table 2.
The difference between the experimental and calcu-
lated results may be explained on the basis of the dif-
ferent methodology used for getting the data; the
experimental data are measured in the solid state while
the calculated data were deduced from the isolated
RESULTS AND DISCUSSION
The analytical and spectral data of the prepared
ruthenium complexes 1–4 are given in Table 1. The
complexes are air stable and soluble in water. It is
worth to mention that Ru(III) has been reduced to
Ru(II) during the complex formation and this is consis-
tent with the reported amine and phosphine complexes
such as [Ru(bipy)3]Cl2] [26], [RuCl2(PPh3)3] [27],
[Ru(tpy)(bpy)(4-NH2-py)](PF6)2] [28], [Ru(phen)2Cl2] ·
2H2O
[29],
[Ru(bipy)(DABA)(NCS)2],
and
[Ru(hzpy)(DABA)(NCS)2] [30] have been reported to
reduce Ru(III) to Ru(II) which is stabilized by com-
plexation.
IR Spectra
The experimental and calculated IR peaks of the
Ru(II) complexes prepared are given in Table 2. The
ν(N‒H) stretching vibrations peak of the amino
groups of 2-hydrazinopyridine at 3305‒3256 cm‒1 in gaseous molecular state.
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SOLUBLE CYTOTOXIC RUTHENIUM(II) COMPLEXES
745
peak at m/z = 349 (M+), peaks at m/z = 313
(M-2H2O), m/z = 217 (ML), and m/z = 110 for the
2-hydrazinopyridine ligand. The spectrum of complex 4
(FW = 422.20) gave a parent peak at m/z = 424 (M+),
peaks at m/z = 388 (M+-2H2O), m/z = 212 (ML), m/z =
160 (H2P2O6), and m/z = 110 for the 2-hydrazinopyr-
idine ligand. The spectra of complexes 1–4 showed
also peaks at m/z 98, 99, 100, 101, and 102 which are
assigned to the stable ruthenium isotopes [37].
Table 2. Experimental and calculated vibrational frequen-
cies for Ru(II) complexes, cm‒1
Complex
Exp.
Calc.
Assignment
2-Hydrazinopyri- 3395, 3308 3508, 3444 ν(N‒H)
dine
1246
1086
804
1299
1193
856
ρtNH2
ρwNH2
ρrNH2
3431
1249
1055
768
3535
1290
1157
776
ν(N–H)
ρtNH2
ρwNH2
ρrNH2
Electrochemical Data
1
2
The electrochemical measurements were obtained
by cyclic voltammetry in a cell containing glassy car-
bon working electrode, a Pt wire counter electrode, an
Ag wire reference electrode, and supporting electro-
lyte, i.e. 0.1 M TBAPF6 in DMF. The HOMO and
LUMO energy levels of the complexes were calculated
by using ferrocene (0.65 V vs. Ag/Ag+) as the internal
standard and the maxima of first oxidation and reduc-
tion potentials, respectively [38]. The obtained data
were summarized in Table 3.
The cyclic voltammogram of 2-hydrazinopyridine
ligand exhibited one oxidation (1.09 V) and one
reduction peaks (‒1.30 V) assigned to the hydrazine
and pyridine parts of the ligand, respectively. The dif-
ferential cyclic voltammogram of complex 1 shows
one broad oxidation peak at 1.29 V which is attributed
to the ruthenium metal as the main character and the
contribution of 2-hydrazinopyridine ligand to the
highest occupied molecular orbital (HOMO) (Fig. 1).
The reduction peaks of ‒1.05 V and ‒1.70 V are
attributed to the 2-hydrazinopyridine ligand and chlo-
ride, respectively. The contribution of Ru and 2-hydraz-
inopyridine ligand to HOMO and 2-hydrazinopyri-
dine ligand and malate to LUMO energy states in
complex 3 exhibits the same trend as complex 1. The
HOMO and LUMO energy levels of the complexes are
in the range from 5.28 to 5.44 eV and 3.10 to 3.21 eV,
respectively. Consecutive cyclic behaviors of the com-
plexes presented no significant change in peak cur-
rents and potentials of anodic and cathodic areas.
3430
1250
1154
776
3540
1280
1151
715
ν(N–H)
ρtNH2
ρwNH2
ρrNH2
1624
1653
ν(C=O)
3429
1247
1115
774
3420
1263
1148
721
ν(N–H)
ρtNH2
ρwNH2
ρrNH2
3
4
1626
1648
ν(C=O)
3427
1159
1246
775
3418
1148
1234
771
ν(N–H)
ρtNH2
ρwNH2
ρrNH2
1187, 1075 1176, 1068 ν(O‒P‒O)
892 881 ν(P=O)
Mass Spectral Analysis
The major fragmentations in the mass spectra of the
prepared Ru(II) complexes are present in Figs. S6‒S9 in
SI. The spectrum of complex 1 (FW = 317.14) showed
a parent peak at m/z = 318 (M+), peaks at m/z = 281
(M-2H2O), m/z = 209 (ML) and m/z = 110 for the
2-hydrazinopyridine ligand. The spectrum of complex
2 (FW = 334.25) gave a parent peak at m/z = 334 (M),
peaks at m/z = 297 (M-2H2O), m/z = 210 (ML), and
m/z = 110 for the 2-hydrazinopyridine ligand. The
Electronic Spectra
The electronic spectral measurements were
recorded using the aqueous solution of complexes 1–
4 in the 200‒1100 nm range. The experimental and
calculated absorption spectra of complexes 1–4 are
spectrum of complex 3 (FW = 347.27) gave a parent shown in Figs. S10‒S13 in SI. The resulted data are
Table 3. Electrochemical data of the 2-hydrazinopyridine ligand and the complexes 1 and 3 in DMF
Eox1, V
Ered1, V
Ered2, V
Molecules
HOMO, eV
LUMO, eV
2-Hydrazinopyridine
1.09
1.29
1.13
–1.30
–1.05
–0.94
–
–1.70
–1.21
–5.24
–5.44
–5.28
–2.85
–3.10
–3.21
1
3
RUSSIAN JOURNAL OF INORGANIC CHEMISTRY Vol. 64 No. 6 2019

746
SOLIMAN et al.
given in Table 1. The spectra showed absorption bands
in the range 260‒310 nm and 360‒380 nm which can
be assigned to the π → π* and n → π* transitions of the
pyridine ring group of the 2-hydrazinopyridine ligand,
respectively [39]. The spectra showed also shoulders at
460‒580 nm which are due to LMCT (ligand-to-
metal charge transfer) within octahedral species,
ν4(σL → Meg(σ*)) transition [39, 40]. It is worth to
mention that both ν1(πL → Mt2g(π*)) and ν3(σL →
Mt2g(π*)) transitions have not been observed as the
metal t2g is completely filled in low spin complexes
[39]. The possibility of back donation from Ru(II) to
the 2-hydrazinopyridine ligand (MLCT) is also
inferred from the computational studies (vide infra).
The d–d transitions within the low spin octahedral
ruthenium(II) d6-complexes are very weak and have
not been not observed because of the high intensity of
the strong LMCT [39‒41]. The configurations of the
computed main excitation electronic transition as well
as the oscillator strength of Ru(II) complexes are given
in Table 4. The predicted transitions are in good agree-
ment with the experimental values. The experimental
and calculated electronic transitions for complex 4 are
presented in Fig. 2; the data for complexes 1–3 are
shown in Figs. S14‒S16 in SI. The assignment of the
calculated orbital excitations to the experimental
bands was based on the relative HOMO and LUMO
energies involved in the electronic transitions.
1.5
0.4
–0.7
–1.8
–2.9
1.8 1.2 0.6
0
–0.6 –1.2 –1.8 –2.4
Potential, V
Fig. 1. Differential cyclic voltammogram of
[Ru(C H N )Cl (H O) ] (1) measured in DMF solution
5
7
3
2
2
2
–1
containing 0.1 M TBAPF with scan speed of 100 mVs
.
6
netic which can be explained on the fact that Ru(II) is
divalent (d6), (t2g eg ) in a low spin octahedral geome-
6
0
try with all electrons are paired [42].
Thermal Studies
In order to investigate the thermal stability of com-
plexes, the thermogravimetric analysis (TGA) of the
complexes has been performed. The derivative ther-
mogravimetric analysis (DrTGA) has been also used
to describe the steps ranges with better precision. The
data obtained for complexes 1–4 are shown in
Figs. S17–S20 in SI. The TG curves of the Ru(II) com-
plexes were carried out under nitrogen atmosphere
Magnetic Susceptibility Measurements
Magnetic susceptibility measurements of Ru(II) 20 mL/min with a heating rate of 10°C/min over a
complexes 1–4 showed that all complexes are diamag- temperature range from room temperature up to
Table 4. Main excitation energies (nm), electronic transition configurations, and oscillator strengths (f) of the Ru(II) com-
plexes
Oscillator
strengths
Complex Calcd., nm
Exp., nm
Composition (>10%)
265
359
410
310
380
470
0.075
0.098
0.009
HOMO-3 → LUMO (59%), HOMO → LUMO + 5 (28%)
HOMO-2 → LUMO (50%), HOMO-1 → LUMO (30%)
HOMO → LUMO (44%), HOMO-2 → LUMO + 3 (38%)
1
2
263
328
389
432
300
360
0.079
0.014
0.105
0.025
HOMO-3 → LUMO + 1 (66%)
HOMO-1 → LUMO + 3 (63%)
HOMO → LUMO + 1 (46%), HOMO-2 → LUMO + 7 (28%)
HOMO → LUMO (51%), HOMO-1 → LUMO (26%)
460
580
285
367
459
582
310
370
460
560
0.063
0.143
0.025
0.028
HOMO-6 → LUMO (50%), HOMO → LUMO + 4 (29%)
HOMO-2 → LUMO + 2 (53%), HOMO-2 → LUMO + 2 (34%)
HOMO → LUMO + 3 (34%), HOMO-1 → LUMO + 3 (34%)
HOMO → LUMO (42%), HOMO-2 → LUMO (39%)
3
4
264
371
450
460
300
360
460
580
0.067
0.033
0.089
0.021
HOMO-3 → LUMO (68%)
HOMO-1 → LUMO + 2 (66%)
HOMO → LUMO (46%)
HOMO-1 → LUMO + 5 (41%), HOMO-2 → LUMO (30%)
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SOLUBLE CYTOTOXIC RUTHENIUM(II) COMPLEXES
Molecular orbitals
747
L + 4 = 0.169 a.u.
L + 3 = 0.228 a.u.
L + 2 = 0.210 a.u.
371 nm
L + 1 = 0.191 a.u.
450 nm
250 nm
L = 0.169 a.u.
H = 0.074 a.u.
H – 1 = 0.062 a.u.
H – 2 = 0.047 a.u.
H – 3 = 0.034 a.u.
H = 0.027 a.u.
Fig. 2. The calculated electronic transition (TD-DFT/B3LYP/LANL2DZ) of [Ru(C H N )(H P O )(H O) ] complex 4 (iso-
5
7
3
2
2
7
2
2
value = 0.02).
1000°C. All complexes have been decomposed in three 834–1000 K is assigned to loss of two chlorides with
steps. The first decomposition step of complex 1 has mass losses of 23.09% (calcd. 22.32%). For complex 2:
been observed at 305–511 K and is assigned to loss of first decomposition step, 296–393 K, loss of two coordi-
two coordinated water molecules with mass loss of nated water molecules with mass loss of 9.64%
11.42% (calcd. 11.32%). The second decomposition (calcd. 10.77%); second decomposition step, 394–504 K,
step observed at 512–833 K is assigned to loss of the loss of the ligand (C5H7N3) with mass loss of 32.07%
ligand (C5H7N3) with mass loss of 35.11% (calcd.
(calcd. 32.63%); third decomposition step, 505–998 K,
34.27%) and the last decomposition step observed at loss of two carbon dioxide with mass losses of 26.61%
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748
SOLIMAN et al.
5.0
4.5
4.0
3.5
3.0
2.5
2.0
1.5
1.0
0.5
0
0.0005
0
–0.0005
–0.0010
–0.0015
–0.0020
–0.0025
TGA mg
DrTGA mg/s
–0.0030
–0.0035
Temperature, ꢀC
Fig. 3. TG and DTG plot of [Ru(C H N )Cl (H O) ] complex 1.
5
7
3
2
2
2
(calcd. 22.37%). For complex 3: first decomposition complexes as the starting reactants in each step
step, 303–466 K, loss of two coordinated water mole- [45‒47].
cules with mass loss of 10.88% (calcd. 10.31%); second
decomposition step, 467–551 K, loss of ligand
Theoretical Studies
(C5H7N3) with mass loss of 30.17% (calcd. 31.23%);
last decomposition step, 552‒720 K, loss of (C3H2O4)
with mass loss of 29.88% (calcd. 29.22%). For com-
plex 4: first decomposition step, 295‒376 K, loss of
two coordinated water molecules with mass losses of
8.54% (calcd. 8.49%); second decomposition step,
459‒505 K, loss of H2P2O6 with mass loss of 37.55%
(calcd. 37.73%); last decomposition step, 506‒999 K,
loss of C5H7N3 with mass losses of 26.61% (calcd.
25.70%).
The energy minimization studies were carried out
using the GAUSSIAN 09W software program. Molec-
ular geometries of the singlet ground state of the com-
plexes were fully optimized in the gas phase at the
B3LYP/LanL2DZ basis set [48, 49]. The optimized
geometries of complexes 1‒4 are given in Fig. 4.
Selected bond angles and bond lengths are given in
Table S2. The angles between Ru(ΙΙ) and the sur-
rounded atoms of chloride and oxygen of secondary
ligands vary from (80.44° to 94.25°) and dihedral
angles from (169.64° to 175.04°) which are deviated
from those of perfect octahedral (90°, 180°) indicating
distorted octahedral structures [50]. The Cl‒Ru‒Cl
bond angle in complex 1 (94.25°) is comparable with
the ruthenium(II) diamine dichloride complex
(92.66°) in cis-[RuCl2(dppme)(2-diaminocyclohex-
ane)] [51]. The O‒Ru‒O bond angles in complexes 2
and 3 (83.30° and 82.02°); respectively arecomparable
with the ruthenium (II) diamine oxalate complex
(78.70°) in [Ru(C2O4)(C10H14)(C7H5NO4)] [52].
The N‒Ru‒N bond angles (80.22°–81.48°) are
also deviating from (90°). A comparison of the calcu-
lated Ru‒Cl and Ru‒N bond lengths with those of
reported Ru(II) complexes involving bidentate
N-donor ligands reveals that the average values found
for Ru‒Cl (2.493 Å) is consistent with the range of the
reported values {2.473 (p-cymene)Ru(curcumi-
nato)chloro} [49].The calculated Ru‒O bond lengths val-
ues found (2.051‒2.117 Å) are consistent with the range of
reported values {2.083 [Ru-(C2O4)(C10H14)(C7H5NO4)]}
The residue in all complexes has found to be the
metallic ruthenium with mass 30.38% (calcd.
31.76%), 25.55% (calcd. 26.34%), 29.10% (calcd.
28.93%), and 27.30% (calcd. 27.59%) for complexes 1,
2, 3, and 4, respectively [43, 44].
The thermal stability of the complexes is indicated
from their relatively high overall activation energies
(101‒254 kJ mol‒1). The steps of decomposition are
consistent with the proposed complexes formulae. The
thermogram of complex 1 is shown in Fig. 3 as an exam-
ple. The thermodynamic parameters have been calcu-
lated using the integral method, the Coats–Redfern and
Approximation method, Horowitz–Metzger [45, 46]
method considering the Ozawa correction [47].
The decomposition temperature ranges with mass
losses are given in Table 5. The values of the thermo-
dynamic parameters of the complexes are given in
Table S1 shown in SI. The values of the entropy of the
formation (ΔS*) of Ru(II) complexes were negative in
all decomposition steps which is consistent with the of
structural complexity (arrangement) of the activated
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2019

SOLUBLE CYTOTOXIC RUTHENIUM(II) COMPLEXES
Table 5. Thermogravimetric decomposition data of Ru(II) complexes
749
Mass loss, found
Assignment of the
removed species
Metallic residue,
found/calcd.
DTA max, K
Complex
FW
TG range, K
(calcd.), %
1
317.14
305‒511
512‒833
834‒1000
296‒393
394‒504
505‒998
303‒466
467‒551
552‒720
295‒376
459‒505
506‒999
406
611
11.42/11.32
35.11/34.27
23.09/22.32
9.64/10.77
32.07/32.63
26.61/26.34
10.88/10.31
30.17/31.23
29.88/29.22
8.54/8.49
2H2O
C5H7N3
Cl2
Ru
30.38/31.76)
1248
347
500
770
354
510
640
347
500
770
2
3
4
334.24
348.28
422.19
2H2O
C5H7N3
2CO2
Ru
31.68/30.23)
2H2O
C5H7N3
C3H2O4
Ru
29.10/28.93)
2H2O
H2P2O6
C5H7N3
RuO
27.30/(27.59)
37.55/37.73
26.61/25.70
Table 6. The calculated quantum chemical parameters of Ru(II) complexes by DFT/B3LYP method and LanL2DZ basis set
Electronic
energy, a.u
Complex
HOMO, a.u
LUMO, a.u
η
ΔE, a.u
D.M., Debye
2-Hydrazinopyridine
‒0.216
‒0.182
‒0.181
‒0.187
0.073
‒0.025
‒0.056
‒0.060
‒0.060
0.167
0.095
0.063
0.060
0.059
0.047
0.191
0.126
0.121
0.118
0.094
‒359
‒635
‒982
‒1022
‒1145
1.46
9.39
14.27
14.00
13.27
1
2
3
4
[53].The calculation of atomic charges explains the A)/2, where I is the ionization energy, A is the electron
potential donor and acceptor property of atoms [54]. affinity, and I ‒ A is the gap between the HOMO and
The higher charge density in the 2-hydrazinopyridine
ligand is allocated on nitrogen atoms of amine groups.
This high charge explains their expected donor prop-
erties. Ruthenium has positive charge and acts as the
acceptor atom. The increasing in the negative charges
in the nitrogen atoms of the 2-hydrazinopyridine
ligand in all complexes may be explain as MLCT from
the ruthenium to the π* orbitals of the 2-hydrazinopy-
ridine ligand. The dipole moment is an indicator of
the polarity of molecules, the resulted data from cal-
culations showed that the complexes are more polar-
ized than the 2-hydrazinopyridine ligand. This is
inferred from the values of the dipole moments
(9.39‒14.27 Debye) for complexes and (1.46 Debye)
for the 2-hydrazinopyridine ligand [22‒24].
LUMO energy levels. The higher the value of I ‒ A the
harder is the molecules and vice versa [56, 57]. The η
values and ΔE (HOMO‒LUMO) are given in Table 6.
The transition is easier in complexes as compared
with the 2-hydrazinopyridine ligand as indicated from
ΔE of complexes (0.094‒0.126) to that of the 2-hydra-
zinopyridine ligand (0.191) and hence the complexes
are softer (η = 0.047‒0.063) than the 2-hydrazinopy-
ridine ligand (0.095) [55]. The negative values of the
HOMO and the LUMO energies in the complexes
indicate their stability [55, 56, 58]. The isodensity sur-
face plots of the HOMO and the LUMO for 2-hydra-
zinopyridine ligand and complex 1 are shown in Fig. 5.
Natural Bond Orbital (NBO) calculations were per-
formed [59]. According to NBO analysis for complex 1,
the electronic configuration of ruthenium is: [core]
5s0.22 4d7.14 5p0.15 5d0.02 6p0.34, 36 core electrons, 7.87
valence electrons, and 0.03 Rydberg electrons, which
gives 43.90 total electrons and +0.132 e charge on
ruthenium atom. The occupancies of ruthenium 4d
The calculated electronic energy of the complexes as
well as their dipole moments are tabulated in Table 6.
The electronic energies of the complexes (‒635 to
‒1145 a.u.) indicating that the complexes are more
stable than the 2-hydrazinopyridine ligand (electronic
energy = ‒359 a.u.) [22‒24, 55]. The calculated
HOMO and LUMO energies of the complexes 1‒4
are given in Table 6. The hardness η values indicate the
ease or difficulty to donate; it is calculated as η = (I ‒
orbitals are d 1.33; d 1.22; d 1.09;
1.58 and
dz2
dx2 −y2
xy
xz
yz
1.92. The 4d-electron population of Ru(II) oxidation
sate is 7.14 which indicates ligand-to-dRu electron
RUSSIAN JOURNAL OF INORGANIC CHEMISTRY Vol. 64 No. 6 2019

750
SOLIMAN et al.
–0.508
–0.542
0.152
–0.622
–0.448
–0.455
–0.485
2-Hydrazinopyridine (C5H7N3)
[Ru(C5H7N3)Cl2(H2O)2] (1)
–0.607
–0.453
–0.603
–0.462
–0.733
0.442
0.461
–0.598
–0.715
–0.703
[Ru(C5H7N3)(C3H2O4)(H2O)2] (3)
[Ru(C5H7N3)(C2O4)(H2O)2] (2)
–0.401
–1.071
0.458
–0.601
–1.036
[Ru(C5H7N3)(H2P2O7)(H2O)2] (4)
Fig. 4. Optimized molecular structure and atomic charges of Ru(II) complexes prepared; Carbon (gray), Nitrogen (blue), Chlo-
rine (green), Oxygen (red), Phosphorous (orange) and Ruthenium (deep green). Hydrogen atoms are omitted.
transfer. Therefore, the natural charge of Ru(III) ion is Similar trends are shown by complexes 2‒4 with Ru
reduced to Ru(II), which supports the higher com- 4d populations 7.00‒7.04 confirming the ligand-to-
plexation ability of the former ion towards ligand. metal electron transfer [59].
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SOLUBLE CYTOTOXIC RUTHENIUM(II) COMPLEXES
751
LUMO = –0.056
LUMO = –0.025
E = 0.126
E = 0.191
HOMO = –0.216
HOMO = –0.182
Fig. 5. The isodensity surface of 2-hydrazinopyridine ligand (left) and [Ru(C H N )Cl (H O) ] complex 1 (right) and energy
5
7
3
2
2
2
splitting (isovalue 0.02).
The transition energy of the complexes has been as the main character. Therefore, the electronic tran-
calculated from TD-DFT (time-dependent density sition of the type π → π* within complex 1 may be
functional linear response theory). The electron den- arisen from the HOMO states of high Cl(π) character
to LUMO states with high L(π*) character. The ruthe-
nium % contribution to the HOMO states varies from
2 to 6% by Ru(t2g) as the main character (except H-1
and H-2 which have 84 and 81% contribution)
through Ru(t2g) and Ru(eg), respectively, which gives
rise to the possibility of MLCT from Ru(t2g) to either
(Cl)(π*) and/or L(π*). On the other hand, the % con-
tribution of Ru to the LUMO states varies from 2 to
47% (except L + 2 and L + 3 in which the contribution
of Ru is 55%) which points to the possibility of LMCT
from Cl(π*) and/or L(π*) to Ru(eg) [22‒24, 55]. The
% contribution and the main characters of Ru, Cl, ox,
ma, PPi, and 2-hydrazinopyridine ligand to the differ-
ent HOMO and LUMO states in complexes 2‒4
showed more or less the same trend as complex 1.
sities in ligand are localized on the pyridine part which
may point to a mixed π → π* and n → π* transition
[56]. The energies of HOMO sates (H to H-4), the %
contribution and the main characters of the 2-hydraz-
inopyridine ligand, Cl, ox, ma, PPi as well as ruthe-
nium are calculated for complexes 1‒4 and tabulated
in Table S3 shown in SI. It has been found that in com-
plex 1, the % contribution of chloride to the HOMO
states (H to H-4) varies in a wide range from 9 to 86%
with the main character is Cl(π). On the other hand,
the % contribution of chloride to LUMO states (L to
L + 4) is much lower (0‒14%). The % contribution of
2-hydrazinopyridine ligand in complex 1 to the
HOMO states has been found to be low and varies
from 4 to 8% through L(π) as the main character. The
2-hydrazinopyridine ligand % contribution to LUMO
states has been found to be much higher than to the
The molecular electrostatic potential (MEP) of
HOMO states and varies from 8 to 98% through L(π*) complexes has been calculated and shown in Fig. 6,
RUSSIAN JOURNAL OF INORGANIC CHEMISTRY Vol. 64 No. 6 2019

752
SOLIMAN et al.
Fig. 6. Molecular electronic potential (MEP) of the 2-hydrazinopyridine ligand and Ru(II) complexes 1‒4 (isocontour value =
0.0004) mapped with ESP. Hydrogen atoms are omitted for simplicity.
with the red regions indicate an electrophilic reactivity
and the blue regions indicate a nucleophilic reactivity.
The nitrogen atoms of the 2-hydrazinopyridine ligand
with their negative (red) regions are the reactive sites
for electrophilic attack [22‒24]. On contrary, the neg-
ative (red) regions in complexes are mainly localized
over the chlorine and oxygen atoms for oxalate, malate
and pyrophosphate ligands.
In vitro Cytotoxicity
In vitro cytotoxic activities of the complexes 1‒4
were determined in aqueous solutions against the
HepG-2 (hepatocellular carcinoma cell line), MCF-7
(human breast adenocarcinoma cell line), PC-3
(prostate carcinoma cell line), and HTC-116 (colon
carcinoma cell line). The IC50 values of the tested
complexes are given in Table 7. The complexes have
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SOLUBLE CYTOTOXIC RUTHENIUM(II) COMPLEXES
Table 7. IC50 values of Ru(II) complexes
753
Complex
HepG-2
PC-3
HCT-116
MCF-7
1
2
3
4
0.027 0.014
0.071 0.022
0.078 0.027
0.088 0.006
0.038 0.012
0.034 0.011
0.125 0.008
0.117 0.004
0.012 0.006
0.136 0.019
0.134 0.007
0.154 0.006
0.034 0.004
0.109 0.008
0.034 0.006
0.112 0.007
good cytotoxicity with IC50 (μM) against HepG-2
(0.027‒0.088), MCF-7 (0.034‒0.112), PC-3
(0.034‒0.125), and HCT-116 (0.012-0.154) cell lines
(Figs. S21 and S22, see SI). The complexes are prom-
ising antitumor candidates because of their high solu-
bility in water which may ease their injection and/or
may enhance the chance of oral administration trial.
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