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Synthesis, characterization, anticancer efficacy evaluation of ruthenium(II) and iridium(III) polypyridyl complexes toward A549 cells

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Abstract

A new ligand DFIP (2-(dibenzo[b,d]furan-3-yl)-1H-imidazo[4,5-f][1,10]phenanthroline) and its two complexes iridium(III) [Ir(ppy)2(DFIP)](PF6) (ppy = 2-phenylpyridine, Ir1) and ruthenium(II) [Ru(bpy)2(DFIP)](PF6)2 (bpy = 2,2′-bipyridine, Ru1) were synthesized and characterized. The anticancer effects of the two complexes on A549, BEL-7402, HepG2, SGC-7901, HCT116 and normal LO2 cells were tested by 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) method. Complex Ir1 shows high cytotoxic activity on A549, BEL-7402, SGC-7901 and HepG2, Ru1 exhibits moderate anticancer activity toward A549, BEL-7402 and SGC-7901 cells. The IC50 values of Ir1 and Ru1 toward A549 are 7.2 ± 0.1 and 22.6 ± 1.4 μM, respectively. The localization of complexes Ir1 and Ru1 in the mitochondrial, intracellular accumulation of reactive oxygen species (ROS) levels, and the changes of mitochondrial membrane potential (MMP) and cytochrome c (cyto-c) were investigated. Apoptosis and cell cycle were detected by flow cytometry. Immunogenic cell death (ICD) was used to detect the effects of Ir1 and Ru1 on the A549 using a confocal laser scanning microscope. The expression of apoptosis-related proteins was detected by western blotting. Ir1 and Ru1 can increase the intracellular ROS levels and release cyto-c, reduce the MMP, leading to the apoptosis of A549 cells and blocking the A549 cells at the G0/G1 phase. Additionally, the complexes caused a decrease of the expression of polyADP-ribose polymerase (PARP), caspase 3, Bcl-2 (B-cell lymphoma-2), PI3K (phosphoinositide-3 kinase) and upregulated the expression of Bax. All these findings indicated that the complexes exert anticancer efficacy to induce cell death through immunogenic cell death, apoptosis, and autophagy.

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Abbreviations

A549:

Human lung cells

anti-p-mTOR:

Anti-p-mammalian target of rapamycin

AKT:

Protein kinase B

Bax:

Bcl-2 associated x protein

BCA:

Bicinchoninic acid

Bcl-2:

B-cell lymphoma-2

Beclin-1:

Bcl-2-interacting protein-1

BEL-7402:

Human hepatocellular carcinoma

BH3:

Bcl-2 homology-3

bpy:

2,2′-Bipyridine

CCCP:

Carbonyl cyanide m-chlorophenyl hydrazone

CRT:

Calreticulin

cyto-c:

Cytochrome c

DAPI:

4′,6-Diamidino-2-phenylindole

DCFH-DA:

2′,7′-Dichlorodihydrofluorescein diacetate

DFIP:

2-(Dibenzo[b,d]furan-3-yl)-1H-imidazo[4,5-f][1,10]phenanthroline

DMEM:

Dulbecco’s modified Eagle’s medium

DMSO:

Dimethyl sulfoxide

ECL:

Electrochemiluminescence

FAK:

Focal adhesion kinase

FBS:

Fetal bovine serum

GSH:

Glutathione

HCT116:

Human colon cancer

HepG2:

Human hepatocellular carcinoma

HMGB1:

High mobility group box 1

HSP70:

Heat-shock protein 70 kDa

ICD:

Immunogenic cell death

JC-1:

5,5′,6,6′-Tetrachloro-1,1′,3,3′-tetraethylimiacarbocyanine iodide

LO2:

Human liver cell

MDC:

Monodansylcadaerine

MTT:

3-(4,5-Dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide

MMP:

Mitochondrial membrane potential

mTOR:

Mammalian target of rapamycin

PARP:

PolyADP-ribose polymerase

PBS:

Phosphate buffer solution

PI:

Propidium iodide

PI3K:

Phosphoinositide-3 kinase

ppy:

2-Phenylpyridine

RNase:

Ribonuclease

ROS:

Reactive oxygen species

SGC-7901:

Human gastric cancer

TMS:

Tetramethylsilane

Tris:

Tris(hydroxymethylaminomethane

Tween:

Polyoxyethylene monolaurate sorbitan

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 21877018).

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Authors and Affiliations

  1. School of Pharmacy, Guangdong Pharmaceutical University, Guangzhou, 510006, People’s Republic of China

    Lijuan Liang, Haimei Liu, Fang Yuan, Yuhan Yuan, Wenlong Li, Chunxia Huang, Jing Chen & Yunjun Liu

  2. Department of Pharmacy, Guangdong Second Provincial General Hospital, Guangzhou, 510317, People’s Republic of China

    Yan Yang

  3. Guangdong Provincial Key Laboratory of Advanced Drug Delivery, Guangdong Provincial Engineering Center of Topical Precise Drug Delivery System, Guangdong Pharmaceutical University, Guangzhou, 510006, People’s Republic of China

    Yunjun Liu

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  1. Lijuan Liang
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Liang, L., Yang, Y., Liu, H. et al. Synthesis, characterization, anticancer efficacy evaluation of ruthenium(II) and iridium(III) polypyridyl complexes toward A549 cells. J Biol Inorg Chem 28, 421–437 (2023). https://doi.org/10.1007/s00775-023-01997-0

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