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Inhibition of VDAC1 prevents Ca2+-mediated oxidative stress and apoptosis induced by 5-aminolevulinic acid mediated sonodynamic therapy in THP-1 macrophages

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Abstract

Ultrasound combined with endogenous protoporphyrin IX derived from 5-aminolevulinic acid (ALA-SDT) is known to induce apoptosis in multiple cancer cells and macrophages. Persistent retention of macrophages in the plaque has been implicated in the pathophysiology and progression of atherosclerosis. Here we investigated the effects of inhibition of voltage-dependent anion channel 1 (VDAC1) on ALA-SDT-induced THP-1 macrophages apoptosis. Cells were pre-treated with VDAC1 inhibitor 4,4′-diisothiocyanostilbene-2,2′-disulfonic acid (DIDS) disodium salt for 1 h or downregulated VDAC1 expression by small interfering RNA and exposed to ultrasound. Cell viability was assessed by MTT assay, and cell apoptosis along with necrosis was evaluated by Hoechst 33342/propidium iodide staining and flow cytometry. Levels of cytochrome c release was assessed by confocal microscope and Western blot. The levels of full length caspases, caspase activation, and VDAC isoforms were analyzed by Western blot. Intracellular reactive oxygen species generation, mitochondrial membrane permeability, and intracellular Ca2+ [Ca2+]i levels were measured with fluorescent probes. We confirmed that the pharmacological inhibition of VDAC1 by DIDS notably prevented ALA-SDT-induced cell apoptosis in THP-1 macrophages. Additionally, DIDS significantly inhibited intracellular ROS generation and apoptotic biochemical changes such as inner mitochondrial membrane permeabilization, loss of mitochondrial membrane potential, cytochrome c release and activation of caspase-3 and caspase-9. Moreover, ALA-SDT elevated the [Ca2+]i levels and it was also notably reduced by DIDS. Furthermore, both of intracellular ROS generation and cell apoptosis were predominately inhibited by Ca2+ chelating reagent BAPTA-AM. Intriguingly, ALA-treatment markedly augmented VDAC1 protein levels exclusively, and the downregulation of VDAC1 expression by specific siRNA also significantly abolished cell apoptosis. Altogether, these results suggest that VDAC1 plays a crucial role in ALA-SDT-induced THP-1 macrophages apoptosis, and targeting VDAC1 is a potential way regulating macrophages apoptosis, a finding that may be relevant to therapeutic strategies against atherosclerosis.

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Abbreviations

ALA:

5 aminolevulinic acid

BAPTA-AM:

1,2-bis (2-aminophenoxy) ethane-N,N,N’,N’-tetraaceti acid tetrakis (acetoxymethylester)

DIDS:

4,4′-diisothiocyanostilbene-2,2′-disulfonic acid

HEPES:

4-(2-Hydroxyethyl)-1-piperazineethanesulfonic acid

IMM:

Inner mitochondrial membrane

NAC:

N-acetyl-l-cysteine

NAO:

Acridine orange 10-nonyl bromide (nonyl acridine orange)

PpIX:

Protoporphyrin IX

ROS:

Reactive oxygen species

SDT:

Sonodynamic therapy

THP-1:

A human acute monocytic leukemia cell line

VDAC1:

Voltage-dependent anion channel 1

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (81101164, 81171483, 81371709) and the Scientific and Technical Key Task of Heilongjiang Province, China (GC10C306). This work was also supported by the National key clinical specialist construction Programs of China.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Cardiology, The First Affiliated Hospital, Cardiovascular Institute, Harbin Medical University, 23 Youzheng Street, Harbin, 150001, Heilongjiang, China

    Haibo Chen, Yang Yang, Shuyuan Guo, Huan Wang, Wei Wang, Haobo Xu, Jianting Yao, Bicheng Li & Ye Tian

  2. Department of Pathophysiology, The State-Province Key Laboratories of Biomedicine-Pharmaceutics of China, Key Laboratory of Cardiovascular Research, Ministry of Education, Harbin Medical University, Harbin, 150081, Heilongjiang, China

    Weiwei Gao, Zhen Tian & Ye Tian

  3. Department of Interventional Radiology and Vascular Surgery, Peking University First Hospital, Xi Shi Ku Street No. 8, Xi Cheng District, Beijing, 100034, China

    Shuisheng Zhang

  4. Laboratory of Photo- and Sono-theranostic Technologies and Condensed Matter Science and Technology Institute, Harbin Institute of Technology, Harbin, 150081, Heilongjiang, China

    Qi Zhou & Zhiguo Zhang

  5. Materials Research Institute, The Pennsylvania State University, University Park, PA, 16802, USA

    Wenwu Cao

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  1. Haibo Chen
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  2. Weiwei Gao
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Chen, H., Gao, W., Yang, Y. et al. Inhibition of VDAC1 prevents Ca2+-mediated oxidative stress and apoptosis induced by 5-aminolevulinic acid mediated sonodynamic therapy in THP-1 macrophages. Apoptosis 19, 1712–1726 (2014). https://doi.org/10.1007/s10495-014-1045-5

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