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Article

Electrical Stimulation Increases the Secretion of Cardioprotective Extracellular Vesicles from Cardiac Mesenchymal Stem Cells

by
Haitao Zhang
1,
Yan Shen
1,
Il-man Kim
2,
Yutao Liu
1,
Jingwen Cai
1,
Adam E. Berman
1,
Kent R. Nilsson
3,
Neal L. Weintraub
1 and
Yaoliang Tang
1,*
1
Medical College of Georgia, Augusta University, Augusta, GA 30912, USA
2
Cell Biology and Physiology, School of Medicine, Indiana University, Indianapolis, IN 47405, USA
3
Medical College of Georgia, Augusta University/University of Georgia Partnership, Athens, GA 30602, USA
*
Author to whom correspondence should be addressed.
Cells 2023, 12(6), 875; https://doi.org/10.3390/cells12060875
Submission received: 19 January 2023 / Revised: 6 March 2023 / Accepted: 8 March 2023 / Published: 11 March 2023
(This article belongs to the Special Issue The Role of Oxidative Stress in Cardiovascular Diseases)
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Abstract

Clinical trials have shown that electric stimulation (ELSM) using either cardiac resynchronization therapy (CRT) or cardiac contractility modulation (CCM) approaches is an effective treatment for patients with moderate to severe heart failure, but the mechanisms are incompletely understood. Extracellular vesicles (EV) produced by cardiac mesenchymal stem cells (C-MSC) have been reported to be cardioprotective through cell-to-cell communication. In this study, we investigated the effects of ELSM stimulation on EV secretion from C-MSCs (C-MSCELSM). We observed enhanced EV-dependent cardioprotection conferred by conditioned medium (CM) from C-MSCELSM compared to that from non-stimulated control C-MSC (C-MSCCtrl). To investigate the mechanisms of ELSM-stimulated EV secretion, we examined the protein levels of neutral sphingomyelinase 2 (nSMase2), a key enzyme of the endosomal sorting complex required for EV biosynthesis. We detected a time-dependent increase in nSMase2 protein levels in C-MSCELSM compared to C-MSCCtrl. Knockdown of nSMase2 in C-MSC by siRNA significantly reduced EV secretion in C-MSCELSM and attenuated the cardioprotective effect of CM from C-MSCELSM in HL-1 cells. Taken together, our results suggest that ELSM-mediated increases in EV secretion from C-MSC enhance the cardioprotective effects of C-MSC through an EV-dependent mechanism involving nSMase2.
Keywords: electrical stimulation; intracellular communication; extracellular vesicle; nSMase2; hypoxia electrical stimulation; intracellular communication; extracellular vesicle; nSMase2; hypoxia

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MDPI and ACS Style

Zhang, H.; Shen, Y.; Kim, I.-m.; Liu, Y.; Cai, J.; Berman, A.E.; Nilsson, K.R.; Weintraub, N.L.; Tang, Y. Electrical Stimulation Increases the Secretion of Cardioprotective Extracellular Vesicles from Cardiac Mesenchymal Stem Cells. Cells 2023, 12, 875. https://doi.org/10.3390/cells12060875

AMA Style

Zhang H, Shen Y, Kim I-m, Liu Y, Cai J, Berman AE, Nilsson KR, Weintraub NL, Tang Y. Electrical Stimulation Increases the Secretion of Cardioprotective Extracellular Vesicles from Cardiac Mesenchymal Stem Cells. Cells. 2023; 12(6):875. https://doi.org/10.3390/cells12060875

Chicago/Turabian Style

Zhang, Haitao, Yan Shen, Il-man Kim, Yutao Liu, Jingwen Cai, Adam E. Berman, Kent R. Nilsson, Neal L. Weintraub, and Yaoliang Tang. 2023. "Electrical Stimulation Increases the Secretion of Cardioprotective Extracellular Vesicles from Cardiac Mesenchymal Stem Cells" Cells 12, no. 6: 875. https://doi.org/10.3390/cells12060875

APA Style

Zhang, H., Shen, Y., Kim, I.-m., Liu, Y., Cai, J., Berman, A. E., Nilsson, K. R., Weintraub, N. L., & Tang, Y. (2023). Electrical Stimulation Increases the Secretion of Cardioprotective Extracellular Vesicles from Cardiac Mesenchymal Stem Cells. Cells, 12(6), 875. https://doi.org/10.3390/cells12060875

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