A review on bioelectrical effects of cellular organelles by high voltage nanosecond pulsed electric fields

Guo Yu-Yi; Shi Fu-Kun; Wang Qun; Ji Zhen-Yu; Zhuang Jie

doi:10.7498/aps.71.20211850

Abstract

The biomedical application of high-voltage nanosecond pulsed electric fields (nsPEFs) has become an emerging interdisciplinary research field in recent years. Compared with microsecond and millisecond pulsed electric fields, high-voltage nsPEFs can not only lead the cell membrane structure to polarize and dielectric break down the cell membrane structure, i.e. membrane electroporation, but also penetrate into the cell, triggering off organelle bioelectrical effects such as cytoskeleton depolymerization, intracellular calcium ion release, and mitochondrial membrane potential dissipation. Extensive attention has been attracted from related academic communities. In this article, the following aspects are involved. First, the physical model of high-voltage nsPEFs and its bioelectrical effects on cellular organelles are introduced. Then, the existing researches of the interactions of high-voltage nsPEFs with cytoskeleton, mitochondria, endoplasmic reticulum, cell nucleus and other subcellular structure are reviewed and summarized; the relationship between the influence on cellular organelles by high-voltage nsPEFs and the biological effects such as cell death and intercellular communication is highlighted. Finally, the key technical challenges to high-voltage nsPEFs in biomedical research are condensed, followed by the prospects of future research directions.

Keywords:

Authors and contacts

1.
Division of Life Sciences and Medicine, School of Biomedical Engineering (Suzhou), University of Science and Technology of China, Suzhou 215000, China
2.
Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences, Suzhou 215000, China
3.
Faculty of Military Biomedical Engineering, Air Force Military Medical University, Xi’an 710032, China

Corresponding author: Zhuang Jie, jzhuang@sibet.ac.cn

Funds: Project supported by the National Key R&D Program of China (Grant Nos. 2019YFC0119102, 2019YFC0118004, 2020YFC0122301) .

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图 1 PEFs导致的细胞膜EP示意图

Figure 1. Schematic diagram of PEF-induced membrane electroporation.

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图 2 PEFs中哺乳动物细胞等效电路模型

Figure 2. Equivalent circuit model for the mammalian cells with the exposure to PEFs, where individual subcellular components are described by a combination of the resistor or capacitor.

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图 3 NsPEFs细胞器效应的文献发表情况

Figure 3. Literature research about the intracellular effects for cells exposured to nsPEFs.

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图 4 NsPEFs对贴壁细胞的影响. 1, 破坏细胞与细胞间连接; 2, 细胞膜电穿孔; 3, 细胞脱落

Figure 4. Effect of nsPEFs on adherent cells. 1, Disruption of the intercallular connections; 2, electroporation; 3, cell necrosis or shedding.

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图 5 NsPEFs诱导的细胞内凋亡途径

Figure 5. Apoptosis pathways for cells after exposure to nsPEFs

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表 1 nsPEFs的细胞器生物电效应总结

Table 1. Summary of effects of nsPEFs on cell organelles.

细胞器	细胞类型	脉冲宽度/ns	电场强度/(kV·cm^–1)	主要结果概述
细胞骨架	GH3, HeLa^[47]	60	12	肌动蛋白丝变短、变细、碎片化、解聚、收缩、分离, 细胞弹性降低; 微管屈曲、解聚、破碎; 微管聚合速率和聚合数量发生变化; 中间丝破坏; 细胞通透性改变; 细胞肿胀、起泡、细胞质颗粒化; 细胞间通讯受抑制; 细胞骨架的破坏受钙离子调控: 1)高钙离子浓度溶液中, nsPEFs处理会使微管解聚, 破坏肌动蛋白丝; 2) 低钙离子浓度溶液中, nsPEFs处理后微管显示正常结构
	BY-2^[48]	10	33
	Jurkat, HeLa, SV40^[49]	60	15, 60
	CHO-K1^[50]	600	19.2
	Jurkat, U937, CHO-K1^[51]	10	150
	WB-F344^[52]	100	5—35
	U87-MG^[53]	10, 100	44
	CHO^[54]	600	16.2
	GUV^[55]		3—10
	tubulin^[56]	10	20
	U2OS^[57]
	CHO-K1^[58]	10, 60	27.7, 150
	HepG2^[59]	450	8
	B16-F10^[60]	300	12, 18, 26, 40, 60
	WB-F344, WB-Ras^[61]	100	20
	U-937^[62]	60	10
线粒体	Jurkat^[63]	60	0—60	线粒体膜通透性改变, 线粒体的通透性转换孔(MPTP)不可逆过度开放; 线粒体膜电位损失; 线粒体肿胀; 线粒体膜蛋白受影响, 线粒体膜间隙蛋白 Cyt-C, AIF 释放入胞浆; 调控线粒体凋亡途径, Caspase-3表达量增加, Bax 表达量增加; 线粒体释放细胞色素C; 影响线粒体信号传导途径; ATP消耗; 胞内ROS水平升高
	N1-S1^[36]	600	0—80
	Jurkat, U-937^[46]	10	50, 150
	Jurkat^[64]	600	0—60
	HeLa S3^[65]	80	20
	HCT116, NCM460^[66]	10, 600, 800	3, 4, 5
	Jurkat, B10-2^[67]	10—300	≤ 300
	Jurkat, HL-60^[68]	10, 60, 300	150, 60, 25
	Jurkat, HL-60^[34]	10—300	15—60
	Hela^[69]	10, 20, 30, 50	40, 45
	CT-26 tumor cells^[70]	10	22
	MCA205, McA-RH7777, JurkatE6-1^[71]	100	6—25
	4T1^[72]	100	46—54
内质网	Jurkat^[73]	7, 10, 30	25	内质网穿孔、损伤; 钙离子释放, 引发胞内钙离子浓度升高; 内质网应激响应; 免疫原性细胞死亡; 肿瘤细胞内与内质网凋亡相关蛋白Caspase-3的释放量增加; 内质网凋亡信号通路起作用
	Jurkat, HL-60^[74]	60, 300	15—60
	Jurkat, HL-60^[75]	10, 60, 300	26, 40, 60, 150, 300 (10 ns); 16, 26, 40, 60 (60 ns); 40 (300 ns)
	Newly outdated platelet^[76]	300	0—30
	Cardiac cells from rats^[77]	4	10—80
	Jurkat^[15]	60	25, 50, 100
	NG108-15^[78]	4	16.2
	CHO-K1^[79]	60	3.7—30
	U937, CHO-K1, BPAE^[80]	300
	HeLa, HEK293T, C2C12^[40]	7, 10, 20	10—50
	HeLa, HEK293, MEF^[81]	14	10, 20, 25, 30, 40, 50
	MG63^[82]	60	6.7, 13.3, 16.7, 20, 26.7, 33.3
	HeLa, MEF^[83]	14, 70	80, 100 (14 ns), 30, 50, 70, 75 (70 ns)
	Bovine chromaffin cells ^[84]	5	170
	B16 F10, EL-4^[39]	200	7
	Hela^[85]	20, 500	100, 20
	Murine secondary oocytes ^[86]	10	4—10
	MEF^[87]	60—300	30, 60
	CHO-K1, NG108^[88]	300, 600	3.7, 7.4, 11, 1
细胞核	HL-60^[89]	10, 60	65 (10 ns), 25 (60 ns)	核膜穿孔; DNA双链破坏、DNA片段化; 选择性降低DNA甲基化; 核蛋白复合物改变, 抑制snRNA的生成, 改变亚核结构
	B16 F10^[18,90,91]	300	40
	Jurkat^[92]	10	150
	Jurkat, U-937^[93]	10, 300	2.25, 4.5, 150, 290
	B16F10^[60]	300	0—60
	E4 squamous cell ^[94]	300	0—60
	Jurkat^[16]	60	10, 15, 25
	N1-S1^[17]	600	0—80
	N1-S1^[95]	100	50
	CHO^[58]	10, 600	18.2, 27.7, 16.7
	HEK 293^[96]	300	25.5
	HL-60^[36]	80	20
	K562, CT26. WT^[97]	600	50
	HL60, Jurkat, ALL^[98]	10, 60, 300	26, 60, 150, 300
	B10-2, HL-60^[99]	10, 50, 60, 300	26, 60, 75, 150
溶酶体	CHO-K1^[41]	1, 20, 600	16.2	溶酶体去膜化、溶酶体损伤; 溶酶体运动受影响, 高钙离子浓度溶液下, 溶酶体迁移停止;
溶酶体	CHO-K1^[42]	600	16.2	溶酶体去膜化、溶酶体损伤; 溶酶体运动受影响, 高钙离子浓度溶液下, 溶酶体迁移停止;
囊泡	Human eosinophils ^[100]	60	36, 53	囊泡穿孔; 诱导细胞外囊泡的释放
囊泡	COS-7^[101]	50	20—300	囊泡穿孔; 诱导细胞外囊泡的释放

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Vol. 71, Issue 6 - 2022-03-20

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