红外及太赫兹辐照下细胞膜生物效应的研究进展

薄文斐; 车嵘; 孔磊; 张明洁; 张晓波

doi:10.7498/aps.70.20212030

摘要

太赫兹电磁波辐照, 包括其短波段红外波辐照, 因具有无创和非电离特性在生物科学中展现出广泛和重要的应用前景. 细胞膜是生物细胞保持完整性和内稳态的重要生物屏障, 也是太赫兹辐照时电磁场首先作用到的细胞结构, 细胞膜对电磁场的响应是大部分太赫兹生物效应产生的机理. 本文首先论述了太赫兹辐照应用的安全性及其在生命医药、神经调节以及人工智能领域中应用的新前景, 然后从太赫兹电磁辐照下磷脂膜的介电响应特性、细胞膜离子通道蛋白的离子跨膜输运、磷脂膜上大分子及离子的跨膜输运、以及太赫兹辐照下细胞膜生物效应的潜在应用和作用四方面, 对太赫兹电磁辐照下细胞膜生物效应领域的研究发展进行系统论述, 同时介绍了太赫兹电磁辐照时能够开启细胞膜上压控钙离子通道、压控钾离子通道和主动运输的钙离子通道、以及在磷脂膜上产生亲水孔等科学发现. 最后, 总结并展望了太赫兹辐照下细胞膜生物效应研究的努力方向.

关键词:

Abstract

Irradiation of terahertz electromagnetic wave including its short-wave band in infrared wave shows broad and important application prospects in biological science due to its noninvasive and nonionizing nature. Cell membrane is an important biological barrier for keeping cell integrity and homeostasis, and it is also the cellular structure that electromagnetic fields act first on in the case of terahertz irradiation. The responses of cell membrane to the electromagnetic fields are the mechanisms for most of the biological effects of terahertz irradiation. First, in this paper are expatiated the application safety of terahertz irradiation and its new application prospects in life medicine, neural regulation and artificial intelligence. Then, systematically described are the researches and developments in the biological effects of cell membrane under terahertz electromagnetic irradiation from the following four aspects: the dielectric response characteristics of phospholipid membrane to terahertz electromagnetic irradiation, the transmembrane transport of ions through membrane ion channel proteins under the irradiation, the transmembrane transport of macromolecules and ions through phospholipid membrane under the irradiation, and the potential applications and role of biological effects of cell membrane under the irradiation. Meanwhile, introduced in this paper are the scientific discoveries that terahertz electromagnetic irradiation is able to activate voltage-gated calcium channels, voltage-gated potassium channels and active transport calcium channels in cell membrane and to create hydrophilic pores on the phospholipid membrane of cell membrane. Finally, the directions of future efforts to study the biological effects of cell membrane under terahertz irradiation are presented.

Keywords:

作者及机构信息

国防科技大学信息通信学院, 西安　710106

通信作者: 薄文斐, bowf@foxmail.com ; 车嵘, anion007@126.com ;

Authors and contacts

College of Information and Communication, National University of Defense Technology, Xi’an 710106, China

Corresponding author: Bo Wen-Fei, bowf@foxmail.com ; Che Rong, anion007@126.com ;

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施引文献

图 1 中心频率为30 THz的高斯脉冲垂直辐照DOPC磷脂膜时电场的分布(DOPC磷脂膜的水合程度分别为95%, 83%, 67%和47%)　(a)不同水合程度的磷脂膜在太赫兹高斯脉冲垂直辐照时电场的分布; (b) 图(a)中太赫兹辐照时磷脂膜产生的反射脉冲的电场波形放大图^[48]

Fig. 1. Electric field distribution in the case of DOPC phospholipid membrane irradiated perpendicularly by Gaussian pulse at center frequency of 30 THz. The hydration levels of the DOPC phospholipid membrane are 95%, 83%, 67% and 47%: (a) Electric field distribution in the case of different hydrated phospholipid membrane irradiated perpendicularly by terahertz Gauss pulse; (b) enlarged view of the reflected pulse electric field waveform in panel (a) due to phospholipid membrane under terahertz irradiation^[48].

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图 2 太赫兹辐照开启细胞膜压控钙离子通道, 产生跨膜输运的钙离子内流　(a) 50 ps脉冲时间、2.5 THz频率的太赫兹辐照下细胞膜压控钙离子通道模型C1, C2, ···, C12的钙离子流; (b) 图(a)中太赫兹辐照期间1 ps时间内的放大图^[14]

Fig. 2. Terahertz irradiation activates cell membrane voltage-gated calcium channels, inducing transmembrane transport calcium influx: (a) Calcium fluxes at voltage-gated calcium channel models C1, C2, ···, C12 in cell membrane under the terahertz irradiation with pulse duration of 50 ps and frequency of 2.5 THz; (b) enlarged view in 1 ps during terahertz irradiation in panel (a)^[14].

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图 3 相比于低频太赫兹正弦波辐照(图中sine)时, 低频太赫兹高斯脉冲辐照(图中Gauss)下减小对压控钙离子通道的抑制效应且伴随的系统温度增加量更小, ([Ca]i表示太赫兹电磁辐照下, 细胞膜压控钙离子通道开启产生的跨膜输运的钙离子流引起的浓度增加后的细胞内钙离子浓度, ∆T表示太赫兹辐照下细胞系统中最大温度升高值) 　(a) 太赫兹高斯脉冲辐照下相比于太赫兹正弦波辐照时[Ca]i随太赫兹辐照的电场幅值的变化曲线更加平缓, 说明减小了对压控钙离子通道的抑制效应; (b) 太赫兹高斯脉冲辐照下相比于太赫兹正弦波辐照时在引起相同[Ca]i增加量时伴随的∆T更小^[18]

Fig. 3. The reduction in the inhibition effect on voltage-gated calcium channel and in the concurrent system temperature rise in the case of low-frequency terahertz Gauss pulse irradiation (‘Gauss’ in the figure) compared with low-frequency terahertz sine wave irradiation (‘sine’ in the figure). [Ca]i is the intracellular calcium concentration after increase induced by the transmembrane transport calcium flux due to the activation of voltage-gated calcium channel in cell membrane under terahertz electromagnetic irradiation, ∆T is the maximum temperature rise in the cell system under terahertz irradiation. (a) THz Gauss pulse flattens more the relation curve of [Ca]i with terahertz-irradiated electric field amplitude compared with THz sine wave irradiation, and it indicates the reduction in the inhibition effect on voltage-gated calcium channel. (b) To raise the [Ca]i to a same amount, terahertz Gauss pulse irradiation induces much less concurrent ∆T than terahertz sine wave irradiation^[18].

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图 4 硝苯地平阻断压控钙离子通道或者EGTA减小细胞外钙离子浓度时太赫兹电磁辐照对精子活力的影响结果图. 100 μL清洗过的精子细胞培养在磷酸缓冲盐溶液中, 不再添加任何溶液时为正常组(Normal组), 在该溶液中添加30 mmol/L硝苯地平溶液时为Nifidipine组, 添加1 mmol/L EGTA溶液时为EGTA组, 添加1 mmol/L EGTA且还添加钙离子时为EGTA+Ca²⁺组. 10 min后实验组辐照60 min. 太赫兹辐照后采用计算机辅助精子分析对精子活力进行测量. 精子样本采样自10 位中度精子活力不足的病人, 每位的样本均分给各组. *p < 0.05 ^[15]

Fig. 4. Effect of terahertz electromagnetic irradiation on sperm motility in the case of blocking voltage-gated calcium channels with nifedipine or reducing the extracellular calcium concentration with EGTA. 100 μL washed sperm cells were incubated with phosphate-buffered saline with nothing (Normal), 30 mmol/L nifedipine (Nifidipine), 1 mmol/L EGTA (EGTA), or 1 mmol/L EGTA supplemented with calcium ions (EGTA+Ca²⁺). Then 10 minutes later, experimental groups were irradiated for 60 minutes. Sperm motility was measured using computer-assisted semen analysis after the terahertz irradiation. Sperm samples were taken from 10 mild asthenospermia patients and each sample was divided into all groups. *p < 0.05 ^[15]

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图 5 低频太赫兹辐照下压控钙离子通道内钙离子跨膜输运的布朗动力学仿真　(a) 压控钙离子通道蛋白的布朗动力学二维模型结构, ▲表示偶极子, ◆表示负电荷残基; (b) 不同电场幅值的1 THz重频脉冲串辐照下通道方向上钙离子跨膜输运的运动轨迹线^[55]

Fig. 5. Brownian dynamics simulation of calcium ion transmembrane transport in voltage-gated calcium channel under low-frequency terahertz irradiation: (a) Brownian dynamics two-dimensional structure model of a voltage-gated calcium channel protein. ▲ denotes dipole, ◆ denotes negative charge residues; (b) the motion trajectories of calcium ion transmembrane transport in the direction of the channel irradiated by 1 THz pulse train with different electric field amplitudes^[55].

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图 6 距离辐射源300 μm处53.53 THz电磁波(5.6 μm中红外波)辐照前以及辐照期间锥体细胞压控钾离子通道的电流-电压曲线以及动作电位波形图(辐照前的曲线标示为蓝色, 辐照期间的曲线标示为橘黄色)　(a)细胞膜压控钾离子通道对钾离子跨膜输运的电流-电压曲线; (b) 锥体细胞动作电位波形和其相位图^[19]

Fig. 6. Current-voltage curves of voltage-gated potassium channel and action potential waveform in pyramidal cells before and during high-frequency terahertz electromagnetic irradiation in midinfrared frequency range at 300 μm away. The curves before the irradiation are shown in blue, and the curves during the irradiation are shown in orange. (a) Current-voltage curves of potassium ion transmembrane transport in voltage-gated potassium channel in cell membrane. (b) Action potential waveforms and their phase plots in pyramidal cells^[19].

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图 7 太赫兹重频的皮秒脉冲串辐照下嵌有KcsA钾离子通道蛋白的磷脂双层膜片段穿孔的分子动力学仿真　(a) 嵌有KcsA钾离子通道蛋白的磷脂双层膜片段的分子动力学模型, 黄色小球表示磷脂头部基团, 浅蓝色球珠链表示磷脂分子链, 灰色螺旋结构为KcsA通道蛋白, 水分子用透明色表示; (b) 0.9 THz重频的皮秒脉冲串辐照下4.24 ns时刻水桥形成, 产生膜穿孔^[63]

Fig. 7. Molecular dynamics simulation of electroporation of phospholipid bilayer membrane inserted with a KcsA potassium channel protein irradiated by picosecond pulse trains (psPT) with terahertz repetition frequency. (a) Molecular dynamics simulation model of phospholipid bilayer membrane inserted with a KcsA potassium channel protein. The phospholipid headgroups are represented as yellow balls, the lipid chains are represented as light blue beaded chains, the KcsA channel is shown as gray helical structure, and water is shown as transparent. (b) Membrane electroporation forms by the formation of water bridge at 4.24 ns with the applied psPT with 0.9 THz^[63].

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图 8 太赫兹重频的皮秒高斯脉冲串辐照下细胞膜穿孔形成的亲水孔对跨膜输运的离子的电导的影响　(a) 0.4 THz重复频率的2.5 ps高斯脉冲串辐照单个细胞的模型示意图, θ表示球坐标系中的极角, 辐照的电场矢量表示为红色箭头; (b) 细胞膜亲水孔形成引起的细胞不同θ处细胞膜对跨膜输运的离子的电导密度随时间的变化; 电导密度的大小由右侧颜色条表示, 单位为S/m^{2 [64]}

Fig. 8. Effect of picosecond Gauss pulse train with terahertz repetition frequency on the conductance of transmembrane transport ions due to the formation of hydrophilic pores by membrane electroporation: (a) Schematic illustration of the model of a cell irradiated by 2.5 ps Gauss pulse train with repetition frequency of 0.4 THz. θ is the polar angle in spherical coordinate system, the electric field E-filed vector of irradiation is shown as red arrow. (b) Membrane conductance per area to the transmembrane transport ions at different θ of the cell versus time because of the formation of cell membrane hydrophilic pores. Conductance per area is shown by color bar on the right side in S/m^{2 [64]}.

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表 1 太赫兹辐照下细胞膜生物效应的实验详细内容

Table 1. Experimental details about the biological effects of terahertz irradiation on cell membrane.

光源类型	光源波段	光源功率及方式 (脉冲/连续)	光源极化情况	实验目的	实验载体	实验结果	参考文献
光导天线	0.1—3 mm (0.1—3 THz)	平均功率密度约 60 μW/cm², /(辐照时间60 min)	—	研究太赫兹辐照对精子的影响	精子细胞	太赫兹辐照增强精子活力(相比对照组增大21%)、增加细胞内钙离子浓度(钙离子标记物的荧光强度相比对照组增加21%); 当去掉细胞外钙离子或阻断细胞膜压控钙离子通道时, 该效应的结果与对照组相比不具有统计显著性	[15]
量子级联激光器	5—11 μm (27—60 THz)	距离激光器光源 300 μm处功率密度为0.003 μW/μm², 脉冲(100—500 ns脉宽, 10—100 kHz 重复频率, 辐照时间10—200 s)	—	研究特定波长的中红外波能否对离子通道活动、神经信号和运动感觉行为产生非热的调节效应	小鼠前额叶皮层切片中锥体细胞, 斑马鱼幼体	5.6 μm波长(53.53 THz)电磁波辐照期间能够非热地增大压控钾离子通道的钾离子流(电流-电压曲线斜率相比对照组增大9%)、使锥体细胞的动作电位波形变窄(相比对照组减小21%), 当停止辐照时调节效应消失, 再次辐照时调节效应再次出现. 对于紫外光刺激引起的斑马鱼C状弯曲的惊跳反应, 5.6 μm波长辐照抑制了弱紫外光刺激下惊跳反应、而增强了强紫外光刺激下的惊跳反应(惊跳反应中鱼尾部的角度-紫外光强度曲线斜率相比对照组增大109%, 尾部的角速度-紫外光强度曲线斜率相比对照组增大116%)	[19]
自由电子激光器	130和150 μm (2.3 和2.0 THz)	平均功率密度 0.5—20 mW/cm², 脉冲(30—100 ps脉宽, 4.6—11.2 MHz重复频率, 2.3 THz时辐照时间0.6 min, 2.0 THz时辐照60 min)	—	研究太赫兹辐照能否引起细胞膜完整性、屏障特性功能的改变	离体培养的静水椎实螺神经细胞	2.3 THz辐照能够引起细胞膜可逆的穿孔(相比对照组增大87%), 将细胞外染料分子导入细胞内, 引起细胞膜屏障特性及完整性的改变; 2.0 THz没有引起细胞膜穿孔	[41,60]
返波管	0.9—1.7 mm (0.18—0.33 THz)	3 mW/cm², /(辐照时间180 min)	—	研究太赫兹辐照对血细胞的影响	红细胞	太赫兹辐照引起红细胞渗透压的减小, 血红蛋白大分子从红细胞内释放进入细胞外溶液环境	[41]
自由电子激光器	130 μm (2.3 THz)	平均功率密度 0.5—20 mW/cm², 脉冲(30—100 ps脉宽, 4.6—11.2 MHz重复频率, 辐照时间30 s)	—	检测2.3 THz辐照下细胞膜穿孔能否由膜上激活的氧化代谢物导致	离体培养的静水椎实螺神经细胞	添加抗氧化剂后细胞膜穿孔的效应减弱(相比对照组减小93%), 抗氧化剂能够作为细胞膜通透性改变的调节因子, 保护细胞不受这一过程的不利效应的影响	[60]

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