Neuronal growth and development promoted by low-intensity roadband terahertz radiation

Ma Shao-Qing; Gong Shi-Xiang; Zhang Wei; Lu Cheng-Biao; Li Xiao-Li; Li Ying-Wei

doi:10.7498/aps.71.20220636

Abstract

Terahertz waves are located in the energy level range of hydrogen bonding and van der Waals forces, and can directly couple with proteins to excite the nonlinear resonance effect of proteins. Therefore, terahertz wave can affect the conformation of proteins, the structure and function of neurons. Primary cerebral cortex neurons of SD rats are cultured in vitro. Neurons are radiated 3 days by THz wave with 0.3–3.0 THz in frequency and 100 μW in power; the growth and development indicators of neurons (Cell body area, total length of process) are recorded. At the end of a radiation programme, Western blotting is used to detect the protein expressions of GluA1, GluN1, postsynaptic density protein-95 (PSD-95) and synaptophysin 38 (SYP-38). After the first day of terahertz wave radiation, the cell area is increased by 144.9% (P < 0.05); on the second day and third day of terahertz wave radiation, the growth value of the total length of neuronal neurites are increased by 65.1% (P < 0.05) and 109.4% (P < 0.05), respectively. After the three-day terahertz wave irradiation, the protein expressions of GluA1 and SY-38 are increased by 38.1% (P < 0.05) and 19.2% (P < 0.05), respectively. In addition,some results show below. 1) The use of low-intensity broadband terahertz wave in this study will not cause the cortical neurons to die, and will not affect their regular growth. 2) Low-intensity broadband terahertz radiation can promote the growth of cortical neuron cell bodies and processes, but the effects on cortical neuron cell bodies and processes are different. This may be related to the developmental cycle of cultured cortical neurons in vitro, and there is a cumulative effect on the promotion of neuronal processes by low-intensity broadband terahertz. 3) The promotion of neuronal growth and development by low-intensity broadband terahertz wave radiation may be related to the proportion of AMPA receptor subtypes and the expression of presynaptic specific protein SY-38. These results herald a specific-frequency and specific-energy terahertz radiation can be developed into a novel neuromodulation technology for the treatment or intervention of diseases such as neurodevelopmental disorders.

Keywords:

Authors and contacts

1.
School of Information Science and Engineering, Yanshan University, Qinhuangdao 066004, China
2.
Hebei Key Laboratory of Information Transmission and Signal Processing, Qinhuangdao 066004, China
3.
Henan International Key Laboratory for Noninvasive Neuromodulation, Xinxiang Medical University, Xinxiang 453000, China
4.
State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China

Corresponding author: Li Xiao-Li, xiaoli@bnu.edu.cn ; Li Ying-Wei, lyw@ysu.edu.cn

Funds: Project supported by the National Natural Science Foundation of China (Grant No. 61827811), the Natural Science Foundation of Hebei Province, China (Grant No. F2020203099), the Hebei Key Laboratory Project, China (Grant No. 202250701010046), and the Hebei Province Introduced Personnel Studying Abroad Project, China (Grant No. C20200364)

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References

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Cited By

图 1 实验平台、实验协议和太赫兹波衰减测试　(a)太赫兹辐射神经元实验平台; (b)太赫兹辐射神经元实验协议; (c)太赫兹波穿透培养液后的时域图; (d)太赫兹波穿透培养液后的频域图

Figure 1. Experimental platform, protocol and terahertz wave attenuation test: (a) Terahertz radiation neuron experimental platform; (b) experimental protocol for terahertz radiation neurons; (c) time domain diagram of terahertz wave after penetrating culture medium; (d) frequency domain map of terahertz wave after penetrating culture medium.

DownLoad: Full-Size Img PowerPoint

图 2 太赫兹辐射前后神经元的胞体面积和突起总长度变化　(a)太赫兹辐射1 d后对照组和太赫兹组神经元生长发育状态; (b)太赫兹辐射2 d后对照组和太赫兹组神经元生长发育状态; (c)太赫兹辐射3 d后对照组和太赫兹组神经元生长发育状态(t检验显著性差异: $ p < 0.05 $, *; $ p < 0.01 $, **)

Figure 2. Changes in cell body area and total neurite length of neurons before and after terahertz radiation: (a) The growth and development status of neurons in the control group and the terahertz group after 1 d of terahertz radiation; (b) the growth and development status of neurons in the control group and the terahertz group after 2 d of terahertz radiation; (c) the growth and development status of neurons in the control group and the terahertz group after 3 d of terahertz radiation(significance of t-test:$ p < 0.05 $, *; $ p < 0.01 $, **).

DownLoad: Full-Size Img PowerPoint

图 3 太赫兹辐射时间与神经元胞体面积和突起总长度的相关性　(a)对照组和太赫兹组神经元胞体面积增长均值误差曲线; (b)对照组和太赫兹组神经元突起总长度增长均值误差曲线

Figure 3. Correlation between terahertz radiation time and neuronal cell body area and total neurite length: (a) The mean error curve of neuronal cell body area growth in the control group and the terahertz group; (b) the mean error curve of the total length of neurites in the control group and the terahertz group.

DownLoad: Full-Size Img PowerPoint

图 4 太赫兹辐射前后神经元相关蛋白表达变化　(a) GluA1蛋白表达变化; (b) GluN1蛋白表达变化; (c) SY38蛋白表达变化; (d) PSD-95蛋白表达变化 (t检验显著性差异: $ p < 0.05 $, *; $ p < 0.01 $, **)

Figure 4. Changes of neuron-related protein expression before and after terahertz radiation: (a) Changes of GluA1 protein expression; (b) changes of GluN1 protein expression; (c) expression changes of SY38 protein; (d) changes of PSD-95 protein expression (significance of t-test:$ p < 0.05 $, *; $ p < 0.01 $, **).

DownLoad: Full-Size Img PowerPoint

[1]	Giovanni A, Capone F, di Biase L, Ferreri F, Florio L, Guerra A, Marano M, Paolucci M, Ranieri F, Salomone G, Tombini M, Thut G, Di Lazzaro V 2017 Front. Aging Neurosci. 9 189 Google Scholar
[2]	Lui JH, Hansen DV, Kriegstein AR 2011 Cell 146 18 Google Scholar
[3]	Jones S R, Kerr C E, Wan Q, Pritchett D L, Hämäläinen Moore C I 2010 J. Neurosci. 30 13760 Google Scholar
[4]	Kanaan N M, Pigino G F, Brady S T, Lazarov O, Binder L I, Morfini G A 2013 Exp. Neurol 246 44 Google Scholar
[5]	Van Battum E Y, Brignani S, Pasterkamp R J 2015 Lancet Neurol. 14 532 Google Scholar
[6]	MacLeod D, Dowman J, Hammond R, Leete T, Inoue K, Abeliovich A 2006 Neuron 52 587 Google Scholar
[7]	Tang F R, Yu P P, Wang L, Guo S, Yang Q 2017 Acta. Anat. Sin. 48 1 Google Scholar
[8]	郁盛雪, 屈文慧, 隋海娟, 金迎新, 金向楠, 金英 2013 中国药理学通报 29 126 Google Scholar Yu S X, Qu W H, Sui H J, Jin Y X, Jin X N, Jin Y 2013 Chin. Pharmacol. Bull. 29 126 Google Scholar
[9]	Zorkina Y, Abramova O, Ushakova V, Morozova A, Zubkov E, Valikhov M, Melnikov P, Majouga A, Chekhonin V 2020 Molecules 25 5294 Google Scholar
[10]	Cullen CL, Young KM 2016 Front. Neural. Circuits 10 26 Google Scholar
[11]	Zhang N, Xing M, Wang Y, Tao H, Cheng Y 2015 Neuroscience 311 284 Google Scholar
[12]	Bashir S, Uzair M, Abualait T, Arshad M, Khallaf RA, Niaz A, Thani Z, Yoo WK, Túnez I, Demirtas-Tatlidede A, Meo SA 2022 Mol. Med. Rep. 25 109 Google Scholar
[13]	Hu Y, Zhong W, Wan J M, Yu A C 2013 Ultrasound. Med. Biol. 39 915 Google Scholar
[14]	Peng X Y, Zhou H 2021 Acta Phys. Sin. 70 240701 Google Scholar
[15]	Tan S Z, Tan P C, Luo L Q, Chi Y L, Yang Z L, Zhao X L, Zhao L, Dong J, Zhang J, Yao B W, Xu X P, Tian G, Chen J K, Wang H, Peng R Y 2019 Biomed. Environ. Sci. 32 739 Google Scholar
[16]	Andrey S, Sergey V P 2013 Bioelectromagnetics 34 133 Google Scholar
[17]	Olshevskaya J S, Kozlov A S, Petrov A K, Zapara T A, Ratushnyak A S 2010 Phys. Sci. 5 177
[18]	Olshevskaya J S, Kozlov A S, Petrov A K, Zapara T A, Ratushnyak A S 2009 J. Higher Nervous Activ. 59 353
[19]	Guo Z Y, Li C Z, Li X J, Wang Y L, Mattson M P, Lu C B 2013 NeuroReport 24 492 Google Scholar
[20]	Wang J G, Wang Y L, Xu F, Zhao J X, Zhou S Y, Yu Y, Chazot P L, Wang X F, Lu C B 2016 Acta Pharmacol. Sin. 37 303 Google Scholar
[21]	Tiziana M, Rosanna M, Augusto M, Massimo P, Stefano L, Annalisa D 2022 Radiation 2 100 Google Scholar
[22]	He Y F, Chen J Y, Knab, Zheng W J, Markelz A G 2010 IEEE Trans. Terahertz. Sci. Technol. 3 149 Google Scholar
[23]	Sun L, Zhao L, Peng R Y 2021 Mil. Med. Res. 8 28
[24]	Cherkasova O P, Fedorov V I, Nemova E F, Pogodin A S 2009 Opt. Spectrosc. 107 534 Google Scholar
[25]	Kummer E, Ban N 2021 Nat. Rev. Mol. Cell. Biol. 22 307 Google Scholar
[26]	Masayoshi T 2007 Nat. Photonics 1 97 Google Scholar
[27]	Zhao X, Zhang M, Liu Y, Liu H, Ren K, Xue Q, Zhang H, Zhi N, Wang W, Wu S 2021 iScience 24 103485 Google Scholar
[28]	Stuart C C, Leah K, Mark F 2006 Curr. Opin. Neurobiol. 16 288 Google Scholar
[29]	Jonas P, Racca C, Sakmann B, Seeburg P H, Monyer H 1994 Neuron 12 1281 Google Scholar
[30]	Kater S B, Mills L R 1991 J. Neurosci. 14 891 Google Scholar
[31]	Greger I H, Watson J F, Cull-Candy S G 2017 Neuron 94 713 Google Scholar
[32]	Sun S, Igor T, Jeffrey V, Michael C 2012 J. Radiat. Res. 53 159 Google Scholar
[33]	Titushkin I A, Rao V S, Pickard W F, Moros G, Shafirstein G, Cho M R 2009 Radiat. Res. 172 725 Google Scholar
[34]	张欣欣, 何明霞, 赵晋武, 陈勰宇, 刘立媛, 卢晓云, 田甜, 陈孟秋, 王璞 2020 中国激光 47 0207023 Google Scholar Zhang X X, He M X, Zhao J W, Chen X Y, Liu L Y, Lu X Y, Tian T, Chen M Q, Wang P 2020 Chin. J. Lasers 47 0207023 Google Scholar
[35]	Kao H T, Ryoo K, Lin A, Janoschka S R, Augustine G J, Porton B 2017 Eur. J. Neurosci. 45 1085 Google Scholar
[36]	Fornasiero E F, Bonanomi D, Benfenati F, Valtorta F 2010 Cell. Mol. Life. Sci. 67 1383 Google Scholar
[37]	Bottauscio O, Chiampi M, Zilberti L 2015 IEEE Trans. Magn. 51 7400504 Google Scholar
[38]	Anush D, Armenuhi H, Anna N, Erna D, Sinerik A 2012 Electromagn. Biol. Med. 31 132 Google Scholar
[39]	Sulatsky M I, Duka M V, Smolyanskaya O A 2014 Phys. Wave Phenom. 22 197 Google Scholar
[40]	查彩慧 2016 博士学位论文(广州: 暨南大学) Cha C H 2016 Ph. D. Dissertation (Guangzhou: Jinan University) (in Chinese)
[41]	Melinda K K, Christopher G L, Vincent L, Hersh L, Bonnie L F 2010 J. Vis. Exp. 45 e2354 Google Scholar

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