Issue

Vol. 16 (2024)

Active Micro-Nano-Collaborative Bioelectronic Device for Advanced Electrophysiological Recording

https://doi.org/10.1007/s40820-024-01336-1
Yuting Xiang
Department of Chemistry, Zhejiang‑Israel Joint Laboratory of Self‑Assembling Functional Materials, ZJU‑Hangzhou Global Scientific and Technological Innovation Center, Zhejiang University, Hangzhou 310058, People’s Republic of China
Keda Shi
Department of Lung Transplantation and General Thoracic Surgery, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou 310003, People’s Republic of China
Ying Li
School of Basic Medical Sciences, Zhejiang Chinese Medical University, Hangzhou 310053, People’s Republic of China
Jiajin Xue
General Surgery Department, Children’s Hospital, Zhejiang University School of Medicine, National Clinical Research Center for Children’s Health, Hangzhou 310052, People’s Republic of China
Zhicheng Tong
Department of Orthopedics, The Fourth Affiliated Hospital, Zhejiang University School of Medicine, Yiwu 322005, People’s Republic of China
Huiming Li
Department of Orthopedics, The Fourth Affiliated Hospital, Zhejiang University School of Medicine, Yiwu 322005, People’s Republic of China
Zhongjun Li
Department of Obstetrics and Gynecology, The Tenth Affiliated Hospital, Southern Medical University, Dongguan 523059, People’s Republic of China
Chong Teng
Department of Orthopedics, The Fourth Affiliated Hospital, Zhejiang University School of Medicine, Yiwu 322005, People’s Republic of China
Jiaru Fang
School of Electronics and Information Technology, Sun Yat-Sen University, Guangzhou 510006, People’s Republic of China
Ning Hu
Department of Chemistry, Zhejiang‑Israel Joint Laboratory of Self‑Assembling Functional Materials, ZJU‑Hangzhou Global Scientific and Technological Innovation Center, Zhejiang University, Hangzhou 310058, People’s Republic of China

Corresponding Author: Ning Hu

huning@zju.edu.cn

Nano-Micro Letters, Vol. 16 (2024), Article Number: 132

Abstract

The development of precise and sensitive electrophysiological recording platforms holds the utmost importance for research in the fields of cardiology and neuroscience. In recent years, active micro/nano-bioelectronic devices have undergone significant advancements, thereby facilitating the study of electrophysiology. The distinctive configuration and exceptional functionality of these active micro-nano-collaborative bioelectronic devices offer the potential for the recording of high-fidelity action potential signals on a large scale. In this paper, we review three-dimensional active nano-transistors and planar active micro-transistors in terms of their applications in electro-excitable cells, focusing on the evaluation of the effects of active micro/nano-bioelectronic devices on electrophysiological signals. Looking forward to the possibilities, challenges, and wide prospects of active micro-nano-devices, we expect to advance their progress to satisfy the demands of theoretical investigations and medical implementations within the domains of cardiology and neuroscience research.


Highlights:
1 The factors affecting electrophysiological recordings from active micro-nano-collaborative bioelectronic devices were discussed in terms of principle and fabrication.
2 An overview of the applications of active micro-nano-collaborative bioelectronic devices in cardiomyocytes and neurons was further presented.
3 The challenges faced by active micro-nano-collaborative bioelectronic devices in intracellular electrophysiological studies and their prospective biomedical applications are discussed.

Keywords

Active micro/nano collaborative bioelectronic device Three-dimensional active nano-transistor Planar active micro-transistor Electrophysiology
Xiang, Yuting, Keda Shi, Ying Li, Jiajin Xue, Zhicheng Tong, Huiming Li, Zhongjun Li, Chong Teng, Jiaru Fang, and Ning Hu. 2024. “Active Micro-Nano-Collaborative Bioelectronic Device for Advanced Electrophysiological Recording”. Nano-Micro Letters 16 (February):132. https://doi.org/10.1007/s40820-024-01336-1.
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References
  1. M. Jia, H. Dechiruji, J. Selberg, P. Pansodtee, J. Mathews et al., Bioelectronic control of chloride ions and concentration with Ag/AgCl contacts. APL Mater. 8, 091106 (2020). https://doi.org/10.1063/5.0013867
  2. P.R.F. Rocha, P. Schlett, U. Kintzel, V. Mailänder, L.K.J. Vandamme et al., Electrochemical noise and impedance of Au electrode/electrolyte interfaces enabling extracellular detection of glioma cell populations. Sci. Rep. 6, 34843 (2016). https://doi.org/10.1038/srep34843
  3. J. Dunlop, M. Bowlby, R. Peri, D. Vasilyev, R. Arias, High-throughput electrophysiology: an emerging paradigm for ion-channel screening and physiology. Nat. Rev. Drug Discov. 7, 358–368 (2008). https://doi.org/10.1038/nrd2552
  4. R. Liu, R. Chen, A.T. Elthakeb, S.H. Lee, S. Hinckley et al., High density individually addressable nanowire arrays record intracellular activity from primary rodent and human stem cell derived neurons. Nano Lett. 17, 2757–2764 (2017). https://doi.org/10.1021/acs.nanolett.6b04752
  5. S. Sundelacruz, M. Levin, D.L. Kaplan, Role of membrane potential in the regulation of cell proliferation and differentiation. Stem Cell Rev. Rep. 5, 231–246 (2009). https://doi.org/10.1007/s12015-009-9080-2
  6. D.J. Blackiston, K.A. McLaughlin, M. Levin, Bioelectric controls of cell proliferation: ion channels, membrane voltage and the cell cycle. Cell Cycle 8, 3527–3536 (2009). https://doi.org/10.4161/cc.8.21.9888
  7. A. Timmis, N. Townsend, C. Gale, R. Grobbee, N. Maniadakis et al., European society of cardiology: Cardiovascular disease statistics 2017. Oxford University Press, Oxford. (2018)
  8. Correction to: heart disease and stroke statistics-2023 update: a report from the American heart association. Circulation 148, e4 (2023). https://doi.org/10.1161/CIR.0000000000001167
  9. G. Vorobiof, C. Silverstein, Non-invasive cardiac imaging for evaluation of cardiotoxicity in cancer patients-early detection and follow-up. SA Heart (2017). https://doi.org/10.24170/9-4-1829
  10. Y. Yang, A. Liu, C.-T. Tsai, C. Liu, J.C. Wu et al., Cardiotoxicity drug screening based on whole-panel intracellular recording. Biosens. Bioelectron. 216, 114617 (2022). https://doi.org/10.1016/j.bios.2022.114617
  11. L. Xiao, Z. Hu, W. Zhang, C. Wu, H. Yu et al., Evaluation of doxorubicin toxicity on cardiomyocytes using a dual functional extracellular biochip. Biosens. Bioelectron. 26, 1493–1499 (2010). https://doi.org/10.1016/j.bios.2010.07.093
  12. A.L. Hodgkin, A.F. Huxley, Action potentials recorded from inside a nerve fibre. Nature 144, 710–711 (1939). https://doi.org/10.1038/144710a0
  13. L. Berdondini, K. Imfeld, A. Maccione, M. Tedesco, S. Neukom et al., Active pixel sensor array for high spatio-temporal resolution electrophysiological recordings from single cell to large scale neuronal networks. Lab Chip 9, 2644–2651 (2009). https://doi.org/10.1039/B907394A
  14. C.-X. Lin, J.-L. Gu, J.-M. Cao, The acute toxic effects of platinum nanops on ion channels, transmembrane potentials of cardiomyocytes in vitro and heart rhythm in vivo in mice. Int. J. Nanomedicine 14, 5595–5609 (2019). https://doi.org/10.2147/IJN.S209135
  15. T. Meyer, K.-H. Boven, E. Günther, M. Fejtl, Micro-electrode arrays in cardiac safety pharmacology: a novel tool to study QT interval prolongation. Drug Saf. 27, 763–772 (2004). https://doi.org/10.2165/00002018-200427110-00002
  16. D. Xu, J. Mo, X. Xie, N. Hu, In-cell nanoelectronics: opening the door to intracellular electrophysiology. Nano-Micro Lett. 13, 127 (2021). https://doi.org/10.1007/s40820-021-00655-x
  17. J. Fang, S. Huang, F. Liu, G. He, X. Li et al., Semi-implantable bioelectronics. Nano-Micro Lett. 14, 125 (2022). https://doi.org/10.1007/s40820-022-00818-4
  18. D. Ossola, M.-Y. Amarouch, P. Behr, J. Vörös, H. Abriel et al., Force-controlled patch clamp of beating cardiac cells. Nano Lett. 15, 1743–1750 (2015). https://doi.org/10.1021/nl504438z
  19. B. Hille, Ion channels of excitable membranes sunderland. Sinauer Associates Inc. (2001)
  20. A. Molleman, Patch clamping: an introductory guide to patch clamp electrophysiology (Patch Clamping: An Introductory Guide To Patch Clamp Electrophysiology; 2003)
  21. D. C. Sigg, P. A. Iaizzo, Y. F. Xiao, B. He. Electrophysiology of single cardiomyocytes: Patch clamp and other recording methods. (Chapter 16), 329–348 (2010). https://doi.org/10.1007/978-1-4419-6658-2_16
  22. R.L. Schrøder, M. Christensen, B. Anson, M. Sunesen, Exploring stem cell-derived cardiomyocytes with automated patch clamp techniques. Biophys. J. 102, 544a (2012). https://doi.org/10.1016/j.bpj.2011.11.2968
  23. B. Amuzescu, S. Frech, K. Lin, J. Eisfeld, J. Kudolo et al., Electrophysiology Characterization of Human Induced Pluripotent Stem Cell-derived Cardiomyocytes Using Automated Patch-clamp. (2015)
  24. A. Marques-Smith, J.P. Neto, G. Lopes, J. Nogueira, L. Calcaterra et al., Recording from the same neuron with high-density CMOS probes and patch-clamp: a ground-truth dataset and an experiment in collaboration. bioRxiv (2018). https://doi.org/10.1101/370080
  25. V. Grenier, K.N. Martinez, B.R. Benlian, D.M. García-Almedina, B.K. Raliski et al., Molecular prosthetics for long-term functional imaging with fluorescent reporters. ACS Cent. Sci. 8, 118–121 (2022). https://doi.org/10.1021/acscentsci.1c01153
  26. A. Grinvald, R. Hildesheim, VSDI: a new era in functional imaging of cortical dynamics. Nat. Rev. Neurosci. 5, 874–885 (2004). https://doi.org/10.1038/nrn1536
  27. L.N. Kahyaoglu, R. Madangopal, M. Stensberg, Rickus J.L, Light-directed functionalization methods for high-resolution optical fiber based biosensors. SPIE Sensing Technology + Applications. Proc SPIE 9486, Advanced Environmental, Chemical, and Biological Sensing Technologies XII Baltimore, MD, USA 9486, 9–18 (2015). https://doi.org/10.1117/12.2177178
  28. A. Matiukas, B.G. Mitrea, M. Qin, A.M. Pertsov, A.G. Shvedko et al., Near-infrared voltage-sensitive fluorescent dyes optimized for optical mapping in blood-perfused myocardium. Heart Rhythm 4, 1441–1451 (2007). https://doi.org/10.1016/j.hrthm.2007.07.012
  29. M. Warren, K.W. Spitzer, B.W. Steadman, T.D. Rees, P. Venable et al., High-precision recording of the action potential in isolated cardiomyocytes using the near-infrared fluorescent dye di-4-ANBDQBS. Am. J. Physiol. Heart Circ. Physiol. 299, H1271–H1281 (2010). https://doi.org/10.1152/ajpheart.00248.2010
  30. M. Warren, K.W. Spitzer, B.W. Steadman, P. Venable, T. Taylor et al., Near infrared emitting dye di-4-ANBDQBS for recording action potentials in isolated cardiomyocytes. Biophys. J. 96, 293a (2009). https://doi.org/10.1016/j.bpj.2008.12.1453
  31. J. Abbott, T. Ye, K. Krenek, R.S. Gertner, S. Ban et al., A nanoelectrode array for obtaining intracellular recordings from thousands of connected neurons. Nat. Biomed. Eng. 4, 232–241 (2020). https://doi.org/10.1038/s41551-019-0455-7
  32. T. Banno, S. Tsuruhara, Y. Seikoba, R. Tonai, K. Yamashita et al., Nanoneedle-electrode devices for in vivo recording of extracellular action potentials. ACS Nano 16, 10692–10700 (2022). https://doi.org/10.1021/acsnano.2c02399
  33. A. Barbaglia, M. Dipalo, G. Melle, G. Iachetta, L. Deleye et al., Mirroring action potentials: label-free, accurate, and noninvasive electrophysiological recordings of human-derived cardiomyocytes. Adv. Mater. 33, e2004234 (2021). https://doi.org/10.1002/adma.202004234
  34. B.X.E. Desbiolles, E. de Coulon, A. Bertsch, S. Rohr, P. Renaud, Intracellular recording of cardiomyocyte action potentials with nanopatterned volcano-shaped microelectrode arrays. Nano Lett. 19, 6173–6181 (2019). https://doi.org/10.1021/acs.nanolett.9b02209
  35. J. Fang, D. Xu, H. Wang, J. Wu, Y. Li et al., Scalable and robust hollow nanopillar electrode for enhanced intracellular action potential recording. Nano Lett. 23, 243–251 (2023). https://doi.org/10.1021/acs.nanolett.2c04222
  36. Z. Jahed, Y. Yang, C.-T. Tsai, E.P. Foster, A.F. McGuire et al., Nanocrown electrodes for parallel and robust intracellular recording of cardiomyocytes. Nat. Commun. 13, 2253 (2022). https://doi.org/10.1038/s41467-022-29726-2
  37. J.T. Robinson, M. Jorgolli, A.K. Shalek, M.-H. Yoon, R.S. Gertner et al., Vertical nanowire electrode arrays as a scalable platform for intracellular interfacing to neuronal circuits. Nat. Nanotechnol. 7, 180–184 (2012). https://doi.org/10.1038/nnano.2011.249
  38. M. Abarkan, A. Pirog, D. Mafilaza, G. Pathak, G. N’Kaoua et al., Vertical organic electrochemical transistors and electronics for low amplitude micro-organ signals. Adv. Sci. 9, e2105211 (2022). https://doi.org/10.1002/advs.202105211
  39. B. Tian, T. Cohen-Karni, Q. Qing, X. Duan, P. Xie et al., Three-dimensional, flexible nanoscale field-effect transistors as localized bioprobes. Science 329, 830–834 (2010). https://doi.org/10.1126/science.1192033
  40. T. Cohen-Karni, Q. Qing, Q. Li, Y. Fang, C.M. Lieber, Graphene and nanowire transistors for cellular interfaces and electrical recording. Nano Lett. 10, 1098–1102 (2010). https://doi.org/10.1021/nl1002608
  41. X. Duan, R. Gao, P. Xie, T. Cohen-Karni, Q. Qing et al., Intracellular recordings of action potentials by an extracellular nanoscale field-effect transistor. Nat. Nanotechnol. 7, 174–179 (2011). https://doi.org/10.1038/nnano.2011.223
  42. Q. Qing, Z. Jiang, L. Xu, R. Gao, L. Mai et al., Free-standing kinked nanowire transistor probes for targeted intracellular recording in three dimensions. Nat. Nanotechnol. 9, 142–147 (2014). https://doi.org/10.1038/nnano.2013.273
  43. S. Asgarifar, H. Gomes, A. Mestre, P.M. C. Inácio, J. Bragança et al., in Electrochemically Gated Graphene Field-effect Transistor for Extracellular Cell Signal Recording. ed. by (2016), pp. 558–564.
  44. Y. Gu, C. Wang, N. Kim, J. Zhang, T.M. Wang et al., Three-dimensional transistor arrays for intra- and inter-cellular recording. Nat. Nanotechnol. 17, 292–300 (2022). https://doi.org/10.1038/s41565-021-01040-w
  45. A. Kyndiah, F. Leonardi, C. Tarantino, T. Cramer, R. Millan-Solsona et al., Bioelectronic recordings of cardiomyocytes with accumulation mode electrolyte gated organic field effect transistors. Biosens. Bioelectron. 150, 111844 (2020). https://doi.org/10.1016/j.bios.2019.111844
  46. H. Gao, F. Yang, K. Sattari, X. Du, T. Fu et al., Bioinspired two-in-one nanotransistor sensor for the simultaneous measurements of electrical and mechanical cellular responses. Sci. Adv. 8, eabn2485 (2022). https://doi.org/10.1126/sciadv.abn2485
  47. P. Connolly, P. Clark, A.S.G. Curtis, J.A.T. Dow, C.D.W. Wilkinson, An Extracellular microelectrode Array for monitoring electrogenic cells in culture. Biosens. Bioelectron. 5, 223–234 (1990). https://doi.org/10.1016/0956-5663(90)80011-2
  48. T.J. Blanche, M.A. Spacek, J.F. Hetke, N.V. Swindale, Polytrodes: high-density silicon electrode arrays for large-scale multiunit recording. J. Neurophysiol. 93, 2987–3000 (2005). https://doi.org/10.1152/jn.01023.2004
  49. P.J. Koester, C. Tautorat, H. Beikirch, J. Gimsa, W. Baumann, Recording electric potentials from single adherent cells with 3D microelectrode arrays after local electroporation. Biosens. Bioelectron. 26, 1731–1735 (2010). https://doi.org/10.1016/j.bios.2010.08.003
  50. M.E. Spira, A. Hai, Multi-electrode array technologies for neuroscience and cardiology. Nat. Nanotechnol. 8, 83–94 (2013). https://doi.org/10.1038/nnano.2012.265
  51. V. Zlochiver, S.L. Kroboth, C.R. Beal, J.A. Cook, R. Joshi-Mukherjee, Human iPSC-derived cardiomyocyte networks on multiwell micro-electrode arrays for recurrent action potential recordings. J. Vis. Exp. 149, e59906 (2019). https://doi.org/10.3791/59906
  52. X. Wei, C. Qin, C. Gu, C. He, Q. Yuan et al., A novel bionic in vitro bioelectronic tongue based on cardiomyocytes and microelectrode array for bitter and umami detection. Biosens. Bioelectron. 145, 111673 (2019). https://doi.org/10.1016/j.bios.2019.111673
  53. A. Zhang, C.M. Lieber, Nano-bioelectronics. Chem. Rev. 116, 215–257 (2016). https://doi.org/10.1021/acs.chemrev.5b00608
  54. I. Zadorozhnyi, H. Hlukhova, Y. Kutovyi, V. Handziuk, N. Naumova et al., Towards pharmacological treatment screening of cardiomyocyte cells using Si nanowire FETs. Biosens. Bioelectron. 137, 229–235 (2019). https://doi.org/10.1016/j.bios.2019.04.038
  55. G. Presnova, D. Presnov, V. Krupenin, V. Grigorenko, A. Trifonov et al., Biosensor based on a silicon nanowire field-effect transistor functionalized by gold nanops for the highly sensitive determination of prostate specific antigen. Biosens. Bioelectron. 88, 283–289 (2017). https://doi.org/10.1016/j.bios.2016.08.054
  56. J. Abbott, T. Ye, L. Qin, M. Jorgolli, R.S. Gertner et al., CMOS nanoelectrode array for all-electrical intracellular electrophysiological imaging. Nat. Nanotechnol. 12, 460–466 (2017). https://doi.org/10.1038/nnano.2017.3
  57. J.S. Park, S.I. Grijalva, D. Jung, S. Li, G.V. Junek et al., Intracellular cardiomyocytes potential recording by planar electrode array and fibroblasts co-culturing on multi-modal CMOS chip. Biosens. Bioelectron. 144, 111626 (2019). https://doi.org/10.1016/j.bios.2019.111626
  58. J. Müller, M. Ballini, P. Livi, Y. Chen, M. Radivojevic et al., High-resolution CMOS MEA platform to study neurons at subcellular, cellular, and network levels. Lab Chip 15, 2767–2780 (2015). https://doi.org/10.1039/C5LC00133A
  59. C.M. Lieber, Semiconductor nanowires: a platform for nanoscience and nanotechnology. MRS Bull. 36, 1052–1063 (2011). https://doi.org/10.1557/mrs.2011.269
  60. B.P. Timko, T. Cohen-Karni, Q. Qing, B. Tian, C.M. Lieber, Design and implementation of functional nanoelectronic interfaces with biomolecules, cells, and tissue using nanowire device arrays. IEEE Trans. Nanotechnol. 9, 269–280 (2010). https://doi.org/10.1109/TNANO.2009.2031807
  61. P.B. Kruskal, Z. Jiang, T. Gao, C.M. Lieber, Beyond the patch clamp: nanotechnologies for intracellular recording. Neuron 86, 21–24 (2015). https://doi.org/10.1016/j.neuron.2015.01.004
  62. Y. Zhang, L.F. Duan, Y. Zhang, J. Wang, H. Geng et al., Advances in conceptual electronic nanodevices based on 0D and 1D nanomaterials. Nano-Micro Lett. 6, 1–19 (2014). https://doi.org/10.1007/BF03353763
  63. M. Liu, Z. Wu, W.M. Lau, J. Yang, Recent advances in directed assembly of nanowires or nanotubes. Nano-Micro Lett. 4, 142–153 (2012). https://doi.org/10.1007/BF03353705
  64. Y. Fang, Y. Jiang, H. Acaron Ledesma, J. Yi, X. Gao et al., Texturing silicon nanowires for highly localized optical modulation of cellular dynamics. Nano Lett. 18, 4487–4492 (2018). https://doi.org/10.1021/acs.nanolett.8b01626
  65. P. Singh, S.K. Pandey, J. Singh, S. Srivastava, S. Sachan et al., Biomedical perspective of electrochemical nanobiosensor. Nano-Micro Lett. 8, 193–203 (2016). https://doi.org/10.1007/s40820-015-0077-x
  66. J. Li, Y. Ma, D. Huang, Z. Wang, Z. Zhang et al., High-performance flexible microneedle array as a low-impedance surface biopotential dry electrode for wearable electrophysiological recording and polysomnography. Nano-Micro Lett. 14, 132 (2022). https://doi.org/10.1007/s40820-022-00870-0
  67. Y. Qiao, J. Luo, T. Cui, H. Liu, H. Tang et al., Soft electronics for health monitoring assisted by machine learning. Nano-Micro Lett. 15, 66 (2023). https://doi.org/10.1007/s40820-023-01029-1
  68. D. Jäckel, D.J. Bakkum, T.L. Russell, J. Müller, M. Radivojevic et al., Combination of high-density microelectrode array and patch clamp recordings to enable studies of multisynaptic integration. Sci. Rep. 7, 978 (2017). https://doi.org/10.1038/s41598-017-00981-4
  69. Y. Zhang, Y. Tang, Y. Wang, L. Zhang, Nanomaterials for cardiac tissue engineering application. Nano-Micro Lett. 3, 270–277 (2011). https://doi.org/10.1007/BF03353683
  70. J. Lou-Franco, B. Das, C. Elliott, C. Cao, Gold nanozymes: from concept to biomedical applications. Nano-Micro Lett. 13, 10 (2020). https://doi.org/10.1007/s40820-020-00532-z
  71. Y. Jin, H. Wang, K. Yi, S. Lv, H. Hu et al., Applications of nanobiomaterials in the therapy and imaging of acute liver failure. Nano-Micro Lett. 13, 25 (2020). https://doi.org/10.1007/s40820-020-00550-x
  72. S. Kim, J. Seo, J. Choi, H. Yoo, Vertically integrated electronics: new opportunities from emerging materials and devices. Nano-Micro Lett. 14, 201 (2022). https://doi.org/10.1007/s40820-022-00942-1
  73. X. Dai, W. Zhou, T. Gao, J. Liu, C.M. Lieber, Three-dimensional mapping and regulation of action potential propagation in nanoelectronics-innervated tissues. Nat. Nanotechnol. 11, 776–782 (2016). https://doi.org/10.1038/nnano.2016.96
  74. C. Xie, J. Liu, T.-M. Fu, X. Dai, W. Zhou et al., Three-dimensional macroporous nanoelectronic networks as minimally invasive brain probes. Nat. Mater. 14, 1286–1292 (2015). https://doi.org/10.1038/nmat4427
  75. S.K. Krishnan, N. Nataraj, M. Meyyappan, U. Pal, Graphene-based field-effect transistors in biosensing and neural interfacing applications: recent advances and prospects. Anal. Chem. 95, 2590–2622 (2023). https://doi.org/10.1021/acs.analchem.2c03399
  76. S. Wang, M.Z. Hossain, K. Shinozuka, N. Shimizu, S. Kitada et al., Graphene field-effect transistor biosensor for detection of biotin with ultrahigh sensitivity and specificity. Biosens. Bioelectron. 165, 112363 (2020). https://doi.org/10.1016/j.bios.2020.112363
  77. L. Xu, Z. Jiang, L. Mai, Q. Qing, Multiplexed free-standing nanowire transistor bioprobe for intracellular recording: a general fabrication strategy. Nano Lett. 14, 3602–3607 (2014). https://doi.org/10.1021/nl5012855
  78. C. Yao, Q. Li, J. Guo, F. Yan, I.-M. Hsing, Rigid and flexible organic electrochemical transistor arrays for monitoring action potentials from electrogenic cells. Adv. Healthc. Mater. 4, 528–533 (2015). https://doi.org/10.1002/adhm.201400406
  79. S.J. Luck, An introduction to the event-related potential technique. Sveučilište u Rijeci. (2005)
  80. S. Cabrini, Sub-10-nm three-dimensional plasmonic probes and sensors. 2016 Progress in Electromagnetic Research Symposium (PIERS). Shanghai, China. IEEE, (2016). p 836
  81. R. Gao, S. Strehle, B. Tian, T. Cohen-Karni, P. Xie et al., Outside looking in: nanotube transistor intracellular sensors. Nano Lett. 12, 3329–3333 (2012). https://doi.org/10.1021/nl301623p
  82. T.P. Dasari Shareena, D. McShan, A.K. Dasmahapatra, P.B. Tchounwou, A review on graphene-based nanomaterials in biomedical applications and risks in environment and health. Nano-Micro Lett. 10, 53 (2018). https://doi.org/10.1007/s40820-018-0206-4
  83. S. Luo, L. Peng, Y. Xie, X. Cao, X. Wang et al., Flexible large-area graphene films of 50–600nm thickness with high carrier mobility. Nano-Micro Lett. 15, 61 (2023). https://doi.org/10.1007/s40820-023-01032-6
  84. L. Tang, Y. Wang, Y. Li, H. Feng, J. Lu et al., Preparation, structure, and electrochemical properties of reduced graphene sheet films. Adv. Funct. Mater. 19, 2782–2789 (2009). https://doi.org/10.1002/adfm.200900377
  85. W.C. Lee, C.H. Lim, H. Shi, L.A. Tang, Y. Wang et al., Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide. ACS Nano 5, 7334–7341 (2011). https://doi.org/10.1021/nn202190c
  86. M. Kaisti, Detection principles of biological and chemical FET sensors. Biosens. Bioelectron. 98, 437–448 (2017). https://doi.org/10.1016/j.bios.2017.07.010
  87. W. Fu, L. Jiang, E.P. van Geest, L.M. Lima, G.F. Schneider, Sensing at the surface of graphene field-effect transistors. Adv. Mater. 29, 1603610 (2017). https://doi.org/10.1002/adma.201603610
  88. R. Stine, S.P. Mulvaney, J.T. Robinson, C.R. Tamanaha, P.E. Sheehan, Fabrication, optimization, and use of graphene field effect sensors. Anal. Chem. 85, 509–521 (2013). https://doi.org/10.1021/ac303190w
  89. T. Feuk, On the transparency of the stroma in the mammalian Cornea. IEEE Trans. Biomed. Eng. BME-17, 186–190 (1970). https://doi.org/10.1109/tbme.1970.4502732
  90. S.-A. Peng, Z. Jin, P. Ma, D.-Y. Zhang, J.-Y. Shi et al., The sheet resistance of graphene under contact and its effect on the derived specific contact resistivity. Carbon 82, 500–505 (2015). https://doi.org/10.1016/j.carbon.2014.11.001
  91. W. Fu, C. Nef, A. Tarasov, M. Wipf, R. Stoop et al., High mobility graphene ion-sensitive field-effect transistors by noncovalent functionalization. Nanoscale 5, 12104–12110 (2013). https://doi.org/10.1039/C3NR03940D
  92. L.H. Hess, M. Seifert, J.A. Garrido, Graphene transistors for bioelectronics. Proc. IEEE 101, 1780–1792 (2013). https://doi.org/10.1109/JPROC.2013.2261031
  93. F. Veliev, Z. Han, D. Kalita, A. Briançon-Marjollet, V. Bouchiat et al., Recording spikes activity in cultured hippocampal neurons using flexible or transparent graphene transistors. Front. Neurosci. 11, 466 (2017). https://doi.org/10.3389/fnins.2017.00466
  94. L. Xu, Z. Jiang, Q. Qing, L. Mai, Q. Zhang et al., Design and synthesis of diverse functional kinked nanowire structures for nanoelectronic bioprobes. Nano Lett. 13, 746–751 (2013). https://doi.org/10.1021/nl304435z
  95. Z. Jiang, Q. Qing, P. Xie, R. Gao, C.M. Lieber, Kinked p-n junction nanowire probes for high spatial resolution sensing and intracellular recording. Nano Lett. 12, 1711–1716 (2012). https://doi.org/10.1021/nl300256r
  96. T.-M. Fu, X. Duan, Z. Jiang, X. Dai, P. Xie et al., Sub-10-nm intracellular bioelectronic probes from nanowire–nanotube heterostructures. Proc. Natl. Acad. Sci. U.S.A. 111, 1259–1264 (2014). https://doi.org/10.1073/pnas.1323389111
  97. T. Cohen-Karni, D. anova, J.F. Cahoon, Q. Qing, D.C. Bell et al., Synthetically encoded ultrashort-channel nanowire transistors for fast, pointlike cellular signal detection. Nano Lett. 12, 2639–2644 (2012). https://doi.org/10.1021/nl3011337
  98. R. Elnathan, M. Kwiat, F. Patolsky, N.H. Voelcker, Engineering vertically aligned semiconductor nanowire arrays for applications in the life sciences. Nano Today 9, 172–196 (2014). https://doi.org/10.1016/j.nantod.2014.04.001
  99. J. Westwater, D.P. Gosain, S. Tomiya, S. Usui, H. Ruda, Growth of silicon nanowires via gold/silane vapor–liquid–solid reaction. J. Vac. Sci. Technol. B Microelectron. Nanometer Struct. Process. Meas. Phenom. 15, 554–557 (1997). https://doi.org/10.1116/1.589291
  100. Q. Gao, V.G. Dubrovskii, P. Caroff, J. Wong-Leung, L. Li et al., Simultaneous selective-area and vapor-liquid-solid growth of InP nanowire arrays. Nano Lett. 16, 4361–4367 (2016). https://doi.org/10.1021/acs.nanolett.6b01461
  101. S. Barth, F. Hernandez-Ramirez, J.D. Holmes, A. Romano-Rodriguez, Synthesis and applications of one-dimensional semiconductors. Prog. Mater. Sci. 55, 563–627 (2010). https://doi.org/10.1016/j.pmatsci.2010.02.001
  102. J. Hu, T.W. Odom, C.M. Lieber, Chemistry and physics in one dimension: synthesis and properties of nanowires and nanotubes. Acc. Chem. Res. 32, 435–445 (1999). https://doi.org/10.1021/ar9700365
  103. A.K. Shalek, J.T. Robinson, E.S. Karp, J.S. Lee, D.-R. Ahn et al., Vertical silicon nanowires as a universal platform for delivering biomolecules into living cells. Proc. Natl. Acad. Sci. U.S.A. 107, 1870–1875 (2010). https://doi.org/10.1073/pnas.0909350107
  104. Y.J. Hwang, C. Hahn, B. Liu, P. Yang, Photoelectrochemical properties of TiO2 nanowire arrays: a study of the dependence on length and atomic layer deposition coating. ACS Nano 6, 5060–5069 (2012). https://doi.org/10.1021/nn300679d
  105. Y. Zhao, S.S. You, A. Zhang, J.H. Lee, J. Huang et al., Scalable ultrasmall three-dimensional nanowire transistor probes for intracellular recording. Nat. Nanotechnol. 14, 783–790 (2019). https://doi.org/10.1038/s41565-019-0478-y
  106. Z. Huang, H. Fang, J. Zhu, Fabrication of silicon nanowire arrays with controlled diameter, length, and density. Adv. Mater. 19, 744–748 (2007). https://doi.org/10.1002/adma.200600892
  107. Y.Q. Fu, A. Colli, A. Fasoli, J.K. Luo, A.J. Flewitt et al., Deep reactive ion etching as a tool for nanostructure fabrication. J. Vac. Sci. Technol. B Microelectron. Nanometer Struct. Process. Meas. Phenom. 27, 1520–1526 (2009). https://doi.org/10.1116/1.3065991
  108. R. Juhasz, N. Elfström, J. Linnros, Controlled fabrication of silicon nanowires by electron beam lithography and electrochemical size reduction. Nano Lett. 5, 275–280 (2005). https://doi.org/10.1021/nl0481573
  109. Y. Zhang, J. Clausmeyer, B. Babakinejad, A.L. Córdoba, T. Ali et al., Spearhead nanometric field-effect transistor sensors for single-cell analysis. ACS Nano 10, 3214–3221 (2016). https://doi.org/10.1021/acsnano.5b05211
  110. F. Torricelli, D.Z. Adrahtas, Z. Bao, M. Berggren, F. Biscarini et al., Electrolyte-gated transistors for enhanced performance bioelectronics. Nat. Rev. Meth. Primers 1, 66 (2021). https://doi.org/10.1038/s43586-021-00065-8
  111. D. Kireev, M. Brambach, S. Seyock, V. Maybeck, W. Fu et al., Graphene transistors for interfacing with cells: towards a deeper understanding of liquid gating and sensitivity. Sci. Rep. 7, 6658 (2017). https://doi.org/10.1038/s41598-017-06906-5
  112. L. Capua, S. Sheibani, S. Kamaei, J. Zhang, A.M. Ionescu, Extended-Gate FET cortisol sensor for stress disorders based on aptamers-decorated graphene electrode: fabrication, Experiments and Unified Analog Predictive Modeling. 2020 IEEE International Electron Devices Meeting (IEDM). San Francisco, CA, USA. IEEE, (2020), 35.2.1–35.2.4.
  113. S.J. Park, S.E. Seo, K.H. Kim, S.H. Lee, J. Kim et al., Real-time monitoring of geosmin based on an aptamer-conjugated graphene field-effect transistor. Biosens. Bioelectron. 174, 112804 (2021). https://doi.org/10.1016/j.bios.2020.112804
  114. A.K. Geim, D. Jiang, E.H. Hill, F. Schedin, K.S. Novoselov et al., Detection of individual gas molecules absorbed on graphene. arXiv e-prints. (2006)
  115. J. Ristein, W. Zhang, F. Speck, M. Ostler, L. Ley et al., Characteristics of solution gated field effect transistors on the basis of epitaxial graphene on silicon carbide. J. Phys. D Appl. Phys. 43, 345303 (2010). https://doi.org/10.1088/0022-3727/43/34/345303
  116. Y. Ohno, K. Maehashi, Y. Yamashiro, K. Matsumoto, Electrolyte-gated graphene field-effect transistors for detecting pH and protein orption. Nano Lett. 9, 3318–3322 (2009). https://doi.org/10.1021/nl901596m
  117. C. Homma, M. Tsukiiwa, H. Noguchi, M. Tanaka, M. Okochi et al., Designable peptides on graphene field-effect transistors for selective detection of odor molecules. Biosens. Bioelectron. 224, 115047 (2023). https://doi.org/10.1016/j.bios.2022.115047
  118. R. Negishi, H. Hirano, Y. Ohno, K. Maehashi, K. Matsumoto et al., Layer-by-layer growth of graphene layers on graphene substrates by chemical vapor deposition. Thin Solid Films 519, 6447–6452 (2011). https://doi.org/10.1016/j.tsf.2011.04.229
  119. B.M. Blaschke, M. Lottner, S. Drieschner, A.B. Calia, K. Stoiber et al., Flexible graphene transistors for recording cell action potentials. 2D Mater. 3, 025007 (2016). https://doi.org/10.1088/2053-1583/3/2/025007
  120. L.H. Hess, M. Jansen, V. Maybeck, M.V. Hauf, M. Seifert et al., Graphene transistor arrays for recording action potentials from electrogenic cells. Adv. Mater. 23, 5045–5049, 4968 (2011). https://doi.org/10.1002/adma.201102990
  121. C. Xie, Z. Lin, L. Hanson, Y. Cui, B. Cui, Intracellular recording of action potentials by nanopillar electroporation. Nat. Nanotechnol. 7, 185–190 (2012). https://doi.org/10.1038/nnano.2012.8
  122. J. Abbott, T. Ye, D. Ham, H. Park, Optimizing nanoelectrode arrays for scalable intracellular electrophysiology. Acc. Chem. Res. 51, 600–608 (2018). https://doi.org/10.1021/acs.accounts.7b00519
  123. M. Dipalo, G. Melle, L. Lovato, A. Jasi, F. Santoro et al., Plasmonic meta-electrodes allow intracellular recordings at network level on high-density CMOS-multi-electrode arrays. Nat. Nanotechnol. 13, 965–971 (2018). https://doi.org/10.1038/s41565-018-0222-z
  124. M. Dipalo, H. Amin, L. Lovato, F. Moia, V. Caprettini et al., Intracellular and extracellular recording of spontaneous action potentials in mammalian neurons and cardiac cells with 3D plasmonic nanoelectrodes. Nano Lett. 17, 3932–3939 (2017). https://doi.org/10.1021/acs.nanolett.7b01523
  125. M. Dipalo, G.C. Messina, H. Amin, R. La Rocca, V. Shalabaeva et al., 3D plasmonic nanoantennas integrated with MEA biosensors. Nanoscale 7, 3703–3711 (2015). https://doi.org/10.1039/c4nr05578k
  126. E.A. Woodcock, S.J. Matkovich, Cardiomyocytes structure, function and associated pathologies. Int. J. Biochem. Cell Biol. 37, 1746–1751 (2005). https://doi.org/10.1016/j.biocel.2005.04.011
  127. D.M. Bers, S. Despa, Cardiac excitation–contraction coupling. Encyclopedia of Biological Chemistry. Amsterdam: Elsevier, (2013), 379–383. https://doi.org/10.1016/b978-0-12-378630-2.00221-8
  128. T. Kuo, Peter, Cardiac electrophysiology: From cell to bedside. JAMA 274(6), 507 (1991). https://doi.org/10.1001/jama.1995.03530060083043
  129. D. Später, E.M. Hansson, L. Zangi, K.R. Chien, How to make a cardiomyocyte. Development 141, 4418–4431 (2014). https://doi.org/10.1242/dev.091538
  130. A. Leri, M. Rota, F.S. Pasqualini, P. Goichberg, P. Anversa, Origin of cardiomyocytes in the adult heart. Circ. Res. 116, 150–166 (2015). https://doi.org/10.1161/CIRCRESAHA.116.303595
  131. L.F. Santana, E.P. Cheng, W.J. Lederer, How does the shape of the cardiac action potential control calcium signaling and contraction in the heart? J. Mol. Cell. Cardiol. 49, 901–903 (2010). https://doi.org/10.1016/j.yjmcc.2010.09.005
  132. E. Carmeliet, J. Vereecke, Adrenaline and the plateau phase of the cardiac action potential. Importance of Ca++, Na+ and K+ conductance. Pflugers Arch. 313, 300–315 (1969). https://doi.org/10.1007/BF00593955
  133. C.H. Luo, Y. Rudy, A model of the ventricular cardiac action potential. Depolarization, repolarization, and their interaction. Circ. Res. 68, 1501–1526 (1991). https://doi.org/10.1161/01.res.68.6.1501
  134. Z.C. Lin, A.F. McGuire, P.W. Burridge, E. Matsa, H.Y. Lou et al., Accurate nanoelectrode recording of human pluripotent stem cell-derived cardiomyocytes for assaying drugs and modeling disease. Microsyst. Nanoeng. 3, 16080 (2017). https://doi.org/10.1038/micronano.2016.80
  135. Y. Liang, M. Ernst, F. Brings, D. Kireev, V. Maybeck et al., High performance flexible organic electrochemical transistors for monitoring cardiac action potential. Adv. Healthc. Mater. 7, e1800304 (2018). https://doi.org/10.1002/adhm.201800304
  136. S. Syama, P.V. Mohanan, Comprehensive application of graphene: emphasis on biomedical concerns. Nano-Micro Lett. 11, 6 (2019). https://doi.org/10.1007/s40820-019-0237-5
  137. L. Zhou, K. Wang, H. Sun, S. Zhao, X. Chen et al., Novel graphene biosensor based on the functionalization of multifunctional nano-bovine serum albumin for the highly sensitive detection of cancer biomarkers. Nano-Micro Lett. 11, 20 (2019). https://doi.org/10.1007/s40820-019-0250-8
  138. Z. Zhu, An overview of carbon nanotubes and graphene for biosensing applications. Nano-Micro Lett. 9, 25 (2017). https://doi.org/10.1007/s40820-017-0128-6
  139. D. Kireev, S. Seyock, J. Lewen, V. Maybeck, B. Wolfrum et al., Graphene multielectrode arrays as a versatile tool for extracellular measurements. Adv. Healthc. Mater. 6, 1601433 (2017). https://doi.org/10.1002/adhm.201601433
  140. P.D. Nguyen, F. Ding, S.A. Fischer, W. Liang, X. Li, Solvated first-principles excited-state charge-transfer dynamics with time-dependent polarizable continuum model and solvent dielectric relaxation. J. Phys. Chem. Lett. 3, 2898–2904 (2012). https://doi.org/10.1021/jz301042f
  141. L.H. Hess, C. Becker-Freyseng, M.S. Wismer, B.M. Blaschke, M. Lottner et al., Electrical coupling between cells and graphene transistors. Small 11, 1703–1710 (2015). https://doi.org/10.1002/smll.201402225
  142. F. Veliev, A. Cresti, D. Kalita, A. Bourrier, T. Belloir et al., Sensing ion channel in neuron networks with graphene field effect transistors. 2D Mater. 5, 045020 (2018). https://doi.org/10.1088/2053-1583/aad78f
  143. J. Chen, D. Chen, Y. Xie, T. Yuan, X. Chen, Progress of microfluidics for biology and medicine. Nano-Micro Lett. 5, 66–80 (2013). https://doi.org/10.1007/BF03354852
  144. V. Dupuit, O. Terral, G. Bres, A. Claudel, B. Fernandez et al., A multifunctional hybrid graphene and microfluidic platform to interface topological neuron networks. Adv. Funct. Mater. 32, 2207001 (2022). https://doi.org/10.1002/adfm.202207001
  145. J.A. Huang, V. Caprettini, Y. Zhao, G. Melle, N. Maccaferri et al., On-demand intracellular delivery of single ps in single cells by 3D hollow nanoelectrodes. Nano Lett. 19, 722–731 (2019). https://doi.org/10.1021/acs.nanolett.8b03764
  146. V. Caprettini, J.A. Huang, F. Moia, A. Jasi, C.A. Gonano et al., Enhanced Raman investigation of cell membrane and intracellular compounds by 3D plasmonic nanoelectrode arrays. Adv. Sci. 5, 1800560 (2018). https://doi.org/10.1002/advs.201800560
  147. M. Donnelly, D. Mao, J. Park, G. Xu, Graphene field-effect transistors: the road to bioelectronics. J. Phys. D Appl. Phys. 51, 493001 (2018). https://doi.org/10.1088/1361-6463/aadcca
  148. D. Xu, Z. Hu, J. Su, F. Wu, W. Yuan, Micro and nanotechnology for intracellular delivery therapy protein. Nano-Micro Lett. 4, 118–123 (2012). https://doi.org/10.1007/BF03353702
  149. L. Raes, S. Stremersch, J.C. Fraire, T. Brans, G. Goetgeluk et al., Intracellular delivery of mRNA in adherent and suspension cells by vapor nanobubble photoporation. Nano-Micro Lett. 12, 185 (2020). https://doi.org/10.1007/s40820-020-00523-0
  150. H. Yin, W. Jiang, Y. Liu, D. Zhang, F. Wu et al., Advanced near-infrared light approaches for neuroimaging and neuromodulation. BMEMat 1, e12023 (2023). https://doi.org/10.1002/bmm2.12023
  151. C. Lin, X. Li, T. Wu, J. Xu, Z. Gong et al., Optofluidic identification of single microorganisms using fiber-optical-tweezer-based Raman spectroscopy with artificial neural network. BMEMat 1, e12007 (2023). https://doi.org/10.1002/bmm2.12015
  152. H. Song, M. Kim, E. Kim, J. Lee, I. Jeong et al., Neuromodulation of the peripheral nervous system: Bioelectronic technology and prospective developments. BMEMat 1, e12048 (2023). https://doi.org/10.1002/bmm2.12048
  153. Y. Wang, M.L. Adam, Y. Zhao, W. Zheng, L. Gao et al., Machine learning-enhanced flexible mechanical sensing. Nano-Micro Lett. 15, 55 (2023). https://doi.org/10.1007/s40820-023-01013-9
  154. B. Hou, X. Liu, Stretching boundaries in neurophysiological monitoring. BMEMat 1, e12054 (2023). https://doi.org/10.1002/bmm2.12054
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