Thermoplasmonic Scaffold Design for the Modulation of Neural Activity in Three-Dimensional Neuronal Cultures
Tóm tắt
Neuromodulation has made great strides in recent years, but in vitro studies have been limited to two-dimensional cell cultures, far from in vivo conditions. In this study, we realized a novel thermoplasmonic platform for modulating the neural activity of three-dimensional cell cultures, providing a new tool to bring in vitro neuromodulation studies into a three-dimensional environment. The photosensitive scaffold, obtained by covering soda-lime glass microbeads (diameter about 40 µm) with gold nanorods, integrates microbeads’ structural properties, intended to support the development of the neural network in three dimensions, with the photothermal properties of plasmonic nanoparticles. We demonstrate its efficiency in providing support for the construction of three-dimensional cell culture and how, under Near-infrared laser irradiation, their photothermal effect can precisely and non-invasively modulate the activity of the neural network. Our platform is expected to be a useful tool for improving neural network studies to better understand complex brain functions and neural disorders.
Tài liệu tham khảo
Wells, J., Kao, C., Jansen, E.D., Konrad, P., Mahadevan-Jansen, A.: Application of infrared light for in vivo neural stimulation. J. Biomed. Opt. 10, 64003 (2005). https://doi.org/10.1117/1.2121772
Bernstein, J.G., Garrity, P.A., Boyden, E.S.: Optogenetics and thermogenetics: technologies for controlling the activity of targeted cells within intact neural circuits. Curr. Opin. Neurobiol. 22, 61–71 (2012). https://doi.org/10.1016/j.conb.2011.10.023
Chen, R., Romero, G., Christiansen, M.G., Mohr, A., Anikeeva, P.: Wireless magnetothermal deep brain stimulation. Science 347(2015), 1477–1480 (1979). https://doi.org/10.1126/science.1261821
Shapiro, M.G., Homma, K., Villarreal, S., Richter, C.P., Bezanilla, F.: Infrared light excites cells by changing their electrical capacitance. Nat. Commun. 3, 736 (2012). https://doi.org/10.1038/ncomms1742
Boyden, E.S., Zhang, F., Bamberg, E., Nagel, G., Deisseroth, K.: Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. (2005). https://doi.org/10.1038/nn1525
Zhang, F., Wang, L.P., Brauner, M., Liewald, J.F., Kay, K., Watzke, N., Wood, P.G., Bamberg, E., Nagel, G., Gottschalk, A., Deisseroth, K.: Multimodal fast optical interrogation of neural circuitry. Nature (2007). https://doi.org/10.1038/nature05744
Williams, J.C., Denison, T.: From optogenetic technologies to neuromodulation therapies. Sci. Transl. Med. (2013). https://doi.org/10.1126/scitranslmed.3003100
Dreaden, E.C., Alkilany, A.M., Huang, X., Murphy, C.J., El-Sayed, M.A.: The golden age: gold nanoparticles for biomedicine. Chem. Soc. Rev. 41, 2740–2779 (2012). https://doi.org/10.1039/C1CS15237H
Carvalho-de-Souza, J.L., Treger, J.S., Dang, B., Kent, S.B.H., Pepperberg, D.R., Bezanilla, F.: Photosensitivity of neurons enabled by cell-targeted gold nanoparticles. Neuron 86, 207–217 (2015). https://doi.org/10.1016/j.neuron.2015.02.033
Eom, K., Kim, J., Choi, J.M., Kang, T., Chang, J.W., Byun, K.M., Jun, S.B., Kim, S.J.: Enhanced infrared neural stimulation using localized surface plasmon resonance of gold nanorods. Small 10, 3853–3857 (2014). https://doi.org/10.1002/smll.201400599
Yoo, S., Hong, S., Choi, Y., Park, J.-H., Nam, Y.: Photothermal inhibition of neural activity with near-infrared-sensitive nanotransducers. ACS Nano 8, 8040–8049 (2014). https://doi.org/10.1021/nn5020775
Yoo, S., Kim, R., Park, J.-H., Nam, Y.: Electro-optical neural platform integrated with nanoplasmonic inhibition interface. ACS Nano 10, 4274–4281 (2016). https://doi.org/10.1021/acsnano.5b07747
Jung, H., Kang, H., Nam, Y.: Digital micromirror based near-infrared illumination system for plasmonic photothermal neuromodulation. Biomed. Opt. Express 8, 2866 (2017). https://doi.org/10.1364/boe.8.002866
Yoo, S., Park, J.-H., Nam, Y.: Single-cell photothermal neuromodulation for functional mapping of neural networks. ACS Nano 13, 544–551 (2019). https://doi.org/10.1021/acsnano.8b07277
Carvalho-de-Souza, J.L., Pinto, B.I., Pepperberg, D.R., Bezanilla, F.: Optocapacitive generation of action potentials by microsecond laser pulses of nanojoule energy. Biophys. J. 114, 283–288 (2018). https://doi.org/10.1016/j.bpj.2017.11.018
Cukierman, E.: Taking cell-matrix adhesions to the third dimension. Science 294(2001), 1708–1712 (1979). https://doi.org/10.1126/science.1064829
Frega, M., Tedesco, M., Massobrio, P., Pesce, M., Martinoia, S.: Network dynamics of 3D engineered neuronal cultures: a new experimental model for in-vitro electrophysiology. Sci. Rep. (2014). https://doi.org/10.1038/srep05489
Birgersdotter, A., Sandberg, R., Ernberg, I.: Gene expression perturbation in vitro—a growing case for three-dimensional (3D) culture systems. Semin. Cancer Biol. (2005). https://doi.org/10.1016/j.semcancer.2005.06.009
Behravesh, E., Emami, K., Wu, H., Gonda, S.: Comparison of genotoxic damage in monolayer cell cultures and three-dimensional tissue-like cell assemblies. Adv. Space Res. 35, 260–267 (2005). https://doi.org/10.1016/j.asr.2005.01.066
Pedersen, J.A., Swartz, M.A.: Mechanobiology in the third dimension. Ann. Biomed. Eng. 33, 1469–1490 (2005). https://doi.org/10.1007/s10439-005-8159-4
Smalley, K.S., Lioni, M., Herlyn, M.: Life isn’t flat: taking cancer biology to the next dimension. In Vitro Cell Dev Biol Anim. 42, 242–247 (2006). https://doi.org/10.1290/0604027.1
Tedesco, M., Frega, M., Martinoia, S., Pesce, M., Massobrio, P.: Interfacing 3D engineered neuronal cultures to micro-electrode arrays: an innovative in vitro experimental model. J. Vis. Exp. (2015). https://doi.org/10.3791/53080
Kim, D., Kang, H., Nam, Y.: Compact 256-channel multi-well microelectrode array system for in vitro neuropharmacology test. Lab Chip (2020). https://doi.org/10.1039/D0LC00384K
Kim, R., Nam, Y.: Polydopamine-doped conductive polymer microelectrodes for neural recording and stimulation. J. Neurosci. Methods (2019). https://doi.org/10.1016/j.jneumeth.2019.108369
Pautot, S., Wyart, C., Isacoff, E.Y.: Colloid-guided assembly of oriented 3D neuronal networks. Nat. Methods 5, 735–740 (2008). https://doi.org/10.1038/nmeth.1236
Tabor, C., van Haute, D., El-Sayed, M.A.: Effect of orientation on plasmonic coupling between gold nanorods. ACS Nano 3, 3670–3678 (2009). https://doi.org/10.1021/nn900779f
Jokerst, J.V., Lobovkina, T., Zare, R.N., Gambhir, S.S.: Nanoparticle PEGylation for imaging and therapy. Nanomedicine 6, 715–728 (2011). https://doi.org/10.2217/nnm.11.19
Haro-González, P., Sevilla, P.R., Sanz-Rodríguez, F., Rodríguez, E.M., Bogdan, N., Capobianco, J.A., Dholakia, K., Jaque, D.: Gold nanorod assisted intracellular optical manipulation of silica microspheres. Opt. Express 22, 19735 (2014). https://doi.org/10.1364/OE.22.019735
Hong, N., Nam, Y.: Thermoplasmonic neural chip platform for in situ manipulation of neuronal connections in vitro. Nat. Commun. (2020). https://doi.org/10.1038/s41467-020-20060-z