Hostname: page-component-7479d7b7d-jwnkl Total loading time: 0 Render date: 2024-07-13T12:56:55.224Z Has data issue: false hasContentIssue false
  • English
  • Français

Wireless nanotechnologies light up the next frontier in cell Calcium signalling

Published online by Cambridge University Press:  24 September 2020

Ilaria Abdel Aziz Open the ORCID record for Ilaria Abdel Aziz [Opens in a new window]  and
Maria Rosa Antognazza
Ilaria Abdel Aziz*
Affiliation:
Center for Nano Science and Technology@PoliMi, Istituto Italiano di Tecnologia, via Pascoli 70/3, 20133, Milano, Italy Politecnico di Milano, Dipartimento di Fisica, Piazza L. Da Vinci 32, 20133, Milano, Italy
Maria Rosa Antognazza
Affiliation:
Center for Nano Science and Technology@PoliMi, Istituto Italiano di Tecnologia, via Pascoli 70/3, 20133, Milano, Italy
*
*corresponding author, email: ilaria.aziz@iit.it
Get access

Abstract

Calcium ions impact nearly every aspect of cellular life, playing crucial roles as secondary messengers in regulation of neurotransmission, cell proliferation, migration and differentiation processes, intracellular homeostasis, long-distance signal propagation and stimuli physiological response. Despite its key-role, available techniques to study and selectively regulate Ca2+ signalling largely rely on chemical and electrical approaches, which often cannot ensure the necessary spatial and temporal resolution, specificity, modulation and reversal capability. In this context, Ca2+ modulation based on physical stimuli, such as magnetic, mechanical and optical tools, are emerging ass promising innovative solutions. Here, we focus our attention on a subclass of these approaches, namely wireless-activated techniques, and on functional materials able to act as non-invasive transduction elements. We present an overview of most recent outcomes in the field, and we critically evaluate their advantages and drawbacks. This work is mainly directed to the material science community, but hopefully it will provide a useful perspective also to the broader readership of biotechnologists, physiologists and clinicians.

Type
Review Article
Information
MRS Advances , Volume 5 , Issue 64: Snapshot reviews in materials advances 2020 , 2020 , pp. 3473 - 3489
Check for updates
Copyright
Copyright © The Author(s), 2020, published on behalf of Materials Research Society by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Berridge, M. J., Lipp, P., and Bootman, M. D., “The versatility and universality of calcium signalling,” Nature Reviews Molecular Cell Biology, vol. 1, no. 1. European Association for Cardio-Thoracic Surgery, pp. 11–21, 2000.CrossRefGoogle ScholarPubMed
Clapham, D. E., “Calcium Signaling,” Cell, vol. 131, no. 6. pp. 1047–1058, 2007.CrossRefGoogle ScholarPubMed
Antognazza, M. R., Abdel Aziz, I., and Lodola, F., “Use of exogenous and endogenous photomediators as efficient ROS modulation tools: Results and perspectives for therapeutic purposes,” Oxid. Med. Cell. Longev., vol. 2019, 2019.CrossRefGoogle ScholarPubMed
Romero, G., Christiansen, M. G., Stocche Barbosa, L., Garcia, F., and Anikeeva, P., “Localized Excitation of Neural Activity via Rapid Magnetothermal Drug Release,” Adv. Funct. Mater., vol. 26, no. 35, pp. 6471–6478, 2016.CrossRefGoogle Scholar
Munshi, R., Qadri, S. M., Zhang, Q., Rubio, I. C., del Pino, P., and Pralle, A., “Magnetothermal genetic deep brain stimulation of motor behaviors in awake, freely moving mice,” Elife, vol. 6, pp. 1–26, 2017.CrossRefGoogle ScholarPubMed
Munshi, R., Qadri, S. M., and Pralle, A., “Transient magnetothermal neuronal silencing using the chloride channel anoctamin 1 (TMEM16A),” Front. Neurosci., vol. 12, no. AUG, pp. 1–13, 2018.CrossRefGoogle Scholar
Rosenfeld, D. et al. , “Transgene-free remote magnetothermal regulation of adrenal hormones,” Sci. Adv., vol. 6, no. 15, pp. 1–12, 2020.CrossRefGoogle ScholarPubMed
Tay, A., Kunze, A., Murray, C., and Di Carlo, D., “Induction of Calcium Influx in Cortical Neural Networks by Nanomagnetic Forces,” ACS Nano, vol. 10, no. 2, pp. 2331–2341, 2016.CrossRefGoogle ScholarPubMed
Tay, A. and Di Carlo, D., “Magnetic Nanoparticle-Based Mechanical Stimulation for Restoration of Mechano-Sensitive Ion Channel Equilibrium in Neural Networks,” Nano Lett., vol. 17, no. 2, pp. 886–892, 2017.CrossRefGoogle ScholarPubMed
Suarez Castellanos, I. M., Balteanu, B., Singh, T., and Zderic, V., “Therapeutic modulation of calcium dynamics using ultrasound and other energy-based techniques,” IEEE Rev. Biomed. Eng., vol. 9, no. November, pp. 177–191, 2016.CrossRefGoogle Scholar
Tandon, B., Blaker, J. J., and Cartmell, S. H., “Piezoelectric materials as stimulatory biomedical materials and scaffolds for bone repair,” Acta Biomater., vol. 73, pp. 1–20, 2018.CrossRefGoogle ScholarPubMed
Ciofani, G. et al. , “Enhancement of neurite outgrowth in neuronal-like cells following boron nitride nanotube-mediated stimulation,” ACS Nano, vol. 4, no. 10, pp. 6267–6277, Oct. 2010.CrossRefGoogle ScholarPubMed
Danti, S. et al. , “Boron nitride nanotube-functionalised myoblast/microfibre constructs: A nanotech-assisted tissue-engineered platform for muscle stimulation,” J. Tissue Eng. Regen. Med., vol. 9, no. 7, pp. 847–851, Jul. 2015.CrossRefGoogle ScholarPubMed
Marino, A. et al. , “Piezoelectric Nanoparticle-Assisted Wireless Neuronal Stimulation,” ACS Nano, vol. 9, no. 7, pp. 7678–7689, 2015.CrossRefGoogle ScholarPubMed
Lee, Y.-S., Wu, S., Arinzeh, T. L., and Bunge, M. B., “Enhanced noradrenergic axon regeneration into schwann cell-filled PVDF-TrFE conduits after complete spinal cord transection,” Biotechnol. Bioeng., vol. 114, no. 2, pp. 444–456, Feb. 2017.CrossRefGoogle ScholarPubMed
Marino, A. et al. , “Piezoelectric barium titanate nanostimulators for the treatment of glioblastoma multiforme,” J. Colloid Interface Sci., vol. 538, pp. 449–461, 2019.CrossRefGoogle ScholarPubMed
Murillo, G. et al. , “Electromechanical Nanogenerator–Cell Interaction Modulates Cell Activity,” Adv. Mater., vol. 29, no. 24, pp. 1–7, 2017.Google ScholarPubMed
Ma, G., Wen, S., He, L., Huang, Y., Wang, Y., and Zhou, Y., “Optogenetic toolkit for precise control of calcium signaling,” Cell Calcium, vol. 64. Elsevier Ltd, pp. 36–46, 01-Jun-2017.CrossRefGoogle ScholarPubMed
H., D. and Bozhi Tian, Y. J., Xu, Shuai, Rogers, John A, Cestellos-Blanco, Stefano, Yang, Peidong, Carvalho-de-Souza, Joao L, Bezanilla, Francisco, Liu, Jia, Bao, Zhenan, Hjort, Martino, Cao, Yuhong, Melosh, Nicholas, Lanzani, Guglielmo, Benfenati, Fabio, Galli, Giulia, Gygi, Francois, R, “Roadmap on semiconductor – cell biointerfaces,” Phys. Biol., vol. 15, no. 031002, 2018.Google Scholar
Aziz, I. A., Malferrari, M., Roggiani, F., Tullii, G., Rapino, S., and Antognazza, M. R., “Journal Pre-proof Light Triggered Electron Transfer between a Conjugated Polymer and Cytochrome C for Optical Modulation of Redox Signalling,” ISCIENCE, p. 101091, 2020.CrossRefGoogle Scholar
Gryszel, M. and Głowacki, E. D., “Organic thin film photofaradaic pixels for on-demand electrochemistry in physiological conditions,” Chem. Commun., vol. 56, no. 11, pp. 1705–1708, 2020.CrossRefGoogle ScholarPubMed
Parameswaran, R. et al. , “Optical stimulation of cardiac cells with a polymer-supported silicon nanowire matrix,” Proc. Natl. Acad. Sci. U. S. A., vol. 116, no. 2, pp. 413–421, 2019.CrossRefGoogle ScholarPubMed
Rotenberg, M. Y. et al. , “Silicon Nanowires for Intracellular Optical Interrogation with Subcellular Resolution,” Nano Lett., vol. 20, no. 2, pp. 1226–1232, 2020.CrossRefGoogle ScholarPubMed
Sanchez-Rodriguez, S. P. et al. , “Plasmonic activation of gold nanorods for remote stimulation of calcium signaling and protein expression in HEK 293T cells,” Biotechnol. Bioeng., vol. 113, no. 10, pp. 2228–2240, 2016.CrossRefGoogle ScholarPubMed
Gao, W. et al. , “Copper sulfide nanoparticles as a photothermal switch for TRPV1 signaling to attenuate atherosclerosis,” Nat. Commun., vol. 9, no. 1, pp. 1–10, 2018.Google ScholarPubMed
Ma, Z. et al. , “Intracellular Ca2+ Cascade Guided by NIR-II Photothermal Switch for Specific Tumor Therapy,” iScience, vol. 23, no. 5, p. 101049, 2020.CrossRefGoogle ScholarPubMed
Bossio, C. et al. , “Photocatalytic activity of polymer nanoparticles modulates intracellular calcium dynamics and reactive oxygen species in HEK-293 cells,” Front. Bioeng. Biotechnol., vol. 6, no. AUG, 2018.CrossRefGoogle ScholarPubMed
Wu, Y. et al. , “Photoconductive Micro/Nanoscale Interfaces of a Semiconducting Polymer for Wireless Stimulation of Neuron-Like Cells,” ACS Appl. Mater. Interfaces, vol. 11, no. 5, pp. 4833–4841, 2019.CrossRefGoogle ScholarPubMed
Rand, D. et al. , “Direct Electrical Neurostimulation with Organic Pigment Photocapacitors,” Adv. Mater., vol. 30, no. 25, pp. 1–11, 2018.Google ScholarPubMed
Lyu, Y., Xie, C., Chechetka, S. A., Miyako, E., and Pu, K., “Semiconducting Polymer Nanobioconjugates for Targeted Photothermal Activation of Neurons,” J. Am. Chem. Soc., vol. 138, pp. 9049–9052, 2016.CrossRefGoogle ScholarPubMed
Jiang, Y. and Pu, K., “Multimodal Biophotonics of Semiconducting Polymer Nanoparticles,” Acc. Chem. Res., vol. 51, pp. 1840–1849, 2018.CrossRefGoogle ScholarPubMed
Miyako, E. et al. , “Photofunctional nanomodulators for bioexcitation,” Angew. Chemie - Int. Ed., vol. 53, no. 48, pp. 13121–13125, 2014.CrossRefGoogle ScholarPubMed
Carroll, E. C. et al. , “Two-photon brightness of azobenzene photoswitches designed for glutamate receptor optogenetics,” Proc. Natl. Acad. Sci. U. S. A., vol. 112, no. 7, pp. E776–E785, 2015.CrossRefGoogle ScholarPubMed
Cabré, G. et al. , “Rationally designed azobenzene photoswitches for efficient two-photon neuronal excitation,” Nat. Commun., vol. 10, no. 1, 2019.CrossRefGoogle ScholarPubMed
Fehrentz, T. et al. , “Optical control of L-type Ca 2+ channels using a diltiazem photoswitch,” Nat. Chem. Biol., vol. 14, no. 8, pp. 764–767, 2018.CrossRefGoogle ScholarPubMed