Genetically Encoded Circuit for Remote Regulation of Cell Migration by Magnetic Fields
Abstract
Magnetoreception can be generally defined as the ability to transduce the effects of a magnetic field into a cellular response. Magnetic stimulation at the cellular level is particularly attractive due to its ability for deep penetration and minimal invasiveness, allowing remote regulation of engineered biological processes. Previously, a magnetic-responsive genetic circuit was engineered using the transient receptor potential vanilloid 1 (TRPV1) and the iron containing ferritin protein (i.e., the TF circuit). In this study, we combined the TF circuit with a Ca2+ activated RhoA protein (CaRQ) to allow a magnetic field to remotely regulate cell migration. Cells expressing the TF circuit and CaRQ exhibited consistent dynamic protrusions, leading to migration along a porous membrane, directed spreading in response to a magnetic field gradient, as well as wound healing. This work offers a compelling interface for programmable electrical devices to control the migration of living systems for potential applications in cell-based therapy.
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This article is cited by 19 publications.
- Changyou Chen, Haitao Chen, Pingping Wang, Xue Wang, Xuting Wang, Chuanfang Chen, Weidong Pan. Reactive Oxygen Species Activate a Ferritin-Linked TRPV4 Channel under a Static Magnetic Field. ACS Chemical Biology 2024, 19 (5) , 1151-1160. https://doi.org/10.1021/acschembio.4c00090
- Mohammed Nadim Sardoiwala, Ankur Sood, Liku Biswal, Subhasree Roy Choudhury, Surajit Karmakar. Reconstituted Super Paramagnetic Protein “Magnetotransferrin” for Brain Targeting to Attenuate Parkinsonism. ACS Applied Materials & Interfaces 2023, 15 (10) , 12708-12718. https://doi.org/10.1021/acsami.2c20990
- Jordan W. Mundell, Matthew I. Brier, Everest Orloff, Sarah A. Stanley, Jonathan S. Dordick. Alternating magnetic fields drive stimulation of gene expression via generation of reactive oxygen species. iScience 2024, 27 (3) , 109186. https://doi.org/10.1016/j.isci.2024.109186
- Xiang Wang, Qianyi Liang, Yixuan Luo, Jianwen Ye, Yin Yu, Fei Chen. Engineering the next generation of theranostic biomaterials with synthetic biology. Bioactive Materials 2024, 32 , 514-529. https://doi.org/10.1016/j.bioactmat.2023.10.018
- Santiago R. Unda, Lisa E. Pomeranz, Roberta Marongiu, Xiaofei Yu, Leah Kelly, Gholamreza Hassanzadeh, Henrik Molina, George Vaisey, Putianqi Wang, Jonathan P. Dyke, Edward K. Fung, Logan Grosenick, Rick Zirkel, Aldana M. Antoniazzi, Sofya Norman, Conor M. Liston, Chris Schaffer, Nozomi Nishimura, Sarah A. Stanley, Jeffrey M. Friedman, Michael G. Kaplitt. Bidirectional Regulation of Motor Circuits Using Magnetogenetic Gene Therapy. 2023https://doi.org/10.1101/2023.07.13.548699
- Xiaofeng Lu, Galong Li, Wangbo Jiao, Kuo Li, Tingbin Zhang, Xiaoli Liu, Haiming Fan. Magnetic nanomaterials‐mediated neuromodulation. WIREs Nanomedicine and Nanobiotechnology 2023, 15 (4) https://doi.org/10.1002/wnan.1890
- Lisa Pomeranz, Rosemary Li, Xiaofei Yu, Leah Kelly, Gholamreza Hassanzadeh, Henrik Molina, Daniel Gross, Matthew Brier, George Vaisey, Putianqi Wang, Maria Jimenez-Gonzalez, Adolfo Garcia-Ocana, Jonathan Dordick, Jeffrey Friedman, Sarah Stanley. Magnetogenetic cell activation using endogenous ferritin. 2023https://doi.org/10.1101/2023.06.20.545120
- Clare M. Robinson, Nina E. Short, David T. Riglar. Achieving spatially precise diagnosis and therapy in the mammalian gut using synthetic microbial gene circuits. Frontiers in Bioengineering and Biotechnology 2022, 10 https://doi.org/10.3389/fbioe.2022.959441
- Maryam Moarefian, Antonia McDonnell Capossela, Ryan Eom, Kiana Aran. Single-Cell Technologies: Advances in Single-Cell Migration and Multi-Omics. GEN Biotechnology 2022, 1 (3) , 246-261. https://doi.org/10.1089/genbio.2022.0014
- Maren Laughlin, Bradley Cooke, Kerri Boutelle, Cary R. Savage, Alexxai Kravitz, Dana Small, Zoe Arvanitakis, Alex Martin, Luke E. Stoeckel. Neuroimaging and modulation in obesity and diabetes research: 10th anniversary meeting. International Journal of Obesity 2022, 46 (4) , 718-725. https://doi.org/10.1038/s41366-021-01025-8
- Susel Del Sol-Fernández, Pablo Martínez-Vicente, Pilar Gomollón-Zueco, Christian Castro-Hinojosa, Lucía Gutiérrez, Raluca M. Fratila, María Moros. Magnetogenetics: remote activation of cellular functions triggered by magnetic switches. Nanoscale 2022, 14 (6) , 2091-2118. https://doi.org/10.1039/D1NR06303K
- Xiuying Li, Hejian Xiong, Nicholas Rommelfanger, Xueqi Xu, Jonghae Youn, Paul A. Slesinger, Guosong Hong, Zhenpeng Qin. Nanotransducers for wireless neuromodulation. Matter 2021, 4 (5) , 1484-1510. https://doi.org/10.1016/j.matt.2021.02.012
- Yang Cui, Ying Yang, Dong Qiu. Design of selective cell migration biomaterials and their applications for tissue regeneration. Journal of Materials Science 2021, 56 (6) , 4080-4096. https://doi.org/10.1007/s10853-020-05537-y
- Matthew I. Brier, Jordan W. Mundell, Xiaofei Yu, Lichao Su, Alexander Holmann, Jessica Squeri, Baolin Zhang, Sarah A. Stanley, Jeffrey M. Friedman, Jonathan S. Dordick. Uncovering a possible role of reactive oxygen species in magnetogenetics. Scientific Reports 2020, 10 (1) https://doi.org/10.1038/s41598-020-70067-1
- Michael A. Wheeler, Christopher D. Deppmann, Manoj K. Patel, Ali D. Güler. Reply to: Magneto is ineffective in controlling electrical properties of cerebellar Purkinje cells, Assessing the utility of Magneto to control neuronal excitability in the somatosensory cortex and Revaluation of magnetic properties of Magneto. Nature Neuroscience 2020, 23 (9) , 1051-1054. https://doi.org/10.1038/s41593-019-0472-6
- Matthew I. Brier, Jonathan S. Dordick. Remote activation of cellular signaling. Science 2020, 368 (6494) , 936-937. https://doi.org/10.1126/science.abb9122
- Miriam Hernández-Morales, Trisha Shang, Jingjia Chen, Victor Han, Chunlei Liu. Lipid Oxidation Induced by RF Waves and Mediated by Ferritin Iron Causes Activation of Ferritin-Tagged Ion Channels. Cell Reports 2020, 30 (10) , 3250-3260.e7. https://doi.org/10.1016/j.celrep.2020.02.070
- Mladen Barbic. Possible magneto-mechanical and magneto-thermal mechanisms of ion channel activation in magnetogenetics. eLife 2019, 8 https://doi.org/10.7554/eLife.45807
- Sarah A. Stanley, Jeffrey M. Friedman. Electromagnetic Regulation of Cell Activity. Cold Spring Harbor Perspectives in Medicine 2019, 9 (5) , a034322. https://doi.org/10.1101/cshperspect.a034322