Calcium signaling plays a crucial role in various physiological processes, including muscle contraction, cell division, and neurotransmitter release. Dysregulation of calcium levels and signaling has been linked to a range of pathological conditions such as neurodegenerative disorders, cardiovascular disease, and cancer. Here, we propose a theoretical model that predicts the modulation of calcium ion channel activity and calcium signaling in the endothelium through the application of either a time-varying or static gradient magnetic field (MF). This modulation is achieved by exerting magnetic forces or torques on either biogenic or non-biogenic magnetic nanoparticles that are bound to endothelial cell membranes. Since calcium signaling in endothelial cells induces neuromodulation and influences blood flow control, treatment with a magnetic field shows promise for regulating neurovascular coupling and treating vascular dysfunctions associated with aging and neurodegenerative disorders. Furthermore, magnetic treatment can enable control over the decoding of Ca signals, ultimately impacting protein synthesis. The ability to modulate calcium wave frequencies using MFs and the MF-controlled decoding of Ca signaling present promising avenues for treating diseases characterized by calcium dysregulation.

Institute of Physics of the Czech Academy of Sciences Prague Czech Republic

International Magnetobiology Frontier Research Center Science Island Hefei China

National Technical University of Ukraine Igor Sikorsky Kyiv Polytechnic Institute Ukraine

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Xiong L. Garfinkel A. Are physiological oscillations physiological? J. Physiol. 2023 doi: 10.1113/JP285015. PubMed DOI

Garaschuk O. Linn J. Eilers J. Konnerth A. Large-Scale Oscillatory Calcium Waves in the Immature Cortex. Nat. Neurosci. 2000;3:452. doi: 10.1038/74823. PubMed DOI

Choi W.-G. Hilleary R. Swanson S. J. Kim S.-H. Gilroy S. Rapid, Long-Distance Electrical and Calcium Signaling in Plants. Annu. Rev. Plant Biol. 2016;67:287. doi: 10.1146/annurev-arplant-043015-112130. PubMed DOI

Tian W. Wang C. Gao Q. Li L. Luan S. Calcium Spikes, Waves and Oscillations in Plant Development and Biotic Interactions. Nat. Plants. 2020;6:750. doi: 10.1038/s41477-020-0667-6. PubMed DOI

Smedler E. Uhlén P. Frequency Decoding of Calcium Oscillations. Biochim. Biophys. Acta - Gen. Subj. 2014;1840:964. doi: 10.1016/j.bbagen.2013.11.015. PubMed DOI

Whitaker M. Calcium at Fertilization and in Early Development. Physiol. Rev. 2006;86:25. doi: 10.1152/physrev.00023.2005. PubMed DOI PMC

Coburn C. Allman E. Mahanti P. Benedetto A. Cabreiro F. Pincus Z. Matthijssens F. Araiz C. Mandel A. Vlachos M. Edwards S.-A. Fischer G. Davidson A. Pryor R. E. Stevens A. Slack F. J. Tavernarakis N. Braeckman B. P. Schroeder F. C. Nehrke K. Gems D. Anthranilate Fluorescence Marks a Calcium-Propagated Necrotic Wave That Promotes Organismal Death in C. Elegans. PLoS Biol. 2013;11:e1001613. doi: 10.1371/journal.pbio.1001613. PubMed DOI PMC

De Koninck P. Schulman H. Sensitivity of CaM Kinase II to the Frequency of Ca 2+ Oscillations. Science. 1998;279:227. doi: 10.1126/science.279.5348.227. PubMed DOI

Colella M. Grisan F. Robert V. Turner J. D. Thomas A. P. Pozzan T. Ca 2+ Oscillation Frequency Decoding in Cardiac Cell Hypertrophy: Role of Calcineurin/NFAT as Ca 2+ Signal Integrators. Proc. Natl. Acad. Sci. 2008;105:2859. doi: 10.1073/pnas.0712316105. PubMed DOI PMC

Buzsáki G. Draguhn A. Neuronal Oscillations in Cortical Networks. Science. 2004;304:1926. doi: 10.1126/science.1099745. PubMed DOI

Jokisch D. Jensen O. Modulation of Gamma and Alpha Activity during a Working Memory Task Engaging the Dorsal or Ventral Stream. J. Neurosci. 2007;27:3244. doi: 10.1523/JNEUROSCI.5399-06.2007. PubMed DOI PMC

Rubio Ayala M. Syrovets T. Hafner S. Zablotskii V. Dejneka A. Simmet T. Spatiotemporal Magnetic Fields Enhance Cytosolic Ca 2+ Levels and Induce Actin Polymerization via Activation of Voltage-Gated Sodium Channels in Skeletal Muscle Cells. Biomaterials. 2018;163:174. doi: 10.1016/j.biomaterials.2018.02.031. PubMed DOI

Carson J. J. Prato F. S. Drost D. J. Diesbourg L. D. Dixon S. J. Time-Varying Magnetic Fields Increase Cytosolic Free Ca2+ in HL-60 Cells. Am. J. Physiol. Physiol. 1990;259:C687. doi: 10.1152/ajpcell.1990.259.4.C687. PubMed DOI

Wu H. Li C. Masood M. Zhang Z. González-Almela E. Castells-Garcia A. Zou G. Xu X. Wang L. Zhao G. Yu S. Zhu P. Wang B. Qin D. Liu J. Static Magnetic Fields Regulate T-Type Calcium Ion Channels and Mediate Mesenchymal Stem Cells Proliferation. Cells. 2022;11:2460. doi: 10.3390/cells11152460. PubMed DOI PMC

Ikehara T. Nishisako H. Minami Y. Ichinose H. Shiraishi T. Kitamura M. Shono M. Houchi H. Kawazoe K. Minakuchi K. Yoshizaki K. Kinouchi Y. Miyamoto H. Effects of Exposure to a Time-Varying 1.5 T Magnetic Field on the Neurotransmitter-Activated Increase in Intracellular Ca2+ in Relation to Actin Fiber and Mitochondrial Functions in Bovine Adrenal Chromaffin Cells. Biochim. Biophys. Acta - Gen. Subj. 2010;1800:1221. doi: 10.1016/j.bbagen.2010.09.001. PubMed DOI

Heinrich A. Szostek A. Nees F. Meyer P. Semmler W. Flor H. Effects of Static Magnetic Fields on Cognition, Vital Signs, and Sensory Perception: A Meta-Analysis. J. Magn. Reson. Imaging. 2011;34:758. doi: 10.1002/jmri.22720. PubMed DOI

Navarro E. A. Gomez-Perretta C. Montes F. Low Intensity Magnetic Field Influences Short-Term Memory: A Study in a Group of Healthy Students. Bioelectromagnetics. 2016;37:37. doi: 10.1002/bem.21944. PubMed DOI

Navarro E. A. Navarro-Modesto E. A Mathematical Model and Experimental Procedure to Analyze the Cognitive Effects of Audio Frequency Magnetic Fields. Front. Hum. Neurosci. 2023;17:1–13. PubMed PMC

Henley J. M. Wilkinson K. A. Synaptic AMPA Receptor Composition in Development, Plasticity and Disease. Nat. Rev. Neurosci. 2016;17:337. doi: 10.1038/nrn.2016.37. PubMed DOI

Bers D. M. Cardiac Excitation–Contraction Coupling. Nature. 2002;415:198. doi: 10.1038/415198a. PubMed DOI

Xu J. Liu K. Chen T. Zhan T. Ouyang Z. Wang Y. Liu W. Zhang X. Sun Y. Xu G. Wang X. Rotating Magnetic Field Delays Human Umbilical Vein Endothelial Cell Aging and Prolongs the Lifespan of Caenorhabditis Elegans. Aging. 2019;11:10385. doi: 10.18632/aging.102466. PubMed DOI PMC

Monteith G. R. Davis F. M. Roberts-Thomson S. J. Calcium Channels and Pumps in Cancer: Changes and Consequences. J. Biol. Chem. 2012;287:31666. doi: 10.1074/jbc.R112.343061. PubMed DOI PMC

Feske S. Calcium Signalling in Lymphocyte Activation and Disease. Nat. Rev. Immunol. 2007;7:690. doi: 10.1038/nri2152. PubMed DOI

European Bioinformatics Institute, ChEMBL Database, https://www.ebi.ac.uk/chembl/

Hutchings C. J. Colussi P. Clark T. G. Ion Channels as Therapeutic Antibody Targets. MAbs. 2019;11:265. doi: 10.1080/19420862.2018.1548232. PubMed DOI PMC

Montnach J. Blömer L. A. Lopez L. Filipis L. Meudal H. Lafoux A. Nicolas S. Chu D. Caumes C. Béroud R. Jopling C. Bosmans F. Huchet C. Landon C. Canepari M. De Waard M. In Vivo Spatiotemporal Control of Voltage-Gated Ion Channels by Using Photoactivatable Peptidic Toxins. Nat. Commun. 2022;13:417. doi: 10.1038/s41467-022-27974-w. PubMed DOI PMC

Zhu Z. Deng Z. Wang Q. Wang Y. Zhang D. Xu R. Guo L. Wen H. Simulation and Machine Learning Methods for Ion-Channel Structure Determination, Mechanistic Studies and Drug Design. Front. Pharmacol. 2022;13:939555. doi: 10.3389/fphar.2022.939555. PubMed DOI PMC

Plank M. J. Wall D. J. N. David T. Atherosclerosis and Calcium Signalling in Endothelial Cells. Prog. Biophys. Mol. Biol. 2006;91:287. doi: 10.1016/j.pbiomolbio.2005.07.005. PubMed DOI

Wiesner T. F. Berk B. C. Nerem R. M. A Mathematical Model of the Cytosolic-Free Calcium Response in Endothelial Cells to Fluid Shear Stress. Proc. Natl. Acad. Sci. 1997;94:3726. doi: 10.1073/pnas.94.8.3726. PubMed DOI PMC

Dull R. O. Davies P. F. Flow Modulation of Agonist (ATP)-Response (Ca2+) Coupling in Vascular Endothelial Cells. Am. J. Physiol. Circ. Physiol. 1991;261:H149. doi: 10.1152/ajpheart.1991.261.1.H149. PubMed DOI

Shen J. Luscinskas F. W. Connolly A. Dewey C. F. Gimbrone M. A. Fluid Shear Stress Modulates Cytosolic Free Calcium in Vascular Endothelial Cells. Am. J. Physiol. Physiol. 1992;262:C384. doi: 10.1152/ajpcell.1992.262.2.C384. PubMed DOI

Yamamoto K. Korenaga R. Kamiya A. Ando J. Fluid Shear Stress Activates Ca 2+ Influx Into Human Endothelial Cells via P2X4 Purinoceptors. Circ. Res. 2000;87:385. doi: 10.1161/01.RES.87.5.385. PubMed DOI

Jacob R. Calcium Oscillations in Endothelial Cells. Cell Calcium. 1991;12:127. doi: 10.1016/0143-4160(91)90014-6. PubMed DOI

Yokota Y. Nakajima H. Wakayama Y. Muto A. Kawakami K. Fukuhara S. Mochizuki N. Endothelial Ca2+ Oscillations Reflect VEGFR Signaling-Regulated Angiogenic Capacity in Vivo. Elife. 2015;4:e08817. doi: 10.7554/eLife.08817. PubMed DOI PMC

Kirschvink J. L. Kobayashi-Kirschvink A. Woodford B. J. Magnetite Biomineralization in the Human Brain. Proc. Natl. Acad. Sci. 1992;89:7683. doi: 10.1073/pnas.89.16.7683. PubMed DOI PMC

Brem F. Hirt A. M. Winklhofer M. Frei K. Yonekawa Y. Wieser H.-G. Dobson J. Magnetic Iron Compounds in the Human Brain: A Comparison of Tumour and Hippocampal Tissue. J. R. Soc. Interface. 2006;3:833. doi: 10.1098/rsif.2006.0133. PubMed DOI PMC

Grassi-Schultheiss P. P. Heller F. Dobson J. Analysis of Magnetic Material in the Human Heart, Spleen and Liver. Biometals. 1997;10:351. doi: 10.1023/A:1018340920329. PubMed DOI

Robin Baker R. Mather J. G. Kennaugh J. H. Magnetic Bones in Human Sinuses. Nature. 1983;301:78. doi: 10.1038/301078a0. PubMed DOI

Kirschvink J. Ferromagnetic Crystals (Magnetite?) In Human Tissue. J. Exp. Biol. 1981;92:333. doi: 10.1242/jeb.92.1.333. PubMed DOI

Gorobets S. V. Medviediev O. V. Gorobets O. Y. Ivanchenko A. Biogenic Magnetic Nanoparticles in Human Organs and Tissues. Prog. Biophys. Mol. Biol. 2018;135:49. doi: 10.1016/j.pbiomolbio.2018.01.010. PubMed DOI

Gorobets O. Gorobets S. Koralewski M. Physiological Origin of Biogenic Magnetic Nanoparticles in Health and Disease: From Bacteria to Humans. Int. J. Nanomedicine. 2017;12:4371. doi: 10.2147/IJN.S130565. PubMed DOI PMC

Gorobets S. Gorobets O. Bulaievska M. Sharau I. Magnetic Force Microscopy of the Ethmoid Bones of Migratory and Non-Migratory Fishes. Acta Phys. Pol. A. 2018;133:734. doi: 10.12693/APhysPolA.133.734. DOI

Mikeshyna H. I. Darmenko Y. A. Gorobets O. Y. Gorobets S. V. Sharay I. V. Lazarenko O. M. Influence of Biogenic Magnetic Nanoparticles on the Vesicular Transport. Acta Phys. Pol. A. 2018;133:731. doi: 10.12693/APhysPolA.133.731. DOI

Gorobets S. Gorobets O. Bulaievska M. Sharay I. Detection of Biogenic Magnetic Nanoparticles in Ethmoid Bones of Migratory and Non-Migratory Fishes. SN Appl. Sci. 2019;1:63. doi: 10.1007/s42452-018-0072-1. DOI

Gorobets S. Gorobets O. Gorobets Y. Bulaievska M. Chain-Like Structures of Biogenic and Nonbiogenic Magnetic Nanoparticles in Vascular Tissues. Bioelectromagnetics. 2022;43:119. doi: 10.1002/bem.22390. PubMed DOI

Darmenko Y. A. Gorobets O. Y. Gorobets S. V. Sharay I. V. Lazarenko O. M. Detection of Biogenic Magnetic Nanoparticles in Human Aortic Aneurysms. Acta Phys. Pol. A. 2018;133:738. doi: 10.12693/APhysPolA.133.738. DOI

Brem F. Hirt A. M. Simon C. Wieser H.-G. Dobson J. Characterization of Iron Compounds in Tumour Tissue from Temporal Lobe Epilepsy Patients Using Low Temperature Magnetic Methods. BioMetals. 2005;18:191. doi: 10.1007/s10534-004-6253-y. PubMed DOI

Gorobets O. Gorobets S. Sharai I. Polyakova T. Zablotskii V. Interaction of Magnetic Fields with Biogenic Magnetic Nanoparticles on Cell Membranes: Physiological Consequences for Organisms in Health and Disease. Bioelectrochemistry. 2023;151:108390. doi: 10.1016/j.bioelechem.2023.108390. PubMed DOI

Kelly C. Couch R. K. Ha V. T. Bodart C. M. Wu J. Huff S. Herrel N. T. Kim H. D. Zimmermann A. O. Shattuck J. Pan Y.-C. Kaeberlein M. Grillo A. S. Iron Status Influences Mitochondrial Disease Progression in Complex I-Deficient Mice. Elife. 2023;12:e75825. doi: 10.7554/eLife.75825. PubMed DOI PMC

Gieré R. Magnetite in the Human Body: Biogenic vs. Anthropogenic. Proc. Natl. Acad. Sci. U. S. A. 2016;113(43):11986–11987. doi: 10.1073/pnas.1613349113. PubMed DOI PMC

Maher B. A. Airborne Magnetite- and Iron-Rich Pollution Nanoparticles: Potential Neurotoxicants and Environmental Risk Factors for Neurodegenerative Disease, Including Alzheimer's Disease. J. Alzheimer’s Dis. 2019;71:361. PubMed

Winkler S. A. Schmitt F. Landes H. de Bever J. Wade T. Alejski A. Rutt B. K. Gradient and Shim Technologies for Ultra High Field MRI. Neuroimage. 2018;168:59. doi: 10.1016/j.neuroimage.2016.11.033. PubMed DOI PMC

Avasthi A. Caro C. Pozo-Torres E. Leal M. P. García-Martín M. L. Magnetic Nanoparticles as MRI Contrast Agents. Top. Curr. Chem. 2020;378:40. doi: 10.1007/s41061-020-00302-w. PubMed DOI PMC

Kirschvink J. L. Kobayashi-Kirschvink A. Woodford B. J. Magnetite Biomineralization in the Human Brain. Proc. Natl. Acad. Sci. 1992;89:7683. doi: 10.1073/pnas.89.16.7683. PubMed DOI PMC

Van de Walle A. Plan Sangnier A. Abou-Hassan A. Curcio A. Hémadi M. Menguy N. Lalatonne Y. Luciani N. Wilhelm C. Biosynthesis of Magnetic Nanoparticles from Nano-Degradation Products Revealed in Human Stem Cells. Proc. Natl. Acad. Sci. 2019;116:4044. doi: 10.1073/pnas.1816792116. PubMed DOI PMC

Gorobets S. V. Gorobets O. Y. Functions of Biogenic Magnetic Nanoparticles in Organisms. Funct. Mater. 2012;19:18.

Gorobets S. Gorobets O. Gorobets Y. Bulaievska M. Chain-Like Structures of Biogenic and Nonbiogenic Magnetic Nanoparticles in Vascular Tissues. Bioelectromagnetics. 2022;43:119. doi: 10.1002/bem.22390. PubMed DOI

Medviediev O. Gorobets O. Y. Gorobets S. V. Yadrykhins’Ky V. S. The Prediction of Biogenic Magnetic Nanoparticles Biomineralization in Human Tissues and Organs. J. Phys.: Conf. Ser. 2017;903:012002. doi: 10.1088/1742-6596/903/1/012002. DOI

Gorobets O. Gorobets S. Koralewski M. Physiological Origin of Biogenic Magnetic Nanoparticles in Health and Disease: From Bacteria to Humans. Int. J. Nanomedicine. 2017;12:4371. doi: 10.2147/IJN.S130565. PubMed DOI PMC

Hautot D. Pankhurst Q. A. Morris C. M. Curtis A. Burn J. Dobson J. Preliminary Observation of Elevated Levels of Nanocrystalline Iron Oxide in the Basal Ganglia of Neuroferritinopathy Patients. Biochim. Biophys. Acta - Mol. Basis Dis. 2007;1772:21. doi: 10.1016/j.bbadis.2006.09.011. PubMed DOI PMC

Kobayashi A. Yamamoto N. Kirschvink J. Studies of Inorganic Crystals in Biological Tissue: Magnetic in Human Tumor. J. Japan Soc. Powder Powder Metall. 1997;44:294. doi: 10.2497/jjspm.44.294. DOI

Dobson J. Nanoscale Biogenic Iron Oxides and Neurodegenerative Disease. FEBS Lett. 2001;496:1–5. doi: 10.1016/S0014-5793(01)02386-9. PubMed DOI

Vainshtein M. Suzina N. Kudryashova E. Ariskina E. New Magnet-Sensitive Structures in Bacterial and Archaeal Cells. Biol. Cell. 2002;94:29–35. doi: 10.1016/S0248-4900(02)01179-6. PubMed DOI

Gorobets O. Y. Gorobets S. V. Sorokina L. V. Biomineralization and Synthesis of Biogenic Magnetic Nanoparticles and Magnetosensitive Inclusions in Microorganisms and Fungi. Funct. Mater. 2014;21:373. doi: 10.15407/fm21.04.373. DOI

Gorobets Y. Gorobets S. Gorobets O. Magerman A. Sharai I. Biogenic and Anthropogenic Magnetic Nanoparticles in the Ploem Sieve Tubes of Plants. J. Microbiol. Biotechnol. Food Sci. 2023:e5484. doi: 10.55251/jmbfs.5484. DOI

Gorobets S. Gorobets O. Sharay I. Yevzhyk L. The Influence of Artificial and Biogenic Magnetic Nanoparticles on the Metabolism of Fungi. Funct. Mater. 2021;28:315.

Gorobets S. V. Gorobets O. Y. Medviediev O. V. Golub V. O. Kuzminykh L. V. Biogenic Magnetic Nanoparticles in Lung, Heart and Liver. Funct. Mater. 2017;24:405.

Veiseh O. Gunn J. W. Zhang M. Design and Fabrication of Magnetic Nanoparticles for Targeted Drug Delivery and Imaging. Adv. Drug Deliv. Rev. 2010;62:284. doi: 10.1016/j.addr.2009.11.002. PubMed DOI PMC

Chomoucka J. Drbohlavova J. Huska D. Adam V. Kizek R. Hubalek J. Magnetic Nanoparticles and Targeted Drug Delivering. Pharmacol. Res. 2010;62:144. doi: 10.1016/j.phrs.2010.01.014. PubMed DOI

Price P. M. Mahmoud W. E. Al-Ghamdi A. A. Bronstein L. M. Magnetic Drug Delivery: Where the Field Is Going. Front. Chem. 2018;6:1. doi: 10.3389/fchem.2018.00001. PubMed DOI PMC

Mirvakili S. M. Langer R. Wireless On-Demand Drug Delivery. Nat. Electron. 2021;4:464. doi: 10.1038/s41928-021-00614-9. DOI

Gorobets S. V. Gorobets O. Y. Chyzh Y. M. Sivenok D. V. Magnetic Dipole Interaction of Endogenous Magnetic Nanoparticles with Magnetoliposomes for Targeted Drug Delivery. Biophys. 2013;58:379. doi: 10.1134/S000635091303007X. PubMed DOI

Gavilán H. Avugadda S. K. Fernández-Cabada T. Soni N. Cassani M. Mai B. T. Chantrell R. Pellegrino T. Magnetic Nanoparticles and Clusters for Magnetic Hyperthermia: Optimizing Their Heat Performance and Developing Combinatorial Therapies to Tackle Cancer. Chem. Soc. Rev. 2021;50:11614. doi: 10.1039/D1CS00427A. PubMed DOI

Rajan A. Sahu N. K. Review on Magnetic Nanoparticle-Mediated Hyperthermia for Cancer Therapy. J. Nanoparticle Res. 2020;22:319. doi: 10.1007/s11051-020-05045-9. DOI

Kirschvink J. L. Walker M. M. Chang S.-B. Dizon A. E. Peterson K. A. Chains of Single-Domain Magnetite Particles in Chinook Salmon,Oncorhynchus Tshawytscha. J. Comp. Physiol. A. 1985;157:375. doi: 10.1007/BF00618127. DOI

Kirschvink J. Magnetite-Based Magnetoreception. Curr. Opin. Neurobiol. 2001;11:462. doi: 10.1016/S0959-4388(00)00235-X. PubMed DOI

Alfsen E. M. Størmer F. C. Njå A. Walløe L. A Proposed Tandem Mechanism for Memory Storage in Neurons Involving Magnetite and Prions. Med. Hypotheses. 2018;119:98. doi: 10.1016/j.mehy.2018.07.003. PubMed DOI

Miclaus S. Iftode C. Miclaus A. Would the human brain be able to erect specific effects due to the magnetic field component of an uhf field via magnetite nanoparticles? Prog. Electromagn. Res. M. 2018;69:23. doi: 10.2528/PIERM18030806. DOI

Miller I. Lonetree B. The Sedona Effect: Correlations between Geomagnetic Anomalies, EEG Brainwaves & Schumann Resonance. J. Conscious. Explor. Res. 2013;4:630.

Gorobets S. Gorobets O. Gorobets Y. Bulaievska M. Chain-Like Structures of Biogenic and Nonbiogenic Magnetic Nanoparticles in Vascular Tissues. Bioelectromagnetics. 2022;43:119. doi: 10.1002/bem.22390. PubMed DOI

Kobayashi A. Yamamoto N. Kirschvink J. Studies of Inorganic Crystals in Biological Tissue: Magnetic in Human Tumor. J. Japan Soc. Powder Powder Metall. 1997;44:294. doi: 10.2497/jjspm.44.294. DOI

Gorobets O. Y., Gorobets S. V., and Gorobets Y. I., Biogenic Magnetic Nanoparticles. Biomineralization in Prokaryotes and Eukaryotes, in In Dekker Encyclopedia of Nanoscience and Nanotechnology, CRC Press, New York, 3rd edn, 2014, pp. 300–308

Putney J. W. Broad L. M. Braun F.-J. Lievremont J.-P. Bird G. S. J. Mechanisms of Capacitative Calcium Entry. J. Cell Sci. 2001;114:2223. doi: 10.1242/jcs.114.12.2223. PubMed DOI

Roux E. Bougaran P. Dufourcq P. Couffinhal T. Fluid Shear Stress Sensing by the Endothelial Layer. Front. Physiol. 2020;11:861. doi: 10.3389/fphys.2020.00861. PubMed DOI PMC

Skalak R. Tozeren A. Zarda R. P. Chien S. Strain Energy Function of Red Blood Cell Membranes. Biophys. J. 1973;13:245. doi: 10.1016/S0006-3495(73)85983-1. PubMed DOI PMC

Lacroix J. J. Botello-Smith W. M. Luo Y. Probing the Gating Mechanism of the Mechanosensitive Channel Piezo1 with the Small Molecule Yoda1. Nat. Commun. 2018;9:2029. doi: 10.1038/s41467-018-04405-3. PubMed DOI PMC

Chiu J.-J. Chien S. Effects of Disturbed Flow on Vascular Endothelium: Pathophysiological Basis and Clinical Perspectives. Physiol. Rev. 2011;91:327. doi: 10.1152/physrev.00047.2009. PubMed DOI PMC

Sonam S. Balasubramaniam L. Lin S.-Z. Ivan Y. M. Y. Pi-Jaumà I. Jebane C. Karnat M. Toyama Y. Marcq P. Prost J. Mège R.-M. Rupprecht J.-F. Ladoux B. Mechanical Stress Driven by Rigidity Sensing Governs Epithelial Stability. Nat. Phys. 2023;19:132. PubMed PMC

Cheng L. Li J. Sun H. Jiang H. Appropriate Mechanical Confinement Inhibits Multipolar Cell Division via Pole-Cortex Interaction. Phys. Rev. X. 2023;13:011036.

Jaffe L. F. Fast Calcium Waves. Cell Calcium. 2010;48:102. doi: 10.1016/j.ceca.2010.08.007. PubMed DOI

Galvanovskis J. Sandblom J. Bergqvist B. Galt S. Hamnerius Y. Cytoplasmic Ca2+ Oscillations in Human Leukemia T-Cells Are Reduced by 50 Hz Magnetic Fields. Bioelectromagnetics. 1999;20:269. doi: 10.1002/(SICI)1521-186X(1999)20:5<269::AID-BEM2>3.0.CO;2-S. PubMed DOI

Wang C. X. Hilburn I. A. Wu D.-A. Mizuhara Y. Cousté C. P. Abrahams J. N. H. Bernstein S. E. Matani A. Shimojo S. Kirschvink J. L. Transduction of the Geomagnetic Field as Evidenced from Alpha-Band Activity in the Human Brain. Eneuro. 2019;6:e0483. PubMed PMC

Kasai Y. Yamazawa T. Sakurai T. Taketani Y. Iino M. Endothelium-Dependent Frequency Modulation of Ca 2+ Signalling in Individual Vascular Smooth Muscle Cells of the Rat. J. Physiol. 1997;504:349. doi: 10.1111/j.1469-7793.1997.349be.x. PubMed DOI PMC

ZHANG W. LIU H. T. MAPK Signal Pathways in the Regulation of Cell Proliferation in Mammalian Cells. Cell Res. 2002;12:9. doi: 10.1038/sj.cr.7290105. PubMed DOI

Roth Flach R. J. Guo C.-A. Danai L. V. Yawe J. C. Gujja S. Edwards Y. J. K. Czech M. P. Endothelial Mitogen-Activated Protein Kinase Kinase Kinase Kinase 4 Is Critical for Lymphatic Vascular Development and Function. Mol. Cell. Biol. 2016;36:1740. doi: 10.1128/MCB.01121-15. PubMed DOI PMC

Kempe S. NF- B Controls the Global pro-Inflammatory Response in Endothelial Cells: Evidence for the Regulation of a pro-Atherogenic Program. Nucleic Acids Res. 2005;33:5308. doi: 10.1093/nar/gki836. PubMed DOI PMC

Hoesel B. Schmid J. A. The Complexity of NF-κB Signaling in Inflammation and Cancer. Mol. Cancer. 2013;12:86. doi: 10.1186/1476-4598-12-86. PubMed DOI PMC

Lawrence T. The Nuclear Factor NF- B Pathway in Inflammation. Cold Spring Harb. Perspect. Biol. 2009;1:a001651. PubMed PMC

Liu T. Zhang L. Joo D. Sun S.-C. NF-κB Signaling in Inflammation. Signal Transduct. Target. Ther. 2017;2:17023. doi: 10.1038/sigtrans.2017.23. PubMed DOI PMC

Crabtree G. R. Olson E. N. NFAT Signaling. Cell. 2002;109:S67. doi: 10.1016/S0092-8674(02)00699-2. PubMed DOI

Manabe T. Park H. Minami T. Calcineurin-Nuclear Factor for Activated T Cells (NFAT) Signaling in Pathophysiology of Wound Healing. Inflamm. Regen. 2021;41:26. doi: 10.1186/s41232-021-00176-5. PubMed DOI PMC

Rinne A. Banach K. Blatter L. A. Regulation of Nuclear Factor of Activated T Cells (NFAT) in Vascular Endothelial Cells. J. Mol. Cell. Cardiol. 2009;47:400. doi: 10.1016/j.yjmcc.2009.06.010. PubMed DOI PMC

Moccia F. Negri S. Shekha M. Faris P. Guerra G. Endothelial Ca2+ Signaling, Angiogenesis and Vasculogenesis: Just What It Takes to Make a Blood Vessel. Int. J. Mol. Sci. 2019;20:3962. doi: 10.3390/ijms20163962. PubMed DOI PMC

Simonetti G. Mohaupt M. Kalzium Und Blutdruck. Ther. Umschau. 2007;64:249. doi: 10.1024/0040-5930.64.5.249. PubMed DOI

Curry F. E. Modulation of Venular Microvessel Permeability by Calcium Influx into Endothelial Cells. FASEB J. 1992;6:2456. doi: 10.1096/fasebj.6.7.1563597. PubMed DOI

Dalal P. J. Sullivan D. P. Weber E. W. Sacks D. B. Gunzer M. Grumbach I. M. Heller Brown J. Muller W. A. Spatiotemporal Restriction of Endothelial Cell Calcium Signaling Is Required during Leukocyte Transmigration. J. Exp. Med. 2021;218:e20192378. doi: 10.1084/jem.20192378. PubMed DOI PMC

Guerra G. Lucariello A. Perna A. Botta L. De Luca A. Moccia F. The Role of Endothelial Ca2+ Signaling in Neurovascular Coupling: A View from the Lumen. Int. J. Mol. Sci. 2018;19:938. doi: 10.3390/ijms19040938. PubMed DOI PMC

Zhang M. Fendler B. Peercy B. Goel P. Bertram R. Sherman A. Satin L. Long Lasting Synchronization of Calcium Oscillations by Cholinergic Stimulation in Isolated Pancreatic Islets. Biophys. J. 2008;95:4676. doi: 10.1529/biophysj.107.125088. PubMed DOI PMC

Taylor M. S. Francis M. Decoding Dynamic Ca2+ Signaling in the Vascular Endothelium. Front. Physiol. 2014;5:447. PubMed PMC

Cheng J. Wen J. Wang N. Wang C. Xu Q. Yang Y. Ion Channels and Vascular Diseases. Arterioscler. Thromb. Vasc. Biol. 2019;39:e146–e156. PubMed

Landstrom A. P. Dobrev D. Wehrens X. H. T. Calcium Signaling and Cardiac Arrhythmias. Circ. Res. 2017;120:1969. doi: 10.1161/CIRCRESAHA.117.310083. PubMed DOI PMC

Moccia F. Endothelial Ca2+ Signaling and the Resistance to Anticancer Treatments: Partners in Crime. Int. J. Mol. Sci. 2018;19:217. doi: 10.3390/ijms19010217. PubMed DOI PMC

Ghodbane S. Lahbib A. Sakly M. Abdelmelek H. Bioeffects of Static Magnetic Fields: Oxidative Stress, Genotoxic Effects, and Cancer Studies. Biomed Res. Int. 2013;2013:1. doi: 10.1155/2013/602987. PubMed DOI PMC

Rosen A. D. Mechanism of Action of Moderate-Intensity Static Magnetic Fields on Biological Systems. Cell Biochem. Biophys. 2003;39:163. doi: 10.1385/CBB:39:2:163. PubMed DOI

Lei H. Pan Y. Wu R. Lv Y. Innate Immune Regulation Under Magnetic Fields With Possible Mechanisms and Therapeutic Applications. Front. Immunol. 2020;11:582772. doi: 10.3389/fimmu.2020.582772. PubMed DOI PMC

Kolosnjaj-Tabi J. Wilhelm C. Clément O. Gazeau F. Cell Labeling with Magnetic Nanoparticles: Opportunity for Magnetic Cell Imaging and Cell Manipulation. J. Nanobiotechnology. 2013;11:S7. doi: 10.1186/1477-3155-11-S1-S7. PubMed DOI PMC

Nowak-Jary J. Machnicka B. In Vivo Biodistribution and Clearance of Magnetic Iron Oxide Nanoparticles for Medical Applications. Int. J. Nanomedicine. 2023;18:4067. doi: 10.2147/IJN.S415063. PubMed DOI PMC

Han D. Zhang B. Su L. Yang B. Attachment of Streptavidin-Modified Superparamagnetic Iron Oxide Nanoparticles to the PC-12 Cell Membrane. Biomed. Mater. 2020;15:045014. doi: 10.1088/1748-605X/ab7764. PubMed DOI

Dieckhoff J. Kaul M. G. Mummert T. Jung C. Salamon J. Adam G. Knopp T. Ludwig F. Balceris C. Ittrich H. In Vivo Liver Visualizations with Magnetic Particle Imaging Based on the Calibration Measurement Approach. Phys. Med. Biol. 2017;62:3470. doi: 10.1088/1361-6560/aa562d. PubMed DOI

Shang Y. Liu J. Zhang L. Wu X. Zhang P. Yin L. Hui H. Tian J. Deep Learning for Improving the Spatial Resolution of Magnetic Particle Imaging. Phys. Med. Biol. 2022;67:125012. doi: 10.1088/1361-6560/ac6e24. PubMed DOI

Takahashi A. Camacho P. Lechleiter J. D. Herman B. Measurement of Intracellular Calcium. Physiol. Rev. 1999;79:1089. doi: 10.1152/physrev.1999.79.4.1089. PubMed DOI

Dupont G. Combettes L. Bird G. S. Putney J. W. Calcium Oscillations. Cold Spring Harb. Perspect. Biol. 2011;3:a004226. PubMed PMC

Tóth S. Huneau D. Banrezes B. Ozil J. P. Egg Activation Is the Result of Calcium Signal Summation in the Mouse. Reproduction. 2006;131:27–34. PubMed

Salazar C. Politi A. Z. Höfer T. Decoding of Calcium Oscillations by Phosphorylation Cycles: Analytic Results. Biophys. J. 2008;94:1203–1215. doi: 10.1529/biophysj.107.113084. PubMed DOI PMC

Moccia F. Update on Vascular Endothelial Ca 2+ Signalling: A Tale of Ion Channels, Pumps and Transporters. World J. Biol. Chem. 2012;3:127. doi: 10.4331/wjbc.v3.i7.127. PubMed DOI PMC

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