Induction of Calcium Influx in Cortical Neural Networks by Nanomagnetic Forces

ACS Nano

Volumn 10, Issue 2, 2016, Pages 2331-2341

  Tay, Andy ^a   Kunze, Anja ^a   Murray, Coleman ^a   Di Carlo, Dino ^a,b,c  

^a Engineering IV   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

calcium imaging; conditioned media; cortical neurons; ferromagnetic nanoparticles; magnetic forces; mechano sensitive ion channels

Indexed keywords

FERROMAGNETIC MATERIALS; FERROMAGNETISM; FLUORESCENCE; MAGNETIC FIELD EFFECTS; MAGNETIC FIELDS; NANOMAGNETICS; NANOPARTICLES;

CALCIUM IMAGING; CONDITIONED MEDIAS; CORTICAL NEURONS; FERROMAGNETIC NANOPARTICLES; ION CHANNEL; MAGNETIC FORCE;

CALCIUM;

CALCIUM; CALCIUM CHANNEL N TYPE; MAGNETITE NANOPARTICLE;

ANIMAL; BRAIN CORTEX; CALCIUM SIGNALING; CELL CULTURE; CYTOLOGY; MAGNETIC FIELD; METABOLISM; NERVE CELL; NERVE CELL NETWORK; RAT;

ANIMALS; CALCIUM; CALCIUM CHANNELS, N-TYPE; CALCIUM SIGNALING; CELLS, CULTURED; CEREBRAL CORTEX; MAGNETIC FIELDS; MAGNETITE NANOPARTICLES; NERVE NET; NEURONS; RATS;

EID: 84960192370     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.5b07118     Document Type: Article

References (57)

1. West, A. E.; Chen, W. G.; Dalva, M. B.; Dolmetsch, R. E.; Kornhauser, J. M.; Shaywitz, A. J.; Takasu, M. A.; Tao, X.; Greenberg, M. E. Calcium Regulation of Neuronal Gene Expression Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 11024-11031 10.1073/pnas.191352298
2. Mattson, M. P.; LaFerla, F. M.; Chan, S. L.; Leissring, M. A.; Shepel, P. N.; Geiger, J. D. Calcium Signaling in the ER: Its Role in Neuronal Plasticity and Neurodegenerative Disorders Trends Neurosci. 2000, 23, 222-229 10.1016/S0166-2236(00)01548-4
3. Berridge, M. J.; Bootman, M. D.; Lipp, P. Calcium- A Life and Death Signal Nature 1998, 395, 645-648 10.1038/27094
4. Tsai, H.-C.; Zhang, F.; Adamantidis, A.; Stuber, G. D.; Bonci, A.; de Lecea, L.; Deisseroth, K. Phasic Firing in Dopaminergic Neurons Is Sufficient for Behavioral Conditioning Science 2009, 324, 1080-1084 10.1126/science.1168878
5. 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. 2012, 22, 61-71 10.1016/j.conb.2011.10.023
6. Banghart, M.; Borges, K.; Isacoff, E.; Trauner, D.; Kramer, R. H. Light-Activated Ion Channels for Remote Control of Neuronal Firing Nat. Neurosci. 2004, 7, 1381-1386 10.1038/nn1356
7. Tyler, W. J.; Tufail, Y.; Finsterwald, M.; Tauchmann, M. L.; Olson, E. J.; Majestic, C. Remote Excitation of Neuronal Circuits Using Low-Intensity, Low-Frequency Ultrasound PLoS One 2008, 3, e3511 10.1371/journal.pone.0003511
8. Marino, A.; Arai, S.; Hou, Y.; Sinibaldi, E.; Pellegrino, M.; Chang, Y.-T.; Mazzolai, B.; Mattoli, V.; Suzuki, M.; Ciofani, G. Piezoelectric Nanoparticle-Assisted Wireless Neuronal Stimulation ACS Nano 2015, 9, 7678 10.1021/acsnano.5b03162
9. Zemelman, B. V.; Lee, G. A.; Ng, M.; Miesenböck, G. Selective Photostimulation of Genetically chARGed Neurons Neuron 2002, 33, 15-22 10.1016/S0896-6273(01)00574-8
10. Boyden, E. S.; Zhang, F.; Bamberg, E.; Nagel, G.; Deisseroth, K. Millisecond-Timescale, Genetically Targeted Optical Control of Neural Activity Nat. Neurosci. 2005, 8, 1263-1268 10.1038/nn1525
11. Sparta, D. R.; Stamatakis, A. M.; Phillips, J. L.; Hovelsø, N.; van Zessen, R.; Stuber, G. D. Construction of Implantable Optical Fibers for Long-Term Optogenetic Manipulation of Neural Circuits Nat. Protoc. 2012, 7, 12-23 10.1038/nprot.2011.413
12. Wang, N.; Butler, J. P.; Ingber, D. E. Mechanotransduction across the Cell Surface and through the Cytoskeleton Science 1993, 260, 1124-1127 10.1126/science.7684161
13. Hughes, S.; McBain, S.; Dobson, J.; El Haj, A. J. Selective Activation of Mechanosensitive Ion Channels Using Magnetic Particles J. R. Soc., Interface 2008, 5, 855-863 10.1098/rsif.2007.1274
14. Huang, H.; Delikanli, S.; Zeng, H.; Ferkey, D. M.; Pralle, A. Remote Control of Ion Channels and Neurons through Magnetic-Field Heating of Nanoparticles Nat. Nanotechnol. 2010, 5, 602-606 10.1038/nnano.2010.125
15. Chen, R.; Romero, G.; Christiansen, M. G.; Mohr, A.; Anikeeva, P. Wireless Magnetothermal Deep Brain Stimulation Science 2015, 347, 1477-1480 10.1126/science.1261821
16. Yuste, R. From the Neuron Doctrine to Neural Networks Nat. Rev. Neurosci. 2015, 16, 487-497 10.1038/nrn3962
17. Kisaalita, W. S.; Evans, M.; Lund, R. B. Size Changes in Differentiating Neuroblastoma Cells In Vitro Cell. Dev. Biol.: Anim. 1997, 33, 734-737 10.1007/s11626-997-0148-5
18. Clement, G. T.; Nomura, H.; Adachi, H.; Kamakura, T. The Feasibility of Non-Contact Ultrasound for Medical Imaging Phys. Med. Biol. 2013, 58, 6263-6278 10.1088/0031-9155/58/18/6263
19. Steketee, M. B.; Moysidis, S. N.; Jin, X.-L.; Weinstein, J. E.; Pita-Thomas, W.; Raju, H. B.; Iqbal, S.; Goldberg, J. L. Nanoparticle-Mediated Signaling Endosome Localization Regulates Growth Cone Motility and Neurite Growth Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 19042-19047 10.1073/pnas.1019624108
20. Kunze, A.; Tseng, P.; Godzich, C.; Murray, C.; Caputo, A.; Schweizer, F. E.; Di Carlo, D. Engineering Cortical Neuron Polarity with Nanomagnets on a Chip ACS Nano 2015, 9, 3664 10.1021/nn505330w
21. Tay, A. K.; Dhar, M.; Pushkarsky, I.; Di Carlo, D. Research Highlights: Manipulating Cells inside and Out Lab Chip 2015, 15, 2533-2537 10.1039/C5LC90060C
22. Dobson, J. Remote Control of Cellular Behaviour with Magnetic Nanoparticles Nat. Nanotechnol. 2008, 3, 139-143 10.1038/nnano.2008.39
23. Jung, S.; Bang, M.; Kim, B. S.; Lee, S.; Kotov, N. A.; Kim, B.; Jeon, D. Intracellular Gold Nanoparticles Increase Neuronal Excitability and Aggravate Seizure Activity in the Mouse Brain PLoS One 2014, 9, e91360 10.1371/journal.pone.0091360
24. Kim, S.; Im, W. S.; Kang, L.; Lee, S. T.; Chu, K.; Kim, B. I. The Application of Magnets Directs the Orientation of Neurite Outgrowth in Cultured Human Neuronal Cells J. Neurosci. Methods 2008, 174, 91-96 10.1016/j.jneumeth.2008.07.005
25. Etoc, F.; Vicario, C.; Lisse, D.; Siaugue, J.-M.; Piehler, J.; Coppey, M.; Dahan, M. Magnetogenetic Control of Protein Gradients inside Living Cells with High Spatial and Temporal Resolution Nano Lett. 2015, 15, 3487 10.1021/acs.nanolett.5b00851
26. Walkey, C. D.; Olsen, J. B.; Song, F.; Liu, R.; Guo, H.; Olsen, D. W. H.; Cohen, Y.; Emili, A.; Chan, W. C. W. Protein Corona Fingerprinting Predicts the Cellular Interaction of Gold and Silver Nanoparticles ACS Nano 2014, 8, 2439-2455 10.1021/nn406018q
27. Lesniak, A.; Fenaroli, F.; Monopoli, M. P.; Åberg, C.; Dawson, K. A.; Salvati, A. Effects of the Presence or Absence of a Protein Corona on Silica Nanoparticle Uptake and Impact on Cells ACS Nano 2012, 6, 5845-5857 10.1021/nn300223w
28. He, C.; Hu, Y.; Yin, L.; Tang, C.; Yin, C. Effects of Particle Size and Surface Charge on Cellular Uptake and Biodistribution of Polymeric Nanoparticles Biomaterials 2010, 31, 3657-3666 10.1016/j.biomaterials.2010.01.065
29. Gao, H.; Yang, Z.; Zhang, S.; Cao, S.; Shen, S.; Pang, Z.; Jiang, X. Ligand Modified Nanoparticles Increases Cell Uptake, Alters Endocytosis and Elevates Glioma Distribution and Internalization Sci. Rep. 2013, 3, 2534 10.1038/srep02534
30. Westenbroek, R. E.; Hell, J. W.; Warner, C.; Dubel, S. J.; Snutch, T. P.; Catterall, W. A. Biochemical Properties and Subcellular Distribution of an N-Type Calcium Channel Alpha 1 Subunit Neuron 1992, 9, 1099-1115 10.1016/0896-6273(92)90069-P
31. Rao, W.; Wang, H.; Han, J.; Zhao, S.; Dumbleton, J.; Agarwal, P.; Zhang, W.; Zhao, G.; Yu, J.; Zynger, D. L. et al. Chitosan-Decorated Doxorubicin-Encapsulated Nanoparticle Targets and Eliminates Tumor Reinitiating Cancer Stem-like Cells ACS Nano 2015, 9, 5725-5740 10.1021/nn506928p
32. Fajardo, O.; Meseguer, V.; Belmonte, C.; Viana, F. TRPA1 Channels Mediate Cold Temperature Sensing in Mammalian Vagal Sensory Neurons: Pharmacological and Genetic Evidence J. Neurosci. 2008, 28, 7863-7875 10.1523/JNEUROSCI.1696-08.2008
33. Emptage, N. J.; Reid, C. A.; Fine, A. Calcium Stores in Hippocampal Synaptic Boutons Mediate Short-Term Plasticity, Store-Operated Ca2+ Entry, and Spontaneous Transmitter Release Neuron 2001, 29, 197-208 10.1016/S0896-6273(01)00190-8
34. Delmas, P.; Coste, B. Mechano-Gated Ion Channels in Sensory Systems Cell 2013, 155, 278-284 10.1016/j.cell.2013.09.026
35. Pravettoni, E.; Bacci, a.; Coco, S.; Forbicini, P.; Matteoli, M.; Verderio, C. Different Localizations and Functions of L-Type and N-Type Calcium Channels during Development of Hippocampal Neurons Dev. Biol. 2000, 227, 581-594 10.1006/dbio.2000.9872
36. Cai, D.; Mataraza, J. M.; Qin, Z.-H.; Huang, Z.; Huang, J.; Chiles, T. C.; Carnahan, D.; Kempa, K.; Ren, Z. Highly Efficient Molecular Delivery into Mammalian Cells Using Carbon Nanotube Spearing Nat. Methods 2005, 2, 449-454 10.1038/nmeth761
37. Plank, C.; Schillinger, U.; Scherer, F.; Bergemann, C.; Rémy, J. S.; Krötz, F.; Anton, M.; Lausier, J.; Rosenecker, J. The Magnetofection Method: Using Magnetic Force to Enhance Gene Delivery Biol. Chem. 2003, 384, 737-747 10.1515/BC.2003.082
38. Santos, L. J.; Reis, R. L.; Gomes, M. E. Harnessing Magnetic-Mechano Actuation in Regenerative Medicine and Tissue Engineering Trends Biotechnol. 2015, 33, 471-479 10.1016/j.tibtech.2015.06.006
39. Ito, A.; Akiyama, H.; Kawabe, Y.; Kamihira, M. Magnetic Force-Based Cell Patterning Using Arg-Gly-Asp (RGD) Peptide-Conjugated Magnetite Cationic Liposomes J. Biosci. Bioeng. 2007, 104, 288-293 10.1263/jbb.104.288
40. Kriha, O.; Becker, M.; Lehmann, M.; Kriha, D.; Krieglstein, J.; Yosef, M.; Schlecht, S.; Wehrspohn, R. B.; Wendorff, J. H.; Greiner, A. Connection of Hippocampal Neurons by Magnetically Controlled Movement of Short Electrospun Polymer Fibers-A Route to Magnetic Micromanipulators Adv. Mater. 2007, 19, 2483-2485 10.1002/adma.200601937
41. Sakar, M. S.; Steager, E. B.; Cowley, A.; Kumar, V.; Pappas, G. J. Wireless Manipulation of Single Cells Using Magnetic Microtransporters 2011 IEEE Int. Conf. Robot. Autom. 2011, 2668-2673 10.1109/ICRA.2011.5980100
42. Xie, J.; Chen, L.; Varadan, V. K.; Yancey, J.; Srivatsan, M. The Effects of Functional Magnetic Nanotubes with Incorporated Nerve Growth Factor in Neuronal Differentiation of PC12 Cells Nanotechnology 2008, 19, 105101 10.1088/0957-4484/19/10/105101
43. Fischer, T. M.; Steinmetz, P. N.; Odde, D. J. Robust Micromechanical Neurite Elicitation in Synapse-Competent Neurons via Magnetic Bead Force Application Ann. Biomed. Eng. 2005, 33, 1229-1237 10.1007/s10439-005-5509-1
44. Mannix, R. J.; Kumar, S.; Cassiola, F.; Montoya-Zavala, M.; Feinstein, E.; Prentiss, M.; Ingber, D. E. Nanomagnetic Actuation of Receptor-Mediated Signal Transduction Nat. Nanotechnol. 2008, 3, 36-40 10.1038/nnano.2007.418
45. Tyler, W. J. The Mechanobiology of Brain Function Nat. Rev. Neurosci. 2012, 13, 867-878 10.1038/nrn3383
46. Rosenberg, S. S.; Spitzer, N. C. Calcium Signaling in Neuronal Development Cold Spring Harbor Perspect. Biol. 2011, 3, a004259 10.1101/cshperspect.a004259
47. Perlmutter, J. S.; Mink, J. W. Deep Brain Stimulation Annu. Rev. Neurosci. 2006, 29, 229-257 10.1146/annurev.neuro.29.051605.112824
48. Matthews, B. D.; Lavan, D. A.; Overby, D. R.; Karavitis, J.; Ingber, D. E. Electromagnetic Needles with Submicron Pole Tip Radii for Nanomanipulation of Biomolecules and Living Cells Appl. Phys. Lett. 2004, 85, 2968-2970 10.1063/1.1802383
49. Summers, H. D.; Rees, P.; Holton, M. D.; Brown, M. R.; Chappell, S. C.; Smith, P. J.; Errington, R. J. Statistical Analysis of Nanoparticle Dosing in a Dynamic Cellular System Nat. Nanotechnol. 2011, 6, 170-174 10.1038/nnano.2010.277
50. Jiang, W.; Kim, B. Y. S.; Rutka, J. T.; Chan, W. C. W. Nanoparticle-Mediated Cellular Response Is Size-Dependent Nat. Nanotechnol. 2008, 3, 145-150 10.1038/nnano.2008.30
51. Grünberg, K.; Wawer, C.; Tebo, B. M.; Schüler, D. A Large Gene Cluster Encoding Several Magnetosome Proteins Is Conserved in Different Species of Magnetotactic Bacteria Appl. Environ. Microbiol. 2001, 67, 4573-4582 10.1128/AEM.67.10.4573-4582.2001
52. Chen, T.-W.; Wardill, T. J.; Sun, Y.; Pulver, S. R.; Renninger, S. L.; Baohan, A.; Schreiter, E. R.; Kerr, R. a; Orger, M. B.; Jayaraman, V.; Looger, L. L.; Svoboda, K.; Kim, D. S. Ultrasensitive Fluorescent Proteins for Imaging Neuronal Activity Nature 2013, 499, 295-300 10.1038/nature12354
53. Bulte, J. W. M.; Kraitchman, D. L. Iron Oxide MR Contrast Agents for Molecular and Cellular Imaging NMR Biomed. 2004, 17, 484-499 10.1002/nbm.924
54. Silva, G. A. Neuroscience Nanotechnology: Progress, Opportunities and Challenges Nat. Rev. Neurosci. 2006, 7, 65-74 10.1038/nrn1827
55. Eggeman, A. S.; Majetich, S. a.; Farrell, D.; Pankhurst, Q. a. Size and Concentration Effects on High Frequency Hysteresis of Iron Oxide Nanoparticles IEEE Trans. Magn. 2007, 43, 2451-2453 10.1109/TMAG.2007.894127
56. Cole, A. J.; David, A. E.; Wang, J.; Galbán, C. J.; Hill, H. L.; Yang, V. C. Polyethylene Glycol Modified, Cross-Linked Starch-Coated Iron Oxide Nanoparticles for Enhanced Magnetic Tumor Targeting Biomaterials 2011, 32, 2183-2193 10.1016/j.biomaterials.2010.11.040
57. Kong, S. D.; Zhang, W.; Lee, J. H.; Brammer, K.; Lal, R.; Karin, M.; Jin, S. Magnetically Vectored Nanocapsules for Tumor Penetration and Remotely Switchable on-Demand Drug Release Nano Lett. 2010, 10, 5088-5092 10.1021/nl1033733