Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-27T07:28:43.310Z Has data issue: false hasContentIssue false

Electromagnetic communication between cells through tunneling nanotubes

Published online by Cambridge University Press:  13 May 2020

Jan Pokorný*
Affiliation:
Institute of Physics of the Czech Academy of Sciences, Na Slovance 2, 182 21 Prague 8, Czech Republic
Jiří Pokorný
Affiliation:
Institute of Physics of the Czech Academy of Sciences, Na Slovance 2, 182 21 Prague 8, Czech Republic
Jan Vrba
Affiliation:
Faculty of Electrical Engineering, Czech Technical University, Technická 2, 166 27 Prague 6, Czech Republic
*
Author for correspondence: Jan Pokorný, E-mail: pokorny@fzu.cz

Abstract

Structures of tunneling nanotubes (TNTs) of the circular cross-section of 50 and 200 nm and length up to 1 mm form a communication system between cells. While transport of material such as endocytic vesicles, mitochondria, proteins, cytoplasmic molecules, etc., is experimentally proven, a possible transfer of electric and electromagnetic energy across TNTs corresponding to electrotechnical processes of excitation, propagation, and amplification in cavity systems is yet in a beginning stage of research. The ideas presented in this paper are based on technical mechanisms applied to submicroscopic systems. Main features of corrugated periodic structures, electromagnetic circular waveguides, the Manley–Rowe amplification, the Fröhlich non-linear interaction of coherent electric polar vibrations, and description of cut-off frequency propagating limits in the waveguide and cavities and along periodic structures are discussed. We suggest that cell-to-cell connection with TNTs may form a unified coherent cavity system which enables simultaneity and mutual cooperation in multicellular organisms.

Type
Research Paper
Copyright
Copyright © Cambridge University Press and the European Microwave Association 2020

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

Fröhlich, H (1968 a) Long-range coherence and energy storage in biological systems. International Journal of Quantum Chemistry II, 641649.10.1002/qua.560020505CrossRefGoogle Scholar
Fröhlich, H (1968 b) Bose condensation of strongly excited longitudinal electric modes. Physics Letters A 26, 402403.10.1016/0375-9601(68)90242-9CrossRefGoogle Scholar
Fröhlich, H (1969) Quantum mechanical concepts in biology. In Marois, M (ed.), Theoretical Physics and Biology. Amsterdam, Netherland: North Holland, pp. 1322. Proc. 1st Int. Conf. Theor. Phys. Biol., Versailles, France, 1967.Google Scholar
Fröhlich, H (1973) Collective behaviour of non-linearly coupled oscillating fields (with applications to biological systems). Journal of Collective Phenomena 1, 101109.Google Scholar
Fröhlich, H (1980) The biological effects of microwaves and related questions. In Marton, L and Marton, C (eds), Advances in Electronics and Electron Physics, vol. 53. Elsevier, Academic Press, New York, London, Toronto, Sydney, San Francisco, pp. 85152.Google Scholar
Pohl, HA, Braden, T, Robinson, S, Piclardi, J and Pohl, DG (1981) Life cycle alterations of the micro-dielectrophoretic effects of cells. Journal of Biological Physics 9, 133154.10.1007/BF01988247CrossRefGoogle Scholar
Hölzel, R (2001) Electric activity of non-excitable biological cells at radio frequencies. Electro- and Magnetobiology 20, 113.CrossRefGoogle Scholar
Pokorný, J, Hašek, J, Jelínek, F, Šaroch, J and Palán, B (2001) Electromagnetic activity of yeast cells in the M phase. Electro- and Magnetobiology 20, 371396.10.1081/JBC-100108577CrossRefGoogle Scholar
Sahu, S, Ghosh, S, Ghosh, B, Aswani, K, Hirata, K, Fujita, D and Bandyopadhyay, A (2013) Atomic water channel controlling remarkable properties of a single brain microtubule: correlating single protein to its supramolecular assembly. Biosensors & Bioelectronics 47, 141148.10.1016/j.bios.2013.02.050CrossRefGoogle ScholarPubMed
Sahu, S, Ghosh, S, Fujita, D and Bandyopadhyay, A (2014) Live visualizations of single isolated tubulin protein self-assembly via tunneling current: effect of electromagnetic pumping during spontaneous growth of microtubule. Scientific Reports 4, 7303.10.1038/srep07303CrossRefGoogle ScholarPubMed
Kasas, S, Ruggeri, FS, Benadiba, C, Maillard, C, Stupar, P, Tournu, H, Dietler, G and Longo, G (2015) Detecting nanoscale vibrations as signature of life. PNAS 112, 378381.10.1073/pnas.1415348112CrossRefGoogle ScholarPubMed
Pokorný, J, Pokorný, J and Kobilková, J (2013) Postulates on electromagnetic activity in biological systems and cancer. Integrative Biology 5, 14391446.10.1039/c3ib40166aCrossRefGoogle ScholarPubMed
Pokorný, J, Pokorný, J, Foletti, A, Kobilková, J, Vrba, J and Vrba, J Jr. (2015) Mitochondrial dysfunction and disturbed coherence: gate to cancer. Pharmaceuticals 8, 675695.10.3390/ph8040675CrossRefGoogle Scholar
Pokorný, J, Pokorný, J and Vrba, J (2019) Electromagnetic communication between cells through tunnelling nanotubes. 2019 European Microwave Conference in Central Europe (EuMCE), Prague, Czech Republic.Google Scholar
Rustom, A, Saffrich, R, Markovic, I, Walther, P and Gerdes, H-H (2004) Nanotubular highways for intercellular organelle transport. Science (New York, NY) 303, 10071010.10.1126/science.1093133CrossRefGoogle ScholarPubMed
Scholkmann, F (2016) Long range physical cell-to-cell signalling via mitochondria inside membrane nanotubes: a hypothesis. Theoretical Biology and Medical Modelling 13, 16.10.1186/s12976-016-0042-5CrossRefGoogle ScholarPubMed
Zhang, JH and Zhang, YY (2013) Membrane nanotubes: novel communication between distant cells. Science China Life Sciences 56, 994999.10.1007/s11427-013-4548-3CrossRefGoogle ScholarPubMed
Hurtig, J, Chiu, DT and Onfelt, B (2010) Intercellular nanotubes insights from imaging studies and beyond. Wiley Interdisciplinary Reviews. Nanomedicine and Nanobiotechnology 2, 260276.10.1002/wnan.80CrossRefGoogle ScholarPubMed
Antanavičiūtė, I, Rysevaite, K, Liutkevicius, V, Marandykina, A, Rimkutė, L, Sveikatienė, R, Uloza, V and Skeberdis, VA (2014) Long-distance communication between laryngeal carcinoma cells. PLoS ONE 9, e99196.10.1371/journal.pone.0099196CrossRefGoogle ScholarPubMed
Gerdes, HH, Rustom, A and Wang, X (2013) Tunneling nanotubes, an emerging intercellular communication route in development. Mechanisms of Development 130, 381387.10.1016/j.mod.2012.11.006CrossRefGoogle ScholarPubMed
Gerdes, HH and Pepperkok, R (2013) Cell-to-cell communication: current views and future perspectives. Cell and Tissue Research 352, 13.10.1007/s00441-013-1590-1CrossRefGoogle ScholarPubMed
Bloemendal, S and Kück, U (2013) Cell-to-cell communication in plants, animals, and fungi: a comparative review. Naturwissenschaften 100, 319.CrossRefGoogle ScholarPubMed
Sisakhtnezhad, S and Khosravi, L (2015) Emerging physiological and pathological implications of tunneling nanotubes formation between cells. European Journal of Cell Biology 94, 429443.10.1016/j.ejcb.2015.06.010CrossRefGoogle ScholarPubMed
Lu, J, Zheng, X, Li, F, Yu, Y, Chen, Z, Liu, Z, Wang, Z, Xu, H and Yang, W (2017) Tunneling nanotubes promote intercellular mitochondria transfer followed by increased invasiveness in bladder cancer cells. Oncotarget 8, 1553915552.10.18632/oncotarget.14695CrossRefGoogle ScholarPubMed
Bathany, C, Beahm, DL, Besch, S, Sachs, F and Hua, SZ (2012) A microfluidic platform for measuring electrical activity across cells. Biomicrofluidics 6, 034121.10.1063/1.4754599CrossRefGoogle ScholarPubMed
Jackson, MV, Morrison, TJ, Doherty, DF, McAuley, DF, Matthay, MA, Kissenpfennig, A, O'Kane, CM and Krasnodembskaya, AD (2016) Mitochondrial transfer via tunneling nanotubes is an important mechanism by which mesenchymal stem cells enhance macrophage phagocytosis in the in vitro and in vivo models of ARDS. Stem Cells (Dayton, Ohio) 34, 22102223.10.1002/stem.2372CrossRefGoogle ScholarPubMed
Vignais, ML, Caicedo, A, Brondello, J-M and Jorgensen, C (2017) Cell connections by tunneling nanotubes: effects of mitochondrial trafficking on target cell metabolism, homeostasis, and response to therapy. Stem Cells International 2017, 6917941.10.1155/2017/6917941CrossRefGoogle ScholarPubMed
Chaban, VV, Cho, T, Reid, CB and Norris, KC (2013) Physically disconnected non-diffusible cell-to-cell communication between neuroblastoma. American Journal of Translational Research 6, 6979.Google Scholar
Reguera, G (2011) When microbial conversation gets physical. Trends in Microbiology 19, 105113.10.1016/j.tim.2010.12.007CrossRefGoogle Scholar
Wang, X and Gerdes, H-H (2012) Long-distance electrical coupling via tunneling nanotubes. Biochimica et Biophysica Acta 1818, 20822086.10.1016/j.bbamem.2011.09.002CrossRefGoogle ScholarPubMed
Scholkmann, F (2015) Two emerging topics regarding long-range physical signaling in neurosystems: membrane nanotubes and electromagnetic fields. Journal of Integrative Neuroscience 14, 135153.10.1142/S0219635215300115CrossRefGoogle ScholarPubMed
Wang, X, Veruki, M, Bukoreshtliev, NV, Hartveit, E and Gerdes, H-H (2010) Animal cells connected by nanotubes can be electrically coupled through interposed gap-junction channels. PNAS 107, 1719417199.10.1073/pnas.1006785107CrossRefGoogle ScholarPubMed
Schulz, GE and Schirmer, RH (1979) Principles of Protein Structures. New York, Berlin, Heidelberg: Springer.10.1007/978-1-4612-6137-7CrossRefGoogle Scholar
Satarić, M, Tuszyński, JA and Žakula, RB (1993) Kinklike excitations as an energy transfer mechanism in microtubules. Physical Review E 48, 589597.10.1103/PhysRevE.48.589CrossRefGoogle ScholarPubMed
Tuszyński, JA, Hameroff, S, Satarić, MV, Trpisova, B and Nip, MLA (1995) Ferroelectric behavior in microtubule dipole lattices: implications for information processing, signaling and assembly/disassembly. Journal of Theoretical Biology 174, 371380.10.1006/jtbi.1995.0105CrossRefGoogle Scholar
Hyman, AA, Chrétien, D, Arnal, I and Wade, RH (1995) Structural changes accompanying GTP hydrolysis in microtubules: information from a slowly hydrolyzable analogue guanylyl-(α,β)-methylene-diphosphonate. Journal of Cell Biology 128, 117125.10.1083/jcb.128.1.117CrossRefGoogle ScholarPubMed
Melki, R, Carlier, M-F, Pantaloni, D and Timasheff, SN (1989) Cold depolymerization of microtubules to double ring: geometric stabilization of assemblies. Biochemistry 28, 91439152.10.1021/bi00449a028CrossRefGoogle ScholarPubMed
Böhm, KJ, Mavromatos, NE, Michette, A, Stracke, R and Unger, E (2005) Movement and alignment of microtubules in electric fields and electric-dipole-moment estimates. Electromagnetic Biology and Medicine 24, 319330.10.1080/15368370500380010CrossRefGoogle Scholar
Sataric, MV and Tuszynski, JA (2005) Nonlinear dynamics of microtubules: biophysical implications. Journal of Biological Physics 31, 487500.10.1007/s10867-005-7288-1CrossRefGoogle ScholarPubMed
Pokorný, J, Pokorný, J, Kobilková, J, Jandová, A, Vrba, J and Vrba, J Jr. (2014) Cancer–pathological breakdown of coherent energy states. Biophysical Reviews and Letters 9, 115133.CrossRefGoogle Scholar
Gurwitsch, A (1924) Physikalisches über mitogenetische Strahlen. Archiv für Mikroskopische Anatomie und Entwicklungsmechanik 103, 490498.10.1007/BF02107498CrossRefGoogle Scholar
Frank, GM and Gurwitsch, A (1927) Zur Frage der Identität mitogenetischer und ultravioletter Strahlen. Wilhelm Roux’ Archiv für Entwicklungsmechanik der Organismen 109, 451454.10.1007/BF02080806CrossRefGoogle Scholar
Jelínek, F and Pokorný, J (2001) Microtubules in biological cells as circular waveguides and resonators. Electro- and Magnetobiology 20, 7580.CrossRefGoogle Scholar
Collin, RE (1966) Foundations for Microwave Engineering. New York, St. Louis, San Francisco, Toronto, London, Sydney: McGraw–Hill Inc.Google Scholar
Pokorný, J, Pokorný, J and Borodavka, F (2017) Warburg effect – damping of electromagnetic oscillations. Electromagnetic Biology and Medicine 36, 270276.CrossRefGoogle ScholarPubMed
Zheng, J and Pollack, GH (2003) Long-range forces extending from polymer–gel surfaces. Physical Review E 68, 031408-1–7.10.1103/PhysRevE.68.031408CrossRefGoogle ScholarPubMed
Manley, JM and Rowe, HE (1956) Some general properties of nonlinear elements – part I. General energy relations. Proc. IRE 44, 904913.CrossRefGoogle Scholar
Pokorný, J and Wu, T-M (1998) Biophysical Aspects of Coherence and Biological Order. Praha: Academia; Berlin–Heidelberg–New York: Springer.CrossRefGoogle Scholar
Fröhlich, H (1978) Coherent electric vibrations in biological systems and the cancer problem. IEEE Transactions on Microwave Theory and Techniques 26, 613617.10.1109/TMTT.1978.1129446CrossRefGoogle Scholar
Amos, LA and Klug, AJ (1974) Arrangement of subunits in flagellar microtubules. Journal of Cell Science 14, 523549.Google ScholarPubMed
Schoutens, JE (2005) Dipole–dipole interactions in microtubules. Journal of Biological Physics 31, 3555.10.1007/s10867-005-3886-1CrossRefGoogle ScholarPubMed
Pokorný, J, Jelínek, F, Trkal, V, Lamprecht, I and Hölzel, R (1997) Vibrations in microtubules. Journal of Biological Physics 3, 171179.10.1023/A:1005092601078CrossRefGoogle Scholar
Pokorný, J (2004) Excitation of vibration in microtubules in living cell. Bioelectrochemistry 63, 321326.10.1016/j.bioelechem.2003.09.028CrossRefGoogle Scholar
Pelling, AE, Sehati, S, Gralla, EB, Valentine, JS and Gimzewski, JK (2004) Local nanomechanical motion of the cell wall of Saccharomyces cerevisiae. Science (New York, N.Y.) 305, 11471150.10.1126/science.1097640CrossRefGoogle ScholarPubMed
Pokorný, J (2009) Biophysical cancer transformation pathway. Electromagnetic Biology and Medicine 28, 105123.10.1080/15368370802711615CrossRefGoogle ScholarPubMed
Scholkmann, F, Fels, D and Cifra, M (2013) Non-chemical and non-contact cell-to-cell communication: a short review. American Journal of Translational Research 5, 586593.Google ScholarPubMed