All Title Author
Keywords Abstract

Publish in OALib Journal
ISSN: 2333-9721
APC: Only $99


Relative Articles


Electromagnetic Fields and Calcium Signaling by the Voltage Dependent Anion Channel

DOI: 10.4236/ojvm.2021.111004, PP. 57-86

Keywords: Ca Signaling, VDAC, Benzodiazepine Receptor, Mechanistic Concept, Pulsed EMFs, Electromagnetic Hypersensitivity, TSPO, Erythrocytes, NADH-Oxidase, Apoptosis, Magnetosensor, Membrane Potential, Oxidative Stress, Brain Signaling, Autism

Full-Text   Cite this paper   Add to My Lib


Electromagnetic fields (EMFs) can interact with biological tissues exerting positive as well as negative effects on cell viability, but the underlying sensing and signaling mechanisms are largely unknown. So far in excitable cells EMF exposure was postulated to cause Ca2+ influx through voltage-dependent Ca channels (VDCC) leading to cell activation and an antioxidant response. Upon further activation oxidative stress causing DNA damage or cell death may follow. Here we report collected evidence from literature that voltage dependent anion channels (VDAC) located not only in the outer microsomal membrane but also in the cytoplasmic membrane convert to Ca2+ conducting channels of varying capacities upon subtle changes of the applied EMF even in non-excitable cells like erythrocytes. Thus, VDAC can be targeted by external EMF in both types of membranes to release Ca2+ into the cytosol. The role of frequency, pulse modulation or polarization remains to be investigated in suitable cellular models. VDACs are associated with several other proteins, among which the 18 kDa translocator (TSPO) is of specific interest since it was characterized as the central benzodiazepine receptor in neurons. Exhibiting structural similarities with magnetoreceptors we propose that TSPO could sense the magnetic component of the EMF and thus together with VDAC could trigger physiological as well as pathological cellular responses. Pulsed EMFs in the frequency range of the brain-wave communication network may explain psychic disturbances of electromagnetic hypersensitive persons. An important support is provided from human psychology that states deficits like insomnia, anxiety or depression can be treated with diazepines that indicates apparent connections between the TSPO/VDAC complex and organismic responses to EMF.


[1]  Levitt, B.B. and Lai, H. (2010) Biological Effects from Exposure to Electromagnetic Radiation Emitted by Cell Tower Base Stations and Other Antenna Arrays. Environmental Reviews, 18, 365-395.
[2]  Carpenter, D.O. (2013) Human Disease Resulting from Exposure to Electromagnetic Fields. Reviews on Environmental Health, 28, 159-172.
[3]  Blank, M. and Goodman, R. (2009) Electromagnetic Fields Stress Living Cells. Pathophysiology, 16, 71-78.
[4]  Hardell, L. and Sage, C. (2008) Biological Effects from Electromagnetic Field Exposure and Public Exposure Standards. Biomed. Pharmacotherapy, 62, 104-109.
[5]  Johansson, O. (2006) Electrohypersensitivity: State-of-the-Art of a Functional Impairment. Electromagnetic Biology and Medicine, 25, 245-258.
[6]  McCarty, D.E., Carrubba, S., Chesson, A.L., Frilot, C., Gonzalez-Toledo, E. and Marino, A.A. (2011) Electromagnetic Hypersensitivity: Evidence for a Novel Neurological Syndrome. International Journal of Neuroscience, 121, 670-676.
[7]  Warnke, U. and Hensinger, P. (2013) Steigende “Burnout”-Indiz durch technisch erzeugte magnetische und elektromagnetische Felder des Mabilund Mommunikationsfunks. Kompetenzinitiative zum Schutz von Mensch, Umwelt und Demokratie e.V.
[8]  La, V.S., Condorelli, R.A., Vicari, E., D’Agata, R. and Calogero, A.E. (2012) Effects of the Exposure to Mobile Phones on Male Reproduction: A Review of the Literature. Journal of Andrology, 33, 350-356.
[9]  West, J.G., Kapoor, N.S., Liao, S.-Y., Chen, J.W., Bailey, L. and Nagavney, R.A. (2013) Multifocal Breast Cancer in Young Women with Prolonged Contact between Their Breasts and Cellular Phones. Case Reports in Medicine, 2013, Article ID: 354682.
[10]  Falcioni, L., Bua, L., Tibaldi, E., Lauriola, M., De, A.L., Gnudi, F., Mandrioli, D., Manservigi, M., Manservisi, F., Manzoli, I., Menghetti, I., Montella, R., Panzacchi, S., Sgargi, D., Strollo, V., Vornoli, A. and Belpoggi, F. (2018) Report of Final Results Regarding Brain And heart Tumors in Sprague-Dawley Rats Exposed from Prenatal Life Until Natural Death to Mobile Phone Radiofrequency Field Representative of 1.8GHz GSM Base Station Environmental Emission. Environmental Research, 165, 496-503.
[11]  Sahin, D., Ozgur, E., Guler, G., Tomruk, A., Unlu, I., Sepici-Dincel, A. and Seyhan, N. (2016) The 2100 MHz Radiofrequency Radiation of a 3G-Mobile Phone and the DNA Oxidative Damage in Brain. Journal of Chemical Neuroanatomy, 75, 94-98.
[12]  Yakymenko, I. and Sidorik, E. (2010) Risks of Carcinogenesis from Electromagnetic Radiation of Mobile Telephony Devices. Experimental Oncology, 32, 54-60.
[13]  D’Silva, M.H., Swer, R.T., Anbalagan, J. and Rajesh, B. (2017) Effect of Radiofrequency Radiation Emitted from 2G and 3G Cell Phone on Developing Liver of Chick Embryo—A Comparative Study. Journal of Clinical and Diagnostic Research, 11, AC05-AC09.
[14]  Siddiqi, N.S., Mathusami, J.C., Saad, S.M., Shafac, A. and Zaki, M. (2015) Effects of Mobile Phone 1800 Hz Electromagnetic Fields on the Development of Chick Embryo—A Pilot Study. International Conference on Chemical, Environmental and Biological Sciences, Dubai, 18-19 March 2015, 198-202.
[15]  Hässig, M.R., Jud, F. and Spiess, B. (2012) Increased Occurrence of Nuclear Cataract in the Calf after Erection of a Mobile Phone Base Station. Schweizer Archiv für Tierheilkunde, 154, 82-86.
[16]  Dube, J., Rochette-Drouin, O., Levesque, P., Gauvin, R., Roberge, C.J., Auger, F.A., Goulet, D., Bourdages, M., Plante, M., Moulin, V.J. and Germain, L. (2012) Human Keratinocytes Respond to Direct Current Stimulation by Increasing Intracellular Calcium: Preferential Response of Poorly Differentiated Cells. Journal of Cellular Physiology, 227, 2660-2667.
[17]  Nuccitelli, R. (2003) A Role for Endogenous Electric Fields in Wound Healing. Current Topics in Developmental Biology, 58, 1-26.
[18]  Zhang, X., Liu, X., Pan, L. and Lee, I. (2010) Magnetic Fields at Extremely Low-Frequency (50 Hz, 0.8 mT) Can Induce the Uptake of Intracellular Calcium Levels in Osteoblasts. Biochemical and Biophysical Research Communications, 396, 662-666.
[19]  Zhou, J., Wang, J.Q., Ge, B.F., Ma, X.N., Ma, H.P., Xian, C.J. and Chen, K.M. (2014) Different Electromagnetic Field Waveforms Have Different Effects on Proliferation, Differentiation and Mineralization of Osteoblasts in Vitro. Bioelectromagnetics, 35, 30-38.
[20]  Kirson, E.D., Gurvich, Z., Schneiderman, R., Dekel, E., Itzhaki, A., Wasserman, Y., Schatzberger, R. and Palti, Y. (2004) Disruption of Cancer Cell Replication by Alternating Electric Fields. Cancer Research, 64, 3288-3295.
[21]  Blackman, C.F. (1992) Calcium Release from Neural Tissue: Experimental Results and Possible Mechanisms. In: Norden, B. and Ramel, C., Eds., Interaction Mechanisms of Low-Level Electromagnetic Fields in Living Systems, Oxford University Press, Oxford, 107-129.
[22]  Pette, D. and Vrbova, G. (1992) Adaptation of Mammalian Skeletal Muscle Fibers to Chronic Electrical Stimulation. In: Reviews of Physiology, Biochemistry and Pharmacology, Vol. 120, Springer, Berlin, Heidelberg, 115-202.
[23]  Klebl, B.M., Ayoub, A.T. and Pette, D. (1998) Protein Oxidation, Tyrosine Nitration, and Inactivation of Sarcoplasmic Reticulum Ca2+-ATPase in Low-Frequency Stimulated Rabbit Muscle. FEBS Letters, 422, 381-384.
[24]  Beckman, J.S. and Koppenol, W.H. (1996) Nitric Oxide, Superoxide, and Peroxynitrite: The Good, the Bad, and Ugly. American Journal of Physiology, 271, C1424-C1437.
[25]  Carroll, S., Nicotera, P. and Pette, D. (1999) Calcium Transients in Single Fibers of Low-Frequency Stimulated Fast-Twitch Muscle of Rat. American Journal of Physiology, 277, C1122-C1129.
[26]  Ermak, G. and Davies, K.J. (2002) Calcium and Oxidative Stress: From Cell Signaling to Cell Death. Molecular Immunology, 38, 713-721.
[27]  Pall, M.L. (2013) Electromagnetic Fields Act via Activation of Voltage-Gated Calcium Channels to Produce Beneficial or Adverse Effects. Journal of Cellular and Molecular Medicine, 17, 958-965.
[28]  Berridge, M.J., Bootman, M.D. and Lipp, P. (1998) Calcium—A Life and Death Signal. Nature, 395, 645-648.
[29]  Peng, T.I. and Jou, M.J. (2010) Oxidative Stress Caused by Mitochondrial Calcium Overload. Annals of the New York Academy of Sciences, 1201, 183-188.
[30]  Brookes, P.S., Yoon, Y., Robotham, J.L., Anders, M.W. and Sheu, S.S. (2004) Calcium, ATP, and ROS: A Mitochondrial Love-Hate Triangle. American Journal of Physiology: Cell Physiology, 287, C817-C833.
[31]  Pall, M.L. (2018) 5G: Great Risk for EU, U.S. and International Health! Compelling Evidence for Eight Distinct Types of Great Harm Caused by Eectromagnetic Field (EMF) Exposures and the Mechanism That Causes Them. 1-90.
[32]  Pilla, A.A. (2012) Electromagnetic Fields Instantaneously Modulate Nitric Oxide Signaling in Challenged Biological Systems. Biochemical and Biophysical Research Communications, 426, 330-333.
[33]  Lim, J.L., Wilhelmus, M.M., de Vries, H.E., Drukarch, B., Hoozemans, J.J. and van, H.J. (2014) Antioxidative Defense Mechanisms Controlled by Nrf2: State-of-the-Art and Clinical Perspectives in Neurodegenerative Diseases. Archives of Toxicology, 88, 1773-1786.
[34]  Friedman, J., Kraus, S., Hauptman, Y., Schiff, Y. and Seger, R. (2007) Mechanism of Short-Term ERK Activation by Electromagnetic Fields at Mobile Phone Frequencies. Biochemical Journal, 405, 559-568.
[35]  Yumoto, H., Hirao, K., Tominaga, T., Bando, N., Takahashi, K. and Matsuo, T. (2015) Electromagnetic Wave Irradiation Promotes Osteoblastic Cell Proliferation and Up-Regulates Growth Factors via Activation of the ERK1/2 and p38 MAPK Pathways. Cellular Physiology and Biochemistry, 35, 601-615.
[36]  Wyatt, C.N., Weir, E.K. and Peers, C. (1994) Diphenylene Iodonium Blocks K+ and Ca2+ Currents in Type I Cells Isolated from the Neonatal Rat Carotid Body. Neuroscience Letters, 172, 63-66.
[37]  Morré, D.J. and Brightman, A.O. (1991) NADH Oxidase of Plasma Membranes. Journal of Bioenergetics and Biomembranes, 23, 469-489.
[38]  Viappiani, S., Nicolescu, A.C., Holt, A., Sawicki, G., Crawford, B.D., Leon, H., van, M.T. and Schulz, R. (2009) Activation and Modulation of 72 kDa Matrix Metalloproteinase-2 by Peroxynitrite and Glutathione. Biochemical Pharmacology, 77, 826-834.
[39]  Bruno, M., Brightman, A.O., Lawrence, J., Werderitsh, D., Morré, D.M. and Morré, D.J. (1992) Stimulation of NADH Oxidase Activity from Rat Liver Plasma Membranes by Growth Factors and Hormones Is Decreased or Absent with Hepatoma Plasma Membranes. Biochemical Journal, 284, 625-628.
[40]  Pou, S., Keaton, L., Surichamorn, W. and Rosen, G.M. (1999) Mechanism of Superoxide Generation by Neuronal Nitric-Oxide Synthase. Journal of Biological Chemistry, 274, 9573-9580.
[41]  Sharpe, M.A. and Cooper, C.E. (1998) Reactions of Nitric Oxide with Mitochondrial Cytochrome C: A Novel Mechanism for the Formation of Nitroxyl Anion and Peroxynitrite. Biochemical Journal, 332, 9-19.
[42]  Ullrich, V. and Kissner, R. (2006) Redox Signaling: Bioinorganic Chemistry at Its Best. Journal of Inorganic Biochemistry, 100, 2079-2086.
[43]  Ullrich, V. and Schildknecht, S. (2014) Sensing Hypoxia by Mitochondria: A Unifying Hypothesis Involving S-Nitrosation. Antioxidants & Redox Signaling, 20, 325-338.
[44]  Cheng, Q., Sedlic, F., Pravdic, D., Bosnjak, Z.J. and Kwok, W.M. (2011) Biphasic Effect of Nitric Oxide on the Cardiac Voltage-Dependent Anion Channel. FEBS Letters, 585, 328-334.
[45]  De Pinto, V., Messina, A., Lane, D.J. and Lawen, A. (2010) Voltage-Dependent Anion-Selective Channel (VDAC) in the Plasma Membrane. FEBS Letters, 584, 1793-1799.
[46]  Lawen, A., Ly, J.D., Lane, D.J., Zarschler, K., Messina, A. and De Pinto, V. (2005) Voltage-Dependent Anion-Selective Channel 1 (VDAC1)—A Mitochondrial Protein, Rediscovered as a Novel Enzyme in the Plasma Membrane. The International Journal of Biochemistry & Cell Biology, 37, 277-282.
[47]  Low, H., Crane, F.L. and Morré, D.J. (2012) Putting Together a Plasma Membrane NADH Oxidase: A Tale of Three Laboratories. The International Journal of Biochemistry & Cell Biology, 44, 1834-1838.
[48]  Ly, J.D. and Lawen, A. (2003) Transplasma Membrane Electron Transport: Enzymes Involved and Biological Function. Redox Report, 8, 3-21.
[49]  Tang, X., Chueh, P.J., Jiang, Z., Layman, S., Martin, B., Kim, C., Morré, D.M. and Morré, D.J. (2010) Essential Role of Copper in the Activity and Regular Periodicity of a Recombinant, Tumor-Associated, Cell Surface, Growth-Related and Time-Keeping Hydroquinone (NADH) Oxidase with Protein Disulfide-Thiol Interchange Activity (ENOX2). Journal of Bioenergetics and Biomembranes, 42, 355-360.
[50]  Shoshan-Barmatz, V. and Ginzel, D. (2003) The Voltage-Dependent Anion Channel. Cell Biochemistry and Biophysics, 39, 279-292.
[51]  Yu, W.H., Wolfgang, W. and Forte, M. (1995) Subcellular Localization of Human Voltage-Dependent Anion Channel Isoforms. Journal of Biological Chemistry, 270, 13998-14006.
[52]  Baker, M.A., Lane, D.J., Ly, J.D., De Pinto, V. and Lawen, A. (2004) VDAC1 Is a Transplasma Membrane NADH-Ferricyanide Reductase. Journal of Biological Chemistry, 279, 4811-4819.
[53]  Buettner, R., Papoutsoglou, G., Scemes, E., Spray, D.C. and Dermietzel, R. (2000) Evidence for Secretory Pathway Localization of a Voltage-Dependent Anion Channel Isoform. Proceedings of the National Academy of Sciences of the United States of America, 97, 3201-3206.
[54]  Báthori, G., Parolini, I., Tombola, F., Szabó, I., Messina, A., Oliva, M., De Pinto, V., Lisanti, M., Sargiacomo, M. and Zoratti, M. (1999) Porin Is Present in the Plasma Membrane Where It Is Concentrated in Caveolae and Caveolae-Related Domains. Journal of Biological Chemistry, 274, 29607-29612.
[55]  Bahamonde, M.I. and Valverde, M.A. (2003) Voltage-Dependent Anion Channel Localises to the Plasma Membrane and Peripheral but Not Perinuclear Mitochondria. Pflügers Archiv, 446, 309-313.
[56]  Crane, F.L. and Low, H. (2012) The Oxidative Function of Diferric Transferrin. Biochemistry Research International, 2012, Article ID: 592806.
[57]  Merker, M.P., Olson, L.E., Bongard, R.D., Patel, M.K., Linehan, J.H. and Dawson, C.A. (1998) Ascorbate-Mediated Transplasma Membrane Electron Transport in Pulmonary Arterial Endothelial Cells. American Journal of Physiology, 274, L685-L693.
[58]  Messina, A., Reina, S., Guarino, F. and De Pinto, V. (2012) VDAC Isoforms in Mammals. Biochimica et Biophysica Acta, 1818, 1466-1476.
[59]  Aram, L., Geula, S., Arbel, N. and Shoshan-Barmatz, V. (2010) VDAC1 Cysteine Residues: Topology and Function in Channel Activity and Apoptosis. Biochemical Journal, 427, 445-454.
[60]  Crane, F.L., Low, H., Navas, P. and Sun, I.L. (2013) Control of Cell Growth by Plasma Membrane NADH Oxidation. Pure and Applied Chemical Sciences, 1, 31-42.
[61]  Cheng, H.L., Lee, Y.H., Yuan, T.M., Chen, S.W. and Chueh, P.J. (2016) Update on a Tumor-Associated NADH Oxidase in Gastric Cancer Cell Growth. World Journal of Gastroenterology, 22, 2900-2905.
[62]  Hiller, S., Abramson, J., Mannella, C., Wagner, G. and Zeth, K. (2010) The 3D Structures of VDAC Represent a Native Conformation. Trends in Biochemical Sciences, 35, 514-521.
[63]  Briones, R., Weichbrodt, C., Paltrinieri, L., Mey, I., Villinger, S., Giller, K., Lange, A., Zweckstetter, M., Griesinger, C., Becker, S., Steinem, C. and de Groot, B.L. (2016) Voltage Dependence of Conformational Dynamics and Subconducting States of VDAC-1. Biophysical Journal, 111, 1223-1234.
[64]  Pastorino, J.G. and Hoek, J.B. (2008) Regulation of Hexokinase Binding to VDAC. Journal of Bioenergetics and Biomembranes, 40, 171-182.
[65]  Sun, J. and Liao, J.K. (2002) Functional Interaction of Endothelial Nitric Oxide Synthase with a Voltage-Dependent Anion Channel. Proceedings of the National Academy of Sciences of the United States of America, 99, 13108-13113.
[66]  Tan, W. and Colombini, M. (2007) VDAC Closure Increases Calcium Ion Flux. Biochimica et Biophysica Acta, 1768, 2510-2515.
[67]  Villinger, S., Briones, R., Giller, K., Zachariae, U., Lange, A., de Groot, B.L., Griesinger, C., Becker, S. and Zweckstetter, M. (2010) Functional Dynamics in the Voltage-Dependent Anion Channel. Proceedings of the National Academy of Sciences of the United States of America, 107, 22546-22551.
[68]  Pavlov, E., Grigoriev, S.M., Dejean, L.M., Zweihorn, C.L., Mannella, C.A. and Kinnally, K.W. (2005) The Mitochondrial Channel VDAC Has a Cation-Selective Open State. Biochimica et Biophysica Acta, 1710, 96-102.
[69]  Noskov, S.Y., Rostovtseva, T.K., Chamberlin, A.C., Teijido, O., Jiang, W. and Bezrukov, S.M. (2016) Current State of Theoretical and Experimental Studies of the Voltage-Dependent Anion Channel (VDAC). Biochimica et Biophysica Acta, 1858, 1778-1790.
[70]  Colombini, M. (2016) The VDAC Channel: Molecular Basis for Selectivity. Biochimica et Biophysica Acta, 1863, 2498-2502.
[71]  Bahamonde, M.I., Fernandez-Fernandez, J.M., Guix, F.X., Vazquez, E. and Valverde, M.A. (2003) Plasma Membrane Voltage-Dependent Anion Channel Mediates Antiestrogen-Activated Maxi Cl- Currents in C1300 Neuroblastoma Cells. Journal of Biological Chemistry, 278, 33284-33289.
[72]  Elinder, F., Akanda, N., Tofighi, R., Shimizu, S., Tsujimoto, Y., Orrenius, S. and Ceccatelli, S. (2005) Opening of Plasma Membrane Voltage-Dependent Anion Channels (VDAC) Precedes Caspase Activation in Neuronal Apoptosis Induced by Toxic Stimuli. Cell Death and Differentiation, 12, 1134-1140.
[73]  Kozuch, J., Weichbrodt, C., Millo, D., Giller, K., Becker, S., Hildebrandt, P. and Steinem, C. (2014) Voltage-Dependent Structural Changes of the Membrane-Bound Anion Channel hVDAC1 Probed by SEIRA and Electrochemical Impedance Spectroscopy. Physical Chemistry Chemical Physics, 16, 9546-9555.
[74]  Song, J., Midson, C., Blachly-Dyson, E., Forte, M. and Colombini, M. (1998) The Sensor Regions of VDAC Are Translocated from within the Membrane to the Surface during the Gating Processes. Biophysical Journal, 74, 2926-2944.
[75]  Báthori, G., Szabó, I., Schmehl, I., Tombola, F., Messina, A., De Pinto, V. and Zoratti, M. (1998) Novel Aspects of the Electrophysiology of Mitochondrial Porin. Biochemical and Biophysical Research Communications, 243, 258-263.
[76]  Benz, R. (1994) Permeation of Hydrophilic Solutes through Mitochondrial Outer Membranes: Review on Mitochondrial Porins. Biochimica et Biophysica Acta, 1197, 167-196.
[77]  Tsujimoto, Y. and Shimizu, S. (2002) The Voltage-Dependent Anion Channel: An Essential Player in Apoptosis. Biochimie, 84, 187-193.
[78]  Ben-Hail, D. and Shoshan-Barmatz, V. (2016) VDAC1-Interacting Anion Transport Inhibitors Inhibit VDAC1 Oligomerization and Apoptosis. Biochimica et Biophysica Acta, 1863, 1612-1623.
[79]  Rostovtseva, T.K. and Bezrukov, S.M. (2008) VDAC Regulation: Role of Cytosolic Proteins and Mitochondrial Lipids. Journal of Bioenergetics and Biomembranes, 40, 163-170.
[80]  Xu, Z., Zhang, D., He, X., Huang, Y. and Shao, H. (2016) Transport of Calcium Ions into Mitochondria. Current Genomics, 17, 215-219.
[81]  Montero, M., Alonso, M.T., Carnicero, E., Cuchillo-Ibanez, I., Albillos, A., Garcia, A.G., Garcia-Sancho, J. and Alvarez, J. (2000) Chromaffin-Cell Stimulation Triggers fast Millimolar Mitochondrial Ca2+ Transients That Modulate Secretion. Nature Cell Biology, 2, 57-61.
[82]  Gincel, D., Silberberg, S.D. and Shoshan-Barmatz, V. (2000) Modulation of the Voltage-Dependent Anion Channel (VDAC) by Glutamate. Journal of Bioenergetics and Biomembranes, 32, 571-583.
[83]  Gincel, D., Vardi, N. and Shoshan-Barmatz, V. (2002) Retinal Voltage-Dependent Anion Channel: Characterization and Cellular Localization. Investigative Ophthalmology & Visual Science, 43, 2097-2104.
[84]  Thinnes, F.P. (2013) New Findings Concerning Vertebrate Porin II—On the Relevance of Glycine Motifs of Type-1 VDAC. Molecular Genetics and Metabolism, 108, 212-224.
[85]  Denora, N. and Natile, G. (2017) An Updated View of Translocator Protein (TSPO). International Journal of Molecular Sciences, 18, 2640.
[86]  Rupprecht, R., Papadopoulos, V., Rammes, G., Baghai, T. C., Fan, J., Akula, N., Groyer, G., Adams, D. and Schumacher, M. (2010) Translocator Protein (18 kDa) (TSPO) as a Therapeutic Target for Neurological and Psychiatric Disorders. Nature Reviews Drug Discovery, 9, 971-988.
[87]  Barichello, T., Simoes, L.R., Collodel, A., Giridharan, V.V., Dal-Pizzol, F., Macedo, D. and Quevedo, J. (2017) The Translocator Protein (18 kDa) and Its Role in Neuropsychiatric Disorders. Neuroscience & Biobehavioral Reviews, 83, 183-199.
[88]  Braestrup, C. and Squires, R.F. (1977) Specific Benzodiazepine Receptors in Rat Brain Characterized by High-Affinity (3H)Diazepam Binding. Proceedings of the National Academy of Sciences of the United States of America, 74, 3805-3809.
[89]  Wang, H., Zhai, K., Xue, Y., Yang, J., Yang, Q., Fu, Y., Hu, Y., Liu, F., Wang, W., Cui, L., Chen, H., Zhang, J. and He, W. (2016) Global Deletion of TSPO Does Not Affect the Viability and Gene Expression Profile. PLoS ONE, 11, e0167307.
[90]  Liu, G.J., Middleton, R.J., Hatty, C.R., Kam, W.W., Chan, R., Pham, T., Harrison-Brown, M., Dodson, E., Veale, K. and Banati, R.B. (2014) The 18 kDa Translocator Protein, Microglia and Neuroin-flammation. Brain Pathology, 24, 631-653.
[91]  Czajkowski, C., Gibbs, T.T. and Farb, D.H. (1989) Transmembrane Topology of the Gamma-Aminobutyric AcidA/Benzodiazepine Receptor: Subcellular Distribution and Allosteric Coupling Determined in Situ. Molecular Pharmacology, 35, 75-84.
[92]  Liedvogel, M. and Mouritsen, H. (2010) Cryptochromes—A Potential Magnetoreceptor: What Do We Know and What Do We Want to Know? Journal of the Royal Society Interface, 7, S147-S162.
[93]  Byrdin, M., Eker, A.P., Vos, M.H. and Brettel, K. (2003) Dissection of the Triple Tryptophan Electron Transfer Chain in Escherichia coli DNA Photolyase: Trp382 Is the Primary Donor in Photoactivation. Proceedings of the National Academy of Sciences of the United States of America, 100, 8676-8681.
[94]  Henbest, K.B., Maeda, K., Hore, P.J., Joshi, M., Bacher, A., Bittl, R., Weber, S., Timmel, C.R. and Schleicher, E. (2008) Magnetic-Field Effect on the Photoactivation Reaction of Escherichia coli DNA Photolyase. Proceedings of the National Academy of Sciences of the United States of America, 105, 14395-14399.
[95]  Maeda, K., Robinson, A.J., Henbest, K.B., Hogben, H.J., Biskup, T., Ahmad, M., Schleicher, E., Weber, S., Timmel, C.R. and Hore, P.J. (2012) Magnetically Sensitive Light-Induced Reactions in Cryptochrome Are Consistent with Its Proposed Role as a Magnetoreceptor. Proceedings of the National Academy of Sciences of the United States of America, 109, 4774-4779.
[96]  Cashmore, A.R., Jarillo, J.A., Wu, Y.J. and Liu, D. (1999) Cryptochromes: Blue Light Receptors for Plants and Animals. Science, 284, 760-765.
[97]  Kattnig, D.R. (2017) Radical-Pair-Based Magnetoreception Amplified by Radical Scavenging: Resilience to Spin Relaxation. The Journal of Physical Chemistry B, 121, 10215-10227.
[98]  Rodgers, C.T. and Hore, P.J. (2009) Chemical Magnetoreception in Birds: The Radical Pair Mechanism. Proceedings of the National Academy of Sciences of the United States of America, 106, 353-360.
[99]  Bialas, C., Jarocha, L.E., Henbest, K.B., Zollitsch, T.M., Kodali, G., Timmel, C.R., Mackenzie, S.R., Dutton, P.L., Moser, C.C. and Hore, P.J. (2016) Engineering an Artificial Flavoprotein Magnetosensor. Journal of the American Chemical Society, 138, 16584-16587.
[100]  Grebing, C., Crane, F.L., Low, H. and Hall, K. (1984) A Trans-membranous NADH-Dehydrogenase in Human Erythrocyte Membranes. Journal of Bioenergetics and Biomembranes, 16, 517-533.
[101]  Kennett, E.C. and Kuchel, P.W. (2003) Redox Reactions and Electron Transfer across the Red Cell Membrane. IUBMB Life, 55, 375-385.
[102]  Matteucci, E. and Giampietro, O. (2007) Electron Pathways through Erythrocyte Plasma Membrane in Human Physiology and Pathology: Potential Redox Biomarker? Biomarker Insights, 2, 321-329.
[103]  Sridharan, M., Bowles, E.A., Richards, J.P., Krantic, M., Davis, K.L., Dietrich, K.A., Stephenson, A.H., Ellsworth, M.L. and Sprague, R.S. (2012) Prostacyclin Receptor-Mediated ATP Release from Erythrocytes Requires the Voltage-Dependent Anion Channel. American Journal of Physiology-Heart and Circulatory Physiology, 302, H553-H559.
[104]  Kaestner, L., Wang, X., Hertz, L. and Bernhardt, I. (2018) Voltage-Activated Ion Channels in Non-Excitable Cells—A Viewpoint Regarding Their Physiological Justification. Frontiers in Physiology, 9, 450.
[105]  Kaestner, L., Christophersen, P., Bernhardt, I. and Bennekou, P. (2000) The Non-Selective Voltage-Activated Cation Channel in the Human Red Blood Cell Membrane: Reconciliation between Two Conflicting Reports and Further Characterisation. Bioelectrochemistry, 52, 117-125.
[106]  Marginedas-Freixa, I., Alvarez, C.L., Moras, M., Leal Denis, M.F., Hattab, C., Halle, F., Bihel, F., Mouro-Chanteloup, I., Lefevre, S.D., Le Van, K.C., Schwarzbaum, P.J. and Ostuni, M.A. (2018) Human Erythrocytes Release ATP by a Novel Pathway Involving VDAC Oligomerization Independent of Pannexin-1. Scientific Reports, 8, Article No. 11384.
[107]  Baskurt, O., Neu, B. and Meiselman, H.J. (2019) Red Blood Cell Aggregation. CRC Press, Boca Raton, FL.
[108]  Wagner, C., Steffen, P. and Svetina, S. (2013) Aggregation of Red Blood Cells: From Rouleaux to Clot Formation. Comptes Rendus Physique, 14, 459-469.
[109]  Danielczok, J.G., Terriac, E., Hertz, L., Petkova-Kirova, P., Lautenschlager, F., Laschke, M.W. and Kaestner, L. (2017) Red Blood Cell Passage of Small Capillaries Is Associated with Transient Ca2+-Mediated Adaptations. Frontiers in Physiology, 8, 979.
[110]  Sebastián, J.L., San Martín, S.M., Sancho, M., Miranda, J.M. and álvarez, G. (2005) Erythrocyte Rouleau Formation under Polarized Electromagnetic Fields. Physical Review E, 72, Article ID: 031913.
[111]  Kaestner, L., Bogdanova, A. and Egee, S. (2020) Calcium Channels and Calcium-Regulated Channels in Human Red Blood Cells. In: Islam, M., Eds., Advances in Experimental Medicine and Biology, Vol. 1131, Springer, Cham, 625-648.
[112]  Lang, K.S., Duranton, C., Poehlmann, H., Myssina, S., Bauer, C., Lang, F., Wieder, T. and Huber, S.M. (2003) Cation Channels Trigger Apoptotic Death of Erythrocytes. Cell Death and Differentiation, 10, 249-256.
[113]  Cortese-Krott, M.M. and Kelm, M. (2014) Endothelial Nitric Oxide Synthase in Red Blood Cells: Key to a New Erythrocrine Function? Redox Biology, 2, 251-258.
[114]  Raccuglia, D., Huang, S., Ender, A., Heim, M.M., Laber, D., Suarez-Grimalt, R., Liotta, A., Sigrist, S.J., Geiger, J.R.P. and Owald, D. (2019) Network-Specific Synchronization of Electrical Slow-Wave Oscillations Regulates Sleep Drive in Drosophila. Current Biology, 29, 3611-3621.
[115]  Igarashi, J., Isomura, Y., Arai, K., Harukuni, R. and Fukai, T. (2013) A θ-γ Oscillation Code for Neuronal Coordination during Motor Behavior. Journal of Neuroscience, 33, 18515-18530.
[116]  Weintraub, K. (2011) The Prevalence Puzzle: Autism Counts. Nature, 479, 22-24.
[117]  Mariea, T.J. and Carlo, G. L. (2007) Wireless Radiation in the Etiology and Treatment of Autism: Clinical Observations and Mechanisms. Journal of the Australasian College of Nutritional & Environmental Medicine, 26, 3-7.
[118]  Gonzalez-Gronow, M., Cuchacovich, M., Francos, R., Cuchacovich, S., Fernandez, M.P., Blanco, A., Bowers, E.V., Kaczowka, S. and Pizzo, S.V. (2010) Antibodies against the Voltage-Dependent Anion Channel (VDAC) and Its Protective Ligand Hexokinase-I in Children with Autism. Journal of Neuroimmunology, 227, 153-161.
[119]  Kern, J.K. (2002) The Possible Role of the Cerebellum in Autism/PDD: Disruption of a Multisensory Feedback Loop. Medical Hypotheses, 59, 255-260.
[120]  Langen, M., Durston, S., Staal, W.G., Palmen, S.J. and van, E.H. (2007) Caudate Nucleus Is Enlarged in High-Functioning Medication-Naive Subjects with Autism. Biological Psychiatry, 62, 262-266.
[121]  Sogut, S., Zoroglu, S.S., Ozyurt, H., Yilmaz, H.R., Ozugurlu, F., Sivasli, E., Yetkin, O., Yanik, M., Tutkun, H., Savas, H.A., Tarakcioglu, M. and Akyol, O. (2003) Changes in Nitric Oxide Levels and Antioxidant Enzyme Activities May Have a Role in the Pathophysiological Mechanisms Involved in Autism. Clinica Chimica Acta, 331, 111-117.
[122]  Crane, F.L., Low, H., Sun, I., Navas, P. and Gvozdjakova, A. (2014) Plasma Membrane Coenzyme Q: Evidence for a Role in Autism. Biologics, 8, 199-205.
[123]  Mutter, J., Naumann, J., Schneider, R., Walach, H. and Haley, B. (2005) Mercury and Autism: Accelerating Evidence? Neuro Enocrinology Letters, 26, 439-446.
[124]  Hashimoto, T., Tayama, M., Murakawa, K., Yoshimoto, T., Miyazaki, M., Harada, M. and Kuroda, Y. (1995) Development of the Brainstem and Cerebellum in Autistic Patients. Journal of Autism and Developmental Disorders, 25, 1-18.
[125]  Kubova, H., Bendova, Z., Moravcova, S., Pacesova, D., Rocha, L.L. and Mares, P. (2018) Neonatal Clonazepam Administration Induces Long-Lasting Changes in Glutamate Receptors. Frontiers in Molecular Neuroscience, 11, 382.


comments powered by Disqus

Contact Us


WhatsApp +8615387084133

WeChat 1538708413