Neuronal Spines Can be Affected by Static Magnetic Fields: The Impact on Microtubule Dynamic Nature

Document Type : Original Articles

Authors

IBB, Tehran University

Abstract

Recently, the hypothesis in which memory and information would be stored as magnetic forms in astrocytes is expanding and neuromagnetic interactions between neurons and neighboring astrocytes in neocortex have potential to be the basis of memory formation. It has been proposed that all sorts of information may be maintained in form of neuronal activity-associated magnetic fields (NAAMFs) and thereby alterations of magnetic fields in the brain may potentially affect the memory function. On the other hand, microtubules (MTs), the most essential elements of cytoskeleton, are crucial in regulation of spine development and morphology, brain cognitive behavior, consciousness and information storage. Because of MT dynamic nature, it can produce local magnetic field in neurons through vibration. According to size, number, structure and function of microtubule proteins, they are the most eligible components of neurons to be affected by endogenous and exogenous magnetic fields. In this study we tried to investigate the possible effects of exogenous static magnetic fields (SMFs) on memory through examining the structural and functional changes in MT dynamic activity and neural cell morphology. MT activity results revealed that MT polymerization process was not attained to steady state at the right time in the presence of SMF at 300 mT and the ascending slope at the steady state phase was found as abnornmal. In addition, MT structure was relatively changed. On the influence of SMF, PC12 neuron-liked cells’ spines decreased significantly and their morphology altered to pyramidal form.

Keywords


  1. Verkhratsky A. Physiology of neuronal-glial networking. Neurochem Int. 2010 Nov;57(4):332-43.
  2. Banaclocha MA. Architectural organisation of neuronal activity-associated magnetic fields: a hypothesis for memory. Med Hypotheses. 2004;63(3):481-4.
  3. Fellin T. Communication between neurons and astrocytes: relevance to the modulation of synaptic and network activity. J Neurochem. 2009 Feb;108(3):533-44.
  4. Wikswo JP, Barach JP, Freeman JA. Magnetic field of a nerve impulse: first measurements. Science. 1980 Apr 4;208(4439):53-5.
  5. Roth BJ, Wikswo JP, Jr. The magnetic field of a single axon. A comparison of theory and experiment. Biophys J. 1985 Jul;48(1):93-109.
  6. Banaclocha MA. Are neuronal activity-associated magnetic fields the physical base for memory? Med Hypotheses. 2002 Nov;59(5):555-9.
  7. Banaclocha MA. Neuromagnetic dialogue between neuronal minicolumns and astroglial network: a new approach for memory and cerebral computation. Brain Res Bull. 2007 Jun 15;73(1-3):21-7.
  8. Martinez Banaclocha MA. Magnetic storage of information in the human cerebral cortex: a hypothesis for memory. Int J Neurosci. 2005 Mar;115(3):329-37.
  9. Caudle RM. Memory in astrocytes: a hypothesis. Theor Biol Med Model. 2006;3:2.
  10. Kirschvink JL, Kobayashi-Kirschvink A, Woodford BJ. Magnetite biomineralization in the human brain. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7683-7.
  11. Dobson J. Nanoscale biogenic iron oxides and neurodegenerative disease. FEBS Lett. 2001 May 4;496(1):1-5.
  12. Kirschvink JL, Kobayashi-Kirschvink A, Diaz-Ricci JC, Kirschvink SJ. Magnetite in human tissues: a mechanism for the biological effects of weak ELF magnetic fields. Bioelectromagnetics. 1992;Suppl 1:101-13.
  13. Banaclocha MA, Bokkon I, Banaclocha HM. Long-term memory in brain magnetite. Med Hypotheses. 2010 Feb;74(2):254-7.
  14. Bokkon I, Salari V. Information storing by biomagnetites. J Biol Phys. 2010 Jan;36(1):109-20.
  15. Mershin A, Kolomenski AA, Schuessler HA, Nanopoulos DV. Tubulin dipole moment, dielectric constant and quantum behavior: computer simulations, experimental results and suggestions. Biosystems. 2004 Nov;77(1-3):73-85.
  16. Faber J, Portugal R, Rosa LP. Information processing in brain microtubules. Biosystems. 2006 Jan;83(1):1-9.
  17. Hameroff SR, Watt RC. Information processing in microtubules. J Theor Biol. 1982 Oct 21;98(4):549-61.
  18. Pokorny J, Hasek J, Jelinek F. Electromagnetic Field of Microtubules: Effects on Transfer of Mass Particles and Electrons. Journal of Biological Physics. 2005;31(3-4):501-14.
  19. Pokorny J. Excitation of vibrations in microtubules in living cells. Bioelectrochemistry. 2004 Jun;63(1-2):321-6.
  20. Downing KH, Nogales E. Tubulin structure: insights into microtubule properties and functions. Curr Opin Struct Biol. 1998 Dec;8(6):785-91.
  21. Luduena RF, Shooter EM, Wilson L. Structure of the tubulin dimer. J Biol Chem. 1977 Oct 25;252(20):7006-14.
  22. Nogales E. Structural insights into microtubule function. Annu Rev Biochem. 2000;69:277-302.
  23. Iqbal K, Grundke-Iqbal I, Zaidi T, Merz PA, Wen GY, Shaikh SS, et al. Defective brain microtubule assembly in Alzheimer's disease. Lancet. 1986 Aug 23;2(8504):421-6.
  24. Shevtsov PN, Shevtsova EF, Burbaeva G, Bachurin SO. Disturbed assembly of human cerebral microtubules in Alzheimer's disease. Bull Exp Biol Med. 2006 Feb;141(2):265-8.
  25. Cappelletti G, Surrey T, Maci R. The parkinsonism producing neurotoxin MPP+ affects microtubule dynamics by acting as a destabilising factor. FEBS Lett. 2005 Aug 29;579(21):4781-6.
  26. Stracke R, Bohm KJ, Wollweber L, Tuszynski JA, Unger E. Analysis of the migration behaviour of single microtubules in electric fields. Biochem Biophys Res Commun. 2002 Apr 26;293(1):602-9.
  27. J. A. Tuszynski, J. A. Brown, E. Crawford, Carpenter EJ. Molecular Dynamics Simulations of Tubulin Structure and Calculations of Electrostatic Properties of Microtubules. Mathematical and Computer Modelling. 2005;41(10):1055-70.
  28. Emura R, Ashida N, Higashi T, Takeuchi T. Orientation of bull sperms in static magnetic fields. Bioelectromagnetics. 2001 Jan;22(1):60-5.
  29. Minoura I, Muto E. Dielectric measurement of individual microtubules using the electroorientation method. Biophys J. 2006 May 15;90(10):3739-48.
  30. Havelka D, Cifra M. Calculation of the Electromagnetic Field Around a Microtubule. Acta Polytechnica. 2009;49:58-63.
  31. J. Pokorny , F. Jelinek, V. Trkal , I. Lamprecht, Holzel R. Vibrations in Microtubules Journal of Biological Physics. 1997;23(3):171-9.
  32. Hameroff S, Nip A, Porter M, Tuszynski J. Conduction pathways in microtubules, biological quantum computation, and consciousness. Biosystems. 2002 Jan;64(1-3):149-68.
  33. Cifra M, Pokorny J, Havelka D, Kucera O. Electric field generated by axial longitudinal vibration modes of microtubule. Biosystems. 2010 May;100(2):122-31.
  34. Vassilev PM, Dronzine RT, Vassileva MP, Georgiev GA. Parallel arrays of microtubules formed in electric and magnetic fields. Biosci Rep. 1982 Dec;2(12):1025-9.
  35. Brown JA, Tuszynski JA. A review of the ferroelectric model of microtubules. Ferroelectrics. 1999;220(1):141-55.
  36. Tuszyński JA, Hameroff S, Satarić MV, Trpisova B, Nip MLA. Ferroelectric behavior in microtubule dipole lattices: Implications for information processing, signaling and assembly/disassembly. Journal of Theoretical Biology. 1995;174(4):371-80.
  37. Afrasiabi A, Riazi GH, Dadras A, Tavili E, Ghalandari B, Naghshineh A, et al. Electromagnetic fields with 217 Hz and 0.2 mT as hazardous factors for tubulin structure and assembly (in vitro study). J Iran Chem Soc. 2014;11(5):1295-304.
  38. Williams RC, Jr., Lee JC. Preparation of tubulin from brain. Methods Enzymol. 1982;85 Pt B:376-85.
  39. Miller HP, Wilson L. Preparation of microtubule protein and purified tubulin from bovine brain by cycles of assembly and disassembly and phosphocellulose chromatography. Methods Cell Biol. 2010;95:3-15.
  40. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248-54.
  41. Gaskin F, Cantor CR, Shelanski ML. Turbidimetric studies of the in vitro assembly and disassembly of porcine neurotubules. J Mol Biol. 1974 Nov 15;89(4):737-55.
  42. Bhattacharyya B, Wolff J. The interaction of 1-anilino-8-naphthalene sulfonate with tubulin: a site independent of the colchicine-binding site. Arch Biochem Biophys. 1975 Mar;167(1):264-9.
  43. Steiner M. Flourescence studies of platelet tubulin. Biochemistry. 1980 Sep 16;19(19):4492-9.
  44. Greene LA, Tischler AS. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2424-8.
  45. Scudiero DA, Shoemaker RH, Paull KD, Monks A, Tierney S, Nofziger TH, et al. Evaluation of a soluble tetrazolium/formazan assay for cell growth and drug sensitivity in culture using human and other tumor cell lines. Cancer Res. 1988 Sep 1;48(17):4827-33.
  46. Repacholi MH, Greenebaum B. Interaction of static and extremely low frequency electric and magnetic fields with living systems: health effects and research needs. Bioelectromagnetics. 1999;20(3):133-60.
  47. Valberg PA, Kavet R, Rafferty CN. Can low-level 50/60 Hz electric and magnetic fields cause biological effects? Radiat Res. 1997 Jul;148(1):2-21.
  48. Dadras A, Riazi GH, Afrasiabi A, Naghshineh A, Ghalandari B, Mokhtari F. In vitro study on the alterations of brain tubulin structure and assembly affected by magnetite nanoparticles. J Biol Inorg Chem. 2013 Mar;18(3):357-69.
  49. Schoutens JE. Dipole–Dipole Interactions in Microtubules. Journal of Biological Physics. 2005;31(1):35-55.
  50. Repacholi MH. Low-level exposure to radiofrequency electromagnetic fields: health effects and research needs. Bioelectromagnetics. 1998;19(1):1-19.
  51. Baulin VA, Marques CM, Thalmann F. Collision induced spatial organization of microtubules. Biophys Chem. 2007 Jul;128(2-3):231-44.
  52. Mavromatos NE, Mershin A, Nanopoulos DV. QED-cavity model of microtubules implies dissipationless energy transfer and biological quantum teleportation. International Journal of Modern Physics B. 2002;16(24):3623-42.
  53. Cavelier G. Short note: are electron-transport and electron-transfer involved in intracellular signaling? Med Hypotheses. 1995 Apr;44(4):261-2.
  54. Hanssens I, Baert J, Van Cauwelaert F. Effect of guanine nucleotides on the hydrophobic interaction of tubulin. Biochemistry. 1990 May 29;29(21):5160-5.
  55. Santoro N, Lisi A, Pozzi D, Pasquali E, Serafino A, Grimaldi S. Effect of extremely low frequency (ELF) magnetic field exposure on morphological and biophysical properties of human lymphoid cell line (Raji). Biochim Biophys Acta. 1997 Jul 24;1357(3):281-90.