Advertisement

Rendiconti Lincei. Scienze Fisiche e Naturali

, Volume 30, Issue 4, pp 775–784 | Cite as

Magnetic field gradient inhibits Saccharomyces cerevisiae growth

  • Milena Oliveira KalileEmail author
  • Raquel Guimarães Benevides
  • André Costa Cardoso
  • Mirco Ragni
Article
  • 67 Downloads

Abstract

The daily exposure of humans to artificial magnetic fields has inspired studies of their effects on biological systems. Different views are advocated by many research groups and few studies have clarified the role of magnetic field gradients in observed results. We investigated the effect of strong gradients and continuous magnetic fields in a cellular system. Colonies of Saccharomyces cerevisiae CCMB 355 were grown in solid and liquid media and exposed to the neodymium–iron–boron magnets. Notably, in solid medium, cells exposed to previously demagnetized NdFeB magnets or to the metals contained in magnets exhibited normal activities, but when exposed to the gradient, growth drastically fails near the magnet, even when the intensity of magnetism was near zero. Increasing the distance of the magnet to regions of weak magnetic field gradient caused decreased cellular malaise. When the magnet was removed, the cells were not capable of growing again, indicating that the gradient killed the exposed cells. In liquid medium, we observed a decrease in the absorbance values in the region of 560 nm when the substrate was directly permeated by a strong magnetic field gradient in comparison with a control without the magnet or with a magnet covered with a thin layer of silicone. This study helps to clarify the effect of the magnetic field gradient in biological systems.

Graphic abstract

Keywords

NdFeB magnets Magnetobiology Yeast Cell reduction Biocide 

Notes

Acknowledgements

We thank the Collection of Cultured Microorganisms of Bahia (CCMB-UEFS) for providing the Saccharomyces cerevisiae cells. We also wish to thank Drª Alice Ferreira da Silva for her assistance with the theoretical work and constructive comments. Maria Gorette Silva do Carmo, Cleidineia Souza de Santana and Pollyana Lopes Valle are acknowledged for their assistance with the practical work.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Compliance with ethical standards

Conflict of interest

The author(s) declare that they have no conflict of interest

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

12210_2019_848_MOESM1_ESM.pdf (529 kb)
Supplementary material 1 (PDF 528 kb)

References

  1. Abdel Fattah AR, Ghosh S, Puri IK (2016) High gradient magnetic field microstructures for magnetophoretic cell separation. J Chromatogr B 1027:194–199.  https://doi.org/10.1016/j.jchromb.2016.05.046 CrossRefGoogle Scholar
  2. Albuquerque WWC, Costa RMPB, Fernandes TDS, Porto ALF (2016) Evidences of the static magnetic field influence on cellular systems. Prog Biophys Mol Biol 121(1):16–28.  https://doi.org/10.1016/j.pbiomolbio.2016.03.003 CrossRefGoogle Scholar
  3. Bondemark L, Kurol J, Wennberg A (1994) Orthodontic rare earth magnets—in vitro assessment of cytotoxicity. BJO 21:335–341.  https://doi.org/10.1179/bjo.21.4.335 CrossRefGoogle Scholar
  4. Buemi M, Marino D, Di Pasquale G, Floccari F, Senatore M, Aloisi C, Grasso F, Mondio G, Perillo P, Frisina N, Corical F (2001) Cell proliferation/cell death balance in renal cell cultures after exposure to a static magnetic field. Nephron 87:269–273.  https://doi.org/10.1159/000045925 CrossRefGoogle Scholar
  5. Cazzanelli G, Pereira F, Alves S, Francisco R, Azevedo L, Dias Carvalho P, Almeida A, Côrte-Real M, Oliveira MJ, Lucas C, Sousa MJ, Preto A (2018) The yeast Saccharomyces cerevisiae as a model for understanding RAS proteins and their role in human tumorigenesis. Cells 7:14.  https://doi.org/10.3390/cells7020014 CrossRefGoogle Scholar
  6. Daoud J, Asami K, Rosenberg L, Tabrizian M (2012) Dielectric spectroscopy for non-invasive monitoring of epithelial cell differentiation within three-dimensional scaffolds. Phys Med Biol 57:5097–5112.  https://doi.org/10.1088/0031-9155/57/16/5097 CrossRefGoogle Scholar
  7. Dini L, Abbro L (2005) Bioeffects of moderate-intensity static magnetic fields on cell cultures. Micron 36:195–217.  https://doi.org/10.1016/j.micron.2004.12.009 CrossRefGoogle Scholar
  8. Du X, Graedel TE (2011) Global rare earth in-use stocks in NdFeB permanent magnets. J Ind Ecol 15:836–843.  https://doi.org/10.1111/j.1530-9290.2011.00362.x CrossRefGoogle Scholar
  9. Dürr S, Volz T, Marte A, Rempe G (2004) Observation of molecules produced from a Bose-Einstein condensate. Phys Rev Lett 92:020406.  https://doi.org/10.1103/PhysRevLett.92.020406 CrossRefGoogle Scholar
  10. Egami S, Naruse Y, Watarai H (2010) Effect of static magnetic fields on the budding of yeast cells. Bioelectromagnetics 31:622–629.  https://doi.org/10.1002/bem.20599 CrossRefGoogle Scholar
  11. Fanelli C, Coppola S, Barone R, Colussi C, Gualandi G, Volpe P, Ghibelli L (1999) Magnetic, fields increase cell survival by inhibiting apoptosis via modulation of Ca2+ influx. FASEB J 13:95–102.  https://doi.org/10.1096/fasebj.13.1.95 CrossRefGoogle Scholar
  12. Galonja-Coghill TA, Kostadinovic LM, Bojat NC (2009) Magnetically altered ethanol fermentation capacity of Saccharomyces cerevisiae. Proc Nat Sci Matica Srpska Novi Sad 117:119–123.  https://doi.org/10.2298/ZMSPN0917119G CrossRefGoogle Scholar
  13. Hirose H, Nakahara T, Zhang QM, Yonei S, Miyakoshi J (2003) Static magnetic field with a strong magnetic field gradient (41.7 T/m) induces c-Jun expression in HL-60 cells. Vitro Cell Dev Biol Anim 39:348–352.  https://doi.org/10.1290/1543-706X(2003)039 CrossRefGoogle Scholar
  14. Iwasaka M, Ikehata M, Miyakoshi J, Ueno S (2004) Strong static magnetic field effects on yeast proliferation and distribution. Bioelectrochemistry 65:59–68.  https://doi.org/10.1016/j.bioelechem.2004.04.002 CrossRefGoogle Scholar
  15. Kimball GC (1938) The growth of yeast in a magnetic field. J Bacteriol 35:109. (PMC374431) Google Scholar
  16. Kohno M, Yamazaki M, Kimura I, Wada M (2000) Effect of static magnetic fields on bacteria: Streptococcus mutans, Staphylococcus aureus, and Escherichia coli. Pathophysiology. 1 7(2):143–148.  https://doi.org/10.1016/S0928-4680(00)00042-0 CrossRefGoogle Scholar
  17. Mancini GP, Noar JH, Evans RD (1999) The physical characteristics of neodymium iron boron magnets for tooth extrusion. Eur J Orthod 21:541–550.  https://doi.org/10.1093/ejo/21.5.541 CrossRefGoogle Scholar
  18. Miyakoshi J (2005) Effects of static magnetic fields at the cellular level. Prog Biophys Mol Biol 87:213–223.  https://doi.org/10.1016/j.pbiomolbio.2004.08.008 CrossRefGoogle Scholar
  19. Miyakoshi J (2006) The review of cellular effects of a static magnetic field. Sci Technol Adv Mater 7:305.  https://doi.org/10.1016/j.stam.2006.01.004 CrossRefGoogle Scholar
  20. Motta MA, Muniz JBF, Schuler A, Motta M (2004) Static magnetic fields enhancement of Saccharomyces cerevisiae ethanolic fermentation. Biotechnol Prog 20:393–396.  https://doi.org/10.1021/bp034263j CrossRefGoogle Scholar
  21. München DD, Veit HM (2017) Neodymium as the main feature of permanent magnets from hard disk drives (HDDs). Waste Manag 61:372–376.  https://doi.org/10.1016/j.wasman.2017.01.032 CrossRefGoogle Scholar
  22. Muniz JB, Marcelino M, da Motta M, Schuler A, da Motta MA (2007) Influence of static magnetic fields on S. cerevisiae biomass growth. Braz Arch Biol Technol 50:515–520.  https://doi.org/10.1590/S1516-89132007000300017 CrossRefGoogle Scholar
  23. Nakahara T, Yaguchi H, Yoshida M, Miyakoshi J (2002) Effects of exposure of CHO-K1 cells to a 10-T static magnetic field. Radiology 224:817–822.  https://doi.org/10.1148/radiol.2243011300 CrossRefGoogle Scholar
  24. Neurath PW (1968) High gradient magnetic field inhibits embryonic development of frogs. Nature 219:1358.  https://doi.org/10.1038/2191358a0 CrossRefGoogle Scholar
  25. Nielsen J (2019) Yeast systems biology: model organism and cell factory. Biotechnol J.  https://doi.org/10.1002/biot.201800421 CrossRefGoogle Scholar
  26. Okano H (2008) Effects of static magnetic fields in biology: role of free radicals. Front Biosci 13:610–625.  https://doi.org/10.2741/3141 CrossRefGoogle Scholar
  27. Pelloni S, Lazzeretti P, Monaco G, Zanasi R (2011) Magnetic-field induced electronic anapoles in small molecules. Rend Lincei Sci Fis Nat 22:105–112.  https://doi.org/10.1007/s12210-011-0117-5 CrossRefGoogle Scholar
  28. Phelan A, Tarraf NE, Taylor P, Hönscheid R, Drescher D, Baccetti T, Darendeliler MA (2012) Skeletal and dental outcomes of a new magnetic functional appliance, the Sydney Magnoglide, in Class II correction. Am J Orthod Dentofacial Orthop 141:759–772.  https://doi.org/10.1016/j.ajodo.2012.01.014 CrossRefGoogle Scholar
  29. Polyakova T, Zablotskii V, Dejneka A (2017) Cell membrane pore formation and change in ion channel activity in high-gradient magnetic fields. IEEE Magn Lett 8:1–5.  https://doi.org/10.1109/lmag.2017.2732361 CrossRefGoogle Scholar
  30. Prijic S, Scancar J, Cemazar M, Bregar VB, Znidarsic A, Sersa G (2010) Increased cellular uptake of biocompatible superparamagnetic iron oxide nanoparticles into malignant cells by an external magnetic field. J Membrane Biol 236:167–179.  https://doi.org/10.1007/s00232-010-9271-4 CrossRefGoogle Scholar
  31. Rogero SO, Saiki M, Dantas ESK, Oliveira MCL, Cruz AS, Ikeda TI, Costa I (2003) Corrosion performance and cytotoxicity of sintered Nd-Fe-B magnets. Mater Sci Forum 416:76–81.  https://doi.org/10.4028/www.scientific.net/MSF.416-418.76 CrossRefGoogle Scholar
  32. Rollat A, Guyonnet D, Planchon M, Tuduri J (2016) Prospective analysis of the flows of certain rare earths in Europe at the 2020 horizon. Waste Manag 49:427–436.  https://doi.org/10.1016/j.wasman.2016.01.011 CrossRefGoogle Scholar
  33. Rosen AD (2003) Mechanism of action of moderate-intensity static magnetic fields on biological systems. Cell Biochem Biophys 39:163–174.  https://doi.org/10.1385/CBB:39:2:163 CrossRefGoogle Scholar
  34. Ruiz-Gómez MJ, Prieto-Barcia MI, Ristori-Bogajo E, Martínez-Morillo M (2004) Static and 50 Hz magnetic fields of 0.35 and 2.45 mT have no effect on the growth of Saccharomyces cerevisiae. Bioelectrochemistry 64:151–155.  https://doi.org/10.1016/j.bioelechem.2004.04.003 CrossRefGoogle Scholar
  35. Ryf S, Wolber T, Duru F, Luechinger R (2008) Interference of neodymium magnets with cardiac pacemakers and implantable cardioverter-defibrillators: an in vitro study. Technol Health Care 16:13–18.  https://doi.org/10.5167/uzh-6215 CrossRefGoogle Scholar
  36. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
  37. Salvadó Z, Arroyo-Lopez FN, Guillamon JM, Salazar G, Querol A, Barrio E (2011) Temperature adaptation markedly determines evolution within the Saccharomyces genus. Appl Environ Microbiol 77:2292–2302.  https://doi.org/10.1128/AEM.01861-10 CrossRefGoogle Scholar
  38. Santos LO, Alegre RM, Garcia-Diego C, Cuellar J (2010) Effects of magnetic fields on biomass and glutathione production by the yeast Saccharomyces cerevisiae. Process Biochem 45:1362–1367.  https://doi.org/10.1016/j.procbio.2010.05.008 CrossRefGoogle Scholar
  39. Santos LOD, Gonzales TA, Úbeda BT, Alegre RM (2012) Glutathione production using magnetic fields generated by magnets. Braz Arch Biol Technol 55:921–926.  https://doi.org/10.1590/S1516-89132012000600016 CrossRefGoogle Scholar
  40. Tian X, Wang D, Zha M, Yang X, Ji X, Zhang L, Zhang X (2018) Magnetic field direction differentially impacts the growth of different cell types. Electromagn Biol Med 37:114–125.  https://doi.org/10.1080/15368378.2018.1458627 CrossRefGoogle Scholar
  41. Wang H, Zhang X (2017) Magnetic fields and reactive oxygen species. IJMS 18:2175.  https://doi.org/10.3390/ijms18102175 CrossRefGoogle Scholar
  42. Wang Z, Yang P, Xu H, Qian A, Hu L, Shang P (2009) Inhibitory effects of a gradient static magnetic field on normal angiogenesis. Bioelectromagnetics 30:446–453.  https://doi.org/10.1002/bem.20501 CrossRefGoogle Scholar
  43. Wang Z, Hao F, Ding C, Yang Z, Shang P (2014) Effects of static magnetic field on cell biomechanical property and membrane ultrastructure. Bioelectromagnetics 35:251–261.  https://doi.org/10.1002/bem.21847 CrossRefGoogle Scholar
  44. Wosik J, Chen W, Qin K, Ghobrial RM, Kubiak JZ, Kloc M (2018) Magnetic field changes macrophage phenotype. Biophys J 114:2001–2013.  https://doi.org/10.1016/j.bpj.2018.03.002 CrossRefGoogle Scholar
  45. Yuksel C, Ankarali S, Yuksel NA (2018) The use of neodymium magnets in healthcare and their effects on health. North Clin Istanb 5:268.  https://doi.org/10.14744/nci.2017.00483 CrossRefGoogle Scholar
  46. Zablotskii V, Dejneka A, Kubinová Š, Le-Roy D, Dumas-Bouchiat F, Givord D, Dempsey NM, Syková E (2013) Life on magnets: stem cell networking on micro-magnet arrays. PLoS One 8:e70416.  https://doi.org/10.1371/journal.pone.0070416 CrossRefGoogle Scholar
  47. Zablotskii V, Syrovets T, Schmidt ZW, Dejneka A, Simmet T (2014) Modulation of monocytic leukemia cell function and survival by high gradient magnetic fields and mathematical modeling studies. Biomaterials 35:3164–3171.  https://doi.org/10.1016/j.biomaterials.2013.12.098 CrossRefGoogle Scholar
  48. Zablotskii V, Lunov O, Kubinov S, Polyakova T, Sykova E, Dejneka A (2016a) Effects of high-gradient magnetic fields on living cell machinery. J Phys D Appl Phys 49:493003.  https://doi.org/10.1088/0022-3727/49/49/493003 CrossRefGoogle Scholar
  49. Zablotskii V, Polyakova T, Lunov O, Dejneka A (2016b) How a high-gradient magnetic field could affect cell life. Sci Rep 6:37407.  https://doi.org/10.1038/srep37407 CrossRefGoogle Scholar
  50. Zablotskii V, Polyakova T, Dejneka A (2018) Cells in the non-uniform magnetic world: how cells respond to high-gradient magnetic fields. BioEssays 40:1800017.  https://doi.org/10.1002/bies.201800017 CrossRefGoogle Scholar
  51. Zhang Y (1997) Investigation of oxidation resistance of magnetic power coated with silicone. J Magn Magn Mater 171:305–308.  https://doi.org/10.1016/S0304-8853(96)00692-0 CrossRefGoogle Scholar
  52. Zhang QM, Tokiwa M, Doi T, Nakahara T, Chang P, Nakamura N, Hori M, Miyakoshi J, Yonei S (2003) Strong static magnetic field and the induction of mutations through elevated production of reactive oxygen species in Escherichia coli soxR. Int J Radiat Biol 79:281–286.  https://doi.org/10.1080/0955300031000096289 CrossRefGoogle Scholar

Copyright information

© Accademia Nazionale dei Lincei 2019

Authors and Affiliations

  1. 1.Department of BiologyFeira de Santana State UniversityFeira De SantanaBrazil
  2. 2.Department of EntomologyFederal University of ViçosaViçosaBrazil
  3. 3.Department of EntomologyFederal University of ViçosaViçosaBrazil
  4. 4.Physics DepartmentFeira de Santana State UniversityFeira De SantanaBrazil

Personalised recommendations