Physical limits to magnetogenetics

Abstract

This is an analysis of how magnetic fields affect biological molecules and cells. It was prompted by a series of prominent reports regarding magnetism in biological systems. The first claims to have identified a protein complex that acts like a compass needle to guide magnetic orientation in animals (<xref ref-type="bibr" rid="bib38">Qin et al., 2016</xref>). Two other articles report magnetic control of membrane conductance by attaching ferritin to an ion channel protein and then tugging the ferritin or heating it with a magnetic field (<xref ref-type="bibr" rid="bib46">Stanley et al., 2015</xref>; <xref ref-type="bibr" rid="bib47">Wheeler et al., 2016</xref>). Here I argue that these claims conflict with basic laws of physics. The discrepancies are large: from 5 to 10 log units. If the reported phenomena do in fact occur, they must have causes entirely different from the ones proposed by the authors. The paramagnetic nature of protein complexes is found to seriously limit their utility for engineering magnetically sensitive cells.

Full text

Its licence does not allow us to show the full text. Read it at PubMed Central:

References 48

1. 1.

   Arosio P, Ingrassia R, Cavadini P. Ferritins: a family of molecules for iron storage, antioxidation and more. Biochimica Et Biophysica Acta. 2009;1790:589-599.

   Not in our library10.1016/j.bbagen.2008.09.004 (opens in a new tab)

2. 2.

   Babincová M, Leszczynska D, Sourivong P, Babinec P. Selective treatment of neoplastic cells using ferritin-mediated electromagnetic hyperthermia. Medical Hypotheses. 2000;54:177-179.

   Not in our library10.1054/mehy.1999.0011 (opens in a new tab)

3. 3.

   Bazylinski DA, Frankel RB. Magnetosome formation in prokaryotes. Nature Reviews Microbiology. 2004;2:217-230.

   Not in our library10.1038/nrmicro842 (opens in a new tab)

4. 4.

   Cao E, Cordero-Morales JF, Liu B, Qin F, Julius D. TRPV1 channels are intrinsically heat sensitive and negatively regulated by phosphoinositide lipids. Neuron. 2013;77:667-679.

   Not in our library10.1016/j.neuron.2012.12.016 (opens in a new tab)

5. 5.

   Chen G. Nonlocal and nonequilibrium heat conduction in the vicinity of nanoparticles. Journal of Heat Transfer. 1996;118:539-545.

   Not in our library10.1115/1.2822665 (opens in a new tab)

6. 6.

   Davila AF, Fleissner G, Winklhofer M, Petersen N. A new model for a magnetoreceptor in homing pigeons based on interacting clusters of superparamagnetic magnetite. Physics and Chemistry of the Earth, Parts A/B/C. 2003;28:647-652.

   Not in our library10.1016/s1474-7065(03)00118-9 (opens in a new tab)

7. 7.

   Demir S, Jeon I-R, Long JR, Harris TD. Radical ligand-containing single-molecule magnets. Coordination Chemistry Reviews. 2015;289-290:149-176.

   Not in our library10.1016/j.ccr.2014.10.012 (opens in a new tab)

8. 8.

   Dunlop DJ. Magnetite: behavior near the single-domain threshold. Science. 1972;176:41-43.

   Not in our library10.1126/science.176.4030.41 (opens in a new tab)

9. 9.

   Dutz S, Hergt R. Magnetic nanoparticle heating and heat transfer on a microscale: Basic principles, realities and physical limitations of hyperthermia for tumour therapy. International Journal of Hyperthermia. 2013;29:790-800.

   Not in our library10.3109/02656736.2013.822993 (opens in a new tab)

10. 10.

    Dutz S, Hergt R. Magnetic particle hyperthermia--a promising tumour therapy? Nanotechnology. 2014;25:e17210.

    Not in our library10.1088/0957-4484/25/45/452001 (opens in a new tab)

11. 11.

    Fantechi E, Innocenti C, Zanardelli M, Fittipaldi M, Falvo E, Carbo M, Shullani V, Di Cesare Mannelli L, Ghelardini C, Ferretti AM, Ponti A, Sangregorio C, Ceci P. A smart platform for hyperthermia application in cancer treatment: cobalt-doped ferrite nanoparticles mineralized in human ferritin cages. ACS Nano. 2014;8:4705-4719.

    Not in our library10.1021/nn500454n (opens in a new tab)

12. 12.

    Fantechi E, Innocenti C, Albino M, Lottini E, Sangregorio C. Influence of cobalt doping on the hyperthermic efficiency of magnetite nanoparticles. Journal of Magnetism and Magnetic Materials. 2015;380:365-371.

    Not in our library10.1016/j.jmmm.2014.10.082 (opens in a new tab)

13. 13.

    Feynman RP, Leighton RB, Sands ML. The Feynman Lectures on Physics, Vol. 2. 1963.

    Not in our library

14. 14.

    Fortin JP, Wilhelm C, Servais J, Ménager C, Bacri JC, Gazeau F. Size-sorted anionic iron oxide nanomagnets as colloidal mediators for magnetic hyperthermia. Journal of the American Chemical Society. 2007;129:2628-2635.

    Not in our library10.1021/ja067457e (opens in a new tab)

15. 15.

    Ge Z, Cahill DG, Braun PV. AuPd metal nanoparticles as probes of nanoscale thermal transport in aqueous solution. Journal of Physical Chemistry B. 2004;108:18870-18875.

    Not in our library10.1021/jp048375k (opens in a new tab)

16. 16.

    Gupta A, Kane RS, Borca-Tasciuc D-A. Local temperature measurement in the vicinity of electromagnetically heated magnetite and gold nanoparticles. Journal of Applied Physics. 2010;108:064901.

    Not in our library10.1063/1.3485601 (opens in a new tab)

17. 17.

    Hergt R, Hiergeist R, Zeisberger M, Glöckl G, Weitschies W, Ramirez LP, Hilger I, Kaiser WA. Enhancement of AC-losses of magnetic nanoparticles for heating applications. Journal of Magnetism and Magnetic Materials. 2004;280:358-368.

    Not in our library10.1016/j.jmmm.2004.03.034 (opens in a new tab)

18. 18.

    Hergt R, Dutz S, Müller R, Zeisberger M, Mueller R. Magnetic particle hyperthermia: nanoparticle magnetism and materials development for cancer therapy. Journal of Physics. 2006;18:S2919-S2934.

    Not in our library10.1088/0953-8984/18/38/s26 (opens in a new tab)

19. 19.

    Howard J, Hudspeth AJ. Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the bullfrog's saccular hair cell. Neuron. 1988;1:189-199.

    Not in our library10.1016/0896-6273(88)90139-0 (opens in a new tab)

20. 20.

    Huang H, Delikanli S, Zeng H, Ferkey DM, Pralle A. Remote control of ion channels and neurons through magnetic-field heating of nanoparticles. Nature Nanotechnology. 2010;5:602-606.

    Not in our library10.1038/nnano.2010.125 (opens in a new tab)

21. 21.

    Jackson JD. Chapter 5.16. Classical Electrodynamics. 1998.

    Not in our library

22. 22.

    Jandacka P, Burda H, Pistora J. Magnetically induced behaviour of ferritin corpuscles in avian ears: can cuticulosomes function as magnetosomes? Journal of the Royal Society Interface. 2015;12:20141087.

    Not in our library10.1098/rsif.2014.1087 (opens in a new tab)

23. 23.

    Johnsen S, Lohmann KJ. The physics and neurobiology of magnetoreception. Nature Reviews Neuroscience. 2005;6:703-712.

    Not in our library10.1038/nrn1745 (opens in a new tab)

24. 24.

    Keblinski P, Cahill DG, Bodapati A, Sullivan CR, Taton TA. Limits of localized heating by electromagnetically excited nanoparticles. Journal of Applied Physics. 2006;100:e17210.

    Not in our library10.1063/1.2335783 (opens in a new tab)

25. 25.

    Kirschvink JL, Walker MM, Diebel CE. Magnetite-based magnetoreception. Current Opinion in Neurobiology. 2001;11:462-467.

    Not in our library10.1016/s0959-4388(00)00235-x (opens in a new tab)

26. 26.

    Kirschvink JL, Winklhofer M, Walker MM. Biophysics of magnetic orientation: strengthening the interface between theory and experimental design. Journal of the Royal Society Interface. 2010;7:S179-191.

    Not in our library10.1098/rsif.2009.0491.focus (opens in a new tab)

27. 27.

    Leibiger IB, Berggren PO. Regulation of glucose homeostasis using radiogenetics and magnetogenetics in mice. Nature Medicine. 2015;21:14-16.

    Not in our library10.1038/nm.3782 (opens in a new tab)

28. 28.

    Lewis S. Techniques: Magnetic manipulation. Nature Reviews Neuroscience. 2016;17:262-263.

    Not in our library10.1038/nrn.2016.42 (opens in a new tab)

29. 29.

    Lohmann KJ. Protein complexes: A candidate magnetoreceptor. Nature Materials. 2016;15:136-138.

    Not in our library10.1038/nmat4550 (opens in a new tab)

30. 30.

    Maddox J, Randi J, Stewart WW. "High-dilution" experiments a delusion. Nature. 1988;334:287-291.

    Not in our library10.1038/334287a0 (opens in a new tab)

31. 31.

    Maier-Hauff K, Ulrich F, Nestler D, Niehoff H, Wust P, Thiesen B, Orawa H, Budach V, Jordan A. Efficacy and safety of intratumoral thermotherapy using magnetic iron-oxide nanoparticles combined with external beam radiotherapy on patients with recurrent glioblastoma multiforme. Journal of Neuro-Oncology. 2011;103:317-324.

    Not in our library10.1007/s11060-010-0389-0 (opens in a new tab)

32. 32.

    Michaelis L, Coryell CD, Granick S. Ferritin III. The magnetic properties of ferritin and some other colloidal ferric compounds. Journal of Biological Chemistry. 1943;148:463-480.

    Not in our library

33. 33.

    Owen CS, Lindsay JG. Ferritin as a label for high-gradient magnetic separation. Biophysical Journal. 1983;42:145-150.

    Not in our library10.1016/s0006-3495(83)84380-x (opens in a new tab)

34. 34.

    Pankhurst QA, Connolly J, Jones SK, Dobson J. Applications of magnetic nanoparticles in biomedicine. Journal of Physics D. 2003;36:R167-R181.

    Not in our library10.1088/0022-3727/36/13/201 (opens in a new tab)

35. 35.

    Papaefthymiou GC. The Mössbauer and magnetic properties of ferritin cores. Biochimica Et Biophysica Acta. 2010;1800:886-897.

    Not in our library10.1016/j.bbagen.2010.03.018 (opens in a new tab)

36. 36.

    Piñol R, Brites CD, Bustamante R, Martínez A, Silva NJ, Murillo JL, Cases R, Carrey J, Estepa C, Sosa C, Palacio F, Carlos LD, Millán A. Joining time-resolved thermometry and magnetic-induced heating in a single nanoparticle unveils intriguing thermal properties. ACS Nano. 2015;9:3134-3142.

    Not in our library10.1021/acsnano.5b00059 (opens in a new tab)

37. 37.

    Purushotham S, Ramanujan RV. Modeling the performance of magnetic nanoparticles in multimodal cancer therapy. Journal of Applied Physics. 2010;107:e17210.

    Not in our library10.1063/1.3432757 (opens in a new tab)

38. 38.

    Qin S, Yin H, Yang C, Dou Y, Liu Z, Zhang P, Yu H, Huang Y, Feng J, Hao J, Hao J, Deng L, Yan X, Dong X, Zhao Z, Jiang T, Wang HW, Luo SJ, Xie C. A magnetic protein biocompass. Nature Materials. 2016;15:217-226.

    Not in our library10.1038/nmat4484 (opens in a new tab)

39. 39.

    Rabin Y. Is intracellular hyperthermia superior to extracellular hyperthermia in the thermal sense? International Journal of Hyperthermia. 2002;18:194-202.

    Not in our library10.1080/02656730110116713 (opens in a new tab)

40. 40.

    Ranade SS, Qiu Z, Woo SH, Hur SS, Murthy SE, Cahalan SM, Xu J, Mathur J, Bandell M, Coste B, Li YS, Chien S, Patapoutian A. Piezo1, a mechanically activated ion channel, is required for vascular development in mice. PNAS. 2014;111:10347-10352.

    Not in our library10.1073/pnas.1409233111 (opens in a new tab)

Cited by papers we hold 3

• Magnetothermal genetic deep brain stimulation of motor behaviors in awake, freely moving mice · 2017
  No notice
• Next-generation probes, particles, and proteins for neural interfacing · 2017
  No notice
• Neuronal control of peripheral insulin sensitivity and glucose metabolism · 2017
  No notice

Questions about this paper

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.