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European Biophysics Journal

, Volume 44, Issue 8, pp 647–654 | Cite as

Magnetic nanoparticles for “smart liposomes”

  • Yoshitaka Nakayama
  • Mislav Mustapić
  • Haleh Ebrahimian
  • Pawel Wagner
  • Jung Ho Kim
  • Md Shahriar Al Hossain
  • Joseph Horvat
  • Boris MartinacEmail author
Original Paper

Abstract

Liposomal drug delivery systems (LDDSs) are promising tools used for the treatment of diseases where highly toxic pharmacological agents are administered. Currently, destabilising LDDSs by a specific stimulus at a target site remains a major challenge. The bacterial mechanosensitive channel of large conductance (MscL) presents an excellent candidate biomolecule that could be employed as a remotely controlled pore-forming nanovalve for triggered drug release from LDDSs. In this study, we developed superparamagnetic nanoparticles for activation of the MscL nanovalves by magnetic field. Synthesised CoFe2O4 nanoparticles with the radius less than 10 nm were labelled by SH groups for attachment to MscL. Activation of MscL by magnetic field with the nanoparticles attached was examined by the patch clamp technique showing that the number of activated channels under ramp pressure increased upon application of the magnetic field. In addition, we have not observed any cytotoxicity of the nanoparticles in human cultured cells. Our study suggests the possibility of using magnetic nanoparticles as a specific trigger for activation of MscL nanovalves for drug release in LDDSs.

Keywords

Magnetic nanoparticles CoFe2O4 Mechanosensitive channels MscL Liposomes Drug delivery system Patch clamp 

Notes

Acknowledgments

We thank Paul Rhode for the purification of M42C MscL, Gilberto Casillas for transmission electron microscopy, and Prof. Yoon-Bo Shim for the cytotoxicity test. We also thank Dr. Edward J. Beck for critical reading of the manuscript and useful suggestions for its improvement. This work was supported by the ‘AIIM (Australian Institute for Innovative Materials) for Gold/2014’ grant in collaboration with Victor Chang Cardiac Research Institute, the Japanese Society for Promotion of Science (JSPS), for a fellowship to YN and the National Health and Medical Research Council of Australia for a Principal Research Fellowship to BM. This research used equipment funded by the Australian Research Council (ARC)—Linkage, Infrastructure, Equipment and Facilities (LIEF) grant LE120100104, located at the UOW Electron Microscopy Centre.

Conflict of interest

The authors declare no competing financial interests.

Supplementary material

249_2015_1059_MOESM1_ESM.avi (5.5 mb)
Supplementary material 1 (AVI 5605 kb)

Supplementary material 2 (MOV 8443 kb)

References

  1. Ajouz B, Berrier C, Besnard M, Martinac B, Ghazi A (2000) Contributions of the different extramembranous domains of the mechanosensitive ion channel MscL to its response to membrane tension. J Biol Chem 275(2):1015–1022CrossRefPubMedGoogle Scholar
  2. Ayyappan S, Baldev R (2009) Effect of digestion time on size and magnetic properties of spinel CoFe2O4 nanoparticles. J Phys Chem C 113:590–596CrossRefGoogle Scholar
  3. Chang G, Spencer RH, Lee AT, Barclay MT, Rees DC (1998) Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science 282:2220–2226CrossRefPubMedGoogle Scholar
  4. Corry B et al (2010) An improved open-channel structure of MscL determined from FRET confocal microscopy and simulation. J Gen Physiol 136:483–494. doi: 10.1085/jgp.200910376 PubMedCentralCrossRefPubMedGoogle Scholar
  5. Cruickshank CC, Minchin RF, Le Dain AC, Martinac B (1997) Estimation of the pore size of the large-conductance mechanosensitive ion channel of Escherichia coli. Biophys J 73:1925–1931. doi: 10.1016/S0006-3495(97)78223-7 PubMedCentralCrossRefPubMedGoogle Scholar
  6. Delcour AH, Martinac B, Adler J, Kung C (1989) A modified reconstitution method used in patch-clamp studies of Escherichia coli ion channels. Biophys J 56:631–636PubMedCentralCrossRefPubMedGoogle Scholar
  7. Guilherme VM, Jacintho, Brolo AG, Paola C, Suarez PAZ, Rubim JC (2009) Structural investigation of MFe2O4 (M) Fe, Co) magnetic fluids. J Phys Chem 113:7684–7691Google Scholar
  8. Häse CC, Le Dain AC, Martinac B (1995) Purification and functional reconstitution of the recombinant large mechanosensitive ion channel (MscL) of Escherichia coli. J Biol Chem 270:18329–18334CrossRefPubMedGoogle Scholar
  9. Janoff AS (1999). Marcel Dekker, New YorkGoogle Scholar
  10. Kim BH et al (2011) Large-scale synthesis of uniform and extremely small-sized iron oxide nanoparticles for high-resolution T1 magnetic resonance imaging contrast agents. J Am Chem Soc 133:12624–12631. doi: 10.1021/ja203340u CrossRefPubMedGoogle Scholar
  11. Koçer A (2007) A remote controlled valve in liposomes for triggered liposomal release. J Liposome Res 17:219–225. doi: 10.1080/08982100701528203 CrossRefPubMedGoogle Scholar
  12. Lee JG, Kim CS (1998) Growth of ultra-fine cobalt ferrite particles by a sol–gel method and their magnetic properties. J Mater Sci 3:3965–3968CrossRefGoogle Scholar
  13. Levina N et al (1999) Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J 18:1730–1737. doi: 10.1093/emboj/18.7.1730 PubMedCentralCrossRefPubMedGoogle Scholar
  14. Martinac B (2011) Bacterial mechanosensitive channels as a paradigm for mechanosensory transduction. Cell Physiol Biochem 28:1051–1060. doi: 10.1159/000335842 CrossRefPubMedGoogle Scholar
  15. Nomura T et al (2012) Differential effects of lipids and lyso-lipids on the mechanosensitivity of the mechanosensitive channels MscL and MscS. Proc Natl Acad Sci USA 109:8770–8775. doi: 10.1073/pnas.1200051109 PubMedCentralCrossRefPubMedGoogle Scholar
  16. Ozturk N, Semiha Bahceli CC (2005) FT-IR spectroscopic study of 1,5-Pentanedithiol and 1,6-Hexanedithiol adsorbed on NaA, CaA and NaY Zeolites. Z. Naturforsch 60:633–636Google Scholar
  17. Pankhurst QA, Jones SK, Dobson J (2003) Applications of magnetic nanoparticles in biomedicine. J Phys D Appl Phys 36:R167–R181CrossRefGoogle Scholar
  18. Pankhurst QA, Jones SK, Dobson J (2009) Progress in applications of magnetic nanoparticles in biomedicine. J Phys D Appl Phys 42:224001CrossRefGoogle Scholar
  19. Pauline SPAP (2012) Size and shape control evaluation of cobalt (Co) and cobalt ferrite (CoFe2O4) magnetic nanoparticles. Arch Phys Res 3:78–83Google Scholar
  20. Perozo E, Kloda A, Cortes DM, Martinac B (2001) Site-directed spin-labeling analysis of reconstituted Mscl in the closed state. J Gen Physiol 118:193–206PubMedCentralCrossRefPubMedGoogle Scholar
  21. Perozo E, Kloda A, Cortes DM, Martinac B (2002) Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat Struct Biol 9:696–703. doi: 10.1038/nsb827 CrossRefPubMedGoogle Scholar
  22. Shen L, Wang D, Wang Y, Chen Z, Ren L, Zhou X, Ke X, Chena M, Yang A (2013) One-step synthesis of monodisperse, water-soluble ultra-small Fe3O4 nanoparticles for potential bioapplication. Nanoscale 5:2133–2141CrossRefPubMedGoogle Scholar
  23. Sun C, Lee JS, Zhang M (2008) Magnetic nanoparticles in MR imaging and drug delivery. Adv Drug Deliv Rev 60:1252–1265. doi: 10.1016/j.addr.2008.03.018 PubMedCentralCrossRefPubMedGoogle Scholar
  24. Sun QC, Cao J, Tremel W, Musfeldt JL (2012) Spectroscopic signature of the superparamagnetic transition and surface spin disorder in CoFe2O4 nanoparticles. ACS Nano 6:4876–4883CrossRefPubMedGoogle Scholar
  25. Suntres ZE (2011) Liposomal antioxidants for protection against oxidant-induced damage. J Toxicol 2011:152474. doi: 10.1155/2011/152474 PubMedCentralCrossRefPubMedGoogle Scholar
  26. Svenson S. Ed. (2004). American Chemical Society in ACS Symposium Series 879, WashingtonGoogle Scholar
  27. Teng J, Loukin S, Anishkin A, Kung C (2015) The force-from-lipid (FFL) principle of mechanosensitivity, at large and in elements. Pflugers Arch 467:27–37. doi: 10.1007/s00424-014-1530-2 CrossRefPubMedGoogle Scholar
  28. van den Bogaart G, Krasnikov V, Poolman B (2007) Dual-color fluorescence-burst analysis to probe protein efflux through the mechanosensitive channel MscL. Biophys J 92:1233–1240. doi: 10.1529/biophysj.106.088708 PubMedCentralCrossRefPubMedGoogle Scholar
  29. Wahajuddin Arora S (2012) Superparamagnetic iron oxide nanoparticles: magnetic nanoplatforms as drug carriers. Int J Nanomed 7:3445–3471. doi: 10.2147/IJN.S30320 CrossRefGoogle Scholar
  30. Wang Y et al (2014) Single molecule FRET reveals pore size and opening mechanism of a mechano-sensitive ion channe. eLife 3:01834. doi: 10.7554/eLife.01834 Google Scholar

Copyright information

© European Biophysical Societies' Association 2015

Authors and Affiliations

  • Yoshitaka Nakayama
    • 1
  • Mislav Mustapić
    • 2
  • Haleh Ebrahimian
    • 1
  • Pawel Wagner
    • 2
  • Jung Ho Kim
    • 2
  • Md Shahriar Al Hossain
    • 2
  • Joseph Horvat
    • 2
  • Boris Martinac
    • 1
    • 3
    Email author
  1. 1.Molecular Cardiology and Biophysics DivisionVictor Chang Cardiac Research InstituteDarlinghurstAustralia
  2. 2.Institute for Superconducting and Electronic Material (ISEM)University of WollongongNorth WollongongAustralia
  3. 3.St Vincent’s Clinical SchoolUniversity of New South WalesDarlinghurstAustralia

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