Tumour cell labelling by magnetic nanoparticles with determination of intracellular iron content and spatial distribution of the intracellular iron

International Journal of Molecular Sciences

Volumn 14, Issue 5, 2013, Pages 9111-9125

  Wang, Zhigang ^a   Cuschieri, Alfred ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Magnetic cell labelling; Magnetic force microscopy; Magnetic nanoparticles; Nanomedicine; SPIONs; Superparamagnetic

Indexed keywords

IRON; PROTAMINE SULFATE; SUPERPARAMAGNETIC IRON OXIDE; MAGNETITE NANOPARTICLE;

ARTICLE; CELL LABELING; CELL VIABILITY; CELLULAR DISTRIBUTION; COLORIMETRY; CONTROLLED STUDY; ELECTROPORATION; HUMAN; HUMAN CELL; INTERNALIZATION; IRON TRANSPORT; MAGNETIC FORCE MICROSCOPY; MICROSCOPY; TUMOR CELL; CELL SURVIVAL; CHEMISTRY; ENDOCYTOSIS; GENETIC TRANSFECTION; INTRACELLULAR SPACE; METABOLISM; NEOPLASM; STAINING; STANDARD; TUMOR CELL LINE; ULTRASTRUCTURE;

CELL LINE, TUMOR; CELL SURVIVAL; ELECTROPORATION; ENDOCYTOSIS; HUMANS; INTRACELLULAR SPACE; IRON; MAGNETITE NANOPARTICLES; NEOPLASMS; REFERENCE STANDARDS; STAINING AND LABELING; TRANSFECTION;

EID: 84876904919     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14059111     Document Type: Article

References (42)

1. Thorek, D.L.; Chen, A.K.; Czupryna, J.; Tsourkas, A. Superparamagnetic iron oxide nanoparticle probes for molecular imaging. Ann. Biomed. Eng. 2006, 34, 23-38.
2. Pankhurst, Q.A.; Thanh, N.T.K.; Jones, S.K.; Dobson, J. Progress in applications of magnetic nanoparticles in biomedicine. J. Phys. D Appl. Phys. 2009, 42, doi:10.1088/0022-3727/ 42/22/224001.
3. Frimpong, R.A.; Hilt, J.Z. Magnetic nanoparticles in biomedicine: synthesis, functionalization and applications. Nanomedicine (Lond) 2010, 5, 1401-1414.
4. Pinkse, G.G.; Steenvoorde, E.; Hogendoorn, S.; Noteborn, M.; Terpstra, O.T.; Bruijn, J.A.; de Heer, E. Stable transplantation results of magnetically retracted islets: A novel method. Diabetologia 2004, 47, 55-61.
5. Alexiou, C.; Jurgons, R.; Schmid, R.J.; Bergemann, C.; Henke, J.; Erhardt, W.; Huenges, E.; Parak, F. Magnetic drug targeting-biodistribution of the magnetic carrier and the chemotherapeutic agent mitoxantrone after locoregional cancer treatment. J. Drug Target. 2003, 11, 139-149.
6. Alexiou, C.; Arnold, W.; Klein, R.J.; Parak, F.G.; Hulin, P.; Bergemann, C.; Erhardt, W.; Wagenpfeil, S.; Lubbe, A.S. Locoregional cancer treatment with magnetic drug targeting. Cancer Res. 2000, 60, 6641-6648.
7. Ivkov, R.; DeNardo, S.J.; Daum, W.; Foreman, A.R.; Goldstein, R.C.; Nemkov, V.S.; DeNardo, G.L. Application of high amplitude alternating magnetic fields for heat induction of nanoparticles localized in cancer. Clin. Cancer Res. 2005, 11, 7093s-7103s.
8. Matuszewski, L.; Persigehl, T.; Wall, A.; Schwindt, W.; Tombach, B.; Fobker, M.; Poremba, C.; Ebert, W.; Heindel, W.; Bremer, C. Cell tagging with clinically approved iron oxides: Feasibility and effect of lipofection, particle size, and surface coating on labeling efficiency. Radiology 2005, 235, 155-161.
9. Oudkerk, M.; van den Heuvel, A.G.; Wielopolski, P.A.; Schmitz, P.I.; Borel Rinkes, I.H.; Wiggers, T. Hepatic lesions: detection with ferumoxide-enhanced T1-weighted MR imaging. Radiology 1997, 203, 449-456.
10. Zhang, B.; Jiang, B.; Chen, Y.; Huang, H.; Xie, Q.; Kang, M.; Zhang, H.; Zhai, C.; Wu, Y. Detection of viability of transplanted beta cells labeled with a novel contrast agent-polyvinylpyrrolidone-coated superparamagnetic iron oxide nanoparticles by magnetic resonance imaging. Contrast Media Mol. Imaging 2012, 7, 35-44.
11. Bulte, J.W.; Kraitchman, D.L. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed. 2004, 17, 484-499.
12. Sykova, E.; Jendelova, P. In vivo tracking of stem cells in brain and spinal cord injury. Prog. Brain Res. 2007, 161, 367-383.
13. Jiang, J.; Chen, Y.; Zhu, Y.; Yao, X.; Qi, J. Efficient in vitro labeling of human prostate cancer cells with superparamagnetic iron oxide nanoparticles. Cancer Biother. Radiopharm. 2011, 26, 461-467.
14. Sun, J.H.; Zhang, Y.L.; Nie, C.H.; Qian, S.P.; Yu, X.B.; Xie, H.Y.; Zhou, L.; Zheng, S.S. In vitro labeling of endothelial progenitor cells isolated from peripheral blood with superparamagnetic iron oxide nanoparticles. Mol. Med. Rep. 2012, 6, 282-286.
15. Wang, Y.X. Superparamagnetic iron oxide based MRI contrast agents: Current status of clinical application. Quant. Imaging Med. Surg. 2012, 1, 35-40.
16. Corot, C.; Robert, P.; Idee, J.-M.; Port, M. Recent advances in iron oxide nanocrystal technology for medical imaging. Adv. Drug Deliv. Rev. 2006, 58, 1471-1504.
17. Zhu, X.M.; Wang, Y.X.; Leung, K.C.; Lee, S.F.; Zhao, F.; Wang, D.W.; Lai, J.M.; Wan, C.; Cheng, C.H.; Ahuja, A.T. Enhanced cellular uptake of aminosilane-coated superparamagnetic iron oxide nanoparticles in mammalian cell lines. Int. J. Nanomed. 2012, 7, 953-964.
18. Zhang, Y.; Kohler, N.; Zhang, M. Surface modification of superparamagnetic magnetite nanoparticles and their intracellular uptake. Biomaterials 2002, 23, 1553-1561.
19. Foster, P.J.; Dunn, E.A.; Karl, K.E.; Snir, J.A.; Nycz, C.M.; Harvey, A.J.; Pettis, R.J. Cellular magnetic resonance imaging: In vivo imaging of melanoma cells in lymph nodes of mice. Neoplasia 2008, 10, 207-216.
20. Lewin, M.; Carlesso, N.; Tung, C.H.; Tang, X.W.; Cory, D.; Scadden, D.T.; Weissleder, R. Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells. Nat. Biotechnol. 2000, 18, 410-414.
21. Buerli, T.; Pellegrino, C.; Baer, K.; Lardi-Studler, B.; Chudotvorova, I.; Fritschy, J.M.; Medina, I.; Fuhrer, C. Efficient transfection of DNA or shRNA vectors into neurons using magnetofection. Nat. Protoc. 2007, 2, 3090-3101.
22. Walczak, P.; Ruiz-Cabello, J.; Kedziorek, D.A.; Gilad, A.A.; Lin, S.; Barnett, B.; Qin, L.; Levitsky, H.; Bulte, J.W.M. Magnetoelectroporation: improved labeling of neural stem cells and leukocytes for cellular magnetic resonance imaging using a single FDA-approved agent. Nanomed. Nanotechnol. Biol. Med. 2006, 2, 89-94.
23. Prentice, P.; Cuschierp, A.; Dholakia, K.; Prausnitz, M.; Campbell, P. Membrane disruption by optically controlled microbubble cavitation. Nat. Phys. 2005, 1, 107-110.
24. Bulte, J.W.M.; Douglas, T.; Witwer, B.; Zhang, S.C.; Strable, E.; Lewis, B.K.; Zywicke, H.; Miller, B.; van Gelderen, P.; Moskowitz, B.M.; et al. Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nat. Biotechnol. 2001, 19, 1141-1147.
25. Leung, K. Ferumoxides. Molecular Imaging and Contrast Agent Database (MICAD). Available online: http://www.ncbi.nlm.nih.gov/books/NBK23037/(accessed on 26 January 2013).
26. Frank, J.A.; Miller, B.R.; Arbab, A.S.; Zywicke, H.A.; Jordan, E.K.; Lewis, B.K.; Bryant, L.H., Jr.; Bulte, J.W. Clinically applicable labeling of mammalian and stem cells by combining superparamagnetic iron oxides and transfection agents. Radiology 2003, 228, 480-487.
27. Wang, L.; Wang, Z.; Frank, T.G.; Brown, S.I.; Chudek, S.A.; Cuschieri, A. Rapid and efficient cell labeling with a MRI contrast agent by electroporation in the presence of protamine sulfate. Nanomedicine (Lond) 2009, 4, 305-315.
28. Amemiya, Y.; Tanaka, T.; Yoza, B.; Matsunaga, T. Novel detection system for biomolecules using nano-sized bacterial magnetic particles and magnetic force microscopy. J. Biotechnol. 2005, 120, 308-314.
29. Shen, H.B.; Long, D.H.; Zhu, L.Z.; Li, X.Y.; Dong, Y.M.; Jia, N.Q.; Zhou, H.Q.; Xin, X.; Sun, Y. Magnetic force microscopy analysis of apoptosis of HL-60 cells induced by complex of antisense oligonucleotides and magnetic nanoparticles. Biophys. Chem. 2006, 122, 1-4.
30. Zhang, Y.; Yang, M.; Ozkan, M.; Ozkan, C.S. Magnetic force microscopy of iron oxide nanoparticles and their cellular uptake. Biotechnol. Prog. 2009, 25, 923-928.
31. Huberman, A.; Perez, C. Nonheme iron determination. Anal. Biochem. 2002, 307, 375-378.
32. Wu, Y.J.; Muldoon, L.L.; Varallyay, C.; Markwardt, S.; Jones, R.E.; Neuwelt, E.A. In vivo leukocyte labeling with intravenous ferumoxides/protamine sulfate complex and in vitro characterization for cellular magnetic resonance imaging. Am. J. Physiol. Cell Physiol. 2007, 293, C1698-C1708.
33. Riemer, J.; Hoepken, H.H.; Czerwinska, H.; Robinson, S.R.; Dringen, R. Colorimetric ferrozine-based assay for the quantitation of iron in cultured cells. Anal. Biochem. 2004, 331, 370-375.
34. Brekke, C.; Morgan, S.C.; Lowe, A.S.; Meade, T.J.; Price, J.; Williams, S.C.; Modo, M. The in vitro effects of a bimodal contrast agent on cellular functions and relaxometry. NMR Biomed. 2007, 20, 77-89.
35. Kamau, S.W.; Hassa, P.O.; Steitz, B.; Petri-Fink, A.; Hofmann, H.; Hofmann-Amtenbrink, M.; von Rechenberg, B.; Hottiger, M.O. Enhancement of the efficiency of non-viral gene delivery by application of pulsed magnetic field. Nucleic Acids Res. 2006, 34, e40.
36. Mykhaylyk, O.; Antequera, Y.S.; Vlaskou, D.; Plank, C. Generation of magnetic nonviral gene transfer agents and magnetofection in vitro. Nat. Protoc. 2007, 2, 2391-2411.
37. Lee, C.H.; Kim, E.Y.; Jeon, K.; Tae, J.C.; Lee, K.S.; Kim, Y.O.; Jeong, M.Y.; Yun, C.W.; Jeong, D.K.; Cho, S.K.; et al. Simple, efficient, and reproducible gene transfection of mouse embryonic stem cells by magnetofection. Stem Cells Dev. 2008, 17, 133-141.
38. Park, H.Y.; Noh, E.H.; Chung, H.M.; Kang, M.J.; Kim, E.Y.; Park, S.P. Efficient generation of virus-free iPS cells using liposomal magnetofection. PLoS One 2012, 7, e45812.
39. Furlani, E.P.; Xue, X. A model for predicting field-directed particle transport in the magnetofection process. Pharm. Res. 2012, 29, 1366-1379.
40. Hoskins, C.; Wang, L.; Cheng, W.P.; Cuschieri, A. Dilemmas in the reliable estimation of the in vitro cell viability in magnetic nanoparticle engineering: which tests and what protocols? Nanoscale Res. Lett. 2012, 7, 77.
41. Liu, D.; Wang, L.; Wang, Z.; Cuschieri, A. Magnetoporation and magnetolysis of cancer cells via carbon nanotubes induced by rotating magnetic fields. Nano Lett. 2012, 12, 5117-5121.
42. Hong, R.; Cima, M.J.; Weissleder, R.; Josephson, L. Magnetic microparticle aggregation for viscosity determination by MR. Magn. Reson. Med. 2008, 59, 515-520.