Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-17T19:21:33.019Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparative and quantitative investigation of cell labeling of a 12-nm DMSA-coated Fe3O4 magnetic nanoparticle with multiple mammalian cell lines

Published online by Cambridge University Press:  17 January 2011

Yingxun Liu  and
Jinke Wang
Yingxun Liu
Affiliation:
State Key Laboratory of Bioelectronics, School of Biological Science and Medical Engineering, Southeast University, Nanjing 210096, China
Jinke Wang*
Affiliation:
State Key Laboratory of Bioelectronics, School of Biological Science and Medical Engineering, Southeast University, Nanjing 210096, China
*
a)Address all correspondence to this author. e-mail: wangjinke@seu.edu.cn
Get access

Abstract

This work investigated the cell labeling of 12-nm meso-2,-3-dimercaptosuccinic acid (DMSA)-coated Fe3O4 magnetic nanoparticles with multiple mammalian cells. Six different cells, including RAW264.7, Hepa1-6, THP-1, HepG2, HeLa, and HL-7702, were treated with the nanoparticles at various concentrations (20~100 μg/mL) for different times (2~72 h), and the labeling effect was evaluated by observing the intracellular internalization of the nanoparticles with Prussian blue staining and measuring the corresponding cellular iron loading with colorimetric assay. The results demonstrated that the nanoparticles could label all cells studied. However, the labeling efficiency was not the same between different cells, which depended on the cell types, the nanoparticles’ concentration, and the time of treating cells with the nanoparticles. In comparison, RAW264.7 was labeled more effectively than other cells at any concentration of the nanoparticles. The iron loading of RAW264.7 significantly increased with the concentration of the nanoparticles and the treatment time. However, both human liver cells (HepG2 and HL-7720) were labeled with the lowest iron loading. The measurement of cell viability revealed that the growth of all cells was not affected by the nanoparticles at a common in vivo application dose of iron nanoparticles (30 μg/mL), demonstrating that the nanoparticles have better biocompatability.

Keywords

MagneticNanoscaleParticulate
Type
Articles
Information
Journal of Materials Research , Volume 26 , Issue 6 , 28 March 2011 , pp. 822 - 831
Copyright
Copyright © Materials Research Society 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

1.Shaw, S.Y., Westly, E.C., Pittet, M.J., Subramanian, A., Schreiber, S.L., and Weissleder, R.: Perturbational profiling of nanomaterial biologic activity. Proc. Natl. Acad. Sci. USA 105, 7387 (2008).CrossRefGoogle ScholarPubMed
2.Miller, M.M., Prinz, G.A., Cheng, S.F., and Bounnak, S.: Detection of a micron-sized magnetic sphere using a ring-shaped anisotropic magnetoresistance-based sensor: A model for a magnetoresistance-based biosensor. Appl. Phys. Lett. 81, 2211 (2002).CrossRefGoogle Scholar
3.Jain, T.K., Morales, M.A., Sahoo, S.K., Leslie-Pelecky, D.L., and Labhasetwar, V.: Iron oxide nanoparticles for sustained delivery of anticancer agents. Mol. Pharm. 2, 194 (2005).CrossRefGoogle ScholarPubMed
4.Chourpa, I., Douziech-Eyrolles, L., Ngaboni-Okassa, L., Fouquenet, J.F., Cohen-Jonathan, S., Souce, M., Marchais, H., and Dubois, P.: Molecular composition of iron oxide nanoparticles, precursors for magnetic drug targeting, as characterized by confocal Raman microspectroscopy. Analyst (Lond.) 130, 1395 (2005).CrossRefGoogle ScholarPubMed
5.Tiefenauer, L.X.: Magnetic nanoparticles as contrast agents for medical diagnosis in nanotechnology, in Biology and Medicine: Methods, Devices, and Applications, edited by Vo-Dinh, T. (CRC Press, Taylor and Francis, Boca Raton, FL, 2007), pp. 1–20.Google Scholar
6.Morana, G., Salviato, E., and Guarise, A.: Contrast agents for hepatic MRI. Cancer Imaging 7(Special issue A), S24 (2007).CrossRefGoogle ScholarPubMed
7.Modo, M.M.J. and Bulteì, J.W.M.: Molecular and Cellular MR Imaging (CRC Press, Boca Raton, FL, 2007).CrossRefGoogle Scholar
8.Corot, C., Robert, P., Idee, J.M., and Port, M.: Recent advances in iron oxide nanocrystal technology for medical imaging. Adv. Drug Delivery Rev. 58, 1471 (2006).CrossRefGoogle ScholarPubMed
9.Ito, A., Shinkai, M., Honda, H., and Kobayashi, T.: Heat-inducible TNF-alpha gene therapy combined with hyperthermia using magnetic nanoparticles as a novel tumor-targeted therapy. Cancer Gene Ther. 8, 649 (2001).CrossRefGoogle ScholarPubMed
10.Hergt, R. and Dutz, S.: Magnetic particle hyperthermia-biophysical limitations of a visionary tumour therapy. J. Magn. Magn. Mater. 311, 187 (2007).CrossRefGoogle Scholar
11.Nam, H.Y., Kwon, S.M., Chung, H., Lee, S.Y., Kwon, S.H., Jeon, H., Kim, Y., Park, J.H., Kim, J., Her, S., Oh, Y.K., Kwon, I.C., Kim, K., and Jeong, S.Y.: Cellular uptake mechanism and intracellular fate of hydrophobically modified glycol chitosan nanoparticles. J. Controlled Release 135, 259 (2009).CrossRefGoogle ScholarPubMed
12.Chithrani, B.D., Ghazani, A.A., and Chan, W.C.: Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett. 6, 662 (2006).CrossRefGoogle ScholarPubMed
13.Chen, Z.P., Zhang, Y., Zhang, S., Xia, J.G., Liu, J.W., Xu, K., and Gu, N.: Preparation and characterization of water-soluble monodisperse magnetic iron oxide nanoparticles via surface double-exchange with DMSA. Colloids Surf., A: 316, 210 (2008).CrossRefGoogle Scholar
14.Pieters, R., Huismans, D.R., Leyva, A., and Veerman, A.J.P.: Comparison of the rapid automated MTT-assay with a dye exclusion assay for chemosensitivity testing in childhood leukaemia. Br. J. Cancer 59, 217 (1989).CrossRefGoogle ScholarPubMed
15.Häfeli, U.O., Riffle, J.S., Harris-Shekhawat, L., Carmichael-Baranauskas, A., Mark, F., Dailey, J.P., and Bardenstein, D.: Cell uptake and in vitro toxicity of magnetic nanoparticles suitable for drug delivery. Mol. Pharm. 6, 1417 (2009).CrossRefGoogle ScholarPubMed
16.Wilhelm, C., Billotey, C., Roger, J., Pons, J.N., Bacri, J.C., and Gazeau, F.: Intracellular uptake of anionic superparamagnetic nanoparticles as a function of their surface coating. Biomaterials 24, 1001 (2003).CrossRefGoogle ScholarPubMed
17.Wilhelm, C., Gazeau, F., Roger, J., Pons, J.N., and Bacri, J.C.: Interaction of anionic superparamagnetic nanoparticles with cells: Kinetic analyses of membrane adsorption and subsequent internalization. Langmuir 18, 8148 (2002).CrossRefGoogle Scholar
18.Wilhelm, C. and Gazeau, F.: Universal cell labelling with anionic magnetic nanoparticles. Biomaterials 29, 3161 (2008).CrossRefGoogle ScholarPubMed
19.Zhou, J., Leuschner, C., Kumar, C., Hormes, J., and Soboyejo, W.O.: A TEM study of functionalized magnetic nanoparticles targeting breast cancer cells. Mater. Sci. Eng., C: Biomim. Supramol. Syst. 26, 1451 (2006).CrossRefGoogle Scholar
20.Arbab, A.S., Bashaw, L.A., Miller, B.R., Jordan, E.K., Lewis, B.K., Kalish, H., and Frank, J.A.: Characterization of biophysical and metabolic properties of cells labeled with superparamagnetic iron oxide nanoparticles and transfection agent for cellular MR imaging. Radiology 229, 838 (2003).CrossRefGoogle ScholarPubMed
21.Frank, J.A., Miller, B.R., Arbab, A.S., Zywicke, H.A., Jordan, E.K., Lewis, B.K., Bryant, L.H., and Bulte, J.W.M. Jr: Clinically applicable labeling of mammalian cells and stem cells by combining superparamagnetic iron oxides and commonly available transfection agents. Radiology 228, 480 (2003).CrossRefGoogle Scholar
22.Rivière, C., Boudghène, F.P., Gazeau, F., Roger, J., Pons, J.N., Laissy, J.P., Allaire, E., Michel, J.B., Letourneur, D., and Deux, J.F.: Iron oxide nanoparticle–labeled rat smooth muscle cells: Cardiac MR imaging for cell graft monitoring and quantitation. Radiology 235, 959 (2005).CrossRefGoogle ScholarPubMed
23.Ju, S.H., Teng, G.J., Zhang, Y., Ma, M., Chen, F., and Ni, Y.Y.: In vitro labeling and MRI of mesenchymal stem cells from human umbilical cord blood. Magn. Reson. Imaging 24, 611 (2006).CrossRefGoogle ScholarPubMed
24.Song, M., Moon, W.K., Kim, Y., Lim, D., Song, I.C., and Yoon, B.W.: Labeling efficacy of superparamagnetic iron oxide nanoparticles to human neural stem cells: Comparison of ferumoxides, monocrystalline iron oxide, cross-linked iron oxide (CLIO)-NH2 and tat-CLIO. Korean J. Radiol. 8, 365 (2007).CrossRefGoogle ScholarPubMed
25.Schwarz, S., Fernandes, F., Sanroman, L., Hodenius, M., Lang, C., Himmelreich, U., Schmitz-Rode, T., Schueler, D., Hoehn, M., Zenke, M., and Hieronymus, T.: Synthetic and biogenic magnetite nanoparticles for tracking of stem cells and dendritic cells. J. Magn. Magn. Mater. 321, 1533 (2009).CrossRefGoogle Scholar
26.Farrell, E., Wielopolski, P., Pavljasevic, P., Kops, N., Weinans, H., Bernsen, M.R., and van Osch, G.J.: Cell labelling with superparamagnetic iron oxide has no effect on chondrocyte behaviour. Osteoarthritis Cartilage 17, 961 (2009).CrossRefGoogle ScholarPubMed
27.Slavin, W.: Atomic absorption spectrometry. Methods Enzymol. 158, 117 (1988).CrossRefGoogle ScholarPubMed
28.Hoepken, H.H., Korten, T., Robinson, S.R., and Dringen, R.: Iron accumulation, iron-mediated toxicity and altered levels of ferritin and transferrin receptor in cultured astrocytes during incubation with ferric ammonium citrate. J. Neurochem. 88, 1194 (2004).CrossRefGoogle ScholarPubMed
29.Woodmansee, A.N. and Imlay, J.A.: Quantitation of intracellular free iron by electron paramagnetic resonance spectroscopy. Methods Enzymol. 349, 3 (2002).CrossRefGoogle ScholarPubMed
30.Strom, V., Hultenby, K., Gruttner, C., Teller, J., Xu, B., and Holgersson, J.: A novel and rapid method for quantification of magnetic nanoparticle–cell interactions using a desktop susceptometer. Nanotechnology 15, 457 (2004).CrossRefGoogle Scholar
31.LeVine, S.M., Wulser, M.J., and Lynch, S.G.: Iron quantification in cerebrospinal fluid. Anal. Biochem. 265, 74 (1998).CrossRefGoogle ScholarPubMed
32.Fish, W.W.: Rapid colorimetric micromethod for the quantitation of complexed iron in biological samples. Methods Enzymol. 158, 357 (1988).CrossRefGoogle ScholarPubMed
33.Adams, P.E.: Determining iron content in foods by spectrophotometry. J. Chem. Educ. 72, 649 (1995).CrossRefGoogle Scholar
34.Gay, C., Collins, J., and Gebicki, J.M.: Determination of iron in solutions with the ferric-xylenol orange complex. Anal. Biochem. 27, 143 (1999).CrossRefGoogle Scholar
35.Kalambur, V.S., Longmire, E.K., and Bischof, J.C.: Cellular level loading and heating of superparamagnetic iron oxide nanoparticles. Langmuir 23, 12329 (2007).CrossRefGoogle ScholarPubMed
36.Huberman, A. and Perez, C.: Nonheme iron determination. Anal. Biochem. 307, 375 (2002).CrossRefGoogle ScholarPubMed
37.Rad, A.M., Janic, B., Iskander, A.S.M., Soltanian-Zadeh, H., and Arbab, A.S.: Measurement of quantity of iron in magnetically labeled cells: Comparison among different UV/VIS spectrometric methods. Biotechniques 43, 627 (2007).CrossRefGoogle ScholarPubMed
38.Jordan, A., Scholz, R., Wust, P., Schirra, H., Schiestel, T., Schmidt, H., and Felix, R.: Endocytosis of dextran and silan-coated magnetite nanoparticles and the effect of intracellular hyperthermia on human mammary carcinoma cells in vitro. J. Magn. Magn. Mater. 194, 185 (1999).CrossRefGoogle Scholar
39.Ho, V.H.B., Barcza, A., Chen, R., Müller, K.H., Darton, N.J., and Slater, N.K.H.: The precise control of cell labelling with streptavidin paramagnetic particles. Biomaterials 30, 6548 (2009).CrossRefGoogle ScholarPubMed
40.Harisinghani, M.G., Barentsz, J., Hahn, P.F., Deserno, W.M., Tabatabaei, S., van de Kaa, C.H., de la Rosette, J., and Weissleder, R.: Noninvasive detection of clinically occult lymph-node metastases in prostate cancer. N. Engl. J. Med. 348, 2491 (2003).CrossRefGoogle ScholarPubMed
41.Bacon, B.R., Stark, D.D., Park, C.H., Saini, S., Groman, E.V., Hahn, P.F., Compton, C.C., and Ferrucci, J.T.: Ferrite particles: A new magnetic resonance imaging contrast agent. Lack of acute or chronic hepatotoxicity after intravenous administration. J. Lab. Clin. Med. 110, 164 (1987).Google ScholarPubMed
42.Weissleder, R., Stark, D.D., Engelstad, B.L., Bacon, B.R., Compton, C.C., White, D.L., Jacobs, P., and Lewis, J.: Superparamagnetic iron oxide: Pharmacokinetics and toxicity. AJR Am. J. Roentgenol. 152, 167 (1989).CrossRefGoogle ScholarPubMed