Effects of DMSA-Coated Fe3O4 nanoparticles on the transcription of genes related to iron and osmosis homeostasis

Toxicological Sciences

Volumn 131, Issue 2, 2013, Pages 521-536

  Liu, Yingxun ^a   Wang, Jinke ^a  

^a SOUTHEAST UNIVERSITY   (China)

Author keywords

DMSA coated Fe3O4 nanoparticles; Gene transcription; Iron and osmosis homeostasis

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; DEFEROXAMINE; FERRIC OXIDE NANOPARTICLE; IRON; METAL NANOPARTICLE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; SLC44A1 PROTEIN; SLC5A3 PROTEIN; SUCCIMER; TFRC PROTEIN; TRANSFERRIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL TRANSPORT; CONTROLLED STUDY; CYTOTOXICITY; DRUG COATING; ENDOCYTOSIS; GENE EXPRESSION; HOMEOSTASIS; INTERNALIZATION; INTRACELLULAR MEMBRANE; IRON KINETICS; IRON METABOLISM; MACROPHAGE; MATERIAL COATING; NONHUMAN; OSMOSIS; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RECEPTOR DOWN REGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION;

FERUMOXYTOL; HOMEOSTASIS; IRON; METAL NANOPARTICLES; MICROSCOPY, ELECTRON, TRANSMISSION; OSMOSIS; SUCCIMER; TRANSCRIPTION, GENETIC;

EID: 84873819801     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfs300     Document Type: Article

References (82)

1. Antosiewicz, J., Ziolkowski, W., Kaczor, J. J., and Herman-Antosiewicz, A. (2007). Tumor necrosis factor-alpha-induced reactive oxygen species formation is mediated by JNK1-dependent ferritin degradation and elevation of labile iron pool. Free Radic. Biol. Med. 43, 265-270.
2. Arbab, A. S., Wilson, L. B., Ashari, P., Jordan, E. K., Lewis, B. K., and Frank, J. A. (2005). A model of lysosomal metabolism of dextran coated superparamagnetic iron oxide (SPIO) nanoparticles: Implications for cellular magnetic resonance imaging. NMR Biomed. 18, 383-389.
3. Arbab, A. S., Yocum, G. T., Kalish, H., Jordan, E. K., Anderson, S. A., Khakoo, A. Y., Read, E. J., and Frank, J. A. (2004). Efficient magnetic cell labeling with protamine sulfate complexed to ferumoxides for cellular MRI. Blood 104, 1217-1223.
4. Auffan, M., Decome, L., Rose, J., Orsiere, T., De Meo, M., Briois, V., Chaneac, C., Olivi, L., Berge-Lefranc, J. L., Botta, A., et al. (2006). In vitro interactions between DMSA-coated maghemite nanoparticles and human fibroblasts: A physicochemical and cyto-genotoxical study. Environ. Sci. Technol. 40, 4367-4373.
5. Balakumaran, A., Pawelczyk, E., Ren, J., Sworder, B., Chaudhry, A., Sabatino, M., Stroncek, D., Frank, J. A., and Robey, P. G. (2010). Superparamagnetic iron oxide nanoparticles labeling of bone marrow stromal (mesenchymal) cells does not affect their "stemness". PLoS ONE 5, e11462.
6. Berry, C. C., Charles, S., Wells, S., Dalby, M. J., and Curtis, A. S. (2004). The influence of transferrin stabilised magnetic nanoparticles on human dermal fibroblasts in culture. Int. J. Pharm. 269, 211-225.
7. Berry, G. T., Mallee, J. J., Kwon, H. M., Rim, J. S., Mulla, W. R., Muenke, M., and Spinner, N. B. (1995). The human osmoregulatory Na+/myo-inositol cotransporter gene (SLC5A3): Molecular cloning and localization to chromosome 21. Genomics 25, 507-513.
8. Bolstad, B. M., Irizarry, R. A., Astrand, M., and Speed, T. P. (2003). A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185-193.
9. Brayner, R. (2008). The toxicological impact of nanoparticles. Nano Today. 3, 48-55.
10. Briley-Saebo, K., Bjørnerud, A., Grant, D., Ahlstrom, H., Berg, T., and Kindberg, G. M. (2004). Hepatic cellular distribution and degradation of iron oxide nanoparticles following single intravenous injection in rats: Implications for magnetic resonance imaging. Cell Tissue Res. 316, 315-323.
11. Brown, P. O., and Botstein, D. (1999). Exploring the new world of the genome with DNA microarrays. Nat. Genet. 21(Suppl. 1), 33-37.
12. Bulte, J. W., and Kraitchman, D. L. (2004). Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed. 17, 484-499.
13. Chen, N. H., Reith, M. E., and Quick, M. W. (2004). Synaptic uptake and beyond: The sodium- and chloride-dependent neurotransmitter transporter family SLC6. Pflugers Arch. 447, 519-531.
14. Chen, Z. P., Zhang, Y., Zhang, S., Xia, J. G., Liu, J. W., Xu, K., and Gu, N. (2008). Preparation and characterization of water-soluble monodisperse magnetic iron oxide nanoparticles via surface double-exchange with DMSA. Colloid Surf. A 316, 210-216.
15. Cozar, O., Leopold, N., Jelic, C., Chiş, V., David, L., Mocanu, A., and Tomoaia-Cotişel, M. (2006). IR, Raman and surface-enhanced Raman study of desferrioxamine B and its Fe(III) complex, ferrioxamine B. J. Mol. Struct. 788, 1-6.
16. Duguet, E., Vasseur, S., Mornet, S., and Devoisselle, J. M. (2006). Magnetic nanoparticles and their applications in medicine. Nanomedicine (Lond.). 1, 157-168.
17. Feelders, R. A., Kuiper-Kramer, E. P., and van Eijk, H. G. (1999). Structure, function and clinical significance of transferrin receptors. Clin. Chem. Lab. Med. 37, 1-10.
18. Flo, T. H., Smith, K. D., Sato, S., Rodriguez, D. J., Holmes, M. A., Strong, R. K., Akira, S., and Aderem, A. (2004). Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432, 917-921.
19. Gupta, A. K., and Gupta, M. (2005). Cytotoxicity suppression and cellular uptake enhancement of surface modified magnetic nanoparticles. Biomaterials 26, 1565-1573.
20. Hafeli, U. O., and Pauer, G. J. (1999). In vitro and in vivo toxicity of magnetic microspheres. J. Magn. Magn. Mater. 194, 76-82.
21. Hafeli, U. O., Riffle, J. S., Harris-Shekhawat, L., Carmichael-Baranauskas, A., Mark, F., Dailey, J. P., and Bardenstein, D. (2009). Cell uptake and in vitro toxicity of magnetic nanoparticles suitable for drug delivery. Mol. Pharm. 6, 1417-1428.
22. Handler, J. S., and Kwon, H. M. (1996). Regulation of the myo-inositol and betaine cotransporters by tonicity. Kidney Int. 49, 1682-1683.
23. Hentze, M. W., and Kuhn, L. C. (1996). Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 93, 8175-8182.
24. Holub, B. J. (1986). Metabolism and function of myo-inositol and inositol phospholipids. Annu. Rev. Nutr. 6, 563-597.
25. 4 nanoparticles and their applications in cell labeling and in vivo imaging. J. Nanobiotechnology 8, 25.
26. Huang, F., Shi, L. J., Heng, H. H., Fei, J., and Guo, L. H. (1995). Assignment of the human GABA transporter gene (GABATHG) locus to chromosome 3p24-p25. Genomics 29, 302-304.
27. Karpinets, T. V., Foy, B. D., and Frazier, J. M. (2004). Tailored gene array databases: Applications in mechanistic toxicology. Bioinformatics 20, 507-517.
28. Kedziorek, D. A., Muja, N., Walczak, P., Ruiz-Cabello, J., Gilad, A. A., Jie, C. C., and Bulte, J. W. (2010). Gene expression profiling reveals early cellular responses to intracellular magnetic labeling with superparamagnetic iron oxide nanoparticles. Magn. Reson. Med. 63, 1031-1043.
29. Kerr, M. K., Martin, M., and Churchill, G. A. (2000). Analysis of variance for gene expression microarray data. J. Comput. Biol. 7, 819-837.
30. Kruszewski, M. (2003). Labile iron pool: The main determinant of cellular response to oxidative stress. Mutat. Res. 531, 81-92.
31. Kusuhara, H., and Sugiyama, Y. (2005). Active efflux across the blood-brain barrier: Role of the solute carrier family. NeuroRx 2, 73-85.
32. Laurent, S., Burtea, C., Thirifays, C., Häfeli, U. O., and Mahmoudi, M. (2012). Crucial ignored parameters on nanotoxicology: The importance of toxicity assay modifications and "cell vision". PLoS ONE 7, e29997.
33. Lee, C. M., Jeong, H. J., Kim, E. M., Kim, D. W., Lim, S. T., Kim, H. T., Park, I. K., Jeong, Y. Y., Kim, J. W., and Sohn, M. H. (2009). Superparamagnetic iron oxide nanoparticles as a dual imaging probe for targeting hepatocytes in vivo. Magn. Reson. Med. 62, 1440-1446.
34. Lévy, M., Lagarde, F., Maraloiu, V. A., Blanchin, M. G., Gendron, F., Wilhelm, C., and Gazeau, F. (2010). Degradability of superparamagnetic nanoparticles in a model of intracellular environment: Follow-up of magnetic, structural and chemical properties. Nanotechnology 21, 395103.
35. 4 nanoparticles with six different mammalian cell lines. J. Nanopart. Res. 13, 199-212.
36. 4 magnetic nanoparticles into mouse macrophage cells. Adv. Mater. Res. 455-456, 1221-1227.
37. 4 magnetic nanoparticle with multiple mammalian cell lines. J. Mater. Res. 26, 822-831.
38. Lunov, O., Syrovets, T., Röcker, C., Tron, K., Nienhaus, G. U., Rasche, V., Mailänder, V., Landfester, K., and Simmet, T. (2010). Lysosomal degradation of the carboxydextran shell of coated superparamagnetic iron oxide nanoparticles and the fate of professional phagocytes. Biomaterials 31, 9015-9022.
39. MacKenzie, E. L., Iwasaki, K., and Tsuji, Y. (2008). Intracellular iron transport and storage: From molecular mechanisms to health implications. Antioxid. Redox Signal. 10, 997-1030.
40. Mahmoudi, M., Simchi, A., Imani, M., Milani, A. S., and Stroeve, P. (2009). An in vitro study of bare and poly(ethylene glycol)-co-fumarate-coated superparamagnetic iron oxide nanoparticles: A new toxicity identification procedure. Nanotechnology 20, 225104.
41. Mallee, J. J., Atta, M. G., Lorica, V., Rim, J. S., Kwon, H. M., Lucente, A. D., Wang, Y., and Berry, G. T. (1997). The structural organization of the human Na+/myo-inositol cotransporter (SLC5A3) gene and characterization of the promoter. Genomics 46, 459-465.
42. Marquis, B. J., Love, S. A., Braun, K. L., and Haynes, C. L. (2009). Analytical methods to assess nanoparticle toxicity. Analyst 134, 425-439.
43. McCarthy, J. R., and Weissleder, R. (2008). Multifunctional magnetic nanoparticles for targeted imaging and therapy. Adv. Drug Deliv. Rev. 60, 1241-1251.
44. Nakanishi, T., Turner, R. J., and Burg, M. B. (1989). Osmoregulatory changes in myo-inositol transport by renal cells. Proc. Natl. Acad. Sci. U.S.A. 86, 6002-6006.
45. 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., et al. (2009). Cellular uptake mechanism and intracellular fate of hydrophobically modified glycol chitosan nanoparticles. J. Control. Release 135, 259-267.
46. Namgung, R., Singha, K., Yu, M. K., Jon, S., Kim, Y. S., Ahn, Y., Park, I. K., and Kim, W. J. (2010). Hybrid superparamagnetic iron oxide nanoparticlebranched polyethylenimine magnetoplexes for gene transfection of vascular endothelial cells. Biomaterials 31, 4204-4213.
47. Neri, M., Maderna, C., Cavazzin, C., Deidda-Vigoriti, V., Politi, L. S., Scotti, G., Marzola, P., Sbarbati, A., Vescovi, A. L., and Gritti, A. (2008). Efficient in vitro labeling of human neural precursor cells with superparamagnetic iron oxide particles: Relevance for in vivo cell tracking. Stem Cells 26, 505-516.
48. Pankhurst, Q. A., Connolly, J., Jones, S., and Dobson, J. (2003). Applications of magnetic nanoparticles in biomedicine. J. Phys. Appl. Phys. 36, R167.
49. Pawelczyk, E., Arbab, A. S., Pandit, S., Hu, E., and Frank, J. A. (2006). Expression of transferrin receptor and ferritin following ferumoxides-protamine sulfate labeling of cells: Implications for cellular magnetic resonance imaging. NMR Biomed. 19, 581-592.
50. Peng, X. H., Qian, X., Mao, H., Wang, A. Y., Chen, Z. G., Nie, S., and Shin, D. M. (2008). Targeted magnetic iron oxide nanoparticles for tumor imaging and therapy. Int. J. Nanomed. 3, 311-321.
51. Petri-Fink, A., Chastellain, M., Juillerat-Jeanneret, L., Ferrari, A., and Hofmann, H. (2005). Development of functionalized superparamagnetic iron oxide nanoparticles for interaction with human cancer cells. Biomaterials 26, 2685-2694.
52. Pisanic, T. R., 2nd, Blackwell, J. D., Shubayev, V. I., Fiñones, R. R., and Jin, S. (2007). Nanotoxicity of iron oxide nanoparticle internalization in growing neurons. Biomaterials 28, 2572-2581.
53. Rad, A. M., Janic, B., Iskander, A. S., Soltanian-Zadeh, H., and Arbab, A. S. (2007). Measurement of quantity of iron in magnetically labeled cells: Comparison among different UV/VIS spectrometric methods. BioTechniques 43, 627-636.
54. Richards, R. I., Heguy, A., and Karin, M. (1984). Structural and functional analysis of the human metallothionein-IA gene: Differential induction by metal ions and glucocorticoids. Cell 37, 263-272.
55. Richardson, D. R., and Ponka, P. (1997). The molecular mechanisms of the metabolism and transport of iron in normal and neoplastic cells. Biochim. Biophys. Acta 1331, 1-40.
56. Rodriguez, A., Hilvo, M., Kytömäki, L., Fleming, R. E., Britton, R. S., Bacon, B. R., and Parkkila, S. (2007). Effects of iron loading on muscle: Genomewide mRNA expression profiling in the mouse. BMC Genomics 8, 379.
57. Rouault, T. A. (2006). The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat. Chem. Biol. 2, 406-414.
58. Schafer, R., Bantleon, R., Kehlbach, R., Siegel, G., Wiskirchen, J., Wolburg, H., Kluba, T., Eibofner, F., Northoff, H., Claussen, C. D., et al. (2010). Functional investigations on human mesenchymal stem cells exposed to magnetic fields and labeled with clinically approved iron nanoparticles. BMC Cell Biol. 11, 22.
59. Schafer, R., Kehlbach, R., Wiskirchen, J., Bantleon, R., Pintaske, J., Brehm, B. R., Gerber, A., Wolburg, H., Claussen, C. D., and Northoff, H. (2007). Transferrin receptor upregulation: In vitro labeling of rat mesenchymal stem cells with superparamagnetic iron oxide. Radiology 244, 514-523.
60. Simen, A. A., Hirunsatit, R., George, E. D., Lipska, B. K., Elwafi, H. M., Sander, L., Yrigollen, C. M., Gelernter, J., Grigorenko, E. L., Lappalainen, J., et al. (2009). Twenty-one-base-pair insertion polymorphism creates an enhancer element and potentiates SLC6A1 GABA transporter promoter activity. Pharmacogenet. Genom. 19, 53-65.
61. Soenen, S. J., Himmelreich, U., Nuytten, N., and De Cuyper, M. (2011). Cytotoxic effects of iron oxide nanoparticles and implications for safety in cell labelling. Biomaterials 32, 195-205.
62. Strange, K., Emma, F., Paredes, A., and Morrison, R. (1994). Osmoregulatory changes in myo-inositol content and Na+/myo-inositol cotransport in rat cortical astrocytes. Glia 12, 35-43.
63. Sun, C., Lee, J. S., and Zhang, M. (2008). Magnetic nanoparticles in MR imaging and drug delivery. Adv. Drug Deliv. Rev. 60, 1252-1265.
64. Templeton, D. M., and Liu, Y. (2003). Genetic regulation of cell function in response to iron overload or chelation. Biochim. Biophys. Acta 1619, 113-124.
65. Theil, E. C., and Eisenstein, R. S. (2000). Combinatorial mRNA regulation: Iron regulatory proteins and iso-iron-responsive elements (Iso-IREs). J. Biol. Chem. 275, 40659-40662.
66. Thurston, J. H., Sherman, W. R., Hauhart, R. E., and Kloepper, R. F. (1989). Myo-inositol: A newly identified nonnitrogenous osmoregulatory molecule in mammalian brain. Pediatr. Res. 26, 482-485.
67. Valois, C. R., Braz, J. M., Nunes, E. S., Vinolo, M. A., Lima, E. C., Curi, R., Kuebler, W. M., and Azevedo, R. B. (2010). The effect of DMSAfunctionalized magnetic nanoparticles on transendothelial migration of monocytes in the murine lung via a beta2 integrin-dependent pathway. Biomaterials 31, 366-374.
68. Wallander, M. L., Leibold, E. A., and Eisenstein, R. S. (2006). Molecular control of vertebrate iron homeostasis by iron regulatory proteins. Biochim. Biophys. Acta 1763, 668-689.
69. Werner, T. (2008). Bioinformatics applications for pathway analysis of microarray data. Curr. Opin. Biotechnol. 19, 50-54.
70. Wilhelm, C., and Gazeau, F. (2008). Universal cell labelling with anionic magnetic nanoparticles. Biomaterials 29, 3161-3174.
71. Wilhelm, C., Lavialle, F., Péchoux, C., Tatischeff, I., and Gazeau, F. (2008). Intracellular trafficking of magnetic nanoparticles to design multifunctional biovesicles. Small 4, 577-582.
72. Wu, Y. N., Chen, D. H., Shi, X. Y., Lian, C. C., Wang, T. Y., Yeh, C. S., Ratinac, K. R., Thordarson, P., Braet, F., and Shieh, D. B. (2011). Cancer-cell-specific cytotoxicity of non-oxidized iron elements in iron core-gold shell NPs. Nanomedicine 7, 420-427.
73. Xia, Z., and Triffitt, J. T. (2006). A review on macrophage responses to biomaterials. Biomed. Mater. 1, R1-R9.
74. Xie, J., Huang, J., Li, X., Sun, S., and Chen, X. (2009). Iron oxide nanoparticle platform for biomedical applications. Curr. Med. Chem. 16, 1278-1294.
75. Yang, J., Goetz, D., Li, J. Y., Wang, W., Mori, K., Setlik, D., Du, T., Erdjument-Bromage, H., Tempst, P., Strong, R., et al. (2002). An iron delivery pathway mediated by a lipocalin. Mol. Cell 10, 1045-1056.
76. Yang, J., Mori, K., Li, J. Y., and Barasch, J. (2003). Iron, lipocalin, and kidney epithelia. Am. J. Physiol. Renal Physiol. 285, F9-18.
77. Yang, C. Y., Tai, M. F., Lin, C. P., Lu, C. W., Wang, J. L., Hsiao, J. K., and Liu, H. M. (2011). Mechanism of cellular uptake and impact of ferucarbotran on macrophage physiology. PLoS ONE 6, e25524.
78. Young, R. A. (2000). Biomedical discovery with DNA arrays. Cell 102, 9-15.
79. Zhang, S., Chen, X. J., Gu, C. R., Zhang, Y., Xu, J. D., Bian, Z. P., Yang, D., and Gu, N. (2009). The effect of iron oxide magnetic nanoparticles on smooth muscle cells. Nanoscale Res. Lett. 4, 70-77.
80. Zhu, M. T., Feng, W. Y., Wang, Y., Wang, B., Wang, M., Ouyang, H., Zhao, Y. L., and Chai, Z. F. (2009). Particokinetics and extrapulmonary translocation of intratracheally instilled ferric oxide nanoparticles in rats and the potential health risk assessment. Toxicol. Sci. 107, 342-351.
81. Ziegler, S., Röhrs, S., Tickenbrock, L., Langerak, A., Chu, S. T., Feldmann, I., Jakubowski, N., and Müller, O. (2007). Lipocalin 24p3 is regulated by the Wnt pathway independent of regulation by iron. Cancer Genet. Cytogenet. 174, 16-23.
82. Zoller, H., Koch, R. O., Theurl, I., Obrist, P., Pietrangelo, A., Montosi, G., Haile, D. J., Vogel, W., and Weiss, G. (2001). Expression of the duodenal iron transporters divalent-metal transporter 1 and ferroportin 1 in iron deficiency and iron overload. Gastroenterology 120, 1412-1419.