Effects of iron oxide nanoparticle labeling on human endothelial cells

Cell Transplantation

Volumn 21, Issue 9, 2012, Pages 1805-1820

  Yang, Fu Yuan ^a   Yu, Ming Xi ^a   Zhou, Quan ^b   Chen, Wen Li ^a   Gao, Peng ^b   Huang, Zheng ^c  

^a SOUTH CHINA NORMAL UNIVERSITY   (China)

^b JINAN UNIVERSITY   (China)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

Cell labeling; Cell tracking; Iron oxide nanoparticles (INOPS); Magnetic resonance imaging (MRI)

Indexed keywords

CONTRAST MEDIUM; IRON OXIDE NANOPARTICLE; POLYLYSINE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; AUTOLYSOSOME; AUTOPHAGY; CELL LABELING; CELL PROLIFERATION; CELL VACUOLE; CELL VIABILITY; CONTROLLED STUDY; CYTOPLASM; ENDOTHELIUM CELL; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL;

CELL DIFFERENTIATION; CELLS, CULTURED; CONTRAST MEDIA; ENDOTHELIAL CELLS; FERRIC COMPOUNDS; HUMANS; LYSINE; MAGNETITE NANOPARTICLES; MICROSCOPY, ELECTRON, TRANSMISSION; NANOPARTICLES;

EID: 84869765389     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368912X652986     Document Type: Article

References (67)

1. Arbab, A. S.; Frank, J. A. Cellular MRI and its role 1. in stem cell therapy. Regen. Med. 3(2):199-215; 2009.
2. Arbab, A. S.; Liu, W.; Frank, J. A. Cellular magnetic resonance imaging: Current status and future prospects. Expert Rev. Med. Devices 3(4):427-439; 2006.
3. Arbab, A. S.; Wilson, L. B.; Ashari, P.; Jordan, E. K.; Lewis, B. K.; Frank, J. A. A model of lysosomal metabolism of dextran coated superparamagnetic iron oxide (SPIO) nanoparticles: Implications for cellular magnetic resonance imaging. NMR Biomed. 18(6):383-389; 2005.
4. Arbab, A. S.; Yocum, G. T.; Kalish, H.; Jordan, E. K; Anderson, S. A.; Khakoo, A. Y.; Read, E. J; Frank, J. A. Efficient magnetic cell labeling with protamine sulfate complexed to ferumoxides for cellular MRI. Blood 104(4):1217-1223; 2004.
5. Bailey, A. S.; Jiang, S.; Afentoulis, M.; Baumann, C. I.; Schroeder, D. A.; Olson, S. B.; Wong, M. H.; Fleming, W. H. Transplanted adult hematopoietic stem cells differentiate into functional endothelial cells. Blood 103(1):13-19; 2004.
6. Baklanov, D. V.; Demuinck, E. D.; Thompson, C. A.; Pearlman, J. D. Novel double contrast MRI technique for intramyocardial detection of percutaneously transplanted autologous cells. Magn. Reson. Med. 52(6):1438-1442; 2004.
7. Baysan, A.; Yel, L.; Gollapudi, S.; Su, H.; Gupta, S. Arsenic trioxide induces apoptosis via the mitochondrial pathway by upregulating the expression of Bax and Bim in human B cells. Int. J. Oncol. 30(2):313-318; 2007.
8. Beer, A. J.; Holzapfel, K.; Neudorfer, J.; Piontek, G.; Settles, M.; Krönig, H.; Peschel, C.; Schlegel, J.; Rummeny, E. J.; Bernhard, H. Visualization of antigenspecific human cytotoxic T lymphocytes labeled with superparamagnetic iron-oxide particles. Eur. Radiol. 18(6):1087-1095; 2008.
9. Bowen, C. V.; Zhang, X.; Saab, G.; Gareau, P. J.; Rutt, B. K. Application of the static dephasing regime theory to superparamagnetic iron-oxide loaded cells. Magn. Reson. Med. 48(1):52-61; 2002.
10. Bulte, J. W.; Arbab, A. S.; Douglas. T.; Frank., J. A. Preparation of magnetically labeled cells for cell tracking by magnetic resonance imaging. Methods Enzymol. 386:275-299; 2004.
11. Bulte, J. W.; Douglas, T.; Witwer, B.; Zhang, S. C.; Strable, E.; Lewis, B. K.; Zywicke, H.; Miller, B.; van Gelderen, P.; Moskowitz, B. M.; Duncan, I. D.; Frank, J. A. Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nat. Biotechnol. 19(12):1141-1147; 2001.
12. Bulte, J. W.; Kraitchman, D. L. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed. 17(7):484-499; 2004.
13. Byun, J. Y.; Yoon, C. H.; An, S.; Park, I. C.; Kang, C. M.; Kim, M. J.; Lee, S. J. The Rac1/MKK7/JNK pathway signals upregulation of Atg5 and subsequent autophagic cell death in response to oncogenic Ras. Carcinogenesis 30(11):1880-1888; 2009.
14. Chen, M. J.; Xing, D.; Chen, T.; Zhang, L. BimL involvement in Bax activation during UV irradiation-induced apoptosis. Biochem. Biophys. Res. Commun. 358(4):559-565; 2007.
15. Chen, R.; Yu, H.; Jia, Z. Y.; Yao, Q. L.; Teng, G. J. Efficient nano iron particle-labeling and noninvasive MR imaging of mouse bone marrow-derived endothelial progenitor cells. Int. J. Nanomedicine 6:511-519; 2011.
16. Corot, C.; Robert, P.; Idée, J. M.; Port, M. Recent advances in iron oxide nanocrystal technology for medical imaging. Adv. Drug Deliv. Rev. 58(14):1471-1504; 2006.
17. Delcroix, Jr., G.; Jacquart, M.; Lemaire, L.; Sindji, L.; Franconi, F.; Jeune, J. J.; Montero-Menei, C. N. Mesenchymal and neural stem cells labeled with HEDP-coated SPIO nanoparticles: In vitro characterization and migration potential in rat. Brain Res. 1255(2):18-31; 2009.
18. Dimmeler, S.; Zeiher, A. M. Vascular repair by circulating endothelial progenitor cells: The missing link in atherosclerosis. J. Mol. Med. 82(10):671-677; 2004.
19. Frangioni, J. V.; Hajjar, R. J. In vivo tracking of stem cells for clinical trials in cardiovascular disease. Circulation. 110(21):3378-3383; 2004.
20. Frank, J. A.; Miller, B. R.; Arbab, A. S.; Zywicke, H. A.; Jordan, E. K.; Lewis, B. K.; Bryant, L. H.; Bulte, J. W. Clinically applicable labeling of mammalian and stem cells by combining superparamagnetic iron oxides and transfection agents. Radiology 228(2):480-487; 2003.
21. 3 particles-induced lung tissue injury: Role of free radicals. Cancer Lett. 167(1):7-15; 2001.
22. Gupta, A. K.; Gupta, M. Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 26(18):3995-4021; 2005.
23. Hill, J. M.; Dick, A. J.; Raman, V. K.; Thompson, R. B.; Yu, Z. X.; Hinds, K. A.; Pessanha, B. S.; Guttman, M. A.; Varney, T. R.; Martin, B. J.; Dunbar, C. E.; McVeigh, E. R.; Lederman, R. J. Serial cardiac magnetic resonance imaging of injected mesenchymal stem cells. Circulation 108(8):1009-1014; 2003.
24. Huang, X.; Zhai, D.; Huang, Y. Study on the relationship between calcium-induced calcium release from mitochondria and PTP opening. Mol. Cell. Biochem. 213(1-2): 29-35; 2000.
25. Jasmin,; Torres, A. L.; Nunes, H. M.; Passipieri, J. A.; Jelicks, L. A.; Gasparetto, E. L.; Spray, D. C.; Campos de Carvalho, A. C.; Mendez-Otero, R. Optimized labeling of bone marrow mesenchymal cells with superparamagnetic iron oxide nanoparticles and in vivo visualization by magnetic resonance imaging. J. Nanobiotechnology 9(1):4; 2011.
26. Jing, X. H.; Yang, L.; Duan, X. J.; Xie, B.; Chen, W.; Li, Z.; Tan, H. B. In vivo MR imaging tracking of magnetic iron oxide nanoparticle labeled, engineered, autologous bone marrow mesenchymal stem cells following intra-articular injection. Joint Bone Spine 75(4):432-438; 2008.
27. Josephson, L.; Tung, C. H.; Moore, A.; Weissleder, R. High efficiency intracellular magnetic labeling with novel superparamagnetic-tat peptide conjugates. Bioconjug. Chem. 10(2):186-191; 1999.
28. Ju, S.; Teng, G.; Zhang, Y.; Ma, M.; Chen, F.; Ni, Y. In vitro labeling and MRI of mesenchymal stem cells from human umbilical cord blood. Magn. Reson. Imaging 24(5):611-617; 2006.
29. Keaney, J. F. Atherosclerosis: From lesion formation to plaque activation and endothelial dysfunction. Mol. Aspects Med. 21(4-5):99-166; 2000.
30. J.; Lee, S. J.; Choi, K. S. Sodium selenite induces superoxide-mediated mitochondrial damage and subsequent autophagic cell death in malignant glioma cells. Cancer Res. 67(13):6314-6324; 2007.
31. Lewinski, N.; Colvin, V.; Drezek, R. Cytotoxicity of nanoparticles. Small 4(1):26-49; 2008.
32. Li, J. J.; Hartono, D.; Ong, C. N.; Bay, B. H.; Yung, L. Y. Autophagy and oxidative stress associated with gold nanoparticles. Biomaterials 31(23):5996-6003; 2010.
33. Lindholm, D.; Eriksson, O.; Korhonen, L. Mitochondrial proteins in neuronal degeneration. Biochem. Biophys. Res. Commun. 321(4):753-758; 2004.
34. Liu, L.; Xing, D.; Chen, W. R. l-Calpain regulates caspase-dependent and apoptosis inducing factor-mediated caspase-independent apoptotic pathways in cisplatin-induced apoptosis. Int. J. Cancer 125(12):2757-2766; 2009.
35. Liu, W.; Frank, J. A. Detection and quantification of magnetically labeled cells by cellular MRI. Eur. J. Radiol. 70(2):258-264; 2009.
36. Ma, Z. L.; Mai, X. L.; Sun, J. H.; Ju, S. H.; Yang, X.; Ni, Y.; Teng, G. J. Inhibited atherosclerotic plaque formation by local administration of magnetically labeled endothelial progenitor cells (EPCs) in a rabbit model. Atherosclerosis 205(1):80-86; 2009.
37. Mai, X. L.; Ma, Z. L.; Sun, J. H.; Ju, S. H.; Ma, M.; Teng, G. J.; Assessments of proliferation capacity and viability of New Zealand rabbit peripheral blood Eendothelial progenitor cells labeled with superparamagnetic particles. Cell Transplant. 18(2):171-181; 2009.
38. 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 235(1):155-161; 2005.
39. 2 agents. Magn. Reson. Med. 57(2):442-447; 2007.
40. Modo, M.; Hoehn, M.; Bulte, J. W. Cellular MR imaging. Mol. Imaging 4(3):143-164; 2005.
41. Muldoon, L. L.; Sàndor, M.; Pinkston, K. E.; Neuwelt, E. A. Imaging, distribution and toxicity of superparamagnetic iron oxide magnetic resonance nanoparticles in the rat brain and intra cerebral tumor. Neurosurgery 57(4):785-796; 2005.
42. Nakamura, T.; Sakamoto, K. Reactive oxygen species up-regulates cyclooxygenase-2, p53, and Bax mRNA expression in bovine luteal cells. Biochem. Biophys. Res. Commun. 284(1):203-210; 2001.
43. Neri, M.; Maderna, C.; Cavazzin, C.; Deidda-Vigoriti, V.; Politi, L. S.; Scotti, G.; Marzola, P.; Sbarbati, A.; Vescovi, A. L.; Gritti, A. efficient in vitro labeling of human neural precursor cells with superparamagnetic iron oxide particles: Relevance for in vivo cell tracking. Stem Cells 26(2):505-516; 2008.
44. Nie, L.; Ou, Z.; Yang, S.; Xing, D. Thermoacoustic molecular tomography with magnetic nanoparticle contrast agents for targeted tumor detection. Med. Phys. 37(8):4193-200; 2010.
45. Oude Engberink, R. D.; Blezer, E. L.; Hoff, E. I.; van der Pol, S. M.; van der Toorn, A.; Dijkhuizen, R. M.; de Vries, H. E. MRI of monocyte infiltration in an animal model of neuroinflammation using SPIO-labeled monocytes or free USPIO. J. Cereb. Blood Flow Metab. 28(11):841-851; 2008.
46. Oude Engberink, R. D.; van der Pol, S. M.; Döpp, E. A.; de Vries, H. E.; Blezer, E. L. Comparison of SPIO and USPIO for in vitro labeling of human monocytes: MR detection and cell function. Radiology 243(2):467-474; 2007.
47. Park, K. J.; Lee, S. H.; Kim, T. I.; Lee, H. W.; Lee, C. H.; Kim, E. H.; Jang, J. Y.; Choi, K. S.; Kwon, M. H.; Kim, Y. S. A human scFv antibody against TRAIL receptor 2 induces autophagic cell death in both TRAIL-sensitive and TRAIL-resistant cancer cells. Cancer Res. 67(15):7327-7334; 2007.
48. Pyo, J. O.; Jang, M. H.; Kwon, Y. K.; Lee, H. J.; Jun, J. I.; Woo, H. N.; Cho, D. H.; Choi, B.; Lee, H.; Kim, J. H.; Mizushima, N.; Oshumi, Y.; Jung, Y. K. Essential roles of Atg5 and FADD in autophagic cell death: Dissection of autophagic cell death into vacuole formation and cell death. J. Biol. Chem. 280(21):20722-20729; 2005.
49. Rice, H. E.; Hsu, E. W.; Sheng, H.; Evenson, D. A.; Freemerman, A. J.; Safford, K. M.; Provenzale, J. M.; Warner, D. S.; Johnson, G. A. Superparamagnetic iron oxide labeling and transplantation of adipose-derived stem cells in middle cerebral artery occlusion-injured mice. AJR. Am. J. Roentgenol. 188(4):1101-1108; 2007.
50. Sales, K. M.; Salacinski, H. J.; Alobaid, N.; Mikhail, M.; Balakrishnan, V.; Seifalian, A. M. Advancing vascular tissue engineering: The role of stem cell technology. Trends Biotechnol. 23(9):461-467; 2005.
51. Santra, S.; Kaittanis, C.; Grimm, J.; Perez, J. M. Drug/dyeloaded, multifunctional iron oxide nanoparticles for combined targeted cancer therapy and dual optical/magnetic resonance imaging. Small 5(16):1862-1868; 2009.
52. Schäfer, R.; Kehlbach, R.; Wiskirchen, J.; Bantleon, R.; Pintaske, J.; Brehm, B. R.; Gerber, A.; Wolburg, H.; Claussen, C. D.; Northoff, H. transferrin receptor upregulation: In vitro labeling of rat mesenchymal stem cells with superparamagnetic iron oxide. Radiology 244(2):514-523; 2007.
53. Schmidt-Lucke, C.; Rössig, L.; Fichtlscherer, S.; Vasa, M.; Britten, M.; Kämper, U.; Dimmeler, S.; Zeiher, A. M. Reduced number of circulating endothelial progenitor cells predicts future cardiovascular events: proof of concept for the clinical importance of endogenous vascular repair. Circulation 111(22):2981-2987; 2005.
54. So, P. W.; Kalber, T.; Hunt, D.; Farquharson, M.; Al-Ebraheem, A.; Parkes, H. G.; Simon, R.; Bell, J. D. Efficient and rapid labeling of transplanted cell populations with superparamagnetic iron oxide nanoparticles using cell surface chemical biotinylation for in vivo monitoring by MRI. Cell Transplant. 19(4):419-429; 2010.
55. Soenen, S. J.; De Meyer, S. F.; Dresselaers, T.; Vande Velde, G.; Pareyn, I. M.; Braeckmans, K.; De Cuyper, M.; Himmelreich, U.; Vanhoorelbeke, K. I. MRI assessment of blood outgrowth endothelial cell homing using cationic magnetoliposomes. Biomaterials 32(17):4140-4150; 2011.
56. Soenen, S. J.; Himmelreich, U.; Nuytten, N.; De Cuyper, M. Cytotoxic effects of iron oxide nanoparticles and implications for safety in cell labelling. Biomaterials 32(1):195-205; 2011.
57. Tiwari, A.; Punshon, G.; Kidane, A.; Hamilton, G.; Seifalian, A. M. Magnetic beads (Dynabead) toxicity to endothelial cells at high bead concentration: implication for tissue engineering of vascular prosthesis. Cell Biol. Toxicol. 19(5):265-272; 2003.
58. Wang, Y. X.; Hussain, S. M.; Krestin, G. P. Superparamagnetic iron oxide contrast agents: physcochemical characteristics and applications in MR imaging. Eur. Radiol. 11(11):2319-2331; 2001.
59. Wilhelm, C.; Bal, L.; Smirnov, P.; Galy-Fauroux, I.; Clément, O.; Gazeau, F.; Emmerich, J. Magnetic control of vascular network formation with magnetically labeled endothelial progenitor cells. Biomaterials 28(26):3797-3806; 2007.
60. Wu, S.; Xing, D.; Wang, F.; Chen, T.; Chen, W. R. Mechanistic study of apoptosis induced by high-fluence low-power laser irradiation using fluorescence imaging techniques. J. Biomed. Opt. 12(6):4015-4025; 2007.
61. Wu, S.; Zhou, F.; Zhang, Z.; Xing, D. Bax is essential for Drp1-mediated mitochondrial fission but not for mitochondrial outer membrane permeabilization caused by photodynamic therapy. J. Cell. Physiol. 226(2):530-541; 2011.
62. Wu, Y.; Xing, D.; Chen, W. R.; Wang, X. Bid is not required for Bax translocation during UV-induced apoptosis. Cell. Signal. 19(12):2468-2478; 2007.
63. Xu, Y. N.; Cui, X. S.; Sun, S. C.; Lee, S. E.; Li, Y. H.; Kwon, J. S.; Lee, S. H.; Hwang, K. C.; Kim, N. H. mitochondrial dysfunction influences apoptosis and autophagy in porcine parthenotes developing in vitro. J. Reprod. Dev. 57(1):143-150; 2011.
64. Yu, M. X.; Chen, W. L.; Zhou, Q.; Gao, P. Study on ASTCa-1 cells labeled with superparamagnetic iron oxide and its magnetic resonance imaging. Exp. Biol. Med. 235(9):1053-1061; 2010.
65. Zhou, F.; Xing, D.; Chen, W. R. Dynamics and mechanism of HSP70 translocation induced by photodynamic therapy treatment. Cancer Lett. 264(1):135-144; 2008.
66. Zhou, F.; Xing, D.; Wu, B.; Wu, S.; Ou, Z.; Chen, W. R. New insights of transmembranal mechanism and subcellular localization of noncovalently modified single-walled carbon nanotubes. Nano Lett. 10(5):1677-1681; 2010.
67. Zhou, L. J.; Zhu, X. Z. Reactive oxygen species-induced apoptosis in PC12 cells and protective effect of bilobalide. J. Pharmacol. Exp. Ther. 293(3):982-988; 2000.