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Stem Cells International
Volume 2017 (2017), Article ID 4837503, 14 pages
https://doi.org/10.1155/2017/4837503
Research Article

Biological Characteristics of Fluorescent Superparamagnetic Iron Oxide Labeled Human Dental Pulp Stem Cells

1State Key Laboratory of Military Stomatology & National Clinical Research Center for Oral Diseases & Shaanxi Key Laboratory of Oral Diseases, Department of Operative Dentistry and Endodontics, The Fourth Military Medical University, Xi’an, China
2Department of Stomatology, No. 44 Hospital of Chinese PLA, Guiyang, Guizhou, China
3State Key Laboratory of Military Stomatology & National Clinical Research Center for Oral Diseases & Shaanxi Key Laboratory of Oral Diseases, Department of Preventive Dentistry, School of Stomatology, The Fourth Military Medical University, Xi’an, China

Correspondence should be addressed to Sheng-chao Wang; nc.ude.ummf@oahcgnehsgnaw and Qing Yu; nc.ude.ummf@gniquy

Received 20 August 2016; Revised 8 October 2016; Accepted 23 November 2016; Published 16 February 2017

Academic Editor: Marc L. Turner

Copyright © 2017 Liang Ma et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. Gronthos, M. Mankani, J. Brahim, P. G. Robey, and S. Shi, “Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 25, pp. 13625–13630, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. D. Ponnaiyan and V. Jegadeesan, “Comparison of phenotype and differentiation marker gene expression profiles in human dental pulp and bone marrow mesenchymal stem cells,” European Journal of Dentistry, vol. 8, no. 3, pp. 307–313, 2014. View at Publisher · View at Google Scholar
  3. Y. Isobe, N. Koyama, K. Nakao et al., “Comparison of human mesenchymal stem cells derived from bone marrow, synovial fluid, adult dental pulp, and exfoliated deciduous tooth pulp,” International Journal of Oral and Maxillofacial Surgery, vol. 45, no. 1, pp. 124–131, 2016. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Aurrekoetxea, P. Garcia-Gallastegui, I. Irastorza et al., “Dental pulp stem cells as a multifaceted tool for bioengineering and the regeneration of craniomaxillofacial tissues,” Frontiers in Physiology, vol. 6, article 289, 2015. View at Publisher · View at Google Scholar · View at Scopus
  5. W.-B. Shen, C. Plachez, A. Chan et al., “Human neural progenitor cells retain viability, phenotype, proliferation, and lineage differentiation when labeled with a novel iron oxide nanoparticle, Molday ION Rhodamine B,” International Journal of Nanomedicine, vol. 8, pp. 4593–4600, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. C. McFadden, C. L. Mallett, and P. J. Foster, “Labeling of multiple cell lines using a new iron oxide agent for cell tracking by MRI,” Contrast Media & Molecular Imaging, vol. 6, no. 6, pp. 514–522, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. R. Guzman, N. Uchida, T. M. Bliss et al., “Long-term monitoring of transplanted human neural stem cells in developmental and pathological contexts with MRI,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 24, pp. 10211–10216, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. N. Wang, J.-Y. Zhao, X. Guan et al., “Biological characteristics of adipose tissue-derived stem cells labeled with amine-surface-modified superparamagnetic iron oxide nanoparticles,” Cell Biology International, vol. 39, no. 8, pp. 899–909, 2015. View at Publisher · View at Google Scholar · View at Scopus
  9. K. Cheng, T.-S. Li, K. Malliaras, D. R. Davis, Y. Zhang, and E. Marbán, “Magnetic targeting enhances engraftment and functional benefit of iron-labeled cardiosphere-derived cells in myocardial infarction,” Circulation Research, vol. 106, no. 10, pp. 1570–1581, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Song, Y.-J. Kim, Y.-H. Kim, J. Roh, S. U. Kim, and B.-W. Yoon, “Using a neodymium magnet to target delivery of ferumoxide-labeled human neural stem cells in a rat model of focal cerebral ischemia,” Human Gene Therapy, vol. 21, no. 5, pp. 603–610, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. W. Jin, X. Yang, Z. Li et al., “Non-invasive tracking of CD4+ T cells with a paramagnetic and fluorescent nanoparticle in brain ischemia,” Journal of Cerebral Blood Flow & Metabolism, vol. 36, no. 8, pp. 1464–1476, 2016. View at Publisher · View at Google Scholar
  12. G. Zhang, Z. Na, B. Ren, X. Zhao, and W. Liu, “Impacts of fluorescent superparamagnetic iron oxide (SPIO)-labeled materials on biological characteristics and osteogenesis of bone marrow mesenchymal stem cells (BMSCs),” International Journal of Clinical and Experimental Medicine, vol. 8, no. 8, pp. 12172–12181, 2015. View at Google Scholar · View at Scopus
  13. T. He, Y. Wang, J. Xiang, and H. Zhang, “In vivo tracking of novel SPIO-molday ION rhodamine-B™-labeled human bone marrow-derived mesenchymal stem cells after lentivirus-mediated COX-2 silencing: a preliminary study,” Current Gene Therapy, vol. 14, no. 2, pp. 136–145, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. Z. Ren, J. Wang, C. Zou, Y. Guan, and Y. A. Zhang, “Labeling of cynomolgus monkey bone marrow-derived mesenchymal stem cells for cell tracking by multimodality imaging,” Science China Life Sciences, vol. 54, no. 11, pp. 981–987, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. B. Addicott, M. Willman, J. Rodriguez et al., “Mesenchymal stem cell labeling and in vitro MR characterization at 1.5 T of new SPIO contrast agent: molday ION rhodamine-B™,” Contrast Media and Molecular Imaging, vol. 6, no. 1, pp. 7–18, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. W.-D. Xiao, A.-X. Yu, and D.-L. Liu, “Fasudil hydrochloride could promote axonal growth through inhibiting the activity of ROCK,” International Journal of Clinical and Experimental Pathology, vol. 7, no. 9, pp. 5564–5568, 2014. View at Google Scholar · View at Scopus
  17. H.-H. Sun, B. Chen, Q.-L. Zhu et al., “Investigation of dental pulp stem cells isolated from discarded human teeth extracted due to aggressive periodontitis,” Biomaterials, vol. 35, no. 35, pp. 9459–9472, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. Z. Wang, L. Ding, S. Zhang, T. Jiang, Y. Yang, and R. Li, “Effects of icariin on the regulation of the OPG-RANKL-RANK system are mediated through the MAPK pathways in IL-1β-stimulated human SW1353 chondrosarcoma cells,” International Journal of Molecular Medicine, vol. 34, no. 6, pp. 1720–1726, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. B. Chen, H.-H. Sun, H.-G. Wang, H. Kong, F.-M. Chen, and Q. Yu, “The effects of human platelet lysate on dental pulp stem cells derived from impacted human third molars,” Biomaterials, vol. 33, no. 20, pp. 5023–5035, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. G. T.-J. Huang, T. Yamaza, L. D. Shea et al., “Stem/Progenitor cell-mediated de novo regeneration of dental pulp with newly deposited continuous layer of dentin in an in vivo model,” Tissue Engineering A, vol. 16, no. 2, pp. 605–615, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. S. G. Kim, Y. Zheng, J. Zhou et al., “Dentin and dental pulp regeneration by the patient's endogenous cells,” Endodontic Topics, vol. 28, no. 1, pp. 106–117, 2013. View at Publisher · View at Google Scholar
  22. J. J. Connell, P. S. Patrick, Y. Yu, M. F. Lythgoe, and T. L. Kalber, “Advanced cell therapies: targeting, tracking and actuation of cells with magnetic particles,” Regenerative Medicine, vol. 10, no. 6, pp. 757–772, 2015. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Gronthos, J. Brahim, W. Li et al., “Stem cell properties of human dental pulp stem cells,” Journal of Dental Research, vol. 81, no. 8, pp. 531–535, 2002. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Gandia, A. N. A. Armiñan, J. M. García-Verdugo et al., “Human dental pulp stem cells improve left ventricular function, induce angiogenesis, and reduce infarct size in rats with acute myocardial infarction,” Stem Cells, vol. 26, no. 3, pp. 638–645, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. A. S. Arbab, G. T. Yocum, L. B. Wilson et al., “Comparison of transfection agents in forming complexes with ferumoxides, cell labeling efficiency, and cellular viability,” Molecular Imaging, vol. 3, no. 1, pp. 24–32, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. A. K. Gupta and M. Gupta, “Cytotoxicity suppression and cellular uptake enhancement of surface modified magnetic nanoparticles,” Biomaterials, vol. 26, no. 13, pp. 1565–1573, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. J. A. Imlay, S. M. Chin, and S. Linn, “Toxic DNA damage by hydrogen peroxide through the fenton reaction in vivo and in vitro,” Science, vol. 240, no. 4852, pp. 640–642, 1988. View at Publisher · View at Google Scholar · View at Scopus
  28. N. Lewinski, V. Colvin, and R. Drezek, “Cytotoxicity of nanopartides,” Small, vol. 4, no. 1, pp. 26–49, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. M. A. Voinov, J. O. S. Pagán, E. Morrison, T. I. Smirnova, and A. I. Smirnov, “Surface-mediated production of hydroxyl radicals as a mechanism of iron oxide nanoparticle biotoxicity,” Journal of the American Chemical Society, vol. 133, no. 1, pp. 35–41, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. H. Nan, J. Huang, H. Li, Q. Li, and D. Liu, “Assessment of biological characteristics of adipose tissue-derived stem cells co-labeled with Molday ION Rhodamine B™ and green fluorescent protein in vitro,” Molecular Medicine Reports, vol. 8, no. 5, pp. 1446–1452, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. T. Struys, A. Ketkar-Atre, P. Gervois et al., “Magnetic resonance imaging of human dental pulp stem cells in vitro and in vivo,” Cell Transplantation, vol. 22, no. 10, pp. 1813–1829, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. D.-M. Huang, J.-K. Hsiao, Y.-C. Chen et al., “The promotion of human mesenchymal stem cell proliferation by superparamagnetic iron oxide nanoparticles,” Biomaterials, vol. 30, no. 22, pp. 3645–3651, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. O. Lunov, T. Syrovets, B. Büchele et al., “The effect of carboxydextran-coated superparamagnetic iron oxide nanoparticles on c-Jun N-terminal kinase-mediated apoptosis in human macrophages,” Biomaterials, vol. 31, no. 19, pp. 5063–5071, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. Q. Ran, Y. Xiang, Y. Liu et al., “Eryptosis indices as a novel predictive parameter for biocompatibility of Fe3O4 magnetic nanoparticles on erythrocytes,” Scientific Reports, vol. 5, Article ID 16209, 2015. View at Publisher · View at Google Scholar · View at Scopus
  35. S. J. H. Soenen, N. Nuytten, S. F. De Meyer, S. C. De Smedt, and M. De Cuyper, “High intracellular iron oxide nanoparticle concentrations affect cellular cytoskeleton and focal adhesion kinase-mediated signaling,” Small, vol. 6, no. 7, pp. 832–842, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. V. Temkin and M. Karin, “From death receptor to reactive oxygen species and c-Jun N-terminal protein kinase: the receptor-interacting protein 1 odyssey,” Immunological Reviews, vol. 220, pp. 8–21, 2007. View at Google Scholar
  37. A. Lin, “Activation of the JNK signaling pathway: breaking the brake on apoptosis,” BioEssays, vol. 25, no. 1, pp. 17–24, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. G. A. Dekaban, A. M. Hamilton, C. A. Fink et al., “Tracking and evaluation of dendritic cell migration by cellular magnetic resonance imaging,” Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology, vol. 5, no. 5, pp. 469–483, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. M. R. Loebinger, P. G. Kyrtatos, M. Turmaine et al., “Magnetic resonance imaging of mesenchymal stem cells homing to pulmonary metastases using biocompatible magnetic nanoparticles,” Cancer Research, vol. 69, no. 23, pp. 8862–8867, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. C. M. Long and J. W. M. Bulte, “In vivo tracking of cellular therapeutics using magnetic resonance imaging,” Expert Opinion on Biological Therapy, vol. 9, no. 3, pp. 293–306, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. C. Lalande, S. Miraux, S. M. Derkaoui et al., “Magnetic resonance imaging tracking of human adipose derived stromal cells within three-dimensional scaffolds for bone tissue engineering,” European Cells and Materials, vol. 21, pp. 341–354, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. J. V. Terrovitis, J. W. M. Bulte, S. Sarvananthan et al., “Magnetic resonance imaging of ferumoxide-labeled mesenchymal stem cells seeded on collagen scaffolds—relevance to tissue engineering,” Tissue Engineering, vol. 12, no. 10, pp. 2765–2775, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Matsuura, R. Utoh, K. Nagase, and T. Okano, “Cell sheet approach for tissue engineering and regenerative medicine,” Journal of Controlled Release, vol. 190, pp. 228–239, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Shimizu, M. Yamato, T. Akutsu et al., “Electrically communicating three-dimensional cardiac tissue mimic fabricated by layered cultured cardiomyocyte sheets,” Journal of Biomedical Materials Research, vol. 60, no. 1, pp. 110–117, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. K. Watanabe, M. Yamato, Y. Hayashida et al., “Development of transplantable genetically modified corneal epithelial cell sheets for gene therapy,” Biomaterials, vol. 28, no. 4, pp. 745–749, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. Z.-S. Wang, Z.-H. Feng, G.-F. Wu et al., “The use of platelet-rich fibrin combined with periodontal ligament and jaw bone mesenchymal stem cell sheets for periodontal tissue engineering,” Scientific Reports, vol. 6, Article ID 28126, 2016. View at Publisher · View at Google Scholar · View at Scopus