Cytotoxicity and non-specific cellular uptake of bare and surface-modified upconversion nanoparticles in human skin cells

Nano Research

Volumn 8, Issue 5, 2015, Pages 1546-1562

  Guller, Anna E ^a,b,d   Generalova, Alla N ^c,d   Petersen, Elena V ^e   Nechaev, Andrey V ^d,f   Trusova, Inna A ^e   Landyshev, Nikolay N ^e   Nadort, Annemarie ^a,g   Grebenik, Ekaterina A ^a,c,d   Deyev, Sergey M ^c,d   Shekhter, Anatoly B ^b   Zvyagin, Andrei V ^a,d  

^a MACQUARIE UNIVERSITY   (Australia)

^b I M SECHENOV FIRST MOSCOW STATE MEDICAL UNIVERSITY   (Russian Federation)

^c SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^d LOBACHEVSKY STATE UNIVERSITY OF NIZHNY NOVGOROD   (Russian Federation)

^e MOSCOW INSTITUTE OF PHYSICS AND TECHNOLOGY   (Russian Federation)

^f MIREA RUSSIAN TECHNOLOGICAL UNIVERSITY   (Russian Federation)

^g UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

biocompatibility; cytotoxicity; human skin; nanoparticle; surface modification; upconversion

Indexed keywords

EID: 84939945240     PISSN: 19980124     EISSN: 19980000     Source Type: Journal    
DOI: 10.1007/s12274-014-0641-6     Document Type: Article

References (60)

1. Hilderbrand, S. A.; Weissleder, R. Near-infrared fluorescence: Application to in vivo molecular imaging. Curr. Opin. Chem. Biol.2010, 14, 71–79.
2. Resch-Genger, U.; Grabolle, M.; Cavaliere-Jaricot, S.; Nitschke, R.; Nann, T. Quantum dots versus organic dyes as fluorescent labels. Nat. Methods2008, 5, 763–775.
3. 4:Yb,Er infrared-to-visible up-conversion phosphors. Nano Lett.2004, 4, 2191–2196.
4. Edmonds, A. M.; Sobhan, M. A.; Sreenivasan, V. K. A.; Grebenik, E. A.; Rabeau, J. R.; Goldys, E. M.; Zvyagin, A. V. Nano-ruby: A promising fluorescent probe for background-free cellular imaging. Part. Part. Syst. Charact.2013, 30, 506–513.
5. Lu, Y. Q.; Zhao, J. B.; Zhang, R.; Liu, Y. J.; Liu, D. M.; Goldys, E. M.; Yang, X. S.; Xi, P.; Sunna, A.; Lu, J. et al. Tunable lifetime multiplexing using luminescent nanocrystals. Nat. Photonics2013, 8, 32–36.
6. Sreenivasan, V. K. A.; Kelf, T. A.; Grebenik, E. A.; Stremovskiy, O. A.; Say, J. M.; Rabeau, J. R.; Zvyagin, A. V.; Deyev, S. M. A modular design of low-background bioassays based on a high-affinity molecular pair barstar: Barnase. Proteomics2013, 13, 1437–1443.
7. Maeda, H. Tumor-selective delivery of macromolecular drugs via the EPR effect: Background and future prospects. Bioconjugate Chem.2010, 21, 797–802.
8. Wang, F.; Liu, X. G. Recent advances in the chemistry of lanthanide-doped upconversion nanocrystals. Chem. Soc. Rev.2009, 38, 976–989.
9. 3+ doped fluoride nanophosphors. Nano Lett.2008, 8, 3834–3838.
10. 4 upconversion nanocrystals for sensitive bioimaging in vivo. J. Am. Chem. Soc.2011, 133, 17122–17125.
11. Morgan, C. G.; Dad, S.; Mitchell, A. C. Present status of, and future prospects for, upconverting phosphors in proximity-based bioassay. J. Alloys Compd.2008, 451, 526–529.
12. Wang, C.; Tao, H. Q.; Cheng, L.; Liu, Z. Near-infrared light induced in vivo photodynamic therapy of cancer based on upconversion nanoparticles. Biomaterials2011, 32, 6145–6154.
13. Min, Y. Z.; Li, J. M.; Liu, F.; Yeow, E. K. L.; Xing, B. G. Near-infrared light-mediated photoactivation of a platinum antitumor prodrug and simultaneous cellular apoptosis imaging by upconversion-luminescent nanoparticles. Angew. Chem. Int. Ed.2014, 53, 1012–1016.
14. Achatz, D. E.; Meier, R. J.; Fischer, L. H.; Wolfbeis, O. S. Luminescent sensing of oxygen using a quenchable probe and upconverting nanoparticles. Angew. Chem. Int. Ed.2011, 50, 260–263.
15. Chatterjee, D. K.; Gnanasammandhan, M. K.; Zhang, Y. Small upconverting fluorescent nanoparticles for biomedical applications. Small2010, 6, 2781–2795.
16. Zhou, J.; Liu, Z.; Li, F. Y. Upconversion nanophosphors for small-animal imaging. Chem. Soc. Rev.2012, 41, 1323–1349.
17. Haase, M.; Schäfer, H. Upconverting nanoparticles. Angew. Chem. Int. Ed.2011, 50, 5808–5829.
18. Chen, Y.; Ai, K. L.; Liu, Y. L.; Lu, L. H. Tailor-made charge-conversional nanocomposite for pH-responsive drug delivery and cell imaging. ACS Appl. Mater. Interfaces2014, 6, 655–663.
19. 5-based upconversion nanoparticles as drug carriers and multimodal imaging probes. Biomaterials2014, 35, 2011–2023.
20. Li, C. X.; Yang, D. M.; Ma, P. A.; Chen, Y. Y.; Wu, Y.; Hou, Z. Y.; Dai, Y. L.; Zhao, J. H.; Sui, C. P.; Lin, J. Multifunctional upconversion mesoporous silica nanostructures for dual modal imaging and in vivo drug delivery. Small2013, 9, 4150–4159.
21. Wang, C.; Cheng, L.; Liu, Z. Drug delivery with upconversion nanoparticles for multi-functional targeted cancer cell imaging and therapy. Biomaterials2011, 32, 1110–1120.
22. Das, G. K.; Stark, D. T.; Kennedy, I. M. Potential toxicity of up-converting nanoparticles encapsulated with a bilayer formed by ligand attraction. Langmuir2014, 30, 8167–8176.
23. Atabaev, T. Sh.; Lee, J. H.; Han, D. W.; Hwang, Y. H.; Kim, H. K. Cytotoxicity and cell imaging potentials of submicron color-tunable yttria particles. J. Biomed. Mater. Res. Part A2012, 100, 2287–2294.
24. Gao, G.; Zhang, C. L.; Zhou, Z. J.; Zhang, X.; Ma, J. B.; Li, C.; Jin, W. L.; Cui, D. X. One-pot hydrothermal synthesis of lanthanide ions doped one-dimensional upconversion submicrocrystals and their potential application in vivo CT imaging. Nanoscale2013, 5, 351–362.
25. Gupta, B. K.; Narayanan, T. N.; Vithayathil, S. A.; Lee, Y.; Koshy, S.; Reddy, A. L. M.; Saha, A.; Shanker, V.; Singh, V. N.; Kaipparettu, B. A. et al. Highly luminescent-paramagnetic nanophosphor probes for in vitro high-contrast imaging of human breast cancer cells. Small2012, 8, 3028–3034.
26. Guo, H. C.; Hao, R. Z.; Qian, H. S.; Sun, S. Q.; Sun, D. H.; Yin, H.; Liu, Z. X.; Liu, X. T. Upconversion nanoparticles modified with aminosilanes as carriers of DNA vaccine for foot-and-mouth disease. Appl. Microbiol. Biotechnol.2012, 95, 1253–1263.
27. 4 upconversion nanoparticles for in vitro cell imaging and drug delivery. Chem. Eur. J.2013, 19, 2685–2694.
28. Wang, C.; Cheng, L.; Xu, H.; Liu, Z. Towards whole-body imaging at the single cell level using ultra-sensitive stem cell labeling with oligo-arginine modified upconversion nanoparticles. Biomaterials2012, 33, 4872–4881.
29. 2 upconversion nanoparticles. Theranostics2013, 3, 249–257.
30. 4 upconversion fluorescent nanocrystals. Biomaterials2008, 29, 4122–4128.
31. Nadort, A.; Sreenivasan, V. K. A.; Song, Z.; Grebenik, E. A.; Nechaev, A. V.; Semchishen, V. A.; Panchenko, V. Y.; Zvyagin, A. V. Quantitative imaging of single upconversion nanoparticles in biological tissue. PloS One2013, 8, e63292.
32. Mahajan, S.; Aalinkeel, R.; Reynolds, J.; Nair, B.; Sykes, D.; Law, W. C.; Prasad, P.; Schwartz, S. Innovative nanotherapy for the treatment of the chronic skin condition, rosacea (P3259). J. Immunol.2013, 190, 192.
33. Chatterjee, D. K.; Rufaihah, A. J.; Zhang, Y. Upconversion fluorescence imaging of cells and small animals using lanthanide doped nanocrystals. Biomaterials2008, 29, 937–943.
34. 4-based upconversion nanophosphors for trimodality imaging of nir-to-nir upconversion luminescence, X-ray computed tomography and magnetic resonance. Biomaterials2012, 33, 5394–5405.
35. 2 nanoprobes for targeting dual-modality imaging of upconversion luminescence and X-ray computed tomography. J. Phys. Chem. B2012, 116, 14062–14070.
36. 4:Yb,Er nanocrystals by a surfactant-assistant two-phase system. Nanoscale Res. Lett.2013, 8, 518.
37. Grebenik, E. A.; Nadort, A.; Generalova, A. N.; Nechaev, A. V.; Sreenivasan, V. K.; Khaydukov, E. V.; Semchishen, V. A.; Popov, A. P.; Sokolov, V. I.; Akhmanov, A. S. et al. Feasibility study of the optical imaging of a breast cancer lesion labeled with upconversion nanoparticle biocomplexes. J. Biomed. Opt.2013, 18, 076004.
38. Andrade, Â. L.; Fabris, J. D.; Ardisson, J. D.; Valente, M. A.; Ferreira, J. M. F. Effect of tetramethylammonium hydroxide on nucleation, surface modification and growth of magnetic nanoparticles. J. Nanomater.2012, 2012, 1–10.
39. Generalova, A. N.; Kochneva, I. K.; Khaydukov, E. V.; Semchishen, V. A.; Guller, A. E.; Nechaev, A. V.; Shekhter, A. B.; Zubov, V. P.; Zvyagin, A. V.; Deyev, S. M. Submicron polyacrolein particles in situ embedded with upconversion nanoparticles for bioassay. Nanoscale2014, DOI: 10.1039/c4nr05908e.
40. Li, M.; Rouaud, O.; Poncelet, D. Microencapsulation by solvent evaporation: State of the art for process engineering approaches. Int. J. Pharm.2008, 363, 26–39.
41. Bao, Y.; Luu, Q. A. N.; Lin, C. K.; Schloss, J. M.; May, P. S.; Jiang, C. Y. Layer-by-layer assembly of freestanding thin films with homogeneously distributed upconversion nanocrystals. J. Mater. Chem.2010, 20, 8356–8361.
42. Generalova, A. N.; Oleinikov, V. A.; Zarifullina, M. M.; Lankina, E. V.; Sizova, S. V.; Artemyev, M. V.; Zubov, V. P. Optical sensing quantum dot-labeled polyacrolein particles prepared by layer-by-layer deposition technique. J. Colloid Interface Sci.2011, 357, 265–272.
43. Boukamp, P.; Petrussevska, R. T.; Breitkreutz, D.; Hornung, J.; Markham, A.; Fusenig, N. E. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol.1988, 106, 761–771.
44. Breitkreutz, D.; Schoop, V. M.; Mirancea, N.; Baur, M.; Stark, H. J.; Fusenig, N. E. Epidermal differentiation and basement membrane formation by hacat cells in surface transplants. Eur. J. Cell Biol.1998, 75, 273–286.
45. Takashima A. Establishment of fibroblast cultures. Curr. Protoc. Cell Biol.2001, Chapter 2: Unit 2.1. DOI: 10.1002/0471143030.cb0201s00.
46. Mosmann, T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods1983, 65, 55–63.
47. Cao, T. Y.; Yang, Y.; Gao, Y.; Zhou, J.; Li, Z. Q.; Li, F. Y. High-quality water-soluble and surface-functionalized upconversion nanocrystals as luminescent probes for bioimaging. Biomaterials2011, 32, 2959–2968.
48. Chen, Z. G.; Chen, H. L.; Hu, H.; Yu, M. X.; Li, F. Y.; Zhang, Q.; Zhou, Z. G.; Yi, T.; Huang, C. H. Versatile synthesis strategy for carboxylic acid-functionalized upconverting nanophosphors as biological labels. J. Am. Chem. Soc.2008, 130, 3023–3029.
49. Bogdan, N.; Vetrone, F.; Ozin, G. A.; Capobianco, J. A. Synthesis of ligand-free colloidally stable water dispersible brightly luminescent lanthanide-doped upconverting nanoparticles. Nano Lett.2011, 11, 835–840.
50. Bumajdad, A.; Eastoe, J.; Zaki, M. I.; Heenan, R. K.; Pasupulety, L. Generation of metal oxide nanoparticles in optimised microemulsions. J. Colloid Interface Sci.2007, 312, 68–75.
51. Pellegrino, T.; Manna, L.; Kudera, S.; Liedl, T.; Koktysh, D.; Rogach, A. L.; Keller, S.; Rädler, J.; Natile, G.; Parak, W. J. Hydrophobic nanocrystals coated with an amphiphilic polymer shell: A general route to water soluble nanocrystals. Nano Lett.2004, 4, 703–707.
52. 3+ upconversion nanoparticles for charge-dependent cellular imaging. ACS Nano2011, 5, 7838–7847.
53. Sheftel, V. O.; Kataeva, S. E. Migration of Harmful Chemicals from Polymeric Materials. Khimiya: Moscow, 1978.
54. Forrest, M. L.; Koerber, J. T.; Pack, D. W. A degradable polyethylenimine derivative with low toxicity for highly efficient gene delivery. Bioconjugate Chem.2003, 14, 934–940.
55. Tiyaboonchai, W.; Woiszwillo, J.; Middaugh, C. R. Formulation and characterization of DNA-polyethylenimine-dextran sulfate nanoparticles. Eur. J. Pharm. Sci.2003, 19, 191–202.
56. Chen, G. Y.; Qiu, H. L.; Prasad, P. N.; Chen, X. Y. Upconversion nanoparticles: Design, nanochemistry, and applications in theranostics. Chem. Rev.2014, 114, 5161–5214.
57. Müller, R. H.; Maaßen, S.; Weyhers, H.; Specht, F.; Lucks, J. S. Cytotoxicity of magnetite-loaded polylactide, polylactide/glycolide particles and solid lipid nanoparticles. Int. J. Pharm.1996, 138, 85–94.
58. Pham, Q. P.; Sharma, U.; Mikos, A. G. Electrospinning of polymeric nanofibers for tissue engineering applications: A review. Tissue Eng.2006, 12, 1197–1211.
59. Ogawara, K. I.; Yoshida, M.; Takakura, Y.; Hashida, M.; Higaki, K.; Kimura, T. Interaction of polystyrene microspheres with liver cells: Roles of membrane receptors and serum proteins. Biochim. Biophys. Acta1999, 1472, 165–172.
60. Kelf, T. A.; Sreenivasan, V. K. A.; Sun, J.; Kim, E. J.; Goldys, E. M.; Zvyagin, A. V. Non-specific cellular uptake of surface-functionalized quantum dots. Nanotechnology2010, 21, 285105.