Boron Nitride Nanoparticles with a Petal-Like Surface as Anticancer Drug-Delivery Systems

ACS Applied Materials and Interfaces

Volumn 7, Issue 31, 2015, Pages 17217-17225

  Sukhorukova, Irina V ^a   Zhitnyak, Irina Y ^b   Kovalskii, Andrey M ^a   Matveev, Andrei T ^a   Lebedev, Oleg I ^c   Li, Xia ^d   Gloushankova, Natalia A ^b   Golberg, Dmitri ^d   Shtansky, Dmitry V ^a  

^a NATIONAL UNIVERSITY OF SCIENCE AND TECHNOLOGY MISIS   (Russian Federation)

^b N N BLOKHIN RUSSIAN CANCER RESEARCH CENTER   (Russian Federation)

^c UNIVERSITÉ DE CAEN   (France)

^d NATIONAL INSTITUTE FOR MATERIALS SCIENCE   (Japan)

Author keywords

BN nanoparticles; chemical vapor deposition; doxorubicin; drug release; drug delivery nanocarriers; neoplastic cells

Indexed keywords

ASSAYS; BORON NITRIDE; CELL DEATH; CHEMICAL VAPOR DEPOSITION; CYTOLOGY; DEPOSITION; DRUG PRODUCTS; NANOPARTICLES; NITRIDES; TUMORS; VAPOR DEPOSITION;

ANTI-CANCER DRUG DELIVERY; DOXORUBICIN; DRUG DELIVERY CARRIER; DRUG RELEASE; ENDOCYTIC PATHWAYS; NANO-CARRIERS; NEOPLASTIC CELLS; NITRIDE NANOPARTICLES;

CELLS;

ANTINEOPLASTIC AGENT; BORON DERIVATIVE; BORON NITRIDE; DOXORUBICIN; DRUG CARRIER; NANOPARTICLE;

CELL SURVIVAL; CHEMISTRY; CONFOCAL MICROSCOPY; DRUG EFFECTS; DRUG RELEASE; HUMAN; INFRARED SPECTROSCOPY; PH; SURFACE PROPERTY; TUMOR CELL LINE; ULTRASTRUCTURE;

ANTINEOPLASTIC AGENTS; BORON COMPOUNDS; CELL LINE, TUMOR; CELL SURVIVAL; DOXORUBICIN; DRUG CARRIERS; DRUG LIBERATION; HUMANS; HYDROGEN-ION CONCENTRATION; MICROSCOPY, CONFOCAL; NANOPARTICLES; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SURFACE PROPERTIES;

EID: 84939124892     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.5b04101     Document Type: Article

References (54)

1. Zhang, L.; Gu, F. X.; Chan, J. M.; Wang, A. Z.; Langer, R. S.; Farokhzad, O. C. Nanoparticles in Medicine: Therapeutic Applications and Developments Clin. Pharmacol. Ther. 2008, 83, 761-769 10.1038/sj.clpt.6100400
2. Fukumori, Y.; Ichikawa, H. Nanoparticles for Cancer Therapy and Diagnosis Adv. Powder Technol. 2006, 17, 1-28 10.1163/156855206775123494
3. Kane, S. E. Multidrug Resistance of Cancer Cells Adv. Drug Res. 1996, 28, 181-252 10.1016/S0065-2490(96)80005-0
4. Bolhuis, H.; van Veen, H. W.; Poolman, B.; Driessen, A. J. M.; Konings, W. N. Mechanism of Multidrug Transporters FEMS Microbiol. Rev. 1997, 21, 55-84 10.1111/j.1574-6976.1997.tb00345.x
5. Soma, C. E.; Dubernet, C.; Barratt, G.; Nemati, F.; Appel, M.; Benita, S.; Couvreur, P. Ability of Doxorubicin-loaded Nanoparticles to Overcome Multidrug Resistance of Tumor Cells After Their Capture by Macrophages Pharm. Res. 1999, 16, 1710-1716 10.1023/A:1018902031370
6. Wang, F.; Wang, Y. C.; Dou, S.; Xiong, M. H.; Sun, T. M.; Wang, J. Doxorubicin-tethered Responsive Gold Nanoparticles Facilitate Intracellular Drug Delivery for Overcoming Multidrug Resistance in Cancer Cells ACS Nano 2011, 5, 3679-3692 10.1021/nn200007z
7. Kievit, F. M.; Wang, F. Y.; Fang, C.; Mok, H.; Wang, K.; Silber, J. R.; Ellenbogen, R. G.; Zhang, M. Doxorubicin Loaded Iron Oxide Nanoparticles Overcome Multidrug Resistance in Cancer in Vitro J. Controlled Release 2011, 152, 76-83 10.1016/j.jconrel.2011.01.024
8. Park, J.; Fong, P. M.; Lu, J.; Russell, K. S.; Booth, C. J.; Saltzman, W. M.; Fahmy, T. M. PEGylated PLGA Nanoparticles for the Improved Delivery of Doxorubicin Nanomedicine 2009, 5, 410-418 10.1016/j.nano.2009.02.002
9. Kang, K. W.; Chun, M. K.; Kim, O.; Subedi, R. K.; Ahn, S. G.; Yoon, J. H.; Choi, H. K. Doxorubicin-loaded Solid Lipid Nanoparticles to Overcome Multidrug Resistance in Cancer Therapy Nanomedicine 2010, 6, 210-213 10.1016/j.nano.2009.12.006
10. Soma, C. E.; Dubernet, C.; Barratt, G.; Benita, S.; Couvreur, P. Investigation of the Role of Macrophages on the Cytotoxicity of Doxorubicin and Doxorubicin-loaded Nanoparticles on M5076 Cells in Vitro J. Controlled Release 2000, 68, 283-289 10.1016/S0168-3659(00)00269-8
11. Chiannilkulchai, N.; Driouich, Z.; Benoit, J. P.; Parodi, A. L.; Couvreur, P. Doxorubicin-loaded Nanoparticles: Increased Efficiency in Murine Hepatic Metastases Sel. Cancer Ther. 1989, 5, 1-11 10.1089/sct.1989.5.1
12. Steiniger, S. C. J.; Kreuter, J.; Khalansky, A. S.; Skidan, I. N.; Bobruskin, A. I.; Smirnova, Z. S.; Severin, S. E.; Uhl, R.; Kock, M.; Geiger, K. D.; Gelperina, S. E. Chemotherapy of Glioblastoma in Rats Using Doxorubicin-loaded Nanoparticles Int. J. Cancer 2004, 109, 759-767 10.1002/ijc.20048
13. Dreher, M. R.; Liu, W.; Michelich, C. R.; Dewhirst, M. W.; Yuan, F.; Chilkoti, A. Tumor Vascular Permeability, Accumulation, and Penetration of Macromolecular Drug Carriers J. Natl. Cancer Inst. 2006, 98, 335-344 10.1093/jnci/djj070
14. Champion, J. A.; Katare, Y. K.; Mitragotri, S. Particle Shape: A New Design Parameter for Micro- and Nanoscale Drug Delivery Carriers J. Controlled Release 2007, 121, 3-9 10.1016/j.jconrel.2007.03.022
15. May, R. C.; Machesky, L. M. Phagocytosis and Actin Cytoskeleton J. Cell. Sci. 2001, 114, 1061-1077
16. Rejman, J.; Oberle, V.; Zuhorn, I. S.; Hoekstra, D. Size-dependent Internalization of Particles Via the Pathways of Clathrin- and Caveolae-mediated Endocytosis Biochem. J. 2004, 377, 159-169 10.1042/BJ20031253
17. Qi, X.; Maitani, Y.; Nagai, T.; Wei, S. Comparative Pharmacokinetics and Antitumor Efficacy of Doxorubicin Encapsulated in Soybean-derived Sterols and Poly(ethylene glycol) Liposomes in Mice Int. J. Pharm. 1997, 146, 31-39 10.1016/S0378-5173(96)04753-9
18. Chithrani, B. D.; Chan, W. C. W. Elucidating the Mechanism of Cellular Uptake and Removal of Protein-coated Gold Nanoparticles of Different Sizes and Shapes Nano Lett. 2007, 7, 1542-50 10.1021/nl070363y
19. Chithrani, B. D.; Ghazani, A. A.; Chan, W. C. W. Determining the Size and Shape Dependence of Gold Nanoparticle Uptake into Mammalian Cells Nano Lett. 2006, 6, 662-668 10.1021/nl052396o
20. Ciofani, G.; Danti, S.; Genchi, G. G.; Mazzolai, B.; Mattoli, V. Boron Nitride Nanotubes: Biocompatibility and Potential Spill-over in Medicine Small 2013, 9, 1672-1685 10.1002/smll.201201315
21. Chen, X.; Wu, P.; Rousseas, M.; Okawa, D.; Gartner, Z.; Zettl, A.; Bertozzi, C. R. Boron Nitride Nanotubes Are Noncytotoxic and Can be Functionalized for Interaction with Proteins and Cells J. Am. Chem. Soc. 2009, 131, 890-891 10.1021/ja807334b
22. Horváth, L.; Magrez, A.; Golberg, D.; Zhi, C. Y.; Bando, Y.; Smajda, R.; Horváth, E.; Forró, L.; Schwaller, B. In Vitro Investigation of the Cellular Toxicity of Boron Nitride Nanotubes ACS Nano 2011, 5, 3800-3810 10.1021/nn200139h
23. Ciofani, G.; Del Turco, S.; Rocca, A.; de Vito, G.; Cappello, V.; Yamaguchi, M.; Li, X.; Mazzolai, B.; Basta, G.; Gemmi, M.; Piazza, V.; Golberg, D.; Mattoli, V. Cytocompatibility Evaluation of Gum Arabic-coated Ultra-pure Boron Nitride Nanotubes on Human Cells Nanomedicine 2014, 9, 773-788 10.2217/nnm.14.25
24. Li, X.; Zhi, C.; Hanagata, N.; Yamaguchi, M.; Bando, Y.; Golberg, D. Boron Nitride Nanotubes Functionalized with Mesoporous Silica for Intracellular Delivery of Chemotherapy Drugs Chem. Commun. 2013, 49, 7337-7339 10.1039/c3cc42743a
25. Li, X.; Hanagata, N.; Wang, X.; Yamaguchi, M.; Yi, W.; Bando, Y.; Golberg, D. Multimodal Luminescent-magnetic Boron Nitride Nanotubes@NaGdF4:Eu Structures for Cancer Therapy Chem. Commun. 2014, 50, 4371-4374 10.1039/c4cc00990h
26. Tang, C.; Bando, Y.; Sato, T.; Kurashima, K. A Novel Precursor for Synthesis of Pure Boron Nitride Nanotubes Chem. Commun. 2002, 12, 1290-1291 10.1039/b202177c
27. Terrones, M.; Charlier, J. C.; Gloter, A.; Cruz-Silva, E.; Terrés, E.; Li, Y. B.; Vinu, A.; Zanolli, Z.; Dominguez, J. M.; Terrones, H.; Bando, Y.; Golberg, D. Experimental and Theoretical Studies Suggesting the Possibility of Metallic Boron Nitride Edges in Porous Nanourchins Nano Lett. 2008, 8, 1026-1032 10.1021/nl072713m
28. Moon, O. M.; Kang, B. C.; Lee, S. B.; Boo, J. H. Temperature Effect on Structural Properties of Boron Oxide Thin Films Deposited by MOCVD Method Thin Solid Films 2004, 464-465, 164-169 10.1016/j.tsf.2004.05.107
29. Ying, Z. F.; Yu, D.; Ling, H.; Xu, N.; Lu, Y. F.; Sun, J.; Wu, J. D. Synthesis of BCN Thin Films by Nitrogen Ion Beam Assisted Pulsed Laser Deposition From a B4C Target Diamond Relat. Mater. 2007, 16, 1579-1585 10.1016/j.diamond.2007.01.021
30. Ciofani, G.; Danti, S.; D'Alessandro, D.; Moscato, S.; Menciassi, A. Assessing Cytotoxicity of Boron Nitride Nanotubes: Interference with the MTT Assay Biochem. Biophys. Res. Commun. 2010, 394, 405-411 10.1016/j.bbrc.2010.03.035
31. Belyanskaya, L.; Manser, P.; Spohn, P.; Bruinink, A.; Wick, P. The Reliability and Limits of the MTT Reduction Assay for Carbon Nanotubes-cell Interaction Carbon 2007, 45, 2643-2648 10.1016/j.carbon.2007.08.010
32. Macia, E.; Ehrlich, M.; Massol, R.; Boucrot, E.; Brunner, C.; Kirchhausen, T. Dynasore, a Cell-permeable Inhibitor of Dynamin Dev. Cell 2006, 10, 839-850 10.1016/j.devcel.2006.04.002
33. Fletcher, J. I.; Haber, M.; Henderson, M. J.; Norris, M. D. ABC Transporters in Cancer: More than Just Drug Efflux Pumps Nat. Rev. Cancer 2010, 10, 147-156 10.1038/nrc2789
34. Kirtane, A.; Kalscheuer, S.; Panyam, J. Exploiting Nanotechnology to Overcome Tumor Drug Resistance: Challenges and Opportunities Adv. Drug Delivery Rev. 2013, 65, 1731-1747 10.1016/j.addr.2013.09.001
35. Lengyel, E. Ovarian Cancer Development and Metastasis Am. J. Pathol. 2010, 177, 1053-1064 10.2353/ajpath.2010.100105
36. Hao, H.; Ma, Q.; He, F.; Yao, P. Doxorubicin and Fe3O4 Loaded Albumin Nanoparticles with Folic Acid Modified Dextran Surface for Tumor Diagnosis and Therapy J. Mater. Chem. B 2014, 2, 7978-7987 10.1039/C4TB01359J
37. Wu, J.; Wang, Y.; Jiang, W.; Xu, S.; Tian, R. Synthesis and Characterization of Recyclable Clusters of Magnetic Nanoparticles as Doxorubicin Carriers for Cancer Therapy Appl. Surf. Sci. 2014, 321, 43-9 10.1016/j.apsusc.2014.09.184
38. Regli, S.; Kelly, J. A.; Barnes, M. A.; Andrei, C. M.; Veinot, J. G. C. Mesoporous Silica Encapsulation of Silicon Nanocrystals: Synthesis, Aqueous Dispersibility and Drug Release Mater. Lett. 2014, 115, 21-24 10.1016/j.matlet.2013.10.006
39. Vimala, K.; Sundarraj, S.; Paulpandi, M.; Vengatesan, S.; Kannan, S. Green Synthesized Doxorubicin Loaded Zinc Oxide Nanoparticles Regulates the Bax and Bcl-2 Expression in Breast and Colon Carcinoma Process Biochem. 2014, 49, 160-172 10.1016/j.procbio.2013.10.007
40. Nigam, S.; Chandra, S.; Newgreen, D. F.; Bahadur, D.; Chen, Q. Poly(ethylene glycol)-modified PAMAM-Fe3O4-doxorubicin Triads with the Potential for Improved Therapeutic Efficacy: Generation-dependent Increased Drug Loading and Retention at Neutral pH and Increased Release at Acidic pH Langmuir 2014, 30, 1004-1011 10.1021/la404246h
41. Murali, R.; Vidhya, P.; Thanikaivelan, P. Thermoresponsive Magnetic Nanoparticle-Aminated Guar Gum Hydrogel System for Sustained Release of Doxorubicin Hydrochloride Carbohydr. Polym. 2014, 110, 440-445 10.1016/j.carbpol.2014.04.076
42. Gillies, E. R.; Fréchet, J. M. pH-Responsive Copolymer Assemblies for Controlled Release of Doxorubicin Bioconjugate Chem. 2005, 16, 361-368 10.1021/bc049851c
43. Che, E.; Wan, L.; Zhang, Y.; Zhao, Q.; Han, X.; Li, J.; Liu, J.; Wang, J. Development of Phosphonate-terminated Magnetic Mesoporous Silica Nanoparticles for pH-controlled Release of Doxorubicin and Improved Tumor Accumulation Asian J. Pharm. Sci. 2014, 9, 317 10.1016/j.ajps.2014.07.003
44. Yang, C. K. Exploring the Interaction Between the Boron Nitride Nanotube and Biological Molecules Comput. Phys. Commun. 2011, 182, 39-42 10.1016/j.cpc.2010.07.040
45. Mukhopadhyay, S.; Gowtham, S.; Scheicher, R. H.; Pandey, R.; Karna, S. P. Theoretical Study of Physisorption of Nucleobases on Boron Nitride Nanotubes: a New Class of Hybrid Nano-biomaterials Nanotechnology 2010, 21, 165703-165709 10.1088/0957-4484/21/16/165703
46. Moradi, A. V.; Peyghan, A. A.; Hashemian, S.; Baei, M. T. Theoretical Study of Thiazole Adsorption on the (6,0) zigzag Single-Walled Boron Nitride Nanotube Bull Bull. Korean Chem. Soc. 2012, 33, 3285-3292 10.5012/bkcs.2012.33.10.3285
47. André, C.; Guillaume, Y. C. Boron Nitride Nanotubes and Their Functionalization via Quinuclidine-3-thiol with Gold Nanoparticles for the Development and Enhancement of the HPLC Performance of HPLC Monolithic Columns Talanta 2012, 93, 274-278 10.1016/j.talanta.2012.02.033
48. Ciofani, G.; del Turco, S. T.; Genchi, G. G.; D'Alessandro, D.; Basta, G.; Mattoli, V. Transferrin-conjugated Boron Nitride Nanotubes: Protein Grafting, Characterization, and Interaction with Human Endothelial Cells Int. J. Pharm. 2012, 436, 444-453 10.1016/j.ijpharm.2012.06.037
49. Ferreira, T. H.; Marino, A.; Rocca, A.; Liakos, I.; Nitti, S.; Athanassiou, A.; Mattoli, V.; Mazzolai, B.; de Sousa, E. M. B.; Ciofani, G. Folate-grafted Boron Nitride Nanotubes: Possible Exploitation in Cancer Therapy Int. J. Pharm. 2015, 481, 56-63 10.1016/j.ijpharm.2015.01.048
50. Menichetti, L.; De Marchi, D.; Calucci, L.; Ciofani, G.; Menciassi, A.; Forte, C. Boron Nitride Nanotubes for Boron Neutron Capture Therapy as Contrast Agents in Magnetic Resonance Imaging at 3 T Appl. Radiat. Isot. 2011, 69, 1725-1727 10.1016/j.apradiso.2011.02.032
51. Iizumi, Y.; Okazaki, T.; Zhang, M.; Yuge, R.; Ichihashi, T.; Nakamura, M.; Ikehara, Y.; Iijima, S.; Yudasaka, M. Preparation and Functionalization of Boron Nitride Containing Carbon Nanohorns for Boron Neutron Capture Therapy Carbon 2015, 93, 595-603 10.1016/j.carbon.2015.05.085
52. Yamakov, V.; Park, C.; Kang, J. H.; Wise, K. E.; Fay, C. Piezoelectric Molecular Dynamics Model for Boron Nitride Nanotubes Comput. Mater. Sci. 2014, 95, 362-370 10.1016/j.commatsci.2014.07.047
53. Zhong, B.; Tang, X. H.; Huang, X. X.; Xia, L.; Zhang, X. D.; Wang, C. J.; Wen, G. W. Boron Nitride Hollow Nanospheres: Synthesis, Formation Mechanism and Dielectric Property Mater. Res. Bull. 2015, 64, 61-67 10.1016/j.materresbull.2014.12.048
54. Ciofani, G.; Raffa, V.; Menciassi, A.; Cuschieri, A. Boron Nitride Nanotubes: An Innovative Tool for Nanomedicine Nano Today 2009, 4, 8-10 10.1016/j.nantod.2008.09.001