The morphology of self-assembled lipid-based nanoparticles affects their uptake by cancer cells

Journal of Biomedical Nanotechnology

Volumn 12, Issue 10, 2016, Pages 1852-1863

  Aresh, Wafa ^a   Liu, Ying ^a   Sine, Jessica ^b   Thayer, Derek ^b   Puri, Anu ^b   Huang, Yike ^c   Wang, Yong ^c   Nieh, Mu Ping ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c The Pennsylvania State University   (United States)

Author keywords

Bicelles; Cancer Cellular Internalization; Morphology Targeting; SANS; Spontaneous Formation; Vesicles

Indexed keywords

CELL CULTURE; CELLS; DISEASES; HIGH RESOLUTION TRANSMISSION ELECTRON MICROSCOPY; LIGHT SCATTERING; LIGHT TRANSMISSION; MOLECULAR BIOLOGY; MORPHOLOGY; NANOPARTICLES; TRANSMISSION ELECTRON MICROSCOPY;

BICELLES; CELLULAR INTERNALIZATION; SANS; SPONTANEOUS FORMATION; VESICLES;

NEUTRON SCATTERING;

AMILORIDE; CHLORPROMAZINE; CLATHRIN; CYTOCHALASIN D; FILIPIN; NANODISC; NANOPARTICLE; NANOVESICLE; NOCODAZOLE; UNCLASSIFIED DRUG; WORTMANNIN; LIPID;

ARTICLE; CANCER CELL LINE; CAVEOLA; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOTOXICITY; ENDOCYTOSIS; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE CONFOCAL OPTICAL MICROSCOPY; HUMAN; HUMAN CELL; HYDRODYNAMICS; HYDROPHOBICITY; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; LIPID BILAYER; LIPID COMPOSITION; MICROTUBULE; MOLECULAR STABILITY; NEUTRON SCATTERING; PARTICLE SIZE; PHOTON CORRELATION SPECTROSCOPY; PINOCYTOSIS; TRANSITION TEMPERATURE; TRANSMISSION ELECTRON MICROSCOPY; CHEMISTRY; DRUG EFFECTS; METABOLISM; NEOPLASM; TUMOR CELL LINE; ULTRASTRUCTURE;

CELL LINE, TUMOR; CLATHRIN; DYNAMIC LIGHT SCATTERING; ENDOCYTOSIS; HUMANS; LIPIDS; MICROSCOPY, ELECTRON, TRANSMISSION; NANOPARTICLES; NEOPLASMS;

EID: 84990842391     PISSN: 15507033     EISSN: 15507041     Source Type: Journal    
DOI: 10.1166/jbn.2016.2292     Document Type: Article

References (42)

1. S. J. Tan, P. Kiatwuthinon, Y. H. Roh, J. S. Kahn, and D. Luo, Engineering nanocarriers for siRNA delivery. Small 7, 841 (2011).
2. A. Verma and F. Stellacci, Effect of surface properties on nanoparticle-cell interactions. Small 6, 12 (2010).
3. L. Zhang, F. X. Gu, J. M. Chan, A. Z. Wang, R. S. Langer, and O. C. Farokhzad, Nanoparticles in medicine: Therapeutic applications and developments. Clin. Pharmacol. Ther. 83, 761 (2008).
4. R. de la Rica, D. Aili, and M. M. Stevens, Enzyme-responsive nanoparticles for drug release and diagnostics. Adv. Drug Deliv. Rev. 64, 967 (2012).
5. G. Liu, M. Swierczewska, S. Lee, and X. Chen, Functional nanopar-ticles for molecular imaging guided gene delivery. Nano Today 5, 524 (2010).
6. B. D. Chithrani, A. A. Ghazani, and W. C. Chan, Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett. 6, 662 (2006).
7. E. C. Cho, L. Au, Q. Zhang, and Y. Xia, The effects of size, shape, and surface functional group of gold nanostructures on their adsorption and internalization by cells. Small 6, 517 (2010).
8. M. P. Desai, V. Labhasetwar, E. Walter, R. J. Levy, and G. L. Amidon, The mechanism of uptake of biodegradable microparticles in Caco-2 cells is size dependent. Pharm. Res. 14, 1568 (1997).
9. X. Li, Size and shape effects on receptor-mediated endocytosis of nanoparticles. J. Appl. Phys. 111 (2012).
10. N. P. Truong, M. R. Whittaker, C. W. Mak, and T. P. Davis, The importance of nanoparticle shape in cancer drug delivery. Expert Opin. Drug Deliv. 12, 129 (2015).
11. S. Barua, J.-W. Yoo, P. Kolhar, A. Wakankar, Y. R. Gokarn, and S. Mitragotri, Particle shape enhances specificity of antibody-displaying nanoparticles. Proceedings of the National Academy of Sciences 110, 3270 (2013).
12. K. Zhang, H. Fang, Z. Chen, J. S. Taylor, and K. L. Wooley, Shape effects of nanoparticles conjugated with cell-penetrating peptides (HIV Tat PTD) on CHO cell uptake. Bioconjug Chem. 19, 1880 (2008).
13. F. E. Alemdaroglu, N. C. Alemdaroglu, P. Langguth, and A. Herrmann, Cellular uptake of DNA block copolymer micelles with different shapes. Macromol. Rapid Commun. 29, 326 (2008).
14. D. P. Ferris, J. Lu, C. Gothard, R. Yanes, C. R. Thomas, J. C. Olsen, J. F. Stoddart, F. Tamanoi, and J. I. Zink, Synthesis of biomolecule-modified mesoporous silica nanoparticles for targeted hydrophobic drug delivery to cancer cells. Small 7, 1816 (2011).
15. L. Shang, K. Nienhaus, and G. U. Nienhaus, Engineered nanoparti-cles interacting with cells: Size matters. J. Nanobiotechnology 12, 5 (2014).
16. T. Shanmugam and R. Banerjee, Nanostructured self assembled lipid materials for drug delivery and tissue engineering. Ther. Delivery 2, 1485 (2011).
17. T. T. Goodman, P. L. Olive, and S. H. Pun, Increased nanoparti-cle penetration in collagenase-treated multicellular spheroids. Int. J. Nanomed. 2, 265 (2007).
18. K. Huang, H. Ma, J. Liu, S. Huo, A. Kumar, T. Wei, X. Zhang, S. Jin, Y. Gan, P. C. Wang, S. He, X. Zhang, and X.J. Liang, Sizen-: dependent localization and penetration of ultrasmall gold nanoparticles in cancer cells, multicellular spheroids, and tumors in vivo. ACS Nano 6, 4483 (2012).
19. H. Cabral, Y. Matsumoto, K. Mizuno, Q. Chen, M. Murakami, M. Kimura, Y. Terada, M. R. Kano, K. Miyazono, M. Uesaka, N. Nishiyama, and K. Kataoka, Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size. Nat. Nanotechnol. 6, 815 (2011).
20. M. Al Kobiasi, B. Y. Chua, D. Tonkin, D. C. Jackson, and D. E. Mainwaring, Control of size dispersity of chitosan biopolymer microparticles and nanoparticles to influence vaccine trafficking and cell uptake. J. Biomed. Mater. Res., Part A 100, 1859 (2012).
21. Arnida, A. Malugin, and H. Ghandehari, Cellular uptake and toxicity of gold nanoparticles in prostate cancer cells: A comparative study of rods and spheres. J. Appl. Toxicol. 30, 212 (2010).
22. L. Florez, C. Herrmann, J. M. Cramer, C. P. Hauser, K. Koynov, K. Landfester, D. Crespy, and V. Mailander, How shape influences uptake: Interactions of anisotropic polymer nanoparticles and human mesenchymal stem cells. Small 8, 2222 (2012).
23. J. F. Stefanick, J. D. Ashley, T. Kiziltepe, and B. Bilgicer, A systematic analysis of peptide linker length and liposomal polyethylene glycol coating on cellular uptake of peptide-targeted liposomes. ACS Nano 7, 2935 (2013).
24. M.-P. Nieh, C. J. Glinka, S. Krueger, R. S. Prosser, and J. Katsaras, SANS study on the effect of lanthanide ions and charged lipids on the morphology of phospholipid mixtures. Biophys. J. 82, 2487 (2002).
25. U. Iqbal, H. Albaghdadi, M. P. Nieh, U. I. Tuor, Z. Mester, D. Stanimirovic, J. Katsaras, and A. Abulrob, Small unilamellar vesicles: A platform technology for molecular imaging of brain tumors. Nanotechnology 22, 195102 (2011).
26. M. P. Nieh, N. Kucerka, and J. Katsaras, Spontaneously formed unilamellar vesicles. Methods Enzymol. 465, 3 (2009).
27. M. P. Nieh, P. Dolinar, N. Kucerka, S. R. Kline, L. M. Debeer-Schmitt, K. C. Littrell, and J. Katsaras, Formation of kinetically trapped nanoscopic unilamellar vesicles from metastable nanodiscs. Langmuir 27, 14308 (2011).
28. M. P. Nieh, V. A. Raghunathan, S. R. Kline, T. A. Harroun, C. Y. Huang, J. Pencer, and J. Katsaras, Spontaneously formed unilamellar vesicles with path-dependent size distribution. Langmuir 21, 6656 (2005).
29. B. N. Ames and D. T. Dubin, The role of polyamines in the neutralization of bacteriophage deoxyribonucleic acid. J. Biol. Chem. 235, 769 (1960).
30. B. Smith, I. Lyakhov, K. Loomis, D. Needle, U. Baxa, A. Yavlovich, J. Capala, R. Blumenthal, and A. Puri, Hyperthermia-triggered intracellular delivery of anticancer agent to HER2(+) cells by HER2-specific affibody (ZHER2-GS-Cys)-conjugated thermosensi-tive liposomes (HER2(+) affisomes). J. Controlled Release 153, 187 (2011).
31. Y. Liu, M. Li, Y Yang, Y Xia, and M. P. Nieh, The effects of temperature, salinity, concentration and PEGylated lipid on the spontaneous nanostructures of bicellar mixtures. Biochim. Biophys. Acta 1838, 1871 (2014).
32. M. P. Nieh, T. A. Harroun, V. A. Raghunathan, C. J. Glinka, and J. Katsaras, Spontaneously formed monodisperse biomimetic unilamellar vesicles: The effect of charge, dilution, and time. Biophys. J. 86, 2615 (2004).
33. Z. J. Deng, M. Liang, I. Toth, M. Monteiro, and R. F. Minchin, Plasma protein binding of positively and negatively charged polymer-coated gold nanoparticles elicits different biological responses. Nanotoxicology 7, 314 (2013).
34. M. L. Immordino, F. Dosio, and L. Cattel, Stealth liposomes: Review of the basic science, rationale, and clinical applications, existing and potential. Int. J. Nanomed. 1, 297 (2006).
35. P. Aggarwal, J. B. Hall, C. B. McLeland, M. A. Dobrovolskaia, and S. E. McNeil, Nanoparticle interaction with plasma proteins as it relates to particle biodistribution, biocompatibility and therapeutic efficacy. Adv. Drug Delivery Rev. 61, 428 (2009).
36. A. Hu, T. H. Fan, J. Katsaras, Y Xia, M. Li, and M. P. Nieh, Lipid-based nanodiscs as models for studying mesoscale coalescence-a transport limited case. Soft Matter. 10, 5055 (2014).
37. A. Puri, G. Kramer-Marek, R. Campbell-Massa, A. Yavlovich, S. C. Tele, S. B. Lee, J. D. Clogston, A. K. Patri, R. Blumenthal, and J. Capala, HER2-specific affibody-conjugated thermosensitive liposomes (Affisomes) for improved delivery of anticancer agents. J. Liposome Res. 18, 293 (2008).
38. R. Agarwal, V. Singh, P. Jurney, L. Shi, S. V. Sreenivasan, and K. Roy, Mammalian cells preferentially internalize hydrogel nanodiscs over nanorods and use shape-specific uptake mechanisms. PNAS 110, 17247 (2013).
39. H. Herd, N. Daum, A. T. Jones, H. Huwer, H. Ghandehari, and C. M. Lehr, Nanoparticle geometry and surface orientation influence mode of cellular uptake. ACS Nano 7, 1961 (2013).
40. S. Vranic, N. Boggetto, V. Contremoulins, S. Mornet, N. Reinhardt, F. Marano, A. Baeza-Squiban, and S. Boland, Deciphering the mechanisms of cellular uptake of engineered nanoparticles by accurate evaluation of internalization using imaging flow cytometry. Part. Fibre Toxicol. 10, 2 (2013).
41. A. I. Ivanov, Pharmacological inhibition of endocytic pathways: Is it specific enough to be useful? Methods Mol. Biol. (N. Y.) 440, 15 (2008).
42. T. dos Santos, J. Varela, I. Lynch, A. Salvati, and K. A. Dawson, Effects of transport inhibitors on the cellular uptake of carboxylated polystyrene nanoparticles in different cell lines. PLoS One 6, e24438 (2011).