Engineered nanoparticles interacting with cells: Size matters

Journal of Nanobiotechnology

Volumn 12, Issue 1, 2014, Pages

  Shang, Li ^a   Nienhaus, Karin ^a   Nienhaus, Gerd U ^a,b,c  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^c University of Illinois at Urbana Champaign   (United States)

Author keywords

Cellular uptake; Cytotoxicity; Endocytosis; Nanoparticle; Protein corona; Red blood cell

Indexed keywords

ANIMALS; ENDOCYTOSIS; HUMANS; NANOPARTICLES; NANOTECHNOLOGY; PARTICLE SIZE;

EID: 84893175988     PISSN: None     EISSN: 14773155     Source Type: Journal    
DOI: 10.1186/1477-3155-12-5     Document Type: Review

References (100)

1. Astruc D. Transition - metal nanoparticles in catalysis: from historical background to the state - of - the art. Nanoparticles and Catalysis 2008, KGaA, Weinheim: WILEY-VCH Verlag GmbH & Co, Astruc D.
2. Saha K, Agasti SS, Kim C, Li XN, Rotello VM. Gold nanoparticles in chemical and biological sensing. Chem Rev 2012, 112:2739-2779. 10.1021/cr2001178, 22295941.
3. Stratakis E, Kymakis E. Nanoparticle-based plasmonic organic photovoltaic devices. Mater Today 2013, 16:133-146.
4. Saroja C, Lakshmi P, Bhaskaran S. Recent trends in vaccine delivery systems: a review. Int J Pharm Invest 2011, 1:64-74.
5. Meng FH, Cheng R, Deng C, Zhong ZY. Intracellular drug release nanosystems. Mater Today 2012, 15:436-442.
6. Yoo JW, Irvine DJ, Discher DE, Mitragotri S. Bio-inspired, bioengineered and biomimetic drug delivery carriers. Nat Rev Drug Discov 2011, 10:521-535. 10.1038/nrd3499, 21720407.
7. Stark WJ. Nanoparticles in biological systems. Angew Chem Int Ed 2011, 50:1242-1258.
8. Cheng LC, Jiang XM, Wang J, Chen CY, Liu RS. Nano-bio effects: interaction of nanomaterials with cells. Nanoscale 2013, 5:3547-3569. 10.1039/c3nr34276j, 23532468.
9. Röcker C, Pötzl M, Zhang F, Parak WJ, Nienhaus GU. A quantitative fluorescence study of protein monolayer formation on colloidal nanoparticles. Nat Nanotechnol 2009, 4:577-580. 10.1038/nnano.2009.195, 19734930.
10. Jiang X, Weise S, Hafner M, Röcker C, Zhang F, Parak WJ, Nienhaus GU. Quantitative analysis of the protein corona on FePt nanoparticles formed by transferrin binding. J R Soc Interface 2010, 7(Suppl 1):S5-S13. 2843989, 19776149.
11. Maffre P, Nienhaus K, Amin F, Parak WJ, Nienhaus GU. Characterization of protein adsorption onto FePt nanoparticles using dual-focus fluorescence correlation spectroscopy. Beilstein J Nanotechnol 2011, 2:374-383. 3190609, 22003445.
12. Lynch I, Salvati A, Dawson KA. Protein-nanoparticle interactions: what does the cell see?. Nat Nanotechnol 2009, 4:546-547. 10.1038/nnano.2009.248, 19734922.
13. Lundqvist M, Stigler J, Cedervall T, Berggard T, Flanagan MB, Lynch I, Elia G, Dawson K. The evolution of the protein corona around nanoparticles: a test study. ACS Nano 2011, 5:7503-7509. 10.1021/nn202458g, 21861491.
14. Verma A, Stellacci F. Effect of surface properties on nanoparticle-cell interactions. Small 2010, 6:12-21. 10.1002/smll.200901158, 19844908.
15. Mahmoudi M, Saeedi-Eslami SN, Shokrgozar MA, Azadmanesh K, Hassanlou M, Kalhor HR, Burtea C, Rothen-Rutishauser B, Laurent S, Sheibani S, Vali H. Cell "vision": complementary factor of protein corona in nanotoxicology. Nanoscale 2012, 4:5461-5468. 10.1039/c2nr31185b, 22842341.
16. Cho EC, Zhang Q, Xia Y. The effect of sedimentation and diffusion on cellular uptake of gold nanoparticles. Nat Nanotechnol 2011, 6:385-391. 10.1038/nnano.2011.58, 3227810, 21516092.
17. Li LW, Mu QX, Zhang B, Yan B. Analytical strategies for detecting nanoparticle-protein interactions. Analyst 2010, 135:1519-1530. 10.1039/c0an00075b, 20502814.
18. Saptarshi S, Duschl A, Lopata A. Interaction of nanoparticles with proteins: relation to bio-reactivity of the nanoparticle. J Nanobiotechnol 2013, 11:26.
19. Mahl D, Diendorf J, Meyer-Zaika W, Epple M. Possibilities and limitations of different analytical methods for the size determination of a bimodal dispersion of metallic nanoparticles. Colloids Surf A 2011, 377:386-392.
20. Cho EJ, Holback H, Liu KC, Abouelmagd SA, Park J, Yeo Y. Nanoparticle characterization: state of the art, challenges, and emerging technologies. Mol Pharm 2013, 10:2093-2110. 10.1021/mp300697h, 23461379.
21. Zemanova L, Schenk A, Nienhaus GU, Valler MJ, Heilker R. Confocal optics microscopy for biochemical and cellular high-throughput screening. Drug Discov Today 2004, 9:26-26.
22. Nienhaus GU, Maffre P, Nienhaus K. Studying the protein corona on nanoparticles by FCS. Methods Enzymol 2013, 519:115-137.
23. Saveyn H, De Baets B, Thas O, Hole P, Smith J, Van der Meeren P. Accurate particle size distribution determination by nanoparticle tracking analysis based on 2-D Brownian dynamics simulation. J Colloid Interf Sci 2010, 352:593-600.
24. Glatzel T, Hölscher H, Schimmel T, Baykara MZ, Schwarz UD, Garcia R. Advanced atomic force microscopy techniques. Beilstein J Nanotechnol 2012, 3:893-894. 3554267, 23365802.
25. Haiss W, Thanh NTK, Aveyard J, Fernig DG. Determination of size and concentration of gold nanoparticles from UV-vis spectra. Anal Chem 2007, 79:4215-4221. 10.1021/ac0702084, 17458937.
26. Planken KL, Colfen H. Analytical ultracentrifugation of colloids. Nanoscale 2010, 2:1849-1869. 10.1039/c0nr00215a, 20820642.
27. Hoo C, Starostin N, West P, Mecartney M. A comparison of atomic force microscopy (AFM) and dynamic light scattering (DLS) methods to characterize nanoparticle size distributions. J Nanopart Res 2008, 10:89-96.
28. MacCuspie R. Colloidal stability of silver nanoparticles in biologically relevant conditions. J Nanopart Res 2011, 13:2893-2908.
29. Malugin A, Ghandehari H. Cellular uptake and toxicity of gold nanoparticles in prostate cancer cells: a comparative study of rods and spheres. J Appl Toxicol 2010, 30:212-217.
30. Treuel L, Nienhaus G. Toward a molecular understanding of nanoparticle-protein interactions. Biophys Rev 2012, 4:137-147.
31. Monopoli MP, Walczyk D, Campbell A, Elia G, Lynch I, Baldelli Bombelli F, Dawson KA. Physical-chemical aspects of protein corona: relevance to in vitro and in vivo biological impacts of nanoparticles. J Am Chem Soc 2011, 133:2525-2534. 10.1021/ja107583h, 21288025.
32. Shang L, Dörlich RM, Trouillet V, Bruns M, Nienhaus GU. Ultrasmall fluorescent silver nanoclusters: protein adsorption and its effects on cellular responses. Nano Res 2012, 5:531-542.
33. Wang J, Jensen UB, Jensen GV, Shipovskov S, Balakrishnan VS, Otzen D, Pedersen JS, Besenbacher F, Sutherland DS. Soft interactions at nanoparticles alter protein function and conformation in a size dependent manner. Nano Lett 2011, 11:4985-4991. 10.1021/nl202940k, 21981115.
34. Tenzer S, Docter D, Rosfa S, Wlodarski A, Kuharev J, Rekik A, Knauer SK, Bantz C, Nawroth T, Bier C, et al. Nanoparticle size is a critical physicochemical determinant of the human blood plasma corona: a comprehensive quantitative proteomic analysis. ACS Nano 2011, 5:7155-7167. 10.1021/nn201950e, 21866933.
35. Shang W, Nuffer JH, Muniz-Papandrea VA, Colon W, Siegel RW, Dordick JS. Cytochrome c on silica nanoparticles: influence of nanoparticle size on protein structure, stability, and activity. Small 2009, 5:470-476. 10.1002/smll.200800995, 19189325.
36. Tenzer S, Docter D, Kuharev J, Musyanovych A, Fetz V, Hecht R, Schlenk F, Fischer D, Kiouptsi K, Reinhardt C, et al. Rapid formation of plasma protein corona critically affects nanoparticle pathophysiology. Nat Nanotechnol 2013, 8:772-781. 10.1038/nnano.2013.181, 24056901.
37. Iversen TG, Skotland T, Sandvig K. Endocytosis and intracellular transport of nanoparticles: present knowledge and need for future studies. Nano Today 2011, 6:176-185.
38. Canton I, Battaglia G. Endocytosis at the nanoscale. Chem Soc Rev 2012, 41:2718-2739. 10.1039/c2cs15309b, 22389111.
39. Chithrani BD, Ghazani AA, Chan WCW. Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett 2006, 6:662-668. 10.1021/nl052396o, 16608261.
40. Wang SH, Lee CW, Chiou A, Wei PK. Size-dependent endocytosis of gold nanoparticles studied by three-dimensional mapping of plasmonic scattering images. J Nanobiotechnol 2010, 8:33.
41. Lu F, Wu SH, Hung Y, Mou CY. Size effect on cell uptake in well-suspended, uniform mesoporous silica nanoparticles. Small 2009, 5:1408-1413. 10.1002/smll.200900005, 19296554.
42. Varela JA, Bexiga MG, Aberg C, Simpson JC, Dawson KA. Quantifying size-dependent interactions between fluorescently labeled polystyrene nanoparticles and mammalian cells. J Nanobiotechnol 2012, 10:39.
43. Huang J, Bu L, Xie J, Chen K, Cheng Z, Li X, Chen X. Effects of nanoparticle size on cellular uptake and liver MRI with polyvinylpyrrolidone-coated iron oxide nanoparticles. ACS Nano 2010, 4:7151-7160. 10.1021/nn101643u, 3011031, 21043459.
44. Huang K, Ma H, Liu J, Huo S, Kumar A, Wei T, Zhang X, Jin S, Gan Y, Wang PC, et al. Size-dependent localization and penetration of ultrasmall gold nanoparticles in cancer cells, multicellular spheroids, and tumors in vivo. ACS Nano 2012, 6:4483-4493. 10.1021/nn301282m, 3370420, 22540892.
45. Dong C, Irudayaraj J. Hydrodynamic size-dependent cellular uptake of aqueous QDs probed by fluorescence correlation spectroscopy. J Phys Chem B 2012, 116:12125-12132. 10.1021/jp305563p, 22950363.
46. Oh E, Delehanty JB, Sapsford KE, Susumu K, Goswami R, Blanco-Canosa JB, Dawson PE, Granek J, Shoff M, Zhang Q, et al. Cellular uptake and fate of PEGylated gold nanoparticles is dependent on both cell-penetration peptides and particle size. ACS Nano 2011, 5:6434-6448. 10.1021/nn201624c, 21774456.
47. Jiang W, Kim BYS, Rutka JT, Chan WCW. Nanoparticle-mediated cellular response is size-dependent. Nat Nanotechnol 2008, 3:145-150. 10.1038/nnano.2008.30, 18654486.
48. Shan Y, Ma S, Nie L, Shang X, Hao X, Tang Z, Wang H. Size-dependent endocytosis of single gold nanoparticles. Chem Commun 2011, 47:8091-8093.
49. Andersson PO, Lejon C, Ekstrand-Hammarstrom B, Akfur C, Ahlinder L, Bucht A, Osterlund L. Polymorph- and size-dependent uptake and toxicity of TiO(2) nanoparticles in living lung epithelial cells. Small 2011, 7:514-523. 10.1002/smll.201001832, 21265017.
50. Mironava T, Hadjiargyrou M, Simon M, Jurukovski V, Rafailovich MH. Gold nanoparticles cellular toxicity and recovery: effect of size, concentration and exposure time. Nanotoxicology 2010, 4:120-137. 10.3109/17435390903471463, 20795906.
51. Cho EC, Au L, Zhang Q, Xia Y. The effects of size, shape, and surface functional group of gold nanostructures on their adsorption and internalization by cells. Small 2010, 6:517-522. 10.1002/smll.200901622, 3011366, 20029850.
52. Walkey CD, Olsen JB, Guo H, Emili A, Chan WC. Nanoparticle size and surface chemistry determine serum protein adsorption and macrophage uptake. J Am Chem Soc 2012, 134:2139-2147. 10.1021/ja2084338, 22191645.
53. Liu X, Huang N, Li H, Jin Q, Ji J. Surface and size effects on cell interaction of gold nanoparticles with both phagocytic and nonphagocytic cells. Langmuir 2013, 29:9138-9148. 10.1021/la401556k, 23815604.
54. Elbakry A, Wurster EC, Zaky A, Liebl R, Schindler E, Bauer-Kreisel P, Blunk T, Rachel R, Goepferich A, Breunig M. Layer-by-layer coated gold nanoparticles: size-dependent delivery of DNA into cells. Small 2012, 8:3847-3856. 10.1002/smll.201201112, 22911477.
55. Schübbe S, Schumann C, Cavelius C, Koch M, Müller T, Kraegeloh A. Size-dependent localization and quantitative evaluation of the intracellular migration of silica nanoparticles in caco-2 cells. Chem Mater 2012, 24:914-923.
56. dos Santos T, Varela J, Lynch I, Salvati A, Dawson KA. Quantitative assessment of the comparative nanoparticle-uptake efficiency of a range of cell lines. Small 2011, 7:3341-3349. 10.1002/smll.201101076, 22009913.
57. Xu A, Yao M, Xu G, Ying J, Ma W, Li B, Jin Y. A physical model for the size-dependent cellular uptake of nanoparticles modified with cationic surfactants. Int J Nanomedicine 2012, 7:3547-3554. 3405883, 22848178.
58. He C, Hu Y, Yin L, Tang C, Yin C. Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles. Biomaterials 2010, 31:3657-3666. 10.1016/j.biomaterials.2010.01.065, 20138662.
59. Rejman J, Oberle V, Zuhorn IS, 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, 1223843, 14505488.
60. Jiang X, Röcker C, Hafner M, Brandholt S, Dörlich RM, Nienhaus GU. Endo- and exocytosis of zwitterionic quantum dot nanoparticles by live HeLa cells. ACS Nano 2010, 4:6787-6797. 10.1021/nn101277w, 21028844.
61. Yang L, Shang L, Nienhaus GU. Mechanistic aspects of fluorescent gold nanocluster internalization by live HeLa cells. Nanoscale 2013, 5:1537-1543. 10.1039/c2nr33147k, 23322237.
62. Shang L, Stockmar F, Azadfar N, Nienhaus GU. Intracellular thermometry by using fluorescent gold nanoclusters. Angew Chem Int Ed Engl 2013, 52:11154-11157. 10.1002/anie.201306366, 24039076.
63. Jiang X, Dausend J, Hafner M, Musyanovych A, Röcker C, Landfester K, Mailänder V, Nienhaus GU. Specific effects of surface amines on polystyrene nanoparticles in their interactions with mesenchymal stem cells. Biomacromolecules 2010, 11:748-753. 10.1021/bm901348z, 20166675.
64. Jiang X, Musyanovych A, Röcker C, Landfester K, Mailänder V, Nienhaus GU. Specific effects of surface carboxyl groups on anionic polystyrene particles in their interactions with mesenchymal stem cells. Nanoscale 2011, 3:2028-2035. 10.1039/c0nr00944j, 21409242.
65. Lunov O, Syrovets T, Loos C, Beil J, Delacher M, Tron K, Nienhaus GU, Musyanovych A, Mailänder V, Landfester K, Simmet T. Differential uptake of functionalized polystyrene nanoparticles by human macrophages and a monocytic cell line. ACS Nano 2011, 5:1657-1669. 10.1021/nn2000756, 21344890.
66. Lunov O, Syrovets T, Loos C, Nienhaus GU, Mailänder V, Landfester K, Rouis M, Simmet T. Amino-functionalized polystyrene nanoparticles activate the NLRP3 inflammasome in human macrophages. ACS Nano 2011, 5:9648-9657. 10.1021/nn203596e, 22111911.
67. Hühn D, Kantner K, Geidel C, Brandholt S, De Cock I, Soenen SJ, Rivera Gil P, Montenegro JM, Braeckmans K, Mullen K, et al. Polymer-coated nanoparticles interacting with proteins and cells: focusing on the sign of the net charge. ACS Nano 2013, 7:3253-3263. 10.1021/nn3059295, 23566380.
68. Albanese A, Tang PS, Chan WC. The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu Rev Biomed Eng 2012, 14:1-16. 10.1146/annurev-bioeng-071811-150124, 22524388.
69. Lunov O, Zablotskii V, Syrovets T, Röcker C, Tron K, Nienhaus GU, Simmet T. Modeling receptor-mediated endocytosis of polymer-functionalized iron oxide nanoparticles by human macrophages. Biomaterials 2011, 32:547-555. 10.1016/j.biomaterials.2010.08.111, 20880574.
70. Yuan H, Li J, Bao G, Zhang S. Variable nanoparticle-cell adhesion strength regulates cellular uptake. Phys Rev Lett 2010, 105:138101.
71. Shang L, Yang L, Seiter J, Heinle M, Brenner-Weiss G, Gerthsen D, Nienhaus GU. Nanoparticles interacting with proteins and cells: a systematic study of protein surface charge effects. Adv Mater Interfaces 2014, 10.1002/admi.201300079.
72. Lovrić J, Bazzi H, Cuie Y, Fortin GA, Winnik F, Maysinger D. Differences in subcellular distribution and toxicity of green and red emitting CdTe quantum dots. J Mol Med 2005, 83:377-385. 10.1007/s00109-004-0629-x, 15688234.
73. Parak WJ, Boudreau R, Le Gros MA, Gerion D, Zanchet D, Micheel CM, Williams SC, Alivisatos AP, Larabell C. Cell motility and metastatic potential studies based on quantum dot imaging of phagokinetic tracks. Adv Mater 2002, 14:882-885.
74. Underhill DM, Ozinsky A. Phagocytosis of microbes: complexity in action. Annu Rev Immunol 2002, 20:825-852. 10.1146/annurev.immunol.20.103001.114744, 11861619.
75. Geiser M, Rothen-Rutishauser B, Kapp N, Schurch S, Kreyling W, Schulz H, Semmler M, Im Hof V, Heyder J, Gehr P. Ultrafine particles cross cellular membranes by nonphagocytic mechanisms in lungs and in cultured cells. Environ Health Perspect 2005, 113:1555-1560. 10.1289/ehp.8006, 1310918, 16263511.
76. Rothen-Rutishauser BM, Schurch S, Haenni B, Kapp N, Gehr P. Interaction of fine particles and nanoparticles with red blood cells visualized with advanced microscopic techniques. Environ Sci Technol 2006, 40:4353-4359. 10.1021/es0522635, 16903270.
77. Wang T, Bai J, Jiang X, Nienhaus GU. Cellular uptake of nanoparticles by membrane penetration: a study combining confocal microscopy with FTIR spectroelectrochemistry. ACS Nano 2012, 6:1251-1259. 10.1021/nn203892h, 22250809.
78. Slowing II, Wu CW, Vivero-Escoto JL, Lin VS. Mesoporous silica nanoparticles for reducing hemolytic activity towards mammalian red blood cells. Small 2009, 5:57-62. 10.1002/smll.200800926, 19051185.
79. Zhao Y, Sun X, Zhang G, Trewyn BG, Slowing II, Lin VS. Interaction of mesoporous silica nanoparticles with human red blood cell membranes: size and surface effects. ACS Nano 2011, 5:1366-1375. 10.1021/nn103077k, 21294526.
80. Han Y, Wang X, Dai H, Li S. Nanosize and surface charge effects of hydroxyapatite nanoparticles on Red blood cell suspensions. ACS Appl Mater Interfaces 2012, 4:4616-4622. 10.1021/am300992x, 22860897.
81. Verma A, Uzun O, Hu Y, Han HS, Watson N, Chen S, Irvine DJ, Stellacci F. Surface-structure-regulated cell-membrane penetration by monolayer-protected nanoparticles. Nat Mater 2008, 7:588-595. 10.1038/nmat2202, 2684029, 18500347.
82. Van Lehn RC, Atukorale PU, Carney RP, Yang YS, Stellacci F, Irvine DJ, Alexander-Katz A. Effect of particle diameter and surface composition on the spontaneous fusion of monolayer-protected gold nanoparticles with lipid bilayers. Nano Lett 2013, 13:4060-4067. 10.1021/nl401365n, 23915118.
83. Koren E, Torchilin VP. Cell-penetrating peptides: breaking through to the other side. Trends Mol Med 2012, 18:385-393. 10.1016/j.molmed.2012.04.012, 22682515.
84. Heitz F, Morris MC, Divita G. Twenty years of cell-penetrating peptides: from molecular mechanisms to therapeutics. Br J Pharmacol 2009, 157:195-206. 10.1111/j.1476-5381.2009.00057.x, 2697800, 19309362.
85. Kostarelos K, Lacerda L, Pastorin G, Wu W, Wieckowski S, Luangsivilay J, Godefroy S, Pantarotto D, Briand JP, Muller S, et al. Cellular uptake of functionalized carbon nanotubes is independent of functional group and cell type. Nat Nanotechnol 2007, 2:108-113. 10.1038/nnano.2006.209, 18654229.
86. Sharifi S, Behzadi S, Laurent S, Forrest ML, Stroeve P, Mahmoudi M. Toxicity of nanomaterials. Chem Soc Rev 2012, 41:2323-2343. 10.1039/c1cs15188f, 22170510.
87. Nel A, Xia T, Madler L, Li N. Toxic potential of materials at the nanolevel. Science 2006, 311:622-627. 10.1126/science.1114397, 16456071.
88. Love SA, Maurer-Jones MA, Thompson JW, Lin Y-S, Haynes CL. Assessing nanoparticle toxicity. Annu Rev Anal Chem 2012, 5:181-205.
89. Pan Y, Neuss S, Leifert A, Fischler M, Wen F, Simon U, Schmid G, Brandau W, Jahnen-Dechent W. Size-dependent cytotoxicity of gold nanoparticles. Small 2007, 3:1941-1949. 10.1002/smll.200700378, 17963284.
90. Park J, Lim DH, Lim HJ, Kwon T, Choi JS, Jeong S, Choi IH, Cheon J. Size dependent macrophage responses and toxicological effects of Ag nanoparticles. Chem Commun 2011, 47:4382-4384.
91. Ariano P, Zamburlin P, Gilardino A, Mortera R, Onida B, Tomatis M, Ghiazza M, Fubini B, Lovisolo D. Interaction of spherical silica nanoparticles with neuronal cells: size-dependent toxicity and perturbation of calcium homeostasis. Small 2011, 7:766-774. 10.1002/smll.201002287, 21302356.
92. Bhattacharjee S, Ershov D, Fytianos K, van der Gucht J, Alink GM, Rietjens IMCM, Marcelis ATM, Zuilhof H. Cytotoxicity and cellular uptake of tri-block copolymer nanoparticles with different size and surface characteristics. Part Fibre Toxicol 2012, 9:11. 10.1186/1743-8977-9-11, 3419642, 22546147.
93. Yen HJ, Hsu SH, Tsai CL. Cytotoxicity and immunological response of gold and silver nanoparticles of different sizes. Small 2009, 5:1553-1561. 10.1002/smll.200900126, 19326357.
94. Chen YS, Hung YC, Liau I, Huang GS. Assessment of the in vivo toxicity of gold nanoparticles. Nanoscale Res Lett 2009, 4:858-864. 10.1007/s11671-009-9334-6, 2894102,2894102, 20596373.
95. Coradeghini R, Gioria S, Garcia CP, Nativo P, Franchini F, Gilliland D, Ponti J, Rossi F. Size-dependent toxicity and cell interaction mechanisms of gold nanoparticles on mouse fibroblasts. Toxicol Lett 2013, 217:205-216. 10.1016/j.toxlet.2012.11.022, 23246733.
96. Freese C, Uboldi C, Gibson MI, Unger RE, Weksler BB, Romero IA, Couraud PO, Kirkpatrick CJ. Uptake and cytotoxicity of citrate-coated gold nanospheres: Comparative studies on human endothelial and epithelial cells. Part Fibre Toxicol 2012, 9:23. 10.1186/1743-8977-9-23, 3407003, 22759355.
97. Carlson C, Hussain SM, Schrand AM K, Braydich-Stolle L, Hess KL, Jones RL, Schlager JJ. Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J Phys Chem B 2008, 112:13608-13619. 10.1021/jp712087m, 18831567.
98. Kim T-H, Kim M, Park H-S, Shin US, Gong M-S, Kim H-W. Size-dependent cellular toxicity of silver nanoparticles. J Biomed Mater Res A 2012, 100A:1033-1043.
99. Cai K, Hou Y, Hu Y, Zhao L, Luo Z, Shi Y, Lai M, Yang W, Liu P. Correlation of the cytotoxicity of TiO2 nanoparticles with different particle sizes on a sub-200-nm scale. Small 2011, 7:3026-3031. 10.1002/smll.201101170, 21919195.
100. Vedantam P, Huang G, Tzeng TRJ. Size-dependent cellular toxicity and uptake of commercial colloidal gold nanoparticles in DU-145 cells. Cancer Nanotechnol 2013, 4:13-20.