Endocytosis of PEGylated nanoparticles accompanied by structural and free energy changes of the grafted polyethylene glycol

Biomaterials

Volumn 35, Issue 30, 2014, Pages 8467-8478

  Li, Ying ^a   Kröger, Martin ^b   Liu, Wing Kam ^a,c  

^a Northwestern University   (United States)

^b ETH ZURICH   (Switzerland)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

Cell membrane; Drug delivery; Particle internalization; PEGylated NP; Surface grafting

Indexed keywords

CARDIOVASCULAR SYSTEM; CELL MEMBRANES; CYTOLOGY; DRUG DELIVERY; FREE ENERGY; GRAFTING (CHEMICAL); MEAN FIELD THEORY; MOLECULAR BIOLOGY; MOLECULAR ORBITALS; POLYETHYLENE OXIDES; POLYMERIZATION; POLYMERS;

DISSIPATIVE PARTICLE DYNAMICS; LIGAND-RECEPTOR BINDING STRENGTH; PEGYLATED; PEGYLATED NANOPARTICLE; POLYETHYLENE GLYCOL (PEG); POLYMERIZATION DEGREE; SELF CONSISTENT FIELD THEORY; SURFACE GRAFTING;

POLYETHYLENE GLYCOLS;

MACROGOL; NANOCARRIER; NANOPARTICLE; MACROGOL DERIVATIVE;

ARTICLE; DRUG DELIVERY SYSTEM; ENDOCYTOSIS; INTERNALIZATION; MOLECULAR DYNAMICS; MORPHOLOGY; POLYMERIZATION; PRIORITY JOURNAL; SURFACE CHARGE; ANIMAL; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; MOLECULAR WEIGHT; MOUSE; PARTICLE SIZE; THERMODYNAMICS; ULTRASTRUCTURE;

ANIMALS; CELL LINE; COMPUTER SIMULATION; ENDOCYTOSIS; MICE; MODELS, MOLECULAR; MOLECULAR WEIGHT; NANOPARTICLES; PARTICLE SIZE; POLYETHYLENE GLYCOLS; THERMODYNAMICS;

EID: 84918802208     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.06.032     Document Type: Article

References (65)

1. Alivisatos P. The use of nanocrystals in biological detection. Nat Biotechnol 2004, 22:47-52.
2. Zhang L.F., Chan J.M., Gu F.X., Rhee J.W., Wang A.Z., Radovic-Moreno A.F., et al. Self-assembled lipid-polymer hybrid nanoparticles: a robust drug delivery platform. ACS Nano 2008, 2:1696-1702.
3. Doherty G.J., McMahon H.T. Mechanisms of endocytosis. Annu Rev Biochem 2009, 78:857-902.
4. Chou L.Y.T., Ming K., Chan W.C.W. Strategies for the intracellular delivery of nanoparticles. Chem Soc Rev 2011, 40:233-245.
5. Yan Y., Such G.K., Johnston A.P.R., Best J.P., Caruso F. Engineering particles for therapeutic delivery: prospects and challenges. ACS Nano 2012, 6:3663-3669.
6. Canton I., Battaglia G. Endocytosis at the nanoscale. Chem Soc Rev 2012, 41:2718-2739.
7. Li Y., Stroberg W., Lee T.R., Kim H.S., Man H., Ho D., et al. Multiscale modeling and uncertainty quantification in nanoparticle-mediated drug/gene delivery. Comput Mech 2014, 53:511-537.
8. Gao H.J., Shi W.D., Freund L.B. Mechanics of receptor-mediated endocytosis. P Natl Acad Sci U S A 2005, 102:9469-9474.
9. Zhang S.L., Li J., Lykotrafitis G., Bao G., Suresh S. Size-dependent endocytosis of nanoparticles. Adv Mater 2009, 21:419-424.
10. Decuzzi P., Ferrari M. The role of specific and non-specific interactions in receptor-mediated endocytosis of nanoparticles. Biomaterials 2007, 28:2915-2922.
11. Aoyama Y., Kanamori T., Nakai T., Sasaki T., Horiuchi S., Sando S., et al. Artificial viruses and their application to gene delivery. size-controlled gene coating with glycocluster nanoparticles. J Am Chem Soc 2003, 125:3455-3457.
12. Jiang W., Kim B.Y.S., Rutka J.T., Chan W.C.W. Nanoparticle-mediated cellular response is size-dependent. Nat Nanotechnol 2008, 3:145-150.
13. Yuan H.Y., Li J., Bao G., Zhang S.L. Variable nanoparticle-cell adhesion strength regulates cellular uptake. Phys Rev Lett 2010, 105:138101.
14. Decuzzi P., Ferrari M. Design maps for nanoparticles targeting the diseased microvasculature. Biomaterials 2008, 29:377-384.
15. Vacha R., Martinez-Veracoechea F.J., Frenkel D. Receptor-mediated endocytosis of nanoparticles of various shapes. Nano Lett 2011, 11:5391-5395.
16. Yue T.T., Zhang X.R. Cooperative effect in receptor-mediated endocytosis of multiple nanoparticles. ACS Nano 2012, 6:3196-3205.
17. Huang C.J., Zhang Y., Yuan H.Y., Gao H.J., Zhang S.L. Role of nanoparticle geometry in endocytosis: laying down to stand up. Nano Lett 2013, 13:4546-4550.
18. Decuzzi P., Ferrari M. The receptor-mediated endocytosis of nonspherical particles. Biophys J 2008, 94:3790-3797.
19. Cho E.C., Zhang Q., Xia Y.N. The effect of sedimentation and diffusion on cellular uptake of gold nanoparticles. Nat Nanotechnol 2011, 6:385-391.
20. Yang K., Ma Y.Q. Computer simulation of the translocation of nanoparticles with different shapes across a lipid bilayer. Nat Nanotechnol 2010, 5:579-583.
21. Ding H.M., Tian W.D., Ma Y.Q. Designing nanoparticle translocation through membranes by computer simulations. ACS Nano 2012, 6:1230-1238.
22. Li Y.F., Yuan H.Y., von dem Bussche A., Creighton M., Hurt R.H., Kane A.B., et al. Graphene microsheets enter cells through spontaneous membrane penetration at edge asperities and corner sites. P Natl Acad Sci U S A 2013, 110:12295-12300.
23. Dellian M., Yuan F., Trubetskoy V.S., Torchilin V.P., Jain R.K. Vascular permeability in a human tumour xenograft: molecular charge dependence. Br J Cancer 2000, 82:1513-1518.
24. De Jong W.H., Hagens W.I., Krystek P., Burger M.C., Sips A.J.A.M., Geertsma R.E. Particle size-dependent organ distribution of gold nanoparticles after intravenous administration. Biomaterials 2008, 29:1912-1919.
25. Immordino M.L., Dosio F., Cattel L. Stealth liposomes: review of the basic science, rationale, and clinical applications, existing and potential. Int J Nanomed 2006, 1:297-315.
26. Nativo P., Prior I.A., Brust M. Uptake and intracellular fate of surface-modified gold nanoparticles. ACS Nano 2008, 2:1639-1644.
27. Tkachenko A.G., Xie H., Coleman D., Glomm W., Ryan J., Anderson M.F., et al. Multifunctional gold nanoparticle-peptide complexes for nuclear targeting. J Am Chem Soc 2003, 125:4700-4701.
28. Oh E., Delehanty J.B., Sapsford K.E., Susumu K., Goswami R., Blanco-Canosa J.B., 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.
29. de la Zerda A., Bodapati S., Teed R., May S.Y., Tabakman S.M., Liu Z., et al. Family of enhanced photoacoustic imaging agents for high-sensitivity and multiplexing studies in living mice. ACS Nano 2012, 6:4694-4701.
30. Chen H.W., Paholak H., Ito M., Sansanaphongpricha K., Qian W., Che Y., et al. 'Living' PEGylation on gold nanoparticles to optimize cancer cell uptake by controlling targeting ligand and charge densities. Nanotechnology 2013, 24:355101.
31. Arnida, 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.
32. Cho E.C., Au L., Zhang Q., Xia Y.N. The effects of size, shape, and surface functional group of gold nanostructures on their adsorption and internalization by cells. Small 2010, 6:517-522.
33. Walkey C.D., Olsen J.B., Guo H.B., Emili A., Chan W.C.W. Nanoparticle size and surface chemistry determine serum protein adsorption and macrophage uptake. J Am Chem Soc 2012, 134:2139-2147.
34. Groot R.D., Rabone K.L. Mesoscopic simulation of cell membrane damage, morphology change and rupture by nonionic surfactants. Biophys J 2001, 81:725-736.
35. Li Y.F., Li X.J., Li Z.H., Gao H.J. Surface-structure-regulated penetration of nanoparticles across a cell membrane. Nanoscale 2012, 4:3768-3775.
36. Mao J., Guo R., Yan L.T. Simulation and analysis of cellular internalization pathways and membrane perturbation for graphene nanosheets. Biomaterials 2014, 35:6069-6077.
37. Guo R.H., Mao J., Yan L.T. Unique dynamical approach of fully wrapping dendrimer-like soft nanoparticles by lipid bilayer membrane. ACS Nano 2013, 7:10646-10653.
38. Hong B.B., Qiu F., Zhang H.D., Yang Y.L. Budding dynamics of individual domains in multicomponent membranes simulated by N-varied dissipative particle dynamics. J Phys Chem B 2007, 111:5837-5849.
39. Yue T.T., Zhang X.R. Molecular modeling of the pathways of vesicle-membrane interaction. Soft Matter 2013, 9:559-569.
40. Yue T.T., Zhang X.R., Huang F. Membrane monolayer protrusion mediates a new nanoparticle wrapping pathway. Soft Matter 2014, 10:2024-2034.
41. Lee H., de Vries A.H., Marrink S.J., Pastor R.W. A coarse-grained model for polyethylene oxide and polyethylene glycol: conformation and hydrodynamics. J Phys Chem B 2009, 113:13186-13194.
42. Ding H.M., Ma Y.Q. Controlling cellular uptake of nanoparticles with pH-sensitive polymers. Sci Rep 2013, 3:2804.
43. Li Y., Yue T.T., Yang K., Zhang X.R. Molecular modeling of the relationship between nanoparticle shape anisotropy and endocytosis kinetics. Biomaterials 2012, 33:4965-4973.
44. Halperin A., Kröger M., Zhulina E.B. Colloid-brush interactions: the effect of solvent quality. Macromolecules 2011, 44:3622-3638.
45. Wijmans C.M., Zhulina E.B. Polymer brushes at curved surfaces. Macromolecules 1993, 26:7214-7224.
46. Scheutjens J.M.H.M., Fleer G.J. Statistical-theory of the adsorption of interacting chain molecules. 1. partition-function, segment density distribution, and adsorption-isotherms. J Phys Chem 1979, 83:1619-1635.
47. Szleifer I., Carignano M.A. Tethered polymer layers: phase transitions and reduction of protein adsorption. Macromol Rapid Comm 2000, 21:423-448.
48. Szleifer I. Protein adsorption on surfaces with grafted polymers: a theoretical approach. Biophys J 1997, 72:595-612.
49. Unsworth L.D., Sheardown H., Brash J.L. Protein-resistant poly(ethylene oxide)-grafted surfaces: chain density-dependent multiple mechanisms of action. Langmuir 2008, 24:1924-1929.
50. Kröger M., Peleg O., Halperin A. From dendrimers to dendronized polymers and forests: scaling theory and its limitations. Macromolecules 2010, 43:6213-6224.
51. Chen X.M., Tian F.L., Zhang X.R., Wang W.C. Internalization pathways of nanoparticles and their interaction with a vesicle. Soft Matter 2013, 9:7592-7600.
52. Footer M.J., Kerssemakers J.W.J., Theriot J.A., Dogterom M. Direct measurement of force generation by actin filament polymerization using an optical trap. P Natl Acad Sci U S A 2007, 104:2181-2186.
53. Galletta B.J., Cooper J.A. Actin and endocytosis: mechanisms and phylogeny. Curr Opin Cell Biol 2009, 21:20-27.
54. Liu J., Weller G.E.R., Zern B., Ayyaswamy P.S., Eckmann D.M., Muzykantov V.R., et al. Computational model for nanocarrier binding to endothelium validated using in vivo, in vitro, and atomic force microscopy experiments. P Natl Acad Sci U S A 2010, 107:16530-16535.
55. Bradley R., Radhakrishnan R. Coarse-grained models for protein-cell membrane interactions. Polymers 2013, 5:890-936.
56. Deserno M., Gelbart W.M. Adhesion and wrapping in colloid-vesicle complexes. J Phys Chem B 2002, 106:5543-5552.
57. Ruiz-Herrero T., Velasco E., Hagan M.F. Mechanisms of budding of nanoscale particles through lipid bilayers. J Phys Chem B 2012, 116:9595-9603.
58. Yi X., Shi X.H., Gao H.J. A universal law for cell uptake of one-dimensional nanomaterials. Nano Lett 2014, 14:1049-1055.
59. Byfield F.J., Aranda-Espinoza H., Romanenko V.G., Rothblat G.H., Levitan I. Cholesterol depletion increases membrane stiffness of aortic endothelial cells. Biophys J 2004, 87:3336-3343.
60. Halperin A., Kröger M. Theoretical considerations on mechanisms of harvesting cells cultured on thermoresponsive polymer brushes. Biomaterials 2012, 33:4975-4987.
61. Halperin A., Kröger M. Thermoresponsive cell culture substrates based on PNIPAM brushes functionalized with adhesion peptides: theoretical considerations of mechanism and design. Langmuir 2012, 28:16623-16637.
62. Markovitch O., Agmon N. Structure and energetics of the hydronium hydration shells. J Phys Chem A 2007, 111:2253-2256.
63. Shi X.H., von dem Bussche A., Hurt R.H., Kane A.B., Gao H.J. Cell entry of one-dimensional nanomaterials occurs by tip recognition and rotation. Nat Nanotechnol 2011, 6:714-719.
64. van de Ven A.L., Kim P., Haley O., Fakhoury J.R., Adriani G., Schmulen J., et al. Rapid tumoritropic accumulation of systemically injected plateloid particles and their biodistribution. J Control Release 2012, 158:148-155.
65. Liu J., Bradley R., Eckmann D.M., Ayyaswamy P.S., Radhakrishnan R. Multiscale modeling of functionalized nanocarriers in targeted drug delivery. Curr Nanosci 2011, 7:727-735.