Improving targeting of metal-phenolic capsules by the presence of protein coronas

ACS Applied Materials and Interfaces

Volumn 8, Issue 35, 2016, Pages 22914-22922

  Ju, Yi ^a   Dai, Qiong ^a   Cui, Jiwei ^a   Dai, Yunlu ^a   Suma, Tomoya ^a   Richardson, Joseph J ^a,b   Caruso, Frank ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b CSIRO   (Australia)

Author keywords

cell targeting; hyaluronic acid; polymer capsules; polyphenols; protein corona

Indexed keywords

COMPLEX NETWORKS; HYALURONIC ACID; MOLECULAR WEIGHT; ORGANIC ACIDS;

CELL TARGETING; HIGH MOLECULAR WEIGHT; MOLECULAR WEIGHT DEPENDENT; PHYSIOLOGICAL ENVIRONMENT; POLYMER CAPSULES; POLYPHENOLS; PROTEIN CORONAS; SPECIFIC INTERACTION;

PROTEINS;

HYALURONIC ACID; METAL; PHENOL DERIVATIVE; PROTEIN CORONA;

CHEMISTRY; HUMAN; MICROCAPSULE;

CAPSULES; HUMANS; HYALURONIC ACID; METALS; PHENOLS; PROTEIN CORONA;

EID: 84986537217     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.6b07613     Document Type: Article

References (55)

1. Byrne, J. D.; Betancourt, T.; Brannon-Peppas, L. Active Targeting Schemes for Nanoparticle Systems in Cancer Therapeutics Adv. Drug Delivery Rev. 2008, 60, 1615-1626 10.1016/j.addr.2008.08.005
2. Farokhzad, O. C.; Langer, R. Impact of Nanotechnology on Drug Delivery ACS Nano 2009, 3, 16-20 10.1021/nn900002m
3. Peer, D.; Karp, J. M.; Hong, S.; Farokhzad, O. C.; Margalit, R.; Langer, R. Nanocarriers as an Emerging Platform for Cancer Therapy Nat. Nanotechnol. 2007, 2, 751-760 10.1038/nnano.2007.387
4. Cui, J.; Richardson, J. J.; Björnmalm, M.; Faria, M.; Caruso, F. Nanoengineered Templated Polymer Particles: Navigating the Biological Realm Acc. Chem. Res. 2016, 49, 1139-1148 10.1021/acs.accounts.6b00088
5. Weiner, L. M.; Surana, R.; Wang, S. Monoclonal Antibodies: Versatile Platforms for Cancer Immunotherapy Nat. Rev. Immunol. 2010, 10, 317-327 10.1038/nri2744
6. Yang, L.; Mao, H.; Wang, Y. A.; Cao, Z.; Peng, X.; Wang, X.; Duan, H.; Ni, C.; Yuan, Q.; Adams, G. Single Chain Epidermal Growth Factor Receptor Antibody Conjugated Nanoparticles for in Vivo Tumor Targeting and Imaging Small 2009, 5, 235-243 10.1002/smll.200800714
7. Xia, W.; Low, P. S. Folate-Targeted Therapies for Cancer J. Med. Chem. 2010, 53, 6811-6824 10.1021/jm100509v
8. Yang, G.; Wang, J.; Wang, Y.; Li, L.; Guo, X.; Zhou, S. An Implantable Active-Targeting Micelle-in-Nanofiber Device for Efficient and Safe Cancer Therapy ACS Nano 2015, 9, 1161-1174 10.1021/nn504573u
9. Choi, C. H. J.; Alabi, C. A.; Webster, P.; Davis, M. E. Mechanism of Active Targeting in Solid Tumors with Transferrin-Containing Gold Nanoparticles Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 1235-1240 10.1073/pnas.0914140107
10. Sykes, E. A.; Chen, J.; Zheng, G.; Chan, W. C. Investigating the Impact of Nanoparticle Size on Active and Passive Tumor Targeting Efficiency ACS Nano 2014, 8, 5696-5706 10.1021/nn500299p
11. García, I.; Sánchez-Iglesias, A.; Henriksen-Lacey, M.; Grzelczak, M.; Penadés, S.; Liz-Marzán, L. M. Glycans as Biofunctional Ligands for Gold Nanorods: Stability and Targeting in Protein-Rich Media J. Am. Chem. Soc. 2015, 137, 3686-3692 10.1021/jacs.5b01001
12. Kang, B.; Okwieka, P.; Schöttler, S.; Winzen, S.; Langhanki, J.; Mohr, K.; Opatz, T.; Mailänder, V.; Landfester, K.; Wurm, F. R. Carbohydrate-Based Nanocarriers Exhibiting Specific Cell Targeting with Minimum Influence from the Protein Corona Angew. Chem., Int. Ed. 2015, 54, 7436-7440 10.1002/anie.201502398
13. Arpicco, S.; Milla, P.; Stella, B.; Dosio, F. Hyaluronic Acid Conjugates as Vectors for the Active Targeting of Drugs, Genes and Nanocomposites in Cancer Treatment Molecules 2014, 19, 3193-3230 10.3390/molecules19033193
14. Qhattal, H. S. S.; Hye, T.; Alali, A.; Liu, X. Hyaluronan Polymer Length, Grafting Density, and Surface Poly(ethylene glycol) Coating Influence in Vivo Circulation and Tumor Targeting of Hyaluronan-Grafted Liposomes ACS Nano 2014, 8, 5423-5440 10.1021/nn405839n
15. Qhattal, H. S. S.; Liu, X. Characterization of CD44-Mediated Cancer Cell Uptake and Intracellular Distribution of Hyaluronan-Grafted Liposomes Mol. Pharmaceutics 2011, 8, 1233-1246 10.1021/mp2000428
16. Ganesh, S.; Iyer, A. K.; Morrissey, D. V.; Amiji, M. M. Hyaluronic Acid Based Self-Assembling Nanosystems for CD44 Target Mediated siRNA Delivery to Solid Tumors Biomaterials 2013, 34, 3489-3502 10.1016/j.biomaterials.2013.01.077
17. Han, X.; Li, Z.; Sun, J.; Luo, C.; Li, L.; Liu, Y.; Du, Y.; Qiu, S.; Ai, X.; Wu, C. Stealth CD44-Targeted Hyaluronic Acid Supramolecular Nanoassemblies for Doxorubicin Delivery: Probing the Effect of Uncovalent PEGylation Degree on Cellular Uptake and Blood Long Circulation J. Controlled Release 2015, 197, 29-40 10.1016/j.jconrel.2014.10.024
18. Dreaden, E. C.; Morton, S. W.; Shopsowitz, K. E.; Choi, J.-H.; Deng, Z. J.; Cho, N.-J.; Hammond, P. T. Bimodal Tumor-Targeting from Microenvironment Responsive Hyaluronan Layer-by-Layer (LbL) Nanoparticles ACS Nano 2014, 8, 8374-8382 10.1021/nn502861t
19. Lee, M. S.; Lee, J. E.; Byun, E.; Kim, N. W.; Lee, K.; Lee, H.; Sim, S. J.; Lee, D. S.; Jeong, J. H. Target-Specific Delivery of siRNA by Stabilized Calcium Phosphate Nanoparticles Using Dopa-Hyaluronic Acid Conjugate J. Controlled Release 2014, 192, 122-130 10.1016/j.jconrel.2014.06.049
20. Ossipov, D. A. Nanostructured Hyaluronic Acid-Based Materials for Active Delivery to Cancer Expert Opin. Drug Delivery 2010, 7, 681-703 10.1517/17425241003730399
21. Mattheolabakis, G.; Milane, L.; Singh, A.; Amiji, M. M. Hyaluronic Acid Targeting of CD44 for Cancer Therapy: From Receptor Biology to Nanomedicine J. Drug Targeting 2015, 23, 605-618 10.3109/1061186X.2015.1052072
22. Platt, V. M.; Szoka, F. C., Jr. Anticancer Therapeutics: Targeting Macromolecules and Nanocarriers to Hyaluronan or CD44, a Hyaluronan Receptor Mol. Pharmaceutics 2008, 5, 474-486 10.1021/mp800024g
23. Peer, D.; Margalit, R. Tumor-Targeted Hyaluronan Nanoliposomes Increase the Antitumor Activity of Liposomal Doxorubicin in Syngeneic and Human Xenograft Mouse Tumor Models Neoplasia 2004, 6, 343-353 10.1593/neo.03460
24. Song, S.; Chen, F.; Qi, H.; Li, F.; Xin, T.; Xu, J.; Ye, T.; Sheng, N.; Yang, X.; Pan, W. Multifunctional Tumor-Targeting Nanocarriers Based on Hyaluronic Acid-Mediated and pH-Sensitive Properties for Efficient Delivery of Docetaxel Pharm. Res. 2014, 31, 1032-1045 10.1007/s11095-013-1225-y
25. Mizrahy, S.; Raz, S. R.; Hasgaard, M.; Liu, H.; Soffer-Tsur, N.; Cohen, K.; Dvash, R.; Landsman-Milo, D.; Bremer, M. G.; Moghimi, S. M. Hyaluronan-Coated Nanoparticles: The Influence of the Molecular Weight on CD44-Hyaluronan Interactions and on the Immune Response J. Controlled Release 2011, 156, 231-238 10.1016/j.jconrel.2011.06.031
26. Walkey, C. D.; Chan, W. C. Understanding and Controlling the Interaction of Nanomaterials with Proteins in a Physiological Environment Chem. Soc. Rev. 2012, 41, 2780-2799 10.1039/C1CS15233E
27. Gref, R.; Lück, M.; Quellec, P.; Marchand, M.; Dellacherie, E.; Harnisch, S.; Blunk, T.; Müller, R. 'Stealth' Corona-Core Nanoparticles Surface Modified by Polyethylene Glycol (PEG): Influences of the Corona (PEG Chain Length and Surface Density) and of the Core Composition on Phagocytic Uptake and Plasma Protein Adsorption Colloids Surf., B 2000, 18, 301-313 10.1016/S0927-7765(99)00156-3
28. Schöttler, S.; Becker, G.; Winzen, S.; Steinbach, T.; Mohr, K.; Landfester, K.; Mailänder, V.; Wurm, F. R. Protein Adsorption Is Required for Stealth Effect of Poly(ethylene glycol)- and Poly(phosphoester)-Coated Nanocarriers Nat. Nanotechnol. 2016, 11, 372-377 10.1038/nnano.2015.330
29. Monopoli, M. P.; Åberg, C.; Salvati, A.; Dawson, K. A. Biomolecular Coronas Provide the Biological Identity of Nanosized Materials Nat. Nanotechnol. 2012, 7, 779-786 10.1038/nnano.2012.207
30. Yan, Y.; Gause, K. T.; Kamphuis, M. M.; Ang, C.-S.; O'Brien-Simpson, N. M.; Lenzo, J. C.; Reynolds, E. C.; Nice, E. C.; Caruso, F. Differential Roles of the Protein Corona in the Cellular Uptake of Nanoporous Polymer Particles by Monocyte and Macrophage Cell Lines ACS Nano 2013, 7, 10960-10970 10.1021/nn404481f
31. Mirshafiee, V.; Mahmoudi, M.; Lou, K.; Cheng, J.; Kraft, M. L. Protein Corona Significantly Reduces Active Targeting Yield Chem. Commun. 2013, 49, 2557-2559 10.1039/c3cc37307j
32. Salvati, A.; Pitek, A. S.; Monopoli, M. P.; Prapainop, K.; Bombelli, F. B.; Hristov, D. R.; Kelly, P. M.; Åberg, C.; Mahon, E.; Dawson, K. A. Transferrin-Functionalized Nanoparticles Lose Their Targeting Capabilities When a Biomolecule Corona Adsorbs on the Surface Nat. Nanotechnol. 2013, 8, 137-143 10.1038/nnano.2012.237
33. Zarschler, K.; Prapainop, K.; Mahon, E.; Rocks, L.; Bramini, M.; Kelly, P.; Stephan, H.; Dawson, K. Diagnostic Nanoparticle Targeting of the EGF-Receptor in Complex Biological Conditions Using Single-Domain Antibodies Nanoscale 2014, 6, 6046-6056 10.1039/c4nr00595c
34. Dai, Q.; Yan, Y.; Ang, C.-S.; Kempe, K.; Kamphuis, M. M.; Dodds, S. J.; Caruso, F. Monoclonal Antibody-Functionalized Multilayered Particles: Targeting Cancer Cells in the Presence of Protein Coronas ACS Nano 2015, 9, 2876-2885 10.1021/nn506929e
35. Dai, Q.; Yan, Y.; Guo, J.; Björnmalm, M.; Cui, J.; Sun, H.; Caruso, F. Targeting Ability of Affibody-Functionalized Particles is Enhanced by Albumin but Inhibited by Serum Coronas ACS Macro Lett. 2015, 4, 1259-1263 10.1021/acsmacrolett.5b00627
36. Ejima, H.; Richardson, J. J.; Liang, K.; Best, J. P.; van Koeverden, M. P.; Such, G. K.; Cui, J.; Caruso, F. One-Step Assembly of Coordination Complexes for Versatile Film and Particle Engineering Science 2013, 341, 154-157 10.1126/science.1237265
37. Guo, J.; Ping, Y.; Ejima, H.; Alt, K.; Meissner, M.; Richardson, J. J.; Yan, Y.; Peter, K.; von Elverfeldt, D.; Hagemeyer, C. E. Engineering Multifunctional Capsules through the Assembly of Metal-Phenolic Networks Angew. Chem., Int. Ed. 2014, 53, 5546-5551 10.1002/anie.201311136
38. Ping, Y.; Guo, J.; Ejima, H.; Chen, X.; Richardson, J. J.; Sun, H.; Caruso, F. pH-Responsive Capsules Engineered from Metal-Phenolic Networks for Anticancer Drug Delivery Small 2015, 11, 2032-2036 10.1002/smll.201403343
39. Ju, Y.; Cui, J.; Müllner, M.; Suma, T.; Hu, M.; Caruso, F. Engineering Low-Fouling and pH-Degradable Capsules through the Assembly of Metal-Phenolic Networks Biomacromolecules 2015, 16, 807-814 10.1021/bm5017139
40. Ju, Y.; Cui, J.; Sun, H.; Müllner, M.; Dai, Y.; Guo, J.; Bertleff-Zieschang, N.; Suma, T.; Richardson, J. J.; Caruso, F. Engineered Metal-Phenolic Capsules Show Tunable Targeted Delivery to Cancer Cells Biomacromolecules 2016, 17, 2268-2276 10.1021/acs.biomac.6b00537
41. 3 Nanospheres and Their Transformation to Hollow Hydroxyapatite Nanospheres J. Colloid Interface Sci. 2010, 352, 393-400 10.1016/j.jcis.2010.08.060
42. Schindelin, J.; Arganda-Carreras, I.; Frise, E.; Kaynig, V.; Longair, M.; Pietzsch, T.; Preibisch, S.; Rueden, C.; Saalfeld, S.; Schmid, B. Fiji: An Open-Source Platform for Biological-Image Analysis Nat. Methods 2012, 9, 676-682 10.1038/nmeth.2019
43. Holten-Andersen, N.; Harrington, M. J.; Birkedal, H.; Lee, B. P.; Messersmith, P. B.; Lee, K. Y. C.; Waite, J. H. pH-Induced Metal-Ligand Cross-Links Inspired by Mussel Yield Self-Healing Polymer Networks with Near-Covalent Elastic Moduli Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 2651-2655 10.1073/pnas.1015862108
44. Sukhorukov, G. B.; Volodkin, D. V.; Gunther, A. M.; Petrov, A. I.; Shenoy, D. B.; Möhwald, H. Porous Calcium Carbonate Microparticles as Templates for Encapsulation of Bioactive Compounds J. Mater. Chem. 2004, 14, 2073-2081 10.1039/B402617A
45. Yashchenok, A.; Parakhonskiy, B.; Donatan, S.; Kohler, D.; Skirtach, A.; Möhwald, H. Polyelectrolyte Multilayer Microcapsules Templated on Spherical, Elliptical and Square Calcium Carbonate Particles J. Mater. Chem. B 2013, 1, 1223-1228 10.1039/c2tb00416j
46. Richardson, J. J.; Maina, J. W.; Ejima, H.; Hu, M.; Guo, J.; Choy, M. Y.; Gunawan, S. T.; Lybaert, L.; Hagemeyer, C. E.; De Geest, B. G.; Caruso, F. Versatile Loading of Diverse Cargo into Functional Polymer Capsules Adv. Sci. 2015, 2, 1400007 10.1002/advs.201400007
47. Cedervall, T.; Lynch, I.; Lindman, S.; Berggård, T.; Thulin, E.; Nilsson, H.; Dawson, K. A.; Linse, S. Understanding the Nanoparticle-Protein Corona Using Methods to Quantify Exchange Rates and Affinities of Proteins for Nanoparticles Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 2050-2055 10.1073/pnas.0608582104
48. Milani, S.; Baldelli Bombelli, F.; Pitek, A. S.; Dawson, K. A.; Rädler, J. Reversible versus Irreversible Binding of Transferrin to Polystyrene Nanoparticles: Soft and Hard Corona ACS Nano 2012, 6, 2532-2541 10.1021/nn204951s
49. Jedlovszky-Hajdú, A. l.; Bombelli, F. B.; Monopoli, M. P.; Tombácz, E.; Dawson, K. A. Surface Coatings Shape the Protein Corona of Spions with Relevance to Their Application in Vivo Langmuir 2012, 28, 14983-14991 10.1021/la302446h
50. Hühn, D.; Kantner, K.; Geidel, C.; Brandholt, S.; De Cock, I.; Soenen, S. J.; Rivera-Gil, P.; Montenegro, J.-M.; Braeckmans, K.; Müllen, K. 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
51. Murohashi, M.; Hinohara, K.; Kuroda, M.; Isagawa, T.; Tsuji, S.; Kobayashi, S.; Umezawa, K.; Tojo, A.; Aburatani, H.; Gotoh, N. Gene Set Enrichment Analysis Provides Insight into Novel Signalling Pathways in Breast Cancer Stem Cells Br. J. Cancer 2010, 102, 206-212 10.1038/sj.bjc.6605468
52. Lesniak, A.; Salvati, A.; Santos-Martinez, M. J.; Radomski, M. W.; Dawson, K. A.; Åberg, C. Nanoparticle Adhesion to the Cell Membrane and Its Effect on Nanoparticle Uptake Efficiency J. Am. Chem. Soc. 2013, 135, 1438-1444 10.1021/ja309812z
53. Papadopoulou, A.; Frazier, R. A. Characterization of Protein-Polyphenol Interactions Trends Food Sci. Technol. 2004, 15, 186-190 10.1016/j.tifs.2003.09.017
54. Shutava, T. G.; Balkundi, S. S.; Lvov, Y. M. (-)-Epigallocatechin Gallate/Gelatin Layer-by-Layer Assembled Films and Microcapsules J. Colloid Interface Sci. 2009, 330, 276-283 10.1016/j.jcis.2008.10.082
55. Williamson, M. P.; McCormick, T. G.; Nance, C. L.; Shearer, W. T. Epigallocatechin Gallate, the Main Polyphenol in Green Tea, Binds to the T-Cell Receptor, CD4: Potential for HIV-1 Therapy J. Allergy Clin. Immunol. 2006, 118, 1369-1374 10.1016/j.jaci.2006.08.016