Intravenous delivery of hydrophobin-functionalized porous silicon nanoparticles: Stability, plasma protein adsorption and biodistribution

Molecular Pharmaceutics

Volumn 9, Issue 3, 2012, Pages 654-663

  Sarparanta, Mirkka ^a   Bimbo, Luis M ^a   Rytkoänen, Jussi ^b   Mäkilä, Ermei ^c   Laaksonen, Timo J ^a   Laaksonen, Päivi ^d   Nyman, Markus ^a   Salonen, Jarno ^c   Linder, Markus B ^d   Hirvonen, Jouni ^a   Santos, Hélder A ^a   Airaksinen, Anu J ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c UNIVERSITY OF TURKU   (Finland)

^d VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

Author keywords

biodistribution; hydrophobin; nanoparticle; porous silicon; protein adsorption

Indexed keywords

FIBRINOGEN; FLUORINE 18; FUNCTIONAL GROUP; HYDROPHOBIN; NANOPARTICLE; SERUM ALBUMIN; SILICON; THERMALLY HYDROCARBONIZED POROUS SILICON NANOPARTICLE FLUORINE 18; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN RECOGNITION; ARTICLE; BIOCOMPATIBILITY; CONTROLLED STUDY; DRUG ADSORPTION; DRUG COATING; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG LIVER LEVEL; DRUG STABILITY; HUMAN; HUMAN TISSUE; HYDROPHOBICITY; HYPOCREA JECORINA; IN VIVO STUDY; ISOTOPE LABELING; NONHUMAN; PHAGOCYTE; PLASMA PROTEIN BINDING; POROSITY; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RADIOMETRY; RAT;

ADSORPTION; ANIMALS; BLOOD PROTEINS; CELL LINE; DRUG STABILITY; HEP G2 CELLS; HUMANS; MICE; NANOPARTICLES; POROSITY; SILICON;

EID: 84858052867     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp200611d     Document Type: Article

References (53)

1. Salonen, J.; Kaukonen, A. M.; Hirvonen, J.; Lehto, V. Mesoporous Silicon in Drug Delivery Applications J. Pharm. Sci. 2008, 97, 632-653 (Pubitemid 351293873)
2. Anglin, E. J.; Cheng, L.; Freeman, W. R. Sailor, M.J. Porous Silicon in Drug Delivery Devices and Materials Adv. Drug Delivery Rev. 2008, 60, 1266-1277
3. Prestidge, C. A.; Barnes, T. J.; Lau, C.; Barnett, C.; Loni, A.; Canham, L. Mesoporous Silicon: a Platform for the Delivery of Therapeutics Expert Opin. Drug Delivery 2007, 4, 101-110 (Pubitemid 46389909)
4. Wang, F.; Hui, H.; Barnes, T. J.; Barnett, C.; Prestidge, C. A. Oxidized Mesoporous Silicon Microparticles for Improved Oral Delivery of Poorly Soluble Drugs Mol. Pharmaceutics 2010, 7, 227-236
5. Bimbo, L. M.; Mäkilä, E.; Laaksonen, T.; Lehto, V.; Salonen, J.; Hirvonen, J.; Santos, H. A. Drug Permeation Across Intestinal Epithelial Cells Using Porous Silicon Nanoparticles Biomaterials 2011, 32, 2625-2633
6. Salonen, J.; Laitinen, L.; Kaukonen, A. M.; Tuura, J.; Bjoärkqvist, M.; Heikkilä, T.; Vähä-Heikkilä, K.; Hirvonen, J.; Lehto, V.-P. Mesoporous Silicon Microparticles for Oral Drug Delivery: Loading and Release of Five Model Drugs J. Controlled Release 2005, 108, 362-374 (Pubitemid 41608668)
7. Kilpeläinen, M.; Riikonen, J.; Vlasova, M. A.; Huotari, A.; Lehto, V. P.; Salonen, J.; Herzig, K. H.; Järvinen, K. In vivo Delivery of a Peptide, Ghrelin Antagonist, with Mesoporous Silicon Microparticles J. Controlled Release 2009, 137, 166-170
8. Kilpeläinen, M.; Moänkäre, J.; Vlasova, M. A.; Riikonen, J.; Lehto, V.; Salonen, J.; Järvinen, K.; Herzig, K. Nanostructured Porous Silicon Microparticles Enable Sustained Peptide (Melanotan II) Delivery Eur. J. Pharm. Biopharm. 2011, 77, 20-25
9. Tanaka, T.; Mangala, L. S.; Vivas-Mejia, P. E.; Nieves-Alicea, R.; Mann, A. P.; Mora, E.; Han, H.; Shahzad, M. M. K.; Liu, X.; Bhavane, R.; Gu, J.; Fakhoury, J. R.; Chiappini, C.; Lu, C.; Matsuo, K.; Godin, B.; Stone, R. L.; Nick, A. M.; Lopez-Berestein, G.; Sood, A. K.; Ferrari, M. Sustained Small Interfering RNA Delivery by Mesoporous Silicon Particles Cancer Res. 2010, 70, 3687-3696
10. Tasciotti, E.; Liu, X.; Bhavane, R.; Plant, K.; Leonard, A. D.; Price, B. K.; Cheng, M. M.; Decuzzi, P.; Tour, J. M.; Robertson, F.; Ferrari, M. Mesoporous Silicon Particles as a Multistage Delivery System for Imaging and Therapeutic Applications Nat. Nanotechnol. 2008, 3, 151-157 (Pubitemid 351355132)
11. Godin, B.; Gu, J.; Serda, R. E.; Bhavane, R.; Tasciotti, E.; Chiappini, C.; Liu, X.; Tanaka, T.; Decuzzi, P.; Ferrari, M. Tailoring the Degradation Kinetics of Mesoporous Silicon Structures Through PEGylation J. Biomed. Mater. Res., Part A 2010, 94A, 1236-1243
12. Canham, L. T.; Reeves, C. L.; Newey, J. P.; Houlton, M. R.; Cox, T. I.; Buriak, J. M.; Stewart, M. P. Derivatized Mesoporous Silicon with Dramatically Improved Stability in Simulated Human Blood Plasma Adv. Mater. 1999, 11, 1505-1507 (Pubitemid 30519083)
13. Dobrovolskaia, M. A.; Aggarwal, P.; Hall, J. B.; McNeil, S. E. Preclinical Studies To Understand Nanoparticle Interaction with the Immune System and Its Potential Effects on Nanoparticle Biodistribution Mol. Pharmaceutics 2008, 5, 487-495
14. Cedervall, T.; Lynch, I.; Lindman, S.; Berggǎrd, 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 (Pubitemid 46391350)
15. Walczyk, D.; Bombelli, F. B.; Monopoli, M. P.; Lynch, I.; Dawson, K. A. What the Cell "Sees" in Bionanoscience J. Am. Chem. Soc. 2010, 132, 5761-5768
16. Aggarwal, P.; Hall, J. B.; McLeland, C. B.; Dobrovolskaia, M. A.; McNeil, S. E. Nanoparticle Interaction with Plasma Proteins as it Relates to Particle Biodistribution, Biocompatibility and Therapeutic Efficacy Adv. Drug Delivery Rev. 2009, 61, 428-437
17. Gessner, A.; Waicz, R.; Lieske, A.; Paulke, B.; Mäder, K.; Muäller, R. H. Nanoparticles with Decreasing Surface Hydrophobicities: Influence on Plasma Protein Adsorption Int. J. Pharm. 2000, 196, 245-249 (Pubitemid 30105753)
18. Gessner, A.; Lieske, A.; Paulke, B.; Muäller, R. H. Functional Groups on Polystyrene Model Nanoparticles: Influence on Protein Adsorption J. Biomed. Mater. Res., Part A 2003, 65A, 319-326 (Pubitemid 37517267)
19. Tenzer, S.; Docter, D.; Rosfa, S.; Wlodarski, A.; Kuharev, J.; Rekik, A.; Knauer, S. K.; Bantz, C.; Nawroth, T.; Bier, C.; Sirirattanapan, J.; Mann, W.; Treuel, L.; Zellner, R.; Maskos, M.; Schild, H.; Stauber, R. H. Nanoparticle Size Is a Critical Physicochemical Determinant of the Human Blood Plasma Corona: A Comprehensive Quantitative Proteomic Analysis ACS Nano 2011, 5, 7155-7167
20. Owens, D. E., III; Peppas, N. A. Opsonization, Biodistribution, and Pharmacokinetics of Polymeric Nanoparticles Int. J. Pharm. 2006, 307, 93-102 (Pubitemid 41773257)
21. Simberg, D.; Park, J.; Karmali, P. P.; Zhang, W.; Merkulov, S.; McCrae, K.; Bhatia, S. N.; Sailor, M.; Ruoslahti, E. Differential Proteomics Analysis of the Surface Heterogeneity of Dextran Iron Oxide Nanoparticles and the Implications for Their In Vivo Clearance Biomaterials 2009, 30, 3926-3933
22. Ogawara, K.; Furumoto, K.; Nagayama, S.; Minato, K.; Higaki, K.; Kai, T.; Kimura, T. Pre-coating with Serum Albumin Reduces Receptor-Mediated Hepatic Disposition of Polystyrene Nanosphere: Implications for Rational Design of Nanoparticles J. Controlled Release 2004, 100, 451-455 (Pubitemid 39572924)
23. Tanaka, T.; Godin, B.; Bhavane, R.; Nieves-Alicea, R.; Gu, J.; Liu, X.; Chiappini, C.; Fakhoury, J. R.; Amra, S.; Ewing, A.; Li, Q.; Fidler, I. J.; Ferrari, M. In Vivo Evaluation of Safety of Nanoporous Silicon Carriers Following Single and Multiple Dose Intravenous Administrations in Mice Int. J. Pharm. 2010, 402, 190-197
24. Serda, R. E.; Gu, J.; Bhavane, R. C.; Liu, X.; Chiappini, C.; Decuzzi, P.; Ferrari, M. The Association of Silicon Microparticles with Endothelial Cells in Drug Delivery to the Vasculature Biomaterials 2009, 30, 2440-2448
25. Park, J.; Gu, L.; von Maltzahn, G.; Ruoslahti, E.; Bhatia, S. N.; Sailor, M. J. Biodegradable Luminescent Porous Silicon Nanoparticles for In Vivo Applications Nat. Mater. 2009, 8, 331-336
26. Hakanpää, J.; Paananen, A.; Askolin, S.; Nakari- Setälä, T.; Parkkinen, T.; Penttilä, M.; Linder, M. B.; Rouvinen, J. Atomic Resolution Structure of the HFBII Hydrophobin, a Self-assembling Amphiphile J. Biol. Chem. 2004, 279, 534-539 (Pubitemid 38044855)
27. Linder, M. B. Hydrophobins: Proteins that Self-Assemble at Interfaces Curr. Opin. Colloid Interface Sci. 2009, 14, 356-363
28. Haas Jimoh Akanbi, M.; Post, E.; Meter-Arkema, A.; Rink, R.; Robillard, G. T.; Wang, X.; Woästen, H. A. B.; Scholtmeijer, K. Use of Hydrophobins in Formulation of Water Insoluble Drugs for Oral Administration Colloids Surf., B 2010, 75, 526-531
29. Valo, H. K.; Laaksonen, P. H.; Peltonen, L. J.; Linder, M. B.; Hirvonen, J. T.; Laaksonen, T. J. Multifunctional Hydrophobin: Toward Functional Coatings for Drug Nanoparticles ACS Nano 2010, 4, 1750-1758
30. Varjonen, S.; Laaksonen, P.; Paananen, A.; Valo, H.; Hahl, H.; Laaksonen, T.; Linder, M. B. Self-Assembly of Cellulose Nanofibrils by Genetically Engineered Fusion Proteins Soft Matter 2011, 7, 2402-2411
31. Valo, H.; Kovalainen, M.; Laaksonen, P.; Häkkinen, M.; Auriola, S.; Peltonen, L.; Linder, M.; Järvinen, K.; Hirvonen, J.; Laaksonen, T. Immobilization of Protein-Coated Drug Nanoparticles in Nanofibrillar Cellulose Matrices-Enhanced Stability and Release J. Controlled Release 2011, 156, 390-397
32. Bimbo, L. M.; Mäkilä, E.; Raula, J.; Laaksonen, T.; Laaksonen, P.; Strommer, K.; Kauppinen, E. I.; Salonen, J.; Linder, M. B.; Hirvonen, J.; Santos, H. A. Functional Hydrophobin-Coating of Thermally Hydrocarbonized Porous Silicon Microparticles Biomaterials 2011, 32, 9089-9099
33. Janssen, M. I.; van Leeuwen, M. B. M.; Scholtmeijer, K.; van Kooten, T. G.; Dijkhuizen, L.; Woästen, H. A. B. Coating with Genetic Engineered Hydrophobin Promotes Growth of Fibroblasts on a Hydrophobic Solid Biomaterials 2002, 23, 4847-4854 (Pubitemid 35286707)
34. Scholtmeijer, K.; Janssen, M. I.; Gerssen, B.; de Vocht, M. L.; van Leeuwen, B. M.; van Kooten, T. G.; Wosten, H. A. B.; Wessels, J. G. H. Surface Modifications Created by Using Engineered Hydrophobins Appl. Environ. Microbiol. 2002, 68, 1367-1373 (Pubitemid 34205378)
35. Aimanianda, V.; Bayry, J.; Bozza, S.; Kniemeyer, O.; Perruccio, K.; Elluru, S. R.; Clavaud, C.; Paris, S.; Brakhage, A. A.; Kaveri, S. V.; Romani, L.; Latge, J. Surface Hydrophobin Prevents Immune Recognition of Airborne Fungal Spores Nature 2009, 460, 1117-1121
36. Bimbo, L. M.; Sarparanta, M.; Santos, H. A.; Airaksinen, A. J.; Mäkilä, E.; Laaksonen, T.; Peltonen, L.; Lehto, V.; Hirvonen, J.; Salonen, J. Biocompatibility of Thermally Hydrocarbonized Porous Silicon Nanoparticles and their Biodistribution in Rats ACS Nano 2010, 4, 3023-3032
37. Salonen, J.; Bjoärkqvist, M.; Laine, E.; Niinistoä, L. Stabilization of Porous Silicon Surface by Thermal Decomposition of Acetylene Appl. Surf. Sci. 2004, 225, 389-394
38. 18F-Labeled Modified Porous Silicon Particles for Investigation of Drug Delivery Carrier Distribution in Vivo with Positron Emission Tomography Mol. Pharmaceutics 2011, 8, 1799-1806
39. 125I-Containing Acylating Agent Biochem. J. 1973, 133, 529-538
40. Li, C.; Greenwood, T. R.; Bhujwalla, Z. M.; Glunde, K. Synthesis and Characterization of Glucosamine-Bound Near-Infrared Probes for Optical Imaging Org. Lett. 2006, 8, 3623-3626 (Pubitemid 44378323)
41. Cox, A. R.; Cagnol, F.; Russell, A. B.; Izzard, M. J. Surface Properties of Class II Hydrophobins from Trichoderma reesei and Influence on Bubble Stability Langmuir 2007, 23, 7995-8002 (Pubitemid 47155306)
42. Santos, H. A.; Riikonen, J.; Salonen, J.; Mäkilä, E.; Heikkilä, T.; Laaksonen, T.; Peltonen, L.; Lehto, V.; Hirvonen, J. In Vitro Cytotoxicity of Porous Silicon Microparticles: Effect of the Particle Concentration, Surface Chemistry and Size Acta Biomater. 2010, 6, 2721-2731
43. Choi, J.; Zhang, Q.; Reipa, V.; Wang, N. S.; Stratmeyer, M. E.; Hitchins, V. M.; Goering, P. L. Comparison of Cytotoxic and Inflammatory Responses of Photoluminescent Silicon Nanoparticles with Silicon Micron-Sized Particles in RAW 264.7 macrophages J. Appl. Toxicol. 2009, 29, 52-60
44. Serda, R. E.; Blanco, E.; Mack, A.; Stafford, S. J.; Amra, S.; Li, Q.; van, d.V.; Tanaka, T.; Torchilin, V. P.; Wiktorowicz, J. E.; Ferrari, M. Proteomic Analysis of Serum Opsonins Impacting Biodistribution and Cellular Association of Porous Silicon Microparticles Mol. Imaging 2011, 10, 43-55
45. 18F]fluoride Kinetics in Rats J. Nucl. Med. 1979, 20, 1150-1157 (Pubitemid 10209199)
46. Vroman, L.; Adams, A.; Fischer, G.; Munoz, P. Interaction of High Molecular Weight Kininogen, Factor XII, and Fibrinogen in plasma at interfaces Blood 1980, 55, 156-159 (Pubitemid 10211912)
47. Goäppert, T. M.; Muäller, R. H. Adsorption Kinetics of Plasma Proteins on Solid Lipid Nanoparticles for Drug Targeting Int. J. Pharm. 2005, 302, 172-186
48. Swanson, J. A.; Hoppe, A. D. The Coordination of Signaling During Fc Receptor-Mediated Phagocytosis J. Leukocyte Biol. 2004, 76, 1093-1103 (Pubitemid 39602944)
49. Moghimi, S. M.; Hunter, A. C.; Murray, J. C. Long-Circulating and Target-Specific Nanoparticles: Theory to Practice Pharmacol. Rev. 2001, 53, 283-318 (Pubitemid 32476118)
50. Dams, E. T. M.; Laverman, P.; Oyen, W. J. G.; Storm, G.; Scherphof, G. L.; van der Meer, J. W. M.; Corstens, F. H. M.; Boerman, O. C. Accelerated Blood Clearance and Altered Biodistribution of Repeated Injections of Sterically Stabilized Liposomes J. Pharmacol. Exp. Ther. 2000, 292, 1071-1079 (Pubitemid 30136603)
51. Yan, X.; Kuipers, F.; Havekes, L. M.; Havinga, R.; Dontje, B.; Poelstra, K.; Scherphof, G. L.; Kamps, J. A. A. M. The Role of Apolipoprotein E in the Elimination of Liposomes from Blood by Hepatocytes in the Mouse Biochem. Biophys. Res. Commun. 2005, 328, 57-62 (Pubitemid 40164635)
52. Bartl, M. M.; Luckenbach, T.; Bergner, O.; Ullrich, O.; Koch-Brandt, C. Multiple Receptors Mediate apoJ-Dependent Clearance of Cellular Debris into Nonprofessional Phagocytes Exp. Cell Res. 2001, 271, 130-141 (Pubitemid 33071000)
53. Soo Choi, H.; Liu, W.; Misra, P.; Tanaka, E.; Zimmer, J. P.; Itty Ipe, B.; Bawendi, M. G.; Frangioni, J. V. Renal Clearance of Quantum Dots Nat. Biotechnol. 2007, 25, 1165-1170 (Pubitemid 47538116)