Identification of polyethylene glycol-resistant macrophages on stealth imaging in vitro using fluorescent organosilica nanoparticles

ACS Nano

Volumn 9, Issue 2, 2015, Pages 1058-1071

  Nakamura, Michihiro ^a   Hayashi, Koichiro ^a,e   Nakano, Mutsuki ^a,b   Kanadani, Takafumi ^a,b   Miyamoto, Kazue ^a,b   Kori, Toshinari ^c   Horikawa, Kazuki ^d  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

^c Tokushima Prefectural Industrial Technology Center   (Japan)

^d UNIVERSITY OF TOKUSHIMA   (Japan)

^e NAGOYA UNIVERSITY   (Japan)

Author keywords

accelerated blood clearance; macrophages; polyethylene glycol; single cell analysis; stealth nanoparticles

Indexed keywords

ALIPHATIC COMPOUNDS; FLUORESCENCE IMAGING; FUNCTION EVALUATION; MACROPHAGES; POLYETHYLENE GLYCOLS; POLYETHYLENES; SILICA;

ACCELERATED BLOOD CLEARANCES; FLOW CYTOMETRY ANALYSIS; FUNCTIONALIZED; MICROSCOPIC IMAGING; ONE-STEP PROCESS; PEGYLATED NANOPARTICLE; SINGLECELL ANALYSIS; STEALTH NANOPARTICLES;

NANOPARTICLES;

(3-MERCAPTOPROPYL)TRIMETHOXYSILANE; BIOLOGICAL MARKER; DRUG CARRIER; FLUORESCENT DYE; MACROGOL DERIVATIVE; NANOPARTICLE; ORGANOSILICON DERIVATIVE; SILANE DERIVATIVE;

ANIMAL; CHEMISTRY; FLUORESCENCE MICROSCOPY; MACROPHAGE; METABOLISM; MOUSE; SURFACE PROPERTY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; BIOMARKERS; DRUG CARRIERS; FLUORESCENT DYES; MACROPHAGES; MICE; MICROSCOPY, FLUORESCENCE; NANOPARTICLES; ORGANOSILICON COMPOUNDS; POLYETHYLENE GLYCOLS; SILANES; SURFACE PROPERTIES;

EID: 84923509070     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn502319r     Document Type: Article

References (77)

1. Moghimi, S. M.; Hunter, A. C.; Murray, J. C. Nanomedicine: Current Status and Future Prospects FASEB J. 2005, 19, 311-330
2. Liu, Y.; Miyoshi, H.; Nakamura, M. Nanomedicine for Drug Delivery and Imaging: A Promising Avenue for Cancer Therapy and Diagnosis Using Targeted Functional Nanoparticles Int. J. Cancer 2007, 120, 2527-2537
3. Liong, M.; Lu, J.; Kovochich, M.; Xia, T.; Ruehm, S. G.; Nel, A. E.; Tamanoi, F.; Zink, J. I. Multifunctional Inorganic Nanoparticles for Imaging, Targeting, and Drug Delivery ACS Nano 2008, 2, 889-896
4. Namiki, Y.; Fuchigami, T.; Tada, N.; Kawamura, R.; Matsunuma, S.; Kitamoto, Y.; Nakagawa, M. Nanomedicine for Cancer: Lipid-Based Nanostructures for Drug Delivery and Monitoring Acc. Chem. Res. 2011, 44, 1080-1093
5. Tassa, C.; Shaw, S. Y.; Weissleder, R. Dextran-Coated Iron Oxide Nanoparticles: A Versatile Platform for Targeted Molecular Imaging, Molecular Diagnostics, and Therapy Acc. Chem. Res. 2011, 44, 842-852
6. Lee, J. E.; Lee, N.; Kim, T.; Kim, J.; Hyeon, T. Multifunctional Mesoporous Silica Nanocomposite Nanoparticles for Theranostic Applications Acc. Chem. Res. 2011, 44, 893-902
7. Khandare, J.; Calderón, M.; Dagia, N. M.; Haag, R. Multifunctional Dendritic Polymers in Nanomedicine: Opportunities and Challenges Chem. Soc. Rev. 2012, 41, 2824-2848
8. Yang, P.; Gai, S.; Lin, J. Functionalized Mesoporous Silica Materials for Controlled Drug Delivery Chem. Soc. Rev. 2012, 41, 3679-3698
9. Li, Z.; Barnes, J. C.; Bosoy, A.; Stoddart, J. F.; Zink, J. I. Mesoporous Silica Nanoparticles in Biomedical Applications Chem. Soc. Rev. 2012, 41, 2590-2605
10. Dreaden, E. C.; Alkilany, A. M.; Huang, X.; Murphy, C. J.; El-Sayed, M. A. The Golden Age: Gold Nanoparticles for Biomedicine Chem. Soc. Rev. 2012, 41, 2740-2779
11. Rosen, J. E.; Chan, L.; Shieh, D. B.; Gu, F. X. Iron Oxide Nanoparticles for Targeted Cancer Imaging and Diagnostics Nanomedicine 2012, 8, 275-290
12. Doane, T. L.; Burda, C. The Unique Role of Nanoparticles in Nanomedicine: Imaging, Drug Delivery and Therapy Chem. Soc. Rev. 2012, 41, 2885-2911
13. Matsumura, Y.; Maeda, H. A New Concept for Macromolecular Therapeutics in Cancer Chemotherapy: Mechanism of Tumoritropic Accumulation of Proteins and the Antitumor Agent Smancs Cancer Res. 1986, 46, 6387-6392
14. Maeda, H.; Matsumura, Y. Tumoritropic and Lymphotropic Principles of Macromolecular Drugs Crit. Rev. Ther. Drug Carrier Syst. 1989, 6, 193-210
15. Fang, J.; Nakamura, H.; Maeda, H. The EPR effect: Unique Features of Tumor Blood Vessels for Drug Delivery, Factors Involved, and Limitations and Augmentation of the Effect Adv. Drug Delivery Rev. 2011, 63, 136-151
16. Moghimi, S. M.; Hunter, A. C.; Murray, J. C. Long-Circulating and Target-Specific Nanoparticles: Theory to Practice Pharmacol. Rev. 2001, 53, 283-318
17. Dams, E. T.; Laverman, P.; Oyen, W. J.; Storm, G.; Scherphof, G. L.; van Der Meer, J. W.; Corstens, F. H.; Boerman, O. C. Accelerated Blood Clearance and Altered Biodistribution of Repeated Injections of Sterically Stabilized Liposomes J. Pharmacol. Exp. Ther. 2000, 29, 1071-1079
18. Laverman, P.; Carstens, M. G.; Boerman, O. C.; Dams, E. T.; Oyen, W. J.; van Rooijen, N.; Corstens, F. H.; Storm, G. Factors Affecting the Accelerated Blood Clearance of Polyethylene Glycol-Liposomes Upon Repeated Injection J. Pharmacol. Exp. Ther. 2001, 298, 607-612
19. Ishida, T.; Maeda, R.; Ichihara, M.; Mukai, Y.; Motoki, Y.; Manabe, Y.; Irimura, K.; Kiwada, H. The Accelerated Clearance on Repeated Injection of PEGylated Liposomes in Rats: Laboratory and Histopathological Study Cell. Mol. Biol. Lett. 2002, 7, 286
20. Ishida, T.; Maeda, R.; Ichihara, M.; Irimura, K.; Kiwada, H. Accelerated Clearance of PEGylated Liposomes in Rats After Repeated Injections J. Controlled Release 2003, 88, 35-42
21. Abu Lila, A. S.; Kiwada, H.; Ishida, T. The Accelerated Blood Clearance (ABC) Phenomenon: Clinical Challenge and Approaches to Manage J. Controlled Release 2013, 172, 38-47
22. Ishida, T.; Wang, X.; Shimizu, T.; Nawata, K.; Kiwada, H. PEGylated Liposomes Elicit an Anti-PEG IgM Response in a T Cell-Independent Manner J. Controlled Release 2007, 122, 349-355
23. Wang, X.; Ishida, T.; Kiwada, H. Anti-PEG IgM Elicited By Injection of Liposomes Is Involved in the Enhanced Blood Clearance of a Subsequent Dose of PEGylated Liposomes J. Controlled Release 2007, 119, 236-244
24. Nakamura, M.; Ishimura, K. Synthesis and Characterization of Organosilica Nanoparticles Prepared from 3-Mercaptopropyltrimethoxysilane as the Single Silica Source J. Phys. Chem. C 2007, 111, 18892-18898
25. Nakamura, M.; Ishimura, K. One-Pot Synthesis and Characterization of Three Kinds of Thiol-Organosilica Nanoparticles Langmuir 2008, 24, 5099-5108
26. Nakamura, M.; Ishimura, K. Size-Controlled, One-Pot Synthesis, Characterization, and Biological Applications of Epoxy-Organosilica Particles Possessing Positive Zeta Potential as Prepared Langmuir 2008, 24, 12228-12234
27. Nakamura, M. Nanostructured Oxides; Wiley-VCH: Weinheim, 2009; pp 109-161.
28. Nakamura, M.; Ozaki, S.; Abe, M.; Doi, H.; Matsumoto, T.; Ishimura, K. One-pot Synthesis, Characterization, and Biological Applications of Size-Controlled Thiol-Organosilica Nanoparticles Prepared from 3-Mercaptopropyltrimethoxysilane Colloids Surf. B: Biointerfaces 2010, 79, 19-26
29. Nakamura, M.; Ozaki, S.; Abe, M.; Matsumoto, T.; Ishimura, K. One-pot synthesis and Characterization of Dual Fluorescent Thiol-Organosilica Nanoparticles as Non-Photoblinking Quantum Dots and Their Applications for Biological Imaging J. Mater. Chem. 2011, 21, 4689-4695
30. Nakamura, M.; Awaad, A.; Hayashi, K.; Ochiai, K.; Ishimura, K. Thiol-organosilica Particles Internally Functionalized with Propidium Iodide as a Multicolor Fluorescence and X-Ray Computed Tomography Probe and Application for Non-Invasive Functional Gastrointestinal Tract Imaging Chem. Mater. 2012, 24, 3772-3779
31. Nakamura, M. Biomedical Applications of Organosilica Nanoparticles Toward Theranostics Nanotechnol. Rev. 2012, 1, 469-491
32. Awaad, A.; Nakamura, M.; Ishimura, K. Imaging of Size Dependent Uptake and Identification of Novel Pathway in Mouse Peyer's Patches Using Fluorescent Organosilica Particles Nanomed.: NBM 2012, 8, 627-636
33. Awaad, A.; Nakamura, M.; Ishimura, K. Histochemical and Biochemical Analysis of the Size-Dependent Nanoimmunoresponse in Mouse Peyer's Patches Using Fluorescent Organosilica Particles Int. J. Nanomed. 2012, 7, 1423-1439
34. Nakamura, M.; Miyamoto, K.; Hayashi, K.; Awaad, A.; Ochiai, M.; Ishimura, K. Time-Lapse Fluorescence Imaging and Quantitative Single Cell and Endosomal Analysis of Peritoneal Macrophages Using Fluorescent Organosilica Nanoparticles Nanomed.: NBM 2013, 9, 274-283
35. Nakamura, M.; Ishimura, K. Rapid Size Evaluation of Nanoparticles Using Flow Cytometry Adv. Sci. Lett. 2010, 3, 130-137
36. Tirosh, O.; Barenholz, Y.; Katzhendler, J.; Priev, A. Hydration of Polyethylene Glycol-Grafted Liposomes Biophys. J. 1998, 74, 1371-1379
37. Gref, R.; Lück, M.; Quellec, P.; Marchand, M.; Dellacherie, E.; Harnisch, S.; Blunk, T.; Müller, R. H. '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: Biointerfaces 2000, 18, 301-313
38. Medintz, I. L.; Uyeda, H. T.; Goldman, E. R.; Mattoussi, H. Quantum Dot Bioconjugates for Imaging, Labelling and Sensing Nat. Mater. 2005, 4, 435-446
39. Hanaki, K.; Momo, A.; Oku, T.; Komoto, A.; Maenosono, S.; Yamaguchi, Y.; Yamamoto, K. Semiconductor Quantum Dot/Albumin Complex Is a Long-life and Highly Photostable Endosome Marker Biochem. Biophys. Res. Commun. 2003, 302, 496-501
40. Mancini, M. C.; Kairdolf, B. A.; Smith, A. M.; Nie, S. Oxidative Quenching and Degradation of Polymer-Encapsulated Quantum Dots: New Insights into The Long-Term Fate and Toxicity Of Nanocrystals In Vivo J. Am. Chem. Soc. 2008, 130, 10836-10837
41. Heald, C. R.; Stolnik, S.; Kujawinski, K. S.; De Matteis, C.; Garnett, M. C.; Illum, L.; Davis, S. S.; Purkiss, S. C.; Barlow, R. J.; Gellert, P. R. Poly(Lactic Acid)-Poly(Ethylene Oxide) (PLA-PEG) Nanoparticles: NMR Studies of the Central Solid Like PLA Core and the Liquid PEG Corona Langmuir 2002, 18, 3669-3675
42. Moffatt, S.; Cristiano, R. J. Uptake Characteristics of NGR-Coupled Stealth PEI/PDNA Nanoparticles Loaded with PLGA-PEG-PLGA Tri-Block Copolymer for Targeted Delivery to Human Monocyte- Derived Dendritic Cells Int. J. Pharm. 2006, 321, 143-154
43. Kenausis, G. L.; Vörös, J.; Elbert, D. L.; Huang, N.; Hofer, R.; Ruiz-Taylor, L.; Textor, M.; Hubbell, J. A.; Spencer, N. D. Poly(l-lysine)-g-Poly(ethylene glycol) Layers on Metal Oxide Surfaces: Attachment Mechanism and Effects of Polymer Architecture on Resistance to Protein Adsorption J. Phys. Chem. B 2000, 104, 3298-3309
44. Szleifer, I. Protein Adsorption on Surfaces with Grafted Polymers: A Theoretical Approach Biophys. J. 1997, 72, 595-612
45. Jeon, S. I.; Lee, J. H.; Andrade, J. D.; De Gennes, P. G. Protein-Surface Interactions in The Presence of Polyethylene Oxide: I. Simplified Theory J. Colloid Interface Sci. 1991, 142, 149-158
46. Satulovsky, J.; Carignano, M. A.; Szleifer, I. Kinetic and Thermodynamic Control of Protein Adsorption Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 9037-9041
47. Storm, G.; Belliot, S. O.; Daemen, T.; Lasic, D. D. Surface Modification of Nanoparticles to Oppose Uptake By the Mononuclear Phagocyte System Adv. Drug Delivery Rev. 1995, 17, 31-48
48. Mu, Q.; Li, Z.; Li, X.; Mishra, S. R.; Zhang, B.; Si, Z.; Yan, B. Characterization of Protein Clusters of Diverse Magnetic Nanoparticles and Their Dynamic Interactions with Human Cells J. Phys. Chem. C 2009, 113, 5390-5395
49. Walkey, C. D.; Olsen, J. B.; Guo, H.; Emili, A.; Chan, W. C. Nanoparticle Size and Surface Chemistry Determine Serum Protein Adsorption and Macrophage Uptake J. Am. Chem. Soc. 2012, 134, 2139-2147
50. Benetti, F.; Fedel, M.; Minati, L.; Speranza, G.; Migliaresi, C. Gold Nanoparticles: Role of Size and Surface Chemistry on Blood Protein Adsorption J. Nanopart. Res. 2013, 15, 1-9
51. Albanese, A.; Walkey, C. D.; Olsen, J. B.; Guo, H.; Emili, A.; Chan, W. C. Secreted Biomolecules Alter the Biological Identity and Cellular Interactions of Nanoparticles ACS Nano 2014, 8, 5515-5526
52. Ishida, T.; Harada, M.; Wang, X. Y.; Ichihara, M.; Irimura, K.; Kiwada, H. Accelerated Blood Clearance of PEGylated Liposomes Following Preceding Liposome Injection: Effects of Lipid Dose and PEG Surface-Density and Chain Length of the First-Dose Liposomes J. Controlled Release 2005, 105, 305-317
53. Perry, J. L.; Reuter, K. G.; Kai, M. P.; Herlihy, K. P.; Jones, S. W.; Luft, J. C.; Napier, M.; Bear, J. E.; DeSimone, J. M. PEGylated PRINT Nanoparticles: The Impact of PEG Density on Protein Binding, Macrophage Association, Biodistribution, and Pharmacokinetics Nano Lett. 2012, 12, 5304-5310
54. Rejman, J.; Oberle, V.; Zuhorn, I. S.; Hoekstra, D. Size-Dependent Internalization of Particles via the Pathways of Clathrin-and Caveolae-Mediated Endocytosis Biochem. J. 2004, 377, 159-169
55. Mohanraj, V. J.; Chen, Y. Nanoparticles-A Review Trop. J. Pharm. Res. 2006, 5, 561-573
56. Chithrani, B. D.; Ghazani, A. A.; Chan, W. C. Determining the Size and Shape Dependence of Gold Nanoparticle Uptake into Mammalian Cells Nano Lett. 2006, 6, 662-668
57. Motskin, M.; Müller, K. H.; Genoud, C.; Monteith, A. G.; Skepper, J. N. The Sequestration of Hydroxyapatite Nanoparticles by Human Monocyte-Macrophages in a Compartment that Allows Free Diffusion with the Extracellular Environment Biomaterials 2011, 32, 9470-9482
58. Kang, Y. S.; Yamazaki, S.; Iyoda, T.; Pack, M.; Bruening, S. A.; Kim, J. Y.; Takahara, K.; Inaba, K.; Steinman, R. M.; Park, C. G. SIGN-R1, A Novel C-Type Lectin Expressed by Marginal Zone Macrophages in Spleen, Mediates Uptake of the Polysaccharide Dextran Int. Immunol. 2003, 15, 177-186
59. Kang, Y. S.; Kim, J. Y.; Bruening, S. A.; Pack, M.; Charalambous, A.; Pritsker, A.; Moran, T. M.; Loeffler, J. M.; Steinman, R. M.; Park, C. G. The C-Type Lectin SIGN-R1Mediates Uptake of the Capsular Polysaccharide of Streptococcus Pneumoniae in the Marginal Zone of Mouse Spleen Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 215-220
60. Aderem, A.; Underhill, D. M. Mechanisms of Phagocytosis in Macrophages Annu. Rev. Immunol. 1999, 17, 593-623
61. Greaves, D. R.; Gordon, S. The Macrophage Scavenger Receptor at 30 Years of Age: Current Knowledge and Future challenges J. Lipid Res. 2009, 50, S282-286
62. Ishida, T.; Ichihara, M.; Wang, X.; Yamamoto, K.; Kimura, J.; Majima, E.; Kiwada, H. Injection of PEGylated Liposomes in Rats Elicits PEG-Specific IgM, Which Is Responsible for Rapid Elimination of a Second Dose of PEGylated Liposomes J. Controlled Release 2006, 112, 15-25
63. Ishida, T.; Masuda, K.; Ichikawa, T.; Ichihara, M.; Irimura, K.; Kiwada, H. Accelerated Clearance of a Second Injection of PEGylated Liposomes in Mice Int. J. Pharm. 2003, 255, 167-174
64. 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
65. Martin, F.; Oliver, A. M.; Kearney, J. F. Marginal Zone and B1 B Cells Unite in the Early Response Against T-Independent Blood-Borne Particulate Antigens Immunity 2001, 14, 617-629
66. Zandvoort, A.; Timens, W. The Dual Function of the Splenic Marginal Zone: Essential for Initiation of Anti-TI-2 Responses but also Vital in the General First-Line Defense Against Blood-Borne Antigens Clin. Exp. Immunol. 2002, 130, 4-11
67. Martin, F.; Oliver, A. M.; Kearney, J. F. Marginal Zone and B1 B Cells Unite in the Early Response Against T-Independent Blood-Borne Particulate Antigens Immunity 2001, 14, 617-629
68. Colino, J.; Shen, Y.; Snapper, C. M. Dendritic Cells Pulsed with Intact Streptococcus Pneumoniae Elicit Both Prowtein- and Polysaccharide-Specific Immunoglobulin Isotype Responses In Vivo Through Distinct Mechanisms J. Exp. Med. 2002, 195, 1-13
69. Do, R. K.; Hatada, E.; Lee, H.; Tourigny, M. R.; Hilbert, D.; Chen-Kiang, S. Attenuation of Apoptosis Underlies B Lymphocyte Stimulator Enhancement of Humoral Immune Response J. Exp. Med. 2002, 192, 953-964
70. Chen, Y.; Pikkarainen, T.; Elomaa, O.; Soininen, R.; Kodama, T.; Kraal, G.; Tryggvason, K. Defective Microarchitecture of the Spleen Marginal Zone and Impaired Response to a Thymus-Independent Type 2 Antigen in Mice Lacking Scavenger Receptors MARCO and SR-A J. Immunol. 2005, 175, 8173-8180
71. Kang, Y. S.; Do, Y.; Lee, H. K.; Park, S. H.; Cheong, C.; Lynch, R. M.; Loeffler, J. M.; Steinman, R. M.; Park, C. G. A Dominant Complement Fixation Pathway for Pneumococcal Polysaccharides Initiated By SIGN-R1 Interacting with C1q Cell 2006, 125, 47-58
72. Mond, J. J.; Lees, A.; Snapper, C. M. T Cell-Independent Antigens Type 2 Annu. Rev. Immunol. 1995, 13, 655-692
73. Mebius, R. E.; Kraal, G. Structure and Function of the Spleen Nature Rev. Immunol. 2005, 5, 606-616
74. Pone, E. J.; Zhang, J.; Mai, T.; White, C. A.; Li, G.; Sakakura, J. K.; Patel, P. J.; Al-Qahtani, A.; Zan, H.; Xu, Z.; Casali, P. BCR-Signalling Synergizes with TLR- Signalling for Induction of AID and Immunoglobulin Class-Switching Through the Non-Canonical NF-KB Pathway Nature Commun. 2012, 3, 767
75. Mond, J. J.; Lees, A.; Snapper, C. M. T cell-independent antigens type 2 Annu. Rev. Immunol. 1995, 13, 655-692
76. Bergtold, A.; Desai, D. D.; Gavhane, A.; Clynes, R. Cell surface recycling of internalized antigen permits dendritic cell priming of B cells Immunity 2005, 23, 503-514
77. Rodriguez, P. L.; Harada, T.; Christian, D. A.; Pantano, D. A.; Tsai, R. K.; Discher, D. E. Minimal "Self" Peptides That Inhibit Phagocytic Clearance and Enhance Delivery of Nanoparticles Science 2013, 339, 971-975