High-relaxivity superparamagnetic iron oxide nanoworms with decreased immune recognition and long-circulating properties

ACS Nano

Volumn 8, Issue 12, 2014, Pages 12437-12449

  Wang, Guankui ^a   Inturi, Swetha ^a   Serkova, Natalie J ^b   Merkulov, Sergey ^c   McCrae, Keith ^c   Russek, Stephen E ^d   Banda, Nirmal K ^b   Simberg, Dmitri ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

^d NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

Author keywords

blood circulation; complement activation; component 3; cross linking; dextran; epichlorohydrin; iron oxide; magnetic resonance imaging; nanoworms

Indexed keywords

BLOOD; CROSSLINKING; DEXTRAN; HYDROGELS; MAGNETIC NANOPARTICLES; MAGNETIC RESONANCE IMAGING; MAMMALS; METAL NANOPARTICLES; PROTEINS; SODIUM HYDROXIDE; SUPERPARAMAGNETISM;

BLOOD CIRCULATION; COMPLEMENT ACTIVATIONS; COMPONENT 3; EPICHLOROHYDRIN; NANOWORMS;

IRON OXIDES;

DEXTRAN; FERRIC ION; FERRIC OXIDE; NANOPARTICLE; SODIUM HYDROXIDE;

ANIMAL; BLOOD; CHEMISTRY; HALF LIFE TIME; IMMUNOLOGY; MACROPHAGE; MALE; METABOLISM; MOUSE; PARTICLE SIZE; TEMPERATURE; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; DEXTRANS; FERRIC COMPOUNDS; HALF-LIFE; MACROPHAGES; MALE; MICE; NANOPARTICLES; PARTICLE SIZE; SODIUM HYDROXIDE; TEMPERATURE;

EID: 84919779786     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn505126b     Document Type: Article

References (64)

1. Gupta, A. K.; Gupta, M. Synthesis and Surface Engineering of Iron Oxide Nanoparticles for Biomedical Applications Biomaterials 2005, 26, 3995-4021
2. Molday, R. S.; MacKenzie, D. Immunospecific Ferromagnetic Iron-Dextran Reagents for the Labeling and Magnetic Separation of Cells J. Immunol. Methods 1982, 52, 353-367
3. Boehm, H. Acidic and Basic Properties of Hydroxylated Metal Oxide Surfaces Discuss. Faraday Soc. 1971, 52, 264-275
4. Jung, C. W. Surface Properties of Superparamagnetic Iron Oxide MR Contrast Agents: Ferumoxides, Ferumoxtran, Ferumoxsil Magn. Reson. Imaging 1995, 13, 675-691
5. Raynal, I.; Prigent, P.; Peyramaure, S.; Najid, A.; Rebuzzi, C.; Corot, C. Macrophage Endocytosis of Superparamagnetic Iron Oxide Nanoparticles: Mechanisms and Comparison of Ferumoxides and Ferumoxtran-10 Invest. Radiol. 2004, 39, 56-63
6. Simberg, D.; Park, J. H.; Karmali, P. P.; Zhang, W. M.; 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
7. Bulte, J. W.; Kraitchman, D. L. Iron Oxide MR Contrast Agents for Molecular and Cellular Imaging NMR Biomed. 2004, 17, 484-5499
8. Moore, A.; Weissleder, R.; Bogdanov, A., Jr. Uptake of Dextran-Coated Monocrystalline Iron Oxides in Tumor Cells and Macrophages J. Magn. Reson. Imaging: JMRI 1997, 7, 1140-1145
9. Kiessling, F.; Mertens, M. E.; Grimm, J.; Lammers, T. Nanoparticles for Imaging: Top or Flop Radiology 2014, 273, 10-28
10. Nahrendorf, M.; Keliher, E.; Marinelli, B.; Waterman, P.; Feruglio, P. F.; Fexon, L.; Pivovarov, M.; Swirski, F. K.; Pittet, M. J.; Vinegoni, C.; Weissleder, R. Hybrid PET-Optical Imaging Using Targeted Probes Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 7910-7915
11. Wunderbaldinger, P.; Josephson, L.; Weissleder, R. Crosslinked Iron Oxides (CLIO): A New Platform for the Development of Targeted MR Contrast Agents Acad. Radiol 2002, 9 (Suppl 2) S304-306
12. Park, J. H.; von Maltzahn, G.; Zhang, L.; Derfus, A. M.; Simberg, D.; Harris, T. J.; Ruoslahti, E.; Bhatia, S. N.; Sailor, M. J. Systematic Surface Engineering of Magnetic Nanoworms for in Vivo Tumor Targeting Small 2009, 5, 694-700
13. Park, J. H.; von Maltzahn, G.; Zhang, L.; Schwartz, M. P.; Ruoslahti, E.; Bhatia, S.; Sailor, M. J. Magnetic Iron Oxide Nanoworms for Tumor Targeting and Imaging Adv. Mater. 2008, 20, 1630-1635
14. Agemy, L.; Sugahara, K. N.; Kotamraju, V. R.; Gujraty, K.; Girard, O. M.; Kono, Y.; Mattrey, R. F.; Park, J. H.; Sailor, M. J.; Jimenez, A. I.; Cativiela, C.; Zanuy, D.; Sayago, F. J.; Aleman, C.; Nussinov, R.; Ruoslahti, E. Nanoparticle-Induced Vascular Blockade in Human Prostate Cancer Blood 2010, 116, 2847-2856
15. Park, J. H.; von Maltzahn, G.; Xu, M. J.; Fogal, V.; Kotamraju, V. R.; Ruoslahti, E.; Bhatia, S. N.; Sailor, M. J. Cooperative Nanomaterial System to Sensitize, Target, and Treat Tumors Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 981-986
16. von Maltzahn, G.; Park, J. H.; Lin, K. Y.; Singh, N.; Schwoppe, C.; Mesters, R.; Berdel, W. E.; Ruoslahti, E.; Sailor, M. J.; Bhatia, S. N. Nanoparticles That Communicate in Vivo to Amplify Tumour Targeting Nat. Mater. 2011, 10, 545-552
17. Ren, Y.; Cheung, H. W.; von Maltzhan, G.; Agrawal, A.; Cowley, G. S.; Weir, B. A.; Boehm, J. S.; Tamayo, P.; Karst, A. M.; Liu, J. F.; Hirsch, M. S.; Mesirov, J. P.; Drapkin, R.; Root, D. E.; Lo, J.; Fogal, V.; Ruoslahti, E.; Hahn, W. C.; Bhatia, S. N. Targeted Tumor-Penetrating Sirna Nanocomplexes for Credentialing the Ovarian Cancer Oncogene Id4. Sci. Transl. Med. 2012, 4, 147ra112.
18. Girard, O. M.; Du, J.; Agemy, L.; Sugahara, K. N.; Kotamraju, V. R.; Ruoslahti, E.; Bydder, G. M.; Mattrey, R. F. Optimization of Iron Oxide Nanoparticle Detection Using Ultrashort Echo Time Pulse Sequences: Comparison of T1, T2∗, and Synergistic T1-T2∗ Contrast Mechanisms Magnetic Reson. Med. 2011, 65, 1649-1660
19. Thorek, D. L.; Chen, A. K.; Czupryna, J.; Tsourkas, A. Superparamagnetic Iron Oxide Nanoparticle Probes for Molecular Imaging Ann. Biomed. Eng. 2006, 34, 23-38
20. LaConte, L. E.; Nitin, N.; Zurkiya, O.; Caruntu, D.; OConnor, C. J.; Hu, X.; Bao, G. Coating Thickness of Magnetic Iron Oxide Nanoparticles Affects R2 Relaxivity J. Magn. Reson. Imaging: JMRI 2007, 26, 1634-1641
21. Tong, S.; Hou, S. J.; Zheng, Z. L.; Zhou, J.; Bao, G. Coating Optimization of Superparamagnetic Iron Oxide Nanoparticles for High T-2 Relaxivity Nano Lett. 2010, 10, 4607-4613
22. Choo, E. S. G.; Tang, X. S.; Sheng, Y.; Shuter, B.; Xue, J. M. Controlled Loading of Superparamagnetic Nanoparticles in Fluorescent Nanogels as Effective T-2-Weighted MRI Contrast Agents J. Mater. Chem. 2011, 21, 2310-2319
23. Yoon, T. J.; Lee, H.; Shao, H.; Hilderbrand, S. A.; Weissleder, R. Multicore Assemblies Potentiate Magnetic Properties of Biomagnetic Nanoparticles Adv. Mater. 2011, 23, 4793-4797
24. Poselt, E.; Kloust, H.; Tromsdorf, U.; Janschel, M.; Hahn, C.; Masslo, C.; Weller, H. Relaxivity Optimization of a Pegylated Iron-Oxide-Based Negative Magnetic Resonance Contrast Agent for T(2)-Weighted Spin-Echo Imaging ACS Nano 2012, 6, 1619-16124
25. Gazeau, F.; Levy, M.; Wilhelm, C. Optimizing Magnetic Nanoparticle Design for Nanothermotherapy Nanomedicine (London) 2008, 3, 831-844
26. Wu, Y. J.; Muldoon, L. L.; Varallyay, C.; Markwardt, S.; Jones, R. E.; Neuwelt, E. A. In Vivo Leukocyte Labeling with Intravenous Ferumoxides/Protamine Sulfate Complex and in Vitro Characterization for Cellular Magnetic Resonance Imaging Am. J. Physiol. 2007, 293, C1698-1708
27. Arbab, A. S.; Yocum, G. T.; Kalish, H.; Jordan, E. K.; Anderson, S. A.; Khakoo, A. Y.; Read, E. J.; Frank, J. A. Efficient Magnetic Cell Labeling with Protamine Sulfate Complexed to Ferumoxides for Cellular MRI Blood 2004, 104, 1217-1223
28. Janic, B.; Iskander, A. S.; Rad, A. M.; Soltanian-Zadeh, H.; Arbab, A. S. Effects of Ferumoxides-Protamine Sulfate Labeling on Immunomodulatory Characteristics of Macrophage-Like Thp-1 Cells PloS One 2008, 3, e2499
29. Lanza, G. M.; Caruthers, S. D.; Winter, P. M.; Hughes, M. S.; Schmieder, A. H.; Hu, G.; Wickline, S. A. Angiogenesis Imaging with Vascular-Constrained Particles: The Why and How Eur. J. Nucl. Med. Mol. Imaging 2010, 37 (Suppl 1) S114-126
30. Howard, M.; Zern, B. J.; Anselmo, A. C.; Shuvaev, V. V.; Mitragotri, S.; Muzykantov, V. Vascular Targeting of Nanocarriers: Perplexing Aspects of the Seemingly Straightforward Paradigm ACS Nano 2014, 8, 4100-4132
31. 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
32. Karmali, P. P.; Chao, Y.; Park, J. H.; Sailor, M. J.; Ruoslahti, E.; Esener, S. C.; Simberg, D. Different Effect of Hydrogelation on Antifouling and Circulation Properties of Dextran-Iron Oxide Nanoparticles Mol. Pharmaceutics 2012, 9, 539-545
33. Denizli, B. K.; Can, H. K.; Rzaev, Z. M. O.; Guner, A. Preparation Conditions and Swelling Equilibria of Dextran Hydrogels Prepared by Some Crosslinking Agents Polymer 2004, 45, 6431-6435
34. Renard, E.; Deratani, A.; Volet, G.; Sebille, B. Preparation and Characterization of Water Soluble High Molecular Weight Beta-Cyclodextrin-Epichlorohydrin Polymers Eur. Polym. J. 1997, 33, 49-57
35. Holmberg, L.; Lindberg, B.; Lindqvist, B. The Reaction between Epichlorohydrin and Polysaccharides: Part 1. Syntheses of Some Model Substances with Non-Cyclic Substituents Carbohydr. Res. 1994, 262, 213-221
36. Hansen, M. F.; Morup, S. Estimation of Blocking Temperatures from ZFC/FC Curves J. Magn. Magn. Mater. 1999, 203, 214-216
37. Coffey, W. T.; Kalmykov, Y. P. Thermal Fluctuations of Magnetic Nanoparticles: Fifty Years after Brown J. Appl. Phys. 2012, 112
38. Baleux, B. Colorimetric Determination of Nonionic Polyethylene Oxide Surfactants Using an Iodine-Iodide Solution C. R. Acad. Sci., Ser. C 1972, 279
39. Abbott, A. J.; Nelsestuen, G. L. Association of a Protein with Membrane Vesicles at the Collisional Limit: Studies with Blood Coagulation Factor Va Light Chain Also Suggest Major Differences between Small and Large Unilamellar Vesicles Biochemistry 1987, 26, 7994-8003
40. Pedersen, M. B.; Zhou, X.; Larsen, E. K.; Sorensen, U. S.; Kjems, J.; Nygaard, J. V.; Nyengaard, J. R.; Meyer, R. L.; Boesen, T.; Vorup-Jensen, T. Curvature of Synthetic and Natural Surfaces Is an Important Target Feature in Classical Pathway Complement Activation J. Immunol. 2010, 184, 1931-1945
41. Goldstein, I. J.; Hollerman, C. E.; Smith, E. E. Protein-Carbohydrate Interaction. II. Inhibition Studies on the Interaction of Concanavalin A with Polysaccharides Biochemistry 1965, 4, 876-883
42. Smith, E. E.; Goldstein, I. J. Protein-Carbohydrate Interaction. V. Further Inhibition Studies Directed toward Defining the Stereochemical Requirements of the Reactive Sites of Concanavalin A Arch. Biochem. Biophys. 1967, 121, 88-95
43. Alexis, F.; Pridgen, E.; Molnar, L. K.; Farokhzad, O. C. Factors Affecting the Clearance and Biodistribution of Polymeric Nanoparticles Mol. Pharmaceutics 2008, 5, 505-515
44. Perrault, S. D.; Walkey, C.; Jennings, T.; Fischer, H. C.; Chan, W. C. Mediating Tumor Targeting Efficiency of Nanoparticles through Design Nano Lett. 2009, 9, 1909-1915
45. Moghimi, S. M.; Hunter, A. C.; Murray, J. C. Long-Circulating and Target-Specific Nanoparticles: Theory to Practice Pharmacol. Rev. 2001, 53, 283-318
46. Simberg, D.; Zhang, W. M.; Merkulov, S.; McCrae, K.; Park, J. H.; Sailor, M. J.; Ruoslahti, E. Contact Activation of Kallikrein-Kinin System by Superparamagnetic Iron Oxide Nanoparticles in Vitro and in Vivo J. Controlled Release 2009, 140, 301-305
47. Moghimi, S. M.; Hunter, A. C.; Andresen, T. L. Factors Controlling Nanoparticle Pharmacokinetics: An Integrated Analysis and Perspective Annu. Rev. Pharmacol. Toxicol. 2012, 52, 481-503
48. Moghimi, S. M.; Farhangrazi, Z. S. Nanomedicine and the Complement Paradigm Nanomed.: Nanotechnol., Biol., Med. 2013, 9, 458-460
49. Ricklin, D.; Hajishengallis, G.; Yang, K.; Lambris, J. D. Complement: A Key System for Immune Surveillance and Homeostasis Nat. Immunol. 2010, 11, 785-797
50. Brown, E. J. Complement Receptors, Adhesion, and Phagocytosis Infect. Agents Dis. 1992, 1, 63-70
51. Sengelov, H. Complement Receptors in Neutrophils Crit. Rev. Immunol. 1995, 15, 107-131
52. Peng, Q.; Li, K.; Sacks, S. H.; Zhou, W. The Role of Anaphylatoxins C3a and C5a in Regulating Innate and Adaptive Immune Responses Inflammation Allergy: Drug Targets 2009, 8, 236-246
53. Mestas, J.; Hughes, C. C. W. Of Mice and Not Men: Differences between Mouse and Human Immunology J. Immunol. 2004, 172, 2731-2738
54. Chao, Y.; Makale, M.; Karmali, P. P.; Sharikov, Y.; Tsigelny, I.; Merkulov, S.; Kesari, S.; Wrasidlo, W.; Ruoslahti, E.; Simberg, D. Recognition of Dextran-Superparamagnetic Iron Oxide Nanoparticle Conjugates (Feridex) via Macrophage Scavenger Receptor Charged Domains Bioconjugate Chem. 2012, 23, 1003-1009
55. Chao, Y.; Karmali, P. P.; Mukthavaram, R.; Kesari, S.; Kouznetsova, V. L.; Tsigelny, I. F.; Simberg, D. Direct Recognition of Superparamagnetic Nanocrystals by Macrophage Scavenger Receptor Sr-Ai ACS Nano 2013, 7, 4289-4298
56. Karmali, P. P.; Simberg, D. Interactions of Nanoparticles with Plasma Proteins: Implication on Clearance and Toxicity of Drug Delivery Systems Expert Opin. Drug Delivery 2011, 8, 343-357
57. Li, S. D.; Huang, L. Pharmacokinetics and Biodistribution of Nanoparticles Mol. Pharmaceutics 2008, 5, 496-504
58. Klibanov, A. L.; Maruyama, K.; Beckerleg, A. M.; Torchilin, V. P.; Huang, L. Activity of Amphipathic Poly(Ethylene Glycol) 5000 to Prolong the Circulation Time of Liposomes Depends on the Liposome Size and Is Unfavorable for Immunoliposome Binding to Target Biochim. Biophys. Acta 1991, 1062, 142-148
59. Duncanson, W. J.; Figa, M. A.; Hallock, K.; Zalipsky, S.; Hamilton, J. A.; Wong, J. Y. Targeted Binding of Pla Microparticles with Lipid-PEG-Tethered Ligands Biomaterials 2007, 28, 4991-4999
60. Cai, W.; Chen, X. Multimodality Molecular Imaging of Tumor Angiogenesis J. Nucl. Med. 2008, 49 (Suppl 2) 113S-28S
61. Barrett, T.; Brechbiel, M.; Bernardo, M.; Choyke, P. L. MRI of Tumor Angiogenesis J. Magn. Reson. Imaging: JMRI 2007, 26, 235-249
62. Iagaru, A.; Chen, X.; Gambhir, S. S. Molecular Imaging Can Accelerate Anti-Angiogenic Drug Development and Testing Nat. Clin. Pract. Oncol. 2007, 4, 556-557
63. Thorek, D. L.; Tsourkas, A. Size, Charge and Concentration Dependent Uptake of Iron Oxide Particles by Non-Phagocytic Cells Biomaterials 2008, 29, 3583-3590
64. Schnell, M. A.; Hardy, C.; Hawley, M.; Propert, K. J.; Wilson, J. M. Effect of Blood Collection Technique in Mice on Clinical Pathology Parameters Human Gene Ther. 2002, 13, 155-161