Clearance Pathways and Tumor Targeting of Imaging Nanoparticles

ACS Nano

Volumn 9, Issue 7, 2015, Pages 6655-6674

  Yu, Mengxiao ^a   Zheng, Jie ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

cancer diagnosis; clinical translation; enhanced permeability and retention (EPR) effect; imaging nanoparticles; molecular nanoprobes; renal clearance; reticuloendothelial system (RES); tumor targeting

Indexed keywords

DISEASES; MOLECULAR IMAGING; NANOPARTICLES; NANOPROBES; SURFACE CHEMISTRY; TUMORS;

CANCER DIAGNOSIS; CLINICAL TRANSLATION; ENHANCED PERMEABILITY AND RETENTION EFFECTS; RENAL CLEARANCE; RETICULOENDOTHELIAL SYSTEMS; TUMOR TARGETING;

DIAGNOSIS;

NANOPARTICLE;

ANIMAL; CHEMISTRY; DIAGNOSTIC IMAGING; HUMAN; METABOLISM; NEOPLASMS; PROCEDURES; URINARY EXCRETION;

ANIMALS; DIAGNOSTIC IMAGING; HUMANS; NANOPARTICLES; NEOPLASMS; RENAL ELIMINATION;

EID: 84938118607     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.5b01320     Document Type: Review

References (121)

1. Weissleder, R.; Pittet, M. J. Imaging in the Era of Molecular Oncology Nature 2008, 452, 580-589 10.1038/nature06917
2. Frangioni, J. V. New Technologies for Human Cancer Imaging J. Clin. Oncol. 2008, 26, 4012-4021 10.1200/JCO.2007.14.3065
3. Choi, H. S.; Liu, W.; Misra, P.; Tanaka, E.; Zimmer, J. P.; Ipe, B. I.; Bawendi, M. G.; Frangioni, J. V. Renal Clearance of Quantum Dots Nat. Biotechnol. 2007, 25, 1165-1170 10.1038/nbt1340
4. Weissleder, R.; Kelly, K.; Sun, E. Y.; Shtatland, T.; Josephson, L. Cell-Specific Targeting of Nanoparticles by Multivalent Attachment of Small Molecules Nat. Biotechnol. 2005, 23, 1418-1423 10.1038/nbt1159
5. Gao, X.; Cui, Y.; Levenson, R. M.; Chung, L. W.; Nie, S. In Vivo Cancer Targeting and Imaging with Semiconductor Quantum Dots Nat. Biotechnol. 2004, 22, 969-976 10.1038/nbt994
6. Rhyner, M. N.; Smith, A. M.; Gao, X. H.; Mao, H.; Yang, L. L.; Nie, S. M. Quantum Dots and Multifunctional Nanoparticles: New Contrast Agents for Tumor Imaging Nanomedicine 2006, 1, 209-217 10.2217/17435889.1.2.209
7. Choi, H. S.; Liu, W.; Liu, F.; Nasr, K.; Misra, P.; Bawendi, M. G.; Frangioni, J. V. Design Considerations for Tumour-Targeted Nanoparticles Nat. Nanotechnol. 2010, 5, 42-47 10.1038/nnano.2009.314
8. Choi, H. S.; Frangioni, J. V. Nanoparticles for Biomedical Imaging: Fundamentals of Clinical Translation Mol. Imaging 2010, 9, 291-310
9. Kamaly, N.; Miller, A. D.; Bell, J. D. Chemistry of Tumour Targeted T-1 Based MRI Contrast Agents Curr. Top. Med. Chem. 2010, 10, 1158-1183 10.2174/156802610791384199
10. Prijic, S.; Sersa, G. Magnetic Nanoparticles as Targeted Delivery Systems in Oncology Radiol. Oncol. 2011, 45, 1-16 10.2478/v10019-011-0001-z
11. Boisselier, E.; Astruc, D. Gold Nanoparticles in Nanomedicine: Preparations, Imaging, Diagnostics, Therapies and Toxicity Chem. Soc. Rev. 2009, 38, 1759-1782 10.1039/b806051g
12. Lal, S.; Clare, S. E.; Halas, N. J. Nanoshell-Enabled Photothermal Cancer Therapy: Impending Clinical Impact Acc. Chem. Res. 2008, 41, 1842-1851 10.1021/ar800150g
13. Jokerst, J. V.; Lobovkina, T.; Zare, R. N.; Gambhir, S. S. Nanoparticle Pegylation for Imaging and Therapy Nanomedicine 2011, 6, 715-728 10.2217/nnm.11.19
14. Longmire, M.; Choyke, P. L.; Kobayashi, H. Clearance Properties of Nano-Sized Particles and Molecules as Imaging Agents: Considerations and Caveats Nanomedicine 2008, 3, 703-717 10.2217/17435889.3.5.703
15. Harpur, E. S.; Worah, D.; Hals, P. A.; Holtz, E.; Furuhama, K.; Nomura, H. Preclinical Safety Assessment and Pharmacokinetics of Gadodiamide Injection, a New Magnetic Resonance Imaging Contrast Agent Invest. Radiol. 1993, 28 (Suppl 1) S28-S43 10.1097/00004424-199303001-00004
16. McLachlan, S. J.; Eaton, S.; Desimone, D. N. Pharmacokinetic Behavior of Gadoteridol Injection Invest. Radiol. 1992, 27, S12-S15 10.1097/00004424-199208001-00004
17. Bourin, M.; Jolliet, P.; Ballereau, F. An Overview of the Clinical Pharmacokinetics of X-Ray Contrast Media Clin. Pharmacokinet. 1997, 32, 180-193 10.2165/00003088-199732030-00002
18. Arnold, R. W.; Subramanian, G.; McAfee, J. G.; Blair, R. J.; Thomas, F. D. Comparison of 99mTc Complexes for Renal Imaging J. Nucl. Med. 1975, 16, 357-367
19. Taylor, A.; Eshima, D.; Fritzberg, A. R.; Christian, P. E.; Kasina, S. Comparison of Iodine-131 OIH and Technetium-99m MAG3 Renal Imaging in Volunteers J. Nucl. Med. 1986, 27, 795-803
20. Moran, J. K.; Lee, H. B.; Blaufox, M. D. Optimization of Urinary FDG Excretion During PET Imaging J. Nucl. Med. 1999, 40, 1352-1357
21. Choi, H. S.; Nasr, K.; Alyabyev, S.; Feith, D.; Lee, J. H.; Kim, S. H.; Ashitate, Y.; Hyun, H.; Patonay, G.; Strekowski, L. Synthesis and In Vivo Fate of Zwitterionic near-Infrared Fluorophores Angew. Chem., Int. Ed. 2011, 50, 6258-6263 10.1002/anie.201102459
22. Liu, J.; Yu, M.; Zhou, C.; Yang, S.; Ning, X.; Zheng, J. Passive Tumor Targeting of Renal-Clearable Luminescent Gold Nanoparticles: Long Tumor Retention and Fast Normal Tissue Clearance J. Am. Chem. Soc. 2013, 135, 4978-4981 10.1021/ja401612x
23. Xie, H.; Wang, Z. J.; Bao, A.; Goins, B.; Phillips, W. T. In Vivo PET Imaging and Biodistribution of Radiolabeled Gold Nanoshells in Rats with Tumor Xenografts Int. J. Pharm. 2010, 395, 324-330 10.1016/j.ijpharm.2010.06.005
24. Liu, R. S.; Chou, T. K.; Chang, C. H.; Wu, C. Y.; Chang, C. W.; Chang, T. J.; Wang, S. J.; Lin, W. J.; Wang, H. E. Biodistribution, Pharmacokinetics and PET Imaging of [18F]FMISO, [18F]FDG and [18F]FAc in a Sarcoma- and Inflammation-Bearing Mouse Model Nucl. Med. Biol. 2009, 36, 305-312 10.1016/j.nucmedbio.2008.12.011
25. Andros, G.; Harper, P. V.; Lathrop, K. A.; McCardle, R. J. Pertechnetate-99m Localization in Man with Application to Thyroid Scanning and the Study of Thyroid Physiology J. Clin. Endocrinol. Metab. 1965, 25, 1067-1076 10.1210/jcem-25-8-1067
26. Zhao, Y.; Sultan, D.; Detering, L.; Cho, S.; Sun, G.; Pierce, R.; Wooley, K. L.; Liu, Y. Copper-64-Alloyed Gold Nanoparticles for Cancer Imaging: Improved Radiolabel Stability and Diagnostic Accuracy Angew. Chem., Int. Ed. 2014, 53, 156-159 10.1002/anie.201308494
27. Zhang, G.; Yang, Z.; Lu, W.; Zhang, R.; Huang, Q.; Tian, M.; Li, L.; Liang, D.; Li, C. Influence of Anchoring Ligands and Particle Size on the Colloidal Stability and In Vivo Biodistribution of Polyethylene Glycol-Coated Gold Nanoparticles in Tumor-Xenografted Mice Biomaterials 2009, 30, 1928-1936 10.1016/j.biomaterials.2008.12.038
28. Melancon, M. P.; Lu, W.; Yang, Z.; Zhang, R.; Cheng, Z.; Elliot, A. M.; Stafford, J.; Olson, T.; Zhang, J. Z.; Li, C. In Vitro and In Vivo Targeting of Hollow Gold Nanoshells Directed at Epidermal Growth Factor Receptor for Photothermal Ablation Therapy Mol. Cancer Ther. 2008, 7, 1730-1739 10.1158/1535-7163.MCT-08-0016
29. Cheng, K.; Kothapalli, S.-R.; Liu, H.; Koh, A. L.; Jokerst, J. V.; Jiang, H.; Yang, M.; Li, J.; Levi, J.; Wu, J. C. Construction and Validation of Nano Gold Tripods for Molecular Imaging of Living Subjects J. Am. Chem. Soc. 2014, 136, 3560-3571 10.1021/ja412001e
30. Wang, Y.; Liu, Y.; Luehmann, H.; Xia, X.; Brown, P.; Jarreau, C.; Welch, M.; Xia, Y. Evaluating the Pharmacokinetics and In Vivo Cancer Targeting Capability of Au Nanocages by Positron Emission Tomography Imaging ACS Nano 2012, 6, 5880-5888 10.1021/nn300464r
31. Piao, J.-G.; Wang, L.; Gao, F.; You, Y.-Z.; Xiong, Y.; Yang, L. Erythrocyte Membrane Is an Alternative Coating to Polyethylene Glycol for Prolonging the Circulation Lifetime of Gold Nanocages for Photothermal Therapy ACS Nano 2014, 8, 10414-10425 10.1021/nn503779d
32. Hong, G. S.; Robinson, J. T.; Zhang, Y. J.; Diao, S.; Antaris, A. L.; Wang, Q. B.; Dai, H. J. In Vivo Fluorescence Imaging with Ag2S Quantum Dots in the Second Near-Infrared Region Angew. Chem., Int. Ed. 2012, 51, 9818-9821 10.1002/anie.201206059
33. Sun, X.; Huang, X.; Guo, J.; Zhu, W.; Ding, Y.; Niu, G.; Wang, A.; Kiesewetter, D. O.; Wang, Z. L.; Sun, S. Self-Illuminating 64Cu-Doped CdSe/ZnS Nanocrystals for In Vivo Tumor Imaging J. Am. Chem. Soc. 2014, 136, 1706-1709 10.1021/ja410438n
34. Guo, W.; Sun, X.; Jacobson, O.; Yan, X.; Min, K.; Srivatsan, A.; Niu, G.; Kiesewetter, D. O.; Chang, J.; Chen, X. Intrinsically Radioactive [64Cu]CuInS/ZnS Quantum Dots for PET and Optical Imaging: Improved Radiochemical Stability and Controllable Cerenkov Luminescence ACS Nano 2015, 9, 488-495 10.1021/nn505660r
35. Gao, J.; Chen, K.; Xie, R.; Xie, J.; Lee, S.; Cheng, Z.; Peng, X.; Chen, X. Ultrasmall Near-Infrared Non-Cadmium Quantum Dots for In Vivo Tumor Imaging Small 2010, 6, 256-261 10.1002/smll.200901672
36. Gao, J.; Chen, K.; Xie, R.; Xie, J.; Yan, Y.; Cheng, Z.; Peng, X.; Chen, X. In Vivo Tumor-Targeted Fluorescence Imaging Using Near-Infrared Non-Cadmium Quantum Dots Bioconjugate Chem. 2010, 21, 604-609 10.1021/bc900323v
37. Gao, J.; Chen, K.; Miao, Z.; Ren, G.; Chen, X.; Gambhir, S. S.; Cheng, Z. Affibody-Based Nanoprobes for HER2-Expressing Cell and Tumor Imaging Biomaterials 2011, 32, 2141-2148 10.1016/j.biomaterials.2010.11.053
38. Li, Z.; Wang, C.; Cheng, L.; Gong, H.; Yin, S.; Gong, Q.; Li, Y.; Liu, Z. PEG-Functionalized Iron Oxide Nanoclusters Loaded with Chlorin e6 for Targeted, NIR Light Induced, Photodynamic Therapy Biomaterials 2013, 34, 9160-9170 10.1016/j.biomaterials.2013.08.041
39. Song, X.; Gong, H.; Yin, S.; Cheng, L.; Wang, C.; Li, Z.; Li, Y.; Wang, X.; Liu, G.; Liu, Z. Ultra-Small Iron Oxide Doped Polypyrrole Nanoparticles for In Vivo Multimodal Imaging Guided Photothermal Therapy Adv. Funct. Mater. 2014, 24, 1194-1201 10.1002/adfm.201302463
40. Crayton, S. H.; Tsourkas, A. pH-Titratable Superparamagnetic Iron Oxide for Improved Nanoparticle Accumulation in Acidic Tumor Microenvironments ACS Nano 2011, 5, 9592-9601 10.1021/nn202863x
41. 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 10.1002/smll.200801789
42. Liu, C.; Gao, Z.; Zeng, J.; Hou, Y.; Fang, F.; Li, Y.; Qiao, R.; Shen, L.; Lei, H.; Yang, W. Magnetic/Upconversion Fluorescent NaGdF4:Yb,Er Nanoparticle-Based Dual-Modal Molecular Probes for Imaging Tiny Tumors In Vivo ACS Nano 2013, 7, 7227-7240 10.1021/nn4030898
43. Jin, J.; Xu, Z.; Zhang, Y.; Gu, Y.-J.; Lam, M.H.-W.; Wong, W.-T. Upconversion Nanoparticles Conjugated with Gd3+-Dota and RGD for Targeted Dual-Modality Imaging of Brain Tumor Xenografts Adv. Healthcare Mater. 2013, 2, 1501-1512 10.1002/adhm.201300102
44. Lee, J.; Lee, T. S.; Ryu, J.; Hong, S.; Kang, M.; Im, K.; Kang, J. H.; Lim, S. M.; Park, S.; Song, R. RGD Peptide-Conjugated Multimodal NaGdF4:Yb3+/Er3+ Nanophosphors for Upconversion Luminescence, MR, and PET Imaging of Tumor Angiogenesis J. Nucl. Med. 2013, 54, 96-103 10.2967/jnumed.112.108043
45. Wang, X.; Chen, J. T.; Zhu, H.; Chen, X.; Yan, X.-P. One-Step Solvothermal Synthesis of Targetable Optomagnetic Upconversion Nanoparticles for In Vivo Bimodal Imaging Anal. Chem. 2013, 85, 10225-10231 10.1021/ac401934p
46. Chen, F.; Hong, H.; Zhang, Y.; Valdovinos, H. F.; Shi, S.; Kwon, G. S.; Theuer, C. P.; Barnhart, T. E.; Cai, W. In Vivo Tumor Targeting and Image-Guided Drug Delivery with Antibody-Conjugated, Radiolabeled Mesoporous Silica Nanoparticles ACS Nano 2013, 7, 9027-9039 10.1021/nn403617j
47. Robinson, J. T.; Hong, G.; Liang, Y.; Zhang, B.; Yaghi, O. K.; Dai, H. In Vivo Fluorescence Imaging in the Second near-Infrared Window with Long Circulating Carbon Nanotubes Capable of Ultrahigh Tumor Uptake J. Am. Chem. Soc. 2012, 134, 10664-10669 10.1021/ja303737a
48. Hong, H.; Yang, K.; Zhang, Y.; Engle, J. W.; Feng, L.; Yang, Y.; Nayak, T. R.; Goel, S.; Bean, J.; Theuer, C. P. In Vivo Targeting and Imaging of Tumor Vasculature with Radiolabeled, Antibody-Conjugated Nanographene ACS Nano 2012, 6, 2361-2370 10.1021/nn204625e
49. Benezra, M.; Penate-Medina, O.; Zanzonico, P. B.; Schaer, D.; Ow, H.; Burns, A.; DeStanchina, E.; Longo, V.; Herz, E.; Iyer, S. Multimodal Silica Nanoparticles Are Effective Cancer-Targeted Probes in a Model of Human Melanoma J. Clin. Invest. 2011, 121, 2768-2780 10.1172/JCI45600
50. Zhou, C.; Long, M.; Qin, Y.; Sun, X.; Zheng, J. Luminescent Gold Nanoparticles with Efficient Renal Clearance Angew. Chem., Int. Ed. 2011, 50, 3168-3172 10.1002/anie.201007321
51. Liu, J.; Yu, M.; Ning, X.; Zhou, C.; Yang, S.; Zheng, J. Pegylation and Zwitterionization: Pros and Cons in the Renal Clearance and Tumor Targeting of Near-IR-Emitting Gold Nanoparticles Angew. Chem., Int. Ed. 2013, 52, 12572-12576 10.1002/anie.201304465
52. Alric, C.; Miladi, I.; Kryza, D.; Taleb, J.; Lux, F.; Bazzi, R.; Billotey, C.; Janier, M.; Perriat, P.; Roux, S. The Biodistribution of Gold Nanoparticles Designed for Renal Clearance Nanoscale 2013, 5, 5930-5939 10.1039/c3nr00012e
53. Huang, X.; Zhang, F.; Zhu, L.; Choi, K. Y.; Guo, N.; Guo, J.; Tackett, K.; Anilkumar, P.; Liu, G.; Quan, Q. Effect of Injection Routes on the Biodistribution, Clearance, and Tumor Uptake of Carbon Dots ACS Nano 2013, 7, 5684-5693 10.1021/nn401911k
54. 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 10.1039/C1CS15237H
55. Pérez-Juste, J.; Pastoriza-Santos, I.; Liz-Marzán, L. M.; Mulvaney, P. Gold Nanorods: Synthesis, Characterization and Applications Coord. Chem. Rev. 2005, 249, 1870-1901 10.1016/j.ccr.2005.01.030
56. Skrabalak, S. E.; Chen, J.; Sun, Y.; Lu, X.; Au, L.; Cobley, C. M.; Xia, Y. Gold Nanocages: Synthesis, Properties, and Applications Acc. Chem. Res. 2008, 41, 1587-1595 10.1021/ar800018v
57. Lee, N.; Hyeon, T. Designed Synthesis of Uniformly Sized Iron Oxide Nanoparticles for Efficient Magnetic Resonance Imaging Contrast Agents Chem. Soc. Rev. 2012, 41, 2575-2589 10.1039/C1CS15248C
58. Wang, F.; Liu, X. Recent Advances in the Chemistry of Lanthanide-Doped Upconversion Nanocrystals Chem. Soc. Rev. 2009, 38, 976-989 10.1039/b809132n
59. Zhou, J.; Liu, Z.; Li, F. Upconversion Nanophosphors for Small-Animal Imaging Chem. Soc. Rev. 2012, 41, 1323-1349 10.1039/C1CS15187H
60. Vivero-Escoto, J. L.; Huxford-Phillips, R. C.; Lin, W. Silica-Based Nanoprobes for Biomedical Imaging and Theranostic Applications Chem. Soc. Rev. 2012, 41, 2673-2685 10.1039/c2cs15229k
61. 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 10.1039/c1cs15246g
62. Cao, T.; Yang, Y.; Sun, Y.; Wu, Y.; Gao, Y.; Feng, W.; Li, F. Biodistribution of Sub-10 nm Peg-Modified Radioactive/Upconversion Nanoparticles Biomaterials 2013, 34, 7127-7134 10.1016/j.biomaterials.2013.05.028
63. Walkey, C. D.; Chan, W. C. W. Understanding and Controlling the Interaction of Nanomaterials with Proteins in a Physiological Environment Chem. Soc. Rev. 2012, 41, 2780-2799 10.1039/C1CS15233E
64. Walkey, C. D.; Olsen, J. B.; Guo, H.; 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 10.1021/ja2084338
65. Yong, K.-T.; Roy, I.; Ding, H.; Bergey, E. J.; Prasad, P. N. Biocompatible Near-Infrared Quantum Dots as Ultrasensitive Probes for Long-Term In Vivo Imaging Applications Small 2009, 5, 1997-2004 10.1002/smll.200900547
66. Khlebtsov, N.; Dykman, L. Biodistribution and Toxicity of Engineered Gold Nanoparticles: A Review of In Vitro and In Vivo Studies Chem. Soc. Rev. 2011, 40, 1647-1671 10.1039/C0CS00018C
67. Yong, K.-T.; Law, W.-C.; Hu, R.; Ye, L.; Liu, L.; Swihart, M. T.; Prasad, P. N. Nanotoxicity Assessment of Quantum Dots: From Cellular to Primate Studies Chem. Soc. Rev. 2013, 42, 1236-1250 10.1039/C2CS35392J
68. Sadauskas, E.; Danscher, G.; Stoltenberg, M.; Vogel, U.; Larsen, A.; Wallin, H. Protracted Elimination of Gold Nanoparticles from Mouse Liver Nanomedicine 2009, 5, 162-169 10.1016/j.nano.2008.11.002
69. Ye, L.; Yong, K.-T.; Liu, L.; Roy, I.; Hu, R.; Zhu, J.; Cai, H.; Law, W.-C.; Liu, J.; Wang, K. A Pilot Study in Non-Human Primates Shows No Adverse Response to Intravenous Injection of Quantum Dots Nat. Nanotechnol. 2012, 7, 453-458 10.1038/nnano.2012.74
70. Ballou, B.; Ernst, L. A.; Andreko, S.; Harper, T.; Fitzpatrick, J. A. J.; Waggoner, A. S.; Bruchez, M. P. Sentinel Lymph Node Imaging Using Quantum Dots in Mouse Tumor Models Bioconjugate Chem. 2007, 18, 389-396 10.1021/bc060261j
71. Sun, Y.; Feng, W.; Yang, P.; Huang, C.; Li, F. The Biosafety of Lanthanide Upconversion Nanomaterials Chem. Soc. Rev. 2015, 44, 1509-1525 10.1039/C4CS00175C
72. Kumar, R.; Roy, I.; Ohulchanskky, T. Y.; Vathy, L. A.; Bergey, E. J.; Sajjad, M.; Prasad, P. N. In Vivo Biodistribution and Clearance Studies Using Multimodal Organically Modified Silica Nanoparticles ACS Nano 2010, 4, 699-708 10.1021/nn901146y
73. Gu, L.; Fang, R. H.; Sailor, M. J.; Park, J. H. In Vivo Clearance and Toxicity of Monodisperse Iron Oxide Nanocrystals ACS Nano 2012, 6, 4947-4954 10.1021/nn300456z
74. Singh, R.; Pantarotto, D.; Lacerda, L.; Pastorin, G.; Klumpp, C.; Prato, M.; Bianco, A.; Kostarelos, K. Tissue Biodistribution and Blood Clearance Rates of Intravenously Administered Carbon Nanotube Radiotracers Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 3357-3362 10.1073/pnas.0509009103
75. Hall, J. E. Guyton and Hall Textbook of Medical Physiology, 12 th ed.; Saunders: Philadelphia. PA, 2011.
76. Burns, A. A.; Vider, J.; Ow, H.; Herz, E.; Penate-Medina, O.; Baumgart, M.; Larson, S. M.; Wiesner, U.; Bradbury, M. Fluorescent Silica Nanoparticles with Efficient Urinary Excretion for Nanomedicine Nano Lett. 2009, 9, 442-448 10.1021/nl803405h
77. Zhou, Z.; Wang, L.; Chi, X.; Bao, J.; Yang, L.; Zhao, W.; Chen, Z.; Wang, X.; Chen, X.; Gao, J. Engineered Iron-Oxide-Based Nanoparticles as Enhanced T-1 Contrast Agents for Efficient Tumor Imaging ACS Nano 2013, 7, 3287-3296 10.1021/nn305991e
78. Tang, S.; Chen, M.; Zheng, N. Sub-10-nm Pd Nanosheets with Renal Clearance for Efficient near-Infrared Photothermal Cancer Therapy Small 2014, 10, 3139-3144 10.1002/smll.201303631
79. Yang, S.; Sun, S.; Zhou, C.; Hao, G.; Liu, J.; Ramezani, S.; Yu, M.; Sun, X.; Zheng, J. Renal Clearance and Degradation of Glutathione-Coated Copper Nanoparticles Bioconjugate Chem. 2015, 26, 511-519 10.1021/acs.bioconjchem.5b00003
80. Park, J. H.; 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 10.1038/nmat2398
81. Chou, L. Y. T.; Zagorovsky, K.; Chan, W. C. W. DNA Assembly of Nanoparticle Superstructures for Controlled Biological Delivery and Elimination Nat. Nanotechnol. 2014, 9, 148-155 10.1038/nnano.2013.309
82. Yang, K.; Wan, J.; Zhang, S.; Zhang, Y.; Lee, S.-T.; Liu, Z. In Vivo Pharmacokinetics, Long-Term Biodistribution, and Toxicology of Pegylated Graphene in Mice ACS Nano 2011, 5, 516-522 10.1021/nn1024303
83. Zhao, Y.; Sultan, D.; Detering, L.; Luehmann, H.; Liu, Y. Facile Synthesis, Pharmacokinetic and Systemic Clearance Evaluation, and Positron Emission Tomography Cancer Imaging of 64Cu-Au Alloy Nanoclusters Nanoscale 2014, 6, 13501-13509 10.1039/C4NR04569F
84. Lynch, I.; Dawson, K. A. Protein-Nanoparticle Interactions Nano Today 2008, 3, 40-47 10.1016/S1748-0132(08)70014-8
85. Zhou, C.; Long, M.; Qin, Y. P.; Sun, X. K.; Zheng, J. Luminescent Gold Nanoparticles with Efficient Renal Clearance Angew. Chem., Int. Ed. 2011, 50, 3168-3172 10.1002/anie.201007321
86. Meister, A.; Anderson, M. E. Glutathione Ann. Rev. Biochem. 1983, 52, 711-760
87. Rosi, N. L.; Giljohann, D. A.; Thaxton, C. S.; Lytton-Jean, A. K. R.; Han, M. S.; Mirkin, C. A. Oligonucleotide-Modified Gold Nanoparticles for Intracellular Gene Regulation Science 2006, 312, 1027-1030 10.1126/science.1125559
88. Hong, R.; Han, G.; Fernandez, J. M.; Kim, B. J.; Forbes, N. S.; Rotello, V. M. Glutathione-Mediated Delivery and Release Using Monolayer Protected Nanoparticle Carriers J. Am. Chem. Soc. 2006, 128, 1078-1079 10.1021/ja056726i
89. Yu, M.; Zhou, C.; Liu, J.; Hankins, J. D.; Zheng, J. Luminescent Gold Nanoparticles with pH-Dependent Membrane Adsorption J. Am. Chem. Soc. 2011, 133, 11014-11017 10.1021/ja201930p
90. Semmler-Behnke, M.; Kreyling, W. G.; Lipka, J.; Fertsch, S.; Wenk, A.; Takenaka, S.; Schmid, G.; Brandau, W. Biodistribution of 1.4-and 18-nm Gold Particles in Rats Small 2008, 4, 2108-2111 10.1002/smll.200800922
91. Arvizo, R. R.; Miranda, O. R.; Moyano, D. F.; Walden, C. A.; Giri, K.; Bhattacharya, R.; Robertson, J. D.; Rotello, V. M.; Reid, J. M.; Mukherjee, P. Modulating Pharmacokinetics, Tumor Uptake and Biodistribution by Engineered Nanoparticles PLoS One 2011, 6, e24374 10.1371/journal.pone.0024374
92. Zhang, C.; Li, C.; Liu, Y.; Zhang, J.; Bao, C.; Liang, S.; Wang, Q.; Yang, Y.; Fu, H.; Wang, K. Gold Nanoclusters-Based Nanoprobes for Simultaneous Fluorescence Imaging and Targeted Photodynamic Therapy with Superior Penetration and Retention Behavior in Tumors Adv. Funct. Mater. 2015, 25, 1314-1325 10.1002/adfm.201403095
93. Zhou, C.; Hao, G. Y.; Thomas, P.; Liu, J. B.; Yu, M. X.; Sun, S. S.; Oz, O. K.; Sun, X. K.; Zheng, J. Near-Infrared Emitting Radioactive Gold Nanoparticles with Molecular Pharmacokinetics Angew. Chem., Int. Ed. 2012, 51, 10118-10122 10.1002/anie.201203031
94. Simpson, C. A.; Salleng, K. J.; Cliffel, D. E.; Feldheim, D. L. In Vivo Toxicity, Biodistribution, and Clearance of Glutathione-Coated Gold Nanoparticles Nanomedicine 2013, 9, 257-263 10.1016/j.nano.2012.06.002
95. Chen, H.; Wang, G. D.; Tang, W.; Todd, T.; Zhen, Z.; Tsang, C.; Hekmatyar, K.; Cowger, T.; Hubbard, R. B.; Zhang, W. Gd-Encapsulated Carbonaceous Dots with Efficient Renal Clearance for Magnetic Resonance Imaging Adv. Mater. 2014, 26, 6761-6766 10.1002/adma.201402964
96. Li, S. D.; Huang, L. Pharmacokinetics and Biodistribution of Nanoparticles Mol. Pharmaceutics 2008, 5, 496-504 10.1021/mp800049w
97. Perrault, S. D.; Walkey, C.; Jennings, T.; Fischer, H. C.; Chan, W. C. W. Mediating Tumor Targeting Efficiency of Nanoparticles through Design Nano Lett. 2009, 9, 1909-1915 10.1021/nl900031y
98. Xing, H.; Zheng, X.; Ren, Q.; Bu, W.; Ge, W.; Xiao, Q.; Zhang, S.; Wei, C.; Qu, H.; Wang, Z. Computed Tomography Imaging-Guided Radiotherapy by Targeting Upconversion Nanocubes with Significant Imaging and Radiosensitization Enhancements Sci. Rep. 2013, 3, 1751 10.1038/srep01751
99. Liu, Z.; Cai, W.; He, L.; Nakayama, N.; Chen, K.; Sun, X.; Chen, X.; Dai, H. In Vivo Biodistribution and Highly Efficient Tumour Targeting of Carbon Nanotubes in Mice Nat. Nanotechnol. 2007, 2, 47-52 10.1038/nnano.2006.170
100. 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
101. Toy, R.; Bauer, L.; Hoimes, C.; Ghaghada, K. B.; Karathanasis, E. Targeted Nanotechnology for Cancer Imaging Adv. Drug Delivery Rev. 2014, 76, 79-97 10.1016/j.addr.2014.08.002
102. 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 10.1016/j.addr.2010.04.009
103. Maeda, H. Tumor-Selective Delivery of Macromolecular Drugs via the EPR Effect: Background and Future Prospects Bioconjugate Chem. 2010, 21, 797-802 10.1021/bc100070g
104. Wang, Y.; Liu, Y.; Luehmann, H.; Xia, X.; Wan, D.; Cutler, C.; Xia, Y. Radioluminescent Gold Nanocages with Controlled Radioactivity for Real-Time In Vivo Imaging Nano Lett. 2013, 13, 581-585 10.1021/nl304111v
105. Wang, Y.; Black, K. C. L.; Luehmann, H.; Li, W.; Zhang, Y.; Cai, X.; Wan, D.; Liu, S.-Y.; Li, M.; Kim, P. Comparison Study of Gold Nanohexapods, Nanorods, and Nanocages for Photothermal Cancer Treatment ACS Nano 2013, 7, 2068-2077 10.1021/nn304332s
106. Antaris, A. L.; Robinson, J. T.; Yaghi, O. K.; Hong, G.; Diao, S.; Luong, R.; Dai, H. Ultra-Low Doses of Chirality Sorted (6,5) Carbon Nanotubes for Simultaneous Tumor Imaging and Photothermal Therapy ACS Nano 2013, 7, 3644-3652 10.1021/nn4006472
107. Liu, X.; Tao, H.; Yang, K.; Zhang, S.; Lee, S.-T.; Liu, Z. Optimization of Surface Chemistry on Single-Walled Carbon Nanotubes for In Vivo Photothermal Ablation of Tumors Biomaterials 2011, 32, 144-151 10.1016/j.biomaterials.2010.08.096
108. Sykes, E. A.; Chen, J.; Zheng, G.; Chan, W. C. W. Investigating the Impact of Nanoparticle Size on Active and Passive Tumor Targeting Efficiency ACS Nano 2014, 8, 5696-5706 10.1021/nn500299p
109. Phillips, E.; Penate-Medina, O.; Zanzonico, P. B.; Carvajal, R. D.; Mohan, P.; Ye, Y. P.; Humm, J.; Gonen, M.; Kalaigian, H.; Schoder, H. Clinical Translation of an Ultrasmall Inorganic Optical-PET Imaging Nanoparticle Probe Sci. Transl. Med. 2014, 6, 260ra149 10.1126/scitranslmed.3009524
110. Jiang, T.; Olson, E. S.; Nguyen, Q. T.; Roy, M.; Jennings, P. A.; Tsien, R. Y. Tumor Imaging by Means of Proteolytic Activation of Cell-Penetrating Peptides Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 17867-17872 10.1073/pnas.0408191101
111. Maeda, H.; Nakamura, H.; Fang, J. The Epr Effect for Macromolecular Drug Delivery to Solid Tumors: Improvement of Tumor Uptake, Lowering of Systemic Toxicity, and Distinct Tumor Imaging Adv. Drug Delivery Rev. 2013, 65, 71-79 10.1016/j.addr.2012.10.002
112. Choi, H. S.; Gibbs, S. L.; Lee, J. H.; Kim, S. H.; Ashitate, Y.; Liu, F.; Hyun, H.; Park, G.; Xie, Y.; Bae, S. Targeted Zwitterionic near-Infrared Fluorophores for Improved Optical Imaging Nat. Biotechnol. 2013, 31, 148-153 10.1038/nbt.2468
113. Guerrero, S.; Herance, J. R.; Rojas, S.; Mena, J. F.; Gispert, J. D.; Acosta, G. A.; Albericio, F.; Kogan, M. J. Synthesis and In Vivo Evaluation of the Biodistribution of a 18F-Labeled Conjugate Gold-Nanoparticle-Peptide with Potential Biomedical Application Bioconjugate Chem. 2012, 23, 399-408 10.1021/bc200362a
114. Malfatti, M. A.; Palko, H. A.; Kuhn, E. A.; Turteltaub, K. W. Determining the Pharmacokinetics and Long-Term Biodistribution of SiO2 Nanoparticles In Vivo Using Accelerator Mass Spectrometry Nano Lett. 2012, 12, 5532-5538 10.1021/nl302412f
115. He, X.; Nie, H.; Wang, K.; Tan, W.; Wu, X.; Zhang, P. In Vivo Study of Biodistribution and Urinary Excretion of Surface-Modified Silica Nanoparticles Anal. Chem. 2008, 80, 9597-9603 10.1021/ac801882g
116. Lu, J.; Liong, M.; Li, Z.; Zink, J. I.; Tamanoi, F. Biocompatibility, Biodistribution, and Drug-Delivery Efficiency of Mesoporous Silica Nanoparticles for Cancer Therapy in Animals Small 2010, 6, 1794-1805 10.1002/smll.201000538
117. Tang, S.; Chen, M.; Zheng, N. Multifunctional Ultrasmall Pd Nanosheets for Enhanced near-Infrared Photothermal Therapy and Chemotherapy of Cancer Nano Res. 2015, 8, 165-174 10.1007/s12274-014-0605-x
118. Zhang, X. D.; Luo, Z.; Chen, J.; Shen, X.; Song, S.; Sun, Y.; Fan, S.; Fan, F.; Leong, D. T.; Xie, J. Ultrasmall Au10-12(SG)10-12 Nanomolecules for High Tumor Specificity and Cancer Radiotherapy Adv. Mater. 2014, 26, 4565-4568 10.1002/adma.201400866
119. Zhang, X. D.; Luo, Z.; Chen, J.; Song, S.; Yuan, X.; Shen, X.; Wang, H.; Sun, Y.; Gao, K.; Zhang, L. Ultrasmall Glutathione-Protected Gold Nanoclusters as Next Generation Radiotherapy Sensitizers with High Tumor Uptake and High Renal Clearance Sci. Rep. 2015, 5, 8669 10.1038/srep08669
120. Lammers, T.; Aime, S.; Hennink, W. E.; Storm, G.; Kiessling, F. Theranostic Nanomedicine Acc. Chem. Res. 2011, 44, 1029-1038 10.1021/ar200019c
121. Ernsting, M. J.; Murakami, M.; Roy, A.; Li, S. D. Factors Controlling the Pharmacokinetics, Biodistribution and Intratumoral Penetration of Nanoparticles J. Controlled Release 2013, 172, 782-794 10.1016/j.jconrel.2013.09.013