Dual-Enzyme-Loaded Multifunctional Hybrid Nanogel System for Pathological Responsive Ultrasound Imaging and T 2-Weighted Magnetic Resonance Imaging

ACS Nano

Volumn 9, Issue 6, 2015, Pages 5646-5656

  Wang, Xia ^a   Niu, Dechao ^b   Li, Pei ^c   Wu, Qing ^a   Bo, Xiaowan ^c   Liu, Boji ^c   Bao, Song ^a   Su, Teng ^a   Xu, Huixiong ^c   Wang, Qigang ^a  

^a TONGJI UNIVERSITY   (China)

^b EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c TENTH PEOPLE S HOSPITAL OF TONGJI UNIVERSITY   (China)

Author keywords

hybrid nanogels; magnetic resonance imaging; pathological responsiveness; ultrasound imaging

Indexed keywords

IRON OXIDES; MAGNETIC RESONANCE IMAGING; MAGNETISM; NANOSTRUCTURED MATERIALS; PROBES; RESONANCE; ULTRASONIC IMAGING;

ACIDIC ENVIRONMENT; CATIONIC POLYMERS; HYBRID NANOGELS; IMAGING CAPABILITIES; PATHOLOGICAL RESPONSIVENESS; SUPER OXIDE DISMUTASE; SUPERPARAMAGNETIC IRON OXIDES; ULTRASOUND IMAGING;

ENZYMES;

CATALASE; MACROGOL DERIVATIVE; MULTIFUNCTIONAL ENZYME; NANOGEL; POLYETHYLENEIMINE; SUPEROXIDE DISMUTASE;

BIOCATALYSIS; CELL SURVIVAL; CHEMISTRY; HEPG2 CELL LINE; HUMAN; LIVER NEOPLASMS; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; ULTRASOUND;

BIOCATALYSIS; CATALASE; CELL SURVIVAL; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MAGNETIC RESONANCE IMAGING; MULTIFUNCTIONAL ENZYMES; POLYETHYLENE GLYCOLS; POLYETHYLENEIMINE; SUPEROXIDE DISMUTASE; ULTRASONICS;

EID: 84934924563     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn5068094     Document Type: Article

References (64)

1. Louie, A. Y. Multimodality Imaging Probes: Design and Challenges Chem. Rev. 2010, 110, 3146-3195
2. Massoud, T. F.; Gambhir, S. S. Molecular Imaging in Living Subjects: Seeing Fundamental Biological Processes in a New Light Gene Dev. 2003, 17, 545-580
3. Major, J. L.; Meade, T. J. Bioresponsive, Cell-Penetrating, and Multimeric MR Contrast Agents Acc. Chem. Res. 2009, 42, 893-903
4. Terreno, E.; Delli Castelli, D.; Viale, A.; Aime, S. Challenges for Molecular Magnetic Resonance Imaging Chem. Rev. 2010, 110, 3019-3042
5. Yang, F.; Li, L.; Li, Y.; Chen, Z.; Wu, J.; Gu, N. Superparamagnetic Nanoparticle-Inclusion Microbubbles for Ultrasound Contrast Agents Phys. Med. Biol. 2008, 53, 6129-6141
6. Yang, F.; Li, Y.; Chen, Z.; Zhang, Y.; Wu, J.; Gu, N. Superparamagnetic Iron Oxide Nanoparticle-Embedded Encapsulated Microbubbles as Dual Contrast Agents of Magnetic Resonance and Ultrasound Imaging Biomaterials 2009, 30, 3882-3890
7. Sun, Y.; Zheng, Y.; Ran, H.; Zhou, Y.; Shen, H.; Chen, Y.; Chen, H.; Krupka, T. M.; Li, A.; Li, P. et al. Superparamagnetic PLGA-Iron Oxide Microcapsules for Dual-Modality US/MR Imaging and High Intensity Focused US Breast Cancer Ablation Biomaterials 2012, 33, 5854-5864
8. Ao, M.; Wang, Z.; Ran, H.; Guo, D.; Yu, J.; Li, A.; Chen, W.; Wu, W.; Zheng, Y. Gd-DTPA-Loaded PLGA Microbubbles as Both Ultrasound Contrast Agent and MRI Contrast Agent-a Feasibility Research J. Bio. Med. Mater. Res. B 2010, 93B, 551-556
9. Chen, Y.; Chen, H.; Sun, Y.; Zheng, Y.; Zeng, D.; Li, F.; Zhang, S.; Wang, X.; Zhang, K.; Ma, M. et al. Multifunctional Mesoporous Composite Nanocapsules for Highly Efficient MRI-Guided High-Intensity Focused Ultrasound Cancer Surgery Angew. Chem., Int. Ed. 2011, 50, 12505-12509
10. Niu, D. C.; Wang, X.; Li, Y. S.; Zheng, Y. Y.; Li, F. Q.; Chen, H. R.; Gu, J. L.; Zhao, W. R.; Shi, J. L. Facile Synthesis of Magnetite/Perfluorocarbon Co-Loaded Organic/Inorganic Hybrid Vesicles for Dual-Modality Ultrasound/Magnetic Resonance Imaging and Imaging-Guided High-Intensity Focused Ultrasound Ablation Adv. Mater. 2013, 25, 2686-2692
11. Albini, A.; Sporn, M. B. The Tumour Microenvironment as a Target for Chemoprevention Nat. Rev. Cancer 2007, 7, 139-147
12. Danhier, F.; Feron, O.; Preat, V. To Exploit the Tumor Microenvironment: Passive and Active Tumor Targeting of Nanocarriers for Anti-Cancer Drug Delivery J. Controlled Release 2010, 148, 135-146
13. Cao, C. Y.; Shen, Y. Y.; Wang, J. D.; Li, L.; Liang, G. L. Controlled Intracellular Self-Assembly of Gadolinium Nanoparticles as Smart Molecular MR Contrast Agents Sci. Rep.-Uk 2013, 3, 1024
14. An, L. N.; Gilani, M. R. H. S.; Liang, G. L. Peptide-Based Nanostructures for Cancer Diagnosis and Therapy Curr. Med. Chem. 2014, 21, 2453-2466
15. Shuhendler, A. J.; Pu, K. Y.; Cui, L.; Uetrecht, J. P.; Rao, J. H. Real-Time Imaging of Oxidative and Nitrosative Stress in the Liver of Live Animals for Drug-Toxicity Testing Nat. Biotechnol. 2014, 32, 373-U240
16. Ye, D. J.; Shuhendler, A. J.; Cui, L. N.; Tong, L.; Tee, S. S.; Tikhomirov, G.; Felsher, D. W.; Rao, J. H. Bioorthogonal Cyclization-Mediated in Situ Self-Assembly of Small-Molecule Probes for Imaging Caspase Activity in Vivo. Nat. Chem. 2014, 6, 519-526
17. Fang, J.; Seki, T.; Maeda, H. Therapeutic Strategies by Modulating Oxygen Stress in Cancer and Inflammation Adv. Drug Delivery Rev. 2009, 61, 290-302
18. Barnes, P. J. Immunology of Asthma and Chronic Obstructive Pulmonary Disease Nat. Rev. Immunol. 2008, 8, 183-192
19. Chen, X.; Tian, X.; Shin, I.; Yoon, J. Fluorescent and Luminescent Probes for Detection of Reactive Oxygen and Nitrogen Species Chem. Soc. Rev. 2011, 40, 4783-804
20. Asanuma, D.; Takaoka, Y.; Namiki, S.; Takikawa, K.; Kamiya, M.; Nagano, T.; Urano, Y.; Hirose, K. Acidic-pH-Activatable Fluorescence Probes for Visualizing Exocytosis Dynamics Angew. Chem., Int. Ed. 2014, 53, 6085-6089
21. Ling, D.; Park, W.; Park, S. J.; Lu, Y.; Kim, K. S.; Hackett, M. J.; Kim, B. H.; Yim, H.; Jeon, Y. S.; Na, K. et al. Multifunctional Tumor pH-Sensitive Self-Assembled Nanoparticles for Bimodal Imaging and Treatment of Resistant Heterogeneous Tumors J. Am. Chem. Soc. 2014, 136, 5647-5655
22. 2 Nanogenerator for Ultrasound and Magnetic-Resonance Dual Modality Imaging Adv. Mater. 2012, 24, 5205-5211
23. Nayak, S.; Lyon, L. A. Soft Nanotechnology with Soft Nanoparticles Angew. Chem., Int. Ed. 2005, 44, 7686-7708
24. Sasaki, Y.; Akiyoshi, K. Nanogel Engineering for New Nanobiomaterials: From Chaperoning Engineering to Biomedical Applications Chem. Rec. 2010, 10, 366-376
25. Appel, E. A.; Loh, X. J.; Jones, S. T.; Biedermann, F.; Dreiss, C. A.; Scherman, O. A. Ultrahigh-Water-Content Supramolecular Hydrogels Exhibiting Multistimuli Responsiveness J. Am. Chem. Soc. 2012, 134, 11767-11773
26. Li, J. Y.; Li, X. M.; Kuang, Y.; Gao, Y.; Du, X. W.; Shi, J. F.; Xu, B. Self-Delivery Multifunctional Anti-HIV Hydrogels for Sustained Release Adv. Healthcare Mater. 2013, 2, 1586-1590
27. Morris, K. L.; Chen, L.; Raeburn, J.; Sellick, O. R.; Cotanda, P.; Paul, A.; Griffiths, P. C.; King, S. M.; O'Reilly, R. K.; Serpell, L. C. et al. Chemically Programmed Self-Sorting of Gelator Networks Nat. Commun. 2013, 4, 1480
28. Thornton, P. D.; Mart, R. J.; Ulijn, R. V. Enzyme-Responsive Polymer Hydrogel Particles for Controlled Release Adv. Mater. 2007, 19, 1252-1256
29. Thornton, P. D.; Mart, R. J.; Webb, S. J.; Ulijn, R. V. Enzyme-Responsive Hydrogel Particles for the Controlled Release of Proteins: Designing Peptide Actuators to Match Payload Soft Matter 2008, 4, 821-827
30. Kabanov, A. V.; Vinogradov, S. V. Nanogels as Pharmaceutical Carriers: Finite Networks of Infinite Capabilities Angew. Chem., Int. Ed. 2009, 48, 5418-5429
31. Nochi, T.; Yuki, Y.; Takahashi, H.; Sawada, S.; Mejima, M.; Kohda, T.; Harada, N.; Kong, I. G.; Sato, A.; Kataoka, N. et al. Nanogel Antigenic Protein-Delivery System for Adjuvant-Free Intranasal Vaccines Nat. Mater. 2010, 9, 572-578
32. Wang, Q. G.; Yang, Z. M.; Zhang, X. Q.; Xiao, X. D.; Chang, C. K.; Xu, B. A Supramolecular-Hydrogel-Encapsulated Hemin as an Artificial Enzyme to Mimic Peroxidase Angew. Chem., Int. Ed. 2007, 46, 4285-4289
33. Gao, Y.; Zhao, F.; Wang, Q. G.; Zhang, Y.; Xu, B. Small Peptide Nanofibers as the Matrices of Molecular Hydrogels for Mimicking Enzymes and Enhancing the Activity of Enzymes Chem. Soc. Rev. 2010, 39, 3425-3433
34. Kudina, O.; Zakharchenko, A.; Trotsenko, O.; Tokarev, A.; Ionov, L.; Stoychev, G.; Puretskiy, N.; Pryor, S. W.; Voronov, A.; Minko, S. Highly Efficient Phase Boundary Biocatalysis with Enzymogel Nanoparticles Angew. Chem., Int. Ed. 2014, 53, 483-487
35. Paquet, C.; de Haan, H. W.; Leek, D. M.; Lin, H. Y.; Xiang, B.; Tian, G. H.; Kell, A.; Simard, B. Clusters of Superparamagnetic Iron Oxide Nanoparticles Encapsulated in a Hydrogel: A Particle Architecture Generating a Synergistic Enhancement of the T-2 Relaxation ACS Nano 2011, 5, 3104-3112
36. Santra, S.; Jativa, S. D.; Kaittanis, C.; Normand, G.; Grimm, J.; Perez, J. M. Gadolinium-Encapsulating Iron Oxide Nanoprobe as Activatable NMR/MRI Contrast Agent ACS Nano 2012, 6, 7281-7294
37. Courant, T.; Roullin, V. G.; Cadiou, C.; Callewaert, M.; Andry, M. C.; Portefaix, C.; Hoeffel, C.; de Goltstein, M. C.; Port, M.; Laurent, S. et al. Hydrogels Incorporating GdDOTA: Towards Highly Efficient Dual T1/T2MRI Contrast Agents Angew. Chem., Int. Ed. 2012, 51, 9119-9122
38. Hasserodt, J.; Kolanowski, J. L.; Touti, F. Magnetogenesis in Water Induced by a Chemical Analyte Angew. Chem., Int. Ed. 2014, 53, 60-73
39. Hollmann, F.; Arends, I. W. C. E. Enzyme Initiated Radical Polymerizations Polymers-Basel 2012, 4 (1) 759-793
40. Su, T.; Zhang, D.; Tang, Z.; Wu, Q.; Wang, Q. G. HRP-Mediated Polymerization Forms Tough Nanocomposite Hydrogels with High Biocatalytic Performance Chem. Commun. 2013, 49, 8033-8035
41. Su, T.; Tang, Z.; He, H. J.; Li, W. J.; Wang, X.; Liao, C. N.; Sun, Y.; Wang, Q. G. Glucose Oxidase Triggers Gelation of N-Hydroxyimide-Heparin Conjugates to Form Enzyme-Responsive Hydrogels for Cell-Specific Drug Delivery Chem. Sci. 2014, 5, 4204-4209
42. Mao, Y. J.; Su, T.; Wu, Q.; Liao, C. A.; Wang, Q. G. Dual Enzymatic Formation of Hybrid Hydrogels with Supramolecular-Polymeric Networks Chem. Commun. 2014, 50, 14429-14432
43. Mates, J. M. Effects of Antioxidant Enzymes in the Molecular Control of Reactive Oxygen Species Toxicology Toxicology 2000, 153, 83-104
44. Fan, J.; Yin, J. J.; Ning, B.; Wu, X. C.; Hu, Y.; Ferrari, M.; Anderson, G. J.; Wei, J. Y.; Zhao, Y. L.; Nie, G. J. Direct Evidence for Catalase and Peroxidase Activities of Ferritin-Platinum Nanoparticles Biomaterials 2011, 32, 1611-1618
45. Okada, S.; Mizukami, S.; Matsumura, Y.; Yoshioka, Y.; Kikuchi, K. A Nanospherical Polymer as an MRI Sensor without Paramagnetic or Superparamagnetic Species Dalton Trans. 2013, 42, 15864-15867
46. Okada, S.; Mizukami, S.; Sakata, T.; Matsumura, Y.; Yoshioka, Y.; Kikuchi, K. Ratiometric MRI Sensors Based on Core-Shell Nanoparticles for Quantitative pH Imaging Adv. Mater. 2014, 26, 2989-2992
47. Shapiro, Y. E. Structure and Dynamics of Hydrogels and Organogels: An NMR Spectroscopy Approach Prog. Polym. Sci. 2011, 36, 1184-1253
48. Crayton, S. H.; Tsourkas, A. pH-Titratable Superparamagnetic Iron Oxide for Improved Nanoparticle Accumulation in Acidic Tumor Microenvironments ACS Nano 2011, 5, 9592-9601
49. Bronstein, L. M.; Huang, X. L.; Retrum, J.; Schmucker, A.; Pink, M.; Stein, B. D.; Dragnea, B. Influence of Iron Oleate Complex Structure on Iron Oxide Nanoparticle Formation Chem. Mater. 2007, 19, 3624-3632
50. 4 Nanoparticles in the Scale-up Synthesis Nanoscale 2013, 5, 2804-2810
51. Liu, G. H.; Gan, J. Q.; Chen, A. M.; Liu, Q.; Zhao, X. S. Synthesis and Characterization of an Amphiphilic Chitosan Bearing Octyl and Methoxy Polyethylene Nat. Sci. 2010, 2, 707-712
52. Gupta, A. K.; Wells, S. Surface-Modified Superparamagnetic Nanoparticles for Drug Delivery: Preparation, Characterization, and Cytotoxicity Studies IEEE Trans. Nanobiosci. 2004, 3, 66-73
53. David, C.; d'Andrea, C.; Lancelot, E.; Bochterle, J.; Guillot, N.; Fazio, B.; Marago, O. M.; Sutton, A.; Charnaux, N.; Neubrech, F. et al. Raman and IR Spectroscopy of Manganese Superoxide Dismutase, a Pathology Biomarker Vib. Spectrosc. 2012, 62, 50-58
54. Schutt, E. G.; Klein, D. H.; Mattrey, R. M.; Riess, J. G. Injectable Microbubbles as Contrast Agents for Diagnostic Ultrasound Imaging: The Key Role of Perfluorochemicals Angew. Chem., Int. Ed. 2003, 42, 3218-3235
55. Niu, D. C.; Li, Y. S.; Qiao, X. L.; Li, L.; Zhao, W. R.; Chen, H. R.; Zhao, Q. L.; Ma, Z.; Shi, J. L. A Facile Approach to Fabricate Functionalized Superparamagnetic Copolymer-Silica Nanocomposite Spheres Chem. Commun. 2008, 4463-4465
56. Chen, Z. T.; Niu, D. C.; Li, Y. S.; Shi, J. L. One-Step Approach to Synthesize Hollow Mesoporous Silica Spheres Colated by an Amphiphilic Block Copolymer and Cationic Surfactant RSC Adv. 2013, 3 (19) 6767-6770
57. Li, L.; Jiang, W.; Luo, K.; Song, H. M.; Lan, F.; Wu, Y.; Gu, Z. W. Superparamagnetic Iron Oxide Nanoparticles as MRI Contrast Agents for Non-invasive Stem Cell Labeling and Tracking Theranostics 2013, 3, 595-615
58. 4 Nanoparticles Trapped in a Porous Silicon Nanoparticle Host Adv. Mater. 2011, 23, H248-H253
59. Wang, X.; Chen, H. R.; Chen, Y.; Ma, M.; Zhang, K.; Li, F. Q.; Zheng, Y. Y.; Zeng, D. P.; Wang, Q.; Shi, J. L. Perfluorohexane-Encapsulated Mesoporous Silica Nanocapsules as Enhancement Agents for Highly Efficient High Intensity Focused Ultrasound (HIFU) Adv. Mater. 2012, 24, 785-791
60. 4 (M = Fe, Co, Mn) Nanoparticles J. Am. Chem. Soc. 2004, 126, 273-279
61. Aebi, H. Catalase in Vitro Methods Enzymol. 1984, 105, 121-126
62. Beers, R. F., Jr.; Sizer, I. W. A Spectrophotometric Method for Measuring the Breakdown of Hydrogen Peroxide by Catalase J. Biol. Chem. 1952, 195, 133-140
63. Kim, S. J.; Han, D.; Moon, K. D.; Rhee, J. S. Measurement of Superoxide Dismutase-Like Activity of Natural Antioxidants Biosci. Biotechnol. Biochem. 1995, 59, 822-826
64. Gao, R. M.; Yuan, Z. B.; Zhao, Z. Q.; Gao, X. R. Mechanism of Pyrogallol Autoxidation and Determination of Superoxide Dismutase Enzyme Activity Bioelectrochem. Bioenerg. 1998, 45, 41-45