Stimuli-Responsive Biodegradable Hyperbranched Polymer-Gadolinium Conjugates as Efficient and Biocompatible Nanoscale Magnetic Resonance Imaging Contrast Agents

ACS Applied Materials and Interfaces

Volumn 8, Issue 16, 2016, Pages 10499-10512

  Sun, Ling ^a   Li, Xue ^a   Wei, Xiaoli ^a   Luo, Qiang ^a   Guan, Pujun ^a   Wu, Min ^a   Zhu, Hongyan ^a   Luo, Kui ^a   Gong, Qiyong ^a  

^a SICHUAN UNIVERSITY   (China)

Author keywords

biocompatibility; biodegradable; cancer diagnosis; hyperbranched polymer; nanoscale MRI contrast agent

Indexed keywords

BIOCOMPATIBILITY; BIODEGRADABLE POLYMERS; CYTOTOXICITY; DENDRIMERS; DIAGNOSIS; DISEASES; ENZYMES; ETHYLENE; ETHYLENE GLYCOL; FREE RADICAL POLYMERIZATION; FUNCTIONAL POLYMERS; GADOLINIUM; MACROMOLECULES; MAGNETIC RESONANCE IMAGING; MOLECULAR IMAGING; NANOTECHNOLOGY; STRUCTURAL OPTIMIZATION; TUMORS;

BIODEGRADABLE; CANCER DIAGNOSIS; DENDRITIC MACROMOLECULES; HYPERBRANCHED POLYMERS; MAGNETIC RESONANCE IMAGING CONTRAST AGENTS; MRI CONTRAST AGENTS; POLY(OLIGO(ETHYLENE GLYCOL) METHACRYLATE); REVERSIBLE ADDITION-FRAGMENTATION CHAIN TRANSFER POLYMERIZATION;

NANOMAGNETICS;

BIOMATERIAL; CONTRAST MEDIUM; GADOLINIUM; NANOMATERIAL; POLYMER;

ANIMAL; MACROMOLECULE; MOUSE; NUCLEAR MAGNETIC RESONANCE IMAGING;

ANIMALS; BIOCOMPATIBLE MATERIALS; CONTRAST MEDIA; GADOLINIUM; MACROMOLECULAR SUBSTANCES; MAGNETIC RESONANCE IMAGING; MICE; NANOSTRUCTURES; POLYMERS;

EID: 84966300028     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.6b00980     Document Type: Article

References (65)

1. Bennett, K. M.; Jo, J.-i.; Cabral, H.; Bakalova, R.; Aoki, I. MR Imaging Techniques for Nano-Pathophysiology and Theranostics Adv. Drug Delivery Rev. 2014, 74, 75-94 10.1016/j.addr.2014.04.007
2. Peer, D.; Karp, J. M.; Hong, S.; Farokhzad, O. C.; Margalit, R.; Langer, R. Nanocarriers as an Emerging Platform for Cancer Therapy Nat. Nanotechnol. 2007, 2, 751-760 10.1038/nnano.2007.387
3. Hanahan, D.; Weinberg, R. A. Hallmarks of Cancer: the Next Generation Cell 2011, 144, 646-674 10.1016/j.cell.2011.02.013
4. Davis, M. E.; Chen, Z.; Shin, D. M. Nanoparticle Therapeutics: an Emerging Treatment Modality for Cancer Nat. Rev. Drug Discovery 2008, 7, 771-782 10.1038/nrd2614
5. Farokhzad, O. C.; Langer, R. Impact of Nanotechnology on Drug Delivery ACS Nano 2009, 3, 16-20 10.1021/nn900002m
6. Lv, F.; Qiu, T.; Liu, L.; Ying, J.; Wang, S. Recent Advances in Conjugated Polymer Materials for Disease Diagnosis Small 2016, 12, 696-705 10.1002/smll.201501700
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 10.1039/C1CS15242D
8. Wang, X.; Cai, X.; Hu, J.; Shao, N.; Wang, F.; Zhang, Q.; Xiao, J.; Cheng, Y. Glutathione-Triggered "off-on" Release of Anticancer Drugs from Dendrimer-Encapsulated Gold Nanoparticles J. Am. Chem. Soc. 2013, 135, 9805-9810 10.1021/ja402903h
9. Jia, H.-Z.; Zhang, W.; Zhu, J.-Y.; Yang, B.; Chen, S.; Chen, G.; Zhao, Y.-F.; Feng, J.; Zhang, X.-Z. Hyperbranched-hyperbranched Polymeric Nanoassembly to Mediate Controllable Co-delivery of siRNA and Drug for Synergistic Tumor Therapy J. Controlled Release 2015, 216, 9-17 10.1016/j.jconrel.2015.08.006
10. Liu, J.; Huang, W.; Pang, Y.; Yan, D. Hyperbranched Polyphosphates: Synthesis, Functionalization and Biomedical Applications Chem. Soc. Rev. 2015, 44, 3942-3953 10.1039/C5CS00318K
11. Kaneshiro, T. L.; Wang, X.; Lu, Z.-R. Synthesis, Characterization, and Gene Delivery of Poly-L-Lysine Octa(3-aminopropyl) Silsesquioxane Dendrimers: Nanoglobular Drug Carriers with Precisely Defined Molecular Architectures Mol. Pharmaceutics 2007, 4, 759-768 10.1021/mp070036z
12. Lim, J.; Simanek, E. E. Triazine Dendrimers as Drug Delivery Systems: from Synthesis to Therapy Adv. Drug Delivery Rev. 2012, 64, 826-835 10.1016/j.addr.2012.03.008
13. Zhang, C.; Pan, D.; Luo, K.; She, W.; Guo, C.; Yang, Y.; Gu, Z. Peptide Dendrimer-Doxorubicin Conjugate-Based Nanoparticle as an Enzyme-Responsive Drug Delivery System for Cancer Therapy Adv. Healthcare Mater. 2014, 3, 1299-1308 10.1002/adhm.201300601
14. Luo, K.; Liu, G.; Zhang, X.; She, W.; He, B.; Nie, Y.; Li, L.; Wu, Y.; Zhang, Z.; Gong, Q.; Gao, F.; Song, B.; Ai, H.; Gu, Z. Functional L-Lysine Dendritic Macromolecules as Liver-Imaging Probes Macromol. Biosci. 2009, 9, 1227-1236 10.1002/mabi.200900231
15. Tomalia, D. A.; Naylor, A. M.; Goddard, W. A. Starburst Dendrimers: Molecular-level Control of Size, Shape, Surface Chemistry, Topology, and Flexibility from Atoms to Macroscopic Matter Angew. Chem., Int. Ed. Engl. 1990, 29, 138-175 10.1002/anie.199001381
16. Li, Y.; Zhu, H.; Wang, S.; Qian, X.; Fan, J.; Wang, Z.; Song, P.; Zhang, X.; Lu, W.; Ju, D. Interplay of Oxidative Stress and Autophagy in PAMAM Dendrimers-induced Neuronal Cell Death Theranostics 2015, 5, 1363-1377 10.7150/thno.13181
17. Wolinsky, J. B.; Grinstaff, M. W. Therapeutic and Diagnostic Applications of Dendrimers for Cancer Treatment Adv. Drug Delivery Rev. 2008, 60, 1037-1055 10.1016/j.addr.2008.02.012
18. Li, T.; Smet, M.; Dehaen, W.; Xu, H. Selenium-Platinum Coordination Dendrimers with Controlled Anti-cancer Activity ACS Appl. Mater. Interfaces 2016, 8, 3609-3614 10.1021/acsami.5b07877
19. Pan, D.; Guo, C.; Luo, K.; Yi, Q.; Gu, Z.; She, W. PEGylated Dendritic Diaminocyclohexyl-Platinum(II) Conjugates as pH-Responsive Drug Delivery Vehicles with Enhanced Tumor Accumulation and Antitumor Efficacy Biomaterials 2014, 35, 10080-10092 10.1016/j.biomaterials.2014.09.006
20. Luo, K.; Liu, G.; She, W.; Wang, Q.; Wang, G.; He, B.; Ai, H.; Gong, Q.; Song, B.; Gu, Z. Gadolinium-Labeled Peptide Dendrimers with Controlled Structures as Potential Magnetic Resonance Imaging Contrast Agents Biomaterials 2011, 32, 7951-7960 10.1016/j.biomaterials.2011.07.006
21. Qiao, Z.; Shi, X. Dendrimer-Based Molecular Imaging Contrast Agents Prog. Polym. Sci. 2015, 44, 1-27 10.1016/j.progpolymsci.2014.08.002
22. Luo, K.; Li, C.; Li, L.; She, W.; Wang, G.; Gu, Z. Arginine Functionalized Peptide Dendrimers as Potential Gene Delivery Vehicles Biomaterials 2012, 33, 4917-4927 10.1016/j.biomaterials.2012.03.030
23. Ardana, A.; Whittaker, A. K.; Thurecht, K. J. PEG-based Hyperbranched Polymer Theranostics: Optimizing Chemistries for Improved Bioconjugation Macromolecules 2014, 47, 5211-5219 10.1021/ma501196h
24. Chauhan, V. P.; Stylianopoulos, T.; Martin, J. D.; Popović, Z.; Chen, O.; Kamoun, W. S.; Bawendi, M. G.; Fukumura, D.; Jain, R. K. Normalization of Tumour Blood Vessels Improves the Delivery of Nanomedicines in a Size-dependent Manner Nat. Nanotechnol. 2012, 7, 383-388 10.1038/nnano.2012.45
25. Qiao, R.; Jia, Q.; Hüwel, S.; Xia, R.; Liu, T.; Gao, F.; Galla, H.-J.; Gao, M. Receptor-Mediated Delivery of Magnetic Nanoparticles Across the Blood-Brain Barrier ACS Nano 2012, 6, 3304-3310 10.1021/nn300240p
26. Xie, J.; Liu, G.; Eden, H. S.; Ai, H.; Chen, X. Surface-engineered Magnetic Nanoparticle Platforms for Cancer Imaging and Therapy Acc. Chem. Res. 2011, 44, 883-892 10.1021/ar200044b
27. Yan, H.; Wang, L.; Wang, J.; Weng, X.; Lei, H.; Wang, X.; Jiang, L.; Zhu, J.; Lu, W.; Wei, X. et al. Two-order Targeted Brain Tumor Imaging by Using an Optical/Paramagnetic Nanoprobe Across the Blood Brain Barrier ACS Nano 2012, 6, 410-420 10.1021/nn203749v
28. 3 Biomaterials 2014, 35, 1667-1675 10.1016/j.biomaterials.2013.10.072
29. Li, Z.; Huang, P.; Zhang, X.; Lin, J.; Yang, S.; Liu, B.; Gao, F.; Xi, P.; Ren, Q.; Cui, D. RGD-Conjugated Dendrimer-Modified Gold Nanorods for In Vivo Tumor Targeting and Photothermal Therapy Mol. Pharmaceutics 2010, 7, 94-104 10.1021/mp9001415
30. Seymour, L.; Duncan, R.; Strohalm, J.; Kopeček, J. Effect of Molecular Weight (Mw) of N-(2-hydroxypropyl) Methacrylamide Copolymers on Body Distribution and Rate of Excretion After Subcutaneous, Intraperitoneal, and Intravenous Administration to Rats J. Biomed. Mater. Res. 1987, 21, 1341-1358 10.1002/jbm.820211106
31. Allmeroth, M.; Moderegger, D.; Biesalski, B.; Koynov, K.; Rösch, F.; Thews, O.; Zentel, R. Modifying the Body Distribution of HPMA-based Copolymers by Molecular Weight and Aggregate Formation Biomacromolecules 2011, 12, 2841-2849 10.1021/bm2005774
32. Zhang, R.; Luo, K.; Yang, J.; Sima, M.; Sun, Y.; Janát-Amsbury, M. M.; Kopeček, J. Synthesis and Evaluation of a Backbone Biodegradable Multiblock HPMA Copolymer Nanocarrier for the Systemic Delivery of Paclitaxel J. Controlled Release 2013, 166, 66-74 10.1016/j.jconrel.2012.12.009
33. Yang, Y.; Pan, D.; Luo, K.; Li, L.; Gu, Z. Biodegradable and Amphiphilic Block Copolymer-Doxorubicin Conjugate as Polymeric Nanoscale Drug Delivery Vehicle for Breast Cancer Therapy Biomaterials 2013, 34, 8430-8443 10.1016/j.biomaterials.2013.07.037
34. Zhang, R.; Yang, J.; Sima, M.; Zhou, Y.; Kopeček, J. Sequential Combination Therapy of Ovarian Cancer with Degradable N-(2-Hydroxypropyl) Methacrylamide Copolymer Paclitaxel and Gemcitabine Conjugates Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 12181-12186 10.1073/pnas.1406233111
35. Marckmann, P.; Skov, L.; Rossen, K.; Dupont, A.; Damholt, M. B.; Heaf, J. G.; Thomsen, H. S. Nephrogenic Systemic Fibrosis: Suspected Causative Role of Gadodiamide Used for Contrast-enhanced Magnetic Resonance Imaging J. Am. Soc. Nephrol. 2006, 17, 2359-2362 10.1681/ASN.2006060601
36. Kaewlai, R.; Abujudeh, H. Nephrogenic Systemic Fibrosis AJR, Am. J. Roentgenol. 2012, 199, W17-W23 10.2214/AJR.11.8144
37. Luo, K.; Yang, J.; Kopečková, P.; Kopeček, J. Biodegradable Multiblock Poly[N-(2-hydroxypropyl) Methacrylamide] via Reversible Addition-Fragmentation Chain Transfer Polymerization and Click Chemistry Macromolecules 2011, 44, 2481-2488 10.1021/ma102574e
38. Duangjai, A.; Luo, K.; Zhou, Y.; Yang, J.; Kopeček, J. Combination Cytotoxicity of Backbone Degradable HPMA Copolymer Gemcitabine and Platinum Conjugates Toward Human Ovarian Carcinoma Cells Eur. J. Pharm. Biopharm. 2014, 87, 187-196 10.1016/j.ejpb.2013.11.008
39. Li, N.; Li, N.; Yi, Q.; Luo, K.; Guo, C.; Pan, D.; Gu, Z. Amphiphilic Peptide Dendritic Copolymer-Doxorubicin Nanoscale Conjugate Self-assembled to Enzyme-Responsive Anti-cancer Agent Biomaterials 2014, 35, 9529-9545 10.1016/j.biomaterials.2014.07.059
40. Vasey, P. A.; Kaye, S. B.; Morrison, R.; Twelves, C.; Wilson, P.; Duncan, R.; Thomson, A. H.; Murray, L. S.; Hilditch, T. E.; Murray, T. Phase I Clinical and Pharmacokinetic Study of PK1 [N-(2-hydroxypropyl) Methacrylamide Copolymer Doxorubicin]: First Member of a New Class of Chemotherapeutic Agents-Drug-Polymer Conjugates Clin. Cancer Res. 1999, 5, 83-94
41. Ye, Y.; Zhu, L.; Ma, Y.; Niu, G.; Chen, X. Synthesis and Evaluation of New iRGD Peptide Analogs for Tumor Optical Imaging Bioorg. Med. Chem. Lett. 2011, 21, 1146-1150 10.1016/j.bmcl.2010.12.112
42. Zhang, C.; Pan, D.; Luo, K.; Li, N.; Guo, C.; Zheng, X.; Gu, Z. Dendrimer-Doxorubicin Conjugate as Enzyme-Sensitive and Polymeric Nanoscale Drug Delivery Vehicle for Ovarian Cancer Therapy Polym. Chem. 2014, 5, 5227-5235 10.1039/C4PY00601A
43. Jing, H.; Guo, Z.; Guo, W.; Yang, W.; Xu, P.; Zhang, X. Synthesis and Characterization of Folic Acid Modified Water-Soluble Chitosan Derivatives for Folate-Receptor-Mediated Targeting Bioorg. Med. Chem. Lett. 2012, 22, 3418-3424 10.1016/j.bmcl.2012.03.102
44. Huang, C.-H.; Nwe, K.; Al Zaki, A.; Brechbiel, M. W.; Tsourkas, A. Biodegradable Polydisulfide Dendrimer Nanoclusters as MRI Contrast Agents ACS Nano 2012, 6, 9416-9424 10.1021/nn304160p
45. Ye, M.; Qian, Y.; Tang, J.; Hu, H.; Sui, M.; Shen, Y. Targeted Biodegradable Dendritic MRI Contrast Agent for Enhanced Tumor Imaging J. Controlled Release 2013, 169, 239-245 10.1016/j.jconrel.2013.01.034
46. Fischer, D.; Li, Y.; Ahlemeyer, B.; Krieglstein, J.; Kissel, T. In Vitro Cytotoxicity Testing of Polycations: Influence of Polymer Structure on Cell Viability and Hemolysis Biomaterials 2003, 24, 1121-1131 10.1016/S0142-9612(02)00445-3
47. Fu, Y.; Hu, R.; Li, C.; Wang, Q.; Liu, Z.; Xue, W. Effects of Poly(amidoamine) Dendrimers on the Structure and Function of Key Blood Components J. Bioact. Compat. Polym. 2014, 29, 165-179 10.1177/0883911514521921
48. Caravan, P.; Ellison, J. J.; McMurry, T. J.; Lauffer, R. B. Gadolinium (III) Chelates as MRI Contrast Agents: Structure, Dynamics, and Applications Chem. Rev. 1999, 99, 2293-2352 10.1021/cr980440x
49. L. Villaraza, A. J.; Bumb, A.; Brechbiel, M. W. Macromolecules, Dendrimers, and Nanomaterials in Magnetic Resonance Imaging: the Interplay Between Size, Function, and Pharmacokinetics Chem. Rev. 2010, 110, 2921-2959 10.1021/cr900232t
50. Luo, K.; Yang, J.; Kopečková, P.; Kopeček, J. Biodegradable Multiblock Poly[N-(2-hydroxypropyl) methacrylamide] via Reversible Addition-Fragmentation Chain Transfer Polymerization and Click Chemistry Macromolecules 2011, 44, 2481-2488 10.1021/ma102574e
51. Yang, J.; Luo, K.; Pan, H.; Kopečková, P.; Kopeček, J. Synthesis of Biodegradable Multiblock Copolymers by Click Coupling of RAFT-Generated Heterotelechelic PolyHPMA Conjugates React. Funct. Polym. 2011, 71, 294-302 10.1016/j.reactfunctpolym.2010.10.005
52. 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 10.1016/j.addr.2009.03.009
53. Kennan, R. P.; Zhong, J.; Gore, J. C. Intravascular Susceptibility Contrast Mechanisms in Tissues Magn. Reson. Med. 1994, 31, 9-21 10.1002/mrm.1910310103
54. Thomssen, C.; Schmitt, M.; Goretzki, L.; Oppelt, P.; Pache, L.; Dettmar, P.; Janicke, F.; Graeff, H. Prognostic Value of the Cysteine Proteases Cathepsins B and Cathepsin L in Human Breast Cancer Clin. Cancer Res. 1995, 1, 741-746
55. Zhong, D.; Jiao, Y.; Zhang, Y.; Zhang, W.; Li, N.; Zuo, Q.; Wang, Q.; Xue, W.; Liu, Z. Effects of the Gene Carrier Polyethyleneimines on Structure and Function of Blood Components Biomaterials 2013, 34, 294-305 10.1016/j.biomaterials.2012.09.060
56. Sarath Chandra, V.; Baskar, G.; Suganthi, R.; Elayaraja, K.; Ahymah Joshy, M.; Sofi Beaula, W.; Mythili, R.; Venkatraman, G.; Narayana Kalkura, S. Blood Compatibility of Iron-Doped Nanosize Hydroxyapatite and Its Drug Release ACS Appl. Mater. Interfaces 2012, 4, 1200-1210 10.1021/am300140q
57. Hu, M.; Chen, M.; Li, G.; Pang, Y.; Wang, D.; Wu, J.; Qiu, F.; Zhu, X.; Sun, J. Biodegradable Hyperbranched Polyglycerol with Ester Linkages for Drug Delivery Biomacromolecules 2012, 13, 3552-3561 10.1021/bm300966d
58. Kainthan, R. K.; Janzen, J.; Levin, E.; Devine, D. V.; Brooks, D. E. Biocompatibility Testing of Branched and Linear Polyglycidol Biomacromolecules 2006, 7, 703-709 10.1021/bm0504882
59. Mayer, A.; Vadon, M.; Rinner, B.; Novak, A.; Wintersteiger, R.; Fröhlich, E. The Role of Nanoparticle Size in Hemocompatibility Toxicology 2009, 258, 139-147 10.1016/j.tox.2009.01.015
60. Luddington, R. Thrombelastography/Thromboelastometry Clin. Lab. Haematol. 2005, 27, 81-90 10.1111/j.1365-2257.2005.00681.x
61. Nel, A.; Xia, T.; Mädler, L.; Li, N. Toxic Potential of Materials at the Nanolevel Science 2006, 311, 622-627 10.1126/science.1114397
62. Aillon, K. L.; Xie, Y.; El-Gendy, N.; Berkland, C. J.; Forrest, M. L. Effects of Nanomaterial Physicochemical Properties on In Vivo Toxicity Adv. Drug Delivery Rev. 2009, 61, 457-466 10.1016/j.addr.2009.03.010
63. Wang, K.; Ma, J.; He, M.; Gao, G.; Xu, H.; Sang, J.; Wang, Y.; Zhao, B.; Cui, D. Toxicity Assessments of Near-Infrared Upconversion Luminescent LaF3: Yb, Er in Early Development of Zebrafish Embryos Theranostics 2013, 3, 258-266 10.7150/thno.5701
64. Hung, C.-C.; Huang, W.-C.; Lin, Y.-W.; Yu, T.-W.; Chen, H.-H.; Lin, S.-C.; Chiang, W.-H.; Chiu, H.-C. Active Tumor Permeation and Uptake of Surface Charge-Switchable Theranostic Nanoparticles for Imaging-Guided Photothermal/Chemo Combinatorial Therapy Theranostics 2016, 6, 302-317 10.7150/thno.13686
65. Ke, T.; Feng, Y.; Guo, J.; Parker, D. L.; Lu, Z.-R. Biodegradable Cystamine Spacer Facilitates the Clearance of Gd(III) Chelates in Poly(glutamic acid) Gd-DO3A Conjugates for Contrast-Enhanced MR Imaging Magn. Reson. Imaging 2006, 24, 931-940 10.1016/j.mri.2006.03.009