Gadolinium-encapsulating iron oxide nanoprobe as activatable NMR/MRI contrast agent

ACS Nano

Volumn 6, Issue 8, 2012, Pages 7281-7294

  Santra, Santimukul ^a   Jativa, Samuel D ^a   Kaittanis, Charalambos ^b   Normand, Guillaume ^b   Grimm, Jan ^b   Perez, J Manuel ^a  

^a UNIVERSITY OF CENTRAL FLORIDA   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

activatable MRI imaging; Gd DTPA complex; iron oxide nanoprobe; magnetic relaxation; theranostic application

Indexed keywords

ACIDIC MEDIA; ANTICANCER DRUG; CANCER CELL LINES; CONTRAST AGENT; CYTOTOXIC EFFECTS; DEQUENCHING; DRUG RELEASE; DRUG-TARGETING; FOLATE RECEPTOR; GD-DTPA; HELA CELL; POLYACRYLIC ACIDS; POLYMER COATING; POLYMERIC COATINGS; RELAXATION RATES; SPIN LATTICES; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLES;

CARBOXYLIC ACIDS; CELL CULTURE; COATINGS; CYTOTOXICITY; GADOLINIUM; IRON OXIDES; MAGNETIC RELAXATION; METAL NANOPARTICLES; SIGNAL SYSTEMS; SUPERPARAMAGNETISM;

NANOPROBES;

CONTRAST MEDIUM; DIAGNOSTIC AGENT; GADOLINIUM; MAGNETITE NANOPARTICLE; NANOCAPSULE;

ARTICLE; CELL LINE; CHEMISTRY; CYTOLOGY; HEART MUSCLE CELL; HELA CELL; HUMAN; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SYNTHESIS;

CELL LINE; CONTRAST MEDIA; GADOLINIUM; HELA CELLS; HUMANS; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MAGNETITE NANOPARTICLES; MYOCYTES, CARDIAC; NANOCAPSULES;

EID: 84865592337     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn302393e     Document Type: Article

References (68)

1. Winter, P. M.; Caruthers, S. D.; Wickline, S. A.; Lanza, G. M. Molecular Imaging by MRI Curr. Cardiol. Rep. 2006, 8, 65-69
2. Hu, X.; Norris, D. G. Advances in High-Field Magnetic Resonance Imaging Annu. Rev. Biomed. Eng. 2004, 6, 157-184
3. Aime, S.; Cabella, C.; Colombatto, S.; Geninatti Crich, S.; Gianolio, E.; Maggioni, F. Insights into the Use of Paramagnetic Gd(III) Complexes in MR-Molecular Imaging Investigations J. Magn. Reson. Imaging 2002, 16, 394-406
4. Louie, A. Multimodality Imaging Probes: Design and Challenges Chem. Rev. 2010, 110, 3146-3195
5. Mulder, W. J.; Strijkers, G. J.; Griffioen, A. W.; van Bloois, L.; Molema, G.; Storm, G.; Koning, G. A.; Nicolay, K. A Liposomal System for Contrast-Enhanced Magnetic Resonance Imaging of Molecular Targets Bioconjugate Chem. 2004, 15, 799-806
6. Mazooz, G.; Mehlman, T.; Lai, T. S.; Greenberg, C. S.; Dewhirst, M. W.; Neeman, M. Development of Magnetic Resonance Imaging Contrast Material for In Vivo Mapping of Tissue Transglutaminase Activity Cancer Res. 2005, 65, 1369-1375
7. Josephson, L.; Tung, C. H.; Moore, A.; Weissleder, R. High-Efficiency Intracellular Magnetic Labeling with Novel Superparamagnetic-Tat Peptide Conjugates Bioconjugate Chem. 1999, 10, 186-191
8. 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
9. Song, Y.; Zong, H.; Trivedi, E. R.; Vesper, B. J.; Waters, E. A.; Barrett, A. G.; Radosevich, J. A.; Hoffman, B. M.; Meade, T. J. Synthesis and Characterization of New Porphyrazine-Gd(III) Conjugates as Multimodal MR Contrast Agents Bioconjugate Chem. 2010, 21, 2267-2275
10. Frullano, L.; Meade, T. J. Multimodal MRI Contrast Agents J. Biol. Inorg. Chem. 2007, 12, 939-949
11. Tu, C. Q.; Louie, A. Y. Photochromically-Controlled, Reversibly-Activated MRI and Optical Contrast Agent Chem. Commun. 2007, 1331-1333
12. Uzgiris, E. E.; Cline, H.; Moasser, B.; Grimmond, B.; Amaratunga, M.; Smith, J. F.; Goddard, G. Conformation and Structure of Polymeric Contrast Agents for Medical Imaging Biomacromolecules 2004, 5, 54-61
13. Endres, P. J.; MacRenaris, K. W.; Vogt, S.; Meade, T. J. Cell-Permeable MR Contrast Agents with Increased Intracellular Retention Bioconjugate Chem. 2008, 19, 2049-2059
14. Laurent, S.; Forge, D.; Port, M.; Roch, A.; Robic, C.; Vander Elst, L.; Muller, R. N. Magnetic Iron Oxide Nanoparticles: Synthesis, Stabilization, Vectorization, Physicochemical Characterizations, and Biological Applications Chem. Rev. 2008, 108, 2064-2110
15. Hu, F.; Macrenaris, K. W.; Waters, E. A.; Schultz-Sikma, E. A.; Eckermann, A. L.; Meade, T. J. Highly Dispersible, Superparamagnetic Magnetite Nanoflowers for Magnetic Resonance Imaging Chem. Commun. 2010, 46, 73-75
16. Cho, S. J.; Jarrett, B. R.; Louie, A. Y.; Kauzlarich, S. M. Gold-Coated Iron Nanoparticles: A Novel Magnetic Resonance Agent for T-1 and T-2 Weighted Imaging Nanotechnology 2006, 17, 640-644
17. Huber, M. M.; Staubli, A. B.; Kustedjo, K.; Gray, M. H.; Shih, J.; Fraser, S. E.; Jacobs, R. E.; Meade, T. J. Fluorescently Detectable Magnetic Resonance Imaging Agents Bioconjugate Chem. 1998, 9, 242-249
18. Hooker, J. M.; Datta, A.; Botta, M.; Raymond, K. N.; Francis, M. B. Magnetic Resonance Contrast Agents from Viral Capsid Shells: A Comparison of Exterior and Interior Cargo Strategies Nano Lett. 2007, 7, 2207-2210
19. Crich, S. G.; Biancone, L.; Cantaluppi, V.; Duo, D.; Esposito, G.; Russo, S.; Camussi, G.; Aime, S. Improved Route for the Visualization of Stem Cells Labeled with a Gd-/Eu-Chelate as Dual (MRI and Fluorescence) Agent Magn. Reson. Med. 2004, 51, 938-944
20. Brekke, C.; Morgan, S. C.; Lowe, A. S.; Meade, T. J.; Price, J.; Williams, S. C.; Modo, M. The In Vitro Effects of a Bimodal Contrast Agent on Cellular Functions and Relaxometry NMR Biomed. 2007, 20, 77-89
21. Anderson, E. A.; Isaacman, S.; Peabody, D. S.; Wang, E. Y.; Canary, J. W.; Kirshenbaum, K. Viral Nanoparticles Donning a Paramagnetic Coat: Conjugation of MRI Contrast Agents to the MS2 Capsid Nano Lett. 2006, 6, 1160-1164
22. Santra, S.; Kaittanis, C.; Grimm, J.; Perez, J. M. Drug/Dye-Loaded, Multifunctional Iron Oxide Nanoparticles for Combined Targeted Cancer Therapy and Dual Optical/Magnetic Resonance Imaging Small 2009, 5, 1862-1868
23. Chen, T.; Shukoor, M. I.; Wang, R.; Zhao, Z.; Yuan, Q.; Bamrungsap, S.; Xiong, X.; Tan, W. Smart Multifunctional Nanostructure for Targeted Cancer Chemotherapy and Magnetic Resonance Imaging ACS Nano 2011, 5, 7866-7873
24. Kim, H. M.; Lee, H.; Hong, K. S.; Cho, M. Y.; Sung, M. H.; Poo, H.; Lim, Y. T. Synthesis and High Performance of Magnetofluorescent Polyelectrolyte Nanocomposites as MR/Near-Infrared Multimodal Cellular Imaging Nanoprobes ACS Nano 2011, 5, 8230-8240
25. Paquet, C.; de Haan, H. W.; Leek, D. M.; Lin, H. Y.; Xiang, B.; Tian, G.; Kell, A.; Simard, B. Clusters of Superparamagnetic Iron Oxide Nanoparticles Encapsulated in a Hydrogel: A Particle Architecture Generating a Synergistic Enhancement of the T2 Relaxation ACS Nano 2011, 5, 3104-3112
26. 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, 1619-1624
27. Tromsdorf, U. I.; Bigall, N. C.; Kaul, M. G.; Bruns, O. T.; Nikolic, M. S.; Mollwitz, B.; Sperling, R. A.; Reimer, R.; Hohenberg, H.; Parak, W. J. et al. Size and Surface Effects on the MRI Relaxivity of Manganese Ferrite Nanoparticle Contrast Agents Nano Lett. 2007, 7, 2422-2427
28. Tu, C.; Ng, T. S.; Sohi, H. K.; Palko, H. A.; House, A.; Jacobs, R. E.; Louie, A. Y. Receptor-Targeted Iron Oxide Nanoparticles for Molecular MR Imaging of Inflamed Atherosclerotic Plaques Biomaterials 2011, 32, 7209-7216
29. Bae, K. H.; Kim, Y. B.; Lee, Y.; Hwang, J.; Park, H.; Park, T. G. Bioinspired Synthesis and Characterization of Gadolinium-Labeled Magnetite Nanoparticles for Dual Contrast T(1)- and T(2)-Weighted Magnetic Resonance Imaging Bioconjugate Chem. 2010, 21, 505-512
30. Bull, S. R.; Guler, M. O.; Bras, R. E.; Meade, T. J.; Stupp, S. I. Self-Assembled Peptide Amphiphile Nanofibers Conjugated to MRI Contrast Agents Nano Lett. 2005, 5, 1-4
31. Bull, S. R.; Guler, M. O.; Bras, R. E.; Venkatasubramanian, P. N.; Stupp, S. I.; Meade, T. J. Magnetic Resonance Imaging of Self-Assembled Biomaterial Scaffolds Bioconjugate Chem. 2005, 16, 1343-1348
32. Datta, A.; Hooker, J. M.; Botta, M.; Francis, M. B.; Aime, S.; Raymond, K. N. High Relaxivity Gadolinium Hydroxypyridonate-Viral Capsid Conjugates: Nanosized MRI Contrast Agents J. Am. Chem. Soc. 2008, 130, 2546-2552
33. Drake, P.; Cho, H. J.; Shih, P. S.; Kao, C. H.; Lee, K. F.; Kuo, C. H.; Lin, X. Z.; Lin, Y. J. Gd-Doped Iron-Oxide Nanoparticles for Tumor Therapy via Magnetic Field Hyperthermia J. Mater. Chem. 2007, 17, 4914-4918
34. Pan, D.; Caruthers, S. D.; Hu, G.; Senpan, A.; Scott, M. J.; Gaffney, P. J.; Wickline, S. A.; Lanza, G. M. Ligand-Directed Nanobialys as Theranostic Agent for Drug Delivery and Manganese-Based Magnetic Resonance Imaging of Vascular Targets J. Am. Chem. Soc. 2008, 130, 9186-9187
35. Song, Y.; Kohlmeir, E. K.; Meade, T. J. Synthesis of Multimeric MR Contrast Agents for Cellular Imaging J. Am. Chem. Soc. 2008, 130, 6662-6663
36. Song, Y.; Xu, X.; MacRenaris, K. W.; Zhang, X. Q.; Mirkin, C. A.; Meade, T. J. Multimodal Gadolinium-Enriched DNA-Gold Nanoparticle Conjugates for Cellular Imaging Angew. Chem., Int. Ed. 2009, 48, 9143-9147
37. Cheng, Z.; Thorek, D. L.; Tsourkas, A. Gadolinium-Conjugated Dendrimer Nanoclusters as a Tumor Targeted T1 Magnetic Resonance Imaging Contrast Agent Angew. Chem., Int. Ed. 2010, 49, 346-350
38. Cheng, Z. L.; Thorek, D. L. J.; Tsourkas, A. Porous Polymersomes with Encapsulated Gd-Labeled Dendrimers as Highly Efficient MRI Contrast Agents Adv. Funct. Mater. 2009, 19, 3753-3759
39. Allen, M. J.; MacRenaris, K. W.; Venkatasubramanian, P. N.; Meade, T. J. Cellular Delivery of MRI Contrast Agents Chem. Biol. 2004, 11, 301-307
40. Manus, L. M.; Mastarone, D. J.; Waters, E. A.; Zhang, X. Q.; Schultz-Sikma, E. A.; Macrenaris, K. W.; Ho, D.; Meade, T. J. Gd(III)-Nanodiamond Conjugates for MRI Contrast Enhancement Nano Lett. 2010, 10, 484-489
41. Mastarone, D. J.; Harrison, V. S.; Eckermann, A. L.; Parigi, G.; Luchinat, C.; Meade, T. J. A Modular System for the Synthesis of Multiplexed Magnetic Resonance Probes J. Am. Chem. Soc. 2011, 133, 5329-5337
42. Major, J. L.; Meade, T. J. Bioresponsive, Cell-Penetrating, and Multimeric MR Contrast Agents Acc. Chem. Res. 2009, 42, 893-903
43. Kalman, F. K.; Woods, M.; Caravan, P.; Jurek, P.; Spiller, M.; Tircso, G.; Kiraly, R.; Brucher, E.; Sherry, A. D. Potentiometric and Relaxometric Properties of a Gadolinium-Based MRI Contrast Agent for Sensing Tissue pH Inorg. Chem. 2007, 46, 5260-5270
44. Duimstra, J. A.; Femia, F. J.; Meade, T. J. A Gadolinium Chelate for Detection of Beta-Glucuronidase: A Self-Immolative Approach J. Am. Chem. Soc. 2005, 127, 12847-12855
45. Caravan, P.; Cloutier, N. J.; Greenfield, M. T.; McDermid, S. A.; Dunham, S. U.; Bulte, J. W.; Amedio, J. C., Jr.; Looby, R. J.; Supkowski, R. M.; Horrocks, W. D. et al. The Interaction of MS-325 with Human Serum Albumin and Its Effect on Proton Relaxation Rates J. Am. Chem. Soc. 2002, 124, 3152-3162
46. Caravan, P. Strategies for Increasing the Sensitivity of Gadolinium Based MRI Contrast Agents Chem. Soc. Rev. 2006, 35, 512-523
47. Aime, S.; Castelli, D. D.; Crich, S. G.; Gianolio, E.; Terreno, E. Pushing the Sensitivity Envelope of Lanthanide-Based Magnetic Resonance Imaging (MRI) Contrast Agents for Molecular Imaging Applications Acc. Chem. Res. 2009, 42, 822-831
48. Tu, C.; Osborne, E. A.; Louie, A. Y. Activatable T1 and T2 Magnetic Resonance Imaging Contrast Agents Annu. Biomed. Eng. 2011, 39, 1335-1348
49. Major, J. L.; Parigi, G.; Luchinat, C.; Meade, T. J. The Synthesis and In Vitro Testing of a Zinc-Activated MRI Contrast Agent Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 13881-13886
50. Zhang, X. A.; Lovejoy, K. S.; Jasanoff, A.; Lippard, S. J. Water-Soluble Porphyrins as a Dual-Function Molecular Imaging Platform for MRI and Fluorescence Zinc Sensing Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 10780-10785
51. Louie, A. Y.; Huber, M. M.; Ahrens, E. T.; Rothbacher, U.; Moats, R.; Jacobs, R. E.; Fraser, S. E.; Meade, T. J. In Vivo Visualization of Gene Expression Using Magnetic Resonance Imaging Nat. Biotechnol. 2000, 18, 321-325
52. Urbanczyk-Pearson, L. M.; Meade, T. J. Preparation of Magnetic Resonance Contrast Agents Activated by Beta-Galactosidase Nat. Protoc. 2008, 3, 341-350
53. Frullano, L.; Tejerina, B.; Meade, T. J. Synthesis and Characterization of a Doxorubicin-Gd(III) Contrast Agent Conjugate: A New Approach toward Prodrug-Procontrast Complexes Inorg. Chem. 2006, 45, 8489-8491
54. Lee, J.; Burdette, J. E.; MacRenaris, K. W.; Mustafi, D.; Woodruff, T. K.; Meade, T. J. Rational Design, Synthesis, and Biological Evaluation of Progesterone-Modified MRI Contrast Agents Chem. Biol. 2007, 14, 824-834
55. Yang, H.; Zhuang, Y.; Sun, Y.; Dai, A.; Shi, X.; Wu, D.; Li, F.; Hu, H.; Yang, S. Targeted Dual-Contrast T1- and T2-Weighted Magnetic Resonance Imaging of Tumors Using Multifunctional Gadolinium-Labeled Superparamagnetic Iron Oxide Nanoparticles Biomaterials 2011, 32, 4584-4593
56. Perez, J. M.; Josephson, L.; O'Loughlin, T.; Hogemann, D.; Weissleder, R. Magnetic Relaxation Switches Capable of Sensing Molecular Interactions Nat. Biotechnol. 2002, 20, 816-820
57. Kaittanis, C.; Boukhriss, H.; Santra, S.; Naser, S. A.; Perez, J. M. Rapid and Sensitive Detection of an Intracellular Pathogen in Human Peripheral Leukocytes with Hybridizing Magnetic Relaxation Nanosensors PloS One 2012, 7, e35326
58. Kaittanis, C.; Santra, S.; Perez, J. M. Role of Nanoparticle Valency in the Nondestructive Magnetic-Relaxation-Mediated Detection and Magnetic Isolation of Cells in Complex Media J. Am. Chem. Soc. 2009, 131, 12780-12791
59. Kaittanis, C.; Santra, S.; Santiesteban, O. J.; Henderson, T. J.; Perez, J. M. The Assembly State between Magnetic Nanosensors and Their Targets Orchestrates Their Magnetic Relaxation Response J. Am. Chem. Soc. 2011, 133, 3668-3676
60. Haun, J. B.; Castro, C. M.; Wang, R.; Peterson, V. M.; Marinelli, B. S.; Lee, H.; Weissleder, R. Micro-NMR for Rapid Molecular Analysis of Human Tumor Samples Sci. Trans. Med. 2011, 3, 71ra16
61. Asati, A.; Santra, S.; Kaittanis, C.; Nath, S.; Perez, J. M. Oxidase-like Activity of Polymer-Coated Cerium Oxide Nanoparticles Angew. Chem., Int. Ed. 2009, 48, 2308-2312
62. Asati, A.; Santra, S.; Kaittanis, C.; Perez, J. M. Surface-Charge- Dependent Cell Localization and Cytotoxicity of Cerium Oxide Nanoparticles ACS Nano 2010, 4, 5321-5331
63. Santra, S.; Kaittanis, C.; Perez, J. M. Aliphatic Hyperbranched Polyester: A New Building Block in the Construction of Multifunctional Nanoparticles and Nanocomposites Langmuir 2010, 26, 5364-5373
64. Lattuada, L.; Lux, G. Synthesis of Gd-DTPA-Cholesterol: A New Lipophilic Gadolinium Complex as a Potential MRI Contrast Agent Tetrahedron Lett. 2003, 44, 3893-3895
65. Weinmann, H. J.; Brasch, R. C.; Press, W. R.; Wesbey, G. E. Characteristics of Gadolinium-DTPA Complex: A Potential NMR Contrast Agent Am. J. Roentgenol. 1984, 142, 619-624
66. McCarthy, J. R.; Perez, J. M.; Bruckner, C.; Weissleder, R. Polymeric Nanoparticle Preparation That Eradicates Tumors Nano Lett. 2005, 5, 2552-2556
67. Sun, E. Y.; Josephson, L.; Weissleder, R. Clickable Nanoparticles for Targeted Imaging Mol. Imaging 2006, 5, 122-128
68. Perez, J. M.; Asati, A.; Nath, S.; Kaittanis, C. Synthesis of Biocompatible Dextran-Coated Nanoceria with pH-Dependent Antioxidant Properties Small 2008, 4, 552-556