Redox-triggered self-assembly of gadolinium-based MRI probes for sensing reducing environment

Bioconjugate Chemistry

Volumn 25, Issue 8, 2014, Pages 1526-1536

  Ye, Deju ^a   Pandit, Prachi ^a   Kempen, Paul ^b   Lin, Jianguo ^b,c   Xiong, Liqin ^a   Sinclair, Robert ^b   Rutt, Brian ^a   Rao, Jianghong ^a  

^a STANFORD UNIVERSITY   (United States)

^b Stanford University   (United States)

^c JIANGSU INSTITUTE OF NUCLEAR MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GADOLINIUM COMPOUNDS; MOLECULES; NANOMAGNETICS; PROBES; SELF ASSEMBLY; SULFUR COMPOUNDS;

% REDUCTIONS; CONTROLLED SELF-ASSEMBLY; EFFECTIVE APPROACHES; GADOLINIA; GADOLINIUM COMPLEXES; IMAGING PROBE; MACROCYCLIZATION REACTIONS; REDUCING ENVIRONMENT; RELAXIVITY; SMALL MOLECULES;

MAGNETIC RESONANCE IMAGING;

CHELATE; CONTRAST MEDIUM; DISULFIDE; GADOLINIUM; GADOLINIUM NANOPARTICLE; MACROCYCLIC COMPOUND; METAL NANOPARTICLE; THIOL; UNCLASSIFIED DRUG; 1,4,7,10-TETRAAZACYCLODODECANE- 1,4,7,10-TETRAACETIC ACID; GLUTATHIONE; SINGLE HETEROCYCLIC RINGS;

ARTICLE; CYCLIZATION; DISULFIDE BOND; FEMALE; HELA CELL LINE; HUMAN; HUMAN CELL; HYDROPHOBICITY; NUCLEAR MAGNETIC RESONANCE IMAGING; RADIATION DETECTION; SENSITIVITY AND SPECIFICITY; CHEMISTRY; METABOLISM; OXIDATION REDUCTION REACTION; PROCEDURES;

GADOLINIUM; GLUTATHIONE; HELA CELLS; HETEROCYCLIC COMPOUNDS, 1-RING; HUMANS; MAGNETIC RESONANCE IMAGING; METAL NANOPARTICLES; OXIDATION-REDUCTION;

EID: 84906350982     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc500254g     Document Type: Article

References (60)

1. Terreno, E., Castelli, D. D., Viale, A., and Aime, S. (2010) Challenges for molecular magnetic resonance imaging Chem. Rev. 110, 3019-3042
2. Weissleder, R. and Pittet, M. J. (2008) Imaging in the era of molecular oncology Nature 452, 580-589
3. 2 magnetic resonance imaging contrast agents Ann. Biomed. Eng. 39, 1335-1348
4. Heffern, M. C., Matosziuk, L. M., and Mead, T. J. (2014) Lanthanide probes for bioresponsive imaging Chem. Rev. 114, 4496-4539
5. De Leon-Rodriguez, L. M., Lubag, A. J., Malloy, C. R., Martinez, G. V., Gillies, R. J., and Sherry, A. D. (2009) Responsive MRI agents for sensing metabolism in vivo Acc. Chem. Res. 42, 948-957
6. Caravan, P. (2009) Protein-targeted gadolinium-based magnetic resonance imaging (MRI) contrast agents: design and mechanism of action Acc. Chem. Res. 42, 851-862
7. Ye, F., Wu, X., Jeong, E. K., Jia, Z., Yang, T., Parker, D., and Lu, Z.-R. (2008) A peptide targeted contrast agent specific to fibrin-fibronectin complexes for cancer molecular imaging with MRI Bioconjugate Chem. 19, 2300-2303
8. Zhang, Z., Kolodziej, A. F., Greenfield, M. T., and Caravan, P. (2011) Heteroditopic binding of magnetic resonance contrast agents for increased relaxivity Angew. Chem., Int. Ed. 50, 2621-2624
9. Que, E. L. and Chang, C. J. (2010) Responsive magnetic resonance imaging contrast agents as chemical sensors for metals in biology and medicine Chem. Soc. Rev. 39, 51-60
10. Louie, A. Y., Huber, M. M., Ahrens, E. T., Rothbacher, U., Moats, R., Jacobs, R. E., Fraser, S. E., and Meade, T. J. (2000) In vivo visualization of gene expression using magnetic resonance imaging Nat. Biotechnol. 18, 321-325
11. Arena, F., Singh, J. B., Gianolio, E., Stefania, R., and Aime, S. (2011) Beta-Gal gene expression MRI reporter in melanoma tumor cells. Design, synthesis, and in vitro and in vivo testing of a Gd(III) containing probe forming a high relaxivity, melanin-like structure upon beta-Gal enzymatic activation Bioconjugate Chem. 22, 2625-2635
12. Bogdanov, A., Matuszewski, L., Bremer, C., Petrovsky, A., and Weissleder, R. (2002) Oligomerization of paramagnetic substrates result in signal amplification and can be used for MR imaging of molecular targets Mol. Imaging 1, 16-23
13. Lowe, M. P., Parker, D., Reany, O., Aime, S., Botta, M., Castellano, G., Gianolio, E., and Pagliarin, R. (2001) pH-Dependent modulation of relaxivity and luminescence in macrocyclic gadolinium and europium complexes based on reversible intramolecular sulfonamide ligation J. Am. Chem. Soc. 123, 7601-7609
14. Ronald, J. A., Chen, J. W., Chen, Y., Hamilton, A. M., Rodriguez, E., Reynolds, F., Hegele, R. A., Rogers, K. A., Querol, M., Bogdanov, A., Weissleder, R., and Rutt, B. K. (2009) Enzyme-sensitive magnetic resonance imaging targeting myeloperoxidase identifies active inflammation in experimental rabbit atherosclerotic plaques Circulation 120, 592-599
15. Shen, C. and New, E. J. (2013) Promising strategies for Gd-based responsive magnetic resonance imaging contrast agents Curr. Opin. Chem. Biol. 17, 158-166
16. Davies, G.-L., Kramberger, I., and Davis, J. J. (2013) Environmentally responsive MRI contrast agents Chem. Commun. 49, 9704-9721
17. Tsitovich, P. B., Burns, P. J., McKay, A. M., and Morrow, J. R. (2014) Redox-activated MRI contrast agents based on lanthanide and transition metal ions J. Inorg. Biochem. 133, 143-154
18. Loving, G. S., Mukherjee, S., and Caravan, P. (2013) Redox-activated manganese-based MR contrast agent J. Am. Chem. Soc. 135, 4620-4623
19. Que, E. L., New, E. J., and Chang, C. J. (2012) A cell-permeable gadolinium contrast agent for magnetic resonance imaging of copper in a Menkes disease model Chem. Sci. 3, 1829-1834
20. Endres, P. J., MacRenaris, K. W., Vogt, S., and Meade, T. J. (2008) Cell-permeable MR contrast agents with increased intracellular retention Bioconjugate Chem. 19, 2049-2059
21. Do, Q. N., Ratnakar, J. S., Kovács, Z., and Sherry, A. D. (2014) Redox- and hypoxia-responsive MRI contrast agents ChemMedChem 9, 1116-1129
22. Sarsour, E. H., Kumar, M. G., Chaudhuri, L., Kalen, A. L., and Goswami, P. C. (2009) Redox control of the cell cycle in health and disease Antioxid. Redox Signaling 11, 2985-3011
23. Yuan, Y., Zhang, J., Wang, M., Mei, B., Guan, Y., and Liang, G. (2013) Detection of glutathione in vitro and in cells by the controlled self-assembly of nanorings Anal. Chem. 85, 1280-1284
24. Lim, S. Y., Hong, K. H., Kim, D. I., Kwon, H., and Kim, H. J. (2014) Tunable heptamethine-azo dye conjugate as an NIR fluorescent probe for the selective detection of mitochondrial glutathione over cysteine and homocysteine J. Am. Chem. Soc. 136, 7018-7025
25. Song, Y., Suntharalingam, K., Yeung, J. S., Royzen, M., and Lippard, S. J. (2013) Synthesis and characterization of Pt(IV) fluorescein conjugates to investigate Pt(IV) intracellular transformations Bioconjugate Chem. 24, 1733-1740
26. Liu, J., Bao, C., Zhong, X., Zhao, C., and Zhu, L. (2010) Highly selective detection of glutathione using a quantum-dot-based OFF-ON fluorescent probe Chem. Commun. 46, 2971-2973
27. Tang, Y., Song, H., Su, Y., and Lv, Y. (2013) Turn-on persistent luminescence probe based on graphitic carbon nitride for imaging detection of biothiols in biological fluids Anal. Chem. 85, 11876-11884
28. Martinelli, J., Fekete, M., Tei, L., and Botta, M. (2011) Cleavable beta-cyclodextrin nanocapsules incorporating Gd(III)-chelates as bioresponsive MRI probes Chem. Commun. 47, 3144-3146
29. Carrera, C., Digilio, G., Baroni, S., Burgio, D., Consol, S., Fedeli, F., Longo, D., Mortillaro, A., and Aime, S. (2007) Synthesis and characterization of a Gd(III) based contrast agent responsive to thiol containing compounds Dalton Trans. 4980-4987
30. Menchise, V., Digilio, G., Fianolio, E., Cittadino, E., Catanzaro, V., Carrera, C., and Aime, S. (2011) In vivo labeling of B16 melanoma tumor xenograft with a thiol-reactive gadolinium based MRI contrast agent Mol. Pharmaceutics 8, 1750-1756
31. Raghunand, N., Guntle, G. P., Gokhale, V., Nichol, G. S., Mash, E. A., and Jagadish, B. (2009) Design, synthesis, and evaluation of 1,4,7,10-tetraazacyclododecane-1,4,7-triacetic acid derived, redox-sensitive contrast agents for magnetic resonance imaging J. Med. Chem. 53, 6747-6757
32. Lu, Z.-R., Mohs, A. M., Zong, Y., and Feng, Y. (2006) Polydisulfide Gd(III) chelates as biodegradable macromolecular magnetic resonance imaging contrast agents Int. J. Nanomed. 1, 31-40
33. Ye, Z., Wu, X.-M., Tan, M.-Q., Jesberger, J., Griswold, M., and Lu, Z.-R. (2013) Synthesis and evaluation of a polydisulfide with Gd-DOTA monoamide side chains as a biodegradable macromolecular contrast agent for MR blood pool imaging Contrast Media Mol. Imaging 8, 220-228
34. Zhou, Z.-X. and Lu, Z.-R. (2013) Gadolinium-based contrast agents for MR cancer imaging Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 5, 1-18
35. Liang, G., Ronald, J., Chen, Y., Ye, D., Pandit, P., Ma, M. L., Rutt, B., and Rao, J. (2011) Controlled self-assembling of gadolinium nanoparticles as smart molecular magnetic resonance imaging contrast agents Angew. Chem., Int. Ed. 50, 6283-6286
36. Liang, G., Ren, H., and Rao, J. (2010) A biocompatible condensation reaction for controlled assembly of nanostructures in living cells Nat. Chem. 2, 54-60
37. New, K., Bryant, L. H., and Brechbiel, M. W. (2010) Poly(amidoamine) dendrimer based MRI contrast agents exhibiting enhanced relaxivities derived via metal preligation techniques Bioconjugate Chem. 21, 1014-1017
38. Song, Y., Zong, H., Trivedi, E. R., Vesper, B. J., Waters, E. A., Barrett, A. G. M., Radosevich, J. A., Hoffman, B. M., and Meade, T. J. (2010) Synthesis and characterization of new prophyrazine-Gd(III) conjugates as multimodal MR contrast agents Bioconjugate Chem. 21, 2267-2275
39. Accardo, A., Tesauro, D., Aloj, L., Pedone, C., and Morelli, G. (2009) Supramolecular aggregates containing lipophilic Gd(III) complexes as contrast agents in MRI Coord. Chem. Rev. 253, 1293-2213
40. Ye, D., Liang, G., Ma, M. L., and Rao, J. (2011) Controlling intracellular macrocyclization for the imaging of protease activity Angew. Chem., Int. Ed. 50, 2275-2279
41. Ye, D., Shuhendler, A. J., Cui, L., Tong, L., Tee, S. S., Tikhomirov, G., Felsher, D. W., and Rao, J. (2014) Bioorthogonal cyclization-mediated in situ self-assembly of small-molecule probes for imaging caspase activity in vivo Nat. Chem. 6, 519-526
42. Shen, B., Jeon, J., Palner, M., Ye, D., Shuhendler, A., Chin, F. T., and Rao, J. (2013) Positron emission tomography imaging of drug-induced tumor apoptosis with a caspase-triggered nanoaggregation probe Angew. Chem., Int. Ed. 52, 10511-10514
43. Ye, D., Shuhendler, A. J., Pandit, P., Brewer, K. D., Tee, S. S., Cui, L., Tikhomirov, G., Rutt, B., and Rao, J. (2014) Caspase-responsive smart gadolinium-based contrast agent for magnetic resonance imaging of drug-induced apoptosis Chem. Sci. 10.1039/c4sc01392a
44. Bloembergen, N. and Morgan, L. O. (1961) Proton relaxation times in paramagnetic solutions. Effects of electron spin relaxation J. Chem. Phys. 34, 842-850
45. Driggers, E. M., Hale, S. P., Lee, J., and Terrett, N. K. (2008) The exploration of macrocycles for drug discovery―an underexploited structural class Nat. Rev. Drug. Discovery 7, 608-624
46. Feng, W., Yamato, K., Yang, L., Ferguson, J. S., Zhong, L., Zou, S., Yuan, L., Zeng, X. C., and Gong, B. (2009) Efficient kinetic macrocyclization J. Am. Chem. Soc. 131, 2629-2637
47. Marsault, E. and Peterson, M. L. (2011) Macrocycles are great cycles: application, opportunities, and challenges of synthetic macrocycles in drug discovery J. Med. Chem. 54, 1961-2004
48. Seo, S. H., Jones, T. V., Seyler, H., Peters, J. O., Kim, T. H., Chang, J. Y., and Tew, G. N. (2006) Liquid crystalline order from ortho-phenylene ethynylene macrocycles J. Am. Chem. Soc. 128, 9264-9265
49. Yang, W.-Y., Ahn, J.-H., Yoo, Y.-S., Oh, N.-E., and Lee, M. (2005) Supramolecular barrels from amphiphilic rigid-flexible macrocycles Nat. Mater. 4, 399-503
50. Mulder, W. J., Strijkers, G. J., van Tilborg, G. A., Griffioen, A. W., and Nicolay, K. (2006) Lipid-based nanoparticles for contrast-enhanced MRI and molecular imaging NMR Biomed. 19, 142-164
51. Kielar, F., Tei, L., Terreno, E., and Botta, M. (2010) Large relaxivity enhancement of paramagnetic lipid nanoparticles by restricting the local motions of the Gd(III) chelates J. Am. Chem. Soc. 132, 7836-7837
52. Mastarone, D. J., Harrison, V. S., Eckermann, A. L., Parigi, G., Luchinat, C., and Meade, T. J. (2011) A modular system for the synthesis of multiplexed magnetic resonance probes J. Am. Chem. Soc. 133, 5329-5337
53. Garimella, P. D., Datta, A., Romanini, D. W., Raymond, K. N., and Francis, M. B. (2011) Multivalent, high-relaxivity MRI contrast agents using rigid cysteine-reactive gadolinium complexes J. Am. Chem. Soc. 133, 14704-14709
54. Livramento, J. B., Toth, E., Sour, A., Borel, A., Merbach, A. E., and Ruloff, R. (2005) High relaxivity confined to a small molecular space: a metallostar-based, potential MRI contrast agent Angew. Chem., Int. Ed. 44, 1480-1484
55. Boden, C. D. J., Pattenden, G., and Ye, T. (1995) The synthesis of optically-active thiazoline and thiazole derived peptides from N-protected alpha-amino-acids Synlett 417-419
56. Niwa, K., Nakamura, M., and Ohmiya, Y. (2006) Stereoisomeric bio-inversion key to biosynthesis of firefly d -luciferin FEBS Lett. 580, 5283-5287
57. Caravan, P. (2006) Strategies for increasing the sensitivity of gadolinium based MRI contrast agents Chem. Soc. Rev. 35, 512-523
58. Wang, S.-Q., Wu, Q.-H., Wang, H.-Y., Zheng, X.-X., Shen, S.-L., Zhang, Y.-R., Miao, J.-Y., and Zhao, B.-X. (2014) Novel pyrazoline-based fluorescent probe for detecting glutathione and its application in cells Biosens. Bioelectron. 55, 386-390
59. Ortega, A. L., Mena, S., and Estrela, J. M. (2011) Glutathione in cancer cell death Cancer 3, 1285-1310
60. Cacciatore, I., Cornacchia, C., Pinnen, F., Mollica, A., and Di Stefano, A. (2010) Prodrug approach for increasing cellular glutathione levels Molecules 15, 1242-1264