Bioorthogonal cyclization-mediated in situ self-assembly of small-molecule probes for imaging caspase activity in vivo

Nature Chemistry

Volumn 6, Issue 6, 2014, Pages 519-526

  Ye, Deju ^a   Shuhendler, Adam J ^a   Cui, Lina ^a   Tong, Ling ^b   Tee, Sui Seng ^a   Tikhomirov, Grigory ^a   Felsher, Dean W ^b   Rao, Jianghong ^a  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; DIAGNOSTIC AGENT; DOXYCYCLINE; FLUORESCENT DYE; NANOPARTICLE;

ANIMAL; APOPTOSIS; ARTICLE; CYCLIZATION; DRUG EFFECT; DRUG SCREENING; EXPERIMENTAL NEOPLASM; FLUORESCENCE MICROSCOPY; HELA CELL LINE; HUMAN; IMAGE PROCESSING; METABOLISM; MOUSE; PATHOLOGY;

ANIMALS; APOPTOSIS; CASPASES; CYCLIZATION; DOXYCYCLINE; FLUORESCENT DYES; HELA CELLS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MICE; MICROSCOPY, FLUORESCENCE; NANOPARTICLES; NEOPLASMS, EXPERIMENTAL; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84901351258     PISSN: 17554330     EISSN: 17554349     Source Type: Journal    
DOI: 10.1038/nchem.1920     Document Type: Article

References (49)

1. Whitesides, G. M., Mathias, J. P. & Seto, C. T. Molecular self-Assembly and nanochemistry: A chemical strategy for the synthesis of nanostructures. Science 254, 1312-1319 (1991).
2. Capito, R. M., Azevedo, H. S., Velichko, Y. S., Mata, A. & Stupp, S. I. Selfassembly of large and small molecules into hierarchically ordered sacs and membranes. Science 319, 1812-1816 (2008).
3. O'Leary, L. E., Fallas, J. A., Bakota, E. L., Kang, M. K. & Hartgerink, J. D. Multi-hierarchical self-Assembly of a collagen mimetic peptide from triple helix to nanofibre and hydrogel. Nature Chem. 3, 821-828 (2011).
4. Gazit, E. Bioinspired chemistry: Diversity for self-Assembly. Nature Chem. 2, 1010-1011 (2010).
5. Yang, Z., Liang, G. & Xu, B. Enzymatic hydrogelation of small molecules. Acc. Chem. Res. 41, 315-326 (2008).
6. Liang, G., Ren, H. & Rao, J. A biocompatible condensation reaction for controlled assembly of nanostructures in living cells. Nature Chem. 2, 54-60 (2010).
7. Gao, Y., Shi, J., Yuan, D. & Xu, B. Imaging enzyme-Triggered self-Assembly of small molecules inside live cells. Nature Commun. 3, 1033 (2012).
8. Adler-Abramovich, L. et al. Phenylalanine assembly into toxic fibrils suggests amyloid etiology in phenylketonuria. Nature Chem. Biol. 8, 701-706 (2012).
9. Williams, R. J. et al. The in vivo performance of an enzyme-Assisted selfassembled peptide/protein hydrogel. Biomaterials 32, 5304-5310 (2011).
10. Ye, D., Liang, G., Ma, M. L. & Rao, J. Controlling intracellular macrocyclization for the imaging of protease activity. Angew. Chem. Int. Ed. 50, 2275-2279 (2011).
11. Vemula, P. K. et al. On-demand drug delivery from self-Assembled nanofibrous gels: A new approach for treatment of proteolytic disease. J. Biomed. Mater. Res. A 97, 103-110 (2011).
12. Saxon, E. & Bertozzi, C. R. Cell surface engineering by a modified Staudinger reaction. Science 287, 2007-2010 (2000).
13. Lin, F. L., Hoyt, H. M., van Halbeek, H., Bergman, R. G. & Bertozzi, C. R. Mechanistic investigation of the Staudinger ligation. J. Am. Chem. Soc. 127, 2686-2695 (2005).
14. Agard, N. J., Prescher, J. A. & Bertozzi, C. R. A strain-promoted [3+2] azide-Alkyne cycloaddition for covalent modification of biomolecules in living systems. J. Am. Chem. Soc. 126, 15046-15047 (2004).
15. Ning, X., Guo, J.,Wolfert, M. A. & Boons, G. J. Visualizing metabolically labeled glycoconjugates of living cells by copper-free and fast Huisgen cycloadditions. Angew. Chem. Int. Ed. 47, 2253-2255 (2008).
16. Devaraj, N. K., Upadhyay, R., Haun, J. B., Hilderbrand, S. A. & Weissleder, R. Fast and sensitive pretargeted labeling of cancer cells through a tetrazine/transcyclooctene cycloaddition. Angew. Chem. Int. Ed. 48, 7013-7016 (2009).
17. Blackman, M. L., Royzen, M. & Fox, J. M. Tetrazine ligation: Fast bioconjugation based on inverse-electron-demand Diels-Alder reactivity. J. Am. Chem. Soc. 130, 13518-13519 (2008).
18. Lang, K. et al. Genetically encoded norbornene directs site-specific cellular protein labelling via a rapid bioorthogonal reaction. Nature Chem. 4, 298-304 (2012).
19. Agarwal, P., van der Weijden, J., Sletten, E. M., Rabuka, D. & Bertozzi, C. R. A Pictet-Spengler ligation for protein chemical modification. Proc. Natl Acad. Sci. USA 110, 46-51 (2013).
20. Yusop, R. M., Unciti-Broceta, A., Johansson, E. M., Sanchez-Martin, R. M. & Bradley, M. Palladium-mediated intracellular chemistry. Nature Chem. 3, 239-243 (2011).
21. Chan, J., Dodani, S. C. & Chang, C. J. Reaction-based small-molecule fluorescent probes for chemoselective bioimaging. Nature Chem. 4, 973-984 (2012).
22. Prescher, J. A., Dube, D. H. & Bertozzi, C. R. Chemical remodelling of cell surfaces in living animals. Nature 430, 873-877 (2004).
23. Laughlin, S. T., Baskin, J. M., Amacher, S. L. & Bertozzi, C. R. In vivo imaging of membrane-Associated glycans in developing zebrafish. Science 320, 664-667 (2008).
24. Devaraj, N. K., Thurber, G. M., Keliher, E. J., Marinelli, B. & Weissleder, R. Reactive polymer enables efficient in vivo bioorthogonal chemistry. Proc. Natl Acad. Sci. USA 109, 4762-4767 (2012).
25. Sletten, E. M. & Bertozzi, C. R. From mechanism to mouse: A tale of two bioorthogonal reactions. Acc. Chem. Res. 44, 666-676 (2011).
26. Ren, H. et al. A biocompatible condensation reaction for the labeling of terminal cysteine residues on proteins. Angew. Chem. Int. Ed. 48, 9658-9662 (2009).
27. Van de Bittner, G. C., Bertozzi, C. R. & Chang, C. J. Strategy for dual-Analyte luciferin imaging: In vivo bioluminescence detection of hydrogen peroxide and caspase activity in a murine model of acute inflammation. J. Am. Chem. Soc. 135, 1783-1795 (2013).
28. Brindle, K. New approaches for imaging tumour responses to treatment. Nature Rev. Cancer 8, 94-107 (2008).
29. Blankenberg, F. G. In vivo detection of apoptosis. J. Nucl. Med. 49 (suppl. 2), 81S-95S (2008).
30. Nguyen, Q. D. et al. Positron emission tomography imaging of drug-induced tumor apoptosis with a caspase-3/7 specific 18F-labeled isatin sulfonamide. Proc. Natl Acad. Sci. USA 106, 16375-16380 (2009).
31. Johnson, J. R., Kocher, B., Barnett, E. M., Marasa, J. & Piwnica-Worms, D. Caspase-Activated cell-penetrating peptides reveal temporal coupling between endosomal release and apoptosis in an RGC-5 cell model. Bioconjugate Chem. 1783-1793 (2012).
32. Edgington, L. E. et al. Noninvasive optical imaging of apoptosis by caspasetargeted activity-based probes. Nature Med. 15, 967-973 (2009).
33. Thornberry, N. A. et al. A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J. Biol. Chem. 272, 17907-17911 (1997).
34. Pozarowski, P. et al. Interactions of fluorochrome-labeled caspase inhibitors with apoptotic cells: A caution in data interpretation. Cytometry A 55, 50-60 (2003).
35. Park, D. et al. Noninvasive imaging of cell death using an Hsp90 ligand. J. Am. Chem. Soc. 133, 2832-2835 (2011).
36. Pace, N. J., Pimental, D. R. & Weerapana, E. An inhibitor of glutathione S-Transferase Omega 1 that selectively targets apoptotic cells. Angew. Chem. Int. Ed. 51, 8365-8368 (2012).
37. Tetko, I. V. et al. Virtual computational chemistry laboratory-design and description. J. Comput. Aided Mol. Des. 19, 453-463 (2005).
38. Maxwell, D., Chang, Q., Zhang, X., Barnett, E. M. & Piwnica-Worms, D. An improved cell-penetrating, caspase-Activatable, near-infrared fluorescent peptide for apoptosis imaging. Bioconjugate Chem. 20, 702-709 (2009).
39. Edgington, L. E., Verdoes, M. & Bogyo, M. Functional imaging of proteases: Recent advances in the design and application of substrate-based and activitybased probes. Curr. Opin. Chem. Biol. 15, 798-805 (2011).
40. Stepczynska, A. et al. Staurosporine and conventional anticancer drugs induce overlapping, yet distinct pathways of apoptosis and caspase activation. Oncogene 20, 1193-1202 (2001).
41. Wang, S. et al. Doxorubicin induces apoptosis in normal and tumor cells via distinctly different mechanisms. Intermediacy of H2O2-And p53-dependent pathways. J. Biol. Chem. 279, 25535-25543 (2004).
42. Schermelleh, L. et al. Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 320, 1332-1336 (2008).
43. Westphal, V. et al. Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science 320, 246-249 (2008).
44. Wang, K. et al. In vivo imaging of tumor apoptosis using histone H1-Targeting peptide. J. Control. Release 148, 283-291 (2010).
45. Brigham, M. P., Stein, W. H. & Moore, S. The concentrations of cysteine and cystine in human blood plasma. J. Clin. Invest. 39, 1633-1638 (1960).
46. Salemi, G. et al. Blood levels of homocysteine, cysteine, glutathione, folic acid, and vitamin B12 in the acute phase of atherothrombotic stroke. Neurol. Sci. 30, 361-364 (2009).
47. 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. 3, 1024 (2013).
48. Wysocki, L. M. & Lavis, L. D. Advances in the chemistry of small molecule fluorescent probes. Curr. Opin. Chem. Biol. 15, 752-759 (2011).
49. Merian, J., Gravier, J., Navarro, F. & Texier, I. Fluorescent nanoprobes dedicated to in vivo imaging: From preclinical validations to clinical translation. Molecules 17, 5564-5591 (2012).