Activatable near-infrared fluorescent probe for in vivo imaging of fibroblast activation protein-alpha

Bioconjugate Chemistry

Volumn 23, Issue 8, 2012, Pages 1704-1711

  Li, Jinbo ^a,b   Chen, Kai ^a   Liu, Hongguang ^a   Cheng, Kai ^a   Yang, Meng ^a   Zhang, Jiping ^c   Cheng, Jonathan D ^c   Zhang, Yan ^b   Cheng, Zhen ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NANJING UNIVERSITY   (China)

^c FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL MEMBRANES; CHEMICAL ACTIVATION; ENERGY TRANSFER; FIBROBLASTS; FLUORESCENCE IMAGING; FORSTER RESONANCE ENERGY TRANSFER; INFRARED DEVICES; PEPTIDES; PROBES;

CELL SURFACES; FLUORESCENT PROBES; IN-VIVO; IN-VIVO IMAGING; MALIGNANT TUMORS; NEAR-INFRARED FLUORESCENT; PEPTIDE SEQUENCES; SURFACE GLYCOPROTEINS; TUMOR UPTAKE; VIVO OPTICAL IMAGING;

TUMORS;

FLUORESCENT DYE; SEPRASE;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION; SYNTHESIS;

EID: 84865152111     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc300278r     Document Type: Article

References (35)

1. Rettig, W. J., Garin-Chesa, P., Beresford, H. R., Oettgen, H. F., Melamed, M. R., and Old, L. J. (1988) Cell-surface glycoproteins of human sarcomas: differential expression in normal and malignant tissues and cultured cells Proc. Natl. Acad. Sci. U. S. A. 85, 3110-4
2. Scanlan, M. J., Raj, B. K., Calvo, B., Garin-Chesa, P., Sanz-Moncasi, M. P., Healey, J. H., Old, L. J., and Rettig, W. J. (1994) Molecular cloning of fibroblast activation protein alpha, a member of the serine protease family selectively expressed in stromal fibroblasts of epithelial cancers Proc. Natl. Acad. Sci. U. S. A. 91, 5657-61 (Pubitemid 24174387)
3. Garin-Chesa, P., Old, L. J., and Rettig, W. J. (1990) Cell surface glycoprotein of reactive stromal fibroblasts as a potential antibody target in human epithelial cancers Proc. Natl. Acad. Sci. U. S. A. 87, 7235-9
4. Kalluri, R. and Zeisberg, M. (2006) Fibroblasts in cancer Nat. Rev. Cancer 6, 392-401
5. Cheng, J. D., Dunbrack, R. L., Jr., Valianou, M., Rogatko, A., Alpaugh, R. K., and Weiner, L. M. (2002) Promotion of tumor growth by murine fibroblast activation protein, a serine protease, in an animal model Cancer Res. 62, 4767-72
6. Huang, Y., Simms, A. E., Mazur, A., Wang, S., Leon, N. R., Jones, B., Aziz, N., and Kelly, T. (2011) Fibroblast activation protein-alpha promotes tumor growth and invasion of breast cancer cells through non-enzymatic functions Clin. Exp. Metastasis 28, 567-79
7. Lee, H. O., Mullins, S. R., Franco-Barraza, J., Valianou, M., Cukierman, E., and Cheng, J. D. (2011) FAP-overexpressing fibroblasts produce an extracellular matrix that enhances invasive velocity and directionality of pancreatic cancer cells BMC Cancer 11, 245
8. Kraman, M., Bambrough, P. J., Arnold, J. N., Roberts, E. W., Magiera, L., Jones, J. O., Gopinathan, A., Tuveson, D. A., and Fearon, D. T. (2010) Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-alpha Science 330, 827-30
9. Lo, P. C., Chen, J., Stefflova, K., Warren, M. S., Navab, R., Bandarchi, B., Mullins, S., Tsao, M., Cheng, J. D., and Zheng, G. (2009) Photodynamic molecular beacon triggered by fibroblast activation protein on cancer-associated fibroblasts for diagnosis and treatment of epithelial cancers J. Med. Chem. 52, 358-68
10. Narra, K., Mullins, S. R., Lee, H. O., Strzemkowski-Brun, B., Magalong, K., Christiansen, V. J., McKee, P. A., Egleston, B., Cohen, S. J., Weiner, L. M., Meropol, N. J., and Cheng, J. D. (2007) Phase II trial of single agent Val-boroPro (Talabostat) inhibiting Fibroblast Activation Protein in patients with metastatic colorectal cancer Cancer Biol. Ther. 6, 1691-9 (Pubitemid 351590302)
11. Petrovsky, A., Schellenberger, E., Josephson, L., Weissleder, R., and Bogdanov, A., Jr. (2003) Near-infrared fluorescent imaging of tumor apoptosis Cancer Res. 63, 1936-42 (Pubitemid 36460861)
12. Cheng, Z., Levi, J., Xiong, Z., Gheysens, O., Keren, S., Chen, X., and Gambhir, S. S. (2006) Near-infrared fluorescent deoxyglucose analogue for tumor optical imaging in cell culture and living mice Bioconjugate Chem. 17, 662-9 (Pubitemid 43794375)
13. Miao, Z., Ren, G., Liu, H., Jiang, L., and Cheng, Z. (2010) Cy5.5-labeled Affibody molecule for near-infrared fluorescent optical imaging of epidermal growth factor receptor positive tumors J. Biomed. Opt. 15, 036007
14. Weissleder, R., Tung, C. H., Mahmood, U., and Bogdanov, A., Jr. (1999) In vivo imaging of tumors with protease-activated near-infrared fluorescent probes Nat. Biotechnol. 17, 375-8 (Pubitemid 29166041)
15. Pham, W., Choi, Y., Weissleder, R., and Tung, C. H. (2004) Developing a peptide-based near-infrared molecular probe for protease sensing Bioconjugate Chem. 15, 1403-7 (Pubitemid 39552031)
16. Chen, J., Tung, C. H., Allport, J. R., Chen, S., Weissleder, R., and Huang, P. L. (2005) Near-infrared fluorescent imaging of matrix metalloproteinase activity after myocardial infarction Circulation 111, 1800-5 (Pubitemid 40525145)
17. Yoon, S. M., Myung, S. J., Ye, B. D., Kim, I. W., Lee, N. G., Ryu, Y. M., Park, K., Kim, K., Kwon, I. C., Park, Y. S., Park, C. S., Moon, D. H., Kim do, H., Do, M. Y., Byeon, J. S., Yang, S. K., and Kim, J. H. (2010) Near-infrared fluorescence imaging using a protease-specific probe for the detection of colon tumors Gut Liver 4, 488-97
18. Zhu, L., Xie, J., Swierczewska, M., Zhang, F., Quan, Q., Ma, Y., Fang, X., Kim, K., Lee, S., and Chen, X. (2011) Real-time video imaging of protease expression in vivo Theranostics 1, 18-27
19. Zhu, L., Zhang, F., Ma, Y., Liu, G., Kim, K., Fang, X., Lee, S., and Chen, X. (2011) In vivo optical imaging of membrane-type matrix metalloproteinase (MT-MMP) activity Mol. Pharm. 8, 2331-8
20. Jaffer, F. A., Kim, D. E., Quinti, L., Tung, C. H., Aikawa, E., Pande, A. N., Kohler, R. H., Shi, G. P., Libby, P., and Weissleder, R. (2007) Optical visualization of cathepsin K activity in atherosclerosis with a novel, protease-activatable fluorescence sensor Circulation 115, 2292-8 (Pubitemid 46685897)
21. Kim, D. E., Kim, J. Y., Schellingerhout, D., Shon, S. M., Jeong, S. W., Kim, E. J., and Kim, W. K. (2009) Molecular imaging of cathepsin B proteolytic enzyme activity reflects the inflammatory component of atherosclerotic pathology and can quantitatively demonstrate the antiatherosclerotic therapeutic effects of atorvastatin and glucosamine Mol. Imaging 8, 291-301
22. Abd-Elgaliel, W. R., Cruz-Monserrate, Z., Logsdon, C. D., and Tung, C. H. (2011) Molecular imaging of Cathepsin E-positive tumors in mice using a novel protease-activatable fluorescent probe Mol. Biosyst. 7, 3207-13
23. Bullok, K. and Piwnica-Worms, D. (2005) Synthesis and characterization of a small, membrane-permeant, caspase-activatable far-red fluorescent peptide for imaging apoptosis J. Med. Chem. 48, 5404-7 (Pubitemid 41209236)
24. Barnett, E. M., Zhang, X., Maxwell, D., Chang, Q., and Piwnica-Worms, D. (2009) Single-cell imaging of retinal ganglion cell apoptosis with a cell-penetrating, activatable peptide probe in an in vivo glaucoma model Proc. Natl. Acad. Sci. U. S. A. 106, 9391-6
25. Park, J. E., Lenter, M. C., Zimmermann, R. N., Garin-Chesa, P., Old, L. J., and Rettig, W. J. (1999) Fibroblast activation protein, a dual specificity serine protease expressed in reactive human tumor stromal fibroblasts J. Biol. Chem. 274, 36505-12
26. Edosada, C. Y., Quan, C., Wiesmann, C., Tran, T., Sutherlin, D., Reynolds, M., Elliott, J. M., Raab, H., Fairbrother, W., and Wolf, B. B. (2006) Selective inhibition of fibroblast activation protein protease based on dipeptide substrate specificity J. Biol. Chem. 281, 7437-44 (Pubitemid 43847515)
27. Aertgeerts, K., Levin, I., Shi, L., Snell, G. P., Jennings, A., Prasad, G. S., Zhang, Y., Kraus, M. L., Salakian, S., Sridhar, V., Wijnands, R., and Tennant, M. G. (2005) Structural and kinetic analysis of the substrate specificity of human fibroblast activation protein alpha J. Biol. Chem. 280, 19441-4 (Pubitemid 41379462)
28. Edosada, C. Y., Quan, C., Tran, T., Pham, V., Wiesmann, C., Fairbrother, W., and Wolf, B. B. (2006) Peptide substrate profiling defines fibroblast activation protein as an endopeptidase of strict Gly(2)-Pro(1)-cleaving specificity FEBS Lett. 580, 1581-6 (Pubitemid 43290354)
29. Lai, K. S., Ho, N. H., Cheng, J. D., and Tung, C. H. (2007) Selective fluorescence probes for dipeptidyl peptidase activity-fibroblast activation protein and dipeptidyl peptidase IV Bioconjugate Chem. 18, 1246-50 (Pubitemid 47122647)
30. Kong, Y., Yao, H., Ren, H., Subbian, S., Cirillo, S. L., Sacchettini, J. C., Rao, J., and Cirillo, J. D. (2010) Imaging tuberculosis with endogenous beta-lactamase reporter enzyme fluorescence in live mice Proc. Natl. Acad. Sci. U. S. A. 107, 12239-44
31. Balaziova, E., Busek, P., Stremenova, J., Sromova, L., Krepela, E., Lizcova, L., and Sedo, A. (2011) Coupled expression of dipeptidyl peptidase-IV and fibroblast activation protein-alpha in transformed astrocytic cells Mol. Cell. Biochem. 354, 283-9
32. Collins, P. J., McMahon, G., OBrien, P., and OConnor, B. (2004) Purification, identification and characterisation of seprase from bovine serum Int. J. Biochem. Cell Biol. 36, 2320-33 (Pubitemid 39094452)
33. Cha, E. J., Jang, E. S., Sun, I. C., Lee, I. J., Ko, J. H., Kim, Y. I., Kwon, I. C., Kim, K., and Ahn, C. H. (2011) Development of MRI/NIRF activatable multimodal imaging probe based on iron oxide nanoparticles J. Controlled Release 155, 152-8
34. Park, J., Yang, J., Lim, E. K., Kim, E., Choi, J., Ryu, J. K., Kim, N. H., Suh, J. S., Yook, J. I., Huh, Y. M., and Haam, S. (2012) Anchored proteinase-targetable optomagnetic nanoprobes for molecular imaging of invasive cancer cells Angew. Chem., Int. Ed. Engl. 51, 945-8
35. Levi, J., Kothapalli, S. R., Ma, T. J., Hartman, K., Khuri-Yakub, B. T., and Gambhir, S. S. (2010) Design, synthesis, and imaging of an activatable photoacoustic probe J. Am. Chem. Soc. 132, 11264-9