Biochemical and in vivo characterization of a small, membrane-permeant, caspase-activatable far-red fluorescent peptide for imaging apoptosis

Biochemistry

Volumn 46, Issue 13, 2007, Pages 4055-4065

  Bullok, Kristin E ^a   Maxwell, Dustin ^a   Kesarwala, Aparna H ^a   Gammon, Seth ^a   Prior, Julie L ^a   Snow, Margaret ^b   Stanley, Sam ^b   Piwnica Worms, David ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CELL MEMBRANES; DISEASES; FLUORESCENCE; PEPTIDES; SYNTHESIS (CHEMICAL);

CASPASE ACTIVATABLE FAR RED FLUORESCENT PEPTIDES; DIVERSE DEVELOPMENTAL PATHWAYS; EFFECTOR CASPASES; HOMEOSTASIS;

CELL DEATH;

CASPASE; CASPASE 3; CERAMIDE; FLUORESCENT DYE; PEPTIDE;

AMEBIASIS; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DEATH; COLON ABSORPTION; CONTROLLED STUDY; ENZYME ACTIVATION; FLUORESCENCE; HELA CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; LEUKEMIA CELL LINE; MOUSE; NONHUMAN; PRIORITY JOURNAL; XENOGRAFT;

ANIMALIA;

EID: 34047219123     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061959n     Document Type: Article

References (39)

1. Grutter, M. (2000) Caspases: key players in programmed cell death, Curr. Opin. Struct. Biol. 10, 649-655.
2. Shi, Y. (2001) A structural view of mitochondria-mediated apoptosis, Nat. Struct. Biol. 8, 394-401.
3. Kroemer, G., and Martin, S. (2005) Caspase-independent cell death, Nat. Med. 11, 725-730.
4. Fischer, U., and Schulze-Osthoff, K. (2005) New approaches and therapeutics targeting apoptosis in disease, Pharmacol. Rev. 57, 187-215.
5. Ran, S., and Thorpe, P. E. (2002) Phosphatidylserine is a marker of tumor vasculature and a potential target for cancer imaging and therapy, Int. J. Radiat. Oncol. Biol. Phys. 54, 1479-1484.
6. Van De Wiele, C., Lahorte, C., Vermeersch, H., Loose, D., Mervillie, K., Steinmetz, N., Vanderheyden, J., Cuvelier, C.. Slegers, G., and Dierck, R. (2003) Quantitative tumor apoptosis imaging using technetium-99m HYNIC annexin V single photon emission computed tomography, J. Clin. Oncol. 21, 3483-3487.
7. Petrovsky, A., Schellenberger, E., Josephson, L., Weissleder, R., and Bogdanov, A. J. (2003) Near-infrared fluorescent imaging of tumor apoptosis, Cancer Res. 63, 1936-1942.
8. Schellenberger, E., Bogdanov, A. J., Petrovsky, A., Ntziachristos, V., Weissleder, R., and Josephson, L. (2003) Optical imaging of apoptosis as a biomarker of tumor response to chemotherapy, Neoplasia 5, 187-192.
9. Hamstra, D., Chenevert, T., Moffat, B., Johnson, T., Meyer, C., Mukherji, S., Quint, D., Gebarski, S., Fan, X., Tsien, C., Lawrence, T., Junck, L., Rehemtulla, A., and Ross, B. (2005) Evaluation of the functional diffusion map as an early biomarker of time-to-progression and overall survival in high-grade glioma, Proc. Natl. Acad. Sci. U.S.A. 102, 16759-16764.
10. Jain, R. (2005) Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy, Science 307, 58-62.
11. Jung, H., Kettunen, M., Davletov, B., and Brindle, K. (2004) Detection of apoptosis using the C2A domain of synaptotagmin I, Bioconjugate Chem. 15, 983-987.
12. Riedl, S., and Shi, Y. (2004) Molecular mechanisms of caspase regulation during apoptosis, Nat. Rev. Mol Cell Biol. 5, 897-906.
13. Thornberry, N. A. (1997) A combinatorial approach defines specificities of members of the caspase family and granzyme B, J. Biol. Chem. 272, 17907-17912.
14. Lien, S., Pastor, R., Sutherlin, R., and Lowman, H. (2004) A substrate-phage approach for investigating caspase specificity, Protein J. 23, 413-425.
15. Smolewski, P., Bedner, E., Du, L., Hsieh, T. C., Wu, J. M., Phelps, D. J., and Darzynkiewicz, Z. (2001) Detection of caspases activation by fluorochrome-labeled inhibitors: Multiparameter analysis by laser scanning cytometry, Cytometry 44, 73-82.
16. Komoriya, A., Packard, B. Z., Brown, M. J., Wu, M. L., and Henkart, P. A. (2000) Assessment of caspase activities in intact apoptotic thymocytes using cell-permeable fluorogenic caspase substrates, J. Exp. Med. 191, 1819-28.
17. Zhang, K-Z., Kasibhatla, S., Guastella, J., Tseng, B., Drewe, J., and Cai, S. X. (2003) N-Ac-DEVD-N′-(Polyfluorobenzoyl)-R110: Novel cell-permeable fluorogenic caspase substrates for the detection of caspase activity and apoptosis, Bioconjugate Chem. 14, 458-463.
18. 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, 5404-5407.
19. Akiyama, S. I., Fojo, A., Hanover, J. A., Pastan, I., and Gottesman, M. M. (1985) Isolation and genetic characterization of human KB cell lines resistant to multiple drugs, Somatic Cell Mol. Genet. 11, 117-126.
20. Piwnica-Worms, D., Chiu, M., Budding, M., Kronauge, J., Kramer, R., and Croop, J. (1993) Functional imaging of multidrug-resistant P-glycoprotein with an organotechnetium complex, Cancer Res. 53, 977-984.
21. Polyakov, V., Sharma, V., Dahlheimer, J., Pica, C., Luker, G., and Piwnica-Worms, D. (2000) Novel Tat-peptide chelates for direct transduction of technetium-99m and rhenium into human cells for imaging and radiotherapy, Bioconjugate Chem. 11, 762-771.
22. Luker, G. D., Flagg, T. P., Sha, Q., Luker, K. E., Pica, C. M., Nichols, C. G., and Piwnica-Worms, D. (2001) MDR1 P-glycoprotein reduces influx of substrates without affecting membrane potential, J. Biol. Chem. 276, 49053-49060.
23. Burlingham, B. T., and Widlanski, T. S. (2003) An intuitive look at the relationship of Ki and IC50: a more general use for the Dixon Plot, J. Chem. Educ. 80, 214-218.
24. Mathews, C., van Holde, K., and Ahern, K. (2000) Biochemistry, 3rd ed., Benjamin Cummings, San Francisco.
25. Zhang, Z., Wang, L., Seydel, K., Li, E., Ankri, S., Mirelman, D., and Stanley, S. (2000) Entamoeba histolytica cysteine proteinases with interleukin-1 beta converting enzyme (ICE) activity cause intestinal inflammation and tissue damage in amoebiasis, Mol. Microbiol. 37, 542-548.
26. Stanley, S. J., Becker, A., Kunz-Jenkins, C., Foster, L., and Li, E. (1990) Cloning and expression of a membrane antigen of Entamoeba histolytica possessing multiple tandem repeats, Proc. Natl. Acad. Sci. U.S.A. 87, 4976-4980.
27. Glantz, S. A. (1987) Primer of Biostatistics, 2nd ed., p 379, McGraw-Hill, Inc., New York.
28. Salgado, J., Garcia-saez, A., Malet, G., Mingarro, I., and Perez-Paya, E. (2002) Peptide in apoptosis research, J. Pept. Sci. 8, 543-560.
29. Ekert, P., Silke, J., and Vaux, D. (1999) Caspase inhibitors, Cell Death Differ. 6, 1081-1086.
30. Talanian, R. V., Quinlan, C., Trautz, S., Hackett, M. C., Mankovich, J. A., Banach, D., Ghayur, T., Brady, K. D., and Wong, W. W. (1997) Substrate specificities of caspase family proteases, J. Biol. Chem. 272, 9677-9682.
31. Dimanche-Boitrel, M., Meurette, O., Rebillard, A., and Lacour, S. (2005) Role of early plasma membrane events in chemotherapy-induced cell death, Drug Resist. Updates 8, 5 -14.
32. Herr, L., Wilhelm, D., Bohler, T., Angel, P., and Debatin, K.-M. (1997) Activation of CD95 (APO-I/Fas) signaling by ceiamide mediates cancer therapy-induced apoptosis, EMBO J. 16, 6200-6208.
33. Lin, C., Chen, C., Chang, W., Jan, M., Hsu, L., Wu, R., Tang, M., Chang, W., and Lin, Y. (2004) Sequential caspase-2 and caspase-8 activation upstream of mitochondria during ceramide and etoposide-induced apoptosis, J. Biol. Chem. 279, 40755-40761.
34. Huston, C., Boettner, D., Miller-Sims, V., and Petri, W. J. (2003) Apoptotic killing and phagocytosis of host cells by the parasite Entamoeba histolytica, Infect. Immun. 71, 964-972.
35. Kasha, M. (1963) Energy transfer mechanism and molecular exciton model for molecular aggregates, Radiat. Res. 20, 55-71.
36. Hernando, J., van der Schaaf, M., van Dijk, E., Sauer, M., Garcia-Parajo, M., and van Hulst, N. (2003) Excitonic behavior of rhodamine dimers: a single-molecule study, J. Phys. Chem. A 107, 43-52.
37. Bernacchi, S., and Mély, Y. (2001) Exciton interaction in molecular beacons: a sensitive sensor for short range modifications of the nucleic acid structure, Nucleic Acids Res. 29, e62.
38. Johansson, M., Fidder, H., Dick, D., and Cook, R. (2002) Intramolecular dimers: a new strategy to fluorescence quenching in dual-labeled oligonucleotide probes, J. Am. Chem. Soc. 124, 6950-6956.
39. Packard, B., Toptygin, D., Komoriya, A., and Brand, L. (1997) Design of profluorescent protease substrates guided by exciton theory, Methods Enzymol. 278, 15-23.