Abstract
Cysteine proteases, caspases, play an important role in the process of programmed cell death. In apoptosis, the cell signaling pathways overlap at executioner caspases regardless of the initial stimulus. Caspase-3 is the key one. This review considers the sensors for activity of caspase-3 and some other caspases. Over the past decade, many such sensors utilizing a variety of detection principles have been created; fluorescence and luminescence are the most common detection methods. The intracellular sensors are of particular interest; they allow visualization of the activation of caspases in living systems. Herein, we briefly describe sensors of various designs, the advantages and disadvantages of which must be taken into account when choosing a sensor for a particular experimental system.
Similar content being viewed by others
Abbreviations
- BRET:
-
bioluminescence resonance energy transfer
- FСS:
-
fluorescence correlation spectroscopy
- FLIM:
-
fluorescence lifetime imaging microscopy
- FRET:
-
Förster resonance energy transfer
- GFP:
-
green fluorescent protein
- TIRFM:
-
total internal reflection fluorescence microscopy
References
Alnemri, E.S., Livingston, D.J., Nicholson, D.W., Salvesen, G., Thornberry, N.A., Wong, W.W., and Yuan, J., Cell, 1996, vol. 87, p. 171.
Los, M., Van de Craen, M., Penning, L.C., Schenk, H., Westendorp, M., Baeuerle, P.A., Dröge, W., Krammer, P.H., Fiers, W., and Schulze-Osthoff, K., Nature, 1995, vol. 375, pp. 81–83.
Belema-Bedada, F., Uchida, S., Martire, A., Kostin, S., and Braun, T., Cell Stem Cell, 2008, vol. 2, pp. 566–575.
Janzen, V., Fleming, H.E., Riedt, T., Karlsson, G., Riese, M.J., Lo, CelsoC., Reynolds, G., Milne, C.D., Paige, C.J., Karlsson, S., Woo, M., and Scadden, D.T., Cell Stem Cell, 2008, vol. 2, pp. 584–594.
Shalini, S., Dorstyn, L., Dawar, S., and Kumar, S., Cell Death Differ., 2015, vol. 22, pp. 526–539.
Wu, C.C., Lee, S., Malladi, S., Chen, M.D., Mastrandrea, N.J., Zhang, Z., and Bratton, S.B., Nat. Commun., 2016, vol. 7, p. 13565.
Dorstyn, L., Akey, C.W., and Kumar, S., Cell Death Differ., 2018, vol. 25, pp. 1194–1208.
Li, J., Figueira, S.K., Vrazo, A.C.A., Binkowski, B.F., Butler, B.L., Tabata, Y., Filipovich, A., Jordan, M.B., and Risma, K.A., J. Immunol., 2014, vol. 193, pp. 519–528.
Juraver-Geslin, H.A. and Durand, B.C., Genesis, 2015, vol. 53, pp. 203–224.
Engels, I.H., Totzke, G., Fischer, U., Schulze-Osthoff, K., and Jänicke, R.U., Mol. Cell. Biol., 2005, vol. 25, pp. 2808–2818.
Zhao, Y., Lei, M., Wang, Z., Qiao, G., Yang, T., and Zhang, J., Biochem. Biophys. Res. Commun., 2014, vol. 450, pp. 526–531.
Slee, E.A., Adrain, C., and Martin, S.J., J. Biol. Chem., 2001, vol. 276, pp. 7320–7326.
Walsh, J.G., Cullen, S.P., Sheridan, C., Lüthi, A.U., Gerner, C., and Martin, S.J., Proc. Natl. Acad. Sci. U. S. A., 2008, vol. 105, pp. 12815–12819.
Martynova, E.A., Russ. J. Bioorg. Chem., 2003, vol. 29, no. 5, pp. 471–495.
Wall, D.M. and McCormick, B.A., Cell. Microbiol., 2014, vol. 16, pp. 1746–1756.
Chen, H., Yang, X., Feng, Z., Tang, R., Ren, F., Wei, K., and Chen, G., Int. J. Clin. Exp. Med., 2015, vol. 8, pp. 10225–10234.
Guliaeva, N.V., Zh. Vyssh. Nerv. Deiat. im. I.P. Pavlova, 2004, vol. 54, pp. 437–447.
Li, Z., Jo, J., Jia, J.-M., Lo, S.-C., Whitcomb, D.J., Jiao, S., Cho, K., and Sheng, M., Cell, 2010, vol. 141, pp. 859–871.
Huesmann, G.R. and Clayton, D.F., Neuron, 2006, vol. 52, pp. 1061–1072.
Dash, P.K., Blum, S., and Moore, A.N., Neuroreport, 2000, vol. 11, pp. 2811–2816.
Stepanichev, M.Y., Kudryashova, I.V., Yakovlev, A.A., Onufriev, M.V., Khaspekov, L.G., Lyzhin, A.A., Lazareva, N.A., and Gulyaeva, N.V., Neuroscience, 2005, vol. 136, pp. 579–591.
Zhao, X., Wang, D., Zhao, Z., Xiao, Y., Sengupta, S., Xiao, Y., Zhang, R., Lauber, K., Wesselborg, S., Feng, L., Rose, T.M., Shen, Y., Zhang, J., Prestwich, G., and Xu, Y., J. Biol. Chem., 2006, vol. 281, pp. 29357–29368.
Laplante, P., Sirois, I., Raymond, M.-A., Kokta, V., Beliveau, A., Prat, A., Pshezhetsky, A.V., and Hebert, M.-J., Cell Death Differ., 2010, vol. 17, pp. 291–303.
Bonner, C., Bacon, S., Concannon, C.G., Rizvi, S.R., Baquié, M., Farrelly, A.M., Kilbride, S.M., Dussmann, H., Ward, M.W., Boulanger, C.M., Wollheim, C.B., Graf, R., Byrne, M.M., and Prehn, J.H.M., Diabetes, 2010, vol. 59, pp. 2799–2808.
Huang, Q., Li, F., Liu, X., Li, W., Shi, W., Liu, F.-F., O’Sullivan, B., He, Z., Peng, Y., Tan, A.-C., Zhou, L., Shen, J., Han, G., Wang, X.-J., Thorburn, J., Thorburn, A., Jimeno, A., Raben, D., Bedford, J.S., and Li, C.-Y., Nat. Med., 2011, vol. 17, pp. 860–866.
McStay, G.P., Salvesen, G.S., and Green, D.R., Cell Death Differ., 2008, vol. 15, pp. 322–331.
Kosaihira, A. and Ona, T., Anal. Bioanal. Chem., 2008, vol. 391, pp. 1889–1897.
Park, K., Ahn, J., Yi, S.Y., Kim, M., and Chung, B.H., Biochem. Biophys. Res. Commun., 2008, vol. 368, pp. 684–689.
Chen, H., Mei, Q., Hou, Y., Zhu, X., Koh, K., Li, X., and Li, G., Analyst, 2013, vol. 138, pp. 5757–5761.
Zhou, S., Zheng, T., Chen, Y., Zhang, J., Li, L., Lu, F., and Zhu, J.-J., Biosens. Bioelectron., 2014, vol. 61, pp. 648–654.
Kumaraswamy, S., Bergstedt, T., Shi, X., Rininsland, F., Kushon, S., Xia, W., Ley, K., Achyuthan, K., McBranch, D., and Whitten, D., Proc. Natl. Acad. Sci. U. S. A., 2004, vol. 101, pp. 7511–7515.
Boeneman, K., Mei, B.C., Dennis, A.M., Bao, G., Deschamps, J.R., Mattoussi, H., and Medintz, I.L., J. Am. Chem. Soc., 2009, vol. 131, pp. 3828–3829.
Prasuhn, D.E., Feltz, A., Blanco-Canosa, J.B., Susumu, K., Stewart, M.H., Mei, B.C., Yakovlev, A.V., Loukov, C., Mallet, J.-M., Oheim, M., Dawson, P.E., and Medintz, I.L., ACS Nano, 2010, vol. 4, pp. 5487–5497.
Goryashchenko, A.S., Khrenova, M.G., Bochkova, A.A., Ivashina, T.V., Vinokurov, L.M., and Savitsky, A.P., Int. J. Mol. Sci., 2015, vol. 16, pp. 16642–16654.
Berezin, M.Y. and Achilefu, S., Chem. Rev., 2010, vol. 110, pp. 2641–2684.
Kang, H.J., Kim, J.H., and Chung, S.J., Biosens. Bioelectron., 2015, vol. 67, pp. 413–418.
Yuan, Y., Kwok, R.T.K., Tang, B.Z., and Liu, B., J. Am. Chem. Soc., 2014, vol. 136, pp. 2546–2554.
Stefflova, K., Chen, J., Marotta, D., Li, H., and Zheng, G., J. Med. Chem., 2006, vol. 49, pp. 3850–3856.
Yan, H., He, L., Zhao, W., Li, J., Xiao, Y., Yang, R., and Tan, W., Anal. Chem., 2014, vol. 86, pp. 11440–11450.
Wang, H., Zhang, Q., Chu, X., Chen, T., Ge, J., and Yu, R., Angew. Chem., Int. Ed. Engl., 2011, vol. 50, pp. 7065–7069.
Kaskova, Z.M., Tsarkova, A.S., and Yampolsky, I.V., Chem. Soc. Rev., 2016, vol. 45, pp. 6048–6077.
Coppola, J.M., Ross, B.D., and Rehemtulla, A., Clin. Cancer Res., 2008, vol. 14, pp. 2492–2501.
Lee, H.W., Singh, T.D., Lee, S.-W., Ha, J.-H., Rehemtulla, A., Ahn, B.-C., Jeon, Y.H., and Lee, J., FASEB J., 2014, vol. 28, pp. 2932–2941.
Shekhawat, S.S., Porter, J.R., Sriprasad, A., and Ghosh, I., J. Am. Chem. Soc., 2009, vol. 131, pp. 15284–15290.
Dacres, H., Dumancic, M.M., Horne, I., and Trowell, S.C., Anal. Biochem., 2009, vol. 385, pp. 194–202.
den Hamer, A., Dierickx, P., Arts, R., de Vries, J.S.P.M., Brunsveld, L., and Merkx, M., ACS Sens., 2017, vol. 2, pp. 729–734.
Chudakov, D.M., Matz, M.V., Lukyanov, S., and Lukyanov, K.A., Physiol. Rev., 2010, vol. 90, pp. 1103–1163.
Bardet, P.-L., Kolahgar, G., Mynett, A., Miguel-Aliaga, I., Briscoe, J., Meier, P., and Vincent, J.-P., Proc. Natl. Acad. Sci. U. S. A., 2008, vol. 105, pp. 13901–13905.
Werner, J.M. and Steinfelder, H.J., J. Pharmacol. Toxicol. Methods, 2008, vol. 57, pp. 131–137.
Vagner, T., Mouravlev, A., and Young, D., J. Pharmacol. Toxicol. Methods, 2015, vol. 72, pp. 11–18.
Zhang, J., Wang, X., Cui, W., Wang, W., Zhang, H., Liu, L., Zhang, Z., Li, Z., Ying, G., Zhang, N., and Li, B., Nat. Commun., 2013, vol. 4, p. 2157.
To, T.-L., Piggott, B.J., Makhijani, K., Yu, D., Jan, Y.N., and Shu, X., Proc. Natl. Acad. Sci. U. S. A., 2015, vol. 112, pp. 3338–3343.
To, T.-L., Schepis, A., Ruiz-González, R., Zhang, Q., Yu, D., Dong, Z., Coughlin, S.R., and Shu, X., Cell Chem. Biol., 2016, vol. 23, pp. 875–882.
Xie, J., Wang, C., Virostko, J., Manning, H.C., Pham, W., Bauer, J., and Gore, J.C., Chembiochem, 2013, vol. 14, pp. 1494–1503.
Bajar, B.T., Wang, E.S., Zhang, S., Lin, M.Z., and Chu, J., Sensors, 2016, vol. 16, p. 1488.
Pietraszewska-Bogiel, A. and Gadella, T.W.J., J. Microsc., 2011, vol. 241, pp. 111–118.
Carlson, H.J. and Campbell, R.E., Curr. Opin. Biotechnol., 2009, vol. 20, pp. 19–27.
Campbell, R.E., Anal. Chem., 2009, vol. 81, pp. 5972–5979.
van Munster, E.B. and Gadella, T.W.J., Adv. Biochem. Eng. Biotechnol., 2005, vol. 95, pp. 143–175.
Xu, X., Gerard, A.L., Huang, B.C., Anderson, D.C., Payan, D.G., and Luo, Y., Nucleic Acids Res., 1998, vol. 26, pp. 2034–2035.
Ge, J., Wood, D.K., Weingeist, D.M., Prasongtanakij, S., Navasumrit, P., Ruchirawat, M., and Engelward, B.P., Cytometry A, 2013, vol. 83, pp. 552–560.
Wäldchen, S., Lehmann, J., Klein, T., van de Linde, S., and Sauer, M., Sci. Rep., vol. 5, p. 15348.
Luo, K.Q., Yu, V.C., Pu, Y., and Chang, D.C., Biochem. Biophys. Res. Commun., 2001, vol. 283, pp. 1054–1060.
Angres, B., Steuer, H., Weber, P., Wagner, M., and Schneckenburger, H., Cytometry A, 2009, vol. 75, pp. 420–427.
Kominami, K., Nagai, T., Sawasaki, T., Tsujimura, Y., Yashima, K., Sunaga, Y., Tsuchimochi, M., Nishimura, J., Chiba, K., Nakabayashi, J., Koyamada, K., Endo, Y., Yokota, H., Miyawaki, A., Manabe, N., and Sakamaki, K., PLoS One, 2012, vol. 7, e50218.
Sha, S., Jin, H., Li, X., Yang, J., Ai, R., and Lu, J., Protein Cell, 2012, vol. 3, pp. 392–399.
Kohl, T. and Schwille, P., Adv. Biochem. Eng. Biotechnol., 2005, vol. 95, pp. 107–142.
Keese, M., Offterdinger, M., Tischer, C., Girod, A., Lommerse, P.H.M., Yagublu, V., Magdeburg, R., and Bastiaens, P.I.H., Differentiation, 2007, vol. 75, pp. 809–818.
Keese, M., Yagublu, V., Schwenke, K., Post, S., and Bastiaens, P., Int. J. Cancer, 2010, vol. 126, pp. 104–113.
Shcherbo, D., Souslova, E.A., Goedhart, J., Chepurnykh, T.V., Gaintzeva, A., Shemiakina, I.I., Gadella, T.W.J., Lukyanov, S., and Chudakov, D.M., BMC Biotechnol., 2009, vol. 9, p. 24.
Weissleder, R. and Ntziachristos, V., Nat. Med., 2003, vol. 9, pp. 123–128.
Li, I.T., Pham, E., and Truong, K., Biotechnol. Lett., 2006, vol. 28, pp. 1971–1982.
Miyamoto, A., Miyauchi, H., Kogure, T., Miyawaki, A., Michikawa, T., and Mikoshiba, K., Biochem. Biophys. Res. Commun., 2015, vol. 460, pp. 82–87.
Rusanov, A.L., Ivashina, T.V., Vinokurov, L.M., Fiks, I.I., Orlova, A.G., Turchin, I.V., Meerovich, I.G., Zherdeva, V.V., and Savitsky, A.P., J. Biophotonics, 2010, vol. 3, pp. 774–783.
Savitsky, A.P., Rusanov, A.L., Zherdeva, V.V., Gorodnicheva, T.V., Khrenova, M.G., and Nemukhin, A.V., Theranostics, 2012, vol. 2, pp. 215–226.
Zherdeva, V., Kazachkina, N.I., Shcheslavskiy, V., and Savitsky, A.P., J. Biomed. Opt., 2018, vol. 23, no. 3, pp. 1–11.
Zlobovskaya, O.A., Sergeeva, T.F., Shirmanova, M.V., Dudenkova, V.V., Sharonov, G.V., Zagaynova, E.V., and Lukyanov, K.A., BioTechniques, 2016, vol. 60, pp. 62–68.
Dubinnyi, M.A., Kaskova, Z.M., Rodionova, N.S., Baranov, M.S., Gorokhovatsky, A.Y., Kotlobay, A., Solntsev, K.M., Tsarkova, A.S., Petushkov, V.N., and Yampolsky, I.V., Angew. Chem., Int. Ed. Engl., 2015, vol. 54, pp. 7065–7067.
Purtov, K.V., Petushkov, V.N., Baranov, M.S., Mineev, K.S., Rodionova, N.S., Kaskova, Z.M., Tsarkova, A.S., Petunin, A.I., Bondar, V.S., Rodicheva, E.K., Medvedeva, S.E., Oba, Y., Oba, Y., Arseniev, A.S., Lukyanov, S., Gitelson, J.I., and Yampolsky, I.V., Angew. Chem., Int. Ed. Engl., 2015, vol. 54, pp. 8124–8128.
Kaskova, Z.M., Dörr, F.A., Petushkov, V.N., Purtov, K.V., Tsarkova, A.S., Rodionova, N.S., Mineev, K.S., Guglya, E.B., Kotlobay, A., Baleeva, N.S., Baranov, M.S., Arseniev, A.S., Gitelson, J.I., Lukyanov, S., Suzuki, Y., Kanie, S., Pinto, E., Di Mascio, P., Waldenmaier, H.E., Pereira, T.A., Carvalho, R.P., Oliveira, A.G., Oba, Y., Bastos, E.L., Stevani, C.V., and Yampolsky, I.V., Sci. Adv., 2017, vol. 3, e1602847.
Oba, Y., Suzuki, Y., Martins, G.N.R., Carvalho, R.P., Pereira, T.A., Waldenmaier, H.E., Kanie, S., Naito, M., Oliveira, A.G., Dorr, F.A., Pinto, E., Yampolsky, I.V., and Stevani, C.V., Photochem. Photobiol. Sci., 2017, vol. 16, pp. 1435–1440.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zlobovskaya, O.A., Shirmanova, M.V., Kovaleva, T.F. et al. Sensors for Caspase Activities. Russ J Bioorg Chem 44, 645–652 (2018). https://doi.org/10.1134/S1068162018060109
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1068162018060109