Shining light on cell death processes - a novel biosensor for necroptosis, a newly described cell death program

Biotechnology Journal

Volumn 9, Issue 2, 2014, Pages 224-240

  Sipieter, François ^a,b,c,d,e   Ladik, Maria ^b,c   Vandenabeele, Peter ^b,c   Riquet, Franck ^a,b,d,e  

^a UNIV LILLE   (France)

^b GHENT UNIVERSITY   (Belgium)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d CNRS   (France)

^e GDR2588 CNRS   (France)

Author keywords

Biosensors; Caspase; Cell death; Cytochrome C; Receptor interacting protein kinase

Indexed keywords

CASPASES; CYTOCHROME C; DYNAMIC MEASUREMENT; FLUORESCENT PROBES; MOLECULAR MECHANISM; PROGRAMMED CELL DEATHS; RECEPTOR-INTERACTING PROTEINS; RESONANCE ENERGY TRANSFER;

BIOSENSORS; DIAGNOSIS; DYNAMICS; ENERGY TRANSFER;

CELL DEATH;

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; BH3 PROTEIN; CASPASE; CASPASE 7; CASPASE 8; CYTOCHROME C; DEATH DOMAIN RECEPTOR SIGNALING ADAPTOR PROTEIN; FAS LIGAND; INITIATOR CASPASE; INITIATOR CASPASE 9; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BCL 2; PROTEIN BCL W; PROTEIN BCL XL; PROTEIN MCL 1; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

APOPTOSIS; BIOSENSOR; CELL DEATH; CONFORMATIONAL TRANSITION; DNA CLEAVAGE; DNA STRAND BREAKAGE; ENERGY TRANSFER; ENZYME ACTIVITY; FORSTER RESONANCE ENERGY TRANSFER; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; NECROPTOSIS; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

BIOSENSORS; CASPASE; CELL DEATH; CYTOCHROME C; RECEPTOR INTERACTING PROTEIN KINASE;

ANIMALS; BIOSENSING TECHNIQUES; CELL DEATH; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; HUMANS; MICE;

EID: 84893728757     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201300200     Document Type: Review

References (187)

1. Allen, P. J., J. Agric. Res. 1923, 23, 131-152.
2. Greenberg, J. T., Programmed cell death: A way of life for plants. Proc. Natl. Acad. Sci. USA 1996, 93, 12094-12097.
3. Jones, A. M., Programmed cell death in development and defense. Plant Physiol. 2001, 125, 94-97.
4. Reape, T. J., McCabe, P. F., Apoptotic-like regulation of programmed cell death in plants. Apoptosis 2010, 15, 249-256.
5. Bozhkov, P. V., Lam, E., Green death: Revealing programmed cell death in plants. Cell Death Differ. 2011, 18, 1239-1240.
6. Lindsten, T., Ross, A. J., King, A., Zong, W. X. et al., The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol. Cell 2000, 6, 1389-1399.
7. Henson, P. M., Hume, D. A., Apoptotic cell removal in development and tissue homeostasis. Trends Immunol. 2006, 27, 244-250.
8. Fuchs, Y., Steller, H., Programmed cell death in animal development and disease. Cell 2011, 147, 742-758.
9. Declercq, W., Vanden Berghe, T., Vandenabeele, P., RIP kinases at the crossroads of cell death and survival. Cell 2009, 138, 229-232.
10. Galluzzi, L., Kroemer, G., Necroptosis: A specialized pathway of programmed necrosis. Cell 2008, 135, 1161-1163.
11. Galluzzi, L., Vanden Berghe, T., Vanlangenakker, N., Buettner, S. et al., Programmed necrosis from molecules to health and disease. Int. Rev. Cell Mol. Biol. 2011, 289, 1-35.
12. Ouyang, L., Shi, Z., Zhao, S., Wang, F. T. et al., Programmed cell death pathways in cancer: A review of apoptosis, autophagy and programmed necrosis. Cell Prolif. 2012, 45, 487-498.
13. Vandenabeele, P., Declercq, W., Van Herreweghe, F., Vanden Berghe, T., The role of the kinases RIP1 and RIP3 in TNF-induced necrosis. Sci. Signal. 2010, 3, re4.
14. Vandenabeele, P., Galluzzi, L., Vanden Berghe, T., Kroemer, G., Molecular mechanisms of necroptosis: An ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 2010, 11, 700-714.
15. Vanlangenakker, N., Vanden Berghe, T., Vandenabeele, P., Many stimuli pull the necrotic trigger, an overview. Cell Death Differ. 2012, 19, 75-86.
16. Ghavami, S., Hashemi, M., Ande, S. R., Yeganeh, B. et al., Apoptosis and cancer: Mutations within caspase genes. J. Med. Genet. 2009, 46, 497-510.
17. Wong, R. S., Apoptosis in cancer: From pathogenesis to treatment. J. Exp. Clin. Cancer Res. 2011, 30, 87.
18. Golstein, P., Controlling cell death. Science 1997, 275, 1081-1082.
19. Kaiser, W. J., Upton, J. W., Mocarski, E. S., Viral modulation of programmed necrosis. Curr. Opin. Virol. 2013, 3, 296-306.
20. Upton, J. W., Kaiser, W. J., Mocarski, E. S., Virus inhibition of RIP3-dependent necrosis. Cell Host Microbe 2010, 7, 302-313.
21. Mattson, M. P., Apoptosis in neurodegenerative disorders. Nat. Rev. Mol. Cell Biol. 2000, 1, 120-129.
22. Murphy, A. C., Weyhenmeyer, B., Schmid, J., Kilbride, S. M. et al., Activation of executioner caspases is a predictor of progression-free survival in glioblastoma patients: A systems medicine approach. Cell Death Dis. 2013, 4, e629.
23. Konstantinidis, K., Whelan, R. S., Kitsis, R. N., Mechanisms of cell death in heart disease. Arterioscler. Thromb. Vasc. Biol. 2012, 32, 1552-1562.
24. Kung, G., Konstantinidis, K., Kitsis, R. N., Programmed necrosis, not apoptosis, in the heart. Circ. Res. 2011, 108, 1017-1036.
25. Whelan, R. S., Kaplinskiy, V., Kitsis, R. N., Cell death in the pathogenesis of heart disease: Mechanisms and significance. Annu. Rev. Physiol. 2010, 72, 19-44.
26. Chiong, M., Wang, Z. V., Pedrozo, Z., Cao, D. J. et al., Cardiomyocyte death: Mechanisms and translational implications. Cell Death Dis. 2011, 2, e244.
27. Carter, J., Lippa, C. F., Beta-amyloid, neuronal death and Alzheimer's disease. Curr. Mol. Med. 2001, 1, 733-737.
28. Castro, R. E., Santos, M. M., Gloria, P. M., Ribeiro, C. J. et al., Cell death targets and potential modulators in Alzheimer's disease. Curr. Pharm. Des. 2010, 16, 2851-2864.
29. Benedict, C. A., Norris, P. S., Ware, C. F., To kill or be killed: Viral evasion of apoptosis. Nat. Immunol. 2002, 3, 1013-1018.
30. Hanahan, D., Weinberg, R. A., The hallmarks of cancer. Cell 2000, 100, 57-70.
31. Hanahan, D., Weinberg, R. A., Hallmarks of cancer: The next generation. Cell 2011, 144, 646-674.
32. Igney, F. H., Krammer, P. H., Immune escape of tumors: Apoptosis resistance and tumor counterattack. J. Leukoc. Biol. 2002, 71, 907-920.
33. Kroemer, G., Galluzzi, L., Vandenabeele, P., Abrams, J. et al., Classification of cell death: Recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 2009, 16, 3-11.
34. Das, G., Shravage, B. V., Baehrecke, E. H., Regulation and function of autophagy during cell survival and cell death. Cold Spring Harb. Perspect. Biol. 2012, 4, pii: a008813.
35. Tichy, E. D., Stephan, Z. A., Osterburg, A., Noel, G., Stambrook, P. J., Mouse embryonic stem cells undergo charontosis, a novel programmed cell death pathway dependent upon cathepsins, p53, and EndoG, in response to etoposide treatment. Stem Cell Res. 2013, 10, 428-441.
36. Dixon, S. J., Lemberg, K. M., Lamprecht, M. R., Skouta, R. et al., Ferroptosis: An iron-dependent form of nonapoptotic cell death. Cell 2012, 149, 1060-1072.
37. Caunt, C. J., Finch, A. R., Sedgley, K. R., McArdle, C. A., GnRH receptor signalling to ERK: Kinetics and compartmentalization. Trends Endocrinol. Metab. 2006, 17, 308-313.
38. Ebisuya, M., Kondoh, K., Nishida, E., The duration, magnitude and compartmentalization of ERK MAP kinase activity: Mechanisms for providing signaling specificity. J. Cell Sci. 2005, 118, 2997-3002.
39. Herbst, K. J., Allen, M. D., Zhang, J., Spatiotemporally regulated protein kinase A activity is a critical regulator of growth factor-stimulated extracellular signal-regulated kinase signaling in PC12 cells. Mol. Cell. Biol. 2011, 31, 4063-4075.
40. Mebratu, Y., Tesfaigzi, Y., How ERK1/2 activation controls cell proliferation and cell death: Is subcellular localization the answer? Cell Cycle 2009, 8, 1168-1175.
41. Riquet, F. B., Vandame, P., Sipieter, F., Cailliau-Maggio, K. et al., Reporting kinase activities: Paradigms, tools and perspectives. J. Biol. Med. 2011, 1, 10-18.
42. Cagnol, S., Chambard, J. C., ERK and cell death: Mechanisms of ERK-induced cell death - apoptosis, autophagy and senescence. FEBS J. 2010, 277, 2-21.
43. Bartholomeusz, C., Rosen, D., Wei, C., Kazansky, A. et al., PEA-15 induces autophagy in human ovarian cancer cells and is associated with prolonged overall survival. Cancer Res. 2008, 68, 9302-9310.
44. Tresini, M., Lorenzini, A., Torres, C., Cristofalo, V. J., Modulation of replicative senescence of diploid human cells by nuclear ERK signaling. J. Biol. Chem. 2007, 282, 4136-4151.
45. Kohda, Y., Matsunaga, Y., Shiota, R., Satoh, T. et al., Involvement of Raf-1/MEK/ERK1/2 signaling pathway in zinc-induced injury in rat renal cortical slices. J. Toxicol. Sci. 2006, 31, 207-217.
46. Sipieter, F., Vandame, P., Spriet, C., Leray, A. et al., From FRET imaging to practical methodology for kinase activity sensing in living cells. Prog. Mol. Biol. Transl. Sci. 2013, 113, 145-216.
47. Arosio, D., Ricci, F., Marchetti, L., Gualdani, R. et al., Simultaneous intracellular chloride and pH measurements using a GFP-based sensor. Nat. Methods 2010, 7, 516-518.
48. Belousov, V. V., Fradkov, A. F., Lukyanov, K. A., Staroverov, D. B. et al., Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods 2006, 3, 281-286.
49. Tantama, M., Hung, Y. P., Yellen, G., Imaging intracellular pH in live cells with a genetically encoded red fluorescent protein sensor. J. Am. Chem. Soc. 2011, 133, 10034-10037.
50. Zhang, Y., Xie, Q., Robertson, J. B., Johnson, C. H., pHlash: A new genetically encoded and ratiometric luminescence sensor of intracellular pH. PLoS One 2012, 7, e43072.
51. Ibraheem, A., Campbell, R. E., Designs and applications of fluorescent protein-based biosensors. Curr. Opin. Chem. Biol. 2010, 14, 30-36.
52. Kerppola, T. K., Bimolecular fluorescence complementation (BiFC) analysis as a probe of protein interactions in living cells. Annu. Rev. Biophys. 2008, 37, 465-487.
53. Lukasiewicz, S., Faron-Gorecka, A., Dobrucki, J., Polit, A., Dziedzicka-Wasylewska, M., Studies on the role of the receptor protein motifs possibly involved in electrostatic interactions on the dopamine D1 and D2 receptor oligomerization. FEBS J. 2009, 276, 760-775.
54. Aye-Han, N. N., Ni, Q., Zhang, J., Fluorescent biosensors for real-time tracking of post-translational modification dynamics. Curr. Opin. Chem. Biol. 2009, 13, 392-397.
55. Kunkel, M. T., Newton, A. C., Spatiotemporal dynamics of kinase signaling visualized by targeted reporters. Curr. Protoc. Chem. Biol. 2009, 1, 17-18.
56. Ai, H. W., Hazelwood, K. L., Davidson, M. W., Campbell, R. E., Fluorescent protein FRET pairs for ratiometric imaging of dual biosensors. Nat. Methods 2008, 5, 401-403.
57. Shekhawat, S. S., Campbell, S. T., Ghosh, I., A comprehensive panel of turn-on caspase biosensors for investigating caspase specificity and caspase activation pathways. Chembiochem 2011, 12, 2353-2364.
58. Wu, X., Simone, J., Hewgill, D., Siegel, R. et al., Measurement of two caspase activities simultaneously in living cells by a novel dual FRET fluorescent indicator probe. Cytometry A 2006, 69, 477-486.
59. Herold, C., Rennekampff, H. O., Engeli, S., Apoptotic pathways in adipose tissue. Apoptosis 2013, 18, 911-916.
60. Montero, J. A., Hurle, J. M., Sculpturing digit shape by cell death. Apoptosis 2010, 15, 365-375.
61. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M. et al., Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997, 91, 479-489.
62. Elmore, S., Apoptosis: A review of programmed cell death. Toxicol. Pathol. 2007, 35, 495-516.
63. Lindsay, J., Esposti, M. D., Gilmore, A. P., Bcl-2 proteins and mitochondria - specificity in membrane targeting for death. Biochim. Biophys. Acta 2011, 1813, 532-539.
64. Mikhailov, V., Mikhailova, M., Degenhardt, K., Venkatachalam, M. A. et al., Association of Bax and Bak homo-oligomers in mitochondria. Bax requirement for Bak reorganization and cytochrome c release. J. Biol. Chem. 2003, 278, 5367-5376.
65. Letai, A., Bassik, M. C., Walensky, L. D., Sorcinelli, M. D. et al., Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2002, 2, 183-192.
66. Willis, S. N., Chen, L., Dewson, G., Wei, A. et al., Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev. 2005, 19, 1294-1305.
67. Chipuk, J. E., Green, D. R., How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol. 2008, 18, 157-164.
68. Andera, L., Signaling activated by the death receptors of the TNFR family. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub. 2009, 153, 173-180.
69. Mahoney, D. J., Cheung, H. H., Mrad, R. L., Plenchette, S. et al., Both cIAP1 and cIAP2 regulate TNFalpha-mediated NF-kappaB activation. Proc. Natl. Acad. Sci. USA 2008, 105, 11778-11783.
70. Varfolomeev, E., Goncharov, T., Fedorova, A. V., Dynek, J. N. et al., c-IAP1 and c-IAP2 are critical mediators of tumor necrosis factor alpha (TNFalpha)-induced NF-kappaB activation. J. Biol. Chem. 2008, 283, 24295-24299.
71. Duprez, L., Bertrand, M. J., Vanden Berghe, T., Dondelinger, Y. et al., Intermediate domain of receptor-interacting protein kinase 1 (RIPK1) determines switch between necroptosis and RIPK1 kinase-dependent apoptosis. J. Biol. Chem. 2012, 287, 14863-14872.
72. Shembade, N., Ma, A., Harhaj, E. W., Inhibition of NF-kappaB signaling by A20 through disruption of ubiquitin enzyme complexes. Science 2010, 327, 1135-1139.
73. Kovalenko, A., Kim, J. C., Kang, T. B., Rajput, A. et al., Caspase-8 deficiency in epidermal keratinocytes triggers an inflammatory skin disease. J. Exp. Med. 2009, 206, 2161-2177.
74. Wertz, I. E., O'Rourke, K. M., Zhou, H., Eby, M. et al., De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 2004, 430, 694-699.
75. Wu, W., Liu, P., Li, J., Necroptosis: An emerging form of programmed cell death. Crit. Rev. Oncol. Hematol. 2012, 82, 249-258.
76. Park, H. H., Structural features of caspase-activating complexes. Int. J. Mol. Sci. 2012, 13, 4807-4818.
77. Boatright, K. M., Renatus, M., Scott, F. L., Sperandio, S. et al., A unified model for apical caspase activation. Mol. Cell 2003, 11, 529-541.
78. Kaufmann, S. H., Desnoyers, S., Ottaviano, Y., Davidson, N. E., Poirier, G. G., Specific proteolytic cleavage of poly(ADP-ribose) polymerase: An early marker of chemotherapy-induced apoptosis. Cancer Res. 1993, 53, 3976-3985.
79. Nicholson, D. W., Ali, A., Thornberry, N. A., Vaillancourt, J. P. et al., Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995, 376, 37-43.
80. Arends, M. J., Morris, R. G., Wyllie, A. H., Apoptosis. The role of the endonuclease. Am. J. Pathol. 1990, 136, 593-608.
81. Jin, H., Zhao, H., Liu, L., Jiang, J. et al., Apoptosis induction of K562 cells by lymphocytes: An AFM study. Scanning 2013, 35, 7-11.
82. Kim, Y. S., Kim, K. S., Cho, C. H., Yoon, K. S. et al., Quantitative analysis with atomic force microscopy of cisplatin-induced morphological changes in HeLa and Ishikawa cells. J. Nippon Med. Sch. 2012, 79, 320-326.
83. Gavrieli, Y., Sherman, Y., Ben-Sasson, S. A., Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 1992, 119, 493-501.
84. Gorczyca, W., Bruno, S., Darzynkiewicz, R., Gong, J., Darzynkiewicz, Z., DNA strand breaks occurring during apoptosis - their early insitu detection by the terminal deoxynucleotidyl transferase and nick translation assays and prevention by serine protease inhibitors. Int. J. Oncol. 1992, 1, 639-648.
85. Gorczyca, W., Gong, J., Darzynkiewicz, Z., Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl transferase and nick translation assays. Cancer Res. 1993, 53, 1945-1951.
86. Li, X., Darzynkiewicz, Z., Labelling DNA strand breaks with BrdUTP. Detection of apoptosis and cell proliferation. Cell Prolif. 1995, 28, 571-579.
87. Vanden Berghe, T., Grootjans, S., Goossens, V., Dondelinger, Y. et al., Determination of apoptotic and necrotic cell death in vitro and in vivo. Methods 2013, 61, 117-129.
88. Fadok, V. A., Voelker, D. R., Campbell, P. A., Cohen, J. J. et al., Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 1992, 148, 2207-2216.
89. Koopman, G., Reutelingsperger, C. P., Kuijten, G. A., Keehnen, R. M. et al., Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 1994, 84, 1415-1420.
90. van Engeland, M., Nieland, L. J., Ramaekers, F. C., Schutte, B., Reutelingsperger, C. P. et al., Annexin V-affinity assay: A review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 1998, 31, 1-9.
91. Belloc, F., Belaud-Rotureau, M. A., Lavignolle, V., Bascans, E. et al., Flow cytometry detection of caspase 3 activation in preapoptotic leukemic cells. Cytometry 2000, 40, 151-160.
92. Zhang, L., Jiang, J. H., Luo, J. J., Cai, J. Y. et al., A label-free electrochemiluminescence cytosensors for specific detection of early apoptosis. Biosens. Bioelectron. 2013, 49C, 46-52.
93. Arnoult, D., Apoptosis-associated mitochondrial outer membrane permeabilization assays. Methods 2008, 44, 229-234.
94. Arnoult, D., Gaume, B., Karbowski, M., Sharpe, J. C. et al., Mitochondrial release of AIF and EndoG requires caspase activation downstream of Bax/Bak-mediated permeabilization. EMBO J. 2003, 22, 4385-4399.
95. Li, X., Darzynkiewicz, Z., Cleavage of poly(ADP-ribose) polymerase measured in situ in individual cells: Relationship to DNA fragmentation and cell cycle position during apoptosis. Exp. Cell Res. 2000, 255, 125-132.
96. Nguyen, Q. D., Lavdas, I., Gubbins, J., Smith, G. et al., Temporal and spatial evolution of therapy-induced tumor apoptosis detected by caspase-3-selective molecular imaging. Clin. Cancer Res. 2013, 19, 3914-3924.
97. Xia, C. F., Chen, G., Gangadharmath, U., Gomez, L. F. et al., In vitro and in vivo evaluation of the caspase-3 substrate-based radiotracer [(18)F]-CP18 for PET imaging of apoptosis in tumors. Mol. Imaging Biol. 2013, 15, 748-757.
98. Su, H., Chen, G., Gangadharmath, U., Gomez, L. F. et al., Evaluation of [(18)F]-CP18 as a PET imaging tracer for apoptosis. Mol. Imaging Biol. 2013, 15, 739-747.
99. Lee, B. W., Johnson, G. L., Hed, S. A., Darzynkiewicz, Z. et al., DEVDase detection in intact apoptotic cells using the cell permeant fluorogenic substrate, (z-DEVD)2-cresyl violet. Biotechniques 2003, 35, 1080-1085.
100. Cen, H., Mao, F., Aronchik, I., Fuentes, R. J., Firestone, G. L., DEVD-NucView488: A novel class of enzyme substrates for real-time detection of caspase-3 activity in live cells. FASEB J. 2008, 22, 2243-2252.
101. Keppler-Hafkemeyer, A., Brinkmann, U., Pastan, I., Role of caspases in immunotoxin-induced apoptosis of cancer cells. Biochemistry 1998, 37, 16934-16942.
102. Stennicke, H. R., Salvesen, G. S., Biochemical characteristics of caspases-3, -6, -7, and -8. J. Biol. Chem. 1997, 272, 25719-25723.
103. Liu, J., Bhalgat, M., Zhang, C., Diwu, Z. et al., Fluorescent molecular probes V: A sensitive caspase-3 substrate for fluorometric assays. Bioorg. Med. Chem. Lett. 1999, 9, 3231-3236.
104. Antczak, C., Takagi, T., Ramirez, C. N., Radu, C., Djaballah, H., Live-cell imaging of caspase activation for high-content screening. J. Biomol. Screen. 2009, 14, 956-969.
105. Kasili, P. M., Song, J. M., Vo-Dinh, T., Optical sensor for the detection of caspase-9 activity in a single cell. J. Am. Chem. Soc. 2004, 126, 2799-2806.
106. Nicholls, S. B., Chu, J., Abbruzzese, G., Tremblay, K. D., Hardy, J. A., Mechanism of a genetically encoded dark-to-bright reporter for caspase activity. J. Biol. Chem. 2011, 286, 24977-24986.
107. Huang, Q., Li, F., Liu, X., Li, W. et al., Caspase 3-mediated stimulation of tumor cell repopulation during cancer radiotherapy. Nat. Med. 2011, 17, 860-866.
108. Chudakov, D. M., Matz, M. V., Lukyanov, S., Lukyanov, K. A., Fluorescent proteins and their applications in imaging living cells and tissues. Physiol. Rev. 2010, 90, 1103-1163.
109. Luo, K. Q., Yu, V. C., Pu, Y., Chang, D. C., Application of the fluorescence resonance energy transfer method for studying the dynamics of caspase-3 activation during UV-induced apoptosis in living HeLa cells. Biochem. Biophys. Res. Commun. 2001, 283, 1054-1060.
110. Luo, K. Q., Yu, V. C., Pu, Y., Chang, D. C., Measuring dynamics of caspase-8 activation in a single living HeLa cell during TNFalpha-induced apoptosis. Biochem. Biophys. Res. Commun. 2003, 304, 217-222.
111. Zhu, X., Fu, A., Luo, K. Q., A high-throughput fluorescence resonance energy transfer (FRET)-based endothelial cell apoptosis assay and its application for screening vascular disrupting agents. Biochem. Biophys. Res. Commun. 2012, 418, 641-646.
112. Delgado, M. E., Olsson, M., Lincoln, F. A., Zhivotovsky, B., Rehm, M., Determining the contributions of caspase-2, caspase-8 and effector caspases to intracellular VDVADase activities during apoptosis initiation and execution. Biochim. Biophys. Acta 2013, 1833, 2279-2292.
113. Nagai, T., Miyawaki, A., A high-throughput method for development of FRET-based indicators for proteolysis. Biochem. Biophys. Res. Commun. 2004, 319, 72-77.
114. Shcherbo, D., Souslova, E. A., Goedhart, J., Chepurnykh, T. V. et al., Practical and reliable FRET/FLIM pair of fluorescent proteins. BMC Biotechnol. 2009, 9, 24.
115. Nguyen, A. W., Daugherty, P. S., Evolutionary optimization of fluorescent proteins for intracellular FRET. Nat. Biotechnol. 2005, 23, 355-360.
116. Tawa, P., Tam, J., Cassady, R., Nicholson, D. W., Xanthoudakis, S., Quantitative analysis of fluorescent caspase substrate cleavage in intact cells and identification of novel inhibitors of apoptosis. Cell Death Differ. 2001, 8, 30-37.
117. Onuki, R., Nagasaki, A., Kawasaki, H., Baba, T. et al., Confirmation by FRET in individual living cells of the absence of significant amyloid beta-mediated caspase 8 activation. Proc. Natl. Acad. Sci. USA 2002, 99, 14716-14721.
118. Li, H., Zhu, H., Xu, C. J., Yuan, J., Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 1998, 94, 491-501.
119. Kominami, K., Nagai, T., Sawasaki, T., Tsujimura, Y. et al., In vivo imaging of hierarchical spatiotemporal activation of caspase-8 during apoptosis. PLoS One 2012, 7, e50218.
120. Goldstein, J. C., Waterhouse, N. J., Juin, P., Evan, G. I., Green, D. R., The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat. Cell Biol. 2000, 2, 156-162.
121. Vanden Berghe, T., Vanlangenakker, N., Parthoens, E., Deckers, W. et al., Necroptosis, necrosis and secondary necrosis converge on similar cellular disintegration features. Cell Death Differ. 2010, 17, 922-930.
122. Mahajan, N. P., Linder, K., Berry, G., Gordon, G. W. et al., Bcl-2 and Bax interactions in mitochondria probed with green fluorescent protein and fluorescence resonance energy transfer. Nat. Biotechnol. 1998, 16, 547-552.
123. De Giorgi, F., Lartigue, L., Bauer, M. K., Schubert, A. et al., The permeability transition pore signals apoptosis by directing Bax translocation and multimerization. FASEB J. 2002, 16, 607-609.
124. Munoz-Pinedo, C., Guio-Carrion, A., Goldstein, J. C., Fitzgerald, P. et al., Different mitochondrial intermembrane space proteins are released during apoptosis in a manner that is coordinately initiated but can vary in duration. Proc. Natl. Acad. Sci. USA 2006, 103, 11573-11578.
125. Albeck, J. G., Burke, J. M., Aldridge, B. B., Zhang, M. et al., Quantitative analysis of pathways controlling extrinsic apoptosis in single cells. Mol. Cell 2008, 30, 11-25.
126. Laster, S. M., Wood, J. G., Gooding, L. R., Tumor necrosis factor can induce both apoptic and necrotic forms of cell lysis. J. Immunol. 1988, 141, 2629-2634.
127. Degterev, A., Huang, Z., Boyce, M., Li, Y. et al., Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 2005, 1, 112-119.
128. Chan, F. K., Shisler, J., Bixby, J. G., Felices, M. et al., A role for tumor necrosis factor receptor-2 and receptor-interacting protein in programmed necrosis and antiviral responses. J. Biol. Chem. 2003, 278, 51613-51621.
129. Cho, Y. S., Challa, S., Moquin, D., Genga, R. et al., Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 2009, 137, 1112-1123.
130. Kaiser, W. J., Upton, J. W., Long, A. B., Livingston-Rosanoff, D. et al., RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 2011, 471, 368-372.
131. Oberst, A., Dillon, C. P., Weinlich, R., McCormick, L. L. et al., Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 2011, 471, 363-367.
132. Mareninova, O. A., Sung, K. F., Hong, P., Lugea, A. et al., Cell death in pancreatitis: Caspases protect from necrotizing pancreatitis. J. Biol. Chem. 2006, 281, 3370-3381.
133. Duprez, L., Takahashi, N., Van Hauwermeiren, F., Vandendriessche, B. et al., RIP kinase-dependent necrosis drives lethal systemic inflammatory response syndrome. Immunity 2011, 35, 908-918.
134. Smith, C. C., Davidson, S. M., Lim, S. Y., Simpkin, J. C. et al., Necrostatin: A potentially novel cardioprotective agent? Cardiovasc. Drugs Ther. 2007, 21, 227-233.
135. He, S., Wang, L., Miao, L., Wang, T. et al., Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 2009, 137, 1100-1111.
136. Zhang, D. W., Shao, J., Lin, J., Zhang, N. et al., RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 2009, 325, 332-336.
137. Sun, L., Wang, H., Wang, Z., He, S. et al., Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 2012, 148, 213-227.
138. Zhao, J., Jitkaew, S., Cai, Z., Choksi, S. et al., Mixed lineage kinase domain-like is a key receptor interacting protein 3 downstream component of TNF-induced necrosis. Proc. Natl. Acad. Sci. USA 2012, 109, 5322-5327.
139. Kersse, K., Verspurten, J., Vanden Berghe, T., Vandenabeele, P., The death-fold superfamily of homotypic interaction motifs. Trends Biochem. Sci. 2011, 36, 541-552.
140. Stanger, B. Z., Leder, P., Lee, T. H., Kim, E., Seed, B., RIP: A novel protein containing a death domain that interacts with Fas/APO-1 (CD95) in yeast and causes cell death. Cell 1995, 81, 513-523.
141. Sakon, S., Xue, X., Takekawa, M., Sasazuki, T. et al., NF-kappaB inhibits TNF-induced accumulation of ROS that mediate prolonged MAPK activation and necrotic cell death. EMBO J. 2003, 22, 3898-3909.
142. Temkin, V., Huang, Q., Liu, H., Osada, H., Pope, R. M., Inhibition of ADP/ATP exchange in receptor-interacting protein-mediated necrosis. Mol. Cell Biol. 2006, 26, 2215-2225.
143. Vanlangenakker, N., Vanden Berghe, T., Bogaert, P., Laukens, B. et al., cIAP1 and TAK1 protect cells from TNF-induced necrosis by preventing RIP1/RIP3-dependent reactive oxygen species production. Cell Death Differ. 2011, 18, 656-665.
144. Vanlangenakker, N., Bertrand, M. J., Bogaert, P., Vandenabeele, P., Vanden Berghe, T., TNF-induced necroptosis in L929 cells is tightly regulated by multiple TNFR1 complex I and II members. Cell Death Dis. 2011, 2, e230.
145. Zhang, Z., Larner, S. F., Liu, M. C., Zheng, W. et al., Multiple alphaII-spectrin breakdown products distinguish calpain and caspase dominated necrotic and apoptotic cell death pathways. Apoptosis 2009, 14, 1289-1298.
146. Vanderklish, P. W., Krushel, L. A., Holst, B. H., Gally, J. A. et al., Marking synaptic activity in dendritic spines with a calpain substrate exhibiting fluorescence resonance energy transfer. Proc. Natl. Acad. Sci. USA 2000, 97, 2253-2258.
147. Boya, P., Kroemer, G., Lysosomal membrane permeabilization in cell death. Oncogene 2008, 27, 6434-6451.
148. Repnik, U., Stoka, V., Turk, V., Turk, B., Lysosomes and lysosomal cathepsins in cell death. Biochim. Biophys. Acta 2012, 1824, 22-33.
149. Kagedal, K., Johansson, U., Ollinger, K., The lysosomal protease cathepsin D mediates apoptosis induced by oxidative stress. FASEB J. 2001, 15, 1592-1594.
150. Drake, C. R., Miller, D. C., Jones, E. F., Activatable optical probes for the detection of enzymes. Curr. Org. Synth. 2011, 8, 498-520.
151. Yhee, J. Y., Kim, S. A., Koo, H., Son, S. et al., Optical imaging of cancer-related proteases using near-infrared fluorescence matrix metalloproteinase-sensitive and cathepsin B-sensitive probes. Theranostics 2012, 2, 179-189.
152. Ryu, J. H., Kim, S. A., Koo, H., Yhee, J. Y. et al., Cathepsin B-sensitive nanoprobe for in vivo tumor diagnosis. J. Mater. Chem. 2011, 21, 17631-17634.
153. Joyce, J. A., Baruch, A., Chehade, K., Meyer-Morse, N. et al., Cathepsin cysteine proteases are effectors of invasive growth and angiogenesis during multistage tumorigenesis. Cancer Cell 2004, 5, 443-453.
154. Lane, D. P., Cheok, C. F., Lain, S., p53-based cancer therapy. Cold Spring Harb. Perspect. Biol. 2010, 2, a001222.
155. Kroemer, G., Pouyssegur, J., Tumor cell metabolism: Cancer's Achilles' heel. Cancer Cell 2008, 13, 472-482.
156. Zhao, Y., Butler, E. B., Tan, M., Targeting cellular metabolism to improve cancer therapeutics. Cell Death Dis. 2013, 4, e532.
157. Jones, R. G., Thompson, C. B., Tumor suppressors and cell metabolism: A recipe for cancer growth. Genes Dev. 2009, 23, 537-548.
158. Borst, P., Rottenberg, S., Cancer cell death by programmed necrosis? Drug Resist. Updat. 2004, 7, 321-324.
159. Zong, W. X., Ditsworth, D., Bauer, D. E., Wang, Z. Q., Thompson, C. B., Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev. 2004, 18, 1272-1282.
160. Cande, C., Vahsen, N., Garrido, C., Kroemer, G., Apoptosis-inducing factor (AIF): Caspase-independent after all. Cell Death Differ. 2004, 11, 591-595.
161. Moubarak, R. S., Yuste, V. J., Artus, C., Bouharrour, A. et al., Sequential activation of poly(ADP-ribose) polymerase 1, calpains, and Bax is essential in apoptosis-inducing factor-mediated programmed necrosis. Mol. Cell Biol. 2007, 27, 4844-4862.
162. Baritaud, M., Cabon, L., Delavallee, L., Galan-Malo, P. et al., AIF-mediated caspase-independent necroptosis requires ATM and DNA-PK-induced histone H2AX Ser139 phosphorylation. Cell Death Dis. 2012, 3, e390.
163. Delavallee, L., Cabon, L., Galan-Malo, P., Lorenzo, H. K., Susin, S. A., AIF-mediated caspase-independent necroptosis: A new chance for targeted therapeutics. IUBMB Life 2011, 63, 221-232.
164. Scaffidi, P., Misteli, T., Bianchi, M. E., Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002, 418, 191-195.
165. Hu, X., Han, W., Li, L., Targeting the weak point of cancer by induction of necroptosis. Autophagy 2007, 3, 490-492.
166. Han, W., Li, L., Qiu, S., Lu, Q. et al., Shikonin circumvents cancer drug resistance by induction of a necroptotic death. Mol. Cancer Ther. 2007, 6, 1641-1649.
167. Tenev, T., Bianchi, K., Darding, M., Broemer, M. et al., The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol. Cell 2011, 43, 432-448.
168. Jain, M. V., Paczulla, A. M., Klonisch, T., Dimgba, F. N. et al., Interconnections between apoptotic, autophagic and necrotic pathways: Implications for cancer therapy development. J. Cell Mol. Med. 2013, 17, 12-29.
169. Nikoletopoulou, V., Markaki, M., Palikaras, K., Tavernarakis, N., Crosstalk between apoptosis, necrosis and autophagy. Biochim. Biophys. Acta 2013, 1833, 3448-3459.
170. Walsh, C. M., Edinger, A. L., The complex interplay between autophagy, apoptosis, and necrotic signals promotes T-cell homeostasis. Immunol. Rev. 2010, 236, 95-109.
171. Lim, S. C., Choi, J. E., Kang, H. S., Han, S. I., Ursodeoxycholic acid switches oxaliplatin-induced necrosis to apoptosis by inhibiting reactive oxygen species production and activating p53-caspase 8 pathway in HepG2 hepatocellular carcinoma. Int. J. Cancer 2010, 126, 1582-1595.
172. Prabhakaran, K., Li, L., Borowitz, J. L., Isom, G. E., Caspase inhibition switches the mode of cell death induced by cyanide by enhancing reactive oxygen species generation and PARP-1 activation. Toxicol. Appl. Pharmacol. 2004, 195, 194-202.
173. Earley, S., Vinegoni, C., Dunham, J., Gorbatov, R. et al., In vivo imaging of drug-induced mitochondrial outer membrane permeabilization at single-cell resolution. Cancer Res. 2012, 72, 2949-2956.
174. Andresen, V., Pollok, K., Rinnenthal, J. L., Oehme, L. et al., High-resolution intravital microscopy. PLoS One 2012, 7, e50915.
175. Bagci-Onder, T., Agarwal, A., Flusberg, D., Wanningen, S. et al., Real-time imaging of the dynamics of death receptors and therapeutics that overcome TRAIL resistance in tumors. Oncogene 2013, 32, 2818-2827.
176. Nesterenko, I., Wanninge, S., Bagci-Onder, T., Anderegg, M., Shah, K., Evaluating the effect of therapeutic stem cells on TRAIL resistant and sensitive medulloblastomas. PLoS One 2012, 7, e49219.
177. Piljic, A., Schultz, C., Simultaneous recording of multiple cellular events by FRET. ACS Chem. Biol. 2008, 3, 156-160.
178. Welch, C. M., Elliott, H., Danuser, G., Hahn, K. M., Imaging the coordination of multiple signalling activities in living cells. Nat. Rev. Mol. Cell Biol. 2011, 12, 749-756.
179. Yu, J. Q., Liu, X. F., Chin, L. K., Liu, A. Q., Luo, K. Q., Study of endothelial cell apoptosis using fluorescence resonance energy transfer (FRET) biosensor cell line with hemodynamic microfluidic chip system. Lab. Chip 2013, 13, 2693-2700.
180. Grassilli, E., Narloch, R., Federzoni, E., Ianzano, L. et al., Inhibition of GSK3B bypass drug resistance of p53-null colon carcinomas by enabling necroptosis in response to chemotherapy. Clin. Cancer Res. 2013, 19, 3820-3831.
181. Taelman, V. F., Dobrowolski, R., Plouhinec, J. L., Fuentealba, L. C. et al., Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell 2010, 143, 1136-1148.
182. Mizutani, T., Kondo, T., Darmanin, S., Tsuda, M. et al., A novel FRET-based biosensor for the measurement of BCR-ABL activity and its response to drugs in living cells. Clin. Cancer Res. 2010, 16, 3964-3975.
183. Shi, S., Yao, W., Xu, J., Long, J. et al., Combinational therapy: New hope for pancreatic cancer? Cancer Lett. 2012, 317, 127-135.
184. Weisberg, E., Manley, P. W., Cowan-Jacob, S. W., Hochhaus, A., Griffin, J. D., Second generation inhibitors of BCR-ABL for the treatment of imatinib-resistant chronic myeloid leukaemia. Nat. Rev. Cancer 2007, 7, 345-356.
185. Al-Lazikani, B., Banerji, U., Workman, P., Combinatorial drug therapy for cancer in the post-genomic era. Nat. Biotechnol. 2012, 30, 679-692.
186. Kohnke, M., Schmitt, S., Ariotti, N., Piggott, A. M. et al., Design and application of in vivo FRET biosensors to identify protein prenylation and nanoclustering inhibitors. Chem. Biol. 2012, 19, 866-874.
187. Komatsu, N., Aoki, K., Yamada, M., Yukinaga, H. et al., Development of an optimized backbone of FRET biosensors for kinases and GTPases. Mol. Biol. Cell 2011, 22, 4647-4656.