In Vivo Imaging of Hierarchical Spatiotemporal Activation of Caspase-8 during Apoptosis

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Kominami, Katsuya ^a   Nagai, Takeharu ^b,c,i   Sawasaki, Tatsuya ^d   Tsujimura, Yuki ^e   Yashima, Kenta ^f   Sunaga, Yasuhiro ^e   Tsuchimochi, Masateru ^d   Nishimura, Jun ^a   Chiba, Kumiko ^a   Nakabayashi, Jun ^g   Koyamada, Koji ^a   Endo, Yaeta ^d   Yokota, Hideo ^e   Miyawaki, Atsushi ^b   Manabe, Noboru ^h   Sakamaki, Kazuhiro ^a  

^a KYOTO UNIVERSITY   (Japan)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

^d EHIME UNIVERSITY   (Japan)

^e RIKEN   (Japan)

^f MEIJI UNIVERSITY   (Japan)

^g YOKOHAMA CITY UNIVERSITY   (Japan)

^h UNIVERSITY OF TOKYO   (Japan)

ⁱ OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 8; DEATH RECEPTOR; PROCASPASE 3; PROCASPASE 9; RECOMBINANT PROTEIN;

APOPTOSIS; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DIFFUSION; ENZYME ACTIVATION; ENZYME RECONSTITUTION; ENZYMIC BIOSENSOR; FLUORESCENCE IMAGING; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; POSITIVE FEEDBACK; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; APOPTOSIS; BIOSENSING TECHNIQUES; CASPASE 3; CASPASE 8; ENZYME ACTIVATION; ENZYME PRECURSORS; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION REGULATION; HEK293 CELLS; HELA CELLS; HUMANS; MOLECULAR IMAGING; MOLECULAR SEQUENCE DATA; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; SINGLE-CELL ANALYSIS; TRANSFECTION;

MAMMALIA;

EID: 84869845897     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050218     Document Type: Article

References (45)

1. Stennicke HR, Salvesen GS, (1998) Properties of the caspases. Biochim Biophys Acta 1387: 17-31.
2. Thornberry NA, Lazebnik Y, (1998) Caspases: enemies within. Science 281: 1312-1316.
3. Earnshaw WC, Martins LM, Kaufmann SH, (1999) Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68: 383-424.
4. Taylor RC, Cullen SP, Martin SJ, (2008) Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 9: 231-241.
5. Chudakov DM, Matz MV, Lukyanov S, Lukyanov KA, (2010) Fluorescent proteins and their applications in imaging living cells and tissues. Physiol Rev 90: 1103-1163.
6. Luo KQ, Yu VC, Pu Y, Chang DC, (2003) Measuring dynamics of caspase-8 activation in a single living HeLa cell during TNFalpha-induced apoptosis. Biochem Biophys Res Commun 304: 217-222.
7. Kawai H, Suzuki T, Kobayashi T, Sakurai H, Ohata H, et al. (2005) Simultaneous real-time detection of initiator- and effector-caspase activation by double fluorescence resonance energy transfer analysis. J Pharmacol Sci 97: 361-368.
8. Albeck JG, Burke JM, Aldridge BB, Zhang M, Lauffenburger DA, et al. (2008) Quantitative analysis of pathways controlling extrinsic apoptosis in single cells. Mol Cell 30: 11-25.
9. Hellwig CT, Kohler BF, Lehtivarjo AK, Dussmann H, Courtney MJ, et al. (2008) Real time analysis of tumor necrosis factor-related apoptosis-inducing ligand/cycloheximide-induced caspase activities during apoptosis initiation. J Biol Chem 283: 21676-21685.
10. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, et al. (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20: 87-90.
11. Campbell RE, Tour O, Palmer AE, Steinbach PA, Baird GS, et al. (2002) A monomeric red fluorescent protein. Proc Natl Acad Sci U S A 99: 7877-7882.
12. Talanian RV, Quinlan C, Trautz S, Hackett MC, Mankovich JA, et al. (1997) Substrate specificities of caspase family proteases. J Biol Chem 272: 9677-9682.
13. Thornberry NA, Chapman KT, Nicholson DW, (2000) Determination of caspase specificities using a peptide combinatorial library. Methods Enzymol 322: 100-110.
14. Chereau D, Kodandapani L, Tomaselli KJ, Spada AP, Wu JC, (2003) Structural and functional analysis of caspase active sites. Biochemistry 42: 4151-4160.
15. Muzio M, Stockwell BR, Stennicke HR, Salvesen GS, Dixit VM, (1998) An induced proximity model for caspase-8 activation. J Biol Chem 273: 2926-2930.
16. Germain M, Affar EB, D'Amours D, Dixit VM, Salvesen GS, et al. (1999) Cleavage of automodified poly(ADP-ribose) polymerase during apoptosis. Evidence for involvement of caspase-7. J Biol Chem 274: 28379-28384.
17. Sawasaki T, Ogasawara T, Morishita R, Endo Y, (2002) A cell-free protein synthesis system for high-throughput proteomics. Proc Natl Acad Sci U S A 99: 14652-14657.
18. Chen M, Orozco A, Spencer DM, Wang J, (2002) Activation of initiator caspases through a stable dimeric intermediate. J Biol Chem 277: 50761-50767.
19. Nagai T, Miyawaki A, (2004) A high-throughput method for development of FRET-based indicators for proteolysis. Biochem Biophys Res Commun 319: 72-77.
20. Kominami K, Nakabayashi J, Nagai T, Tsujimura Y, Chiba K, et al. (2012) The molecular mechanism of apoptosis upon caspase-8 activation: Quantitative experimental validation of a mathematical model. Biochim Biophys Acta 1823: 1825-1840.
21. Tanaka M, Itai T, Adachi M, Nagata S, (1998) Downregulation of Fas ligand by shedding. Nat Med 4: 31-36.
22. Habuchi S, Tsutsui H, Kochaniak AB, Miyawaki A, van Oijen AM, (2008) mKikGR, a monomeric photoswitchable fluorescent protein. PLoS One 3: e3944.
23. Wu X, Simone J, Hewgill D, Siegel R, Lipsky PE, et al. (2006) Measurement of two caspase activities simultaneously in living cells by a novel dual FRET fluorescent indicator probe. Cytometry A 69: 477-486.
24. Rehm M, Huber HJ, Dussmann H, Prehn JH, (2006) Systems analysis of effector caspase activation and its control by X-linked inhibitor of apoptosis protein. EMBO J 25: 4338-4349.
25. Kischkel FC, Hellbardt S, Behrmann I, Germer M, Pawlita M, et al. (1995) Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 14: 5579-5588.
26. Boatright KM, Renatus M, Scott FL, Sperandio S, Shin H, et al. (2003) A unified model for apical caspase activation. Mol Cell 11: 529-541.
27. Donepudi M, Sweeney AM, Briand C, Grutter MG, (2003) Insights into the regulatory mechanism for caspase-8 activation. Mol Cell 11: 543-549.
28. Murphy BM, Creagh EM, Martin SJ, (2004) Interchain proteolysis, in the absence of a dimerization stimulus, can initiate apoptosis-associated caspase-8 activation. J Biol Chem 279: 36916-36922.
29. Sohn D, Schulze-Osthoff K, Janicke RU, (2005) Caspase-8 can be activated by interchain proteolysis without receptor-triggered dimerization during drug-induced apoptosis. J Biol Chem 280: 5267-5273.
30. Van de Craen M, Declercq W, Van den brande I, Fiers W, Vandenabeele P, (1999) The proteolytic procaspase activation network: an in vitro analysis. Cell Death Differ 6: 1117-1124.
31. Cowling V, Downward J, (2002) Caspase-6 is the direct activator of caspase-8 in the cytochrome c-induced apoptosis pathway: absolute requirement for removal of caspase-6 prodomain. Cell Death Differ 9: 1046-1056.
32. Inoue S, Browne G, Melino G, Cohen GM, (2009) Ordering of caspases in cells undergoing apoptosis by the intrinsic pathway. Cell Death Differ 16: 1053-1061.
33. Oberst A, Pop C, Tremblay AG, Blais V, Denault JB, et al. (2010) Inducible dimerization and inducible cleavage reveal a requirement for both processes in caspase-8 activation. J Biol Chem 285: 16632-16642.
34. Conus S, Pop C, Snipas SJ, Salvesen GS, Simon HU, (2012) Cathepsin D Primes Caspase-8 Activation by Multiple Intra-chain Proteolysis. J Biol Chem 287: 21142-21151.
35. Desai BN, Krapivinsky G, Navarro B, Krapivinsky L, Carter BC, et al. (2012) Cleavage of TRPM7 Releases the Kinase Domain from the Ion Channel and Regulates Its Participation in Fas-Induced Apoptosis. Dev Cell 22: 1149-1162.
36. Matsuda T, Miyawaki A, Nagai T, (2008) Direct measurement of protein dynamics inside cells using a rationally designed photoconvertible protein. Nat Methods 5: 339-345.
37. Tenev T, Bianchi K, Darding M, Broemer M, Langlais C, et al. (2011) The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol Cell 43: 432-448.
38. Feoktistova M, Geserick P, Kellert B, Dimitrova DP, Langlais C, et al. (2011) cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol Cell 43: 449-463.
39. Schleich K, Warnken U, Fricker N, Ozturk S, Richter P, et al. (2012) Stoichiometry of the CD95 Death-Inducing Signaling Complex: Experimental and Modeling Evidence for a Death Effector Domain Chain Model. Mol Cell 47: 306-319.
40. Huber HJ, Laussmann MA, Prehn JH, Rehm M, (2010) Diffusion is capable of translating anisotropic apoptosis initiation into a homogeneous execution of cell death. BMC Syst Biol 4: 9.
41. Niwa H, Yamamura K, Miyazaki J, (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193-199.
42. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, et al. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22: 1567-1572.
43. Sakamaki K, Miyajima I, Kitamura T, Miyajima A, (1992) Critical cytoplasmic domains of the common beta subunit of the human GM-CSF, IL-3 and IL-5 receptors for growth signal transduction and tyrosine phosphorylation. EMBO J 11: 3541-3549.
44. Kobayashi Y, Yonehara S, (2009) Novel cell death by downregulation of eEF1A1 expression in tetraploids. Cell Death Differ 16: 139-150.
45. Shimozono S, Miyawaki A, (2008) Engineering FRET constructs using CFP and YFP. Methods Cell Biol 85: 381-393.