A whole cell assay to measure caspase-6 activity by detecting cleavage of lamin A/C

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Mintzer, Robert ^a   Ramaswamy, Sreemathy ^a   Shah, Kinjalkumar ^a   Hannoush, Rami N ^a   Pozniak, Christine D ^a   Cohen, Frederick ^a   Zhao, Xianrui ^a   Plise, Emile ^a   Lewcock, Joseph W ^a   Heise, Christopher E ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 6; CASPASE 7; LACTATE DEHYDROGENASE; LAMIN A; LAMIN C; ISOPROTEIN; PEPTIDE; PROTEINASE INHIBITOR; RECOMBINANT PROTEIN; STAUROSPORINE;

ANIMAL CELL; ANTIBODY DETECTION; ANTIGEN BINDING; APOPTOSIS; ARTICLE; BINDING AFFINITY; CELL ASSAY; CONTROLLED STUDY; DRUG DEVELOPMENT; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME RELEASE; GENE DELETION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN TARGETING; AMINO ACID SEQUENCE; ANIMAL; BIOASSAY; CELL LINE; CELL MEMBRANE; CELLS; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; ENZYME ASSAY; ENZYME SPECIFICITY; ENZYMOLOGY; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; PROTEIN PROCESSING; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; BIOLOGICAL ASSAY; BLOTTING, WESTERN; CASPASE 6; CELL LINE; CELL MEMBRANE; CELLS; ENZYME ACTIVATION; ENZYME ASSAYS; HUMANS; L-LACTATE DEHYDROGENASE; LAMIN TYPE A; MICE; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEASE INHIBITORS; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT PROTEINS; STAUROSPORINE; SUBSTRATE SPECIFICITY;

EID: 84855786390     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030376     Document Type: Article

References (41)

1. Earnshaw WC, Martins LM, Kaufmann SH, (1999) Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68: 383-424.
2. Albrecht S, Bourdeau M, Bennett D, Mufson EJ, Bhattacharjee M, et al. (2007) Activation of caspase-6 in aging and mild cognitive impairment. Am J Pathol 170: 1200-1209.
3. Guo H, Albrecht S, Bourdeau M, Petzke T, Bergeron C, et al. (2004) Active caspase-6 and caspase-6-cleaved tau in neuropil threads, neuritic plaques, and neurofibrillary tangles of Alzheimer's disease. Am J Pathol 165: 523-531.
4. Basurto-Islas G, Luna-Munoz J, Guillozet-Bongaarts AL, Binder LI, Mena R, et al. (2008) Accumulation of aspartic acid421- and glutamic acid391-cleaved tau in neurofibrillary tangles correlates with progression in Alzheimer disease. J Neuropathol Exp Neurol 67: 470-483.
5. Gervais FG, Xu D, Robertson GS, Vaillancourt JP, Zhu Y, et al. (1999) Involvement of caspases in proteolytic cleavage of Alzheimer's amyloid-beta precursor protein and amyloidogenic A beta peptide formation. Cell 97: 395-406.
6. Nikolaev A, McLaughlin T, O'Leary DD, Tessier-Lavigne M, (2009) APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 457: 981-989.
7. Graham RK, Deng Y, Slow EJ, Haigh B, Bissada N, et al. (2006) Cleavage at the caspase-6 site is required for neuronal dysfunction and degeneration due to mutant huntingtin. Cell 125: 1179-1191.
8. Hermel E, Gafni J, Propp SS, Leavitt BR, Wellington CL, et al. (2004) Specific caspase interactions and amplification are involved in selective neuronal vulnerability in Huntington's disease. Cell Death Differ 11: 424-438.
9. Leyva MJ, Degiacomo F, Kaltenbach LS, Holcomb J, Zhang N, et al. (2010) Identification and evaluation of small molecule pan-caspase inhibitors in Huntington's disease models. Chem Biol 17: 1189-1200.
10. Giaime E, Sunyach C, Druon C, Scarzello S, Robert G, et al. (2009) Loss of function of DJ-1 triggered by Parkinson's disease-associated mutation is due to proteolytic resistance to caspase-6. Cell Death Differ 17: 158-169.
11. Boatright KM, Salvesen GS, (2003) Mechanisms of caspase activation. Curr Opin Cell Biol 15: 725-731.
12. Salvesen GS, Dixit VM, (1999) Caspase activation: the induced-proximity model. Proc Natl Acad Sci U S A 96: 10964-10967.
13. Wang XJ, Cao Q, Liu X, Wang KT, Mi W, et al. (2010) Crystal structures of human caspase 6 reveal a new mechanism for intramolecular cleavage self-activation. EMBO Rep 11: 841-847.
14. Timmer JC, Salvesen GS, (2007) Caspase substrates. Cell Death Differ 14: 66-72.
15. 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.
16. Klaiman G, Petzke TL, Hammond J, Leblanc AC, (2008) Targets of caspase-6 activity in human neurons and Alzheimer disease. Mol Cell Proteomics 7: 1541-1555.
17. McStay GP, Salvesen GS, Green DR, (2008) Overlapping cleavage motif selectivity of caspases: implications for analysis of apoptotic pathways. Cell Death Differ 15: 322-331.
18. Pereira NA, Song Z, (2008) Some commonly used caspase substrates and inhibitors lack the specificity required to monitor individual caspase activity. Biochem Biophys Res Commun 377: 873-877.
19. Orth K, Chinnaiyan AM, Garg M, Froelich CJ, Dixit VM, (1996) The CED-3/ICE-like protease Mch2 is activated during apoptosis and cleaves the death substrate lamin A. J Biol Chem 271: 16443-16446.
20. Ruchaud S, Korfali N, Villa P, Kottke TJ, Dingwall C, et al. (2002) Caspase-6 gene disruption reveals a requirement for lamin A cleavage in apoptotic chromatin condensation. Embo J 21: 1967-1977.
21. Takahashi A, Alnemri ES, Lazebnik YA, Fernandes-Alnemri T, Litwack G, et al. (1996) Cleavage of lamin A by Mch2 alpha but not CPP32: multiple interleukin 1 beta-converting enzyme-related proteases with distinct substrate recognition properties are active in apoptosis. Proc Natl Acad Sci U S A 93: 8395-8400.
22. Berger AB, Sexton KB, Bogyo M, (2006) Commonly used caspase inhibitors designed based on substrate specificity profiles lack selectivity. Cell Res 16: 961-963.
23. Schotte P, Declercq W, Van Huffel S, Vandenabeele P, Beyaert R, (1999) Non-specific effects of methyl ketone peptide inhibitors of caspases. FEBS Lett 442: 117-121.
24. Komoriya A, Packard BZ, Brown MJ, Wu ML, Henkart PA, (2000) Assessment of caspase activities in intact apoptotic thymocytes using cell-permeable fluorogenic caspase substrates. J Exp Med 191: 1819-1828.
25. Maxwell D, Chang Q, Zhang X, Barnett EM, Piwnica-Worms D, (2009) An improved cell-penetrating, caspase-activatable, near-infrared fluorescent peptide for apoptosis imaging. Bioconjug Chem 20: 702-709.
26. Packard BZ, Komoriya A, (2008) A method in enzymology for measuring hydrolytic activities in live cell environments. Methods Enzymol 450: 1-19.
27. Zhang HZ, Kasibhatla S, Guastella J, Tseng B, Drewe J, et al. (2003) N-Ac-DEVD-N'-(Polyfluorobenzoyl)-R110: novel cell-permeable fluorogenic caspase substrates for the detection of caspase activity and apoptosis. Bioconjug Chem 14: 458-463.
28. Gray DC, Mahrus S, Wells JA, (2010) Activation of specific apoptotic caspases with an engineered small-molecule-activated protease. Cell 142: 637-646.
29. Figueroa RA, Ramberg V, Gatsinzi T, Samuelsson M, Zhang M, et al. (2011) Anchored FRET sensors detect local caspase activation prior to neuronal degeneration. Mol Neurodegener 6: 35.
30. Chang HK, Oh YS, Jang YJ, Kim SS, Min KS, et al. (2008) LG Life Sciences LTD. Caspase Inhibitors Based on Pyridazinone Scaffold. WO 2008/ 056897.
31. Knegtel R, Mortimore M, Studley J, Millan D, (2004) Vertex Pharmaceuticals. Caspase Inhibitors and Uses Thereof. WO 2004/ 002961.
32. Elliott JM, Rouge L, Wiesmann C, Scheer JM, (2009) Crystal structure of procaspase-1 zymogen domain reveals insight into inflammatory caspase autoactivation. J Biol Chem 284: 6546-6553.
33. Liu P, Jenkins NA, Copeland NG, (2003) A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res 13: 476-484.
34. Warming S, Rachel RA, Jenkins NA, Copeland NG, (2006) Zfp423 is required for normal cerebellar development. Mol Cell Biol 26: 6913-6922.
35. Lee EC, Yu D, Martinez de Velasco J, Tessarollo L, Swing DA, et al. (2001) A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73: 56-65.
36. Warming S, Costantino N, Court DL, Jenkins NA, Copeland NG, (2005) Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res 33: e36.
37. Mounkes LC, Burke B, Stewart CL, (2001) The A-type lamins: nuclear structural proteins as a focus for muscular dystrophy and cardiovascular diseases. Trends Cardiovasc Med 11: 280-285.
38. Warby SC, Doty CN, Graham RK, Carroll JB, Yang YZ, et al. (2008) Activated caspase-6 and caspase-6-cleaved fragments of huntingtin specifically colocalize in the nucleus. Hum Mol Genet 17: 2390-2404.
39. Boulares AH, Yakovlev AG, Ivanova V, Stoica BA, Wang G, et al. (1999) Role of poly(ADP-ribose) polymerase (PARP) cleavage in apoptosis. Caspase 3-resistant PARP mutant increases rates of apoptosis in transfected cells. J Biol Chem 274: 22932-22940.
40. Fennell M, Chan H, Wood A, (2006) Multiparameter measurement of caspase 3 activation and apoptotic cell death in NT2 neuronal precursor cells using high-content analysis. J Biomol Screen 11: 296-302.
41. Zhang D, Beresford PJ, Greenberg AH, Lieberman J, (2001) Granzymes A and B directly cleave lamins and disrupt the nuclear lamina during granule-mediated cytolysis. Proc Natl Acad Sci U S A 98: 5746-5751.