Cacidases: Caspases can cleave after aspartate, glutamate and phosphoserine residues

Cell Death and Differentiation

Volumn 23, Issue 10, 2016, Pages 1717-1726

  Seaman, J E ^a   Julien, O ^a   Lee, P S ^a   Rettenmaier, T J ^a,b   Thomsen, N D ^a,c   Wells, J A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c GILEAD SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; CASPASE 3; CASPASE 7; GLUTAMIC ACID; PHOSPHOSERINE; CASPASE; PEPTIDE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONSENSUS SEQUENCE; ENZYME SPECIFICITY; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; KINETICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PHOSPHORYLATION; PROTEOMICS; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CONSERVED SEQUENCE; HEK293 CELL LINE; METABOLISM; PHOSPHORYLATION; PROTEIN DEGRADATION;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; ASPARTIC ACID; CASPASES; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; GLUTAMIC ACID; HEK293 CELLS; HUMANS; KINETICS; MICE; PEPTIDES; PHOSPHORYLATION; PHOSPHOSERINE; PROTEOLYSIS; SUBSTRATE SPECIFICITY;

EID: 84976559172     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2016.62     Document Type: Article

References (59)

1. Alnemri ES, Livingston DJ, Nicholson DW, Salvesen G, Thornberry NA, Wong WW, et al. Human ICE/CED-3 protease nomenclature. Cell 1996; 87: 171.
2. Schechter I, Berger A. On the size of the active site in proteases. I. Papain. Biochem Biophys Res Commun 1967; 27: 157-162.
3. Thornberry NA, Rano TA, Peterson EP, Rasper DM, Timkey T, Garcia-Calvo M, et al. A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J Biol Chem 1997; 272: 17907-17911.
4. Poreba M, Strozyk A, Salvesen GS, Drag M. Caspase substrates and inhibitors. Cold Spring Harb Perspect Biol 2013; 5: a008680.
5. Rano TA, Timkey T, Peterson EP, Rotonda J, Nicholson DW, Becker JW, et al. A combinatorial approach for determining protease specificities: application to interleukin- 1beta converting enzyme (ICE). Chem Biol 1997; 4: 149-155.
6. Pham VC, Anania VG, Phung QT, Lill JR. Complementary methods for the identification of substrates of proteolysis. Methods Enzymol 2014; 544: 359-380.
7. van den Berg BH, Tholey A. Mass spectrometry-based proteomics strategies for protease cleavage site identification. Proteomics 2012; 12: 516529.
8. Staes A, Impens F, Van Damme P, Ruttens B, Goethals M, Demol H, et al. Selecting protein N-terminal peptides by combined fractional diagonal chromatography. Nat Protoc 2011; 6: 1130-1141.
9. Impens F, Colaert N, Helsens K, Ghesquiere B, Timmerman E, De Bock PJ, et al. A quantitative proteomics design for systematic identification of protease cleavage events. Mol Cell Proteomics 2010; 9: 2327-2333.
10. Drag M, Bogyo M, Ellman JA, Salvesen GS. Aminopeptidase fingerprints, an integrated approach for identification of good substrates and optimal inhibitors. J Biol Chem 2010; 285: 3310-3318.
11. Wejda M, Impens F, Takahashi N, Van Damme P, Gevaert K, Vandenabeele P. Degradomics reveals that cleavage specificity profiles of caspase-2 and effector caspases are alike. J Biol Chem 2012; 287: 33983-33995.
12. Turowec JP, Zukowski SA, Knight JD, Smalley DM, Graves LM, Johnson GL, et al. An unbiased proteomic screen reveals caspase cleavage is positively and negatively regulated by substrate phosphorylation. Mol Cell Proteomics 2014; 13: 1184-1197.
13. Dix MM, Simon GM, Cravatt BF. Global identification of caspase substrates using PROTOMAP (protein topography and migration analysis platform). Methods Mol Biol 2014; 1133: 61-70.
14. Julien O, Zhuang M, Wiita AP, O'Donoghue AJ, Knudsen GM, Craik CS, et al. Quantitative MS-based enzymology of caspases reveals distinct protein substrate specificities, hierarchies, and cellular roles. Proc Natl Acad Sci USA 2016; 113: E2001-E2010.
15. Stoehr G, Schaab C, Graumann J, Mann M. A SILAC-based approach identifies substrates of caspase-dependent cleavage upon TRAIL-induced apoptosis. Mol Cell Proteomics 2013; 12: 1436-1450.
16. Shimbo K, Hsu GW, Nguyen H, Mahrus S, Trinidad JC, Burlingame AL, et al. Quantitative profiling of caspase-cleaved substrates reveals different drug-induced and cell-type patterns in apoptosis. Proc Natl Acad Sci USA 2012; 109: 12432-12437.
17. Lamkanfi M, Kanneganti TD, Van Damme P, Vanden Berghe T, Vanoverberghe I, Vandekerckhove J, et al. Targeted peptidecentric proteomics reveals caspase-7 as a substrate of the caspase-1 inflammasomes. Mol Cell Proteomics 2008; 7: 2350-2363.
18. Crawford ED, Seaman JE, Agard N, Hsu GW, Julien O, Mahrus S, et al. The DegraBase: a database of proteolysis in healthy and apoptotic human cells. Mol Cell Proteomics 2013; 12: 813-824.
19. Mahrus S, Trinidad JC, Barkan DT, Sali A, Burlingame AL, Wells JA. Global sequencing of proteolytic cleavage sites in apoptosis by specific labeling of protein N termini. Cell 2008; 134: 866-876.
20. Timmer JC, Zhu W, Pop C, Regan T, Snipas SJ, Eroshkin AM, et al. Structural and kinetic determinants of protease substrates. Nat Struct Mol Biol 2009; 16: 1101-1108.
21. Agard NJ, Mahrus S, Trinidad JC, Lynn A, Burlingame AL, Wells JA. Global kinetic analysis of proteolysis via quantitative targeted proteomics. Proc Natl Acad Sci USA 2012; 109: 1913-1918.
22. Srinivasula SM, Hegde R, Saleh A, Datta P, Shiozaki E, Chai J, et al. A conserved XIAPinteraction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature 2001; 410: 112-116.
23. Soares J, Lowe MM, Jarstfer MB. The catalytic subunit of human telomerase is a unique caspase-6 and caspase-7 substrate. Biochemistry 2011; 50: 9046-9055.
24. Moretti A, Weig HJ, Ott T, Seyfarth M, Holthoff HP, Grewe D, et al. Essential myosin light chain as a target for caspase-3 in failing myocardium. Proc Natl Acad Sci USA 2002; 99: 11860-11865.
25. Krippner-Heidenreich A, Talanian RV, Sekul R, Kraft R, Thole H, Ottleben H, et al. Targeting of the transcription factorMax during apoptosis: phosphorylation-regulated cleavage by caspase-5 at an unusual glutamic acid residue in position P1. Biochem J 2001; 358: 705-715.
26. Checinska A, Giaccone G, Rodriguez JA, Kruyt FA, Jimenez CR. Comparative proteomics analysis of caspase-9-protein complexes in untreated and cytochrome c/dATP stimulated lysates of NSCLC cells. J Proteomics 2009; 72: 575-585.
27. Crawford ED, Seaman JE, Barber AE 2nd, David DC, Babbitt PC, Burlingame AL, et al. Conservation of caspase substrates across metazoans suggests hierarchical importance of signaling pathways over specific targets and cleavage site motifs in apoptosis. Cell Death Differ 2012; 19: 2040-2048.
28. Talanian RV, Quinlan C, Trautz S, Hackett MC, Mankovich JA, Banach D, et al. Substrate specificities of caspase family proteases. J Biol Chem 1997; 272: 9677-9682.
29. Pop C, Salvesen GS. Human caspases: activation, specificity, and regulation. J Biol Chem 2009; 284: 21777-21781.
30. Thomsen ND, Koerber JT, Wells JA. Structural snapshots reveal distinct mechanisms of procaspase-3 and -7 activation. Proc Natl Acad Sci USA 2013; 110: 8477-8482.
31. Ganesan R, Mittl PR, Jelakovic S, Grutter MG. Extended substrate recognition in caspase-3 revealed by high resolution X-ray structure analysis. J Mol Biol 2006; 359: 1378-1388.
32. Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG, Earnshaw WC. Cleavage of poly (ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 1994; 371: 346-347.
33. Witkowski WA, Hardy JA. L2' loop is critical for caspase-7 active site formation. Protein Sci 2009; 18: 1459-1468.
34. Hornbeck PV, Chabra I, Kornhauser JM, Skrzypek E, Zhang B. PhosphoSite: a bioinformatics resource dedicated to physiological protein phosphorylation. Proteomics 2004; 4: 1551-1561.
35. Park K, Kuechle MK, Choe Y, Craik CS, Lawrence OT, Presland RB. Expression and characterization of constitutively active human caspase-14. Biochem Biophys Res Commun 2006; 347: 941-948.
36. Quistad SD, Stotland A, Barott KL, Smurthwaite CA, Hilton BJ, Grasis JA, et al. Evolution of TNF-induced apoptosis reveals 550 My of functional conservation. Proc Natl Acad Sci USA 2014; 111: 9567-9572.
37. Kumar S, van Raam BJ, Salvesen GS, Cieplak P. Caspase cleavage sites in the human proteome: CaspDB, a database of predicted substrates. PLoS One 2014; 9: e110539.
38. Wee LJ, Tan TW, Ranganathan S. CASVM: web server for SVM-based prediction of caspase substrates cleavage sites. Bioinformatics 2007; 23: 3241-3243.
39. Hawkins CJ, Yoo SJ, Peterson EP, Wang SL, Vernooy SY, Hay BA. The Drosophila caspase DRONC cleaves following glutamate or aspartate and is regulated by DIAP1, HID, and GRIM. J Biol Chem 2000; 275: 27084-27093.
40. Kumar S, Doumanis J. The fly caspases. Cell Death Differ 2000; 7: 1039-1044.
41. Snipas SJ, Drag M, Stennicke HR, Salvesen GS. Activation mechanism and substrate specificity of the Drosophila initiator caspase DRONC. Cell Death Differ 2008; 15: 938-945.
42. Song Z, Guan B, Bergman A, Nicholson DW, Thornberry NA, Peterson EP, et al. Biochemical and genetic interactions between Drosophila caspases and the proapoptotic genes rpr, hid, and grim. Mol Cell Biol 2000; 20: 2907-2914.
43. Kurokawa M, Kornbluth S. Caspases and kinases in a death grip. Cell 2009; 138: 838-854.
44. Dix MM, Simon GM, Wang C, Okerberg E, Patricelli MP, Cravatt BF. Functional interplay between caspase cleavage and phosphorylation sculpts the apoptotic proteome. Cell 2012; 150: 426-440.
45. Thorsness PE, Koshland DE Jr. Inactivation of isocitrate dehydrogenase by phosphorylation is mediated by the negative charge of the phosphate. J Biol Chem 1987; 262: 10422-10425.
46. Pearlman SM, Serber Z, Ferrell JE Jr. A mechanism for the evolution of phosphorylation sites. Cell 2011; 147: 934-946.
47. Colaert N, Helsens K, Martens L, Vandekerckhove J, Gevaert K. Improved visualization of protein consensus sequences by iceLogo. Nat Methods 2009; 6: 786-787.
48. Petersen B, Petersen TN, Andersen P, Nielsen M, Lundegaard C. A generic method for assignment of reliability scores applied to solvent accessibility predictions. BMC Struct Biol 2009; 9: 51.
49. Boyle EI,Weng S, Gollub J, Jin H, Botstein D, Cherry JM, et al. GO::TermFinder-open source software for accessing gene ontology information and finding significantly enriched gene ontology terms associated with a list of genes. Bioinformatics 2004; 20: 3710-3715.
50. Wolan DW, Zorn JA, Gray DC, Wells JA. Small-molecule activators of a proenzyme. Science 2009; 326: 853-858.
51. Kabsch W. XDS. Acta Crystallogr D Biol Crystallogr 2010; 66: 125-132.
52. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. Phaser crystallographic software. J Appl Crystallogr 2007; 40: 658-674.
53. Agniswamy J, Fang B, Weber IT. Plasticity of S2-S4 specificity pockets of executioner caspase-7 revealed by structural and kinetic analysis. FEBS J 2007; 274: 4752-4765.
54. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 2010; 66: 486-501.
55. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solutionActa Crystallogr D Biol Crystallogr 2010; 66: 213-221.
56. Lebedev AA, Young P, Isupov MN, Moroz OV, Vagin AA, Murshudov GN. JLigand: a graphical tool for the CCP4 template-restraint library. Acta Crystallogr D Biol Crystallogr 2012; 68: 431-440.
57. Chen VB, Arendall WB 3rd, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 2010; 66: 12-21.
58. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL. NCBI BLAST: a better web interface. Nucleic Acids Res 2008; 36: W5-W9.
59. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011; 7: 539.