The arabidopsis METACASPASE9 degradome

Plant Cell

Volumn 25, Issue 8, 2013, Pages 2831-2847

  Tsiatsiani, Liana ^a,b,c   Timmerman, Evy ^a,b   De Bock, Pieter Jan ^a,b   Vercammen, Dominique ^a,b,d   Stael, Simon ^a,b   van de Cotte, Brigitte ^a,b   Staes, An ^a,b   Goethals, Marc ^a,b   Beunens, Tine ^a,b   Van Damme, Petra ^a,b   Gevaert, Kris ^a,b   Van Breusegem, Frank ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c UTRECHT UNIVERSITY   (Netherlands)

^d deVGen   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; FUNGI; METAZOA; PROTISTA;

AMINO ACID; ARABIDOPSIS PROTEIN; CASPASE; METACASPASE 9, ARABIDOPSIS; MUTANT PROTEIN; PEPTIDE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP); PROTEOME; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; BIOCATALYSIS; CELL FRACTIONATION; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GLUCONEOGENESIS; METABOLISM; MOLECULAR GENETICS; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; REPRODUCIBILITY; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; AMINO ACIDS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOCATALYSIS; CASPASES; GENE EXPRESSION REGULATION, PLANT; GLUCONEOGENESIS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PEPTIDES; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP); PLANTS, GENETICALLY MODIFIED; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEOLYSIS; PROTEOME; RECOMBINANT PROTEINS; REPRODUCIBILITY OF RESULTS; SUBCELLULAR FRACTIONS; SUBSTRATE SPECIFICITY;

EID: 84884679387     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.115287     Document Type: Article

References (86)

1. Abramoff, M., Magalhães, P., and Ram, S. (2004). Image processing with Image. J. Biophotonics International 11: 36-42.
2. Agard, N.J., Mahrus, S., Trinidad, J.C., Lynn, A., Burlingame, A.L., and Wells, J.A. (2012). Global kinetic analysis of proteolysis via quantitative targeted proteomics. Proc. Natl. Acad. Sci. USA 109: 1913-1918.
3. Ambit, A., Fasel, N., Coombs, G.H., and Mottram, J.C. (2008). An essential role for the Leishmania major metacaspase in cell cycle progression. Cell Death Differ. 15: 113-122.
4. Aravind, L., Dixit, V.M., and Koonin, E.V. (1999). The domains of death: Evolution of the apoptosis machinery. Trends Biochem. Sci. 24: 47-53.
5. Aravind, L., and Koonin, E.V. (2002). Classification of the caspasehemoglobinase fold: Detection of new families and implications for the origin of the eukaryotic separins. Proteins 46: 355-367.
6. Avci, U., Petzold, H.E., Ismail, I.O., Beers, E.P., and Haigler, C.H. (2008). Cysteine proteases XCP1 and XCP2 aid micro-autolysis within the intact central vacuole during xylogenesis in Arabidopsis roots. Plant J. 56: 303-315.
7. 4 photosynthesis. Plant Physiol. 144: 479-486.
8. Belenghi, B., Romero-Puertas, M.C., Vercammen, D., Brackenier, A., Inzé, D., Delledonne, M., and Van Breusegem, F. (2007). Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. J. Biol. Chem. 282: 1352-1358.
9. Bollhöner, B., Zhang, B., Stael, S., Denancé, N., Overmyer, K., Goffner, D., Van Breusegem, F., and Tuominen, H. (July 8, 2013). Post mortem function of AtMC9 in xylem vessel elements. New Phytol. http://dx.doi.org/10.1111/nph.12387.
10. Bonneau, L., Ge, Y., Drury, G.E., and Gallois, P. (2008). What happened to plant caspases? J. Exp. Bot. 59: 491-499.
11. Boucher, V., Buitink, J., Lin, X., Boudet, J., Hoekstra, F.A., Hundertmark, M., Renard, D., and Leprince, O. (2010). MtPM25 is an atypical hydrophobic late embryogenesis-abundant protein that dissociates cold and desiccation-aggregated proteins. Plant Cell Environ. 33: 418-430.
12. Boyes, D.C., Zayed, A.M., Ascenzi, R., McCaskill, A.J., Hoffman, N.E., Davis, K.R., and Görlach, J. (2001). Growth stage-based phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants. Plant Cell 13: 1499-1510.
13. Bozhkov, P.V., Suarez, M.F., Filonova, L.H., Daniel, G., Zamyatnin, A.A., Jr., Rodriguez-Nieto, S., Zhivotovsky, B., and Smertenko, A. (2005). Cysteine protease mcII-Pa executes programmed cell death during plant embryogenesis. Proc. Natl. Acad. Sci. USA 102: 14463-14468.
14. Chahomchuen, T., Akiyama, K., Sekito, T., Sugimoto, N., Okabe, M., Nishimoto, S., Sugahara, T., and Kakinuma, Y. (2009). Tributyltin induces Yca1p-dependent cell death of yeast Saccharomyces cerevisiae. J. Toxicol. Sci. 34: 541-545.
15. Chakrabortee, S., Boschetti, C., Walton, L.J., Sarkar, S., Rubinsztein, D.C., and Tunnacliffe, A. (2007). Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function. Proc. Natl. Acad. Sci. USA 104: 18073-18078.
16. Chatelain, E., Hundertmark, M., Leprince, O., Le Gall, S., Satour, P., Deligny-Penninck, S., Rogniaux, H., and Buitink, J. (2012). Temporal profiling of the heat-stable proteome during late maturation of Medicago truncatula seeds identifies a restricted subset of late embryogenesis abundant proteins associated with longevity. Plant Cell Environ. 35: 1440-1455.
17. Colaert, N., Helsens, K., Martens, L., Vandekerckhove, J., and Gevaert, K. (2009). Improved visualization of protein consensus sequences by iceLogo. Nat. Methods 6: 786-787.
18. Coll, N.S., Epple, P., and Dangl, J.L. (2011). Programmed cell death in the plant immune system. Cell Death Differ. 18: 1247-1256.
19. Coll, N.S., Vercammen, D., Smidler, A., Clover, C., Van Breusegem, F., Dangl, J.L., and Epple, P. (2010). Arabidopsis type I metacaspases control cell death. Science 330: 1393-1397.
20. Crawford, E.D., Seaman, J.E., Barber II, A.E., David, D.C., Babbitt, P.C., Burlingame, A.L., and Wells, J.A. (2012). Conservation of caspase substrates across metazoans suggests hierarchical importance of signaling pathways over specific targets and cleavage site motifs in apoptosis. Cell Death Differ. 19: 2040-2048.
21. Crawford, E.D., and Wells, J.A. (2011). Caspase substrates and cellular remodeling. Annu. Rev. Biochem. 80: 1055-1087.
22. Cumming, G., Fidler, F., and Vaux, D.L. (2007). Error bars in experimental biology. J. Cell Biol. 177: 7-11.
23. Delgado-Alvarado, A., Walker, R.P., and Leegood, R.C. (2007). Phosphoenolpyruvate carboxykinase in developing pea seeds is associated with tissues involved in solute transport and is nitrogenresponsive. Plant Cell Environ. 30: 225-235.
24. Dittrich, P., Campbell, W.H., and Black, C.C., Jr. (1973). Phosphoenolpyruvate carboxykinase in plants exhibiting Crassulacean acid metabolism. Plant Physiol. 52: 357-361.
25. 4-dicarboxylic acid cycle of photosynthesis. Biochem. Biophys. Res. Commun. 45: 278-285.
26. Fuentes-Prior, P., and Salvesen, G.S. (2004). The protein structures that shape caspase activity, specificity, activation and inhibition. Biochem. J. 384: 201-232.
27. Galau, G.A., Bijaisoradat, N., and Hughes, D.W. (1987). Accumulation kinetics of cotton late embryogenesis-abundant mRNAs and storage protein mRNAs: Coordinate regulation during embryogenesis and the role of abscisic acid. Dev. Biol. 123: 198-212.
28. Gevaert, K., Goethals, M., Martens, L., Van Damme, J., Staes, A., Thomas, G.R., and Vandekerckhove, J. (2003). Exploring proteomes and analyzing protein processing by mass spectrometric identification of sorted N-terminal peptides. Nat. Biotechnol. 21: 566-569.
29. González, I.J., Desponds, C., Schaff, C., Mottram, J.C., and Fasel, N. (2007). Leishmania major metacaspase can replace yeast metacaspase in programmed cell death and has arginine-specific cysteine peptidase activity. Int. J. Parasitol. 37: 161-172.
30. Hamann, A., Brust, D., and Osiewacz, H.D. (2007). Deletion of putative apoptosis factors leads to lifespan extension in the fungal ageing model Podospora anserina. Mol. Microbiol. 65: 948-958.
31. Hara-Nishimura, I., and Hatsugai, N. (2011). The role of vacuole in plant cell death. Cell Death Differ. 18: 1298-1304. Erratum. Cell Death Differ. 18: 1950.
32. Helms, M.J., Ambit, A., Appleton, P., Tetley, L., Coombs, G.H., and Mottram, J.C. (2006). Bloodstream form Trypanosoma brucei depend upon multiple metacaspases associated with RAB11-positive endosomes. J. Cell Sci. 119: 1105-1117.
33. Herker, E., Jungwirth, H., Lehmann, K.A., Maldener, C., Fröhlich, K.-U., Wissing, S., Büttner, S., Fehr, M., Sigrist, S., and Madeo, F. (2004). Chronological aging leads to apoptosis in yeast. J. Cell Biol. 164: 501-507.
34. Huesgen, P.F., and Overall, C.M. (2012). N-and C-terminal degradomics: New approaches to reveal biological roles for plant proteases from substrate identification. Physiol. Plant. 145: 5-17.
35. Ivanovska, I., and Hardwick, J.M. (2005). Viruses activate a genetically conserved cell death pathway in a unicellular organism. J. Cell Biol. 170: 391-399.
36. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
37. Laverrière, M., Cazzulo, J.J., and Alvarez, V.E. (2012). Antagonic activities of Trypanosoma cruzi metacaspases affect the balance between cell proliferation, death and differentiation. Cell Death Differ. 19: 1358-1369.
38. Lee, R.E.C., Brunette, S., Puente, L.G., and Megeney, L.A. (2010). Metacaspase Yca1 is required for clearance of insoluble protein aggregates. Proc. Natl. Acad. Sci. USA 107: 13348-13353.
39. Lee, R.E.C., Puente, L.G., Kærn, M., and Megeney, L.A. (2008). A non-death role of the yeast metacaspase: Yca1p alters cell cycle dynamics. PLoS ONE 3: e2956.
40. Leegood, R.C., and Walker, R.P. (2003). Regulation and roles of phosphoenolpyruvate carboxykinase in plants. Arch. Biochem. Biophys. 414: 204-210.
41. Liu, J.-X., Srivastava, R., Che, P., and Howell, S.H. (2007). An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membraneassociated transcription factor, bZIP28. Plant Cell 19: 4111-4119.
42. Madeo, F., Herker, E., Maldener, C., Wissing, S., Lächelt, S., Herlan, M., Fehr, M., Lauber, K., Sigrist, S.J., Wesselborg, S., and Fröhlich, K.-U. (2002). A caspase-related protease regulates apoptosis in yeast. Mol. Cell 9: 911-917.
43. Malone, S., Chen, Z.-H., Bahrami, A.R., Walker, R.P., Gray, J.E., and Leegood, R.C. (2007). Phosphoenolpyruvate carboxykinase in Arabidopsis: Changes in gene expression, protein and activity during vegetative and reproductive development. Plant Cell Physiol. 48: 441-450.
44. Martens, L., Vandekerckhove, J., and Gevaert, K. (2005). DBToolkit: Processing protein databases for peptide-centric proteomics. Bioinformatics 21: 3584-3585.
45. Martín, M., Rius, S.P., andPodestá, F.E. (2011). Two phosphoenolpyruvate carboxykinases coexist in the Crassulacean Acid Metabolism plant Ananas comosus. Isolation and characterization of the smaller 65 kDa form. Plant Physiol. Biochem. 49: 646-653.
46. McLuskey, K., Rudolf, J., Proto, W.R., Isaacs, N.W., Coombs, G.H., Moss, C.X., andMottram, J.C. (2012). Crystal structure of a Trypanosoma brucei metacaspase. Proc. Natl. Acad. Sci. USA 109: 7469-7474.
47. Meng, L., and Feldman, L. (2010). A rapid TRIzol-based two-step method for DNA-free RNA extraction from Arabidopsis siliques and dry seeds. Biotechnol. J. 5: 183-186.
48. Meslin, B., Beavogui, A.H., Fasel, N., and Picot, S. (2011). Plasmodium falciparum metacaspase PfMCA-1 triggers a z-VAD-fmk inhibitable protease to promote cell death. PLoS ONE 6: e23867.
49. Moss, C.X., Westrop, G.D., Juliano, L., Coombs, G.H., and Mottram, J.C. (2007). Metacaspase 2 of Trypanosoma brucei is a calcium-dependent cysteine peptidase active without processing. FEBS Lett. 581: 5635-5639.
50. Ojha, M., Cattaneo, A., Hugh, S., Pawlowski, J., and Cox, J.A. (2010). Structure, expression and function of Allomyces arbuscula CDP II (metacaspase) gene. Gene 457: 25-34.
51. Oliveros, J.C. (2007). VENNY. An Interactive Tool for Comparing Lists with Venn Diagrams. http://bioinfogp.cnb.csic.es/tools/venny/index.html.
52. Overall, C.M., Tam, E.M., Kappelhoff, R., Connor, A., Ewart, T., Morrison, C.J., Puente, X., López-Otín, C., and Seth, A. (2004). Protease degradomics: Mass spectrometry discovery of protease substrates and the CLIP-CHIP, a dedicated DNA microarray of all human proteases and inhibitors. Biol. Chem. 385: 493-504.
53. Patterson, G.H., Knobel, S.M., Sharif, W.D., Kain, S.R., and Piston, D.W. (1997). Use of the green fluorescent protein and its mutants in quantitative fluorescence microscopy. Biophys. J. 73: 2782-2790.
54. Penfield, S., Rylott, E.L., Gilday, A.D., Graham, S., Larson, T.R., and Graham, I.A. (2004). Reserve mobilization in the Arabidopsis endosperm fuels hypocotyl elongation in the dark, is independent of abscisic acid, and requires PHOSPHOENOLPYRUVATE CARBOXYKINASE1. Plant Cell 16: 2705-2718.
55. Pesquet, E. (2012). Plant proteases-From detection to function. Physiol. Plant. 145: 1-4.
56. Proto, W.R., Castanys-Munoz, E., Black, A., Tetley, L., Moss, C.X., Juliano, L., Coombs, G.H., and Mottram, J.C. (2011). Trypanosoma brucei metacaspase 4 is a pseudopeptidase and a virulence factor. J. Biol. Chem. 286: 39914-39925.
57. Rawlings, N.D., and Barrett, A.J. (1993). Evolutionary families of peptidases. Biochem. J. 290: 205-218.
58. Richie, D.L., Miley, M.D., Bhabhra, R., Robson, G.D., Rhodes, J.C., and Askew, D.S. (2007). The Aspergillus fumigatus metacaspases CasA and CasB facilitate growth under conditions of endoplasmic reticulum stress. Mol. Microbiol. 63: 591-604.
59. Rylott, E.L., Gilday, A.D., and Graham, I.A. (2003). The gluconeogenic enzyme phosphoenolpyruvate carboxykinase in Arabidopsis is essential for seedling establishment. Plant Physiol. 131: 1834-1842.
60. Schechter, I., and Berger, A. (1967). On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27: 157-162.
61. Schilling, O., and Overall, C.M. (2008). Proteome-derived, databasesearchable peptide libraries for identifying protease cleavage sites. Nat. Biotechnol. 26: 685-694.
62. Silva, A., Almeida, B., Sampaio-Marques, B., Reis, M.I.R., Ohlmeier, S., Rodrigues, F., do Vale, A., and Ludovico, P. (2011). Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) is a specific substrate of yeast metacaspase. Biochim. Biophys. Acta 1813: 2044-2049.
63. Staes, A., Impens, F., Van Damme, P., Ruttens, B., Goethals, M., Demol, H., Timmerman, E., Vandekerckhove, J., and Gevaert, K. (2011). Selecting protein N-terminal peptides by combined fractional diagonal chromatography. Nat. Protoc. 6: 1130-1141.
64. Sundström, J.F., et al. (2009). Tudor staphylococcal nuclease is an evolutionarily conserved component of the programmed cell death degradome. Nat. Cell Biol. 11: 1347-1354.
65. Timmer, J.C., and Salvesen, G.S. (2007). Caspase substrates. Cell Death Differ. 14: 66-72.
66. Timmer, J.C., Zhu, W., Pop, C., Regan, T., Snipas, S.J., Eroshkin, A.M., Riedl, S.J., and Salvesen, G.S. (2009). Structural and kinetic determinants of protease substrates. Nat. Struct. Mol. Biol. 16: 1101-1108.
67. Tsiatsiani, L., Gevaert, K., and Van Breusegem, F. (2012). Natural substrates of plant proteases: How can protease degradomics extend our knowledge? Physiol. Plant. 145: 28-40.
68. Tsiatsiani, L., Van Breusegem, F., Gallois, P., Zavialov, A., Lam, E., and Bozhkov, P.V. (2011). Metacaspases. Cell Death Differ. 18: 1279-1288.
69. Turk, B., Turk, D., and Turk, V. (2012). Protease signalling: The cutting edge. EMBO J. 31: 1630-1643.
70. Uren, A.G., O'Rourke, K., Aravind, L., Pisabarro, M.T., Seshagiri, S., Koonin, E.V., and Dixit, V.M. (2000). Identification of paracaspases and metacaspases: Two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol. Cell 6: 961-967.
71. Van Damme, P., Martens, L., Van Damme, J., Hugelier, K., Staes, A., Vandekerckhove, J., and Gevaert, K. (2005). Caspase-specific and nonspecific in vivo protein processing during Fas-induced apoptosis. Nat. Methods 2: 771-777.
72. Van Damme, P., Maurer-Stroh, S., Hao, H., Colaert, N., Timmerman, E., Eisenhaber, F., Vandekerckhove, J., and Gevaert, K. (2010). The substrate specificity profile of human granzyme A. Biol. Chem. 391: 983-997.
73. van der Hoorn, R.A.L. (2008). Plant proteases: From phenotypes to molecular mechanisms. Annu. Rev. Plant Biol. 59: 191-223.
74. Vartapetian, A.B., Tuzhikov, A.I., Chichkova, N.V., Taliansky, M., and Wolpert, T.J. (2011). A plant alternative to animal caspases: Subtilisin-like proteases. Cell Death Differ. 18: 1289-1297.
75. Vercammen, D., Belenghi, B., van de Cotte, B., Beunens, T., Gavigan, J.-A., De Rycke, R., Brackenier, A., Inzé, D., Harris, J.L., and Van Breusegem, F. (2006). Serpin1 of Arabidopsis thaliana is a suicide inhibitor for metacaspase 9. J. Mol. Biol. 364: 625-636.
76. Vercammen, D., Declercq, W., Vandenabeele, P., and Van Breusegem, F. (2007). Are metacaspases caspases? J. Cell Biol. 179: 375-380.
77. Vercammen, D., van de Cotte, B., De Jaeger, G., Eeckhout, D., Casteels, P., Vandepoele, K., Vandenberghe, I., Van Beeumen, J., Inzé, D., and Van Breusegem, F. (2004). Type II metacaspases Atmc4 and Atmc9 of Arabidopsis thaliana cleave substrates after arginine and lysine. J. Biol. Chem. 279: 45329-45336.
78. 4 plants: Its role and regulation. Aust. J. Plant Physiol. 24: 459-468.
79. Walker, R.P., Chen, Z.-H., Acheson, R.M., and Leegood, R.C. (2002). Effects of phosphorylation on phosphoenolpyruvate carboxykinase from the C4 plant Guinea grass. Plant Physiol. 128: 165-172.
80. Walker, R.P., and Leegood, R.C. (1995). Purification, and phosphorylation in vivo and in vitro, of phosphoenolpyruvate carboxykinase from cucumber cotyledons. FEBS Lett. 362: 70-74.
81. Walker, R.P., Trevanion, S.J., and Leegood, R.C. (1995). Phosphoenolpyruvate carboxykinase from higher plants: Purification from cucumber and evidence of rapid proteolytic cleavage in extracts from a range of plant tissues. Planta 196: 58-63.
82. Ward, W.W. (1981). Properties of the coelenterate green-fluorescent proteins. In Bioluminescence and Chemiluminescence: Basic Chemistry and Analytical Applications, M.A. DeLuca and W.D. McElroy, eds (New York: Academic Press), pp. 235-242.
83. Watanabe, N., and Lam, E. (2005). Two Arabidopsis metacaspases AtMCP1b and AtMCP2b are arginine/lysine-specific cysteine proteases and activate apoptosis-like cell death in yeast. J. Biol. Chem. 280: 14691-14699.
84. Watanabe, N., and Lam, E. (2011a). Arabidopsis metacaspase 2d is a positive mediator of cell death induced during biotic and abiotic stresses. Plant J. 66: 969-982.
85. Watanabe, N., and Lam, E. (2011b). Calcium-dependent activation and autolysis of Arabidopsis metacaspase 2d. J. Biol. Chem. 286: 10027-10040.
86. Zalila, H., González, I.J., El-Fadili, A.K., Delgado, M.B., Desponds, C., Schaff, C., and Fasel, N. (2011). Processing of metacaspase into a cytoplasmic catalytic domain mediating cell death in Leishmania major. Mol. Microbiol. 79: 222-239.