Death by proteases in plants: Whodunit

Physiologia Plantarum

Volumn 123, Issue 4, 2005, Pages 376-385

  Rotari, Vitalie I ^a   He, Rui ^a   Gallois, Patrick ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; ENZYME INHIBITION; ENZYMES; GENES; PLANT CELL CULTURE; TISSUE;

CASPASE INHIBITORS; CELL DEATH; PLANT GENOMES; PROTEASES;

PLANTS (BOTANY);

ANIMALIA;

EID: 17444416726     PISSN: 00319317     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1399-3054.2005.00465.x     Document Type: Review

References (77)

1. Aravind L, Koonin EV (2002) Classification of the caspase-hemoglobinase fold: detection of new families and implications for the origin of the eukaryotic separins. Proteins 46: 355-367
2. Baehrecke EH (2002) How death shapes life during development. Nat Rev Mol Cell Biol 3: 779-787
3. Beers EP, Freeman TB (1997) Proteinase activity during tracheary element differentiation in Zinnia mesophyl cultures. Plant Physiol 113: 873-880
4. Beers EP, McDowell JM (2001) Regulation and execution of programmed cell death in response to pathogens, stress and developmental cues. Curr Opin Plant Biol 4: 561-567
5. Beers EP, Woffenden BJ, Zhao C (2000) Plant proteolytic enzymes: possible roles during programmed cell death. Plant Mol Biol 44: 399-415
6. Belenghi B, Acconcia F, Trovato M, Perazzolli M, Bocedi A, Polticelli F, Ascenzi P, Delledonne M (2003) AtCYS1, a cystatin from Arabidopsis thaliana, suppresses hypersensitive cell death. Eur J Biochem 270: 2593-2604.
7. Belenghi B, Salomon M, Levine A (2004) Caspase-like activity in the seedlings of Pisum sativum eliminates weaker shoots during early vegetative development by induction of cell death. J Exp Bot 55: 889-897
8. Bozhkov PV, Filonova LH, Suarez MF, Helmersson A, Smertenko AP, Zhivotovsky B, Von Arnold S (2004) VEIDase is a principal caspase-like activity involved in plant programmed cell death and essential for embryonic pattern formation. Cell Death Diff 11: 175-182
9. Chen J-M, Rawlings ND, Stevens RAE, Barrett AJ (1998) Identification of the active site of legumain links it to caspases, clostripain and gingipains in a new clan of cysteine endopeptidases. FEBS Lett 441: 361-365
10. Chichkova NV, Kim SH, Titova ES, Kalkum M, Morozov VS, Rubtsov YP, Kalinina NO, Taliansky ME, Vartapetian AB (2004) A plant caspase-like protease activated during the hypersensitive response. Plant Cell 16: 157-171
11. Clarke A, Desikan R, Hurst RD, Hancock JT, Neill SJ (2000) NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. Plant J 24: 667-677
12. Coffeen WC, Wolpert TJ (2004) Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell 16: 857-873
13. Danon A, Delorme V, Mailhac N, Gallois P (2000) Plant programmed cell death: a common way to die. Plant Physiol Biochem 38: 647-655
14. Danon A, Rotari VI, Gordon A, Mailhac M, Gallois P (2004) Ultraviolet-C overexposure induces programmed cell death in Arabidopsis, which is mediated by caspase-like activities and which can be suppressed by caspase inhibitors, p35 and Defender against Apoptotic Death. J Biol Chem 279: 779-787
15. De Jong AJ, Hoeberichts FA, Yakimova ET, Maximova E, Woltering EJ (2000) Chemical-induced apoptotic cell death in tomato cells: involvement of caspase-like proteases. Planta 211: 656-662
16. Dietrich RA, Richberg MH, Schmidt R, Dean C, Dangl JL (1997) A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell 88: 685-694
17. Doucet-Chabeaud G, Godon C, Brutesco C, de Murcia G, Kazmaier M (2001) Ionising radiation induces the expression of PARP-1 and PARP-2 genes in Arabidopsis. Mol Genet Genomics 265: 954-963
18. Eichinger A, Beisel HG, Jacob U, Huber R, Medrano FJ, Banbula A, Potempa J, Travis J, Bode W (1999) Crystal structure of gingipain R: an Arg-specific bacterial cysteine proteinase with a caspase-like fold. EMBO J 18: 5453-5462
19. Elbaz M, Avni A, Weil M (2002) Constitutive caspase-like machinery executes programmed cell death in plant cells. Cell Death Diff 9: 726-733
20. Faleiro L, Kobayashi R, Fearnhead H, Lazebnik Y (1997) Multiple species of CPP32 and Mch2 are the major active caspases present in apoptotic cells. EMBO J 16: 2271-2281
21. Filonova LH, Bozhkov PV, Brukhin VB, Daniel G, Zhivotovsky B, von Arnold S (2000) Two waves of programmed cell death occur during formation and development of somatic embryos in the gymnosperm, Norway spruce. J Cell Sci 113: 4399-4411
22. Froelich CJ, Metkar SS, Raja SM (2004) Granzyme B-mediated apoptosis - the elephant and the blind men? Cell Death Diff 11: 369-371
23. Garcia-Calvo M, Peterson EP, Leiting B, Ruel R, Nicholson DW, Thornberry NA (1998) Inhibition of human caspases by peptide-based and macromolecular inhibitors. J Biol Chem 273: 32608-32613
24. Granell A, Cercós M, Carbonell J (1998) Plant cysteine proteinases in germination and senescence. In: Barrett AJ, Rawlings ND, Woessner JF (eds) Handbook of Proteolytic Enzymes. Academic Press, London, pp 578-583
25. Groover A, Jones AM (1999) Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiol 119: 375-384
26. Hamilton JMU, Simpson DJ, Hyman SC, Ndimba BK, Slabas AR (2003) Ara12 subtilisin-like protease from Arabidopsis thaliana: purification, substrate specificity and tissue localisation. Biochem J 370: 57-67
27. Hansen G (2000) Evidence for Agrobacterium-induced apoptosis in maize cells. Mol Plant-Microbe Interact 13: 649-657
28. Hara-Nishimura I (1998) Asparaginyl endopeptidase. In: Barrett AJ, Rawlings ND, Woessner JF (eds) Handbook of Proteolytic Enzymes. Academic Press, London, pp 746-749
29. Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S, Kondo M, Nishimura M, Hara-Nishimura I (2004) A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305: 855-858
30. Hayashi Y, Yamada Shimada T, Matsushima R, Nishizawa NK, Nishimura M, Hara-Nishimura I (2001) A proteinase-storing body that prepares for cell death or stresses in the epidermal cells of Arabidopsis. Plant Cell Physiol 42: 894-899
31. He X, Kermode AR (2003) Proteases associated with programmed cell death of megagametophyte cells after germination of white spruce (Picea glauca) Seeds Plant Mol Biol 52: 729-744
32. Hoeberichts FA, ten Have A, Woltering EJ (2003) A tomato metacaspase gene is upregulated during programmed cell death in Botrytis cinerea-infected leaves. Planta 217: 517-522
33. Hoeberichts FA, Woltering EJ (2002) Multiple mediators of plant programmed cell death: interplay of conserved cell death mechanisms and plant-specific regulators. Bioessays 25: 47-57
34. Jones AM (2001) Programmed Cell Death in development and defence. Plant Physiol 125: 94-97
35. Kim M, Ahn J-W, Jin U-H, Choi D, Paek K-H, Pai H-S (2003) Activation of the programmed cell death pathway by inhibition of proteasome function in plants. J Biol Chem 278: 19406-19415
36. Kinoshita T, Yamada K, Hiraiwa N, Kondo M, Nishimura M, Hara-Nishimura I (1999) Vacuolar processing enzyme is up-regulated n the lytic vacuoles of vegetative tissues during senescence and under various stress conditions. Plant J 19: 43-53
37. Kisselev AF, Garcia-Calvo, Overkleeft HS, Peterson E. Pennington MW, Ploegh HL, Thornberry NA, Goldberg AL (2003) The caspase-like sites of proteasome, their substrate specificity, new inhibitors and substrates, and allosteric interactions with the trypsin-like sites. J Biol Chem 278: 35869-35877
38. Koonin E, V, Aravind L (2002) Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Diff 9: 394-404
39. Korthout H, Berecki G, Bruin W, van Duijn B, Wang M (2000) The presence and subcellular localization of caspase 3-like proteinases in plant cells. FEBS Lett 475: 139-144
40. Kuriyama H, Fukuda H (2002) Developmental programmed cell death in plants. Curr Opin Plant Biol 5: 568-573
41. Lincoln JE, Richael C, Overduin B, Smith K, Bostock R, Gilchrist DG (2002) Expression of the antiapoptotic baculovirus p35 gene in tomato blocks programmed cell death and provide broad-spectrum resistance to disease. Proc Natl Acad Sci USA 99: 15217-15221
42. Lockshin RA, Zakeri Z (2004) Caspase-independent cell death? Oncogene 23: 2766-2773
43. Lopez-Otin C, Overall CM (2002) Protease degradomics: a new challenge for proteomics. Nat Rev Mol Cell Biol 3: 509-519
44. Madeo F, Herker E, Maldener C, Wissing S, Lächelt S, Herlan M, Fehr M, Lauber K, Sigrist SJ, Wesselborg S, Fröhlich K-U (2002) A caspase-related protease regulates apoptosis in yeast. Mol Cell 9: 911-917
45. Martins LM, Kottke T, Mesner PW, Basi GS, Sinha S, Frigon NJ, Tatar E, Tung JS, Bryant K, Takahashi A, Svingen PA, Madden BJ, McCormick DJ, Earnshaw WC, Kaufmann SH (1997) Activation of multiple interleukin-1 converting enzyme homologues in cytosol and nuclei of HL-60 cells during etoposide-induced apoptosis. J Biol Chem 272: 7421-7430
46. Matile P (1978) Biochemistry and function of vacuoles. Ann Rev Plant Physiol 29: 193-213
47. Meichtry J, Amrhein N, Schaller A (1999) Characterization of the subtilase gene family in tomato (Lycopersicon esculentum Mill.). Plant Mol Biol 39: 749-760
48. Minami A, Fukuda H (1995) Transient and specific expression of a cysteine endopeptidase associated with autolysis during differentiation of Zinnia mesophyll cells into tracheary elements. Plant Cell Physiol 36: 1599-1606
49. Mlejnek P, Procházka S (2002) Activation of caspase-like proteases and induction of apoptosis by isopentenyladenosine tobacco BY-2 cells. Planta 215: 158-166
50. Müntz K, Shutov AD (2002) Legumains and their functions in plants. Trends Plant Sci 7: 340-344
51. Nicholson DW (1999) Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Diff 6: 1028-1042
52. Orlowski RZ (1999) The role of the ubiquitin-proteasome pathway in apoptosis. Cell Death Diff 6: 303-313
53. Pennell RI, Lamb C (1997) Programmed cell death in plants. Plant Cell 9: 1157-1168
54. del Pozo O, Lam E (1998) Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr Biol 8: 1129-1132
55. del Pozo O, Lam E (2003) Expression of the baculovirus p35 protein in tobacco affects cell death progression and compromise N gene-mediated disease resistance response to Tobacco mosaic virus. Mol Plant-Microbe Interact 16: 485-494
56. Rotari VI, Dando PM, Barrett AJ (2001) Legumain forms from plants and animals differ in their specificity. Biol Chem 382: 953-959
57. Schmid M, Simpson D, Gietl C (1999) Programmed cell death in castor bean endosperm is associated with the accumulation and release of a cysteine endopeptidase from ricinosomes. Proc Natl Acad Sci USA 96: 14159-14164
58. Snipas SJ, Stennicke HR, Riedl S, Potempa J, Travis J, Barrett AJ, Salvesen GS (2001) Inhibition of distant caspase homologues by natural caspase inhibitors. Biochem J 357: 575-580
59. Solomon M, Belenghi B, Delledonne M, Menachem E, Levine A (1999) The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11: 431-443
60. Stennicke HR, Salvesen GS (1997) Biochemical characteristics of caspases-3-6-7, and -8. J Biol Chem 272: 25719-25723
61. Suarez MF, Filonova LH, Smertenko A, Savenkov EI, Clapham DH, von Arnold S, Zhivotovsky B, Bozhkov PV (2004) Metacaspase-dependent programmed cell death is essential for plant embryogenesis. Curr Biol 14: R339-R340
62. Sun Y-L, Zhao Y, Hong X, Zhai Z-H (1999) Cytocrome c release and caspase activation during menadion-induced apoptosis in plants. FEBS Lett 462: 317-321
63. Thomas SG, Franklin-Tong VE (2004) Self-incompatibility triggers programmed cell death in Papaver pollen. Nature 429: 305-309
64. Thornberry NA (1998) Caspases: key mediators of apoptosis. Chem Biol 5: R97-R103
65. Thornberry NA, Rano TA, Peterson EP, Rasper DM, Timkey T, Garcia-Calvo M, Houtzager VM, Nordstrom PA, Roy S, Vaillancourt JP, Chapman KT, Nicholson DW (1997) A combinational approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J Biol Chem 272: 17907-17911
66. Tian R-H, Zhang G-Y, Yan C-H, Dai Y-R (2000) Involvement of poly (ADP-ribose) polymerase and activation of caspase-3-like protease in heat shock-induced apoptosis in tobacco suspension cells, FEBS Lett 474: 11-15
67. Turk B, Stoka V, Rozman-Pungercar J, Cirman T. Droga-Mazovec G, Ore?ic K, Turk V (2002) Apoptotic pathways: involvement of lysosomal protease. Biol Chem 383: 1035-1044
68. Uren AG, O'Rourke K, Aravind L, Pisabarro MT, Seshagiri S, Koonin EV, Dixit VM (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
69. Vercammen D, Van De Cotte B, De Jaeger G, Eeckhout D, Casteels P, Vandepoele K, Vandenberghe I, Van Beeumen J, Inze D, Van Breusegem F (2004) Type-II metacaspases Atmc4 and Atmc9 of Arabidopsis thaliana cleave substrates after arginine and lysine. J Biol Chem 279: 45329-36
70. Wan L, Xia Q, Qui X, Selvaraj G (2002) Early stages of seed development in Brassica napus: a seed coat-specific cysteine proteinese associated with programmed cell death of the inner integument. Plant J 30: 1-10
71. Watanabe N, Lam E (2004) Recent advances in the study of caspase-like proteases and Bax inhibitor-1 in plants: their possible roles as regulators of programmed cell death. Mol Plant Path 5: 65-70
72. Woffenden BJ, Freeman TB, Beers EP (1998) Proteasome inhibitors prevent tracheary element differentiation in Zinnia mesophyll cell cultures. Plant Physiol 118: 419-430
73. Wolf BB, Green DR (1999) Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem 274: 20049-20052
74. Woltering EJ (2004) Death proteases come alive. Trends Plant Sci 9: 469-472
75. Woltering EJ, van der Bent A, Hoeberichts FA (2002) Do plant caspases exist? Plant Physiol 130: 1764-1769
76. Ye Z-H, Varner JE (1996) Induction of cysteine and serine proteases during xylogenesis of Zinnia elegans. Plant Mol Biol 30: 1233-1246
77. Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR (1993) The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 75: 641-652