The intermembrane space of plant mitochondria contains a DNase activity that may be involved in programmed cell death

Plant Journal

Volumn 34, Issue 5, 2003, Pages 573-583

  Balk, Janneke ^a,b   Chew, Su Kit ^a   Leaver, Christopher J ^a   McCabe, Paul F ^a,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

AIF; Apoptosis; Cytochrome c; DNA laddering; Endonuclease; Mitochondria

Indexed keywords

BIOCHEMISTRY; CELLS; DNA;

INTERMEMBRANES;

PLANTS (BOTANY);

APOPTOSIS; ARABIDOPSIS; CELL EXTRACTS; CELL NUCLEUS; DEOXYRIBONUCLEASES; DNA; DNA FRAGMENTATION; HEAT; MITOCHONDRIA; MOLECULAR SEQUENCE DATA;

ANIMALIA; ARABIDOPSIS; EMBRYOPHYTA; MAMMALIA;

EID: 0038129757     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2003.01748.x     Document Type: Article

References (57)

1. Arnoult, D., Tatischeff, I., Estaquier, J. et al. (2001) On the evolutionary conservation of the cell death pathway: mitochondrial release of an apoptosis-inducing factor during Dictyostelium discoideum cell death. Mol. Biol. Cell, 12, 3016-3030.
2. Arpagaus, S., Rawyler, A. and Braendle, R. (2002) Occurrence and characteristics of the mitochondrial permeability transition in plants. J. Biol. Chem. 277, 1780-1787.
3. Balk, J. and Leaver, C.J. (2001) The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell, 13, 1803-1818.
4. Balk, J., Leaver, C.J. and McCabe, P.F. (1999) Translocation of cytochrome c from mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants. FEBS Lett. 463, 151-154.
5. Bartfai, T. (1979) Preparation of metal-chelate complexes and the design of steady-state kinetic experiments involving metal nucleotide complexes. Adv. Cyclic Nucleotide Res. 10, 219-242.
6. Beers, E.P., Woffenden, B.J. and Zhao, C. (2000) Plant proteolytic enzymes: possible roles during programmed cell death. Plant Mol. Biol. 44, 399-415.
7. Bouchier-Hayes, L. and Martin, S.J. (2002) CARD games in apoptosis and immunity. EMBO Rep. 3, 616-621.
8. Diano, M. and Martinez, G. (1971) Le cytochrome c des mitochondries du tubercule de pomme de terre. C.R. Acad. Sci. Paris, 272, 2692-2694.
9. Ellerby, H.M., Martin, S.J., Ellerby, L.M., Naiem, S.S., Rabizadeh, S., Salvesen, G.S., Casiano, C.A., Cashman, N.R., Green, D.R. and Bredesen, D.E. (1997) Establishment of a cell-free system of neuronal apoptosis: comparison of pre-mitochondrial, mitochondrial, and post-mitochondrial phases. J. Neurosci. 17, 6165-6178.
10. Emanuelsson, O., Nielsen, H., Brunak, S. and von Heijne, G. (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005-1016.
11. Filonova, L., Bozhkov, P., Brukhin, V., Daniel, G., Zhivotovsky, B. and 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.
12. Gunawardena, A.H.L.A.N., Pearce, D.M., Jackson, M.B., Hawes, C.R. and Evans, D.E. (2001) Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta, 212, 205-214.
13. Hicks, G.R. and Raikhel, N.V. (1995) Protein import into the nucleus: an integrated view. Annu. Rev. Cell Dev. Biol. 11, 155-188.
14. Hossain, M.A. and Asada, K. (1985) Monodehydroascorbate reductase from cucumber is a flavin adenine dinucleotide enzyme. J. Biol. Chem. 260, 12920-12926.
15. Houot, V., Etienne, P., Petitot, A.-S., Barbier, S., Blein, J.P. and Suty, L. (2001) Hydrogen peroxide induces programmed cell death features in cultured tobacco BY-2 cells, in a dose-dependent manner. J. Exp. Bot. 52, 1721-1730.
16. Jiménez, A., Hernández, J.A., del Río, L.A. and Sevilla, F. (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol. 114, 275-284.
17. Jones, A. (2000) Does the plant mitochondrion integrate cellular stress and regulate programmed cell death? Trends Plant Sci. 5, 225-230.
18. Kluck, R.M., Ellerby, L.M., Ellerby, H.M., Naiem, S., Yaffe, M.P., Margoliash, E., Bredesen, D., Mauk, A.G., Sherman, F. and Newmeyer, D.D. (2000) Determinants of cytochrome c pro-apoptotic activity. The role of lysine 72 trimethylation. J. Biol. Chem. 275, 16127-16133.
19. Lam, E. and del Pozo, O. (2000) Caspase-like protease involvement in the control of plant cell death. Plant Mol. Biol. 44, 417-428.
20. Levine, A., Pennell, R.I., Alvarez, M.E., Palmer, R. and Lamb, C. (1996) Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr. Biol. 6, 427-437.
21. Li, L.Y., Luo, X. and Wang, X. (2001) Endonuclease G is an apoptotic DNase when released from mitochondria. Nature, 412, 95-99.
22. Liu, X., Kim, C.N., Yang, J., Jemmerson, R. and Wang, X. (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell, 86, 147-157.
23. Lorenzo, H.K., Susin, S.A. and Kroemer, G. (2000) Cytofluorometric quantification of nuclear apoptosis induced in a cell-free system. Meth. Enzymol. 322, 198-201.
24. Lorenzo, H.K., Susin, S.A., Penninger, J. and Kroemer, G. (1999) Apoptosis-inducing factor (AIF): a phylogenetically old, caspase-independent effector of cell death. Cell Death Diff. 6, 516-524.
25. Madeo, F., Herker, E., Maldener, C. et al. (2002) A caspase-related protease regulates apoptosis in yeast. Mol. Cell, 9, 911-917.
26. Martin, S.J., Newmeyer, D.D., Mathias, S., Farschon, D.M., Wang, H.-G., Reed, J.C., Kolesnick, R.N. and Green, D.R. (1995) Cell-free reconstitution of Fas-, UV radiation- and ceramide-induced apoptosis. EMBO J. 14, 5191-5200.
27. May, M.J. and Leaver, C.J. (1993) Oxidative stimulation of glutathione synthesis in Arabidopsis thaliana suspension cultures. Plant Physiol. 103, 621-627.
28. McCabe, P.F., Levine, A., Meijer, P.-J., Tapon, N.A. and Pennell, R.I. (1997) A programmed cell death pathway activated in carrot cells cultured at low cell density. Plant J. 12, 267-280.
29. Millar, A.H., Sweetlove, L.J., Giegé, P. and Leaver, C.J. (2001) Analysis of the Arabidopsis mitochondrial proteome. Plant Physiol. 127, 1711-1727.
30. Miramar, M.D., Costantini, P., Ravagnan, L., Saraiva, L.M., Haouzi, D., Brothers, G., Penninger, J.M., Peleato, M.L., Kroemer, G. and Susin, S.A. (2001) NADH-oxidase activity of mitochondrial apoptosis-inducing factor (AIF). J. Biol. Chem. 276, 16391-16398.
31. Mittler, R., Simon, L. and Lam, E. (1997) Pathogen-induced programmed cell death in tobacco. J. Cell Sci. 110, 1333-1344.
32. Newmeyer, D.D., Farschon, D.M. and Reed, J.C. (1994) Cell-free apoptosis in Xenopus egg extracts - inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell, 79, 353-364.
33. Newmeyer, D.D. and Wilson, K.L. (1991) Egg extracts for nuclear import and nuclear assembly reactions. Meth. Cell Biol. 36, 607-634.
34. O'Brien, I.E.W., Baguley, B.C., Murray, B.G., Morris, B.A.M. and Ferguson, I.B. (1998) Early stages of the apoptotic pathway in plant cells are reversible. Plant J. 13, 803-814.
35. Parrish, J., Li, L., Klotz, K., Ledwich, D., Wang, X. and Xue, D. (2001) Mitochondrial endonuclease G is important for apoptosis in C. elegans. Nature, 412, 90-94.
36. Polevoda, B., Martzen, M.R., Das, B., Phizicky, E.M. and Sherman, F. (2000) Cytochrome c methyltransferase, Ctm1p, of yeast. J. Biol. Chem. 275, 20508-20513.
37. Sano, S., Miyake, C., Mikami, B. and Asada, K. (1995) Molecular characterization of monodehydroascorbate radical reductase from cucumber highly expressed in Escherichia coli. J. Biol. Chem. 270, 21354-21361.
38. Slee, E.A., Harte, M.T., Kluck, R.M. et al. (1999) Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J. Cell Biol. 144, 281-292.
39. Stein, J.C. and Hansen, G. (1999) Mannose induces an endonuclease responsible for DNA laddering in plant cells. Plant Physiol. 121, 71-79.
40. Sugiyama, M., Ito, J., Aoyagi, S. and Fukuda, H. (2000) Endonucleases. Plant Mol. Biol. 44, 387-397.
41. Sun, Y.-L., Zhao, Y., Hong, X. and Zhai, Z.-H. (1999) Cytochrome c release and caspase activation during menadione-induced apoptosis in plants. FEBS Lett. 462, 317-321.
42. Susin, S.A., Daugas, E., Ravagnan, L. et al. (2000) Two distinct pathways leading to nuclear apoptosis. J. Exp. Med. 192, 571-579.
43. Susin, S.A., Lorenzo, H.K., Zamzami, N. et al. (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature, 397, 441-446.
44. Susin, S.A., Zamzami, N., Castedo, M., Hirsch, T., Marchetti, P., Macho, A., Daugas, E., Geuskens, M. and Kroemer, G. (1996) Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J. Exp. Med. 184, 1331-1341.
45. Swidzinski, J.A., Sweetlove, L.J. and Leaver, C.J. (2002) A custom microarray analysis of gene expression during programmed cell death in Arabidopsis thaliana. Plant J. 30, 431-446.
46. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796-815.
47. 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.
48. Van der Biezen, E.A. and Jones, J.D.G. (1998) The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr. Biol. 8, R226-R227.
49. Vincent, R.D., Hofmann, T.J. and Zassenhaus, H.P. (1988) Sequence and expression of NUC1, the gene encoding the mitochondrial nuclease in Saccharomyces cerevisiae. Nucl. Acids Res. 16, 3297-3312.
50. Wang, X. (2001) The expanding role of mitochondria in apoptosis. Genes Dev. 15, 2922-2933.
51. Wang, H., Li, J., Bostock, R.M. and Gilchrist, D.G. (1996) Apoptosis: a functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell, 8, 375-391.
52. Wang, X., Yang, C., Chai, J., Shi, Y. and Xue, D. (2002) Mechanisms of AIF-mediated apoptotic DNA degradation in Caenorhabditis elegans. Science, 298, 1587-1592.
53. Wu, M., Xu, L.-G., Li, X., Zhai, Z. and Shu, H.B. (2002) AMID, an AIF homologous mitochondrion-associated protein, induces caspase-independent apoptosis. J. Biol. Chem. 277, 25617-25623.
54. Yarmolinsky, M.B. (1995) Programmed cell death in bacterial populations. Science, 267, 836-837.
55. Yu, X.-H., Perdue, T.D., Heimer, Y.M. and Jones, A.M. (2002) Mitochondrial involvement in tracheary element programmed cell death. Cell Death Diff. 9, 189-198.
56. Yu, T., Wang, X., Purring-Koch, C., Wei, Y. and McLendon, G.L. (2001) A mutational epitope for cytochrome c binding to the apoptosis protease activation factor-1. J. Biol. Chem. 276, 13034-13038.
57. Zhao, Y., Jiang, Z.-F., Sun, Y.-L. and Zhai, Z.-H. (1999) Apoptosis of mouse liver nuclei induced in the cytosol of carrot cells. FEBS Lett. 448, 197-200.