Dissection of Arabidopsis Bax Inhibitor-1 Suppressing Bax-, Hydrogen Peroxide-, and Salicylic Acid-Induced Cell Death

Plant Cell

Volumn 16, Issue 1, 2004, Pages 21-32

  Kawai Yamada, Maki ^a   Ohori, Yuri ^a   Uchimiya, Hirofumi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ANIMAL CELL CULTURE; BIODIVERSITY; HYDROPHILICITY; OXYGEN; YEAST;

CELL DEATH;

PLANT CELL CULTURE;

ANIMALIA; ARABIDOPSIS; EMBRYOPHYTA; MAMMALIA; NICOTIANA TABACUM;

EID: 0842313320     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.014613     Document Type: Article

References (60)

1. Abramovitch, R.B., Kim, Y.J., Chen, S., Dickman, M.B., and Martin, G.B. (2003). Pseudomonas type III effecter AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 22, 60-69.
2. An, G., Ebert, R.R., Mitra, A., and Ha, S.B. (1998). Binary vectors. In Plant Molecular Biology Manual, S.B. Gelvin and R.A. Schilperoort, eds (Dordrecht, The Netherlands: Kluwer Academic Publishers), pp. 1-19.
3. Bischoff, J.R., Casso, D., and Beach, D. (1992). Human p53 inhibits growth in Schizosaccharomyces pombe. Mol. Cell. Biol. 12, 1405-1411.
4. Brisson, L.F., Tenhanken, R., and Kamb, C. (1994). Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6, 1703-1712.
5. Bolduc, N., and Brisson, L.F. (2003). Antisense down regulation of NtBI-1 in tobacco BY-2 cells induces accelerated cell death upon carbon starvation. FEBS Lett. 532, 111-114.
6. Bolduc, N., Ouellet, M., Pitre, F., and Brisson, L.F. (2003). Molecular characterization of two plant BI-1 homologues which suppress Bax-induced apoptosis in human 293 cells. Planta 216, 377-386.
7. Chamnongpol, S., Wlllekens, H., Langebartels, C., van Montagu, M., Inze, D., and van Camp, W. (1996). Transgenic tobacco with a reduced catalase activity develops necrotic lesions and induces pathogenesis-related expression under high light. Plant J., 10, 491-503.
8. Chivasa, S., and Carr, J.P. (1998). Cyanide restores N gene-mediated resistance to tobacco mosaic virus in transgenic tobacco expressing salicylic hydroxylase. Plant Cell 10, 1489-1498.
9. Delaney, T.P., Uknes, S., Vernooji, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffne, T., Gu-Rella, M., Kessmann, H., Ward, E., and Ryals, J. (1994). A central role of salicylic acid in plant disease resistance. Science 266, 1247-1250.
10. Desikan, R., Reynolds, A., Hancock, J.T., and Neill, S.J. (1998). Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on defense gene expression in Arabidopsis suspension cultures. Biochem. J. 330, 115-120.
11. Dixon, R.A., Harrison, M.J., and Lamb, C.J. (1994). Early events in the activation of plant defense responses. Annu. Rev. Phytopathol. 32, 479-501.
12. Draper, J. (1997). Salicylate, superoxide synthesis and cell suicide in plant defense. Trends Plant Sci. 2, 162-165.
13. Fauth, M., Merten, A., Hahn, M.G., Jeblick, E., and Kauss, H. (1996). Competence for elicitation of hydrogen peroxide in hypocotyls of cucumber is induced by breaching the cuticle and is enhanced by salicylic acid. Plant Physiol. 110, 347-354.
14. Green, D.R., and Reed, J.C. (1998). Mitochondria and apoptosis. Science 281, 1309-1312.
15. Greenhalf, W., Steohan, C., and Chaudhuri, B. (1996). Role of mitochondria and C-terminal membrane anchor of Bcl-2 in Bax induced growth arrest and mortality in Saccharomyces cerevisiae. FEBS Lett. 380, 169-175.
16. Hanada, M., Aimé-Sempé, C., Sato, T., and Reed, J.C. (1995). Structure-function analysis of Bcl-2 protein: Identification of conserved domains important for homodimerization with Bcl-2 and heterodimerization with Bax. J. Biol. Chem. 270, 11962-11968.
17. Hengartner, M., and Horvitz, H.R. (1994). C. elegans cell survival gene ced-9 encodes a functional homologue of the mammalian protooncogene bcl-2. Cell 76, 665-676.
18. Hernandez, J.A., Corpas, F.J., Gomez, M., Del Rio, L.A., and Sevilla, F. (1993). Salt-induced oxidative stress mediated by activated oxygen species in pea leaf mitochondria. Physiol. Plant. 89, 103-110.
19. Hood, E.E., Gelvin, S.B., Melchers, L.S., and Hoekema, A. (1993). New Agrobacterium vector for plant transformation. Transgenic Res. 2, 208-218.
20. 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.
21. Hückelhoven, R., Dechert, C., and Kogel, K.H. (2003). Overexpression of barley BAX inhibitor 1 induces breakdown of Mlo-mediated penetration resistance to Blumeria graminis. Proc. Natl. Acad. Sci. USA 100, 5550-5560.
22. Hückelhoven, R., Dechert, C., Trujillo, M., and Kogel, K.H. (2001). Differential expression of putative cell death regulator genes in near-isogenic, resistant and susceptible barley lines during interaction with the powdery mildew fungus. Plant Mol. Biol. 47, 739-748.
23. Kauss, H., Jeblick, W., Zielger, J., and Kraber, W. (1994). Pretreatment of parsley (Petroselinum crispum L.) suspension culture with methyl jasmonate enhances the elicitation of active oxygen species. Plant Physiol. 105, 89-94.
24. Kawai, M., Pan, L., Reed, J.C., and Uchimiya, H. (1999). Evolutionally conserved plant homologue of the Bax inhibitor-1 (BI-1) gene capable of suppressing Bax-induced cell death in yeast. FEBS Lett. 464, 143-147.
25. Kawai, M., Samarajeewa, P.K., Barrero, R.A., Nishiguchi, M., and Uchimiya, H. (1998). Cellular dissection of the degradation pattern of cortical cell death during aerenchyma formation of rice roots. Planta 204, 277-287.
26. Kawai, M., and Uchimiya, H. (2000). Coleoptile senescence in rice (Oryza sativa L.). Ann. Bot. 86, 405-414.
27. Kawai-Yamada, M., Jin, L., Yoshinaga, K., Hirata, A., and Uchimiya, H. (2001). Mammalian Bax-induced plant cell death can be down-regulated by overexpression of Arabidopsis Bax Inhibitor-1 (AtBI-1). Proc. Natl. Acad. Sci. USA 98, 12295-12300.
28. Kroemer, G. (1997). The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat. Med. 3, 614-620.
29. Lacomme, C., and Cruz, S.S. (1999). Bax-induced cell death in tobacco is similar to the hypersensitive response. Proc. Natl. Acad. Sci. USA 96, 7956-7961.
30. Lam, E., Kato, N., and Lawton, M. (2001). Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411, 848-853.
31. Lamb, C., and Dixon, R.A. (1997). The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 251-275.
32. 2 stimulates salicylic acid biosynthesis in tobacco. Plant Physiol. 108, 1673-1678.
33. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79, 583-593.
34. Linsmaier, E.M., and Skoog, F. (1965). Organic growth factor requirements of tobacco tissue cultures. Physiol. Plant 18, 100-127.
35. Madeo, F., Fröhlich, E., Ligr, M., Grey, M., Sigrist, S.J., Wolf, D.H., and Fröhlich, K.U. (1999). Oxygen stress: A regulator of apoptosis in yeast. J. Cell Biol. 145, 757-767.
36. 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.
37. Manon, S., Chaudhuri, B., and Bueerin, M. (1997). Release of cytochrome c and decrease of cytochrome c oxidase in Bax expressing yeast cells, and prevention of these effects by coexpression of Bcl-XL. FEBS Lett. 415, 29-32.
38. Matsumura, H., Nirasawa, S., Kiba, A., Urasaki, N., Saitoh, H., Ito, M., Kawai-Yamada, M., Uchimiya, H., and Terauchi, R. (2003). Overexpression of Bax inhibitor suppresses the fungal elicitor-induced cell death in rice (Oryza sativa L.) cells. Plant J. 33, 425-434.
39. Maxwell, D.P., Nickels, R., and McIntosh, L. (2002). Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. Plant J. 29, 269-279.
40. Mitsuhara, I., Malik, K.A., Miura, M., and Ohashi, Y. (1999). Animal cell-death suppressors Bcl-x(L) and Ced-9 inhibit cell death in tobacco plants. Curr. Biol. 9, 775-778.
41. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405-410.
42. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant 15, 473-497.
43. Nagata, T., Nemoto, Y., and Hasezawa, S. (1992). Tobacco BY2 cell line as the "HeLa" cell line in the cell biology of higher plants. Int. Rev. Cytol. 132, 1-30.
44. Niwa, Y., Hirano, T., Yoshimoto, K., Shimizu, M., and Kobayashi, H. (1999). Non-invasive quantitative detection and applications of non-toxic, S65T-type green fluorescent protein in living plants. Plant J. 18, 455-463.
45. Prasad, T.K., Anderson, M.D., Martin, B.A., and Stewart, C.R. (1994). Evidence for chilling-induced oxidative stress in maize and a regulatory role for hydrogen peroxide. Plant Cell 6, 65-74.
46. Rao, M.Y., and Davis, K.R. (1999). Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: The role of salicylic acid. Plant J. 17, 603-614.
47. Reed, J.C. (1994). Bcl2 and the regulation of programmed cell death. J. Cell Biol. 124, 1-6.
48. Rizhsky, L., Hallak-Herr, E., Van Breusegem, F., Rachmilevitch, S., Barr, J.E., Rodermel, S., Inze, D., and Mittler, R. (2002). Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J. 32, 329-342.
49. Sanchez, P., de Torres-Zabala, M., and Grant, M. (2000). AtBI-1, a plant homologue of Bax inhibitor-1, suppresses Bax-induced cell death in yeast and is rapidly up regulated during wounding and pathogen challenge. Plant J. 21, 393-399.
50. Sato, R., Hanada, M., Bodrug, S., Irie, S., Iwama, N., Boise, L.H., Thompson, C.B., Golernis, E., Fong, L., Wang, H.G., and Reed, J.C. (1994). Interactions among members of the bcl-2 protein family analyzed with a yeast two-hybrid system. Proc. Natl. Acad. Sci. USA 91, 9238-9242.
51. Shaul, O., Nironov, V., Burssens, S., Montague, M.V., and Inze, D. (1996). Two Arabidopsis cyclin promoters mediate distinctive transcriptional oscillation in synchronized tobacco BY-2 cells. Proc. Natl. Acad. Sci. USA 93, 4868-4872.
52. Shirasu, K., Nakajima, H., Rajashekar, K., Dixon, R.A., and Lamb, C. (1997). Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9, 261-270.
53. Solomon, M., Belenghi, B., Delledonne, M., and Levine, A. (1999). The involvement of cysteine proteases and protease inhibitor genes in programmed cell death in plants. Plant Cell 11, 431-444.
54. Summermatter, K., Sticher, L., and Metraux, J.P. (1995). Systemic response in Arabidopsis thaliana infected and challenged with Pseudomonas syringae pv. syringae. Plant Physiol. 108, 1379-1385.
55. Tiwari, B.S., Belenghi, B., and Levine, A. (2002). Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol. 128, 1271-1281.
56. Varner, J.E., and Lin, L.S. (1989). Plant cell wall architecture. Cell 56, 231-239.
57. Yu, L.H., Kawai-Yamada, M., Naito, M., Watanabe, K., Reed, J.C., and Uchimiya, H. (2002). Induction of mammalian cell death by a plant Bax inhibitor. FEBS Lett. 512, 308-312.
58. Yuan, J.Y., Shaham, S., Ledoux, S., Ellis, H.M., and Horvitz, R. (1993). The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1β converting enzyme. Cell 75, 641-652.
59. Xu, Q., and Reed, J.C. (1998). Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Mol. Cell 1, 337-346.
60. Zha, H., Fisk, H.A., Yaffe, M.P., Mahajan, N., Herman, B., and Reed, J.C. (1996). Structure-function comparison of the proapoptotic protein Bax in yeast and mammalian cells. Mol. Cell. Biol. 16, 6494-6508.