Mitochondria-associated hexokinases play a role in the control of programmed cell death in Nicotiana benthamiana

Plant Cell

Volumn 18, Issue 9, 2006, Pages 2341-2355

  Kim, Moonil ^a   Lim, Jeong Hwa ^b,e   Ahn, Chang Sook ^c   Park, Kyoungsook ^a   Kim, Gyung Tae ^d   Kim, Woo Taek ^c   Pai, Hyun Sook ^c  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b Myong Ji University   (South Korea)

^c Yonsei University   (South Korea)

^d Dong A University   (South Korea)

^e BioHelix Corporation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; GENES; MORPHOLOGY;

LEAF MORPHOLOGY; NICOTIANA BENTHAMIANA; PROGRAMMED CELL DEATH (PCD);

ENZYMES;

ANATOMY; CELLS; ENZYMES; GENES;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; NICOTIANA BENTHAMIANA;

EID: 33749240936     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.106.041509     Document Type: Article

References (63)

1. Ahn, J.-W., Kim, M., Lim, J.H., Kim, G.-T., and Pai, H.-S. (2004). Phytocalpain controls the proliferation and differentiation fates of cells in plant organ development. Plant J. 38, 969-981.
2. Austin, M.J., Muskett, P., Kahn, K., Feys, B.J., Jones, J.D., and Parker, J.E. (2002). Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295, 2077-2080.
3. Azevedo, C., Sadanandom, A., Kitagawa, K., Freialdenhoven, A., Shirasu, K., and Schulze-Lefert, P. (2002). The RAR1 interact or SGT1, an essential component of R gene-triggered disease resistance. Science 295, 2073-2076.
4. Azoulay-Zohar, H., Israelson, A., Abu-Hamad, S., and Shoshan-Barmatz, V. (2004). In self-defence: Hexokinase promotes voltage-dependent anion channel closure and prevents mitochondria-mediated apoptotic cell death. Biochem. J. 377, 347-355.
5. Baines, C.P., Kaiser, R.A., Purcell, N.H., Blair, N.S., Osinska, H., Hambleton, M.A., Brunskill, E.W., Sayen, M.R., Gottlieb, R.A., Dom, G.W., Robbins, J., and Molkentin, J.D. (2005). Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434, 658-662.
6. Balk, J., Leaver, C.J., and McCabe, P.F. (1999). Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants. FEBS Lett. 463, 151-154.
7. Beers, E.P., Woffenden, B.J., and Zhao, C. (2000). Plant proteolytic enzymes: Possible roles during programmed cell death. Plant Mol. Biol. 44, 99-415.
8. Bethke, P.C., and Jones, R.L. (2001). Cell death of barley aleurone protoplasts is mediated by reactive oxygen species. Plant J. 25, 19-29.
9. Birnbaum, M.J. (2004). On the InterAktion between hexokinase and the mitochondrion. Dev. Cell 7, 781-782.
10. Bryson, J.M., Coy, P.E., Gottlob, K., Hay, N., and Robey, R.B. (2002). Increased hexokinase activity, of either ectopic or endogenous origin, protects renal epithelial cells against acute oxidant-induced cell death. J. Biol. Chem. 277, 11392-11400.
11. Cho, H.S., Lee, S.S., Kim, K.D., Kim, S.J., Hwang, I., Lim, J.S., Park, Y.I., and Pai, H.-S. (2004). DNA gyrase is involved in chloroplast nucleoid partitioning. Plant Cell 16, 2665-2682.
12. Danial, N.N., Gramm, C.F., Scorrano, L., Zhang, C.-Y., Krauss, S., Ranger, A.M., Datta, S.R., Greenberg, M.E., Licklider, L.J., Lowell, B.B., Gygi, S.P., and Korsmeyer, S.J. (2003). BAD and glucokinase reside in a mitochondrial complex that integrates glycolysis and apoptosis. Nature 424, 952-956.
13. Danon, A., Rotari, V.I., Gordon, A., Mailhac, N., and 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.
14. da-Silva, W.S., Gomez-Puyou, A., de Gomez-Puyou, M.T., Moreno-Sanchez, R., De Felice, F.G., de Meis, L., Oliveira, M.F., and Galina, A. (2004). Mitochondrial bound hexokinase activity as a preventive antioxidant defense: Steady-state ADP formation as a regulatory mechanism of membrane potential and reactive oxygen species generation in mitochondria. J. BIoI. Chem. 279, 39846-39855.
15. del Pozo, O., and Lam, E. (1998). Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr. Biol. 8, 1129-1132.
16. Desikan, R., Reynolds, A., Hancock, J.T., and Neill, SJ. (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.
17. Downward, J. (2003). Metabolism meets death. Nature 424, 896-897.
18. Elkeles, A., Breiman, A., and Zizi, M. (1997). Functional differences among wheat voltage-dependent anion channel (VDAC) isoforms expressed in yeast. Indication for the presence of a novel VDAC-modulating protein? J. Biol. Chem. 272, 6252-6260.
19. Frommer, W.B., Schultze, W.X., and Lalonde, S. (2003). Hexokinase, jack-of-all-trades. Science 300, 261-263.
20. Galina, A., Reis, M., Albuquerque, M.C., Puyou, A.G., Puyou, M.T., and de Meis, L. (1995). Different properties of the mitochondrial and cytosolic hexokinases in maize roots. Biochem. J. 309, 105-112.
21. Giegé, P., Heazlewood, J.L., Roessner-Tunali, U., Millar, A.H., Femie, A.R., Leaver, C.J., and Sweetlove, L.J. (2003). Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. Plant Cell 15, 2140-2151.
22. Giese, J.O., Herbers, K., Hoffmann, M., Klosgen, R.B., and Sonnewald, U. (2005). Isolation and functional characterization of a novel plastidic hexokinase from Nicotiana tabacum. FEBS Lett. 579, 827-831.
23. Godbole, A., Varghese, J., Sarin, A., and Mathew, M.K. (2003). VDAC is a conserved element of death pathways in plant and animal systems. Biochim. Biophys. Acta 1642, 87-96.
24. Gottlob, K., Majewski, N., Kennedy, S., Kandel, E., Robey, R.B., and Hay, N. (2001). Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase. Genes Dev. 15, 1406-1418.
25. Green, D.R., and Kroemer, G. (2004). The pathophysiology of mitochondrial cell death. Science 305, 627-629.
26. Heath, M.C. (2000). Hypersensitive response-related death. Plant Mol. Biol. 44, 321-324.
27. 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.
28. Ishitani, R., and Chuang, D.M. (1996). Glyceralaldehyde-3-phosphate dehydrogenase antisense oligonucleotides protect against cytosine arabinonucleoside-induced apoptosis in cultured cerebellar neurons. Proc. Natl. Acad. Sci. USA 93, 9937-9941.
29. Jang, J.-C., Leon, P., Zhou, L., and Sheen, J. (1997). Hexokinases as a sugar sensor in higher plants. Plant Cell 9, 5-19.
30. Kim, G.T., Tsukaya, H., and Uchimiya, H. (1998). The ROTUNDIFOLIA3 gene of Arabidopsis thaliana encodes a new member of the cytochrome P-450 family that is required for the regulated polar elongation of leaf cells. Genes Dev. 12, 2381-2391.
31. Kim, J.-W., and Dang, C.V. (2005). Multifaceted roles of glycolytic enzymes. Trends Biochem. Sci. 30, 142-150.
32. Kim, M., Ahn, J.-W., Jin, U.-H., Paek, K.-H., and Pai, H.-S. (2003). Activation of the programmed cell death pathway by inhibition of proteasome function in plants. J. Biol. Chem. 278, 19406-19415.
33. Leon, P., and Sheen, J. (2003). Sugar and hormone connections. Trends Plant Sci. 8, 110-116.
34. Lilliehook, C., Chan, S., Choi, E.K., Zaidi, N.F., Wasco, W., Mattson, M.P., and Duxbaum, J.D. (2002). Calsenilin enhances apoptosis by altering endoplasmic reticulum calcium signaling. Mol. Cell. Neurosci. 19, 552-559.
35. Machida, K., Ohta, Y., and Osada, H. (2006). Suppression of apoptosis by cyclophilin D via stabilization of hexokinase II mitochondrial binding in cancer cells. J. Biol. Chem. 281, 14314-14320.
36. Majewski, N., Noqueira, V., Bhaskar, P., Coy, P.E., Skeen, J.E., Gottlob, K., Chandel, N.S., Thompson, C.B., Robey, R.B., and Hay, N. (2004). Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol. Cell 16, 819-830.
37. Martinou, J.C., and Green, D.R. (2001). Breaking the mitochondrial barrier. Nat. Rev. Mol. Cell Biol. 2, 63-67.
38. Mlejnek, P., and Prochazka, S. (2002). Activation of caspase-like proteases and induction of apoptosis by isopentenyladenosine in tobacco BY-2 cells. Planta 215, 158-166.
39. Moore, B., Zhou, L., Rolland, F., Hall, Q., Cheng, W.-H., Liu, Y.-X., Hwang, I., Jones, T., and Sheen, J. (2003). Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormone signaling. Science 300, 332-336.
40. Nakagawa, T., Shimizu, S., Watanabe, T., Yamaguchi, O., Otsu, K., Yamagata, H., Inohara, H., Kubo, T., and Tsujimoto, Y. (2005). Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434, 652-658.
41. Nimchuk, Z., Eulgem, T., Holt, B.F., III, and Dangl, J.L. (2003). Recognition and response in the plant immune system. Annu. Rev. Genet. 37, 579-609.
42. 2+ pump is present in the pea Golgi apparatus membrane. Plant Physiol. 129, 1820-1828.
43. Pastorino, J.G., Shulga, N., and Hoek, J.B. (2002). Mitochondrial binding of hexokinase II inhibits Bax-induced cytochrome c release and apoptosis. J. Biol. Chem. 277, 7610-7618.
44. Penso, J., and Beitner, R. (1998). Clotrimazole and bifonazole detach hexokinase from mitochondria of melanoma cells. Eur. J. Pharmacol. 342, 113-117.
45. Ratcliff, F., Martin-Hernandez, A.M., and Baulcombe, D.C. (2001). Tobacco rattle virus as a vector for analysis of gene function by silencing. Plant J. 25, 237-245.
46. Rolland, F., and Sheen, J. (2005). Sugar sensing and signaling networks in plants. Biochem. Soc. Trans. 33, 269-271.
47. Rolland, F., Winderickx, J., and Thevelein, J.M. (2001). Glucose-sensing mechanisms in eukaryotic cells. Trends Biochem. Sci. 26, 310-317.
48. Saunders, P.A., Chen, R.W., and Chuang, D.M. (1999). Nuclear translocation of glyceralaldehyde-3-phosphate dehydrogenase isoforms during neuronal apoptosis. J. Neurochem. 72, 925-932.
49. Stulke, J., and Hillen, W. (1999). Carbon catabolite repression in bacteria. Curr. Opin. Microbiol. 2, 195-201.
50. 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.
51. Tajima, H., Tsuchiya, K., Yamada, M., Kondo, K., Katsube, N., and Ishitani, R. (1999). Over-expression of GAPDH induces apoptosis in COS-7 cells transfected with cloned GAPDH cDNAs. Neuroreport 10, 2029-2033.
52. Thomas, C.L., Jones, L., Baulcombe, D.C., and Maule, A.J. (2001). Size constraints for targeting post-transcriptional gene silencing and for RNA-directed methylation in Nicotiana benthamiana using a potato virus X vector. Plant J. 25, 417-425.
53. Thomas, S.G., and Franklin-Tong, V.E. (2004). Self-incompatibility triggers programmed cell death in Papaver pollen. Nature 429, 305-309.
54. Travis, A.J., Sui, D., Riedel, K.D., Hofmann, N.R., Moss, S.B., Wilson, J.E., and Kopf, G.S. (1999). A novel NH(2)-terminal, nonhydrophobic motif targets a male germ cell-specific hexokinase to the endoplasmic reticulum and plasma membrane. J. Biol. Chem. 274, 34467-34475.
55. Tsujimoto, Y., and Shimizu, S. (2002). The voltage-dependent anion channel: An essential player in apoptosis. Biochimie 84, 187-193.
56. Vyssokikh, M.Y., and Brdiczha, D. (2003). The function of complexes between the outer mitochondrial membrane pore (VDAC) and the adenine nucleotide translocase in regulation of energy metabolism and apoptosis. Acta Biochim. Pol. 50, 389-404.
57. Wiese, A., Gröner, F., Sonnewald, U., Deppner, H., Lerchl, J., Hebberker, U., Flügge, U.-I., and Weber, A. (1999). Spinach hexokinase I is located in the outer envelope membrane of plastids. FEBS Lett. 461, 13-18.
58. Wilson, J.E. (2003). Isozymes of mammalian hexokinase: Structure, subcellular localization and metabolic function. J. Exp. Biol. 206, 2049-2057.
59. Xiao, W., Sheen, J., and Jang, J.-C. (2000). The role of hexokinase in plant sugar signal transduction and growth and development. Plant Mol. Biol. 44, 451-461.
60. Yanagisawa, S., Yoo, S.-D., and Sheen, J. (2003). Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425, 521-525.
61. Zhang, H., Huang, H.M., Carson, R.C., Mahmood, J., Thomas, H.M., and Gibson, G.E. (2001). Assessment of membrane potentials of mitochondrial populations in living cells. Anal. Biochem. 298, 170-180.
62. Zhang, H.K., Zhang, X., Mao, B.Z., Li, Q., and He, Z.H. (2004). Alpha-picolinic acid, a fungal toxin and mammal apoptosis-inducing agent, elicits hypersensitive-like response and enhances disease resistance in rice. Cell Res. 14, 27-33.
63. Zheng, L., Roeder, R.G., and Luo, Y. (2003). S phase activation of the histone H2B promoter by OCA-S, a coactivator complex that contains GAPDH as a key component. Cell 114, 255-266.