Plant Biotechnology Reports

The Korean Society of Plant Biotechnology (한국식물생명공학회)
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Role of ${\alpha}$-tocopherol in cellular signaling: ${\alpha}$-tocopherol inhibits stress-induced mitogen-activated protein kinase activation

  • Received : 2010.05.17
  • Accepted : 2010.10.02
  • Published : 2011.01.31
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Abstract

Tocopherols belong to the plant-derived poly phenolic compounds known for antioxidant functions in plants and animals. Activation of mitogen-activated protein kinases (MAPK) is a common reaction of plant cells in defense-related signal transduction pathways. We report a novel non-antioxidant function of ${\alpha}$-tocopherol in higher plants linking the physiological role of tocopherol with stress signalling pathways. Pre-incubation of a low concentration of $50{\mu}M$ ${\alpha}$-tocopherol negatively interferes with MAPK activation in elicitor-treated tobacco BY2 suspension culture cells and wounded tobacco leaves, whereas pre-incubated BY2 cells with ${\alpha}$-tocopherol phosphate did not show the inhibitory effect on stimuli-induced MAPK activation. The decreased MAPK activity was neither due to a direct inhibitory effect of ${\alpha}$-tocopherol nor due to the induction of an inhibitory or inactivating activity directly affecting MAPK activity. The data support that the target of ${\alpha}$-tocopherol negatively regulates an upstream component of the signaling pathways that leads to stress dependent MAPK activation.

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References

  1. Abbasi A-R, Hajirezaei M, Hofius D, Sonnewald U, Voll LM (2007) Specific roles of $\alpha$- and $\gamma$- tocopherol in abiotic stress responses of transgenic tobacco. Plant Physiol 143:1720-1738 https://doi.org/10.1104/pp.106.094771
  2. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331-1341 https://doi.org/10.1093/jexbot/53.372.1331
  3. Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21-39 https://doi.org/10.1146/annurev.arplant.59.032607.092830
  4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254 https://doi.org/10.1016/0003-2697(76)90527-3
  5. Breyer I, Azzi A (2001) Differential inhibition by alpha- and betatocopherol of human erythroleukemia cell adhesion: role of integrings. Free Radic Biol Med 30:1381-1389 https://doi.org/10.1016/S0891-5849(01)00541-X
  6. Chan SS, Monteiro HP, Schindler F, Stern A, Junqueria VB (2001) Alpha-tocopherol modulates tyrosine phosphorylation in human neutrophils by inhibition of protein kinase C activity and activation of tyrosine phosphatases. Free Radic Res 35:843-856 https://doi.org/10.1080/10715760100301341
  7. 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 https://doi.org/10.1046/j.1365-313x.2000.00911.x
  8. Clement S, Tasinato A, Boscoboinik D, Azzi A (1997) The effect of a-tocopherol on the synthesis, phosphorylation, and activity of protein kinase C in smooth muscle cells after phorbol 12-myristate 13-acetate downregulation. Eur J Biochem 246:745-749 https://doi.org/10.1111/j.1432-1033.1997.t01-2-00745.x
  9. Clement SA, Tan CC, Guo J, Kitta K, Suzuki YJ (2002) Roles of protein kinase C and a-tocopherol in regulation of signal transduction for GATA-4 phosphorylation in HL-1 cardiac muscle cells. Free Radic Biol Med 32:341-349 https://doi.org/10.1016/S0891-5849(01)00802-4
  10. Colcombet J, Hirt H (2008) Arabidopsis MAPKs: a complex signaling network involved in multiple biological processes. Biochem J 413:217-226 https://doi.org/10.1042/BJ20080625
  11. Dahan J, Pichereau C, Rossignol M, Blanc S, Wendehenne D, Pugin A, Bourque S (2009) Activation of nuclear-localized SIPK in tobacco cells challenged by cryptogein, an elicitor of plant defence reactions. Biochem J 418:191-200 https://doi.org/10.1042/BJ20081465
  12. Egger T, Hammer A, Wintersperger A, Goti D, Malle E, Saltier W (2001) Modulation of microglial superoxide production by alpha-tocopherol in vitro: attenuation of p67phox translocation by a protein phosphatase-dependent pathway. J Neurochem 79:1169-1182
  13. Ehness R, Ecker M, Godt D, Roitsch T (1997) Glucose and stress independently regulate source/sink relations and defense mechanisms via signal transduction pathways involving protein phosphorylation. Plant Cell 9:1825-1841 https://doi.org/10.1105/tpc.9.10.1825
  14. Ekstrand-Hammarstroem B, O¨sterlund C, Lilliehook B, Bucht A (2006) Vitamin E down-modulates mitogen-activated protein kinases, nuclear factor-kB and inflammatory responses in lung epithelial cells. Clin Exp Immunol 147:359-369 https://doi.org/10.1111/j.1365-2249.2006.03285.x
  15. Foryer CH, Noctor G (2003) Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes, and mitochondria. Physiol Plant 119:355-364 https://doi.org/10.1034/j.1399-3054.2003.00223.x
  16. Frank GD, Eguchi S, Yamakawa T, Tanaka S, Inagami T, Motley ED (2000) Involvement of reactive oxygen species in the activation of tyrosine kinase and extracellular signal-regulated kinase by angiotensin II. Endocrinology 141:3120-3126 https://doi.org/10.1210/en.141.9.3120
  17. Garcia-Brugger A, Lamotte O, Vandelle E, Bourque S, Lecourieux D, Poinssot B, Wendehenne D, Pugin A (2006) Early signaling events induced by elicitors of plant defense. Mol Plant Microbe Interact 19:711-724 https://doi.org/10.1094/MPMI-19-0711
  18. Gossett DR, Millhollon EP, Lucas MC (1994) Antioxidant response to NaCl stress in salt-tolerant and salt-sensitive cultivars of cotton. Crop Sci 34:706-714 https://doi.org/10.2135/cropsci1994.0011183X003400030020x
  19. Kumar D, Klessig DF (2000) Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene, and jasmonic acid. Mol Plant Microbe Interact 13:347-351 https://doi.org/10.1094/MPMI.2000.13.3.347
  20. Leipner J, Frachebound Y, Stamp P (1999) Effect of growing season on the photosynthetic apparatus and leaf antioxidative defenses in two maize genotypes of different chilling tolerance. Environ Exp Bot 42:129-139 https://doi.org/10.1016/S0098-8472(99)00026-X
  21. Link V, Hofmann MG, Sinha AK, Ehness R, Strnad M, Roitsch T (2002) Biochemical evidence for the activation of distinct subsets of mitogen-activated protein kinases by voltage and defense-related stimuli. Plant Physiol 128:271-281 https://doi.org/10.1104/pp.010569
  22. Liu X, Hua X, Guo J, Qi D, Wang L, Liu Z, Jin Z, Chen S, Liu G (2008) Enhanced tolerance to drought stress in transgenic tobacco plants overexpressing VTE1 for increased tocopherol production from Arabidopsis thaliana. Biotechnol Lett 30:1275-1280 https://doi.org/10.1007/s10529-008-9672-y
  23. Maeda H, Song W, Sage TL, DellaPenna D (2006) Tocopherols play a crucial role in low temperature adaptation and phloem loading in Arabidopsis. Plant Cell 18:2710-2732 https://doi.org/10.1105/tpc.105.039404
  24. Matsuzawa A, Ichijo H (2008) Redox control of cell fate by MAP kinase: physiological roles of ASK1-MAP kinase pathway in stress signaling. Biochim Biophys Acta 1780:1325-1336 https://doi.org/10.1016/j.bbagen.2007.12.011
  25. Mattie MD, McElwee MK, Freedman JH (2008) Mechanism of copper-activated transcription: activation of AP-1, and the JNK/ SAPK and p38 signal transduction pathways. J Mol Biol 383:1008-1018 https://doi.org/10.1016/j.jmb.2008.08.080
  26. Munne-Bosch S, Alegre I (2000) Changes in carotenoids, tocopherols and diterpenes during drought and recovery, and the biological significance of chlorophyll loss in Rosmarinus officinalis plants. Planta 210:925-931 https://doi.org/10.1007/s004250050699
  27. Numakawa Y, Numakawa T, Matsumoto T, Yagasaki Y, Kumamaru E, Kunugi H, Taguchi T, Niki E (2006) Vitamin E protected cultured cortical neurons from oxidative stress-induced cell death through the activation of mitogen-activated protein kinase and phosphatidylinositol 3-kinase. J Neurochem 97:1191-1202 https://doi.org/10.1111/j.1471-4159.2006.03827.x
  28. Pitzschke A, Hirt H (2006) Mitogen-activated protein kinases and reactive oxygen species signaling in plants. Plant Physiol 141:351-356 https://doi.org/10.1104/pp.106.079160
  29. Rezk BM, Haenen GRMM, van der Vijgh WJF, Bast A (2004) The extraordinary antioxidant activity of vitamin E phosphate. Biochim Biophys Acta 1683:16-21 https://doi.org/10.1016/j.bbalip.2004.03.005
  30. Sattler SE, Cahoon EB, Coughlan SJ, DellaPenna D (2004) Vitamin E is essential for seed longevity, and for preventing lipid peroxidation during germination. Plant Cell 16:1419-1432 https://doi.org/10.1105/tpc.021360
  31. Sattler SE, Mene-Saffrane L, Farmer EE, Kischke M, Mueller MJ, DellaPenna D (2006) Nonenzymatic lipid peroxidation reprograms gene expression and activates defense markers in Arabidopsis tocopherol-deficient mutants. Plant Cell 18:3706-3720 https://doi.org/10.1105/tpc.106.044065
  32. Stocker A, Fretz H, Frick H, Ruttimann A, Woggon WD (1996) The substrate specificity of tocopherol cyclase. Bioorg Med Chem 4:1129-1134 https://doi.org/10.1016/0968-0896(96)00125-3
  33. Thoma I, Loeffler C, Sinha AK, Gupta M, Krischke M, Steffan B, Roitsch T, Mueller MJ (2003) Cyclopentenone isoprostanes induced by reactive oxygen species trigger defense gene activation and phytoalexin accumulation in plants. Plant J 34:363-375 https://doi.org/10.1046/j.1365-313X.2003.01730.x
  34. Vidi P-A, Kanwischer M, Banginsky S, Austin JR, Csucs G, Dormann P, Kessler F, Brehelin C (2006) Tocopherol cyclase (VTE1) localization and Vitamin E accumulation in chloroplast plastoglobule lipoprotein particles. J Biol Chem 281:11225-11234 https://doi.org/10.1074/jbc.M511939200
  35. Yang K-Y, Liu Y, Zhang S (2001) Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc Natl Acad Sci USA 98:741-746 https://doi.org/10.1073/pnas.98.2.741
  36. Zhang S, Klessig DF (1997) Salicylic acid activates a 48-kD MAP kinase in tobacco. Plant Cell 9:809-824 https://doi.org/10.1105/tpc.9.5.809
  37. Zingg JM (2007) Modulation of signal transduction by vitamin E. Mol Aspects Med 28:481-506 https://doi.org/10.1016/j.mam.2006.12.009

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