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The redox state of the ascorbate-dehydroascorbate pair as a specific sensor of cell division in tobacco BY-2 cells

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Summary

The effects of ascorbate (ASC) and dehydroascorbate (DHA) on cell proliferation were examined in the tobacco Bright Yellow 2 (TBY-2) cell line to test the hypothesis that the ASC-DHA pair is a specific regulator of cell division. The hypothesis was tested by measuring the levels of ASC and DHA or another general redox pair, glutathione (GSH) and glutathione disulfide (GSSG), during the exponential-growth phase of TBY-2 cells. A peak in ASC, but not GSH, levels coincided with a peak in the mitotic index. Moreover, when the cells were enriched with ascorbate, a stimulation of cell division occurred whereas, when the cells were enriched with DHA, the mitotic index was reduced. In contrast, glutathione did not affect the mitotic-index peak during this exponential-growth phase. The data are consistent in showing that the ASC-DHA pair acts as a specific redox sensor which is part of the mechanism that regulates cell cycle progression in this cell line.

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References

  • Abate C, Patel L, Rauscher FJ, Curran T (1990) Redox regulation of fos and jun DNA-binding activity in vitro. Science 249: 1157–1161

    Article  PubMed  CAS  Google Scholar 

  • Alcaín FJ, Buròn MI (1994) Ascorbate on cell growth and differentation. J Bioenerg Biomembr 26: 393–398

    Article  PubMed  Google Scholar 

  • — —, Rodriguez-Aguilera JC, Villalba JM, Navas P (1990) Ascorbate free radical stimulates the growth of a human promyelocytic leukemia cell line. Cancer Res 50: 5887–5891

    PubMed  Google Scholar 

  • Arrigoni O (1994) Ascorbate system in plant development. J Bioenerg Biomembr 26: 407–419

    Article  PubMed  CAS  Google Scholar 

  • Citterio S, Sgorbati S, Scippa S, Sparvoli E (1994) Ascorbic acid effect on the onset of cell proliferation in pea root. Physiol Plant 92: 601–607

    Article  CAS  Google Scholar 

  • Córdoba-Pedregosa MC, González-Reyes JA, Cañadillas MS, Navas P, Córdoba F (1996) Role of apoplastic and cell-wall peroxidases on the stimulation of root elongation by ascorbate. Plant Physiol 112: 1119–1125

    PubMed  Google Scholar 

  • De Cabo RC, Gonzalez-Reyes JA, Navas P (1993) The onset of cell proliferation is stimulated by ascorbate free radical in onion root primordia. Biol Cell 77: 231–233

    Article  Google Scholar 

  • De Gara L, Tommasi F (1999) Ascorbate redox enzyme: a network of reactions involved in plant development. Recent Res Dev Phytochem 3: 1–15

    Google Scholar 

  • —, Paciolla C, Tommasi F, Arrigoni O (1994) In vivo inhibition of galactono-γ-lactone conversion to ascorbate by lycorine. J Plant Physiol 144: 649–653

    Google Scholar 

  • Francis D (1998) Environmental control of the cell cycle in higher plants. In: Bryant JA, Chiatante D (eds) Plant cell proliferation and its regulation in growth and development. Wiley, New York, pp 79–98

    Google Scholar 

  • —, Davies MS, Braybrook C, James NC (1995) An effect of zinc on M-phase and Gl of the plant cell cycle in the synchronous TBY-2 tobacco cell suspension. J Exp Bot 293: 1887–1894

    Article  Google Scholar 

  • Fry SC (1998) Oxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals. Biochem J 332: 507–515

    PubMed  CAS  Google Scholar 

  • Horemans N, Asard H, Caubergs RJ (1997) The ascorbate carrier of higher plant plasma membranes preferentially translocates the fully oxidized (dehydroascorbate) molecule. Plant Physiol 114: 1247–1253

    PubMed  CAS  Google Scholar 

  • — — — (1998) Carrier mediated uptake of dehydroascorbate into higher plant plasma membrane vesicles shows Irans stimulation. FEBS Lett 421: 41–44

    Article  PubMed  CAS  Google Scholar 

  • Innocenti AM, Bitonti MB, Arrigoni O, Liso R (1990) The size of quiescent centre in roots ofAllium cepa L. grown with ascorbic acid. New Phytol 114: 507–509

    Article  Google Scholar 

  • Kampfenkel K, Van Montagu M, Inzè D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Anal Biochem 225: 165–167

    Article  PubMed  CAS  Google Scholar 

  • Kerk NM, Feldman LJ (1995) A biochemical model for the initiation and maintenance of the quiescent centre: implications for organisation of root meristems. Development 121: 2825–2833

    CAS  Google Scholar 

  • Linsmayer EM, Skoog F (1965) Organic growth factor requirements of tobacco tissue cultures. Physiol Plant 18: 100–127

    Article  Google Scholar 

  • Liso R, Calabrese G, Bitonti MB, Arrigoni O (1984) Relationship between ascorbic acid and cell division. Exp Cell Res 150: 314–320

    Article  PubMed  CAS  Google Scholar 

  • —, Innocenti AM, Bitonti MB, Arrigoni O (1988) Ascorbic acid-induced progression of quiescent centre cells from g1 to S phase. New Phytol 110: 469–471

    Article  CAS  Google Scholar 

  • —, Takahama U, Heber U (1993) Role of ascorbate in detoxifying ozone in the apoplast of spinach (Spinada oleracea L.) leaves. Plant Physiol 101: 969–976

    Google Scholar 

  • Luwe M (1996) Antioxidants in the apoplast and symplast of beech (Fagus sylvatica L.) leaves: seasonal variations and responses to changing ozone concentrations in air. Plant Cell Environ 19: 321–328

    Article  CAS  Google Scholar 

  • Matsumura H, Miyachi S (1980) Cycling assay for nicotinamide adenine dinucleotide. Methods Enzymol 69: 465–471

    Article  CAS  Google Scholar 

  • Matthews JR, Wakasugi N, Virelizier JL, Yodoi J, Hay RT (1992) Thioredoxin regulates the DNA binding activity of NF-kappaB by reduction of a disulfide bond involving cysteine 62. Nucleic Acids Res 20: 3821–3830

    Article  PubMed  CAS  Google Scholar 

  • May JM, Mendiratta S, Hill KE, Burk RF (1997) Reduction of dehydroascorbate to ascorbate by the selenoenzyme thioredoxin reductase. J Biol Chem 272: 22607–22610

    Article  PubMed  CAS  Google Scholar 

  • Morell S, Follmann H, De Tullio M, Haberlein I (1997) Dehydroascorbate and dehydroascorbate reductase are phantom indicators of oxidative stress in plants. FEBS Lett 414: 567–570

    Article  PubMed  CAS  Google Scholar 

  • Nagata T, Nemoto Y, Hasezawa S (1992) Tobacco BY-2 cell line as the “HeLa” cell in the cell biology of higher plants. Int Rev Cytol 132: 1–30

    Article  CAS  Google Scholar 

  • Navas P, Gomez-Diaz C (1995) Ascorbate free radical and its role in growth control. Protoplasma 184: 8–13

    Article  CAS  Google Scholar 

  • Polle A, Wieser G, Havranek WM (1995) Quantification of ozone influx and apoplastic ascorbate content in needles of Norway spruce trees (Picea abies L., Karst) at high altitude. Plant Cell Environ 18: 681–688

    Article  CAS  Google Scholar 

  • Powis G, Briehl M, Oblong J (1995) Redox signalling and the control of cell growth and death. Pharmacol Ther 68: 149–173

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Fernandez R, Fricker M, Corben LB, White NS, Sheard N, Leaver CJ, Van Montagu M, Inzé D, May MJ (1997) Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. Proc Natl Acad Sci USA 94: 2745–2750

    Article  PubMed  CAS  Google Scholar 

  • Trumper S, Follman H, Haberlein I (1994) A novel dehydroascorbate reductase from spinach chloroplasts homologous to plant trypsin inhibitor. FEBS Lett 352: 159–162

    Article  PubMed  CAS  Google Scholar 

  • Wells WW, Peng Xus D, Yang Y, Rocque PA (1990) Mammalian thioltransferase (glutaredoxin) and protein disulfide isomerase have dehydroascorbate reductase activity. J Biol Chem 256: 15361–15364

    Google Scholar 

  • Zhang F, Kirkham MB (1996) Antioxidant responses to drought in sunflower and sorghum seedlings. New Phytol 132: 361–373

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Dipartimento di Biologia e Patologia Vegetale, Università degli Studi di Bari, via E. Orabona 4, I-70125, Bari, Italy

    M. C. de Pinto & L. De Gara

  2. School of Biosciences, Cardiff University, Cardiff

    D. Francis

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  1. M. C. de Pinto
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  2. D. Francis
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  3. L. De Gara
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Correspondence to L. De Gara.

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de Pinto, M.C., Francis, D. & De Gara, L. The redox state of the ascorbate-dehydroascorbate pair as a specific sensor of cell division in tobacco BY-2 cells. Protoplasma 209, 90–97 (1999). https://doi.org/10.1007/BF01415704

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  • DOI: https://doi.org/10.1007/BF01415704

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