Ascorbate and glutathione: Guardians of the cell cycle, partners in crime?

Plant Physiology and Biochemistry

Volumn 40, Issue 6-8, 2002, Pages 537-548

  Potters, Geert ^a   De Gara, Laura ^b,c   Asard, Han ^a,d   Horemans, Nele ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b UNIVERSITY OF BARI   (Italy)

^c UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^d UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Ascorbate; Cell cycle; Cell growth; Dehydroascorbate; Dehydroascorbate reductase; Glutathione; Redox status

Indexed keywords

EID: 0036619384     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0981-9428(02)01414-6     Document Type: Conference Paper

References (97)

1. F.J. Alcaín, M.I. Burón, J.C. Rodríguez-Aguilera, J.M. Villalba, P. Navas, Ascorbate free radical stimulates the growth of a human promyelocytic leukemia cell line, Cancer Res. 50 (1990) 5887-5891.
2. O. Arrigoni, R. Arrigoni-Liso, G. Calabrese, Lycorine as an inhibitor of ascorbic acid biosynthesis, Nature 256 (1975) 513-514.
3. O. Arrigoni, M.B. Bitonti, R. Cozza, A.M. Innocenti, R. Liso, R. Veltri, Ascorbic acid effect on pericycle cell line in Allium cepa root, Caryologia 42 (1989) 213-216.
4. O. Arrigoni, G. Calabrese, L. De Gara, M.B. Bitonti, R. Liso, Correlation between changes in cell ascorbate and growth of Lupinus albus seedlings, J. Plant Physiol. 150 (1997) 302-308.
5. O. Arrigoni, L, De Gara, F. Tommasi, R. Liso, Changes in the ascorbate systcm during seed development of Vicia faba L, Plant Physiol. 99 (1992) 235-238.
6. O. Arrigoni, M.C. De Tullio, The role of ascorbic acid in cell metabolism: between gene-directed functions and unpredictable chemical reactions. J. Plant Physiol. 157 (2000) 481-488.
7. K. Asada, Production and action of active oxygen species in photosynthetic tissues, in: C.H. Foyer, P.M. Mullineaux (Eds.), Causes of Photooxidative Stress and Amelioration of Defence Systems in Plants, CRC Press, Boca Raton, 1994, pp. 77-104.
8. K. Asada, The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons, Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 (1999) 601-639.
9. H. Asard, J. Kapila, W. Verelst, A. Bérczi, Higher-plant plasma membrane cytochrome b561: a protein in search of a function, Protoplasma 217 (2001) 77-93.
10. A. Bérczi, I.M. Møller, NADH-monodehydroascorbate oxidoreductase is one of the redox enzymes in spinach leaf plasma membrane, Plant Physiol. 116 (1998) 1029-1036.
11. G.N. Bijur, B. Briggs, C.L. Hitchcock, M.V. Williams, Ascorbic acid-dehydroascorbate induces cell cycle arrest at G2-M DNA damage' checkpoint during oxidative stress, Environ. Mol. Mutagen. 33 (1999) 144-152.
12. G. Borracino, S. Dipierro, O. Arrigoni, Purification and properties of ascorbate free radical reductase from potato tubers, Planta 167 (1986) 521-526.
13. G. Borraccino, L. Mastropasqua, S. De Leonardis, S. Dipierro, The role of ascorbic acid system in delaying the senescence of oat (Avena sativa L.) leaf segments, J. Plant. Physiol. 144 (1994) 161-166.
14. W.L. Chameides, The chemistry of ozone deposition to plant leaves: Role of ascorbic acid, Environ. Sci. Technol. 23 (1989) 595-600.
15. S. Citterio, S. Sgorbati, S. Scippa, E. Sparvoli, Ascorbic acid effect on the onset of cell proliferation in pea root, Physiol. Plant. 92 (1994) 601-607.
16. P.L. Conklin, E.H. Williams, R.L. Last, Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant, Proc. Natl. Acad. Sci. USA 93 (1996) 9970-9974.
17. J.B. Cooper, J.B. Heuser, J.E. Varner, 3,4-dehydroproline inhibits cell wall assembly and cell division in tobacco protoplasts, Plant Physiol. 104 (1994) 747-752.
18. M.C. Cordoba-Pedregosa, J.A. González-Reyes, M. del Sagrario Canadillas, P. Navas, F. Cordoba, Role of apoplastic and cell wall peroxidases on the stimulation of root elongation by ascorbate, Plant Physiol. 112 (1996) 1119-1126.
19. R.R. Crichton, Y. Ponce-Otiz, M.H.J. Koch, R. Parfait, H.B. Stuhrmann, Isolation and characterization of phytoferritin from pea (Pisum sativum) and lentil (Lens esculenta), Biochem. J. 171 (1978) 349-356.
20. M.W. Davey, C. Gilot, G. Persiau, J. Østergaard, Y. Han, G.C. Bauw, et al., Ascorbate biosynthesis in Arabidopsis cell suspension culture, Plant Physiol. 121 (1999) 535-544.
21. R.C. De Cabo, J.A. González-Reyes, P. Navas, The onset of cell proliferation is stimulated by ascorbate free radical in onion root primordia, Biol. Cell. 77 (1993) 231-233.
22. L. De Gara, M.C. de Pinto, O. Arrigoni, Ascorbate synthesis and asorbate peroxidase activity during the early stage of wheat germination, Physiol. Plant. 100 (1997) 894-900.
23. L. De Gara, C. Paciolla, M.C. De Tullio, M. Motto, O. Arrigoni, Ascorbate-dependent hydrogen peroxide detoxification and ascorbate regeneration during germination of a highly productive maize hybrid: evidence of an improved detoxification mechanism against reactive oxygen species, Physiol. Plant. 109 (2000) 7-13.
24. L. De Gara, C. Paciolla, R. Liso, A. Stefani, A. Blanco, O. Arrigoni, Ascorbate metabolism in mature pollen grains of Dasypyrum villosum (L.) Borb. during imbibition, J. Plant Physiol. 141 (1993) 405-409.
25. L. De Gara, C. Paciolla, F. Tommasi, R. Liso, O. Arrigoni, In vivo inhibition of galactono-γ-lactone conversion to ascorbate by lycorine, J. Plant Physiol. 144 (1994) 649-653.
26. L. De Gara, F. Tommasi, R. Liso, O. Arrigoni, Ascorbic acid utilization by prolyl hydroxylase in vivo, Phytochemistry 30 (1991) 1397-1399.
27. S. De Leonardis, G. De Lorezo, G. Borracino, S. Dipierro, A specific ascorbate free radical reductase insozyme participates in the regeneration of ascorbate for scavenging toxic oxygen species in potato tuber mitochondria, Plant Physiol. 109 (1995) 847-851.
28. M.C. De Pinto, D. Francis, L. De Gara, The redox state of the ascorbate-dehydroascorbate pair as a specific sensor of cell division in tobacco BY-2 cells, Protoplasma 209 (1999) 90-97.
29. M.C. De Pinto, F. Tommasi, L. De Gara, Enzymes of the ascorbate biosynthesis and ascorbate-glutathione cycle in cultured cells of tobacco Bright Yellow-2, Plant Physiol. Biochem. 38 (2000) 541-550.
30. M.C. De Tullio, C. Paciolla, F. Della Vecchia, N. Rascio, S. D'Emerico, L. De Gara, et al., Changes in onion root development induced by the inhibition of peptidyl prolyl hydroxylase and influence of the ascorbate system on cell division and elongation, Planta 209 (1999) 424-434.
31. B. Del Bello, E. Maellaro, L. Sugherini, A. Santucci, M. Comporti, A.F. Casini, Purification of NADPH-dependent dehydroascorbate reductase from rat liver and its identification with 3α-hydroxysteroid dehydrogenase, Biochem. J. 304 (1994) 385-390.
32. J.C. Deutsch, Dehydroascorbic acid, J. Chromat. 881 (2000) 301-309.
33. R. Di Cagno, L. Guidi, L. De Gara, G.F. Soldatini, Combined cadmium and ozone treatments affects photosynthesis and ascorbate-dependent defences in sunflower, New Phytolog. 151 (2001) 627-636.
34. S. Dipierro, G. Borracino, Dehydroascorbate reductase from potato tubers, Phytochemistry 30 (1991) 427-429.
35. C.H. Foyer, B. Halliwell, Presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism, Planta 133 (1976) 21-25.
36. C.H. Foyer, B. Halliwell, Purification and properties of dehydroascorbate reductase from spinach leaves, Phytochemistry 16 (1977) 1347-1350.
37. C.H. Foyer, F.L. Theodoulou, S. Delrot, The functions of intracellular glutathione transport systems in plants, Trends Plant Sci. 6 (2001) 486-492.
38. M. González, F.J. de Quevedo, J.A. Alcaín, P. González-Reyes, Navas Growth patters of the HL-60 human promyelocyte cell line stimulated by ascorbate free radical, Cancer J. 4 (1991) 262-266.
39. J.A. González-Reyes, F. Córdoba, P. Navas, Involvement of plasma membrane redox systems in growth control of animal and plant cells, in: H. Asard, A. Bérczi, R.J. Caubergs (Eds.), Plasma membrane redox systems and their role in biological stress and disease, Kluwer Academic Publishers, Dordrecht, 1998, pp. 193-213.
40. L.H. Hartwell, T.A. Weinert, Checkpoints: controls that ensure the order of cell cycle events, Science 246 (1989) 629-634.
41. U. Heber, C. Miyake, J. Mano, C. Ohno, K. Asada, Monodehydroascorbate radical detected by electron paramagnetic resonance spectrometry is a sensitive probe of oxidative stress in intact leaves, Plant Cell Physiol. 37 (1996) 1066-1072.
42. C. Herschbach, H. Rennenberg, Influence of glutathione on net uptake of sulphate and sulphate transport in tobacco plants, J. Exp. Bot. 45 (1994) 1069-1076.
43. N. Horemans, C.H. Foyer, G. Potters, H. Asard, Ascorbate function and associated transport systems in plants, Plant Physiol. Biochem. 38 (2000) 531-540.
44. N. Horemans, G. Potters, R.J. Caubergs, H. Asard, Transport of ascorbate into protoplasts of Nicotiana tabacum Bright Yellow-2 cell line, Protoplasma 205 (1998) 114-121.
45. M.A. Hossain, K. Asada, Purification of dehydroascorbate reductase from spinach and its characterisation as a thiol enzyme, Plant Cell Physiol. 25 (1984) 85-92.
46. W.C. Hou, H.J. Chen, Y.H. Lin, Dioscorins, the major tuber storage proteins of yam (Dioscorea batatas Decne), with dehydroascorbate reductase and monodehydroascorbate reductase activities, Plant Sci. 149 (1999) 151-156.
47. W.C. Hou, Y.H. Lin, Dehydroascorbate reductase and monodehydroascorbate reductase activities of trypsin inhibitors, the major sweet potato (Ipomoea batatas (L.) Lam) root storage protein, Plant Sci. 128 (1997) 151-158.
48. R. Howden, C.R. Andersen, P.B. Goldsbrough, C.S. Cobbett, Cadmium sensitive, glutathione-deficient mutant of Arabidopsis thaliana, Plant Physiol. 107 (1995) 1067-1073.
49. T. Hunter, T. Hunt, R.J. Jackson, H.D. Robertson, The characteristics of inhibition of protein synthesis by double stranded ribonucleic acid in reticulocyte lysates, J. Biol. Chem. 250 (1975) 409-417.
50. T. Imai, S. Karita, G. Shiratori, M. Hattori, T. Nunome, K. Oba, et al., L-galactono-γ-lactone dehydrogenase from sweet potato: purification and cDNA sequence analysis. Plant Cell Physiol. 39 (1998) 1350-1358.
51. A.M. Innocenti, M.B. Bitonti, O. Arrigoni, R. Liso, The size of quiescent centre in roots of Allium cepa L. grown with ascorbic acid, New Phytol. 110 (1990) 507-509.
52. A. Jiménez, J.A. Hernández, L.A. Del Río, F. Sevilla, Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves, Plant Physiol. 114 (1997) 275-284.
53. R.W. Joy, K.R. Patel, T.A. Thorpe, Ascorbic acid enhancement of organogenesis in tobacco, Plant Cell Tissue Organ. Cult. 13 (1988) 219-228.
54. N. Kato, M. Esaka, Changes in ascorbate oxidase gene expression and ascorbate levels in cell division and cell elongation in tobacco cells, Physiol. Plant. 105 (1999) 321-329.
55. Y. Kato, J. Urano, Y. Maki, T. Ushimaru, Purification and characterization of dehydroascorbate reductase from rice, Plant Cell Physiol. 38 (1997) 173-178.
56. S.E. Keates, N.M. Tarlyn, F.A. Loewus, V.R. Franceschi, L-ascorbic acid and L-galactose are sources for oxalic acid and calicium oxalate in Pistia stratiotes, Phytochemistry 53 (2000) 433-440.
57. N.M. Kerk, L.J. Feldman, A biochemical model for the initiation and maintenance of the quiescent center: implications for organization of root meristems, Development 121 (1995) 2825-2833.
58. R. Liso, G. Calabrese, M.B. Bitonti, O. Arrigoni, Relationship between ascorbic acid and cell division, Exp. Cell Res. 150 (1984) 314-320.
59. R. Liso, A.M. Innocenti, M.B. Bitonti, O. Arrigoni, Ascorbic acid-induced progression of quiescent centre cells from G1 to S-phase, New Phytol. 110 (1988) 469-471.
60. M.W.F. Luwe, U. Takahama, U. Heber, Role of ascorbate in detoxifying ozone in the apoplast of spinach (Spinacia oleracea L.) leaves, Plant Physiol. 101 (1993) 969-976.
61. K. Marrs, The functions and regulation of glutathione S-transferases in plants, Annu. Rev. Plant Physiol. Plant Mol. Biol. 47 (1996) 127-158.
62. J.M. May, C.E. Cobb, S. Mendiretta, K.E. Hill, R.F. Burk, Reduction of the ascorbyl free radical to ascorbate by thioredoxin reductase, J. Biol. Chem. 273 (1998) 23039-23045.
63. J.M. May, S. Mendiretta, K.E. Hill, R.F. Burk, Reduction of dehydroascorbate to ascorbate by the selenoenzyme thioredoxin reductase, J. Biol. Chem. 272 (1997) 22607-22610.
64. M.J. May, C.J. Leaver, Oxidative stimulation of glutathione synthesis in Arabidopsis thaliana suspension cultures, Plant Physiol. 103 (1993) 621-627.
65. M.J. May, T. Vernoux, C. Leaver, M. Van Montagu, D. Inzé, Glutathione homeostasis in plants: implications for environmental sensing and plant development, J. Exp. Bot. 49 (1998) 649-667.
66. G.A. McClarty, A.K. Chan, B.K. Choy, J.A. Wright, Increased ferritin gene expression is associated with ribonucleotide reductase gene expression and the establishment of hydroxyurea resistance in mammalian cells, J. Biol. Chem. 265 (1990) 7539-7547.
67. C. Miyake, K. Asada, Ferredoxin-dependent photorednction of the lnonodehydroascorbate radical in spinach thylakoids, Plant Cell Physiol. 35 (1995) 539-549.
68. S. Morell, H. Follmann, M. De Tullio, I. Häberlein, Dehydroascorbate and dehydroascorbate reductase are phantom indicators of oxidative stress in plants, FEBS Lett. 414 (1997) 567-570.
69. F. Navarro, J.C. Rodriguez-Anguilera, F.J. Alcain, M.I. Buron, P. Navas. Ascorbate potentiates serum-induced S-phase entry of quiescent 3T3 cells, Protoplasma 169 (1992) 85-87.
70. P. Navas, J.M. Villalba, F. Córdoba, Ascorbate function at the plasma membrane, Biochim. Biophys. Acta 1197 (1994) 1-13.
71. G. Noctor, A.C.M. Arisi, L. Jouanin, K.J. Kunert, H. Rennenberg, C.H. Foyer, Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants, J. Exp. Bot. 49 (1998) 623-647.
72. G. Noctor, C.H. Foyer, Ascorbate and glutathione: keeping active oxygen under control, Annu. Rev. Plant Physiol. Plant Mol. Biol. 49 (1998) 249-279.
73. C. Paciolla, M.C. De Tullio, A. Chiappetta, A.M. Innocenti, M.B. Bitonti, R. Liso, et al., Short- and long-term effects of dehydroascorbate in Lupinus albus and Allium cepa roots, Plant Cell Physiol. 42 (2001) 857-863.
74. C.H. Park, B.F. Kimler, Growth modulation of human leukemic, preleukemic and myeloma progenitor cells by L-ascorbic acid, Am. J. Clin. Nutr. 54 (1991) 12415-12465.
75. G. Potters, N. Horemans, R.J. Caubergs, H. Asard, Ascorbate and dehydroascorbate influence cell cycle progression in a Nicotiana tabacum cell suspension, Plant Physiol. 124 (2000) 17-20.
76. W.E. Rauser, Phytochelatins, Annu. Rev. Biochem. 59 (1990) 61-86.
77. J.P. Reichheld, T. Vernoux, F. Lardon, M. Van Montagu, D. Inzé, Specific checkpoint regulate plant cell cycle progression in response to oxidative stress, Plant J. 17 (1999) 647-656.
78. M.E. Reid, Relation of vitamin C to cell size in the growing region of the primary root of cowpea seedlings, Am. J. Bot. 28 (1941) 410-415.
79. T. Russo, N. Zambrano, F. Esposito, R. Ammendola, F. Cimino, M. Fiscella, et al., A p53-independent pathway for activation of WAF1/CIP1 expression following oxidative stress, J. Biol. Chem. 270 (1995) 29386-29391.
80. M. Sánchez, E. Queijeiro, G. Revilla, I. Zarra, Changes in ascorbic acid levels in apoplastic fluid during growth of pine hypocotyls. Effect on peroxidase activities associated with cell walls, Physiol. Plant. 101 (1997) 815-820.
81. R. Sánchez-Fernández, M. Fricker, L.B. Corben, N.S. White, N. Sheard, C.J. Leaver, et al., Cell proliferation and hair tip growth in the Arabidopsis root under mechanistically different forms of redox control, Proc. Natl. Acad. Sci. USA 94 (1997) 2745-2750.
82. A. Sen Gupta, R.G. Alscher, D. McCume, Response of photosynthesis and cellular antioxidants to ozone in Populus leaves, Plant Physiol. 96 (1991) 650-655.
83. N. Smirnoff, P.L. Conklin, F.A. Loewus, Biosynthesis of ascorbic acid in plants: a renaissance, Annu. Rev. Plant Physiol. Plant Mol. Biol. 52 (2001) 437-468.
84. C. Stasolla, E.C. Yeung, Ascorbic acid improves conversion of white spruce somatic embryos, In Vitro Cell Dev. Biol. 35 (1999) 316-319.
85. C. Stasolla, E.C. Yeung, Ascorbic acid metabolism during white spruce somatic embryo maturation and germination, Physiol. Plant. 111 (2001) 196-205.
86. M. Suthantiran, M.E. Anderson, V.K. Sharma, A. Meister, Glutathione regulates activation-dependent DNA synthesis in highly purified normal human T lyphocytes via the CD2 and CD3 antigens, Proc. Natl. Acad. Sci. USA 87 (1990) 3343-3347.
87. U. Takahama, Redox state of ascorbic acid in the apoplast of stems of Kalanchoe daigremontiana, Physiol. Plant. 89 (1993) 791-798.
88. U. Takahama, Changes induced by abscisic acid and light in the redox state of ascorbate in the apoplast of epicotyls of Vigna angularis, Plant Cell Physiol. 35 (1994) 975-978.
89. U. Takahama, M. Hirotsu, T. Oniki, Age-dependent changes in levels of ascorbic acid and chlorogenic acid, and activities of peroxidase and superoxide dismutase in the apoplast of tobacco leaves: mechanism of the oxidation of chlorogenic acid in the apoplast, Plant Cell Physiol. 40 (1999) 716-724.
90. F. Tommasi, C. Paciolla, M.C. de Pinto, L. De Gara, A comparative study of glutathione and ascorbate metabolism during germination of Pinus pinea L. seeds, J. Exp. Bot. 52 (2001) 1647-1654.
91. S. Trümper, H. Follmann, I. Häberlein, A novel dehydroascorbate reductase from spinach chloroplasts homologous to plant trypsin inhibitor, FEBS Left. 352 (1994) 159-162.
92. J. Urano, T, Nakagawa, Y. Maki, T Masumura, K. Tanaka, N. Murata, et al., Molecular cloning and characterization of a rice dehydroascorbate reductase, FEBS Lett. 466 (2000) 107-111.
93. H. Vanacker, T.L.W. Carter, C.H. Foyer, Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves, Plant Physiol. 117 (1998) 1103-1114.
94. S.D. Veljovic-Jovanovic, C. Pignocchi, G. Noctor, C.H. Foyer, Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system, Plant Physiol. 127 (2001) 426-435.
95. T. Vernoux, R.C. Wilson, K.A. Seeley, J.P. Reichheld, S. Muroy, S. Brown, et al., The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development, Plant Cell 12 (2000) 97-109.
96. W.W. Wells, D.P. Xu, Y. Yanf, P.A. Rocque, Mammalian thioltransferase (glutaredoxin) and protein disulfide isomerase have dehydroascorbate reductase activity, J. Biol. Chem. 265 (1990) 15361-15364.
97. C. Xiang, B.L. Werner, E.M. Christensen, D.J. Olver, The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels, Plant Physiol. 126 (2001) 564-574.