Low concentrations of the toxin ophiobolin a lead to an arrest of the cell cycle and alter the intracellular partitioning of glutathione between the nuclei and cytoplasm

Journal of Experimental Botany

Volumn 66, Issue 10, 2015, Pages 2991-3000

  Locato, Vittoria ^a   Uzal, Esther Novo ^a,b   Cimini, Sara ^a   Zonno, Maria Chiara ^c   Evidente, Antonio ^d   Micera, Alessandra ^e   Foyer, Christine H ^f   De Gara, Laura ^a  

^a UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^b UNIVERSITY OF MURCIA   (Spain)

^c INSTITUTE OF SCIENCES OF FOOD PRODUCTION   (Italy)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^e IRCCS FONDAZIONE BIETTI   (Italy)

^f UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Cell cycle; Glutathione; Glutathionylation; Ophiobolin A; Poly ADP ribosylation; Tobacco Bright Yellow 2

Indexed keywords

GLUTATHIONE; MYCOTOXIN; OPHIOBOLIN A; SESTERTERPENE;

ASCOMYCETES; CELL CYCLE; CELL NUCLEUS; CELL PROLIFERATION; CHEMISTRY; CYTOPLASM; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PLANT CELL; PLANT DISEASE; TOBACCO;

ASCOMYCOTA; CELL CYCLE; CELL NUCLEUS; CELL PROLIFERATION; CYTOPLASM; GLUTATHIONE; MYCOTOXINS; OXIDATION-REDUCTION; PLANT CELLS; PLANT DISEASES; SESTERTERPENES; TOBACCO;

EID: 84940702443     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv110     Document Type: Article

References (41)

1. Au TK, Chick WSH, Leung PC. 2000. The biology of ophiobolins. Life Science 67, 733-742.
2. Bradford MM. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
3. Bury M, Novo-Uzal E, Andolfi A, et al. 2013. Ophiobolin A, a sesterterpenoid fungal phytotoxin, displays higher in vitro growth-inhibitory effects in mammalian than in plant cells and displays in vivo antitumor activity. International Journal of Oncology 43, 573-585.
4. Canonica L, Fiecchi A, Galli Kienle M, Scala A. 1966. Isolation and constitution of cochliobolin B. Tetrahedron Letters 13, 1329-1333.
5. Chiu J, Dawes IW. 2012. Redox control of cell proliferation. Trends in Cell Biology 22, 592-601.
6. Cross JV, Templeton DJ. 2004. Oxidative stress inhibits MEKK1 by sitespecific glutathionylation in the ATP-binding domain. Biochemical Journal 381, 675-683.
7. de Pinto MC, Francis D, De Gara L. 1999. The redox state of the ascorbate-dehydroascorbate pair as a specific sensor of cell division in tobacco BY-2 cells. Protoplasma 209, 90-97.
8. de Pinto MC, Locato V, De Gara L. 2012. Redox regulation in plant programmed cell death. Plant, Cell and Environment 35, 234-244.
9. Dinneny JR, Long TA, Wang JY, Jung JW, Mace D, Pointer S, Barron C, Brady SM, Schiefelbein J, Benfey PN. 2008. Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320, 942-945.
10. Evidente A, Andolfi A, Cimmino A, Vurro M, Fracchiolla M, Charudattan R. 2006. Herbicidal potential of ophiobolins produced by Drechslera gigantea. Journal of Agricultural and Food Chemistry 54, 1779-1783.
11. Foyer CH, Noctor G. 2009. Redox regulation in photosynthetic organisms: signalling, acclimation, and practical implications. Antioxidants and Redox Signalling 11, 861-905.
12. Foyer CH, Pellny TK, Locato V, De Gara L. 2008. Analysis of redox relationships in the plant cell cycle: determinations of ascorbate, glutathione and poly (ADPribose) polymerase (PARP) in plant cell cultures. Methods in Molecular Biology 476, 193-209.
13. Fried J, Perez AG, Clarkson BD. 1976. Flow cytofluorometric analysis of cell cycle distributions using propidium iodide. Properties of the method and mathematical analysis of the data. The Journal of Cell Biology 71, 172-181.
14. García-Giménez JL, Markovic J, Dasí F, Queval G, Schnaubelt D, Foyer CH, Pallardó FV. 2013. Nuclear glutathione. Biochimica et Biophysica Acta 1830, 3304-3316.
15. Hatem E, Berthonaud, V, Dardalhon M, Lagniel G, Baudouin-Cornu P, Huang M-E, Labarre J, Chédin S. 2014. Glutathione is essential to preserve nuclear function and cell survival under oxidative stress. Free Radical Biology and Medicine 67, 103-114, Hill BG, Ramana KV, Cai J, Bhatnagar A, Srivastava SK. 2010.
16. Hill BG, Ramana KV, Cai J, Bhatnagar A, Srivastava SK. 2010. Measurement and identification of S-glutathiolated proteins. Methods in Enzymology 473, 179-197.
17. Hoffman A, Spetner LM, Burke M. 2008. Ramifications of a redox switch within a normal cell: its absence in a cancer cell. Free Radical Biology and Medicine 45, 265-268.
18. Houot V, Etienne P, Petitot AS, Barbier S, Blein JP, Suty L. 2001. Hydrogen peroxide induces programmed cell death features in cultured tobacco BY-2 cells in a dose-dependent manner. Journal of Experimental Botany 52, 1721-1730.
19. Jiang K, Ballinger T, Li D, Zhang S, Feldman L. 2006. A role for mitochondria in the establishment and maintenance of the maize root quiescent center. Plant Physiology 140, 1118-1125.
20. Jiang K, Feldman LJ. 2005. Regulation of root apical meristem development. Annual Review of Cell Development and Biology 21, 485-509.
21. Klatt P, Lamas S. 2000. Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. European Journal of Biochemistry 267, 4928-4944.
22. Klatt P, Molina EP, De Lacoba MG, Padilla CA, Martinez-Galesteo E, Barcena JA, Lamas S. 1999. Redox regulation of c-Jun DNA binding by reversible S-glutathiolation. FASEB Journal 13, 1481-1490.
23. Leung PC, Taylor WA, Wang JH, Tipton CL. 1984. Ophiobolin A. A natural product inhibitor of calmodulin. Journal of Biological Chemistry 259, 2742-2747.
24. Leung PC, Taylor WA, Wang JH, Tipton CL. 1985. Role of calmodulin inhibition in the mode of action of ophiobolin A. Plant Physiology 77, 303-308.
25. Liang YC, Hsu CY, Yao YL, Yang WM. 2013. PARP-2 regulates cell cycle-related genes through histone deacetylation and methylation independently of poly(ADP-ribosyl)ation. Biochemical and Biophysics Research Communication 431, 58-64.
26. Locato V, de Pinto MC, De Gara L. 2009. Different involvement of the mitochondrial, plastidial, and cytosolic ascorbate-glutathione redox enzymes in heat shock responses. Physiologia Plantarum 135, 296-306.
27. Locato V, Gadaleta C, De Gara L, de Pinto MC. 2008. Production of reactive species and modulation of antioxidant network in response to heat shock: a critical balance for cell fate. Plant, Cell and Environment 31, 1606-1619.
28. Markovic J, Borrás C, Ortega A, Sastre J, Viña J, Pallardó FV. 2007. Glutathione is recruited into the nucleus in the early phases of cell proliferation. Journal of Biological Chemistry 282, 20416-20424.
29. Markovic J, Mora NJ, Broseta AM, Gimeno A, de-la-Concepción N, Viña J, Pallardó FV. 2009. Nuclear GSH depletion impairs cell proliferation in 3T3 fibroblasts. PLoS ONE 29, e6413.
30. Mauro F, Grasso A, Tolmach LJ. 1969. Variations in sulfhydryl, disulfide, and protein content during synchronous and asynchronous growth of HeLa cells. Biophysics Journal 9, 1377-1397.
31. Menon SG, Goswami PC. 2007. A redox cycle within the cell cycle: ring in the old with the new. Oncogene 26, 1101-1109.
32. Menon SG, Sarsour EH, Spitz DR, Higashikubo R, Sturm M, Zhang H, Goswami PC. 2003. Redox regulation of the G1 to S phase transition in the mouse embryo fibroblast cell cycle. Cancer Research 63, 2109-2117.
33. Nagata T, Nemoto Y, Hasezawa S. 1992. Tobacco BY-2 cell line as the 'HeLa' cell biology of higher plants. International Review of Cytology 132, 1-30.
34. Noctor G, Mhamdi A, Queval G, Foyer CH. 2014. Regulating the redox gatekeeper: vacuolar sequestration puts glutathione disulfide in its place. Plant Physiology. 163, 665-671.
35. 25 terpenoid having a novel skeleton. Journal of American Chemistry Society 87, 4968-4970.
36. Pallardó FV, Markovic J, García JL, Viña J. 2009. Role of nuclear glutathione as a key regulator of cell proliferation. Molecular Aspects of Medicine 30, 77-85.
37. Pellny TK, Locato V, Vivancos PD, Markovic J, De Gara L, Pallardó FV, Foyer CH. 2009. Pyridine nucleotide cycling and control of intracellular redox state in relation to poly (ADP-ribose) polymerase activity and nuclear localization of glutathione during exponential growth of Arabidopsis cells in culture. Molecular Plant 2, 442-456.
38. Robu M, Shah RG, Petitclerc N, Brind'amour J, Kandan-Kulangara F, Shah GM. 2013. Role of poly (ADP-ribose) polymerase-1 in the removal of UV-induced DNA lesions by nucleotide excision repair. Proceedings of the National Academy of Sciences, USA 110, 1658-1663.
39. Vivancos PD, Dong Y, Ziegler K, Markovic J, Pallardo FV, Pellny TK, Verrier PJ, Foyer CH. 2010. Recruitment of glutathione into the nucleus during cell proliferation adjusts whole-cell redox homeostasis in Arabidopsis thaliana and lowers the oxidative defence shield. The Plant Journal 64, 825-838.
40. Voehringer DW, McConkey DJ, McDonnell TJ, Brisbay S, Meyn RE. 1998. Bcl-2 expression causes redistribution of glutathione to the nucleus. Proceedings of the National Academy of Sciences, USA 95, 2956-2960.
41. Zaffagnini M, Bedhomme M, Lemaire SD, Trost P. 2012. The emerging roles of protein glutathionylation in chloroplasts. Plant Science 186, 86-96.