Calcium channel blockers protect against aluminium-induced DNA damage and block adaptive response to genotoxic stress in plant cells

Mutation Research - Genetic Toxicology and Environmental Mutagenesis

Volumn 751, Issue 2, 2013, Pages 130-138

  Achary, V Mohan M ^a,c   Parinandi, Narasimham L ^b   Panda, Brahma B ^a  

^a BERHAMPUR UNIVERSITY   (India)

^b OHIO STATE UNIVERSITY   (United States)

^c INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

Aluminium genotoxicity; Calcium signalling; DNA damage; Genome protection; Oxidative stress; Plant stress adaptation

Indexed keywords

ALUMINUM; CELL DNA; EGTAZIC ACID; LANTHANUM CHLORIDE; VERAPAMIL;

ARTICLE; CALCIUM SIGNALING; CELL DEATH; CELL PROTECTION; COMET ASSAY; CONTROLLED STUDY; DNA DAMAGE; GENOTOXICITY; MERISTEM; NONHUMAN; ONION; PHYTOTOXICITY; PLANT RESPONSE; PLANT STRESS; PRIORITY JOURNAL; ROOT CELL;

ADAPTATION, PHYSIOLOGICAL; ALUMINUM; CALCIUM CHANNEL BLOCKERS; CELL SURVIVAL; COMET ASSAY; DNA DAMAGE; ETHYL METHANESULFONATE; METHYLMERCURY COMPOUNDS; ONIONS; PLANT ROOTS;

ALLIUM CEPA;

EID: 84874279758     PISSN: 13835718     EISSN: 18793592     Source Type: Journal    
DOI: 10.1016/j.mrgentox.2012.12.008     Document Type: Article

References (70)

1. Kochian L.V., Hoekenga O.A., Pineros M.A. How do crop plants tolerate acid soil? Mechanisms of aluminum tolerance and phosphorous deficiency. Annu. Rev. Plant Biol. 2004, 55:459-493.
2. Poschenrieder C., Amenos M., Corrales I., Doncheva S., Barcelo J. Root behavior in response to aluminum toxicity. Plant-Environment Interactions, Signaling and Communication in Plants 2009, 21-43. Springer-Verlag, Berlin. F. Baluska (Ed.).
3. Zheng S.J., Yang J.L. Target sites of aluminum phytotoxicity. Biol. Plant. 2005, 49:321-331.
4. Ma J.F. Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. Int. Rev. Cytol. 2007, 264:225-252.
5. Rengel Z., Zhang W.-H. Role of dynamics of intracellular calcium in aluminium-toxicity syndrome. New Phytol. 2003, 159:295-314.
6. Yamamoto Y., Kobayashi Y., Devi S.R., Rikiishi S., Matsumoto H. Oxidative stress triggered by aluminum in plant roots. Plant Soil 2003, 255:239-243.
7. 2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiol. 2004, 135:702-708.
8. Rentel M.C., Knight M.R. Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol. 2004, 135:1471-1479.
9. Kudla J., Batistic O., Hashimoto K. Calcium signals: the lead currency of plant information processing. Plant Cell 2010, 22:541-563.
10. Lecourieux D., Ranjeva R., Pugin A. Calcium in plant defense-signaling pathways. New Phytol. 2006, 171:249-269.
11. Tuteja N., Sopory S.K. Chemical signaling under abiotic stress environment in plants. Plant Signal. Behav. 2008, 3:525-536.
12. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 2002, 7:405-410.
13. Kobayashi M., Ohura I., Kawakita K., Yokota N., Fujiwara M., Shimamoto K., Doke N., Yoshioka H. Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 2007, 19:1065-1080.
14. 2+ homeostasis in root hairs of Arabidopsis thaliana (L.). Planta 1998, 206:378-387.
15. Panda S.K., Baluska F., Matsumoto H. Aluminum stress signaling in plants. Plant Signal. Behav. 2009, 4:592-597.
16. Achary V.M.M., Jena S., Panda K.K., Panda B.B. Aluminium induced oxidative stress and DNA damage in root cells of Allium cepa L. Ecotoxicol. Environ. Saf. 2008, 70:300-310.
17. Achary V.M.M., Parinandi N.L., Panda B.B. Aluminum induces oxidative burst, cell wall NADH peroxidase activity, and DNA damage in root cells of Allium cepa L. Environ. Mol. Mutagen. 2012, 53:550-560.
18. Achary V.M.M., Panda B.B. Aluminium-induced DNA-damage and adaptive response to genotoxic stress in plant cells are mediated through reactive oxygen intermediates. Mutagenesis 2010, 25:201-209.
19. Achary V.M.M., Patnaik A.R., Panda B.B. Oxidative biomarkers in leaf tissue of barley seedlings in response to aluminum stress. Ecotoxicol. Environ. Saf. 2012, 75:16-26.
20. Bolwell G.P., Davies D.R., Gerrish C., Auh C.-K., Murphy T.M. Comparative biochemistry of the oxidative burst produced by rose and French bean cells reveals two distinct mechanisms. Plant Physiol. 1998, 116:1379-1385.
21. Almagro L., Gomez Ros L.V., Belchi-Navarro S., Bru R., Ros Barcelo A., Pedreno M.A. Class III peroxidases in plant defence reactions. J. Exp. Bot. 2009, 60:377-390.
22. Kawano T., Kadono T., Furuichi T., Muto S., Lapeyrie F. Aluminum-induced distortion in calcium signaling involving oxidative bursts and channel regulation in tobacco BY-2 cells. Biochem. Biophys. Res. Commun. 2003, 308:35-42.
23. Kunihiro S., Hiramatsu T., Kawano T. Involvement of salicylic acid signal transduction in aluminum-responsive oxidative burst in Arabidopsis thaliana cell suspension culture. Plant Signal. Behav. 2011, 6:611-616.
24. 2+ channels. Biochem. Biophys. Res. Commun. 2004, 324:40-45.
25. Rounds M.A., Larsen P.B. Aluminum-dependent root-growth inhibition in Arabidopsis results from AtATR-regulated cell cycle arrest. Curr. Biol. 2008, 18:1495-1500.
26. Nezames C.D., Sjogren C.A., Barajas J.F., Larsen P.B. The Arabidopsis cell cycle checkpoint regulators TANMEI/ALT2 and ATR mediate the active process of aluminum-dependent root growth inhibition. Plant Cell 2012, 24:608-621.
27. Dimova E.G., Bryant P.E., Chankova S.G. " Adaptive response" -some underlying mechanisms and open questions. Genet. Mol. Biol. 2008, 31:396-408.
28. Calabrese E.J. Biological stress response terminology: Integrating the concepts of adaptive response and preconditioning stress within a hormetic dose-response framework. Toxicol. Appl. Pharmacol. 2007, 222:122-128. and 57 coauthors.
29. Patra J., Sahoo M.K., Panda B.B. Persistence and prevention of aluminium- and paraquat- induced adaptive response to methyl mercuric chloride in plant cells in vivo. Mutat. Res. 2003, 538:51-61.
30. Schat C.H., Ten Bookum W.M. Genetic control of copper tolerance in Silene vulgaris, Heredity 1992, 68:219-229.
31. Baker C.J., Mock N.M. An improved method for monitoring cell death in cell suspension and leaf disc assays using Evans blue. Plant Cell Tissue Organ Cult. 1994, 39:7-12.
32. Kumaravel T.S., Vilhar B., Faux S.P., Jha A.N. Comet Assay measurements: a perspective. Cell Biol. Toxicol. 2000, 25:53-64.
33. Sharma A.K., Sharma A. Chromosome techniques - Theory and Practice 1980, Butterworths, London. 3rd ed.
34. Daniel W.W. Biostatistics - A Foundation for Analysis in the Health Sciences 1995, John Wiley, New York. 6th ed.
35. Clarkoson D.T. The effect of aluminium and some other trivalent metal cations on cell division in the root apices of Allium cepa. Ann. Bot. 1965, 29:309-315.
36. Morimura S., Takahashi E., Matsumoto H. Association of aluminium with nuclei and inhibition of cell division in onion (Allium cepa) roots. Z. Pflanzenphysiol. 1978, 88:395-401.
37. Matsumoto H. Changes of the structure of pea chromatin by aluminum. Plant Cell Physiol. 1988, 29:281-287.
38. de Campos J.M.S., Viccini L.F. Cytotoxicity of aluminum on meristematic cells of Zea mays and Allium cepa. Caryologia 2003, 56:65-73.
39. Sivaguru M., Yamamoto Y., Matsumoto H. Differential impacts of aluminium on microtubule organisation depends on growth phase in suspension-cultured tobacco cells. Physiol. Plant. 1999, 107:110-119.
40. Silva I.R., Smyth T.J., Moxley D.F., Carter T.E., Allen N.S., Rufty T.W. Aluminum accumulation at nuclei of cells in the root tip. fluorescence detection using lumogallion and confocal laser scanning microscopy. Plant Physiol. 2000, 123:543-552.
41. Silva S., Santosa C., Matos M., Pinto-Carnide O. Al toxicity mechanism in tolerant and sensitive rye genotypes. Environ. Exp. Bot. 2012, 75:89-97.
42. Sivaguru M., Horst W.J. The distal part of the transition zone is the most aluminum-sensitive apical root zone of maize. Plant Physiol. 1998, 116:155-163.
43. Doncheva S., Amenos M., Poschenrieder C., Barcelo J. Root cell patterning: a primary target for aluminium toxicity in maize. J. Exp. Bot. 2005, 56:1213-1220.
44. Illes P., Schlicht M., Pavlovkin J., Lichtscheidl I., Baluska F., Ovecka M. Aluminium toxicity in plants: internalization of aluminium into cells of the transition zone in Arabidopsis root apices related to changes in plasma membrane potential, endosomal behaviour, and nitric oxide production. J. Exp. Bot. 2006, 57:4201-4213.
45. Price A.H., Taylor A., Ripley S.J., Griffiths A., Trewavas A.J., Knight M.R. Oxidative signals in tobacco increase cytosolic calcium. Plant Cell 1994, 6:1301-1310.
46. Knight H., Knight M.R. Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci. 2001, 6:262-267.
47. Sanders D., Pelloux J., Brownlee C., Harper J.F. Calcium at the crossroads of signaling. Plant Cell 2002, 14:S401-S417.
48. Yan Y., Wei C-l., Zhang W-r., Cheng H-p., liu J. Cross-talk between calcium and reactive oxygen species signaling. Acta Pharmacol. Sin. 2006, 27:821-826.
49. Mittler R., Vanderauwera S., Gollery M., Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci. 2004, 9:490-498.
50. Levine A., Pennell R.I., Alvarez M.E., Palmer R., Lamb C. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr. Biol. 1996, 6:427-437.
51. Turner J.G., Novacky A. The quantitative relation between plant and bacterial cells involved in the hypersensitive reaction. Phytopathology 1974, 64:885-890.
52. Chang H.-B., Lin C.-W., Huang H.-J. Zinc induced cell death in rice (Oryza sativa L.) roots. Plant Growth Regul. 2005, 46:261-266.
53. Banu M.N.A., Hoque M.A., Watanabe-Sugimoto M., Matsuoka K., Nakamura Y., Shimoishi Y., Murata Y. Proline and glycinebetaine induce antioxidant defense gene expression and suppress cell death in cultured tobacco cells under salt stress. J. Plant Physiol. 2009, 166:146-156.
54. Cantoni O., Sestili P., Cattabeni F., Bellomo G., Pou S., Cohen M., Cerutti A.P. Calcium chelator Quin 2 prevents hydrogen-peroxide-induced DNA breakage and cytotoxicity. Eur. J. Biochem. 1989, 182:209-212.
55. Jones D.P., McConkey D.J., Nicotera P., Orrenius S. Calcium-activated DNA fragmentation in rat liver nuclei. J. Biol. Chem. 1989, 264:6398-6403.
56. Yakimova E.T., Kapchina-Toteva V.M., Woltering E.J. Signal transduction events in aluminum-induced cell death in tomato suspension cells. J. Plant Physiol. 2007, 164:702-708.
57. Amor Y., Babiychuk E., Inzee D., Levine A. The involvement of poly(ADP-ribose) polymerase in the oxidative stress responses in plants. FEBS Lett. 1998, 440:1-7.
58. Briggs A.G., Bent A.F. Poly(ADP-ribosyl)ation in plants. Trends Plant Sci. 2011, 16:372-380.
59. 2+. New Phytol. 2001, 151:185-194.
60. 2 production in leaves of maize (Zea mays) plants. New Phytol. 2007, 173:27-38.
61. Zheng K., Pan J.-W., Ye L., Fu Y., Peng H.-Z., Wan B.-Y., Gu Q., Bian H.-W., Han N., Wang J.-H., Kang B., Pan J.-H., Shao H.-H., Wang W.-Z., Zhu M.-Y. Programmed cell death-involved aluminum toxicity in yeast alleviated by antiapoptotic members with decreased calcium signals. Plant Physiol. 2007, 143:38-49.
62. Kinraide T.B. Aluminum enhancement of plant growth in acid rooting media. A case of reciprocal alleviation of toxicity by two toxic cations. Physiol. Plant. 1993, 88:619-625.
63. Clune T.S., Copeland L. Effects of aluminium on canola roots. Plant Soil 1999, 216:27-33.
64. Qin R., Jiao Y., Zhang S., Jiang W., Liu D. Effects of aluminum on nucleoli in root tip cells and selected physiological and biochemical characters in Allium cepa var. agrogarum L. BMC Plant Biol. 2010, 10:225. http://www.biomedcentral.com/1471-2229/10/225.
65. Culligan K., Tissier A., Britt A. ATR regulates a G2-phase cell-cycle checkpoint in Arabidopsis thaliana. Plant Cell 2004, 16:1091-1104.
66. Harper J.W., Elledge S.E. The DNA damage response: ten years after. Mol. Cell. 2007, 28:739-745.
67. Betti C., Davini T., Barale R. Genotoxicity of methyl mercury chloride and dimethyl mercury in human lymphocytes. Mutat. Res. 1992, 281:255-260.
68. Natarajan A.T., Palitti F. DNA repair and chromosomal alterations. Mutat. Res. 2008, 657:3-7.
69. Anuszewska E.L., Koziorowska J.H. Adaptive response towards adriamycin in vitro: circumvention with verapamil. Mutat. Res. 1999, 431:25-30.
70. Wojewodzka M., Walicka M., Sochanowicz B., Szumiel I. Calcium antagonist, TMB-8, prevents the induction of adaptive response by hydrogen peroxide or X-rays in human lymphocytes. Int. J. Radiat. Biol. 1994, 66:99-109.