Microcystin-LR induced oxidative stress and ultrastructural alterations in mesophyll cells of submerged macrophyte Vallisneria natans (Lour.) Hara

Journal of Hazardous Materials

Volumn 190, Issue 1-3, 2011, Pages 188-196

  Jiang, Jinlin ^a   Gu, Xueyuan ^a   Song, Rui ^a   Wang, Xiaorong ^a   Yang, Liuyan ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

Microcystin LR; Oxidative stress; Reactive oxygen species; Ultrastructure; Vallisneria natans (Lour.) Hara

Indexed keywords

ANTIOXIDANT RESPONSE; AQUATIC ENVIRONMENTS; AQUATIC PLANTS; BIOCHEMICAL EFFECTS; ECOLOGICAL IMPACTS; GLUTATHIONE-S-TRANSFERASE; GLUTATHIONES; MACROPHYTES; MALONDIALDEHYDE; MESOPHYLL CELLS; MICROCYSTIN-LR; MICROCYSTINS; MOLECULAR LEVELS; OXIDATIVE DAMAGE; PATTERN CHANGE; POTENTIAL RISKS; REACTIVE OXYGEN SPECIES; SUB-CELLULAR; SUPEROXIDE DISMUTASES; ULTRASTRUCTURE; VALLISNERIA;

ALDEHYDES; DETOXIFICATION; MAMMALS; PRINCIPAL COMPONENT ANALYSIS;

OXYGEN;

CATALASE; CHLOROPHYLL; GLUTATHIONE; GLUTATHIONE TRANSFERASE; MALONALDEHYDE; MICROCYSTIN LR; PEROXIDASE; SUPEROXIDE DISMUTASE;

AQUATIC ENVIRONMENT; CHEMICAL POLLUTANT; CYANOBACTERIUM; ENZYME ACTIVITY; INHIBITION; MACROPHYTE; OXIDATION; OXYGEN; PHYSIOLOGICAL RESPONSE; PHYTOTOXICITY; SUBMERGED VEGETATION; TOXICITY TEST; ULTRASTRUCTURE;

ARTICLE; CELL STRUCTURE; DETOXIFICATION; ENZYME ACTIVITY; ENZYME INHIBITION; LIPID PEROXIDATION; MACROPHYTE; MESOPHYLL CELL; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; VALLISNERIA NATANS;

CARCINOGENS; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUTATHIONE; GLUTATHIONE TRANSFERASE; MESOPHYLL CELLS; MICROCYSTINS; OXIDATIVE STRESS; PEROXIDASE; PLANTS; SUPEROXIDE DISMUTASE;

CYANOBACTERIA; VALLISNERIA NATANS;

EID: 79956089668     PISSN: 03043894     EISSN: 18733336     Source Type: Journal    
DOI: 10.1016/j.jhazmat.2011.03.023     Document Type: Article

References (49)

1. Codd G.A. Cyanobacterial toxins: occurrence, properties and biological significance. Water Sci. Technol. 1995, 32:149-156.
2. Sivonen K. Cyanobacterial toxins and toxin production. Phycologia 1996, 35:12-24.
3. Wu Q.L., Xie P., Yang L.Y., Gao G., Liu Z.W., Pan G., Zhu B.Z. Ecological consequences of cyanobacetrial blooms in lakes and their countermeasures. Adv. Earth Sci. (in Chinese) 2008, 23:1115-1123.
4. Dietrich D.R., Hoeger S.J. Guidance values for microcystin in water and cyanobacterial supplement products (blue-green algae supplements): a reasonable or misguided approach?. Toxicol. Appl. Pharmacol. 2005, 203:273-289.
5. Pérez S., Aga D.S. Recent advances in the sample preparation, liquid chromatography tandem mass spectrometric analysis and environmental fate of microcystins in water. TrAC Trends Anal. Chem. 2005, 24:658-670.
6. Lahti K., Rapala J., Färdig M., Niemelä M., Sivonen K. Persistence of cyanobacterial hepatotoxin microcystin-LR in particulate material and dissolved in lake water. Water Res. 1997, 31:1005-1012.
7. WHO Guidlines for drinking-water quality. Health Criteria and Other Supporting Information 1998, World Health Organization, Geneva, (addendum to vol. 2). Second ed.
8. Carmichael W.W. Cyanobacteria secondary metabolites-the cyanotoxins. J. Appl. Bacteriol. 1992, 72:445-459.
9. Casanova M.T., Burch M.D., Brock M.A., Bond P.M. Does toxic Microcystis aeruginosa affect aquatic plant establishment?. Environ. Toxicol. 1999, 14:97-109.
10. Körner S. Development of submerged macrophytes in the shallow Lake Müggelsee (Berlin, Germany) before and after its switch to the phytoplankton-dominated state. Arch. Hydrobiol. 2001, 152:395-409.
11. Wiegand C., Pflugmacher S. Ecotoxicological effects of selected cyanobacterial secondary metabolites a short review. Toxicol. Appl. Pharmacol. 2005, 203:201-218.
12. Pflugmacher S. Possible allelopathic effects of cyanotoxins, with reference to microcystin-LR, in aquatic ecosystems. Environ. Toxicol. 2002, 17:407-413.
13. Pflugmacher S. Promotion of oxidative stress in the aquatic macrophyte Ceratophyllum demersum during biotransformation of the cyanobacterial toxin microcystin-LR. Aquat. Toxicol. 2004, 70:169-178.
14. Pflugmacher S., Wiegand C., Oberemm A., Beattie K.A., Krause E., Codd G.A., Steinberg C.E.W. Identification of an enzymatically formed glutathione conjugate of the cyanobacterial hepatotoxin microcystin-LR: the first step of detoxication. Biochem. Biophys. Acta 1998, 1425:527-533.
15. Pflugmacher S., Wiegand C., Beattie K.A., Codd G.A., Steinberg C.E.W. Uptake of the cyanobacterial hepatotoxin microcystin-LR by aquatic macrophytes. J. Appl. Bot. 1999, 72:228-232.
16. Yin L.Y., Huang J.Q., Li D.H., Liu Y.D. Microcystin-RR uptake and its effects on the growth of submerged macrophyte Vallisneria natans (Lour.) Hara. Environ. Toxicol. 2005, 20:308-313.
17. Mackintosh C., Beattie K., Klumpp S., Cohen P., Codd G.A. Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants. FEBS Lett. 1990, 264:187-192.
18. Hu Z.Q., Liu Y.D., Li D.H., Dauta A. Growth and antioxydant system of the cyanobacterium Synechococcus elongatus in response to microcystin-RR. Hydrobiologia 2005, 534:23-29.
19. Pflugmacher S., Jung K., Lundvall L., Neumann S., Peuthert A. Effects of cyanobacterial toxins and cyanobacterial cell-free crude extract on germination of alfalfa (Medicago sativa) and induction of oxidative stress. Environ. Toxicol. Chem. 2006, 25:2381-2387.
20. Leflaive J., Hage-Ten L. Algal and cyanobacterial secondary metabolites in freshwaters: a comparison of allelopathic compounds and toxins. Freshwater Biol. 2007, 52:199-214.
21. Mitrovic S.M., Allis O., Furey A., James K.J. Bioaccumulation and harmful effects of microcystin-LR in the aquatic plants Lemna minor and Wolffia arrhiza and the filamentous alga Chladophora fracta. Ecotoxicol. Environ. Saf. 2005, 61:345-352.
22. Wang C., Zhang S.H., Wang P.F., Hou J., Li W., Zhang W.J. Metabolic adaptations to ammonia-induced oxidative stress in leaves of the submerged macrophyte Vallisneria natans (Lour.) Hara. Aquat. Toxicol. 2008, 87:88-98.
23. Aranda-Rodriguez R., Tillmanns A., Benoit F.M., Pick F.R., Harvie J., Solenaia L. Pressurized liquid extraction of toxins from cyanobacterial cells. Environ. Toxicol. 2005, 20:390-396.
24. Lynch D.V., Thompson J.E. Lipoxygenase-mediated production of superoxide anion in senescing plant tissue. FEBS Lett. 1984, 173:251-254.
25. Giannopolitis C.N., Ries A.K. Superoxide dismutase. I. Occurrence in higher plants. Plant Physiol. 1977, 59:309-314.
26. Bestwick C.S., Adam A.L., Puri N., Mansfield J.W. Characterisation of and changes to pro- and anti-oxidant enzyme activities during the hypersensitive reaction in lettuce (Lactuca satia L.). Plant Sci. 2001, 161:497-506.
27. Kochharm S., Kochhar V.K., Khanduja S.D. Changes in the pattern of isoperoxidases during maturation of grape berries cv. Gulabi as affected by ethephon (2-chloroethyl phosphoric acid). Am. J. Enol. Vitic. 1979, 30:275-277.
28. Habig W.H., Pabst M.J., Jakoby W.B. Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. J. Biol. Chem. 1974, 249:7130-7139.
29. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
30. Hissin P.J., Hilf R. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal. Biochem. 1976, 74:214-226.
31. Porra R.J., Thompson W.A., Kriedemann P.E. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 1989, 975:384-394.
32. Bowler C., Montagu M.V., Inze D. Superoxide dismutase and stress tolerance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1992, 43:83-116.
33. Takeshita K., Fujii K., Anzai K. In vivo monitoring of hydroxyl radical generation caused by X-ray irradiation of rats using the spin trapping/EPR technique. Free Radic. Biol. Med. 2004, 36:1134-1143.
34. Cadenas E. Biochemistry of oxygen toxicity. Annu. Rev. Biochem. 1989, 58:79-110.
35. Pflugmacher S., Aulhorn M., Grimm B. Influence of a cyanobacterial crude extract containing microcystin-LR on the physiology and antioxidative defence systems of different spinach variants. New Phytol. 2007, 175:482-489.
36. Stüven J., Pflugmacher S. Antioxidative stress response of Lepidium sativum due to exposure to cyanobacterial secondary metabolites. Toxicon 2007, 50:85-93.
37. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 2002, 7:405-410.
38. Yin Y, Wang X.R., Sun Y.Y., Guo H.Y., Yin D.Q. Bioaccumulation and oxidative stress in submerged macrophyte Ceratophyllum demersum L. upon exposure to pyrene. Environ. Toxicol. 2007, 23:328-336.
39. Asada K. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999, 50:601-639.
40. Pflugmacher S., Codd G.A., Steinberg C.E.W. Effects of the cyanobacterial toxin microcystin-LR on detoxication enzymes in aquatic plants. Environ. Toxicol. 1999, 14:111-115.
41. Takenaka S. Covalent glutathione conjugation to cyanobacterial hepatotoxin microcystin-LR by F344 rat cytosolic and microsomal glutathione S-transferases. Environ. Toxicol. Pharmacol. 2001, 9:135-139.
42. Ding W.X., Shen H.M., Ong C.N. Microcystic cyanobacteria extract induces cytoskeletal disruption and intracellular glutathione alteration in hepatocytes. Environ. Health Perspect. 2000, 108:605-609.
43. Amado L.L., Monserrat J.M. Oxidative stress generation by microcystins in aquatic animals: why and how. Environ. Int. 2010, 36:226-235.
44. Gutteridge J.M.C., Halliwell B. The measurement and mechanism of lipid peroxidation in biological systems. Trends Biochem. Sci. 1990, 35:129-135.
45. Wang C.R., Wang X.R., Tian Y., Yu H.X., Gu X.Y., Du W.C., Zhou H. Oxidative stress, defense response, and early biomarkers for lead-contaminated soil in Vicia faba seedlings. Environ. Toxicol. Chem. 2008, 27:970-977.
46. Gehringer M.M. Microcystin-LR and okadaic acid-induced cellular effects: a dualistic response. FEBS Lett. 2004, 557:1-8.
47. Coleman J.O.D., Blakekalff M.M.A., Davis T.G.E. Detoxification of xenobiotics by plants: chemical modifications and vacuolar compartmentation. Trends Plant Sci. 1997, 2:144-151.
48. Huang W.M., Xing W., Li D.H., Liu Y.D. Microcystin-RR induced apoptosis in tobacco BY-2 suspension cells is mediated by reactive oxygen species and mitochondrial permeability transition pore status. Toxicol. In Vitro 2008, 22:328-337.
49. Campos A., Vasconcelos V. Molecular mechanisms of microcystin toxicity in animal cells. Int. J. Mol. Sci. 2010, 11:268-287.