Biomarkers of prolonged exposure to microcystin-LR in mice

Toxicon

Volumn 68, Issue , 2013, Pages 9-17

  Sedan, Daniela ^b   Giannuzzi, Leda ^a,b   Rosso, Lorena ^b   Marra, Carlos Alberto ^c   Andrinolo, Darío ^b  

^a CENTRO DE INVESTIGACIÓN Y DESARROLLO EN CRIOTECNOLOGÍA DE ALIMENTOS CIDCA   (Argentina)

^b FACULTAD DE CIENCIAS EXACTAS   (Argentina)

^c INSTITUTO DE INVESTIGACIONES BIOQUÍMICAS DE LA PLATA INIBIOLP   (Argentina)

Author keywords

Biomarkers; Mice; Microcystins; Prolonged exposure

Indexed keywords

ALPHA TOCOPHEROL; BIOLOGICAL MARKER; CATALASE; GLUTATHIONE; HEMOGLOBIN; HYDROPEROXIDE; LIPID; METHEMOGLOBIN; MICROCYSTIN LR; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE MARKER; ERYTHROCYTE; FECES; HEMOGLOBIN BLOOD LEVEL; INTOXICATION; KIDNEY; LIPID BLOOD LEVEL; LIVER; LONG TERM EXPOSURE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; URINE;

ALPHA-TOCOPHEROL; ANIMALS; ANTIOXIDANTS; BIOLOGICAL MARKERS; CATALASE; ERYTHROCYTES; GLUTATHIONE; HEMOGLOBINS; HYDROGEN PEROXIDE; KIDNEY; LIPIDS; LIVER; MALE; METHEMOGLOBIN; MICE; MICROCYSTINS; OXIDATIVE STRESS; SPECIFIC PATHOGEN-FREE ORGANISMS; SUPEROXIDE DISMUTASE;

ANIMALIA; MUS;

EID: 84875798770     PISSN: 00410101     EISSN: 18793150     Source Type: Journal    
DOI: 10.1016/j.toxicon.2013.03.002     Document Type: Article

References (76)

1. Aebi H. Oxygen radicals in biological systems. Meth. Enzymol. 1984, 105:121-126. Nutr. Res. 22: 1265-1273.
2. Allain C.C., Poon L.S., Chan C.S., Richmond W., Fu P.C. Enzymatic determination of total serum cholesterol. Clin. Chem. 1974, 20:470-475.
3. Amstrong B. The epidemiology of cancer in the people of China. Int. J. Epidemiol. 1980, 9:305-315.
4. Andrinolo D., Sedan D., Telese L., Aura C., Masera S., Giannuzzi L., Marra C., Alaniz M.T. Recovery after damage produced by subchronic intoxication with the cyanotoxin microcystin LR. Toxicon 2008, 51:457-467.
5. Annadotter H., Cronberg G., Lawton L., Hansson H.B., Göthe U., Skulberg O.M. An extensive outbreak of gastroenteritis associated with the toxic cyanobacterium planktothrix agardhii (oscillatoriales, cyanophyceae) in Scania, South Sweden. Cyanotoxins 2001, 200-208. Springer, Berlin. I. Chorus (Ed.).
6. Asensi M., Sastre J., Pallardo F.V., García de la Asunción J., Estrela J.M., Viña J. A high-performance liquid chromatography method for measurement of oxidized glutathion in biological samples. Anal. Biochem. 1994, 217:323-328.
7. Barco M., Rivera J., Caixach J. Analysis of cyanobacterial hepatotoxins in water samples by microbore reversed-phase liquid chromatography-electrospray ionisation mass spectrometry. J. Chromatogr. A 2002, 959:103-111.
8. Bell S.G., Codd G.A. Cyanobacterial toxins and human health. Rev. Med. Microbiol. 1994, 5(4):256-264.
9. Bradford M.M. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal. Biochem. 1976, 72:248-254.
10. Brigelius R., Muckel C., Akerboom T.P., Sies H. Identification and quantitation of glutathione in hepatic protein mixed disulfides and its relationship to glutathione disulfide. Biochem. Pharmacol. 1983, 32:2529-2534.
11. Buttriss J.L., Diplock A.T. High-performance liquid chromatography methods for vitamin E in tissues. Methods Enzymol. 1984, 105:131-138.
12. Carmichael W.W. The toxins of cyanobacteria. Sci. Am. 1994, 270(1):78-86.
13. Carmichael W.W. The cyanotoxins. Advances in Botanical Research 1997, vol. 27:211-256. Academic Press, London.
14. Cazenave J., Bistoni M.A., Pesce S.F., Wunderlin D.A. Differential detoxification and antioxidant response in diverse organs of Corydoras paleatus exposed to Microcystin-RR. Aquat. Toxicol. 2006, 76:1-12.
15. Chen P.S., Toribara T.Y., Warner H. Microdetermination of phosphorus. Anal. Chem. 1956, 28:1756-1758.
16. Chen Y.M., Lee T.H., Lee S.J., Huang H.B., Huang R., Chou H.N. Comparison of protein phosphatase inhibition activities and mouse toxicities of microcystins. Toxicon 2006, 47:742-746.
17. Chen J., Xie P., Li L., Jun X. First identification of the hepatotoxic microcystins in the serum of a chronically exposed human population together with indication of hepatocellular damage. Toxicol. Sci. 2009, 108:81-89.
18. Cheng T.Y., Zhu Z., Masuda S., Morcos N.C. Effects of multinutrient supplementation on antioxidant defence systems in healthy human being. J. Nutr. Biochem. 2001, 12:388-395.
19. Craig M., Luu H.A., McCready T.L., Williams D., Andersen R.J., Holmes C.F. Molecular mechanisms underlying the interaction of motuporin and microcystins with type-1 and type-2A protein phosphatases. Biochem. Cell. Biol. 1996, 74:569-578.
20. Dietrich D., Ernest B., Day B. Human consumer death and algal supplement consumption: a post mortem assessment of potential microcystin-intoxication via microcystin inmunohistochemical (MC-IHC) analyses. Oral Presentation 7th International Conference of Toxic Cyanobacteria 2007, Brasil; 132.
21. Ding W., Ong C. Role of oxidative stress and mitochondrial changes in cyanobacteria-induced apoptosis and hepatotoxicity. FEMS Microbiol. Lett. 2003, 220:1-7.
22. Ding W.X., Shen H.M., Zhu H.G., Ong C.N. Studies on oxidative damage induced by cyanobacteria extract in primary cultured rat hepatocytes. Environ. Res. 1998, 78(1):12-18.
23. Ding W.X., Shen H.M., Zhu H.G., Lee B.L., Ong C.N. Genotoxicity of microcystic cyanobacteria extract of a water source in China. Mutat. Res. 1999, 442:69-77.
24. 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(7):605-609.
25. Ding W.X., Shen H.M., Ong C.N. Pivotal role of mitochondrial Ca(2+) in microcystin-induced mitochondrial permeability transition in rat hepatocytes. Biochem. Biophys. Res. Commun. 2001, 285(5):1155-1161.
26. Evelyn K.A., Malloy H.T. Microdetermination of oxyhemoglobin, methemoglobin and sulphemoglobin in a single sample of blood. J. Biol. Chem. 1938, 126:655-662.
27. Falconer I.R. Tumor promotion and liver injury caused by oral consumption of cyanobacteria. Environ. Toxicol. Water Qual. 1991, 6:177-184.
28. Falconer I.R., Humpage A.R. Tumor promotion by cyanobacterial toxins. Phycologia 1996, 35(6):74-79.
29. Flohé L., Ötting F. Superoxide dismutase assays. Methods Enzymol. 1984, 105:93-104.
30. Folch J., Lees M., Sloane Stanley G.H. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 1957, 226:497-509.
31. Gehringer M.M. Microcystin-LR and okadaic acid-induced cellular effects: a dualistic response. FEBS Lett. 2004, 57(1-3):1-8.
32. Giannuzzi L., Sedan D., Echenique R., Andrinolo D. An acute case of intoxication with cyanobacteria and cyanotoxins in recreational water in Salto Grande Dam, Argentina. Mar. Drugs 2011, 9.
33. Guzman R.E., Solter P.F. Characterization of sublethal MCLR exposure in mice. Vet. Pathol. 2002, 39(1):17-26.
34. Guzman R.E., Solter P.F., Runnegar M.T. Inhibition of nuclear protein phosphatase activity in mouse hepatocytes by the cyanobacterial toxin microcystin-LR. Toxicon 2003, 41(7):773-781.
35. Hooser S.B., Beasley V.R., Waite L.L., Kuhlenschmidt M.S., Carmichael W.W., Haschek W.M. Actin filament alterations in rat hepatocytes induced invivo and invitro by microcystin-LR, a hepatotoxin from the blue-green alga, Microcystis aeruginosa. Vet. Pathol. 1991, 28(4):259-266.
36. Ishii M., Washioka H., Tonosaki A., Toyota T. Regional orientation of actin filaments in the pericanalicular cytoplasm of rat hepatocytes. Gastroenterology 1991, 101:1663-1672.
37. Ito E., Kondo F., Terao K., Harada K. Neoplastic nodular formation in mouse liver induced by repeated intraperitoneal injections of MCLR. Toxicon 1997, 35(9):1453-1457.
38. Jochimsen E.M., Carmichael W.W., An J., Denise M.C., Cookson S.T., Holmes C.E.M., Antunes M.B.C., Melo F.D.A., Lyra T.M., Barreto V.S.T., Azevedo S.M.F.O., Jarvis W.R. Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. N. Engl. J. Med. 1998, 338(13):873-878.
39. Kondo F., Matsumoto H., Yamada S., Ishikawa N., Ito E., Nagata S., Ueno Y., Suzuki M., Harada K. Detection and identification of metabolites of microcystins formed invivo in mouse and rat livers. Chem. Res. Toxicol. 1996, 9:1355-1359.
40. Kritchevsky D., Davidson L.M., Kim H.K., Malhotra S. Quantitation of serum lipids by a simple TLC-charring method. Clin. Chim. Acta 1973, 46:63-68.
41. Lezcano N., Sedan D., Lucotti I., Giannuzzi L., Vittone L., Andrinolo D., Mundiña-Weilenmann C. Subchronic Microcystin-LR exposure increased hepatic apoptosis and induced compensatory mechanisms in mice. J. Biochem. Mol. Toxicol. 2012, 26(4):131-138.
42. Lippy E.C., Erb J. Gastrointestinal illness at Sewickley, PA. J. Am. Water Works Assoc. 1976, 68:606-610.
43. Lowe J., Souza-Menezes J., Freire D.S., Mattos L.J., Castiglione R.C., Barbosa C.M.L., Santiago L., Ferrão F.M., Cardoso L.H.D., da Silva R.T., Vieira-Beiral H.J., Vieyra A., Morales M.M., Azevedo S.M.F.O., Soares R.M. Single sublethal dose of microcystin-LR is responsible for different alterations in biochemical, histological and physiological renal parameters. Toxicon 2012, 59:601-609.
44. MacKintosh R.W., Dalby K.N., Campbell D.G., Cohen P.T., Cohen P., MacKintosh C. The cyanobacterial toxin microcystin binds covalently to cysteine-273 on protein phosphatase 1. FEBS Lett. 1995, 371:236-240.
45. Marra C.A., de Alaniz M.J.T. Incorporation and metabolic conversión of saturated and unsaturated fatty acids in SK-Hep1 human hepatoma cells in culture. Mol. Cell. Biochem. 1992, 117:107-118.
46. Marra C.A., Zaidenmerg A., de Alaniz M.J.T., Buschiazzo H. The restoring effect of trifluralin and benznidazole on the abnormal fattyacid pattern induced by Trypanosoma cruzi in the liver microsomes of infected mice. Ann. Trop. Med. Pharmacol. 2002, 96:249-264.
47. Moreno I., Repetto G., y Cameán A. Interés toxicológico de las microcistinas. Rev. Toxicol. 2003, 20:159-165.
48. Morrison W.R., Smith L.M. Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoride-methanol. J. Lipid Res. 1964, 5:600-608.
49. Nakamura K., Handa S. Coomasie brilliant blue staining of lipids on thin-layer plates. Anal. Biochem. 1984, 142:406-410.
50. National Research Council Guide for the Use and Care of Laboratory Animals 1985, Publication No. 85-23 (rev.), National Institutes of Health, Bethesda, MD.
51. Nourooz-Zadeh J., Tajaddimi-Sarmandi J., McCarthy S., Betteridge D.J., Wolff S.P. Elevated levels of authentic plasma hydroperoxides in NIDDM. Diabetes 1995, 44:1054-1058.
52. Ohta T., Nishiwaki R., Yatsunami J., Komori A., Suganuma M., Fujiki H. Hyperphosphorylation of cytokeratins 8 and 18 by microcystin-LR, A new liver tumor promotor, in primary cultures of rats. Carcinogenesis 1992, 13:2443-2447.
53. Rahman T., Kode A., Biswas S.K. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat. Protoc. 2006, 1:3159-3165.
54. Robinson N.A., Pace J.G., Matson C.F., Miura G.A., Lawrence W.B. Tissue distribution, excretion and hepatic biotransformation of MCLR in mice. J. Pharmacol. Exp. Ther. 1991, 256(1):176-182.
55. Runnegar M.T.C., Andrews J., Gerdes R.G., Falconer I.R. Injury to hepatocytes induced by a peptide toxin from the cyanobacterium Microcystis aeruginosa. Toxicon 1987, 25:1235-1239.
56. Runnegar M., Berndt N., Kaplowitz N. Microcystin uptake and inhibition of protein phosphatases: effects of chemoprotectants and self-inhibition in relation to known hepatic transporters. Toxicol. Appl. Pharmacol. 1995, 134:264-272.
57. Sedan D., Andrinolo D., Telese L., Giannuzzi L., Alaniz M.T., Marra C.A. Alteration and recovery of the antioxidant system induced by sub-chronic exposure to microcystin-LR in mice: its relation to liver lipid composition. Toxicon 2010, 55:333-342.
58. Sicinska P., Bukowska B., Michałowicz J., Duda W. Damage of cell membrane and antioxidative system in human erythrocytes incubated with microcystin-LR invitro. Toxicon 2006, 47:387-397.
59. Sivonen K., Jones G. Cyanobacterial toxins. Toxic Cyanobacteria in Water: a Guide to Public Health Significance, Monitoring and Management 1999, Chorus, J. Bertram (Eds.).
60. Soares R., Yuan M., Servaites J., Delgado A., Magalhaes V., Hilborn E., Carmichael W., Azevedo S. Sublethal exposure from microcystins to renal insufficiency patients in Rio de Janeiro, Brazil. Environ. Toxicol. 2006, 21:95-103.
61. Soares R., Cagido V., Ferraro R., Meyer-Fernandes J., Rocco P., Zin W., Azevedo S. Effects of microcystin-LR on mouse lungs. Toxicon 2007, 50:330-338.
62. Solter P., Wollenberg G., Huang X., Chu F., Runnegar M. Prolonged sublethal exposure to the protein phosphatase inhibitor, microcystin-LR results in multiple dosedependant hepatotoxic effects. Toxicol. Sci. 1998, 44:87-96.
63. Teixera M., Costa M., Carvalho V., Pereira M., Hage E. Gastroenteritis epidemic in the area of the Itaparica Dam, Bahia, Brazil. Bull. Pan Am. Health Org. 1993, 27:244-253.
64. Tisdale J. Epidemic of intestinal disorders in Charleston (West Virginia) occurring simultaneously with unprecedented water supply conditions. Am. J. Pub Health 1931, 21:198-200.
65. Toivola D.M., Eriksson J.E., Brautigan D.L. Identification of protein phosphatase 2A as the primary target for microcystin-LR in rat liver homogenates. FEBS Lett. 1994, 344:175-180.
66. Turner P.C., Gammie A.J., Hollinrake K., Codd G.A. Pneumonia associated with cyanobacteria. Br. Med. J. 1990, 300:1440-1441.
67. WHO Guidelines for Drinking-water Quality. Recommendations Chemical Fact. Sheets 2004, vol. 1:407-408. World Health Organization, Geneva, Switzerland. third ed.
68. Williams D.E., Craig M., Dawe S.C., Kent M.L., Holmes C.F.B., Andersen R.J. Evidence for a covalently bound form of microcystin-LR in salmon liver and dungeness crab larvae. Chem. Res. Toxicol. 1997, 10:463-469.
69. Xia Primary Liver Cancer 2002, 30:674-682. China Academic Publishers, New York.
70. Yanamoto K., Shibahara A., Nakayama T., Kajimoto G. Determination of double-bond positions in methylene-interrupted dienoic fatty acids by GC-MS as their dimethyl disulfide adducts. Chem. Phys. Lipids 1991, 60:39-50.
71. Yoshizawa S., Matsushima R., Watanabe M.F., Harada K., Ichihara A., Carmichael W.W., Fujiki H. Inhibition of protein phosphatases by microcystis and nodularin associated with hepatotoxicity. J. Cancer Res. Clin. Oncol. 1990, 116(6):609-614.
72. Yu S. Drinking water and primary liver cancer. Primary Liver Cancer 1989, 30-37. Spring-Verlag, Berlin. Z. Tang, M. Wu, S.-S. Xia (Eds.).
73. Yu S.-J. Primary prevention of hepatocellular carcinoma. J. Gastroenterol. Hepatol. 1995, 10:674-682.
74. Zhang X., Xie P., Lia D., Shi Z. Hematological and plasma biochemical responses of crucian carp (Carassius auratus) to intraperitoneal injection of extracted microcystins with the possible mechanisms of anemia. Toxicon 2007, 49:1150-1157.
75. Zhao Y., Xieb P., Zhang X. Oxidative stress response after prolonged exposure of domestic rabbit to a lower dosage of extracted microcystins. Environ. Toxicol. Pharmacol. 2009, 27:195-199.
76. Zilberg B. Gastroenteritis in Salisbury European children - a five year study. Centr Afr. J. Med. 1966, 12:164-168.