Microcystin-LR-Caused ROS generation involved in p38 activation and tau hyperphosphorylation in neuroendocrine (PC12) cells

Environmental Toxicology

Volumn 30, Issue 3, 2015, Pages 366-374

  Meng, Guanmin ^a,b   Liu, Jinghui ^b   Lin, Shuyan ^b   Guo, Zonglou ^c   Xu, Lihong ^b  

^a TONGDE HOSPITAL OF ZHEJIANG PROVINCE   (China)

^b ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c ZHEJIANG UNIVERSITY   (China)

Author keywords

Microcystin LR; P38 mitogen activated protein kinase; Reactive oxygen species; Tau hyperphosphorylation

Indexed keywords

CELL CULTURE; ENZYMES; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES;

CONCENTRATION-DEPENDENT; HYPERPHOSPHORYLATION; MICROCYSTIN-LR; MICROTUBULE ASSOCIATED PROTEIN; N-ACETYLCYSTEINE; P38 MITOGEN-ACTIVATED PROTEIN KINASE; REDOX SENSITIVES; TAU HYPERPHOSPHORYLATION;

CHEMICAL ACTIVATION;

ACETYLCYSTEINE; ASCORBIC ACID; MICROCYSTIN LR; MICROTUBULE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE; TAU PROTEIN; ANTIOXIDANT; MICROCYSTIN;

ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVATION; ENZYME INDUCTION; HUMAN; HUMAN CELL; MALE; NEUROSECRETORY CELL; OXIDATION REDUCTION REACTION; PC12 CELL LINE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ANIMAL; METABOLISM; PHOSPHORYLATION; RAT;

CYANOBACTERIA;

ANIMALS; ANTIOXIDANTS; MICROCYSTINS; OXIDATION-REDUCTION; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PC12 CELLS; PHOSPHORYLATION; RATS; REACTIVE OXYGEN SPECIES; TAU PROTEINS;

EID: 84921743473     PISSN: 15204081     EISSN: 15227278     Source Type: Journal    
DOI: 10.1002/tox.21914     Document Type: Article

References (60)

1. Ahn J, Won M, Choi JH, Kim YS, Jung CR, Im DS, Kyun ML, Lee K, Song KB, Chung KS. 2013. Reactive oxygen species-mediated activation of the Akt/ASK1/p38 signaling cascade and p21(Cip1) downregulation are required for shikonin-induced apoptosis. Apoptosis 18:870-881.
2. Asuni AA, Perry VH, O'Connor V. 2010. Change in tau phosphorylation associated with neurodegeneration in the ME7 model of prion disease. Biochem Soc Trans 38:545-551.
3. Ballatore C, Lee VM, Trojanowski JQ. 2007. Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nat Rev Neurosci 8:663-672.
4. Cai T, Che H, Yao T, Chen Y, Huang C, Zhang W, Du K, Zhang J, Cao Y, Chen J, Luo W. 2011. Manganese induces tau hyperphosphorylation through the activation of ERK MAPK pathway in PC12 cells. Toxicol Sci 119:169-177.
5. Campos A, Vasconcelos V. 2010. Molecular mechanisms of microcystin toxicity in animal cells. Int J Mol Sci 11:268-287.
6. Cao M, Liu F, Ji F, Liang J, Liu L, Wu Q, Wang T. 2013. Effect of c-Jun N-terminal kinase (JNK)/p38 mitogen-activated protein kinase (p38 MAPK) in morphine-induced tau protein hyperphosphorylation. Behav Brain Res 237:249-255.
7. Chen L, Liu L, Huang S. 2008a. Cadmium activates the mitogen-activated protein kinase (MAPK) pathway via induction of reactive oxygen species and inhibition of protein phosphatases 2A and 5. Free Radic Biol Med 45:1035-1044.
8. Chen S, Li B, Grundke-Iqbal I, Iqbal K. 2008b. I1PP2A affects tau phosphorylation via association with the catalytic subunit of protein phosphatase 2A. J Biol Chem 283:10513-10521.
9. Chen HC, Su LT, Gonzalez-Pagan O, Overton JD, Runnels LW. 2012. A key role for Mg(2+) in TRPM7's control of ROS levels during cell stress. Biochem J 445:441-448.
10. Chen L, Zhang X, Zhou W, Qiao Q, Liang H, Li G, Wang J, Cai F. 2013. The Interactive Effects of Cytoskeleton Disruption and Mitochondria Dysfunction Lead to Reproductive Toxicity Induced by Microcystin-LR. PLoS One 8:e53949.
11. Cleveland DW, Hwo SY, Kirschner MW. 1977. Purification of tau, a microtubule-associated protein that induces assembly of microtubules from purified tubulin. J Mol Biol 116:207-225.
12. D'Autréaux B, Toledano MB. 2007. ROS as signalling molecules: Mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8:813-824.
13. Ding WX, Shen HM, Ong CN. 2000. Microcystic cyanobacteria extract induces cytoskeletal disruption and intracellular glutathione alteration in hepatocytes. Environ Health Perspect 108:605-609.
14. Ding WX, Shen HM, Ong CN. 2001. Critical role of reactive oxygen species formation in microcystin-induced cytoskeleton disruption in primary cultured hepatocytes. J Toxicol Environ Health A 64:507-519.
15. Ferrer I, Gomez-Isla T, Puig B, Freixes M, Ribé E, Dalfó E, Avila J. 2005. Current advances on different kinases involved in tau phosphorylation, and implications in Alzheimer's disease and tauopathies. Curr Alzheimer Res 2:3-18.
16. Forman HJ, Maiorino M, Ursini F. 2010. Signaling functions of reactive oxygen species. Biochemistry 49:835-842.
17. Gómez-Ramos A, Díaz-Nido J, Smith MA, Perry G, Avila J. 2003. Effect of the lipid peroxidation product acrolein on tau phosphorylation in neural cells. J Neurosci Res 71:863-870.
18. Gong CX, Iqbal K. 2008. Hyperphosphorylation of microtubule-associated protein tau: A promising therapeutic target for Alzheimer disease. Curr Med Chem 15:2321-2328.
19. He H, Zang LH, Feng YS, Chen LX, Kang N, Tashiro S, Onodera S, Qiu F, Ikejima T. 2013. Physalin A induces apoptosis via p53-Noxa-mediated ROS generation, and autophagy plays a protective role against apoptosis through p38-NF-kappaB survival pathway in A375-S2 cells. J Ethnopharmacol 148:544-555.
20. Hertze J, Palmqvist S, Minthon L, Hansson O. 2013. Tau pathology and parietal white matter lesions have independent but synergistic effects on early development of Alzheimer's disease. Dement Geriatr Cogn Dis Extra 3:113-122.
21. Ho SY, Wu WJ, Chiu HW, Chen YA, Ho YS, Guo HR, Wang YJ. 2011. Arsenic trioxide and radiation enhance apoptotic effects in HL-60 cells through increased ROS generation and regulation of JNK and p38 MAPK signaling pathways. Chem Biol Interact 193:162-171.
22. Iqbal K, Liu F, Gong CX, Alonso Adel C, Grundke-Iqbal I. 2009. Mechanisms of tau-induced neurodegeneration. Acta Neuropathol 118:53-69.
23. Jenkins SM, Zinnerman M, Garner C, Johnson GV. 2000. Modulation of tau phosphorylation and intracellular localization by cellular stress. Biochem J 345 (Pt 2):263-270.
24. Kim DH, Lee JH, Park S, Oh SS, Kim S, Kim DW, Park KH, Kim KD. 2013. 6-Acetonyl-5, 6-dihydrosanguinarine (ADS) from Chelidonium majus L. triggers proinflammatory cytokine production via ROS-JNK/ERK-NFkappaB signaling pathway. Food Chem Toxicol 58:273-279.
25. Komatsu M, Furukawa T, Ikeda R, Takumi S, Nong Q, Aoyama K, Akiyama S, Keppler D, Takeuchi T. 2007. Involvement of mitogen-activated protein kinase signaling pathways in microcystin-LR-induced apoptosis after its selective uptake mediated by OATP1B1 and OATP1B3. Toxicol Sci 97:407-416.
26. Lee VM, Goedert M, Trojanowski JQ. 2001. Neurodegenerative tauopathies. Annu Rev Neurosci 24:1121-1159.
27. Lee H, Perry G, Moreira P, Garrett M, Liu Q, Zhu X, Takeda A, Nunomura A, Smith M. 2005. Tau phosphorylation in Alzheimer's disease: Pathogen or protector? Trends Mol Med 11:164-169.
28. Li HL, Wang HH, Liu SJ, Deng YQ, Zhang YJ, Tian Q, Wang XC, Chen XQ, Yang Y, Zhang JY, Wang Q, Xu H, Liao FF, Wang JZ. 2007. Phosphorylation of tau antagonizes apoptosis by stabilizing beta-catenin, a mechanism involved in Alzheimer's neurodegeneration. Proc Natl Acad Sci USA 104:3591-3596.
29. Li ZY, Yang Y, Ming M, Liu B. 2011. Mitochondrial ROS generation for regulation of autophagic pathways in cancer. Biochem Biophys Res Commun 414:5-8.
30. Li G, Cai F, Yan W, Li C, Wang J. 2012a. A proteomic analysis of MCLR-induced neurotoxicity: Implications for Alzheimer's disease. Toxicol Sci 127:485-495.
31. Li T, Ying L, Wang H, Li N, Fu W, Guo Z, Xu L. 2012b. Microcystin-LR induces ceramide to regulate PP2A and destabilize cytoskeleton in HEK293 cells. Toxicol Sci 128:147-157.
32. Li G, Yan W, Cai F, Li C, Chen N, Wang J. Spatial learning and memory impairment and pathological change in rats induced by acute exposure to microcystin-LR. Environ Toxicol (in press).
33. Liang J, Li T, Zhang YL, Guo ZL, Xu LH. 2011. Effect of microcystin-LR on protein phosphatase 2A and its function in human amniotic epithelial cells. J Zhejiang Univ Sci B 12:951-960.
34. Liu F, Grundke-Iqbal I, Iqbal K, Gong CX. 2005. Contributions of protein phosphatases PP1, PP2A, PP2B and PP5 to the regulation of tau phosphorylation. Eur J Neurosci 22:1942-1950.
35. Liu CM, Sun YZ, Sun JM, Ma JQ, Cheng C. 2012a. Protective role of quercetin against lead-induced inflammatory response in rat kidney through the ROS-mediated MAPKs and NF-κB pathway. Biochim Biophys Acta 1820:1693-1703.
36. Liu L, Fu J, Li T, Cui R, Ling J, Yu X, Ji H, Zhang Y. 2012b. NG, a novel PABA/NO-based oleanolic acid derivative, induces human hepatoma cell apoptosis via a ROS/MAPK-dependent mitochondrial pathway. Eur J Pharmacol 691:61-68.
37. MacKintosh C, Beattie KA, Klumpp S, Cohen P, Codd GA. 1990. Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants. FEBS Lett 264:187-192.
38. Melov S, Adlard PA, Morten K, Johnson F, Golden TR, Hinerfeld D, Schilling B, Mavros C, Masters CL, Volitakis I, Li QX, Laughton K, Hubbard A, Cherny RA, Gibson B, Bush AI. 2007. Mitochondrial oxidative stress causes hyperphosphorylation of tau. PLoS One 2:e536.
39. Meng G, Sun Y, Fu W, Guo Z, Xu L. 2011. Microcystin-LR induces cytoskeleton system reorganization through hyperphosphorylation of tau and HSP27 via PP2A inhibition and subsequent activation of the p38 MAPK signaling pathway in neuroendocrine (PC12) cells. Toxicology 290:218-229.
40. Mezhoud K, Praseuth D, Puiseux-Dao S, François JC, Bernard C, Edery M. 2008. Global quantitative analysis of protein expression and phosphorylation status in the liver of the medaka fish (Oryzias latipes) exposed to microcystin-LR I. Balneation study. Aquat Toxicol 86:166-175.
41. Puerto M, Pichardo S, Jos A, Camean AM. 2009. Oxidative stress induced by microcystin-LR on PLHC-1 fish cell line. Toxicol In Vitro 23:1445-1449.
42. Qiu T, Xie P, Liu Y, Li G, Xiong Q, Hao L, Li H. 2009. The profound effects of microcystin on cardiac antioxidant enzymes, mitochondrial function and cardiac toxicity in rat. Toxicology 257:86-94.
43. Rametti A, Esclaire F, Yardin C, Terro F. 2004. Linking alterations in tau phosphorylation and cleavage during neuronal apoptosis. J Biol Chem 279:54518-54528.
44. Rudrabhatla P, Pant HC. 2011. Role of protein phosphatase 2A in Alzheimer's disease. Curr Alzheimer Res 8:623-632.
45. Smith MA, Casadesus G, Joseph JA, Perry G. 2002. Amyloid-beta and tau serve antioxidant functions in the aging and Alzheimer brain. Free Radic Biol Med 33:1194-1199.
46. Son Y, Cheong YK, Kim NH, Chung HT, Kang DG, Pae HO. 2011. Mitogen-Activated Protein Kinases and Reactive Oxygen Species: How Can ROS Activate MAPK Pathways? J Signal Transduct 2011:792639.
47. Sontag E, Nunbhakdi-Craig V, Lee G, Bloom GS, Mumby MC. 1996. Regulation of the phosphorylation state and microtubule-binding activity of Tau by protein phosphatase 2A. Neuron 17:1201-1207.
48. Su B, Wang X, Lee HG, Tabaton M, Perry G, Smith MA, Zhu X. 2010. Chronic oxidative stress causes increased tau phosphorylation in M17 neuroblastoma cells. Neurosci Lett 468:267-271.
49. Sun X, Mi L, Liu J, Song L, Chung FL, Gan N. 2011a. Sulforaphane prevents microcystin-LR-induced oxidative damage and apoptosis in BALB/c mice. Toxicol Appl Pharmacol 255:9-17.
50. Sun Y, Meng GM, Guo ZL, Xu LH. 2011b. Regulation of heat shock protein 27 phosphorylation during microcystin-LR-induced cytoskeletal reorganization in a human liver cell line. Toxicol Lett 207:270-277.
51. Sun Y, Zheng Q, Sun YT, Huang P, Guo ZL, Xu LH. Microcystin-LR induces protein phosphatase 2A alteration in a human liver cell line. Environ Toxicol (in press).
52. Toivola DM, Goldman RD, Garrod DR, Eriksson JE. 1997. Protein phosphatases maintain the organization and structural interactions of hepatic keratin intermediate filaments. J Cell Sci 110:23-33.
53. Ueno Y, Nagata S, Tsutsumi T, Hasegawa A, Watanabe MF, Park HD, Chen GC, Chen G, Yu SZ. 1996. Detection of microcystins, a blue-green algal hepatotoxin, in drinking water sampled in Haimen and Fusui, endemic areas of primary liver cancer in China, by highly sensitive immunoassay. Carcinogenesis 17:1317-1321.
54. Wang Z, Yin J, Zhang Y, Zhu L, Tian Q, Wang X, Li H, Wang J. 2010. Overexpression of tau proteins antagonizes amyloid-beta-potentiated apoptosis through mitochondria-caspase-3 pathway in N2a cells. J Alzheimers Dis 20:145-157.
55. Wang X, Liu JZ, Hu JX, Wu H, Li YL, Chen HL, Bai H, Hai CX. 2011. ROS-activated p38 MAPK/ERK-Akt cascade plays a central role in palmitic acid-stimulated hepatocyte proliferation. Free Radic Biol Med 51:539-551.
56. Weng D, Lu Y, Wei Y, Liu Y, Shen P. 2007. The role of ROS in microcystin-LR-induced hepatocyte apoptosis and liver injury in mice. Toxicology 232:15-23.
57. Wickstrom ML, Khan SA, Haschek WM, Wyman JF, Eriksson JE, Schaeffer DJ, Beasley VR. 1995. Alterations in microtubules, intermediate filaments, and microfilaments induced by microcystin-LR in cultured cells. Toxicol Pathol 23:326-337.
58. Yamada T, Egashira N, Bando A, Nishime Y, Tonogai Y, Imuta M, Yano T, Oishi R. 2012. Activation of p38 MAPK by oxidative stress underlying epirubicin-induced vascular endothelial cell injury. Free Radic Biol Med 52:1285-1293.
59. Zhang CE, Tian Q, Wei W, Peng JH, Liu GP, Zhou XW, Wang Q, Wang DW, Wang JZ. 2008. Homocysteine induces tau phosphorylation by inactivating protein phosphatase 2A in rat hippocampus. Neurobiol Aging 29:1654-1665.
60. Zhou Y, Yuan J, Wu J, Han X. 2012. The toxic effects of microcystin-LR on rat spermatogonia in vitro. Toxicol Lett 212:48-56.