Hydrogen peroxide responsive miR153 targets Nrf2/ARE cytoprotection in paraquat induced dopaminergic neurotoxicity

Toxicology Letters

Volumn 228, Issue 3, 2014, Pages 179-191

  Narasimhan, Madhusudhanan ^a,b   Riar, Amanjot Kaur ^a   Rathinam, Mary Latha ^a   Vedpathak, Dhanashree ^a   Henderson, George ^a,b   Mahimainathan, Lenin ^a,b  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

MiR153; Neurotoxicity; Nrf2; Paraquat

Indexed keywords

ANTIOXIDANT; CASPASE 3; CASPASE 7; CATALASE; COMPLEMENTARY DNA; HYDROGEN PEROXIDE; MICRORNA; MICRORNA 153; PARAQUAT; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ADENOVIRUS; ARTICLE; CELL DEATH; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; MUTATION; NEUROBLASTOMA CELL; NEUROTOXICITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN TARGETING; REAL TIME POLYMERASE CHAIN REACTION; TRANSACTIVATION;

H(2)O(2); MIR153; NEUROTOXICITY; NRF2; PARAQUAT;

3' UNTRANSLATED REGIONS; ANTIOXIDANT RESPONSE ELEMENTS; BINDING SITES; CASPASE 3; CASPASE 7; CATALASE; CELL DEATH; CELL LINE, TUMOR; CYTOPROTECTION; DOPAMINERGIC NEURONS; GENE EXPRESSION REGULATION; HUMANS; HYDROGEN PEROXIDE; MICRORNAS; NEUROTOXICITY SYNDROMES; NF-E2-RELATED FACTOR 2; OXIDATION-REDUCTION; PARAQUAT; REACTIVE OXYGEN SPECIES; TRANSFECTION;

EID: 84901781833     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2014.05.020     Document Type: Article

References (80)

1. Alesci S., Ramsey W.J., Bornstein S.R., Chrousos G.P., Hornsby P.J., Benvenga S., Trimarchi F., Ehrhart-Bornstein M. Adenoviral vectors can impair adrenocortical steroidogenesis: clinical implications for natural infections and gene therapy. Proc. Natl. Acad. Sci. USA 2002, 99(11):7484-7489.
2. Alvarez-Erviti L., Seow Y., Schapira A.H., Rodriguez-Oroz M.C., Obeso J.A., Cooper J.M. Influence of microRNA deregulation on chaperone-mediated autophagy and alpha-synuclein pathology in Parkinson's disease. Cell Death Dis. 2013, 4:e545.
3. Aw Yeang H.X., Hamdam J.M., Al-Huseini L.M., Sethu S., Djouhri L., Walsh J., Kitteringham N., Park B.K., Goldring C.E., Sathish J.G. Loss of transcription factor nuclear factor-erythroid 2 (NF-E2) p45-related factor-2 (Nrf2) leads to dysregulation of immune functions, redox homeostasis, and intracellular signaling in dendritic cells. J. Biol. Chem. 2012, 287(13):10556-10564.
4. Bak R.O., Mikkelsen J.G. miRNA sponges: soaking up miRNAs for regulation of gene expression. Wiley Interdiscip. Rev. RNA 2014, 5(3):313-333.
5. Benbrook C.M. Impacts of genetically engineered crops on pesticide use in the US - the first 16 years. Environ. Sci. Eur. 2012, 24:24.
6. Betarbet R., Sherer T.B., MacKenzie G., Garcia-Osuna M., Panov A.V., Greenamyre J.T. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 2000, 3(12):1301-1306.
7. Brooks A.I., Chadwick C.A., Gelbard H.A., Cory-Slechta D.A., Federoff H.J. Paraquat elicited neurobehavioral syndrome caused by dopaminergic neuron loss. Brain Res. 1999, 823(1/2):1-10.
8. Burk R.F., Lawrence R.A., Lane J.M. Liver necrosis and lipid peroxidation in the rat as the result of paraquat and diquat administration: effect of selenium deficiency. J. Clin. Invest. 1980, 65(5):1024-1031.
9. Cardo L.F., Coto E., de Mena L., Ribacoba R., Moris G., Menendez M., Alvarez V. Profile of microRNAs in the plasma of Parkinson's disease patients and healthy controls. J. Neurol. 2013, 260(5):1420-1422.
10. CDC Fourth National Report on Human Exposure to Environmental Chemicals 2009.
11. Cesana M., Cacchiarelli D., Legnini I., Santini T., Sthandier O., Chinappi M., Tramontano A., Bozzoni I. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 2011, 147:358-369.
12. Chatterjee N., Wang W.L., Conklin T., Chittur S., Tenniswood M. Histone deacetylase inhibitors modulate miRNA and mRNA expression, block metaphase, and induce apoptosis in inflammatory breast cancer cells. Cancer Biol. Ther. 2013, 14(7):658-671.
13. Correa F., Mallard C., Nilsson M., Sandberg M. Dual TNFalpha-induced effects on NRF2 mediated antioxidant defence in astrocyte-rich cultures: role of protein kinase activation. Neurochem. Res. 2012, 37(12):2842-2855.
14. De N., Young L., Lau P.W., Meisner N.C., Morrissey D.V., MacRae I.J. Highly complementary target RNAs promote release of guide RNAs from human Argonaute2. Mol. Cell 2013, 50:344-355.
15. Dekkers M.P., Nikoletopoulou V., Barde Y.A. Cell biology in neuroscience: death of developing neurons: new insights and implications for connectivity. J. Cell Biol. 2013, 203(3):385-393.
16. Doxakis E. Post-transcriptional regulation of alpha-synuclein expression by mir-7 and mir-153. J. Biol. Chem. 2010, 285(17):12726-12734.
17. Ebert M.S., Sharp P.A. MicroRNA sponges: progress and possibilities. RNA 2010, 16:2043-2050.
18. Fabian M.R., Sonenberg N., Filipowicz W. Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem. 2010, 79:351-379.
19. Filomeni G., Piccirillo S., Rotilio G., Ciriolo M.R. p38(MAPK) and ERK1/2 dictate cell death/survival response to different pro-oxidant stimuli via p53 and Nrf2 in neuroblastoma cells SH-SY5Y. Biochem. Pharmacol. 2012, 83(10):1349-1357.
20. Flores O., Kennedy E.M., Skalsky R.L., Cullen B.R. Differential RISC association of endogenous human microRNAs predicts their inhibitory potential. Nucleic Acids Res. 2014, 42(7):4629-4639.
21. Fukushima T., Tawara T., Isobe A., Hojo N., Shiwaku K., Yamane Y. Radical formation site of cerebral complex I and Parkinson's disease. J. Neurosci. Res. 1995, 42(3):385-390.
22. Gabbianelli R., Ferri A., Rotilio G., Carri M.T. Aberrant copper chemistry as a major mediator of oxidative stress in a human cellular model of amyotrophic lateral sclerosis. J. Neurochem. 1999, 73(3):1175-1180.
23. Gounder S.S., Kannan S., Devadoss D., Miller C.J., Whitehead K.S., Odelberg S.J., Firpo M.A., Paine R., Hoidal J.R., Abel E.D., Rajasekaran N.S. Impaired transcriptional activity of Nrf2 in age-related myocardial oxidative stress is reversible by moderate exercise training. PLoS ONE 2012, 7(9):e45697.
24. Harding A.J., Lakay B., Halliday G.M. Selective hippocampal neuron loss in dementia with Lewy bodies. Ann. Neurol. 2002, 51(1):125-128.
25. Harvey C.J., Thimmulappa R.K., Singh A., Blake D.J., Ling G., Wakabayashi N., Fujii J., Myers A., Biswal S. Nrf2-regulated glutathione recycling independent of biosynthesis is critical for cell survival during oxidative stress. Free Radic. Biol. Med. 2009, 46(4):443-453.
26. Hebert S.S., Horre K., Nicolai L., Papadopoulou A.S., Mandemakers W., Silahtaroglu A.N., Kauppinen S., Delacourte A., De Strooper B. Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer's disease correlates with increased BACE1/beta-secretase expression. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(17):6415-6420.
27. Henchcliffe C., Beal M.F. Mitochondrial biology and oxidative stress in Parkinson disease pathogenesis: nature clinical practice. Neurology 2008, 4(11):600-609.
28. Hoenig E.M., Margolis G., Kilham L. Experimental adenovirus infection of the mouse adrenal gland: II. Electron microscopic observations. Am. J. Pathol. 1974, 75(2):375-394.
29. Hofer T., Seo A.Y., Prudencio M., Leeuwenburgh C. A method to determine RNA and DNA oxidation simultaneously by HPLC-ECD: greater RNA than DNA oxidation in rat liver after doxorubicin administration. Biol. Chem. 2006, 387(1):103-111.
30. Hyslop P.A., Hinshaw D.B., Scraufstatter I.U., Cochrane C.G., Kunz S., Vosbeck K. Hydrogen peroxide as a potent bacteriostatic antibiotic: implications for host defense. Free Radic. Biol. Med. 1995, 19(1):31-37.
31. Kang K.W., Lee S.J., Park J.W., Kim S.G. Phosphatidylinositol 3-kinase regulates nuclear translocation of NF-E2-related factor 2 through actin rearrangement in response to oxidative stress. Mol. Pharmacol. 2002, 62(5):1001-1010.
32. Khoo S.K., Petillo D., Kang U.J., Resau J.H., Berryhill B., Linder J., Forsgren L., Neuman L.A., Tan A.C. Plasma-based circulating MicroRNA biomarkers for Parkinson's disease. J. Parkinson's Dis. 2012, 2(4):321-331.
33. Kim J., Inoue K., Ishii J., Vanti W.B., Voronov S.V., Murchison E., Hannon G., Abeliovich A. A MicroRNA feedback circuit in midbrain dopamine neurons. Science 2007, 317(5842):1220-1224.
34. Klann E., Thiels E. Modulation of protein kinases and protein phosphatases by reactive oxygen species: implications for hippocampal synaptic plasticity. Prog. Neuropsychopharmacol. Biol. Psychiatry 1999, 23(3):359-376.
35. Kobayashi A., Kang M.I., Okawa H., Ohtsuji M., Zenke Y., Chiba T., Igarashi K., Yamamoto M. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol. Cell. Biol. 2004, 24(16):7130-7139.
36. Le Belle J.E., Orozco N.M., Paucar A.A., Saxe J.P., Mottahedeh J., Pyle A.D., Wu H., Kornblum H.I. Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell 2011, 8(1):59-71.
37. Lee J.M., Li J., Johnson D.A., Stein T.D., Kraft A.D., Calkins M.J., Jakel R.J., Johnson J.A. Nrf2, a multi-organ protector?. FASEB J. 2005, 19(9):1061-1066.
38. Lee Y., Samaco R.C., Gatchel J.R., Thaller C., Orr H.T., Zoghbi H.Y. miR-19, miR-101 and miR-130 co-regulate ATXN1 levels to potentially modulate SCA1 pathogenesis. Nat. Neurosci. 2008, 11(10):1137-1139.
39. Leidinger P., Backes C., Deutscher S., Schmitt K., Mueller S.C., Frese K., Haas J., Ruprecht K., Paul F., Stahler C., Lang C.J., Meder B., Bartfai T., Meese E., Keller A. A blood based 12-miRNA signature of Alzheimer disease patients. Genome Biol. 2013, 14(7):R78.
40. Li J., Johnson D., Calkins M., Wright L., Svendsen C., Johnson J. Stabilization of Nrf2 by tBHQ confers protection against oxidative stress-induced cell death in human neural stem cells. Toxicol. Sci. 2005, 83(2):313-328.
41. Liu N., Landreh M., Cao K., Abe M., Hendriks G.J., Kennerdell J.R., Zhu Y., Wang L.S., Bonini N.M. The microRNA miR-34 modulates ageing and neurodegeneration in Drosophila. Nature 2012, 482(7386):519-523.
42. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25(4):402-408.
43. Mandemakers W., Abuhatzira L., Xu H., Caromile L.A., Hebert S.S., Snellinx A., Morais V.A., Matta S., Cai T., Notkins A.L., De Strooper B. Co-regulation of intragenic microRNA miR-153 and its host gene Ia-2 beta: identification of miR-153 target genes with functions related to IA-2beta in pancreas and brain. Diabetologia 2013, 56(7):1547-1556.
44. Maracchioni A., Totaro A., Angelini D.F., Di Penta A., Bernardi G., Carri M.T., Achsel T. Mitochondrial damage modulates alternative splicing in neuronal cells: implications for neurodegeneration. J. Neurochem. 2007, 100(1):142-153.
45. Margolis G., Kilham L., Hoenig E.M. Experimental adenovirus infection of the mouse adrenal gland: I. Light microscopic observations. Am. J. Pathol. 1974, 75(2):363-374.
46. McCormack A.L., Di Monte D.A. Effects of l-DOPA and other amino acids against paraquat-induced nigrostriatal degeneration. J. Neurochem. 2003, 85(1):82-86.
47. McKeith I., Mintzer J., Aarsland D., Burn D., Chiu H., Cohen-Mansfield J., Dickson D., Dubois B., Duda J.E., Feldman H., Gauthier S., Halliday G., Lawlor B., Lippa C., Lopez O.L., Carlos Machado J., O'Brien J., Playfer J., Reid W. Dementia with Lewy bodies. Lancet Neurol. 2004, 3(1):19-28.
48. Moi P., Chan K., Asunis I., Cao A., Kan Y.W. Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proc. Natl. Acad. Sci. U. S. A. 1994, 91(21):9926-9930.
49. Mollace V., Iannone M., Muscoli C., Palma E., Granato T., Rispoli V., Nistico R., Rotiroti D., Salvemini D. The role of oxidative stress in paraquat-induced neurotoxicity in rats: protection by non peptidyl superoxide dismutase mimetic. Neurosci. Lett. 2003, 335(3):163-166.
50. Mukherji S., Ebert M.S., Zheng G.X., Tsang J.S., Sharp P.A., van Oudenaarden A. MicroRNAs can generate thresholds in target gene expression. Nat. Genet. 2011, 43(9):854-859.
51. Narasimhan M., Mahimainathan L., Rathinam M.L., Riar A.K., Henderson G.I. Overexpression of Nrf2 protects cerebral cortical neurons from ethanol-induced apoptotic death. Mol. Pharmacol. 2011, 80(6):988-999.
52. Narasimhan M., Patel D., Vedpathak D., Rathinam M., Henderson G., Mahimainathan L. Identification of novel microRNAs in post-transcriptional control of Nrf2 expression and redox homeostasis in neuronal, SH-SY5Y cells. PLoS ONE 2012, 7(12):e51111.
53. Nguyen T., Huang H.C., Pickett C.B. Transcriptional regulation of the antioxidant response element: activation by Nrf2 and repression by MafK. J. Biol. Chem. 2000, 275(20):15466-15473.
54. O'Brien J.T., Colloby S., Fenwick J., Williams E.D., Firbank M., Burn D., Aarsland D., McKeith I.G. Dopamine transporter loss visualized with FP-CIT SPECT in the differential diagnosis of dementia with Lewy bodies. Arch. Neurol. 2004, 61(6):919-925.
55. Oppenheim R.W. Cell death during development of the nervous system. Annu. Rev. Neurosci. 1991, 14:453-501.
56. Peng J., Mao X.O., Stevenson F.F., Hsu M., Andersen J.K. The herbicide paraquat induces dopaminergic nigral apoptosis through sustained activation of the JNK pathway. J. Biol. Chem. 2004, 279(31):32626-32632.
57. Poliseno L., Salmena L., Zhang J., Carver B., Haveman W.J., Pandolfi P.P. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 2010, 465:1033-1038.
58. Prasad K., Winnik B., Thiruchelvam M.J., Buckley B., Mirochnitchenko O., Richfield E.K. Prolonged toxicokinetics and toxicodynamics of paraquat in mouse brain. Environ. Health Perspect. 2007, 115(10):1448-1453.
59. Prozorovski T., Schulze-Topphoff U., Glumm R., Baumgart J., Schroter F., Ninnemann O., Siegert E., Bendix I., Brustle O., Nitsch R., Zipp F., Aktas O. Sirt1 contributes critically to the redox-dependent fate of neural progenitors. Nat. Cell Biol. 2008, 10(4):385-394.
60. Ramachandiran S., Hansen J.M., Jones D.P., Richardson J.R., Miller G.W. Divergent mechanisms of paraquat, MPP+, and rotenone toxicity: oxidation of thioredoxin and caspase-3 activation. Toxicol. Sci. 2007, 95(1):163-171.
61. Ramsey C.P., Glass C.A., Montgomery M.B., Lindl K.A., Ritson G.P., Chia L.A., Hamilton R.L., Chu C.T., Jordan-Sciutto K.L. Expression of Nrf2 in neurodegenerative diseases. J. Neuropathol. Exp. Neurol. 2007, 66(1):75-85.
62. Raver-Shapira N., Marciano E., Meiri E., Spector Y., Rosenfeld N., Moskovits N., Bentwich Z., Oren M. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol. Cell 2007, 26(5):731-743.
63. Rhee S.G., Bae Y.S., Lee S.R., Kwon J. Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Sci. STKE 2000, 53:pe1.
64. Rojo A.I., Sagarra M.R., Cuadrado A. GSK-3beta down-regulates the transcription factor Nrf2 after oxidant damage: relevance to exposure of neuronal cells to oxidative stress. J. Neurochem. 2008, 105(1):192-202.
65. Rushworth S.A., Shah S., MacEwan D.J. TNF mediates the sustained activation of Nrf2 in human monocytes. J. Immunol. 2011, 187(2):702-707.
66. Sempere L.F., Freemantle S., Pitha-Rowe I., Moss E., Dmitrovsky E., Ambros V. Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 2004, 5(3):R13.
67. Shimizu K., Ohtaki K., Matsubara K., Aoyama K., Uezono T., Saito O., Suno M., Ogawa K., Hayase N., Kimura K., Shiono H. Carrier-mediated processes in blood-brain barrier penetration and neural uptake of paraquat. Brain Res. 2001, 906(1/2):135-142.
68. Soreq L., Salomonis N., Bronstein M., Greenberg D.S., Israel Z., Bergman H., Soreq H. Small RNA sequencing-microarray analyses in Parkinson leukocytes reveal deep brain stimulation-induced splicing changes that classify brain region transcriptomes. Front. Mol. Neurosci. 2013, 6:10.
69. Sun Z., Zhang S., Chan J.Y., Zhang D.D. Keap1 controls postinduction repression of the Nrf2-mediated antioxidant response by escorting nuclear export of Nrf2. Mol. Cell. Biol. 2007, 27(18):6334-6349.
70. Suzukawa K., Miura K., Mitsushita J., Resau J., Hirose K., Crystal R., Kamata T. Nerve growth factor-induced neuronal differentiation requires generation of Rac1-regulated reactive oxygen species. J. Biol. Chem. 2000, 275(18):13175-13178.
71. Suzuki H.I., Yamagata K., Sugimoto K., Iwamoto T., Kato S., Miyazono K. Modulation of microRNA processing by p53. Nature 2009, 460(7254):529-533.
72. Tsatmali M., Walcott E.C., Makarenkova H., Crossin K.L. Reactive oxygen species modulate the differentiation of neurons in clonal cortical cultures. Mol. Cell. Neurosci. 2006, 33(4):345-357.
73. van Jaarsveld M.T., Helleman J., Boersma A.W., van Kuijk P.F., van Ijcken W.F., Despierre E., Vergote I., Mathijssen R.H., Berns E.M., Verweij J., Pothof J., Wiemer E.A. miR-141 regulates KEAP1 and modulates cisplatin sensitivity in ovarian cancer cells. Oncogene 2013, 32(36):4284-4293.
74. von Otter M., Landgren S., Nilsson S., Celojevic D., Bergstrom P., Hakansson A., Nissbrandt H., Drozdzik M., Bialecka M., Kurzawski M., Blennow K., Nilsson M., Hammarsten O., Zetterberg H. Association of Nrf2-encoding NFE2L2 haplotypes with Parkinson's disease. BMC Med. Genet. 2010, 11:36.
75. Wei C., Thatcher E.J., Olena A.F., Cha D.J., Perdigoto A.L., Marshall A.F., Carter B.D., Broadie K., Patton J.G. miR-153 regulates SNAP-25, synaptic transmission, and neuronal development. PLoS ONE 2013, 8(2):e57080.
76. Widdowson P.S., Farnworth M.J., Simpson M.G., Lock E.A. Influence of age on the passage of paraquat through the blood-brain barrier in rats: a distribution and pathological examination. Hum. Exp. Toxicol. 1996, 15(3):231-236.
77. Williams G.C. Pleiotropy, natural selection, and the evolution of senescence. Evolution 1957, 11(4):398-411.
78. Yates M.S., Kensler T.W. Chemopreventive promise of targeting the Nrf2 pathway. Drug News Perspect. 2007, 20(2):109-117.
79. Zhang H.J., Drake V.J., Xu L., Hu J., Domann F.E., Oberley L.W., Kregel K.C. Redox regulation of adenovirus-induced AP-1 activation by overexpression of manganese-containing superoxide dismutase. J. Virol. 2002, 76(1):355-363.
80. Zhang L., Yu H., Sun Y., Lin X., Chen B., Tan C., Cao G., Wang Z. Protective effects of salidroside on hydrogen peroxide-induced apoptosis in SH-SY5Y human neuroblastoma cells. Eur. J. Pharmacol. 2007, 564(1-3):18-25.