Phosphoproteomic profiling of selenate-treated Alzheimer's disease model cells

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Chen, Ping ^a   Wang, Lixiang ^a   Wang, Yong ^a   Li, Shuiming ^a   Shen, Liming ^a   Liu, Qiong ^a   Ni, Jiazuan ^a  

^a SHENZHEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSYLHOMOCYSTEINASE; ASPARTATE AMINOTRANSFERASE; CYCLIC AMP DEPENDENT PROTEIN KINASE; ELONGATION FACTOR 2; F ACTIN; GALECTIN 1; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; HEAT SHOCK PROTEIN 90; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HOMOCYSTEINE; ISOCITRATE DEHYDROGENASE (NAD); LACTOYLGLUTATHIONE LYASE; MALATE DEHYDROGENASE; PEROXIREDOXIN 4; PEROXIREDOXIN 6; PHOSPHOPROTEIN; PHOSPHOSERINE; PHOSPHOTHREONINE; PHOSPHOTYROSINE; PROTEIN DNAJ; RAN PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); RIBOSOME PROTEIN; SELENATE; SERINE TRANSFER RNA LIGASE; TAU PROTEIN; UBIQUITIN THIOLESTERASE; VINCULIN; AMYLOID BETA PROTEIN; ANTIOXIDANT; PROTEOME; SELENIC ACID;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; ENERGY METABOLISM; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE ONTOLOGY; ISOELECTRIC FOCUSING; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOTOR PERFORMANCE; MOUSE; NEUROBLASTOMA CELL; NEUROFIBRILLARY TANGLE; NONHUMAN; OXIDATIVE STRESS; PHOSPHOPROTEOMICS; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEOMICS; SPATIAL LEARNING; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION; WESTERN BLOTTING; BIOLOGY; CELL LINE; CELL SURVIVAL; DRUG EFFECTS; HUMAN; METABOLISM; MOLECULAR GENETICS; PATHOLOGY; PROCEDURES;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANTIOXIDANTS; CELL LINE; CELL SURVIVAL; COMPUTATIONAL BIOLOGY; HUMANS; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR SEQUENCE ANNOTATION; PHOSPHOPROTEINS; PROTEOME; PROTEOMICS; SELENIC ACID;

EID: 84915749583     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113307     Document Type: Article

References (75)

1. Cohen P (2002) The origins of protein phosphorylation. Nat Cell Biol4: E127-130.
2. Cohen P (2001) The role of protein phosphorylation in human health and disease. The Sir Hans Krebs Medal Lecture. Eur J Biochem268: 5001-5010.
3. Tenreiro S, Eckermann K, Outeiro TF (2014) Protein phosphorylation in neurodegeneration: friend or foe? Front Mol Neurosci7: 42.
4. Pillai R, Uyehara-Lock JH, Bellinger FP (2014) Selenium and selenoprotein function in brain disorders. IUBMB Life66: 229-239.
5. Ishrat T, Parveen K, Khan MM, Khuwaja G, Khan MB, et al. (2009) Selenium prevents cognitive decline and oxidative damage in rat model of streptozotocin-induced experimental dementia of Alzheimer's type. Brain Res1281: 117-127.
6. Berr C, Arnaud J, Akbaraly TN (2012) Selenium and cognitive impairment: a brief-review based on results from the EVA study. Biofactors38: 139-144.
7. Cheng Y, Jin Y, Ma F, Liang C, Liu Y, et al. (2010) Study on selenium exposure level related to cognitive function in rural elderly people. Wei Sheng Yan Jiu 39: 483-485.
8. Loef M, Schrauzer GN, Walach H (2011) Selenium and Alzheimer's disease: a systematic review. J Alzheimers Dis26: 81-104.
9. Xiong S, Markesbery WR, Shao C, Lovell MA (2007) Seleno-L-methionine protects against beta-amyloid and iron/hydrogen peroxide-mediated neuron death. Antioxid Redox Signal 9: 457-467.
10. Song G, Zhang Z, Wen L, Chen C, Shi Q, et al. (2014) Selenomethionine ameliorates cognitive decline, reduces tau hyperphosphorylation, and reverses synaptic deficit in the triple transgenic mouse model of Alzheimer's disease. J Alzheimers Dis 41: 85-99.
11. Tung YT, Hsu WM, Wang BJ, Wu SY, Yen CT, et al. (2008) Sodium selenite inhibits gamma-secretase activity through activation of ERK. Neurosci Lett 440: 38-43.
12. van Eersel J, Ke YD, Liu X, Delerue F, Kril JJ, et al. (2010) Sodium selenate mitigates tau pathology, neurodegeneration, and functional deficits in Alzheimer's disease models. Proc Natl Acad Sci U S A107: 13888-13893.
13. Corcoran NM, Martin D, Hutter-Paier B, Windisch M, Nguyen T, et al. (2010) Sodium selenate specifically activates PP2A phosphatase, dephosphorylates tau and reverses memory deficits in an Alzheimer's disease model. J Clin Neurosci 17: 1025-1033.
14. Chen P, Wang C, Ma X, Zhang Y, Liu Q, et al. (2013) Direct Interaction of Selenoprotein R with Clusterin and Its Possible Role in Alzheimer's Disease. PLoS One8: e66384.
15. Wang ZF, Li HL, Li XC, Zhang Q, Tian Q, et al. (2006) Effects of endogenous beta-amyloid overproduction on tau phosphorylation in cell culture. J Neurochem 98: 1167-1175.
16. Wang YP, Wang XC, Tian Q, Yang Y, Zhang Q, et al. (2006) Endogenous overproduction of beta-amyloid induces tau hyperphosphorylation and decreases the solubility of tau in N2a cells. J Neural Transm 113: 1723-1732.
17. Thinakaran G, Teplow DB, Siman R, Greenberg B, Sisodia SS (1996) Metabolism of the "Swedish" amyloid precursor protein variant in neuro2a (N2a) cells. Evidence that cleavage at the "beta-secretase" site occurs in the golgi apparatus. J Biol Chem 271: 9390-9397.
18. Gao S, Jin Y, Hall KS, Liang C, Unverzagt FW, et al. (2007) Selenium level and cognitive function in rural elderly Chinese. Am J Epidemiol 165: 955-965.
19. Akbaraly TN, Hininger-Favier I, Carriere I, Arnaud J, Gourlet V, et al. (2007) Plasma selenium over time and cognitive decline in the elderly. Epidemiology 18: 52-58.
20. Ceccatelli S, Tamm C, Zhang Q, Chen M (2007) Mechanisms and modulation of neural cell damage induced by oxidative stress. Physiol Behav 92: 87-92.
21. Yan MH, Wang X, Zhu X (2013) Mitochondrial defects and oxidative stress in Alzheimer disease and Parkinson disease. Free Radic Biol Med 62: 90-101.
22. Browne GJ, Proud CG (2002) Regulation of peptide-chain elongation in mammalian cells. Eur J Biochem 269: 5360-5368.
23. Garcia L, O'Loghlen A, Martin ME, Burda J, Salinas M (2004) Does phosphorylation of eukaryotic elongation factor eEF2 regulate protein synthesis in ischemic preconditioning? Journal of Neuroscience Research 77: 292-298.
24. Nakamura M, Yamada M, Ohsawa T, Morisawa H, Nishine T, et al. (2006) Phosphoproteomic profiling of human SH-SY5Y neuroblastoma cells during response to 6-hydroxydopamine-induced oxidative stress. Bba-Mol Cell Res 1763: 977-989.
25. Stone JR, Collins T (2002) Rapid phosphorylation of heterogeneous nuclear ribonucleoprotein C1/C2 in response to physiologic levels of hydrogen peroxide in human endothelial cells. J Biol Chem 277: 15621-15628.
26. Kattapuram T, Yang S, Maki JL, Stone JR (2005) Protein kinase CK1alpha regulates mRNA binding by heterogeneous nuclear ribonucleoprotein C in response to physiologic levels of hydrogen peroxide. J Biol Chem 280: 15340-15347.
27. Walsh B, Pearl A, Suchy S, Tartaglio J, Visco K, et al. (2009) Overexpression of Prdx6 and resistance to peroxide-induced death in Hepa1-6 cells: Prdx suppression increases apoptosis. Redox Rep 14: 275-284.
28. Zhang H, Go YM, Jones DP (2007) Mitochondrial thioredoxin-2/peroxiredoxin-3 system functions in parallel with mitochondrial GSH system in protection against oxidative stress. Arch Biochem Biophys 465: 119-126.
29. De Simoni S, Goemaere J, Knoops B (2008) Silencing of peroxiredoxin 3 and peroxiredoxin 5 reveals the role of mitochondrial peroxiredoxins in the protection of human neuroblastoma SH-SY5Y cells toward MPP+. Neurosci Lett 433: 219-224.
30. Rahaman H, Zhou SP, Dodia C, Shuvaeva T, Feinstein SI, et al. (2012) Phosphorylation of Prdx6 mediated by MAPkinase induces conformational change with concomitant increase in its phospholipase A(2) activity. Faseb Journa l26.
31. Tanaka K (1998) Proteasomes: structure and biology. J Biochem 123: 195-204.
32. Tanaka K, Chiba T (1998) The proteasome: a protein-destroying machine. Genes Cells 3: 499-510.
33. Schmitt HP (2006) Protein ubiquitination, degradation and the proteasome in neuro-degenerative disorders: no clear evidence for a significant pathogenetic role of proteasome failure in Alzheimer disease and related disorders. Med Hypotheses 67: 311-317.
34. Keller JN, Hanni KB, Markesbery WR (2000) Impaired proteasome function in Alzheimer's disease. J Neurochem 75: 436-439.
35. Keck S, Nitsch R, Grune T, Ullrich O (2003) Proteasome inhibition by paired helical filament-tau in brains of patients with Alzheimer's disease. J Neurochem 85: 115-122.
36. Oh S, Hong HS, Hwang E, Sim HJ, Lee W, et al. (2005) Amyloid peptide attenuates the proteasome activity in neuronal cells. Mech Ageing Dev 126: 1292-1299.
37. Gillardon F, Kloss A, Berg M, Neumann M, Mechtler K, et al. (2007) The 20S proteasome isolated from Alzheimer's disease brain shows post-translational modifications but unchanged proteolytic activity. J Neurochem 101: 1483-1490.
38. Pedros I, Petrov D, Allgaier M, Sureda F, Barroso E, et al. (2014) Early alterations in energy metabolism in the hippocampus of APPSwe/PS1dE9 mouse model of Alzheimer's disease. Biochim Biophys Acta 1842(9): 1556-1566.
39. Ferreira IL, Resende R, Ferreiro E, Rego AC, Pereira CF (2010) Multiple defects in energy metabolism in Alzheimer's disease. Curr Drug Targets11: 1193-1206.
40. Kapogiannis D, Mattson MP (2011) Disrupted energy metabolism and neuronal circuit dysfunction in cognitive impairment and Alzheimer's disease. Lancet Neuro l10: 187-198.
41. Arias C, Montiel T, Quiroz-Baez R, Massieu L (2002) beta-Amyloid neurotoxicity is exacerbated during glycolysis inhibition and mitochondrial impairment in the rat hippocampus in vivo and in isolated nerve terminals: implications for Alzheimer's disease. Exp Neurol 176: 163-174.
42. Vlassenko AG, Vaishnavi SN, Couture L, Sacco D, Shannon BJ, et al. (2010) Spatial correlation between brain aerobic glycolysis and amyloid-beta (A beta) deposition. P Natl Acad Sci USA 107: 17763-17767.
43. Vaishnavi SN, Vlassenko AG, Rundle MM, Snyder AZ, Mintun MA, et al. (2010) Regional aerobic glycolysis in the human brain. Proc Natl Acad Sci U S A 107: 17757-17762.
44. Di Domenico F, Sultana R, Barone E, Perluigi M, Cini C, et al. (2011) Quantitative proteomics analysis of phosphorylated proteins in the hippocampus of Alzheimer's disease subjects. J Proteomics 74: 1091-1103.
45. Palmer AM (1999) The activity of the pentose phosphate pathway is increased in response to oxidative stress in Alzheimer's disease. Journal of Neural Transmission 106: 317-328.
46. Horecker BL (2002) The pentose phosphate pathway. J Biol Chem277: 47965-47971.
47. Bolanos JP, Almeida A (2010) The pentose-phosphate pathway in neuronal survival against nitrosative stress. IUBMB Life 62: 14-18.
48. Tiwari V, Patel AB (2014) Pyruvate Carboxylase and Pentose Phosphate Fluxes are Reduced in AbetaPP-PS1 Mouse Model of Alzheimer's Disease: A 13C NMR Study. J Alzheimers Dis 41: 387-399.
49. Morris MS (2003) Homocysteine and Alzheimer's disease. Lancet Neurology 2: 425-428.
50. Stipanuk MH, Ueki I (2011) Dealing with methionine/homocysteine sulfur: cysteine metabolism to taurine and inorganic sulfur. J Inherit Metab Dis 34: 17-32.
51. Li JG, Chu J, Barrero C, Merali S, Pratico D (2014) Homocysteine exacerbates beta-amyloid pathology, tau pathology, and cognitive deficit in a mouse model of Alzheimer disease with plaques and tangles. Ann Neurol 75(6): 851-863.
52. Xiang TX, Li LL, Yin XD, Yuan CF, Tan C, et al. (2012) The Ubiquitin Peptidase UCHL1 Induces G0/G1 Cell Cycle Arrest and Apoptosis Through Stabilizing p53 and Is Frequently Silenced in Breast Cancer. PLoS One 7(1): e29783.
53. Jin CM, Yu W, Lou XY, Zhou F, Han X, et al. (2013) UCHL1 Is a Putative Tumor Suppressor in Ovarian Cancer Cells and Contributes to Cisplatin Resistance. Journal of Cancer4: 662-670.
54. Costes S, Gurlo T, Rivera JF, Butler PC (2014) UCHL1 deficiency exacerbates human islet amyloid polypeptide toxicity in beta-cells: Evidence of interplay between the ubiquitin/proteasome system and autophagy. Autophagy 10: 1004-1014.
55. Nagamine S, Kabuta T, Furuta A, Yamamoto K, Takahashi A, et al. (2010) Deficiency of ubiquitin carboxy-terminal hydrolase-L1 (UCH-L1) leads to vulnerability to lipid peroxidation. Neurochem Int 57: 102-110.
56. Day IN, Thompson RJ (2010) UCHL1 (PGP 9.5): neuronal biomarker and ubiquitin system protein. Prog Neurobio l90: 327-362.
57. Lombardino AJ, Li XC, Hertel M, Nottebohm F (2005) Replaceable neurons and neurodegenerative disease share depressed UCHL1 levels. Proc Natl Acad Sci U S A 102: 8036-8041.
58. Zetterberg M, Sjolander A, von Otter M, Palmer MS, Landgren S, et al. (2010) Ubiquitin carboxy-terminal hydrolase L1 (UCHL1) S18Y polymorphism in Alzheimer's disease. Mol Neurodegener 5: 11.
59. Bilguvar K, Tyagi NK, Ozkara C, Tuysuz B, Bakircioglu M, et al. (2013) Recessive loss of function of the neuronal ubiquitin hydrolase UCHL1 leads to early-onset progressive neurodegeneration. Proc Natl Acad Sci U S A 110: 3489-3494.
60. Zhao ZB, Wu L, Xiong R, Wang LL, Zhang B, et al. (2014) MicroRNA-922 promotes tau phosphorylation by downregulating ubiquitin carboxy-terminal hydrolase L1 (UCHL1) expression in the pathogenesis of Alzheimer's disease. Neuroscience 275: 232-237.
61. Hetz C, Soto C (2003) Protein misfolding and disease: the case of prion disorders. Cell Mol Life Sci 60: 133-143.
62. Golji J, Wendorff T, Mofrad MR (2012) Phosphorylation primes vinculin for activation. Biophys J 102: 2022-2030.
63. Tolbert CE, Burridge K, Campbell SL (2013) Vinculin regulation of F-actin bundle formation: what does it mean for the cell? Cell Adh Migr 7: 219-225.
64. Golji J, Mofrad MR (2010) A molecular dynamics investigation of vinculin activation. Biophys J 99: 1073-1081.
65. Halegoua S (1987) Changes in the phosphorylation and distribution of vinculin during nerve growth factor induced neurite outgrowth. Dev Biol 121: 97-104.
66. Zhang Z, Izaguirre G, Lin SY, Lee HY, Schaefer E, et al. (2004) The phosphorylation of vinculin on tyrosine residues 100 and 1065, mediated by SRC kinases, affects cell spreading. Mol Biol Cell 15: 4234-4247.
67. Wahlstrom G, Vartiainen M, Yamamoto L, Mattila PK, Lappalainen P, et al. (2001) Twinfilin is required for actin-dependent developmental processes in Drosophila. J Cell Biol 155: 787-796.
68. Goode BL, Drubin DG, Lappalainen P (1998) Regulation of the cortical actin cytoskeleton in budding yeast by twinfilin, a ubiquitous actin monomer-sequestering protein. J Cell Biol 142: 723-733.
69. Wang D, Zhang L, Zhao G, Wahlstrom G, Heino TI, et al. (2010) Drosophila twinfilin is required for cell migration and synaptic endocytosis. J Cell Sci 123: 1546-1556.
70. Yamada S, Uchimura E, Ueda T, Nomura T, Fujita S, et al. (2007) Identification of twinfilin-2 as a factor involved in neurite outgrowth by RNAi-based screen. Biochem Biophys Res Commun 363: 926-930.
71. Bouhouche A, Benomar A, Bouslam N, Chkili T, Yahyaoui M (2006) Mutation in the epsilon subunit of the cytosolic chaperonin-containing t-complex peptide-1 (Cct5) gene causes autosomal recessive mutilating sensory neuropathy with spastic paraplegia. J Med Genet 43: 441-443.
72. Martin L, Latypova X, Wilson CM, Magnaudeix A, Perrin ML, et al. (2013) Tau protein phosphatases in Alzheimer's disease: the leading role of PP2A. Ageing Res Rev12: 39-49.
73. Sontag E, Nunbhakdi-Craig V, Lee G, Brandt R, Kamibayashi C, et al. (1999) Molecular interactions among protein phosphatase 2A, tau, and microtubules - Implications for the regulation of tau phosphorylation and the development of tauopathies. Journal of Biological Chemistry 274: 25490-25498.
74. Yin YY, Liu H, Cong XB, Liu Z, Wang Q, et al. (2010) Acetyl-L-carnitine attenuates okadaic acid induced tau hyperphosphorylation and spatial memory impairment in rats. J Alzheimers Dis19: 735-746.
75. Liu GP, Wei W, Zhou X, Shi HR, Liu XH, et al. (2013) Silencing PP2A inhibitor by lenti-shRNA interference ameliorates neuropathologies and memory deficits in tg2576 mice. Mol Ther 21: 2247-2257.