Identification of the responsible proteins for increased selenium bioavailability in the brain of transgenic rats overexpressing selenoprotein M

Kim,Yona; Goo,Jun  Seo; Kim,Il  Yong; Kim,Ji  Eun; Kwak,Moon  Hwa; Go,Jun; Shim,Sunbo; Hong,Jin  Tae; Hwang,Dae  Youn; Seong,Je  Kyung

doi:10.3892/ijmm.2014.1945

Identification of the responsible proteins for increased selenium bioavailability in the brain of transgenic rats overexpressing selenoprotein M

Authors:
- Yona Kim
- Jun Seo Goo
- Il Yong Kim
- Ji Eun Kim
- Moon Hwa Kwak
- Jun Go
- Sunbo Shim
- Jin Tae Hong
- Dae Youn Hwang
- Je Kyung Seong
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Affiliations: Laboratory of Developmental Biology and Genomics, College of Veterinary Medicine, BK21 Program for Veterinary Science, Interdisciplinary Program for Bioinformatics and Program for Cancer Biology, Seoul National University, Seoul 151‑742, Republic of Korea, Department of Biomaterials Science, College of Natural Resources and Life Science, Life and Industry Convergence Research Institute, Pusan National University, Miryang, Gyeongsangnam-do 627‑706, Republic of Korea, Department of Laboratory Animal Resources, National Institute of Food and Drug Safety Evaluation, Korea FDA, Cheongwon, Chungcheongbuk-do 363‑700, Republic of Korea, College of Pharmacy, Chungbuk National University, Cheongju, Chungcheongbuk-do 361‑763, Republic of Korea
Published online on: September 24, 2014 https://doi.org/10.3892/ijmm.2014.1945
Pages: 1688-1698

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Abstract

The present study was conducted to investigate whether the high antioxidant activity induced by selenium (Sel) treatment and selenoprotein M (SelM) overexpression affected the protein profile of the brain cortex. To accomplish this, the changes in global protein expression were measured in transgenic (Tg) rats expressing human SelM (CMV/hSelM) and non‑Tg rats using two‑dimensional electrophoresis (2‑DE). The results revealed that: ⅰ) CMV/hSelM Tg rats showed a high level of enzyme activity for antioxidant protein in the brain cortex compared to non‑Tg rats; ⅱ) the high activity of these enzymes induced a decrease in total antioxidant concentration and γ‑secretase activity in CMV/hSelM Tg rats; ⅲ) five proteins were upregulated and three were downregulated by SelM overexpression; ⅳ) among the five upregulated proteins, two associated with creatine kinase B‑type (B‑CK) and E3 ubiquitin‑protein ligase RING1 (RING finger protein 1) were further increased in the two groups following Sel treatment, whereas synaptotagmin-15 (SytXV), eukaryotic translation initiation factor 4H (eIF-4H) and lactate dehydrogenase B (LDH-B) were increased or decreased under the same conditions; ⅴ) the three downregulated proteins did not induce a significant change in expression following Sel treatment; and ⅵ) the protein expression level alterations of the two selected spots (B‑CK and SytXV) identified by 2‑DE were extremely similar to the results from western blot analysis. Overall, the results of the present study provide primary novel biological evidence that new functional protein groups and individual proteins in the brain cortex of CMV/hSelM Tg rats are associated with Sel biology, including the response to Sel treatment and SelM overexpression.

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1	Wilber CG: Toxicology of selenium: a review. Clin Toxicol. 17:171–230. 1980. View Article : Google Scholar
2	Smith AM and Picciano MF: Evidence for increased selenium requirement for the rat during pregnancy and lactation. J Nutr. 116:1068–1079. 1986.PubMed/NCBI
3	Yang GQ, Chen JS, Wen ZM, Ge KY, Zhu LZ, Chen XC and Chen XS: The role of selenium in Keshan disease. Adv Nutr Res. 6:203–231. 1984. View Article : Google Scholar : PubMed/NCBI
4	van Rij AM, Thomson CD, McKenzie JM and Robinson MF: Selenium deficiency in total parenteral nutrition. Am J Clin Nutr. 32:2076–2085. 1979.PubMed/NCBI
5	Schwarz K and Foltz CM: Selenium as an integral part of factor 3 against dietary necrotic liver degeneration. J Am Chem Soc. 79:3292–3293. 1957. View Article : Google Scholar
6	Reddy PG, Morill JL, Minocha HC and Stevenson JS: Vitamin E is immunostimulatory in calves. J Dairy Sci. 70:993–999. 1987. View Article : Google Scholar : PubMed/NCBI
7	Birringer M, Pilawa S and Flohé L: Trends in selenium biochemistry. Nat Prod Rep. 19:693–718. 2002. View Article : Google Scholar
8	Carlson BA, Novoselov SV, Kumaraswamy E, Lee BJ, Anver MR, Gladyshev VN and Hatfield DL: Specific excision of the selenocysteine tRNA[Ser]Sec (Trsp) gene in mouse liver demonstrates an essential role of selenoproteins in liver function. J Biol Chem. 279:8011–8017. 2004.
9	Berry MJ, Banu L, Chen YY, Mandel SJ, Kieffer JD, Harney JW and Larsen PR: Recognition of UGA as a selenocysteine codon in type I deiodinase requires sequences in the 3′ untransalated region. Nature. 353:273–276. 1991.PubMed/NCBI
10	Kryukov GV, Castellano S, Novoselov SV, Lobanov AV, Zehtab O, Guigó R and Gladyshev VN: Characterization of mammalian selenoproteomes. Science. 300:1439–1443. 2003. View Article : Google Scholar : PubMed/NCBI
11	Korotkov KV, Novoselov SV, Hatfield DL and Gladyshev VN: Mammalian selenoprotein in which selenocysteine (Sec) incorporation is supported by a new form of Sec insertion sequence element. Mol Cell Biol. 22:1402–1411. 2002. View Article : Google Scholar : PubMed/NCBI
12	Müller WE, Borejko A, Brandt D, et al: Selenium affects biosilica formation in the demosponge Suberites domuncula. Effect on gene expression and spicule formation. FEBS J. 272:3838–3852. 2005.PubMed/NCBI
13	Hwang DY, Sin JS, Kim MS, et al: Overexpression of human selenoprotein M differentially regulates the concentrations of antioxidants and H₂O₂, the activity of antioxidant enzymes, and the composition of white blood cells in a transgenic rat. Int J Mol Med. 21:169–179. 2008.PubMed/NCBI
14	Chen J and Berry MJ: Selenium and selenoproteins in the brain and brain diseases (Review). J Neurochem. 86:1–12. 2003. View Article : Google Scholar
15	Ramaekers VT, Calomme M, Vanden Berghe D and Makropoulos W: Selenium deficiency triggering intractable seizures. Neuropediatrics. 25:217–223. 1994. View Article : Google Scholar : PubMed/NCBI
16	Imam SZ, el-Yazal J, Newport GD, Itzhak Y, Cadet JL, Slikker W Jr and Ali SF: Methamphetamine-induced dopaminergic neurotoxicity: role of peroxynitrite and neuroprotective role of antioxidants and peroxynitrite decomposition catalysts. Ann NY Acad Sci. 939:366–380. 2001. View Article : Google Scholar : PubMed/NCBI
17	Zafar KS, Siddiqui A, Sayeed I, Ahmad M, Salim S and Islam F: Dose-dependent protective effect of selenium in rat model of Parkinson’s disease: neurobehavioral and neurochemical evidences. J Neurochem. 84:438–446. 2003.PubMed/NCBI
18	Takizawa S, Matsushima K, Shinohara Y, Ogawa S, Komatsu N, Utsunomiya H and Watanabe K: Immunohistochemical localization of glutathione peroxidase in infarcted human brain. J Neurol Sci. 122:66–73. 1994. View Article : Google Scholar : PubMed/NCBI
19	Saijoh K, Saito N, Lee MJ, Fujii M, Kobayashi T and Sumino K: Molecular cloning of cDNA encoding a bovine selenoprotein P-like protein containing 12 selenocysteines and a (His-Pro) rich domain insertion, and its regional expression. Brain Res Mol Brain Res. 30:301–311. 1995. View Article : Google Scholar : PubMed/NCBI
20	Kim IY, Shin JH and Seong JK: Mouse phenogenomics, toolbox for functional annotation of human genome. BMB Rep. 43:79–90. 2010. View Article : Google Scholar : PubMed/NCBI
21	Schomburg L, Schweizer U, Holtmann B, Flohé L, Sendtner M and Köhrle J: Gene disruption discloses role of selenoprotein P in selenium delivery to target tissues. Biochem J. 370:397–402. 2003. View Article : Google Scholar : PubMed/NCBI
22	Hill KE, Zhou J, McMahan WJ, Motley AK, Atkins JF, Gesteland RF and Burk RF: Deletion of selenoprotein P alters distribution of selenium in the mouse. J Biol Chem. 278:13640–13646. 2003. View Article : Google Scholar : PubMed/NCBI
23	Hwang DY, Seo SJ, Kim YK, et al: Selenium acts as an insulin-like molecule for the downregulation of diabetic symptoms via endoplasmic reticulum stress and insulin signalling proteins in diabetes-induced non-obese diabetic mice. J Biosci. 32:723–735. 2007. View Article : Google Scholar : PubMed/NCBI
24	Yim SY, Chae KR, Shim SB, et al: ERK activation induced by selenium treatment significantly downregulates beta/gamma-secretase activity and Tau phosphorylation in the transgenic rat overexpressing human selenoprotein M. Int J Mol Med. 24:91–96. 2009.
25	Goo JS, Kim YN, Choi KM, et al: Proteomic analysis of kidneys from selenoprotein M transgenic rats in response to increased bioability of selenium. Clin Proteomics. 10:102013. View Article : Google Scholar : PubMed/NCBI
26	Park JY, Seong JK and Paik YK: Proteomic analysis of diet-induced hypercholesterolemic mice. Proteomics. 4:514–523. 2004. View Article : Google Scholar : PubMed/NCBI
27	Kim BH, Park EY, Yoo KH, Choi KM, Kim Y, Seong Jk and Park JH: N-myc downstream-regulated gene 1 is involved in the regulation of cystogenesis in transgenic mice overexpressing human PKD2 gene. Proteomics. 13:134–141. 2013. View Article : Google Scholar : PubMed/NCBI
28	Selkoe DJ: Alzheimer’s disease: genes, proteins, and therapy. Physiol Rev. 81:741–766. 2001.
29	Savaskan NE, Bräuer AU, Kühbacher M, et al: Selenium deficiency increases susceptibility to glutamate-induced excitotoxicity. FASEB J. 17:112–114. 2003.
30	Hu H, Jiang C, Li G and Lü J: PKB/AKT and ERK regulation of caspase-mediated apoptosis by methylseleninic acid in LNCaP prostate cancer cells. Carcinogenesis. 26:1374–1381. 2005. View Article : Google Scholar
31	Jaaro H, Rubinfeld H, Hanoch T and Seger R: Nuclear translocation of mitogen-activated protein kinase kinase (MEK1) in response to mitogenic stimulation. Proc Natl Acad Sci USA. 94:3742–3747. 1997. View Article : Google Scholar : PubMed/NCBI
32	Seger R, Seger D, Reszka AA, et al: Overexpression of mitogen-activated protein kinase kinase (MAPKK) and its mutants in NIH 3T3 cells. Evidence that MAPKK involvement in cellular proliferation is regulated by phosphorylation of serine residues in its kinase subdomains VII and VIII. J Biol Chem. 269:25699–25709. 1994.
33	Kim SK, Park HJ, Hong HS, Baik EJ, Jung MW and Mook-Jung I: ERK1/2 is an endogenous negative regulator of the gamma-secretase activity. FASEB J. 20:157–159. 2006.PubMed/NCBI
34	Iwatsubo T: The gamma-secretase complex: machinery for intramembrane proteolysis. Curr Opin Neurobiol. 14:379–383. 2004. View Article : Google Scholar : PubMed/NCBI
35	Chen F, Hasegawa H, Schmitt-Ulms G, et al: TMP21 is a presenilin complex component that modulates gamma-secretase but not epsilon-secretase activity. Nature. 440:1208–1212. 2006. View Article : Google Scholar
36	Bessman SP and Carpenter CL: The creatine-creatine phosphate energy shuttle. Annu Rev Biochem. 54:831–862. 1985. View Article : Google Scholar : PubMed/NCBI
37	Schnyder T, Winkler H, Gross H, Eppenberger HM and Wallimann T: Crystallization of mitochondrial creatine kinase. Growing of large protein crystals and electron microscopic investigation of microcrystals consisting of octamers. J Biol Chem. 266:5318–5322. 1991.
38	David S, Shoemaker M and Haley BE: Abnormal properties of creatine kinase in Alzheimer’s disease brain: correlation of reduced enzyme activity and active site photolabeling with aberrant cytosol-membrane partitioning. Brain Res Mol Brain Res. 54:276–287. 1998.PubMed/NCBI
39	Tomimoto H, Yamamoto K, Homburger HA and Yanagihara T: Immunoelectron microscopic investigation of creatine kinase BB-isoenzyme after cerebral ischemia in gerbils. Acta Neuropathol. 86:447–455. 1993.PubMed/NCBI
40	Gross WL, Bak MI, Ingwall JS, Arstall MA, Smith TW, Balligand JL and Kelly RA: Nitric oxide inhibits creatine kinase and regulates rat heart contractile reserve. Proc Natl Acad Sci USA. 93:5604–5609. 1996. View Article : Google Scholar : PubMed/NCBI
41	Hamman BL, Bittl JA, Jacobus WE, Allen PD, Spencer RS, Tian R and Ingwall JS: Inhibition of the creatine kinase reaction decreases the contractile reserve of isolated rat hearts. Am J Physiol. 269:H1030–H1036. 1995.PubMed/NCBI
42	Rech VC, Feksa LR, Fleck RM, Athaydes GA, Dornelles PK, Rodrigues-Junior V and Wannmacher CM: Cysteamine prevents inhibition of thiol-containing enzymes caused by cystine or cystine dimethylester loading in rat brain cortex. Metab Brain Dis. 23:133–145. 2008. View Article : Google Scholar : PubMed/NCBI
43	Steece-Collier K, Maries E and Kordower JH: Etiology of Parkinson’s disease: genetics and environment revisited. Proc Natl Acad Sci USA. 99:13972–13974. 2002.
44	Dawson TM: Parkin and defective ubiquitination in Parkinson’s disease. J Neural Transm Suppl. 70:209–213. 2006.
45	Fukuda M and Mikoshiba K: Synaptotagmin-like protein 1–3: a novel family of C-terminal-type tandem C2 proteins. Biochem Biophys Res Commun. 281:1226–1233. 2001.
46	Fukuda M, Saegusa C and Mikoshiba K: Novel splicing isoforms of synaptotagmin-like proteins 2 and 3: identification of the Slp homology domain. Biochem Biophys Res Commun. 283:513–519. 2001. View Article : Google Scholar : PubMed/NCBI
47	Sugita S, Shin OH, Han W, Lao Y and Südhof TC: Synaptotagmins form a hierarchy of exocytotic Ca(2+) sensors with distinct Ca(2+) affinities. EMBO J. 21:270–280. 2002. View Article : Google Scholar : PubMed/NCBI
48	Fukuda M, Kanno E, Ogata Y, Saegusa C, Kim T, Loh YP and Yamamoto A: Nerve growth factor-dependent sorting of synaptotagmin IV protein to mature dense-core vesicles that undergo calcium-dependent exocytosis in PC12 cells. J Biol Chem. 278:3220–3226. 2003. View Article : Google Scholar : PubMed/NCBI
49	Chapman ER: Synaptotagmin: a Ca(2+) sensor that triggers exocytosis? Nat Rev Mol Cell Biol. 3:498–508. 2002. View Article : Google Scholar : PubMed/NCBI
50	Mikoshiba K, Fukuda M, Moreira JE, Lewis FMT, Sugimori M, Niinobe M and Llinás R: Role of the C2A domain of synaptotagmin in transmitter release as determined by specific antibody injection into the squid giant synapse preterminal. Proc Natl Acad Sci USA. 92:10703–10707. 1995. View Article : Google Scholar
51	Detrait ER, Yoo S, Eddleman CS, Fukuda M, Bittner GD and Fishman HM: Plasmalemmal repair of severed neurites of PC12 cells requires Ca(2+) and synaptotagmin. J Neurosci Res. 62:566–573. 2000. View Article : Google Scholar : PubMed/NCBI
52	Reddy A, Caler EV and Andrews NW: Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes. Cell. 106:157–169. 2001. View Article : Google Scholar : PubMed/NCBI
53	Michaut M, De Blas G, Tomes CN, Yunes R, Fukuda M and Mayorga LS: Synaptotagmin VI participates in the acrosome reaction of human spermatozoa. Dev Biol. 235:521–529. 2001. View Article : Google Scholar : PubMed/NCBI
54	Schiavo G, Osborne SL and Sgouros JG: Synaptotagmins: more isoforms than functions? Biochem Biophys Res Commun. 248:1–8. 1998. View Article : Google Scholar : PubMed/NCBI
55	Fukuda M and Mikoshiba K: The function of inositol high polyphosphate binding proteins. Bioessays. 19:593–603. 1997. View Article : Google Scholar : PubMed/NCBI
56	Philibert RA, Nelson JJ, Sandhu HK, Crowe RR and Coryell WH: Association of an exonic LDHA polymorphism with altered respiratory response in probands at high risk for panic disorder. Am J Med Genet B Neuropsychiatr Genet. 117:11–17. 2003. View Article : Google Scholar : PubMed/NCBI
57	Nazam Ansari M, Bhandari U, Islam F and Tripathi CD: Evaluation of antioxidant and neuroprotective effect of ethanolic extract of Embelia ribes Burm in focal cerebral ischemia/reperfusion-induced oxidative stress in rats. Fundam Clin Pharmacol. 22:305–314. 2008.PubMed/NCBI
58	Kim HS, Choi Y, Shin KY, et al: Swedish amyloid precursor protein mutation increases phosphorylation of eIF2alpha in vitro and in vivo. J Neurosci Res. 85:1528–1537. 2007. View Article : Google Scholar : PubMed/NCBI
59	Petrov T, Underwood BD, Braun B, Alousi SS and Rafols JA: Upregulation of iNOS expression and phosphorylation of eIF-2alpha are paralleled by suppression of protein synthesis in rat hypothalamus in a closed head trauma model. J Neurotrauma. 18:799–812. 2001. View Article : Google Scholar : PubMed/NCBI
60	Hayashi T, Saito A, Okuno S, et al: Oxidative damage to the endoplasmic reticulum is implicated in ischemic neuronal cell death. J Cereb Blood Flow Metab. 23:1117–1128. 2003. View Article : Google Scholar : PubMed/NCBI
61	Foltz DR, Jansen LE, Black BE, Bailey AO, Yates JR 3rd and Cleveland DW: The human CENP-A centromeric nucleosome-associated complex. Nat Cell Biol. 8:458–469. 2006. View Article : Google Scholar : PubMed/NCBI
62	Zhang Z, Ottens AK, Sadasivan S, Kobeissy FH, Fang T, Hayes RL and Wang KK: Calpain-mediated collapsin response mediator protein-1, -2, and -4 proteolysis after neurotoxic and traumatic brain injury. J Neurotrauma. 24:460–472. 2007. View Article : Google Scholar : PubMed/NCBI
63	Chung MA, Lee JE, Lee JY, Ko MJ, Lee ST and Kim HJ: Alteration of collapsin response mediator protein-2 expression in focal ischemic rat brain. Neuroreport. 16:1647–1653. 2005. View Article : Google Scholar : PubMed/NCBI