Impaired selenoprotein expression in brain triggers striatal neuronal loss leading to co-ordination defects in mice

Biochemical Journal

Volumn 462, Issue 1, 2014, Pages 67-75

  Seeher, Sandra ^a   Carlson, Bradley A ^b   Miniard, Angela C ^c   Wirth, Eva K ^d   Mahdi, Yassin ^a   Hatfield, Dolph L ^b   Driscoll, Donna M ^c   Schweizer, Ulrich ^a  

^a UNIVERSITY OF BONN   (Germany)

^b NATIONAL CANCER INSTITUTE   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Cholinergic; Glutathione peroxidase; Neurodegeneration; Parvalbumin; Redox; Selenium

Indexed keywords

4 AMINOBUTYRIC ACID; CARRIER PROTEIN; GLUTAMATE DECARBOXYLASE 67; SELENIUM; SELENOPROTEIN; SELENOPROTEIN P; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN FUNCTION; CELL LOSS; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; COORDINATION DISORDER; CORPUS STRIATUM; FEMALE; HIPPOCAMPUS; IN SITU HYBRIDIZATION; INTERNEURON; MALE; MENTAL DEFICIENCY; MOUSE; NERVE CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SELENIUM BLOOD LEVEL; SOMATOSENSORY CORTEX; STRIATE CORTEX; SUBSTANTIA NIGRA;

ANIMALS; CORPUS STRIATUM; GLUTAMATE DECARBOXYLASE; INTERNEURONS; MICE; MOVEMENT DISORDERS; PARVALBUMINS; RNA-BINDING PROTEINS; SELENOCYSTEINE; SELENOPROTEINS; SOMATOSENSORY CORTEX;

EID: 84904697401     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20140423     Document Type: Article

References (39)

1. Hatfield, D. L., Carlson, B. A., Xu, X. M., Mix, H. and Gladyshev, V. N. (2006) Selenocysteine incorporation machinery and the role of selenoproteins in development and health. Prog. Nucleic Acid Res. Mol. Biol. 81, 97-142 CrossRef PubMed (Pubitemid 44767504)
2. Seeher, S., Mahdi, Y. and Schweizer, U. (2012) Post-transcriptional control of selenoprotein biosynthesis. Curr. Protein Pept. Sci. 13, 337-346 CrossRef PubMed
3. Yuan, J., Palioura, S., Salazar, J. C., Su, D., O'Donoghue, P., Hohn, M. J., Cardoso, A. M., Whitman, W. B. and Söll, D. (2006) RNA-dependent conversion of phosphoserine forms selenocysteine in eukaryotes and archaea. Proc. Natl. Acad. Sci. U.S.A. 103, 18923-18927 CrossRef PubMed (Pubitemid 350002804)
4. Xu, X. M., Carlson, B. A., Mix, H., Zhang, Y., Saira, K., Glass, R. S., Berry, M. J., Gladyshev, V. N. and Hatfield, D. L. (2007) Biosynthesis of selenocysteine on its tRNA in eukaryotes. PLoS Biol. 5, e4 CrossRef PubMed
5. Kryukov, G. V., Castellano, S., Novoselov, S. V., Lobanov, A. V., Zehtab, O., Guigo, R. and Gladyshev, V. N. (2003) Characterization of mammalian selenoproteomes. Science 300, 1439-1443 CrossRef PubMed (Pubitemid 36638165)
6. Bösl, M. R., Takaku, K., Oshima, M., Nishimura, S. and Taketo, M. M. (1997) Early embryonic lethality caused by targeted disruption of the mouse selenocysteine tRNA gene (Trsp). Proc. Natl. Acad. Sci. U.S.A. 94, 5531-5534 CrossRef PubMed (Pubitemid 27241803)
7. Seiler, A., Schneider, M., Forster, H., Roth, S., Wirth, E. K., Culmsee, C., Plesnila, N., Kremmer, E., Radmark, O., Wurst, W. et al. (2008) Glutathione peroxidase 4 senses and translates oxidative stress into 12/15-lipoxygenase dependent- and AIF-mediated cell death. Cell Metab. 8, 237-248 CrossRef PubMed
8. Jakupoglu, C., Przemeck, G. K., Schneider, M., Moreno, S. G., Mayr, N., Hatzopoulos, A. K., de Angelis, M. H., Wurst, W., Bornkamm, G. W., Brielmeier, M. and Conrad, M. (2005) Cytoplasmic thioredoxin reductase is essential for embryogenesis but dispensable for cardiac development. Mol. Cell. Biol. 25, 1980-1988 CrossRef PubMed (Pubitemid 40280160)
9. Conrad, M., Jakupoglu, C., Moreno, S. G., Lippl, S., Banjac, A., Schneider, M., Beck, H., Hatzopoulos, A. K., Just, U., Sinowatz, F. et al. (2004) Essential role for mitochondrial thioredoxin reductase in hematopoiesis, heart development, and heart function. Mol. Cell. Biol. 24, 9414-9423 CrossRef PubMed (Pubitemid 39391679)
10. Schomburg, L., Schweizer, U., Holtmann, B., Flohé, L., Sendtner, M. and Köhrle, J. (2003) Gene disruption discloses role of selenoprotein P in selenium delivery to target tissues. Biochem. J. 370, 397-402 CrossRef PubMed (Pubitemid 36315127)
11. Schweizer, U., Michaelis, M., Köhrle, J. and Schomburg, L. (2004) Efficient selenium transfer from mother to offspring in selenoprotein-P- deficient mice enables dose-dependent rescue of phenotypes associated with selenium deficiency. Biochem. J. 378, 21-26 CrossRef PubMed (Pubitemid 38299540)
12. Renko, K., Werner, M., Renner-Muller, I., Cooper, T. G., Yeung, C. H., Hollenbach, B., Scharpf, M., Köhrle, J., Schomburg, L. and Schweizer, U. (2008) Hepatic selenoprotein P (SePP) expression restores selenium transport and prevents infertility and motor-incoordination in Sepp-knockout mice. Biochem. J. 409, 741-749 CrossRef PubMed (Pubitemid 351214200)
13. Hill, K. E., Zhou, J., McMahan, W. J., Motley, A. K., Atkins, J. F., Gesteland, R. F. and Burk, R. F. (2003) Deletion of selenoprotein P alters distribution of selenium in the mouse. J. Biol. Chem. 278, 13640-13646 CrossRef PubMed (Pubitemid 36799899)
14. Hill, K. E., Zhou, J., McMahan, W. J., Motley, A. K. and Burk, R. F. (2004) Neurological dysfunction occurs in mice with targeted deletion of the selenoprotein p gene. J. Nutr. 134, 157-161 PubMed (Pubitemid 38057440)
15. Burk, R. F., Hill, K. E., Olson, G. E., Weeber, E. J., Motley, A. K., Winfrey, V. P. and Austin, L. M. (2007) Deletion of apolipoprotein E receptor-2 in mice lowers brain selenium and causes severe neurological dysfunction and death when a low-selenium diet is fed. J. Neurosci. 27, 6207-6211 CrossRef PubMed (Pubitemid 46890009)
16. Zhang, Y., Zhou, Y., Schweizer, U., Savaskan, N. E., Hua, D., Kipnis, J., Hatfield, D. L. and Gladyshev, V. N. (2008) Comparative analysis of selenocysteine machinery and selenoproteome gene expression in mouse brain identifies neurons as key functional sites of selenium in mammals. J. Biol. Chem. 283, 2427-2438 CrossRef PubMed
17. Wirth, E. K., Conrad, M., Winterer, J., Wozny, C., Carlson, B. A., Roth, S., Schmitz, D., Bornkamm, G. W., Coppola, V., Tessarollo, L. et al. (2010) Neuronal selenoprotein expression is required for interneuron development and prevents seizures and neurodegeneration. FASEB J. 24, 844-852 CrossRef PubMed
18. Pitts, M. W., Raman, A. V., Hashimoto, A. C., Todorovic, C., Nichols, R. A. and Berry, M. J. (2012) Deletion of selenoprotein P results in impaired function of parvalbumin interneurons and alterations in fear learning and sensorimotor gating. Neuroscience. 208, 58-68 CrossRef PubMed
19. Wirth, E. K., Bharathi, B. S., Hatfield, D., Conrad, M., Brielmeier, M. and Schweizer, U. (2014) Cerebellar hypoplasia in mice lacking selenoprotein biosynthesis in neurons. Biol. Trace Elem. Res. 158, 203-210 CrossRef PubMed
20. Agamy, O., Ben Zeev, B., Lev, D., Marcus, B., Fine, D., Su, D., Narkis, G., Ofir, R., Hoffmann, C., Leshinsky-Silver, E. et al. (2010) Mutations disrupting selenocysteine formation cause progressive cerebello-cerebral atrophy. Am. J. Hum. Genet. 87, 538-544 CrossRef PubMed
21. Ben Zeev, B., Hoffman, C., Lev, D., Watemberg, N., Malinger, G., Brand, N. and Lerman-Sagie, T. (2003) Progressive cerebellocerebral atrophy: a new syndrome with microcephaly, mental retardation, and spastic quadriplegia. J. Med. Genet. 40, e96 CrossRef PubMed
22. Dumitrescu, A. M., Liao, X. H., Abdullah, M. S., Lado-Abeal, J., Majed, F. A., Moeller, L. C., Boran, G., Schomburg, L., Weiss, R. E. and Refetoff, S. (2005) Mutations in SECISBP2 result in abnormal thyroid hormone metabolism. Nat. Genet. 37, 1247-1252 CrossRef PubMed (Pubitemid 41568708)
23. Azevedo, M. F., Barra, G. B., Naves, L. A., Ribeiro Velasco, L. F., Godoy Garcia, C. P., de Castro, L. C., Amato, A. A., Miniard, A., Driscoll, D. et al. (2010) Selenoprotein-related disease in a young girl caused by nonsense mutations in the SBP2 gene. J. Clin. Endocrinol. Metab. 95, 4066-4071 CrossRef PubMed
24. Seeher, S., Atassi, T., Mahdi, Y., Carlson, B. A., Braun, D., Wirth, E. K., Klein, M. O., Reix, N., Miniard, A. C., Schomburg, L. et al. (2014) Secisbp2 is essential for embryonic development and enhances selenoprotein expression. Antioxid. Redox Signal., doi:10.1089/ars.2013.5358 PubMed
25. Schweizer, U., Streckfuss, F., Pelt, P., Carlson, B. A., Hatfield, D. L., Köhrle, J. and Schomburg, L. (2005) Hepatically derived selenoprotein P is a key factor for kidney but not for brain selenium supply. Biochem. J. 386, 221-226 CrossRef PubMed (Pubitemid 40343779)
26. Magno, L., Catanzariti, V., Nitsch, R., Krude, H. and Naumann, T. (2009) Ongoing expression of Nkx2.1 in the postnatal mouse forebrain: potential for understanding NKX2.1 haploinsufficiency in humans? Brain Res. 1304, 164-186 CrossRef PubMed
27. Behrens, M. M., Ali, S. S., Dao, D. N., Lucero, J., Shekhtman, G., Quick, K. L. and Dugan, L. L. (2007) Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science 318, 1645-1647 CrossRef PubMed (Pubitemid 350233667)
28. Steullet, P., Cabungcal, J. H., Kulak, A., Kraftsik, R., Chen, Y., Dalton, T. P., Cuenod, M. and Do, K. Q. (2010) Redox dysregulation affects the ventral but not dorsal hippocampus: impairment of parvalbumin neurons, gamma oscillations, and related behaviors. J. Neurosci. 30, 2547-2558 CrossRef PubMed
29. Conrad, M., Sandin, A., Forster, H., Seiler, A., Frijhoff, J., Dagnell, M., Bornkamm, G. W., Radmark, O., Hooft van Huijsduijnen, R., Aspenstrom, P. et al. (2010) 12/15-lipoxygenase-derived lipid peroxides control receptor tyrosine kinase signaling through oxidation of protein tyrosine phosphatases. Proc. Natl. Acad. Sci. U.S.A. 107, 15774-15779 CrossRef PubMed
30. Patz, S., Grabert, J., Gorba, T., Wirth, M. J. and Wahle, P. (2004) Parvalbumin expression in visual cortical interneurons depends on neuronal activity and TrkB ligands during an Early period of postnatal development. Cereb. Cortex. 14, 342-351 CrossRef PubMed (Pubitemid 38252725)
31. Altar, C. A., Cai, N., Bliven, T., Juhasz, M., Conner, J. M., Acheson, A. L., Lindsay, R. M. and Wiegand, S. J. (1997) Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 389, 856-860 CrossRef PubMed (Pubitemid 27462980)
32. da Penha Berzaghi, M., Cooper, J., Castren, E., Zafra, F., Sofroniew, M., Thoenen, H. and Lindholm, D. (1993) Cholinergic regulation of brain-derived neurotrophic factor (BDNF) and nerve growth factor (NGF) but not neurotrophin-3 (NT-3) mRNA levels in the developing rat hippocampus. J. Neurosci. 13, 3818-3826 PubMed (Pubitemid 23264366)
33. Magno, L., Kretz, O., Bert, B., Ersozlu, S., Vogt, J., Fink, H., Kimura, S., Vogt, A., Monyer, H., Nitsch, R. and Naumann, T. (2011) The integrity of cholinergic basal forebrain neurons depends on expression of Nkx2-1. Eur. J. Neurosci. 34, 1767-1782 CrossRef PubMed
34. Fragkouli, A., van Wijk, N. V., Lopes, R., Kessaris, N. and Pachnis, V. (2009) LIM homeodomain transcription factor-dependent specification of bipotential MGE progenitors into cholinergic and GABAergic striatal interneurons. Development 136, 3841-3851 CrossRef PubMed
35. Weber, G. F., Maertens, P., Meng, X. Z. and Pippenger, C. E. (1991) Glutathione peroxidase deficiency and childhood seizures. Lancet 337, 1443-1444 CrossRef PubMed
36. Ramaekers, V. T., Calomme, M., Vanden Berghe, D. and Makropoulos, W. (1994) Selenium deficiency triggering intractable seizures. Neuropediatrics 25, 217-223 CrossRef PubMed (Pubitemid 24304611)
37. Marin, O. (2012) Interneuron dysfunction in psychiatric disorders. Nat. Rev. Neurosci. 13, 107-120 PubMed
38. Dumitrescu, A. M., Di Cosmo, C., Liao, X. H., Weiss, R. E. and Refetoff, S. (2010) The syndrome of inherited partial SBP2 deficiency in humans. Antioxid. Redox Signal. 12, 905-920 CrossRef PubMed
39. Schoenmakers, E., Agostini, M., Mitchell, C., Schoenmakers, N., Papp, L., Rajanayagam, O., Padidela, R., Ceron-Gutierrez, L., Doffinger, R., Prevosto, C. et al. (2010) Mutations in the selenocysteine insertion sequence-binding protein 2 gene lead to a multisystem selenoprotein deficiency disorder in humans. J. Clin. Invest. 120, 4220-4235 CrossRef PubMed