Selenoprotein T Exerts an Essential Oxidoreductase Activity That Protects Dopaminergic Neurons in Mouse Models of Parkinson's Disease

Antioxidants and Redox Signaling

Volumn 24, Issue 11, 2016, Pages 557-574

  Boukhzar, Loubna ^a,b,c   Hamieh, Abdallah ^a,b,c   Cartier, Dorthe ^a,b,c   Tanguy, Yannick ^a,b,c   Alsharif, Ifat ^a,b,c   Castex, Matthieu ^a,b,c   Arabo, Arnaud ^b   Hajji, Sana El ^a,b,c   Bonnet, Jean Jacques ^a,b,c   Errami, Mohammed ^d   Falluel Morel, Anthony ^a,b,c   Chagraoui, Abdeslam ^a,b,c   Lihrmann, Isabelle ^a,b,c   Anouar, Youssef ^a,b,c  

^a Université de Rouen   (France)

^b UNIVERSITÉ DE ROUEN   (France)

^c UNIVERSITY OF ROUEN   (France)

^d ABDELMALEK ESSAADI UNIVERSITY   (Morocco)

Author keywords

[No Author keywords available]

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; DOPAMINE; GLIAL FIBRILLARY ACIDIC PROTEIN; NEUROTOXIN; OXIDOREDUCTASE; REACTIVE OXYGEN METABOLITE; RECOMBINANT PROTEIN; RECOMBINANT SELENOPROTEIN T; ROTENONE; SELENOPROTEIN; SELENOPROTEIN T; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; SELENOPROTEIN T, MOUSE;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CELL VIABILITY; COMPARATIVE STUDY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DORSAL STRIATUM; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; GENE DISRUPTION; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN TISSUE; MOTOR DYSFUNCTION; MOUSE; NERVE DEGENERATION; NEUROPROTECTION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PARKINSONISM; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; REARING; REDOX STRESS; ANIMAL; C57BL MOUSE; CELL DEATH; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY;

ANIMALS; CELL DEATH; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROTOXINS; OXIDATIVE STRESS; OXIDOREDUCTASES; PARKINSON DISEASE; SELENOPROTEINS;

EID: 84964804537     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2015.6478     Document Type: Article

References (59)

1. Aachmann FL, Fomenko DE, Soragni A, Gladyshev VN, and Dikiy A. Solution structure of selenoprotein W and NMR analysis of its interaction with 14-3-3 proteins. J Biol Chem 282: 37036-37044, 2007.
2. Ara J, Przedborski S, Naini AB, Jackson-Lewis V, Trifiletti RR, Horwitz J, and Ischiropoulos H. Inactivation of tyrosine hydroxylase by nitration following exposure to peroxynitrite and 1-methyl-4-phenyl-l, 2, 3, 6-tetrahydropyridine (MPTP). Proc Natl Acad Sci USA 95: 7659-7663, 1998.
3. Arodin L, Miranda-Vizuete A, Swoboda P, and Fernandes AP. Protective effects of the thioredoxin and glutaredoxin systems in dopamine-induced cell death. Free Radio Biol Med 73: 328-336, 2014.
4. Bellinger FP, Bellinger MT, Seale LA, Takemoto AS, Raman AV, Miki T, Manning-Bog AB, Berry MJ, White LR, and Ross GW. Glutathione peroxidase 4 is associated with neuromelanin in substantia nigra and dystrophic axons in putamen of Parkinson's brain. Mol Neurodegener 6: 8, 2011.
5. Bellinger FP, Raman AV, Reeves MA, and Berry MJ. Regulation and function of selenoproteins in human disease. Biochem J 422: 11-22, 2009.
6. Bellinger FP, Raman AV, Rueli RH, Bellinger MT, Dewing AS, Seale LA, Andres MA, Uyehara-Lock JH, White LR, Ross GW, and Berry MJ. Changes in selenoprotein P in substantia nigra and putamen in Parkinson's disease. J Parkinsons Dis 1: 115-126, 2012.
7. Bisaglia M, Greggio E, Beltramini M, and Bubacco L. Dysfunction of dopamine homeostasis: clues in the hunt for novel Parkinson's disease therapies. FASEBJ11:1101-1110, 2013.
8. Blanchard-Fillion B, Prou D, Polydoro M, Spielberg D, Tsika E, Wang Z, Hazen SL, Koval M, Przedborski S, and Ischir opoulos H. Metabolism of 3-nitrotyrosine induces apoptotic death in dopaminergic cells. JNeurosci 26: 6124-6130, 2006.
9. Bove J and Perier C. Neurotoxin-based models of Parkin son's disease. Neuroscience 111: 51-76, 2012.
10. Burke RE and O'Malley K. Axon degeneration in Parkinson's disease. Exp Neurol 146: 72-83, 2013.
11. Cannon JR, Tapias VM, Na HM, Honick AS, Drolet RE, and Greenamyre TJ. A highly reproducible rotenone model of Parkinson's disease. Neurobiol Dis 34: 279-290, 2009.
12. Cassarino DS, Fall CP, Swerdlow RH, Smith TS, Halvor-sen EM, Miller SW, Parks JP, Parker WD, Jr., and Bennett JP, Jr. Elevated reactive oxygen species and antioxidant enzyme activities in animal and cellular models of Parkinson's disease. Biochim Biophys Acta 1362: 77-86, 1997.
13. Castex MT, Arabo A, Benard M, Roy V, Le Joncour V, Prevost G, Bonnet JJ, Anouar Y, and Falluel-Morel A. Selenoprotein T deficiency leads to neurodevelopmental abnormalities and hyperactive behavior in mice. Mol Neurobiol 2015 [Epub ahead of print]. DOI: 10.1007/S12035-015-9505-7.
14. Chinta SJ and Andersen JK. Redox imbalance in Parkinson's disease. Biochim Biophys Acta 1780: 1362-1367, 2008.
15. Ciesielska A, Joniec I, Kurkowska-Jastrzebska I, Cudna A, Przybylkowski A, Czlonkowska A, and Czlonkowski A. The impact of age and gender on the striatal astrocytes activation in murine model of Parkinson's disease. Inflamm Res 58: 747-753, 2009.
16. Conrad M, Jakupoglu C, Moreno SG, Lippl S, Banjac A, Schneider M, Beck H, Hatzopoulos AK, Just U, Sinowatz F, Schmahl W, Chien KR, Wurst W, Bornkamm GW, and Brielmeier M. Essential role for mitochondrial thioredoxin reductase in hematopoiesis, heart development, and heart function. Mol Cell Biol 14: 9414-9423, 2004.
17. de Lau LM and Breteler MM. Epidemiology of Parkinson's disease. Lancet Neurol 5: 525-535, 2006.
18. Deacon RM. Measuring motor coordination in mice. J Vis Exp 75: 1-8, 2013.
19. Dikiy A, Novoselov SV, Fomenko DE, Sengupta A, Carlson BA, Cerny RL, Ginalski K, Grishin NV, Hatfield DL, and Gladyshev VN. SelT, SelW, SelH, and Rdxl2: genomics and molecular insights into the functions of selenoproteins of a novel thioredoxin-like family. Biochem J 46: 6871-6882, 2007.
20. Fleming SM, Zhu C, Fernagut PO, Mehta A, DiCarlo CD, Seaman RL, and Chesselet MF. Behavioral and immuno-histochemical effects of chronic intravenous and subcutaneous influsions of varying doses of rotenone. Exp Neurol 187: 418-429, 2004.
21. Gibrat C, Saint-Pierre M, Bousquet M, Levesque D, Rouillard C, and Cicchetti F. Differences between subacute and chronic MPTP mice models: investigation of dopaminergic neuronal degeneration and alpha-synuclein inclusion. J Neurochem 109: 1469-1482, 2009.
22. Goldberg JA, Guzman JN, Estep CM, Ilijic E, Kondapalli J, Sanchez-Padilla J, and Surmeier DJ. Calcium entry induces mitochondrial oxidant stress in vagal neurons at risk in Parkinson's disease. Nat Neurosci 15: 1414-1421, 2012.
23. Grumolato L, Ghzili H, Montero-Hadjadje M, Gasman S, Lesage J, Tanguy Y, Galas L, Ait-Ali D, Leprince J, Guer-ineau NC, Elkahloun AG, Fournier A, Vieau D, Vaudry H, and Anouar Y. Selenoprotein T is a PACAP-regulated gene involved in intracellular Ca2+ mobilization and neuroendocrine secretion. FASEBJ11: 1756-1768, 2008.
24. Grumolato L, Liu G, Mong P, Mudbhary R, Biswas R, Ar-royave R, Vijayakumar S, Economides AN, and Aaronson SA. Canonical and noncanonical Wnts use a common mechanism to activate completely unrelated coreceptors. Genes Dev 24: 2517-2530, 2010.
25. Hatfield DL, Tsuji PA, Carlson BA, and Gladyshev VN. Selenium and selenocysteine: roles in cancer, health and development. Trends Biochem Sci 39: 112-120, 2014.
26. Hwang O. Role of oxidative stress in Parkinson's disease. Exp Neurobiol 11: 11-17, 2013.
27. Ischiropoulos H. Biological selectivity and functional aspects of protein tyrosine nitration. Biochem Biophys Res Commun 305: 776-783, 2003.
28. Jakupoglu C, Przemeck GKH, Schneider M, Moreno SG, Mayr N, Katzopoulos AK, Hrabe de Angelis M, Wurst W, Bornkamm GW, Brielmeier M, and Conrad M. Cytoplasmic thioredoxin reductase is essential for embryogen-esis but dispensable for cardiac development. Mol Cell Biol 25: 1980-1988, 2005.
29. Jenner P, Schapira AH, and Marsden CD. New insights into the cause of Parkinson's disease. Neurology 42: 2241-2250, 1992.
30. Klivenyi P, Andreassen OA, Ferrante RJ, Dedeoglu A, Mueller G, Lancelot E, Bogdanov M, Andersen JK, Jiang D, and Beal MF. Mice deficient in cellular glutathione peroxidase show increased vulnerability to malonate, 3-nitropropionic acid, and l-methyl-4-phenyl-l, 2, 5, 6-tetrahydropyridine. J Neurosci 20: 1-7, 2000.
31. Kohutnicka M, Lewandowska E, Kurkowska-Jastrzebska I, Czlonkowski A, and Czlonkowska A. Microglial and astro-cytic involvement in a murine model of Parkinson's disease induced by l-methyl-4-phenyl-l, 2, 3, 6-tetrahydropyridine (MPTP). Immunopharmacology 39: 167-180, 1998.
32. Kryukov GV, Kryukov VM, and Gladyshev VN. New mammalian selenocysteine-containing proteins identified with an algorithm that searches for selenocysteine insertion sequence elements. J Biol Chem 21 A: 33888-33897, 1999.
33. Labunskyy VM, Yoo MH, Hatfield DL, and Gladyshev VN. Sepl5, a thioredoxin-like selenoprotein, is involved in the unfolded protein response and differentially regulated by adaptive and acute ER stresses. Biochemistry 48: 8458-8465, 2009.
34. Lee S, Kim SM, and Lee RT. Thioredoxin and thioredoxin target proteins: from molecular mechanisms to functional significance. Antioxid Redox Signal 18: 1165-1207, 2013.
35. Lees AJ, Hardy J, and Revesz T. Parkinson's disease. Lancet 373: 2055-2066, 2009.
36. Lin MT and Beal MF. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443: 787-795, 2006.
37. Lopert P, Day BJ, and Patel M. Thioredoxin reductase deficiency potentiates oxidative stress, mitochondrial dysfunction and cell death in dopaminergic cells. PLoS One 7: e50683, 2012.
38. Lotharious J and Brundin P. Pathogenesis of Parkinson's disease: dopamine, vesicles and a-synuclein. Nature 3: 932-942, 2002.
39. Luthman M and Holmgren A. Rat liver thioredoxin and thioredoxin reductase: purification and characterization. Biochemistry 21: 6628-6633, 1982.
40. Marchi S, Giorgi C, Suski JM, Agnoletto C, Bononi A, Bonora M, De Marchi E, Missiroli S, Patergnani S, Poletti F, Rimessi A, Duszynski J, Wieckowski MR, and Pinton P. Mitochondria-ros crosstalk in the control of cell death and aging. J Signal Transduct 2012: 329635, 2012.
41. Obeso J A, Rodriguez-Oroz MC, Goetz CG, Marin C, Kordower JH, Rodriguez M, Hirsch EC, Farrer M, Schapira AH, and Halliday G. Missing pieces in the Parkinson's disease puzzle. Nat Med 16: 653-661, 2010.
42. Prevost G, Arabo A, Jian L, Quelennec E, Cartier D, Hassan S, Falluel-Morel A, Tanguy Y, Gargani S, Lihrmann I, Kerr-Conte J, Lefebvre H, Pattou F, and Anouar Y. The PACAP-regulated gene selenoprotein T is abundantly expressed in mouse and human beta-cells and its targeted inactivation impairs glucose tolerance. Endocrinology 154: 3796-3806, 2013.
43. Rayman MP. Selenium and human health. Lancet 379: 1256-1268, 2012.
44. Sanchez-Ramos J, Barrett JN, Goldstein M, Weiner WJ, and Hefti F. 1-Methyl-4-phenylpyridinium (MPP+) but not 1-methyl-4-phenyl-l, 2, 3, 6-tetrahydropyridine (MPTP) selectively destroys dopaminergic neurons in cultures of dissociated rat mesencephalic neurons. Neurosci Lett 12: 215-220, 1986.
45. Schapira AHV. Mitochondria in the aetiology and pathogenesis of Parkinson's disease. Lancet Neurol 7: 97-109, 2008.
46. Schultz W. Predictive reward signal of dopamine neurons. J Neurophysiol 80: 1-27, 1998.
47. Seeher S, Carlson BA, Miniard AC, Wirth EK, Mahdi Y, Hatfield DL, Driscoll DM, and Schweizer U. Impaired selenoprotein expression in brain triggers striatal neuronal loss leading to coordination defects in mice. Biochem J 462: 67-75, 2014.
48. Sengupta A, Carlson BA, Labunskyy VM, Gladyshev VN, and Hatfield DL. Selenoprotein T deficiency alters cell adhesion and elevates selenoprotein W expression in murine fibroblast cells. Biochem Cell Biol 87: 953-961, 2009.
49. Shchedrina VA, Everley RA, Zhang Y, Gygi SP, Hatfield DL, and Gladyshev VN. Selenoprotein K binds multiprotein complexes and is involved in the regulation of endoplasmic reticulum homeostasis. J Biol Chem 286:42937-42948, 2011.
50. Shinomol GK, Mythri RB, Srinivas Bharath MM, and Mur-alidhara. Bacopa monnieri extract offsets rotenone-induced cytotoxicity in dopaminergic cells and oxidative impairments in mice brain. Cell Mol Neurobiol 32: 455-465, 2012.
51. Soerensen J, Jakupoglu C, Beck H, Forster H, Schmidt J, Schmahl W, Schweizer U, Conrad M, and Brielmeier M. The role of thioredoxin reductases in brain development. PLoS One 3: el813, 2008.
52. Subramaniam SR and Chesselet MF. Mitochondrial dysfunction and oxidative stress in Parkinson's disease. Prog Neurobiol 106-107: 17-32, 2013.
53. Tanguy Y, Falluel-Morel A, Arthaud S, Boukhzar L, Manecka DL, Chagraoui A, Prevost G, Elias S, Dorval-Coiffec I, Lesage J, Vieau D, Lihrmann I, Jegou B, and Anouar Y. The PACAP-regulated gene selenoprotein T is highly induced in nervous, endocrine, and metabolic tissues during ontogenetic and regenerative processes. Endocrinology 152: 4322-4335, 2011.
54. Teismann P and Schulz JB. Cellular pathology of Parkinson's disease: astrocytes, microglia and inflammation. Cell Tissue Res 318: 149-161, 2004.
55. Thomas B and Beal MF. Parkinson's disease. Hum Mol Genet 2: R183-R194, 2007.
56. Tranche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, Bock R, Klein R, and Schiitz G. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23: 99-103, 1999.
57. Valentine WM, Abel TW, Hill KE, Austin LM, and Burk RF. Neurodegeneration in mice resulting from loss of fonctional selenoprotein P or its receptor apolipoprotein E receptor 2. J Neuropathol Exp Neurol 67: 68-77, 2008.
58. Viggiano D, Vallone D, and Sadile A. Dysfunctions in dopamine systems and ADHD: evidence from animals and modeling. Neural Plast 11: 97-114, 2004.
59. Wirth EK, Conrad M, Winterer J, Wozny C, Carlson BA, Roth S, Schmitz D, Bornkamm GW, Coppola V, Tessarollo L, Schomburg L, Kohrle J, Hatfield DL, and Schweizer U. Neuronal selenoprotein expression is required for inter-neuron development and prevents seizures and neurodegeneration. FASEB J 24: 844-852, 2010.