The expression and activity of thioredoxin reductase 1 splice variants v1 and v2 regulate the expression of genes associated with differentiation and adhesion

Bioscience Reports

Volumn 35, Issue 6, 2015, Pages

  Nalvarte, Ivan ^a   Damdimopoulos, Anastasios E ^a   Rüegg, Jöelle ^a,b   Spyrou, Giannis ^c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b Swedish Toxicology Sciences Research Center   (Sweden)

^c LINKÖPING UNIVERSITY   (Sweden)

Author keywords

Differentiation; Migration; Oxidative stress; Selenium; Thioredoxin reductase

Indexed keywords

CADHERIN; CADHERIN 11; FIBRONECTIN; FIBRONECTIN 1; THIOREDOXIN REDUCTASE 1; THIOREDOXIN REDUCTASE 1 SPLICE VARIANT V1; THIOREDOXIN REDUCTASE 1 SPLICE VARIANT V2; UNCLASSIFIED DRUG; ISOPROTEIN; TXNRD1 PROTEIN, HUMAN;

ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; GENE CONTROL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GROWTH RATE; HEK293 CELL LINE; HUMAN; HUMAN CELL; PROTEIN FUNCTION; ALTERNATIVE RNA SPLICING; BIOSYNTHESIS; GENETICS; OXIDATION REDUCTION REACTION;

ALTERNATIVE SPLICING; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEK293 CELLS; HUMANS; OXIDATION-REDUCTION; PROTEIN ISOFORMS; THIOREDOXIN REDUCTASE 1;

EID: 84956910717     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20150236     Document Type: Article

References (57)

1. Holmgren, A. (1989) Thioredoxin and glutaredoxin systems. J. Biol. Chem. 264, 13963-13966 PubMed
2. Arner, E.S. and Holmgren, A. (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267, 6102-6109 CrossRef PubMed
3. Lu, J., Berndt, C. and Holmgren, A. (2009) Metabolism of selenium compounds catalyzed by the mammalian selenoprotein thioredoxin reductase. Biochim. Biophys. Acta 1790, 1513-1519 CrossRef PubMed
4. Mahmood, D.F., Abderrazak, A., El Hadri, K., Simmet, T. and Rouis, M. (2013) The thioredoxin system as a therapeutic target in human health and disease. Antioxid. Redox Signal. 19, 1266-1303 CrossRef PubMed
5. Mustacich, D. and Powis, G. (2000) Thioredoxin reductase. Biochem. J. 346 (Pt 1), 1-8 CrossRef PubMed
6. Gladyshev, V.N., Jeang, K.T. and Stadtman, T.C. (1996) Selenocysteine, identified as the penultimate C-terminal residue in human T-cell thioredoxin reductase, corresponds to TGA in the human placental gene. Proc. Natl. Acad. Sci. U.S.A. 93, 6146-6151 CrossRef PubMed
7. Zhong, L., Arner, E.S. and Holmgren, A. (2000) Structure and mechanism of mammalian thioredoxin reductase: the active site is a redox-active selenolthiol/selenenylsulfide formed from the conserved cysteine-selenocysteine sequence. Proc. Natl. Acad. Sci. U.S.A. 97, 5854-5859 CrossRef PubMed
8. Sandalova, T., Zhong, L., Lindqvist, Y., Holmgren, A. and Schneider, G. (2001) Three-dimensional structure of a mammalian thioredoxin reductase: implications for mechanism and evolution of a selenocysteine-dependent enzyme. Proc. Natl. Acad. Sci. U.S.A. 98, 9533-9538 CrossRef PubMed
9. Nordberg, J. and Arner, E.S. (2001) Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic. Biol. Med. 31, 1287-1312 CrossRef PubMed
10. Arner, E.S. (2009) Focus on mammalian thioredoxin reductases-important selenoproteins with versatile functions. Biochim. Biophys. Acta 1790, 495-526 CrossRef PubMed
11. Xia, L., Nordman, T., Olsson, J.M., Damdimopoulos, A., Bjorkhem-Bergman, L., Nalvarte, I., Eriksson, L.C., Arner, E.S., Spyrou, G. and Bjornstedt, M. (2003) The mammalian cytosolic selenoenzyme thioredoxin reductase reduces ubiquinone. A novel mechanism for defense against oxidative stress. J. Biol. Chem. 278, 2141-2146 CrossRef PubMed
12. Miranda-Vizuete, A., Damdimopoulos, A.E., Pedrajas, J.R., Gustafsson, J.A. and Spyrou, G. (1999) Human mitochondrial thioredoxin reductase cDNA cloning, expression and genomic organization. Eur. J. Biochem. 261, 405-412 CrossRef PubMed
13. Miranda-Vizuete, A., Damdimopoulos, A.E. and Spyrou, G. (2000) The mitochondrial thioredoxin system. Antioxid. Redox Signal. 2, 801-810 CrossRef PubMed
14. Sun, Q.A., Kirnarsky, L., Sherman, S. and Gladyshev, V.N. (2001) Selenoprotein oxidoreductase with specificity for thioredoxin and glutathione systems. Proc. Natl. Acad. Sci. U.S.A. 98, 3673-3678 CrossRef PubMed
15. Su, D. and Gladyshev, V.N. (2004) Alternative splicing involving the thioredoxin reductase module in mammals: a glutaredoxin-containing thioredoxin reductase 1. Biochemistry 43, 12177-12188 CrossRef PubMed
16. Rundlof, A.K., Fernandes, A.P., Selenius, M., Babic, M., Shariatgorji, M., Nilsonne, G., Ilag, L.L., Dobra, K. and Bjornstedt, M. (2007) Quantification of alternative mRNA species and identification of thioredoxin reductase 1 isoforms in human tumor cells. Differentiation 75, 123-132 CrossRef PubMed
17. Nalvarte, I., Damdimopoulos, A.E., Nystom, C., Nordman, T., Miranda-Vizuete, A., Olsson, J.M., Eriksson, L., Bjornstedt, M., Arner, E.S. and Spyrou, G. (2004) Overexpression of enzymatically active human cytosolic and mitochondrial thioredoxin reductase in HEK-293 cells. Effect on cell growth and differentiation. J. Biol. Chem. 279, 54510-54517 CrossRef PubMed
18. Sroka, J., Antosik, A., Czyz, J., Nalvarte, I., Olsson, J.M., Spyrou, G. and Madeja, Z. (2007) Overexpression of thioredoxin reductase 1 inhibits migration of HEK-293 cells. Biol. Cell 99, 677-687 CrossRef PubMed
19. Rao, A.K., Ziegler, Y.S., McLeod, I.X., Yates, J.R. and Nardulli, A.M. (2009) Thioredoxin and thioredoxin reductase influence estrogen receptor alpha-mediated gene expression in human breast cancer cells. J. Mol. Endocrinol. 43, 251-261 CrossRef PubMed
20. Damdimopoulos, A.E., Miranda-Vizuete, A., Treuter, E., Gustafsson, J.A. and Spyrou, G. (2004) An alternative splicing variant of the selenoprotein thioredoxin reductase is a modulator of estrogen signaling. J. Biol. Chem. 279, 38721-38729 CrossRef PubMed
21. Holmgren, A. and Bjornstedt, M. (1995) Thioredoxin and thioredoxin reductase. Methods Enzymol. 252, 199-208 CrossRef PubMed
22. Psarra, A.M., Hermann, S., Panayotou, G. and Spyrou, G. (2009) Interaction of mitochondrial thioredoxin with glucocorticoid receptor and NF-kappaB modulates glucocorticoid receptor and NF-kappaB signalling in HEK-293 cells. Biochem. J. 422, 521-531 CrossRef PubMed
23. Miranda-Vizuete, A. and Spyrou, G. (1997) The novel oxidoreductase KDRF (KM-102-derived reductase-like factor) is identical with human thioredoxin reductase. Biochem. J. 325 (Pt 1), 287-288 CrossRef PubMed
24. Koishi, R., Kawashima, I., Yoshimura, C., Sugawara, M. and Serizawa, N. (1997) Cloning and characterization of a novel oxidoreductase KDRF from a human bone marrow-derived stromal cell line KM-102. J. Biol. Chem. 272, 2570-2577 CrossRef PubMed
25. Leist, M., Raab, B., Maurer, S., Rosick, U. and Brigelius-Flohe, R. (1996) Conventional cell culture media do not adequately supply cells with antioxidants and thus facilitate peroxide-induced genotoxicity. Free Radic. Biol. Med. 21, 297-306 CrossRef PubMed
26. Madeja, Z., Sroka, J., Nystrom, C., Bjorkhem-Bergman, L., Nordman, T., Damdimopoulos, A., Nalvarte, I., Eriksson, L.C., Spyrou, G., Olsson, J.M. and Bjornstedt, M. (2005) The role of thioredoxin reductase activity in selenium-induced cytotoxicity. Biochem. Pharmacol. 69, 1765-1772 CrossRef PubMed
27. Sallmon, H., Hoene, V., Weber, S.C. and Dame, C. (2010) Differentiation of human SH-SY5Y neuroblastoma cells by all-trans retinoic acid activates the interleukin-18 system. J. Interferon Cytokine Res. 30, 55-58 CrossRef PubMed
28. Kawaguchi, Y. (2013) Sox9 and programming of liver and pancreatic progenitors. J. Clin. Invest. 123, 1881-1886 CrossRef PubMed
29. Pankov, R. and Yamada, K.M. (2002) Fibronectin at a glance. J. Cell Sci. 115, 3861-3863 CrossRef PubMed
30. Huang, C.F., Lira, C., Chu, K., Bilen, M.A., Lee, Y.C., Ye, X., Kim, S.M., Ortiz, A., Wu, F.L., Logothetis, C.J. et al. (2010) Cadherin-11 increases migration and invasion of prostate cancer cells and enhances their interaction with osteoblasts. Cancer Res. 70, 4580-4589 CrossRef PubMed
31. Sheppard, A.M., Brunstrom, J.E., Thornton, T.N., Gerfen, R.W., Broekelmann, T.J., McDonald, J.A. and Pearlman, A.L. (1995) Neuronal production of fibronectin in the cerebral cortex during migration and layer formation is unique to specific cortical domains. Dev. Biol. 172, 504-518 CrossRef PubMed
32. Allen, R.G., Newton, R.K., Sohal, R.S., Shipley, G.L. and Nations, C. (1985) Alterations in superoxide dismutase, glutathione, and peroxides in the plasmodial slime mold Physarum polycephalum during differentiation. J. Cell. Physiol. 125, 413-419 CrossRef PubMed
33. Leonarduzzi, G., Sottero, B., Testa, G., Biasi, F. and Poli, G. (2011) New insights into redox-modulated cell signaling. Curr. Pharm. Des. 17, 3994-4006 CrossRef PubMed
34. Abate, C., Patel, L., Rauscher, 3rd, F.J. and Curran, T. (1990) Redox regulation of fos and jun DNA-binding activity in vitro. Science 249, 1157-1161 CrossRef PubMed
35. Rundlof, A.K. and Arner, E.S. (2004) Regulation of the mammalian selenoprotein thioredoxin reductase 1 in relation to cellular phenotype, growth, and signaling events. Antioxid. Redox Signal. 6, 41-52 CrossRef PubMed
36. Schreck, R. and Baeuerle, P.A. (1991) A role for oxygen radicals as second messengers. Trends Cell Biol. 1, 39-42 CrossRef PubMed
37. 2 for platelet-derived growth factor signal transduction. Science 270, 296-299 CrossRef PubMed
38. Pahlman, S., Ruusala, A.I., Abrahamsson, L., Mattsson, M.E. and Esscher, T. (1984) Retinoic acid-induced differentiation of cultured human neuroblastoma cells: a comparison with phorbolester-induced differentiation. Cell Differ. 14, 135-144 CrossRef PubMed
39. Richardson, S.H., Starborg, T., Lu, Y., Humphries, S.M., Meadows, R.S. and Kadler, K.E. (2007) Tendon development requires regulation of cell condensation and cell shape via cadherin-11-mediated cell-cell junctions. Mol. Cell. Biol. 27, 6218-6228 CrossRef PubMed
40. Schulte, J.D., Srikanth, M., Das, S., Zhang, J., Lathia, J.D., Yin, L., Rich, J.N., Olson, E.C., Kessler, J.A. and Chenn, A. (2013) Cadherin-11 regulates motility in normal cortical neural precursors and glioblastoma. PLoS One 8, e70962 CrossRef PubMed
41. Du, Y.H., Hirooka, K., Miyamoto, O., Bao, Y.Q., Zhang, B., An, J.B. and Ma, J.X. (2013) Retinoic acid suppresses the adhesion and migration of human retinal pigment epithelial cells. Exp. Eye Res. 109, 22-30 CrossRef PubMed
42. Pires Neto, M.A., Braga-de-Souza, S. and Lent, R. (1999) Extracellular matrix molecules play diverse roles in the growth and guidance of central nervous system axons. Braz. J. Med. Biol. Res. 32, 633-638 CrossRef PubMed
43. Gorreta, F., Runfola, T.P., VanMeter, A.J., Barzaghi, D., Chandhoke, V. and Del Giacco, L. (2005) Identification of thioredoxin reductase 1-regulated genes using small interference RNA and cDNA microarray. Cancer Biol. Ther. 4, 1079-1088 CrossRef PubMed
44. Heard, D.J., Norby, P.L., Holloway, J. and Vissing, H. (2000) Human ERRgamma, a third member of the estrogen receptor-related receptor (ERR) subfamily of orphan nuclear receptors: tissue-specific isoforms are expressed during development and in the adult. Mol. Endocrinol. 14, 382-392 PubMed
45. Damdimopoulou, P.E., Miranda-Vizuete, A., Arner, E.S., Gustafsson, J.A. and Damdimopoulos, A.E. (2009) The human thioredoxin reductase-1 splice variant TXNRD1-v3 is an atypical inducer of cytoplasmic filaments and cell membrane filopodia. Biochim. Biophys. Acta 1793, 1588-1596 CrossRef PubMed
46. Cassidy, P.B., Edes, K., Nelson, C.C., Parsawar, K., Fitzpatrick, F.A. and Moos, P.J. (2006) Thioredoxin reductase is required for the inactivation of tumor suppressor p53 and for apoptosis induced by endogenous electrophiles. Carcinogenesis 27, 2538-2549 CrossRef PubMed
47. Moos, P.J., Edes, K., Cassidy, P., Massuda, E. and Fitzpatrick, F.A. (2003) Electrophilic prostaglandins and lipid aldehydes repress redox-sensitive transcription factors p53 and hypoxia-inducible factor by impairing the selenoprotein thioredoxin reductase. J. Biol. Chem. 278, 745-750 CrossRef PubMed
48. Matthews, J.R., Wakasugi, N., Virelizier, J.L., Yodoi, J. and Hay, R.T. (1992) Thioredoxin regulates the DNA binding activity of NF-kappa B by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Res. 20, 3821-3830 CrossRef PubMed
49. Seemann, S. and Hainaut, P. (2005) Roles of thioredoxin reductase 1 and APE/Ref-1 in the control of basal p53 stability and activity. Oncogene 24, 3853-3863 CrossRef PubMed
50. Karimpour, S., Lou, J., Lin, L.L., Rene, L.M., Lagunas, L., Ma, X., Karra, S., Bradbury, C.M., Markovina, S., Goswami, P.C. et al. (2002) Thioredoxin reductase regulates AP-1 activity as well as thioredoxin nuclear localization via active cysteines in response to ionizing radiation. Oncogene 21, 6317-6327 CrossRef PubMed
51. Low, S.C., Grundner-Culemann, E., Harney, J.W. and Berry, M.J. (2000) SECIS-SBP2 interactions dictate selenocysteine incorporation efficiency and selenoprotein hierarchy. EMBO J. 19, 6882-6890 CrossRef PubMed
52. Moustafa, M.E., Carlson, B.A., El-Saadani, M.A., Kryukov, G.V., Sun, Q.A., Harney, J.W., Hill, K.E., Combs, G.F., Feigenbaum, L., Mansur, D.B. et al. (2001) Selective inhibition of selenocysteine tRNA maturation and selenoprotein synthesis in transgenic mice expressing isopentenyladenosine-deficient selenocysteine tRNA. Mol. Cell. Biol. 21, 3840-3852 CrossRef PubMed
53. Bjornstedt, M., Odlander, B., Kuprin, S., Claesson, H.E. and Holmgren, A. (1996) Selenite incubated with NADPH and mammalian thioredoxin reductase yields selenide, which inhibits lipoxygenase and changes the electron spin resonance spectrum of the active site iron. Biochemistry 35, 8511-8516 CrossRef PubMed
54. Bosl, 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
55. McKenzie, R.C., Arthur, J.R. and Beckett, G.J. (2002) Selenium and the regulation of cell signaling, growth, and survival: molecular and mechanistic aspects. Antioxid. Redox Signal. 4, 339-351 CrossRef PubMed
56. 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
57. Matsui, M., Oshima, M., Oshima, H., Takaku, K., Maruyama, T., Yodoi, J. and Taketo, M.M. (1996) Early embryonic lethality caused by targeted disruption of the mouse thioredoxin gene. Dev. Biol. 178, 179-185 CrossRef PubMed