SEPN1, an endoplasmic reticulum-localized selenoprotein linked to skeletal muscle pathology, counteracts hyperoxidation by means of redox-regulating SERCA2 pump activity

Human Molecular Genetics

Volumn 24, Issue 7, 2014, Pages 1843-1855

  Marino, Marianna ^a   Stoilova, Tatiana ^a   Giorgi, Carlotta ^b   Bachi, Angela ^c   Cattaneo, Angela ^c   Auricchio, Alberto ^d   Pinton, Paolo ^b   Zito, Ester ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b UNIVERSITY OF FERRARA   (Italy)

^c FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; PARVOVIRUS VECTOR; PEROXIDE; PROTEIN SEPN1; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SELENOPROTEIN; UNCLASSIFIED DRUG; ATP2A2 PROTEIN, MOUSE; CYSTEINE; MUSCLE PROTEIN; OXIDOREDUCTASE; SEPN1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE; GENE MUTATION; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; MOUSE; MYOPATHY; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEPN1 GENE; ANIMAL; GENETICS; METABOLISM; MUSCLE DISEASE; PATHOLOGY; SKELETAL MUSCLE;

ADENO-ASSOCIATED VIRUS; MUS;

ANIMALS; CYSTEINE; ENDOPLASMIC RETICULUM; HUMANS; MICE; MICE, KNOCKOUT; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR DISEASES; OXIDATION-REDUCTION; OXIDOREDUCTASES; PEROXIDES; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SELENOPROTEINS;

EID: 84926475413     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu602     Document Type: Article

References (50)

1. Petit, N., Lescure, A., Rederstorff, M., Krol, A., Moghadaszadeh, B., Wewer, U.M. and Guicheney, P. (2003) Selenoprotein N: an endoplasmic reticulum glycoprotein with an early developmental expression pattern. Hum. Mol. Genet., 12, 1045-1053.
2. Castets, P., Maugenre, S., Gartioux, C., Rederstorff, M., Krol, A., Lescure, A., Tajbakhsh, S., Allamand, V. and Guicheney, P. (2009) Selenoprotein N is dynamically expressed during mouse development and detected early in muscle precursors. BMC Dev. Biol., 9, 46.
3. Rederstorff, M., Castets, P., Arbogast, S., Laine, J., Vassilopoulos, S., Beuvin, M., Dubourg, O., Vignaud, A., Ferry, A., Krol, A. et al. (2011) Increased muscle stress-sensitivity induced by selenoproteinNinactivation in mouse: a mammalian model for SEPN1-related myopathy. PLoS ONE, 6, e23094.
4. Moghadaszadeh, B., Rider, B.E., Lawlor, M.W., Childers, M.K., Grange, R.W., Gupta, K., Boukedes, S.S., Owen, C.A. and Beggs, A.H. (2013) Selenoprotein N deficiency in mice is associated with abnormal lung development. FASEB J., 27, 1585-1599.
5. Lacourciere, G.M. and Stadtman, T.C. (1999) Catalytic properties of selenophosphate synthetases: comparison of the selenocysteine-containing enzyme from Haemophilus influenzae with the corresponding cysteine-containing enzyme from Escherichia coli. Proc. Natl. Acad. Sci. USA, 96, 44-48.
6. Arbogast, S., Beuvin, M., Fraysse, B., Zhou, H., Muntoni, F. and Ferreiro, A. (2009) Oxidative stress in SEPN1-related myopathy:from pathophysiology to treatment. Ann. Neurol., 65, 677-686.
7. Lescure, A., Rederstorff, M., Krol, A., Guicheney, P. and Allamand, V. (2009) Selenoprotein function and muscle disease. Biochim. Biophys. Acta, 1790, 1569-1574.
8. Ashby, M.C. and Tepikin, A.V. (2001) ER calcium and the functions of intracellular organelles. Semin. Cell Dev. Biol., 12, 11-17.
9. Higo, T., Hattori, M., Nakamura, T.,Natsume, T., Michikawa, T. and Mikoshiba, K. (2005) Subtype-specific and ER lumenal environment-dependent regulation of inositol 1,4,5-trisphosphate receptor type 1 by ERp44. Cell, 120, 85-98.
10. Baba-Aissa, F., Raeymaekers, L., Wuytack, F., Dode, L. and Casteels, R. (1998) Distribution and isoform diversity of the organellar Ca2+ pumps in the brain. Mol. Chem. Neuropathol., 33, 199-208.
11. Li, Y. and Camacho, P. (2004) Ca2+-dependent redox modulation of SERCA 2b by ERp57. J. Cell Biol., 164, 35-46.
12. Frand, A.R. and Kaiser, C.A. (1998) The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol. Cell, 1, 161-170.
13. Pollard, M.G., Travers, K.J. and Weissman, J.S. (1998) Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol. Cell, 1, 171-182.
14. Sevier, C.S., Qu, H., Heldman, N., Gross, E., Fass, D. and Kaiser, C.A. (2007) Modulation of cellular disulfide-bond formation and the ER redox environment by feedback regulation of Ero1. Cell, 129, 333-344.
15. Gross, E., Kastner, D.B., Kaiser, C.A. and Fass, D. (2004) Structure of Ero1p, source of disulfide bonds for oxidative protein folding in the cell. Cell, 117, 601-610.
16. Tu, B.P. andWeissman, J.S. (2002) The FAD- andO(2)-dependent reaction cycle of Ero1-mediated oxidative protein folding in the endoplasmic reticulum. Mol. Cell, 10, 983-994.
17. Harding, H.P., Zhang, Y., Zeng, H., Novoa, I., Lu, P.D., Calfon, M., Sadri, N., Yun, C., Popko, B., Paules, R. et al. (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell, 11, 619-633.
18. Powers, S.K., Nelson, W.B. and Hudson, M.B. (2011) Exerciseinduced oxidative stress in humans: cause and consequences. Free Radic. Biol. Med., 51, 942-950.
19. Kim,H.J., Jamart, C., Deldicque, L., An, G.L., Lee, Y.H., Kim, C.K., Raymackers, J.M. and Francaux, M. (2011) Endoplasmic reticulum stressmarkers and ubiquitin-proteasome pathway activity in response to a 200-km run. Med. Sci. Sports Exerc., 43, 18-25.
20. Wu, J., Ruas, J.L., Estall, J.L., Rasbach, K.A., Choi, J.H., Ye, L., Bostrom, P., Tyra, H.M., Crawford, R.W., Campbell, K.P. et al. (2011) The unfolded protein response mediates adaptation to exercise in skeletal muscle through a PGC-1alpha/ATF6alpha complex. Cell Metab., 13, 160-169.
21. Ron, D. and Walter, P. (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol., 8, 519-529.
22. Curran, S.P. and Ruvkun, G. (2007) Lifespan regulation by evolutionarily conserved genes essential for viability. PLoS Genet., 3, e56.
23. Haynes, C.M., Titus, E.A. and Cooper, A.A. (2004) Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death. Mol. Cell, 15, 767-776.
24. Marciniak, S.J., Yun, C.Y., Oyadomari, S., Novoa, I., Zhang, Y., Jungreis, R., Nagata, K., Harding, H.P. and Ron, D. (2004) CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev., 18, 3066-3077.
25. Zito, E., Chin, K.T., Blais, J., Harding, H.P. and Ron, D. (2010) ERO1-beta, a pancreas-specific disulfide oxidase, promotes insulin biogenesis and glucose homeostasis. J. Cell Biol., 188, 821-832.
26. Kettenhofen, N.J. andWood, M.J. (2010) Formation, reactivity, and detection of protein sulfenic acids. Chem. Res. Toxicol., 23, 1633-1646.
27. Seo, Y.H. and Carroll, K.S. (2009) Profiling protein thiol oxidation in tumor cells using sulfenic acid-specific antibodies. Proc. Natl. Acad. Sci. USA, 106, 16163-16168.
28. Zito, E., Melo, E.P., Yang, Y.,Wahlander, A., Neubert, T.A. and Ron, D. (2010) Oxidative protein folding by an endoplasmic reticulum-localized peroxiredoxin. Mol. Cell, 40, 787-797.
29. Lohman, J.R. and Remington, S.J. (2008) Development of a family of redox-sensitive green fluorescent protein indicators for use in relatively oxidizing subcellular environments. Biochemistry, 47, 8678-8688.
30. Cuozzo, J.W. and Kaiser, C.A. (1999) Competition between glutathione and protein thiols for disulphide-bond formation. Nat. Cell Biol., 1, 130-135.
31. Hayes, J.D. and McLellan, L.I. (1999) Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radic. Res., 31, 273-300.
32. Appenzeller-Herzog, C., Riemer, J., Christensen, B., Sorensen, E.S. and Ellgaard, L. (2008) A novel disulphide switch mechanism in Ero1alpha balances ER oxidation in human cells. EMBO J., 27, 2977-2987.
33. Margittai, E., Low, P., Stiller, I., Greco, A., Garcia-Manteiga, J. M., Pengo, N., Benedetti, A., Sitia, R. and Banhegyi, G. (2012) Production of H(2)O(2) in the endoplasmic reticulum promotes in vivo disulfide bond formation. Antioxid. Redox. Signal., 16, 1088-1099.
34. 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.
35. Lu, J. and Holmgren, A. (2009) Selenoproteins. J. Biol. Chem., 284, 723-727.
36. Turanov, A.A., Kehr, S., Marino, S.M., Yoo, M.H., Carlson, B.A., Hatfield, D.L. and Gladyshev, V.N. (2010) Mammalian thioredoxin reductase 1: roles in redox homoeostasis and characterization of cellular targets. Biochem. J., 430, 285-293.
37. Sandow, A. (1952) Excitation-contraction coupling in muscular response. Yale J. Biol. Med., 25, 176-201.
38. Jurynec, M.J., Xia, R., Mackrill, J.J., Gunther, D., Crawford, T., Flanigan, K.M., Abramson, J.J., Howard, M.T. and Grunwald, D.J. (2008) Selenoprotein N is required for ryanodine receptor calcium release channel activity in human and zebrafish muscle. Proc. Natl. Acad. Sci. USA, 105, 12485-12490.
39. Bonora, M., Giorgi, C., Bononi, A., Marchi, S., Patergnani, S., Rimessi, A., Rizzuto, R. and Pinton, P. (2013) Subcellular calcium measurements in mammalian cells using jellyfish photoprotein aequorin-based probes. Nat. Protoc., 8, 2105-2118.
40. Blais, J.D.,Chin, K.T.,Zito, E.,Zhang,Y.,Heldman,N.,Harding,H. P., Fass, D., Thorpe, C. and Ron, D. (2010) A small molecule inhibitor of endoplasmic reticulum oxidation 1 (ERO1)with selectively reversible thiol reactivity. J. Biol. Chem., 285, 20993-21003.
41. Goonasekera, S.A., Lam, C.K., Millay, D.P., Sargent, M.A., Hajjar, R.J., Kranias, E.G. and Molkentin, J.D. (2011) Mitigation of muscular dystrophy in mice by SERCAoverexpression in skeletal muscle. J. Clin. Invest., 121, 1044-1052.
42. Rayavarapu, S., Coley, W. and Nagaraju, K. (2012) Endoplasmic reticulum stress in skeletal muscle homeostasis and disease. Curr. Rheumatol. Rep., 14, 238-243.
43. Tavender, T.J., Springate, J.J. and Bulleid, N.J. (2010) Recycling of peroxiredoxin IV provides a novel pathway for disulphide formation in the endoplasmic reticulum. EMBO J., 29, 4185-4197.
44. Zito, E., Hansen, H.G., Yeo, G.S., Fujii, J. and Ron, D. (2012) Endoplasmic reticulum thiol oxidase deficiency leads to ascorbic acid depletion and noncanonical scurvy in mice. Mol. Cell, 48, 39-51.
45. Ramming, T., Hansen, H.G., Nagata, K., Ellgaard, L. and Appenzeller-Herzog, C. (2014) GPx8 peroxidase prevents leakage of H2O2 from the endoplasmic reticulum. Free Radic. Biol. Med., 70, 106-116.
46. Auricchio, A., Hildinger, M., O'Connor, E., Gao, G.P. and Wilson, J.M. (2001) Isolation of highly infectious and pure adeno-associated virus type 2 vectors with a single-step gravity-flow column. Hum. Gene Ther., 12, 71-76.
47. Colella, P., Trapani, I., Cesi, G., Sommella, A., Manfredi, A., Puppo, A., Iodice, C., Rossi, S., Simonelli, F., Giunti, M. et al. (2014) Efficient gene delivery to the cone-enriched pig retina by dual AAV vectors. Gene Ther., 21, 450-456.
48. Griffith, O.W. (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem., 106, 207-212.
49. Pinton, P., Pozzan, T. and Rizzuto, R. (1998) The Golgi apparatus is an inositol 1,4,5-trisphosphate-sensitive Ca2+ store, with functional properties distinct from those of the endoplasmic reticulum. EMBO J., 17, 5298-5308.
50. Jonassen, T., Marbois, B.N., Faull, K.F., Clarke, C.F. and Larsen, P.L. (2002) Development and fertility in Caenorhabditis elegans clk-1 mutants depend upon transport of dietary coenzyme Q8 to mitochondria. J. Biol. Chem., 277, 45020-45027.