Increased muscle stress-sensitivity induced by selenoprotein N inactivation in mouse: A mammalian model for SEPN1-related myopathy

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Rederstorff, Mathieu ^a,i   Castets, Perrine ^b,c,d,e,j   Arbogast, Sandrine ^b,e,f   Lainé, Jeanne ^b,c,d,e   Vassilopoulos, Stéphane ^b,e,f   Beuvin, Maud ^b,c,d,e   Dubourg, Odile ^b,e,f   Vignaud, Alban ^b,c,d,e   Ferry, Arnaud ^b,c,d,e,g   Krol, Alain ^a   Allamand, Valérie ^b,c,d,e   Guicheney, Pascale ^b,f   Ferreiro, Ana ^b,e,f,h   Lescure, Alain ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c CNRS   (France)

^d Groupe Hospitalier Pitié Salpêtrière   (France)

^e Institut de Myologie   (France)

^f INSERM   (France)

^g UNIVERSITÉ PARIS DESCARTES   (France)

^h PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

ⁱ UNIVERSITÉ DE LORRAINE   (France)

^j UNIVERSITY HOSPITAL BASEL   (Switzerland)

more..

Author keywords

[No Author keywords available]

Indexed keywords

SELENOPROTEIN; SELENOPROTEIN N; UNCLASSIFIED DRUG; MUSCLE PROTEIN; SEPN1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY MOVEMENT; CONTROLLED STUDY; EXERCISE; FORCED SWIMMING TEST; GENE FUNCTION; GENE INACTIVATION; GENE TARGETING; GROWTH; HOMEOSTASIS; IN VIVO STUDY; LIFESPAN; MICROSCOPY; MORPHOLOGY; MOUSE; MUSCLE CONTRACTILITY; MUSCLE FUNCTION; MUSCLE RIGIDITY; MUSCLE STRESS; MYOPATHY; NONHUMAN; PARAVERTEBRAL MSUCLE; PATHOGENESIS; PHENOTYPE; SEPN1 GENE; SPINE DISEASE; SWIMMING; VERTEBRA BODY; 129 MOUSE; ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; CONGENITAL MALFORMATION; DISEASE MODEL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOBLOTTING; MALE; MENTAL STRESS; METABOLISM; MOTOR ACTIVITY; MOUSE MUTANT; MUSCLE CONTRACTION; MUSCLE DISEASE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PRENATAL DEVELOPMENT; PROTEIN CARBONYLATION; PSYCHOLOGICAL ASPECT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; TRANSGENIC MOUSE;

ANIMALIA; MAMMALIA; MUS;

ANIMALS; DISEASE MODELS, ANIMAL; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOBLOTTING; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MOTOR ACTIVITY; MUSCLE CONTRACTION; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR DISEASES; PHENOTYPE; PROTEIN CARBONYLATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SELENOPROTEINS; STRESS, PSYCHOLOGICAL; SWIMMING;

EID: 79961179963     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023094     Document Type: Article

References (47)

1. Rayman MP, (2009) Selenoproteins and human health: insights from epidemiological data. Biochim Biophys Acta 1790: 1533-1540.
2. Hatfield DL, Yoo MH, Carlson BA, Gladyshev VN, (2009) Selenoproteins that function in cancer prevention and promotion. Biochim Biophys Acta 1790: 1541-1545.
3. Allmang C, Wurth L, Krol A, (2009) The selenium to selenoprotein pathway in eukaryotes: more molecular partners than anticipated. Biochim Biophys Acta 1790: 1415-1423.
4. Arner ES, (2010) Selenoproteins-What unique properties can arise with selenocysteine in place of cysteine? Exp Cell Res 316: 1296-1303.
5. Forman HJ, Maiorino M, Ursini F, (2010) Signaling functions of reactive oxygen species. Biochemistry 49: 835-842.
6. Rederstorff M, Krol A, Lescure A, (2006) Understanding the importance of selenium and selenoproteins in muscle function. Cell Mol Life Sci 63: 52-59.
7. Lescure A, Rederstorff M, Krol A, Guicheney P, Allamand V, (2009) Selenoprotein function and muscle disease. Biochim Biophys Acta 1790: 1569-1574.
8. Moghadaszadeh B, Petit N, Jaillard C, Brockington M, Roy SQ, et al. (2001) Mutations in SEPN1 cause congenital muscular dystrophy with spinal rigidity and restrictive respiratory syndrome. Nat Genet 29: 17-18.
9. Ferreiro A, Quijano-Roy S, Pichereau C, Moghadaszadeh B, Goemans N, et al. (2002) Mutations of the selenoprotein N gene, which is implicated in rigid spine muscular dystrophy, cause the classical phenotype of multiminicore disease: reassessing the nosology of early-onset myopathies. Am J Hum Genet 71: 739-749.
10. Ferreiro A, Ceuterick-de Groote C, Marks JJ, Goemans N, Schreiber G, et al. (2004) Desmin-related myopathy with Mallory body-like inclusions is caused by mutations of the selenoprotein N gene. Ann Neurol 55: 676-686.
11. Clarke NF, Kidson W, Quijano-Roy S, Estournet B, Ferreiro A, et al. (2006) SEPN1: associated with congenital fiber-type disproportion and insulin resistance. Ann Neurol 59: 546-552.
12. Arbogast S, Ferreiro A, (2010) Selenoproteins and protection against oxidative stress: selenoprotein N as a novel player at the crossroads of redox signaling and calcium homeostasis. Antioxid Redox Signal 12: 893-904.
13. Allamand V, Richard P, Lescure A, Ledeuil C, Desjardin D, et al. (2006) A single homozygous point mutation in a 3′untranslated region motif of selenoprotein N mRNA causes SEPN1-related myopathy. EMBO Rep 7: 450-454.
14. Cagliani R, Fruguglietti ME, Berardinelli A, D'Angelo MG, Prelle A, et al. (2010) New molecular findings in congenital myopathies due to selenoprotein N gene mutations. J Neurol Sci 300: 107-113.
15. Scoto M, Cirak S, Mein R, Feng L, Manzur AY, et al. (2011) SEPN1-related myopathies: Clinical course in a large cohort of patients. Neurology 76: 2073-2078.
16. Petit N, Lescure A, Rederstorff M, Krol A, Moghadaszadeh B, et al. (2003) Selenoprotein N: an endoplasmic reticulum glycoprotein with an early developmental expression pattern. Hum Mol Genet 12: 1045-1053.
17. Jurynec MJ, Xia R, Mackrill JJ, Gunther D, Crawford T, et al. (2008) Selenoprotein N is required for ryanodine receptor calcium release channel activity in human and zebrafish muscle. Proc Natl Acad Sci U S A 105: 12485-12490.
18. Arbogast S, Beuvin M, Fraysse B, Zhou H, Muntoni F, et al. (2009) Oxidative stress in SEPN1-related myopathy: from pathophysiology to treatment. Ann Neurol 65: 677-686.
19. Lescure A, Gautheret D, Carbon P, Krol A, (1999) Novel selenoproteins identified in silico and in vivo by using a conserved RNA structural motif. J Biol Chem 274: 38147-38154.
20. Castets P, Maugenre S, Gartioux C, Rederstorff M, Krol A, et al. (2009) Selenoprotein N is dynamically expressed during mouse development and detected early in muscle precursors. BMC Dev Biol 9: 46.
21. Thisse C, Degrave A, Kryukov GV, Gladyshev VN, Obrecht-Pflumio S, et al. (2003) Spatial and temporal expression patterns of selenoprotein genes during embryogenesis in zebrafish. Gene Expr Patterns 3: 525-532.
22. Deniziak M, Thisse C, Rederstorff M, Hindelang C, Thisse B, et al. (2007) Loss of selenoprotein N function causes disruption of muscle architecture in the zebrafish embryo. Exp Cell Res 313: 156-167.
23. Bradford DS, Moe JH, Montalvo FJ, Winter RB, (1974) Scheuermann's kyphosis and roundback deformity. Results of Milwaukee brace treatment. J Bone Joint Surg Am 56: 740-758.
24. Vainzof M, Ayub-Guerrieri D, Onofre PC, Martins PC, Lopes VF, et al. (2008) Animal models for genetic neuromuscular diseases. J Mol Neurosci 34: 241-248.
25. Sacco A, Mourkioti F, Tran R, Choi J, Llewellyn M, et al. (2010) Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell 143: 1059-1071.
26. Lucki I, (1997) The forced swimming test as a model for core and component behavioral effects of antidepressant drugs. Behav Pharmacol 8: 523-532.
27. Wang W, Hu X, Zhao Z, Liu P, Hu Y, et al. (2008) Antidepressant-like effects of liquiritin and isoliquiritin from Glycyrrhiza uralensis in the forced swimming test and tail suspension test in mice. Prog Neuropsychopharmacol Biol Psychiatry 32: 1179-1184.
28. Xia X, Cheng G, Pan Y, Xia ZH, Kong LD, (2007) Behavioral, neurochemical and neuroendocrine effects of the ethanolic extract from Curcuma longa L. in the mouse forced swimming test. J Ethnopharmacol 110: 356-363.
29. Schara U, Kress W, Bonnemann CG, Breitbach-Faller N, Korenke CG, et al. (2008) The phenotype and long-term follow-up in 11 patients with juvenile selenoprotein N1-related myopathy. Eur J Paediatr Neurol 12: 224-230.
30. Castets P, Bertrand AT, Beuvin M, Ferry A, Le Grand F, et al. (2010) Satellite cell loss and impaired muscle regeneration in selenoprotein N deficiency. Hum Mol Genet.
31. Powers SK, Kavazis AN, DeRuisseau KC, (2005) Mechanisms of disuse muscle atrophy: role of oxidative stress. Am J Physiol Regul Integr Comp Physiol 288: R337-344.
32. Powers SK, Kavazis AN, McClung JM, (2007) Oxidative stress and disuse muscle atrophy. J Appl Physiol 102: 2389-2397.
33. Barker T, Traber MG, (2007) From animals to humans: evidence linking oxidative stress as a causative factor in muscle atrophy. J Physiol 583: 421-422.
34. Moylan JS, Reid MB, (2007) Oxidative stress, chronic disease, and muscle wasting. Muscle Nerve 35: 411-429.
35. Serrano AL, Murgia M, Pallafacchina G, Calabria E, Coniglio P, et al. (2001) Calcineurin controls nerve activity-dependent specification of slow skeletal muscle fibers but not muscle growth. Proc Natl Acad Sci U S A 98: 13108-13113.
36. Michel RN, Chin ER, Chakkalakal JV, Eibl JK, Jasmin BJ, (2007) Ca2+/calmodulin-based signalling in the regulation of the muscle fibre phenotype and its therapeutic potential via modulation of utrophin A and myostatin expression. Appl Physiol Nutr Metab 32: 921-929.
37. Chevessier F, Bauche-Godard S, Leroy JP, Koenig J, Paturneau-Jouas M, et al. (2005) The origin of tubular aggregates in human myopathies. J Pathol 207: 313-323.
38. Boncompagni S, Loy RE, Dirksen RT, Franzini-Armstrong C, (2010) The I4895T mutation in the type 1 ryanodine receptor induces fiber-type specific alterations in skeletal muscle that mimic premature aging. Aging Cell 9: 958-970.
39. Maclennan DH, Zvaritch E, (2010) Mechanistic models for muscle diseases and disorders originating in the sarcoplasmic reticulum. Biochim Biophys Acta.
40. Steinbrenner H, Sies H, (2009) Protection against reactive oxygen species by selenoproteins. Biochim Biophys Acta 1790: 1478-1485.
41. Lee BC, Dikiy A, Kim HY, Gladyshev VN, (2009) Functions and evolution of selenoprotein methionine sulfoxide reductases. Biochim Biophys Acta 1790: 1471-1477.
42. Rudert CP, Lawrence JA, Foggin C, Barlow RM, (1978) A rigid lamb syndrome in sheep in Rhodesia. Vet Rec 102: 374-377.
43. Cosgrove D, Gray D, Dierich A, Kaufman J, Lemeur M, et al. (1991) Mice lacking MHC class II molecules. Cell 66: 1051-1066.
44. Porsolt RD, Bertin A, Jalfre M, (1977) Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229: 327-336.
45. Vassilopoulos S, Thevenon D, Rezgui SS, Brocard J, Chapel A, et al. (2005) Triadins are not triad-specific proteins: two new skeletal muscle triadins possibly involved in the architecture of sarcoplasmic reticulum. J Biol Chem 280: 28601-28609.
46. Vignaud A, Hourde C, Torres S, Caruelle JP, Martelly I, et al. (2005) Functional, cellular and molecular aspects of skeletal muscle recovery after injury induced by snake venom from Notechis scutatus scutatus. Toxicon 45: 789-801.
47. Taille C, Foresti R, Lanone S, Zedda C, Green C, et al. (2001) Protective role of heme oxygenases against endotoxin-induced diaphragmatic dysfunction in rats. Am J Respir Crit Care Med 163: 753-761.