Rbfox1 Downregulation and Altered Calpain 3 Splicing by FRG1 in a Mouse Model of Facioscapulohumeral Muscular Dystrophy (FSHD)

PLoS Genetics

Volumn 9, Issue 1, 2013, Pages

  Pistoni, Mariaelena ^a   Shiue, Lily ^b   Cline, Melissa S ^b   Bortolanza, Sergia ^a   Neguembor, Maria Victoria ^a,c   Xynos, Alexandros ^a   Ares, Manuel ^b   Gabellini, Davide ^a  

^a DULBECCO TELETHON INSTITUTE   (Italy)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN 3; MESSENGER RNA;

ALTERNATIVE RNA SPLICING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BICEPS BRACHII MUSCLE; BINDING SITE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; EXON; FACIOSCAPULOHUMERAL MUSCULAR DYSTROPHY; FRG1 GENE; GENE; GENE OVEREXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MOUSE; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHENOTYPE; RBFOX1 GENE; RNA STABILITY; UPREGULATION; VASTUS LATERALIS MUSCLE;

EID: 84873515320     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003186     Document Type: Article

References (84)

1. Cabianca DS, Gabellini D, (2010) The cell biology of disease: FSHD: copy number variations on the theme of muscular dystrophy. J Cell Biol 191: 1049-1060.
2. Flanigan KM, Coffeen CM, Sexton L, Stauffer D, Brunner S, et al. (2001) Genetic characterization of a large, historically significant Utah kindred with facioscapulohumeral dystrophy. Neuromuscul Disord 11: 525-529.
3. Pandya S, King WM, Tawil R, (2008) Facioscapulohumeral dystrophy. Phys Ther 88: 105-113.
4. Shahrizaila N, Wills AJ, (2005) Significance of Beevor's sign in facioscapulohumeral dystrophy and other neuromuscular diseases. J Neurol Neurosurg Psychiatry 76: 869-870.
5. Barro M, Carnac G, Flavier S, Mercier J, Vassetzky Y, et al. (2008) Myoblasts from affected and non-affected FSHD muscles exhibit morphological differentiation defects. J Cell Mol Med 14: 275-289.
6. Celegato B, Capitanio D, Pescatori M, Romualdi C, Pacchioni B, et al. (2006) Parallel protein and transcript profiles of FSHD patient muscles correlate to the D4Z4 arrangement and reveal a common impairment of slow to fast fibre differentiation and a general deregulation of MyoD-dependent genes. Proteomics 6: 5303-5321.
7. Morosetti R, Mirabella M, Gliubizzi C, Broccolini A, Sancricca C, et al. (2007) Isolation and characterization of mesoangioblasts from facioscapulohumeral muscular dystrophy muscle biopsies. Stem Cells 25: 3173-3182.
8. Stadler G, Chen JC, Wagner K, Robin JD, Shay JW, et al. (2011) Establishment of clonal myogenic cell lines from severely affected dystrophic muscles- CDK4 maintains the myogenic population. Skelet Muscle 1: 12.
9. Tupler R, Perini G, Pellegrino MA, Green MR, (1999) Profound misregulation of muscle-specific gene expression in facioscapulohumeral muscular dystrophy. Proc Natl Acad Sci U S A 96: 12650-12654.
10. Winokur ST, Barrett K, Martin JH, Forrester JR, Simon M, et al. (2003) Facioscapulohumeral muscular dystrophy (FSHD) myoblasts demonstrate increased susceptibility to oxidative stress. Neuromuscul Disord 13: 322-333.
11. Winokur ST, Chen YW, Masny PS, Martin JH, Ehmsen JT, et al. (2003) Expression profiling of FSHD muscle supports a defect in specific stages of myogenic differentiation. Hum Mol Genet 12: 2895-2907.
12. Brouwer OF, Padberg GW, Bakker E, Wijmenga C, Frants RR, (1995) Early onset facioscapulohumeral muscular dystrophy. Muscle Nerve 2: S67-72.
13. Funakoshi M, Goto K, Arahata K, (1998) Epilepsy and mental retardation in a subset of early onset 4q35-facioscapulohumeral muscular dystrophy. Neurology 50: 1791-1794.
14. Miura K, Kumagai T, Matsumoto A, Iriyama E, Watanabe K, et al. (1998) Two cases of chromosome 4q35-linked early onset facioscapulohumeral muscular dystrophy with mental retardation and epilepsy. Neuropediatrics 29: 239-241.
15. Saito Y, Miyashita S, Yokoyama A, Komaki H, Seki A, et al. (2007) Facioscapulohumeral muscular dystrophy with severe mental retardation and epilepsy. Brain Dev 29: 231-233.
16. Neguembor M, Gabellini D, (2010) In Junk We Trust: Repetitive DNA, Epigenetics and Facioscapulohumeral Muscular Dystrophy. Epigenomics 2: 271-287.
17. Hewitt JE, Lyle R, Clark LN, Valleley EM, Wright TJ, et al. (1994) Analysis of the tandem repeat locus D4Z4 associated with facioscapulohumeral muscular dystrophy. Hum Mol Genet 3: 1287-1295.
18. van Deutekom JC, Wijmenga C, van Tienhoven EA, Gruter AM, Hewitt JE, et al. (1993) FSHD associated DNA rearrangements are due to deletions of integral copies of a 3.2 kb tandemly repeated unit. Hum Mol Genet 2: 2037-2042.
19. Wijmenga C, Hewitt JE, Sandkuijl LA, Clark LN, Wright TJ, et al. (1992) Chromosome 4q DNA rearrangements associated with facioscapulohumeral muscular dystrophy. Nat Genet 2: 26-30.
20. Winokur ST, Bengtsson U, Feddersen J, Mathews KD, Weiffenbach B, et al. (1994) The DNA rearrangement associated with facioscapulohumeral muscular dystrophy involves a heterochromatin-associated repetitive element: implications for a role of chromatin structure in the pathogenesis of the disease. Chromosome Res 2: 225-234.
21. Cabianca DS, Casa V, Bodega B, Xynos A, Ginelli E, et al. (2012) A long ncRNA links copy number variation to a polycomb/trithorax epigenetic switch in FSHD muscular dystrophy. Cell 149: 819-831.
22. Gabellini D, Green MR, Tupler R, (2002) Inappropriate gene activation in FSHD: a repressor complex binds a chromosomal repeat deleted in dystrophic muscle. Cell 110: 339-348.
23. Lemmers RJ, van der Vliet PJ, Klooster R, Sacconi S, Camano P, et al. (2010) A unifying genetic model for facioscapulohumeral muscular dystrophy. Science 329: 1650-1653.
24. Hanel ML, Wuebbles RD, Jones PL, (2009) Muscular dystrophy candidate gene FRG1 is critical for muscle development. Dev Dyn 238: 1502-1512.
25. Gabellini D, D'Antona G, Moggio M, Prelle A, Zecca C, et al. (2006) Facioscapulohumeral muscular dystrophy in mice overexpressing FRG1. Nature 439: 973-977.
26. Liu Q, Jones TI, Tang VW, Brieher WM, Jones PL, (2010) Facioscapulohumeral muscular dystrophy region gene-1 (FRG-1) is an actin-bundling protein associated with muscle-attachment sites. J Cell Sci 123: 1116-1123.
27. Wuebbles RD, Hanel ML, Jones PL, (2009) FSHD region gene 1 (FRG1) is crucial for angiogenesis linking FRG1 to facioscapulohumeral muscular dystrophy-associated vasculopathy. Dis Model Mech 2: 267-274.
28. Bessonov S, Anokhina M, Krasauskas A, Golas MM, Sander B, et al. (2010) Characterization of purified human Bact spliceosomal complexes reveals compositional and morphological changes during spliceosome activation and first step catalysis. Rna 16: 2384-2403.
29. Davidovic L, Sacconi S, Bechara EG, Delplace S, Allegra M, et al. (2008) Alteration of expression of muscle specific isoforms of the fragile X related protein 1 (FXR1P) in facioscapulohumeral muscular dystrophy patients. J Med Genet 45: 679-685.
30. Jurica MS, Licklider LJ, Gygi SR, Grigorieff N, Moore MJ, (2002) Purification and characterization of native spliceosomes suitable for three-dimensional structural analysis. Rna 8: 426-439.
31. Kim SK, Lund J, Kiraly M, Duke K, Jiang M, et al. (2001) A gene expression map for Caenorhabditis elegans. Science 293: 2087-2092.
32. Makarov EM, Makarova OV, Urlaub H, Gentzel M, Will CL, et al. (2002) Small nuclear ribonucleoprotein remodeling during catalytic activation of the spliceosome. Science 298: 2205-2208.
33. Rappsilber J, Ryder U, Lamond AI, Mann M, (2002) Large-scale proteomic analysis of the human spliceosome. Genome Res 12: 1231-1245.
34. van Koningsbruggen S, Dirks RW, Mommaas AM, Onderwater JJ, Deidda G, et al. (2004) FRG1P is localised in the nucleolus, Cajal bodies, and speckles. J Med Genet 41: e46.
35. Kuroyanagi H, (2009) Fox-1 family of RNA-binding proteins. Cell Mol Life Sci 66: 3895-3907.
36. Damianov A, Black DL, (2009) Autoregulation of Fox protein expression to produce dominant negative splicing factors. Rna 16: 405-416.
37. McKee AE, Minet E, Stern C, Riahi S, Stiles CD, et al. (2005) A genome-wide in situ hybridization map of RNA-binding proteins reveals anatomically restricted expression in the developing mouse brain. BMC Dev Biol 5: 14.
38. Tang ZZ, Zheng S, Nikolic J, Black DL, (2009) Developmental control of CaV1.2 L-type calcium channel splicing by Fox proteins. Mol Cell Biol 29: 4757-4765.
39. Baraniak AP, Chen JR, Garcia-Blanco MA, (2006) Fox-2 mediates epithelial cell-specific fibroblast growth factor receptor 2 exon choice. Mol Cell Biol 26: 1209-1222.
40. Ponthier JL, Schluepen C, Chen W, Lersch RA, Gee SL, et al. (2006) Fox-2 splicing factor binds to a conserved intron motif to promote inclusion of protein 4.1R alternative exon 16. J Biol Chem 281: 12468-12474.
41. Underwood JG, Boutz PL, Dougherty JD, Stoilov P, Black DL, (2005) Homologues of the Caenorhabditis elegans Fox-1 protein are neuronal splicing regulators in mammals. Mol Cell Biol 25: 10005-10016.
42. Yeo GW, Coufal NG, Liang TY, Peng GE, Fu XD, et al. (2009) An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells. Nat Struct Mol Biol 16: 130-137.
43. Kim KK, Adelstein RS, Kawamoto S, (2009) Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. J Biol Chem 284: 31052-31061.
44. Ni JZ, Grate L, Donohue JP, Preston C, Nobida N, et al. (2007) Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay. Genes Dev 21: 708-718.
45. Sugnet CW, Srinivasan K, Clark TA, O'Brien G, Cline MS, et al. (2006) Unusual intron conservation near tissue-regulated exons found by splicing microarrays. PLoS Comput Biol 2: e4 doi:10.1371/journal.pcbi.0020004.
46. Walsh FS, Celeste AJ, (2005) Myostatin: a modulator of skeletal-muscle stem cells. Biochem Soc Trans 33: 1513-1517.
47. Berkes CA, Tapscott SJ, (2005) MyoD and the transcriptional control of myogenesis. Semin Cell Dev Biol 16: 585-595.
48. Finanger Hedderick EL, Simmers JL, Soleimani A, Andres-Mateos E, Marx R, et al. (2011) Loss of sarcolemmal nNOS is common in acquired and inherited neuromuscular disorders. Neurology 76: 960-967.
49. Richard I, Broux O, Allamand V, Fougerousse F, Chiannilkulchai N, et al. (1995) Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell 81: 27-40.
50. Sorimachi H, Imajoh-Ohmi S, Emori Y, Kawasaki H, Ohno S, et al. (1989) Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m- and mu-types. Specific expression of the mRNA in skeletal muscle. J Biol Chem 264: 20106-20111.
51. Bulfield G, Siller WG, Wight PA, Moore KJ, (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci U S A 81: 1189-1192.
52. Sun CY, van Koningsbruggen S, Long SW, Straasheijm K, Klooster R, et al. (2011) Facioscapulohumeral muscular dystrophy region gene 1 is a dynamic RNA-associated and actin-bundling protein. J Mol Biol 411: 397-416.
53. Yamashita R, Sathira NP, Kanai A, Tanimoto K, Arauchi T, et al. (2011) Genome-wide characterization of transcriptional start sites in humans by integrative transcriptome analysis. Genome Res 21: 775-789.
54. Spencer MJ, Guyon JR, Sorimachi H, Potts A, Richard I, et al. (2002) Stable expression of calpain 3 from a muscle transgene in vivo: immature muscle in transgenic mice suggests a role for calpain 3 in muscle maturation. Proc Natl Acad Sci U S A 99: 8874-8879.
55. Snider L, Asawachaicharn A, Tyler AE, Geng LN, Petek LM, et al. (2009) RNA transcripts, miRNA-sized fragments and proteins produced from D4Z4 units: new candidates for the pathophysiology of facioscapulohumeral dystrophy. Hum Mol Genet 18: 2414-2430.
56. Snider L, Geng LN, Lemmers RJ, Kyba M, Ware CB, et al. (2010) Facioscapulohumeral dystrophy: incomplete suppression of a retrotransposed gene. PLoS Genet 6: e1001181 doi:10.1371/journal.pgen.1001181.
57. Wallace LM, Garwick SE, Mei W, Belayew A, Coppee F, et al. (2011) DUX4, a candidate gene for facioscapulohumeral muscular dystrophy, causes p53-dependent myopathy in vivo. Ann Neurol 69: 540-552.
58. Bosnakovski D, Xu Z, Gang EJ, Galindo CL, Liu M, et al. (2008) An isogenetic myoblast expression screen identifies DUX4-mediated FSHD-associated molecular pathologies. EMBO J 27: 2766-2779.
59. Arahata K, Ishihara T, Fukunaga H, Orimo S, Lee JH, et al. (1995) Inflammatory response in facioscapulohumeral muscular dystrophy (FSHD): immunocytochemical and genetic analyses. Muscle Nerve 2: S56-66.
60. Figarella-Branger D, Pellissier JF, Serratrice G, Pouget J, Bianco N, (1989) [Immunocytochemical study of the inflammatory forms of facioscapulohumeral myopathies and correlation with other types of myositis]. Ann Pathol 9: 100-108.
61. Frisullo G, Frusciante R, Nociti V, Tasca G, Renna R, et al. (2011) CD8(+) T cells in facioscapulohumeral muscular dystrophy patients with inflammatory features at muscle MRI. J Clin Immunol 31: 155-166.
62. Munsat TL, Piper D, Cancilla P, Mednick J, (1972) Inflammatory myopathy with facioscapulohumeral distribution. Neurology 22: 335-347.
63. Geng LN, Yao Z, Snider L, Fong AP, Cech JN, et al. (2012) DUX4 activates germline genes, retroelements, and immune mediators: implications for facioscapulohumeral dystrophy. Dev Cell 22: 38-51.
64. Bhalla K, Phillips HA, Crawford J, McKenzie OL, Mulley JC, et al. (2004) The de novo chromosome 16 translocations of two patients with abnormal phenotypes (mental retardation and epilepsy) disrupt the A2BP1 gene. J Hum Genet 49: 308-311.
65. Davis LK, Maltman N, Mosconi MW, Macmillan C, Schmitt L, et al. (2012) Rare inherited A2BP1 deletion in a proband with autism and developmental hemiparesis. Am J Med Genet A 158A: 1654-1661.
66. Fogel BL, Wexler E, Wahnich A, Friedrich T, Vijayendran C, et al. (2012) RBFOX1 regulates both splicing and transcriptional networks in human neuronal development. Hum Mol Genet 21: 4171-4186.
67. Gallant NM, Baldwin E, Salamon N, Dipple KM, Quintero-Rivera F, (2011) Pontocerebellar hypoplasia in association with de novo 19p13.11p13.12 microdeletion. Am J Med Genet A 155A: 2871-2878.
68. Gehman LT, Stoilov P, Maguire J, Damianov A, Lin CH, et al. (2011) The splicing regulator Rbfox1 (A2BP1) controls neuronal excitation in the mammalian brain. Nat Genet 43: 706-711.
69. Kaynak B, von Heydebreck A, Mebus S, Seelow D, Hennig S, et al. (2003) Genome-wide array analysis of normal and malformed human hearts. Circulation 107: 2467-2474.
70. Martin CL, Duvall JA, Ilkin Y, Simon JS, Arreaza MG, et al. (2007) Cytogenetic and molecular characterization of A2BP1/FOX1 as a candidate gene for autism. Am J Med Genet B Neuropsychiatr Genet 144B: 869-876.
71. Mikhail FM, Lose EJ, Robin NH, Descartes MD, Rutledge KD, et al. (2011) Clinically relevant single gene or intragenic deletions encompassing critical neurodevelopmental genes in patients with developmental delay, mental retardation, and/or autism spectrum disorders. Am J Med Genet A 155A: 2386-2396.
72. Sebat J, Lakshmi B, Malhotra D, Troge J, Lese-Martin C, et al. (2007) Strong association of de novo copy number mutations with autism. Science 316: 445-449.
73. Voineagu I, Wang X, Johnston P, Lowe JK, Tian Y, et al. (2011) Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature.
74. Bushby KM, (1999) Making sense of the limb-girdle muscular dystrophies. Brain 122 (Pt 8) (): 1403-1420.
75. van der Kooi AJ, de Visser M, Barth PG, (1994) Limb girdle muscular dystrophy: reappraisal of a rejected entity. Clin Neurol Neurosurg 96: 209-218.
76. Beckmann JS, Spencer M, (2008) Calpain 3, the "gatekeeper" of proper sarcomere assembly, turnover and maintenance. Neuromuscul Disord 18: 913-921.
77. Fougerousse F, Bullen P, Herasse M, Lindsay S, Richard I, et al. (2000) Human-mouse differences in the embryonic expression patterns of developmental control genes and disease genes. Hum Mol Genet 9: 165-173.
78. Tusher VG, Tibshirani R, Chu G, (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116-5121.
79. Eisen MB, Spellman PT, Brown PO, Botstein D, (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863-14868.
80. Saldanha AJ, (2004) Java Treeview-extensible visualization of microarray data. Bioinformatics 20: 3246-3248.
81. Amendola M, Venneri MA, Biffi A, Vigna E, Naldini L, (2005) Coordinate dual-gene transgenesis by lentiviral vectors carrying synthetic bidirectional promoters. Nat Biotechnol 23: 108-116.
82. Nakahata S, Kawamoto S, (2005) Tissue-dependent isoforms of mammalian Fox-1 homologs are associated with tissue-specific splicing activities. Nucleic Acids Res 33: 2078-2089.
83. Lee JA, Tang ZZ, Black DL, (2009) An inducible change in Fox-1/A2BP1 splicing modulates the alternative splicing of downstream neuronal target exons. Genes Dev 23: 2284-2293.
84. Kalsotra A, Wang K, Li PF, Cooper TA, (2010) MicroRNAs coordinate an alternative splicing network during mouse postnatal heart development. Genes Dev 24: 653-658.