Alternative splicing of human insulin receptor gene (INSR) in type i and type II skeletal muscle fibers of patients with myotonic dystrophy type 1 and type 2

Molecular and Cellular Biochemistry

Volumn 380, Issue 1-2, 2013, Pages 259-265

  Santoro, Massimo ^a   Masciullo, Marcella ^c   Bonvissuto, Davide ^b   Bianchi, Maria Laura Ester ^b   Michetti, Fabrizio ^b   Silvestri, Gabriella ^b  

^a IRCCS FONDAZIONE DON CARLO GNOCCHI   (Italy)

^b CATHOLIC UNIVERSITY   (Italy)

^c IRCCS SAN RAFFAELE PISANA   (Italy)

Author keywords

Insulin receptor; Laser capture micro dissection (LCM); Myotonic dystrophy; Type I muscle fiber; Type II muscle fiber

Indexed keywords

INSULIN RECEPTOR;

ADULT; ALTERNATIVE RNA SPLICING; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN TISSUE; INSULIN RESISTANCE; LASER CAPTURE MICRODISSECTION; MUSCLE TISSUE; MYOTONIC DYSTROPHY; PATHOGENESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE;

ADENOSINE TRIPHOSPHATASES; ADULT; ALTERNATIVE SPLICING; ANTIGENS, CD; BIOPSY; GENE EXPRESSION; HISTOCYTOCHEMISTRY; HUMANS; HYDROGEN-ION CONCENTRATION; LASER CAPTURE MICRODISSECTION; MIDDLE AGED; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; MUSCLE, SKELETAL; MYOTONIC DISORDERS; MYOTONIC DYSTROPHY; PROTEIN ISOFORMS; RECEPTOR, INSULIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84879772009     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-013-1681-z     Document Type: Article

References (38)

1. Harper PS (2001) Myotonic dystrophy, 3rd edn. Saunders, London
2. Day JW, Ricker K, Jacobsen JF, Rasmussen LJ, Dick KA, Kress W, Schneider C, Koch MC, Beilman GJ, Harrison AR, Dalton JC, Ranum LP (2003) Myotonic dystrophy type 2: molecular, diagnostic and clinical spectrum. Neurology 60:657-664
3. Brook JD, McCurrach ME, Harley HG, Buckler AJ, Church D, Aburatani H, Hunter K, Stanton VP, Thirion JP, Hudson T, Sohna R, Zemelmana B, Snellb RG, Rundleb SA, Crowb S, Daviesb J, Shelbourneb P, Buxtonb J, Jonesb C, Juvonenb V, Johnsonb K, Harperb PS, Shawb J, Housmana DE (1992) Molecular basis of myotonic dystrophy: expansion of a trinucleotide (CTG) repeat at the 3′ end of a transcript encoding a protein kinase family member. Cell 68:799-808 Erratum in: Cell 69 385
4. Mahadevan M, Tsilfidis C, Sabourin L, Shutler G, Amemiya C, Jansen G, Neville C, Narang M, Barceló J, O'Hoy K, Leblond S, Earle-Macdonald J, de Jong P, Wieringa B, Korneluk RG (1992) Myotonic dystrophy mutation: an unstable CTG repeat in the 3′ untranslated region of the gene. Science 255:1253-1255
5. Liquori CL, Ricker K, Moseley ML, Jacobsen JF, Kress W, Naylor SL, Day JW, Ranum LP (2001) Myotonic dystrophy type 2 caused by a CCTG expansion in intron 1 of ZNF9. Science 293:864-867
6. Udd B, Krahe R (2012) The myotonic dystrophies: molecular, clinical, and therapeutic challenges. Lancet Neurol 11:891-905
7. Taneja KL, McCurrach M, Schalling M, Housman D, Singer RH (1995) Foci of trinucleotide repeat transcripts in nuclei of myotonic dystrophy cells and tissues. J Cell Biol 128:995-1002
8. Davis BM, McCurrach ME, Taneja KL, Singer RH, Housman DE (1997) Expansion of CUG trinucleotide repeat in the 3′ untranslated region of myotonic dystrophy protein kinase transcripts results in nuclear retention of transcripts. Proc Natl Acad Sci USA 94:7388-7393
9. Mankodi A, Teng-Umnuay P, Krym M, Henderson D, Swanson M, Thornton CA (2003) Ribonuclear inclusions in skeletal muscle in myotonic dystrophy types 1 and 2. Ann Neurol 54:760-768
10. Cho DH, Tapscott SJ (2007) Myotonic dystrophy: emerging mechanisms for DM1 and DM2. Biochim Biophys Acta 1772:195-204
11. Philips AV, Timchenko LT, Cooper TA (1998) Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy. Science 280:737-741
12. Savkur RS, Philips AV, Cooper TA (2001) Aberrant regulation of insulin receptor alternative splicing is associated with insulin resistance in myotonic dystrophy. Nat Genet 29:40-47
13. Savkur RS, Philips AV, Cooper TA, Dalton JC, Moseley ML, Ranum LP, Day JW (2004) Insulin receptor splicing alteration in myotonic dystrophy type 2. Am J Hum Genet 74:1309-1313
14. Kanadia RN, Johnstone KA, Mankodi A, Lungu C, Thornton CA, Esson D, Timmers AM, Hauswirth WW, Swanson MS (2003) A muscleblind knockout model for myotonic dystrophy. Science 302:1978-1980
15. Mankodi A, Takahashi MP, Jiang H, Beck CL, Bowers WJ, Moxley RT, Cannon SC, Thornton CA (2002) Expanded CUG repeats trigger aberrant splicing of ClC-1 chloride channel pre-mRNA and hyperexcitability of skeletal muscle in myotonic dystrophy. Mol Cell 10:35-44
16. Charlet-B N, Savkur RS, Singh G, Philips AV, Grice EA, Cooper TA (2002) Loss of the muscle-specific chloride channel in type 1 myotonic dystrophy due to misregulated alternative splicing. Mol Cell 10:45-53
17. Vihola A, Bassez G, Meola G, Zhang S, Haapasalo H, Paetau A, Mancinelli E, Rouche A, Hogrel JY, Laforêt P, Maisonobe T, Pellissier JF, Krahe R, Eymard B, Udd B (2003) Histopathological differences of myotonic dystrophy type 1 (DM1) and PROMM/DM2. Neurology 60:1854-1857
18. Pisani V, Panico MB, Terracciano C, Bonifazi E, Meola G, Novelli G, Bernardi G, Angelini C, Massa R (2008) Preferential central nucleation of type 2 myofibers is an invariable feature of myotonic dystrophy type 2. Muscle Nerve 38:1405-1411
19. Furling D, Coiffier L, Mouly V, Barbet JP, St Guily JL, Taneja K, Gourdon G, Junien C, Butler-Browne GS (2001) Defective satellite cells in congenital myotonic dystrophy. Hum Mol Genet 10:2079-2087
20. Buj-Bello A, Furling D, Tronchère H, Laporte J, Lerouge T, Butler-Browne GS, Mandel JL (2002) Muscle-specific alternative splicing of myotubularin-related 1 gene is impaired in DM1 muscle cells. Hum Mol Genet 11:2297-2307
21. Loro E, Rinaldi F, Malena A, Masiero E, Novelli G, Angelini C, Romeo V, Sandri M, Botta A, Vergani L (2010) Normal myogenesis and increased apoptosis in myotonic dystrophy type-1 muscle cells. Cell Death Differ 17:1315-1324
22. Kimura T, Nakamori M, Lueck JD, Pouliquin P, Aoike F, Fujimura H, Dirksen RT, Takahashi MP, Dulhunty AF, Sakoda S (2005) Altered mRNA splicing of the skeletal muscle ryanodine receptor and sarcoplasmic/endoplasmic reticulum Ca2+ -ATPase in myotonic dystrophy type 1. Hum Mol Genet 14:2189-2200
23. Santoro M, Modoni A, Masciullo M, Gidaro T, Broccolini A, Ricci E, Tonali PA, Silvestri G (2010) Analysis of MTMR1 expression and correlation with muscle pathological features in juvenile/adult onset myotonic dystrophy type 1 (DM1) and in myotonic dystrophy type 2 (DM2). Exp Mol Pathol 89:158-168
24. Morrone A, Pegoraro E, Angelini C, Zammarchi E, Marconi G, Hoffman EP (1997) RNA metabolism in myotonic dystrophy: patient muscle shows decreased insulin receptor RNA and protein consistent with abnormal insulin resistance. J Clin Invest 99:1691-1698
25. Vihola A, Bachinski LL, Sirito M, Olufemi SE, Hajibashi S, Baggerly KA, Raheem O, Haapasalo H, Suominen T, Holmlund-Hampf J, Paetau A, Cardani R, Meola G, Kalimo H, Edström L, Krahe R, Udd B (2010) Differences in aberrant expression and splicing of sarcomeric proteins in the myotonic dystrophies DM1 and DM2. Acta Neuropathol 119:465-479
26. Greco S, Perfetti A, Fasanaro P, Cardani R, Capogrossi MC, Meola G, Martelli F (2012) Deregulated microRNAs in myotonic dystrophy type 2. PLoS ONE 7:e39732
27. Gambardella S, Rinaldi F, Lepore SM, Viola A, Loro E, Angelini C, Vergani L, Novelli G, Botta A (2010) Overexpression of microRNA-206 in the skeletal muscle from myotonic dystrophy type 1 patients. J Transl Med 20(8):48
28. Belfiore A, Frasca F, Pandini G, Sciacca L, Vigneri R (2009) Insulin receptor isoforms and insulin receptor/insulin-like growth factor receptor hybrids in physiology and disease. Endocr Rev 30:586-623
29. Seino S, Bell GI (1989) Alternative splicing of human insulin receptor messenger RNA. Biochem Biophys Res Commun 159:312-316
30. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3:1014-1019
31. Sandri M (2008) Signaling in muscle atrophy and hypertrophy. Physiology (Bethesda) 23:160-170
32. Fend F, Emmert-Buck MR, Chuaqui R, Cole K, Lee J, Liotta LA, Raffeld M (1999) Immuno-LCM: laser capture micro dissection of immunostained frozen sections for mRNA analysis. Am J Pathol 154:61-66
33. Wang S, Wang L, Zhu T, Gao X, Li J, Wu Y, Zhu H (2010) Improvement of tissue preparation for laser capture microdissection: application for cell type-specific miRNA expression profiling in colorectal tumors. BMC Genomics 11:163
34. Keays KM, Owens GP, Ritchie AM, Gilden DH, Burgoon MP (2005) Laser capture micro dissection and single-cell RT-PCR without RNA purification. J Immunol Methods 302:90-98
35. Wacker MJ, Tehel MM, Gallagher PM (2008) Technique for quantitative RT-PCR analysis directly from single muscle fibers. J Appl Physiol 105:308-315
36. Dubowitz V (1985) A pratical approach. In: Bailiere Tindall (ed) Muscle biopsy, 2nd edn. Bailliere Tindall, London, pp 45-53
37. Greenberg SA, Salajegheh M, Judge DP, Feldman MW, Kuncl RW, Waldon Z, Steen H, Wagner KR (2012) Etiology of limb girdle muscular dystrophy 1D/1E determined by laser capture microdissection proteomics. Ann Neurol 71:141-145
38. Orengo JP, Ward AJ, Cooper TA (2011) Alternative splicing dysregulation secondary to skeletal muscle regeneration. Ann Neurol 69:681-690