Expanded CTG repeats trigger miRNA alterations in Drosophila that are conserved in myotonic dystrophy type 1 patients

Human Molecular Genetics

Volumn 22, Issue 4, 2013, Pages 704-716

  Fernandez Costa, Juan M ^a,j   Garcia Lopez, Amparo ^a   Zuñiga, Sheila ^b   Fernandez Pedrosa, Victoria ^b   Felipo Benavent, Amelia ^a   Mata, Manuel ^c   Jaka, Oihane ^d,h   Aiastui, Ana ^d,h   Hernandez Torres, Francisco ^f,k   Aguado, Begoña ^f   Perez Alonso, Manuel ^a   Vilchez, Jesus J ^a,g,h   Lopez de Munain, Adolfo ^d,e,h,i   Artero, Ruben D ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b Sistemas Genomicos Ltd   (Spain)

^c HOSPITAL GENERAL UNIVERSITARIO DE VALENCIA   (Spain)

^d BIODONOSTIA HEALTH RESEARCH INSTITUTE   (Spain)

^e HOSPITAL DONOSTIA   (Spain)

^f CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^g HOSPITAL UNIVERSITARIO LA FE   (Spain)

^h CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

ⁱ UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^j Technology Park of Valencia   (Spain)

^k UNIVERSITY OF JAÉN   (Spain)

more..

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 1; MICRORNA 10; MICRORNA 7; TRANSCRIPTOME; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA; FEMALE; HUMAN; HUMAN TISSUE; MALE; MOLECULAR MECHANICS; MUSCLE BIOPSY; MUTATION; MYOTONIC DYSTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; UPREGULATION;

ANIMALS; BASE SEQUENCE; CELLS, CULTURED; DOWN-REGULATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMANS; LIFE EXPECTANCY; MALE; MICRORNAS; MUSCLE, SKELETAL; MYOTONIC DYSTROPHY; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TRANSCRIPTOME; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 84873043215     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds478     Document Type: Article

References (45)

1. Sicot, G., Gourdon, G. and Gomes-Pereira, M. (2011) Myotonic dystrophy, when simple repeats reveal complex pathogenic entities: new findings and future challenges. Hum. Mol. Genet., 20, R116-R123.
2. Garcia-Lopez, A., Monferrer, L., Garcia-Alcover, I., Vicente-Crespo, M., Alvarez-Abril, M.C. and Artero, R.D. (2008) Genetic and chemical modifiers of a CUG toxicity model in Drosophila. PLoS One, 3, e1595.
3. Mankodi, A., Logigian, E., Callahan, L., McClain, C., White, R., Henderson, D., Krym, M. and Thornton, C.A. (2000) Myotonic dystrophy in transgenic mice expressing an expanded CUG repeat. Science, 289, 1769-1773.
4. Chen, K.Y., Pan, H., Lin, M.J., Li, Y.Y., Wang, L.C., Wu, Y.C. and Hsiao, K.M. (2007) Length-dependent toxicity of untranslated CUG repeats on Caenorhabditis elegans. Biochem. Biophys. Res. Commun., 352, 774-779.
5. Du, H., Cline, M.S., Osborne, R.J., Tuttle, D.L., Clark, T.A., Donohue, J.P., Hall, M.P., Shiue, L., Swanson, M.S., Thornton, C.A. et al. (2010) Aberrant alternative splicing and extracellular matrix gene expression in mouse models of myotonic dystrophy. Nat. Struct. Mol. Biol., 17, 187-193.
6. Jiang, H., Mankodi, A., Swanson, M.S., Moxley, R.T. and Thornton, C.A. (2004) Myotonic dystrophy type 1 is associated with nuclear foci of mutant RNA, sequestration of muscleblind proteins and deregulated alternative splicing in neurons. Hum. Mol. Genet., 13, 3079-3088.
7. Fardaei, M., Rogers, M.T., Thorpe, H.M., Larkin, K., Hamshere, M.G., Harper, P.S. and Brook, J.D. (2002) Three proteins, MBNL, MBLL and MBXL, co-localize in vivo with nuclear foci of expanded-repeat transcripts in DM1 and DM2 cells. Hum. Mol. Genet., 11, 805-814.
8. Miller, J.W., Urbinati, C.R., Teng-Umnuay, P., Stenberg, M.G., Byrne, B.J., Thornton, C.A. and Swanson, M.S. (2000) Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. EMBO J., 19, 4439-4448.
9. Kanadia, R.N., Johnstone, K.A., Mankodi, A., Lungu, C., Thornton, C.A., Esson, D., Timmers, A.M., Hauswirth, W.W. and Swanson, M.S. (2003) A muscleblind knockout model for myotonic dystrophy. Science, 302, 1978-1980.
10. Kuyumcu-Martinez, N.M., Wang, G.S. and Cooper, T.A. (2007) Increased steady-state levels of CUGBP1 in myotonic dystrophy 1 are due to PKC-mediated hyperphosphorylation. Mol. Cell, 28, 68-78.
11. Timchenko, L.T., Miller, J.W., Timchenko, N.A., DeVore, D.R., Datar, K.V., Lin, L., Roberts, R., Caskey, C.T. and Swanson, M.S. (1996) Identification of a (CUG)n triplet repeat RNA-binding protein and its expression in myotonic dystrophy. Nucleic Acids Res., 24, 4407-4414.
12. Lu, X., Timchenko, N.A. and Timchenko, L.T. (1999) Cardiac elav-type RNA-binding protein (ETR-3) binds to RNA CUG repeats expanded in myotonic dystrophy. Hum. Mol. Genet., 8, 53-60.
13. Mahadevan, M.S., Yadava, R.S., Yu, Q., Balijepalli, S., Frenzel-McCardell, C.D., Bourne, T.D. and Phillips, L.H. (2006) Reversible model of RNA toxicity and cardiac conduction defects in myotonic dystrophy. Nat. Genet., 38, 1066-1070.
14. Kalsotra, A., Xiao, X., Ward, A.J., Castle, J.C., Johnson, J.M., Burge, C.B. and Cooper, T.A. (2008) A postnatal switch of CELF and MBNL proteins reprograms alternative splicing in the developing heart. Proc. Natl Acad. Sci. USA, 105, 20333-20338.
15. Lin, X., Miller, J.W., Mankodi, A., Kanadia, R.N., Yuan, Y., Moxley, R.T., Swanson, M.S. and Thornton, C.A. (2006) Failure of MBNL1-dependent post-natal splicing transitions in myotonic dystrophy. Hum. Mol. Genet., 15, 2087-2097.
16. Ho, T.H., Bundman, D., Armstrong, D.L. and Cooper, T.A. (2005) Transgenic mice expressing CUG-BP1 reproduce splicing mis-regulation observed in myotonic dystrophy. Hum. Mol. Genet., 14, 1539-1547.
17. Zu, T., Gibbens, B., Doty, N.S., Gomes-Pereira, M., Huguet, A., Stone, M.D., Margolis, J., Peterson, M., Markowski, T.W., Ingram, M.A. et al. (2011) Non-ATG-initiated translation directed by microsatellite expansions. Proc. Natl Acad. Sci. USA, 108, 260-265.
18. Moseley, M.L., Zu, T., Ikeda, Y., Gao, W., Mosemiller, A.K., Daughters, R.S., Chen, G., Weatherspoon, M.R., Clark, H.B., Ebner, T.J. et al. (2006) Bidirectional expression of CUG and CAG expansion transcripts and intranuclear polyglutamine inclusions in spinocerebellar ataxia type 8. Nat. Genet., 38, 758-769.
19. Lopez Castel, A., Nakamori, M., Thornton, C.A. and Pearson, C.E. (2011) Identification of restriction endonucleases sensitive to 5-cytosine methylation at non-CpG sites, including expanded (CAG)n/(CTG)n repeats. Epigenetics, 6, 416-420.
20. Lopez Castel, A., Nakamori, M., Tome, S., Chitayat, D., Gourdon, G., Thornton, C.A. and Pearson, C.E. (2011) Expanded CTG repeat demarcates a boundary for abnormal CpG methylation in myotonic dystrophy patient tissues. Hum. Mol. Genet., 20, 1-15.
21. Rau, F., Freyermuth, F., Fugier, C., Villemin, J.P., Fischer, M.C., Jost, B., Dembele, D., Gourdon, G., Nicole, A., Duboc, D. et al. (2011) Misregulation of miR-1 processing is associated with heart defects in myotonic dystrophy. Nat. Struct. Mol. Biol., 18, 840-845.
22. Gambardella, S., Rinaldi, F., Lepore, S.M., Viola, A., Loro, E., Angelini, C., Vergani, L., Novelli, G. and Botta, A. (2010) Overexpression of microRNA-206 in the skeletal muscle from myotonic dystrophy type 1 patients. J. Transl. Med., 8, 48.
23. Guo, H., Ingolia, N.T., Weissman, J.S. and Bartel, D.P. (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature, 466, 835-840.
24. Ambros, V. (2001) microRNAs: tiny regulators with great potential. Cell, 107, 823-826.
25. Lewis, B.P., Burge, C.B. and Bartel, D.P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell, 120, 15-20.
26. Fasanaro, P., Greco, S., Ivan, M., Capogrossi, M.C. and Martelli, F. (2010) microRNA: emerging therapeutic targets in acute ischemic diseases. Pharmacol. Ther., 125, 92-104.
27. van Rooij, E., Liu, N. and Olson, E.N. (2008) MicroRNAs flex their muscles. Trends Genet., 24, 159-166.
28. Latronico, M.V. and Condorelli, G. (2009) MicroRNAs and cardiac pathology. Nat. Rev. Cardiol., 6, 419-429.
29. Eisenberg, I., Eran, A., Nishino, I., Moggio, M., Lamperti, C., Amato, A.A., Lidov, H.G., Kang, P.B., North, K.N., Mitrani-Rosenbaum, S. et al. (2007) Distinctive patterns of microRNA expression in primary muscular disorders. Proc. Natl Acad. Sci. USA, 104, 17016-17021.
30. Perbellini, R., Greco, S., Sarra-Ferraris, G., Cardani, R., Capogrossi, M.C., Meola, G. and Martelli, F. (2011) Dysregulation and cellular mislocalization of specific miRNAs in myotonic dystrophy type 1. Neuromuscul. Disord., 21, 81-88.
31. Braida, C., Stefanatos, R.K., Adam, B., Mahajan, N., Smeets, H.J., Niel, F., Goizet, C.,Arveiler, B.,Koenig,M., Lagier-Tourenne, C. et al. (2010) Variant CCG and GGC repeats within the CTG expansion dramatically modify mutational dynamics and likely contribute toward unusual symptoms in some myotonic dystrophy type 1 patients. Hum. Mol. Genet., 19, 1399-1412.
32. Musova, Z., Mazanec, R., Krepelova, A., Ehler, E., Vales, J., Jaklova, R., Prochazka, T., Koukal, P., Marikova, T., Kraus, J. et al. (2009) Highly unstable sequence interruptions of the CTG repeat in the myotonic dystrophy gene. Am. J. Med. Genet. A, 149A, 1365-1374.
33. Leeflang, E.P. and Arnheim, N. (1995) A novel repeat structure at the myotonic dystrophy locus in a 37 repeat allele with unexpectedly high stability. Hum. Mol. Genet., 4, 135-136.
34. Pearson, C.E. (2011) Repeat associated non-ATG translation initiation: one DNA, two transcripts, seven reading frames, potentially nine toxic entities! PLoS Genet., 7, e1002018.
35. Ryazansky, S.S., Gvozdev, V.A. and Berezikov, E. (2011) Evidence for post-transcriptional regulation of clustered microRNAs in Drosophila. BMC Genomics, 12, 371
36. Garcia-Casado, M.Z., Artero, R.D., Paricio, N., Terol, J. and Perez-Alonso, M. (2002) Generation of GAL4-responsive muscleblind constructs. Genesis, 34, 111-114.
37. Llamusi, B., Bargiela, A., Fernandez-Costa, J.M., Garcia-Lopez, A., Klima, R., Feiguin, F. and Artero, R. (2012) Muscleblind, BSF, and TBPH are mis-localized in the muscle sarcomere of a Drosophila myotonic dystrophy model. Dis. Model. Mech., doi:10.1242/dmm.009563.
38. Sokol, N.S. and Ambros, V. (2005) Mesodermally expressed DrosophilamicroRNA-1 is regulated by Twist and is required in muscles during larval growth. Genes. Dev., 19, 2343-2354.
39. Stark, A., Brennecke, J., Russell, R.B. and Cohen, S.M. (2003) Identification of Drosophila microRNA targets. PLoS Biol., 1, E60.
40. Gehrke, S., Imai, Y., Sokol, N. and Lu, B. (2010) Pathogenic LRRK2 negatively regulates microRNA-mediated translational repression. Nature, 466, 637-641.
41. Sobrino, A., Mata, M., Laguna-Fernandez, A., Novella, S., Oviedo, P.J., Garcia-Perez, M.A., Tarin, J.J., Cano, A. and Hermenegildo, C. (2009) Estradiol stimulates vasodilatory and metabolic pathways in cultured human endothelial cells. PLoS One, 4, e8242.
42. Miller, S.A., Dykes, D.D. and Polesky, H.F. (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res., 16, 1215.
43. Aslanidis, C., Jansen, G., Amemiya, C., Shutler, G., Mahadevan, M., Tsilfidis, C., Chen, C., Alleman, J., Wormskamp, N.G., Vooijs, M. et al. (1992) Cloning of the essential myotonic dystrophy region and mapping of the putative defect. Nature, 355, 548-551.
44. Brook, J.D., McCurrach, M.E., Harley, H.G., Buckler, A.J., Church, D., Aburatani, H., Hunter, K., Stanton, V.P., Thirion, J.P., Hudson, T. et al. (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.
45. Buxton, J., Shelbourne, P., Davies, J., Jones, C., Van Tongeren, T., Aslanidis, C., de Jong, P., Jansen, G., Anvret, M., Riley, B. et al. (1992) Detection of an unstable fragment of DNA specific to individuals with myotonic dystrophy. Nature, 355, 547-548.