Drosophila muscleblind is involved in troponin T alternative splicing and apoptosis

PLoS ONE

Volumn 3, Issue 2, 2008, Pages

  Vicente Crespo, Marta ^a   Pascual, Maya ^a,c   Fernandez Costa, Juan M ^a   Garcia Lopez, Amparo ^a   Monferrer, Lidón ^a   Miranda, M Eugenia ^a   Zhou, Lei ^b   Artero, Ruben D ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF FLORIDA   (United States)

^c HOSPITAL UNIVERSITARIO LA FE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DROSOPHILA PROTEIN; FUKUTIN RELATED PROTEIN; GENE PRODUCT; ISOPROTEIN; MUSCLEBLIND LIKE PROTEIN; MUSCLEBLIND LIKE PROTEIN A; MUSCLEBLIND LIKE PROTEIN B; MUSCLEBLIND LIKE PROTEIN C; MUSCLEBLIND LIKE PROTEIN D; PROTEIN ALY; PROTEIN ARET; PROTEIN REAPER; PROTEIN TSUNAGI; TROPONIN T; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 1; RNA BINDING PROTEIN;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; APOPTOSIS; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; DROSOPHILA; EMBRYO; ENHANCER REGION; EYE DEVELOPMENT; GENE OVEREXPRESSION; GENE REPRESSION; GENE SEQUENCE; GENETIC SCREENING; HUMAN; HUMAN CELL; INSECT CELL CULTURE; MOLECULAR EVOLUTION; MUTAGENESIS; NONHUMAN; NUCLEOTIDE REPEAT; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN STRUCTURE; REGULATORY MECHANISM; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; SUMOYLATION; ANIMAL; GENETICS; PHYSIOLOGY; TRINUCLEOTIDE REPEAT;

ALTERNATIVE SPLICING; AMINO ACID MOTIFS; ANIMALS; APOPTOSIS; DROSOPHILA; DROSOPHILA PROTEINS; RNA-BINDING PROTEINS; TRINUCLEOTIDE REPEAT EXPANSION; TROPONIN T;

EID: 45449084242     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0001613     Document Type: Article

References (65)

1. Adereth Y, Dammai V, Kose N, Li R, Hsu T (2005) RNA-dependent integrin alpha(3) protein localization regulated by the Muscleblind-like protein MLP1. Nat Cell Biol 7: 1140-1147.
2. Dean B, Keriakous D, Scarr E, Thomas EA (2001) Gene expression profiling in Brodmann's area 46 from subjects with schizophrenia. Aust N ZJ Psychiatry 41: 308-320.
3. Edgar AJ, Chacon MR, Bishop AE, Yacoub MH, Polak JM (2006) Upregulated genes in sporadic, idiopathic pulmonary arterial hypertension. Respir Res 7: 1.
4. Ranum LP, Cooper TA (2006) RNA-Mediated Neuromuscular Disorders. Annu Rev Neurosci. 29: 259-277.
5. Osborne RJ, Thornton CA (2006) RNA-dominant diseases. Hum Mol Genet 15 Spec No 2: R162-169.
6. Mutsuddi M, Marshall CM, Benzow KA, Koob MD, Rebay I (2004) The spinocerebellar ataxia 8 noncoding RNA causes neurodegeneration and associates with staufen in Drosophila. Curr Biol 14: 302-308.
7. Ho TH, Charter BN, Poulos MG, Singh G, Swanson MS, et al. (2004) Muscleblind proteins regulate alternative splicing Embo J 23: 3103-3112.
8. Lin X, Miller JW, Mankodi A, Kanadia RN, Yuan Y, et al. (2006) Failure of MBNL1-dependent post-natal splicing transitions in myotonic dystrophy. Hum Mol Genet 15: 2087-2097.
9. Kanadia RN, Shin J, Yuan Y, Beattie SG, Wheeler TM, et al. (2006) Reversal of RNA missplicing and myotonia after muscleblind overexpression in a mouse poly(CUG) model for myotonic dystrophy. Proc Natl Acad Sci U S A. 103: 11748-53.
10. Ladd AN, Stenberg MG, Swanson MS, Cooper TA (2005) Dynamic balance between activation and repression regulates pre-mRNA alternative splicing during heart development. Dev Dyn 233: 783-793.
11. Kanadia RN, Johnstone KA, Mankodi A, Lungu C, Thornton CA, et al. (2003) A muscleblind knockout model for myotonic dystrophy. Science 302: 1978-1980.
12. Charlet BN, Savkur RS, Singh G, Philips AV, Grice EA, et al. (2002) Loss of the muscle-specific chloride channel in type 1 myotonic dystrophy due to misregulated alternative splicing. Mol Cell 10: 45-53.
13. 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.
14. Jiang H, Mankodi A, Swanson MS, Moxley RT, Thornton CA (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.
15. Mankodi A, Lin Y, Blaxall BC, Swanson MS, Thornton CA (2005) Nuclear RNA foci in the heart in myotonic dystrophy. Circ Res 97: 1152-1155.
16. 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.
17. Ebralidze A, Wang Y, Petkova. V, Ebralidse Y, Junghans RP (2004) RNA leaching of transcription factors disrupts transcription in myotonic dystrophy. Science 303: 383-387.
18. Krol J, Fiszer A, Mykowska A, Sobczak K, de Mezer M, et al. (2007) Ribonuclease dicer cleaves triplet repeat hairpins into shorter repeats that silence specific targets. Mol Cell 25: 575-586.
19. Fardaei M, Rogers MT, Thorpe HM, Larkin K, Hamshere MG, et al. (2002) Three proteins, MBNI, 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.
20. Mankodi A, Urbinati CR, Yuan QP, Moxley RT, Sansone V, et al. (2001) Muscleblind localizes to nuclear foci of aberrant RNA in myotonic dystrophy types 1 and 2. Hum Mol Genet 10: 2165-2170.
21. Miller JW, Urbinati CR, Teng-Umnuay P, Stenberg MG, Byrne BJ, et al. (2000) Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. Embo J 19: 4439-4448.
22. Paul S, Dansithong W, Kim D, Rossi J, Webster NJ, et al. (2006) Interaction of muscleblind, CUG-BP1 and hnRNP H proteins in DM1-associated aberrant IR splicing. Embo J 25: 4271-4283.
23. Squillace RM, Chenault DM, Wang EH (2002) Inhibition of muscle differentiation by the novel muscleblind-related protein CHCR. Dev Biol 250: 218-230.
24. Lee KS, Smith K, Amieux PS, Wang EH (2007) MBNL3/CHCR prevents myogenic differentiation by inhibiting MyoD-dependent gene transcription. Differentiation.
25. Begemann G, Paricio N, Artero R, Kiss I, Perez-Alonso M, et al. (1997) muscleblind, a gene required for photoreceptor differentiation in Drosophila, encodes novel nuclear Cys3His-type zinc-finger-containing proteins. Development 124: 4321-4331.
26. Artero R, Prokop, A, Paricio N, Begemann G, Pueyo I, et al. (1998) The muscleblind gene participates in the organization of Z-bands and epidermal attachments of Drosophila muscles and is regulated by Dmef2. Dev Biol 195: 131-143.
27. Vicente M, Monferrer L, Poulos MG, Houseley J Monckton DG, et al. (2007) Muscleblind isoforms are functionally distinct and regulate alpha-actinin splicing. Differentiation. 75(5): 427-40.
28. Machuca-Tzili L, Thorpe H, Robinson TE, Scwry C, Brook JD (2006) Flies deficient in Muscleblind protein model features of myotonic dystrophy with altered splice forms of Z-band associated transcripts. Hum Genet 120: 487-499.
29. Monferrer L, Artero R (2006) An Interspecific Functional Complementation Test in Drosophila for Introductory Genetics Laboratory Courses. J Hered. 97(1): 67-73.
30. Pascual M, Vicente M, Monferrer L, Artero R (2006) The Muscleblind family of proteins: an emerging class of regulators of developmentally programmed alternative splicing. Differentiation 74: 65-80.
31. Kino Y, Mori D, Oma Y, Takeshita Y, Sasagawa N, et al. (2004) Muscleblind protein, MBNL1/EXP, binds specifically to CHHG repeats. Hum Mol Genet 13: 495-507.
32. Yuan Y, Compton SA, Sobczak K, Stenberg MG, Thornton CA, et al. (2007) Muscleblind-like 1 interacts with RNA hairpins in splicing target and pathogenic RNAs. Nucleic Acids Res. 35(16): 5474-86.
33. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
34. Garcia-Casado MZ, Artero RD, Paricio N, Terol J, Perez-Alonso M (2002) Generation of GALA-responsive muscleblind constructs. Genesis 34: 111-114.
35. Amparo Garcia-Lopez LM, Irma Garcia-Alcover, Marta Vicente-Crespo MCA-AaRDA (In press) Genetic and chemical modifiers of a GUG toxicity model in Drosophila. PLOS ONE. in press.
36. Hay BA, Wassarman DA, Rubin GM (1995) Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83: 1253-1262.
37. Cheah PY, Chia W, Yang X (2000) Jumeaux, a novel Drosophila winged-helix family protein, is required for generating asymmetric sibling neuronal cell fates. Development 127: 3325-3335.
38. Strodicke M, Karberg S, Korge G (2000) Domina (Dom), a new Drosophila member of the FKH/WH gene family, affects morphogenesis and is a suppressor of position-effect variegation. Mech Dev 96: 67-78.
39. Huang ML, Hsu CH, Chien CT (2000) The proneural gene amos promotes multiple dendritic neuron formation in the Drosophila peripheral nervous system. Neuron 25: 57-67.
40. Goulding SE, zur Lage P, Jarman AP (2000) amos, a proneural gene for Drosophila olfactory sense organs that is regulated by lozenge. Neuron 25: 69-78.
41. Benoist P, Mas JA, Marco R, Cervera M (1998) Differential Muscle-type Expression of the Drosophila Troponin T Genet A 3-base pair microexon is involved in visceral and adult hypodermic muscle specification. J Biol Chem 273: 7538-7546.
42. Hay BA, Huh JR, Guo M (2004) The genetics of cell death: approaches, insights and opportunities in Drosophila. Nat Rev Genet 5: 911-922.
43. Zhou L, Jiang G, Chan G, Santos CP, Serverson DW, et al. (2005) Michelob_x is the missing inhibitor of apoptosis protein antagonist in mosquito genomes. EMBO Rep 6: 769-774.
44. Xue Y, Zhou F, Fu C, Xu Y, Yao X (2006) SUMOsp: a web server for sumoylation site prediction. Nucleic Acids Res 34: W254-257.
45. Bossis G, Malnou CE, Farras R, Andermarcher E, Hipskind R, et al. (2005) Down-regulation of c-Fos/c-Jun AP-1 dimer activity by sumoylation. Mol Cell Biol 25: 6964-6979.
46. Wilson VG, Rangasamy D (2001) Intracellular Targeting of Proteins by Sumoylation. Experimental Cell Research 271: 57.
47. Houseley JM, Wang Z, Brock GJ, Soloway J, Artero R, et al. (2005) Myotonic dystrophy associated expanded CUG repeat muscleblind positive ribonuclear foci are not toxic to Drosophila. Hum Mol Genet 14: 873-883.
48. Ran R, Zhou G, Lu A, Zbang L, Tarig Y, et al. (2004) Hsp70 mutant proteins modulate additional apoptotic pathways and improve cell survival. Cell Stress Chaperones 9: 229-242.
49. Chaudhuri T, Mukherjea M, Sachdev S, Randall JD, Sarkar S (2005) Role of the Fetal and [alpha]/[beta] Exons in the Function of Fast Skeletal Troponin T Isoforms: Correlation with Altered Ca2+ Regulation Associated with Development. Journal of Molecular Biology 352: 58.
50. Park JW, Parisky K, Celotto AM, Reenan RA, Graveley BR (2004) Identification of alternative splicing regulators by RNA interference in Drosophila. Proc Natl Acad Sci U S A 101: 15974-15979.
51. Delaunay J, Le Mee G, Ezzeddine N, Labesse G, Terzian C, et al. (2004) The Drosophila Bruno paralogue Bru-3 specifically binds the EDEN translational repression element. Nucleic Acids Res 32: 3070-3082.
52. Webster PJ, Liang L, Berg CA, Lasko P, Macdonald PM (1997) Translational repressor bruno plays multiple roles in development and is widely conserved. Genes Dev 11: 2510-2521.
53. Chekulaeva M, Hentze MW, Ephrussi A (2006) Bruno acts as a dual repressor of oskar manslation, promoting mRNA oligomerization and formation of silencing particles. Cell 124: 521-533.
54. Yan N, Macdonald PM (2004) Genetic interactions of Drosophila melanogaster arrest reveal roles for translational repressor Bruno in accumulation of Gurken and activity of Delta. Genetics 168: 1433-1442.
55. Schwerk C, Schulze-Osthoff K (2005) Regulation of apoptosis by alternative pre-mRNA splicing. Mol Cell 19: 1-13.
56. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
57. Crosby MA, Goodman JL, Strelets VB, Zhang P, Gelbart WM (2007) FlyBase: genomes by the dozen. Nucleic Acids Res 35: D486-491.
58. Bieri T, Blasiar D, Ozersky P, Antoshechkin I, Bastiani C, et al. (2007) WormBase: new content and better access. Nucleic Acids Res 35: D506-510.
59. Kania A, Salzberg A, Bhat M, D'Evelyn D, He Y, et al. (1995) P-element mutations affecting embryonic peripheral nervous system development in Drosophila melanogaster. Genetics 139: 1663-1678.
60. Toba G, Ohsaku T, Miyata N, Ohtsuka T, Seong KH, et al. (1999) The gene search system. A method for efficient detection and rapid molecular identification of genes in Drosophila melanogaster. Genetics 151: 725-737.
61. Hayashi S, Ito K, Sado Y, Taniguchi M, Akimoto A, et al. (2002) GETDB, a database compiling expression patterns and molecular locations of a collection of Ga14 enhancer traps. Genesis 34: 58-61.
62. Ashburner M (1989) Drosophila, a Laboratory Manual: Cold spring Harbor Press.
63. Shulman JM, Feany MB (2003) Genetic modifiers of tauopathy in Drosophila. Genetics 165: 1233-1242.
64. Kim HJ, Kim SH, Shim SO, Park E, Kim C, et al. (2007) Drosophila homolog of APP-BP1 (dAPP-BP1) interacts antagonistically with APPL during Drosophila development. Cell Death Differ 14: 103-115.
65. Grimaldi DA (1990) A phylogenetic, revised classification of Genera in the Drosophilidae (Diptera). Bulletin of the American Museum of Natural History.