Defining early steps in mRNA transport: Mutant mRNA in myotonic dystrophy type I is blocked at entry into SC-35 domains

Journal of Cell Biology

Volumn 178, Issue 6, 2007, Pages 951-964

  Smith, Kelly P ^a   Byron, Meg ^a   Johnson, Carol ^a   Xing, Yigong ^a   Lawrence, Jeanne B ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MUTANT PROTEIN; MYOTONIC DYSTROPHY PROTEIN KINASE; PROTEIN; PROTEIN MBNL1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ALTERNATIVE RNA SPLICING; ARTICLE; CONTROLLED STUDY; GENE LOCUS; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MYOTONIC DYSTROPHY; PRIORITY JOURNAL; PROTEIN DOMAIN; RNA TRANSPORT; TRINUCLEOTIDE REPEAT;

CELLS, CULTURED; CHILD; HUMANS; MALE; MODELS, MOLECULAR; MUTATION; MYOBLASTS, SKELETAL; MYOTONIC DYSTROPHY; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RNA SPLICING; RNA TRANSPORT; RNA, MESSENGER; RNA-BINDING PROTEINS; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 34548842522     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200706048     Document Type: Article

References (71)

1. Aslanidis, C., G. Jansen, C. Amemiya, G. Shutler, M. Mahadevan, C. Tsilfidis, C. Chen, J. Alleman, N.G. Wormskamp, M. Vooijs, et al. 1992. Cloning of the essential myotonic dystrophy region and mapping of the putative defect. Nature. 355:548-551.
2. Blencowe, B.J., J.A. Nickerson, R. Issner, S. Penman, and P.A. Sharp. 1994. Association of nuclear matrix antigens with exon-containing splicing complexes. J. Cell Biol. 127:593-607.
3. Blencowe, B.J., R. Issner, J.A. Nickerson, and P.A. Sharp. 1998. A coactivator of pre-mRNA splicing. Genes Dev. 12:996-1009.
4. Botta, A., S. Caldarola, L. Vallo, E. Bonifazi, D. Fruci, F. Gullotta, R. Massa, G. Novelli, and F. Loreni. 2006. Effect of the [CCTG]n repeat expansion on ZNF9 expression in myotonic dystrophy type II (DM2). Biochim. Biophys. Acta. 1762:329-334.
5. Brook, J.D., M.E. McCurrach, H.G. Harley, A.J. Buckler, D. Church, H. Aburatani, K. Hunter, V.P. Stanton, J.P. Thirion, T. Hudson, 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. 69:385.
6. Carter, K.C., K.L. Taneja, and J.B. Lawrence. 1991. Discrete nuclear domains of poly(A) RNA and their relationship to the functional organization of the nucleus. J. Cell Biol. 115:1191-1202.
7. Carter, K.C., D. Bowman, W. Carrington, K. Fogarty, J.A. McNeil, F.S. Fay, and J.B. Lawrence. 1993. A three-dimensional view of precursor messenger RNA metabolism within the mammalian nucleus. Science. 259:1330-1335.
8. Caskey, C.T., M.S. Swanson, and L.T. Timchenko. 1996. Myotonic dystrophy: discussion of molecular mechanism. Cold Spring Harb. Symp. Quant. Biol. 61:607-614.
9. Chaumeil, J., P. Le Baccon, A. Wutz, and E. Heard. 2006. A novel role for Xist RNA in the formation of a repressive nuclear compartment into which genes are recruited when silenced. Genes Dev. 20:2223-2237.
10. Cheng, J., P. Kapranov, J. Drenkow, S. Dike, S. Brubaker, S. Patel, J. Long, D. Stern, H. Tammana, G. Helt, et al. 2005. Transcriptional maps of 10 human chromosomes at 5-nucleotide resolution. Science. 308:1149-154.
11. Clemson, C.M., L.L. Hall, M. Byron, J. McNeil, and J.B. Lawrence. 2006. The X chromosome is organized into a gene-rich outer rim and an internal core containing silenced nongenic sequences. Proc. Natl. Acad. Sci. USA. 103:7688-7693.
12. Dansithong, W., S. Paul, L. Comai, and S. Reddy. 2005. MBNL1 is the primary determinant of focus formation and aberrant insulin receptor splicing in DM1. J. Biol. Chem. 280:5773-5780.
13. Davis, B.M., M.E. McCurrach, K.L. Taneja, R.H. Singer, and D.E. Housman. 1997. Expansion of a 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.
14. Day, J.W., and L.P. Ranum. 2005. RNA pathogenesis of the myotonic dystrophies. Neuromuscul. Disord. 15:5-16.
15. Day, J.W., K. Ricker, J.F. Jacobsen, L.J. Rasmussen, K.A. Dick, W. Kress, C. Schneider, M.C. Koch, G.J. Beilman, A.R. Harrison, et al. 2003. Myotonic dystrophy type 2: molecular, diagnostic and clinical spectrum. Neurology. 60:657-664.
16. Ebralidze, A., Y. Wang, V. Petkova, K. Ebralidse, and R.P. Junghans. 2004. RNA leaching of transcription factors disrupts transcription in myotonic dystrophy. Science. 303:383-387.
17. Fakan, S. 1994. Perichromatin fibrils are in situ forms of nascent transcripts. Trends Cell Biol. 4:86-90.
18. Fakan, S., and W. Bernhard. 1971. Localisation of rapidly and slowly labelled nuclear RNA as visualized by high resolution autoradiography. Exp. Cell Res. 67:129-141.
19. Fardaei, M., K. Larkin, J.D. Brook, and M.G. Hamshere. 2001. In vivo colocalisation of MBNL protein with DMPK expanded-repeat transcripts. Nucleic Acids Res. 29:2766-2771.
20. Fox, A.H., Y.W. Lam, A.K. Leung, C.E. Lyon, J. Andersen, M. Mann, and A.I. Lamond. 2002. Paraspeckles: a novel nuclear domain. Curr. Biol. 12:13-25.
21. Fu, X.-D., and T. Maniatis. 1990. Factor required for mammalian spliceo-some assembly is localized to discrete regions in the nucleus. Nature. 343:437-444.
22. Fu, Y.H., A. Pizzuti, R.G. Fenwick Jr., J. King, S. Rajnarayan, P.W. Dunne, J. Dubel, G.A. Nasser, T. Ashizawa, P. de Jong, et al. 1992. An unstable triplet repeat in a gene related to myotonic muscular dystrophy. Science. 255:1256-1258.
23. Gorski, S.A., M. Dundr, and T. Misteli. 2006. The road much traveled: trafficking in the cell nucleus. Curr. Opin. Cell Biol. 18:284-290.
24. Hall, L.L., C.M. Clemson, M. Byron, K. Wydner, and J.B. Lawrence. 2002. Unbalanced X;autosome translocations provide evidence for sequence specificity in the association of XIST RNA with chromatin. Hum. Mol. Genet. 11:3157-3165.
25. Hall, L.L., K.P. Smith, M. Byron, and J.B. Lawrence. 2006. Molecular anatomy of a speckle. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 288:664-675.
26. Hamshere, M.G., E.E. Newman, M. Alwazzan, B.S. Athwal, and J.D. Brook. 1997. Transcriptional abnormality in myotonic dystrophy affects DMPK but not neighboring genes. Proc. Natl. Acad. Sci. USA. 94:7394-7399.
27. Huang, S., T.J. Deerinck, M.H. Ellisman, and D.L. Spector. 1994. In vivo analysis of the stability and transport of nuclear poly(A)+ RNA. J. Cell Biol. 126:877-899.
28. Hutchinson, J.N., A.W. Ensminger, C.M. Clemson, C.R. Lynch, J.B. Lawrence, and A. Chess. 2007. A screen for nuclear transcripts identifies two linked noncoding RNAs associated with SC35 splicing domains. BMC Genomics. 8:39.
29. Jiang, H., A. Mankodi, M.S. Swanson, R.T. Moxley, and C.A. Thornton. 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.
30. Johnson, C.V., R.H. Singer, and J.B. Lawrence. 1991. Fluorescent detection of nuclear RNA and DNA: Implication for genome organization. Methods Cell Biol. 35:73-99.
31. Johnson, C., D. Primorac, M. McKinstry, J. McNeil, D. Rowe, and J.B. Lawrence. 2000. Tracking COL1A1 RNA in Osteogenesis Imperfecta: splicedefective transcripts initiate transport from the gene but are retained within the SC-35 domain. J. Cell Biol. 150:417-431.
32. Johnson, J.M., S. Edwards, D. Shoemaker, and E.E. Schadt. 2005. Dark matter in the genome: evidence of widespread transcription detected by microarray tiling experiments. Trends Genet. 21:93-102.
33. Jolly, C., C. Vourc'h, M. Robert-Nicoud, and R.I. Morimoto. 1999. Intron-independent association of splicing factors with active genes. J. Cell Biol. 145:1133-1143.
34. Kanadia, R.N., K.A. Johnstone, A. Mankodi, C. Lungu, C.A. Thornton, D. Esson, A.M. Timmers, W.W. Hauswirth, and M.S. Swanson. 2003. A muscleblind knockout model for myotonic dystrophy. Science. 302:1978-1980.
35. Kim, D.H., M.A. Langlois, K.B. Lee, A.D. Riggs, J. Puymirat, and J.J. Rossi. 2005. HnRNP H inhibits nuclear export of mRNA containing expanded CUG repeats and a distal branch point sequence. Nucleic Acids Res. 33:3866-3874.
36. Lawrence, J.B., K.C. Carter, and X. Xing. 1993. Probing functional organization within the nucleus: is genome structure integrated with RNA metabolism? Cold Spring Harb. Symp. Quant. Biol. 58:807-818.
37. Lin, X., J.W. Miller, A. Mankodi, R.N. Kanadia, Y. Yuan, R.T. Moxley, M.S. Swanson, and C.A. Thornton. 2006. Failure of MBNL1-dependent post-natal splicing transitions in myotonic dystrophy. Hum. Mol. Genet. 15:2087-2097.
38. Liquori, C.L., K. Ricker, M.L. Moseley, J.F. Jacobsen, W. Kress, S.L. Naylor, J.W. Day, and L.P. Ranum. 2001. Myotonic dystrophy type 2 caused by a CCTG expansion in intron 1 of ZNF9. Science. 293:864-867.
39. Mahadevan, M., C. Tsilfidis, L. Sabourin, G. Shutler, C. Amemiya, G. Jansen, C. Neville, M. Narang, J. Barcelo, K. O'Hoy, et al. 1992. Myotonic dystrophy mutation: an unstable CTG repeat in the 3′ untranslated region of the gene. Science. 255:1253-1255.
40. Mankodi, A., C.R. Urbinati, Q.P. Yuan, R.T. Moxley, V. Sansone, M. Krym, D. Henderson, M. Schalling, M.S. Swanson, and C.A. Thornton. 2001. Muscleblind localizes to nuclear foci of aberrant RNA in myotonic dystrophy types 1 and 2. Hum. Mol. Genet. 10:2165-2170.
41. Margolis, J.M., B.G. Schoser, M.L. Moseley, J.W. Day, and L.P. Ranum. 2006. DM2 intronic expansions: evidence for CCUG accumulation without flanking sequence or effects on ZNF9 mRNA processing or protein expression. Hum. Mol. Genet. 15:1808-1815.
42. Masuda, S., R. Das, H. Cheng, E. Hurt, N. Dorman, and R. Reed. 2005. Recruitment of the human TREX complex to mRNA during splicing. Genes Dev. 19:1512-1517.
43. Miller, J.W., C.R. Urbinati, P. Teng-Umnuay, M.G. Stenberg, B.J. Byrne, C.A. Thornton, and M.S. Swanson. 2000. Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. EMBO J. 19:4439-4448.
44. Moen, P.T., Jr., K.P. Smith, and J.B. Lawrence. 1995. Compartmentalization of specific pre-mRNA metabolism: an emerging view. Hum. Mol. Genet. 4:1779-1789.
45. Moen, P.T., Jr., C.V. Johnson, M. Byron, L.S. Shopland, I.L. de la Serna, A.N. Imbalzano, and J.B. Lawrence. 2004. Repositioning of muscle-specific genes relative to the periphery of SC-35 domains during skeletal myogenesis. Mol. Biol. Cell. 15:197-206.
46. Molenaar, C., A. Abdulle, A. Gena, H.J. Tanke, and R.W. Dirks. 2004. Poly(A)+ RNAs roam the cell nucleus and pass through speckle domains in transcriptionally active and inactive cells. J. Cell Biol. 165:191-202.
47. Nyman, U., H. Hallman, G. Hadlaczky, I. Pettersson, G. Sharp, and N.R. Ringertz. 1986. Intranuclear localization of snRNP antigens. J. Cell Biol. 102:137-144.
48. Osborne, R.J., and C.A. Thornton. 2006. RNA-dominant diseases. Hum. Mol. Genet. 15 Spec No 2:R162-R169.
49. Pascual, M., M. Vicente, L. Monferrer, and R. Artero. 2006. The Muscleblind family of proteins: an emerging class of regulators of developmentally programmed alternative splicing. Differentiation. 74:65-80.
50. Paul, S., W. Dansithong, D. Kim, J. Rossi, N.J. Webster, L. Comai, and S. Reddy. 2006. Interaction of muscleblind, CUG-BP1 and hnRNP H proteins in DM1-associated aberrant IR splicing. EMBO J. 25:4271-4283.
51. Philips, A.V., L.T. Timchenko, and T.A. Cooper. 1998. Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy. Science. 280:737-741.
52. Politz, J.C., R.A. Tuft, and T. Pederson T. 2003. Diffusion-based transport of nascent ribosomes in the nucleus. Mol. Biol. Cell. 14:4805-4812.
53. Salditt-Georgieff, M., M.M. Harpold, M.C. Wilson, and J.E. Darnell Jr. 1981. Large heterogeneous nuclear ribonucleic acid has three times as many 5′ caps as polyadenylic acid segments, and most caps do not enter polyribosomes. Mol. Cell. Biol. 1:179-187
54. Schmidt, U., K. Richter, A.B. Berger, and P. Lichter. 2006. In vivo BiFC analysis of Y14 and NXF1 mRNA export complexes: preferential localization within and around SC35 domains. J. Cell Biol. 172:373-381.
55. Shopland, L.S., C.V. Johnson, and J.B. Lawrence. 2002. Evidence that all SC-35 domains contain mRNAs and that transcripts can be structurally constrained within these domains. J. Struct. Biol. 140:131-139.
56. Shopland, L.S., C.V. Johnson, M. Byron, J. McNeil, and J.B. Lawrence. 2003. Clustering of multiple specific genes and gene-rich R-bands around SC-35 domains: evidence for local euchromatic neighborhoods. J. Cell Biol. 162:981-990.
57. Smith, K.P., P.T. Moen, K.L. Wydner, J.R. Coleman, and J.B. Lawrence. 1999. Processing of endogenous pre-mRNAs in association with SC-35 domains is gene specific. J. Cell Biol. 144:617-629.
58. Spector, D.L. 1993. Macromolecular domains within the cell nucleus. Annu. Rev. Cell Biol. 9:265-315.
59. Spector, D.L., X.D. Fu, and T. Maniatis. 1991. Associations between distinct pre-mRNA splicing components and the cell nucleus. EMBO J. 10:3467-3481.
60. Tam, R., L. Shopland, C.V. Johnson, J. McNeil, and J.B. Lawrence. 2002. Applications of RNA FISH for visualizing gene expression and nuclear architecture. In FISH: a Practical Approach. B. Beatty, S. Mai, and J. Squire, editors. Oxford University Press, New York. 93-118.
61. Taneja, K.L., M. McCurrach, M. Schalling, D. Housman, and R.H. Singer. 1995. Foci of trinucleotide repeat transcripts in nuclei of myotonic dystrophy cells and tissues. J. Cell Biol. 128:995-1002.
62. Tian, B., R.J. White, T. Xia, S. Welle, D.H. Turner, M.B. Mathews, and C.A. Thornton. 2000. Expanded CUG repeat RNAs form hairpins that activate the double-stranded RNA-dependent protein kinase PKR. RNA. 6:79-87.
63. Timchenko, L.T., J.W. Miller, N.A. Timchenko, D.R. DeVore, K.V. Datar, L. Lin, R. Roberts, C.T. Caskey, and M.S. Swanson. 1996. Identification of a (CUG)n triplet repeat RNA-binding protein and its expression in myotonic dystrophy. Nucleic Acids Res. 24:4407-4414.
64. Timchenko, L., W. Nastainczyk, T. Schneider, B. Patel, F. Hofmann, and C.T. Caskey. 1995. Full-length myotonin protein kinase (72 kDa) displays serine kinase activity. Proc. Natl. Acad. Sci. USA. 92:5366-5370.
65. Timchenko, N.A., Z.J. Cai, A.L. Welm, S. Reddy, T. Ashizawa, and L.T. Timchenko. 2001. RNA CUG repeats sequester CUGBP1 and alter protein levels and activity of CUGBP1. J. Biol. Chem. 276:7820-7826.
66. Tokunaga, K., T. Shibuya, Y. Ishihama, H. Tadakuma, M. Ide, M. Yoshida, T. Funatsu, Y. Ohshima, and T. Tani. 2006. Nucleocytoplasmic transport of fluorescent mRNA in living mammalian cells: nuclear mRNA export is coupled to ongoing gene transcription. Genes Cells. 11:305-317.
67. Webster, C., G.K. Pavlath, D.R. Parks, F.S. Walsh, and H.M. Blau. 1988. Isolation of human myoblasts with the fluorescence-activated cell sorter. Exp. Cell Res. 174:252-265.
68. Wei, X., S. Somanathan, J. Samarabandu, and R. Berezney. 1999. Three-dimensional visualization of transcription sites and their association with splicing factor-rich nuclear speckles. J. Cell Biol. 146:543-558.
69. Xing, Y., C.V. Johnson, P.R. Dobner, and J.B. Lawrence. 1993. Higher level organization of individual gene transcription and RNA splicing. Science. 259:1326-1330.
70. Xing, Y., C.V. Johnson, P.T. Moen, J.A. McNeil, and J.B. Lawrence. 1995. Nonrandom gene organization: Structural arrangements of specific pre-mRNA transcription and splicing with SC-35 domains. J. Cell Biol. 131:1635-1647.
71. Zhou, Z., M.J. Luo, K. Straesser, J. Katahira, E. Hurt, and R. Reed. 2000. The protein Aly links pre-messenger-RNA splicing to nuclear export in metazoans. Nature. 407:401-405.