Dysfunction of protein homeostasis in myotonic dystrophies

Histology and Histopathology

Volumn 28, Issue 9, 2013, Pages 1089-1098

  Meola, Giovanni ^a   Jones, Karlie ^b   Wei, Christina ^b   Timchenko, Lubov T ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b Department of Molecular Physiology and Biophysics ^*  (United States)

Author keywords

Aging; CUGBP1; Myotonic dystrophy; Translation; ZNF9

Indexed keywords

CELF1 PROTEIN, HUMAN; CNBP PROTEIN, HUMAN; CYTOSKELETON PROTEIN; DEAD BOX PROTEIN; MBNL1 PROTEIN, HUMAN; PROTEIN; RNA BINDING PROTEIN; STAU1 PROTEIN, HUMAN;

AGING; ANIMAL; CHEMISTRY; CYTOPLASM; DISEASE COURSE; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMAN; METABOLISM; MYOTONIC DYSTROPHY; PATHOLOGY; REVIEW;

AGING; ANIMALS; CYTOPLASM; CYTOSKELETAL PROTEINS; DEAD-BOX RNA HELICASES; DISEASE PROGRESSION; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; MYOTONIC DYSTROPHY; PROTEINS; RNA-BINDING PROTEINS;

EID: 84884361485     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (82)

1. Anderson P. and Kedersha N. (2006). RNA granules. J. Cell Biol. 172, 803-808.
2. Ashizawa T. and Sarkar P.S. (2011). Myotonic dystrophy types 1 and 2. Handb. Clin. Neurol. 101, 193-237.
3. Bachand F., Triki I. and Autexier C. (2001). Human telomerase RNAprotein interactions. Nucl. Acids Res. 29, 3385-3393.
4. Beisang D., Rattenbacher B., Vlasova-St Louis I.A. and Bohjanen P.R. (2012). Regulation of CUG-binding protein 1 (CUGBP1) binding to target transcripts upon T cell activation. J. Biol. Chem. 287, 950-960.
5. Bond A.T., Mangus D.A., He F. and Jacobson A. (2001). Absence of Dbp2p alters both nonsense-mediated mRNA decay and rRNA processing. Mol. Cell. Biol. 21, 7366-7379.
6. Botta A., Caldarola S., Vallo L., Bonifazi E., Fruci D., Gullotta F., Massa R., Novelli G. and Loreni F. (2006). Effect of the [CCTG]n repeat expansion on ZNF9 expression in myotonic dystrophy II (DM2). Biochem. Biophys. Acta 1762, 329-334.
7. Calcaterra N.B., Armas P., Weiner A.M. and Borgognone M. (2010). CNBP: a multifunctional nucleic acid chaperone involved in cell death and proliferation control. IUBMB Life 62, 707-714.
8. Chekulaeva M., Hentze M.W. and Ephrussi A. (2006). Bruno acts a dual repressor of oskar translation, promoting mRNA oligomerization and formation of silencing particles. Cell 124, 521-533.
9. Chen W., Wang Y., Abe Y., Cheney L., Udd B. and Li Y. P. (2007). Haploinsuffciency for ZNF9 in ZNF9+/- mice is associated with multiorgan abnormalities resembling myotonic dystrophy. J. Mol. Biol. 368, 8-17.
10. Damgaard C.K. and Lykke-Andersen J. (2011). Transl ati onal coregulation of 5'TOP mRNAs by TIA-1 and TIAR. Genes Dev. 25, 2057-2068.
11. de la Cruz J., Kressler D. and Linder P. (1999). Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. TIBS 24, 192-198.
12. Edwards J.G., Bahl J.J., Flink I., Milavetz J., Goldman S. and Morkin E. (1992). A repressor region in the human beta-myosin heavy chain gene that has a partial position dependency. Biochem. Biophys. Res. Commun. 189, 504-510.
13. Farina K.L. and Singer R. H. (2002). The nuclear connection in RNA transport and localization. Trends Cell Biol. 12, 466-472.
14. Flink I.L. and Morkin E. (1995). Alternatively processed isoforms of cellular nucleic acid-binding protein interact with a suppressor region of the human beta-myosin heavy chain gene. J. Biol. Chem. 270, 6959-6965.
15. Flink I.L., Blitz I. and Morkin E. (1998). Characterization of cellular nucleic binding protein from Xenopus laevis: expression in all three germ layers during development. Dev. Dyn. 211, 123-130.
16. Fox J.T. and Stover P.J. (2009). Mechanism of the internal ribosome entry site-mediated translation of serine hydroxymethyltransferase 1. J. Biol. Chem. 284, 31085-31096.
17. Fujimura K., Kano F. and Murata M. (2008). Dual localization of the RNA binding proteins CUGBP-1 to stress granules and perinuclear compartment. Exp. Cell. Res. 314, 543-553.
18. Fukao A., Sasano Y., Imataka H., Inoue K., Sakamoto H., Sonenberg N., Thoma C. and Fujiwara T. (2009). The ELAV protein HuD stimulates cap-dependent translation in a poly(A)- and eIF4Adependent manner. Mol. Cell 36, 1007-1017.
19. Fukuda T., Yamagata K., Fujiyma S., Matsumoto T., Koshida I., Yoshimura K., Mihara M., Naitou M., Endoh H., Nakamura T., Akimoto C., Yamamoto Y., Katagiri T., Foulds C., Takezawa S., Kitagawa H., Takeyama K., O'Malley B.W. and Kato S. (2007). DEAD-box RNA helicase subunits of the Drosha complex are required for processing of rRNA and a subset of microRNAs. Nature Cell Biol. 9, 604-611.
20. Gareau C., Fournier M.J., Filion C., Coudert L., Martel D., Labelle Y. and Mazroui R. (2011). p21(WAF1/CIP1) upregulation through the stress granule-associated protein CUGBP1 confers resistance to bortezomib-mediated apoptosis. PloS One 6, e20254.
21. Garrott H.M., Walland M.J. and O'Day J. (2004). Recurrent posterior capsular opacification and capsulorhexis contracture after cataract surgery in myotonic dystrophy. Clin. Ex. Ophthal. 32, 653-655.
22. George A., Schneider-Gold C., Zier S., Reiners K. and Sommer C. (2004). Musculoskeletal pain in patients with myotonic dystrophy type 2. Arch. Neurol. 61, 1938-1942.
23. Gerbasi V.R. and Link A.J. (2007). The myotonic dystrophy 2 protein ZNF9 is part of an ITAF complex that promotes cap-independent translation. Mol. Cell. Proteomics 6, 1049-1058.
24. Groh W.J., Groh M.R., Saha C., Kincaid J.C., Simmons Z., Ciafaloni E., Pourmand R., Otten R.F., Bhakta D., Nair G.V., Marashdeh M.M., Zipes D.P. and Pascuzzi R.M. (2008). Electrocardiographic abnormalities and sudden death in myotonic dystrophy type 1. N. Engl. J. Med. 358, 2688-2697.
25. Harper P.S. (2001). Myotonic Dystrophy. 3rd ed. W.B. Saunders Company. London.
26. Huichalaf C., Schoser B., Schneider-Gold C., Jin B., Sarkar P. and Timchenko L. (2009). Reduction the rate of protein translation in patients with Myotonic Dystrophy 2. J. Neurosci., 29, 9042-9049.
27. Huichalaf C., Sakai K., Jin B., Jones K., Wang G.L., Schoser B., Schneider-Gold C., Sarkar P., Pereira-Smith O.M., Timchenko N. and Timchenko L. (2010). Expansion of CUG RNA repeats causes stress and inhibition of translation in Myotonic Dystrophy 1 cells. FASEB J. 24, 3706-3719.
28. Ikezoe K., Nakamori M., Furuya H., Arahata H., Kanemoto S., Kimura T., Imaizumi K., Takahashi M.P., Sakoda S., Fujii N. and Kira J. (2007). Endoplasmic reticulum stress in myotonic dystrophy type 1 muscle. Acta Neuropathol.114, 527-535.
29. Ivanov P., Kedersha N. and Anderson P. (2011). Stress put TIA on TOP. Genes Dev. 25, 2119-2124.
30. Janknecht R. (2010). Multi-talented DEAD-box proteins and potential tumor promoters: p68 RNA helicase (DDX5) and its paralog, p72 RNA helicase (DDX17). Am. J. Trans. Res. 2, 223-234.
31. Kiebler M.A., Hemraj I., Verkade P., Kohrmann M., Fortes P, Marion R.M., Ortin J. and Dotti C.G. (1999). The mammalian staufen protein localizes to the somatodendritic domain of cultured hippocampal neurons: implications for its involvement in mRNA transport. J. Neurosci. 19, 288-297.
32. Kim Y.K., Furic L., DesGrosei llers L. and Maquat L.E. (2005). Mammalian Staufen1 recruits Upf1 to specific mRNA 3' UTRs so as to elicit mRNA decay. Cell 120, 195-208.
33. Kirwan M. and Dokal I. (2008). Dyskeratosis congenita: a genetic disorder of many faces. Clin. Genet. 73, 103-112.
34. Kress C., Gautier-Courteille C., Osborne H.B., Babinet C. and Paillard L. (2007). Inactivation of CUG-BP1/CELF1 causes growth, viability, and spermatogenesis defects in mice. Mol. Cell. Biol. 27, 1146-1157.
35. Kugler J.M. and Lasko P. (2009). Local i zati on, anchori ng and translational control of oskar, gurken, bicoid and nanos mRNA during Drosophila oogenesis. Fly (Austin) 3, 15-28.
36. Kuyumcu-Martinez N.M., Wang G-S. and Cooper T.A. (2007). Increased steady-state levels of CUGBP1 in myotonic dystrophy are due to PKC-mediated hyperphosphorylation. Mol. Cell 28, 68-78.
37. Laurent F.X., Sureau A., Klein A.F., Trouslard F., Gasnier E., Furling D. and Marie J. (2012). New function for the RNA helicase p68/DDX5 as a modifier of MBNL1 activity on expanded CUG repeats. Nucl. Acids Res. 40, 3159-3171.
38. Lee J.E., Lee J.Y., Wilusz J., Tian B. and Wilusz C.J. (2010). Systematic analysis of cis-elements in unstable mRNAs demonstrates that CUGBP1 is a key regulator of mRNA decay in muscle cells. PLoS One 5, e11201.
39. Liquori C.L., Ricker K., Moseley M.L., Jacobsen J.F., Kress W., Naylor S.L., Day J.W. and Ranum L. P. (2001). Myotonic dystrophy 2 is caused by CCTG expansion in intron 1 of ZNF9. Science 293, 864867.
40. Margolis J.M., Schoser B.G., Moseley M.L., Day J.W. and Ranum L.P. (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.
41. Masuda A., Andersen H.S., Doktor T.K., Okamoto T., Ito M., Andresen B.S. and Ohno K. (2012). CUGBP1 and MBNL1 preferentially bind to 3' UTRs and facilitate mRNA decay. Scientific Reports 2, 209-210.
42. Mathieu J., Allard P., Potvin L., Prevost C. and Begin P. (1999). A 10 year study of mortality in a cohort of patients with myotonic dystrophy. Neurology 12, 1658-1662.
43. Meola G., Sansone V., Perani D., Scarone S., Cappa S., Dragoni C., Cattaneo E., Cotelli M., Gobbo C., Fazio F., Siciliano G., Mancuso M., Vitelli E., Zhang S., Krahe R. and Moxley R.T. (2003). Executive dysfunction and avoidant personality trait in myotonic dystrophy type 1 (DM1) and in proximal myotonic myopathy (DM2/PROMM). Neuromuscul. Disord. 13, 813-821.
44. Meyuhas O. (2000). Synthesis of the translational apparatus is regulated at the translational level. Eur. J. Biochem. 267, 6321-6330.
45. Michelotti E.F., Tomonaga T., Krutzsch H. and Levens D. (1995). Cellular nucleic acid binding protein regulates the CT element of the human c-myc protooncogene. J. Biol. Chem. 270, 9494-9499.
46. Milne C.A. and Hodgkin J. (1999). ETR-1, a homologue of a protein linked to myotonic dystrophy, is essential for muscle development in Caenorhabditis elegans. Curr. Biol. 9, 1243-1246.
47. Minnerop M., Weber B., Schoene-Bake J.C., Roeske S., Mirbach S., Anspach C., Schneider-Gold C., Betz R.C., Helmstaedter C., Tittgemeyer M., Klockgether T. and Kornblum C. (2011). The brain in myotonic dystrophy 1 and 2: evidence for a predominant white matter disease. Brain 134, 3530-3546.
48. Moraes K.C., Wilusz C.J. and Wilusz J. (2006). CUG-BP binds to RNA substrates and recruits PARN deadenylase. RNA. 12, 1084-1091.
49. Onishi H., Kino T., Morita T., Futai E., Sasagawa N. and Ishiura S. (2008). MBNL1 associates with YB-1 in cytoplasmic stress granules. J. Neurol. Res. 86, 1994-2002.
50. Paillard L., Omilli F., Legagneux V., Bassez T., Maniey D. and Osborne H.B. (1998). EDEN and EDEN-BP, a cis element and an associated factor that mediate sequence-specific mRNA deadenylation in Xenopus Laevis embryos. EMBO J. 17, 278-287.
51. Pellizzoni L., Lotti F., Maras B. and Pierandrei-Amaldi P. (1997). Cellular nucleic acid binding protein binds a conserved region of the 5' UTR of Xenopus laevis ribosomal protein mRNAs. J. Mol. Biol. 267, 264-275.
52. Philips A.V., Timchenko L.T. and Cooper T.A. (1998). Disruption of splicing of regulated by CUG binding protein in myotonic dystrophy. Science 280, 737-741.
53. Raheem O., Olufemi S.E., Bachinski L.L., Vihola A., Sirito M., Holmlund Hampf J., Haapasalo H., Li Y.P., Udd B. and Krahe R. (2010). Mutant (CCTG)n expansion causes abnormal expression of Zinc Finger protein 9 (ZNF9) in Myotonic Dystrophy type 2. Am. J. Pathol. 177, 3025-3036.
54. Rajavashisth T.B., Taylor A.K., Andalibi A., Svenson K.L. and Lusis A.J. (1989). Identification of a zinc finger protein that binds to the sterol regulatory element. Science 245, 640-643.
55. Ranum L.P. and Cooper T.A. (2006). RNA-mediated neuromuscular disorders. Annu. Rev. Neurosci. 29, 259-277.
56. Rattenbacher B., Beisang D., Wiesner D.L., Jeschke J.C., von Hohenberg M., St Louis-Vlasova I.A. and Bohjanen P.R. (2010). Analysis of CUGBP1 targets identifies GU-repeat sequences that mediate rapid mRNA decay. Mol. Cell. Biol. 30, 3970-3980.
57. Ravel-Chapuis A., Belanger G., Yadava R.S., Mahadevan M.S., DesGroseillers L., Cote J. and Jasmin B.J. (2012). The RNA-binding protein Staufen1 is increased in DM1 skeletal muscle and promotes alternative pre-mRNA splicing. J. Cell Biol. 19, 699-712.
58. Salisbury E., Sakai K., Schoser B., Huichalaf C., Schneider-Gold C., Nguyen H., Wang G.L., Albrecht J.H. and Timchenko L.T. (2008). Ectopic expression of cyclin D3 corrects differentiation of DM1 myobl asts through acti vati on of RNA CUG-bi ndi ng protei n, CUGBP1. Exp. Cell Res. 314, 2266-2278.
59. Salisbury E., Schoser B., Schneider-Gold C., Wang G.L., Huichalaf C., Jin B., Sirito M., Sarkar P., Krahe R., Timchenko N.A. and Timchenko L.T. (2009). Expressi on of RNA CCUG repeats dysregulates translation and degradation of proteins in DM2 patients. Am. J. Pathol. 175, 748-762.
60. Sammons M.A., Antons A.K., Bendjennat M., Udd B., Krahe R. and Link A.J. (2010). ZNF9 activation of IRES-mediated translation of the human ODC mRNA is decreased in Myotonic Dystrophy type 2. PloS One 5, e09301.
61. Sammons M.A., Samir P. and Link A.J. (2011). Saccharomyces cerevisiae Gis2 interacts with the translation machinery and is orthogonal to myotonic dystrophy type 2 protein ZNF9. Biochem. Biophys. Res. Commun. 406, 13-19.
62. Savkur R.S., Philips A.V. and Cooper T.A. (2001). Aberrant regulation of insulin receptor alternative splicing is associated with insulin resistance in myotonic dystrophy. Nat. Genet. 29, 40-47.
63. Scherrer T., Femmer C., Schiess R., Aebersold R. and Gerber A.P. (2011). Defining potentially conserved RNA regulons of homologous zinc-finger RNA-binding proteins. Genome Biol. 12, R3.
64. Schoser B. and Timchenko L. (2010). Myotonic dystrophies 1 and 2: complex diseases with complex mechanisms. Current Genomics 11, 77-90.
65. Tian B., White R.J., Xia T., Welle S., Turner D.H., Mathews M.B. and Thornton C.A. (2000). Expanded CUG repeat RNAs form hairpins that activate the double-stranded RNA-dependent protein kinase PKR. RNA 6, 79-87.
66. 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. Nucl. Acids Res. 24, 4407-4414.
67. Timchenko N.A., Welm A. L., Lu X. and Timchenko L.T. (1999). CUG repeat binding protein (CUGBP1) interacts with the 5' region of C/EBP beta mRNA and regulates translation of C/EBPbeta isoforms. Nucl. Acids Res. 27, 4517-4525.
68. Timchenko N.A., Cai Z. J., Welm A.L., Reddy S., Ashizawa T. and Timchenko L.T. (2001a). RNA CUG repeats sequester CUGBP1 and alter protein levels and activity of CUGBP1. J. Biol. Chem. 276, 7820-7826.
69. Timchenko N.A., Iakova P., Cai Z.J., Smith J.R. and Timchenko L.T. (2001b). Molecular basis for impaired muscle differentiation in myotonic dystrophy. Mol. Cell. Biol. 21, 6927-6938.
70. Timchenko N.A., Patel R., Iakova P., Cai Z.J., Quan L. and Timchenko L.T. (2004). Overexpression of CUG triplet repeat-binding protein, CUGBP1, in mice inhibits myogenesis. J. Biol. Chem. 279, 13129-13139.
71. Timchenko N.A., Wang G.L. and Timchenko L.T. (2005). RNA CUGbinding protein 1 increases translation of 20-kDa isoform of CCAAT/Enhancer-binding protein beta by interacting with the alpha and beta subunits of eukaryotic initiation translation factor 2. J. Biol. Chem. 280, 20549-20557.
72. Timchenko L.T., Salisbury E., Wang G.L., Nguyen H., Albrecht J.H., Hershey J.W. and Timchenko N.A. (2006). Age-specific CUGBP1eIF2 complex increases translation of CCAAT/Enhancer-binding protein beta in old liver. J. Biol. Chem. 281, 32806-32819.
73. Udd B., Meola G., Krahe R., Wansink D.G., Bassez G., Kress W., Schoser B. and Moxley R. (2011). Myotonic dystrophy type 2 (DM2) and related disorders: report of the 180th ENMC workshop including guidelines on diagnostics and management 3-5 December 2010, Naarden, The Netherlands. Neuromuscul. Disord. 21, 443-450.
74. Vlasova I.A., Tahoe N.M., Fan D., Larsson O., Rattenbacher B., Sternjohn J.R., Vasdewani J., Karypis G., Reilly C.S., Bitterman P.B. and Bohjanen P.R. (2008). Conserved GU-rich elements mediate mRNA decay by binding to CUG-binding protein 1. Mol. Cell 29, 263-270.
75. Wang G. L., Salisbury E., Shi X., Timchenko L., Medrano E.E. and Timchenko N.A. (2008). HDAC1 promotes liver proliferation in young mice via interactions with C/EBPbeta. J. Biol. Chem. 283, 26179-26187.
76. Wang H., Gao X., Huang Y., Yang J. and Liu Z.R. (2009). P68 RNA helicase is a nucleocytoplasmic shuttling protein. Cell Res. 19, 1388-1400.
77. Warden C.H., Krisans S.K., Purcell-Huynh D., Leete L.M., Daluiski A., Diep A., Taylor B.A. and Lusis A.J. (1994). Mouse cellular nucleic acid binding proteins: a highly conserved family identified by genetic mapping and sequencing. Genomics 24, 14-19.
78. Woeller C.F., Fox J.T., Perry C. and Stover P.J. (2007). A ferritinresponsive internal ribosome entry site regulates folate metabolism. J. Biol. Chem. 282, 29927-29935.
79. Xiao L., Cui Y.H., Rao J.N., Zou T., Liu L., Smith A., Turner D.J., Gorospe M. and Wang J.Y. (2011). Regulation of cyclin-dependent kinase 4 translation through CUG-binding protein 1 and microRNA222 by polyamines. Mol. Cell. Biol. 22, 3055-3069.
80. Yasuda J., Mashiyama S., Makino R., Ohyama S., Sekiya T. and Hayashi K. (1995). Cloning and characterization of rat cellular nucleic acid binding protein (CNBP) cDNA. DNA Res. 2, 4549.
81. Zhang L., Lee J.E., Wilusz J. and Wilusz C.J. (2008). The RNA-binding protein CUGBP1 regulates stability of tumor necrosis factor mRNA in muscle cells: implications for myotonic dystrophy. J. Biol. Chem. 283, 22457-22463.
82. Zheng Y. and Miskimins W.K. (2011). CUG-binding protein represses translation of p27Kip1 mRNA through its internal ribosomal entry site. RNA Biol. 8, 365-371.