The utrophin A 5′-UTR drives cap-independent translation exclusively in skeletal muscles of transgenic mice and interacts with eEF1A2

Human Molecular Genetics

Volumn 19, Issue 7, 2010, Pages 1211-1220

  Miura, P ^a   Coriati, A ^a   Belanger G ^a   de Repentigny, Y ^b   Lee, J ^a   Kothary, R ^a,b   Holcik, M ^a,c   Jasmin, B J ^a,b  

^a UNIVERSITY OF OTTAWA   (Canada)

^b OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^c CHILDREN S HOSPITAL OF EASTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR 1; ELONGATION FACTOR 1A2; UNCLASSIFIED DRUG; UTROPHIN; UTROPHIN A; EEF1A2 PROTEIN, HUMAN; UTRN PROTEIN, MOUSE;

5' UNTRANSLATED REGION; AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CROSS LINKING; INTERNAL RIBOSOME ENTRY SITE; MASS SPECTROMETRY; MOUSE; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; RAT; REPORTER GENE; RNA TRANSLATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TISSUE SPECIFICITY; TRANSGENIC MOUSE; ANIMAL; ANTIBODY SPECIFICITY; BINDING SITE; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROTEIN SYNTHESIS; RIBOSOME;

ANIMALIA; EUKARYOTA; MUS MUSCULUS;

5' UNTRANSLATED REGIONS; ANIMALS; BINDING SITES; CELLS, CULTURED; GENE EXPRESSION REGULATION; GENES, REPORTER; MICE; MICE, TRANSGENIC; MUSCLE, SKELETAL; ORGAN SPECIFICITY; PEPTIDE ELONGATION FACTOR 1; PROTEIN BIOSYNTHESIS; RIBOSOMES; UTROPHIN;

EID: 77952494292     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp591     Document Type: Article

References (52)

1. Blake, D.J., Weir, A., Newey, S.E. and Davies, K.E. (2002) Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol. Rev., 82, 291-329.
2. Tinsley, J.M., Potter, A.C., Phelps, S.R., Fisher, R., Trickett, J.I. and Davies, K.E. (1996) Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature, 384, 349-353.
3. Cerletti, M., Negri, T., Cozzi, F., Colpo, R., Andreetta, F., Croci, D., Davies, K.E., Cornelio, F., Pozza, O., Karpati, G. et al. (2003) Dystrophic phenotype of canine X-linked muscular dystrophy is mitigated by adenovirus-mediated utrophin gene transfer. Gene Ther., 10, 750-757.
4. Chakkalakal, J.V., Harrison, M.A., Carbonetto, S., Chin, E., Michel, R.N. and Jasmin, B.J. (2004) Stimulation of calcineurin signaling attenuates the dystrophic pathology in mdx mice. Hum. Mol. Genet., 13, 379-388.
5. Sonnemann, K.J., Heun-Johnson, H., Turner, A.J., Baltgalvis, K.A., Lowe, D.A. and Ervasti, J.M. (2009) Functional substitution by TAT-utrophin in dystrophin-deficient mice. PLoS Med., 6, e1000083.
6. Weir, A.P., Burton, E.A., Harrod, G. and Davies, K.E. (2002) A-and B-utrophin have different expression patterns and are differentially up-regulated in mdx muscle. J. Biol. Chem., 277, 45285-45290.
7. Baby, S.M., Bogdanovich, S., Willmann, G., Basu, U., Lozynska, O. and Khurana, T.S. (2009) Differential expression of utrophin-A and -B promoters in the central nervous system (CNS) of normal and dystrophic mdx mice. Brain Pathol., Epub ahead of print May 22.
8. Chakkalakal, J.V., Miura, P., Belanger, G., Michel, R.N. and Jasmin, B.J. (2008) Modulation of utrophin A mRNA stability in fast versus slow muscles via an AU-rich element and calcineurin signaling. Nucleic Acids Res., 36, 826-838.
9. Chakkalakal, J.V., Stocksley, M.A., Harrison, M.A., Angus, L.M., Deschenes-Furry, J., St-Pierre, S., Megeney, L.A., Chin, E.R., Michel, R.N. and Jasmin, B.J. (2003) Expression of utrophin A mRNA correlates with the oxidative capacity of skeletal muscle fiber types and is regulated by calcineurin/NFAT signaling. Proc. Natl. Acad. Sci. USA, 100, 7791-7796.
10. Gramolini, A.O., Karpati, G. and Jasmin, B.J. (1999) Discordant expression of utrophin and its transcript in human and mouse skeletal muscles. J. Neuropathol. Exp. Neurol., 58, 235-244.
11. Miura, P., Thompson, J., Chakkalakal, J.V., Holcik, M. and Jasmin, B.J. (2005) The utrophin A 5'-untranslated region confers internal ribosome entry site-mediated translational control during regeneration of skeletal muscle fibers. J. Biol. Chem., 280, 32997-33005.
12. Baird, S.D., Turcotte, M., Korneluk, R.G. and Holcik, M. (2006) Searching for IRES. RNA, 12, 1755-1785.
13. Spriggs, K.A., Stoneley, M., Bushell, M. and Willis, A.E. (2008) Re-programming of translation following cell stress allows IRES-mediated translation to predominate. Biol. Cell, 100, 27-38.
14. Miura, P., Andrews, M., Holcik, M. and Jasmin, B.J. (2008) IRES-mediated translation of utrophin A is enhanced by glucocorticoid treatment in skeletal muscle cells. PLoS ONE, 3, e2309.
15. Creancier, L., Morello, D., Mercier, P. and Prats, A.C. (2000) Fibroblast growth factor 2 internal ribosome entry site (IRES) activity ex vivo and in transgenic mice reveals a stringent tissue-specific regulation. J. Cell. Biol., 150, 275-281.
16. Miura, P. and Jasmin, B.J. (2006) Utrophin upregulation for treating Duchenne or Becker muscular dystrophy: how close are we? Trends Mol. Med., 12, 122-129.
17. Kim, J.H., Paek, K.Y., Ha, S.H., Cho, S., Choi, K., Kim, C.S., Ryu, S.H. and Jang, S.K. (2004) A cellular RNA-binding protein enhances internal ribosomal entry site-dependent translation through an interaction downstream of the hepatitis C virus polyprotein initiation codon. Mol. Cell. Biol., 24, 7878-7890.
18. Lewis, S.M., Veyrier, A., Hosszu Ungureanu, N., Bonnal, S., Vagner, S. and Holcik, M. (2007) Subcellular relocalization of a trans-acting factor regulates XIAP IRES-dependent translation. Mol. Biol. Cell, 18, 1302-1311.
19. Amiri, A., Noei, F., Jeganathan, S., Kulkarni, G., Pinke, D.E. and Lee, J.M. (2007) eEF1A2 activates Akt and stimulates Akt-dependent actin remodeling, invasion and migration. Oncogene, 26, 3027-3040.
20. Lee, S., Francoeur, A.M., Liu, S. and Wang, E. (1992) Tissue-specific expression in mammalian brain, heart, and muscle of S1, a member of the elongation factor-1 alpha gene family. J. Biol. Chem., 267, 24064-24068.
21. Chambers, D.M., Peters, J. and Abbott, C.M. (1998) The lethal mutation of the mouse wasted (wst) is a deletion that abolishes expression of a tissue-specific isoform of translation elongation factor 1alpha, encoded by the Eef1a2 gene. Proc. Natl. Acad. Sci. USA, 95, 4463-4468.
22. Matsumura, K., Ervasti, J.M., Ohlendieck, K., Kahl, S.D. and Campbell, K.P. (1992) Association of dystrophin-related protein with dystrophin-associated proteins in mdx mouse muscle. Nature, 360, 588-591.
23. Stocksley, M.A., Chakkalakal, J.V., Bradford, A., Miura, P., De Repentigny, Y., Kothary, R. and Jasmin, B.J. (2005) A 1.3 kb promoter fragment confers spatial and temporal expression of utrophin A mRNA in mouse skeletal muscle fibers. Neuromuscul. Disord., 15, 437-449.
24. Takahashi, J., Itoh, Y., Fujimori, K., Imamura, M., Wakayama, Y., Miyagoe-Suzuki, Y. and Takeda, S. (2005) The utrophin promoter A drives high expression of the transgenic LacZ gene in liver, testis, colon, submandibular gland, and small intestine. J. Gene Med., 7, 237-248.
25. Tanihata, J., Suzuki, N., Miyagoe-Suzuki, Y., Imaizumi, K. and Takeda, S. (2008) Downstream utrophin enhancer is required for expression of utrophin in skeletal muscle. J Gene Med., 10, 702-713.
26. Ye, X., Fong, P., Iizuka, N., Choate, D. and Cavener, D.R. (1997) Ultrabithorax and Antennapedia 5′ untranslated regions promote developmentally regulated internal translation initiation. Mol. Cell. Biol., 17, 1714-1721.
27. Creancier, L., Mercier, P., Prats, A.C. and Morello, D. (2001) c-myc Internal ribosome entry site activity is developmentally controlled and subjected to a strong translational repression in adult transgenic mice. Mol. Cell. Biol., 21, 1833-1840.
28. Teshima-Kondo, S., Kondo, K., Prado-Lourenco, L., Gonzalez-Herrera, I.G., Rokutan, K., Bayard, F., Arnal, J.F. and Prats, A.C. (2004) Hyperglycemia upregulates translation of the fibroblast growth factor 2 mRNA in mouse aorta via internal ribosome entry site. FASEB J., 18, 1583-1585.
29. Gonzalez-Herrera, I.G., Prado-Lourenco, L., Pileur, F., Conte, C., Morin, A., Cabon, F., Prats, H., Vagner, S., Bayard, F., Audigier, S. et al. (2006) Testosterone regulates FGF-2 expression during testis maturation by an IRES-dependent translational mechanism. FASEB J., 20, 476-478.
30. Audigier, S., Guiramand, J., Prado-Lourenco, L., Conte, C., Gonzalez-Herrera, I.G., Cohen-Solal, C., Recasens, M. and Prats, A.C. (2008) Potent activation of FGF-2 IRES-dependent mechanism of translation during brain development. RNA, 14, 1852-1864.
31. Bonnal, S., Pileur, F., Orsini, C., Parker, F., Pujol, F., Prats, A.C. and Vagner, S. (2005) Heterogeneous nuclear ribonucleoprotein A1 is a novel internal ribosome entry site trans-acting factor that modulates alternative initiation of translation of the fibroblast growth factor 2 mRNA. J. Biol. Chem., 280, 4144-4153.
32. Kahns, S., Lund, A., Kristensen, P., Knudsen, C.R., Clark, B.F., Cavallius, J. and Merrick, W.C. (1998) The elongation factor 1 A-2 isoform from rabbit: cloning of the cDNA and characterization of the protein. Nucleic Acids Res., 26, 1884-1890.
33. Ejiri, S. (2002) Moonlighting functions of polypeptide elongation factor 1: from actin bundling to zinc finger protein R1-associated nuclear localization. Biosci. Biotechnol. Biochem., 66, 1-21.
34. Gross, S.R. and Kinzy, T.G. (2005) Translation elongation factor 1A is essential for regulation of the actin cytoskeleton and cell morphology. Nat. Struct. Mol. Biol., 12, 772-778.
35. Khacho, M., Mekhail, K., Pilon-Larose, K., Pause, A., Cote, J. and Lee, S. (2008) eEF1A is a novel component of the mammalian nuclear protein export machinery. Mol. Biol. Cell, 19, 5296-5308.
36. Yan, G., You, B., Chen, S.P., Liao, J.K. and Sun, J. (2008) Tumor necrosis factor-alpha downregulates endothelial nitric oxide synthase mRNA stability via translation elongation factor 1-alpha 1. Circ. Res., 103, 591-597.
37. Zhang, J., Guo, H., Mi, Z., Gao, C., Bhattacharya, S., Li, J. and Kuo, P.C. (2009) EF1A1-actin interactions alter mRNA stability to determine differential osteopontin expression in HepG2 and Hep3B cells. Exp. Cell Res., 315, 304-312.
38. Ruest, L.B., Marcotte, R. and Wang, E. (2002) Peptide elongation factor eEF1A-2/S1 expression in cultured differentiated myotubes and its protective effect against caspase-3-mediated apoptosis. J. Biol. Chem., 277, 5418-5425.
39. Chang, R. and Wang, E. (2007) Mouse translation elongation factor eEF1A-2 interacts with Prdx-I to protect cells against apoptotic death induced by oxidative stress. J. Cell. Biochem., 100, 267-278.
40. Jeganathan, S., Morrow, A., Amiri, A. and Lee, J.M. (2008) Eukaryotic elongation factor 1A2 cooperates with phosphatidylinositol-4 kinase III beta to stimulate production of filopodia through increased phosphatidylinositol-4,5 bisphosphate generation. Mol. Cell. Biol., 28, 4549-4561.
41. Knudsen, S.M., Frydenberg, J., Clark, B.F. and Leffers, H. (1993) Tissue-dependent variation in the expression of elongation factor-1 alpha isoforms: isolation and characterisation of a cDNA encoding a novel variant of human elongation-factor 1 alpha. Eur. J. Biochem., 215, 549-554.
42. Newbery, H.J., Loh, D.H., O'Donoghue, J.E., Tomlinson, V.A., Chau, Y.Y., Boyd, J.A., Bergmann, J.H., Brownstein, D. and Abbott, C.M. (2007) Translation elongation factor eEF1A2 is essential for post-weaning survival in mice. J. Biol. Chem., 282, 28951-28959.
43. Mansilla, F., Dominguez, C.A., Yeadon, J.E., Corydon, T.J., Burden, S.J. and Knudsen, C.R. (2008) Translation elongation factor eEF1A binds to a novel myosin binding protein-C-like protein. J. Cell. Biochem., 105, 847-858.
44. Khalyfa, A., Carlson, B.M., Carlson, J.A. and Wang, E. (1999) Toxin injury-dependent switched expression between EF-1 alpha and its sister, S1, in rat skeletal muscle. Dev. Dyn., 216, 267-273.
45. Lyons, A.J. and Robertson, H.D. (2003) Detection of tRNA-like structure through RNase P cleavage of viral internal ribosome entry site RNAs near the AUG start triplet. J. Biol. Chem., 278, 26844-26850.
46. Wilson, J.E., Pestova, T.V., Hellen, C.U. and Sarnow, P. (2000) Initiation of protein synthesis from the A site of the ribosome. Cell, 102, 511-520.
47. Pestova, T.V. and Hellen, C.U. (2003) Translation elongation after assembly of ribosomes on the Cricket paralysis virus internal ribosomal entry site without initiation factors or initiator tRNA. Genes Dev., 17, 181-186.
48. Lancaster, A.M., Jan, E. and Sarnow, P. (2006) Initiation factor-independent translation mediated by the hepatitis C virus internal ribosome entry site. RNA, 12, 894-902.
49. Ma, X., Idle, J.R., Malfatti, M.A., Krausz, K.W., Nebert, D.W., Chen, C.S., Felton, J.S., Waxman, D.J. and Gonzalez, F.J. (2007) Mouse lung CYP1A1 catalyzes the metabolic activation of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP). Carcinogenesis, 28, 732-737.
50. Kim, J., Namkung, W., Yoon, J.S., Jo, M.J., Lee, S.H., Kim, K.H., Kim, J.Y. and Lee, M.G. (2009) The role of translation elongation factor eEF1A in intracellular alkalinization-induced tumor cell growth. Lab. Invest., 89, 867-874.
51. Sela-Brown, A., Silver, J., Brewer, G. and Naveh-Many, T. (2000) Identification of AUF1 as a parathyroid hormone mRNA 3'-untranslated region-binding protein that determines parathyroid hormone mRNA stability. J. Biol. Chem., 275, 7424-7429.
52. Kulkarni, G., Turbin, D.A., Amiri, A., Jeganathan, S., Andrade-Navarro, M.A., Wu, T.D., Huntsman, D.G. and Lee, J.M. (2007) Expression of protein elongation factor eEF1A2 predicts favorable outcome in breast cancer. Breast Cancer Res. Treat., 102, 31-41.