Role of HuR in skeletal myogenesis through coordinate regulation of muscle differentiation genes

Molecular and Cellular Biology

Volumn 23, Issue 14, 2003, Pages 4991-5004

  Figueroa, Angélica ^a   Cuadrado, Ana ^a   Fan, Jinshui ^c   Atasoy, Ulus ^d   Muscat, George E ^e   Muñoz Canoves, Pura ^b   Gorospe, Myriam ^c   Muñoz, Alberto ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MYOD PROTEIN; MYOGENIC FACTOR; MYOGENIN; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; GENE EXPRESSION REGULATION; GENETIC REGULATION; HALF LIFE TIME; MORPHOGENESIS; MOUSE; MUSCLE DEVELOPMENT; MUSCLE FUNCTION; MUSCLE REGENERATION; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTO ONCOGENE; SKELETAL MUSCLE; TARGET CELL; TRANSCRIPTION REGULATION;

3' UNTRANSLATED REGIONS; ANIMALS; ANTIGENS, SURFACE; BASE SEQUENCE; CELL DIFFERENTIATION; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; CYTOPLASM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HALF-LIFE; INSULIN; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MYOBLASTS; MYOD PROTEIN; MYOGENIN; REGENERATION; RNA, MESSENGER; RNA-BINDING PROTEINS; SELENIUM; TRANSFERRIN;

ANIMALIA;

EID: 0038450334     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.14.4991-5004.2003     Document Type: Article

References (43)

1. Akamatsu, W., et al. 1999. Mammalian ELAV-Iike neuronal RNA-binding proteins HuB and HuC promote neuronal development in both the central and the peripheral nervous systems. Proc. Natl. Acad. Sci. USA 96:9885-9890.
2. Antic, D., and J. D. Keene. 1997. Embryonic lethal abnormal visual RNA-binding proteins involved in growth, differentiation and posttranscriptional gene expression. Am. J. Hum. Genet. 61:273-278.
3. Antic, D., N. Lu, and J. D. Keene. 1999. ELAV tumor antigen, Hel-N1, increases translation of neurofilament M mRNA and induces formation of neurites in human teratocarcinoma cells. Genes Dev. 13:449-461.
4. Atasoy, U., J. Watson, D. Patel, and J. D. Keene. 1998. ELAV protein HuA (HuR) can redistribute between nucleus and cytoplasm and is upregulated during serum stimulation and T cell activation. J. Cell Sci. 111:3145-3156.
5. Beckel-Mitchener, A. C., A. Miera, R. Keller, and N. I. Perrone-Bizzozero. 2002. Poly(A) tail length-dependent stabilization of GAP-43 mRNA by the RNA-binding protein HuD. J. Biol. Chem. 277:27996-28002.
6. Blattner, C., P. Kannouche, M. Litfin, K. Bender, H. J. Rahmsdorf, J. F. Angulo, and P. Herrlich. 2000. UV-induced stabilization of c-fos and other short-lived mRNAs. Mol. Cell. Biol. 20:3616-3625.
7. Brennan, C. M., and J. A. Steitz. 2001. HuR and mRNA stability. Cell. Mol. Life Sci. 58:266-277.
8. Brennan, C. M., I. E. Gallouzi, and J. A. Steitz. 2000. Protein ligands to HuR modulate its interaction with target mRNAs in vivo. J. Cell Biol. 151:1-14.
9. Campos, A. R., D. Grossman, and K. White. 1985. Mutant alleles at the locus elav in Drosophila melanogaster lead to nervous system defects. A developmental-genetic analysis. J. Neurogenet. 2:197-218.
10. Cooper, R. N., S. Tajbakhsh, V. Mouly, G. Cossu, M. Buckingham, and G. S. Butler-Browne. 1999. In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. J. Cell Sci. 112:2895-2901.
11. Chen, C. Y., and A.-B. Shyu. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20:465-470.
12. Dominov, J. A., J. D. Dunn, and J. B. Miller. 1998. Bcl-2 expression identifies an early stage of myogenesis and promotes clonal expansion of muscle cells. J. Cell Biol. 142:537-544.
13. Fan, J., X. Yang, W. Wang, W. H. Wood III, K. G. Becker, and M. Gorospe. 2002. Global analysis of stress-regulated mRNA turnover using cDNA arrays. Proc. Natl. Acad. Sci. USA 99:10611-10616.
14. Fan, X. C., and J. A. Steitz. 1998. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17:3448-3460.
15. Fan, X. C., and J. A. Steitz. 1998. HNS, a nuclear-cytoplasmic shuttling sequence in HuR. Proc. Natl. Acad. Sci. USA 95:15293-15298.
16. Fuchtbauer, E. M., and H. Westphal. 1992. MyoD and Myogenin are coexpressed in regenerating skeletal muscle of the mouse. Dev. Dynam. 193:34-39.
17. Waf1 expression by UV light is mediated through mRNA stabilization and involves a vanadate-sensitive regulatory system. Mol. Cel. Biol. 18:1400-1407.
18. Jackman, J., I. Alamo, Jr., and A. J. Fornace, Jr. 1994. Genotoxic stress confers preferential and coordinate messenger RNA stability on the five gadd genes. Cancer Res. 54:5656-5662.
19. Jain, R. G., L. G. Andrews, K. M. McGowan, P. H. Pekala, and J. D. Keene. 1997. Ectopic expression of Hel-N1, an RNA-binding protein, increases glucose transporter (GLUT1) expression in 3T3-L1 adipocytes. Mol. Cell. Biol. 17:954-962.
20. waf1 mRNA contains a conserved element in its 3′-untranslated region that is bound by the Elav-like mRNA-stabilizing proteins. J. Biol. Chem. 273:20511-20516.
21. Kasashima, K., K. Terashima, K. Yamamoto, E. Sakashita, and H. Sakamoto. 1999. Cytoplasmic localization is required for the mammalian ELAV-like protein HuD to induce neuronal differentiation. Genes Cells 4:667-683.
22. Keene, J. D. 1999. Why is Hu where? Shuttling of early-response-gene messenger RNA subsets. Proc. Natl. Acad. Sci. USA 96:5-7.
23. Keene, J. D., and S. A. Tenenbaum. 2002. Eukaryotic mRNPs may represent posttranscriptional operons. Mol. Cell 9:1161-1167.
24. Loflin, P., C. Y. Chen, and A.-B. Shyu. 1999. Unraveling a cytoplasmic role for hnRNP D in the in vivo mRNA destabilization directed by the AU-rich element. Genes Dev. 13:1884-1897.
25. Ma, W. J., S. Chung, and H. Furneaux. 1997. The Elav-like proteins bind to AU-rich elements and to the poly(A) tail of mRNA. Nucleic Acids Res. 25:3564-3569.
26. Megeney, L. A., B. Kablar, K. Garrett, J. E. Anderson, and M. A. Rudnicki. 1996. MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes Dev. 10:1173-1183.
27. Molkentin, J., and E. N. Olson. 1996. Defining the regulatory networks for muscle development. Curr. Opin. Gen. Dev. 6:445-453.
28. Muscat, G. E., and U. Dressel. 2000. Not a minute to waste. Nat. Med. 6:1216-1217.
29. Olson, E. N. 1992. Interplay between proliferation and differentiation within the myogenic lineage. Dev. Biol. 154:261-272.
30. Peng, S. S., C. Y. Chen, N. Xu, and A.-B. Shyu. 1998. RNA stabilization by the AU-rich element binding protein HuR, an ELAV protein. EMBO J. 17:3461-3470.
31. Ross, J. 1995. mRNA stability in mammalian cells. Microbiol. Rev. 59:423-450.
32. Sachs, A.-B. 1993. Messenger RNA degradation in eukaryotes. Cell 74:413-421.
33. Tenenbaum, S. A., C. C. Carson, P. J. Lager, and J. D. Keene. 2000. Identifying mRNA subsets in messenger ribonucleoprotein complexes by using cDNA arrays. Proc. Natl. Acad. Sci. USA 97:14085-14090.
34. Tenenbaum, S. A., P. J. Lager, C. C. Carson, and J. D. Keene. 2002. Ribonomics: identifying mRNA subsets in mRNP complexes using antibodies to RNA-binding proteins and genomic arrays. Methods 26:191-198.
35. Walsh, K. 1997. Coordinate regulation of cell cycle and apoptosis during myogenesis. Prog. Cell Cycle Res. 3:53-58.
36. Wang, J., and K. Walsh. 1996. Resistance to apoptosis conferred by Cdk inhibitors during myocyte differentiation. Science 273:359-361.
37. Wang, W., H. Furneaux, H. Cheng, M. C. Caldwell, D. Hutter, Y. Liu, N. J. Holbrook, and M. Gorospe. 2000. HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol. 20:760-769.
38. Wang, W., S. Lin, M. C. Caldwell, H. Furneaux, and M. Gorospe. 2000. HuR regulates cyclin A and cyclin B1 mRNA stability during the cell division cycle. EMBO J. 19:2340-2350.
39. Wang, W., X. Yang, V. J. Cristofalo, N. J. Holbrook, and M. Gorospe. 2001. Loss of HuR is linked to reduced expression of proliferative genes during replicative senescence. Mol. Cell. Biol. 21:5889-5898.
40. Wang, W., J. Fan, X. Yang, S. Fürer, I. Lopez de Silanes, C. von Kobbe, J. Guo, S. N. Georas, F. Foufelle, D. G. Hardie, D. Carling, and M. Gorospe. 2002. AMP-activated kinase regulates cytoplasmic HuR. Mol. Cell. Biol. 22:3425-3436.
41. Wisdom, R. 1999. AP-1: one switch for many signals. Exp. Cell Res. 253: 180-185.
42. Xu, N., C. Y. Chen, and A.-B. Shyu. 1997. Modulation of the fate of cytoplasmic mRNA by AU-rich elements: key sequence features controlling mRNA deadenylation and decay. Mol. Cell. Biol. 17:4611-4621.
43. Zhang, W., B. J. Wagner, K. Ehrenman, A. W. Schaefer, C. T. DeMaria, D. Crater, K. DeHaven, L. Long, and G. Brewer. 1993. Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1. Mol. Cell. Biol. 13:7652-7665.