Akt2-mediated phosphorylation of Pitx2 controls Ccnd1 mRNA decay during muscle cell differentiation

Cell Death and Differentiation

Volumn 17, Issue 6, 2010, Pages 975-983

  Gherzi, R ^a   Trabucchi, M ^b   Ponassi, M ^a   Gallouzi, I E ^c   Rosenfeld, M G ^b   Briata, P ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Akt2; HuR; mRNA decay; Myoblasts; Pitx2

Indexed keywords

CYCLIN D1; HUR PROTEIN; MESSENGER RNA; PROTEIN KINASE B BETA; RIBONUCLEOPROTEIN; TRANSCRIPTION FACTOR PITX2;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; COMPLEX FORMATION; CONTROLLED STUDY; MOUSE; MUSCLE CELL; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RNA STABILITY;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CYCLIN D1; HOMEODOMAIN PROTEINS; MICE; MUSCLE FIBERS, SKELETAL; MUSCLES; MYOBLASTS, SKELETAL; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RNA INTERFERENCE; RNA STABILITY; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EID: 77952237641     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2009.194     Document Type: Article

References (40)

1. Semina EV, Reiter R, Leysens NJ, Alward WL, Small KW, Datson NA et al. Cloning and characterization of a novel bicoid-related homeobox transcription factor gene, RIEG, involved in Rieger syndrome. Nat Genet 1996; 14: 392-399.
2. Gage PJ, Suh H, Camper SA. Dosage requirement of Pitx2 for development of multiple organs. Development 1999; 126: 4643-4651.
3. Kitamura K, Miura H, Miyagawa-Tomita S, Yanazawa M, Katoh-Fukui Y, Suzuki R et al. Mouse Pitx2 deficiency leads to anomalies of the ventral body wall, heart, extra-and periocular mesoderm and right pulmonary isomerism. Development 1999; 126: 5749-5758.
4. Lin CR, Kioussi C, O'Connell S, Briata P, Szeto D, Liu F et al. Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature 1999; 401: 279-282.
5. Lu MF, Pressman C, Dyer R, Johnson RL, Martin JF. Function of Rieger syndrome gene in left-right asymmetry and craniofacial development. Nature 1999; 401: 276-278.
6. Kioussi C, Briata P, Baek SH, Rose DW, Hamblet NS, Herman T et al. Identification of a Wnt/Dvl/beta-Catenin-Pitx2 pathway mediating cell-type-specific proliferation during development. Cell 2002; 111: 673-685.
7. L'Honoré A, Coulon V, Marcil A, Lebel M, Lafrance-Vanasse J, Gage P et al. Sequential expression and redundancy of Pitx2 and Pitx3 genes during muscle development. Dev Biol 2007; 307: 421-433.
8. Dong F, Sun X, Liu W, Ai D, Klysik E, Lu MF et al. Pitx2 promotes development of splanchnic mesoderm-derived branchiomeric muscle. Development 2006; 133: 4891-4899.
9. Shih HP, Gross MK, Kioussi C. Cranial muscle defects of Pitx2 mutants result from specification defects in the first branchial arch. Proc Natl Acad Sci USA 2007; 104: 5907-5912.
10. Yoshioka H, Meno C, Koshiba K, Sugihara M, Itoh H, Ishimaru Y et al. Pitx2, a bicoid-type homeobox gene, is involved in a lefty-signaling pathway in determination of left-right asymmetry. Cell 1998; 94: 299-305.
11. Logan M, Pagán-Westphal SM, Smith DM, Paganessi L, Tabin CJ. The transcription factor Pitx2 mediates situs-specific morphogenesis in response to left-right asymmetric signals. Cell 1998; 94: 307-317.
12. Piedra ME, Icardo JM, Albajar M, Rodriguez-Rey JC, Ros MA. Pitx2 participates in the late phase of the pathway controlling left-right asymmetry. Cell 1998; 94: 319-324.
13. Ryan AK, Blumberg B, Rodriguez-Esteban C, Yonei-Tamura S, Tamura K, Tsukui T et al. Pitx2 determines left-right asymmetry of internal organs in vertebrates. Nature 1998; 394: 545-551.
14. Briata P, Ilengo C, Corte G, Moroni C, Rosenfeld MG, Chen CY et al. The Wnt/beta-catenin-Pitx2 pathway controls the turnover of Pitx2 and other unstable mRNAs. Mol Cell 2003; 12: 1201-1211.
15. Hao S, Baltimore D. The stability of mRNA influences the temporal order of the induction of genes encoding inflammatory molecules. Nat Immunol 2009; 10: 281-288.
16. Wilusz CJ, Wilusz J. Bringing the role of mRNA decay in the control of gene expression into focus. Trends Genet 2004; 20: 491-497.
17. Houseley J, Tollervey D. The many pathways of RNA degradation. Cell 2009; 136: 763-776.
18. Yun K, Wold B. Skeletal muscle determination and differentiation: story of a core regulatorynetwork and its context. Curr Opin Cell Biol 1996; 8: 877-889.
19. Chargé SB, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev 2004; 84: 209-238.
20. Buckingham M. Myogenic progenitor cells and skeletal myogenesis in vertebrates. Curr Opin Genet Dev 2006; 16: 525-532.
21. van der Giessen K, Di-Marco S, Clair E, Gallouzi IE. RNAi-mediated HuR depletion leads to the inhibition of muscle cell differentiation. J Biol Chem 2003; 278: 47119-47128.
22. Figueroa A, Cuadrado A, Fan J, Atasoy U, Muscat GE, Muñoz-Canoves P et al. Role of HuR in skeletal myogenesis through coordinate regulation of muscle differentiation genes. Mol Cell Biol 2003; 23: 4991-5004.
23. Briata P, Forcales SV, Ponassi M, Corte G, Chen CY, Karin M et al. p38-dependent phosphorylation of the mRNA decay-promoting factor KSRP controls the stability of select myogenic transcripts. Mol Cell 2005; 20: 891-903.
24. Gherzi R, Trabucchi M, Ponassi M, Ruggiero T, Corte G, Moroni C et al. 2006 The RNA-binding protein KSRP promotes decay of beta-catenin mRNA and is inactivated by PI3K-AKT signaling. PLoS Biol 2006; 5: e5.
25. Espinoza HM, Ganga M, Vadlamudi U, Martin DM, Brooks BP, Semina EV et al. Protein kinase C phosphorylation modulates N-and C-terminal regulatory activities of the PITX2 homeodomain protein. Biochemistry 2005; 44: 3942-3954.
26. Jiang BH, Zheng JZ, Vogt PK. An essential role of phosphatidylinositol 3-kinase in myogenic differentiation. Proc Natl Acad Sci USA 1998; 95: 14179-14183.
27. Xu Q, Wu Z. The insulin-like growth factor-phosphatidylinositol 3-kinase-Akt signaling pathway regulates myogenin expression in normal myogenic cells but not in rhabdomyosarcoma-derived RD cells. J Biol Chem 2000; 275: 36750-36757.
28. van Rooij E, Liu N, Olson EN. MicroRNAs flex their muscles. Trends Genet 2008; 24: 159-166.
29. Wang W, Yang X, Cristofalo VJ, Holbrook NJ, Gorospe M. Loss of HuR is linked to reduced expression of proliferative genes during replicative senescence. Mol Cell Biol 2001; 21: 5889-5898.
30. Lal A, Mazan-Mamczarz K, Kawai T, Yang X, Martindale JL, Gorospe M. Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J 2004; 23: 3092-3102.
31. Yaffe MB, Rittinger K, Volinia S, Caron PR, Aitken A, Leffers H et al. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 1997; 91: 961-971.
32. Héron-Milhavet L, Mamaeva D, Rochat A, Lamb NJ, Fernandez A. Akt2 is implicated in skeletal muscle differentiation and specifically binds Prohibitin2/REA. J Cell Physiol 2008; 214: 158-165.
33. Yamada E, Okada S, Saito T, Ohshima K, Sato M, Tsuchiya T et al. Akt2 phosphorylates Synip to regulate docking and fusion of GLUT4-containing vesicles. J Cell Biol 2005; 168: 921-928.
34. Kato S, Ding J, Du K. Differential activation of CREB by Akt1 and Akt2. Biochem Biophys Res Commun 2007; 354: 1061-1066.
35. Alessi DR, Caudwell FB, Andjelkovic M, Hemmings BA, Cohen P. Molecular basis for the substrate specificity of protein kinase B; comparison with MAPKAP kinase-1 and p70 S6 kinase. FEBS Lett 1996; 399: 333-338.
36. Collins CA, Gnocchi VF, White RB, Boldrin L, Perez-Ruiz A, Relaix F et al. Integrated functions of Pax3 and Pax7 in the regulation of proliferation, cell size and myogenic differentiation. PLoS ONE 2009; 4: e4475.
37. Schmidlin M, Lu M, Leuenberger SA, Stoecklin G, Mallaun M, Gross B et al. The ARE-dependent mRNA destabilizing activity of BRF1 is regulated by protein kinase B. EMBO J 2004; 23: 4760-4769.
38. Gallouzi IE, Brennan CM, Stenberg MG, Swanson MS, Eversole A, Maizels N et al. HuR binding to cytoplasmic mRNA is perturbed by heat shock. Proc Natl Acad Sci USA 2000; 97: 3073-3088.
39. Chen CY, Gherzi R, Andersen JS, Gaietta G, Jürchott K, Royer HD et al. Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation. Genes Dev 2000; 14: 1236-1248.
40. Ruggiero T, Trabucchi M, De Santa F, Zupo S, Harfe BD, McManus MT et al. LPS induces KH-type splicing regulatory protein-dependent processing of microRNA-155 precursors in macrophages. FASEB J 2009; 23: 2898-2908.