Stabilization of Dll1 mRNA by Elavl1/HuR in neuroepithelial cells undergoing mitosis

Molecular Biology of the Cell

Volumn 22, Issue 8, 2011, Pages 1227-1239

  García Domínguez, Daniel J ^a   Morello, Dominique ^b   Cisneros, Elsa ^a   Kontoyiannis, Dimitris L ^c   Frade, José M ^a  

^a INSTITUTO CAJAL   (Spain)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DELTA LIKE 1 PROTEIN; HUR PROTEIN; MESSENGER RNA; NOTCH1 RECEPTOR; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; CYTOPLASM; EPITHELIUM CELL; FEMALE; GENE EXPRESSION; HETEROZYGOTE; IN VIVO STUDY; MITOSIS; MITOSIS INHIBITION; MOUSE; MOUSE MUTANT; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RETINA DEVELOPMENT; RNA INTERFERENCE; RNA STABILITY; SIGNAL TRANSDUCTION; VERTEBRATE;

3' UNTRANSLATED REGIONS; ANIMALS; ANTIGENS, SURFACE; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINE, TRANSFORMED; CHICK EMBRYO; ELECTROPORATION; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MITOSIS; NEUROEPITHELIAL CELLS; NEUROGENESIS; NEURONS; RECEPTOR, NOTCH1; RNA STABILITY; RNA, MESSENGER; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION;

MUS; VERTEBRATA;

EID: 79954622992     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-10-0808     Document Type: Article

References (45)

1. Agathocleous M, Harris WA (2009). From progenitors to differentiated cells in the vertebrate retina. Annu Rev Cell Dev Biol 25, 45-69.
2. Atasoy U, Watson J, Patel D, Keene JD (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. (Pubitemid 28532425)
3. Barreau C, Paillard L, Osborne HB (2005). AU-rich elements and associated factors: Are there unifying principles? Nucleic Acids Res 33, 7138-7150.
4. Bertrand N, Castro DS, Guillemot F (2002). Proneural genes and the specification of neural cell types. Nat Rev Neurosci 3, 517-530. (Pubitemid 135706662)
5. Cisneros E, Latasa MJ, García-Flores M, Frade JM (2008). Instability of Notch1 and Dll1 mRNAs and reduced Notch activity in vertebrate neuroepithelial cells undergoing S-phase. Mol Cell Neurosci 37, 820-831.
6. Colgan DF, Murthy KG, Prives C, Manley JL (1996). Cell-cycle related regulation of poly(A) polymerase by phosphorylation. Nature 384, 282-285. (Pubitemid 26396981)
7. Collier JR, Monk NA, Maini PK, Lewis JH (1996). Pattern formation by lateral inhibition with feedback: A mathematical model of delta-notch intercellular signalling. J Theor Biol 183, 429-446. (Pubitemid 27033749)
8. Das RM et al. (2006). A robust system for RNA interference in the chicken using a modified microRNA operon. Dev Biol 294, 554-563. (Pubitemid 43866674)
9. Del Bene F, Wehman AM, Link BA, Baier H (2008). Regulation of neurogenesis by interkinetic nuclear migration through an apical-basal notch gradient. Cell 134, 1055-1065.
10. Doller A, Akool ES, Huwiler A, Müller R, Radeke HH, Pfeilschifter J, Eberhardt W (2008). Posttranslational modification of the AU-rich element binding protein HuR by protein kinase Cdelta elicits angiotensin II-induced stabilization and nuclear export of cyclooxygenase 2 mRNA. Mol Cell Biol 28, 2608-2625. (Pubitemid 351542362)
11. Fan XC, Steitz JA (1998). HNS, a nuclear-cytoplasmic shuttling sequence in HuR. Proc Natl Acad Sci USA 95, 15293-15298. (Pubitemid 29018692)
12. Figueroa A, Cuadrado A, Fan J, Atasoy U, Muscat GE, Muñoz-Canoves P, Gorospe M, Muñoz A (2003). Role of HuR in skeletal myogenesis through coordinate regulation of muscle differentiation genes. Mol Cell Biol 23, 4991-5004. (Pubitemid 36793344)
13. Frade JM (2002). Interkinetic nuclear movement in the vertebrate neuroepithelium: Encounters with an old acquaintance. Prog Brain Res 136, 67-71. (Pubitemid 35460968)
14. Frade JM, Rodríguez-Tébar A (2000). Neuroepithelial differentiation induced by ECM molecules. Methods Mol Biol 139, 257-264.
15. Ge X, Frank CL, Calderon de Anda F, Tsai LH (2010). Hook3 interacts with PCM1 to regulate pericentriolar material assembly and the timing of neurogenesis. Neuron 65, 191-203.
16. Gonsalves FC, Weisblat DA (2007). MAPK regulation of maternal and zygotic Notch transcript stability in early development. Proc Natl Acad Sci USA 104, 531-536. (Pubitemid 46123059)
17. Hamburger V, Hamilton HL (1951). A series of normal stages in the development of the chick embryo. J Morphol 88, 49-92.
18. Hansson EM, Teixeira AI, Gustafsson MV, Dohda T, Chapman G, Meletis K, Muhr J, Lendahl U (2006). Recording Notch signaling in real time. Dev Neurosci 28, 118-127.
19. Hsu RJ, Yang HJ, Tsai HJ (2009). Labeled microRNA pull-down assay system: An experimental approach for high-throughput identification of microRNA-target mRNAs. Nucleic Acids Res 37, e77.
20. Kageyama R, Ohtsuka T, Shimojo H, Imayoshi I (2009). Dynamic regulation of Notch signaling in neural progenitor cells. Curr Opin Cell Biol 21, 733-740.
21. Katsanou V, Milatos S, Yiakouvaki A, Sgantzis N, Kotsoni A, Alexiou M, Harokopos V, Aidinis V, Hemberger M, Kontoyiannis DL (2009). The RNA-binding protein Elavl1/HuR is essential for placental branching morphogenesis and embryonic development. Mol Cell Biol 29, 2762-2776.
22. Kim HH, Gorospe M (2008). Phosphorylated HuR shuttles in cycles. Cell Cycle 7, 3124-3126.
23. Kim HH et al. (2008). Nuclear HuR accumulation through phosphorylation by Cdk1. Genes Dev 22, 1804-1815.
24. Lal A, Mazan-Mamczarz K, Kawai T, Yang X, Martindale JL, Gorospe M (2004). Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J 23, 3092-3102. (Pubitemid 39093603)
25. Latasa MJ, Cisneros E, Frade JM (2009). Cell cycle control of Notch signaling and the functional regionalization of the neuroepithelium during vertebrate neurogenesis. Int J Dev Biol 53, 895-908.
26. Levine DS, Sánchez CA, Rabinovitch PS, Reid BJ (1991). Formation of the tetraploid intermediate is associated with the development of cells with more than four centrioles in the elastase-SV40 tumor antigen transgenic mouse model of pancreatic cancer. Proc Natl Acad Sci USA 88, 6427-6431. (Pubitemid 21914959)
27. Lindsell CE, Boulter J, diSibio G, Gossler A, Weinmaster G (1996). Expression patterns of Jagged, Delta1, Notch1, Notch2, and Notch3 genes identify ligand-receptor pairs that may function in neural development. Mol Cell Neurosci 8, 14-27. (Pubitemid 26398713)
28. Loápez de Silanes I, Zhan M, Lal A, Yang X, Gorospe M (2004). Identification of a target RNA motif for RNA-binding protein HuR. Proc Natl Acad Sci USA 101, 2987-2992. (Pubitemid 38327723)
29. Louvi A, Artavanis-Tsakonas S (2006). Notch signalling in vertebrate neural development. Nat Rev Neurosci 7, 93-102. (Pubitemid 43151596)
30. Lu JY, Schneider RJ (2004). Tissue distribution of AU-rich mRNA-binding proteins involved in regulation of mRNA decay. J Biol Chem 279, 12974-12979. (Pubitemid 38445873)
31. Ma WJ, Cheng S, Campbell C, Wright A, Furneaux H (1996). Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein. J Biol Chem 271, 8144-8151. (Pubitemid 26108641)
32. Mazan-Mamczarz K, Galbán S, Loápez de Silanes I, Martindale JL, Atasoy U, Keene JD, Gorospe M (2003). RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proc Natl Acad Sci USA 100, 8354-8359. (Pubitemid 36842549)
33. Morillo SM, Escoll P, de la Hera A, Frade JM (2010). Somatic tetraploidy in specific chick retinal ganglion cells induced by nerve growth factor. Proc Natl Acad Sci USA 107, 109-114.
34. Murciano A, Zamora J, Loápez-Sanchez J, Frade JM (2002). Interkinetic nuclear movement may provide spatial clues to the regulation of neurogenesis. Mol Cell Neurosci 21, 285-300. (Pubitemid 35333817)
35. Nardelli J, Catala M, Charnay P (2003). Establishment of embryonic neuroepithelial cell lines exhibiting an epiplastic expression pattern of region specific markers. J Neurosci Res 73, 737-752. (Pubitemid 37071728)
36. Ochiai W et al. (2009). Periventricular Notch activation and asymmetric Ngn2 and Tbr2 expression in pair-generated neocortical daughter cells. Mol Cell Neurosci 40, 225-233.
37. Robinow S, Campos AR, Yao KM, White K (1988). The elav gene product of Drosophila, required in neurons, has three RNP consensus motifs. Science 242, 1570-1572.
38. Sauer FC (1935). Mitosis in the neural tube. J Comp Neurol 62, 377-405.
39. Schenk J, Wilsch-Bräuninger M, Calegari F, Huttner WB (2009). Myosin II is required for interkinetic nuclear migration of neural progenitors. Proc Natl Acad Sci USA 106, 16487-16492.
40. Schmittgen TD, Zakrajsek BA (2000). Effect of experimental treatment on housekeeping gene expression: validation by real time, quantitative RT-PCR. J Biochem Biophys Methods 46, 69-81.
41. Takahashi T, Nowakowski RS, Caviness VS, Jr (1993). Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse. J Neurosci 13, 820-833. (Pubitemid 23045162)
42. Tamberg N, Lulla V, Fragkoudis R, Lulla A, Fazakerley JK, Merits A (2007). Insertion of EGFP into the replicase gene of Semliki Forest virus results in a novel, genetically stable marker virus. J Gen Virol 88, 1225-1230. (Pubitemid 46523511)
43. Wang W, Caldwell MC, Lin S, Furneaux H, Gorospe M (2000). HuR regulates cyclin A and cyclin B1 mRNA stability during cell proliferation. EMBO J 19, 2340-2350. (Pubitemid 30259015)
44. Xie Z, Moy LY, Sanada K, Zhou Y, Buchman JJ, Tsai LH (2007). Cep120 and TACCs control interkinetic nuclear migration and the neural progenitor pool. Neuron 56, 79-93. (Pubitemid 47487500)
45. Xu N, Chen CY, Shyu AB (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. (Pubitemid 27318137)