The H19 lincRNA is a developmental reservoir of miR-675 that suppresses growth and Igf1r

Nature Cell Biology

Volumn 14, Issue 7, 2012, Pages 659-665

  Keniry, Andrew ^a   Oxley, David ^a   Monnier, Paul ^b   Kyba, Michael ^c   Dandolo, Luisa ^b   Smits, Guillaume ^d   Reik, Wolf ^a,e  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b INSTITUT COCHIN   (France)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^d UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DICER; LARGE INTERGENIC NON CODING RNA; MICRORNA; MICRORNA 675; RNA BINDING PROTEIN; RNA BINDING PROTEIN HUR; TRANSCRIPTOME; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL GENE; EMBRYO; EXON; FEMALE; FETUS; GENE EXPRESSION; GENE FUNCTION; GENE LOCUS; H19 GENE; INSULIN LIKE GROWTH FACTOR 1 RECEPTOR GENE; MITOSIS INHIBITION; NONHUMAN; PRIORITY JOURNAL; RECEPTOR GENE; RNA PROCESSING; RNA TRANSCRIPTION;

ANIMALS; CELL LINE; CELL PROLIFERATION; DEAD-BOX RNA HELICASES; DOWN-REGULATION; EXONS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GESTATIONAL AGE; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, KNOCKOUT; MICE, TRANSGENIC; MICRORNAS; PLACENTA; PREGNANCY; RECEPTOR, IGF TYPE 1; RIBONUCLEASE III; RNA INTERFERENCE; RNA, UNTRANSLATED; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

MAMMALIA;

EID: 84863219731     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2521     Document Type: Article

References (46)

1. Brannan, C. I., Dees, E. C., Ingram, R. S. & Tilghman, S. M. The product of the H19 gene may function as an RNA. Mol. Cell. Biol. 10, 28-36 (1990).
2. Seidl, C. I., Stricker, S. H. & Barlow, D. P. The imprinted Air ncRNA is an atypical RNAPII transcript that evades splicing and escapes nuclear export. EMBO. J. 25, 3565-3575 (2006). (Pubitemid 44264867)
3. Bartolomei, M. S. Genomic imprinting: employing and avoiding epigenetic processes. Genes Dev. 23, 2124-2133 (2009).
4. Gabory, A., Jammes, H. & Dandolo, L. The H19 locus: role of an imprinted non-coding RNA in growth and development. Bioessays 32, 473-480 (2010).
5. Hao, Y., Crenshaw, T., Moulton, T., Newcomb, E. & Tycko, B. Tumour-suppressor activity of H19 RNA. Nature 365, 764-767 (1993). (Pubitemid 23339885)
6. Yoshimizu, T. et al. The H19 locus acts in vivo as a tumor suppressor. Proc. Natl Acad. Sci. USA 105, 12417-12422 (2008).
7. Smits, G. et al. Conservation of the H19 noncoding RNA and H19-IGF2 imprinting mechanism in therians. Nat. Genet. 40, 971-976 (2008).
8. Gabory, A. et al. H19 acts as a trans regulator of the imprinted gene network controlling growth in mice. Development 136, 3413-3421 (2009).
9. Wilusz, J. E., Sunwoo, H. & Spector, D. L. Long noncoding RNAs: functional surprises from the RNA world. Genes Dev. 23, 1494-1504 (2009).
10. Bartel, D. P. MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233 (2009).
11. Huntzinger, E. & Izaurralde, E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat. Rev. Genet. 12, 99-110 (2011).
12. Cai, X. & Cullen, B. R. The imprinted H19 noncoding RNA is a primary microRNA precursor. RNA 13, 313-316 (2007). (Pubitemid 46327534)
13. Dudek, K. A., Lafont, J. E., Martinez-Sanchez, A. & Murphy, C. L. Type II collagen expression is regulated by tissue-speci-c miR-675 in human articular chondrocytes. J. Biol. Chem. 285, 24381-24387 (2010).
14. Chiang, H. R. et al. Mammalian microRNAs: experimental evaluation of novel and previously annotated genes. Genes Dev. 24, 992-1009 (2010).
15. Mineno, J. et al. The expression pro-le of microRNAs in mouse embryos. Nucleic Acids Res. 34, 1765-1771 (2006).
16. Yang, J. H., Shao, P., Zhou, H., Chen, Y. Q. & Qu, L. H. deepBase: a database for deeply annotating and mining deep sequencing data. Nucleic Acids Res. 38, D123-D130 (2010).
17. Lee, Y. S. & Dutta, A. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev. 21, 1025-1030 (2007). (Pubitemid 46686471)
18. Lim, L. P. et al. The microRNAs of Caenorhabditis elegans. Genes Dev. 17, 991-1008 (2003). (Pubitemid 36459452)
19. Knox, K. & Baker, J. C. Genomic evolution of the placenta using co-option and duplication and divergence. Genome Res. 18, 695-705 (2008). (Pubitemid 351645060)
20. Zhao, Z., Chang, F. C. & Furneaux, H. M. The identi-cation of an endonuclease that cleaves within an HuR binding site in mRNA. Nucleic Acids Res. 28, 2695-2701 (2000). (Pubitemid 30488013)
21. Katsanou, V. et al. The RNA-binding protein Elavl1/HuR is essential for placental branching morphogenesis and embryonic development. Mol. Cell. Biol. 29, 2762-2776 (2009).
22. Kim, V. N., Han, J. & Siomi, M. C. Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10, 126-139 (2009).
23. Runge, S. et al. H19 RNA binds four molecules of insulin-like growth factor II mRNA-binding protein. J. Biol. Chem. 275, 29562-29569 (2000). (Pubitemid 32043834)
24. Mallanna, S. K. et al. Proteomic analysis of Sox2-associated proteins during early stages of mouse embryonic stem cell differentiation identi-es Sox21 as a novel regulator of stem cell fate. Stem Cells 28, 1715-1727 (2010).
25. Coan, P. M., Ferguson-Smith, A. C. & Burton, G. J. Developmental dynamics of the de-nitive mouse placenta assessed by stereology. Biol. Reprod. 70, 1806-1813 (2004). (Pubitemid 38715638)
26. Angiolini, E. et al. Developmental adaptations to increased fetal nutrient demand in mouse genetic models of Igf2-mediated overgrowth. FASEB J. 25, 1737-1745 (2011).
27. Esquiliano, D. R., Guo, W., Liang, L., Dikkes, P. & Lopez, M. F. Placental glycogen stores are increased in mice with H19 null mutations but not in those with insulin or IGF type 1 receptor mutations. Placenta 30, 693-699 (2009).
28. Leighton, P. A., Ingram, R. S., Eggenschwiler, J., Efstratiadis, A. & Tilghman, S. M. Disruption of imprinting caused by deletion of the H19 gene region in mice. Nature 375, 34-39 (1995).
29. Thorvaldsen, J. L., Duran, K. L. & Bartolomei, M. S. Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes Dev. 12, 3693-3702 (1998). (Pubitemid 29019650)
30. Ripoche, M. A., Kress, C., Poirier, F. & Dandolo, L. Deletion of the H19 transcription unit reveals the existence of a putative imprinting control element. Genes Dev. 11, 1596-1604 (1997). (Pubitemid 27274403)
31. Liu, J. P., Baker, J., Perkins, A. S., Robertson, E. J. & Efstratiadis, A. Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igfi1) and type 1 IGF receptor (Igf1r). Cell 75, 59-72 (1993). (Pubitemid 23306021)
32. Baker, J., Liu, J. P., Robertson, E. J. & Efstratiadis, A. role of insulin-like growth factors in embryonic and postnatal growth. Cell 75, 73-82 (1993). (Pubitemid 23306022)
33. Jeyaraj, S. C., Dakhlallah, D., Hill, S. R. & Lee, B.S. Expression and distribution of HuR during ATP depletion and recovery in proximal tubule cells. Am. J. Physiol. Renal. Physiol. 291, F1255-F1263 (2006). (Pubitemid 44887239)
34. Kim, H. H., Abdelmohsen, K. & Gorospe, M. Regulation of HuR by DNA damage response kinases. J. Nucleic Acids 2010 (2010).
35. Pan, Y. X., Chen, H. & Kilberg, M. S. Interaction of RNA-binding proteins HuR and AUF1 with the human ATF3 mRNA 3'-untranslated region regulates its amino acid limitation-induced stabilization. J. Biol. Chem. 280, 34609-34616 (2005). (Pubitemid 41504591)
36. Wang, W. et al. HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol. 20, 760-769 (2000). (Pubitemid 30044212)
37. Blaxall, B. C. et al. Differential expression and localization of the mRNA binding proteins, AU-rich element mRNA binding protein (AUF1) and Hu antigen R (HuR), in neoplastic lung tissue. Mol. Carcinog. 28, 76-83 (2000). (Pubitemid 30432475)
38. Lebedeva, S. et al. Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR. Mol. Cell 43, 340-352 (2011).
39. Reddy, S. D., Ohshiro, K., Rayala, S. K. & Kumar, R. MicroRNA-7, a homeobox D10 target, inhibits p21-activated kinase 1 and regulates its functions. Cancer Res. 68, 8195-8200 (2008).
40. Saydam, O. et al. miRNA-7 attenuation in Schwannoma tumors stimulates growth by upregulating three oncogenic signaling pathways. Cancer Res. 71, 852-861 (2011).
41. Jiang, L. et al. MicroRNA-7 targets IGF1R (insulin-like growth factor 1 receptor) in tongue squamous cell carcinoma cells. Biochem. J. 432, 199-205 (2010).
42. Lim, D. H. & Maher, E. R. Genomic imprinting syndromes and cancer. Adv. Genet. 70, 145-175 (2010).
43. Tanaka, S., Kunath, T., Hadjantonakis, A. K., Nagy, A. & Rossant, J. Promotion of trophoblast stem cell proliferation by FGF4. Science 282, 2072-2075 (1998). (Pubitemid 29001261)
44. Ficz, G. et al. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 473, 398-402 (2011).
45. Caputi, M., Mayeda, A., Krainer, A. R. & Zahler, A. M. hnRNP A/B proteins are required for inhibition of HIV-1 pre-mRNA splicing. EMBO J. 18, 4060-4067 (1999). (Pubitemid 29335858)
46. Baroni, T. E., Chittur, S. V., George, A. D. & Tenenbaum, S. A. Advances in RIP-chip analysis: RNA-binding protein immunoprecipitation- microarray pro-ling. Methods Mol. Biol. 419, 93-108 (2008).