H19 antisense RNA can up-regulate IGF2 transcription by activation of a novel promoter in mouse myoblasts

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Tran, Van Giang ^a   Court, Franck ^a   Duputié, Anne ^a   Antoine, Etienne ^a   Aptel, Nathalie ^a   Milligan, Laura ^a,e   Carbonell, Françoise ^a   Lelay Taha, Marie Noëlle ^a   Piette, Jacques ^a   Weber, Michaël ^a   Montarras, Didier ^b   Pinset, Christian ^c   Dandolo, Luisa ^d   Forné, Thierry ^a   Cathala, Guy ^a  

^a INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^b INSTITUT PASTEUR   (France)

^c I Stem   (France)

^d INSERM   (France)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY RNA; RNA H19;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; GENETIC COMPLEMENTATION; GENOME IMPRINTING; IGF2 GENE; MARKER GENE; MESODERM; MOUSE; MYOBLAST; NONHUMAN; PROMOTER REGION; RNA ANALYSIS; RNA ISOLATION; TISSUE DISTRIBUTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; BASE SEQUENCE; DNA METHYLATION; GENE EXPRESSION REGULATION; GENE ORDER; GENE SILENCING; GENOMIC IMPRINTING; INSULIN-LIKE GROWTH FACTOR II; MICE; MOLECULAR SEQUENCE DATA; MYOBLASTS; PROMOTER REGIONS, GENETIC; RNA, ANTISENSE; RNA, LONG UNTRANSLATED; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84861476682     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037923     Document Type: Article

References (58)

1. Kapranov P, Willingham A, Gingeras T, (2007) Genome-wide transcription and the implications for genomic organization. Nat Rev Genet 8: 413-423.
2. Gibb E, Brown C, Lam W, (2011) The functional role of long non-coding RNA in human carcinomas. Mol 10: 38.
3. Wilusz J, Sunwoo H, Spector D, (2011) Long noncoding RNAs: functional surprises from the RNA world. Genes Dev 23: 1494-1504.
4. Chaumeil J, Le Baccon P, Wutz A, Heard E, (2006) A novel role for Xist RNA in the formation of a repressive nuclear compartment into which genes are recruited when silenced. Genes Dev 20: 2223-2237.
5. Gupta R, Shah N, Wang K, Kim J, Horlings H, et al. (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464: 1071-1076.
6. Kotake Y, Nakagawa T, Kitagawa K, Suzuki S, Liu N, et al. (2011) Long non-coding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15(INK4B) tumor suppressor gene. Oncogene 30: 1956-1962.
7. Rodriguez C, Borgel J, Court F, Cathala G, Forne T, et al. (2010) CTCF is a DNA methylation-sensitive positive regulator of the INK/ARF locus. Biochem Biophys Res Commun 392: 129-134.
8. Beltran M, Puig I, Pena C, Garcia J, Alvarez A, et al. (2008) A natural antisense transcript regulates Zeb2/Sip1 gene expression during Snail1-induced epithelial-mesenchymal transition. Genes Dev 22: 756-769.
9. Gong C, Maquat L, (2011) lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3' UTRs via Alu elements. Nature 470: 284-288.
10. Wang J, Liu X, Wu H, Ni P, Gu Z, et al. (2010) CREB up-regulates long non-coding RNA, HULC expression through interaction with microRNA-372 in liver cancer. Nucleic 38: 5366-5383. Epub 2010 Apr 5327.
11. Seitz H, Youngson N, Lin S, Dalbert S, Paulsen M, et al. (2003) Imprinted microRNA genes transcribed antisense to a reciprocally imprinted retrotransposon-like gene. Nat Genet 34: 261-262.
12. Wilusz J, Freier S, Spector D, (2008) 3' end processing of a long nuclear-retained noncoding RNA yields a tRNA-like cytoplasmic RNA. Cell 135: 919-932.
13. Martignetti J, Brosius J, (1993) BC200 RNA: a neural RNA polymerase III product encoded by a monomeric Alu element. Proc Natl Acad Sci U S A 90: 11563-11567.
14. Wu Q, Kim Y, Lu J, Xuan Z, Chen J, et al. (2008) Poly A- transcripts expressed in HeLa cells. PLoS One 3: e2803.
15. Kiyosawa H, Mise N, Iwase S, Hayashizaki Y, Abe K, (2005) Disclosing hidden transcripts: mouse natural sense-antisense transcripts tend to be poly(A) negative and nuclear localized. Genome Res 15: 463-474.
16. Watanabe Y, Numata K, Murata S, Osada Y, Saito R, et al. (2010) Genome-wide analysis of expression modes and DNA methylation status at sense-antisense transcript loci in mouse. Genomics 96: 333-341.
17. Latos P, Barlow D, (2009) Regulation of imprinted expression by macro non-coding RNAs. RNA Biol 6: 100-106.
18. Court F, Baniol M, Hagège H, Petit J, Lelay-Taha M, et al. (2011) Long-range chromatin interactions at the mouse Igf2/H19 locus reveal a novel paternally expressed long non-coding RNA. Nucleic Acids Res 39: 5893-5903.
19. Pachnis V, Brannan C, Tilghman S, (1988) The structure and expression of a novel gene activated in early mouse embryogenesis. EMBO J 7: 673-681.
20. Moulton T, Crenshaw T, Hao Y, Moosikasuwan J, Lin N, et al. (1994) Epigenetic lesions at the H19 locus in Wilms' tumour patients. Nat Genet 7: 440-447.
21. Taniguchi T, Sullivan M, Ogawa O, Reeve A, (1995) Epigenetic changes encompassing the IGF2/H19 locus associated with relaxation of IGF2 imprinting and silencing of H19 in Wilms tumor. Proc Natl Acad Sci U S A 92: 2159-2163.
22. Hao Y, Crenshaw T, Moulton T, Newcomb E, Tycko B, (1993) Tumour-suppressor activity of H19 RNA. Nature 365: 764-767.
23. Yoshimizu T, Miroglio A, Ripoche MA, Gabory A, Vernucci M, et al. (2008) The H19 locus acts in vivo as a tumor suppressor. Proc Natl Acad Sci U S A 105: 12417-12422.
24. Adriaenssens E, Dumont L, Lottin S, Bolle D, Lepretre A, et al. (1998) H19 overexpression in breast adenocarcinoma stromal cells is associated with tumor values and steroid receptor status but independent of p53 and Ki-67 expression. Am J Pathol 153: 1597-1607.
25. Biran H, Ariel I, de Groot N, Shani A, Hochberg A, (1994) Human imprinted genes as oncodevelopmental markers. Tumour Biol 15: 123-134.
26. Cooper M, Fischer M, Komitowski D, Shevelev A, Schulze E, et al. (1996) Developmentally imprinted genes as markers for bladder tumor progression. J Urol 155: 2120-2127.
27. Lottin S, Adriaenssens E, Dupressoir T, Berteaux N, Montpellier C, et al. (2002) Overexpression of an ectopic H19 gene enhances the tumorigenic properties of breast cancer cells. Carcinogenesis 23: 1885-1895.
28. Lustig-Yariv O, Schulze E, Komitowski D, Erdmann V, Schneider T, et al. (1997) The expression of the imprinted genes H19 and IGF-2 in choriocarcinoma cell lines. Is H19 a tumor suppressor gene? Oncogene 15: 169-177.
29. Ariel I, Ayesh S, Perlman E, Pizov G, Tanos V, et al. (1997) The product of the imprinted H19 gene is an oncofetal RNA. Mol Pathol 50: 34-44.
30. Thorvaldsen J, Duran K, Bartolomei M, (1998) Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes Dev 12: 3693-3702.
31. Hark A, Schoenherr C, Katz D, Ingram R, Levorse J, et al. (2000) CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405: 486-489.
32. Varrault A, Gueydan C, Delalbre A, Bellmann A, Houssami S, et al. (2006) Zac1 regulates an imprinted gene network critically involved in the control of embryonic growth. Dev Cell 11: 711-722.
33. Gabory A, Ripoche M, Le Digarcher A, Watrin F, Ziyyat A, et al. (2009) H19 acts as a trans regulator of the imprinted gene network controlling growth in mice. Development 136: 3413-3421.
34. Berteaux N, Aptel N, Cathala G, Genton C, Coll J, et al. (2008) A novel H19 antisense RNA overexpressed in breast cancer contributes to paternal IGF2 expression. Mol Cell Biol 28: 6731-6745.
35. Schoenfelder S, Smits G, Fraser P, Reik W, Paro R, (2007) Non-coding transcripts in the H19 imprinting control region mediate gene silencing in transgenic Drosophila. EMBO Rep 8: 1068-1073.
36. Ripoche M, Kress C, Poirier F, Dandolo L, (1997) Deletion of the H19 transcription unit reveals the existence of a putative imprinting control element. Genes Dev 11: 1596-1604.
37. Wilkin F, Paquette J, Ledru E, Hamelin C, Pollak M, et al. (2000) H19 sense and antisense transgenes modify insulin-like growth factor-II mRNA levels. Eur J Biochem 267: 4020-4027.
38. Milligan L, Antoine E, Bisbal C, Weber M, Brunel C, et al. (2000) H19 gene expression is up-regulated exclusively by stabilization of the RNA during muscle cell differentiation. Oncogene 19: 5810-5816.
39. Murrell A, Heeson S, Bowden L, Constancia M, Dean W, et al. (2001) An intragenic methylated region in the imprinted Igf2 gene augments transcription. EMBO Rep 2: 1101-1106.
40. Dejeux E, Olaso R, Dousset B, Audebourg A, Gut I, et al. (2009) Hypermethylation of the IGF2 differentially methylated region 2 is a specific event in insulinomas leading to loss-of-imprinting and overexpression. Endocr Relat Cancer 16: 939-952.
41. Onyango P, Feinberg A, (2011) A nucleolar protein, H19 opposite tumor suppressor (HOTS), is a tumor growth inhibitor encoded by a human imprinted H19 antisense transcript. Proc Natl Acad Sci U S A 108: 16759-16764.
42. Cai X, Cullen B, (2007) The imprinted H19 noncoding RNA is a primary microRNA precursor. RNA 13: 313-316.
43. Smits G, Mungall A, Griffiths-Jones S, Smith P, Beury D, et al. (2008) Conservation of the H19 noncoding RNA and H19-IGF2 imprinting mechanism in therians. Nat Genet 40: 971-976.
44. Tsang W, Ng E, SS N, Jin H, Yu J, et al. (2010) Oncofetal H19-derived miR-675 regulates tumor suppressor RB in human colorectal cancer. Carcinogenesis 31: 350-358.
45. Li Y, Franklin G, Cui H, Svensson K, He X, et al. (1998) The H19 transcript is associated with polysomes and may regulate IGF2 expression in trans. J Biol Chem 273: 28247-28252.
46. Pallafacchina G, Francois S, Regnault B, Czarny B, Dive V, et al. (2010) An adult tissue-specific stem cell in its niche: a gene profiling analysis of in vivo quiescent and activated muscle satellite cells. Stem Cell Res 4: 77-91.
47. Davies K, Bowden L, Smith P, Dean W, Hill D, et al. (2002) Disruption of mesodermal enhancers for Igf2 in the minute mutant. Development 129: 1657-1668.
48. Kurukuti S, Tiwari V, Tavoosidana G, Pugacheva E, Murrell A, et al. (2006) CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2. Proc Natl Acad Sci U S A 103: 10684-10689.
49. Murrell A, Heeson S, Reik W, (2004) Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat Genet 36: 889-893.
50. Leighton P, Saam J, Ingram R, Stewart C, Tilghman S, (1995) An enhancer deletion affects both H19 and Igf2 expression. Genes Dev 9: 2079-2089.
51. Montarras D, Lindon C, Pinset C, Domeyne P, (2000) Cultured myf5 null and myoD null muscle precursor cells display distinct growth defects. Biol Cell 92: 565-572.
52. Weber M, Milligan L, Delalbre A, Antoine E, Brunel C, et al. (2001) Extensive tissue-specific variation of allelic methylation in the Igf2 gene during mouse fetal development: relation to expression and imprinting. Mech Dev 101: 133-141.
53. Milligan L, Forné T, Antoine E, Weber M, Hemonnot B, et al. (2002) Turnover of primary transcripts is a major step in the regulation of mouse H19 gene expression. EMBO Rep 3: 774-779.
54. Lutfalla G, Uzé G, (2006) Performing quantitative reverse-transcribed polymerase chain reaction experiments. Methods Enzymol 410: 386-400.
55. Court F, Miro J, Braem C, Lelay-Taha M, Brisebarre A, et al. (2011) Modulated contact frequencies at gene-rich loci support a statistical helix model for mammalian chromatin organization. Genome Biology 12: R42.
56. Weber M, Hagege H, Lutfalla G, Dandolo L, Brunel C, et al. (2003) A real-time polymerase chain reaction assay for quantification of allele ratios and correction of amplification bias. Anal Biochem 320: 252-258.
57. Braem C, Recolin B, Rancourt R, Angiolini C, Barthes P, et al. (2008) Genomic matrix attachment region and chromosome conformation capture quantitative real time PCR assays identify novel putative regulatory elements at the imprinted Dlk1/Gtl2 locus. J Biol Chem 283: 18612-18620.
58. Moore T, Constancia M, Zubair M, Bailleul B, Feil R, et al. (1997) Multiple imprinted sense and antisense transcripts, differential methylation and tandem repeats in a putative imprinting control region upstream of mouse Igf2. Proc Natl Acad Sci U S A 94: 12509-12514.