RNA transcribed from a distal enhancer is required for activating the chromatin at the promoter of the gonadotropin α-subunit gene

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 14, 2015, Pages 4369-4374

  Pnueli, Lilach ^a   Rudnizky, Sergei ^a   Yosefzon, Yahav ^a   Melamed, Philippa ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Chromatin; Enhancer; Gonadotropin; ncRNA; Pituitary

Indexed keywords

CHORIONIC GONADOTROPIN ALPHA SUBUNIT; GONADORELIN; HISTONE H3; LONG UNTRANSLATED RNA; MESSENGER RNA; RNA; UNTRANSLATED RNA; ALPHA CHAIN; CHROMATIN; HISTONE;

AMPLICON; ANIMAL CELL; ARTICLE; BINDING SITE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; ENHANCER REGION; GENE ACTIVATION; GENE REPRESSION; HISTONE MODIFICATION; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ACETYLATION; RNA TRANSCRIPTION; STABLE TRANSFECTION; ALPHA CHAIN; ANIMAL; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION; GENETICS; HYPOPHYSIS; METABOLISM;

ANIMALS; CELL LINE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CPG ISLANDS; DNA METHYLATION; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; GLYCOPROTEIN HORMONES, ALPHA SUBUNIT; HISTONES; MICE; PITUITARY GLAND; PROMOTER REGIONS, GENETIC; RNA; RNA, MESSENGER;

EID: 84928798828     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1414841112     Document Type: Article

References (44)

1. Ong CT, Corces VG (2012) Enhancers: Emerging roles in cell fate specification. EMBO Rep 13(5):423-430.
2. De Santa F, et al. (2010) A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol 8(5):e1000384.
3. Kim TK, et al. (2010) Widespread transcription at neuronal activity-regulated enhancers. Nature 465(7295):182-187.
4. Koch F, et al. (2011) Transcription initiation platforms and GTF recruitment at tissuespecific enhancers and promoters. Nat Struct Mol Biol 18(8):956-963.
5. Wang D, et al. (2011) Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature 474(7351):390-394.
6. Melgar MF, Collins FS, Sethupathy P (2011) Discovery of active enhancers through bidirectional expression of short transcripts. Genome Biol 12(11):R113.
7. Ebisuya M, Yamamoto T, Nakajima M, Nishida E (2008) Ripples from neighbouring transcription. Nat Cell Biol 10(9):1106-1113.
8. Struhl K (2007) Transcriptional noise and the fidelity of initiation by RNA polymerase II. Nat Struct Mol Biol 14(2):103-105.
9. Natoli G, Andrau JC (2012) Noncoding transcription at enhancers: General principles and functional models. Annu Rev Genet 46:1-19.
10. Li W, et al. (2013) Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature 498(7455):516-520.
11. Mousavi K, et al. (2013) eRNAs promote transcription by establishing chromatin accessibility at defined genomic loci. Mol Cell 51(5):606-617.
12. Melo CA, et al. (2013) eRNAs are required for p53-dependent enhancer activity and gene transcription. Mol Cell 49(3):524-535.
13. Hsieh CL, et al. (2014) Enhancer RNAs participate in androgen receptor-driven looping that selectively enhances gene activation. Proc Natl Acad Sci USA 111(20):7319-7324.
14. Kendall SK, et al. (1994) Enhancer-mediated high level expression of mouse pituitary glycoprotein hormone α-subunit transgene in thyrotropes, gonadotropes, and developing pituitary gland. Mol Endocrinol 8(10):1420-1433.
15. Brinkmeier ML, et al. (1998) Cell-specific expression of the mouse glycoprotein hormone alpha-subunit gene requires multiple interacting DNA elements in transgenic mice and cultured cells. Mol Endocrinol 12(5):622-633.
16. Tremblay JJ, Lanctôt C, Drouin J (1998) The pan-pituitary activator of transcription, Ptx1 (pituitary homeobox 1), acts in synergy with SF-1 and Pit1 and is an upstream regulator of the Lim-homeodomain gene Lim3/Lhx3. Mol Endocrinol 12(3):428-441.
17. Infante CR, Park S, Mihala AG, Kingsley DM, Menke DB (2013) Pitx1 broadly associates with limb enhancers and is enriched on hindlimb cis-regulatory elements. Dev Biol 374(1):234-244.
18. Creyghton MP, et al. (2010) Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci USA 107(50):21931-21936.
19. Bonn S, et al. (2012) Tissue-specific analysis of chromatin state identifies temporal signatures of enhancer activity during embryonic development. Nat Genet 44(2):148-156.
20. Skene PJ, Hernandez AE, Groudine M, Henikoff S (2014) The nucleosomal barrier to promoter escape by RNA polymerase II is overcome by the chromatin remodeler Chd1. eLife 3:e02042.
21. Lai F, et al. (2013) Activating RNAs associate with Mediator to enhance chromatin architecture and transcription. Nature 494(7438):497-501.
22. Lam MT, et al. (2013) Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription. Nature 498(7455):511-515.
23. Heintzman ND, et al. (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39(3):311-318.
24. Rada-Iglesias A, et al. (2011) A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470(7333):279-283.
25. Zentner GE, Tesar PJ, Scacheri PC (2011) Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions. Genome Res 21(8):1273-1283.
26. Benayoun BA, et al. (2014) H3K4me3 breadth is linked to cell identity and transcriptional consistency. Cell 158(3):673-688.
27. Wijerweera A, et al. (2015) Gonadotropin gene transcription is activated by meninmediated effects on the chromatin. Biochim Biophys Acta 1849(3):328-341.
28. Okazaki Y, et al.; FANTOM Consortium; RIKEN Genome Exploration Research Group Phase I & II Team (2002) Analysis of the mouse transcriptome based on functional annotation of 60, 770 full-length cDNAs. Nature 420(6915):563-573.
29. Sanyal A, Lajoie BR, Jain G, Dekker J (2012) The long-range interaction landscape of gene promoters. Nature 489(7414):109-113.
30. Hah N, Murakami S, Nagari A, Danko CG, Kraus WL (2013) Enhancer transcripts mark active estrogen receptor binding sites. Genome Res 23(8):1210-1223.
31. Kagey MH, et al. (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature 467(7314):430-435.
32. Wang KC, et al. (2011) A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472(7341):120-124.
33. Ferrari KJ, et al. (2014) Polycomb-dependent H3K27me1 and H3K27me2 regulate active transcription and enhancer fidelity. Mol Cell 53(1):49-62.
34. Visel A, et al. (2009) ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457(7231):854-858.
35. Kim DH, Villeneuve LM, Morris KV, Rossi JJ (2006) Argonaute-1 directs siRNA-mediated transcriptional gene silencing in human cells. Nat Struct Mol Biol 13(9):793-797.
36. Weinberg MS, et al. (2006) The antisense strand of small interfering RNAs directs histone methylation and transcriptional gene silencing in human cells. RNA 12(2):256-262.
37. Lanctôt C, Gauthier Y, Drouin J (1999) Pituitary homeobox 1 (Ptx1) is differentially expressed during pituitary development. Endocrinology 140(3):1416-1422.
38. Charles MA, et al. (2005) PITX genes are required for cell survival and Lhx3 activation. Mol Endocrinol 19(7):1893-1903.
39. Melamed P, Koh M, Preklathan P, Bei L, Hew C (2002) Multiple mechanisms for Pitx-1 transactivation of a luteinizing hormone beta subunit gene. J Biol Chem 277(29): 26200-26207.
40. Kieffer-Kwon KR, et al. (2013) Interactome maps of mouse gene regulatory domains reveal basic principles of transcriptional regulation. Cell 155(7):1507-1520.
41. Buecker C, et al. (2014) Reorganization of enhancer patterns in transition from naive to primed pluripotency. Cell Stem Cell 14(6):838-853.
42. Nord AS, et al. (2013) Rapid and pervasive changes in genome-wide enhancer usage during mammalian development. Cell 155(7):1521-1531.
43. Pnueli L, Luo M, Wang S, Naor Z, Melamed P (2011) Calcineurin mediates the gonadotropin-releasing hormone effect on expression of both subunits of the folliclestimulating hormone through distinct mechanisms. Mol Cell Biol 31(24):5023-5036.
44. Luo Z, Wijeweera A, Oh Y, Liou YC, Melamed P (2010) Pin1 facilitates the phosphorylation-dependent ubiquitination of SF-1 to regulate gonadotropin beta-subunit gene transcription. Mol Cell Biol 30(3):745-763.