Gonadotropin gene transcription is activated by menin-mediated effects on the chromatin

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1849, Issue 3, 2015, Pages 328-341

  Wijeweera, Andrea ^a   Haj, Majd ^a   Feldman, Alona ^a   Pnueli, Lilach ^a   Luo, Zhuojuan ^b   Melamed, Philippa ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

GnRH; Gonadotrope; Histone; Methylation; Pituitary; Ubiquitination

Indexed keywords

ESTROGEN RECEPTOR; FOLLITROPIN; GONADORELIN; GONADOTROPIN; LUTEINIZING HORMONE; METHIONINE; STEROIDOGENIC FACTOR 1; CHROMATIN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR ALPHA, HUMAN; FOLLICLE STIMULATING HORMONE; GONADOTROPIN-RELEASING HORMONE; GONADOTROPINS; HISTONE DEMETHYLASES; HISTONES; MEN1 PROTEIN, HUMAN; PROTO-ONCOGENE PROTEINS;

ANIMAL CELL; ARTICLE; BETA CHAIN; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; FEMALE; GENE SILENCING; GENETIC CODE; HISTONE MODIFICATION; IMMUNOBLOTTING; MALE; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA TRANSLATION; TRANSCRIPTION INITIATION; ANIMALS; BIOSYNTHESIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETICS; METABOLISM; MICE; PROMOTER REGIONS, GENETIC; TRANSCRIPTIONAL ACTIVATION;

ANIMALS; CHROMATIN; ESTROGEN RECEPTOR ALPHA; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GONADOTROPIN-RELEASING HORMONE; GONADOTROPINS; HISTONE DEMETHYLASES; HISTONES; LUTEINIZING HORMONE; MICE; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS; TRANSCRIPTIONAL ACTIVATION;

EID: 84922980983     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2015.01.001     Document Type: Article

References (65)

1. Naor Z. Signaling by G-protein coupled receptor (GPCR): studies on the GnRH receptor. Front. Neuroendocrinol. 2009, 30:10-29.
2. Jorgensen J.S., Quirk C.C., Nilson J.H. Multiple and overlapping combinatorial codes orchestrate hormonal responsiveness and dictate cell-specific expression of the genes encoding luteinizing hormone. Endocr. Rev. 2004, 25:521-542.
3. Melamed P., Abdul Kadir M.N., Wijeweera A., Seah S. Transcription of gonadotropin β subunit genes involves cross-talk between transcription factors and co-regulators that mediate actions of the regulatory hormones. Mol. Cell. Endocrinol. 2006, 252:167-183.
4. Melamed P. Hormonal signaling to follicle stimulating hormone β-subunit gene expression. Mol. Cell. Endocrinol. 2010, 314:204-212.
5. Melamed P., Savulescu D., Lim S., Wijeweera A., Luo Z., Luo M., Pnueli L. Gonadotrophin-releasing hormone signalling downstream of calmodulin. J. Neuroendocrinol. 2012, 24:1463-1475.
6. Pnueli L., Luo M., Wang S., Naor Z., Melamed P. Calcineurin mediates the gonadotropin-releasing hormone effect on expression of both subunits of the follicle-stimulating hormone through distinct mechanisms. Mol. Cell. Biol. 2011, 31:5023-5036.
7. Lim S., Luo M., Koh M., Yang M., Abdul Kadir M.Z., Tan J.H., Ye Z., Wang W., Melamed P. Distinct mechanisms involving diverse histone deacetylases repress expression of the two gonadotropin β-subunit genes in immature gonadotropes, and their actions are overcome by gonadotropin-releasing hormone. Mol. Cell. Biol. 2007, 27:4105-4120.
8. Melamed P. Histone deacetylases and repression of the gonadotropin genes. Trends Endocrinol. Metab. 2008, 19:25-31.
9. Santos-Rosa H., Schneider R., Bannister A.J., Sherriff J., Bernstein B.E., Emre N.C., Schreiber S.L., Mellor J., Kouzarides T. Active genes are tri-methylated at K4 of histone H3. Nature 2002, 419:407-411.
10. Schneider R., Bannister A.J., Myers F.A., Thorne A.W., Crane-Robinson C., Kouzarides T. Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat. Cell Biol. 2004, 6:73-77.
11. Barski A., Cuddapah S., Cui K., Roh T.Y., Schones D.E., Wang Z., Wei G., Chepelev I., Zhao K. High-resolution profiling of histone methylations in the human genome. Cell 2007, 129:823-837.
12. Mikkelsen T.S., Ku M., Jaffe D.B., Issac B., Lieberman E., Giannoukos G., Alvarez P., Brockman W., Kim T.K., Koche R.P., Lee W., Mendenhall E., O'Donovan A., Presser A., Russ C., Xie X., Meissner A., Wernig M., Jaenisch R., Nusbaum C., Lander E.S., Bernstein B.E. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007, 448:553-560.
13. Li B., Carey M., Workman J.L. The role of chromatin during transcription. Cell 2007, 128:707-719.
14. Shilatifard A. Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation. Curr. Opin. Cell Biol. 2008, 20:341-348.
15. Santos-Rosa H., Schneider R., Bernstein B.E., Karabetsou N., Morillon A., Weise C., Schreiber S.L., Mellor J., Kouzarides T. Methylation of histone H3 K4 mediates association of the Isw1p ATPase with chromatin. Mol. Cell 2003, 12:1325-1332.
16. Sims R.J., Reinberg D. Histone H3 Lys 4 methylation: caught in a bind?. Genes Dev. 2006, 20:2779-2786.
17. Taverna S.D., Ilin S., Rogers R.S., Tanny J.C., Lavender H., Li H., Baker L., Boyle J., Blair L.P., Chait B.T., Patel D.J., Aitchison J.D., Tackett A.J., Allis C.D. Yng1 PHD finger binding to H3 trimethylated at K4 promotes NuA3 HAT activity at K14 of H3 and transcription at a subset of targeted ORFs. Mol. Cell 2006, 24:785-796.
18. Wysocka J., Swigut T., Xiao H., Milne T.A., Kwon S.Y., Landry J., Kauer M., Tackett A.J., Chait B.T., Badenhorst P., Wu C., Allis C.D. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 2006, 442:86-90.
19. Vermeulen M., Mulder K.W., Denissov S., Pijnappel W.W.M.P., van Schaik F.M.A., Varier R.A., Baltissen M.P.A., Stunnenberg H.G., Mann M., Timmers H.T. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 2007, 131:58-69.
20. Shilatifard A. Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu. Rev. Biochem. 2006, 75:243-269.
21. Weake V.M., Workman J.L. Histone ubiquitination: triggering gene activity. Mol. Cell 2008, 29:653-663.
22. Eissenberg J.C., Shilatifard A. Histone H3 lysine 4 (H3K4) methylation in development and differentiation. Dev. Biol. 2010, 339:240-249.
23. Smith E., Shilatifard A. The chromatin signaling pathway: diverse mechanisms of recruitment of histone-modifying enzymes and varied biological outcomes. Mol. Cell 2010, 40:689-701.
24. Minsky N., Shema E., Field Y., Schuster M., Segal E., Oren M. Monoubiquitinated H2B is associated with the transcribed region of highly expressed genes in human cells. Nat. Cell Biol. 2008, 10:483-488.
25. Shema E., Tirosh I., Aylon Y., Huang J., Ye C., Moskovits N., Raver-Shapira N., Minsky N., Pirngruber J., Tarcic G., Hublarova P., Moyal L., Gana-Weisz M., Shiloh Y., Yarden Y., Johnsen S.A., Vojtesek B., Berger S.L., Oren M. The histone H2B-specific ubiquitin ligase RNF20/hBRE1 acts as a putative tumor suppressor through selective regulation of gene expression. Genes Dev. 2008, 22:2664-2676.
26. Lee J.S., Shukla A., Schneider J., Swanson S.K., Washburn M.P., Florens L., Bhaumik S.R., Shilatifard A. Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 2007, 131:1084-1096.
27. Soares L.M., Buratowski S. Histone crosstalk: H2Bub and H3K4 methylation. Mol. Cell 2013, 49:1019-1020.
28. Wu L., Lee S., Zhou B., Nguyen U.T.T., Muir T.M., Tan S., Dou Y. ASH2L regulates ubiquitylation signaling to MLL: trans-regulation of the H3K4 methylation in higher eukaryotes. Mol. Cell 2013, 49:1108-1120.
29. Shilatifard A. The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu. Rev. Biochem. 2012, 81:65-95.
30. Scacheri P.C., Davis S., Odom D.T., Crawford G.E., Perkins S., Halawi M.J., Agarwal S.K., Marx S.J., Spiegel A.M., Meltzer P.S., Collins F.S. Genome-wide analysis of menin binding provides insights into MEN1 tumorigenesis. PLoS Genet. 2006, 2:e51.
31. Luo Z., Wijeweera A., Oh Y., Liou Y.C., Melamed P. Pin1 facilitates the phosphorylation-dependent ubiquitination of SF1 to regulate gonadotropin β-subunit gene transcription. Mol. Cell. Biol. 2010, 30:745-763.
32. Savulescu D., Feng J., Ping Y.S., Mai O., Boehm U., He B., O'Malley B.W., Melamed P. Gonadotropin-releasing hormone-regulated prohibitin mediates apoptosis of the gonadotrope cells. Mol. Endocrinol. 2013, 27:1856-1870.
33. Feng J., Lawson M.A., Melamed P. A proteomic comparison of immature and mature mouse gonadotrophs reveals novel differentially expressed nuclear proteins that regulate gonadotropin gene transcription and RNA splicing. Biol. Reprod. 2008, 79:546-561.
34. Alder O., Lavial F., Helness A., Brookes E., Pinho S., Chandrashekran A., Arnaud P., Pombo A., O'Neill L., Azuara V. Ring1B and Suv39h1 delineate distinct chromatin states at bivalent genes during early mouse lineage commitment. Development 2010, 137:2483-2492.
35. Karnik S.K., Hughes C.M., Gu X., Rozenblastt-Rosen O., McLean G.W., Xiong Y., Meyerson M., Kim S.K. Menin regulates pancreatic islet growth by promoting histone methylation and expression of genes encoding p27Kip1 and p18INK4c. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:14659-14664.
36. Grembecka J., He S., Shi A., Purohit T., Muntean A.G., Sorenson R.J., Showalter H.D., Murai M.J., Belcher A.M., Hartley T., Hess J.L., Cierpicki T. Menin-MLL inhibitors reverse oncogenic activity of MLL fusion proteins in leukemia. Nat. Chem. Biol. 2012, 8:277-284.
37. Dreijerink K.M., Mulder K., Winkler G.S., Höppener J.W., Lips C.J., Timmers H.T. Menin links estrogen receptor activation to histone H3K4 trimethylation. Cancer Res. 2006, 66:4929-4935.
38. Matkar S., Thiel A., Hua X. Menin: a scaffold protein that controls gene expression and cell signaling. Trends Biochem. Sci. 2013, 38:394-402.
39. Luo M., Koh M., Feng J., Wu Q., Melamed P. Cross talk in hormonally regulated gene transcription through induction of estrogen receptor ubiquitylation. Mol. Cell. Biol. 2005, 25:7386-7398.
40. Zhao L., Bakke M., Krimkevich Y., Cushman L.J., Parlow A.F., Camper S.A., Parker K.L. Steroidogenic factor 1 (SF1) is essential for pituitary gonadotrope function. Development 2001, 128:147-154.
41. Pavri R., Zhu B., Li G., Trojer P., Mandal S., Shilatifard A., Reinberg D. Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 2006, 125:703-717.
42. Tanny J.C., Erdjument-Bromage H., Tempst P., Allis C.D. Ubiquitylation of histone H2B controls RNA polymerase II transcription elongation independently of histone H3 methylation. Genes Dev. 2007, 21:835-847.
43. Fleming A.B., Kao C.F., Hillyer C., Pikaart M., Osley M.A. H2B ubiquitylation plays a role in nucleosome dynamics during transcription elongation. Mol. Cell 2008, 31:57-66.
44. Wang P., Lin C., Smith E.R., Guo H., Sanderson B.W., Wu M., Gogol M., Alexander T., Seidel C., Wiedemann L.M., Ge K., Krumlauf R., Shilatifard A. Global analysis of H3K4 methylation defines MLL family member targets and points to a role for MLL1-mediated H3K4 methylation in the regulation of transcriptional initiation by RNA polymerase II. Mol. Cell. Biol. 2009, 29:6074-6085.
45. Pray-Grant M.G., Daniel J.A., Schieltz D., Yates J.R., Grant P.A. Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation. Nature 2005, 433:434-438.
46. Sims R.J., Chen C.F., Santos-Rosa H., Kouzarides T., Patel S.S., Reinberg D. Human but not yeast CHD1 binds directly and selectively to histone H3 methylated at lysine 4 via its tandem chromodomains. J. Biol. Chem. 2005, 280:41789-41792.
47. Nikolov M., Stützer A., Mosch K., Krasauskas A., Soeroes S., Stark H., Urlaub H., Fischle W. Chromatin affinity purification and quantitative mass spectrometry defining the interactome of histone modification patterns. Mol. Cell. Proteomics 2011, 10. (M110.005371).
48. Petty E., Pillus L. Balancing chromatin remodeling and histone modifications in transcription. Trends Genet. 2013, 29:621-629.
49. Hammer G.D., Krylova I., Zhang Y., Darimont B.D., Simpson K., Weigel N.L., Ingraham H.A. Phosphorylation of the nuclear receptor SF-1 modulates cofactor recruitment: integration of hormone signaling in reproduction and stress. Mol. Cell 1999, 3:521-526.
50. Desclozeaux M., Krylova I.N., Horn F., Fletterick R.J., Ingraham H.A. Phosphorylation and intramolecular stabilization of the ligand binding domain in the nuclear receptor steroidogenic factor 1. Mol. Cell. Biol. 2002, 22:7193-7203.
51. Fowkes R.C., Desclozeaux M., Patel M.V., Aylwin S.J., King P., Ingraham H.A., Burrin J.M. Steroidogenic factor-1 and the gonadotrope-specific element enhance basal and pituitary adenylate cyclase-activating polypeptide-stimulated transcription of the human glycoprotein hormone alpha-subunit gene in gonadotropes. Mol. Endocrinol. 2003, 17:2177-2188.
52. Lewis A.E., Rusten M., Hoivik E.A., Vikse E.L., Hansson M.L., Wallberg A.E., Bakke M. Phosphorylation of steroidogenic factor 1 is mediated by cyclin-dependent kinase 7. Mol. Endocrinol. 2008, 22:91-104.
53. Breen K.M., Thackray V.G., Coss D., Mellon P.L. Runt-related transcription factors impair activin induction of the follicle-stimulating hormone β-subunit gene. Endocrinology 2010, 151:2669-2680.
54. Tran S., Lamba P., Wang Y., Bernard D.J. SMADs and FOXL2 synergistically regulate murine Fshβ transcription via a conserved proximal promoter element. Mol. Endocrinol. 2011, 25:1170-1183.
55. Wang Q., Chikina M., Zaslavsky E., Pincas H., Sealfon S.C. β-catenin regulates GnRH-induced Fshβ gene expression. Mol. Endocrinol. 2013, 27:224-237.
56. Fierz B., Chatterjee C., McGinty R.K., Bar-Dagan M., Raleigh D.P., Muir T.W. Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction. Nat. Chem. Biol. 2011, 7:113-119.
57. Lee J.S., Garrett A.S., Yen K., Takahashi Y.H., Hu D., Jackson J., Seidel C., Pugh B.F., Shilatifard A. Codependency of H2B monoubiquitination and nucleosome reassembly on Chd1. Genes Dev. 2012, 26:914-919.
58. Yuen T., Wurmbach E., Ebersole B.J., Ruf F., Pfeffer R.L., Sealfon S.C. Coupling of GnRH concentration and the GnRH receptor-activated gene program. Mol. Endocrinol. 2002, 16:1145-1153.
59. Kakar S.S., Winters S.J., Zacharias W., Miller D.M., Flynn S. Identification of distinct gene expression profiles associated with treatment of LβT2 cells with gonadotropin-releasing hormone agonist using microarray analysis. Gene 2003, 308:67-77.
60. Zhang H., Bailey J.S., Coss D., Lin B., Tsutsumi R., Lawson M.A., Mellon P.L., Webster N.J. Activin modulates the transcriptional response of LβT2 cells to gonadotropin-releasing hormone and alters cellular proliferation. Mol. Endocrinol. 2006, 20:2909-2930.
61. Buro L.J., Chipumuro E., Henriksen M.A. Menin and RNF20 recruitment is associated with dynamic histone modifications that regulate signal transducer and activator of transcription 1 (STAT1)-activated transcription of the interferon regulatory factor 1 gene (IRF1). Epigenetics Chromatin 2010, 3:16.
62. Edmunds J.W., Mahadevan L.C., Clayton A.L. Dynamic histone H3 methylation during gene induction: HYPB/Setd2 mediates all H3K36 trimethylation. EMBO J. 2008, 27:406-420.
63. Métivier R., Penot G., Hübner M.R., Reid G., Brand H., Kos M., Gannon F. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 2003, 115:751-763.
64. Dreijerink K.M., Lips C.J., Timmers H.T. Multiple endocrine neoplasia type 1: a chromatin writer's block. J. Intern. Med. 2009, 266:53-59.
65. Milne T.A., Hughes C.M., Lloyd R., Yang Z., Rozenblatt-Rosen O., Dou Y., Schnepp R.W., Krankel C., Livolsi V.A., Gibbs D., Hua X., Roeder R.G., Meyerson M., Hess J.L. Menin and MLL cooperatively regulate expression of cyclin-dependent kinase inhibitors. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:749-754.