Msx1 homeodomain protein represses the αGSU and GnRH receptor genes during gonadotrope development

Molecular Endocrinology

Volumn 27, Issue 3, 2013, Pages 422-436

  Xie, Huimin ^a   Cherrington, Brian D ^a,b   Meadows, Jason D ^a   Witham, Emily A ^a   Mellon, Pamela L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WYOMING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; ALPHA GLYCOPROTEIN SUBUNIT; DLX2 PROETIN; DLX3 PROTEIN; DOWNSTREAM ACTIVIN REGULATORY ELEMENT; GLYCOPROTEIN; GONADORELIN RECEPTOR; HOMEODOMAIN PROTEIN; MESSENGER RNA; PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR MSX1; UNCLASSIFIED DRUG;

ARTICLE; GENE EXPRESSION; GENE MUTATION; GENE REPRESSION; NONHUMAN; PRIORITY JOURNAL; RECEPTOR GENE; WILD TYPE;

ANIMALS; BASE SEQUENCE; BINDING SITES; CELL DIFFERENTIATION; CELL LINE; CONSENSUS SEQUENCE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOPROTEIN HORMONES, ALPHA SUBUNIT; GONADOTROPHS; HOMEODOMAIN PROTEINS; HUMANS; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; MSX1 TRANSCRIPTION FACTOR; PITUITARY GLAND, ANTERIOR; RATS; RECEPTORS, LHRH; REPRESSOR PROTEINS; RESPONSE ELEMENTS; RNA, MESSENGER; RNA, SMALL INTERFERING; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84874520346     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2012-1289     Document Type: Article

References (66)

1. Simmons DM, Voss JW, Ingraham HA, et al. Pituitary cell phenotypes involve cell-specific Pit-1 mRNA translation and synergistic interactions with other classes of transcription factors. Genes Dev. 1990;4:695-711.
2. Scully KM, Rosenfeld MG. Pituitary development: regulatory codes in mammalian organogenesis. Science. 2002;295:2231-2235.
3. Windle JJ, Weiner RI, Mellon PL. Cell lines of the pituitary gonadotrope lineage derived by targeted oncogenesis in transgenic mice. Mol Endocrinol. 1990;4:597-603.
4. Alarid ET, Windle JJ, Whyte DB, Mellon PL. Immortalization of pituitary cells at discrete stages of development by directed oncogenesis in transgenic mice. Development. 1996;122:3319-3329.
5. Lew D, Brady H, Klausing K, et al. GHF-1 promoter-targeted immortalization of a somatotropic progenitor cell results in dwarfism in transgenic mice. Genes Dev. 1993;7:683-693.
6. Pernasetti F, Spady TJ, Hall SB, et al. Pituitary tumorigenesis targeted by the ovine follicle-stimulating hormone β-subunit gene regulatory region in transgenic mice. Mol Cell Endocrinol. 2003;203: 169-183.
7. Yusta B, Alarid ET, Gordon DF, Ridgway EC, Mellon PL. The thyrotropin β-subunit gene is repressed by thyroid hormone in a novel thryrotrope cell line, mouse TαT1 cells. Endocrinology. 1998;139:4476-4482.
8. Pernasetti F, Vasilyev VV, Rosenberg SB, et al. Cell-specific transcriptional regulation of FSHβ by activin and GnRH in the LβT2 pituitary gonadotrope cell model. Endocrinology. 2001;142:2284-2295.
9. Graham KE, Nusser KD, Low MJ. LβT2 gonadotroph cells secrete follicle stimulating hormone (FSH) in response to activin A. J Endocrinol. 1999;162:R1-R5.
10. McGillivray SM, Bailey JS, Ramezani R, Kirkwood BJ, Mellon PL. Mouse GnRH receptor gene expression is mediated by the LHX3 homeodomain protein. Endocrinology. 2005;146:2180-2185.
11. Barnhart KM, Mellon PL. The orphan nuclear receptor, steroidogenic factor-1, regulates the glycoprotein hormone β-subunit gene in pituitary gonadotropes. Mol Endocrinol. 1994;8:878-885.
12. Steger DJ, Hecht JH, Mellon PL. GATA-binding proteins regulate the human gonadotropin β-subunit gene in placenta and pituitary gland. Mol Cell Biol. 1994;14:5592-5602.
13. Alarid ET, Holley S, Hayakawa M, Mellon PL. Discrete stages of anterior pituitary differentiation recapitulated in immortalized cell lines. Mol Cell Endocrinol. 1998;140:25-30.
14. Rosenberg SB, Mellon PL. An Otx-related homeodomain protein binds an LHβ promoter element important for activation during gonadotrope maturation. Mol Endocrinol. 2002;16:1280-1298.
15. Harris AN, Mellon PL. The basic helix-loop-helix leucine zipper transcription factor USF is a key regulator of SF-1 gene expression in pituitary gonadotrope and steroidogenic cells. Mol Endocrinol. 1998;12:714-727.
16. Corpuz PS, Lindaman LL, Mellon PL, Coss D. FoxL2 is required for activin induction of the mouse and human follicle-stimulating hormone β-subunit genes. Mol Endocrinol. 2010;24:1037-1051.
17. Breen KM, Thackray VG, Coss D, Mellon PL. Runt-related transcription factors impair activin induction of the follicle-stimulating hormone β-subunit gene. Endocrinology. 2010;151:2669-2680.
18. Ghochani Y, Saini JK, Mellon PL, Thackray VG. FOXL2 is involved in the synergy between activin and progestins on the folliclestimulating hormone β-subunit promoter. Endocrinology. 2012; 153:2023-2033.
19. Lamba P, Fortin J, Tran S, Wang Y, Bernard DJ. A novel role for the forkhead transcription factor FOXL2 in activin A-regulated follicle-stimulating hormone β subunit transcription. Mol Endocrinol. 2009;23:1001-1013.
20. Halvorson LM, Kaiser UB, Chin WW. Stimulation of luteinizing hormone β gene promoter activity by the orphan nuclear receptor, steroidogenic factor-1. J Biol Chem. 1996;271:6645-6650.
21. Keri RA, Nilson JH. A steroidogenic factor-1 binding site is required for activity of the luteinizing hormone β subunit promoter in gonadotropes of transgenic mice. J Biol Chem. 1996;271:10782-10785.
22. Mackenzie A, Fergusson MWJ, Sharpie PT. Hox-7 expression during murine craniofacial development. Development. 1991;113: 601-611.
23. Bendall AJ, Abate-Shen C. Roles for Msx and Dlx homeoproteins in vertebrate development. Gene. 2000;247:17-31.
24. Zhang H, Catron KM, Abate-Shen C. A role for the Msx-1 homeodomain in transcriptional regulation: residues in the N-terminal arm mediate TATA binding protein interaction and transcriptional repression. Proc Natl Acad Sci USA. 1996;93:1764-1769.
25. MacKenzie A, Ferguson MW, Sharpe PT. Expression patterns of the homeobox gene, Hox-8, in the mouse embryo suggest a role in specifying tooth initiation and shape. Development. 1992;115: 403-420.
26. Alappat S, Zhang ZY, Chen YP. Msx homeobox gene family and craniofacial development. Cell Res. 2003;13:429-442.
27. Satokata I, Maas R. Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat Genet. 1994;6:348-356.
28. Catron KM, Wang H, Hu G, Shen MM, Abate-Shen C. Comparison of MSX-1 and MSX-2 suggests a molecular basis for functional redundancy. Mech Dev. 1996;55:185-199.
29. Catron KM, Zhang H, Marshall SC, Inostroza JA, Wilson JM, Abate C. Transcriptional repression by Msx-1 does not require homeodomain DNA-binding sites. Mol Cell Biol. 1995;15:861-871.
30. Zhang H, Hu G, Wang H, et al. Heterodimerization of Msx and Dlx homeoproteins results in functional antagonism. Mol Cell Biol. 1997;17:2920-2932.
31. Zerucha T, Stuhmer T, Hatch G, et al. A highly conserved enhancer in the Dlx5/Dlx6 intergenic region is the site of cross-regulatory interactions between Dlx genes in the embryonic forebrain. J Neurosci. 2000;20:709-721.
32. Yu G, Zerucha T, Ekker M, Rubenstein JL. Evidence that GRIP, a PDZ-domain protein which is expressed in the embryonic forebrain, co-activates transcription with DLX homeodomain proteins. Brain Res Dev Brain Res. 2001;130:217-230.
33. Givens ML, Rave-Harel N, Goonewardena VD, et al. Developmental regulation of gonadotropin-releasing hormone gene expression by the MSX and DLX homeodomain protein families. J Biol Chem. 2005;280:19156-19165.
34. Koop KE, MacDonald LM, Lobe CG. Transcripts of Grg4, a murine groucho-related gene, are detected in adjacent tissues to other murine neurogenic gene homologues during embryonic development. Mech Dev. 1996;59:73-87.
35. Leon C, Lobe CG. Grg3, a murine Groucho-related gene, is expressed in the developing nervous system and in mesenchyme-induced epithelial structures. Dev Dyn. 1997;208:11-24.
36. Dehni G, Liu Y, Husain J, Stifani S. TLE expression correlates with mouse embryonic segmentation, neurogenesis, and epithelial determination. Mech Dev. 1995;53:369-381.
37. Mallo M, Franco del Amo F, Gridley T. Cloning and developmental expression of Grg, a mouse gene related to the groucho transcript of the Drosophila enhancer of split complex. Mech Dev. 1993;42:67-76.
38. Paroush Z, Finley RL, Kidd T, Weinwright SM, Ingham PI, Brent RI, Ish-Horowicz D. Groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with Hairy-related bHLH proteins. Cell. 1994;79:805-815.
39. Larder R, Mellon PL. Otx2 induction of the gonadotropin-releasing hormone promoter is modulated by direct interactions with Grg co-repressors. J Biol Chem. 2009;284:16966-16978.
40. Rave-Harel N, Miller NL, Givens ML, Mellon PL. The Grouchorelated gene family regulates the gonadotropin-releasing hormone gene through interaction with the homeodomain proteins MSX1 and OCT1. J Biol Chem. 2005;280:30975-30983.
41. Mallo M, Gendron-Maguire M, Harbison ML, Gridley T. Protein characterization and targeted disruption of Grg, a mouse gene related to the groucho transcript of the Drosophila enhancer of split complex. Dev Dyn. 1995;204:338-347.
42. Brinkmeier ML, Potok MA, Cha KB, et al. TCF and Grouchorelated genes influence pituitary growth and development. Mol Endocrinol. 2003;17:2152-2161.
43. Carvalho LR, Brinkmeier ML, Castinetti F, Ellsworth BS, Camper SA. Corepressors TLE1 and TLE3 interact with HESX1 and PROP1. Mol Endocrinol. 2010;24:754-765.
44. Duval DL, Nelson SE, Clay CM. The tripartite basal enhancer of the gonadotropin-releasing hormone (GnRH) receptor gene promoter regulates cell-specific expression through a novel GnRH receptor activating sequence. Mol Endocrinol. 1997;11:1814-1821.
45. Cherrington BD, Farmerie TA, Lents CA, Cantlon JD, Roberson MS, Clay CM. Activin responsiveness of the murine gonadotropinreleasing hormone receptor gene is mediated by a composite enhancer containing spatially distinct regulatory elements. Mol Endocrinol. 2005;19:898-912.
46. Sasson R, Luu SH, Thackray VG, Mellon PL. Glucocorticoids induce human glycoprotein hormone β-subunit gene expression in the gonadotrope. Endocrinology. 2008;149:3643-3655.
47. Cherrington BD, Bailey JS, Diaz AL, Mellon PL. NeuroD1 and Mash1 temporally regulate GnRH receptor gene expression in immortalized mouse gonadotrope cells. Mol Cell Endocrinol. 2008; 295:106-114.
48. Miller NL, Wevrick R, Mellon PL. Necdin, a Prader-Willi syndrome candidate gene, regulates gonadotropin-releasing hormone neurons during development. Hum Mol Genet. 2009;18:248-260.
49. Houzelstein D, Cohen A, Buckingham ME, Robert B. Insertional mutation of the mouse Msx1 homeobox gene by an nlacZ reporter gene. Mech Dev. 1997;65:123-133.
50. Driegen S, Ferreira R, van Zon A, et al. A generic tool for biotinylation of tagged proteins in transgenic mice. Transgenic Res. 2005; 14:477-482.
51. Wang J, Kumar RM, Biggs VJ, et al. The Msx1 homeoprotein recruits Polycomb to the nuclear periphery during development. Dev Cell. 2011;21:575-588.
52. Sarapura VD, Strouth HL, Gordon DF, Wood WM, Ridgway EC. MsxI is present in thyrotropic cells and binds to a consensus site on the glycoprotein hormone β-subunit promoter. Mol Endocrinol. 1997;11:1782-1794.
53. Kam KY, Jeong KH, Norwitz ER, Jorgensen EM, Kaiser UB. Oct-1 and nuclear factorYbind to the SURG-1 element to direct basal and gonadotropin-releasing hormone (GnRH)-stimulated mouse GnRH receptor gene transcription. Mol Endocrinol. 2005;19:148-162.
54. Roberson MS, Meermann S, Morasso MI, Mulvaney-Musa JM, Zhang T. A role for the homeobox protein Distal-less 3 in the activation of the glycoprotein hormone β subunit gene in choriocarcinoma cells. J Biol Chem. 2001;276:10016-10024.
55. Jiang Q, Jeong KH, Horton CD, Halvorson LM. Pituitary homeobox 1 (Pitx1) stimulates rat LHβ gene expression via two functional DNA-regulatory regions. J Mol Endocrinol. 2005;35:145-158.
56. DiMattia GE, Rhodes SJ, Krones A, et al. The Pit-1 gene is regulated by distinct early and late pituitary-specific enhancers. Dev Biol. 1997;182:180-190.
57. Johnston JD, Klosen P, Barrett P, Hazlerigg DG. Regulation of MT melatonin receptor expression in the foetal rat pituitary. J Neuroendocrinol. 2006;18:50-56.
58. Li S, Crenshaw EB, Rawson EJ, Simmons DM, Swanson LW, Rosenfeld MG. Dwarf locus mutants lacking three pituitary cell types result from mutations in the POU-domain gene pit-1. Nature. 1990;347:528-533.
59. Nilson JH, Bokar JA, Clay CM, et al. Different combinations of regulatory elements may explain why placenta-specific expression of the glycoprotein hormoneβ-subunit gene occurs only in primates and horses. Biol Reprod. 1991;44:231-237.
60. Maurer RA, Kim KE, Schoderbek WE, Roberson MS, Glenn DJ. Regulation of glycoprotein hormone β-subunit gene expression. Recent Prog Horm Res. 1999;54:455-484.
61. Heckert LL, Schultz K, Nilson JH. Different composite regulatory elements direct expression of the human βsubunit gene to pituitary and placenta. J Biol Chem. 1995;270:26497-26504.
62. Budworth PR, Quinn PG, Nilson JH. Multiple characteristics of a pentameric regulatory array endow the human β-subunit glycoprotein hormone promoter with trophoblast specificity and maximal activity. Mol Endocrinol. 1997;11:1669-1680.
63. Yu X, Li P, Roeder RG, Wang Z. Inhibition of androgen receptormediated transcription by amino-terminal enhancer of split. Mol Cell Biol. 2001;21:4614-4625.
64. Palaparti A, Baratz A, Stifani S. The Groucho/transducin-like enhancer of split transcriptional repressors interact with the genetically defined amino-terminal silencing domain of histone H3. J Biol Chem. 1997;272:26604-26610.
65. Salisbury TB, Binder AK, Nilson JH. Welcoming β-catenin to the GnRH transcriptional network in gonadotropes. Mol Endocrinol. 2008;22:1295-1303.
66. Doyle JP, Dougherty JD, Heiman M, et al. Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell. 2008;135:749-762.