Paired-like homeodomain transcription factors 1 and 2 regulate follicle-stimulating hormone β-subunit transcription through a conserved cis-element

Endocrinology

Volumn 149, Issue 6, 2008, Pages 3095-3108

  Lamba, Pankaj ^a,b   Khivansara, Vishal ^b   D'Alessio, Ana C ^a   Santos, Michelle M ^b   Bernard, Daniel J ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b POPULATION COUNCIL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOLLITROPIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FSH BETA; TRANSCRIPTION FACTOR PITX 1; TRANSCRIPTION FACTOR PITX2;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOUTHERN BLOTTING;

ANIMALS; BASE SEQUENCE; CATTLE; CHROMATIN; CONSERVED SEQUENCE; FOLLICLE STIMULATING HORMONE, BETA SUBUNIT; GENES, REPORTER; HOMEODOMAIN PROTEINS; HUMANS; LUCIFERASES; MICE; PAIRED BOX TRANSCRIPTION FACTORS; RNA, SMALL INTERFERING; SHEEP; SWINE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 42549138372     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2007-0425     Document Type: Article

References (62)

1. Brown P, McNeilly AS 1999 Transcriptional regulation of pituitary gonadotrophin subunit genes. Rev Reprod 4:117-124
2. Alarid ET, Windle JJ, Whyte DB, Mellon PL 1996 Immortalization of pituitary cells at discrete stages of development by directed oncogenesis in transgenic mice. Development 122:3319-3329
3. Pernasetti F, Vasilyev VV, Rosenberg SB, Bailey JS, Huang HJ, Miller WL, Mellon PL 2001 Cell-specific transcriptional regulation of follicle-stimulating hormone-β by activin and gonadotropin-releasing hormone in the LβT2 pituitary gonadotrope cell model. Endocrinology 142:2284-2295
4. Gregory SJ, Lacza CT, Detz AA, Xu S, Petrillo LA, Kaiser UB 2005 Synergy between activin A and gonadotropin-releasing hormone in transcriptional activation of the rat follicle-stimulating hormone-β gene. Mol Endocrinol 19: 237-254
5. Bernard DJ 2004 Both SMAD2 and SMAD3 mediate activin-stimulated expression of the follicle-stimulating hormone β-subunit in mouse gonadotrope cells. Mol Endocrinol 18:606-623
6. Bailey JS, Rave-Harel N, McGillivray SM, Coss D, Mellon PL 2004 Activin regulation of the follicle-stimulating hormone β-subunit gene involves Smads and the TALE homeodomain proteins Pbx1 and Prep1. Mol Endocrinol 18:1158-1170
7. Suszko MI, Balkin DM, Chen Y, Woodruff TK 2005 Smad3 mediates activin-induced transcription of follicle-stimulating hormone β-subunit gene. Mol Endocrinol 19:1849-1858
8. Suszko MI, Lo DJ, Suh H, Camper SA, Woodruff TK 2003 Regulation of the rat follicle-stimulating hormone 7beta;-subunit promoter by activin. Mol Endocrinol 17:318-332
9. West BE, Parker GE, Savage JJ, Kiratipranon P, Toomey KS, Beach LR, Colvin SC, Sloop KW, Rhodes SJ 2004 Regulation of the follicle-stimulating hormone β gene by the LHX3 LIM-homeodomain transcription factor. Endocrinology 145:4866-4879
10. Zakaria MM, Jeong KH, Lacza C, Kaiser UB 2002 Pituitary homeobox 1 activates the rat FSHβ (rFSHβ) gene through both direct and indirect interactions with the rFSHβ gene promoter. Mol Endocrinol 16:1840-1852
11. Lamba P, Santos MM, Philips DP, Bernard DJ 2006 Acute regulation of murine follicle-stimulating hormone β-subunit transcription by activin A. J Mol Endocrinol 36:201-220
12. Safwat N, Ninomiya-Tsuji J, Gore AJ, Miller WL 2005 Transforming growth factor β-activated kinase 1 is a key mediator of ovine follicle-stimulating hormone β-subunit expression. Endocrinology 146:4814-4824
13. Huang HJ, Sebastian J, Strahl BD, Wu JC, Miller WL 2001 The promoter for the ovine follicle-stimulating hormone-β gene (FSHβ) confers FSHβ-like expression on luciferase in transgenic mice: regulatory studies in vivo and in vitro. Endocrinology 142:2260-2266
14. Huang HJ, Sebastian J, Strahl BD, Wu JC, Miller WL 2001 Transcriptional regulation of the ovine follicle-stimulating hormone-β gene by activin and gonadotropin-releasing hormone (GnRH): involvement of two proximal activator protein-1 sites for GnRH stimulation. Endocrinology 142:2267-2274
15. Lamonerie T, Tremblay JJ, Lanctot C, Therrien M, Gauthier Y, Drouin J 1996 Ptx1, a bicoid-related homeo box transcription factor involved in transcription of the pro-opiomelanocortin gene. Genes Dev 10:1284-1295
16. Drouin J, Lamolet B, Lamonerie T, Lanctot C, Tremblay JJ 1998 The PTX family of homeodomain transcription factors during pituitary developments. Mol Cell Endocrinol 140:31-36
17. Charles MA, Suh H, Hjalt TA, Drouin J, Camper SA, Gage PJ 2005 PITX genes are required for cell survival and Lhx3 activation. Mol Endocrinol 19:1893-1903
18. Pellegrini-Bouiller I, Manrique C, Gunz G, Grino M, Zamora AJ, Figarella-Branger D, Grisoli F, Jaquet P, Enjalbert A 1999 Expression of the members of the Ptx family of transcription factors in human pituitary adenomas. J Clin Endocrinol Metab 84:2212-2220
19. Lanctot C, Gauthier Y, Drouin J 1999 Pituitary homeobox 1 (Ptx1) is differentially expressed during pituitary development. Endocrinology 140:1416-1422
20. Quentien MH, Manfroid I, Moncet D, Gunz G, Muller M, Grino M, Enjalbert A, Pellegrini I 2002 Pitx factors are involved in basal and hormone-regulated activity of the human prolactin promoter. J Biol Chem 277:44408-44416
21. Tremblay JJ, Lanctot 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 12:428-441
22. Tremblay JJ, Goodyer CG, Drouin J 2000 Transcriptional properties of Ptx1 and Ptx2 isoforms. Neuroendocrinology 71:277-286
23. Jeong KH, Chin WW, Kaiser UB 2004 Essential role of the homeodomain for pituitary homeobox 1 activation of mouse gonadotropin-releasing hormone receptor gene expression through interactions with c-Jun and DNA. Mol Cell Biol 24:6127-6139
24. Quirk CC, Lozada KL, Keri RA, Nilson JH 2001 A single Pitx1 binding site is essential for activity of the LHβ promoter in transgenic mice. Mol Endocrinol 15:734-746
25. Hjalt TA, Semina EV 2005 Current molecular understanding of Axenfeld-Rieger syndrome. Expert Rev Mol Med 7:1-17
26. Semina EV, Reiter R, Leysens NJ, Alward WL, Small KW, Datson NA, Siegel-Bartelt J, Bierke-Nelson D, Bitoun P, Zabel BU, Carey JC, Murray JC 1996 Cloning and characterization of a novel bicoid-related homeobox transcription factor gene, RIEG, involved in Rieger syndrome. Nat Genet 14:392-399
27. Arakawa H, Nakamura T, Zhadanov AB, Fidanza V, Yano T, Bullrich F, Shimizu M, Blechman J, Mazo A, Canaani E, Croce CM 1998 Identification and characterization of the ARP1 gene, a target for the human acute leukemia ALL1 gene. Proc Natl Acad Sci USA 95:4573-4578
28. Gage PJ, Camper SA 1997 Pituitary homeobox 2, a novel member of the bicoid-related family of homeobox genes, is a potential regulator of anterior structure formation. Hum Mol Genet 6:457-464
29. Semina EV, Reiter RS, Murray JC 1997 Isolation of a new homeobox gene belonging to the Pitx/Rieg family: expression during lens development and mapping to the aphakia region on mouse chromosome 19. Hum Mol Genet 6:2109-2116
30. Gage PJ, Suh H, Camper SA 1999 The bicoid-related Pitx gene family in development. Mamm Genome 10:197-200
31. Dave V, Zhao C, Yang F, Tung CS, Ma J 2000 Reprogrammable recognition codes in bicoid homeodomain-DNA interaction. Mol Cell Biol 20:7673-7684
32. Gehring WJ, Affolter M, Burglin T 1994 Homeodomain proteins. Annu Rev Biochem 63:487-526
33. Wilson DS, Sheng G, Jun S, Desplan C 1996 Conservation and diversification in homeodomain-DNA interactions: a comparative genetic analysis. Proc Natl Acad Sci USA 93:6886-6891
34. Chaney BA, Clark-Baldwin K, Dave V, Ma J, Rance M 2005 Solution structure of the K50 class homeodomain PITX2 bound to DNA and implications for mutations that cause Rieger syndrome. Biochemistry 44:7497-7511
35. Baird-Titus JM, Clark-Baldwin K, Dave V, Caperelli CA, Ma J, Rance M 2006 The solution structure of the native K50 bicoid homeodomain bound to the consensus TAATCC DNA-binding site. J Mol Biol 356:1137-1151
36. Coss D, Thackray VG, Deng CX, Mellon PL 2005 Activin regulates luteinizing hormone β-subunit gene expression through Smad-binding and homeobox elements. Mol Endocrinol 19:2610-2623
37. Salisbury TB, Binder AK, Grammer JC, Nilson JH 2007 Maximal activity of the luteinizing hormone β-subunit gene requires β-catenin. Mol Endocrinol 21:963-971
38. Rosenberg SB, Mellon PL 2002 An Otx-related homeodomain protein binds an LHβ promoter element important for activation during gonadotrope maturation. Mol Endocrinol 16:1280-1298
39. Espinoza HM, Cox CJ, Semina EV, Amendt BA 2002 A molecular basis for differential developmental anomalies in Axenfeld-Rieger syndrome. Hum Mol Genet 11:743-753
40. Gehring WJ, Qian YQ, Billeter M, Furukubo-Tokunaga K, Schier AF, Resendez-Perez D, Affolter M, Otting G, Wuthrich K 1994 Homeodomain-DNA recognition. Cell 78:211-223
41. Saadi I, Semina EV, Amendt BA, Harris DJ, Murphy KP, Murray JC, Russo AF 2001 Identification of a dominant negative homeodomain mutation in Rieger syndrome. J Biol Chem 276:23034-23041
42. Cox CJ, Espinoza HM, McWilliams B, Chappell K, Morton L, Hjalt TA, Semina EV, Amendt BA 2002 Differential regulation of gene expression by PITX2 isoforms. J Biol Chem 277:25001-25010
43. Saadi I, Kuburas A, Engle JJ, Russo AF 2003 Dominant negative dimerization of a mutant homeodomain protein in Axenfeld-Rieger syndrome. Mol Cell Biol 23:1968-1982
44. Melamed P, Koh M, Preklathan P, Bei L, Hew C 2002 Multiple mechanisms for Pitx-1 transactivation of a luteinizing hormone β-subunit gene. J Biol Chem 277:26200-26207
45. Burz DS, Rivera-Pomar R, Jackle H, Hanes SD 1998 Cooperative DNAbinding by Bicoid provides a mechanism for threshold-dependent gene activation in the Drosophila embryo. EMBO J 17:5998-6009
46. Green PD, Hjalt TA, Kirk DE, Sutherland LB, Thomas BL, Sharpe PT, Snead ML, Murray JC, Russo AF, Amendt BA 2001 Antagonistic regulation of Dlx2 expression by PITX2 and Msx2: implications for tooth development. Gene Expr 9:265-281
47. McGregor AP 2005 How to get ahead: the origin, evolution and function of bicoid. Bioessays 27:904-913
48. Gore AJ, Philips DP, Miller WL, Bernard DJ 2005 Differential regulation of follicle stimulating hormone by activin A and TGFB1 in murine gonadotropes. Reprod Biol Endocrinol 3:73
49. Kumar TR, Schuff KG, Nusser KD, Low MJ 2006 Gonadotroph-specific expression of the human follicle stimulating hormone β gene in transgenic mice. Mol Cell Endocrinol 247:103-115
50. Quentien MH, Pitoia F, Gunz G, Guillet MP, Enjalbert A, Pellegrini I 2002 Regulation of prolactin, GH, and Pit-1 gene expression in anterior pituitary by Pitx2: an approach using Pitx2 mutants. Endocrinology 143:2839-2851
51. Quentien MH, Barlier A, Franc JL, Pellegrini I, Brue T, Enjalbert A 2006 Pituitary transcription factors: from congenital deficiencies to gene therapy. J Neuroendocrinol 18:633-642
52. Hjalt TA, Amendt BA, Murray JC 2001 PITX2 regulates procollagen lysyl hydroxylase (PLOD) gene expression: implications for the pathology of Rieger syndrome. J Cell Biol 152:545-552
53. Amendt BA, Sutherland LB, Russo AF 1999 Multifunctional role of the Pitx2 homeodomain protein C-terminal tail. Mol Cell Biol 19:7001-7010
54. Lanctot C, Moreau A, Chamberland M, Tremblay ML, Drouin J 1999 Hindlimb patterning and mandible development require the Ptx1 gene. Development 126:1805-1810
55. Szeto DP, Rodriguez-Esteban C, Ryan AK, O'Connell SM, Liu F, Kioussi C, Gleiberman AS, Izpisua-Belmonte JC, Rosenfeld MG 1999 Role of the Bicoid-related homeodomain factor Pitx1 in specifying hindlimb morphogenesis and pituitary development. Genes Dev 13:484-494
56. Kitamura K, Miura H, Miyagawa-Tomita S, Yanazawa M, Katoh-Fukui Y, Suzuki R, Ohuchi H, Suehiro A, Motegi Y, Nakahara Y, Kondo S, Yokoyama M 1999 Mouse Pitx2 deficiency leads to anomalies of the ventral body wall, heart, extra- and periocular mesoderm and right pulmonary isomerism. Development 126:5749-5758
57. Gage PJ, Suh H, Camper SA 1999 Dosage requirement of Pitx2 for development of multiple organs. Development 126:4643-4651
58. Lin CR, Kioussi C, O'Connell S, Briata P, Szeto D, Liu F, Izpisua-Belmonte JC, Rosenfeld MG 1999 Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature 401:279-282
59. Suszko MI, Antenos M, Balkin DM, Woodruff TK 2008 Smad3 and Pitx2 cooperate in stimulation of FSHβ gene transcription. Mol Cell Endocrinol 281:27-36
60. McGillivray SM, Thackray VG, Coss D, Mellon PL 2007 Activin and glucocorticoids synergistically activate follicle-stimulating hormone β-subunit gene expression in the immortalized LβT2 gonadotrope cell line. Endocrinology 148:762-773
61. Tremblay JJ, Marcil A, Gauthier Y, Drouin J 1999 Ptx1 regulates SF-1 activity by an interaction that mimics the role of the ligand-binding domain. EMBO J 18:3431-3441
62. Lamba P, Hjalt TA, Bernard DJ 28 March 2008 Novel forms of Paired-like homeodomain transcription factor 2 (PITX2): generation by alternative translation initiation and mRNA splicing. BMC Mol Biol 9:31 [Epub ahead of print]