Expression of Pit-1 in Nonsomatotrope Cell Lines Induces Human Growth Hormone Locus Control Region Histone Modification and hGH-N Transcription

Journal of Molecular Biology

Volumn 390, Issue 1, 2009, Pages 26-44

  Hogan, Katherine A ^a   Jefferson, Holly S ^a   Karschner, Vesna A ^a   Shewchuk, Brian M ^a  

^a EAST CAROLINA UNIVERSITY   (United States)

Author keywords

chromatin; growth hormone; locus control region; Pit 1; transcription factor

Indexed keywords

CD79B ANTIGEN; HISTONE; HUMAN GROWTH HORMONE; TRANSCRIPTION FACTOR PIT 1;

ACETYLATION; ARTICLE; B LYMPHOCYTE; BINDING SITE; CHROMATIN; CONTROLLED STUDY; DNA MODIFICATION; GENETIC TRANSCRIPTION; GROWTH HORMONE SECRETING CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REGULATOR GENE; TRANSCRIPTION INITIATION;

MUS MUSCULUS; RODENTIA;

EID: 67349186632     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.04.081     Document Type: Article

References (67)

1. Horn P.J., and Peterson C.L. Chromatin higher order folding-wrapping up transcription. Science 297 (2002) 1824-1827
2. Khorasanizadeh S. The nucleosome: from genomic organization to genomic regulation. Cell 116 (2004) 259-272
3. Workman J.L., and Kingston R.E. Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu. Rev. Biochem. 67 (1998) 545-579
4. Mellor J. The dynamics of chromatin remodeling at promoters. Mol. Cell 19 (2005) 147-157
5. Bossard P., and Zaret K.S. GATA transcription factors as potentiators of gut endoderm differentiation. Development 125 (1998) 4909-4917
6. Eissenberg J.C. Decisive factors: a transcription activator can overcome heterochromatin silencing. BioEssays 23 (2001) 767-771
7. Soutoglou E., and Talianidis I. Coordination of PIC assembly and chromatin remodeling during differentiation-induced gene activation. Science 295 (2002) 1901-1904
8. Gualdi R., Bossard P., Zheng M., Hamada Y., Coleman J.R., and Zaret K.S. Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control. Genes Dev. 10 (1996) 1670-1682
9. Cirillo L.A., and Zaret K.S. An early developmental transcription factor complex that is more stable on nucleosome core particles than on free DNA. Mol. Cell 4 (1999) 961-969
10. Maier H., Ostraat R., Gao H., Fields S., Shinton S.A., Medina K.L., et al. Early B cell factor cooperates with Runx1 and mediates epigenetic changes associated with mb-1 transcription. Nat. Immunol. 5 (2004) 1069-1077
11. Cuesta I., Zaret K., and Santisteban P. The Forkhead factor FoxE1 binds to the thyroperoxidase promoter during thyroid cell differentiation and modifies compacted chromatin structure. Mol. Cell. Biol. 27 (2007) 7302-7314
12. Cirillo L.A., Lin F.R., Cuesta I., Friedman D., Jarnik M., and Zaret K.S. Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol. Cell 9 (2002) 279-289
13. Scully K.M., and Rosenfeld M.G. Pituitary development: regulatory codes in mammalian organogenesis. Science 295 (2002) 2231-2235
14. Zhu X., Gleiberman A.S., and Rosenfeld M.G. Molecular physiology of pituitary development: signaling and transcriptional networks. Physiol. Rev. 87 (2007) 933-963
15. Simmons D.M., Voss J.W., Ingraham H.A., Holloway J.M., Broide R.S., Rosenfeld M.G., and Swanson L.W. Pituitary cell phenotypes involve cell-specific Pit-1 mRNA translation and synergistic interactions with other classes of transcription factors. Genes Dev. 4 (1990) 695-711
16. Li S., Crenshaw III E.B., Rawson E.J., Simmons D.M., Swanson L.W., and Rosenfeld M.G. Dwarf locus mutants lacking three pituitary cell types result from mutations in the POU-domain gene pit-1. Nature 347 (1990) 528-533
17. Pfaffle R.W., DiMattia G.E., Parks J.S., Brown M.R., Wit J.M., Jansen M., et al. Mutation of the POU-specific domain of Pit-1 and hypopituitarism without pituitary hypoplasia. Science 257 (1992) 1118-1121
18. Radovick S., Nations M., Du Y., Berg L.A., Weintraub B.D., and Wondisford F.E. A mutation in the POU-homeodomain of Pit-1 responsible for combined pituitary hormone deficiency. Science 257 (1992) 1115-1118
19. Cohen L.E., Wondisford F.E., Salvatoni A., Maghnie M., Brucker-Davis F., Weintraub B.D., and Radovick S. A "hot spot" in the Pit-1 gene responsible for combined pituitary hormone deficiency. J. Clin. Endocrinol. Metab. 80 (1995) 679-684
20. Andersen B., and Rosenfeld M.G. Pit-1 determines cell types during development of the anterior pituitary gland. J. Biol. Chem. 269 (1994) 29335-29338
21. Chen E.Y., Liao Y.C., Smith D.H., Barrera-Saldana H.A., Gelinas R.E., and Seeburg P.H. The human growth hormone locus: nucleotide sequence, biology, and evolution. Genomics 4 (1989) 479-497
22. Jones B.K., Monks B.R., Liebhaber S.A., and Cooke N.E. The human growth hormone gene is regulated by a multicomponent locus control region. Mol. Cell. Biol. 15 (1995) 7010-7021
23. Benani-Baiti I.M., Asa S.L., Song D., Iratni R., Liabhaber S.A., and Cooke N.E. DNase I-hypersensitive sites I and II of the human growth hormone locus control region are a major developmental activator of somatotrope gene expression. Proc. Natl. Acad. Sci. USA 95 (1998) 10655-10660
24. Shewchuk B.M., Asa S.L., Cooke N.E., and Liebhaber S.L. Pit-1 binding sites at the somatotrope-specific DNase I hypersensitive sites I, II of the human growth hormone locus control region are essential for in vivo hGH-N gene activation. J. Biol. Chem. 274 (1999) 35725-35733
25. Elefant F., Cooke N.E., and Liebhaber S.A. Targeted recruitment of histone acetyltransferase activity to a locus control region. J. Biol. Chem. 275 (2000) 13827-13834
26. Shewchuk B.M., Liebhaber S.A., and Cooke N.E. Specification of unique Pit-1 activity in the hGH locus control region. Proc. Natl Acad. Sci. USA 99 (2002) 11784-11789
27. Ho Y., Elefant F., Cooke N., and Liebhaber S. A defined locus control region determinant links chromatin domain acetylation with long-range gene activation. Mol. Cell 9 (2002) 291-302
28. Shewchuk B.M., Ho Y., Liebhaber S.A., and Cooke N.E. A single base difference between Pit-1 binding sites at the hGH promoter and locus control region specifies distinct Pit-1 conformations and functions. Mol. Cell. Biol. 26 (2006) 6535-6546
29. Yoo E.J., Cajiao I., Kim J.-S., Kimura A.P., Zhang A., Cooke N.E., and Liebhaber S.A. Tissue-specific chromatin modifications at a multigene locus generate asymmetric transcriptional interactions. Mol. Cell. Biol. 26 (2006) 5569-5579
30. Harris N.S. Plasma cell surface antigen on human blood lymphocytes. Nature 250 (1974) 507-509
31. Ho Y., Elefant F., Liebhaber S.A., and Cooke N.E. Locus control region transcription plays an active role in long-range gene activation. Mol. Cell 23 (2006) 365-375
32. Lozzio B.B., and Lozzio C.B. Properties of the K562 cell line derived from a patient with chronic myeloid leukemia. Int. J. Cancer 19 (1977) 136
33. Cajiao I., Xhang A., Yoo E.J., Cooke N.E., and Liebhaber S.A. Bystander gene activation by a locus control region. EMBO J. 23 (2004) 3854-3863
34. Malone C.S., Kuraishy A.I., Fike F.M., Loya R.G., Mikkili M.R., Teitell M.A., and Wall R. B29 gene silencing in pituitary cells is regulated by its 3′ enhancer. J. Mol. Biol. 362 (2006) 173-183
35. Dolle P., Castrillo J.L., Theill L.E., Deerinck T., Ellisman M., and Karin M. Expression of GHF-1 protein in mouse pituitaries correlates both temporally and spatially with the onset of growth hormone gene activity. Cell 60 (1990) 809-820
36. Lira S.A., Crenshaw E.B., Glass C.K., Swanson L.W., and Rosenfeld M.G. Identification of rat growth hormone genomic sequences targeting pituitary expression in transgenic mice. Proc. Natl Acad. Sci. USA 85 (1988) 4755-4759
37. Vignali M., Steger D.J., Neely K.E., and Workman J.L. Distribution of acetylated histones resulting from Gal4-VP16 recruitment of SAGA and NuA4 complexes. EMBO J. 19 (2000) 2629-2640
38. Mangalam H.J., Albert V.R., Ingraham H.A., Kapilof M., Wilson L., Nelson C., et al. A pituitary POU domain protein, Pit-1, activates both growth hormone and prolactin promoters transcriptionally. Genes Dev. 3 (1989) 946-958
39. Castrillo J.-L., Theill L.E., and Karin M. Function of the homeodomain protein GHF1 in pituitary cell proliferation. Science 253 (1991) 197-199
40. Bulger M., Schübler D., Bender M.A., Hamilton J., Farrell C.M., Hardison R.C., and Groudine M. A complex chromatin landscape revealed by patterns of nuclease sensitivity and histone modification within the mouse β-globin locus. Mol. Cell. Biol. 23 (2003) 5234-5244
41. Kimura A.P., Liebhaber S.A., and Cooke N.E. Epigenetic modifications at the human growth hormone locus predict distinct roles for histone acetylation and methylation in placental gene activation. Mol. Endocrinol. 18 (2004) 1018-1032
42. Hebbes T.R., Clayton A.L., Thorne A.W., and Crane-Robinson C. Core histone hyperacetylation co-maps with generalized DNaseI sensitivity in the chicken beta-globin chromosomal domain. EMBO J. 13 (1994) 1823-1830
43. Litt M.D., Simpson M., Recillas-Targa F., Prioleau M.N., and Felsenfeld G. Transitions in histone acetylation reveal boundaries of three separately regulated neighboring loci. EMBO J. 20 (2001) 2224-2235
44. Engel J.D., and Tanimoto K. Looping, linking, and chromatin activity: new insights into beta-globin locus regulation. Cell 100 (2000) 499-502
45. Dean A. On a chromosome far, far away: LCRs and gene expression. Trends Genet. 22 (2006) 38-45
46. Xu L., Lavinsky R.M., Dasen J.S., Flynn S.E., McInerny E.M., Mullen T.M., et al. Signal-specific coactivator domain requirements for Pit-1 activation. Nature 395 (1998) 301-306
47. Cohen L.E., Hashimoto Y., Zanger K., Wondisford F., and Radovick S. CREB-independent regulation by CBP is a novel mechanism of human growth hormone gene expression. J. Clin. Invest. 104 (1999) 1123-1130
48. Cohen R.N., Brue T., Naik K., Houlihan A., Wondisford F.E., and Radovick S. The role of CBP/p300 interactions and Pit-1 dimerization in the pathophysiological mechanism of combined pituitary hormone deficiency. J. Clin. Endocrinol. Metab. 91 (2006) 239-247
49. Ho Y., Tadevosyan A., Liebhaber S.A., and Cooke N.E. The juxtaposition of a promoter with a locus control region transcriptional domain activates gene expression. EMBO Rep. 9 (2008) 891-898
50. McDowell J.C., and Dean A. Structural and functional cross-talk between a distant enhancer and the e-globin gene promoter shows interdependence of the two elements in chromatin. Mol. Cell. Biol. 19 (1999) 7600-7609
51. Ashe H.L., Monks J., Wijgerde M., Fraser P., and Proudfoot N.J. Intergenic transcription and transinduction of the human beta-globin locus. Genes Dev. 11 (1997) 2494-2509
52. Gribnau J., Diderich K., Pruzina S., Calzolari R., and Fraser P. Intergenic transcription and developmental remodeling of chromatin subdomains in the human beta-globin locus. Mol. Cell 5 (2000) 377-386
53. Plant K.E., Routledge S.J., and Proudfoot N.J. Intergenic transcription in the human beta-globin gene cluster. Mol. Cell. Biol. 21 (2001) 6507-6514
54. Masternak K., Peyraud N., Krawczyk M., Barras E., and Reith W. Chromatin remodeling and extragenic transcription at the MHC class II locus control region. Nat. Immunol. 4 (2003) 132-137
55. Schmitt S., Prestel M., and Paro R. Intergenic transcription through a polycomb group response element counteracts silencing. Genes Dev. 19 (2005) 697-708
56. Sharp Z.D. Rat Pit-1 stimulates transcription by influencing pre-initiation complex assembly. Biochem. Biophys. Res. Commun. 206 (1995) 40-45
57. Layon M.E., Ackley C.L., West R.J., and Lowrey C.H. Expression of GATA-1 in a non-hematopoietic cell line induces beta-globin locus control region chromatin structure remodeling and an erythroid pattern of gene expression. J. Mol. Biol. 366 (2007) 737-744
58. Weintraub H., Tapscott S.J., Davis R.L., Tayer M.J., Adam M.A., Lassar A.B., and Miller A.D. Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. Proc. Natl Acad. Sci. USA 86 (1989) 5434-5438
59. Gil-Puig C., Blanco M., Garcia-Caballero T., Sugura C., and Perez-Fernandez R. Pit-1/GHF-1 and GH expression in the MCF-7 human breast adenocarcinoma cell line. J. Endocrinol. 173 (2002) 161-167
60. Gil-Puig C., Seoane S., Blanco M., Garcia-Caballero T., Segura C., and Perez-Fernandez R. Pit-1 is expressed in normal and tumorous human breast and regulates GH secretion and cell proliferation. Eur. J. Endocrinol. 153 (2005) 334-335
61. Diamond S.E., and Gutierrez-Hartmann A. The Pit-1β domain dictates active repression and alteration of histone acetylation of the proximal prolactin promoter. J. Biol. Chem. 275 (2000) 30977-30986
62. Kingston R.E., Chen C.A., Okayama H., and Rose J.K. Transfection of DNA into eukaryotic cells. In: Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., and Struhl K. (Eds). Current Protocols in Molecular Biology vol. 1 (1996), John Wiley and Sons, Inc., Hoboken, NJ 9.1.1-9.1.11
63. Dyer R.B., and Herzog N.K. Isolation of intact nuclei for nuclear extract preparation from a fragile B-lymphocyte cell line. BioTechniques 19 (1995) 192-195
64. t) method. Methods 25 (2001) 402-408
65. Bookout A.L., Cummins C.L., Kramer M.F., Pesola J.M., and Mangelsdorf D.J. High-throughput real-time quantitative reverse transcription PCR. In: Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., and Struhl K. (Eds). Current Protocols in Molecular Biology vol. 3 (2006), John Wiley and Sons, Inc., Hoboken, NJ 15.8.1-15.8.28
66. Su Y., Liebhaber S.A., and Cooke N.E. The human growth hormone gene cluster locus control region supports position-independent pituitary- and placenta-specific expression in the transgenic mouse. J. Biol. Chem. 275 (2000) 7902-7909
67. Miles J., Mitchell J.A., Chakalova L., Goyenechea B., Osborne C.S., O'Neill L., et al. Intergenic transcription, cell-cycle and the developmentally regulated epigenetic profile of the human beta-globin locus. PLoS ONE 2 (2007) e630