The Prolactin Gene: A Paradigm of Tissue-Specific Gene Regulation with Complex Temporal Transcription Dynamics

Journal of Neuroendocrinology

Volumn 24, Issue 7, 2012, Pages 977-990

  Featherstone, K ^a   White, M R H ^b   Davis, J R E ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Chromatin; Dynamics; Pituitary; Prolactin; Transcription

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DOPAMINE; ESTROGEN RECEPTOR ALPHA; GREEN FLUORESCENT PROTEIN; PHOSPHATIDYLINOSITOL; PROLACTIN; PROTEIN KINASE C; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR ETS; TRANSCRIPTION FACTOR PIT 1; TRANSCRIPTION FACTOR PITX2;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ADIPOSE TISSUE; ANGIOGENESIS; BACTERIAL ARTIFICIAL CHROMOSOME; BINDING AFFINITY; BINDING SITE; BRAIN; BREAST; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; DNA BINDING; DOPAMINE RELEASE; ENDOMETRIUM; EXON; FLUORESCENCE IN SITU HYBRIDIZATION; GENE ACTIVITY; GENE CONTROL; GENE DOSAGE; GENE EXPRESSION; GENE INSERTION; GENE INTERACTION; GENE LOCUS; GENE SEQUENCE; GENE STRUCTURE; GENETIC TRANSCRIPTION; HEMATOPOIESIS; HEMATOPOIETIC CELL; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE PHOSPHORYLATION; HISTONE UBIQUITINATION; HUMAN; HUMAN GENOME; HYPOPHYSIS; IMMUNE SYSTEM; ISOMERIZATION; LONG TERMINAL REPEAT; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROSTATE; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REPRODUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SIGNAL TRANSDUCTION; SKIN; SUMOYLATION; TRANSCRIPTION INITIATION;

ANIMALS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC LOCI; HUMANS; MODELS, BIOLOGICAL; ORGAN SPECIFICITY; PROLACTIN; TIME FACTORS; TISSUE DISTRIBUTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84862679184     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2012.02310.x     Document Type: Review

References (126)

1. Walker JJ, Terry JR, Tsaneva-Atanasova K, Armstrong SP, McArdle CA, Lightman SL. Encoding and decoding mechanisms of pulsatile hormone secretion. J Neuroendocrinol 2010; 22: 1226-1238.
2. Raj A, van Oudenaarden A. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 2008; 135: 216-226.
3. Suter DM, Molina N, Gatfield D, Schneider K, Schibler U, Naef F. Mammalian genes are transcribed with widely different bursting kinetics. Science 2011; 332: 472-474.
4. Wernet MF, Mazzoni EO, Celik A, Duncan DM, Duncan I, Desplan C. Stochastic spineless expression creates the retinal mosaic for colour vision. Nature 2006; 440: 174-180.
5. Chang HH, Hemberg M, Barahona M, Ingber DE, Huang S. Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 2008; 453: 544-547.
6. Wiemers DO, Shao LJ, Ain R, Dai G, Soares MJ. The mouse prolactin gene family locus. Endocrinology 2003; 144: 313-325.
7. Alam SM, Ain R, Konno T, Ho-Chen JK, Soares MJ. The rat prolactin gene family locus: species-specific gene family expansion. Mamm Genome 2006; 17: 858-877.
8. Schwartz S, Zhang Z, Frazer KA, Smit A, Riemer C, Bouck J, Gibbs R, Hardison R, Miller W. PipMaker-a web server for aligning two genomic DNA sequences. Genome Res 2000; 10: 577-586.
9. Soares MJ, Konno T, Alam SM. The prolactin family: effectors of pregnancy-dependent adaptations. Trends Endocrinol Metab 2007; 18: 114-121.
10. Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Agarwala R, Ainscough R, Alexandersson M, An P, Antonarakis SE, Attwood J, Baertsch R, Bailey J, Barlow K, Beck S, Berry E, Birren B, Bloom T, Bork P, Botcherby M, Bray N, Brent MR, Brown DG, Brown SD, Bult C, Burton J, Butler J, Campbell RD, Carninci P, Cawley S, Chiaromonte F, Chinwalla AT, Church DM, Clamp M, Clee C, Collins FS, Cook LL, Copley RR, Coulson A, Couronne O, Cuff J, Curwen V, Cutts T, Daly M, David R, Davies J, Delehaunty KD, Deri J, Dermitzakis ET, Dewey C, Dickens NJ, Diekhans M, Dodge S, Dubchak I, Dunn DM, Eddy SR, Elnitski L, Emes RD, Eswara P, Eyras E, Felsenfeld A, Fewell GA, Flicek P, Foley K, Frankel WN, Fulton LA, Fulton RS, Furey TS, Gage D, Gibbs RA, Glusman G, Gnerre S, Goldman N, Goodstadt L, Grafham D, Graves TA, Green ED, Gregory S, Guigo R, Guyer M, Hardison RC, Haussler D, Hayashizaki Y, Hillier LW, Hinrichs A, Hlavina W, Holzer T, Hsu F, Hua A, Hubbard T, Hunt A, Jackson I, Jaffe DB, Johnson LS, Jones M, Jones TA, Joy A, Kamal M, Karlsson EK, Karolchik D, Kasprzyk A, Kawai J, Keibler E, Kells C, Kent WJ, Kirby A, Kolbe DL, Korf I, Kucherlapati RS, Kulbokas EJ, Kulp D, Landers T, Leger JP, Leonard S, Letunic I, Levine R, Li J, Li M, Lloyd C, Lucas S, Ma B, Maglott DR, Mardis ER, Matthews L, Mauceli E, Mayer JH, McCarthy M, McCombie WR, McLaren S, McLay K, McPherson JD, Meldrim J, Meredith B, Mesirov JP, Miller W, Miner TL, Mongin E, Montgomery KT, Morgan M, Mott R, Mullikin JC, Muzny DM, Nash WE, Nelson JO, Nhan MN, Nicol R, Ning Z, Nusbaum C, O'Connor MJ, Okazaki Y, Oliver K, Overton-Larty E, Pachter L, Parra G, Pepin KH, Peterson J, Pevzner P, Plumb R, Pohl CS, Poliakov A, Ponce TC, Ponting CP, Potter S, Quail M, Reymond A, Roe BA, Roskin KM, Rubin EM, Rust AG, Santos R, Sapojnikov V, Schultz B, Schultz J, Schwartz MS, Schwartz S, Scott C, Seaman S, Searle S, Sharpe T, Sheridan A, Shownkeen R, Sims S, Singer JB, Slater G, Smit A, Smith DR, Spencer B, Stabenau A, Stange-Thomann N, Sugnet C, Suyama M, Tesler G, Thompson J, Torrents D, Trevaskis E, Tromp J, Ucla C, Ureta-Vidal A, Vinson JP, Von Niederhausern AC, Wade CM, Wall M, Weber RJ, Weiss RB, Wendl MC, West AP, Wetterstrand K, Wheeler R, Whelan S, Wierzbowski J, Willey D, Williams S, Wilson RK, Winter E, Worley KC, Wyman D, Yang S, Yang SP, Zdobnov EM, Zody MC, Lander ES. Initial sequencing and comparative analysis of the mouse genome. Nature 2002; 420: 520-562.
11. Gibbs RA, Weinstock GM, Metzker ML, Muzny DM, Sodergren EJ, Scherer S, Scott G, Steffen D, Worley KC, Burch PE, Okwuonu G, Hines S, Lewis L, DeRamo C, Delgado O, Dugan-Rocha S, Miner G, Morgan M, Hawes A, Celera RG, Holt RA, Adams MD, Amanatides PG, Baden-Tillson H, Barnstead M, Chin S, Evans CA, Ferriera S, Fosler C, Glodek A, Gu Z, Jennings D, Kraft CL, Nguyen T, Pfannkoch CM, Sitter C, Sutton GG, Venter JC, Woodage T, Smith D, Lee HM, Gustafson E, Cahill P, Kana A, Doucette-Stamm L, Weinstock K, Fechtel K, Weiss RB, Dunn DM, Green ED, Blakesley RW, Bouffard GG, De Jong PJ, Osoegawa K, Zhu B, Marra M, Schein J, Bosdet I, Fjell C, Jones S, Krzywinski M, Mathewson C, Siddiqui A, Wye N, McPherson J, Zhao S, Fraser CM, Shetty J, Shatsman S, Geer K, Chen Y, Abramzon S, Nierman WC, Havlak PH, Chen R, Durbin KJ, Egan A, Ren Y, Song XZ, Li B, Liu Y, Qin X, Cawley S, Worley KC, Cooney AJ, D'Souza LM, Martin K, Wu JQ, Gonzalez-Garay ML, Jackson AR, Kalafus KJ, McLeod MP, Milosavljevic A, Virk D, Volkov A, Wheeler DA, Zhang Z, Bailey JA, Eichler EE, Tuzun E, Birney E, Mongin E, Ureta-Vidal A, Woodwark C, Zdobnov E, Bork P, Suyama M, Torrents D, Alexandersson M, Trask BJ, Young JM, Huang H, Wang H, Xing H, Daniels S, Gietzen D, Schmidt J, Stevens K, Vitt U, Wingrove J, Camara F, Mar Alba M, Abril JF, Guigo R, Smit A, Dubchak I, Rubin EM, Couronne O, Poliakov A, Hubner N, Ganten D, Goesele C, Hummel O, Kreitler T, Lee YA, Monti J, Schulz H, Zimdahl H, Himmelbauer H, Lehrach H, Jacob HJ, Bromberg S, Gullings-Handley J, Jensen-Seaman MI, Kwitek AE, Lazar J, Pasko D, Tonellato PJ, Twigger S, Ponting CP, Duarte JM, Rice S, Goodstadt L, Beatson SA, Emes RD, Winter EE, Webber C, Brandt P, Nyakatura G, Adetobi M, Chiaromonte F, Elnitski L, Eswara P, Hardison RC, Hou M, Kolbe D, Makova K, Miller W, Nekrutenko A, Riemer C, Schwartz S, Taylor J, Yang S, Zhang Y, Lindpaintner K, Andrews TD, Caccamo M, Clamp M, Clarke L, Curwen V, Durbin R, Eyras E, Searle SM, Cooper GM, Batzoglou S, Brudno M, Sidow A, Stone EA, Venter JC, Payseur BA, Bourque G, Lopez-Otin C, Puente XS, Chakrabarti K, Chatterji S, Dewey C, Pachter L, Bray N, Yap VB, Caspi A, Tesler G, Pevzner PA, Haussler D, Roskin KM, Baertsch R, Clawson H, Furey TS, Hinrichs AS, Karolchik D, Kent WJ, Rosenbloom KR, Trumbower H, Weirauch M, Cooper DN, Stenson PD, Ma B, Brent M, Arumugam M, Shteynberg D, Copley RR, Taylor MS, Riethman H, Mudunuri U, Peterson J, Guyer M, Felsenfeld A, Old S, Mockrin S, Collins F. Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 2004; 428: 493-521.
12. Geurts AM, Cost GJ, Freyvert Y, Zeitler B, Miller JC, Choi VM, Jenkins SS, Wood A, Cui X, Meng X, Vincent A, Lam S, Michalkiewicz M, Schilling R, Foeckler J, Kalloway S, Weiler H, Menoret S, Anegon I, Davis GD, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Jacob HJ, Buelow R. Knockout rats via embryo microinjection of zinc-finger nucleases. Science 2009; 325: 433.
13. Tong C, Li P, Wu NL, Yan Y, Ying QL. Production of p53 gene knockout rats by homologous recombination in embryonic stem cells. Nature 2010; 467: 211-213.
14. Adamson AD, Jackson D, Davis JR. Novel approaches to in vitro transgenesis. J Endocrinol 2011; 208: 193-206.
15. Semprini S, Friedrichsen S, Harper CV, McNeilly JR, Adamson AD, Spiller DG, Kotelevtseva N, Brooker G, Brownstein DG, McNeilly AS, White MR, Davis JR, Mullins JJ. Real-time visualization of human prolactin alternate promoter usage in vivo using a double-transgenic rat model. Mol Endocrinol 2009; 23: 529-538.
16. Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR, Eeckhoute J, Brodsky AS, Keeton EK, Fertuck KC, Hall GF, Wang Q, Bekiranov S, Sementchenko V, Fox EA, Silver PA, Gingeras TR, Liu XS, Brown M. Genome-wide analysis of estrogen receptor binding sites. Nat Genet 2006; 38: 1289-1297.
17. Schoenfelder S, Clay I, Fraser P. The transcriptional interactome: gene expression in 3D. Curr Opin Genet Dev 2010; 20: 127-133.
18. Peers B, Voz ML, Monget P, Mathy-Hartert M, Berwaer M, Belayew A, Martial JA. Regulatory elements controlling pituitary-specific expression of the human prolactin gene. Mol Cell Biol 1990; 10: 4690-4700.
19. Ben-Jonathan N, LaPensee CR, LaPensee EW. What can we learn from rodents about prolactin in humans? Endocr Rev 2008; 29: 1-41.
20. Van De Weerdt C, Peers B, Belayew A, Martial JA, Muller M. Far upstream sequences regulate the human prolactin promoter transcription. Neuroendocrinology 2000; 71: 124-137.
21. Cullen KE, Kladde MP, Seyfred MA. Interaction between transcription regulatory regions of prolactin chromatin. Science 1993; 261: 203-206.
22. Gothard LQ, Hibbard JC, Seyfred MA. Estrogen-mediated induction of rat prolactin gene transcription requires the formation of a chromatin loop between the distal enhancer and proximal promoter regions. Mol Endocrinol 1996; 10: 185-195.
23. Ingraham HA, Chen RP, Mangalam HJ, Elsholtz HP, Flynn SE, Lin CR, Simmons DM, Swanson L, Rosenfeld MG. A tissue-specific transcription factor containing a homeodomain specifies a pituitary phenotype. Cell 1988; 55: 519-529.
24. Kerr J, Wood W, Ridgway EC. Basic science and clinical research advances in the pituitary transcription factors: Pit-1 and Prop-1. Curr Opin Endocrinol Diabetes Obes 2008; 15: 359-363.
25. Holloway JM, Szeto DP, Scully KM, Glass CK, Rosenfeld MG. Pit-1 binding to specific DNA sites as a monomer or dimer determines gene-specific use of a tyrosine-dependent synergy domain. Genes Dev 1995; 9: 1992-2006.
26. Kapiloff MS, Farkash Y, Wegner M, Rosenfeld MG. Variable effects of phosphorylation of Pit-1 dictated by the DNA response elements. Science 1991; 253: 786-789.
27. Gaddy-Kurten D, Vale WW. Activin increases phosphorylation and decreases stability of the transcription factor Pit-1 in MtTW15 somatotrope cells. J Biol Chem 1995; 270: 28733-28739.
28. Jean A, Gutierrez-Hartmann A, Duval DL. A Pit-1 threonine 220 phosphomimic reduces binding to monomeric DNA sites to inhibit Ras and estrogen stimulation of the prolactin gene promoter. Mol Endocrinol 2010; 24: 91-103.
29. Perissi V, Dasen JS, Kurokawa R, Wang Z, Korzus E, Rose DW, Glass CK, Rosenfeld MG. Factor-specific modulation of CREB-binding protein acetyltransferase activity. Proc Natl Acad Sci USA 1999; 96: 3652-3657.
30. Jonsen MD, Duval DL, Gutierrez-Hartmann A. The 26-amino acid beta-motif of the Pit-1beta transcription factor is a dominant and independent repressor domain. Mol Endocrinol 2009; 23: 1371-1384.
31. Zhu X, Gleiberman AS, Rosenfeld MG. Molecular physiology of pituitary development: signaling and transcriptional networks. Physiol Rev 2007; 87: 933-963.
32. Ho Y, Liebhaber SA, Cooke NE. The role of the hGH locus control region in somatotrope restriction of hGH-N gene expression. Mol Endocrinol 2011; 25: 877-884.
33. Wang J, Scully K, Zhu X, Cai L, Zhang J, Prefontaine GG, Krones A, Ohgi KA, Zhu P, Garcia-Bassets I, Liu F, Taylor H, Lozach J, Jayes FL, Korach KS, Glass CK, Fu XD, Rosenfeld MG. Opposing LSD1 complexes function in developmental gene activation and repression programmes. Nature 2007; 446: 882-887.
34. Ben-Jonathan N, Hnasko R. Dopamine as a prolactin (PRL) inhibitor. Endocr Rev 2001; 22: 724-763.
35. Gourdji D, Laverriere JN. The rat prolactin gene: a target for tissue-specific and hormone-dependent transcription factors. Mol Cell Endocrinol 1994; 100: 133-142.
36. Berwaer M, Monget P, Peers B, Mathy-Hartert M, Bellefroid E, Davis JR, Belayew A, Martial JA. Multihormonal regulation of the human prolactin gene expression from 5000 bp of its upstream sequence. Mol Cell Endocrinol 1991; 80: 53-64.
37. Hoggard N, Davis JR, Berwaer M, Monget P, Peers B, Belayew A, Martial JA. Pit-1 binding sequences permit calcium regulation of human prolactin gene expression. Mol Endocrinol 1991; 5: 1748-1754.
38. Peers B, Nalda AM, Monget P, Voz ML, Belayew A, Martial JA. Binding of a 100-kDa ubiquitous factor to the human prolactin promoter is required for its basal and hormone-regulated activity. Eur J Biochem 1992; 210: 53-58.
39. Fliss MS, Hinkle PM, Bancroft C. Expression cloning and characterization of PREB (prolactin regulatory element binding), a novel WD motif DNA-binding protein with a capacity to regulate prolactin promoter activity. Mol Endocrinol 1999; 13: 644-657.
40. Yu X, Murao K, Imachi H, Li J, Nishiuchi T, Dobashi H, Hosomi N, Masugata H, Zhang GX, Iwama H, Ishida T. The transcription factor prolactin regulatory element-binding protein mediates prolactin transcription induced by thyrotropin-releasing hormone in GH3 cells. Endocrine 2010; 38: 53-59.
41. Day RN, Koike S, Sakai M, Muramatsu M, Maurer RA. Both Pit-1 and the estrogen receptor are required for estrogen responsiveness of the rat prolactin gene. Mol Endocrinol 1990; 4: 1964-1971.
42. Simmons DM, Voss JW, Ingraham HA, Holloway JM, Broide RS, Rosenfeld MG, Swanson LW. 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.
43. Adamson AD, Friedrichsen S, Semprini S, Harper CV, Mullins JJ, White MR, Davis JR. Human prolactin gene promoter regulation by estrogen: convergence with tumor necrosis factor-alpha signaling. Endocrinology 2008; 149: 687-694.
44. Ben-Jonathan N, Mershon JL, Allen DL, Steinmetz RW. Extrapituitary prolactin: distribution, regulation, functions, and clinical aspects. Endocr Rev 1996; 17: 639-669.
45. Gellersen B, Kempf R, Telgmann R, DiMattia GE. Pituitary-type transcription of the human prolactin gene in the absence of Pit-1. Mol Endocrinol 1995; 9: 887-901.
46. Manfroid I, Van de Weerdt C, Baudhuin A, Martial JA, Muller M. EGF stimulates Pit-1 independent transcription of the human prolactin pituitary promoter in human breast cancer SK-BR-3 cells through its proximal AP-1 response element. Mol Cell Endocrinol 2005; 229: 127-139.
47. Dagvadorj A, Collins S, Jomain JB, Abdulghani J, Karras J, Zellweger T, Li H, Nurmi M, Alanen K, Mirtti T, Visakorpi T, Bubendorf L, Goffin V, Nevalainen MT. Autocrine prolactin promotes prostate cancer cell growth via Janus kinase-2-signal transducer and activator of transcription-5a/b signaling pathway. Endocrinology 2007; 148: 3089-3101.
48. Ben-Batalla I, Seoane S, Macia M, Garcia-Caballero T, Gonzalez LO, Vizoso F, Perez-Fernandez R. The Pit-1/Pou1f1 transcription factor regulates and correlates with prolactin expression in human breast cell lines and tumors. Endocr Relat Cancer 2010; 17: 73-85.
49. Jabbour HN, Critchley HO. Potential roles of decidual prolactin in early pregnancy. Reproduction 2001; 121: 197-205.
50. Salker M, Teklenburg G, Molokhia M, Lavery S, Trew G, Aojanepong T, Mardon HJ, Lokugamage AU, Rai R, Landles C, Roelen BA, Quenby S, Kuijk EW, Kavelaars A, Heijnen CJ, Regan L, Macklon NS, Brosens JJ. Natural selection of human embryos: impaired decidualization of endometrium disables embryo-maternal interactions and causes recurrent pregnancy loss. PLoS ONE 2010; 5: e10287.
51. Pellegrini I, Lebrun JJ, Ali S, Kelly PA. Expression of prolactin and its receptor in human lymphoid cells. Mol Endocrinol 1992; 6: 1023-1031.
52. Gellersen B, Kempf R, Telgmann R, DiMattia GE. Nonpituitary human prolactin gene transcription is independent of Pit-1 and differentially controlled in lymphocytes and in endometrial stroma. Mol Endocrinol 1994; 8: 356-373.
53. Bellone G, Astarita P, Artusio E, Silvestri S, Mareschi K, Turletti A, Buttiglieri S, Emanuelli G, Matera L. Bone marrow stroma-derived prolactin is involved in basal and platelet-activating factor-stimulated in vitro erythropoiesis. Blood 1997; 90: 21-27.
54. Gerlo S, Verdood P, Hooghe-Peters EL, Kooijman R. Multiple, PKA-dependent and PKA-independent, signals are involved in cAMP-induced PRL expression in the eosinophilic cell line Eol-1. Cell Signal 2005; 17: 901-909.
55. Semprini S, McNamara AV, Awais R, Featherstone K, Harper CV, McNeilly JR, Patist A, Rossi AG, Dransfield I, McNeilly AS, Davis JRE, White MRH, Mullins JJ. Peritonitis activates transcription of the human prolactin locus in myeloid cells in a humanized transgenic rat model. Endocrinology 2012; April 11 [Epub ahead of print]. doi:10.1210/en.2011-1926.
56. De Bellis A, Bizzarro A, Pivonello R, Lombardi G, Bellastella A. Prolactin and autoimmunity. Pituitary 2005; 8: 25-30.
57. Zinger M, McFarland M, Ben-Jonathan N. Prolactin expression and secretion by human breast glandular and adipose tissue explants. J Clin Endocrinol Metab 2003; 88: 689-696.
58. Bernichtein S, Touraine P, Goffin V. New concepts in prolactin biology. J Endocrinol 2010; 206: 1-11.
59. Langan EA, Foitzik-Lau K, Goffin V, Ramot Y, Paus R. Prolactin: an emerging force along the cutaneous-endocrine axis. Trends Endocrinol Metab 2010; 21: 569-577.
60. El-Khateeb EA, Zuel-Fakkar NM, Eid SM, Abdul-Wahab SE. Prolactin level is significantly elevated in lesional skin of patients with psoriasis. Int J Dermatol 2011; 50: 693-696.
61. Peirce SK, Chen WY, Chen WY. Quantification of prolactin receptor mRNA in multiple human tissues and cancer cell lines by real time RT-PCR. J Endocrinol 2001; 171: R1-R4.
62. van den Burg EH, Neumann ID. Bridging the gap between GPCR activation and behaviour: oxytocin and prolactin signalling in the hypothalamus. J Mol Neurosci 2011; 43: 200-208.
63. Brandebourg T, Hugo E, Ben-Jonathan N. Adipocyte prolactin: regulation of release and putative functions. Diabetes Obes Metab 2007; 9: 464-476.
64. Hugo ER, Borcherding DC, Gersin KS, Loftus J, Ben-Jonathan N. Prolactin release by adipose explants, primary adipocytes, and LS14 adipocytes. J Clin Endocrinol Metab 2008; 93: 4006-4012.
65. Gerlo S, Davis JR, Mager DL, Kooijman R. Prolactin in man: a tale of two promoters. BioEssays 2006; 28: 1051-1055.
66. DiMattia GE, Gellersen B, Duckworth ML, Friesen HG. Human prolactin gene expression. The use of an alternative noncoding exon in decidua and the IM-9-P3 lymphoblast cell line. J Biol Chem 1990; 265: 16412-16421.
67. Shaw-Bruha CM, Pennington KL, Shull JD. Identification in the rat prolactin gene of sequences homologous to the distal promoter of the human prolactin gene. Biochim Biophys Acta 1998; 3: 304-313.
68. Watanabe K, Kessler CA, Bachurski CJ, Kanda Y, Richardson BD, Stanek J, Handwerger S, Brar AK. Identification of a decidua-specific enhancer on the human prolactin gene with two critical activator protein 1 (AP-1) binding sites. Mol Endocrinol 2001; 15: 638-653.
69. Gerlo S, Van den Berghe W, Verdood P, Hooghe-Peters EL, Kooijman R. Regulation of prolactin expression in leukemic cell lines and peripheral blood mononuclear cells. J Neuroimmunol 2003; 135: 107-116.
70. Reem GH, Ray DW, Davis JR. The human prolactin gene upstream promoter is regulated in lymphoid cells by activators of T-cells and by cAMP. J Mol Endocrinol 1999; 22: 285-292.
71. Raj A, van Oudenaarden A. Single-molecule approaches to stochastic gene expression. Annu Rev Biophys 2009; 38: 255-270.
72. Spiller DG, Wood CD, Rand DA, White MR. Measurement of single-cell dynamics. Nature 2010; 465: 736-745.
73. Elowitz MB, Levine AJ, Siggia ED, Swain PS. Stochastic gene expression in a single cell. Science 2002; 297: 1183-1186.
74. Golding I, Paulsson J, Zawilski SM, Cox EC. Real-time kinetics of gene activity in individual bacteria. Cell 2005; 123: 1025-1036.
75. Raj A, Peskin CS, Tranchina D, Vargas DY, Tyagi S. Stochastic mRNA synthesis in mammalian cells. PLoS Biol 2006; 4: e309.
76. Takasuka N, White MR, Wood CD, Robertson WR, Davis JR. Dynamic changes in prolactin promoter activation in individual living lactotrophic cells. Endocrinology 1998; 139: 1361-1368.
77. McFerran DW, Stirland JA, Norris AJ, Khan RA, Takasuka N, Seymour ZC, Gill MS, Robertson WR, Loudon AS, Davis JR, White MR. Persistent synchronized oscillations in prolactin gene promoter activity in living pituitary cells. Endocrinology 2001; 142: 3255-3260.
78. Stirland JA, Seymour ZC, Windeatt S, Norris AJ, Stanley P, Castro MG, Loudon AS, White MR, Davis JR. Real-time imaging of gene promoter activity using an adenoviral reporter construct demonstrates transcriptional dynamics in normal anterior pituitary cells. J Endocrinol 2003; 178: 61-69.
79. Castano JP, Kineman RD, Frawley LS. Dynamic monitoring and quantification of gene expression in single, living cells: a molecular basis for secretory cell heterogeneity. Mol Endocrinol 1996; 10: 599-605.
80. Castano JP, Faught WJ, Glave EE, Russell BS, Frawley LS. Discordance of prolactin gene transcription, mRNA storage, and hormone release in individual mammotropes. Am J Physiol 1997; 272: E390-E396.
81. Villalobos C, Faught WJ, Frawley LS. Dynamics of stimulus-expression coupling as revealed by monitoring of prolactin promoter-driven reporter activity in individual, living mammotropes. Mol Endocrinol 1999; 13: 1718-1727.
82. Shorte SL, Leclerc GM, Vazquez-Martinez R, Leaumont DC, Faught WJ, Frawley LS, Boockfor FR. PRL gene expression in individual living mammotropes displays distinct functional pulses that oscillate in a noncircadian temporal pattern. Endocrinology 2002; 143: 1126-1133.
83. Villalobos C, Nunez L, Faught WJ, Leaumont DC, Boockfor FR, Frawley LS. Calcium dynamics and resting transcriptional activity regulates prolactin gene expression. Endocrinology 2002; 143: 3548-3554.
84. Leclerc GM, Boockfor FR. Pulses of prolactin promoter activity depend on a noncanonical E-box that can bind the circadian proteins CLOCK and BMAL1. Endocrinology 2005; 146: 2782-2790.
85. Bose S, Boockfor FR. Episodes of prolactin gene expression in GH3 cells are dependent on selective promoter binding of multiple circadian elements. Endocrinology 2010; 151: 2287-2296.
86. Guillaumond F, Boyer B, Becquet D, Guillen S, Kuhn L, Garin J, Belghazi M, Bosler O, Franc JL, Francois-Bellan AM. Chromatin remodeling as a mechanism for circadian prolactin transcription: rhythmic NONO and SFPQ recruitment to HLTF. FASEB J 2011; 25: 2740-2756.
87. Harper CV, Finkenstadt B, Woodcock DJ, Friedrichsen S, Semprini S, Ashall L, Spiller DG, Mullins JJ, Rand DA, Davis JR, White MR. Dynamic analysis of stochastic transcription cycles. PLoS Biol 2011; 9: e1000607.
88. Cai L, Dalal CK, Elowitz MB. Frequency-modulated nuclear localization bursts coordinate gene regulation. Nature 2008; 455: 485-490.
89. Ashall L, Horton CA, Nelson DE, Paszek P, Harper CV, Sillitoe K, Ryan S, Spiller DG, Unitt JF, Broomhead DS, Kell DB, Rand DA, See V, White MR. Pulsatile stimulation determines timing and specificity of NF-kappaB-dependent transcription. Science 2009; 324: 242-246.
90. Nagaich AK, Walker DA, Wolford R, Hager GL. Rapid periodic binding and displacement of the glucocorticoid receptor during chromatin remodeling. Mol Cell 2004; 14: 163-174.
91. Shang Y, Hu X, DiRenzo J, Lazar MA, Brown M. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 2000; 103: 843-852.
92. Metivier R, Penot G, Hubner MR, 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.
93. Hager GL, McNally JG, Misteli T. Transcription dynamics. Mol Cell 2009; 35: 741-753.
94. 2 or EGF induces temporally distinct patterns of large-scale chromatin modification and mRNA transcription. PLoS ONE 2008; 3: e2286.
95. Caelles C, Hennemann H, Karin M. M-phase-specific phosphorylation of the POU transcription factor GHF-1 by a cell cycle-regulated protein kinase inhibits DNA binding. Mol Cell Biol 1995; 15: 6694-6701.
96. Friedrichsen S, Harper CV, Semprini S, Wilding M, Adamson AD, Spiller DG, Nelson G, Mullins JJ, White MR, Davis JR. Tumor necrosis factor-alpha activates the human prolactin gene promoter via nuclear factor-kappaB signaling. Endocrinology 2006; 147: 773-781.
97. Reid G, Gallais R, Metivier R. Marking time: the dynamic role of chromatin and covalent modification in transcription. Int J Biochem Cell Biol 2009; 41: 155-163.
98. Metivier R, Reid G, Gannon F. Transcription in four dimensions: nuclear receptor-directed initiation of gene expression. EMBO Rep 2006; 7: 161-167.
99. Malinen M, Ryynanen J, Heinaniemi M, Vaisanen S, Carlberg C. Cyclical regulation of the insulin-like growth factor binding protein 3 gene in response to 1alpha, 25-dihydroxyvitamin D3. Nucleic Acids Res 2011; 39: 502-512.
100. Giglia-Mari G, Theil AF, Mari PO, Mourgues S, Nonnekens J, Andrieux LO, de Wit J, Miquel C, Wijgers N, Maas A, Fousteri M, Hoeijmakers JH, Vermeulen W. Differentiation driven changes in the dynamic organization of Basal transcription initiation. PLoS Biol 2009; 7: e1000220.
101. Lionnet T, Czaplinski K, Darzacq X, Shav-Tal Y, Wells AL, Chao JA, Park HY, de Turris V, Lopez-Jones M, Singer RH. A transgenic mouse for in vivo detection of endogenous labeled mRNA. Nat Methods 2011; 8: 165-170.
102. Harper CV, Featherstone K, Semprini S, Friedrichsen S, McNeilly J, Paszek P, Spiller DG, McNeilly AS, Mullins JJ, Davis JR, White MR. Dynamic organisation of prolactin gene expression in living pituitary tissue. J Cell Sci 2010; 123: 424-430.
103. Featherstone K, Harper CV, McNamara A, Semprini S, Spiller DG, McNeilly J, McNeilly AS, Mullins JJ, White MR, Davis JR. Pulsatile patterns of pituitary hormone gene expression change during development. J Cell Sci 2011; 124: 3484-3491.
104. Bonnefont X, Lacampagne A, Sanchez-Hormigo A, Fino E, Creff A, Mathieu MN, Smallwood S, Carmignac D, Fontanaud P, Travo P, Alonso G, Courtois-Coutry N, Pincus SM, Robinson IC, Mollard P. Revealing the large-scale network organization of growth hormone-secreting cells. Proc Natl Acad Sci USA 2005; 102: 16880-16885.
105. Hodson DJ, Schaeffer M, Romano N, Fontanaud P, Lafont C, Birkenstock J, Molino F, Christian H, Lockey J, Carmignac D, Fernandez-Fuente M, Le Tissier P, Mollard P. Existence of long-lasting experience-dependent plasticity in endocrine cell networks. Nat Commun 2012; 3: 605.
106. Christian HC, Chapman LP, Morris JF. Thyrotrophin-releasing hormone, vasoactive intestinal peptide, prolactin-releasing peptide and dopamine regulation of prolactin secretion by different lactotroph morphological subtypes in the rat. J Neuroendocrinol 2007; 19: 605-613.
107. Scarbrough K, Weiland NG, Larson GH, Sortino MA, Chiu SF, Hirshfield AN, Wise PM. Measurement of peptide secretion and gene expression in the same cell. Mol Endocrinol 1991; 5: 134-142.
108. van Steensel B. Chromatin: constructing the big picture. EMBO J 2011; 30: 1885-1895.
109. Janicki SM, Tsukamoto T, Salghetti SE, Tansey WP, Sachidanandam R, Prasanth KV, Ried T, Shav-Tal Y, Bertrand E, Singer RH, Spector DL. From silencing to gene expression: real-time analysis in single cells. Cell 2004; 116: 683-698.
110. Valouev A, Johnson SM, Boyd SD, Smith CL, Fire AZ, Sidow A. Determinants of nucleosome organization in primary human cells. Nature 2011; 474: 516-520.
111. Lam FH, Steger DJ, O'Shea EK. Chromatin decouples promoter threshold from dynamic range. Nature 2008; 453: 246-250.
112. Segal E, Widom J. From DNA sequence to transcriptional behaviour: a quantitative approach. Nat Rev Genet 2009; 10: 443-456.
113. Willis SD, Seyfred MA. Pituitary-specific chromatin structure of the rat prolactin distal enhancer element. Nucleic Acids Res 1996; 24: 1065-1072.
114. Malayer JR, Gorski J. The role of estrogen receptor in modulation of chromatin conformation in the 5′ flanking region of the rat prolactin gene. Mol Cell Endocrinol 1995; 113: 145-154.
115. Kievit P, Maurer RA. The pituitary-specific transcription factor, Pit-1, can direct changes in the chromatin structure of the prolactin promoter. Mol Endocrinol 2005; 19: 138-147.
116. Rich A, Zhang S. Timeline: Z-DNA: the long road to biological function. Nat Rev Genet 2003; 4: 566-572.
117. Liu H, Mulholland N, Fu H, Zhao K. Cooperative activity of BRG1 and Z-DNA formation in chromatin remodeling. Mol Cell Biol 2006; 26: 2550-2559.
118. Wong B, Chen S, Kwon JA, Rich A. Characterization of Z-DNA as a nucleosome-boundary element in yeast Saccharomyces cerevisiae. Proc Natl Acad Sci USA 2007; 104: 2229-2234.
119. Kladde MP, D'Cunha J, Gorski J. Multiple transitions to non-B-DNA structures occur in the distal regulatory region of the rat prolactin gene. J Mol Biol 1993; 229: 344-367.
120. Naylor LH, Clark EM. d(TG)n.d(CA)n sequences upstream of the rat prolactin gene form Z-DNA and inhibit gene transcription. Nucleic Acids Res 1990; 18: 1595-1601.
121. Zee BM, Levin RS, Dimaggio PA, Garcia BA. Global turnover of histone post-translational modifications and variants in human cells. Epigenetics Chromatin. 2010; 3: 22.
122. Wang Z, Zang C, Cui K, Schones DE, Barski A, Peng W, Zhao K. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 2009; 138: 1019-1031.
123. Xu L, Lavinsky RM, Dasen JS, Flynn SE, McInerney EM, Mullen TM, Heinzel T, Szeto D, Korzus E, Kurokawa R, Aggarwal AK, Rose DW, Glass CK, Rosenfeld MG. Signal-specific co-activator domain requirements for Pit-1 activation. Nature 1998; 395: 301-306.
124. 2 receptor-dependent inhibition of the prolactin gene. Mol Endocrinol 2005; 19: 1904-1917.
125. Sharp ZD, Mancini MG, Hinojos CA, Dai F, Berno V, Szafran AT, Smith KP, Lele TP, Ingber DE, Mancini MA. Estrogen-receptor-alpha exchange and chromatin dynamics are ligand- and domain-dependent. J Cell Sci 2006; 119: 4101-4116.
126. Diamond SE, Gutierrez-Hartmann A. The Pit-1beta domain dictates active repression and alteration of histone acetylation of the proximal prolactin promoter. J Biol Chem 2000; 275: 30977-30986.