Two Tandemly Linked Interferon-γ-Activated Sequence Elements in the Promoter of Glycosylation-Dependent Cell Adhesion Molecule 1 Gene Synergistically Respond to Prolactin in Mouse Mammary Epithelial Cells

Molecular Endocrinology

Volumn 17, Issue 10, 2003, Pages 1910-1920

  Hou, Zhaoyuan ^a   Srivastava, Sunil ^a   Mistry, Meenakshi J ^a   Herbst, Matthew P ^a   Bailey, Jason P ^a   Horseman, Nelson D ^a  

^a UNIVERSITY OF CINCINNATI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; GAMMA INTERFERON; INTERCELLULAR ADHESION MOLECULE 1; JANUS KINASE; LEUCINE; PROLACTIN; SERINE; STAT5 PROTEIN; TRYPTOPHAN;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; BREAST EPITHELIUM; CONSENSUS SEQUENCE; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; GEL MOBILITY SHIFT ASSAY; GENE DELETION; GENE OVEREXPRESSION; MOLECULAR PROBE; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN GLYCOSYLATION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; TANDEM REPEAT;

ANIMALS; BINDING SITES; BLOTTING, WESTERN; CHO CELLS; CRICETINAE; CRICETULUS; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; INTERFERON TYPE II; JANUS KINASE 2; LUCIFERASES; MAMMARY GLANDS, HUMAN; MICE; MICE, INBRED ICR; MILK PROTEINS; MUCINS; MUTAGENESIS, SITE-DIRECTED; PROLACTIN; PROMOTER REGIONS (GENETICS); PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; STAT5 TRANSCRIPTION FACTOR; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC; TRANSFECTION;

ANIMALIA; JANUS;

EID: 0142024974     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2003-0045     Document Type: Article

References (52)

1. Horseman ND, Yu-Lee LY 1994 Transcriptional regulation by the helix bundle peptide hormones: growth hormone, prolactin, and hematopoietic cytokines. Endocr Rev 5:627-649
2. Bole-Feysot C, Goffin V, Edery M, Binart N, Kelly PA 1998 Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr Rev 19:225-268
3. Darnell Jr JE 1997 STATs and gene regulation. Science 277:1630-1635
4. Han Y, Watling D, Rogers NC, Stark GR 1997 JAK2 and STAT5, but not JAK1 and STAT1, are required for prolactin-induced β-lactoglobulin transcription. Mol Endocrinol 11:1180-1188
5. Gao J, Hughes JP, Auperin B, Buteau H, Edery M, Zhuang H, Wojchowski DM, Horseman ND 1996 Interactions among Janus kinases and the prolactin (PRL) receptor in the regulation of a PRL response element. Mol Endocrinol 10:847-856
6. Ihle JN 2001 The Stat family in cytokine signaling. Curr Opin Cell Biol 13:211-217
7. Wakao H, Gouilleux F, Groner B 1994 Mammary gland factor (MGF) is a novel member of the cytokine regulated transcription factor gene family and confers the prolactin response. EMBO J 13:2182-2191
8. Liu X, Robinson GW, Gouilleux F, Groner B, Hennighausen L 1995 Cloning and expression of Stat5 and an additional homologue (Stat5b) involved in prolactin signal transduction in mouse mammary tissue. Proc Natl Acad Sci USA 92:8831-8835
9. Lin JX, Mietz J, Modi WS, John S, Leonard WJ 1996 Cloning of human Stat5B. Reconstitution of interleukin-2-induced Stat5A and Stat5B DNA binding activity in COS-7 cells. J Biol Chem 271:10738-10744
10. Xu X, Sun YL, Hoey T 1996 Cooperative DNA binding and sequence-selective recognition conferred by the STAT amino-terminal domain. Science 273:794-797
11. Vinkemeier U, Cohen SL, Moarefi I, Chait BT, Kuriyan J, Darnell Jr JE 1996 DNA binding of in vitro activated Stat1 α, Stat1 β and truncated Stat1: interaction between NH2-terminal domains stabilizes binding of two dimers to tandem DNA sites. EMBO J 15:5616-5626
12. John S, Vinkemeier U, Soldaini E, Darnell Jr JE, Leonard WJ 1999 The significance of tetramerization in promoter recruitment by Stat5. Mol Cell Biol 19:1910-1918
13. Verdier F, Rabionet R, Gouilleux F, Beisenherz-Huss C, Varlet P, Muller O, Mayeux P, Lacombe C, Gisselbrecht S, Chretien S 1998 A sequence of the CIS gene promoter interacts preferentially with two associated STAT5A dimers: a distinct biochemical difference between STAT5A and STAT5B. Mol Cell Biol 18:5852-5860
14. Rosen JM, Wyszomierski SL, Hadsell D 1999 Regulation of milk protein gene expression. Annu Rev Nutr 19:407-436
15. Wartmann M, Cella N, Hofer P, Groner B, Liu X, Hennighausen L, Hynes NE 1996 Lactogenic hormone activation of Stat5 and transcription of the β-casein gene in mammary epithelial cells is independent of p42 ERK2 mitogen-activated protein kinase activity. J Biol Chem 271:31863-31868
16. Sorensen P, Sheffield LG 1997 Involvement of c-src in β-casein expression by mammary epithelial cells. Biochem Biophys Res Commun 241:710-713
17. al-Sakkaf KA, Dobson PR, Brown BL 1997 Prolactin induced tyrosine phosphorylation of p59fyn may mediate phosphatidylinositol 3-kinase activation in Nb2 cells. J Mol Endocrinol 19:347-350
18. Watson CJ, Burdon TG 1996 Prolactin signal transduction mechanisms in the mammary gland: the role of the Jak/Stat pathway. Rev Reprod 1:1-5
19. Schmitt-Ney M, Doppler W, Ball RK, Groner B 1991 β-Casein gene promoter activity is regulated by the hormone-mediated relief of transcriptional repression and a mammary-gland-specific nuclear factor. Mol Cell Biol 11:3745-3755
20. Pierre S, Jolivet G, Devinoy E, Houdebine LM 1994 A combination of distal and proximal regions is required for efficient prolactin regulation of transfected rabbit α s1-casein chloramphenicol acetyltransferase constructs. Mol Endocrinol 8:1720-1730
21. Burdon TG, Maitland KA, Clark AJ, Wallace R, Watson CJ 1994 Regulation of the sheep β-lactoglobulin gene by lactogenic hormones is mediated by a transcription factor that binds an interferon-γ activation site-related element. Mol Endocrinol 8:1528-1536
22. Devinoy E, Malienou-N' Gassa R, Thepot D, Puissant C, Houdebine LM 1991 Hormone responsive elements within the upstream sequences of the rabbit whey acidic protein (WAP) gene direct chloramphenicol acetyl transferase (CAT) reporter gene expression in transfected rabbit mammary cells. Mol Cell Endocrinol 81:185-193
23. Li S, Rosen JM 1995 Nuclear factor I and mammary gland factor (STAT5) play a critical role in regulating rat whey acidic protein gene expression in transgenic mice. Mol Cell Biol 15:2063-2070
24. Hou Z, Bailey JP, Vomachka AJ, Matsuda M, Lockefeer JA, Horseman ND 2000 Glycosylation-dependent cell adhesion molecule 1 (GlyCAM 1) is induced by prolactin and suppressed by progesterone in mammary epithelium. Endocrinology 141:4278-4283
25. Lasky LA, Singer MS, Dowbenko D, Imai Y, Henzel WJ, Grimley C, Fennie C, Gillett N, Watson SR, Rosen SD 1992 An endothelial ligand for L-selectin is a novel mucin-like molecule. Cell 69:927-938
26. Dowbenko D, Kikuta A, Fennie C, Gillett N, Lasky LA 1993 Glycosylation-dependent cell adhesion molecule 1 (GlyCAM 1) mucin is expressed by lactating mammary gland epithelial cells and is present in milk. J Clin Invest 92:952-960
27. Imagawa W, Bandyopadhyay GK, Nandi S 1995 Analysis of the proliferative response to lysophosphatidic acid in primary cultures of mammary epithelium: differences between normal and tumor cells. Exp Cell Res 216:178-186
28. +-2 Cl-cotransporter. Mol Endocrinol 14:2054-2065
29. Shan L, Rouhani SA, Schut HA, Snyderwine EG 2001 2-Amino-1-methyl-6- phenylimidazo[4,5-b]pyridine (PhlP) modulates lactogenic hormone-mediated differentiation and gene expression in HC11 mouse mammary epithelial cells. Cell Growth Differ 12:649-656
30. Frasor J, Barkai U, Zhong L, Fazleabas AT, Gibori G 2001 PRL-induced ERα gene expression is mediated by Janus kinase 2 (Jak2) while signal transducer and activator of transcription 5b (Stat5b) phosphorylation involves Jak2 and a second tyrosine kinase. Mol Endocrinol 15:1941-1952
31. Wang D, Stravopodis D, Teglund S, Kitazawa J, Ihle JN 1996 Naturally occurring dominant negative variants of Stat5. Mol Cell Biol 16:6141-6148
32. Perrot-Applanat M, Gualillo O, Buteau H, Edery M, Kelly PA 1997 Internalization of prolactin receptor and prolactin in transfected cells does not involve nuclear translocation. J Cell Sci 110:1123-1132
33. Stocklin E, Wissler M, Gouilleux F, Groner B 1996 Functional interactions between Stat5 and the glucocorticoid receptor. Nature 383:726-728
34. Vinkemeier U, Moarefi I, Darnell Jr JE, Kuriyan J 1998 Structure of the amino-terminal protein interaction domain of Stat4. Science 279:1048-1052
35. Meyer WK, Reichenbach P, Schindler U, Soldaini E, Nabholz M 1997 Interaction of STAT5 dimers on two low affinity binding sites mediates interleukin 2 (IL-2) stimulation of IL-2 receptor a gene transcription. J Biol Chem 272:31821-31828
36. Thordarson G, Villalobos R, Colosi P, Southard J, Ogren L, Talamantes F 1986 Lactogenic response of cultured mouse mammary epithelial cells to mouse placental lactogen. J Endocrinol 109:263-274
37. Hennighausen L, Robinson GW, Wagner KU, Liu W 1997 Prolactin signaling in mammary gland development. J Biol Chem 272:7567-7569
38. Clevenger CV, Rycyzyn MA, Syed F, Kline JB 2001 Prolactin receptor signal transduction. In: Horseman ND, ed. Prolactin. Norwell, MA: Kluwer Academic Publishers; 355-380
39. Liu X, Robinson GW, Wagner KU, Garrett L, Wynshaw-Boris A, Hennighausen L 1997 Stat5a is mandatory for adult mammary gland development and lactogenesis. Genes Dev 11:179-186
40. Udy GB, Towers RP, Snell RG, Wilkins RJ, Park SH, Ram PA, Waxman DJ, Davey HW 1997 Requirement of STAT5b for sexual dimorphism of body growth rates and liver gene expression. Proc Natl Acad Sci USA 94:7239-7244
41. Teglund S, McKay C, Schuetz E, van Deursen JM, Stravopodis D, Wang D, Brown M, Bodner S, Grosveld G, Ihle JN 1998 Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell 93:841-850
42. Dusanter-Fourt I, Muller O, Ziemiecki A, Mayeux P, Drucker B, Djiane J, Wilks A, Harpur AG, Fischer S, Gisselbrecht S 1994 Identification of JAK protein tyrosine kinases as signaling molecules for prolactin. Functional analysis of prolactin receptor and prolactin-erythropoietin receptor chimera expressed in lymphoid cells. EMBO J 13:2583-2591
43. Campbell GS, Argetsinger LS, Ihle JN, Kelly PA, Rillema JA, Carter-Su C 1994 Activation of JAK2 tyrosine kinase by prolactin receptors in Nb2 cells and mouse mammary gland explants. Proc Natl Acad Sci USA 91:5232-5236
44. Wang Y, O'Neal KD, Yu-Lee L 1997 Multiple prolactin (PRL) receptor cytoplasmic residues and Stat1 mediate PRL signaling to the interferon regulatory factor-1 promoter. Mol Endocrinol 11:1353-1364
45. DaSilva L, Rui H, Erwin RA, Howard OM, Kirken RA, Malabarba MG, Hackett RH, Larner AC, Farrar WL 1996 Prolactin recruits STAT1, STAT3 and STAT5 independent of conserved receptor tyrosines TYR402, TYR479, TYR515 and TYR580. Mol Cell Endocrinol 117:131-140
46. Durbin JE, Hackenmiller R, Simon MC, Levy DE 1996 Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 84:443-450
47. Philp JA, Burdon TG, Watson CJ 1996 Differential activation of STATs 3 and 5 during mammary gland development. FEBS Lett 396:77-80
48. Strehlow I, Schindler C 1998 Amino-terminal signal transducer and activator of transcription (STAT) domains regulate nuclear translocation and STAT deactivation. J Biol Chem 273:28049-28056
49. Wong P, Severns CW, Guyer NB, Wright TM 1994 A unique palindromic element mediates γ interferon induction of mig gene expression. Mol Cell Biol 14:914-922
50. Guyer NB, Severns CW, Wong P, Feghali CA, Wright TM 1995 IFN-γ induces a p91/Stat1 α-related transcription factor with distinct activation and binding properties. J Immunol 155:3472-3480
51. Soldaini E, John S, Moro S, Bollenbacher J, Schindler U, Leonard WJ 2000 DNA binding site selection of dimeric and tetrameric Stat5 proteins reveals a large repertoire of divergent tetrameric Stat5a binding sites. Mol Cell Biol 20:389-401
52. Sidis Y, Horseman ND 1994 Prolactin induces rapid p95/p70 tyrosine phosphorylation, and protein binding to GAS-like sites in the anx Icp35 and c-fos genes. Endocrinology 134:1979-1985