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
Manfroid, Isabelle; Van de Weerdt, Cécile; Baudhuin, Arianeet al.
2005 • In Molecular and Cellular Endocrinology, 229 (1-2), p. 127-39
[en] Normal and neoplastic human mammary gland cells are targets for the proliferative action of prolactin. These cells also synthesize prolactin, thereby inducing an autocrine/paracrine proliferative loop. We present the first extensive analysis of the transcriptional regulation of the human prolactin gene (hPRL) in human mammary tumor cells, SK-BR-3. We show that the pituitary promoter is functional in these cells in the absence of the pituitary-specific factor Pit-1. Expression of exogenous Pit-1 or epidermal growth factor (EGF) treatment stimulates the transfected hPRL pituitary promoter and the endogenous hPRL expression. EGF stimulation is mediated by increased synthesis of c-fos and c-jun, resulting in AP-1 binding to the proximal hPRL pituitary promoter. This regulation involves the EGF receptor, possibly ErbB2 that is highly expressed in SK-BR-3 cells, and a PI3K/JNK pathway. The stimulation of hPRL gene transcription by EGF in mammary cells may include hPRL in a complex regulatory network controlling growth of human mammary cells.
Van de Weerdt, Cécile ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire
Baudhuin, Ariane
Martial, Joseph ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire
Muller, Marc ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire
Language :
English
Title :
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
Publication date :
2005
Journal title :
Molecular and Cellular Endocrinology
ISSN :
0303-7207
eISSN :
1872-8057
Publisher :
North Holland Publishing Company, Amsterdam, Netherlands
J.J. Acosta, R.M. Munoz, L. Gonzalez, A. Subtil-Rodriguez, M.A. Dominguez-Caceres, J.M. Garcia-Martinez, A. Calcabrini, I. Lazaro-Trueba, and J. Martin-Perez Src mediates prolactin-dependent proliferation of T47D and MCF7 cells via the activation of focal adhesion kinase/Erk1/2 and phosphatidylinositol 3-kinase pathways Mol. Endocrinol. 17 2003 2268 2282
E. Anderson, J.E. Ferguson, H. Morten, S.M. Shalet, E.L. Robinson, and A. Howell Serum immunoreactive and bioactive lactogenic hormones in advanced breast cancer patients treated with bromocriptine and octreotide Eur. J. Cancer 29 1993 209 217
S.S. Bacus, C.R. Zelnick, G. Plowman, and Y. Yarden Expression of the erbB-2 family of growth factor receptors and their ligands in breast cancers Implication for tumor biology and clinical behavior Am. J. Clin. Pathol. 102 1994 13 24
N. Ben-Jonathan, K. Liby, M. McFarland, and M. Zinger Prolactin as an autocrine/paracrine growth factor in human cancer Trends Endocrinol. Metab. 13 2002 245 250
M. Berwaer, J.A. Martial, and J.R. Davis Characterization of an up-stream promoter directing extrapituitary expression of the human prolactin gene Mol. Endocrinol. 8 1994 635 642
M. Berwaer, B. Peers, A.M. Nalda, P. Monget, J.R. Davis, A. Belayew, and J.A. Martial Thyrotropin-releasing hormone and epidermal growth factor induce human prolactin expression via identical multiple cis elements Mol. Cell. Endocrinol. 92 1993 1 7
M. Berwaer, P. Monget, P. Peers, M. Mathy-Hartert, E. Bellefroid, J.R. Davis, A. Belayew, and J.A. Martial Multihormonal regulation of the human prolactin gene expression from 5000 bp of its upstream sequence Mol. Cell. Endocrinol. 80 1991 53 64
J.M. Bhatavdekar, N.G. Shah, D.B. Balar, D.D. Patel, A. Bhaduri, S.N. Trivedi, N.H. Karelia, N. Ghosh, M.K. Shukla, and D.D. Giri Plasma prolactin as an indicator of disease progression in advanced breast cancer Cancer 65 1990 2028 2032
R. Biswas, and B.K. Vonderhaar Role of serum in the prolactin responsiveness of MCF-7 human breast cancer cells in long-term tissue culture Cancer Res. 47 1987 3509 3514
A.K. Brar, C.A. Kessler, and S. Handwerger An Ets motif in the proximal decidual prolactin promoter is essential for basal gene expression J. Mol. Endocrinol. 29 2002 99 112
L. Caccavelli, I. Manfroid, J.A. Martial, and M. Muller Transcription factor AP1 is involved in basal and okadaic acid-stimulated activity of the human PRL promoter Mol. Endocrinol. 12 1998 1215 1227
N.Y. Chen, L. Holle, W. Li, S.K. Peirce, M.T. Beck, and W.Y. Chen In vivo studies of the anti-tumor effects of a human prolactin antagonist, hPRL-G129R Int. J. Oncol. 20 2002 813 818
P. Chomczynski, P.A. Soszynski, and L.A. Frohman Stimulatory effect of thyroid hormone on growth hormone gene expression in a human pituitary cell line J. Clin. Endocrinol. Metab. 77 1993 281 285
C.V. Clevenger, W.P. Chang, W. Ngo, T.L. Pasha, K.T. Montone, and J.E. Tomaszewski Expression of prolactin and prolactin receptor in human breast carcinoma evidence for anautocrine/paracrine loop Am. J. Pathol. 146 1995 695 705
C.V. Clevenger, P.A. Furth, S.E. Hankinson, and L.A. Schuler The role of prolactin in mammary carcinoma Endocr. Rev. 24 2003 1 27
G.E. DiMattia, B. Gellersen, H.G. Bohnet, and H.G. Friesen A human B-lymphoblastoid cell line produces prolactin Endocrinology 122 1988 2508 2517
G.E. DiMattia, B. Gellersen, M.L. Duckworth, and H.G. Friesen Human prolactin gene expression The use of an alternative noncoding exon in decidua and the IM-9-P3 lymphoblast cell line J. Biol. Chem. 265 1990 16412 16421
K. Fields, E. Kulig, and R.V. Lloyd Detection of prolactin messenger RNA in mammary and other normal and neoplastic tissues by polymerase chain reaction Lab. Invest. 68 1993 354 360
G. Fuh, and J.A. Wells Prolactin receptor antagonists that inhibit the growth of breast cancer cell lines J. Biol. Chem. 270 1995 13133 13137
M. Gaasenbeek, B. Gellersen, and G.E. DiMattia DNase I hypersensitivity analysis of non-pituitary human prolactin gene expression Mol. Cell Endocrinol. 152 1999 147 159
B. Gellersen, G.E. DiMattia, H.G. Friesen, and H.G. Bohnet Prolactin (PRL) mRNA from human decidua differs from pituitary PRL mRNA but resembles the IM-9-P3 lymphoblast PRL transcript Mol. Cell. Endocrinol. 64 1989 127 130
B. Gellersen, R. Kempf, R. Telgmann, and G.E. DiMattia Nonpituitary human prolactin gene transcription is independent of Pit-1 and differentially controlled in lymphocytes and in endometrial stroma Mol. Endocrinol. 8 1994 356 373
B. Gellersen, R. Kempf, R. Telgmann, and G.E. DiMattia Pituitary-type transcription of the human prolactin gene in the absence of Pit-1 Mol. Endocrinol. 9 1995 887 901
S. Gerlo, W. Vanden Berghe, P. Verdood, E.L. Hooghe-Peters, and R. Kooijman Regulation of prolactin expression in leukemic cell lines and peripheral blood mononuclear cells J. Neuroimmunol. 135 2003 107 116
E. Ginsburg, and B.K. Vonderhaar Prolactin synthesis and secretion by human breast cancer cells Cancer Res. 55 1995 2591 2595
S.E. Hankinson, W.C. Willett, D.S. Michaud, J.E. Manson, G.A. Colditz, C. Longcope, B. Rosner, and F.E. Speizer Plasma prolactin levels and subsequent risk of breast cancer in postmenopausal women J. Natl. Cancer Inst. 91 1999 629 634
M. Hibi, A. Lin, T. Smeal, A. Minden, and M. Karin Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain Genes Dev. 7 1993 2135 2148
N. Hoggard, J.R. Davis, M. Berwaer, P. Monget, B. Peers, A. Belayew, and J.A. Martial Pit-1 binding sequences permit calcium regulation of human prolactin gene expression Mol. Endocrinol. 5 1991 1748 1754
W. Holtkamp, G.A. Nagel, H.E. Wander, H.F. Rauschecker, and D. von Heyden Hyperprolactinemia is an indicator of progressive disease and poor prognosis in advanced breast cancer Int. J. Cancer 34 1984 323 328
H. Kim, and W.J. Muller The role of the epidermal growth factor receptor family in mammary tumorigenesis and metastasis Exp. Cell Res. 253 1999 78 87
J.S. Lai, and W. Herr Ethidium bromide provides a simple tool for identifying genuine DNA-independent protein associations Proc. Natl. Acad. Sci. U.S.A. 89 1992 6958 6962
F. Le Provost, C. Leroux, P. Martin, P. Gaye, and J. Djiane Prolactin gene expression in ovine and caprine mammary gland Neuroendocrinology 60 1994 305 313
M. Llovera, C. Pichard, S. Bernichtein, S. Jeay, P. Touraine, P.A. Kelly, and V. Goffin Human prolactin (hPRL) antagonists inhibit hPRL-activated signaling pathways involved in breast cancer cell proliferation Oncogene 19 2000 4695 4705
M. Llovera, P. Touraine, P.A. Kelly, and V. Goffin Involvement of prolactin in breast cancer: redefining the molecular targets Exp. Gerontol. 35 2000 41
I. Manfroid, J.A. Martial, and M. Muller Inhibition of protein phosphatase PP1 in GH3B6, but not in GH3 cells, activates the MEK/ERK/c-fos pathway and the human prolactin promoter, involving the coactivator CPB/p300 Mol. Endocrinol. 15 2001 625 637
M. Muller, M. Berwaer, L. Caccavelli, I. Manfroid, A. Nalda, H. Pendeville, F. Pernasetti, C. Van de Weerdt, B. Peers, and J.A. Martial Transcriptional regulation of the prolactin gene Médecine/Sci. 14 1998 580 587
A.M. Nalda, J.A. Martial, and M. Muller The glucocorticoid receptor inhibits the human prolactin gene expression by interference with Pit-1 activity Mol. Cell. Endocrinol. 134 1997 129 137
N. Paris, F. Rentier-Delrue, A. Defontaine, V. Goffin, J.J. Lebrun, L. Mercier, and J.A. Martial Bacterial production and purification of recombinant human prolactin Biotechnol. Appl. Biochem. 12 1990 436 449
B. Peers, P. Monget, M.A. Nalda, M.L. Voz, M. Berwaer, A. Belayew, and J.A. Martial Transcriptional induction of the human prolactin gene by cAMP requires two cis-acting elements and at least the pituitary-specific factor Pit-1 J. Biol. Chem. 266 1991 18127 18134
B. Peers, M.L. Voz, P. Monget, M. Mathy-Hartert, M. Berwaer, A. Belayew, and J.A. Martial Regulatory elements controlling pituitary-specific expression of the human prolactin gene Mol. Cell. Biol. 10 1990 4690 4700
I. Pellegrini, J.J. Lebrun, S. Ali, and P.A. Kelly Expression of prolactin and its receptor in human lymphoid cells Mol. Endocrinol. 6 1992 1023 1031
F. Pernasetti, L. Caccavelli, C. Van de Weerdt, J.A. Martial, and M. Muller Thyroid hormone inhibits the human prolactin gene promoter by interfering with activating protein-1 and estrogen stimulations Mol. Endocrinol. 11 1997 986 996
Y. Pohnke, R. Kempf, and B. Gellersen CCAAT/enhancer-binding proteins are mediators in the protein kinase A-dependent activation of the decidual prolactin promoter J. Biol. Chem. 274 1999 24808 24818
A.C. Poncelet, B. Levavi-Sivan, M. Muller, Z. Yaron, J.A. Martial, and A. Belayew The tilapia prolactin I gene: evolutionary conservation of the regulatory elements directing pituitary-specific expression DNA Cell. Biol. 15 1996 679 692
G.H. Reem, D.W. Ray, and J.R. Davis The human prolactin gene upstream promoter is regulated in lymphoid cells by activators of T-cells and by cAMP J. Mol. Endocrinol. 22 1999 285 292
C. Reynolds, K.T. Montone, C.M. Powell, J.E. Tomaszewski, and C.V. Clevenger Expression of prolactin and its receptor in human breast carcinoma Endocrinology 138 1997 5555 5560
M.D. Schroeder, J.L. Brockman, A.M. Walker, and L.A. Schuler Inhibition of prolactin (PRL)-induced proliferative signals in breast cancer cells by a molecular mimic of phosphorylated PRL S179D-PRL Endocrinology 144 2003 5300 5307
C.M. Shaw-Bruha, S.J. Pirrucello, and J.D. Shull Expression of the prolactin gene in normal and neoplastic human breast tissues and human mammary cell lines: promoter usage and alternative mRNA splicing Breast Cancer Res. Treat. 44 1997 243 253
R.P. Shiu, L.C. Murphy, D. Tsuyuki, Y. Myal, M. Lee-Wing, and B. Iwasiow Biological actions of prolactin in human breast cancer Recent Prog. Horm. Res. 43 1987 277 303
D.J. Slamon, G.M. Clark, S.G. Wong, W.J. Levin, A. Ullrich, and W.L. McGuire Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene Science 235 1987 177 182
I. Struman, F. Bentzien, H. Lee, V. Mainfroid, G. D'Angelo, V. Goffin, R.I. Weiner, and J.A. Martial Opposing actions of intact and N-terminal fragments of the human prolactin/growth hormone family members on angiogenesis: an efficient mechanism for the regulation of angiogenesis Proc. Natl. Acad. Sci. U.S.A. 96 1999 1246 1251
R. Telgmann, E. Maronde, K. Tasken, and B. Gellersen Activated protein kinase A is required for differentiation-dependent transcription of the decidual prolactin gene in human endometrial stromal cells Endocrinology 138 1997 929 937
A.T. Truong, C. Duez, A. Belayew, A. Renard, R. Pictet, G.I. Bell, and J.A. Martial Isolation and characterization of the human prolactin gene EMBO J. 3 1984 429 437
C. Van De Weerdt, B. Peers, A. Belayew, J.A. Martial, and M. Muller Far upstream sequences regulate the human prolactin promoter transcription Neuroendocrinology 71 2000 124 137
J.W. Voss, L. Wilson, and M.G. Rosenfeld POU-domain proteins Pit-1 and Oct-1 interact to form a heteromeric complex and can cooperate to induce expression of the prolactin promoter Genes Dev. 5 1991 1309 1320
T. Yamauchi, N. Yamauchi, K. Ueki, T. Sugiyama, H. Waki, H. Miki, K. Tobe, S. Matsuda, T. Tsushima, T. Yamamoto, T. Fujita, Y. Taketani, M. Fukayama, S. Kimura, Y. Yazaki, R. Nagai, and T. Kadowaki Constitutive tyrosine phosphorylation of ErbB-2 via Jak2 by autocrine secretion of prolactin in human breast cancer J. Biol. Chem. 275 2000 33937 33944