Reproductive actions of prolactin mediated through short and long receptor isoforms

Molecular and Cellular Endocrinology

Volumn 382, Issue 1, 2014, Pages 400-410

  Sangeeta Devi, Y ^a   Halperin, Julia ^b,c  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b DEPARTAMENTO DE CIENCIAS NATURALES Y ANTROPOLOGÍA   (Argentina)

^c Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

Corpus luteum; Endothelial cells; Ovary; Prolactin; Prolactin receptor; Reproduction

Indexed keywords

ISOPROTEIN; PROLACTIN; PROLACTIN RECEPTOR;

FEMALE FERTILITY; HUMAN; MEMBRANE BINDING; NONHUMAN; OVARY; OVARY FUNCTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR BINDING; REVIEW; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; UTERUS;

CORPUS LUTEUM; ENDOTHELIAL CELLS; OVARY; PROLACTIN; PROLACTIN RECEPTOR; REPRODUCTION;

ANIMALS; HUMANS; MODELS, BIOLOGICAL; PROLACTIN; PROTEIN ISOFORMS; RECEPTORS, PROLACTIN; REPRODUCTION; SIGNAL TRANSDUCTION;

EID: 84888301314     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.09.016     Document Type: Review

References (164)

1. Aksamitiene E., Achanta S., Kolch W., Kholodenko B.N., Hoek J.B., Kiyatkin A. Prolactin-stimulated activation of ERK1/2 mitogen-activated protein kinases is controlled by PI3-kinase/Rac/PAK signaling pathway in breast cancer cells. Cell. Signal. 2011, 23:1794-1805.
2. Alam H., Weck J., Maizels E., Park Y., Lee E.J., Ashcroft M., Hunzicker-Dunn M. Role of the phosphatidylinositol-3-kinase and extracellular regulated kinase pathways in the induction of hypoxia-inducible factor (HIF)-1 activity and the HIF-1 target vascular endothelial growth factor in ovarian granulosa cells in response to follicle-stimulating hormone. Endocrinology 2009, 150:915-928.
3. Alam S.M.K., Konno M.A.T., Rumi K., Dong Y., Weiner C.P., Soares M.J. Prolactin family of the Guinea Pig. Cavia porcellus Endocrinology 2010, 151(8):3918.
4. Ali S., Pellegrini I., Kelly P.A. A prolactin-dependent immune cell line (Nb2) expresses a mutant form of prolactin receptor. J. Biol. Chem. 1991, 266:20110-20117.
5. Bachelot A., Beaufaron J., Servel N., Kedzia C., Monget P., Kelly P.A., Gibori G., Binart N. Prolactin independent rescue of mouse corpus luteum life span: identification of prolactin and luteinizing hormone target genes. Am. J. Physiol. Endocrinol. Metab. 2009, 297(3). pp. E676-684.
6. Bao L., Tessier C., Prigent-Tessier A., Li F., Buzzio O.L., Callegari E.A., Horseman N.D., Gibori G. Decidual prolactin silences the expression of genes detrimental to pregnancy. Endocrinology 2007, 148:2326-2334.
7. Ben-Batalla I., Seoane S., Macia M., Garcia-Caballero T., Gonzalez L.O., 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(1):73-85.
8. Ben-Jonathan N. Dopamine: a prolactin-inhibiting hormone. Endocr. Rev. 1985, 6:564-589.
9. Ben-Jonathan N., Mershon J.L., Steinmetz R.W. Extrapituitary prolactin: distribution, regulation, functions, and clinical aspects. Endocr. Rev. 1996, 17:639-669.
10. Ben-Jonathan N., LaPensee C.R., LaPensee E.W. What can we learn from rodents about prolactin in humans?. Endocr. Rev. 2008, 29(1):1-41.
11. Berlanga J.J., Garcia-Ruiz J.P., Perrot-Applanat M., Kelly P.A., Edery M. The short form of the prolactin receptor silences prolactin induction of the β-casein gene promoter. Mol. Endocrinol. 1997, 11:1449-1457.
12. Berwaer M., Monget P., Peers B., Mathy-Hartert M., Bellefroid E., Davis J.R., Belayew A., Martial J.A. Multihormonal regulation of the human prolactin gene expression from 5000 bp of its upstream sequence. Mol. Cell Endocrinol. 1991, 80:53-64.
13. Berwaer M., Martial J.A., Davis J.R. Characterization of an up-stream promoter directing extrapituitary expression of the human prolactin gene. Mol Endocrinol. 1994, 8:635-642.
14. Bignon C., Binart N., Ormandy C., Schuler L.A., Kelly P.A., Djiane J. Long and short forms of the ovine prolactin receptor: cDNA cloning and genomic analysis reveal that the two forms arise by different alternative splicing mechanisms in ruminants and in rodents. J. Mol. Endocrinol. 1997, 19:109-120.
15. Bignon C., Daniel N., Belair L., Djiane J. In vitro expression of long and short ovine prolactin receptors: activation of Jak2/STAT5 pathway is not sufficient to account for prolactin signal transduction to the ovine beta-lactoglobulin gene promoter. J. Mol. Endocrinol. 1999, 23:125-136.
16. Binart N., Helloco C., Ormandy C.J., Barra J., Clement-Lacroix P., Baran N., Kelly P.A. Rescue of preimplantatory egg development and embryo implantation in prolactin receptor-deficient mice after progesterone administration. Endocrinology 2000, 141:2691-2697.
17. Binart N., Imbert-Bollore P., Baran N., Viglietta C., Kelly P.A. A short form of the prolactin (PRL) receptor is able to rescue mammopoiesis in heterozygous PRL receptor mice. Mol. Endocrinol. 2003, 17:1066-1074.
18. Binart N., Bachelot A., Bouilly J. Impact of prolactin receptor isoforms on reproduction. Trends. Endocrinol. Metab. 2010, 21:362-368.
19. Bole-Feysot C., Goffin V., Edery M., Binart N., Kelly P.A. Prolactin and its receptor: actions, signal transduction pathways and phenotypes observed in prolactin receptor knock-out mice. Endocr. Rev. 1998, 19:225-268.
20. Borcherding D.C., Hugo E.R., Idelman G., De Silva A., Richtand N.W., Loftus J., Ben-Jonathan N. Dopamine receptors in human adipocytes: expression and functions. PLoS One 2011, 6(9):e25537.
21. Bouilly J., Sonigo C., Auffret J., Gibori G., Binart N. Prolactin signaling mechanisms in ovary. Mol. Cell Endocrinol. 2012, 356(1-2):80-87.
22. Boutin J.M., Jolicoeur C., Okamura H., Gagnon J., Edery M., Shirota M., Banville D., Dusanter-Fourt I., Djiane J., Kelly P.A. Cloning and expression of the rat prolactin receptor, a member of the growth hormone/prolactin receptor gene family. Cell 1988, 53(1):69-77.
23. Boutin J.M., Edery M., Shirota M., Jolicoeur C., Lesueur L., Ali S., Gould D., Djiane J., Kelly P.A. Identification of a cDNA encoding a long form of prolactin receptor in human hepatoma and breast cancer cells. Mol. Endocrinol. 1989, 3(9):1455-1461.
24. Brisken C., Kaur S., Chavarria T.E., Binart N., Sutherland R.L., Weinberg R.A., Kelly P.A., Ormandy C.J. Prolactin controls mammary gland development via direct and indirect mechanisms. Dev. Biol. 1999, 210:96-106.
25. Brooks C.L. Molecular mechanisms of prolactin and its receptor. Endocr. Rev. 2012, 33(4):504-525.
26. Buzzio O.L., Lu Z., Miller C.D., Unterman T.G., Kim J.J. FOXO1A differentially regulates genes of decidualization. Endocrinology 2006, 147(8):3870-3876.
27. Campbell G.S., Argetsinger L.S., Ihle J.N., Kelly P.A., Rillema J.A., Carter-Su C. Activation of JAK2 tyrosine kinase by prolactin receptors in Nb2 cells and mouse mammary gland explants. Proc. Natl. Acad. Sci. USA 1994, 91:5232-5236.
28. Castrillon D.H., Miao L., Kollipara R., Horner J.W., DePinho R.A. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 2003, 301:215-218.
29. Chen J.C., Lin J.H., Wu L.S., Tsai Y.F., Su T.H., Chen C.J., Chen T.J. Luteotropic roles of prolactin in early pregnant hamsters. Biol. Reprod. 2002, 67:8-13.
30. Christian M., Zhang X., Schneider-Merck T., Unterman T.G., Gellersen B., White J.O., Brosens J.J. Cyclic AMP-induced forkhead transcription factor, FKHR, cooperates with CCAAT/enhancer-binding protein β in differentiating human endometrial stromal cells. J. Biol. Chem. 2002, 277:20825-20832.
31. Clarke D.L., Linzer D.I. Changes in prolactin receptor expression during pregnancy in the mouse ovary. Endocrinology 1993, 133:224-232.
32. Clarke D.L., Arey B.J., Linzer D.I. Prolactin receptor messenger ribonucleic acid expression in the ovary during the rat estrous cycle. Endocrinology 1993, 133:2594-2603.
33. Clevenger C.V., Kline J.B. Prolactin receptor signal transduction. Lupus 2001, 10(10):706-718.
34. Clevenger C.V., Furth P.A., Hankinson S.E., Schuler L.A. The role of prolactin in mammary carcinoma. Endocr. Rev. 2003, 24:1-27.
35. Craven A., Ormandy C., Robertson F., Kelly P., Nixon A., Pearson A. Prolactin signalling influences the timing mechanism of the hair follicle: analysis of hair growth cycles in prolactin receptor knockout mice. Endocrinology 2001, 142:2533-2539.
36. Cunningham B.C., Bass S., Fuh G., Wells J.A. Zinc mediation of the binding of human growth hormone to the human prolactin receptor. Science 1990, 250:1709-1712.
37. Dai G., Chapman B.M., Liu B., Orwig K.E., Wang D., White R.A., Preuett B., Soares M.J. A new member of the mouse prolactin (PRL)-like protein-C subfamily, PRL-like protein-C_: structure and expression. Endocrinology 1998, 139:5157-5163.
38. Das R., Vonderhaar B.K. Transduction of prolactin's (PRL) growth signal through both long and short forms of the PRL receptor. Mol. Endocrinol. 1995, 9:1750-1759.
39. DaSilva L., Rui H., Erwin R.A., Howard O.M., Kirken R.A., Malabarba M.G., Hackett R.H., Larner A.C., Farrar W.L. Prolactin recruits STAT1, STAT3 and STAT5 independent of conserved receptor tyrosines TYR402, TYR479, TYR515 and TYR580. Mol. Cell Endocrinol. 1996, 117:131-140.
40. Davis J.A., Linzer D.I. Expression of multiple forms of the prolactin receptor in mouse liver. Mol. Endocrinol. 1989, 3:674-680.
41. Davis J.A., Linzer D.I. Mutational analysis of mouse placental lactogen II, and molecular characterization of the mouse prolactin receptor. Prog. Clin. Biol. Res. 1990, 342:127-132.
42. Devi Y.S., Shehu A., Halperin J., Stocco C., Le J., Seibold A.M., Gibori G. Prolactin signaling through the short isoform of the mouse prolactin receptor regulates DNA binding of specific transcription factors, often with opposite effects in different reproductive issues. Reprod. Biol. Endocrinol. 2009, 7:87.
43. Devi Y.S., Shehu A., Stocco C., Halperin J., Le J., Seibold A.M., Lahav M., Binart N., Gibori G. Regulation of transcription factors and repression of Sp1 by prolactin signaling through the short isoform of its cognate receptor. Endocrinology 2009, 150(7):3327-3335.
44. Devi Y.S., Seibold A.M., Shehu A., Maizels E., Halperin J., Le J., Binart N., Bao L., Gibori G. Inhibition of MAPK by prolactin signaling through the short form of its receptor in the ovary and decidua: involvement of a novel phosphatase. J. Biol. Chem. 2011, 286:7609-7618.
45. Dorrington J.H., Gore-Langton R.E. Antigonadal action of prolactin: further studies on the mechanism of inhibition of follicle-stimulating hormone-induced aromatase activity in rat granulosa cell cultures. Endocrinology 1982, 110:1701-1707.
46. Duan W.R., Linzer D.I., Gibori G. Cloning and characterization of an ovarian-specific protein that associates with the short form of the prolactin receptor. J. Biol. Chem. 1996, 271(26):15602-15607.
47. Duan W.R., Parmer T.G., Albarracin C.T., Zhong L., Gibori G. PRAP, a prolactin receptor associated protein: its gene expression and regulation in the corpus luteum. Endocrinology 1997, 138(8):3216-3221.
48. Edery M., Jolicoeur C., Levi-Meyrueis C., Dusanter-Fourt I., Pétridou B., Boutin J.M., Lesueur L., Kelly P.A., Djiane J. Identification and sequence analysis of a second form of prolactin receptor by molecular cloning of complementary DNA from rabbit mammary gland. Proc. Natl. Acad. Sci. USA 1989, 86(6):2112-2116.
49. Featherstone K., White M.R., Davis J.R. The prolactin gene: a paradigm of tissue-specific gene regulation with complex temporal transcription dynamics. J. Neuroendocrinol. 2012, 24(7):977-990.
50. Fields K., Kulig E., Lloyd R.V. Detection of prolactin messenger RNA in mammary and other normal and neoplastic tissues by polymerase chain reaction. Lab. Invest. 1993, 68(3):354-360.
51. Foitzik K., Krause K., Nixon A.J., Ford C.A., Ohnemus U., Pearson A.J., et al. Prolactin and its receptor are expressed in murine hair follicle epithelium, show hair cycle-dependent expression, and induce catagen. Am. J. Pathol. 2003, 162:1611-1621.
52. Foitzik K., Krause K., Conrad F., Nakamura M., Funk W., Paus R. Human scalp hair follicles are both a target and a source of prolactin, which serves as an autocrine and/or paracrine promoter of apoptosis-driven hair follicle regression. Am. J. Pathol. 2006, 168:748-756.
53. Frasor J., Gibori G. Prolactin regulation of estrogen receptor expression. Trends Endocrinol. Metab. 2003, 14:118-123.
54. Frasor J., Gaspar C.A., Donnelly K.M., Gibori G., Fazleabas A.T. Expression of prolactin and its receptor in the baboon uterus during the menstrual cycle and pregnancy. J. Clin. Endocrinol. Metab. 1999, 84:3344-3350.
55. Freeman M.E., Kanyicska B., Lerant A., Nagy G. Prolactin: estructure, function, and regulation of secretion. Physiol. Rev. 2000, 80:1523-1631.
56. Gabou L., Boisnard M., Gourdou I., Jammes H., Dulor J.-P., Djiane J. Cloning of rabbit prolactin cDNA and prolactin gene expression in the rabbit mammary gland. J. Mol. Endocrinol. 1996, 16:27-37.
57. Gadd S.L., Clevenger C. Ligand-independent dimerization of the human prolactin receptor isoforms: functional implications. Mol. Endocrinol. 2006, 20(11):2734-2745.
58. Gaddy-Kurten D., Hickey G.J., Fey G.H., Gauldie J., Richards J.S. Hormonal regulation and tissue-specific localization of alpha 2-macroglobulin in rat ovarian follicles and corpora lutea. Endocrinology 1989, 125:2985-2995.
59. Gala R.R., Shevach E.M. Evidence for the release of a prolactin like substance by mouse lymphocytes and macrophages. Proc. Soc. Exp. Biol. Med. 1994, 205:12-19.
60. Gallardo T.D., John G.B., Bradshaw K., Welt C., Reijo-Pera R., Vogt P.H., Touraine P., Bione S., Toniolo D., Nelson L.M., Zinn A.R., Castrillon D.H. Sequence variation at the human FOXO3 locus: a study of premature ovarian failure and primary amenorrhea. Hum. Reprod. 2008, 23:216-221.
61. Gallego M.I., Binart N., Robinson G.W., Okagaki R., Coschigano K.T., Perry J., Kopchick J.J., Oka T., Kelly P.A., Hennighausen L. Prolactin, growth hormone, and epidermal growth factor activate Stat5 in different compartments of mammary tissue and exert different and overlapping developmental effects. Dev. Biol. 2001, 229:163-175.
62. Gaytan F., Morales C., Bellido C., Aguilar E., Sanchez-Criado J.E. Role of prolactin in the regulation of macrophages and in the proliferative activity of vascular cells in newly formed and regressing rat corpora lutea. Biol. Reprod. 1997, 57:478-486.
63. Gellersen B., Kempf R., Telgmann R., DiMattia G.E. 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.
64. Gertler A., Grosclaude J., Strasburger C.J., Nir S., Djiane J. Real-time kinetic measurements of the interactions between lactogenic hormones and prolactin-receptor extracellular domains from several species support the model of hormone-induced transient receptor dimerization. J. Biol. Chem. 1996, 271(40):24482-24491.
65. Gibori G., Rothchild I., Pepe G.J., Morishige W.K., Lam P. Luteotrophic action of decidual tissue in the rat. Endocrinology 1974, 95(4):1113-1118.
66. Gort L., Boleda M.D., Tyfield L., Vilarinho L., Rivera I., Cardoso M.L., Santos-Leite M., Giros M., Briones P. Mutational spectrum of classical galactosaemia in Spain and Portugal. J. Inherit. Metab. Dis. 2006, 29. pp. 739-342.
67. Goupille O., Daniel N., Bignon C., Jolivet G., Djiane J. Prolactin signal transduction to milk protein genes: carboxy-terminal part of the prolactin receptor and its tyrosine phosphorylation are not obligatory for JAK2 and STAT5 activation. Mol Cell Endocrinol. 1997, 127:155-169.
68. Grattan D.R., Kokay I.C. Prolactin: a pleiotropic neuroendocrine hormone. J. Neuroendocrinol. 2008, 20:752-763.
69. Grosdemouge I., Bachelot A., Lucas A., Baran N., Kelly P.A., Binart N. Effects of deletion of the prolactin receptor on ovarian gene expression. Reprod. Biol. Endocrinol. 2003, 1:12.
70. Gu Y., Srivastava R.K., Clarke D.L., Linzer D.I., Gibori G. The decidual prolactin receptor and its regulation by decidua-derived factors. Endocrinology 1996, 137:4878-4885.
71. Gubbins E.J., Maurer R.A., Hartley J.L., Donelson J.E. Construction and analysis of recombinant DNAs containing a structural gene for rat prolactin. Nucl. Acid. Res. 1979, 6(3):915-930.
72. Halperin J., Devi S.Y., Elizur S., Stocco C., Shehu A., Rebourcet D., Unterman T.G., Leslie N.D., Le J., Binart N., Gibori G. Prolactin Signaling through the short form of its receptor represses forkhead transcription factor FOXO3 and its target gene galt causing a severe ovarian defect. Mol. Endo 2008, 22(2):513-522.
73. Harigaya T., Nakayama K., Ohkubo H., Nakanishi S., Seo H., Hoshino K. Cloning and sequence analysis of cDNA for mouse prolactin. Biochim. Biophys. Acta 1986, 868(1):30-38.
74. Harvey S., Scanes C.G., Chadwick A., Bolton N.J. Influence of fasting, glucose and insulin on the levels of growth hormone and prolactin in the plasma of the domestic fowl (Gallus domesticus). J. Endocrinol. 1978, 76(3):501-506.
75. Horseman N.D., Yu-Lee L.Y. Transcriptional regulation by the helix bundle peptide hormones: growth hormone, prolactin, and hematopoietic cytokines. Endocr. Rev. 1994, 15:627-649.
76. Horseman N.D., Zhao W., Montecino-Rodriguez E., Tanaka M., Nakashima K., Engle S.J., Smith F., Markoff E., Dorshkind K. Defective mammopoiesis, but normal hematopoiesis, in mice with a targeted disruption of the prolactin gene. EMBO J. 1997, 16:6926-6935.
77. Hosaka T., Biggs W.H., Tieu D., Boye A.D., Varki N.M., Cavenee W.K., Arden K.C. Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc. Natl. Acad. Sci. USA 2004, 101:2975-2980.
78. Hu Z.Z., Meng J., Dufau M.L. Isolation and characterization of two novel forms of the human prolactin receptor generated by alternative splicing of a newly identified exon 11. J. Biol. Chem. 2001, 276(44):41086-41094.
79. Huang K., Ueda E., Chen Y., Walker A.M. Paradigm-shifters: phosphorylated prolactin and short prolactin receptors. J. Mammary Gland Biol. Neoplasia 2008, 13:69-79.
80. Hugo E.R., Brandebourg T.D., Comstock C.E., Gersin K.S., Sussman J.J., Ben-Jonathan N. LS14: a novel human adipocyte cell line that produces prolactin. Endocrinology 2006, 147(1):306-313.
81. Jabbour H.N., Critchley H.O. Potential roles of decidual prolactin in early pregnancy. Reproduction 2001, 121:197-205.
82. Jayatilak P.G., Gibori G. Ontogeny of prolactin receptors in rat decidual tissue: binding by a locally produced prolactin-like hormone. J. Endocrinol. 1986, 110:115-121.
83. Jayatilak P.G., Glaser L.A., Basuray R., Kelly P.A., Gibori G. Identification and partial characterization of a prolactin-like hormone produced by rat decidual tissue. Proc. Natl. Acad. Sci. USA 1985, 82(1):217-221.
84. John G.B., Gallardo T.D., Shirley L.J., Castrillon D.H. Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev. Biol. 2008, 321:197-204.
85. Jurcovicová J., Day R.N., Macleod R.M. Expression of prolactin in rat lymphocytes. Prog. Neuroendocrinimmunol. 1993, 5:256-263.
86. Kaiser U.B. Hyperprolactinemia and infertility: new insights. J. Clin. Invest. 2012, 122(10):3467-3468.
87. Kaufman F.R., Kogut M.D., Donnell G.N., Goebelsmann U., March C., Koch R. Hypergonadotropic hypogonadism in female patients with galactosemia. N. Engl. J. Med. 1981, 304:994-998.
88. Kelly P.A., Boutin J.M., Jolicoeur C., Okamura H., Shirota M., Edery M., Dusanter-Fourt I., Djiane J. Purification, cloning, and expression of the prolactin receptor. Biol. Reprod. 1989, 40(1):27-32.
89. Kelly P.A., Djiane J., Postel-Vinay M.-C., Edery M. The prolactin/growth hormone receptor family. Endocrinol. Rev. 1991, 12:235-251.
90. Kiapekou E., Loutradis D., Patsoula E., Koussidis G.A., Minas V., Bletsa R., Antsaklis A., Michalas S., Makrigiannakis A. Prolactin receptor mRNA expression in oocytes and preimplantation mouse embryos. Reprod. Biomed. Online 2005, 10:339-346.
91. Kiapekou E., Loutradis D., Mastorakos G., Bletsa R., Beretsos P., Zapanti E., Drakakis P., Antsaklis A., Kiessling A.A. Effect of PRL on in vitro follicle growth, in vitro oocyte maturation, fertilization and early embryonic development in mice. Cloning Stem Cells 2009, 11:293-300.
92. Kingston R.L., Gay L.S., Baase W.S., Matthews B.W. Structure of the nucleocapsid-binding domain from the mumps virus polymerase; an example of protein folding induced by crystallization. J. Mol. Biol. 2008, 379:719-731.
93. Kline J.B., Roehrs H., Clevenger C.V. Functional characterization of the intermediate isoform of the human prolactin receptor. J. Biol. Chem. 1999, 274:35461-35468.
94. Kowalewski M.P., Michel E., Gram A., Boos A., Guscetti F., Hoffmann B., Aslan S., Reichler I. Luteal and placental function in the bitch: spatio-temporal changes in prolactin receptor (PRLr) expression at dioestrus, pregnancy and normal and induced parturition. Reprod. Biol. Endocrinol. 2011, 9:109.
95. Kurtz A., Bristol L.A., Tóth B.E., Lazar-Wesley E., Takács L., Kacsóh B. Mammary epithelial cells of lactating rats express prolactin messenger ribonucleic acid. Biol. Reprod. 1993, 48(5):1095-1103.
96. Lai K.W., Cheng L.Y., Cheung A.L.O.W.S. Inhibitor of apoptosis proteins and ovarian dysfunction in galactosemic rats. Cell Tissue Res. 2003, 311(3):417-425.
97. Le J.A., Wilson H.M., Shehu A., Mao J., Devi Y.S., Halperin J., Aguilar T., Seibold A., Maizels E., Gibori G. Generation of mice expressing only the long form of the prolactin receptor reveals that both isoforms of the receptor are required for normal ovarian function. Biol. Reprod. 2012, 86(3):1-13.
98. Le Provost F., Leroux C., Martin P., Gaye P., Djiane J. Prolactin gene expression in ovine and caprine mammary gland. Neuroendocrinology. 1994, 60(3):305-313.
99. Lebrun J.J., Ali S., Ullrich A., Kelly P.A. Proline-rich sequence-mediated Jak2 association to the prolactin receptor is required but not sufficient for signal transduction. J. Biol. Chem. 1995, 270:10664-10670.
100. Lee J., Kosaras B., Aleyasin H., Han J.A., Park D.S., Ratan R.R., Kowall N.W., Ferrante R.J., Lee S.W., Ryu H. Role of cyclooxygenase-2 induction by transcription factor Sp1 and Sp3 in neuronal oxidative and DNA damage response. FASEB J. 2006, 20:2375-2377.
101. Lesueur L., Edery M., Ali S., Paly J., Kelly P.A., Djiane J. Comparison of long and short forms of the prolactin receptor on prolactin-induced milk protein gene transcription. Proc. Natl. Acad. Sci. USA 1991, 88:824-828.
102. Li H., Ahonen T.J., Alanen K., Xie J., LeBaron M.J., Pretlow T.G., Ealley E.L., Zhang Y., Nurmi M., Singh B., Martikainen P.M., Nevalainen M.T. Activation of signal transducer and activator of transcription 5 in human prostate cancer is associated with high histological grade. Cancer Res. 2004, 64:4774-4782.
103. Linkowski P., Spiegel K., Kerkhofs M., et al. Genetic and environmental influences on prolactin secretion during wake and during sleep. Am. J. Physiol. Endocrinol. Metab. 1998, 274:909-919.
104. Liu G., Shi F., Blas-Machado U., Yu R., Davis V.L., Foster W.G., Magoffin D.A., Hughes C.L. Dietary galactose inhibits GDF-9 mediated follicular development in the rat ovary. Reprod. Toxicol. 2006, 21(1):26-33.
105. Liu L., Rajareddy S., Reddy P., Du C., Jagarlamudi K., Shen Y., Gunnarsson D., Selstam G., Boman K., Liu K. Infertility caused by retardation of follicular development in mice with oocyte-specific expression of Foxo3a. Development 2007, 134:199-209.
106. Lockwood C.J., Schatz F. A biological model for the regulation of peri-implantational hemostasis and menstruation. J. Soc. Gynecol. Invest. 1996, 3(4):159-165.
107. Lowman H.B., Cunningham B.C., Wells J.A. Mutational analysis and protein engineering of receptor-binding determinants in human placental lactogen. J. Biol. Chem. 1991, 266:10982-10988.
108. Lynch V.J., Brayer K., Gellersen B., Wagner G.P. HoxA-11 and FOXO1A Cooperate to Regulate Decidual Prolactin Expression: Towards Inferring the Core Transcriptional Regulators of Decidual Genes. PLoS ONE 2009, 4(9):e6845. 10.1371/journal.pone.0006845.
109. Maslar I.A., Riddick D.H. Prolactin production by human during normal menstrual cycle. Am. J. Obstet. Gynecol. 1979, 135:751-754.
110. McLean M.P., Khan I., Puryear T.K., Gibori G. Induction and repression of specific estradiol sensitive proteins in the rat corpus luteum. Chin. J. Physiol. 1990, 33:353-366.
111. Mercier L., Rentier-Delrue F., Swennen D., Lion M., Le Goff P., Prunet P., Martial J.A. Rainbow trout prolactin cDNA cloning in Escherichia coli. DNA 1989, 8(2):119-125.
112. Milenkovic L., Parlow F., McCann S.M. Physiological significance of the negative short-loop feedback of prolactin. Neuroendocrinology 1990, 52:389-392.
113. Miller S.L., Antico G., Raghunath P.N., Tomaszewski J.E., Clevenger C.V. Nek3 kinase regulates prolactin-mediated cytoskeletal reorganization and motility of breast cancer cells. Oncogene 2007, 26:4668-4678.
114. Nakamura E., Otsuka F., Inagaki K., Miyoshi T., Yamanaka R., Tsukamoto N., Suzuki J., Ogura T., Makino H. A novel antagonistic effect of the bone morphogenetic protein system on prolactin actions in regulating steroidogenesis by granulosa cells. Endocrinology 2010, 151:5506-5518.
115. Nevalainen M.T., Valve E.M., Ingleton P.M., Nurmi M., Martikainen P.M., Harkonen P.L. Prolactin and prolactin receptors are expressed and functioning in human prostate. J. Clin. Invest. 1997, 99:618-627.
116. Ormandy C.J., Camus A., Barra J., Damotte D., Lucas B., Buteau H., Edery M., Brousse N., Babinet C., Binart N., Kelly P.A. Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Gen. Dev. 1997, 11:167-178.
117. Owerbach D., Rutter W.J., Cooke N.E., Martial J.A., Shows T.B. The prolactin gene is located on chromosome 6 in humans. Science 1981, 212:815-816.
118. Perrot-Applanat M., Gualillo O., Pezet A., Vincent V., Edery M., Kelly P.A. Dominant negative and cooperative effects of mutant forms of prolactin receptor. Mol. Endocrinol. 1997, 11:1020-1032.
119. Picazo R.A., Garcia Ruiz J.P., Santiago Moreno J., Gonzalez de Bulnes A., Muñoz J., Silvan G., Lorenzo P.L., Illera J.C. Cellular localization and changes in expression of prolactin receptor isoforms in sheep ovary throughout the estrous cycle. Reproduction 2004, 128:545-553.
120. Piekorz R.P., Gingras S., Hoffmeyer A., Ihle J.N., Weinstein Y. Regulation of progesterone levels during pregnancy and parturition by signal transducer and activator of transcription 5 and 20alpha-hydroxysteroid dehydrogenase. Mol. Endocrinol. 2005, 19:431-440.
121. Pohnke Y., Kempf R., Gellersen B. CCAAT/enhancer-binding proteins are mediators in the protein kinase A-dependent activation of the decidual prolactin promoter. J. Biol. Chem. 1999, 274:24808-24818.
122. Prabhakar V.K., Davis J.R. Hyperprolactinaemia. Best Pract. Res. Clin. Obstet. Gynaecol. 2008, 22:341-353.
123. Prigent-Tessier A., Tessier C., Hirosawa-Takamori M., Boyer C., Ferguson-Gottschall S., Gibori G. Rat decidual prolactin. Identification, molecular cloning, and characterization. J. Biol. Chem. 1999, 274:37982-37989.
124. Prunet P., Sandra O., Le Rouzic P., Marchand O., Laudet V. Molecular characterization of the prolactin receptor in two fish species, tilapia Oreochromis niloticus and rainbow trout, Oncorhynchus mykiss: a comparative approach. Can. J. Physiol. Pharmacol. 2000, 78(12):1086-1096.
125. Qazi A.M., Tsai-Morros C.H., Dufau M.L. Ligand-independent homo- and heterodimerization of human prolactin receptor variants: inhibitory actions of the short forms by heterodimerization. Mol. Endocrinol. 2006, 20:1912-1923.
126. Rat Genome Sequencing Project Consortium Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 2004, 428:493-521.
127. Reddy P., Liu L., Adhikari D., Jagarlamudi K., Rajareddy S., Shen Y., Du C., Tang W., Har̈mar̈ lar̈inen T., Peng S.L., Lan Z.J., Cooney A.J., Huhtaniemi I., Liu K. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 2008, 319:611-613.
128. Reese J., Binart N., Brown N., Ma W.G., Paria B.C., Das S.K., Kelly P.A., Dey S.K. Implantation and decidualization defects in prolactin receptor (PRLR)-deficient mice are mediated by ovarian but not uterine PRLR. Endocrinology 2000, 141:1872-1881.
129. Ricken A.M., Traenkner A., Merkwitz C., Hummitzsch K., Grosche J., Spanel-Borowski K. The short prolactin receptor predominates in endothelial cells of micro- and macrovascular origin. J. Vasc. Res. 2007, 44:19-30.
130. Risk M., Gibori G. Mechanisms of luteal cell regulation by prolactin. Prolactin 2001, 265-295. Kluwer, Boston. N.D. Horseman (Ed.).
131. Risk M., Shehu A., Mao J., Stocco C.O., Goldsmith L.T., Bowen-Shauver J.M., Gibori G. Cloning and characterization of a 5' regulatory region of the prolactin receptor-associated protein/17{beta} hydroxysteroid dehydrogenase 7 gene. Endocrinology 2005, 146(6):2807-2816.
132. Rui H., Lebrun J.-J., Kirken R.A., Kelly P.A., Farrar W.L. JAK2 activation and cell proliferation induced by antibody-mediated prolactin receptor dimerization. Endocrinology 1994, 135:1299-1306.
133. Russell D.L., Richards J.S. Differentiation-dependent prolactin responsiveness and STAT (signal transducers and activators of transcription) signaling in rat ovarian cells. Mol. Endocrinol. 1999, 13:2049-2064.
134. Ryu H., Lee J., Zaman K., Kubilis J., Ferrante R.J., Ross B.D., Neve R., Ratan R.R. Sp1 and Sp3 are oxidative stress-inducible, antideath transcription factors in cortical neurons. J. Neurosci. 2003, 23:3597-3606.
135. Sakamoto K., Creamer B.A., Triplett A.A., Wagner K.U. The Janus kinase 2 is required for expression and nuclear accumulation of cyclin D1 in proliferating mammary epithelial cells. Mol. Endocrinol. 2007, 21:1877-1892.
136. Scott P., Kessler M.A., Schuler L.A. Molecular cloning of the bovine prolactin receptor and distribution of prolactin and growth hormone receptor transcripts in fetal and utero-placental tissues. Mol. Cell Endocrinol. 1992, 89(1-2):47-58.
137. Shao R., Nutu M., Weijdegard B., Egecioglu E., Fernandez-Rodriguez J., Tallet E., Goffin V., Ling C., Billig H. Differences in prolactin receptor (PRLR) in mouse and human fallopian tubes: evidence for multiple regulatory mechanisms controlling PRLR isoform expression in mice. Biol. Reprod. 2008, 79:748-757.
138. Shome B., Parlow A.F. Human pituitary prolactin (hPRL): the entire linear amino acid sequence. J. Clin. Endocrinol. Metab. 1977, 45(5):1112-1115.
139. Sivaprasad U., Canfield J.M., Brooks C.L. Mechanism for ordered receptor binding by human prolactin. Biochemistry 2004, 43:13755-13765.
140. Soares M.J. The prolactin and growth hormone families: pregnancy-specific hormones/cytokines at the maternal-fetal interface. Reprod. Biol. Endocrinol. 2004, 2:51.
141. Sonigo C., Bouilly J., Carré N., Tolle V., Caraty A., Tello J., Simony-Conesa F.J., Millar R., Young J., Binart N. Hyperprolactinemia-induced ovarian acyclicity is reversed by kisspeptin administration. J. Clin. Invest. 2012, 122(10):3791-3795.
142. Steinmetz R.W., Grant A.L., Malven P.V. Transcription of prolactin gene in milk secretory cells of the rat mammary gland. J. Endocrinol. 1993, 136:271-276.
143. Stocco C.O., Zhong L., Sugimoto Y., Ichikawa A., Lau L.F., Gibori G. Prostaglandin F2α-induced expression of 20α-hydroxysteroid dehydrogenase involves the transcription factor NUR77. J. Biol. Chem. 2000, 275:37202-37211.
144. Stocco C., Djiane J., Gibori G. Prostaglandin F(2alpha) (PGF(2alpha)) and prolactin signaling: PGF(2alpha)-mediated inhibition of prolactin receptor expression in the corpus luteum. Endocrinology 2003, 144:3301-3305.
145. Stocco C., Telleria C., Gibori G. The molecular control of corpus luteum formation, function, and regression. Endocrinol. Rev. 2007, 28:117-149.
146. Stricker P., Grueter F. Action du lobe anterieur de l'hypophyse sur la montee laiteuse. CR Soc. Biol. 1928, 99:1978-1980.
147. Tamura H., Greenwald G.S. Angiogenesis and its hormonal control in the corpus luteum of the pregnant rat. Biol. Reprod. 1987, 36:1149-1154.
148. Tan D., Walker A.M. Short form 1b prolactin receptor down-regulates expression of the long form. J. Mol. Endocrinol. 2010, 44(3):187-194.
149. Tan D., Johnson D.A., Wu W., Zeng L., Chen Y.H., Chen W.Y., Vonderharr B.K., Walker A.M. Unmodified prolactin (PRL), and S179D PRL-initiated bioluminescence resonance energy transfer between homo- and hetero-pairs of long and short PRL receptors in living human cells. Mol. Endo 2005, 19:1291-1303.
150. Teglund S., McKay C., Schuetz E., van Deursen J.M., Stravopodis D., Wang D., Brown M., Bodner S., Grosveld G., Ihle J.N. Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell 1998, 93:841-850.
151. Telleria C.M., Parmer T.G., Zhong L., Clarke D.L., Albarracin C.T., Duan W.R., Linzer D.I.H., Gibori G. The different forms of the prolactin receptor in the rat corpus luteum: developmental expression and hormonal regulation in pregnancy. Endocrinology 1997, 138:4812-4820.
152. Tessier C., Prigent-Tessier A., Ferguson-Gottschall S., Gu Y., Gibori G. PRL antiapoptotic effect in the rat decidua involves the PI3K/protein kinase B-mediated inhibition of caspase-3 activity. Endocrinology 2001, 142:4086-4094.
153. Tessier C., Prigent-Tessier A., Bao L., Telleria C.M., Ferguson-Gottschall S., Gibori G.B., Gu Y., Bowen-Shauver J.M., Horseman N.D., Gibori G. Decidual activin: its role in the apoptotic process and its regulation by prolactin. Biol Reprod. 2003, 68:1687-1694.
154. Thompson I.M., Ozawa M., Bubolz J.W., Yang Q., Dahl G.E. Bovine luteal prolactin receptor expression: potential involvement in regulation of progesterone during the estrous cycle and pregnancy. J. Anim. Sci. 2011, 89:1338-1346.
155. Truong A.T., Duez C., Belayew A., Renard A., Pictet R., Bell G.I., Martial J.A. Isolation and characterization of the human prolactin gene. EMBO J. 1984, 3:429-437.
156. Udy G.B., Towers R.P., Snell R.G., Wilkins R.J., Park S.H., Ram P.A., Waxman D.J., Davey H.W. Requirement of STAT5b for sexual dimorphism of body growth rates and liver gene expression. Proc. Natl. Acad Sci. USA 1997, 94:7239-7244.
157. van Agthoven J., Zhang C., Tallet E., Raynal B., Hoos S., Baron B., England P., Goffin V., Broutin I. Structural characterization of the stem-stem dimerization interface between prolactin receptor chains complexed with the natural hormone. J. Mol. Biol. 2010, 404:112-126.
158. Voorhees J.L., Brooks C.L. Obligate ordered binding of human lactogenic cytokines. JBC 2010, 285(26):20022-20030.
159. Walker A.M. Prolactin receptor antagonists. Curr. Opin. Invest. Drugs 2005, 6(4):378-385.
160. Wang B., Mu Y., Ni F., Zhou S., Wang J., Cao Y., Ma X. Analysis of FOXO3 mutation in 114 Chinese women with premature ovarian failure. Reprod. Biomed. Online 2010, 20:499-503.
161. Wierstra I. Sp1: emerging roles beyond constitutive activation of TATA-less housekeeping genes. Biochem. Biophys. Res. Commun. 2008, 372:1-13.
162. Yamamoto T., Nakayama Y., Tajima T., Abe S., Kawahara A. Cloning of a cDNA for Xenopus prolactin receptor and its metamorphic expression profile. Dev. Growth Differ 2000, 42(2):167-174.
163. Yohkaichiya T., Fukaya T., Hoshiai H., Yajima A. Improvement of mouse embryo development in vitro by prolactin. Tohoku J. Exp. Med. 1988, 155(3):241-246.
164. Zhou J.F., Zadworny D., Guémené D., Kuhnlein U. Molecular cloning, tissue distribution, and expression of the prolactin receptor during various reproductive states in Meleagris gallopavo. Biol. Reprod. 1996, 55(5):1081-1090.