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

Reproductive Biology and Endocrinology

Volumn 7, Issue , 2009, Pages 87-

  Devi, Y Sangeeta ^a   Shehu, Aurora ^a   Halperin, Julia ^a,b   Stocco, Carlos ^a   Le, Jamie ^a   Seibold, Anita M ^a   Gibori, Geula ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b DEPARTAMENTO DE CIENCIAS NATURALES Y ANTROPOLOGÍA   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

JANUS KINASE; PROLACTIN; PROLACTIN RECEPTOR; STAT PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DECIDUA; DNA BINDING; DNA MICROARRAY; ENZYME ACTIVATION; FEMALE; GENE ACTIVATION; GENE CONTROL; GENE REPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; HORMONE ACTION; MALE; MOUSE; NONHUMAN; OVARY; OVARY FOLLICLE DEVELOPMENT; PROTEIN MICROARRAY; REPRODUCTION; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY;

ANIMALS; B-CELL-SPECIFIC ACTIVATOR PROTEIN; CORE BINDING FACTOR ALPHA 2 SUBUNIT; DECIDUA; DNA; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EYE PROTEINS; FEMALE; GENE EXPRESSION; HOMEODOMAIN PROTEINS; MALE; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MICE, TRANSGENIC; OVARY; PAIRED BOX TRANSCRIPTION FACTORS; PREGNANCY; PROLACTIN; PROTEIN BINDING; PROTEIN ISOFORMS; RECEPTORS, PROLACTIN; REPRESSOR PROTEINS; TIME FACTORS; TRANSCRIPTION FACTORS;

MUS;

EID: 71049191806     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/1477-7827-7-87     Document Type: Article

References (72)

1. Bole-Feysot C, Goffin V, Edery M, Binart N, Kelly PA. Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr Rev 1998, 19(3):225-268. 10.1210/er.19.3.225, 9626554.
2. Kelly PA, Djiane J, Postel-Vinay MC, Edery M. The prolactin/growth hormone receptor family. Endocr Rev 1991, 12(3):235-251. 10.1210/edrv-12-3-235, 1935820.
3. Gu Y, Srivastava RK, Clarke DL, Linzer DI, Gibori G. The decidual prolactin receptor and its regulation by decidua-derived factors. Endocrinology 1996, 137(11):4878-4885. 10.1210/en.137.11.4878, 8895360.
4. Davis JA, Linzer DI. Expression of multiple forms of the prolactin receptor in mouse liver. Mol Endocrinol 1989, 3(4):674-680. 10.1210/mend-3-4-674, 2725531.
5. Telleria CM, Parmer TG, Zhong L, Clarke DL, Albarracin CT, Duan WR, Linzer DI, Gibori G. The different forms of the prolactin receptor in the rat corpus luteum: developmental expression and hormonal regulation in pregnancy. Endocrinology 1997, 138(11):4812-4820. 10.1210/en.138.11.4812, 9348210.
6. Clevenger CV, Furth PA, Hankinson SE, Schuler LA. The role of prolactin in mammary carcinoma. Endocr Rev 2003, 24(1):1-27. 10.1210/er.2001-0036, 1698952, 12588805.
7. Frasor J, Gibori G. Prolactin regulation of estrogen receptor expression. Trends Endocrinol Metab 2003, 14(3):118-123. 10.1016/S1043-2760(03)00030-4, 12670737.
8. Lebrun JJ, Ali S, Ullrich A, Kelly PA. Proline-rich sequence-mediated Jak2 association to the prolactin receptor is required but not sufficient for signal transduction. J Biol Chem 1995, 270(18):10664-10670. 10.1074/jbc.270.18.10664, 7537736.
9. Lebrun JJ, Ali S, Goffin V, Ullrich A, Kelly PA. A single phosphotyrosine residue of the prolactin receptor is responsible for activation of gene transcription. Proc Natl Acad Sci USA 1995, 92(9):4031-4035. 10.1073/pnas.92.9.4031, 42096, 7537382.
10. Berlanga JJ, Garcia-Ruiz JP, Perrot-Applanat M, Kelly PA, Edery M. The short form of the prolactin (PRL) receptor silences PRL induction of the beta-casein gene promoter. Mol Endocrinol 1997, 11(10):1449-1457. 10.1210/me.11.10.1449, 9280060.
11. Perrot-Applanat M, Gualillo O, Pezet A, Vincent V, Edery M, Kelly PA. Dominant negative and cooperative effects of mutant forms of prolactin receptor. Mol Endocrinol 1997, 11(8):1020-1032. 10.1210/me.11.8.1020, 9212050.
12. Devi YS, Shehu A, Stocco C, Halperin J, Le J, Seibold AM, 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):3327-35. 10.1210/en.2008-1719, 19342455.
13. Halperin J, Devi SY, Elizur S, Stocco C, Shehu A, Rebourcet D, Unterman TG, Leslie ND, 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 Endocrinol 2008, 22(2):513-522. 10.1210/me.2007-0399, 2234584, 17975019.
14. Binart N, Imbert-Bollore P, Baran N, Viglietta C, Kelly PA. A short form of the prolactin (PRL) receptor is able to rescue mammopoiesis in heterozygous PRL receptor mice. Mol Endocrinol 2003, 17(6):1066-1074. 10.1210/me.2002-0181, 12624115.
15. Huang K, Ueda E, Chen Y, Walker AM. Paradigm-shifters: phosphorylated prolactin and short prolactin receptors. J Mammary Gland Biol Neoplasia 2008, 13(1):69-79. 10.1007/s10911-008-9072-x, 18219563.
16. Risk M, Shehu A, Mao J, Stocco CO, Goldsmith LT, Bowen-Shauver JM, 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. 10.1210/en.2004-1673, 15731358.
17. Srivastava S, Matsuda M, Hou Z, Bailey JP, Kitazawa R, Herbst MP, Horseman ND. Receptor activator of NF-kappaB ligand induction via Jak2 and Stat5a in mammary epithelial cells. J Biol Chem 2003, 278(46):46171-46178. 10.1074/jbc.M308545200, 12952963.
18. Telleria CM, Goyeneche AA, Stocco CO, Gibori G. Involvement of nuclear factor kappa B in the regulation of rat luteal function: potential roles as survival factor and inhibitor of 20alpha-hydroxysteroid dehydrogenase. J Mol Endocrinol 2004, 32(2):365-383. 10.1677/jme.0.0320365, 15072545.
19. Cai Z, Kwintkiewicz J, Young ME, Stocco C. Prostaglandin E2 increases cyp19 expression in rat granulosa cells: implication of GATA-4. Mol Cell Endocrinol 2007, 263(1-2):181-189. 10.1016/j.mce.2006.09.012, 1779458, 17097802.
20. Komiyama J, Nishimura R, Lee HY, Sakumoto R, Tetsuka M, Acosta TJ, Skarzynski DJ, Okuda K. Cortisol is a suppressor of apoptosis in bovine corpus luteum. Biol Reprod 2008, 78(5):888-895. 10.1095/biolreprod.107.065656, 18218610.
21. Alam H, Weck J, Maizels E, Park Y, Lee EJ, 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(2):915-928. 10.1210/en.2008-0850, 18845636.
22. Chen JH, Huang CH, Lin LY. Rottlerin stimulates metallothionein gene expression but inhibits metal transport in Chinese hamster ovary cells. Toxicol Appl Pharmacol 2001, 177(3):256-263. 10.1006/taap.2001.9299, 11749125.
23. Sriraman V, Eichenlaub-Ritter U, Bartsch JW, Rittger A, Mulders SM, Richards JS. Regulated expression of ADAM8 (a disintegrin and metalloprotease domain 8) in the mouse ovary: evidence for a regulatory role of luteinizing hormone, progesterone receptor, and epidermal growth factor-like growth factors. Biol Reprod 2008, 78(6):1038-1048. 10.1095/biolreprod.107.066340, 18287572.
24. Liu J, Park ES, Jo M. RUNX1 Transcription Factor Regulates LH-induced Prostaglandin-Endoperoxide Synthase 2 (Ptgs2) Expression in Rat Periovulatory Granulosa Cells. Endocrinology 2009, 150(7):3291-300. 10.1210/en.2008-1527, 19342459.
25. Rae MT, Gubbay O, Kostogiannou A, Price D, Critchley HO, Hillier SG. Thyroid hormone signaling in human ovarian surface epithelial cells. J Clin Endocrinol Metab 2007, 92(1):322-327. 10.1210/jc.2006-1522, 17032711.
26. Kaivo-oja N, Jeffery LA, Ritvos O, Mottershead DG. Smad signalling in the ovary. Reprod Biol Endocrinol 2006, 4:21. 10.1186/1477-7827-4-21, 1459162, 16611366.
27. Takamoto N, Kurihara I, Lee K, Demayo FJ, Tsai MJ, Tsai SY. Haploinsufficiency of chicken ovalbumin upstream promoter transcription factor II in female reproduction. Mol Endocrinol 2005, 19(9):2299-2308. 10.1210/me.2005-0019, 1198323, 15890675.
28. Sato Y, Suzuki T, Hidaka K, Sato H, Ito K, Ito S, Sasano H. Immunolocalization of nuclear transcription factors, DAX-1 and COUP-TF II, in the normal human ovary: correlation with adrenal 4 binding protein/steroidogenic factor-1 immunolocalization during the menstrual cycle. J Clin Endocrinol Metab 2003, 88(7):3415-3420. 10.1210/jc.2002-021723, 12843196.
29. Roy SK, Wang J, Yang P. Dexamethasone inhibits transforming growth factor-beta receptor (Tbeta R) messenger RNA expression in hamster preantral follicles: possible association with NF-YA. Biol Reprod 2003, 68(6):2180-2188. 10.1095/biolreprod.102.013011, 12606399.
30. Xiao X, Liu A, Wen H, Tian Y, Ni J, Liu G. Expression and localization of transcription factor Ets-1 in the rat ovary during the estrous cycle and pregnancy. Fertil Steril 2009, 91(5 Suppl):1998-2005. 10.1016/j.fertnstert.2008.02.166, 18439600.
31. Takai N, Miyazaki T, Nishida M, Nasu K, Miyakawa I. c-Ets1 is a promising marker in epithelial ovarian cancer. Int J Mol Med 2002, 9(3):287-292.
32. Tang M, Mazella J, Gao J, Tseng L. Progesterone receptor activates its promoter activity in human endometrial stromal cells. Mol Cell Endocrinol 2002, 192(1-2):45-53. 10.1016/S0303-7207(02)00111-9, 12088866.
33. Song G, Kim J, Bazer FW, Spencer TE. Progesterone and interferon tau regulate hypoxia-inducible factors in the endometrium of the ovine uterus. Endocrinology 2008, 149(4):1926-1934. 10.1210/en.2007-1530, 2276712, 18174278.
34. Gao J, Mazella J, Tseng L. Partial characterization of the CCAAT box in the promoter of the hLGFBP-1 gene: interaction with negatively acting transcription factors in decidualized human endometrial stromal cells. Mol Cell Endocrinol 2000, 159(1-2):171-177. 10.1016/S0303-7207(99)00192-6, 10687862.
35. Gu Y, Jow GM, Moulton BC, Lee C, Sensibar JA, Park-Sarge OK, Chen TJ, Gibori G. Apoptosis in decidual tissue regression and reorganization. Endocrinology 1994, 135(3):1272-1279. 10.1210/en.135.3.1272, 8070373.
36. Goldhar AS, Vonderhaar BK, Trott JF, Hovey RC. Prolactin-induced expression of vascular endothelial growth factor via Egr-1. Mol Cell Endocrinol 2005, 232(1-2):9-19. 10.1016/j.mce.2005.01.005, 15737464.
37. Yang M, Nomura H, Hu Y, Kaneko S, Kaneko H, Tanaka M, Nakashima K. Prolactin-induced expression of TATA-less cyclin D3 gene is mediated by Sp1 and AP2. Biochem Mol Biol Int 1998, 44(1):51-58.
38. Ichiyama K, Yoshida H, Wakabayashi Y, Chinen T, Saeki K, Nakaya M, Takaesu G, Hori S, Yoshimura A, Kobayashi T. Foxp3 inhibits RORgammat-mediated IL-17A mRNA transcription through direct interaction with RORgammat. J Biol Chem 2008, 283(25):17003-17008. 10.1074/jbc.M801286200, 18434325.
39. McHale K, Tomaszewski JE, Puthiyaveettil R, Livolsi VA, Clevenger CV. Altered expression of prolactin receptor-associated signaling proteins in human breast carcinoma. Mod Pathol 2008, 21(5):565-571. 10.1038/modpathol.2008.7, 18246042.
40. Olazabal IM, Munoz JA, Rodriguez-Navas C, Alvarez L, Delgado-Baeza E, Garcia-Ruiz JP. Prolactin's role in the early stages of liver regeneration in rats. J Cell Physiol 2009, 219(3):626-33. 10.1002/jcp.21707, 19170064.
41. Akbas GE, Taylor HS. HOXC and HOXD gene expression in human endometrium: lack of redundancy with HOXA paralogs. Biol Reprod 2004, 70(1):39-45. 10.1095/biolreprod.102.014969, 12954737.
42. Yu-Lee LY. Molecular actions of prolactin in the immune system. Proc Soc Exp Biol Med 1997, 215(1):35-52.
43. LaVoie HA. The role of GATA in mammalian reproduction. Exp Biol Med (Maywood) 2003, 228(11):1282-1290.
44. Shibata H, Kurihara I, Kobayashi S, Yokota K, Suda N, Saito I, Saruta T. Regulation of differential COUP-TF-coregulator interactions in adrenal cortical steroidogenesis. J Steroid Biochem Mol Biol 2003, 85(2-5):449-456. 10.1016/S0960-0760(03)00217-6, 12943735.
45. Shaw AS, Filbert EL. Scaffold proteins and immune-cell signalling. Nat Rev Immunol 2009, 9(1):47-56. 10.1038/nri2473, 19104498.
46. Johnson LM, Too CK. Prolactin, interleukin-2 and FGF-2 stimulate expression, nuclear distribution and DNA-binding of rat homolog of pombe Cdc5 in Nb2 T lymphoma cells. Molecular and cellular endocrinology 2001, 184(1-2):151-161. 10.1016/S0303-7207(01)00585-8, 11694351.
47. Liu G, Hale GE, Hughes CL. Galactose metabolism and ovarian toxicity. Reprod Toxicol 2000, 14(5):377-384. 10.1016/S0890-6238(00)00096-4, 11020650.
48. Forges T, Monnier-Barbarino P, Leheup B, Jouvet P. Pathophysiology of impaired ovarian function in galactosaemia. Hum Reprod Update 2006, 12(5):573-584. 10.1093/humupd/dml031, 16835432.
49. Kaufman F, Kogut MD, Donnell GN, Koch H, Goebelsmann U. Ovarian failure in galactosaemia. Lancet 1979, 2(8145):737-738. 10.1016/S0140-6736(79)90658-5, 90818.
50. Krasnow JS, Hickey GJ, Richards JS. Regulation of aromatase mRNA and estradiol biosynthesis in rat ovarian granulosa and luteal cells by prolactin. Molecular endocrinology (Baltimore, Md) 1990, 4(1):13-12. 10.1210/mend-4-1-13, 1970119.
51. Zeitoun K, Takayama K, Michael MD, Bulun SE. Stimulation of aromatase P450 promoter (II) activity in endometriosis and its inhibition in endometrium are regulated by competitive binding of steroidogenic factor-1 and chicken ovalbumin upstream promoter transcription factor to the same cis-acting element. Molecular endocrinology (Baltimore, Md) 1999, 13(2):239-253. 10.1210/me.13.2.239, 9973254.
52. Lutwyche JK, Keough RA, Hunter J, Coles LS, Gonda TJ. DNA binding-independent transcriptional activation of the vascular endothelial growth factor gene (VEGF) by the Myb oncoprotein. Biochem Biophys Res Commun 2006, 344(4):1300-1307. 10.1016/j.bbrc.2006.04.045, 16650815.
53. Ricken AM, 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(1):19-30. 10.1159/000097892, 17164560.
54. Fazleabas AT, Kim JJ, Strakova Z. Implantation: embryonic signals and the modulation of the uterine environment - a review. Placenta 2004, 25(Suppl A):S26-31. 10.1016/j.placenta.2004.01.014, 15033303.
55. Bulmer JN, Longfellow M, Ritson A. Leukocytes and resident blood cells in endometrium. Annals of the New York Academy of Sciences 1991, 622:57-68. 10.1111/j.1749-6632.1991.tb37850.x, 2064208.
56. Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D. Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Human reproduction (Oxford, England) 1991, 6(6):791-798.
57. Ben-Jonathan N, LaPensee CR, LaPensee EW. What can we learn from rodents about prolactin in humans?. Endocrine reviews 2008, 29(1):1-41. 10.1210/er.2007-0017, 2244934, 18057139.
58. Chavez-Rueda K, Legorreta-Haquet VM, Cervera-Castillo H, Sanchez L, Jara LJ, Zenteno E, Chavez-Sanchez L, Blanco-Favela F. Effect of prolactin on lymphocyte activation from systemic lupus erythematosus patients. Annals of the New York Academy of Sciences 2007, 1108:157-165. 10.1196/annals.1422.018, 17893982.
59. Janne J, Poso H, Raina A. Polyamines in rapid growth and cancer. Biochim Biophys Acta 1978, 473(3-4):241-293.
60. Dwivedi A, Gupta G, Keshri G, Dhar JD. Changes in uterine ornithine decarboxylase activity and steroid receptor levels during decidualization in the rat induced by CDRI-85/287. Eur J Endocrinol 1999, 141(4):426-430. 10.1530/eje.0.1410426, 10526259.
61. Brar AK, Kessler CA, Meyer AJ, Cedars MI, Jikihara H. Retinoic acid suppresses in-vitro decidualization of human endometrial stromal cells. Mol Hum Reprod 1996, 2(3):185-193. 10.1093/molehr/2.3.185, 9238678.
62. Fromental-Ramain C, Warot X, Lakkaraju S, Favier B, Haack H, Birling C, Dierich A, Doll e P, Chambon P. Specific and redundant functions of the paralogous Hoxa-9 and Hoxd-9 genes in forelimb and axial skeleton patterning. Development (Cambridge, England) 1996, 122(2):461-472.
63. Wu H, Chen Y, Liang J, Shi B, Wu G, Zhang Y, Wang D, Li R, Yi X, Zhang H, Sun L, Shang Y. Hypomethylation-linked activation of PAX2 mediates tamoxifen-stimulated endometrial carcinogenesis. Nature 2005, 438(7070):981-987. 10.1038/nature04225, 16355216.
64. Ballestar E, Paz MF, Valle L, Wei S, Fraga MF, Espada J, Cigudosa JC, Huang TH, Esteller M. Methyl-CpG binding proteins identify novel sites of epigenetic inactivation in human cancer. Embo J 2003, 22(23):6335-6345. 10.1093/emboj/cdg604, 291845, 14633992.
65. Palmisano WA, Crume KP, Grimes MJ, Winters SA, Toyota M, Esteller M, Joste N, Baylin SB, Belinsky SA. Aberrant promoter methylation of the transcription factor genes PAX5 alpha and beta in human cancers. Cancer Res 2003, 63(15):4620-4625.
66. Reddy PM, Reddy PR. Effect of prolactin on DNA methylation in the liver and kidney of rat. Mol Cell Biochem 1990, 95(1):43-47. 10.1007/BF00219528, 2366751.
67. Speck NA, Gilliland DG. Core-binding factors in haematopoiesis and leukaemia. Nat Rev Cancer 2002, 2(7):502-513. 10.1038/nrc840, 12094236.
68. Hess J, Porte D, Munz C, Angel P. AP-1 and Cbfa/runt physically interact and regulate parathyroid hormone-dependent MMP13 expression in osteoblasts through a new osteoblast-specific element 2/AP-1 composite element. J Biol Chem 2001, 276(23):20029-20038. 10.1074/jbc.M010601200, 11274169.
69. Bertrand-Philippe M, Ruddell RG, Arthur MJ, Thomas J, Mungalsingh N, Mann DA. Regulation of tissue inhibitor of metalloproteinase 1 gene transcription by RUNX1 and RUNX2. J Biol Chem 2004, 279(23):24530-24539. 10.1074/jbc.M311804200, 15051730.
70. Stocco C, Telleria C, Gibori G. The molecular control of corpus luteum formation, function, and regression. Endocr Rev 2007, 28(1):117-149. 10.1210/er.2006-0022, 17077191.
71. Jo M, Curry TE. Luteinizing hormone-induced RUNX1 regulates the expression of genes in granulosa cells of rat periovulatory follicles. Mol Endocrinol 2006, 20(9):2156-2172. 10.1210/me.2005-0512, 1783681, 16675540.
72. Park ES, Choi S, Muse KN, Curry TE, Jo M. Response gene to complement 32 expression is induced by the luteinizing hormone (LH) surge and regulated by LH-induced mediators in the rodent ovary. Endocrinology 2008, 149(6):3025-3036. 10.1210/en.2007-1129, 2408821, 18308847.