Impact of prolactin receptor isoforms on reproduction

Trends in Endocrinology and Metabolism

Volumn 21, Issue 6, 2010, Pages 362-368

  Binart, Nadine ^a,b   Bachelot, Anne ^a,c,d   Bouilly, Justine ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^d SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTROLYTE; ISOPROTEIN; PROLACTIN RECEPTOR; WATER;

ADENOHYPOPHYSIS; BEHAVIOR; BRAIN; CELL PROLIFERATION; DEVELOPMENT; FEMALE; FLUID BALANCE; GROWTH; HUMAN; IMMUNOREGULATION; MAMMARY GLAND; METABOLISM; MOUSE; MUTAGENESIS; NONHUMAN; OVARY; OVARY FOLLICLE; PHENOTYPE; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; REPRODUCTION; REVIEW; RODENT; SIGNAL TRANSDUCTION;

ANIMALS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; LACTATION; MICE; PROLACTIN; PROTEIN CONFORMATION; PROTEIN ISOFORMS; RATS; RECEPTORS, PROLACTIN; REPRODUCTION; SECOND MESSENGER SYSTEMS; SIGNAL TRANSDUCTION;

EID: 77953476421     PISSN: 10432760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tem.2010.01.008     Document Type: Review

References (79)

1. Bole-Feysot C., et al. Prolactin and its receptor: actions, signal transduction pathways and phenotypes observed in prolactin receptor knockout mice. Endocr. Rev. 1998, 19:225-268.
2. Clevenger C.V., et al. The role of prolactin in mammary carcinoma. Endocr. Rev. 2003, 24:1-27.
3. Clevenger C.V., et al. New mechanisms for PRLr action in breast cancer. Trends Endocrinol. Metab. 2009, 20:223-229.
4. Grattan D.R., et al. Prolactin: a pleiotropic neuroendocrine hormone. J. Neuroendocrinol. 2008, 20:752-763.
5. Lucas B.K., et al. Null mutation of prolactin receptor gene produces a defect in maternal behavior. Endocrinology 1998, 139:4102-4107.
6. Shingo T., et al. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 2003, 299:117-120.
7. Ben-Jonathan N., et al. Extrapituitary prolactin: distribution, regulation, functions, and clinical aspects. Endocr. Rev. 1996, 17:639-669.
8. Prigent-Tessier A., et al. Rat decidual prolactin. Identification, molecular cloning, and characterization. J. Biol. Chem. 1999, 274:37982-37989.
9. Hugo E.R., et al. LS14: a novel human adipocyte cell line that produces prolactin. Endocrinology 2006, 147:306-313.
10. Freeman M.E., et al. Prolactin: structure, function, and regulation of secretion. Physiol. Rev. 2000, 80:1523-1631.
11. Demaria J.E., et al. Prolactin activates all three populations of hypothalamic neuroendocrine dopaminergic neurons in ovariectomized rats. Brain Res. 1999, 837:236-241.
12. Palm I.F., et al. Control of the estradiol-induced prolactin surge by the suprachiasmatic nucleus. Endocrinology 2001, 142:2296-2302.
13. Kossiakoff A.A. The structural basis for biological signaling, regulation, and specificity in the growth hormone-prolactin system of hormones and receptors. Adv. Protein Chem. 2004, 68:147-169.
14. Davis J.A., et al. Expression of multiple forms of the prolactin receptor. Mol. Endocrinol. 1989, 3:674-680.
15. Kline J.B., et al. Functional characterization of the intermediate isoform of the human prolactin receptor. J. Biol. Chem. 1999, 274:35461-35468.
16. Hu Z.Z., et al. 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, 276:41086-41094.
17. Trott J.F., et al. Multiple new isoforms of the human prolactin receptor gene. Adv. Exp. Med. Biol. 2004, 554:495-499.
18. Brown R.J., et al. Model for growth hormone receptor activation based on subunit rotation within a receptor dimer. Nat. Struct. Mol. Biol. 2005, 12:814-821.
19. Gertler A., et al. 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, 271:24482-24491.
20. Biener E., et al. Ovine placental lactogen-induced heterodimerization of ovine growth hormone and prolactin receptors in living cells is demonstrated by fluorescence resonance energy transfer microscopy and leads to prolonged phosphorylation of signal transducer and activator of transcription (STAT)1 and STAT3. Endocrinology 2003, 144:3532-3540.
21. Tan D., et al. Unmodified prolactin (PRL) and S179D PRL-initiated bioluminescence resonance energy transfer between homo- and hetero-pairs of long and short human PRL receptors in living human cells. Mol. Endocrinol. 2005, 19:1291-1303.
22. Qazi A.M., et al. Ligand-independent homo- and hetero-dimerization of human prolactin receptor variants: inhibitory action of the short forms by heterodimerization. Mol. Endocrinol. 2006, 8:1912-1923.
23. Gadd S.L., et al. Ligand-Independent dimerization of the human prolactin receptor isoforms: functional implications. Mol. Endocrinol. 2006, 11:2734-2746.
24. Goffin V., et al. Prolactin: the new biology of an old hormone. Annu. Rev. Physiol. 2002, 64:47-67.
25. Swaminathan G., et al. Regulation of prolactin receptor levels and activity in breast cancer. J. Mammary. Gland Biol. Neoplasia. 2008, 13:81-91.
26. Berlanga J.J., et al. Prolactin activates tyrosyl phosphorylation of insulin receptor substrate-1 and phosphatidylinositol-3-OH kinase. J. Biol. Chem. 1997, 272:2050-2052.
27. Clevenger C.V. Roles and regulation of stat family transcription factors in human breast cancer. Am. J. Pathol. 2004, 165:1449-1460.
28. Brockman J.L., et al. PRL activates the cyclin D1 promoter via the Jak2/Stat pathway. Mol. Endocrinol. 2002, 16:774-784.
29. Ali S., et al. PTP1D is a positive regulator of the prolactin signal leading to b-casein promoter activation. EMBO J. 1996, 15:135-142.
30. Pezet A., et al. Tyrosine docking sites of the rat prolactin receptor required for association and activation of Stat5. J. Biol. Chem. 1997, 272:25043-25050.
31. Lesueur L., et al. Comparison of long and short forms of the prolactin receptor on prolactin induced milk protein gene transcription. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:824-828.
32. Berlanga J.J., et al. The short form of the prolactin receptor silences prolactin induction of the b-casein gene promoter. Mol. Endocrinol. 1997, 11:1449-1457.
33. Perrot-Applanat M., et al. Dominant negative and cooperative effects of mutant forms of prolactin receptor. Mol. Endocrinol. 1997, 11:1020-1032.
34. Saunier E., et al. Targeted expression of the dominant-negative prolactin receptor in the mammary gland of transgenic mice results in impaired lactation. Endocrinology 2003, 144:2669-2675.
35. Binart N., et al. A short form of the prolactin receptor is able to rescue mammopoiesis in heterozygous prolactin receptor mice. Mol. Endocrinol. 2003, 17:1066-1074.
36. Kline J.B., et al. Identification and characterization of the prolactin-binding protein in human serum and milk. J. Biol. Chem. 2001, 276:24760-24766.
37. Nagano M., et al. Tissue distribution and regulation of rat prolactin receptor gene expression: quantitative analysis by polymerase chain reaction. J. Biol. Chem. 1994, 269:13337-13345.
38. Russell D.L., et al. Differentiation-dependent prolactin responsiveness and stat (signal transducers and activators of transcription) signaling in rat ovarian cells. Mol. Endocrinol. 1999, 13:2049-2064.
39. Devi Y.S., et al. Regulation of transcription factors and repression of Sp1 by prolactin signaling through the short isoform of its cognate receptor. Endocrinology 2009, 150:3327-3335.
40. Soares M.J., et al. The prolactin family: effectors of pregnancy-dependent adaptations. Trends Endocrinol. Metab. 2007, 18:114-121.
41. Stocco C., et al. The molecular control of corpus luteum formation, function and regression. Endocr. Rev. 2007, 28:117-149.
42. Risk M., Gibori G. Mechanisms of luteal cell regulation by prolactin. Prolactin 2001, 265-295. Kluwer Academic Publishers. N.D. Horseman (Ed.).
43. Horseman N.D., et al. Defective mammopoiesis, but normal hematopoiesis, in mice with a targeted disruption of the prolactin gene. EMBO J. 1997, 16:6926-6935.
44. Ormandy C.J., et al. Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev. 1997, 11:167-178.
45. Grosdemouge I., et al. Effects of deletion of the prolactin receptor on ovarian gene expression. Reprod. Biol. Endocrinol. 2003, 1:1-12.
46. Bachelot A., et al. Corpus luteum development: lessons from genetic models in mice. Curr. Top. Dev. Biol. 2005, 68:49-84.
47. Bachelot A., et al. Reproductive role of prolactin. Reproduction. 2007, 133:361-369.
48. Binart N., et al. Rescue of preimplantatory egg development and embryo implantation in prolactin receptor-deficient mice after progesterone administration. Endocrinology 2000, 141:2691-2697.
49. Gafvels M., et al. Prolactin stimulates the expression of luteinizing hormone/chorionic gonadotropin receptor messenger ribonucleic acid in the rat corpus luteum and rescues early pregnancy from bromocriptine-induced abortion. Biol. Reprod. 1992, 47:534-540.
50. Segaloff D.L., et al. Hormonal regulation of luteinizing hormone/chorionic gonadotropin receptor mRNA in rat ovarian cells during follicular development and luteinization. Mol. Endocrinol. 1990, 4:1856-1865.
51. Albarracin C.T., et al. Identification of a major prolactin-regulated protein as 20 alpha- hydroxysteroid dehydrogenase: coordinate regulation of its activity, protein content, and messenger ribonucleic acid expression. Endocrinology 1994, 134:2453-2460.
52. Piquette G.N., et al. Regulation of luteinizing hormone receptor messenger ribonucleic acid levels by gonadotropins, growth factors, and gonadotropin-releasing hormone in cultured rat granulosa cells. Endocrinology 1991, 128:2449-2456.
53. Gunnet J.W., et al. The mating-induced release of prolactin: A unique neuroendocrine response. Endocr. Rev. 1983, 4:44-61.
54. Gunnet J.W., et al. Hypothalamic regulation of mating-induced prolactin release. Effect of electrical stimulation of the medial preoptic area in conscious female rats. Neuroendocrinology 1984, 38:12-16.
55. Gibori G., et al. Dissociation of two distinct luteotropic effects of prolactin: regulation of luteinizing hormone-receptor content and progesterone secretion during pregnancy. Endocrinology 1978, 102:767-774.
56. Bachelot A., et al. Prolactin independent rescue of mouse corpus luteum life span: identification of prolactin and luteinizing hormone target genes. Am. J. Physiol Endocrinol. Metab. 2009, 297:E676-E684.
57. Neeman M., et al. Regulation of angiogenesis by hypoxic stress: from solid tumours to the ovarian follicle. Int. J. Exp. Pathol. 1997, 78:57-70.
58. Weng L., et al. PTEN induces apoptosis and cell cycle arrest through phosphoinositol-3-kinase/Akt-dependent and -independent pathways. Hum. Mol. Genet. 2001, 10:237-242.
59. Leslie N.R., et al. PTEN function: how normal cells control it and tumour cells lose it. Biochem. J. 2004, 382:1-11.
60. Froment P., et al. PTEN expression in ovine granulosa cells increases during terminal follicular growth. FEBS Lett. 2005, 579:2376-2382.
61. Halperin J., et al. 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, 22:513-522.
62. Jagarlamudi K., et al. Genetically modified mouse models for premature ovarian failure (POF). Mol. Cell Endocrinol. 2010, 315:1-10.
63. Telleria C.M., et al. The different forms of the prolactin receptor in the rat corpus luteum: developmental expression and hormonal regulation in pregnancy. Endocrinology 1997, 138:4812-4820.
64. Schuff K.G., et al. Lack of prolactin receptor signaling in mice results in lactotroph proliferation and prolactinomas by dopamine-dependent and -independent mechanisms. J. Clin. Invest. 2002, 110:973-981.
65. Forges T., et al. Pathophysiology of impaired ovarian function in galactosaemia. Hum. Reprod. Update. 2006, 12:573-584.
66. Onuma H., et al. Correlation between FOXO1a (FKHR) and FOXO3a (FKHRL1) binding and the inhibition of basal glucose-6-phosphatase catalytic subunit gene transcription by insulin. Mol. Endocrinol. 2006, 20:2831-2847.
67. Liu G., et al. Galactose metabolism and ovarian toxicity. Reprod. Toxicol. 2000, 14:377-384.
68. Castrillon D.H., et al. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 2003, 301:215-218.
69. Hosaka T., et al. Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:2975-2980.
70. Zinaman M.J., et al. Pulsatile GnRH stimulates normal cyclic ovarian function in amenorrheic lactating postpartum women. J. Clin. Endocrinol. Metab. 1995, 80:2088-2093.
71. Bouchard P., et al. Gonadotropin-releasing hormone pulsatile administration restores luteinizing hormone pulsatility and normal testosterone levels in males with hyperprolactinemia. J. Clin. Endocrinol. Metab. 1985, 60:258-262.
72. Ben Jonathan N., et al. What can we learn from rodents about prolactin in humans?. Endocr. Rev. 2008, 29:1-41.
73. Devoto L., et al. Human corpus luteum physiology and the luteal-phase dysfunction associated with ovarian stimulation. Reprod. Biomed. Online 2009, 18(Suppl 2):19-24.
74. Schwarzler P., et al. Prolactin gene expression and prolactin protein in premenopausal and postmenopausal human ovaries. Fertil. Steril. 1997, 68:696-701.
75. Vlahos N.P., et al. Prolactin receptor gene expression and immunolocalization of the prolactin receptor in human luteinized granulosa cells. Mol. Hum. Reprod. 2001, 7:1033-1038.
76. Perks C.M., et al. Prolactin acts as a potent survival factor against C2-ceramide-induced apoptosis in human granulosa cells. Hum. Reprod. 2003, 18:2672-2677.
77. Beck-Peccoz, P. et al. (2006) Premature ovarian failure. Orphanet. J. Rare. Dis. 1:9, 1-5.
78. Das R., et al. Transduction of prolactin's (PRL) growth signal through both long and short forms of the PRL receptor. Mol. Endocrinol. 1995, 9:1750-1759.
79. Soares, M. J. (2004) The prolactin and growth hormone families: pregnancy-specific hormones/cytokines at the maternal-fetal interface. Reprod. Biol. Endocrinol. 2: 51, 1-15.