Domestic Animal Endocrinology
Volume 33, Issue 3 , Pages 313-334 , October 2007

Cloning and functional characterization of allelic variation in the porcine prolactin receptor

  • Josephine F. Trott

      Affiliations

    • Lactation and Mammary Gland Biology Group, Department of Animal Science, University of Vermont, 221 Terrill Hall, 570 Main Street, Burlington, VT 05405, United States
    • ,
  • Nicholas R. Farley

      Affiliations

    • Lactation and Mammary Gland Biology Group, Department of Animal Science, University of Vermont, 221 Terrill Hall, 570 Main Street, Burlington, VT 05405, United States
    • ,
  • Douglas J. Taatjes

      Affiliations

    • College of Medicine, University of Vermont, 89 Beaumont Avenue, Burlington, VT 05405, United States
    • ,
  • Russell C. Hovey

      Affiliations

    • Lactation and Mammary Gland Biology Group, Department of Animal Science, University of Vermont, 221 Terrill Hall, 570 Main Street, Burlington, VT 05405, United States
    • Corresponding Author InformationCorresponding author. Tel.: +1 802 656 2683; fax: +1 802 656 8196.

Received 28 May 2006 ,Revised 7 July 2006 ,Accepted 9 July 2006.

References 

  1. Lesueur L, Edery M, Ali S, Paly J, Kelly PA, 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;88:482–828
  2. O’Neal KD, Yu-Lee LY. Differential signal transduction of the short, Nb2, and long prolactin receptors. Activation of interferon regulatory factor-1 and cell proliferation. J Biol Chem. 1994;269:26076–26082
  3. Jabbour HN, Critchley HO, Boddy SC. Expression of functional prolactin receptors in nonpregnant human endometrium: Janus Kinase-2, signal transducer and activator of transcription-1 (STAT1), and STAT5 proteins are phosphorylated after stimulation with prolactin. J Clin Endocrinol Metab. 1998;83:2545–2553
  4. Llovera M, Pichard C, Bernichtein S, Jeay S, Touraine P, Kelly PA, et al. Human prolactin (hPRL) antagonists inhibit hPRL-activated signaling pathways involved in breast cancer cell proliferation. Oncogene. 2000;19:4695–4705
  5. Flint DJ, Knight CH. Interactions of prolactin and growth hormone (GH) in the regulation of mammary gland function and epithelial cell survival. J Mammary Gland Biol Neoplasia. 1997;2:41–48
  6. Kaminska B, Opalka M, Ciereszko RE, Dusza L. The involvement of prolactin in the regulation of adrenal cortex function in pigs. Domest Anim Endocrinol. 2000;19:147–157
  7. Farmer C, Robert S, Rushen J. Bromocriptine given orally to periparturient or lactating sows inhibits milk production. J Anim Sci. 1998;76:750–757
  8. Farmer C, Sorensen MT, Robert S, Petitclerc D. Administering exogenous porcine prolactin to lactating sows: milk yield, mammary gland composition, and endocrine and behavioral responses. J Anim Sci. 1999;77:1851–1859
  9. Ciereszko R, Opalka M, Kaminska B, Kaminski T, Dusza L. Prolactin involvement in the regulation of the hypothalamic–pituitary–ovarian axis during the early luteal phase of the porcine estrous cycle. Anim Reprod Sci. 2002;69:99–115
  10. Farmer C, Sorensen MT, Petitclerc D. Inhibition of prolactin in the last trimester of gestation decreases mammary gland development in gilts. J Anim Sci. 2000;78:1303–1309
  11. Sakai S, Katoh M, Berthon P, Kelly PA. Characterization of prolactin receptors in pig mammary gland. Biochem J. 1985;224:911–922
  12. Berthon P, Katoh M, Dusanter-Fourt I, Kelly PA, Djiane J. Purification of prolactin receptors from sow mammary gland and polyclonal antibody production. Mol Cell Endocrinol. 1987;51:71–81
  13. Plaut KI, Kensinger RS, Griel LC, Kavanaugh JF. Relationships among prolactin binding, prolactin concentrations in plasma and metabolic activity of the porcine mammary gland. J Anim Sci. 1989;67:1509–1519
  14. Young KH, Kraeling RR, Bazer FW. Effect of pregnancy and exogenous ovarian steroids on endometrial prolactin receptor ontogeny and uterine secretory response in pigs. Biol Reprod. 1990;43:592–599
  15. Bramley TA, Menzies GS. Receptors for lactogenic hormones in the porcine corpus luteum: properties and luteal phase concentrations. J Endocrinol. 1987;113:355–364
  16. Slomczynska M, Gregoraszczuk E, Kochman K, Stoklosowa S. Prolactin binding analysis and immunohistochemical localization of prolactin receptor in porcine ovarian cells. Endocrinol J. 2001;48:71–80
  17. Young KH, Bazer FW. Porcine endometrial prolactin receptors detected by homologous radioreceptor assay. Mol Cell Endocrinol. 1989;64:145–154
  18. Klemcke HG, Pond WG, Nienaber JA. Porcine adrenal prolactin receptors: characterization, changes during neonatal development and effects of hypoprolactinemia. Comp Biochem Physiol A. 1989;92:197–206
  19. Muccioli G, Bellussi G, Ghe C, Pagnini G, Di Carlo R. Regional distribution and species variation of prolactin binding sites in the brain. Gen Comp Endocrinol. 1988;69:399–405
  20. 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. Endocrinol Rev. 1998;19:225–268
  21. Rothschild MF. Genetics and reproduction in the pig. Anim Reprod Sci. 1996;42:143–151
  22. Vincent AL, Wang L, Tuggle CK, Robic A, Rothschild MF. Prolactin receptor maps to pig chromosome 16. Mammary Genome. 1997;8:793–794
  23. Drogemuller C, Hamann H, Distl O. Candidate gene markers for litter size in different German pig lines. J Anim Sci. 2001;79:2565–2570
  24. Zhang SJ, Xiong YZ, Deng CY, Zeng FT, Qiu XP, Xiao SM, et al. Study of molecular genetics of the size of reproductive organs and litter size in the sow. Yi Chuan Xue Bao. 2002;29:1073–1077
  25. van Rens BT, Evans GJ, van der Lende T. Components of litter size in gilts with different prolactin receptor genotypes. Theriogenology. 2003;59:915–926
  26. Ormandy CJ, Camus A, Barra J, Damotte D, Lucas B, Buteau H, et al. Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev. 1997;11:167–178
  27. Trott JF, Hovey RC, Koduri S, Vonderhaar BK. Alternative splicing to exon 11 of human prolactin receptor gene results in multiple isoforms including a secreted prolactin binding protein. J Mol Endocrinol. 2003;30:31–47
  28. Sambrook J, Russell DW. Molecular cloning: a laboratory manual.. 3rd ed.. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 2001;
  29. Ramakers C, Ruijter JM, Deprez RH, Moorman AF. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett. 2003;339:62–66
  30. Dunand M, Aubert ML, Kraehenbuhl JP, Rossier BC. Specific binding sites for ovine prolactin in three amphibian cell lines. Am J Physiol. 1985;248:C80–C87
  31. Ashkenazi A, Cohen R, Gertler A. Characterization of lactogen receptors in lactogenic hormone-dependent and independent NB2 lymphoma cell lines. FEBS Lett. 1987;210:51–55
  32. Djiane J, Delouis C, Kelly PA. Prolactin receptor turnover in explants of pseudopregnant rabbit mammary gland. Mol Cell Endocrinol. 1982;25:163–170
  33. Sandowski Y, Cohen Y, Le Rouzic P, Bignon C, Rentier-Delrue F, Djiane J, et al. Recombinant prolactin receptor extracellular domain of rainbow trout (Oncorhynchus mykiss): subcloning, preparation, and characterization. Gen Comp Endocrinol. 2000;118:302–309
  34. Claros MG, von Heijne G. TopPred II: an improved software for membrane protein structure predictions. Bioinformatics. 1994;10:685–686
  35. Kline JB, Roehrs H, Clevenger CV. Functional characterization of the intermediate isoform of the human prolactin receptor. J Biol Chem. 1999;274:35461–35468
  36. Hu ZZ, Meng J, Dufau ML. 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
  37. Dorato A, Raguet S, Okamura H, Bergeron JJ, Kelly PA, Posner BI. Characterization of the structure and glycosylation properties of intracellular and cell surface rat hepatic prolactin receptors. Endocrinology. 1992;131:1734–1742
  38. Vincent AL, Evans G, Short TH, Southwood OI, Plastow GS, Tuggle CK, et al. The prolactin receptor gene is associated with increased litter size in pigs. In: Proceedings of the sixth world congress on genetics and applied livestock production armidale, vol. 27. 1998;p. 15–18
  39. Picazo RA, Garcia Ruiz JP, Santiago Moreno J, Gonzalez de Bulnes A, Munoz J, Silvan G, et al. Cellular localization and changes in expression of prolactin receptor isoforms in sheep ovary throughout the estrous cycle. Reproduction. 2004;128:545–553
  40. Kinoshita H, Yasui T, Ushigoe K, Irahara M, Tanaka M, Nakashima K, et al. Expression of ovarian prolactin receptor in relation to hormonal changes during induction of ovulation in the rat. Gynecol Obstet Invest. 2001;52:132–138
  41. Russell DL, Richards JS. Differentiation-dependent prolactin responsiveness and stat (signal transducers and activators of transcription) signaling in rat ovarian cells. Mol Endocrinol. 1999;13:2049–2064
  42. Telleria CM, Parmer TG, Zhong L, Clarke DL, Albarracin CT, Duan WR, 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
  43. Clarke DL, Linzer DI. Changes in prolactin receptor expression during pregnancy in the mouse ovary. Endocrinology. 1993;133:224–232
  44. Duan WR, Linzer DI, Gibori G. Cloning and characterization of an ovarian-specific protein that associates with the short form of the prolactin receptor. J Biol Chem. 1996;271:15602–15607
  45. Boutin JM, Jolicoeur C, Okamura H, Gagnon J, Edery M, Shirota M, et al. Cloning and expression of the rat PRL receptor, a member of the growth hormone/prolactin receptor gene family. Cell. 1988;53:69–77
  46. Davis JA, Linzer DIH. Expression of multiple forms of the prolactin receptor in mouse liver. Mol Endocrinol. 1989;3:674–680
  47. Bignon C, Binart N, Ormandy CJ, Schuler LA, Kelly PA, 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
  48. Dusanter-Fourt I, Kelly PA, Djiane J. Immunological recognition of the prolactin receptor: identification of a single binding unit of molecular weight approximately 42,000. Biochimie. 1987;69:639–646
  49. Berthon P, Kelly PA, Djiane J. Water-soluble prolactin receptors from porcine mammary gland. Proc Soc Exp Biol Med. 1987;184:300–306
  50. Buteau H, Pezet A, Ferrag F, Perrot-Applanat M, Kelly PA, Edery M. N-glycosylation of the prolactin receptor is not required for activation of gene transcription but is crucial for its cell surface targeting. Mol Endocrinol. 1998;12:544–555
  51. Lascols O, Capeau J, Cherqui G, Caron M, Bachimont J, Picard J. Glycosylation characteristics of the mouse liver lactogenic receptor. Mol Cell Endocrinol. 1989;65:145–155
  52. Cahoreau C, Gamier L, Djiane J, Devauchelle G, Cerutti M. Evidence for N-glycosylation and ubiquitination of the prolactin receptor expressed in a baculovirus-insect cell system. FEBS Lett. 1994;350:230–234
  53. Waters MJ, Daniel N, Bignon C, Dijiane J. The rabbit mammary gland prolactin receptor is tyrosine phosphorylated in response to prolactin in vivo and in vitro. J Biol Chem. 1995;270:5136–5143
  54. Lascols O, Cherqui G, Munier A, Picard J, Capeau J. Differences in both glycosylation and binding properties between rat and mouse liver prolactin receptors. Cell Mol Biol (Noisy-le-grand). 1994;40:359–371
  55. Savoie S, Rindress D, Posner BI, Bergeron JJ. Tunicamycin sensitivity of prolactin, insulin and epidermal growth factor receptors in rat liver plasmalemma. Mol Cell Endocrinol. 1986;45:241–246
  56. Gertler A, Grosclaude J, Strasburger CJ, 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;271:24482–24491
  57. Peterson FC, Brooks CL. Identification of a motif associated with the lactogenic actions of human growth hormone. J Biol Chem. 1997;272:21444–21448
  58. Dodd SC, Forsyth IA, Buttle HL, Gurr MI, Dils RR. Hormonal induction of alpha-lactalbumin and beta-lactoglobulin in cultured mammary explants from pregnant pigs. J Dairy Res. 1994;61:35–45
  59. Simpson KJ. The tammar wallaby (Macropus eugenii), a model to study autocrine and endocrine regulation of lactation. Melbourne, Australia: Department of Agriculture, La Trobe University; 1998;

PII: S0739-7240(06)00122-6

doi: 10.1016/j.domaniend.2006.07.001

Domestic Animal Endocrinology
Volume 33, Issue 3 , Pages 313-334 , October 2007

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