[en] This study aims to characterise Prolactin receptor (PRLR) in rainbow trout for which no information is available despite the availability of Salmonid PRL preparations. By screening a freshwater rainbow trout intestine cDNA library with a probe corresponding to the extracellular domain (ECD) of tilapia PRLR, we have cloned a 2.5 kb insert coding for the PRLR. The mature protein of 614 amino acid residues is similar to PRLR isolated in tilapia and also the long form of mammalian PRLR. Analysis of PRLR gene expression in osmoregulatory organs revealed the presence of a unique transcript, thus confirming the involvement of this hormone in the control of osmoregulation in this fish species. By using surface plasmon resonance (SPR) technology, kinetic measurement of interaction between trout PRL and its receptor ECD was studied. This approach allowed us to demonstrate the formation of a transient, unstable homodimeric complex. This unstability could explain the inability to perform binding experiments using homologous PRL. In contrast, heterologous lactogenic ligands were able to interact through a more stable complex. Whether these characteristics of PRL-receptor interaction in rainbow trout are different to what occurs in tilapia where a homologous radioreceptor assay was developed would require further studies.
Le Rouzic, Philippe; Institut Scientifique de Recherche Agronomique - INRA > Station de Recherche Commune en Ichtyophysiologie, Biodiversité et Environnement > Group on Physiology of Adaptation and Stress
Sandra, Olivier; Institut Scientifique de Recherche Agronomique - INRA > Station de Recherche Commune en Ichtyophysiologie, Biodiversité et Environnement > Group on Physiology of Adaptation and Stress
Grosclaude, Jeanne; Institut Scientifique de Recherche Agronomique - INRA > Unité de Virologie et Immunologie Moléculaire
Rentier-Delrue, Françoise ; Université de Liège - ULiège > Département des sciences de la vie > Biologie et génétique moléculaire - GIGA-R : Coordination scientifique
Jolois, Olivier ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Histologie humaine
Tujague, Michel; Centre National de la Recherche Scientifique - CNRS > Unité de recherche 6062 Interaction cellulaire et Moléculaire
Pakdel, Farzad; Centre National de la Recherche Scientifique - CNRS > Unité de recherche 6062 Interaction cellulaire et Moléculaire
Sandowski, Yael; Hebrew University of Jerusalem > Faculty of Agriculture > Institute of Biochemistry, Food and Nutrtion
Cohen, Yael; Hebrew University of Jerusalem > Faculty of Agriculture > Institute of Biochemistry, Food and Nutrtion
Gertler, Arieh; Hebrew University of Jerusalem > Faculty of Agriculture > Institute of Biochemistry, Food and Nutrtion
Prunet, Patrick; Institut Scientifique de Recherche Agronomique - INRA > Station de Recherche Commune en Ichtyophysiologie, Biodiversité et Environnement > Group on Physiology of Adaptation and Stress
Language :
English
Title :
Evidence of rainbow trout prolactin interaction with its receptor through unstable homodimerisation.
Publication date :
2001
Journal title :
Molecular and Cellular Endocrinology
ISSN :
0303-7207
eISSN :
1872-8057
Publisher :
North Holland Publishing Company, Amsterdam, Netherlands
Auperin B., Rentier-Delrue F., Martial J., Prunet P. (1994) Evidence that the two (Oreochromis niloticus) prolactins have different osmoregulatory functions during adaptation to a hyperosmotic environment. J. Mol. Endocrinol. 12:13-24.
Bazan J.F. (1990) Structural design and molecular evolution of a cytokine receptor superfamily. Proc. Natl. Acad. Sci. USA 87:6934-6938.
Björnsson B.T., Hansson T. (1983) Effects of hypophysectomy on the plasma ionic osmotic balance in rainbow trout, Salmo gairdneri. Gen. Comp. Endocrinol. 49:240-247.
Bole-Feysot C., Goffin V., Edery M., Binart N., Kelly P.A. (1998) Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocrine Rev. 19:225-268.
Bignon C., Binart N., Ormandy C., Schuler L.A., Kelly P.A. (1997) 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. 19:109-120.
Boutin J.M., Edery M., Shirota M., Jolicoeur C., Lesueur L., Ali S., Gould D., Djiane J., Kelly P.A. (1989) Identification of a cDNA encoding a long form of prolactin receptor in human hepatoma and breast cancer cells. Mol. Endocrinol. 3:1455-1461.
Chen X., Horseman N.D. (1994) Cloning, expression and mutational analysis of the pigeon prolactin receptor. Endocrinology 135:269-276.
Chomczynski P., Sacchi N. (1987) Simple step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
Devlin R.H., Byatt J.C., McLean E., Yesaki T.Y., Krivi G.G., Jaworski E.G., Clarke W.C., Donaldson E.M. (1994) Bovine placental lactogen is a potent stimulator of growth and displays strong binding to hepatic receptor sites of coho salmon. Gen. Comp. Endocrinol. 95:31-41.
Dharmamba M., Maetz J. (1972) Effects of hypophysectomy and prolactin in on the sodium balance of Tilapia mossambica in fresh water. Gen. Comp. Endocrinol. 19:175-183.
Ducouret B., Tujague M., Ashraf J., Mouchel N., Servel N., Valotaire Y., Thompson E.B. (1995) Cloning of a teleost fish glucocorticoid receptor shows that it contains a deoxyribonucleic acid-binding domain different from that of mammals. Endocrinology 136:3774-3783.
Dusanter-Fourt I., Belair L., Gespach C., Djiane J. (1992) Expression of prolactin (PRL) receptor gene and PRL-binding sites in rabbit intestinal epithelial cells. Endocrinology 130:2877-2882.
Gertler A., Grosclaude J., Starsburger J., Nir S., Djiane J. (1996) 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 dimerisation. J. Biol. Chem. 271:24482-24491.
Hirano T. (1986) The spectrum of prolactin actions in teleosts., Ralph C.L. (Ed.), Comparative Endocrinology: Developments and Directions, New York: Alan R. Liss; 53-74.
Johnsson B., Lofas S., Lindquist G. (1991) Immobilization of proteins to a carboxymethyldextran-modified gold surface for biospecific interaction analysis in surface plasmon resonance sensors. Anal. Biochem. 198:268-277.
Kelly P.A., Djiane J., Postel-Vinay M.C., Edery M. (1991) The growth hormone/prolactin receptor family. Endocrine Rev. 12:235-251.
Kelly P.A., Ali S., Rozakis M., Goujon L., Nagano M., Pellegrini I., Gould D., Djiane J., Edery M., Finidori J., Postel-Vinay M.C. (1993) The growth hormone/prolactin receptor family. Recent Prog. Horm. Res. 48:123-164.
L'Hoir C., Renard A., Martial J.A. (1990) Expression in E. coli of two mutated genes encoding the cholera toxin B subunit. Gene 89:47-52.
Madsen S.S., Bern H.A. (1992) Antagonism of prolactin and growth hormone: impact on seawater adaptation in two salmonids, Salmo trutta and Oncorhynchus mykiss. Zool. Sci. 9:775-784.
McCormick S.D. (1995) Hormonal control of gill Na+K+ATPase and chloride cell function., Wood C.M., Shuttleworth T.J. (Eds.), Cellular and Molecular Approaches to Fish Ionic Regulation, New York: Academic Press; 285-315.
Mercier L., Rentier-Delrue F., Swennen D., Lion M., Le Goff P., Prunet P., Martial J. (1989) Rainbow trout prolactin cDNA cloning in Escherichia coli. DNA 8:119-125.
Moore R.C., Oka T. (1993) Cloning and sequencing of the cDNA encoding the murine mammary gland long-form prolactin receptor. Gene 134:263-266.
Pickford G.E., Phillips J.G. (1959) Prolactin, a factor promoting survival of hypophysectomized killifish in freshwater. Nature 228:378-379.
Prunet P., Houdebine L.M. (1984) Purification and biological characterization of chinook salmon prolactin. Gen. Comp. Endocrinol. 53:49-57.
Prunet P., Avella M., Fostier A., Björnsson B.T., Boeuf G., Haux C. (1990) Roles of prolactin in salmonids., Epple A., Scanes C.G., Stetson M.T. (Eds.), Progress in Comparative Endocrinology, New York: Wiley-Liss; 547-552.
Rentier-Delrue F., Swennen D., Prunet P., Lion M., Martial J.A. (1989) Tilapia prolactin: molecular cloning of two cDNAs and expression in Escherichia coli. DNA 8:271-278.
Sakaï D.K. (1981) Blastogenic response of peripherical lymphocytes separated from rainbow trout to phytohemmagglutinin, concanavalin A and pokeweed mitogen. Bull. Jpn. Sci. Cos. Fish. 47:1545-1550.
Sakaï M., Kobayashi M., Kawauchi H. (1996) Mitogenic effect of growth hormone and prolactin on chum salmon Oncorhynchus keta leukocytes in vitro. Vet. Immunol. Immunopathol. 53:185-189.
Sakal E., Bignon C., Grosclaude J., Kantor A., Shapira R., Leibovitch H., Helman D., Nespoulous C., Shamay A., Rowlinson S.W., Djiane J., Gertler A. (1997) Large-scale preparation and characterization of recombinant ovine placental lactogen. J. Endocrinol. 152:317-327.
.
Sandra O., Sohm F., De Luze A., Prunet P., Edery M., Kelly P.A. (1995) Expression cloning of a cDNA encoding a fish prolactin receptor. Proc. Natl. Acad. Sci. USA 92:6037-6041.
Sandra O., Le Rouzic P., Cauty C., Edery M., Prunet P. (2000) Expression of the prolactin receptor (tiPRL-R) gene in tilapia Oreochromis niloticus: tissue distribution and cellular localization in osmoregulatory organs. J. Mol. Endocrinol. 24:215-224.
Sanger F., Nicklen S., Coulson A.R. (1977) DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
Scott P., Kessler M.A., Schuler L.A. (1992) Molecular cloning of the bovine prolactin receptor transcripts in fetal and utero-placental-tissues. Mol. Cell. Endocrinol. 89:47-58.
Seidelin M., Madsen S.S. (1997) Prolactin antagonizes the seawater-adaptive effect of cortisol and growth hormone in anadromous brown trout (Salmo trutta). Zool. Sci. 14:249-256.
Seidelin M., Madsen S.S. (1999) Endocrine control of Na+K+-ATPase and chloride cell development in brown trout (Salmo trutta): interaction of insulin-like growth factor-I with prolactin and growth hormone. J. Endocrinol. 162:127-135.
Shirota M., Banville D., Ali S., Jolicoeur C., Boutin J.M., Edery M., Djiane J., Kelly P.A. (1990) Expression of two forms of prolactin receptor in rat ovary and liver. Mol. Endocrinol. 4:1136-1143.
Sohm F., Pezet A., Sandra O., Prunet P., De Luze A., Edery M. (1998) Activation of gene transcription by tilapia prolactin variants tiPRL188 and tiPRL177. FEBS Lett. 438:119-123.
Studier F.W., Moffat B.A. (1986) Use of T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189:113-130.
Swennen D., Rentier-Delrue F., Aupérin A., Prunet P., Flik G., Wendelaar Bonga S.E., Lion M., Martial J.A. (1991) Production and purification of biologically active recombinant tilapia (Oreochromis niloticus) prolactins. J. Endocrinol. 131:219-227.
Tanaka M., Maeda K., Okubo T., Nakashima K. (1992) Double antenna structure of chicken prolactin receptor deduced from the cDNA sequence. Biochem. Biophys. Res. Commun. 188:490-496.
Tse D.L., Chow B.K., Chan C.B., Lee L.T., Cheng C.H. (2000) Molecular cloning and expression studies of the prolactin receptor in goldfish (Carassius auratus). Life Sci. 66:593-605.
