Structure and functional analysis of a tilapia (Oreochromis mossambicus) growth hormone gene: activation and repression by pituitary transcription factor Pit-1
Sekkali, Belaid; Brim, Hassan; Muller, Marcet al.
1999 • In DNA and Cell Biology, 18 (6), p. 489-502
[en] A gene encoding the Tilapia mossambica (Oreochromis mossambicus) growth hormone (tiGH) was isolated and sequenced. The gene spans 5.6 kb, including 3.7 kb of 5' and 0.2 kb of 3' flanking sequences and a 1.7-kb transcription unit comprised of six exons and five introns. The gene and the 5' flanking region contain several potential binding sites for Pit-1, a key transcription activator of mammalian GH genes. One of these (-57/-42) is highly conserved in fish GH genes. It activates transcription in pituitary cells and binds Pit-1. Transfection of luciferase reporter plasmids containing either the -3602/+19 tiGH sequence or one of its 5' deletion mutants (-2863/, -1292/, and -463/+19) resulted in strong activity in Pit-1-producing rat pituitary GC cells. A dose-dependent activation of the tiGH promoter was achieved in nonpituitary fish EPC and monkey COS cells cotransfected with a rat Pit-1 expression vector, demonstrating the crucial role played by Pit-1 as an activator of the tiGH gene. Fusion of the tiGH promoter with the beta-galactosidase gene led to transient expression specifically in the nervous system of microinjected zebrafish embryos. The activity of the tiGH promoter in GC and EPC cells was strongly repressed by extending its 3' end from +19 to +40, a sequence in which a Pit-1-binding site was identified using gel retardation assays. Point mutations of the site that suppressed Pit-1 binding in vitro restored full tiGH promoter activity. Thus, a Pit-1-binding site located in the 5' untranslated region mediates Pit-1-dependent repression of the tiGH gene.
Research center :
AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège Giga-Development and Stem Cells - ULiège
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Sekkali, Belaid
Brim, Hassan
Muller, Marc ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire
Argenton, Francesco; Universita di Padova
Bortolussi, Marino; Universita di Padova
Colombo, Lorenzo; Universita di Padova
Belayew, Alexandra
Martial, Joseph ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire
Language :
English
Title :
Structure and functional analysis of a tilapia (Oreochromis mossambicus) growth hormone gene: activation and repression by pituitary transcription factor Pit-1
Publication date :
1999
Journal title :
DNA and Cell Biology
ISSN :
1044-5498
eISSN :
1557-7430
Publisher :
Mary Ann Liebert, Inc., Larchmont, United States - New York
AGELLON, L.B., DAVIES, S.L., CHEN, T.T., and POWERS, D.A. (1988). Structure of a fish (rainbow trout) growth hormone gene and its evolutionary implications. Proc. Natl. Acad. Sci. USA 85, 5136-5140.
ANDERSEN, B., and ROSENFELD, M.G. (1994). Pit-1 determines cell types during development of the anterior pituitary gland: a model for transcriptional regulation of cell phenotypes in mammalian organogenesis. J. Biol. Chem. 269, 29335-29338.
ANGEL, P., IMAGAWA, M., CHIU, R., STEIN, B., IMBRA, R.J., RAHMSDORF, H.J., JONAT, C., HERRLICH, P., and KARIN, M. (1987). Phorbol ester-inducible genes contain a common cis element recognized by a TPA-modulated trans-acting factor. Cell 49, 729-739.
ARGENTON, F., ARAVA, Y., ARHONHEIM, A., and WALKER, M.D. (1996a). An activation domain of the helix-loop-helix transcription factor E2A shows cell type preference in vivo in microinjected zebra fish embryos. Mol. Cell. Biol. 16, 1714-1721.
ARGENTON, F., BERNARDINI, S., PUTTINI, S., COLOMBO, L., and BORTOLUSSI, M. (1996b). A TGACG motif mediates growth-hormone-factor-1/pituitary-transcriptional-activator-1 dependent cAMP regulation of the rainbow trout growth-hormone promoter. Eur. J. Biochem. 238, 591-598.
BARRON, M.G. (1986). Endocrine control of smoltification in anadromous salmonids. J. Endocrinol. 108, 313-319.
BARTA, A., RICHARDS, R.I., BAXTER, J.D., and SHINE, J. (1981). Primary structure and evolution of rat growth hormone gene. Proc. Natl. Acad. Sci. USA 78, 4867-4871.
BER, R., and DANIEL, V. (1992). Structure and sequence of the growth hormone-encoding gene from Tilapia nilotica. Gene 113, 245-250.
BER, R., and DANIEL, V. (1993). Sequence analysis suggests a recent duplication of the growth hormone-encoding gene in Tilapia nilotica. Gene 125, 143-150.
BODNER, M. and KARIN, M. (1987). A pituitary-specific trans-acting factor can stimulate transcription from the growth hormone promoter in extracts of nonexpressing cells. Cell 50, 267-275.
BODNER, M., CASTRILLO, J.L., THEILL, L.E., DEERINCK, T., ELLISMAN, M., and KARIN, M. (1988). The pituitary-specific transcription factor GHF-1 is a homeobox-containing protein. Cell 55, 505-518.
BOLTON, J.P., COLLIE, N.L., KAWAUCHI, H., and HIRANO, T. (1987). Osmoregulatory actions of growth hormone in rainbow trout (Salmo gairdneri). J. Endocrinol. 112, 63-68.
BOSHART, M., KLUPPEL, M., SCHMIDT, A., SCHUTZ. G., and LUCKOW, B. (1992). Reporter constructs with low background activity utilizing the CAT gene. Gene 110, 129-130.
BRADFORD, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
BUCHER, P. (1990). Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J. Mol. Biol. 212, 563-578.
BYRNE, C.R., WILSON, B.W., and WARD, K.A. (1987). The isolation and characterization of the ovine growth hormone gene. Aust. J. Biol. Sci. 40, 459-468.
CHEN, R., INGRAHAM, H.A., TREACY, M.N., ALBERT, V.R., WILSON, L., and ROSENFELD, M.G. (1990). Autoregulation of pit-1 gene expression mediated by two cis-active promoter elements. Nature 346, 583-586.
CHIOU, C.-S., CHEN, H.-T., and CHANG, W.-C. (1990). The complete nucleotide sequence of the growth hormone gene from the common carp (Cyprinus carpio). Biochim. Biophys. Acta 1087, 91-94.
DENOTO, F.M., MOORE, D.D., and GOODMAN, H.M. (1981). Human growth hormone DNA sequence and mRNA structure: possible alternative splicing. Nucleic Acids Res. 9, 3719-3730.
DEVLIN, R.H. (1993). Sequence of sockeye salmon type 1 and 2 growth hormone genes and the relationship of rainbow trout with Atlantic and Pacific salmon. Can. J. Fish. Aqua. Sci. 50, 1738-1748.
DIGNAM, J.D., LEBOVITZ, R.M., and ROEDER, R.G. (1983). Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11, 1475-1489.
DU, S.J., DEVLIN, R.H., and HEW, C.L. (1993). Genomic structure of growth hormone genes in chinook salmon (Oncorhynchus tshawytscha): presence of two functional genes, GH-I and GH-II, and a male-specific pseudogene, GH. DNA Cell Biol. 12, 739-751.
ELSHOLTZ, H.P., ALBERT, V.R., TREACY, M.N., and ROSENFELD, M.G. (1990). A two-base change in a POU factor-binding site switches pituitary-specific to lymphoid-specific gene expression. Genes Dev. 4, 43-51.
ELSHOLTZ, H.P., MAJUMDAR-SONNYLAL, S., XIONG, F., GONG, Z.Y., and HEW, C.L. (1992). Phylogenic specificity of prolactin gene expression with conservation of Pit-1 function. Mol. Endocrinol. 6, 515-522.
FIJAN, N., SULIMANOVIC, D., BEARZOTTI, M., MUZINIC, D., ZWILLENBERG, L.O., CHILMONCZYK, S., VAUTHEROT, J.F., and DE KINKELIN, P. (1983). Some properties of the epithelioma papulosum cyprini (EPC) cell line from carp Cyprinus carpio. Annu. Virol. Inst. Pasteur 134, 207-220.
GEHRING, W.J., AFFOLTER, M., and BURGLIN, T. (1994). Homeodomain proteins. Annu. Rev. Biochem. 63, 487-526.
GORDON, D.F., QUICK, D.P., ERWIN, C.R., DONELSON, J.E., and MAURER, R.A. (1983). Nucleotide sequence of the bovine growth hormone chromosomal gene. Mol. Cell. Endocrinol. 33, 81-95.
GROSSBERGER, D. (1987). Minipreps of DNA from bacteriophage lambda. Nucleic Acids Res. 15, 6737.
HE, X., TREACY, M.N., SIMMONS, D.M., INGRAHAM, H.A., SWANSON, L.W., and ROSENFELD, M.G. (1989). Expression of a large family of POU-domain regulatory genes in mammalian brain development. Nature 340, 3541.
HOLLY, J.M.P., and WASS, J.A.H. (1989). Insulin-like growth factors; autocrine, paracrine or endocrine? new perspectives of the somatomedin hypothesis in the light of recent developments. J. Endocrinol. 122, 611-618.
HONG, Y., and SCHARTL, M. (1993). Sequence of the growth hormone (GH) gene from the silver carp (Hypophthalmichthys molitrix) and evolution of GH genes in vertebrates. Biochim. Biophys. Acta 1174, 285-288.
INGRAHAM, H.A., CHEN, R.P., MANGALAM, H.J., ELSHOLTZ, H.P., FLYNN, S.E., LIN, C.R., SIMMONS, D.M., SWANSON, L., and ROSENFELD, M.G. (1988). A tissue-specific transcription factor containing a homeodomain specifies a pituitary phenotype. Cell 55,519-529.
INOUE, K., AKITA, N., YAMASHITA, S., SHIBA, T., and FUJITA, T. (1990). Constitutive and inducible expression of a transgene directed by heterologous promoters in a trout liver cell line. Biochem. Biophys. Res. Commun. 173, 1311-1316.
JOHANSEN, B., JOHNSEN, O.C., and VALLA, S. (1989). The complete nucleotide sequence of the growth hormone gene from Atlantic salmon (Salmo salar). Gene 77, 317-324.
LEFEVRE, C., IMAGAWA, M., DANA, S., GRINDLY, J., BODNER, M., and KARIN, M. (1987). Tissue-specific expression of the human growth hormone gene is conferred in part by the binding of a specific trans-acting factor. EMBO J. 6, 971-981.
MACGREGOR, G.R., and CASKEY, C.T. (1989). Construction of plasmids that express E. coli β-galactosidase in mammalian cells. Nucleic Acids Res. 17, 2365.
MALE, R., NERLAAND, A.H., LORENS, J.B., TELLE, W., LOSSIUS, I., and TOTLAND, G.K. (1992). The complete nucleotide sequence of the Atlantic salmon growth hormone I gene. Biochim. Biophys. Acta 1130, 345-348.
MANGALAM, H.J., ALBERT, V.R., INGRAHAM, H.A., KAPILOFF, M., WILSON, L., NELSON, C., ELSHOTZ, H., and ROSENFELD, M.G. (1989). A pituitary POU domain protein, Pit-1, activates both growth hormone and prolactin promoters transcriptionally. Genes Dev. 3, 946-958.
MATSUMOTO, K.-I., MURAKAMI, K., and OKADA, N. (1986). Gene for lysine tRNA1 may be a progenitor of the highly repetitive and transcribable sequences present in the salmon genome. Proc. Natl. Acad. Sci. USA 83, 3156-3160.
MILLER, W.L., and EBERHARDT, N.L. (1983). Structure and evolution of the growth hormone gene family. Endocr. Rev. 4, 97-129.
MILLER, W.L., MARTIAL, J.A., and BAXTER, J.D. (1980). Molecular cloning of DNA complementary to bovine growth hormone in mRNA. J. Biol. Chem. 255, 7521-7524.
MIWA, S., and INUI, Y. (1985). Effects of L-thyroxine and ovine growth hormone on smoltification of amago salmon (Oncorhynchus rhodurus). Gen. Comp. Endocrinol. 58, 436-442.
MOORE, D.D., WALKER, M.D., DIAMOND, D.J., CONKLING, M.A., and GOODMAN, H.M. (1982). Structure, expression and evolution of growth hormone genes. Recent Prog. Horm. Res. 38, 197-225.
MOUNT, S.M. (1982). A catalogue of splice junction sequences. Nucleic Acids Res. 10, 459-472.
NELSON, C., ALBERT, V.R., ELSHOLTZ, H.P., LU, L.I.-W., and ROSENFELD, M.G. (1988). Activation of cell-specific expression of rat growth hormone and prolactin genes by a common transcription factor. Science 239, 1400-1405.
NORDEEN, S.K. (1988). Luciferase reporter gene vectors for analysis of promoters and enhancers. Biotechniques 6, 454-457.
ONO, M., and TAKAYAMA, Y. (1992). Structures of cDNAs encoding chum salmon pituitary-specific transcription factor, Pit-1/GHF-1. Gene 126, 275-279.
ONO, M., MOCHIZUKI, E., MORI, Y., AIZAWA, A., and HARIGAI, T. (1995). The regulatory region and transcription factor required for the expression of rat and salmon pituitary hormone-encoding genes show cell-type and species specificity. Gene 153, 267-271.
PERNASETTI, F., MILNER, R.D.G., AL ASHWAL, A.A.Z., DE ZEGHER, F., CHAVEZ, V.M., MULLER, M., and MARTIAL, J.A. (1998). Pro239Ser: a novel recessive mutation of the Pit1 gene in seven Middle Eastern children with combined pituitary hormone deficiency. J. Clin. Endocrinol. Metab. 83, 2079-2083.
PONCELET, A., MULLER, M., YARON, Z., MARTIAL, J.A., and BELAYEW, A. (1996). The Tilapia prolactin I gene: evolutionary conservation of the regulatory elements directing pituitary-specific expression. DNA Cell Biol. 15, 679-692.
PROUDFOOT, N.J., and BROWNLEE, G.G. (1976). 3′-Non-coding region sequences in eukaryotic messenger RNA. Nature 263, 211-214.
RAND-WEAVER, M., SWANSON, P., KAWAUCHI, H., and DICKHOFF, W.W. (1992). Somatolactin, a novel pituitary protein: purification and plasma levels during reproductive maturation of Coho salmon. J. Endocrinol. 133, 393-403.
REINHARD, E., NEDIVI, E., WEGNER, J., SKENE, J.H., and WESTERFIELD, M. (1994). Neural selective activation and temporal regulation of a mammalian GAP-43 promoter in zebrafish. Development 120, 1767-1775.
RENTIER-DELRUE, F., SWENNEN, D., PHILIPPART, J.C., L'HOIR, C., LION, M., BENRUBI, O., and MARTIAL, J.A. (1989). Tilapia growth hormone: molecular cloning of cDNA and expression in Escherichia coli. DNA 8, 271-278.
RINDER, H., BAYER, T.A., GERTZEN, E.M., and HOFFMAN, W. (1992). Molecular analysis of the ependymin gene and functional test of its promoter region by transient expression in Brachydanio rerio. DNA Cell. Biol. 11, 425-432.
SAMBROOK, J., FRITSCH, E.F., and MANIATIS, T. (1989). Molecular Cloning A Laboratory Manual, ed 2. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.)
SANGER, F., NICKLEN, S., and COULSON, A.R. (1977). DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5463-5467.
SEKKALI, B., HELLEMANS, B.A., BELAYEW, A., MARTIAL, J.A., OLLEVIER, F., and VOLCKAERT, F.A. (1994). A comparative study of reporter gene activities in fish cells and embryos. Mol. Mar. Biol. Biotech. 3, 30-34.
SMITH, K.P., and SHARP, Z.D. (1991). A Pit-1 binding site 3′ to the transcription start site inhibits transcription elongation in vitro. Biochem. Biophys. Res. Commun. 177, 790-796.
SWEETING, R.M., and MCKEOWN, B.A. (1987). Growth hormone and seawater adaptation in Coho salmon, Oncorhynchus kisutch. Comp. Biochem. Physiol. 88A, 147-151.
SWENNEN, D., PONCELET, A.-C., SEKKALI, B., RENTIHR-DELRUE, F., MARTIAL, J.A., and BELAYEW, A. (1992). Structure of the Tilapia (Oreochromis mossambicus) prolactin I gene. DNA 11, 673-684.
TANAKA, M., HOSOKAWA, Y., WATAHIKI, M., and NAKA-SHIMA, K. (1992). Structure of the chicken growth hormone-encoding gene and its promoter region. Gene 112, 235-239.
TANG, Y., LIN, C.M., CHEN, T.T., KAWAUCHI, H., DUNHAM, R.A., and POWERS, D.A. (1993). Structure of the channel catfish (Ictalurus punctatus) growth hormone gene and its evolutionary implications. Mol. Mar. Biol. Biotechnol. 2, 198-206.
TASHJIAN, A.H., YASUMURA, Y., LEVINE, L., SATO, G.H., and PARKER, M.L. (1968). Establishment of clonal strains of rat pituitary tumor cells that secrete growth hormone. Endocrinology 82, 342-352.
THEILL, L.E., and KARIN, M. (1993). Transcriptional control of GH expression and anterior pituitary development. Endocr. Rev. 14, 670-689.
VIZE, P.D., and WELLS, J.R.E. (1987). Isolation and characterization of the porcine growth hormone gene. Gene 55, 339-344.
WESTERFIELD, M., WEGNER, J., JEGALIAN, B.G., DEROBERTIS, E.M., and PUSCHEL, A.W. (1992). Specific activation of mammalian Hox promoters in mosaic transgenic zebrafish. Genes Dev. 6, 591-598.
WILLIAMS, D.W., MULLER, F., LAVENDER, F.L., ORBAN. L., and MACLEAN, N. (1996). High transgene activity in the yolk syncytial layer affects quantitative transient expression assays in zebrafish embryos. Transgen. Res. 5, 451-458.
WRIGHT, J.M. (1989). Nucleotide sequence, genomic organization, and evolution of a major repetitive DNA family in tilapia (Oreochromis mossambicus/hornorum). Nucleic Acids Res. 17, 5071-5079.
YAMADA, S., HATA, J.I., and YAMASHITA, S. (1993). Molecular cloning of fish Pit-1 cDNA and its functional binding to promoter of gene expressed in the pituitary. J. Biol. Chem. 268, 24361-24366.
YOWE, D.L., and EPPING. R.J. (1995). Cloning of the barramundi growth hormone-encoding gene: a comparative analysis of higher and lower vertebrate GH genes. Gene 162, 255-259.
ZHU, Z., HE, L., and CHEN, T.T. (1992). Primary-structural and evolutionary analyses of the growth hormone gene from grass carp (Ctenopharyngodon idellus). Eur. J. Biochem. 207, 643-648.
