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The growth hormone-encoding gene isolated and characterized from Labeo rohita Hamilton is expressed in CHO cells under the control of constitutive promoters in ‘autotransgene’ constructs

Fish Physiology and Biochemistry volume 34, pages 413–436 (2008)Cite this article

Abstract

The growth hormone (GH) gene along with its regulatory sequences has been isolated from the blood and pituitary gland of Labeo rohita. This GH gene is approximately 2.8 kb long and consists of five exons and four introns of varying sizes with AG/TA in its exon–intron junctions. The promoter has a single cyclic AMP response unit (CRE) element, TATA, CAT and several Pit 1 binding sequences. The 1169-bp gene transcript starts 54 bp upstream of the ATG initiation codon and has two polyadenylation signals, ATTAAA, after the TAG stop codon. The mature mRNA has the poly (A) tail inserted 16 bp downstream of the second polyadenylation signal. Four chimeric ‘autotransgenes’ were constructed having either histone 3 or β-actin promoter and cDNA or the total GH gene. The functionality of the individual components of the autotransgene was determined in the Chinese hamster ovary (CHO) cells by transfection experiments. Based on the results, the transcription of the GH gene is initiated at the transcription start signal of the respective promoters and terminates at the 3′ regulatory sequence of the GH gene. Expression of GH in CHO cells shows that the fish promoters are active, the splicing signal is recognized, and the mRNA produced is stable and translated. The GH protein produced is effectively translocated and secreted into the medium. These results indicate the usefulness of CHO cells in determining the property of individual components of autotransgenes constructed from L. rohita and overall functional commonality between fish and mammal.

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References

  • Agellon LB, Davies SL, Chen TT, Powers DA (1988) Structure of fish (rainbow trout) growth hormone gene and its evolutionary implications. Proc Natl Acad Sci USA 85:5136–5140

    Article  PubMed  CAS  Google Scholar 

  • Allendorf FW, Thorgaard GH (1984) Tetraploidy and evolution of salmonid fishes. In: Turner BJ (ed) The evolutionary genetics of fishes. Plenum, New York, pp 1–53

    Google Scholar 

  • Almuly R, Cavari B, Ferstman H, Kolodney O, Funkenstein B (2000) Genomic structure and sequence of the gilthead seabream (Sparus aurata) growth hormone encoding gene: identification of minisatellite polymorphism in intron I. Genome 43:836–845

    Article  PubMed  CAS  Google Scholar 

  • Almuly R, Poleg-Danin Y, Gorshkov S, Gorshkova G, Rapoport B, Soller M, Kashi Y, Funkenstein B (2005) Characterization of the 5′ flanking region of the growth hormone gene of the marine teleost, gilthead seabream Sparus aurata: analysis of a polymorphic microsatellite in the proximal promoter. Fish Sci 71:479–490

    Article  CAS  Google Scholar 

  • Andersen DC, Krummen L (2002) Recombinant expression for therapeutic applications. Curr Opin Biotechnol 13:117–123

    Article  PubMed  CAS  Google Scholar 

  • Argenton F, Bernardini S, Puttini S, Colombo L, Bortolussi M (1996) A TGACG motif mediates growth-hormone-factor-1/pituitary-transcriptional-activator-1-dependent cAMP regulation of rainbow trout growth hormone promoter. Eur J Biochem 238:591–598

    Article  PubMed  CAS  Google Scholar 

  • Argenton F, Vianello S, Bernardini S, Lopreiato R, Colombo L, Bortolussi M (2002) Trout GH promoter analysis reveals a modular pattern of regulation consistent with the diversification of GH gene control and function in vertebrates. Mol Cell Endocrin 189:11–23

    Article  CAS  Google Scholar 

  • Barnes LM, Bentley CM, Dickson AJ (2003) Stability of protein production from mammalian cells. Biotechnol Bioeng 81:631–639

    Article  PubMed  CAS  Google Scholar 

  • Barrera-Saldana H-A (1998) Growth hormone and placental lactogen: biology medicine and biotechnology. Gene 211:11–18

    Article  PubMed  CAS  Google Scholar 

  • Beardmore JA (1997) Transgenics: autotransgenics and allotransgenics. Transgenic Res 6:107–108

    Article  CAS  Google Scholar 

  • Beardmore J, Porter JS (2003) Genetically modified organisms and aquaculture. FAO Fisheries Circular No. 989. FAO, Rome

  • Ber R, Daniel V (1992) Structure and sequence of the growth hormone encoding gene from Tilapia nilotica. Gene 113:245–250

    Article  PubMed  CAS  Google Scholar 

  • Ber R, Daniel V (1993) Sequence analysis suggests a recent duplication of growth hormone encoding gene in Tilapia nilotica. Gene 125:143–150

    Article  PubMed  CAS  Google Scholar 

  • Bernardini SM, Argenton F, Vianello SM, Colombo LM, Borolussi MM (1999) Regulatory regions in the promoter and third intron of growth hormone gene in rainbow trout (Oncorhynchus mykiss) Walbaum. Gen Comp Endocrinol 116:261–271

    Article  PubMed  CAS  Google Scholar 

  • Brinster RL, Allen JM, Behringer RR, Gelinas RE, Palmiter RD (1988) Introns increase transcriptional efficiency in transgenic mice. Proc Natl Acad Sci USA 85:836–840

    Article  PubMed  CAS  Google Scholar 

  • Bucher P (1990) Weight matrix description of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J Mol Biol 212:563–578

    Article  PubMed  CAS  Google Scholar 

  • Chan KW, Devlin RH (1993) Polymerase chain reaction amplification and functional characterization of sockeye salmon histone H3, metallothionein-B, and protamine promoters. Mol Mar Biol Biotechnol 2:308–318

    PubMed  CAS  Google Scholar 

  • Chan YH, Cheng CHK, Chan KM (2003) Recombinant gold fish growth hormones (gfGH-I and II) expressed in Escherichia coli have similar biological activities. Comp Biochem Physiol A 135:613–624

    Article  CAS  Google Scholar 

  • Chao S, Pan F, Chang W (1989) Purification of carp growth hormone and cloning of the complementary DNA. Biochim Biophys Acta 1007:233–236

    PubMed  CAS  Google Scholar 

  • Chen Y-H, Thompson EB (1980) Genomic organization of rat prolactin and growth hormone genes. Proc Natl Acad Sci USA 77:4583–4587

    Article  Google Scholar 

  • Chen TT, Lin CM, Dunham RA, Powers DA (1992) Integration, expression and inheritance of foreign fish growth hormone gene in transgenic fish. In: Hew CL, Fletcher GL (eds) Transgenic fish. World Scientific, Singapore, pp 164–175

    Google Scholar 

  • Chen TT, Kight K, Lin CM, Powers DA, Hayat M, Chatakondi N, Ramboux AC, Duncan PL, Dunham RA (1993) Expression and inheritance of RSVLTR-rtGH1 complementary DNA in the transgenic common carp, Cyprinus carpio. Mol Mar Biol Biotechnol 2:88–95

    PubMed  CAS  Google Scholar 

  • Chen WY, Chen NY, Yun J, Wagner TE, Kopchick JJ (1994) In vitro and in vivo studies of antagonistic effects of human growth hormone analogs. J Biol Chem 269:15892–15897. Erratum in: J Biol Chem 269:20806

    Google Scholar 

  • Chiou CS, Chen H-T, Chang W-C (1990) The complete nucleotide sequence of the growth hormone gene from common carp (Cyprinus carpio). Biochim Biophys Acta 1087:91–94

    PubMed  CAS  Google Scholar 

  • Claveau D, Riendeau D, Mancini JA (2000) Expression, maturation and rhodamine-based fluorescence assay of human Cathepsin K expressed in CHO cells. Biochem Pharmacol 60:759–769

    Article  PubMed  CAS  Google Scholar 

  • Connor W, States JC, Mezquita J, Dixon GH (1984) Organization and nucleotide sequence of rainbow trout H2A and H3 genes. J Mol Evol 20:236–250

    Article  PubMed  CAS  Google Scholar 

  • Crenshaw EB, Kalla K, Simmons DM, Swanson LW, Rosenfeld MG (1989) Cell-specific expression of the prolactin gene in transgenic mice is controlled by synergistic interactions between promoter and enhancer elements. Genes Dev 3:959–972

    Article  PubMed  CAS  Google Scholar 

  • David L, Blum S, Feldman MW, Lavi U, Hillel J (2003) Recent duplication of the common carp (Cyprinus carpio L.) genome as revealed by analyses of microsatellite loci. Mol Biol Evol 20:1425–1434

    Article  PubMed  CAS  Google Scholar 

  • Devlin RH (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 Aquat Sci 50:1738–1748

    CAS  Google Scholar 

  • Devlin RH, Yesaki TY, Biagi CA, Donaldson EM, Swanson P, Chan W-K (1994) Extraordinary salmon growth. Nature 371:209–210

    Article  Google Scholar 

  • Devlin RH, Yesaki TY, Donaldson EM, Du SJ, Hew CL (1995) Production of germ line transgenic Pacific salmonids with dramatically increased growth performance. Can J Fish Aquat Sci 52:1376–1384

    Article  Google Scholar 

  • Devlin RH, Biagi CA, Yesaki TY (2004) Growth, viability and genetic characteristics of GH transgenic coho salmon strains. Aquaculture 236:607–632

    Article  CAS  Google Scholar 

  • Du SJ, Gong Z, Hew CL, Tan CH, Fletcher GL (1992a) Development of an all-fish gene cassette for gene transfer in aquaculture. Mol Mar Biol Biotechnol 1:290–300

    PubMed  CAS  Google Scholar 

  • Du SJ, Gong Z, Fletcher GL, Shears MA, King MJ, Idler DR, Hew CL (1992b) Growth enhancement in transgenic Atlantic salmon by the use of an “all fish” chimeric growth hormone gene construct. Bio/Technology 10:176–181

    Article  PubMed  CAS  Google Scholar 

  • Du SJ, Devlin RH, Hew CL (1993) Genomic structure of growth hormone gene in chinook salmon (Oncorhynchus tshawytscha): presence of two functional genes GH1 and GH2 and a male specific pseudogene, GH ψ. DNA Cell Biol 12:739–751

    PubMed  CAS  Google Scholar 

  • Dunham RA, Ramboux AC, Duncan PL, Hayat M, Chen TT, Lin CM, Kight K, Gonzalez-Villasenor LI, Powers DA (1992) Transfer expression and inheritance of salmonid growth hormone genes in channel cat fish, Ictalurus punctatus and effect on performance traits. Mol Mar Biol Biotechnol 1:380–389

    PubMed  CAS  Google Scholar 

  • Edwalds-Gilbert G, Veraldi KL, Milcarek C (1997) Alternative poly (A) site selection in complex transcription units: means to an end? Nucleic Acids Res 25:2547–2561

    Article  PubMed  CAS  Google Scholar 

  • Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13

    Article  PubMed  CAS  Google Scholar 

  • Fine M, Sakal E, Vashdi D, Daniel V, Lavanon A, Lipshitz O, Gertler A (1993) Recombinant carp growth hormone (Cyprinus carpio): expression, purification and determination of biological activity in vitro and in vivo. Gen Comp Endocrin 89:51–61

    Article  CAS  Google Scholar 

  • Fox SR, Jong MTC, Casanova J, Ye SF, Stanley F, Samuels HH (1990) The homeodomain protein, Pit-1/GHF-1 is capable of binding to and activating cell-specific elements of both the growth hormone and prolactin gene promoters. Mol Endocrinol 4:1069–1080

    PubMed  CAS  Google Scholar 

  • Friedenreich H, Schartl M (1990) Transient expression directed by homologous and heterologous promoter and enhancer sequences in fish cells. Nucleic Acids Res 18:3299–3305

    Article  PubMed  CAS  Google Scholar 

  • Fu C, Hu Y, Wang Y, Zhu Z (2005) Developments in transgenic fish in the people’s Republic of China. Rev Sci Tech Off Int Epiz 24:299–307

    CAS  Google Scholar 

  • García del Barco D, Martínez R, Hernández O, Lleonart R, De la Fuente J (1994) Differences in transient expression directed by heterologous promoter and enhancer sequences in fish cells and embryos. J Mar Biotechnol 1:203–205

    Google Scholar 

  • Gentry LE, Webb NR, Lim GJ, Brunner AM, Ranchalis JE, Twardzik DR, Lioubin MN, Marquardt H, Purchio AF (1987) Type 1 transforming growth factor beta: amplified expression and secretion of mature and precursor polypeptides in Chinese hamster ovary cells. Mol Cell Biol 7:3418–3427

    PubMed  CAS  Google Scholar 

  • Gong ZY, Vielkind JR, Hew CL (1991) Functional analysis of promotor regions from fish antifreeze protein genes in transgenic Japanese medaka embryos. Mol Mar Biol Biotechnol 1:64–72

    PubMed  CAS  Google Scholar 

  • Graham DE, Rechler MM, Brown AL, Frunzio R, Romanus JA, Bruni CB, Whitfield HJ, Nissley SP, Seeling S, Berry S (1986) Coordinate developmental regulation of high and low molecular weight mRNAs for rat insulin-like growth factor II. Proc Natl Acad Sci USA 83:4519–4523

    Article  PubMed  CAS  Google Scholar 

  • Grosveld F, van Assendelft GB, Greaves DR, Kollas G (1987) Position-independent, high-level expression of the human beta-globin gene in transgenic mice. Cell 24:975–985

    Article  Google Scholar 

  • Guyomard R, Chourrout D, Houdebin L (1989) Production of stable transgenic fish by cytoplasmic injection of purified genes. In: Beaudet AL, Mulligan R, Verma IM (eds) Gene transfer and gene therapy. Liss, New York, pp 9–18

    Google Scholar 

  • Hallerman EM, Kapuscinski AR (1995) Incorporating risk assessment and risk management into public policies of genetically modified finfish and shellfish. Aquaculture 137:9–17

    Article  Google Scholar 

  • Hanley S, Smith TJ, Muller F, Maclean N, Uzbekova S, Prunet P, Breton B (1998) Isolation and functional analysis of the histone (H3) promoter from Atlantic salmon (Salmo salar L). Mol Mar Biol Biotechnol 7:165–172

    PubMed  CAS  Google Scholar 

  • Hepler JE, Van Wyk JJ, Lund PK (1990) Different half-lives of insulin-like growth factor I mRNAs that differ in length of 3′ untranslated sequence. Endocrinology 127:1550–1552

    Article  PubMed  CAS  Google Scholar 

  • Ho WK, Tsang WH, Dias N (1989) Cloning of the grass carp growth hormone cDNA. Biochem Biophys Res Commun 161:1239–1243

    Article  PubMed  CAS  Google Scholar 

  • Ho WK, Wong MW, Chan AP (1991) Cloning and sequencing of the grass carp (Ctenopharyngodon idellus) growth hormone gene. Biochim Biophys Acta 1090:245–248

    PubMed  CAS  Google Scholar 

  • Hong Y, Schartl M, (1993) Sequence of growth hormone (GH) from silver carp (Hypophthalmicthys molitrix) and evolution of GH genes in vertebrates. Biochim Biophys Acta 1174:285–288

    PubMed  CAS  Google Scholar 

  • Ingraham HA, Chen R, Mangalam HJ, Selsholtz HP, Flyn SE, Lin CR, Simmons DM, Swanson L, Rosenfeld MG (1988) A tissue-specific transcription factor containing a homeo domain specifies a pituitary phenotype. Cell 55:519–529

    Article  PubMed  CAS  Google Scholar 

  • Ingraham HA, Flynn SE, Albert VR, Kapiloff MS, Wilson L, Rosenfeld MG (1990) The POU-specific domain of Pit-1 is essential for sequence-specific, high affinity DNA binding and DNA-independent Pit-1-Pit-1 interactions. Cell 61:1021–1033

    Article  PubMed  CAS  Google Scholar 

  • Israel DI, Nove J, Kerns KM, Moutsatsos IK, Kaufman RJ (1992) Expression and characterization of bone morphogenetic protein-2 in Chinese hamster ovary cells. Growth Factors 7:139–150

    Article  PubMed  CAS  Google Scholar 

  • Jackson RJ, Standart N (1990) Do the poly (A) tail and 3’ untranslated region control mRNA translation? Cell 62:15–24

    Article  PubMed  CAS  Google Scholar 

  • Jhingran VG (1975) Fish and fisheries of India. Hindustan Publ, India

    Google Scholar 

  • Johansen B, Johnsen OC, Valla S (1989) The complete nucleotide sequence of growth hormone gene from Atlantic salmon (Salmo salar). Gene 77:317–324

    Article  PubMed  CAS  Google Scholar 

  • Kapuscinski AR (2005) Current scientific understanding of the environmental biosafety of transgenic fish and shellfish. Rev Sci Tech Off Int Epiz 24:309–322

    CAS  Google Scholar 

  • Koren Y, Sarid S, Ber R, Daniel V (1989) Carp growth hormone: molecular cloning and sequencing of cDNA. Gene 77:309–315

    Article  PubMed  CAS  Google Scholar 

  • Kozak M (1987) Analyasis of 5′ non-coding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res 15:8125–8148

    Article  PubMed  CAS  Google Scholar 

  • Kozak M (1991) Structural features in eukaryotic mRNAs that modulate the initiation of translation. J Biol Chem 266:19867–19870

    PubMed  CAS  Google Scholar 

  • Lao H, Bai J, Ye X, Li Y, Lou J (2001) Molecular clone of Megalobrama hoffmanni GH cDNA. Unpublished. Gene bank accession #AF332563

  • Larhammar D, Risinger C (1994) Molecular genetic aspects of tetraploidy in the common carp, Cyprinus carpio. Mol Phylogenet Evol 3:59–68

    Article  PubMed  CAS  Google Scholar 

  • Law MS, Cheng KW, Fung TK, Chan YH, Yu KL, Chan KM (1996) Isolation and characterization of two distinct growth hormone cDNAs from the goldfish, Carassius auratus. Arch Biochem Biophys 330:19–23

    Article  PubMed  CAS  Google Scholar 

  • Levy JA, Marins LF, Sanchez A (2000) Gene transfer technology in aquaculture. Hydrobiologia 420:91–94

    Article  CAS  Google Scholar 

  • Lewis UJ, Singh RNP, Tutwiller GF, Sigel MB, Vanderlaan EF, Vanderlaan WP (1980) Human growth hormone: a complex of proteins. Rec Progr Horm Res 36:477–509

    PubMed  CAS  Google Scholar 

  • Lin C, Lin SC, Chang CP, Rosenfeld MG (1992) Pit-1 dependent expression of the receptor for growth hormone releasing factor mediates pituitary cell growth. Nature 360:765–768

    Article  PubMed  CAS  Google Scholar 

  • Lira SA, Crenshaw EB, Glass CK, Swanson LW, Rosenfeld MG (1988) Identification of rat growth hormone genomic sequences targeting pituitary expression in transgenic mice. Proc Natl Acad Sci USA 85:4755–4759

    Article  PubMed  CAS  Google Scholar 

  • Liu Z, Zhu Z, Roberg K, Faras AJ, Guise K, Kapuscinski A, Hackett PB (1989) The β-actin gene of carp (Ctenopharyngodon idella). Nuleic Acids Res 7:5850

    Article  Google Scholar 

  • Liu Z, Moav B, Faras AJ, Guise KS, Kapuscinski A, Hackett PB (1990) Functional analysis of elements affecting expression of the β-actin gene of carp. Mol Cell Biol 10:3432–3440

    PubMed  CAS  Google Scholar 

  • Logan JS, Falck-Pedersen E, Darnell JE, Shenk T (1987) A poly (A) addition site and a downstream termination region are required for efficient cessation of transcription by RNA polymerase II in the mouse major beta-globin gene. Proc Natl Acad Sci USA 84:8306–8310

    Article  PubMed  CAS  Google Scholar 

  • Lucas BK, Giere LM, DeMarco RA, Shen A, Chisholm V, Crowley CW (1996) High-level production of recombinant proteins in CHO cells using a dicistronic DHFR intron expression vector. Nucleic Acids Res 24:1774–1779

    Article  PubMed  CAS  Google Scholar 

  • Maclean N, Laight RJ (2000) Transgenic fish: an evaluation of benefits and risks. Fish Fisheries 1:146–172

    Article  Google Scholar 

  • Mahapatra KD, Meher PK, Saha JN, Gjerde B, Reddy PVGK, Jana RK, Sahoo M, Rye M (2000) Selection response of rohu, Labeo rohita, for two generations of selective breeding (abstract). In: Fifth Indian Fisheries Forum, CIFA, Bhubaneshwar

  • Majumdar KC, McAndrew BJ (1986) Relative DNA content of somatic nuclei and chromosomal studies in three genera, Tilapia. Sarotherodon and Oreochromis of the tribe Tilapinii (Pisces, Cichlidae). Genetica 68:175–188

    Article  Google Scholar 

  • Majumdar KC, Ravinder K, Nasaruddin K (1997) DNA fingerprinting in Indian major carps and tilapia by Bkm 2 (8) and M 13 probes. Aquacult Res 28:129–138

    Article  Google Scholar 

  • Male R, Nerland AH, Lorens JB, Telle W, Lossius I, Totland GK (1992) The complete nucleotide sequence of the Atlantic salmon growth hormone I gene. Biochim Biophys Acta 1130:345–348

    PubMed  CAS  Google Scholar 

  • Marchioli CC, Yancey RJ Jr, Petrovskis EA, Timmins JG, Post LE (1987) Evaluation of pseudorabies virus glycoprotein gp50 as a vaccine for Aujeszky’s disease in mice and swine: expression by vaccinia virus and Chinese hamster ovary cells. J Virol 61:3977–3982

    PubMed  CAS  Google Scholar 

  • Marshall RD (1972) Glycoproteins. Ann Rev Biochem 41:673–702

    Article  PubMed  CAS  Google Scholar 

  • Martinez R, Estrada MP, Berlanga J, Guillen I, Hernandez O, Cabera E, Pimentel R, Morales R, Herrera F, Morales A, Pina JC, Abad Z, Sanchez V, Melamed P, Lleonart R, de la Funte J (1996) Growth enhancement in transgenic tilapia by ectopic expression of tilapia growth hormone. Mol Mar Biol Biotechnol 5:62–70

    PubMed  CAS  Google Scholar 

  • McAndrew BJ, Majumdar KC (1983) Tilapia stock identification using electrophoretic markers. Aquaculture 30:249–261

    Article  CAS  Google Scholar 

  • Morgan JG, Courtois G, Fourel G, Chodosh LA, Campbell L, Evans E, Crabtree GR (1988) Sp1, a CAAT-binding factor, and the adenovirus major late promoter transcription factor interact with functional regions of the gamma-fibrinogen promoter. Mol Cell Biol 8:2628–2637

    PubMed  CAS  Google Scholar 

  • Muir WM (2004) The threats and benefits of GM fish. EMBO Rep 5:654–659

    Article  PubMed  CAS  Google Scholar 

  • Muir WM, Howard RD (2001) Fitness components and ecological risk of transgenic release: a model using Japanese medaka (Oryzias latipes). Am Nat 158:1–16

    Article  PubMed  CAS  Google Scholar 

  • Muller F, Williams DW, Kobolak J, Gauvry L, Goldspink G, Orban L, Maclean N (1997) Activator effect of coinjected enhancers on the muscle-specific expression of promoters in zebrafish embryos. Mol Reprod Dev 47:404–412

    Article  PubMed  CAS  Google Scholar 

  • Nam YK, Noh JK, Cho YS, Cho HJ, Cho K-N, Kim CG, Kim DS (2001) Dramatically accelerated growth and extraordinary gigantism of transgenic mud loach, Mizgurnus mizolepis. Transgenic Res 10:353–362

    Article  PubMed  CAS  Google Scholar 

  • Nelson C, Albert VR, Elsholtz HP, Lu LI-W, Rosenfeld MG (1988) Activation of cell-specific expression of rat growth hormone and prolactin genes by a common transcription factor. Science 239:1400–1405

    Article  PubMed  CAS  Google Scholar 

  • Nicoll CS, Steiny SS, King DS, Nishioka RS, Mayer GL, Eberhardt NL, Baxter JD, Yamanaka MK, Miller JA, Seilhamer JJ, Schilling JM, Johnson LK (1987) The primary structure of coho salmon growth hormone and its cDNA. Gen Comp Endocrinol 68:387–399

    Article  PubMed  CAS  Google Scholar 

  • Noh JK, Cho K-N, Han EH, Kim A, Lee J-S, Kim DS, Kim CG (2003) Genomic cloning of mud loach, Misgurnus mizolepis (Cypriniformes, Cobitidae) β-actin gene and usefulness of its promoter region for fish transgenesis. Mar Biotechnol 5:244–252

    Article  PubMed  CAS  Google Scholar 

  • Ohkubo T, Araki M, Tanaka M, Sudo S, Nakashima K (1996) Molecular cloning and characterization of the yellowtail GH gene and its promoter: a consensus sequence for teleost and avian Pit-1/GHF-1 binding sites. J Mol Endocrinol 16:63–72

    Article  PubMed  CAS  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer, New York

    Google Scholar 

  • Ohno S, Wolf U, Atkin NB (1968) Evolution from fish to mammals by gene duplication. Hereditas 59:169–187

    Article  PubMed  CAS  Google Scholar 

  • Paladini AC, Pena C, Edgardo E (1983) Molecular biology of growth hormone. CRC Crit Rev Biochem 15:25–26

    Article  PubMed  CAS  Google Scholar 

  • Palmiter RD, Brinster RL, Hammer RE, Trumbauer ME, Rosenfeld MG, Brinberg NC, Evance RM (1982) Dramatic growth of mice that develop from eggs microinjected with metallothionein-growth hormone fusion genes. Nature 300:611–615

    Article  PubMed  CAS  Google Scholar 

  • Pandian TJ, Marian LA (1994) Problems and prospects of transgenic fish production. Curr Sci 66:635–649

    Google Scholar 

  • Park JH, Kim C, Kim WB, Kim YK, Lee SY, Yang JM (2000) Efficiency of promoter and cell line in high-level expression of erythropoietin. Biotechnol Appl Biochem 32:167–172

    Article  PubMed  CAS  Google Scholar 

  • Patikoglou GA, Kim JL, Sun L, Yang SH, Kodadek T, Burley SK (1999) TATA element recognition by the TATA box-binding protein has been conserved throughout evolution. Genes Dev 13:3217–3230

    Article  PubMed  CAS  Google Scholar 

  • Peer YV, Yaylor JS, Meyer A (2003) Are all fishes ancient polyploids? J Struct Funct Genomics 2:65–73

    Article  Google Scholar 

  • Penman DJ, Iyengar A, Beeching AJ, Rahman A, Sulaiman Z, Maclean N (1991) Patterns of transgene inheritance in rainbow trout (Oncorhynchus mykiss). Mol Reprod Dev 30:201–206

    Article  PubMed  CAS  Google Scholar 

  • Peyush P, Moriyama S, Takahashi A, Kawauchi H (2000) Molecular cloning of Growth hormone complementary DNA in barfin flounder (Verasper moseri). Mar Biotechnol 2:21–26

    PubMed  CAS  Google Scholar 

  • Pitkanen TI, Krasnov A, Teerijoki H, Molsa H (1999) Transfer of growth hormone (GH) transgenes into Arctic charr (Salvelinus alpinus L.) I. Growth response to various GH constructs. Genetic Anal 15:91–98

    CAS  Google Scholar 

  • Proudfoot NJ (1991) Poly (A) signals. Cell 64:671–674

    Article  PubMed  CAS  Google Scholar 

  • Proudfoot NJ, Brownlee GG (1976) 3′ Non-coding region sequences in eukaryotic messenger RNA. Nature 263:211–214

    Article  PubMed  CAS  Google Scholar 

  • Rahman MA, Hwang GL, Razak SA, Sohm F, Maclean N (2000) Copy number related transgene expression and mosaic somatic expression in hemizygous and homozygous transgenic tilapia (Oreochromis niloticus). Transgenic Res 9:417–427

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen RS, Morrissey MT (2007) Biotechnology in aquaculture: transgenic and polyploidy. Compr Rev Food Sci Food Safe 6:2–16

    Article  CAS  Google Scholar 

  • Ravinder K, Nasaruddin K, Majumdar KC, Shivaji S (1997) Computerized analysis of motility, motility patterns and motility parameters of spermatozoa of carp following short-term storage of semen. J Fish Biol 50:1309–1328

    Article  Google Scholar 

  • Reddy PVGK, Gjerde B, Tripathi SD, Jana RK, Mahapatra KD, Gupta SD, Saha JN, Sahoo M, Lenka S, Govindassamy P, Rye M, Gjedrem T (2002) Growth and survival of six stocks of rohu, Labeo rohita Hamilton in mono and polyculture production systems. Aquaculture 203:239–250

    Article  Google Scholar 

  • Rentier-Delrue F, Swennen D, Mercier L, Lion M, Benrubi O, Martial JA (1989a) Molecular cloning and characterization of two forms of trout growth hormone cDNA: expression and secretion of tGH-II by Escherichia coli. DNA 8:109–117

    PubMed  CAS  Google Scholar 

  • Rentier-Delrue F, Swennen D, Philippart JC, L’Hoir C, Lion M, Benrubi O, Martial JA (1989b) Tilapia growth hormone: molecular cloning of cDNA and expression in Escherichia coli. DNA 8:271–278

    PubMed  CAS  Google Scholar 

  • Roychoudhury R, Jay E, Wu R (1976) Terminal labeling and addition of homopolymer tracts to duplex DNA fragments by terminal deoxynucleotidyl transferase. Nucleic Acids Res 3:101–116

    PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning—a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    Article  PubMed  CAS  Google Scholar 

  • Scully KM, Jacobson EM, Jepsen K, Lunyak V, Viadiu H, Carriere C, Rose DW, Hooshmand F, Aggarwal AK, Rosenfeld MG (2000) Allosteric effects of Pit 1 DNA sites on long-term repression in cell type specification. Science 290:1127–1131

    Article  PubMed  CAS  Google Scholar 

  • Sekkali B, Brim H, Muller M, Argenton F, Bortolussi M, Colombo L, Belayew A, Martial JA (1999) Structure and functional analysis of a tilapia (Oreochromis mossambicus) growth hormone gene: activation and repression by pituitary transcription factor Pit 1. DNA Cell Biol 18:489–502

    Article  PubMed  CAS  Google Scholar 

  • Sekine S, Mizukami T, Nishi T, Kuwana Y, Saito A, Sato M, Itoh S, Kawauchi H (1985) Cloning and expression of cDNA for salmon growth hormone in E. coli. Proc Natl Acad Sci USA 82:4306–4310

    Article  PubMed  CAS  Google Scholar 

  • Sekine S, Mizukami T, Saito A, Kawauchi H, Itoh S (1989) Isolation and characterization of a novel growth hormone cDNA from chum salmon (Oncorhynchus keta). Biochim Biophys Acta 1009:117–120

    PubMed  CAS  Google Scholar 

  • Shears MA, Fletcher GL, Hew CL, Gauthier S, Davies PL (1991) Transfer, expression and stable inheritance of antifreeze protein genes in Atlantic salmon, Salmo salar. Mol Mar Biol Biotechnol 1:58–63

    CAS  Google Scholar 

  • Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517

    Article  PubMed  CAS  Google Scholar 

  • Spellman MW, Leonard CK, Basa LJ, Gelineo I, Halbeek H (1991) Carbohydrate structures of recombinant soluble human CD4 expressed in Chinese hamster ovary cells. Biochemistry 30:2395–2406

    Article  PubMed  CAS  Google Scholar 

  • Takagi S, Sasado T, Tamiya G, Ozato K, Wakamatsu Y, Takeshita A, Kimura M (1994) An efficient expression vector for transgenic medaka construction. Mol Mar Biol Biotechnol 3:192–199

    PubMed  CAS  Google Scholar 

  • Tanaka M, Toma Y, Ohkubo T, Sudo S, Nakashima K (1995) Sequence of the flounder growth hormone encoding gene and its promoter region. Gene 165:321–322

    Article  PubMed  CAS  Google Scholar 

  • Tang Y, Lin CM, Chen TT, Kawauchi H, Dunham RA, Powers DA (1993) Structure of channel cat fish (Ictalurus punctatus) growth hormone gene and its evolutionary implications. Mol Mar Biol Biotechnol 2:198–206

    PubMed  CAS  Google Scholar 

  • Uyeno T, Smith GR (1972) Tetraploid origin of the karyotype of catostomid fishes. Science 175:644–646

    Article  PubMed  CAS  Google Scholar 

  • Venkatesh B, Brenner S (1997) Genomic structure and sequence of the puffer fish (Fugu rubripes) growth hormone-encoding gene: a comparative analysis of teleost growth hormone genes. Gene 187:211–215

    Article  PubMed  CAS  Google Scholar 

  • Venugopal T, Anathy V, Pandian TJ, Gong GZ, Mathavan S (2002a) Molecular cloning of growth hormone-encoding cDNA of an Indian major carp, Labeo rohita, and its expression in Escherichia coli and Zebrafish. Gen Comp Endocrinol 125:236–247

    Article  PubMed  CAS  Google Scholar 

  • Venugopal T, Mathavan S, Pandian TJ (2002b) Molecular cloning of growth hormone encoding cDNA of Indian major carps by a modified rapid amplification of cDNA ends strategy. J Biosci 27:261–272

    Article  PubMed  CAS  Google Scholar 

  • Warner TG (1999) Enhancing therapeutic glycoprotein production in Chinese hamster ovary cells by metabolic engineering endogenous gene control with antisense DNA and gene targeting. Glycobiology 9:841–850

    Article  PubMed  CAS  Google Scholar 

  • Wang R, Zhang P, Gong Z, Hew CL (1995) Expression of the antifreeze protein gene in transgenic goldfish (Carassius auratus) and its implication in cold adaptation. Mol Mar Biol Biotechnol 4:20–26

    PubMed  CAS  Google Scholar 

  • Watahiki M, Yamamoto M, Yamakawa M, Tanala M, Nakashima K (1989) Conserved and unique amino acid residues in the domains of the growth hormones. J Biol Chem 264:312–316

    PubMed  CAS  Google Scholar 

  • Watanabe K, Igarashi A, Noso T, Chen TT, Dunham RA, Kawauchi H (1992) Chemical identification of catfish growth hormone and prolactin. Mol Mar Biol Biotechnol 1:239–249

    PubMed  CAS  Google Scholar 

  • Webster J, Donofrio G, Wallace R, Clark AJ, Whitelaw CB (1997) Intronic sequences modulate the sensitivity of beta-lactoglobulin transgenes to position effects. Gene 193:239–243

    Article  PubMed  CAS  Google Scholar 

  • Whitelaw CB, Archibald AL, Harris S, McClenaghan M, Simons JP, Clark AJ (1991) Targeting expression to the mammary gland: intronic sequences can enhance the efficiency of gene expression in transgenic mice. Transgenic Res 1:3–13

    Article  PubMed  CAS  Google Scholar 

  • Williams DW, Muller F, Lavender FL, Orban L, Maclean N (1996) High transgene activity in the yolk syncytial layer affects quantitative transient expression assays in zebrafish (Danio rerio) embryos. Transgenic Res 5:433–442

    Article  PubMed  CAS  Google Scholar 

  • Winkler C, Vielkind JR, Schartl M (1991) Transient expression of foreign DNA during embryonic and larval development of the medaka fish (Oryzias latipes). Mol Gen Genet 226:129–140

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Sun Y, Zhu Z (2003) Growth hormone gene transfer in common carp. Aquat Living Resour 16:416–420

    Article  Google Scholar 

  • Yamada S, Hata J, 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

    PubMed  CAS  Google Scholar 

  • Yang BY, Greene M, Chen TT (1999) Early embryonic expression of the growth hormone family protein genes in the developing rainbow trout, Oncorhynchus mykiss. Mol Reprod Dev 53:127–134

    Article  PubMed  CAS  Google Scholar 

  • Yowe DL, Epping RJ (1995) Cloning of the barramundi growth hormone-encoding gene: a comparative analysis of higher and lower vertebrate GH genes. Gene 162:255–259

    Article  PubMed  CAS  Google Scholar 

  • Zhang P, Hayat M, Joyce C, Gonzalez-Villasenor LI, Lin CM, Dunham RA, Chen TT, Powers DA (1990) Gene transfer, expression and inheritance of pRSV-rainbow trout-GH cDNA in the common carp, Cyprinus carpio (Linnaeus). Mol Reprod Dev 25:3–13

    Article  PubMed  CAS  Google Scholar 

  • Zhu Z, Li G, He L, Chen S (1985) Novel gene transfer into the fertilized eggs of goldfish (Carassius auratus L. 1758). Z Angew Ichthyol 1:31–34

    Article  CAS  Google Scholar 

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Acknowledgements

We are indebted to Dr. L. Singh, Director, CCMB for his constant support; Dr. S.K. Rath for the initial experiments on library construction and screening; Dr. B. Venkatesh, Institute of Molecular Cell Biology, Singapore for providing GH cDNA of goldfish; Dr. Shashi Singh and Mr. Parthasarathy for CHO cell transfection; Dr. K. Uma Devi for correcting; Mr. M. Ranga Rao for typing the manuscript. Thanks are due to two anonymous reviewers for their suggestions. Financial support by the University Grants Commission and the Council of Scientific and Industrial Research, Government of India for a fellowship to RR and the Department of Biotechnology, Government of India for a grant (BT/AA/03/70(A)/94) to KCM is gratefully acknowledged.

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  1. Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad, 500 007, India

    R. Rajesh & K. C. Majumdar

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  1. R. Rajesh
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  2. K. C. Majumdar
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Correspondence to K. C. Majumdar.

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Rajesh, R., Majumdar, K.C. The growth hormone-encoding gene isolated and characterized from Labeo rohita Hamilton is expressed in CHO cells under the control of constitutive promoters in ‘autotransgene’ constructs. Fish Physiol Biochem 34, 413–436 (2008). https://doi.org/10.1007/s10695-008-9201-x

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  • DOI: https://doi.org/10.1007/s10695-008-9201-x

Keywords

  • Autotransgene
  • CHO cells
  • Growth hormone gene
  • Heterologous expression
  • Labeo rohita

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