Abstract
Translationally controlled tumor protein (TCTP) is an important immune regulator that has been implicated in a number of cellular processes, including cell growth, cell cycle progression, apoptosis regulation and protection of cells against various environmental stresses. In this study, we cloned and characterised TCTP from rock bream (Oplegnathus fasciatus), which is an economically important species in the Korean aquaculture industry. The full-length rock bream TCTP (RbTCTP) cDNA was of 1,041 bp and contained an open reading frame of 513 bp, which encoded 170 amino acids. The 5′ untranslated region (UTR) was 90 bp, while the 3′ UTR was 438 bp, containing a polyadenylation signal. RbTCTP showed 76, 75 and 74 % amino acid sequence identities to those of tilapia (Oreochromis niloticus), orange-spotted grouper (Epinephelus coioides) and Japanese sea perch (Lateolabrax japonicus), respectively. The positions of microtubule binding region, Ca+ binding region and TCTP signature regions in RbTCTP were similar to other fish species and mammals. RbTCTP mRNA expression level was highest in the gill compared to other tissues. The level of RbTCTP mRNA expression was significantly regulated by injection of red seabream iridovirus, Streptococcus iniae and Edwardsiella tarda.
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Benndorf R, Nurnberg P, Bielka H (1988) Growth phase-dependent proteins of the Ehrlich ascites tumor analyzed by one- and two- dimensional electrophoresis. Exp Cell Res 174:130–138
Bheekha-Escura R, MacGlashan DW, Langdon JM, MacDonald SM (2000) Human recombinant histamine-releasing factor activates human eosinophils and the eosinophilic cell line, AML14-3D10. Blood 96:2191–2198
Bommer UA, Thiele BJ (2004) The translationally controlled tumour protein (TCTP). Int J Biochem Cell B 36:379–385
Bommer UA, Borovjagin AV, Greagg MA, Jeffrey IW, Russell P, Laing KG (2002) The mRNA of the translationally controlled tumour protein P23/TCTP is a highly structured RNA, which activates the dsRNA-dependent protein kinase PKR. RNA 8:478–496
Bonnet C, Perret E, Dumont X, Picard A, Caput D, Lenaers G (2000) Identification and transcription control of fission yeast genes repressed by an ammonium starvation growth arrest. Yeast 16:23–33
Caipang CM, Hirono I, Aoki T (2003) Development of a real-time PCR assay for the detection and quantification of red seabream iridovirus (RSIV). Fish Pathol 38:1–7
Campos-Perez JJ, Ward M, Grabowski PS, Ellis AE, Secombes CJ (2000) The gills are an important site of iNOS expression in rainbow trout Oncorhynchus mykiss after challenge with the Gram-positive pathogen Renibacterium salmoninarum. Immunology 99:153–161
Chang CI, Zhang YA, Zou J, Nie P, Secombes CJ (2006) Two cathelicidin genes are present in both rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Antimicrob Agents Chemother 50:185–195
Chung S, Kim M, Choi W, Chung J, Lee K (2000) Expression of translationally controlled tumor protein mRNA in human colon cancer. Cancer Lett 156:185–190
Dong WR, Xiang LX, Shao JZ (2007) Cloning and characterisaion of two natural killer enhancing factor genes (NKEF-A and NKEF-B) in pufferfish, Tetraodon nigroviridis. Fish Shellfish Immunol 22:1–15
dos Santos NM, Taverne-Thiele JJ, Barnes AC, van Muiswinkel WB, Ellis AE, Rombout JHWM (2001) The gill is a major organ for antibody secreting cell production following direct immersion of sea bass (Dicentrarchus labrax, L.) in a Photobacterium damselae ssp piscicida bacterin: an ontogenetic study. Fish Shellfish Immunol 11:65–74
Douglas SE, Knickle LC, Kimball J, Reith ME (2007) Comprehensive EST analysis of Atlantic halibut (Hippoglossus hippoglossus), a commercially relevant aquaculture species. BMC Genom 8:144
Gachet Y, Tournier S, Lee M, Lazaris-Karatzas A, Poulton T, Bommer UA (1999) The growth-related, translationally controlled protein P23 has properties of a tubulin binding protein and associates transiently with microtubules during the cell cycle. J Cell Sci 112:1257–1271
Gnanasekar M, Ramaswamy K (2007) Translationally controlled tumor protein of Brugia malayi functions as an antioxidant protein. Parasitol Res 101:1533–1540
Iijima N, Tanimoto N, Emoto Y, Morita Y, Uematsu K, Murakami T, Nakai T (2003) Purification and characterization of three isoforms of chrysophsin, a novel antimicrobial peptide in the gills of the red sea bream, Chrysophrys major. Eur J Biochem 270:675–686
Jung SJ, Oh MJ (2000) Iridovirus-like infection associated with high mortalities of striped beakperch, Oplegnathus fasciatus (Temminck et Schlegel) in southern coastal areas of the Korean peninsula. J Fish Dis 23:223–226
Kang HS, Lee MJ, Song H, Han SH, Kim YM, Im JY, Choi I (2001) Molecular identification of IgE-dependent histamine-releasing factor as a B cell growth factor. J Immunol 166:6545–6554
Kim JW, Kwon MG, Park MA, Hwang JY, Park HJ, Baeck GW (2010) Molecular cloning and expression analysis of an interferon stimulated gene 15 from rock bream Oplegnathus fasciatus. J Fish pathol 23:177–187
Koziol MJ, Gurdon JB (2012) TCTP in development and cancer. Biochem Res Int 2012:105203
Li F, Zhang D, Fujise K (2001) Characterization of fortilin, a novel antiapoptotic protein. J Biol Chem 276:47542–47549
Li C, Qiu L, Ning X, Chen A, Qin S, Wu H, Zhao J (2010) The first molluscan TCTP in Venerupis philippinarum: molecular cloning and expression analysis. Fish Shellfish Immunol 29(3):530–533
Lichtenfels AJ, Lorenzi-Filho G, Guimaraes ET, Macchione M, Saldiva PH (1996) Effects of water pollution on the gill apparatus of fish. J Comp Pathol 115:47–60
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
MacDonald SM, Bhisutthibhan J, Shapiro TA, Rogerson SJ, Taylor TE, Tembo M, Langdon JM, Meshnick SR (2001) Immune mimicry in malaria: plasmodium falciparum secretes a functional histamine-releasing factor homolog in vitro and in vivo. Proc Natl Acad Sci USA 98:10829–10832
Maier VH, Dorn KV, Gudmundsdottir BK, Gudmundsson GH (2008) Characterisation of cathelicidin gene family members in divergent fish species. Mol Immunol 45:3723–3730
Morrison RN, Cooper GA, Koop BF, Rise ML, Bridle AR, Adams MB, Nowak BF (2006) Transcriptome profiling the gills of amoebic gill disease (AGD)-affected Atlantic salmon (Salmo salar L.): a role for tumor suppressor p53 in AGD pathogenesis? Physiol Genomics 26:15–34
Oikawa K, Ohbayashi T, Mimura J, Fujii-Kuriyama Y, Teshima S, Rokutan K, Mukai K, Kuroda M (2002) Dioxin stimulates synthesis and secretion of IgE-dependent histamine-releasing factor. Biochem Biophys Res Commun 290:984–987
Park CI, Kurobe T, Hirono I, Aoki T (2003) Cloning and characterization of cDNA for two distinct tumor necrosis factor receptor genes from Japanese flounder Paralichthys olivaceus. Dev Comp Immunol 27:365–375
Rho SB, Lee JH, Park MS, Byun HJ, Kang S, Seo SS, Kim JY, Park SY (2011) Anti-apoptotic protein TCTP controls the stability of the tumor suppressor p53. FEBS Lett 585(1):29–35
Rinnerthaler M, Jarolim S, Heeren G, Palle E, Perju S, Klinger H, Bogengruber E, Madeo F, Braun RJ, Breitenbach-Koller L, Breitenbach M, Laun P (2006) MMI1 (YKL056c, TMA19), the yeast orthologue of the translationally controlled tumor protein (TCTP) has apoptotic functions and interacts with both microtubules and mitochondria. Biochim Biophys Acta 1757:631–638
Sohn SG, Choi DL, Do JW, Hwang GY, Park JW (2000) Mass mortalities of cultured striped beakperch, Oplegnathus fasciatus by iridoviral infection. J Fish pathol 13:121–127
Sturzenbaum SR, Kille P, Morgan AJ (1998) Identification of heavy metal induced changes in the expressopn patterns of the translationally controlled tumour protein (TCTP) in the earthworm Lumbricus rubellus. Biochim Biophys Acta 1398:294–304
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Thiele H, Berger M, Skalweit A, Thiele BJ (2000) Expression of the gene and processed pseudogenes encoding the human and rabbit translationally controlled tumor protein (TCTP). Eur J Biochem 267:5473–5481
Tuynder M, Fiucci G, Prieur S, Lespagnol A, Geant A, Beaucourt S, Duflaut D, Besse S, Susini L, Cavarelli J, Moras D, Amson R, Telerman A (2004) Translationally controlled tumor protein is a target of tumor reversion. Proc Natl Acad Sci USA 101:15364–15369
Uenobe M, Kohchi C, Yoshioka N, Yuasa A, Inagawa H, Morii K, Nishizawa T, Takahashi Y, Soma GI (2007) Cloning and characterization of a TNF-like protein of Plecoglossus altivelis (ayu fish). Mol Immunol 44(6):1115–1122
Venugopal T (2005) Evolution and expression of translationally controlled tumour protein (TCTP) of fish. Comp Biochem Phys B 142:8–17
Wang SA, Zhao XF, Wang JX (2009) Molecular cloning and characterization of the translationally controlled tumor protein from Fenneropenaeus chinensis. Mol Biol Rep 36:1683–1693
Wei J, Guo M, Ji H, Yan Y, Ouyang Z, Huang X, Hang Y, Qin Q (2012) Grouper translationally controlled tumor protein prevents cell death and inhibits the replication of Singapore grouper iridovirus (SGIV). Fish Shellfish Immunol 33:916–925
Xu A, Bellamy AR, Taylor JA (1999) Expressoin of translationally controlled tumour protein is regulated by calcium at both the transcriptional and post-transcriptional level. J Biochem 342:683–689
Yang Y, Yang F, Xiong ZY, Yan Y, Wang XM, Nishino M, Mirkovic D, Nguyen J, Wang H, Yang XF (2005) An N-terminal region of translationally controlled tumor protein is required for its antiapoptotic activity. Oncogene 24:4778–4788
Yenofsky R, Bergmann I, Brawerman G (1982) Messenger RNA species partially in a repressed state in mouse sarcoma ascites cells. Proc Natl Acad Sci USA 79:5876–5880
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This work was supported by grants from the National Fisheries Research and Development Institute (NFRDI) in Korea (RP-2013-BT-095).
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All authors declared that there is no conflict of interest.
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Chae, Y.S., Lee, JH., Shim, W.J. et al. Molecular cloning, characterisation and expression of the translationally controlled tumor protein gene in rock bream (Oplegnathus fasciatus). Genes Genom 36, 565–572 (2014). https://doi.org/10.1007/s13258-014-0192-y
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DOI: https://doi.org/10.1007/s13258-014-0192-y