The expression of hypoxia-inducible factor-1α gene is not affected by low-oxygen conditions in yellow perch (Perca flavescens) juveniles
Tóm tắt
Hypoxia can affect various fish populations, including yellow perch Perca flavescens, which is an economically and ecologically important species in Lake Erie, a freshwater system that often experiences hypoxia in the hypolimnetic part of the lake. Fish, similarly to mammals, possess molecular oxygen sensor—hypoxia-inducible factor-1 (HIF-1), a transcription factor that can affect expression of many downstream genes related to animal growth and locomotion, protein synthesis, as well as ATP and amino acid metabolism. HIF-1 is a heterodimer, which consists of two subunits: oxygen-sensitive and oxygen-insensitive subunits, α and β, respectively. In this study, we report first on the molecular cloning and sequencing of P. flavescens HIF-1α. The full-length complementary DNA (cDNA) was isolated and submitted to the GenBank with accession number KT783483. It consists of 3529 base pairs (bp) carrying a single open-reading frame that encompasses 2250 bp of the coding region, 247 bp of the 5′ untranslated region (UTR), and 1032 bp of the 3′ UTR. The “de novo” prediction of the 3D structure of HIF-1α protein, which consists of 749 amino acids, is presented, too. We then utilized One-Step Taqman® real-time RT-PCR technology to monitor changes in HIF-1α messenger RNA (mRNA) copies in response to chronic hypoxic stress. An experiment was conducted using 14-day post-swim-up stage yellow perch larvae with uninflated swim bladders. This experiment included three treatment groups: hypoxia, mid-hypoxia, and normoxia, in four replicates (four tanks per treatment) with the following dissolved oxygen levels: 3, 4, and >7 mg O2/L, respectively. At the end (2 weeks) and in the middle (1 week) of the experiment, fish from each tank were sampled for body measurements and molecular biology analysis. The results showed no differences in survival (∼90%) between treatment groups. Oxygen concentration was lowered to 3.02 ± 0.15 (mean ± SE) mg O2/L with no adverse effect on fish survival. The highest growth rate was observed in the normoxic group. A similar trend was observed with fish body length. The growth rate of fish declined with decreasing water-dissolved oxygen. The number of HIF-1α mRNA copies was not significantly different between hypoxic, mid-hypoxic, and normoxic conditions, and this was true for fish obtained in the middle and at the end of the experiment.
Tài liệu tham khảo
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 http://blast.ncbi.nlm.nih.gov/Blast.cgi
Altschul SF, Wootton JC, Gertz EM, Agarwala R, Morgulis A, Schäffer AA, Yu Y-K (2005) Protein database searches using compositionally adjusted substitution matrices. FEBS J 272:5101–5109 http://blast.ncbi.nlm.nih.gov/Blast.cgi
Arend KK, Beletsky D, Depinto JV, Ludsin SA, Roberts JJ, Rucinski DK, Scavia D, Schwab DJ, Höök TO (2011) Seasonal and interannual effects of hypoxia on fish habitat quality in Central Lake Erie. Freshw Biol 56(2):366–383
Bae SH, Jeong JW, Park JA, Kim SH, Bae MK, Choi SJ, Kim KW (2004) Sumoylation increases HIF-1alpha stability and its transcriptional activity. Biochem Bioph Res Co 324(1):394–400
Card PB, Erbel PJ, Gardner KH (2005) Structural basis of ARNT PAS-B dimerization: use of a common beta-sheet interface for hetero- and homodimerization. J Mol Biol 53(3):664–677
Cardoso R, Love R, Nilsson CL, Bergqvist S, Nowlin D, Yan J, Liu KK, Zhu J, Chen P, Deng YL, Dyson HJ, Greig MJ, Brooun A (2012) Identification of Cys255 in HIF-1α as a novel site for development of covalent inhibitors of HIF-1α/ARNT PasB domain protein-protein interaction. Protein Sci 21(12):1885–1896
Carlson AR, Blocher J, Herman LJ (1980) Growth and survival of channel catfish and yellow perch exposed to lowered constant and diurnally fluctuating dissolved oxygen concentrations. Progr Fish Cult 42:73–78
Chen N, Chen LP, Zhang J, Chen C, Wei XL, Gul Y, Wang WM, Wang HL (2012) Molecular characterization and expression analysis of three hypoxia-inducible factor alpha subunits, HIF-1 alpha/2 alpha/3 alpha of the hypoxia-sensitive freshwater species, Chinese sucker. Gene 498(1):81–90
Cheng J, Kang X, Zhang S, Yeh ET (2007) SUMO-specific protease 1 is essential for stabilization of HIF1alpha during hypoxia. Cell 131(3):584–595
Cioffi CL, Liu XQ, Kosinski PA, Garay M, Bowen BR (2003) Differential regulation of HIF-1 alpha prolyl-4-hydroxylase genes by hypoxia in human cardiovascular cells. Biochem Biophys Res Commun 303(3):947–953
Dames SA, Martinez-Yamout M, De Guzman RN, Dyson HJ, Wright PE (2002) Structural basis for HIF-1 alpha /CBP recognition in the cellular hypoxic response. Proc Natl Acad Sci U S A 99(8):5271–5276
Erbel PJ, Card PB, Karakuzu O, Bruick RK, Gardner KH (2003) Structural basis for PAS domain heterodimerization in the basic helix-loop-helix-PAS transcription factor hypoxia-inducible factor. Proc Natl Acad Sci U S A 100(26):15504–155509
Gassmann M, Chilov D, Wenger RH (2002) Regulation of the hypoxia-inducible factor-1α. ARNT is not necessary for hypoxic induction of HIF-1α in the nucleus. In: Lahiri S, Prabhakar NR, Forster REII (eds) Oxygen sensing: molecule to man, Series: Advances in Experimental Medicine and Biology, vol 475. Springer US, Philadelphia, pp 87–99
Gracey AY, Troll JV, Somero GN (2001) Hypoxia-induced gene expression profiling in the euryoxic fish Gillichthys mirabilis. Proc Natl Acad Sci U S A 98:1993–1998
Grasset J, Bougas B, Campbell PGC, Bernattchez L, Couture P (2014) Temperature, oxygen, and diet modulate gene transcription and metabolic capacities in yellow perch. Can J Fish Aquatic Sci 71:1635–1641
Gupta R (2001) Prediction of glycosylation sites in proteomes: from post-translational modifications to protein function. Ph.D. thesis at CBS. http://www.cbs.dtu.dk/services/YinOYang/
Gupta R, Brunak S (2002) Prediction of glycosylation across the human proteome and the correlation to protein function. Pac Symp Biocomput 7:310–322 http://www.cbs.dtu.dk/services/YinOYang/
Hart GW, Housley MP, Slawson C (2007) Cycling of O-linked -N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446:1017–1022
Huang LE, Gu J, Schau M, Bunn HF (1998) Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci U S A 95(14):7987–7992
Kajimura S, Aida K, Duan C (2006) Understanding hypoxia-induced gene expression in early development: in vitro and in vivo analysis of hypoxia-inducible factor 1-regulated zebra fish insulin-like growth factor binding protein 1 gene expression. Mol Cell Biol 26(3):1142–1155
Kang X, Li J, Zou Y, Yi J, Zhang H, Cao M, Yeh ET, Cheng J (2010) PIASy stimulates HIF1α SUMOylation and negatively regulates HIF1α activity in response to hypoxia. Oncogene 29(41):5568–5578
Kwasek K, Terova G, Wojno M, Dabrowski K, Wick M (2012) The effect of the dipeptide, Lys-Gly, supplement on growth, muscle proteins and PEPT1 gene expression in juvenile yellow perch. Rev Fish Biol Fisher 22:797–812
La Cour T, Kiemer L, Mølgaard A, Gupta R, Skriver K, Brunak S (2004) Analysis and prediction of leucine-rich nuclear export signals. Protein Eng Des Sel 17(6):527–536 http://www.cbs.dtu.dk/services/NetNES/
Law SHW, Wu RSS, Ng PKS, Yu RMK, Kong RYC (2006) Cloning and expression analysis of two distinct HIF-alpha isoforms--gcHIF-1alpha and gcHIF-4alpha--from the hypoxia-tolerant grass carp, Ctenopharyngodon idellus. BMC Mol Biol 7:15
Lin Q, Cong X, Yun Z (2011) Differential hypoxic regulation of hypoxia-inducible factors 1 α and 2 α. Mol Cancer Res 9:757–765
Mitchell A, Chang HY, Daugherty L, Fraser M, Hunter S, Lopez R, McAnulla C, McMenamin C, Nuka G, Pesseat S, Sangrador-Vegas A, Scheremetjew M, Rato C, Yong SY, Bateman A, Punta M, Attwood TK, Sigrist CJ, Redaschi N, Rivoire C, Xenarios I, Kahn D, Guyot D, Bork P, Letunic I, Gough J, Oates M, Haft D, Huang H, Natale DA, Wu CH, Orengo C, Sillitoe I, Mi H, Thomas PD, Finn RD (2015) The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res 43:D213–D221
Parker AD, Cooper MJ, Ruetz CR III, Coulter DP, Uzarski DG (2012) Chemical and physical factors associated with yellow perch abundance in Great Lakes coastal wetlands: patterns within and among wetland types. Wetl Ecol Manag 20:137–150
Pescador N, Villar D, Cifuentes D, Garcia-Rocha M, Ortiz-Barahona A, Vazquez S, Ordoñez A, Cuevas Y, Saez-Morales D, Garcia-Bermejo ML, Landazuri MO, Guinovart J, del Peso L (2010) Hypoxia promotes glycogen accumulation through hypoxia inducible factor (HIF)-mediated induction of glycogen synthase 1. PLoS One 5(3):e9644
Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF chimera—a visualization system for exploratory research and analysis. J Comput Chem 25(13):1605–1612 http://www.cgl.ucsf.edu/chimera/index.html
Pichavant K, Person-Le-Ruyet J, Le Bayon N, Severe A, Le Roux A, Boeuf G (2001) Comparative effects of long-term hypoxia on growth, feeding and oxygen consumption in juvenile turbot and European sea bass. J Fish Biol 59:875–883
Pugh CW, O’Rourke JF, Nagao M, Gleadle JM, Ratcliffe PJ (1997) Activation of hypoxia-inducible factor-1; definition of regulatory domains within the α subunit. J Biol Chem 272(17):11205–11214
Qi ZT, Wang ZS, Zhang QH, Huang B, Zhao WH, Qiu M, Peng JQ (2013) Molecular cloning and expression analysis of hypoxia inducible factor 1α in tongue sole, Cynoglossus semilaevis (Actinopterygii: Pleuronectiformes: Cynoglossidae), subjected to acute hypoxia. AIEP 43(3):201–209
Rahman MS, Thomas P (2007) Molecular cloning, characterization and expression of two hypoxia-inducible factor alpha subunits, HIF-1α and HIF-2α, in a hypoxia-tolerant marine teleost, Atlantic croaker (Micropogonias undulatus). Gene 396(2):273–282
Ren J, Gao X, Jin C, Zhu M, Wang X, Shaw A, Wen L, Yao X, Xue Y (2009) Systematic study of protein sumoylation: development of a site-specific predictor of SUMOsp 2.0. Proteomics 9:3409–3412 http://sumosp.biocuckoo.org/online.php
Richard DE, Berra E, Gothié E, Roux D, Pouysségur J (1999) p42/p44 mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1alpha (HIF-1alpha) and enhance the transcriptional activity of HIF-1. J Biol Chem 274(46):32631–32637
Rimoldi S, Terova G, Ceccuzzi P, Marelli S, Antonini M, Saroglia M (2012) HIF-1α mRNA levels in Eurasian perch (Perca fluviatilis) exposed to acute and chronic hypoxia. Mol Biol Rep 39(4):4009–4015
Rissanen E, Tranberg HK, Sollid J, Nilsson GE, Nikinmaa M (2006) Temperature regulates hypoxia-inducible factor-1 (HIF-1) in a poikilothermic vertebrate, crucian carp (Carassius carassius). J Exp Biol 209(Pt 6):994–1003
Roberts JJ, Hook TO, Ludsin SA, Pothoven SA, Vanderploeg HA, Brandt SB (2009) Effects of hypolimnetic hypoxia on foraging and distributions of Lake Erie yellow perch. J Exp Mar Bio Ecol 381(SUPPL):S132–S142
Roberts JJ, Brandt SB, Fanslow D, Ludsin SA, Pothoven SA, Scavia D, Höök TO (2011) Effects of hypoxia on consumption, growth, and RNA:DNA ratios of young yellow perch. Trans Am Fish Soc 140:1574–1586
Robertson CE, Wright PA, Köblitz L, Bernier NJ (2014) Hypoxia-inducible factor-1 mediates adaptive developmental plasticity of hypoxia tolerance in zebrafish, Danio rerio. Proc R Soc B 281:20140637
Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5:725–738 http://zhanglab.ccmb.med.umich.edu/I-TASSER/
Rytkönen KT, Vuori KA, Primmer CR, Nikinmaa M (2007) Comparison of hypoxia-inducible factor-1 alpha in hypoxia-sensitive and hypoxia-tolerant fish species. Comp Biochem Physiol D 2(2):177–186
Shams I, Avivi A, Nevo E (2004) Hypoxic stress tolerance of the blind subterranean mole rat: expression of erythropoietin and hypoxia-inducible factor 1 α. PNAS 101:9698–9703
Shen RJ, Jiang XY, Pu JW, Zou SM (2010) HIF-1α and -2α genes in a hypoxia-sensitive teleost species Megalobrama amblycephala: cDNA cloning, expression and different responses to hypoxia. Comp Biochem Physiol - B Biochem Mol Biol 157(3):273–280
Small K, Kopf RK, Watts RJ, Howitt J (2014) Hypoxia, Blackwater and fish kills: experimental lethal oxygen thresholds in juvenile predatory lowland river fishes. PLoS One 9(4)
Soitamo AJ, Rabergh CMI, Gassmann M, Sistonene L, Nikinmaa M (2001) Characterization of a hypoxia-inducible factor (HIF-1α) from rainbow trout. J Biol Chem 276:19699–19705
Srinivas V, Zhang LP, Zhu XH, Caro J (1999) Characterization of an oxygen/redox-dependent degradation domain of hypoxia-inducible factor a (HIF-a) proteins. Biochem Biophys Res Commun 260:557–561
Stierhoff KL, Tyler RM, Targett TE (2009) Hypoxia tolerance of juvenile weakfish (Cynoscion regalis): laboratory assessment of growth and behavioural avoidance responses. J Exp Biol Ecol 381:173–179
Suthers IM, Gee JH (1986) Role of hypoxia in limiting diel spring and summer distribution of juvenile yellow perch (Perca flavescens) in prairie marsh. Can J Fish Aquatic Sci 43:1562–1570
Suzuki H, Tomida A, Tsuruo T (2001) Dephosphorylated hypoxia-inducible factor 1alpha as a mediator of p53-dependent apoptosis during hypoxia. Oncogene 20(41):5779–5788
Terova G, Rimoldi S, Corà S, Bernardini G, Gornati R, Saroglia M (2008) Acute and chronic hypoxia affects HIF-1α mRNA levels in sea bass (Dicentrarchus labrax). Aquaculture 279(1–4):150–159
Terova G, Rimoldi S, Brambilla F, Gornati R, Bernardini G, Saroglia M (2009) In vivo regulation of GLUT2 mRNA in sea bass (Dicentrarchus labrax) in response to acute and chronic hypoxia. Comp Biochem Physiol B 152:306–316
Tiedke J, Borner J, Beeck H, Kwiatkowski M, Schmidt H, Thiel R, Fabrizius A, Burmester T (2015) Evaluating the hypoxia response of ruffe and flounder gills by a combined proteome and transcriptome approach. PLoS One 10(8):e0135911
Uchida T, Rossignol F, Matthay MA, Mounier R, Couette S, Clottes E, Clerici C (2004) Prolonged hypoxia differentially regulates hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha expression in lung epithelial cells: implication of natural antisense HIF-1alpha. J Biol Chem 279(15):14871–14878
Van Hagen M, Overmeer RM, Abolvardi SS, Vertegaal AC (2010) RNF4 and VHL regulate the proteasomal degradation of SUMO-conjugated hypoxia-inducible factor-2alpha. Nucleic Acids Res 38(6):1922–1931
Wenger RH (2002) Cellular adaptation to hypoxia: O2-sensing protein hydroxylases, hypoxia-inducible transcription factors, and O2-regulated gene expression. FASEB J 16(10):1151–1162
Wu RSS (2002) Hypoxia: From molecular responses to ecosystem responses. Mar Pollut Bull 45:35–45
Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y (2015) The I-TASSER Suite: protein structure and function prediction. Nat Methods 12:7–8
Zambonino-Infante JL, Claireaux G, Ernande BM, Jolivet A, Quazuguel P, Severe A, Huelvan C, Mazurais D (2013) Hypoxia tolerance of common sole juveniles depends on dietary regime and temperature at the larval stage: evidence for environmental conditioning. Proc R Soc B 280:9
Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40 http://zhanglab.ccmb.med.umich.edu/I-TASSER/
Zhao Q, Xie Y, Zheng Y, Jiang S, Liu W, Mu W, Liu Z, Zhao Y, Xue Y, Ren J (2014) GPS-SUMO: a tool for the prediction of sumoylation sites and SUMO-interaction motifs. Nucleic Acids Res 42(Web Server issue):W325–W330. doi:10.1093/nar/gku383