[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content

Advertisement

Log in

Evolution and Regulation of the Downstream Gene of Hypoxia-Inducible Factor-1α in Naked Carp (Gymnocypris przewalskii) from Lake Qinghai, China

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The naked carp (Gymnocypris przewalskii) is a native teleost of Lake Qinghai (altitude, 3.2 km) on the Qinghai-Tibet Plateau in China. Hypoxia-inducible factor (HIF)-1α of Gymnocypris przewalskii was cloned and a phylogenetic tree for vertebrate HIF-1α was constructed. By analysis of maximum likelihood models of codon substitutions for HIF-1α, three positive sites in the branch lineages of crucian carp, eelpout, and flounder, and a higher proportion of neutral sites in naked carp, antarctic eelpout, rainbow trout, and grayling, were detected among all teleosts. It seems that low habitat temperatures relax the purifying selection of HIF-1α in these stenothermal coldwater fish, and both cold and hypoxic lake water contributed to the evolution of the HIF-1α gene in the naked carp. Furthermore, Glut 1 mRNA, a gene downstream from HIF-1α, has a time-course- and tissue-specific dependent response to hypoxic challenge.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Behrooz A, Ismail-Beigi F (1999) Stimulation of glucose transport by hypoxia: signals and mechanisms. News Physiol Sci 14:105–110

    PubMed  CAS  Google Scholar 

  • Benton MJ, Donoghue PC (2007) Paleontological evidence to date the tree of life. Mol Biol Evol 24:26–53

    Article  PubMed  CAS  Google Scholar 

  • Brunet FG, Crollius HR, Paris M, Aury JM, Gibert P, Jaillon O, Laudet V, Robinson-Rechavi M (2006) Gene loss and evolutionary rates following whole-genome duplication in teleost fishes. Mol Biol Evol 23:1808–1816

    Article  PubMed  CAS  Google Scholar 

  • Chen C, Pore N, Behrooz A, Ismail-Beigi F, Maity A (2001) Regulation of glut1 mRNA by hypoxia-inducible factor-1 Interaction between H-ras and hypoxia. J Biol Chem 276:9519–9525

    Article  PubMed  CAS  Google Scholar 

  • Cho S, Choi YJ, Kim JM, Jeong ST, Kim JH, Kim SH, Ryu SE (2001) Binding and regulation of HIF-1alpha by a subunit of the proteasome complex, PSMA7. FEBS Lett 498:62–66

    Article  PubMed  CAS  Google Scholar 

  • Chou CF, Tohari S, Brenner S, Venkatesh B (2004) Erythropoietin gene from a teleost fish, Fugu rubripes. Blood 104:1498–1503

    Article  PubMed  CAS  Google Scholar 

  • Dunn JF, Hochachka PW (1987) Turnover rates of glucose and lactate in rainbow trout during acute hypoxia. Can J Zool 65:1144–1148

    Article  CAS  Google Scholar 

  • Fischer P, Kils U, Rademacher K (1992) In situ investigations on the respiration and behaviour of the eelpout Zoarces viviparus under short-term hypoxia. Mar Ecol Prog Ser 88:181–184

    Article  Google Scholar 

  • Goldman N, Yang Z (1994) A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11:725–736

    PubMed  CAS  Google Scholar 

  • Hall JR, Richards RC, MacCormack TJ, Ewart KV, Driedzic WR (2005) Cloning of GLUT3 cDNA from Atlantic cod (Gadus morhua) and expression of GLUT1 and GLUT3 in response to hypoxia. Biochim Biophys Acta 1730:245–252

    PubMed  CAS  Google Scholar 

  • Heise K, Puntarulo S, Nikinmaa M, Lucassen M, Portner HO, Abele D (2006) Oxidative stress and HIF-1 DNA binding during stressful cold exposure and recovery in the North Sea eelpout (Zoarces viviparus). Comp Biochem Physiol A Mol Integr Physiol 143:494–503

    Article  PubMed  CAS  Google Scholar 

  • Heise K, Estevez MS, Puntarulo S, Galleano M, Nikinmaa M, Portner HO, Abele D (2007) Effects of seasonal and latitudinal cold on oxidative stress parameters and activation of hypoxia inducible factor (HIF-1) in zoarcid fish. J Comp Physiol [B] 177:765–777

    CAS  Google Scholar 

  • Holland PW (1999) Gene duplication: past, present and future. Semin Cell Dev Biol 10:541–547

    Article  PubMed  CAS  Google Scholar 

  • Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, Salic A, Asara JM, Lane WS, Kaelin WG Jr (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292:464–468

    Article  PubMed  CAS  Google Scholar 

  • Iyer NV, Kotch LE, Agani F, Leung SW, Laughner E, Wenger RH, Gassmann M, Gearhart JD, Lawler AM, Yu AY, Semenza GL (1998) Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 12:149–162

    Article  PubMed  CAS  Google Scholar 

  • Kallio PJ, Okamoto K, O’Brien S, Carrero P, Makino Y, Tanaka H, Poellinger L (1998) Signal transduction in hypoxic cells: inducible nuclear translocation and recruitment of the CBP/p300 coactivator by the hypoxia-inducible factor-1alpha. EMBO J 17:6573–6586

    Article  PubMed  CAS  Google Scholar 

  • Kessler KF (1879) Beitrage zur Ichthyologie von Zentral-Asien. Biol Bull Acad Sci 10:233–272

    Google Scholar 

  • Kim W, Kaelin WG Jr (2003) The von Hippel-Lindau tumor suppressor protein: new insights into oxygen sensing and cancer. Curr Opin Genet Dev 13:55–60

    Article  PubMed  CAS  Google Scholar 

  • Law SH, Wu RS, Ng PK, Yu RM, Kong RY (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

    Article  PubMed  CAS  Google Scholar 

  • MacCormack TJ, Driedzic WR (2007) The impact of hypoxia on in vivo glucose uptake in a hypoglycemic fish, Myoxocephalus scorpius. Am J Physiol Regul Integr Comp Physiol 292:R1033–R1042

    PubMed  CAS  Google Scholar 

  • Matey V, Richards JG, Wang Y, Wood CM, Rogers J, Davies R, Murray BW, Chen XQ, Du J, Brauner CJ (2008) The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii. J Exp Biol 211:1063–1074

    Article  PubMed  CAS  Google Scholar 

  • Nikinmaa M, Rees BB (2005) Oxygen-dependent gene expression in fishes. Am J Physiol Regul Integr Comp Physiol 288:R1079–R1090

    PubMed  CAS  Google Scholar 

  • Nilsson GE, Renshaw GM (2004) Hypoxic survival strategies in two fishes: extreme anoxia tolerance in the North European crucian carp and natural hypoxic preconditioning in a coral-reef shark. J Exp Biol 207:3131–3139

    Article  PubMed  CAS  Google Scholar 

  • Portner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97

    Article  PubMed  CAS  Google Scholar 

  • Qin B, Huang Q (1998) Evaluation of the climatic change impacts on the inland lake-a case study of Lake Qinghai, China. Climatic Change 39:695–714

    Article  Google Scholar 

  • Rees BB, Bowman JA, Schulte PM (2001) Structure and sequence conservation of a putative hypoxia response element in the lactate dehydrogenase-B gene of Fundulus. Biol Bull 200:247–251

    Article  PubMed  CAS  Google Scholar 

  • 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 209:994–1003

    Article  PubMed  CAS  Google Scholar 

  • Rytkonen KT, Vuoria KA, Primmera CR, Nikinmaa M (2007) Comparison of hypoxia-inducible factor-1 alpha in hypoxia-sensitive and hypoxia-tolerant fish species. Comp Biochem Physiol [D] 2:177–186

    Google Scholar 

  • Safran M, Kaelin WG Jr (2003) HIF hydroxylation and the mammalian oxygen-sensing pathway. J Clin Invest 111:779–783

    PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Extraction, purification, and analysis of mRNA from eukaryotic cells. In: Molecular cloning: a laboratory manual. 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 731–745

  • Semenza GL, Wang GL (1992) A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol 12:5447–5454

    PubMed  CAS  Google Scholar 

  • Semenza GL, Shimoda LA, Prabhakar NR (2006) Regulation of gene expression by HIF-1. Novartis Found Symp 272:2–8

    Article  PubMed  CAS  Google Scholar 

  • Shi J, Qi HF, Yang JX, Duan DQ, Duan XB, Wang YM (2000) The analysis of the resource of scale-less carp in Lake Qinghai. Fish Fresh Water 30:38–40

    Google Scholar 

  • Soitamo AJ, Rabergh CM, Gassmann M, Sistonen L, Nikinmaa M (2001) Characterization of a hypoxia-inducible factor (HIF-1alpha) from rainbow trout. Accumulation of protein occurs at normal venous oxygen tension. J Biol Chem 276:19699–19705

    Article  PubMed  CAS  Google Scholar 

  • Sollid J, De AP, Gundersen K, Nilsson GE (2003) Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J Exp Biol 206:3667–3673

    Article  PubMed  Google Scholar 

  • Sollid J, Rissanen E, Tranberg HK, Thorstensen T, Vuori KA, Nikinmaa M, Nilsson GE (2006) HIF-1alpha and iNOS levels in crucian carp gills during hypoxia-induced transformation. J Comp Physiol [B] 176:359–369

    CAS  Google Scholar 

  • Steinke D, Salzburger W, Meyer A (2006) Novel relationships among ten fish model species revealed based on a phylogenomic analysis using ESTs. J Mol Evol 62:772–784

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Taylor JC, Miller JM (2001) Physiological performance of juvenile southern flounder, Paralichthys lethostigma (Jordan and Gilbert, 1884), in chronic and episodic hypoxia. J Exp Mar Biol Ecol 258:195–214

    Article  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Walker KF, Dunn IG, Edwards D, Petr T, Yang HZ (1996) A fishery in a changing lake environment: the naked carp Gymnocephalus przewalskii (Kessler) (Cyprinidae: Schizothoracinae) in Qinghai Hu, China. Int J Salt Lake Res 4:222

    Google Scholar 

  • Wang YS, Gonzalez RJ, Patrick ML, Grosell M, Zhang C, Feng Q, Du J, Walsh PJ, Wood CM (2003) Unusual physiology of scale-less carp, Gymnocypris przewalskii, in Lake Qinghai: a high altitude alkaline saline lake. Comp Biochem Physiol A Mol Integr Physiol 134:409–421

    Article  PubMed  Google Scholar 

  • Wernersson R, Pedersen AG (2003) RevTrans: multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res 31:3537–3539

    Article  PubMed  CAS  Google Scholar 

  • Wu YF, Wu CZ (1992) Fish in Qinzang Tibetan. Parasitol Res 101:467–471

    Article  Google Scholar 

  • Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556

    PubMed  CAS  Google Scholar 

  • Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, Bielawski JP (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15:496–503

    Article  PubMed  Google Scholar 

  • Yang JX, Qi HF, Shi JQ, Chen DQ, Huang FX, Tang HY (2005a) Hydrochemistry property and water quality analysis of Qinghaihu Lake. Fish Fresh Water 35:28–32

    Google Scholar 

  • Yang Z, Wong WS, Nielsen R (2005b) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118

    Article  PubMed  CAS  Google Scholar 

  • Yu PQ, Chen YY (1998) China red data book of endangered animals—Pisces. Science Press, Beijing

    Google Scholar 

  • Zhang J, Nielsen R, Yang Z (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22:2472–2479

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Wu RS, Mok HO, Wang Y, Poon WW, Cheng SH, Kong RY (2003) Isolation, characterization and expression analysis of a hypoxia-responsive glucose transporter gene from the grass carp, Ctenopharyngodon idellus. Eur J Biochem 270:3010–3017

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the NSFC (Major Project No. 30393130, Project No. 30128016) and the National Basic Research Program “973” (No. 2006CB504100). We wish to thank Professor Iain C. Bruce, Department of Physiology, Zhejiang University School of Medicine, China, for his help with the English editing of the manuscript. We also thank Yaqing Liu of the Northwest High Plateau Institute of Biology, Chinese Academy of Sciences, Xining, for his excellent logistical assistance.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Xue-Qun Chen or Ji-Zeng Du.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cao, YB., Chen, XQ., Wang, S. et al. Evolution and Regulation of the Downstream Gene of Hypoxia-Inducible Factor-1α in Naked Carp (Gymnocypris przewalskii) from Lake Qinghai, China. J Mol Evol 67, 570–580 (2008). https://doi.org/10.1007/s00239-008-9175-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-008-9175-4

Keywords

Navigation