Advertisement

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

  • Yi-Bin Cao
  • Xue-Qun ChenEmail author
  • Shen Wang
  • Yu-Xiang Wang
  • Ji-Zeng DuEmail author
Article

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.

Keywords

Hypoxia-inducible factor-1α Hypoxia Qinghai Lake Naked carp Glucose transporter 

Notes

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.

References

  1. Behrooz A, Ismail-Beigi F (1999) Stimulation of glucose transport by hypoxia: signals and mechanisms. News Physiol Sci 14:105–110PubMedGoogle Scholar
  2. Benton MJ, Donoghue PC (2007) Paleontological evidence to date the tree of life. Mol Biol Evol 24:26–53PubMedCrossRefGoogle Scholar
  3. 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 23:1808–1816PubMedCrossRefGoogle Scholar
  4. 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 276:9519–9525PubMedCrossRefGoogle Scholar
  5. 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 498:62–66PubMedCrossRefGoogle Scholar
  6. Chou CF, Tohari S, Brenner S, Venkatesh B (2004) Erythropoietin gene from a teleost fish, Fugu rubripes. Blood 104:1498–1503PubMedCrossRefGoogle Scholar
  7. Dunn JF, Hochachka PW (1987) Turnover rates of glucose and lactate in rainbow trout during acute hypoxia. Can J Zool 65:1144–1148CrossRefGoogle Scholar
  8. 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 88:181–184CrossRefGoogle Scholar
  9. Goldman N, Yang Z (1994) A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11:725–736PubMedGoogle Scholar
  10. 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 1730:245–252PubMedGoogle Scholar
  11. 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 143:494–503PubMedCrossRefGoogle Scholar
  12. 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] 177:765–777Google Scholar
  13. Holland PW (1999) Gene duplication: past, present and future. Semin Cell Dev Biol 10:541–547PubMedCrossRefGoogle Scholar
  14. 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 292:464–468PubMedCrossRefGoogle Scholar
  15. 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 12:149–162PubMedCrossRefGoogle Scholar
  16. 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 17:6573–6586PubMedCrossRefGoogle Scholar
  17. Kessler KF (1879) Beitrage zur Ichthyologie von Zentral-Asien. Biol Bull Acad Sci 10:233–272Google Scholar
  18. Kim W, Kaelin WG Jr (2003) The von Hippel-Lindau tumor suppressor protein: new insights into oxygen sensing and cancer. Curr Opin Genet Dev 13:55–60PubMedCrossRefGoogle Scholar
  19. 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 7:15PubMedCrossRefGoogle Scholar
  20. 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–R1042PubMedGoogle Scholar
  21. 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 211:1063–1074PubMedCrossRefGoogle Scholar
  22. Nikinmaa M, Rees BB (2005) Oxygen-dependent gene expression in fishes. Am J Physiol Regul Integr Comp Physiol 288:R1079–R1090PubMedGoogle Scholar
  23. 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 207:3131–3139PubMedCrossRefGoogle Scholar
  24. Portner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97PubMedCrossRefGoogle Scholar
  25. Qin B, Huang Q (1998) Evaluation of the climatic change impacts on the inland lake-a case study of Lake Qinghai, China. Climatic Change 39:695–714CrossRefGoogle Scholar
  26. 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 200:247–251PubMedCrossRefGoogle Scholar
  27. 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 209:994–1003PubMedCrossRefGoogle Scholar
  28. 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] 2:177–186Google Scholar
  29. Safran M, Kaelin WG Jr (2003) HIF hydroxylation and the mammalian oxygen-sensing pathway. J Clin Invest 111:779–783PubMedGoogle Scholar
  30. 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 731–745Google Scholar
  31. 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 12:5447–5454PubMedGoogle Scholar
  32. Semenza GL, Shimoda LA, Prabhakar NR (2006) Regulation of gene expression by HIF-1. Novartis Found Symp 272:2–8PubMedCrossRefGoogle Scholar
  33. 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 30:38–40Google Scholar
  34. 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 276:19699–19705PubMedCrossRefGoogle Scholar
  35. Sollid J, De AP, Gundersen K, Nilsson GE (2003) Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J Exp Biol 206:3667–3673PubMedCrossRefGoogle Scholar
  36. 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] 176:359–369Google Scholar
  37. 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 62:772–784PubMedCrossRefGoogle Scholar
  38. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  39. 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 258:195–214PubMedCrossRefGoogle Scholar
  40. 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 25:4876–4882PubMedCrossRefGoogle Scholar
  41. 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 4:222Google Scholar
  42. 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 134:409–421PubMedCrossRefGoogle Scholar
  43. Wernersson R, Pedersen AG (2003) RevTrans: multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res 31:3537–3539PubMedCrossRefGoogle Scholar
  44. Wu YF, Wu CZ (1992) Fish in Qinzang Tibetan. Parasitol Res 101:467–471CrossRefGoogle Scholar
  45. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556PubMedGoogle Scholar
  46. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591PubMedCrossRefGoogle Scholar
  47. Yang Z, Bielawski JP (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15:496–503PubMedCrossRefGoogle Scholar
  48. 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 35:28–32Google Scholar
  49. Yang Z, Wong WS, Nielsen R (2005b) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118PubMedCrossRefGoogle Scholar
  50. Yu PQ, Chen YY (1998) China red data book of endangered animals—Pisces. Science Press, BeijingGoogle Scholar
  51. 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 22:2472–2479PubMedCrossRefGoogle Scholar
  52. 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 270:3010–3017PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Division of Neurobiology and Physiology, College of Life SciencesZhejiang UniversityHangzhouChina
  2. 2.Division of Neurobiology and Physiology, School of MedicineZhejiang UniversityHangzhouChina
  3. 3.Department of BiologyQueen’s UniversityKingstonCanada

Personalised recommendations