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HIF-1α involvement in low temperature and anoxia survival by a freeze tolerant insect

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Abstract

Winter survival for many insect species relies on the ability to endure the freezing of extracellular body fluids. Because freezing impedes oxygen delivery to tissues, one component of natural freeze tolerance is a well-developed anoxia/ischemia resistance. The present study explores the responses of the hypoxia-inducible factor-1α (HIF-1α) to cold, freezing and anoxia exposures in the freeze tolerant goldenrod gall fly larva, Eurosta solidaginis. Reverse transcription-PCR was used to quantify hif-1α transcript levels; transcripts were significantly elevated by ∼70% in chilled (3 ∘C), frozen (−16 ∘C) and thawed (returned to 3 ∘C) insects, compared with 15 ∘C controls. Transcripts also rose by ∼3-fold in insects given anoxia exposure under a nitrogen gas atmosphere. Cold and freezing exposure also elevated HIF-1α protein content in the larvae and HIF-1α levels increased over the winter months in insects sampled from an outdoor population; levels peaked in February at 2.1-fold higher than in September. A partial sequence of HIF-1α that covers the bHLH and PAS domains of the protein was obtained from E. solidaginis and sequence analysis revealed that this segment shared 62% identity overall with Drosophila melanogaster HIF-1α and higher percent identities within specific domains: 76% within the bHLH domain and 70% within the PAS domain. The data provide the first documentation of a potential role for HIF-1 in regulating the expression of genes that can aid freezing survival in a cold-hardy animal. (Mol Cell Biochem xxx: 99–106, 2005)

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References

  1. Storey KB, Storey JM: Biochemical adaptations for winter survival in insects. In: P.L. Steponkus (ed.), Insects at Low Temperature, Vol 1, JAI Press, London, 1992, pp 101–140

    Google Scholar 

  2. Lee RE, Costanzo JP: Biological ice nucleation and ice distribution in cold-hardy ectothermic animals. Ann Rev Physiol 60: 55–72, 1998

    Article  CAS  Google Scholar 

  3. Scheid P, Hook C, Bridges CR: Diffusion in gas exchange of insects. Fed Proc 41: 2143–2145, 1982

    PubMed  CAS  Google Scholar 

  4. Storey KB, Storey JM: Natural freezing survival in animals. Ann Rev Ecol Syst 27: 365–386, 1996

    Article  Google Scholar 

  5. Storey KB, Storey JM: Freezing and cellular metabolism in the gall fly larva, Eurosta solidaginis. J Comp Physiol B 155: 333–337, 1985

    CAS  Google Scholar 

  6. Irwin JT, Bennett VA, Lee RE: Diapause development in frozen larvae of the goldenrod gall fly, Eurosta solidaginis Fitch (Diptera: Tephritidae). J Comp Physiol B 171: 181–188, 2001

    Article  PubMed  CAS  Google Scholar 

  7. Bunn HF, Poyton RO: Oxygen sensing and molecular adaptation to hypoxia. Physiol Rev 76: 839–885, 1996

    PubMed  CAS  Google Scholar 

  8. Ratcliffe PJ, O'Rourke JF, Maxwell PH, Pugh CW: Oxygen sensing, hypoxia-inducible factor-1 and the regulation of mammalian gene expression. J Exp Biol 201: 1153–1162, 1998

    PubMed  CAS  Google Scholar 

  9. Semenza GL: O2-regulated gene expression: transcriptional control of cardiorespiratory physiology by HIF-1. J Appl Physiol 96: 1173–1177, 2004

    PubMed  CAS  Google Scholar 

  10. Gorr TA: Daphnia and Drosophila: Two invertebrate models for O2 responsive and HIF-mediated regulation of genes and genomes. Int Congress Ser 1275: 55–62, 2004

  11. Jiang L, Crews ST: The Drosophila dysfusion basic helix-loop-helix (bHLH)-PAS gene controls tracheal fusion and levels of the trachealess bHLH-PAS protein. Mol Cell Biol 23: 5625–5637, 2003

    PubMed  CAS  Google Scholar 

  12. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, Gaskell SJ, Kriegsheim Av, Hebestreit HF, Mukherji M, Schofield CJ, Maxwell PH, Pugh CW, Ratcliffe PJ: Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292: 468–472, 2001

    PubMed  CAS  Google Scholar 

  13. Nambu JR, Chen W, Hu S, Crews ST: The Drosophila melanogaster similar bHLH-PAS gene encodes a protein related to human hypoxia-inducible factor 1 alpha and Drosophila single-minded. Gene 172: 249–254, 1996

    Article  PubMed  CAS  Google Scholar 

  14. Nagao M, Ebert BL, Ratcliffe PJ, Pugh CW: Drosophila melanogaster SL2 cells contain a hypoxically inducible DNA binding complex which recognises mammalian HIF-binding sites. FEBS Lett 387: 161–166, 1996

    Article  PubMed  CAS  Google Scholar 

  15. Jiang H, Guo R, Powell-Coffman JA: The Caenorhabditis elegans hif-1 gene encodes a bHLH-PAS protein that is required for adaptation to hypoxia. Proc Natl Acad Sci USA 98: 7916–7921, 2001

    PubMed  CAS  Google Scholar 

  16. Ma E, Haddad GG: Isolation and characterization of the hypoxia-inducible factor 1beta in Drosophila melanogaster. Brain Res Mol Brain Res 73: 11–16, 1999

    PubMed  CAS  Google Scholar 

  17. Bacon NCM, Wappner P, O'Rourke JF, Bartlett SM, Shilo B, Pugh CW, Ratcliffe PJ: Regulation of the Drosophila bHLH-PAS protein Sima by hypoxia: Functional evidence for homology with mammalian HIF-1α. Biochem Biophys Res Commun 249: 811–816, 1998

    Article  PubMed  CAS  Google Scholar 

  18. Lavista-Llanos S, Centanin L, Irisarri M, Russo DM, Gleadle JM, Bocca SN, Muzzopappa M, Ratcliffe PJ, Wappner P: Control of the hypoxic response in Drosophila melanogaster by the basic helix-loop-helix PAS protein similar. Mol Cell Biol 22: 6842–6853, 2002

    Article  PubMed  CAS  Google Scholar 

  19. Eddy SF, Morin P Jr, Storey, KB: Cloning and expression of PPARγ and PGC-1α from the hibernating ground squirrel, Spermophilus tridecemlineatus. Mol Cell Biochem 269, 175–182, 2005

    Article  PubMed  CAS  Google Scholar 

  20. Morin P Jr, Storey KB: Cloning and expression of hypoxia-inducible factor 1α from the hibernating ground squirrel, Spermophilus tridecemlineatus. Biochim Biophys Acta 1729, 32–40, 2005

    PubMed  Google Scholar 

  21. Camenisch G, Tini M, Chilov D, Kvietikova I, Srinivas V, Caro J, Spielmann P, Wenger RH, Gassmann M: General applicability of chicken egg yolk antibodies: the performance of IgY immunoglobulins raised against the hypoxia-inducible factor 1alpha. FASEB J 13: 81–88, 1999

    PubMed  CAS  Google Scholar 

  22. Wang JL, Jiang B, Rue EA, Semenza GL: Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci USA 92: 5510–5514, 1995

    PubMed  CAS  Google Scholar 

  23. Irwin JT, Lee RE: Energy and water conservation in frozen vs. supercooled larvae of the goldenrod gall fly, Eurosta solidaginis (Fitch) (Diptera: Tephritidae). J Exp Zool. 292: 345–350, 2002

    Article  PubMed  Google Scholar 

  24. Storey KB, Storey JM: Biochemical strategies of overwintering in the gall fly larva, Eurosta solidaginis: effect of low temperature acclimation on the activities of enzymes of intermediary metabolism. J Comp Physiol 144: 191–199, 1981

    CAS  Google Scholar 

  25. Storey KB, Baust JM, Storey JM: Intermediary metabolism during low temperature acclimation in the overwintering gall fly larva, Eurosta solidaginis. J Comp Physiol 144: 183–190, 1981

    CAS  Google Scholar 

  26. Morrissey RE, Baust JG: The ontogeny of cold tolerance in the gall fly, Eurosta solidaginis. J Insect Physiol 22: 431–437, 1976

    Article  CAS  Google Scholar 

  27. Lee RE, Hankison SJ: Acquisition of freezing tolerance in early autumn and seasonal changes in gall water content influence inoculative freezing of gall fly larvae, Eurosta solidaginis (Diptera, Tephritidae). J Insect Physiol 49: 385–393, 2003

    PubMed  CAS  Google Scholar 

  28. Treinin M, Shliar J, Jiang H, Powell-Coffman JA, Bromberg Z, Horowitz M: HIF-1 is required for heat acclimation in the nematode Caenorhabditis elegans. Physiol Genomics 14: 17–24, 2003

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Biochemistry and Department of Chemistry, College of Natural Sciences, Carleton University, 1125 Colonel By Drive, Ottawa, Ontario, Canada, K1S 5B6

    Pier Morin Jr., David C. McMullen & Kenneth B. Storey

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  1. Pier Morin Jr.
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  2. David C. McMullen
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  3. Kenneth B. Storey
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Correspondence to Pier Morin Jr..

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Morin, P., McMullen, D.C. & Storey, K.B. HIF-1α involvement in low temperature and anoxia survival by a freeze tolerant insect. Mol Cell Biochem 280, 99–106 (2005). https://doi.org/10.1007/s11010-005-8236-x

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  • DOI: https://doi.org/10.1007/s11010-005-8236-x

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