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First published online March 2, 2006
Journal of Experimental Biology 209, 994-1003 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02103

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Temperature regulates hypoxia-inducible factor-1 (HIF-1) in a poikilothermic vertebrate, crucian carp (Carassius carassius)

Eeva Rissanen^1,, Hanna K. Tranberg¹, Jørund Sollid², Göran E. Nilsson² and Mikko Nikinmaa¹

¹ Centre of Excellence in Evolutionary Genetics and Physiology, Department of Biology, University of Turku, Finland
² Department of Molecular Biosciences, University of Oslo, Norway

^* Author for correspondence (e-mail: eeva.rissanen{at}utu.fi)

Accepted 17 January 2006

Hypoxia-inducible transcription factor-1 (HIF-1) is a master regulator of hypoxia-induced gene responses. To find out whether HIF-1 function is involved in gene expression changes associated with temperature acclimation as well as in hypoxia adaptation in poikilotherms, we studied HIF-1 DNA binding activity and HIF-1 expression in normoxia and during hypoxia (0.7 mg l^–1 O₂) in crucian carp at temperatures of 26, 18 and 8°C. Temperature had a marked influence on HIF-1 in normoxia. Although HIF-1 mRNA levels remained unaltered, cold acclimation (8°C) increased HIF-1 protein amounts in the liver, gills and heart and HIF-1 DNA binding activity in the heart, gills and kidney of crucian carp by two- to threefold compared to warm acclimated fish (26°C). In the heart and kidney HIF-1 activity was already significantly increased in the 18°C acclimated fish. Temperature also affected hypoxic regulation of HIF-1. Although hypoxia initially increased amounts of HIF-1 protein in all studied tissues at every temperature, except for liver at 18°C, HIF-1 activity increased only in the heart of 8°C acclimated and in the gills of 18°C acclimated fish. At 8°C HIF-1 mRNA levels increased transiently in the gills after 6 h of hypoxia and in the kidney after 48 h of hypoxia. In the gills at 26°C HIF-1 mRNA levels increased after 6 h of hypoxia and remained above normoxic levels for up to 48 h of hypoxia. These results show that HIF-1 is involved in controlling gene responses to both oxygen and temperature in crucian carp. No overall transcriptional control mechanism has been described for low temperature acclimation in poikilotherms, but the present results suggest that HIF-1 could have a role in such regulation. Moreover, this study highlights interaction of the two prime factors defining metabolism, temperature and oxygen, in the transcriptional control of metabolic homeostasis in animals.

Key words: HIF-1, temperature, cold acclimation, crucian carp, Carassius carassius, teleost

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