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

: Rissanen E, Tranberg HK, Sollid J, Nilsson GE, Nikinmaa M

Publisher: COMPANY OF BIOLOGISTS LTD

: 2006

: Journal of Experimental Biology

: JOURNAL OF EXPERIMENTAL BIOLOGY

: J EXP BIOL

: 209

: 6

: 994

: 1003

: 10

: 0022-0949

DOI: https://doi.org/10.1242/jeb.02103

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 alpha expression in normoxia and during hypoxia ( 0.7 mg l(-1) O-2) in crucian carp at temperatures of 26, 18 and 8 degrees C. Temperature had a marked influence on HIF-1 in normoxia. Although HIF-1 alpha mRNA levels remained unaltered, cold acclimation ( 8 degrees C) increased HIF-1 alpha 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 degrees C). In the heart and kidney HIF-1 activity was already significantly increased in the 18 degrees C acclimated fish. Temperature also affected hypoxic regulation of HIF-1. Although hypoxia initially increased amounts of HIF-1 alpha protein in all studied tissues at every temperature, except for liver at 18 degrees C, HIF-1 activity increased only in the heart of 8 degrees C acclimated and in the gills of 18 degrees C acclimated fish. At 8 degrees C HIF-1 alpha mRNA levels increased transiently in the gills after 6h of hypoxia and in the kidney after 48h of hypoxia. In the gills at 26 degrees C HIF-1 alpha 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.