Effects of seasonal and latitudinal cold on oxidative stress parameters and activation of hypoxia inducible factor (HIF-1) in zoarcid fish

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 177, Issue 7, 2007, Pages 765-777

  Heise, K ^a   Estevez, M S ^b   Puntarulo, S ^b   Galleano, M ^b   Nikinmaa, M ^c   Portner H O ^a   Abele, D ^a  

^a ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c UNIVERSITY OF TURKU   (Finland)

Author keywords

Glutathione; HIF 1; North Sea eelpout; Oxidative stress; Polar eelpout

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1;

ANIMAL; ANTARCTICA; ARTICLE; ATLANTIC OCEAN; COLD; COMPARATIVE STUDY; GENETICS; LIVER; METABOLISM; OXIDATIVE STRESS; PERCIFORMES; PHYSIOLOGY; SEASON; SPECIES DIFFERENCE;

ANIMALS; ANTARCTIC REGIONS; COLD; HYPOXIA-INDUCIBLE FACTOR 1; LIVER; NORTH SEA; OXIDATIVE STRESS; PERCIFORMES; SEASONS; SPECIES SPECIFICITY;

LYCODES TURNERI; PACHYCARA BRACHYCEPHALUM; ZOARCES VIVIPARUS; ZOARCIDAE;

EID: 34548794162     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-007-0173-4     Document Type: Article

References (68)

1. Abele D, Puntarulo S (2004) Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comp Biochem Physiol 138A:405-415
2. Abele D, Philipp E, Gonzalez P, Puntarulo S (2007) Marine invertebrate mitochondria and oxidative stress. Front Biosci 12:933-946
3. Acker T, Acker H (2004) Cellular oxygen sensing need in CNS function: physiological and pathological implications. J Exp Biol 207:3171-3188
4. Acker T, Fandrey J, Acker H (2006) The good, the bad and the ugly in oxygen sensing: ROS, cytochromes and prolyl-hydroxylases. Cardiovasc Res 71:195-207
5. Atunes F, Boveris A, Cadenas E (2004) On the mechanism and biology of cytochrome oxidase inhibition by nitric oxide. PNAS 101:16774-16779
6. Buettner GR (1987) Spin trapping: ESP parameters of spin adducts. Free Rad Biol Med 3:259-303
7. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 71:248-254
8. Brodte E, Graeve M, Jacob U, Knust R, Pörtner H-O (2006a) Temperature dependent lipid levels and components in polar and temperate eelpout (Zoarcidae). Fish Physiol Biochem (in press)
9. Brodte E, Knust R, Pörtner H-O, Arntz WE (2006b) Biology of the Antarctic eelpout Pachycara brachycephalum. Deep-Sea Res 53:1131-1140
10. Brodte E, Knust R, Pörtner HO (2006c) Temperature dependent energy allocation to growth in Antarctic and boreal eelpout (Zoarcidae). Polar Biol doi:10.1007/s00300-006-0165-y
11. Brumby PE, Massey V (1967) Determination of non-heme iron, total iron and copper. Methods Enzymol 10:464-472
12. Cleeter MWJ, Cooper JM, Darley-Usmar VM, Moncada S, Schapira AHV (1994) Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett 345:50-54
13. Czubryt MP, Panagia V, Pierce GN (1996) The roles of free radicals, peroxides and oxidized lipoproteins in second messenger system dysfunction. EXS 76:57-69
14. Desai I (1984) Vitamin E analysis methods for animal tissues. Methods Enzymol 105:138-146
15. Doege K, Heine S, Jensen I, Jelkmann W, Metzen E (2005) Inhibition of mitochondrial respiration elevates oxygen concentration but leaves regulation of hypoxia-inducible factor (HIF) intact. Blood 106:2311-2317
16. Dunlap WC, FujisawaA, Yamamoto Y, Moylan TJ, Sidell BD (2002) Notothenoid fish, krill and phytoplankton from Antarctica contain a vitamin E constituent (α-tocopherol) functionally associated with cold-water adaptation. Comp Biochem Physiol 133B:299-305
17. Egginton S, Sidell BD (1989) Thermal acclimation induces adaptive changes in subcellular structure of fish skeletal muscle. Am J Physiol 256:R1-R9
18. Fandrey J, Gorr TA, Gassmann M (2006) Regulating cellular oxygen sensing by hydroxylation. Cardiovasc Res 71:642-651
19. Fariss MW, Reed DJ (1987) High-performance liquid chromatography of thiols and disufides: diphenol derivatives. Methods Enzymol 143:101-109
20. Gieseg SP, Cuddihy S, Hill JV, Davison W (2000) A comparison of plasma vitamin C and E levels in two Antarctic and two temperate water fish species. Comp Biochem Physiol 125B:371-378
21. Gonzalez Flecha B, Llesuy S, Boveris A (1991) Hydroperoxide-initiated chemiluminescence: an assay for oxidative stress in biopsies of heart, liver, and muscle. Free Rad Biol Med 10:93-100
22. Gorr TA, Gassmann M, Wappner P (2006) Sensing and responding to hypoxia via HIF in model invertebrates. J Insect Physiol 52:349-364
23. Gracey AY, Fraser FJ, Li W, Fang Y (2004) Coping with cold: an integrative analysis of the transcriptome of a poikilothermic vertebrate. Proc Natl Acad Sci USA 101(48):16970-16975
24. Günzler WA, Flohe L (1985) Glutathione peroxidase. In: Greenwald RA (ed) CRC handbooks of methods for oxygen radical research. CRC, Boca Raton, pp 285-289
25. Haddad JJE, Olvers RE, Land SC (2000) Antioxidant/pro-oxidant equilibrium regulates HIF-1α and NF-κB redox sensitivity. J Biol Chem 275:21130-21139
26. Halliwell B, Gutteridge JMC (1985) Free radicals in biology and medicine, 2nd edn. Clarendon, Oxford, pp 1-543
27. Han D, Hanawa N, Saberi B, Kaplowitz N (2006) Mechanisms of liver injury: role of glutathione redox status in liver injury. Am J Physiol Gastrointest Liver Physiol 291:G1-G7
28. Heise K, Puntarulo S, Nikinmaa M, Lucassen M, Pörtner HO, Abele D (2006a) Oxidative stress and HIF-1 DNA binding during stressful cold exposure and recovery in the North Sea eelpout (Zoarces viviparus). Comp Biochem Physiol 143A:494-503
29. Heise K, Puntarulo S, Nikinmaa M, Abele D, Pörtner HO (2006b) Oxidative stress during stressful heat exposure and recovery in the North Sea eelpout (Zoarces viviparus). J Exp Biol 209:353-363
30. Huang LE, Arany Z, Livingston DM, Bunn FH (1996) Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its α-subunit. J Biol Chem 271(50):32253-32259
31. Huang LE, Bunn FH (2003) Hypoxia-inducible factor and its biomedical relevance. J Biol Chem 278(22):19575-19578
32. Hulbert AJ (2006) The link between membrane composition, metabolic rate and lifespan. Comp Biochem Physiol A (in press)
33. 2 sensing. Sci 292:464-468
34. Johnston IA (1982) Capillarisation, oxygen diffusion distances and mitochondrial content of carp muscles following acclimation to summer and winter temperatures. Cell Tissue Res 222:325-337
35. Katschinski DM, Le L, Heinrich D, Wagner KF, Hofer T, Schindler SG, Wenger RH (2002) Heat induction of the unphosphorylated form of hypoxia-inducible factor-1α is dependent on heat shock protein-90 activity. J Biol Chem 277:9262-9267
36. Kidd PM (1997) Glutathione: systemic protectant against oxidative and free radical damage. Alt Med Rev 1:155-176
37. Klein SM, Cohen G, Lieber CS, Cederbaum AI (1983) Increased microsomal oxidation of hydroxy radical scavengers and ethanol after chronic consumption of ethanol. Arch Biochem Biophys 223:425-433
38. Kvietikova I, Wenger RH, Marti HH, Gassmann M (1995) The transcription factors ATF-1 and CREB-1 bind constitutively to the hypoxia-inducible factor-1 (HIF-1) DNA recognition site. Nucl Acids Res 23:4542-4550
39. Lannig G, Storch D, Pörtner H-O (2005) Aerobic mitochondrial capacities in Antarctic and temperate eelpout (Zoarcidae) subjected to warm versus cold acclimation. Polar Biol 28:575-584
40. Larsen B., Pörtner HO, Jensen FB (1997) Extra- and intracellular acid-base balance and ionic regulation in cod (Gadus morhua) during combined and isolated exposures to hypercapnia and copper. Marine Biol 128:337-346
41. Law S, Wu R, Ng P, Yu R, Kong R (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 doi:10.1186/1471-2199-7-15
42. Lawrie S, Tancock N, McGrowth N, Roger J (1991) Influence of complexation of the uptake by plants of iron, manganese, copper and zinc. I Effect of EDTA in a multimetal and computer simulation study. J Exp Biol 42:509-515
43. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz A-G, Ahn B-W, Shaltiel S, Stadtman ER (1990) Determination of carbonal content in oxidatively modified proteins. Methods Enzymol 186:464-485
44. Linares E, Nakao LS, Augusto O, Kadiiska MB (2003) EPR studies of in vivo radical production by lipopolysaccharide: potential role of iron mobilized from iron-nitrosyl complexes. Free Rad Biol Med 34:766-773
45. Livingstone DR, Lips F, Martinez PG, Pipe RK (1992) Antioxidant enzymes in the digestive gland of the common mussel Mytilus edulis. Marine Biol 112:265-276
46. 31P-MRS. Am J Physiol, Regul Integr Comp Physiol 283:R1254-R1262
47. Mark FC, Lucassen M, Pörtner HO (2006b) Thermal sensitivity of uncoupling proteins in polar and temperate fish. Comp Biochem Physiol D1:365-374
48. Nikinmaa M (2002) Oxygen-dependent cellular functions-why fishes and their aquatic environment are a prime choice of study. Comp Biochem Physiol 133A:1-16
49. Nikinmaa M, Pursiheimo S, Soitamo AJ (2004) Redox state regulates HIF-1α and its DNA binding and phosphorylation in salmonid cells. J Cell Sci 117:3201-3206
50. Nikinmaa M, Rees BB (2005) Oxygen-dependent gene expression in fishes. Am J Physiol Regul Integr Comp Physiol 288R:1079-1090
51. Minet E, Mottet D, Michel G, Roland I, Raes M, Remacle J, Michiels C (1999) Hypoxia-induced activation of HIF-1: role of HIF-1alpha-Hsp90 interaction. FEBS Lett 460(2):251-256
52. Morin PJ, McMullen DC, Storey KB (2005) HIF-1α involvement in low temperature and anoxia survival by a freeze tolerant insect. Mol Cell Biochem 280:99-106
53. Philipp E, Brey T, Pörtner H-O, Abele D (2005) Chronological and physiological ageing in a polar and a temperate mud clam. Mech Ageing Dev 126:598-609
54. Philipp E, Brey T, Heilmayer O, Abele D, Pörtner H-O (2006) Physiological ageing in a polar and a temperate swimming scallop. Mar Ecol Prog Ser 307:187-198
55. Reed DJ (1990) Glutathione: toxicological implications. Annu Rev Pharmacol Toxicol 30:603-631
56. 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
57. 31P-NMR. J Therm Biol 28:363-371
58. Schafer FQ, Buettner GR (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Rad Biol Med 30:1191-1212
59. Shams I, Nevo E, Avivi A (2004) Ontogenetic expression of erythropoietin and hypoxia inducible factor-1 alpha genes in subterranean blind mole rats. FASEB: doi:10.1096/fj.04-2758fje
60. Soitamo AJ, Rabergh CMI, Gassmann M, Sistonen L, Nikinmaa M (2001) Characterization of a hypoxia-inducible factor (HIF-1α) from rainbow trout. J Biol Chem 276:19677-19705
61. Stroka DM, Burkhardt T, Desbaillets I, Wenger RH, Neil DAH, Gassmann M, Candinas D (2001) HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia. FASEB J 15:2445-2453
62. Uchiyama M, Mihara M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86:271-278
63. Van Dijk PLM, Tesch C, Hardewig I, Pörtner H-O (1999) Physiological disturbances at critically high temperatures: a comparison between stenothermal antarctic and eurythermal temperate eelpouts (Zoarcidae). J Exp Biol 202:3611-3621
64. Vegh M, Marton A,Horvath I (1988) Reduction of Fe(III) ADP complex by liver microsomes. Biochim Biophys Act 964:146-150
65. Vuori KAM, Soitamo A, Vuorinen PJ, Nikinmaa M (2004) Baltic salmon (Salmo salar) yolk-sac fry mortality is associated with disturbances in the function of hypoxia-inducible transcription factor (HIF-1α) and consecutive gene expression. Aquat Toxicol 68:301-313
66. Wenger RH (2000) Mammalian oxygen sensing, signalling and gene regulation. J Exp Biol 203:1253-1263
67. Woodmansee AN, Imlay JA (2002) Meth Enzymol 349:3-9
68. Yegorov DY, Kozlov AV, Azizova OA, Vladimorov YA (1993) Simultaneous determination of Fe(III) and Fe(II) in water solutions and tissue homogenates using desferal and 1,10-phenanthroline. Free Rad Biol Med 15:565-574