Environmental acidification triggers oxidative stress and enhances globin expression in zebrafish gills

Biochemical and Biophysical Research Communications

Volumn 441, Issue 3, 2013, Pages 624-629

  Tiedke, Jessica ^a   Cubuk, Ceyda ^a   Burmester, Thorsten ^a  

^a UNIVERSITY OF HAMBURG   (Germany)

Author keywords

Acidification; Myoglobin; Neuroglobin; Oxidative stress

Indexed keywords

GLOBIN;

ACIDIFICATION; AEROBIC METABOLISM; ANIMAL EXPERIMENT; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; ENERGY METABOLISM; ENVIRONMENTAL ACIDIFICATION; GILL; MOLECULAR CLONING; MOLECULAR MECHANICS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; STRESS; WESTERN BLOTTING; ZEBRA FISH;

ANIMALIA; DANIO RERIO;

ACIDIFICATION; MYOGLOBIN; NEUROGLOBIN; OXIDATIVE STRESS;

ACIDS; ANIMALS; FRESH WATER; GENE EXPRESSION; GENE-ENVIRONMENT INTERACTION; GILLS; GLOBINS; HYDROGEN-ION CONCENTRATION; MYOGLOBIN; NERVE TISSUE PROTEINS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84888297068     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2013.10.104     Document Type: Article

References (43)

1. Strayer D.L., Dudgeon D. Freshwater biodiversity conservation: recent progress and future challenges. J. N. Am. Benthol. Soc. 2010, 29:344-358.
2. Ormerod S.J., Dobson M., Hildrew A.G., Townsend C.R. Multiple stressors in freshwater ecosystems. Freshw. Biol. 2010, 55:1-4.
3. Cappuyns V., Swennen R. Kinetics of element release during combined oxidation and pH leaching of anoxic river sediments. Appl. Geochem. 2005, 20:1169-1179.
4. Moiseenko T.I. Effects of acidification on aquatic ecosystems. Russ. J. Ecol. 2005, 36:93-102.
5. Evans D.H., Piermarini P.M., Choe K.P. The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol. Rev. 2005, 85:97-177.
6. Eneji I.S., Sha R., Annune L. Bioaccumulation of heavy metals in fish (Tilapia zilli and Clarias gariepinus) organs from river Benue, North Central Nigeria. Pak. J. Anal. Environ. Chem. 2011, 12:25-31.
7. Kültz D. Evolution of the cellular stress proteome: from monophyletic origin to ubiquitous function. J. Exp. Biol. 2003, 206:3119-3124.
8. Williams L.M., Oleksiak M.F. Signatures of selection in natural populations adapted to chronic pollution. BMC Evol. Biol. 2008, 8:1-12.
9. Kurutas E.B., Sahan A., Altun T. Oxidative stress biomarkers in liver and gill tissues of spotted barb (Capoeta barroisi Lortet, Living in the river Ceyhan, Adana, Turkey. Turk. J. Biol. 1894, 33(2009):275-282.
10. Pandey S., Parvez S., Sayeed I., Haque R., Bin-Hafeez B., Raisuddin S. Biomarkers of oxidative stress: a comparative study of river Yamuna fish Wallago attu (Bl. & Schn.). Sci. Total Environ. 2003, 309:105-115.
11. Apel K., Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 2004, 55:373-399.
12. Beckman K.B., Ames B.N. The free radical theory of aging matures. Physiol. Rev. 1998, 78:547-581.
13. Free Radicals in Biology and Medicine 2007, Oxford University Press Inc, New York. B. Halliwell, J. Gutteridge (Eds.).
14. Flögel U., Gödecke A., Klotz L.O., Schrader J. Role of myoglobin in the antioxidant defense of the heart. FASEB J. 2004, 18:1156-1158.
15. Fordel E., Thijs L., Martinet W., Lenjou M., Laufs T., Van Bockstaele D., Moens L., Dewilde S. Neuroglobin and cytoglobin overexpression protects human SH-SY5Y neuroblastoma cells against oxidative stress-induced cell death. Neurosci. Lett. 2006, 410:146-151.
16. Li R.C., Guo S.Z., Lee S.K., Gozal D. Neuroglobin protects neurons against oxidative stress in global ischemia. J. Cereb. Blood Flow Metab. 2010, 30:1874-1882.
17. Fang J., Ma I., Allalunis-Turner J. Knockdown of cytoglobin expression sensitizes human glioma cells to radiation and oxidative stress. Radiat. Res. 2011, 176:198-207.
18. Awenius C., Hankeln T., Burmester T. Neuroglobins from the zebrafish Danio rerio and the pufferfish Tetraodon nigroviridis. Biochem. Biophys. Res. Commun. 2001, 287:418-421.
19. Burmester T., Ebner B., Weich B., Hankeln T. Cytoglobin: a novel globin type ubiquitously expressed in vertebrate tissues. Mol. Biol. Evol. 2002, 19:416-421.
20. Roesner A., Fuchs C., Hankeln T., Burmester T. A globin gene of ancient evolutionary origin in lower vertebrates: evidence for two distinct globin families in animals. Mol. Biol. Evol. 2005, 22:12-20.
21. -δδCT method. Methods 2001, 25:402-408.
22. Stoschek C.M. Quantitation of protein. Methods Enzymol. 1990, 182:50-68.
23. Fuchs C., Heib V., Kiger L., Haberkamp M., Roesner A., Schmidt M., Hamdane D., Marden M.C., Hankeln T., Burmester T. Zebrafish reveals different and conserved features of vertebrate neuroglobin gene structure, expression pattern, and ligand binding. J. Biol. Chem. 2004, 279:24116-24122.
24. Porter A.G., Jänicke R.U. Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 1999, 6:99-104.
25. Deng Y., Ren X., Yang L., Lin Y., Wu X. A JNK-dependent pathway is required for TNFalpha-induced apoptosis. Cell 2003, 115:61-70.
26. Sanders B.M., Nguyen J., Martin L.S., Howe S.R., Coventry S. Induction and subcellular localization of two major stress proteins in response to copper in the fathead minnow Pimephales promelas. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 1995, 112:335-343.
27. Williams J.H., Farag A.M., Stansbury M.A., Young P.A., Bergman H.L., Petersen N.S. Accumulation of Hsp70 in juvenile and adult rainbow trout gill exposed to metal-contaminated water and/or diet. Environ. Toxicol. Chem. 1996, 15:1324-1328.
28. Parsell D.A., Lindquist S. The function of heat-shock proteins in stress tolerance - degradation and reactivation of damaged proteins. Annu. Rev. Genet. 1993, 27:437-496.
29. Göthel S.F., Marahiel M.A. Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell. Mol. Life Sci. 1999, 55:423-436.
30. Andreeva L., Heads R., Green C.J. Cyclophilins and their possible role in the stress response. Int. J. Exp. Pathol. 1999, 80:305-315.
31. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417:1-13.
32. Tomanek L. Environmental Proteomics: changes in the proteome of marine organisms in response to environmental stress, pollutants, infection, symbiosis, and development. Annu. Rev. Mar. Sci. 2011, 3:373-399.
33. Weber A.K., Pirow R. Physiological responses of Daphnia pulex to acid stress. BMC Physiol. 2009, 9:9.
34. Michaelidis B., Spring A., Portner H.O. Effects of long-term acclimation to environmental hypercapnia on extracellular acid-base status and metabolic capacity in Mediterranean fish Sparus aurata. Mar. Biol. 2007, 150:1417-1429.
35. Giulivi C., Davies K.J. A novel antioxidant role for hemoglobin. The comproportionation of ferrylhemoglobin with oxyhemoglobin. J. Biol. Chem. 1990, 265:19453-19460.
36. Burmester T., Hankeln T. What is the function of neuroglobin?. J. Exp. Biol. 2009, 212:1423-1428.
37. Hankeln T., Ebner B., Fuchs C., Gerlach F., Haberkamp M., Laufs T.L., Roesner A., Schmidt M., Weich B., Wystub S., Saaler-Reinhardt S., Reuss S., Bolognesi M., De Sanctis D., Marden M.C., Kiger L., Moens L., Dewilde S., Nevo E., Avivi A., Weber R.E., Fago A., Burmester T. Neuroglobin and cytoglobin in search of their role in the vertebrate globin family. J. Inorg. Biochem. 2005, 99:110-119.
38. Cossins A.R., Williams D.R., Foulkes N.S., Berenbrink M., Kipar A. Diverse cell-specific expression of myoglobin isoforms in brain, kidney, gill and liver of the hypoxia-tolerant carp and zebrafish. J. Exp. Biol. 2009, 212:627-638.
39. Fraser J., de Mello L.V., Ward D., Rees H.H., Williams D.R., Fang Y., Brass A., Gracey A.Y., Cossins A.R. Hypoxia-inducible myoglobin expression in nonmuscle tissues. Proc. Natl. Acad. Sci. USA 2006, 103:2977-2981.
40. van der Meer D.L., van den Thillart G.E., Witte F., de Bakker M.A., Besser J., Richardson M.K., Spaink H.P., Leito J.T., Bagowski C.P. Gene expression profiling of the long-term adaptive response to hypoxia in the gills of adult zebrafish. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 289:R1512-R1519.
41. Wittenberg J.B., Wittenberg B.A. Myoglobin function reassessed. J. Exp. Biol. 2003, 206:2011-2020.
42. Flögel U., Fago A., Rassaf T. Keeping the heart in balance: the functional interactions of myoglobin with nitrogen oxides. J. Exp. Biol. 2010, 213:2726-2733.
43. Roesner A., Hankeln T., Burmester T. Hypoxia induces a complex response of globin expression in zebrafish (Danio rerio). J. Exp. Biol. 2006, 209:2129-2137.