Abstract
A rapid decline in temperature poses a major challenge for poikilothermic fish, as their entire metabolism depends on ambient temperature. The gene expression of rainbow trout Oncorhynchus mykiss having undergone such a cold shock (\(0{^{\circ }}\hbox {C}\)) was compared to a control (\(5{^{\circ }}\hbox {C}\)) in a microarray and quantitative real-time PCR based study. The tissues of gill, kidney and liver were examined. The most differently expressed genes were found in liver, many of them contributing to the network ‘cellular compromise, cellular growth and proliferation’. However, the number of genes found to be regulated at \(0{^{\circ }}\hbox {C}\) was surprisingly low. Instead of classical genes involved in temperature shock, the three genes encoding fibroblast growth factor 1 (fgf1), growth arrest and DNA-damage-inducible, alpha (gadd45a) and sclerostin domain-containing protein 1 (sostdc1) were upregulated in the liver upon cold shock in two different rainbow trout strains, suggesting that these genes may be considered as general biomarkers for cold shock in rainbow trout.
References
Anders E. 1986 Stand der Züchtung und reproduktion brackwasseradaptierter Regenbogenforellenbestände im Küstenbereich der DDR. Fischerei -Forsch. 24.
Basu N., Todgham A. E., Ackerman P. A., Bibeau M. R., Nakano K., Schulte P. M. and Iwama G. K. 2002 Heat shock protein genes and their functional significance in fish. Gene 295, 173–183.
Bell M. 1990 Fisheries handbook of engineering requirements and biological criteria. Corps of Engineers, North Pacific Division, Portland, USA.
Benjamini Y. and Hochberg Y. 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 57, 289–300.
Borchel A., Verleih M., Rebl A., Kühn C. and Goldammer T. 2014 Creatine metabolism differs between mammals and rainbow trout (Oncorhynchus mykiss). Springer Plus 3, 510.
Clausen K. A., Blish K. R., Birse C. E., Triplette M. A., Kute T. E., Russell G. B. et al. 2011 SOSTDC1 differentially modulates Smad and beta-catenin activation and is down-regulated in breast cancer. Breast Cancer Res. Treat. 129, 737–746.
Donaldson M. R., Cooke S. J., Patterson D. A. and Macdonald J. S. 2008 Cold shock and fish. J. Fish Biol. 73, 1491–1530.
Feder M. E. and Hofmann G. E. 1999 Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61, 243–282.
Gopal G., Raja U. M., Shirley S., Rajalekshmi K. R. and Rajkumar T. 2013 SOSTDC1 down-regulation of expression involves CpG methylation and is a potential prognostic marker in gastric cancer. Cancer Genet. 206, 174–182.
Gracey A. Y., Fraser E. J., Li W., Fang Y., Taylor R. R., Rogers J. et al. 2004 Coping with cold: an integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. Proc. Natl. Acad. Sci. USA 101, 16970–16975.
Jackson A., Friedman S., Zhan X., Engleka K. A., Forough R. and Maciag T. 1992 Heat shock induces the release of fibroblast growth factor 1 from NIH 3T3 cells. Proc. Natl. Acad. Sci. USA 89, 10691–10695.
Liebermann D. A. and Hoffman B. 2008 Gadd45 in stress signaling. J. Mol. Signal. 3, 15.
Long Y., Song G., Yan J., He X., Li Q. and Cui Z. 2013 Transcriptomic characterization of cold acclimation in larval zebrafish. BMC Genomics 14, 612.
Mininni A. N., Milan M., Ferraresso S., Petochi T., Di Marco P., Marino G. et al. 2014 Liver transcriptome analysis in gilthead sea bream upon exposure to low temperature. BMC Genomics 15, 765.
Mizukoshi E., Suzuki M., Loupatov A., Uruno T., Hayashi H., Misono T. et al. 1999 Fibroblast growth factor-1 interacts with the glucose-regulated protein GRP75/mortalin. Biochem. J. 343, 461–466.
Moskalev A., Plyusnina E., Shaposhnikov M., Shilova L., Kazachenok A. and Zhavoronkov A. 2012 The role of D-GADD45 in oxidative, thermal and genotoxic stress resistance. Cell Cycle 11, 4222–4241.
Rebl A., Verleih M., Köbis J. M., Kühn C., Wimmers K., Köllner B. and Goldammer T. 2013 Transcriptome profiling of gill tissue in regionally bred and globally farmed rainbow trout strains reveals different strategies for coping with thermal stress. Mar. Biotechnol. 15, 445–460.
Roberts R. J., Agius C., Saliba C., Bossier P. and Sung Y. Y. 2010 Heat shock proteins (chaperones) in fish and shellfish and their potential role in relation to fish health: a review. J. Fish Dis. 33, 789–801.
Smyth G. K. 2005 Limma: linear models for microarray data. In Bioinformatics and computational biology solutions using R and Bioconductor (ed. R. Gentleman, V. Carey, W. Huber, R. Irizarry and S. Dudoit), pp. 397–420. Springer, New York, USA.
Tutar L. and Tutar Y. 2010 Heat shock proteins: an overview. Curr. Pharm. Biotechnol. 11, 216–222.
Verleih M., Borchel A., Krasnov A., Rebl A., Korytář T., Kühn C. and Goldammer T. 2015 Impact of thermal stress on kidney-specific gene expression in farmed regional and imported rainbow trout. Mar. Biotechnol. 17, 576–592.
Xu H., Zhang D. L., Yu D. H., Lv C. H., Luo H. Y. and Wang Z. Y. 2015 Molecular cloning and expression analysis of scd1 gene from large yellow croaker Larimichthys crocea under cold stress. Gene 568, 100–108.
Acknowledgements
This project was funded by the European Fisheries Fund (EFF) and the Ministry of Agriculture, the Environment and Consumer Protection Mecklenburg-Western Pomerania (pilot project: Rainbow trout BORN; VI-560/7308-4). Carsten Kühn is gratefully acknowledged for keeping the fish. Ingrid Hennings, Brigitte Schöpel, Luisa Falkenthal and Marlies Fuchs are acknowledged for expert technical assistance.
Author information
Authors and Affiliations
Corresponding author
Additional information
Corresponding editor: Silvia Garagna
Rights and permissions
About this article
Cite this article
Borchel, A., Verleih, M., Rebl, A. et al. Identification of genes involved in cold-shock response in rainbow trout (Oncorhynchus mykiss). J Genet 96, 701–706 (2017). https://doi.org/10.1007/s12041-017-0811-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12041-017-0811-x