Abstract
Gene expression profiles during the transition from fasting to refeeding were investigated in the gut and liver of Masu salmon Oncorhynchus masou masou. Fish were starved for 3 days and then fed at 3% of body weight. The gut and liver were resected before and after feeding, and the tissues were used for transcriptome analyses. Twenty-nine and 45 genes were more than eightfold differently expressed in the gut and liver, respectively. Genes involved in fatty acid and carbohydrate metabolism were differentially expressed in the liver tissues. Genes involved in protein folding, such as GRP78 and endoplasmin, were significantly upregulated in both organs at 6, 12, and 24 h after feeding. Furthermore, glycogen synthase kinase (GSK) 3-binding protein, a negative regulator of GSK with pivotal roles in stress response, was downregulated in both organs 6 h after feeding. These results suggest that the change in nutritional status from fasting to refeeding is accompanied by cellular stress.
Similar content being viewed by others
References
Beurel E, Grieco SF, Jope RS (2015) Glycogen synthase kinase-3 (GSK3): regulation, actions, and diseases. Pharmacol Ther 148:114–131. https://doi.org/10.1016/j.pharmthera.2014.11.016
Caruso M, Sheridan M (2011) New insights into the signaling system and function of insulin in fish. Gen Comp Endocr 173:227–247. https://doi.org/10.1016/j.ygcen.2011.06.014
Chen B, Piel WH, Gui L, Bruford E, Monteiro A (2005) The HSP90 family of genes in the human genome: insights into their divergence and evolution. Genomics 86:627–637. https://doi.org/10.1016/j.ygeno.2005.08.012
Cossins AR, Crawford DL (2005) Fish as models for environmental genomics. Nat Rev Genet 6:324–333. https://doi.org/10.1038/nrg1590
Dentin R, Girard J, Postic C (2005) Carbohydrate responsive element binding protein (ChREBP) and sterol regulatory element binding protein-1c (SREBP-1c): two key regulators of glucose metabolism and lipid synthesis in liver. Biochimie 87:81–86. https://doi.org/10.1016/j.biochi.2004.11.008
Foufelle F, Ferré P (2002) New perspectives in the regulation of hepatic glycolytic and lipogenic genes by insulin and glucose: a role for the transcription factor sterol regulatory element binding protein-1c. Biochem J 366:377–391. https://doi.org/10.1042/BJ20020430
Garcia de la Serrana D, Johnston IA (2013) Expression of heat shock protein (Hsp90) paralogues is regulated by amino acids in skeletal muscle of Atlantic salmon. PLoS One 8:e74295. https://doi.org/10.1371/journal.pone.0074295
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. https://doi.org/10.1038/nbt.1883
Haas IG (1994) BiP (GRP78), an essential hsp70 resident protein in the endoplasmic reticulum. Experientia 50:1012–1020. https://doi.org/10.1007/BF01923455
Hemre GI, Mommsen TP, Krogdahl A (2002) Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac Nutr 8:175–194. https://doi.org/10.1046/j.1365-2095.2002.00200.x
Huang A, Patel S, McAlpine CS, Werstuck GH (2018) The role of endoplasmic reticulum stress-glycogen synthase kinase-3 signaling in atherogenesis. Int J Mol Sci 19:E1607. https://doi.org/10.3390/ijms19061607
Johansen KA, Overturf K (2006) Alterations in expression of genes associated with muscle metabolism and growth during nutritional restriction and refeeding in rainbow trout. Comp Biochem Physiol B: Biochem Mol Biol 144:119–127. https://doi.org/10.1016/j.cbpb.2006.02.001
Kondo H, Suda S, Kawana Y, Hirono I, Nagasaka R, Kaneko G, Ushio H, Watabe S (2012) Effects of feed restriction on the expression profiles of the glucose and fatty acid metabolism-related genes in rainbow trout Oncorhynchus mykiss muscle Fish Sci 78:1205–1211. https://doi.org/10.1007/s12562-012-0543-z
Little E, Ramakrishnan M, Roy B, Gazit G, Lee AS (1994) The glucose-regulated proteins (GRP78 and GRP94): functions, gene regulation, and applications. Crit Rev Eukaryot Gene Expr 4:1–18. https://doi.org/10.1615/critreveukargeneexpr.v4.i1.10
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Love RM (1980) The chemical biology of fishes, vol 2. AcademicPress, New York
Martin SAM, Król E (2017) Nutrigenomics and immune function in fish: new insights from omics technologies. Dev Comp Immunol 75:86–98. https://doi.org/10.1016/j.dci.2017.02.024
Maurer U, Preiss F, Brauns-Schubert P, Schlicher L, Charvet C (2014) GSK-3—at the crossroads of cell death and survival. J Cell Sci 127:1369–1378. https://doi.org/10.1242/jcs.138057
Mekuchi M, Sakata K, Yamaguchi T, Koiso M, Kikuchi J (2017) Trans-omics approaches used to characterise fish nutritional biorhythms in leopard coral grouper (Plectropomus leopardus). Sci Rep 7:9372. https://doi.org/10.1038/s41598-017-09531-4
Navarro I, Rojas P, Capilla E, Albalat A, Castillo J, Montserrat N, Codina M, Gutiérrez J (2002) Insights into insulin and glucagon responses in fish. Fish Physiol Biochem 27:205–216. https://doi.org/10.1023/b:fish.0000032726.78074.04
Qian X, Ba Y, Zhuang Q, Zhong G (2014) RNA-Seq technology and its application in fish transcriptomics. OMICS 18(2):98–110. https://doi.org/10.1089/omi.2013.0110
Rescan PY, Montfort J, Rallière C, Le Cam A, Esquerré D, Hugot K (2007) Dynamic gene expression in fish muscle during recovery growth induced by a fasting-refeeding schedule. BMC Genomics 8:438. https://doi.org/10.1186/1471-2164-8-438
Salem M, Silverstein J, Rexroad CE 3rd, Yao J (2007) Effect of starvation on global gene expression and proteolysis in rainbow trout (Oncorhynchus mykiss). BMC Genomics 8:328. https://doi.org/10.1186/1471-2164-8-328
Sasako T, Ohsugi M, Kubota N, Itoh S, Okazaki Y, Terai A, Kubota T, Yamashita S, Nakatsukasa K, Kamura T, Iwayama K, Tokuyama K, Kiyonari H, Furuta Y, Shibahara J, Fukayama M, Enooku K, Okushin K, Tsutsumi T, Tateishi R, Tobe K, Asahara H, Koike K, Kadowaki T, Ueki K (2019) Hepatic Sdf2l1 controls feeding-induced ER stress and regulates metabolism. Nat Commun 10:947. https://doi.org/10.1038/s41467-019-08591-6
Schröder M, Kaufman RJ (2005) ER stress and the unfolded protein response. Mutat Res 569:29–63. https://doi.org/10.1016/j.mrfmmm.2004.06.056
Slimen IB, Najar T, Ghram A, Dabbebi H, Ben Mrad M, Abdrabbah M (2014) Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage. A review. Int J Hyperthermia 30:513–523. https://doi.org/10.3109/02656736.2014.971446
Sudhagar A, Kumar G, El-Matbouli M (2018) Transcriptome analysis based on RNA-Seq in understanding pathogenic mechanisms of diseases and the immune system of fish: a comprehensive review. Int J Mol Sci 19:E245. https://doi.org/10.3390/ijms19010245
Sul HS, Latasa MJ, Moon Y, Kim KH (2000) Regulation of the fatty acid synthase promoter by insulin. J Nutr 130:315S–320S. https://doi.org/10.1093/jn/130.2.315S
Tacchi L, Bickerdike R, Douglas A, Secombes CJ, Martin SA (2011) Transcriptomic responses to functional feeds in Atlantic salmon (Salmo salar). Fish Shellfish Immunol 31:704–715. https://doi.org/10.1016/j.fsi.2011.02.023
Zhu G, Lee AS (2015) Role of the unfolded protein response, GRP78 and GRP94 in organ homeostasis. J Cell Physiol 230:1413–1420. https://doi.org/10.1002/jcp.24923
Acknowledgements
This work was partly supported by JSPS KAKENHI Grant Number 18H03958.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kondo, H., Sano, H., Wang, Y. et al. Starvation–refeeding causes cellular stress responses in the gut and liver of Masu salmon Oncorhynchus masou masou. Fish Sci 86, 1037–1042 (2020). https://doi.org/10.1007/s12562-020-01464-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12562-020-01464-8