Abstract
Growth in fish is regulated in part by the growth hormone (GH)-insulin-like growth factor (IGF) axis, and salmon transgenic for GH are known to show dramatic increased growth. However, little is known concerning the in vivo global levels of metabolites and the mechanism of enhancement of growth in GH transgenic vertebrates. The present study examined the charged metabolites levels in GH transgenic coho salmon (Oncorhynchus kisutch) overexpressing GH by metabolomic analysis. Triplicate groups of size-matched (0 year-old, approx. 60 g) and age-matched (1.5 years-old) GH transgenic (T) and non-transgenic (NT) wild salmon were quantitatively assessed for levels of approximately 200 metabolites in both muscle and liver. The most notable difference found between T and NT fish was that glycolysis metabolite levels were increased in the muscle of transgenic fish. In addition, an increase in some metabolite levels in the transgenic fish muscle was found to be enhanced by ration-restriction. However, these effects observed in muscle were different from that seen in liver. The results suggest that GH transgenesis can improve the use of carbohydrates as a source of energy associated with rapid growth. These effects are likely to depend on the level of total digestible energy intake and type of tissue in transgenic fish.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Change history
07 June 2019
In the original version of the book, the following corrections have been incorporated:
- 1.
Chapter 18 was published with incorrect figures and affiliations of the authors.
- 1.
References
Björnsson BT (1997) The biology of salmon growth hormone: from daylight to dominance. Fish Physiol Biochem 17:9–24
Björnsson BT, Johansson V, Benedet S, Einarsdottir E, Hildahl J, Agustsson T, Jonsson E (2002) Growth hormone endocrinology of salmonids: regulatory mechanisms and mode of action. Fish Physiol Biochem 27:227–242
Deane EE, Woo NYS (2009) Modulation of fish growth hormone levels by salinity, temperature, pollutants and aquaculture related stress: a review. Rev Fish Biol Fish 19:97–120
Deane EE, Woo NYS (2011) Advances and perspectives on the regulation and expression of piscine heat shock proteins. Rev Fish Biol Fish 21:153–185
Devlin RH, Yesaki TY, Biagi C, Donaldson EM, Swanson P, Chan W-K (1994) Extraordinary salmon growth. Nature 371:209–210
Devlin RH, Yesaki TY, Donaldson EM, Hew CL (1995) Transmission and phenotypic effects of an antifreeze/GH gene construct in coho salmon (Oncorhynchus kisutch). Aquaculture 137:161–169
Devlin RH, Biagi C, Yesaki TY, Smailus DE, Byatt JC (2001) Growth of domesticated transgenic fish. Nature 409:781–782
Devlin RH, Biagi C, Yesaki TY (2004) Growth, viability and genetic characteristics of GH transgenic coho salmon strains. Aquaculture 236:607–632
Devlin RH, Sakhrani D, Tymchuk WE, Rise ML, Goh B (2009) Domestication and growth hormone transgenesis cause similar changes in gene expression in coho salmon (Oncorhynchus kisutch). Proc Nat Acad Sci USA 106:3047–3052
Devlin RH, Sundstrom LF, Rosalind AL (2015) Assessing ecological and evolutionary consequences of growth-accelerated genetically engineered fishes. Bioscience 65:685–700
Donaldson EM, Fagerlund UHM, Higgs DA, McBride JR (1979) Hormonal enhancement of growth. In: Hoar WS, Randall DJ, Brett JR (eds) Bioenergetics and Growth, Fish Physiology. Academic Press, New York, pp 455–597
Du SJ, Gong Z, Fletcher GI, Shears MA, King MJ, Idler DR, Hew CL (1992) Growth enhancement in transgenic Atlantic salmon by the use of an “all fish” chimeric growth hormone gene construct. Nat Biotechnol 10:176–181
Duan C (1998) Nutritional and developmental regulation of insulin-like growth factors in fish. J Nutr 128:306S–314S
Gatlin DM III, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, Herman E, Hu G, Krogdahl A, Nelson R, Overturf K, Rust M, Sealey W, Skonberg D, Souza EJ, Stone D, Wilson R, Wurtele E (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquacult Res 38:551–579
Hadjimichael M, Delaney A, Kaiser MJ, Edwards-Jones G (2013) How resilient are Europe’s inshore fishing communities to change? differences between the north and the south. Ambio 42:1037–1046
Higgs DA, Sutton JN, Kim H, Oakes JD, Smith J, Biagi C, Rowshandeli M, Devlin RH (2009) Influence of dietary concentrations of protein, lipid and carbohydrate on growth, protein and energy utilization, body composition, and plasma titres of growth hormone and insulin-like growth factor-1 in non -transgenic and growth hormone transgenic coho salmon, Oncorhynchus kisutch (Walbaum). Aquaculture 286:127–137
Hill AJ, Kiessling A, Devlin RH (2000) Coho salmon (Oncorhynchus kisutch) transgenic for a growth hormone gene construct exhibit increased rates of muscle hyperplasia and detectable levels of differential gene expression. Can J Fish Aqua Sci 57:939–950
Hirayama A, Kami K, Sugimoto M, Sugawara M, Toki N, Onozuka H, Kinoshita T, Saito N, Ochiai A, Tomita M, Esumi H, Soga T (2009) Quantitative metabolome profiling of colon and stomach cancer microenvironment by capillary electrophoresis time-of-flight mass spectrometry. Cancer Res 69:4918–4925
Huang C-H, Higgs DA, Balfry SK, Devlin RH (2004) Effect of dietary vitamin E level on growth, tissue lipid peroxidation, and erythrocyte fragility of transgenic coho salmon, Oncorhynchus kisutch. Comp Biochem Physiol 139A:199–204
Kim J-H, Leggatt RA, Chan M, Vokoff H, Devlin RH (2015) Effects of chronic growth hormone overexpression on appetite-regulating brain gene expression in coho salmon. Mol Cell Endocrinol 413:178–188
Krasnov A, Agren JJ, Pitkanen TI, Molsa H (1999) Transfer of growth hormone (GH) transgenes into Arctic charr (Salvelinus alpinus L.) II. Nutrient partitioning in rapidly growth fish. Gen Analysis 15:99–105
Krogdahl A, Hemre G-I, Mommsen TP (2005) Carbohydrates in fish nutrition: digestion and absorption inpostlarval stages. Aquac Nutr 11:103–122
Ledford H (2015) Transgenic salmon leaps to the dinner table. Nature 527:417–418
Leggatt RA, Raven P, Mommsen TP, Sakhrani D, Higgs DA, Devlin RH (2009) Growth hormone transgenic influences carbohydrate, lipid and protein metabolism capacity for energy production in coho salmon (Oncorhynchus kisutch). Comp Biochem Physiol 154B:121–133
Leggatt RA, Hollo T, Vandersteen WE, McFarlane K, Goh B, Prevost J, Devlin RH (2014) Rearing in seawater mesocosms improves the spawning performance of growth hormone transgenic and wild type coho salmon. PLoS ONE 9:e105377
Leung LY, Woo NYS (2010) Effects of growth hormone, insulin-like growth factor I, triiodothyronine, thyroxine, and cortisol on gene expression of carbohydrate metabolic enzymes in sea bream hepatocytes. Comp Biochem Physiol 157A:272–282
Lohmus M, Sundstrom LF, Bjorklund M, Devlin RH (2010) Genotype-temperature interaction in the regulation of development, growth, and morphometrics in wild-type, and growth-hormone transgenic coho salmon. PLoS ONE 5:e9980
Mori T, Devlin RH (1999) Transgene and host GH gene expression in pituitary and nonpituitary tissues of normal and GH transgenic salmon. Mol Cell Endocrinol 149:129–139
Moriyama S, Ayson FG, Kawauchi H (2000) Growth regulation by insulin-like growth factor-I in fish. Biosci Biotech Biochem 64:1553–1562
Nakano T (2007) Microorganisms. In: Nakagawa H, Sato M, Gatlin DM III (eds) Dietary supplements for the health and quality of cultured fish. CAB International, Oxfordshire, UK, pp 86–108
Nakano T (2011) Stress in fish. Yoshoku (Aquaculture Magazine) 48:64–67
Nakano T, Shoji Y, Shirakawa H, Suda Y, Yamaguchi T, Sato M, Devlin RH (2011) Daily expression patterns of growth-related genes in growth hormone transgenic coho salmon, Oncorhynchus kisutch. La mer 49:111–117
Nakano T, Afonso LO, Beckman BR, Iwama GK, Devlin RH (2013) Acute physiological stress down-regulates mRNA expressions of growth-related genes in coho salmon. PLoS ONE 8:e71421
Nakano T, Kameda M, Yamaguchi T, Sato M, Afonso LOB, Beckman BR, Iwama GK, Devlin RH (2015) Effect of thermal stressors on growth-related gene expressions in cultured fish. In: Ceccaldi H-J, Hénocque Y, Koike Y, Komatsu T, Stora G, Tusseau-Vuillemin M-H (eds) Marine productivity: perturbations and resilience of socio-ecosystems. Springer International Publishing AG, Cham, Switzerland, pp 147–157
Nakano T (2016) Studies on stress and stress tolerance mechanisms in fish. Nippon Suisan Gakkaishi 82:278–281
Naylor RL, Goldburg RJ, Primavera JH, Kautsky N, Beveridge MCM, Clay J, Folke C, Lubchenco J, Mooney H, Troell M (2000) Effect of aquaculture on world fish supplies. Nature 405:1017–1024
Naylor RL, Hardy RW, Bureau DP, Chiu A, Elliott M, Farrell AP, Forster I, Gatlin DM, Goldburg RJ, Hua K, Nichols PD (2009) Feeding aquaculture in an era of finite resources. Proc Nat Acad Sci USA 106:15103–15110
Oakes JD, Higgs DA, Eales JG, Devlin RH (2007) Influence of ration level on the growth performance and body composition of non-transgenic and growth-hormone-transgenic coho salmon (Oncorhynchus kisutch). Aquaculture 265:309–324
Overturf K, Barrows FT, Hardy RW (2013) Effect and interaction of rainbow trout strain (Oncorhynchus mykiss) and diet type on growth and nutrient retention. Aquacult Res 44:604–611
Panserat S, Kamalam BS, Fournier J, Plagnes-Juan E, Woodward K, Devlin RH (2014) Glucose metabolic gene expression in growth hormone transgenic coho salmon. Comp Biochem Physiol 170A:38–45
Pauly D, Christensen V, Guenette S, Pitcher TJ, Sumaila UR, Walters CJ, Watson R, Zeller D (2002) Towards sustainability in world fisheries. Nature 418:689–695
Raven P, Devlin RH, Higgs DA (2006) Influence of dietary digestible energy content on growth, protein and energy utilization and body composition of growth hormone transgenic and non-transgenic coho salmon (Oncorhynchus kisutch). Aquaculure 254:730–747
Raven P, Uh M, Sakhrani D, Beckman BR, Cooper K, Pinter J, Leder EH, Silverstein J, Devlin RH (2008) Endocrine effects of growth hormone overexpression in transgenic coho salmon. Gen Comp Endocrinol 159:26–37
Reichardt T (2000) Will souped up salmon sink or swim? Nature 406:10–12
Reineck M (2010) Influences of the environment on the endocrine and paracrine fish growth hormone-insulin-like growth factor-I system. J Fish Biol 76:1233–1254
Rise ML, Douglas SE, Sakhrani D, Williams J, Ewart KV, Rise M, Davidson WS, Koop BF, Devlin RH (2006) Multiple microarray platforms utilized for hepatic gene expression profiling of GH transgenic coho salmon with and without ration restriction. J Mol Endocrinol 37:259–282
Soga T, Ohashi Y, Ueno Y, Naraoka H, Tomita M, Nishioka T (2003) Quantitative metabolome analysis using capillary electrophoresis mass spectrometry. J Proteome Res 2:488–494
Stokstad E (2002) Engineered fish: Friend or foe of the environment? Science 297:1797–1799
Sugiyama M, Takenaga F, Kitani Y, Yamamoto G, Okamoto H, Masaoka T, Araki K, Nagoya H, Mori T (2012) Homozygous and heterozygous GH transgenesis alters fatty acid composition and content in the liver of Amago salmon (Oncorhynchus masou ishikawae). Biology Open 1:1035–1042
Tacon AGJ, Metian M (2008) Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: Trends and future prospects. Aquaculture 285:146–158
Takeuchi T (2009) Carbohydrate. In: Watanabe T (ed) Nutrition and Feeding in Fish and Crustaceans. Kouseisha Kouseikaku, Tokyo, pp 106–114
Yamamoto T, Murashita K, Matsunari H, Oku H, Furuita H, Okamoto H, Amano S, Suzuki N (2015) Selectively bred juvenile F2 amago salmon Oncorhynchus masou ishikawae fed a low fishmeal diet exhibit growth comparable to unselected juveniles fed a fishmeal-based diet. Fish Sci 81:83–93
Yanai H (1998) Excell Statistics. OMS Publishing, Tokorozawa, Saitama, Japan
Acknowledgements
The authors thank staff at Center for Aquaculture and Environment Research, Fisheries and Oceans Canada, Institute for Advanced Biosciences, Keio University, Japan, and Dr. T. Fujimoto at Hokkaido University, Japan for assistance with lab work. TN acknowledges Dr. J. G. Richards, Mr. D. Chung and Miss. H. Bryant at Department of Zoology, The University of British Columbia, Canada, and Drs. M. Sato, T. Yamaguchi, Y. Ochiai, and I. Gleadall at Tohoku University, Japan for valuable discussion. This study was supported in part by KAKENHI grant (#23580277) and a fund to Core-to-Core Program (A. Advanced Research Networks) entitled “Establishment of international agricultural immunology research-core for a quantum improvement in food safety” from JSPS to TN and by the Canadian Regulatory System for Biotechnology to RHD.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this paper
Cite this paper
Nakano, T., Shirakawa, H., Yeo, G., Devlin, R.H., Soga, T. (2019). Metabolome Profiling of Growth Hormone Transgenic Coho Salmon by Capillary Electrophoresis Time-of-Flight Mass Spectrometry. In: Komatsu, T., Ceccaldi, HJ., Yoshida, J., Prouzet, P., Henocque, Y. (eds) Oceanography Challenges to Future Earth. Springer, Cham. https://doi.org/10.1007/978-3-030-00138-4_18
Download citation
DOI: https://doi.org/10.1007/978-3-030-00138-4_18
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-00137-7
Online ISBN: 978-3-030-00138-4
eBook Packages: Earth and Environmental ScienceEarth and Environmental Science (R0)