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GH–IGF system regulation of attenuated muscle growth and lipolysis in Atlantic salmon reared at elevated sea temperatures

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Abstract

Growth regulation in adult Atlantic salmon (1.6 kg) was investigated during 45 days in seawater at 13, 15, 17, and 19 °C. We focused on feed intake, nutrient uptake, nutrient utilization, and endocrine regulation through growth hormone (GH), insulin-like growth factors (IGF), and IGF-binding proteins (IGFBP). During prolonged thermal exposure, salmon reduced feed intake and growth. Feed utilization was reduced at 19 °C after 45 days compared with fish at lower temperatures, and body lipid storage was depleted with increasing water temperature. Although plasma IGF-1 concentrations did not change, 32-Da and 43-kDa IGFBP increased in fish reared at ≤17 °C, and dropped in fish reared at 19 °C. Muscle igf1 mRNA levels were reduced at 15 and 45 days in fish reared at 15, 17, and 19 °C. Muscle igf2 mRNA levels did not change after 15 days in response to increasing temperature, but were reduced after 45 days. Although liver igf2 mRNA levels were reduced with increasing temperatures after 15 and 45 days, temperature had no effect on igf1 mRNA levels. The liver igfbp2b mRNA level, which corresponds to circulating 43-kDa IGFBP, exhibited similar responses after 45 days. IGFBP of 23 kDa was only detected in plasma in fish reared at 17 °C, and up-regulation of the corresponding igfbp1b gene indicated a time-dependent catabolic response, which was not observed in fish reared at 19 °C. However, higher muscle ghr mRNA levels were detected in fish at 17 and 19 °C than in fish at lower temperatures, indicating lipolytic regulation in muscle. These results show that the reduction of muscle growth in large salmon is mediated by decreased igf1 and igf2 mRNA levels in addition to GH-associated lipolytic action to cope with prolonged thermal exposure. Accordingly, 13 °C appears to be a more optimal temperature for the growth of adult Atlantic salmon at sea.

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References

  • Beckman BR (2011) Perspectives on concordant and discordant relations between insulin-like growth factor 1 (IGF1) and growth in fishes. Gen Comp Endocrinol 170:233–252

    Article  PubMed  CAS  Google Scholar 

  • Benedito-Palos L, Saera-Vila A, Calduch-Giner J-A, Kaushik S, Pérez-Sánchez J (2007) Combined replacement of fish meal and oil in practical diets for fast growth in juveniles of gilthead sea bream (Sparus aurata L.): networking of systemic and local components of GH/IGF axis. Aquaculture 267:199–212

    Article  CAS  Google Scholar 

  • Bower NI, Li XJ, Taylor R, Johnston IA (2008) Switching to fast growth: the insulin-like growth factor (IGF) system in skeletal muscle of Atlantic salmon. J Exp Biol 211:3859–3870

    Article  PubMed  CAS  Google Scholar 

  • Daughaday WH, Mariz IK, Blethen SL (1980) Inhibition of access of bound somatomedin to membrane receptor and immunobinding sites: a comparison of radioreceptor and radioimmunoassay of somatomedin in native and acid-ethanol-extracted serum. J Clin Endocrinol Metabol 51:781–788

    Article  CAS  Google Scholar 

  • Duan CM (1998) Nutritional and developmental regulation of insulin-like growth factors in fish. J Nutr 128:306S–314S

    PubMed  CAS  Google Scholar 

  • Elliott JM (1991) Tolerance and resistance to thermal stress in juvenile Atlantic salmon, Salmo salar. Freshw Biol 25:61–70

    Article  Google Scholar 

  • Elliott JM, Ellott JA (2010) Temperature requirements of Atlantic salmon Salmo salar, brown trout Salmo trutta and Arctic charr Salvelinus alpines: predicting the effects of climate change. J Fish Biol 77:1793–1817

    Article  PubMed  CAS  Google Scholar 

  • El-Mowafi A, Ruohonen K, Hevrøy EM, Espe M (2010) Impact of digestible energy levels at three different dietary amino acid levels on growth performance and protein accretion in Atlantic salmon. Aquac Res 41:373–384

    Article  CAS  Google Scholar 

  • Farrell AP, Eliason EJ, Sandblom E, Clark TD (2009) Fish cardiorespiratory physiology in an area of climate change. Can J Zool 87:835–851

    Article  CAS  Google Scholar 

  • Gómez-Requeni P, Mingarro M, Calduch-Giner JA, Médale F, Martin SAM, Houlihan DF, Kaushik SJ, Perez-Sanchez J (2004) Protein growth performance, amino acid utilisation and somatotropic axis responsiveness to fish meal replacement by plant protein sources in gilthead sea bream (Sparus aurata). Aquaculture 232:493–510

    Article  Google Scholar 

  • Graham MS, Farrell AP (1992) Environmental influences on cardiovascular variables in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Biol 41:851–858

    Article  Google Scholar 

  • Handeland SO, Imsland AK, Stefansson SO (2008) The effect of temperature and fish size on growth, feed intake, food conversion efficiency and stomach evacuation rate of Atlantic salmon post-smolts. Aquaculture 283:36–42

    Article  Google Scholar 

  • Hevrøy EM, Jordal AE, Hordvik I, Espe M, Hemre G-I, Olsvik PA (2005) Myosin heavy chain mRNA expression correlates higher with muscle protein accretion than growth in Atlantic salmon, Salmo salar. Aquaculture 252:453–461

    Article  Google Scholar 

  • Hevrøy EM, El-Mowafi A, Taylor R, Olsvik PA, Norberg B, Espe M (2007) Lysine intake affects gene expression of anabolic hormones in Atlantic salmon (Salmo salar). Gen Comp Endocrinol 152:39–46

    Article  PubMed  Google Scholar 

  • Hevrøy EM, El-Mowafi A, Taylor R, Norberg B, Espe M (2008) Effects of a high plant protein diet on the somatotropic system and cholecystokinin in Atlantic salmon (Salmo salar L.). Comp Biochem Physiol 151A:621–627

    Google Scholar 

  • Hevrøy EM, Azpeleta C, Shimizu M, Lanzén A, Kaiya H, Espe M, Olsvik PA (2011) Effects of short-term starvation on ghrelin, GH-IGF system, and IGF-binding proteins in Atlantic salmon. Fish Physiol Biochem 37:217–232

    Article  PubMed  Google Scholar 

  • Hevrøy EM, Waagbø R, Torstensen BE, Takle H, Stubhaug I, Jørgensen SM, Torgersen T, Tvenning L, Susort S, Breck O, Hansen T (2012) Ghrelin is involved in voluntary anorexia in Atlantic salmon raised at elevated sea temperatures. Gen Comp Endocrinol 175:118–134

    Article  PubMed  Google Scholar 

  • Holliday PN, Hughes LS, Bacon S, Beszcznaka-Möller A, Hansen B, Lavín A, Loeng H, Mork KA, Østerhus S, Sherwin T, Walczowski W (2008) Reversal of the 1960s to 1990s freshening trend in the northeast North Atlantic and Nordic Seas. Geophys Res Letters 35:L03614

    Article  Google Scholar 

  • Hossenlopp P, Seurin D, Segovia-Quinson B, Hardouin S, Binoux M (1986) Analysis of serum insulin-like growth factor binding proteins using Western blotting: use of the method for titration of the binding proteins and competitive binding studies. Anal Biochem 154:138–143

    Article  PubMed  CAS  Google Scholar 

  • Jobling M (1994) Production and growth. In: Jobling M (ed) Fish bioenergetics. Chapman & Hall, London, pp 147–154

    Google Scholar 

  • Katersky RS, Carter CG (2005) Growth efficiency of juvenile barramundi, Lates calcarifer at high temperatures. Aquaculture 250:775–780

    Article  Google Scholar 

  • Kelley KM, Haigwood JT, Perez M, Galima MM (2001) Serum insulin-like growth factor binding proteins (IGFBPs) as markers for anabolic/catabolic condition in fishes. Comp Biochem Physiol 129B:229–236

    CAS  Google Scholar 

  • Kelley KM, Price TD, Galima MM, Sak K, Reyes JA, Zepeda O, Hagstrom R, Truong TA, Lowe CG (2006) Fish Endocrinology. In: Reinecke M, Zaccone G, Kapoor BG (ed) Insulin-like growth factor-binding proteins (IGFBPs) in fish: beacons for (disrupted) growth endocrine physiology. Science Publishers, Enfield, pp 167–195

  • Koskela J, Pirhonen J, Jobling M (1997) Feed intake, growth rate and body composition of juvenile Baltic salmon exposed to different constant temperatures. Aquac Int 5:351–360

    Article  Google Scholar 

  • Luckenbach A, Murashige R, Daniels HV, Godwin J, Borski RJ (2007) Temperature affects insulin-like growth factor I and growth of juvenile southern flounder, Paralichthys lethostigma. Comp Biochem Physiol 146A:95–104

    CAS  Google Scholar 

  • Monahan RL (1993) An overview of salmon aquaculture. In: Heen K, Monahan RL, Utter FP (eds) Salmon aquaculture. Fishing New Books, Oxford, pp 1–9

    Google Scholar 

  • Peterson BC, Waldbieser GC (2009) Effects of fasting on IGF-I, IGF-II and IGF-binding protein mRNA concentrations in channel catfish (Ictalurus punctatus). Domest Anim Endocrinol 37:74–83

    Article  PubMed  CAS  Google Scholar 

  • Pörtner HO (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol 132A:739–761

    Google Scholar 

  • Pörtner HO, Farrell AP (2002) Physiology and climate change. Science 322:690–692

    Article  Google Scholar 

  • Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97

    Article  PubMed  Google Scholar 

  • Shimizu M, Swanson P, Dickhoff WW (1999) Free and protein-bound insulin-like growth factor-I (IGF-I) and IGF-binding proteins in plasma of Coho salmon, Oncorhynchus kisutch. Gen Comp Endocrinol 115:398–405

    Article  PubMed  CAS  Google Scholar 

  • Shimizu M, Swanson P, Fukada H, Hara A, Dickhoff WW (2000) Comparison of extraction methods and assay validation for salmon insulin-like growth factor-I using commercially available components. Gen Comp Endocrinol 119:26–36

    Article  PubMed  CAS  Google Scholar 

  • Shimizu M, Swanson P, Hara A, Dickhoff WW (2003) Purification of a 41-kDa insulin-like growth factor binding protein from serum of Chinook salmon, Oncorhynchus tshawytscha. Gen Com Endocrinol 132:103–111

    Article  CAS  Google Scholar 

  • Shimizu M, Dickey JT, Fukada H, Dickhoff WW (2005) Salmon serum 22 kDa insulin-like growth factor-binding protein (IGFBP) is IGFBP-1. J Endocrinol 184:267–276

    Article  PubMed  CAS  Google Scholar 

  • Shimizu M, Beckman BR, Hara A, Dickhoff WW (2006) Measurement of circulating salmon IGF binding protein-1: assay development, response to feeding ration and temperature, and relation to growth parameters. J Endocrinol 188:101–110

    Article  PubMed  CAS  Google Scholar 

  • Shimizu M, Suzuki S, Horikoshi M, Hara A, Dickhoff WW (2011a) Circulating salmon 41-kDa insulin-like growth factor binding protein (IGFBP) is not IGFBP-3 but an IGFBP-2 subtype. Gen Comp Endocrinol 171:326–331

    Article  PubMed  CAS  Google Scholar 

  • Shimizu M, Kishimoto K, Yamaguchi T, Nakano Y, Hara A, Dickhoff WW (2011b) Circulating salmon 28- and 22-kda insulin-like growth factor binding proteins (IGFBPs) are co-orthologs of IGFBP-1. Gen Comp Endocrinol 174:97–106

    Article  PubMed  CAS  Google Scholar 

  • Sissener NH, Hemre G-I, Espe M, Sanden M, Torstensen BE, Hevrøy EM (2012) Effects of plant based diets on glucose and amino acid metabolism, leptin, ghrelin and GH-IGF system regulation in Atlantic salmon. Aquacult Nutr. doi:10.1111/j.1365-2095.2012.00971.x (in press)

  • Small BC, Peterson BC (2005) Establishment of a time-resolved fluoroimmunoassay for measuring plasma insulin-like growth factor I (IGF-I) in fish: effect of fasting on plasma concentrations and tissue mRNA expression of IGF-I and growth hormone (GH) in channel catfish (Ictalurus punctatus). Domest Anim Endocrinol 28:202–215

    Article  PubMed  CAS  Google Scholar 

  • Thissen JP, Underwood LE, Ketelslegers JM (1999) Regulation of insulin-like growth factor-I in starvation and injury. Nutr Rev 57:167–176

    Article  PubMed  CAS  Google Scholar 

  • Vandesompele J, de Preter K, Pattyn F, Poppe B, van Roy N, de Paepe A, Speleman F (2003) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:1465–1476

    Google Scholar 

  • Vong QP, Chan KM, Cheng CH (2003) Quantification of common carp (Cyprinus carpio) IGF-I and IGF-II mRNA by real-time PCR: differential regulation of expression by GH. J Endocrinol 178:513–521

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors would like to thanks Ivar Helge Matre and Marita Larsen at the IMR Matre Aquaculture Research Station for excellent husbandry of the fish, and Eva Mykkeltvedt and Jacob Wessels at NIFES for great technical help in the molecular lab. This work has been performed with financial support from the Research Council of Norway, Project No. 187306 and Project No. 199683/S40.

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Correspondence to Ernst M. Hevrøy.

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Communicated by I. D. Hume.

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Hevrøy, E.M., Hunskår, C., de Gelder, S. et al. GH–IGF system regulation of attenuated muscle growth and lipolysis in Atlantic salmon reared at elevated sea temperatures. J Comp Physiol B 183, 243–259 (2013). https://doi.org/10.1007/s00360-012-0704-5

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