Hepatic insulin-like growth-factor binding protein (igfbp) responses to food restriction in Atlantic salmon smolts

Breves, Jason P.; Phipps-Costin, Silas K.; Fujimoto, Chelsea; Einarsdóttir, Ingibjörg Eir; Regish, Amy M.; Björnsson, Björn Thrándur; McCormick, Stephen D.

doi:10.1016/j.ygcen.2016.05.015

Cited by 19 publications

(17 citation statements)

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“…Thus, igfbp1b1 and− 1b2 may be further modulating growth and metabolism as part of the metabolic demands of smolt development and in preparation for seaward migration. Interestingly, we detected no seasonal changes in igfbp1a1 , an isoform that is sensitive to nutrient conditions [81]. Hepatic igfbp1a1 was, however, induced by SW exposure, a response also seen with a 32-kD Igfbp (putative Igfbp1) in rainbow trout plasma [30, 82].…”

Section: Discussionmentioning

confidence: 99%

Variation in branchial expression among insulin-like growth-factor binding proteins (igfbps) during Atlantic salmon smoltification and seawater exposure

et al. 2017

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BackgroundIn preparation for migration from freshwater to marine habitats, Atlantic salmon (Salmo salar L.) undergo smoltification, a transformation that includes the acquisition of hyposmoregulatory capacity. The growth hormone (Gh)/insulin-like growth-factor (Igf) axis promotes the development of branchial ionoregulatory functions that underlie ion secretion. Igfs interact with a suite of Igf binding proteins (Igfbps) that modulate hormone activity. In Atlantic salmon smolts, igfbp4,−5a,−5b1,−5b2,−6b1 and−6b2 transcripts are highly expressed in gill. We measured mRNA levels of branchial and hepatic igfbps during smoltification (March, April, and May), desmoltification (July) and following seawater (SW) exposure in March and May. We also characterized parallel changes in a broad suite of osmoregulatory (branchial Na+/K+-ATPase (Nka) activity, Na + /K + /2Cl − cotransporter 1 (nkcc1) and cystic fibrosis transmembrane regulator 1 (cftr1) transcription) and endocrine (plasma Gh and Igf1) parameters.ResultsIndicative of smoltification, we observed increased branchial Nka activity, nkcc1 and cftr1 transcription in May. Branchial igfbp6b1 and -6b2 expression increased coincidentally with smoltification. Following a SW challenge in March, igfbp6b1 showed increased expression while igfbp6b2 exhibited diminished expression. igfbp5a,−5b1 and−5b2 mRNA levels did not change during smolting, but each had lower levels following a SW exposure in March.ConclusionsSalmonids express an especially large suite of igfbps. Our data suggest that dynamic expression of particular igfbps accompanies smoltification and SW challenges; thus, transcriptional control of igfbps may provide a mechanism for the local modulation of Igf activity in salmon gill.

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Section: Discussionmentioning

confidence: 99%

Variation in branchial expression among insulin-like growth-factor binding proteins (igfbps) during Atlantic salmon smoltification and seawater exposure

et al. 2017

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“…For example, Atlantic salmon (Salmo salar L.) fed after a period of fasting showed upregulation of IGF-I and IGFBP-4, whereas IGF-II, IGF1R and IGFBP-2 were downregulated (Bower et al, 2008). Reciprocally, muscle IGF-I transcript levels were downregulated in Atlantic salmon (Breves et al, 2016), yellowtail (Seriola quinqueradiata) (Fukada et al, 2012) and tilapia (Oreochromis mossambicus) (Fox et al, 2010) by fasting, while GHR transcripts were induced by fasting in tilapia (Fox et al, 2010). Despite such gains in understanding, to the best of our knowledge, the regulation of GH and IGF pathway genes during an immune response in teleost skeletal muscle remains uncharacterized.…”

Section: Introductionmentioning

confidence: 99%

Growth hormone transgenesis disrupts immune function in muscle of coho salmon (Oncorhynchus kisutch) impacting cross-talk with growth systems

Alzaid

Kim

Devlin

et al. 2017

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The suppression of growth during infection should facilitate resource allocation towards effective immune function. Work supporting this hypothesis has been recently reported in teleosts, demonstrating immune-responsive regulation of the insulin-like growth factor (IGF) system - a key endocrine growth pathway that acts downstream of growth hormone (GH). Skeletal muscle is the main target for growth and energetic storage in fish, yet little is known about how growth is regulated in this tissue during an immune response. We addressed this knowledge gap by characterizing muscle immune responses in size-matched coho salmon (Oncorhynchus kisutch) achieving different growth rates. We compared a wild-type strain with two GH transgenic groups achieving either maximal or highly-suppressed growth – an experimental design that separates GH’s direct effects from its influence on growth rate. Fish were sampled 30h post-injection with PBS (control) or mimics of bacterial (peptidoglycan) or viral (Poly:IC) infection. We quantified the mRNA level expression of genes from the GH, GH receptor (GHR), IGF hormone, IGF1 receptor (IGF-1R) and IGF binding protein (IGFBP) families, along with marker genes for muscle growth and host defence genes involved in inflammatory or antiviral responses. We provide strong evidence for dampened immunity in the GH transgenics compared to wild-type animals. Strikingly, the muscle of GH transgenics achieving rapid growth showed no detectable antiviral response, coupled with evidence of a constitutive inflammatory state. GH and IGF system gene expression was also strongly altered by GH transgenesis and fast growth, both for baseline expression levels and responses to immune stimulation. Overall, our findings demonstrate that GH transgenesis disrupts normal immune function and growth-immune cross-talk in muscle, with implications for the health and welfare of farmed salmon.

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“…This is supported by the observation of elevated mRNAs encoding the type 1 igfbp gene in the liver of Atlantic salmon, Salmo salar, smolts under food restriction (Hevrøy et al, 2011). Breves et al (2016) likewise observed increased hepatic igfbp1a1 mRNA levels in Atlantic salmon parr fasted for 3 to 10 d.…”

Section: Introductionmentioning

confidence: 65%

“…Such external environmental influences are translated into changes in growth in part via the altered secretion of stimulatory or inhibitory hormones within the somatotropic endocrine axis. In particular, changes in nutritional conditions have been shown to alter liver production of the somatomedin hormone Igf1 in fishes (Breves et al, 2014;Breves et al, 2016). Given that relationship between Igf1 and nutritional status, it has been proposed that circulating concentrations of Igf1 may serve as a reliable indicator of recent growth rate in fishes (Beckman, 2011;Picha et al, 2008a;Reinecke, 2010).…”

Section: Discussionmentioning

confidence: 99%

“…For fish experiencing food limitation or deprivation, circulating concentrations of Igf1 decrease while some Igfbps increase, ultimately contributing to reduced muscle and skeletal growth (e.g., Kelley et al, 2001;Picha et al, 2008a;Reinecke, 2010;Shimizu and Dickhoff, 2017). Such declines in circulating Igf1 with food restriction have been observed in a wide variety of fishes, including Mozambique tilapia (Oreochromis mossambicus, Breves et al, 2014;Uchida et al, 2003), Arctic charr (Salvelinus alpinus, Cameron et al, 2007), gilthead sea bream (Sparus aurata, Pérez-Sánchez et al, 1995), and several species of salmonids (Beckman et al, 2004a,b;Bower et al, 2008;Breves et al, 2016;Kaneko et al, 2015;Pierce et al, 2005;Wilkinson et al, 2006). Igfbp expression in fishes has also been found to be responsive to variation in food consumption.…”

Section: Introductionmentioning

confidence: 99%

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The Insulin-Like Growth Factor-1 (IGF1) System as a Potential Biomarker for Nutritional Status and Growth Rate in Pacific Rockfish (SEBASTES SPP.)

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Hepatic insulin-like growth-factor binding protein (igfbp) responses to food restriction in Atlantic salmon smolts

Cited by 19 publications

References 76 publications

Variation in branchial expression among insulin-like growth-factor binding proteins (igfbps) during Atlantic salmon smoltification and seawater exposure

Variation in branchial expression among insulin-like growth-factor binding proteins (igfbps) during Atlantic salmon smoltification and seawater exposure

Growth hormone transgenesis disrupts immune function in muscle of coho salmon (Oncorhynchus kisutch) impacting cross-talk with growth systems

The Insulin-Like Growth Factor-1 (IGF1) System as a Potential Biomarker for Nutritional Status and Growth Rate in Pacific Rockfish (SEBASTES SPP.)

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