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

Abstract

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.

Circulating insulin-like growth factor binding proteins in fish: Their identities and physiological regulation

“…Activity of the endocrine IGF-I at the gills in turn may be regulated by local IGFBPs. A recent work by Breves et al (2017) reported changes in local igfbp-6bs in the gills and suggested their importance in the development of hypoosmoregulatory ability.…”

Insulin-Like Growth Factor-Binding Proteins of Teleost Fishes

“…There is also emerging evidence that igfbp-5 genes play a role in ionic homeostasis and Igf regulation in zebrafish ( 121 ), stickleback [e.g., Ref. ( 122 )] and Atlantic salmon gills ( 123 ) with Igfbp-5a acting to regulate calcium influx in zebrafish gills ( 121 ) and being differentially expressed and under divergent selective pressures in marine vs. freshwater sticklebacks ( 122 , 124 ).…”

“…In adult Atlantic salmon, neither igfbp-6a1 nor - 6a2 were notably expressed across a panel of 11 tissues, while igfbp-6b1 and 6b2 were each broadly expressed, with the latter being especially highly expressed in gill, brain, and spleen ( 16 ). Both igfbp-6b1 and 6b2 were also reported as being highly expressed in Atlantic salmon gills, where they were dynamically regulated during smoltification ( 123 ).…”

Characterization of Insulin-Like Growth Factor Binding Protein-5 (IGFBP-5) Gene and Its Potential Roles in Ontogenesis in the Pacific Abalone, Haliotis discus hannai

“…The architecture of IGFBPs consists of three domains: N-terminal and C-terminal domains, which both contribute to its high-affinity IGF binding, and the variable central linker domain that is believed to be important for maintaining structural integrity [ 14 ]. Although different forms of IGFBPs share considerable sequence similarities, each IGFBP type possesses distinct properties and performs stimulatory or inhibitory functions in different IGF-mediated biological mechanisms [ 15 , 16 ]. The differences in their functions are influenced by post-transcriptional modification such as N-linked glycosylation, phosphorylation for protein kinase A or C, proteolysis, and cell surface associations [ 17 ].…”