3462
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wileyonlinelibrary.com/journal/are Aquaculture Research. 2019;50:3462–3470.
© 2019 John Wiley & Sons Ltd
1 | INTRODUCTION
Larval development in fish involves tissue organizer activity and pat‐
terning followed by organ differentiation, the rate and success of
which are influenced by thyroid hormones (THs) and the insulin‐like
growth factor (IGF) signalling pathway (Eivers, McCarthy, Glynn,
Nolan, & Byrnes, 2004). Maternally derived THs transferred to fish
embryos act as regulatory compounds as yolk is absorbed. This
trans‐generational signalling pathway has been referred to as ma‐
ternal provisioning (McComb, Gelsleichter, Manire, Brinn, & Brown,
2005). The primary goal of this study was to examine possible inter‐
actions of the TH and IGF pathways.
The zebrafish, Danio rerio, has been identified as a critically im‐
portant model for genetic and endocrine studies with applications
throughout finfish aquaculture (Ribas & Piferrer, 2013). Due to the
ready access to DNA sequence data and commercially available
nucleic acid polymers, this species was chosen for our study of
genetic and endocrine regulation of early development. Abundant
stores of maternal THs are found in unfertilized zebrafish eggs, and
the genes required for the thyroid signalling pathway are expressed
very early in zebrafish development (Campinho, Saraiva, Florindo,
& Power, 2014).
The somatotropin/IGF‐1 and pituitary/thyroid axes are fre‐
quently presented as separate regulatory signalling pathways (e.g.
Reinecke, 2010; Zhu et al., 2017), but their developmental actions
are not isolated. IGF‐1 has been shown to promote peripheral
monodeiodinase activity, leading to enhanced conversion of less
biologically active thyroxin (T
4
) into triiodothyronine (T
3
) in mam‐
mals (Hussain et al., 1996; Lartey, Werneck‐de‐Castro, O‐Sullivan,
Unterman, & Bianco, 2015). The generalized notion that T
3
regulates
Received: 10 April 2019
|
Revised: 10 July 2019
|
Accepted: 4 August 2019
DOI: 10.1111/are.14305
ORIGINAL ARTICLE
Thyroid hormone‐induced swim bladder and eye maturation
are transduced by IGF‐1 in zebrafish embryos
Mohammad Habibur Rahman Molla
1
| Md T. Hasan
2,3
| Won J. Jang
2
|
Cesar D. Soria Diaz
1
| Patrick Appenteng
1
| Haliliy Marufchoni
1
| Bushra Jahan
4
|
Christopher L. Brown
1
1
World Fisheries University Pilot
Programme, Pukyong National University
(PKNU), Busan, South Korea
2
Department of Biotechnology, Pukyong
National University (PKNU), Busan, South
Korea
3
Department of Aquaculture, Sylhet
Agricultural University, Sylhet, Bangladesh
4
Biotechnology and Genetic Engineering
Discipline, Khulna University, Khulna,
Bangladesh
Correspondence
Christopher L. Brown, World Fisheries
University Pilot Programme, Pukyong
National University (PKNU), 45 Yongso‐ro,
Nam‐gu, Busan 48513, South Korea.
Email: brownchristopher38@gmail.com
Funding information
World Fisheries University
Abstract
Maternally derived thyroid hormones (THs) deposited in yolk promote fish embryo‐
genesis and survival, and understanding early regulatory mechanisms could lead to
improved seedstock production. We have tested the hypothesis that some thyroid
actions may be mediated by insulin‐like growth factor I (IGF‐1), another promoter of
embryo development. Differentiation and performance were assessed in embryos
treated with THs in the presence or absence of an IGF‐1 receptor blocking peptide.
Treatment with the TH triiodothyronine (T
3
) promoted IGF‐1 gene expression at days
1 and 5, and advanced swim bladder and eye development, but blocking the IGF‐1
receptor eliminated the swim bladder and eye effects. Growth and survival at 1 week
of age were impaired by the IGF‐1 receptor blocking peptide alone, but concurrent
treatment with T
3
partially restored these indices. Our results confirm interaction of
T
3
and IGF‐1 regulatory signalling in zebrafish embryogenesis and transduction by
IGF‐1 of thyroid‐driven swim bladder and eye maturation.
KEYWORDS
embryo, hormones, insulin‐like growth factor 1, T
3
, thyroid, transduction, zebrafish