The saccus vasculosus of fish is a sensor of seasonal changes in day length

Nakane, Yusuke; Ikegami, Keisuke; Iigo, Masayuki; Ono, Hiroko; Takeda, Kazuya; Takahashi, Daisuke; Uesaka, Maiko; Kimijima, Meita; Hashimoto, R.; Arai, Natsumi; Suga, Tetsuya; Kosuge, Katsuya; Abe, Takeyuki; Maeda, Ryosuke; Senga, Takumi; Amiya, Noriko; Azuma, Teruo; Amano, Masafumi; Abe, Hideki; Yamamoto, Naoyuki; Yoshimura, Takashi

doi:10.1038/ncomms3108

Cited by 163 publications

(129 citation statements)

References 30 publications

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“…First, as in birds and mammals and echoing other recent reports in teleosts [24,25], photoperiodic induction of dio2b gene expression is seen during smoltification, consistent with the view that this is an ancestral mechanism involved in the timing of seasonal life history transitions. This applies both to cyclical changes such as seasonal breeding as well as to seasonally gated unidirectional events such as puberty and metamorphosis, or in this case, smoltification.…”

Section: Discussionsupporting

confidence: 79%

“…At the same time, it forces us to reconsider the regulatory pathways leading to photoperiodic dio2 induction. The current literature, including the recent work in teleosts, as well as that in birds and mammals, empha- sizes the importance of thyrotropin (TSH) produced in the anterior pituitary [30,31] or in the saccus vasculosus (SV) [24] as the upstream signal for dio2 induction. The demonstration of changes in brain dio2b expression in sites remote from the pituitary or SV and the lack of evidence for extra-pituitary sites of TSH expression suggest that additional upstream pathways must be sought.…”

Section: Discussionmentioning

confidence: 99%

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Functional Divergence of Type 2 Deiodinase Paralogs in the Atlantic Salmon

et al. 2015

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Thyroid hormone (TH) is an ancestral signal linked to seasonal life history transitions throughout vertebrates. TH action depends upon tissue-localized regulation of levels of active TH (triiodothyronine, T3), through spatiotemporal expression of thyroid hormone deiodinase (dio) genes. We investigated the dio gene family in juvenile Atlantic salmon (Salmo salar) parr, which prepare for seaward migration in the spring (smoltification) through TH-dependent changes in physiology. We identified two type 2 deiodinase paralogs, dio2a and dio2b, responsible for conversion of thyroxine (T4) to T3. During smoltification, dio2b was induced in the brain and gills in zones of cell proliferation following increasing day length. Contrastingly, dio2a expression was induced in the gills by transfer to salt water (SW), with the magnitude of the response proportional to the plasma chloride level. This response reflected a selective enrichment for osmotic response elements (OREs) in the dio2a promoter region. Transcriptomic profiling of gill tissue from fish transferred to SW plus or minus the deiodinase inhibitor, iopanoic acid, revealed SW-induced increases in cellular respiration as the principal consequence of gill dio2 activity. Divergent evolution of dio2 paralogs supports organ-specific timing of the TH-dependent events governing the phenotypic plasticity required for migration to sea.

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Section: Discussionsupporting

confidence: 79%

Section: Discussionmentioning

confidence: 99%

Functional Divergence of Type 2 Deiodinase Paralogs in the Atlantic Salmon

et al. 2015

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“…Importantly these results have been confirmed by other laboratories and extended by Yoshimura and others to mammals (reviews: Dardente et al, 2014;Ebling 2015;Stevenson & Prendergast, 2015) and fish (Nakane et al, 2013). Earlier I mentioned some of our studies on the role of thyroid hormones in seasonality but our efforts (38 papers) never reached the molecular level.…”

Section: The Thyroid Story: Its Molecular Basissupporting

confidence: 79%

“Seasonal changes in the neuroendocrine system”: Some reflections

Follett

2015

Frontiers in Neuroendocrinology

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“…Recent studies in fish show that specific cells in the brain respond to light and exert neuroendocrine control of testis development [51, 52]. In A. anguilla , behavioral evidence indicates that photoreceptor sites that are independent of the pineal exist in the brain [53].…”

Section: Discussionmentioning

confidence: 99%

Changes in the gene expression profiles of the brains of male European eels (Anguilla anguilla) during sexual maturation

et al. 2014

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BackgroundThe vertebrate brain plays a critical role in the regulation of sexual maturation and reproduction by integrating environmental information with developmental and endocrine status. The European eel Anguilla anguilla is an important species in which to better understand the neuroendocrine factors that control reproduction because it is an endangered species, has a complex life cycle that includes two extreme long distance migrations with both freshwater and seawater stages and because it occupies a key position within the teleost phylogeny. At present, mature eels have never been caught in the wild and little is known about most aspects of reproduction in A. anguilla. The goal of this study was to identify genes that may be involved in sexual maturation in experimentally matured eels. For this, we used microarrays to compare the gene expression profiles of sexually mature to immature males.ResultsUsing a false discovery rate of 0.05, a total of 1,497 differentially expressed genes were identified. Of this set, 991 were expressed at higher levels in brains (forebrain and midbrain) of mature males while 506 were expressed at lower levels relative to brains of immature males. The set of up-regulated genes includes genes involved in neuroendocrine processes, cell-cell signaling, neurogenesis and development. Interestingly, while genes involved in immune system function were down-regulated in the brains of mature males, changes in the expression levels of several receptors and channels were observed suggesting that some rewiring is occurring in the brain at sexual maturity.ConclusionsThis study shows that the brains of eels undergo major changes at the molecular level at sexual maturity that may include re-organization at the cellular level. Here, we have defined a set of genes that help to understand the molecular mechanisms controlling reproduction in eels. Some of these genes have previously described functions while many others have roles that have yet to be characterized in a reproductive context. Since most of the genes examined here have orthologs in other vertebrates, the results of this study will contribute to the body of knowledge concerning reproduction in vertebrates as well as to an improved understanding of eel biology.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-799) contains supplementary material, which is available to authorized users.

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The saccus vasculosus of fish is a sensor of seasonal changes in day length

Cited by 163 publications

References 30 publications

Functional Divergence of Type 2 Deiodinase Paralogs in the Atlantic Salmon

Functional Divergence of Type 2 Deiodinase Paralogs in the Atlantic Salmon

“Seasonal changes in the neuroendocrine system”: Some reflections

Changes in the gene expression profiles of the brains of male European eels (Anguilla anguilla) during sexual maturation

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