Thyroid hormone and retinoid X receptor function and expression during sea lamprey (Petromyzon marinus) metamorphosis

Manzon, Lori A.; Youson, John H.; Holzer, Guillaume; Staiano, Leopoldo; Laudet, Vincent; Manzon, Richard G.

doi:10.1016/j.ygcen.2014.05.030

Cited by 16 publications

(17 citation statements)

References 83 publications

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“…The sea lamprey Petromyzon marinus has two TRs, TR1 and TR2, whose evolution is not clearly understood yet. Indeed, in a phylogenetic reconstruction they do not group with the TRα and TRβ but together within an agnathan group at the base of the gnathostomes (Manzon et al, 2014). The most singular feature of lamprey regarding TH pathway is its involvement in metamorphosis.…”

Section: Even In Vertebrates the Classical Ligand Can Hide An Astonimentioning

confidence: 96%

Evolution of ligands, receptors and metabolizing enzymes of thyroid signaling

Holzer

Roux

Laudet

2017

Molecular and Cellular Endocrinology

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Thyroid hormones (THs) play important roles in vertebrates such as the control of the metabolism, development and seasonality. Given the pleiotropic effects of thyroid disorders (developmental delay, mood disorder, tachycardia, etc), THs signaling is highly investigated, specially using mammalian models. In addition, the critical role of TH in controlling frog metamorphosis has led to the use of Xenopus as another prominent model to study THs action. Nevertheless, animals regarded as non-model species can also improve our understanding of THs signaling. For instance, studies in amphioxus highlighted the role of Triac as a bona fide thyroid hormone receptor (TR) ligand. In this review, we discuss our current understanding of the THs signaling in the different taxa forming the metazoans (multicellular animals) group. We mainly focus on three actors of the THs signaling: the ligand, the receptor and the deiodinases, enzymes playing a critical role in THs metabolism. By doing so, we also pinpoint many key questions that remain unanswered. How can THs accelerate metamorphosis in tunicates and echinoderms while their TRs have not been yet demonstrated as functional THs receptors in these species? Do THs have a biological effect in insects and cnidarians even though they do not have any TR? What is the basic function of THs in invertebrate protostomia? These questions can appear disconnected from pharmacological issues and human applications, but the investigation of THs signaling at the metazoans scale can greatly improve our understanding of this major endocrinological pathway.

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Section: Even In Vertebrates the Classical Ligand Can Hide An Astonimentioning

confidence: 96%

Evolution of ligands, receptors and metabolizing enzymes of thyroid signaling

Holzer

Roux

Laudet

2017

Molecular and Cellular Endocrinology

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“…P. marinus is known to undergo a large-scale programmed elimination of somatic DNA during its development [19,20]. We suspect that TR1 has been cloned from larval DNA [11], which may have been lost during lamprey development and absent from the adult genome, which is the genome of reference [10]. Therefore, we conclude that there are four TR genes in lamprey: TR1, TR2, Pm524 that we propose to call TR3 and Pm8742 that we propose to call TR4.…”

Section: Discussionmentioning

confidence: 86%

“…In lamprey however, it is a decrease of TH, instead of an increase, that triggers metamorphosis [27,28,41]. Intriguingly, the already identified lamprey TRs (TR1 and TR2) behave as genuine TRs: they bind T3 at nanomolar concentration and can activate target gene transcription [11]. Therefore, they cannot explain alone how the system can work in a reverse way in lamprey.…”

Section: Discussionmentioning

confidence: 99%

“…The P. marinus genome and the cloning of TR1 and TR2 have been performed by different labs with different animal and DNA sources [10,11]. Thus, it could be argued that the TRs we newly identified are actually polymorphism between individuals.…”

Section: Discussionmentioning

confidence: 99%

“…However, the precise evolution and timing of duplication of the TRs is difficult to reconcile with the known events of genome duplication that took place earlier on during vertebrate evolution [8][9][10]. The two sea lamprey TR genes (TR1 and TR2) appear to be the product of an independent duplication [11], but this issue is still debated and complicates our understanding of TR evolution.…”

Section: Introductionmentioning

confidence: 99%

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New Insights into Vertebrate Thyroid Hormone Receptor Evolution

Holzer

Laudet

2017

Nuclear Receptor Research

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Abstract. The lamprey Petromyzon marinus belongs to the agnathans, the oldest vertebrate lineage from which jawed vertebrates diverged about 500 million years ago. Therefore, it holds a key phylogenetic position to understand the evolution of vertebrates. As in jawed vertebrates, two thyroid hormone receptors have been described in lamprey. These receptors, referred to as TR1 and TR2, behave as genuine TRs but are considered as an independent duplications when compared to the orthologs characterized in jawed vertebrates, TR and TR . Here, we show that the lamprey genome contains two additional TR sequences. Their assignment to bona fide thyroid hormone receptors is supported by sequence alignments and phylogenetic reconstructions. This led us to revisit the phylogeny of thyroid hormone receptors and to detect an acceleration of their evolutionary rates at the basis of vertebrates. Our analysis therefore suggests that major evolutionary shifts occurred at the receptor level just when the modern synthesis of thyroid hormone was established during early vertebrate evolution.

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