Teleocortin: A Novel Member of the CRH Family in Teleost Fish

Hosono, Kohei; Kikuchi, Yukiko; Miyanishi, Hiroshi; Hiraki-Kajiyama, Towako; Takeuchi, Akio; Nakasone, Kiyoshi; Maehiro, Sayaka; Okubo, Kataaki

doi:10.1210/en.2015-1042

Cited by 27 publications

(24 citation statements)

References 53 publications

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“…However, CRH2 was lost in placental mammals and in teleost genomes. We also confirm by synteny and paralogon analysis that the recently reported CRH-related peptide in teleost fish, named teleocortin and proposed to be an ancestral vertebrate duplicate (Hosono et al 2015), is in fact a teleost-specific gene copy of CRH that arose in the teleost tetraploidization, as recently reported (Grone & Maruska 2015a). The evolutionary implications of this ancient ancestral complexity of the CRH system are discussed.…”

Section: Introductionsupporting

confidence: 85%

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Corticotropin-releasing hormone family evolution: five ancestral genes remain in some lineages

Cardoso¹,

Bergqvist²,

Félix³

et al. 2016

Journal of Molecular Endocrinology

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The evolution of the peptide family consisting of corticotropin-releasing hormone (CRH) and the three urocortins (UCN1-3) has been puzzling due to uneven evolutionary rates. Distinct gene duplication scenarios have been proposed in relation to the two basal rounds of vertebrate genome doubling (2R) and the teleost fish-specific genome doubling (3R). By analyses of sequences and chromosomal regions, including many neighboring gene families, we show here that the vertebrate progenitor had two peptide genes that served as the founders of separate subfamilies. Then, 2R resulted in a total of five members: one subfamily consists of CRH1, CRH2, and UCN1. The other subfamily contains UCN2 and UCN3. All five peptide genes are present in the slowly evolving genomes of the coelacanth Latimeria chalumnae (a lobe-finned fish), the spotted gar Lepisosteus oculatus (a basal ray-finned fish), and the elephant shark Callorhinchus milii (a cartilaginous fish). The CRH2 gene has been lost independently in placental mammals and in teleost fish, but is present in birds (except chicken), anole lizard, and the nonplacental mammals platypus and opossum. Teleost 3R resulted in an additional surviving duplicate only for crh1 in some teleosts including zebrafish (crh1a and crh1b). We have previously reported that the two vertebrate CRH/UCN receptors arose in 2R and that CRHR1 was duplicated in 3R. Thus, we can now conclude that this peptide-receptor system was quite complex in the ancestor of the jawed vertebrates with five CRH/UCN peptides and two receptors, and that crh and crhr1 were duplicated in the teleost fish tetraploidization.

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Section: Introductionsupporting

confidence: 85%

“…After completion of this study, a member of the CRH peptide family was reported in a few species of teleost fish and was named teleocortin (Tcn) (Hosono et al 2015). The gene was reported to be missing in zebrafish.…”

Section: Lineage-specific Differences In Crh Family Evolutionmentioning

confidence: 99%

Corticotropin-releasing hormone family evolution: five ancestral genes remain in some lineages

Cardoso¹,

Bergqvist²,

Félix³

et al. 2016

Journal of Molecular Endocrinology

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show abstract

“…In the latter, two crh ohnologs, named crha and crhb, have been identified (Grone and Maruska, 2015). The expression of crha has been mainly observed in the retina (Grone and Maruska, 2015;Hosono et al, 2015), with weak expression in the brain (about 100 times less than in retina) (Hosono et al, 2015), in fish. By contrast, crhb is mainly expressed in the central nervous system (CNS), i.e.…”

Section: Introductionmentioning

confidence: 99%

“…The action of Crh in the pituitary is mediated by the binding and activation of two highly conserved membrane receptors (Crhr1 and Crhr2), which belong to class B of the G protein-coupled receptors (Lovejoy et al, 2014). Although in tetrapods, it has been reported that Crh has higher affinity for Crhr1 (Vaughan et al, 1995), in teleosts both Crh ligands have similar affinity for both Crh receptors (Hosono et al, 2015). Several studies in mammals have also demonstrated the ability of Crh receptor antagonists to block stress responses, such as anxiety or depression (Backström and Winberg, 2013;Grammatopoulos and Chrousos, 2002;Holsboer and Ising, 2008), placing Crh receptors at a crucial point in regulation of the HPA axis.…”

Section: Introductionmentioning

confidence: 99%

The central nervous system acts as a transducer of stress-induced masculinization through corticotropin-releasing hormone B

et al. 2019

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Exposure to environmental stressors, such as high temperature (HT), during early development of fish induces sex reversal of genotypic females. Nevertheless, the involvement of the brain in this process is not well clarified. In the present work, we investigated the mRNA levels of corticotropin-releasing hormone b (crhb) and its receptors (crhr1 and crhr2), and found that they were upregulated at HT during the crucial period of gonadal sex determination in medaka. In order to clarify their roles in sex reversal, biallelic mutants for crhr1 and crhr2 were produced by CRISPR/Cas9 technology. Remarkably, biallelic mutants of both loci (crhr1 and crhr2) did not undergo female-to-male sex reversal upon exposure to HT. Inhibition of this process in double corticotropin-releasing hormone receptor mutants could be successfully rescued through the administration of the downstream effector of the hypothalamic-pituitary-interrenal axis, cortisol. Taken together, these results reveal for the first time that the CNS acts as a transducer of masculinization induced by thermal stress.

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“…Although crfa was only recently identified, the results of Grone and Maruska (35) suggest that the expression patterns of crfa in teleosts are species-specific. Therefore, although the dominant cardiac mRNA levels of crfa in zebrafish is consistent with the high expression levels of teleocortin (an ortholog of zebrafish crfa) in the heart of medaka (37), further studies may be needed to confirm whether CRFa is the dominant cardiac CRF ligand in teleost fish.…”

Section: Discussionmentioning

confidence: 91%

CRF and urocortin 3 protect the heart from hypoxia/reoxygenation-induced apoptosis in zebrafish

Williams

Bergstrome

Scott

et al. 2017

American Journal of Physiology-Regulatory, Integrative and Comp

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Fish routinely experience environmental hypoxia and have evolved various strategies to tolerate this challenge. Given the key role of the CRF system in coordinating the response to stressors and its cardioprotective actions against ischemia in mammals, we sought to characterize the cardiac CRF system in zebrafish and its role in hypoxia tolerance. We established that all genes of the CRF system, the ligands CRFa, CRFb, urotensin 1 (UTS1), and urocortin 3 (UCN3); the two receptor subtypes (CRFR1 and CRFR2); and the binding protein (CRFBP) are expressed in the heart of zebrafish: > > > > > In vivo, exposure to 5% O saturation for 15 min and 90 min of recovery resulted in four- to five-fold increases in whole heart and mRNA levels but did not affect the gene expression of other CRF system components. In vitro, as assessed by monitoring caspase 3 activity and the number of terminal deoxynucleotidyl transferase dUTP nick-end labeling-positive cells, pretreatment of excised whole hearts with CRF or UCN3 for 30 min prevented the increase in apoptosis associated with exposure to 1% O saturation for 30 min with a 24-h recovery. Lastly, the addition of the nonselective CRF receptor antagonist αh-CRF prevented the cytoprotective effects of CRF. We show that the CRF system is expressed in fish heart, is upregulated by hypoxia, and is cytoprotective. These findings identify a novel role for the CRF system in fish and a new strategy to tolerate hypoxia.

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Teleocortin: A Novel Member of the CRH Family in Teleost Fish

Cited by 27 publications

References 53 publications

Corticotropin-releasing hormone family evolution: five ancestral genes remain in some lineages

Corticotropin-releasing hormone family evolution: five ancestral genes remain in some lineages

The central nervous system acts as a transducer of stress-induced masculinization through corticotropin-releasing hormone B

CRF and urocortin 3 protect the heart from hypoxia/reoxygenation-induced apoptosis in zebrafish

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