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Releasing Hormone Gene (CRH2) Is Conserved Across Vertebrate

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Releasing Hormone Gene (CRH2) Is Conserved Across Vertebrate RESEARCH ARTICLE A Second Corticotropin-Releasing Hormone Gene (CRH2) Is Conserved Across Vertebrate Classes and Expressed in the Hindbrain of a Basal Neopterygian Fish, the Spotted Gar (Lepisosteus oculatus) Brian P. Grone1* and Karen P. Maruska2 1Department of Neurological Surgery, University of California San Francisco, San Francisco, California 94143 2Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803 ABSTRACT retained in other lineages. To determine where CRH2 is To investigate the origins of the vertebrate stress- expressed relative to CRH1 and UTS1, we used in situ response system, we searched sequenced vertebrate hybridization on brain tissue from spotted gar (Lepisos- genomes for genes resembling corticotropin-releasing teus oculatus), a neopterygian fish closely related to hormone (CRH). We found that vertebrate genomes teleosts. In situ hybridization revealed widespread distri- possess, in addition to CRH, another gene that resem- bution of both crh1 and uts1 in the brain. Expression of bles CRH in sequence and syntenic environment. This crh2 was restricted to the putative secondary gusta- paralogous gene was previously identified only in the tory/secondary visceral nucleus, which also expressed elephant shark (a holocephalan), but we find it also in calcitonin-related polypeptide alpha (calca), a marker of marsupials, monotremes, lizards, turtles, birds, and parabrachial nucleus in mammals. Thus, the evolution- fishes. We examined the relationship of this second ver- ary history of CRH2 includes restricted expression in tebrate CRH gene, which we name CRH2,toCRH1 (pre- the brain, sequence changes, and gene loss, likely viously known as CRH) and urocortin1/urotensin1 reflecting release of selective constraints following (UCN1/UTS1) in primitive fishes, teleosts, and tetra- whole-genome duplication. The discovery of CRH2 pods. The paralogs CRH1 and CRH2 likely evolved via opens many new possibilities for understanding the duplication of CRH during a whole-genome duplication diverse functions of the CRH family of peptides across early in the vertebrate lineage. CRH2 was subsequently vertebrates. J. Comp. Neurol. 523:1125–1143, 2015. lost in both teleost fishes and eutherian mammals but VC 2015 Wiley Periodicals, Inc. INDEXING TERMS: neuropeptides; evolution; genome duplication; fishes; pons; parabrachial nucleus Corticotropin-releasing hormone (CRH), also known tion (Vaughan et al., 1995). The peptide UTS1 also has as corticotropin-releasing factor (CRF), a neuropeptide potent corticotropin-releasing activity (Lederis et al., found in all vertebrates, plays a central role in regulat- 1982). Because of its sequence and functional similarity ing physiological and behavioral responses to stressors to CRH, UTS1 is regarded as the closest ortholog of (Vale et al., 1981; Korosi and Baram, 2008). Vertebrate CRH in vertebrates. CRH is homologous to invertebrate diuretic hormone (Kataoka et al., 1989), suggesting an ancient origin of these peptides before 500 million years ago, when Grant sponsor: College of Science and Department of Biological Sci- ancestors of vertebrates and insects diverged (Lovejoy ences at Louisiana State University (to K.P.M.); Grant sponsor: Ralph and Barsyte-Lovejoy, 2010). In most vertebrate species, E. Powe Faculty Enhancement Award from Oak Ridge Associated Uni- versities (to K.P.M.); Grant sponsor: Louisiana Board of Regents urotensin 1 (UTS1), referred to as urocortin 1 (UCN1) in Research Competitiveness Subprogram (to K.P.M.). mammalian species, is the paralogous gene thought to *CORRESPONDENCE TO: Brian P. Grone, Department of Neurological Surgery, University of California San Francisco, 513 Parnassus Ave., Rm. be most closely related to the CRH gene. UTS1 shares HSE-840, San Francisco, CA, 94143. E-mail: [email protected] with CRH a simple two-exon structure, a 41-amino-acid Received September 4, 2014; Revised December 9, 2014; processed peptide, and important roles in stress regula- Accepted December 10, 2014. DOI 10.1002/cne.23729 Published online February 19, 2015 in Wiley Online Library VC 2015 Wiley Periodicals, Inc. (wileyonlinelibrary.com) The Journal of Comparative Neurology | Research in Systems Neuroscience 523:1125–1143 (2015) 1125 B.P. Grone1 and K.P. Maruska2 Recently, two predicted crh genes were identified in species in the genus Lepisosteus, however, have the elephant shark (Callorhinchus milii) genome (Nock received more attention from neuroanatomists, who et al., 2011). Because only one CRH gene has been have generated descriptions that are useful for obtain- identified in other vertebrate genomes, these duplicated ing a comparative understanding of gar neuroanatomy crh genes were proposed to have arisen by gene or (K€allen, 1950; Bradshaw et al., 1969; Northcutt and genome duplication in the elephant shark lineage more Butler, 1976, 1980, 1993; Platel et al., 1977; Parent recently than the second round of vertebrate whole- and Northcutt, 1982; Collin and Northcutt, 1995; Chiba genome duplication (Lovejoy and de Lannoy, 2013). To and Oka, 1999). The recent sequencing of the spotted test this hypothesis and increase our understanding of gar genome has also opened the door for analysis of vertebrate CRH evolution, we asked whether homologs specific mRNA expression by in situ hybridization (ISH). of crh2 as well as crh1 are present in genomes of other Thus, the taxonomic position and available neuroana- vertebrates, including fishes and tetrapods. tomical and genomic resources for gars allow us to Many gene families in vertebrates were generated localize conserved genes in the spotted gar brain to fur- during multiple rounds of whole-genome duplication ther our understanding of the evolution and function of that occurred early in vertebrate evolution (Ohno, 1970; vertebrate neuropeptide signaling systems. In the pres- Abi-Rached et al., 2002; Dehal and Boore, 2005). ent study, we first employed comparative genomic and Recently, genome sequences have become available phylogenetic analyses to identify the evolutionary rela- for several basal vertebrates, including spotted gar tionships of the CRH family of genes: crh1, uts1, and (Lepisosteus oculatus; Amores et al., 2011; Flicek et al., the newly identified crh2. We next used chromogenic 2014). Although spotted gar (Neopterygii; superorder ISH in the brain of the spotted gar to characterize and Ginglymodi) is closely related to teleost fishes (Neopter- analyze expression patterns of these genes. Our analy- ygii; superorder Teleostei), the chromosomal organiza- sis reveals new insights into the evolution of the CRH tion of its genome more closely resembles that of family, with potential functional implications for stress- humans. Neopterygian fishes, including gars, lack the regulating systems across vertebrates. teleost-specific genome duplication that the teleost line- age experienced prior to its massive ecological and evo- MATERIALS AND METHODS lutionary radiation (Christoffels et al., 2004; Hoegg et al., 2004; Jaillon et al., 2004; Amores et al., 2011). Animals The evolutionary position of gars as a sister group to Juvenile spotted gar (sexually immature) were pur- teleosts was proposed based on anatomical data but chased from Rainforest International (53–85 mm stand- has remained controversial. Recent genomic studies ard length [SL]) or caught from the Atchafalaya Basin, using multiple gene sequences or ultraconserved ele- Louisiana (24–26 cm SL). In total nine spotted gar were ments have confirmed that the infraclass Holostei used for the in situ hybridization (ISH) experiments. [orders Lepisosteiformes and Amiiformes; i.e., gars Animal experiments were performed according to regu- (Lepisosteus and Atractosteus spp.) and the bowfin lations established by the Institutional Animal Care and (Amia calva)] forms a monophyletic group that is an out- Use Committee (IACUC) at Louisiana State University. group to the teleosts (Broughton et al., 2013). There are only seven extant species of gar (and one bowfin) Sequence analysis compared with over 30,000 extant teleosts. Despite Throughout this article, we use standard gene this paucity of extant species, Lepisosteiformes are a nomenclature. For fishes, gene names and symbols are hardy group with a fossil record that stretches back italicized and protein names are capitalized. For other over 100 million years to the Albian age (Gayet et al., vertebrates, human conventions are used: gene sym- 2002). Thus, with their ecological and evolutionary prox- bols in all capitals and italicized, protein symbols in all imity to teleosts and the recently sequenced genome of capitals. the spotted gar (L. oculatus), gars are a particularly val- To determine the phylogenetic relationships among uable group for understanding mechanisms of verte- vertebrate CRH gene family members, CRH1, CRH2, brate molecular evolution. and UTS1/UCN1 genes were located by the following The brain anatomy of the spotted gar has been char- searches: TBLASTN searches in Pre-Ensembl for spotted acterized in relatively few histological and immunohisto- gar and painted turtle, TBLASTN searches of the chemical studies. Some spotted gar neuropeptide elephant shark (Callorhinchus milii) genome database expression patterns, including neuropeptide Y and (Venkatesh et al., 2014), GenBank (RRID:nif-0000– gonadotropin-releasing hormone, have been described 02873) for fruitfly (Drosophila melanogaster), peregrine via immunohistochemistry (Chiba, 2005). Other gar falcon (Falco peregrinus;
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