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Characterization of the neurohypophysial hormone gene loci in elephant shark and the Japanese lamprey: origin of the vertebrate neurohypophysial hormone genes.

Gwee PC, Tay BH, Brenner S, Venkatesh B - BMC Evol. Biol. (2009)

Bottom Line: The amphioxus locus encodes a single neurohypophysial hormone, designated as [Ile4]vasotocin.The duplicated genes were linked tail-to-head like their homologs in elephant shark, coelacanth and non-eutherian tetrapods.In contrast to the conserved linkage of the neurohypophysial genes in these vertebrates, the neurohypophysial hormone gene locus has experienced extensive rearrangements in the teleost lineage.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Molecular and Cell Biology, A*STAR (Agency for Science, Technology and Research), Biopolis, 138673 Singapore. pcgwee@imcb.a-star.edu.sg

ABSTRACT

Background: Vasopressin and oxytocin are mammalian neurohypophysial hormones with distinct functions. Vasopressin is involved mainly in osmoregulation and oxytocin is involved primarily in parturition and lactation. Jawed vertebrates contain at least one homolog each of vasopressin and oxytocin, whereas only a vasopressin-family hormone, vasotocin, has been identified in jawless vertebrates. The genes encoding vasopressin and oxytocin are closely linked tail-to-tail in eutherian mammals whereas their homologs in chicken, Xenopus and coelacanth (vasotocin and mesotocin) are linked tail-to-head. In contrast, their pufferfish homologs, vasotocin and isotocin, are located on the same strand of DNA with isotocin located upstream of vasotocin and separated by five genes. These differences in the arrangement of the two genes in different bony vertebrate lineages raise questions about their origin and ancestral arrangement. To trace the origin of these genes, we have sequenced BAC clones from the neurohypophysial gene loci in a cartilaginous fish, the elephant shark (Callorhinchus milii), and in a jawless vertebrate, the Japanese lamprey (Lethenteron japonicum). We have also analyzed the neurohypophysial hormone gene locus in an invertebrate chordate, the amphioxus (Branchiostoma floridae).

Results: The elephant shark neurohypophysial hormone genes encode vasotocin and oxytocin, and are linked tail-to-head like their homologs in coelacanth and non-eutherian tetrapods. Besides the hypothalamus, the two genes are also expressed in the ovary. In addition, the vasotocin gene is expressed in the kidney, rectal gland and intestine. These expression profiles indicate a paracrine role for the two hormones. The lamprey locus contains a single neurohypophysial hormone gene, the vasotocin. The synteny of genes in the lamprey locus is conserved in elephant shark, coelacanth and tetrapods but disrupted in teleost fishes. The amphioxus locus encodes a single neurohypophysial hormone, designated as [Ile4]vasotocin.

Conclusion: The vasopressin- and oxytocin-family of neurohypophysial hormones evolved in a common ancestor of jawed vertebrates through tandem duplication of the ancestral vasotocin gene. The duplicated genes were linked tail-to-head like their homologs in elephant shark, coelacanth and non-eutherian tetrapods. In contrast to the conserved linkage of the neurohypophysial genes in these vertebrates, the neurohypophysial hormone gene locus has experienced extensive rearrangements in the teleost lineage.

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The neurohypophysial gene locus in the elephant shark (A) and Japanese lamprey (B). The BACs used for generating the sequences are shown below. Arrows represent genes and indicate the direction of transcription. Coloured vertical lines represent repetitive sequences. VT, vasotocin gene; OT, oxytocin gene; ProSAPiP1, proline rich synapse associated protein interacting protein 1; UBOX5, U-box domain containing 5; GNRH2, gonadotropin-releasing hormone 2; PTPRA, protein tyrosine phosphatase, receptor type, A.
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Figure 2: The neurohypophysial gene locus in the elephant shark (A) and Japanese lamprey (B). The BACs used for generating the sequences are shown below. Arrows represent genes and indicate the direction of transcription. Coloured vertical lines represent repetitive sequences. VT, vasotocin gene; OT, oxytocin gene; ProSAPiP1, proline rich synapse associated protein interacting protein 1; UBOX5, U-box domain containing 5; GNRH2, gonadotropin-releasing hormone 2; PTPRA, protein tyrosine phosphatase, receptor type, A.

Mentions: We probed an elephant shark BAC library with a fragment of the elephant shark vasotocin gene and identified six overlapping BAC clones. Two of the BAC clones, #191N1 and #208M19, were sequenced completely to obtain 167 kb contiguous sequence (GenBank accession number FJ185172). It contains sequences for vasotocin and oxytocin genes in addition to three other complete genes (Prosapip1, Ubox5 and Gnrh2) and one partial gene (Ptpra) (Fig 2A). Oxytocin is typically only found in placental mammals and is involved in lactation, uterine smooth muscle contraction and maternal behavior. However, oxytocin had been previously purified from the hypothalamus of a holocephalian cartilaginous fish, the ratfish, the only non-mammalian vertebrate to contain oxytocin [14]. The presence of oxytocin gene in elephant shark indicates that oxytocin is most likely common to all holocephalian cartilaginous fishes. The elephant shark vasotocin and oxytocin genes are arranged tail-to-head like their homologs in coelacanth, Xenopus, chicken and opossum. They each comprise three exons and two introns like their homologs in other vertebrates. The introns of elephant shark vasotocin and oxytocin genes (1.16 kb to 3.24 kb) are longer than their homologs in human (84 bp to 1.37 kb) but comparable to that in coelacanth (1.55 kb to 5.57 kb). The intergenic distance between the elephant shark genes is, however, shorter (8.3 kb) than that between the genes in human (12 kb) and coelacanth (15.4 kb). Overall, repetitive sequences account for 41.6% of the elephant shark locus with LINEs and SINEs contributing 16.9% and 20.1% respectively (Fig 2A).


Characterization of the neurohypophysial hormone gene loci in elephant shark and the Japanese lamprey: origin of the vertebrate neurohypophysial hormone genes.

Gwee PC, Tay BH, Brenner S, Venkatesh B - BMC Evol. Biol. (2009)

The neurohypophysial gene locus in the elephant shark (A) and Japanese lamprey (B). The BACs used for generating the sequences are shown below. Arrows represent genes and indicate the direction of transcription. Coloured vertical lines represent repetitive sequences. VT, vasotocin gene; OT, oxytocin gene; ProSAPiP1, proline rich synapse associated protein interacting protein 1; UBOX5, U-box domain containing 5; GNRH2, gonadotropin-releasing hormone 2; PTPRA, protein tyrosine phosphatase, receptor type, A.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2656470&req=5

Figure 2: The neurohypophysial gene locus in the elephant shark (A) and Japanese lamprey (B). The BACs used for generating the sequences are shown below. Arrows represent genes and indicate the direction of transcription. Coloured vertical lines represent repetitive sequences. VT, vasotocin gene; OT, oxytocin gene; ProSAPiP1, proline rich synapse associated protein interacting protein 1; UBOX5, U-box domain containing 5; GNRH2, gonadotropin-releasing hormone 2; PTPRA, protein tyrosine phosphatase, receptor type, A.
Mentions: We probed an elephant shark BAC library with a fragment of the elephant shark vasotocin gene and identified six overlapping BAC clones. Two of the BAC clones, #191N1 and #208M19, were sequenced completely to obtain 167 kb contiguous sequence (GenBank accession number FJ185172). It contains sequences for vasotocin and oxytocin genes in addition to three other complete genes (Prosapip1, Ubox5 and Gnrh2) and one partial gene (Ptpra) (Fig 2A). Oxytocin is typically only found in placental mammals and is involved in lactation, uterine smooth muscle contraction and maternal behavior. However, oxytocin had been previously purified from the hypothalamus of a holocephalian cartilaginous fish, the ratfish, the only non-mammalian vertebrate to contain oxytocin [14]. The presence of oxytocin gene in elephant shark indicates that oxytocin is most likely common to all holocephalian cartilaginous fishes. The elephant shark vasotocin and oxytocin genes are arranged tail-to-head like their homologs in coelacanth, Xenopus, chicken and opossum. They each comprise three exons and two introns like their homologs in other vertebrates. The introns of elephant shark vasotocin and oxytocin genes (1.16 kb to 3.24 kb) are longer than their homologs in human (84 bp to 1.37 kb) but comparable to that in coelacanth (1.55 kb to 5.57 kb). The intergenic distance between the elephant shark genes is, however, shorter (8.3 kb) than that between the genes in human (12 kb) and coelacanth (15.4 kb). Overall, repetitive sequences account for 41.6% of the elephant shark locus with LINEs and SINEs contributing 16.9% and 20.1% respectively (Fig 2A).

Bottom Line: The amphioxus locus encodes a single neurohypophysial hormone, designated as [Ile4]vasotocin.The duplicated genes were linked tail-to-head like their homologs in elephant shark, coelacanth and non-eutherian tetrapods.In contrast to the conserved linkage of the neurohypophysial genes in these vertebrates, the neurohypophysial hormone gene locus has experienced extensive rearrangements in the teleost lineage.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Molecular and Cell Biology, A*STAR (Agency for Science, Technology and Research), Biopolis, 138673 Singapore. pcgwee@imcb.a-star.edu.sg

ABSTRACT

Background: Vasopressin and oxytocin are mammalian neurohypophysial hormones with distinct functions. Vasopressin is involved mainly in osmoregulation and oxytocin is involved primarily in parturition and lactation. Jawed vertebrates contain at least one homolog each of vasopressin and oxytocin, whereas only a vasopressin-family hormone, vasotocin, has been identified in jawless vertebrates. The genes encoding vasopressin and oxytocin are closely linked tail-to-tail in eutherian mammals whereas their homologs in chicken, Xenopus and coelacanth (vasotocin and mesotocin) are linked tail-to-head. In contrast, their pufferfish homologs, vasotocin and isotocin, are located on the same strand of DNA with isotocin located upstream of vasotocin and separated by five genes. These differences in the arrangement of the two genes in different bony vertebrate lineages raise questions about their origin and ancestral arrangement. To trace the origin of these genes, we have sequenced BAC clones from the neurohypophysial gene loci in a cartilaginous fish, the elephant shark (Callorhinchus milii), and in a jawless vertebrate, the Japanese lamprey (Lethenteron japonicum). We have also analyzed the neurohypophysial hormone gene locus in an invertebrate chordate, the amphioxus (Branchiostoma floridae).

Results: The elephant shark neurohypophysial hormone genes encode vasotocin and oxytocin, and are linked tail-to-head like their homologs in coelacanth and non-eutherian tetrapods. Besides the hypothalamus, the two genes are also expressed in the ovary. In addition, the vasotocin gene is expressed in the kidney, rectal gland and intestine. These expression profiles indicate a paracrine role for the two hormones. The lamprey locus contains a single neurohypophysial hormone gene, the vasotocin. The synteny of genes in the lamprey locus is conserved in elephant shark, coelacanth and tetrapods but disrupted in teleost fishes. The amphioxus locus encodes a single neurohypophysial hormone, designated as [Ile4]vasotocin.

Conclusion: The vasopressin- and oxytocin-family of neurohypophysial hormones evolved in a common ancestor of jawed vertebrates through tandem duplication of the ancestral vasotocin gene. The duplicated genes were linked tail-to-head like their homologs in elephant shark, coelacanth and non-eutherian tetrapods. In contrast to the conserved linkage of the neurohypophysial genes in these vertebrates, the neurohypophysial hormone gene locus has experienced extensive rearrangements in the teleost lineage.

Show MeSH
Related in: MedlinePlus