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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.

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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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Comparison of amino acid sequences of vasopressin family hormone precursors in vertebrates. The alignment was generated by ClustalX. Amino acid residues conserved in all vertebrates are marked with an asterisk. B. floridae, Branchiostoma floridae; X. tropicalis, Xenopus tropicalis; and T. scyllium, Triakis scyllium. VP, vasopressin and VT, vasotocin. Accession numbers of sequences used in the alignment: NP_000481.2 (human VP), BAA24026.1 (lungfish VT), O42499 (fugu VT), BAD27476.1 (T. scyllium VT) and BAA06669.1 (lamprey VT). Sequences for Xenopus tropicalis and coelacanth were generated in a previous study [8] while sequences for elephant shark (eshark) and amphioxus (B. floridae) were generated in this study.
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Figure 4: Comparison of amino acid sequences of vasopressin family hormone precursors in vertebrates. The alignment was generated by ClustalX. Amino acid residues conserved in all vertebrates are marked with an asterisk. B. floridae, Branchiostoma floridae; X. tropicalis, Xenopus tropicalis; and T. scyllium, Triakis scyllium. VP, vasopressin and VT, vasotocin. Accession numbers of sequences used in the alignment: NP_000481.2 (human VP), BAA24026.1 (lungfish VT), O42499 (fugu VT), BAD27476.1 (T. scyllium VT) and BAA06669.1 (lamprey VT). Sequences for Xenopus tropicalis and coelacanth were generated in a previous study [8] while sequences for elephant shark (eshark) and amphioxus (B. floridae) were generated in this study.

Mentions: The elephant shark vasotocin gene codes for a 163-amino acid protein comprising a signal peptide, the vasotocin nonapeptide, a neurophysin and a copeptin similar to vasotocin precursors in other vertebrates (Fig 3). An atypical tripeptide sequence, Gly-Arg-Arg, links the hormone to the neurophysin and presumably acts as a signal for proteolytic processing and carboxyl-terminal amidation of vasotocin. All the cysteine residues that are considered important for the conformation of neurophysin are conserved in the elephant shark vasotocin neurophysin (Fig 4). The copeptin moiety at the carboxyl terminal includes an N-linked glycosylation site that is conserved in all vertebrates except teleost fishes and lamprey (Fig. 4). It also includes a leucine-rich core segment similar to the copeptin of vasopressin-family precursors in all vertebrates (Fig 4).


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)

Comparison of amino acid sequences of vasopressin family hormone precursors in vertebrates. The alignment was generated by ClustalX. Amino acid residues conserved in all vertebrates are marked with an asterisk. B. floridae, Branchiostoma floridae; X. tropicalis, Xenopus tropicalis; and T. scyllium, Triakis scyllium. VP, vasopressin and VT, vasotocin. Accession numbers of sequences used in the alignment: NP_000481.2 (human VP), BAA24026.1 (lungfish VT), O42499 (fugu VT), BAD27476.1 (T. scyllium VT) and BAA06669.1 (lamprey VT). Sequences for Xenopus tropicalis and coelacanth were generated in a previous study [8] while sequences for elephant shark (eshark) and amphioxus (B. floridae) were generated in this study.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Comparison of amino acid sequences of vasopressin family hormone precursors in vertebrates. The alignment was generated by ClustalX. Amino acid residues conserved in all vertebrates are marked with an asterisk. B. floridae, Branchiostoma floridae; X. tropicalis, Xenopus tropicalis; and T. scyllium, Triakis scyllium. VP, vasopressin and VT, vasotocin. Accession numbers of sequences used in the alignment: NP_000481.2 (human VP), BAA24026.1 (lungfish VT), O42499 (fugu VT), BAD27476.1 (T. scyllium VT) and BAA06669.1 (lamprey VT). Sequences for Xenopus tropicalis and coelacanth were generated in a previous study [8] while sequences for elephant shark (eshark) and amphioxus (B. floridae) were generated in this study.
Mentions: The elephant shark vasotocin gene codes for a 163-amino acid protein comprising a signal peptide, the vasotocin nonapeptide, a neurophysin and a copeptin similar to vasotocin precursors in other vertebrates (Fig 3). An atypical tripeptide sequence, Gly-Arg-Arg, links the hormone to the neurophysin and presumably acts as a signal for proteolytic processing and carboxyl-terminal amidation of vasotocin. All the cysteine residues that are considered important for the conformation of neurophysin are conserved in the elephant shark vasotocin neurophysin (Fig 4). The copeptin moiety at the carboxyl terminal includes an N-linked glycosylation site that is conserved in all vertebrates except teleost fishes and lamprey (Fig. 4). It also includes a leucine-rich core segment similar to the copeptin of vasopressin-family precursors in all vertebrates (Fig 4).

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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