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Evolutionary origin of a functional gonadotropin in the pituitary of the most primitive vertebrate, hagfish.

ABSTRACT: Hagfish, which lack both jaws and vertebrae, are considered the most primitive vertebrate known, living or extinct. Hagfish have long been the enigma of vertebrate evolution not only because of their evolutionary position, but also because of our lack of knowledge on fundamental processes. Key elements of the reproductive endocrine system in hagfish have yet to be elucidated. Here, the presence and identity of a functional glycoprotein hormone (GPH) have been elucidated from the brown hagfish Paramyxine atami. The hagfish GPH consists of two subunits, alpha and beta, which are synthesized and colocalized in the same cells of the adenohypophysis. The cellular and transcriptional activities of hagfish GPHalpha and -beta were significantly correlated with the developmental stages of the gonad. The purified native GPH induced the release of gonadal sex steroids in vitro. From our phylogenetic analysis, we propose that ancestral glycoprotein alpha-subunit 2 (GPA2) and beta-subunit 5 (GPB5) gave rise to GPHalpha and GPHbeta of the vertebrate glycoprotein hormone family, respectively. The identified hagfish GPHalpha and -beta subunits appear to be the typical gnathostome GPHalpha and -beta subunits based on the sequence and phylogenetic analyses. We hypothesize that the identity of a single functional GPH of the hagfish, hagfish GTH, provides critical evidence for the existence of a pituitary-gonadal system in the earliest divergent vertebrate that likely evolved from an ancestral, prevertebrate exclusively neuroendocrine mechanism by gradual emergence of a previously undescribed control level, the pituitary, which is not found in the Protochordates.

SUBMITTER: Uchida K

PROVIDER: S-EPMC2936635 | biostudies-literature | 2010 Sep

REPOSITORIES: biostudies-literature

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Evolutionary origin of a functional gonadotropin in the pituitary of the most primitive vertebrate, hagfish.

Uchida Katsuhisa K Moriyama Shunsuke S Chiba Hiroaki H Shimotani Toyokazu T Honda Kaori K Miki Makoto M Takahashi Akiyoshi A Sower Stacia A SA Nozaki Masumi M

Proceedings of the National Academy of Sciences of the United States of America 20100823 36

Hagfish, which lack both jaws and vertebrae, are considered the most primitive vertebrate known, living or extinct. Hagfish have long been the enigma of vertebrate evolution not only because of their evolutionary position, but also because of our lack of knowledge on fundamental processes. Key elements of the reproductive endocrine system in hagfish have yet to be elucidated. Here, the presence and identity of a functional glycoprotein hormone (GPH) have been elucidated from the brown hagfish Pa ...[more]

PMID: 20733079

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Project description:Pluripotency is the capacity of early embryonic cells to make all the future lineages of the organism, and the existence of a pluripotent population of cells is important to both germ cell function and the pool of progenitor cells that enable vertebrate development to proceed over time through the process of gastrulation. Oct4, a class V POU transcription factor, is required for maintenance of pluripotency in embryonic stem cells (ESCs) and induction of pluripotency via transcription factor reprogramming. Homologues of Oct4 have been identified in other gnathostomes and classified into two different paralogues: POU5F1 and POU5F3. Here we provide evidence that these proteins are probably derived from a single POUV gene through ancient whole genome duplication events. To approach this issue, we compared the functional conservation and divergence of different POUV proteins in their capacity to support naïve pluripotency in mouse ESCs. We found a strong correlation between POU5F1 activity in naïve pluripotency and the regulation of germ cell specification programs. In contrast, POU5F3 exhibited reduced capacity to support naïve ESCs and its activity in ESCs correlated with the expression of genes associated with pre-gastrulation stages, or primed pluripotency. We detected evidence of this functional segregation as early as Sarcopterygian ancestors, based on the activities of coelacanth POUV proteins. Furthermore, we were able to identify earlier POUV homologues in lamprey and shark, indicating that the earliest point at which mammalian-level pluripotency of both POUV paralogues emerged is between the osteichthyan-chondrichthyan split and the gnathostome-cyclostome split.Taken together, our work highlights the evolutionary history of POUV activities across jawed vertebrates, suggesting that evolutionary pressure has facilitated maintenance of both paralogues over long periods of evolutionary history. In species with both paralogues, subfunctionalization of these proteins appears conserved. However, in many branches of vertebrate evolution, one of these paralogues is lost, suggesting a high level of plasticity in function and precarious balance between retaining both proteins and the overall levels of POUV activity in different developmental systems. While the conserved subfunctionalization of POUV activities evolved at some point just before the appearance of tetrapods, the additional divergent activities of this protein family appear to have evolved independently in each vertebrate lineage after gnathostome radiation.

Dataset Information

Evolutionary origin of a functional gonadotropin in the pituitary of the most primitive vertebrate, hagfish.

Publications

Evolutionary origin of a functional gonadotropin in the pituitary of the most primitive vertebrate, hagfish.

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