Evolution of Hormone Function: Proglucagon-derived Peptides and Their Receptors

Irwin, David M.

doi:10.1641/0006-3568(2005)055[0583:eohfpp]2.0.co;2

Cited by 20 publications

(30 citation statements)

References 54 publications

(109 reference statements)

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“…This conclusion was drawn from an analysis of a more complete set of receptor genes from diverse vertebrate species and was strengthened by the claim that the putative fish Glp1r was in a genomic neighbourhood that was conserved with amphibians and was linked to genes that are on the same chromosome that encodes mouse Glp1r [28]. In contrast to our earlier analysis [17,35], this new study [28] only identified four genes, instead of the five we detected, in the Xenopus genome with similarity to the mammalian receptors for proglucagon‐derived peptides and GIP. These observations prompted us to conduct a new phylogenetic and genomic analysis of diverse vertebrate genomes for genes similar to mammalian Gcgr , Glp1r , Glp2r and Gipr .…”

Section: Glucagon Receptor Gene Subfamilymentioning

confidence: 66%

“…While a Glp1r gene was not identified in fish genomes, orthologs of Gcgr , Glp2r and Gipr were [17,35,36]. In our initial analysis [17,35] the putative Gipr group was poorly supported and did not reflect the accepted species phylogeny. Additionally, in some analyses it was suggested that there were two different types of receptors in this group.…”

Section: Glucagon Receptor Gene Subfamilymentioning

confidence: 76%

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Incretin hormones and the expanding families of glucagon‐like sequences and their receptors

Irwin

Prentice

2011

Diabetes Obesity Metabolism

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Peptide hormones encoded by the proglucagon (Gcg) and glucose-dependent insulinotropic polypeptide (Gip) genes are evolutionarily related glucagon-like sequences and act through a subfamily of G-protein-coupled receptors. A better understanding of the evolutionary history of these hormones and receptors should yield insight into their biological functions. The availability of a large number of near-complete vertebrate genome sequences is a powerful resource to address questions concerning the evolution of sequences; here, we utilize these resources to examine the evolution of glucagon-like sequences and their receptors. These studies led to the discovery of novel genes for a glucagon receptor-like receptor (Grlr) and a glucagon-like sequence (exendin) in vertebrates. Both exendin and GRLR have ancient origins, early in vertebrate evolution, but have been lost on the ancestral lineage leading to extant mammals. We also show that exendin and GRLR are both expressed in the brain of the chicken and Xenopus tropicals, results that suggest that the products of these genes function in this tissue. The lack of exendin or Grlr genes in mammals suggests that other genes may have acquired the functions of exendin and Grlr during mammalian evolution.

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Section: Glucagon Receptor Gene Subfamilymentioning

confidence: 66%

Section: Glucagon Receptor Gene Subfamilymentioning

confidence: 76%

Incretin hormones and the expanding families of glucagon‐like sequences and their receptors

Irwin

Prentice

2011

Diabetes Obesity Metabolism

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“…Studies have revealed that intimate interacting partners do not always emerge simultaneously; specific interactions among biomolecules often form in a stepwise Darwinian fashion, as parts of systems do not remain static and can be co-opted for novel functions (Thornton 2001, Irwin 2005, Bridgham et al 2006, J He, D M Irwin, Y P Zhang, unpublished observations). Gene duplication, and gain and loss of interactions through mutations in existing proteins are the two recognized major evolutionary processes shaping the specific interactions among biomolecules (Wagner 2001, 2003, Berg et al 2004.…”

Section: Introductionmentioning

confidence: 98%

Stepwise loss of motilin and its specific receptor genes in rodents

He¹,

Irwin²,

Chen³

et al. 2009

Journal of Molecular Endocrinology

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Specific interactions among biomolecules drive virtually all cellular functions and underlie phenotypic complexity and diversity. Biomolecules are not isolated particles, but are elements of integrated interaction networks, and play their roles through specific interactions. Simultaneous emergence or loss of multiple interacting partners is unlikely. If one of the interacting partners is lost, then what are the evolutionary consequences for the retained partner? Taking advantages of the availability of the large number of mammalian genome sequences and knowledge of phylogenetic relationships of the species, we examined the evolutionary fate of the motilin (MLN) hormone gene, after the pseudogenization of its specific receptor, MLN receptor (MLNR), on the rodent lineage. We speculate that the MLNR gene became a pseudogene before the divergence of the squirrel and other rodents about 75 mya. The evolutionary consequences for the MLN gene were diverse. While an intact open reading frame for the MLN gene, which appears functional, was preserved in the kangaroo rat, the MLN gene became inactivated independently on the lineages leading to the guinea pig and the common ancestor of the mouse and rat. Gain and loss of specific interactions among biomolecules through the birth and death of genes for biomolecules point to a general evolutionary dynamic: gene birth and death are widespread phenomena in genome evolution, at the genetic level; thus, once mutations arise, a stepwise process of elaboration and optimization ensues, which gradually integrates and orders mutations into a coherent pattern.

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“…Because there is an intimate association between the ligand and receptor, one might expect that the genes for receptors and hormones should co-evolve, and that new ligandreceptor pairs would evolve from parallel duplications of the hormone and receptor genes [35,36]. However, the evolutionary history of MLNR does not match that of its cognate ligands.…”

Section: Discussionmentioning

confidence: 99%

Gene duplication plays a major role in gene co-option: Studies into the evolution of the motilin/ghrelin family and their receptors

David

Zhang

2011

Chin. Sci. Bull.

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Extant genes can be modified, or 'tinkered with', to provide new roles or new characteristics of these genes. At the genetic level, this often involves gene duplication and specialization of the resulting genes into particular functions. We investigate how ligand-receptor partnerships evolve after gene duplication. While significant work has been conducted in this area, the examination of additional models should help us better understand the proposed models and potentially reveal novel evolutionary patterns and dynamics. We use bioinformatics, comparative genomics and phylogenetic analyses to show that preproghrelin and prepromotilin descended from a common ancestor and that a gene duplication generated these two genes shortly after the divergence of amphibians and amniotes. The evolutionary history of the receptor family differs from that of their cognate ligands. GPR39 diverges first, and an ancestral receptor gives rise to receptors classified as fish-specific clade A, GHSR and MLNR by successive gene duplications occurring before the divergence of tetrapods and ray-finned fish. The ghrelin/GHSR system is maintained and functionally conserved from fish to mammals. Motilin-MLNR specificity must have arisen by ligand-receptor coevolution after the MLN hormone gene diverged from the GHRL gene in the amniote lineage. Conserved molecular machinery can give rise to new neuroendocrine response mechanisms by the co-option of duplicated genes. Gene duplication is both parsimonious and creative in producing elements for evolutionary tinkering and plays a major role in gene co-option, thus aiding the evolution of greater biological complexity.ghrelin, motilin, gene family, ligand, receptor, coevolution, gene interaction Citation:He J, David I M, Zhang Y P. Gene duplication plays a major role in gene co-option: Studies into the evolution of the motilin/ghrelin family and their receptors.

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Evolution of Hormone Function: Proglucagon-derived Peptides and Their Receptors

Abstract: The mammalian proglucagon gene encodes three related sequences, glucagon and the glucagon-like peptides 1 and 2

Cited by 20 publications

References 54 publications

Incretin hormones and the expanding families of glucagon‐like sequences and their receptors

Incretin hormones and the expanding families of glucagon‐like sequences and their receptors

Stepwise loss of motilin and its specific receptor genes in rodents

Gene duplication plays a major role in gene co-option: Studies into the evolution of the motilin/ghrelin family and their receptors

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