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Transcriptomic analysis of the lesser spotted catshark (Scyliorhinus canicula) pancreas, liver and brain reveals molecular level conservation of vertebrate pancreas function.

Mulley JF, Hargreaves AD, Hegarty MJ, Heller RS, Swain MT - BMC Genomics (2014)

Bottom Line: Conservation of pancreatic hormones and genes encoding digestive proteins support the single, early evolution of a distinct pancreatic gland with endocrine and exocrine functions in jawed vertebrates.In addition, we demonstrate that chondrichthyes lack pancreatic polypeptide (PP) and that reports of PP in the literature are likely due cross-reaction with PYY and/or NPY in the pancreas.A three hormone islet organ is therefore the ancestral jawed vertebrate condition, later elaborated upon only in the tetrapod lineage.

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, Bangor University, Brambell Building, Deiniol Road, Bangor, Gwynedd LL57 2UW, United Kingdom. j.mulley@bangor.ac.uk.

ABSTRACT

Background: Understanding the evolution of the vertebrate pancreas is key to understanding its functions. The chondrichthyes (cartilaginous fish such as sharks and rays) have often been suggested to possess the most ancient example of a distinct pancreas with both hormonal (endocrine) and digestive (exocrine) roles. The lack of genetic, genomic and transcriptomic data for cartilaginous fish has hindered a more thorough understanding of the molecular-level functions of the chondrichthyan pancreas, particularly with respect to their "unusual" energy metabolism (where ketone bodies and amino acids are the main oxidative fuel source) and their paradoxical ability to both maintain stable blood glucose levels and tolerate extensive periods of hypoglycemia. In order to shed light on some of these processes, we carried out the first large-scale comparative transcriptomic survey of multiple cartilaginous fish tissues: the pancreas, brain and liver of the lesser spotted catshark, Scyliorhinus canicula.

Results: We generated a mutli-tissue assembly comprising 86,006 contigs, of which 44,794 were assigned to a particular tissue or combination of tissues based on mapping of sequencing reads. We have characterised transcripts encoding genes involved in insulin regulation, glucose sensing, transcriptional regulation, signaling and digestion, as well as many peptide hormone precursors and their receptors for the first time. Comparisons to mammalian pancreas transcriptomes reveals that mechanisms of glucose sensing and insulin regulation used to establish and maintain a stable internal environment are conserved across jawed vertebrates and likely pre-date the vertebrate radiation. Conservation of pancreatic hormones and genes encoding digestive proteins support the single, early evolution of a distinct pancreatic gland with endocrine and exocrine functions in jawed vertebrates. In addition, we demonstrate that chondrichthyes lack pancreatic polypeptide (PP) and that reports of PP in the literature are likely due cross-reaction with PYY and/or NPY in the pancreas. A three hormone islet organ is therefore the ancestral jawed vertebrate condition, later elaborated upon only in the tetrapod lineage.

Conclusions: The cartilaginous fish are a great untapped resource for the reconstruction of patterns and processes of vertebrate evolution and new approaches such as those described in this paper will greatly facilitate their incorporation into the rank of "model organism".

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Phylogenetic tree of the major extant vertebrate groups. The relationships of the most common chondrichthyan (cartilaginous fish) model species (Elephant shark, Callorhinchus milii; Little skate, Leucoraja erinacea; Lesser spotted catshark, Scyliorhinus canicula; Spiny dogfish, Squalus acanthias) are shown, as are representative lineages from the ray-finned (actinopterygian) and lobe-finned (sarcopterygian) fish. The origin of the combined endocrine and exocrine pancreatic gland at the base of the jawed vertebrates is indicated.
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Fig1: Phylogenetic tree of the major extant vertebrate groups. The relationships of the most common chondrichthyan (cartilaginous fish) model species (Elephant shark, Callorhinchus milii; Little skate, Leucoraja erinacea; Lesser spotted catshark, Scyliorhinus canicula; Spiny dogfish, Squalus acanthias) are shown, as are representative lineages from the ray-finned (actinopterygian) and lobe-finned (sarcopterygian) fish. The origin of the combined endocrine and exocrine pancreatic gland at the base of the jawed vertebrates is indicated.

Mentions: Chondrichthyans (cartilaginous fish such as sharks, skates, rays (elasmobranchs) and chimeras (holocephalans)) are the most distant group relative to mammals such as ourselves to possess a distinct pancreatic gland containing multiple cell types with both endocrine and exocrine functions[1, 2]. The more distant vertebrate lineages such as the jawless hagfish and lampreys (Figure 1) possess only small islet organs containing insulin- and somatostatin-producing endocrine cells and these islets lack any glucagon-producing cells or exocrine function[2–4]. The accumulation of multiple cell types into a single compact gland was an important step in pancreas evolution (and can be considered to be an evolutionary innovation)[5, 6] and it has been suggested that a switch from sensing gut-glucose to blood-glucose to establish a “stable inner milieu” via homeostatic mechanisms may have been an important factor in the evolution of a more complex glucose-dependent brain in vertebrates, protected from hyper- and hypoglycaemia[7–9]. However, the fact that insulin-like peptides in insects seem to fulfil similar roles in glucose metabolism and other physiological processes such as growth and reproduction suggests that at least some elements of these mechanisms may have a more ancient origin[10].Figure 1


Transcriptomic analysis of the lesser spotted catshark (Scyliorhinus canicula) pancreas, liver and brain reveals molecular level conservation of vertebrate pancreas function.

Mulley JF, Hargreaves AD, Hegarty MJ, Heller RS, Swain MT - BMC Genomics (2014)

Phylogenetic tree of the major extant vertebrate groups. The relationships of the most common chondrichthyan (cartilaginous fish) model species (Elephant shark, Callorhinchus milii; Little skate, Leucoraja erinacea; Lesser spotted catshark, Scyliorhinus canicula; Spiny dogfish, Squalus acanthias) are shown, as are representative lineages from the ray-finned (actinopterygian) and lobe-finned (sarcopterygian) fish. The origin of the combined endocrine and exocrine pancreatic gland at the base of the jawed vertebrates is indicated.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4362833&req=5

Fig1: Phylogenetic tree of the major extant vertebrate groups. The relationships of the most common chondrichthyan (cartilaginous fish) model species (Elephant shark, Callorhinchus milii; Little skate, Leucoraja erinacea; Lesser spotted catshark, Scyliorhinus canicula; Spiny dogfish, Squalus acanthias) are shown, as are representative lineages from the ray-finned (actinopterygian) and lobe-finned (sarcopterygian) fish. The origin of the combined endocrine and exocrine pancreatic gland at the base of the jawed vertebrates is indicated.
Mentions: Chondrichthyans (cartilaginous fish such as sharks, skates, rays (elasmobranchs) and chimeras (holocephalans)) are the most distant group relative to mammals such as ourselves to possess a distinct pancreatic gland containing multiple cell types with both endocrine and exocrine functions[1, 2]. The more distant vertebrate lineages such as the jawless hagfish and lampreys (Figure 1) possess only small islet organs containing insulin- and somatostatin-producing endocrine cells and these islets lack any glucagon-producing cells or exocrine function[2–4]. The accumulation of multiple cell types into a single compact gland was an important step in pancreas evolution (and can be considered to be an evolutionary innovation)[5, 6] and it has been suggested that a switch from sensing gut-glucose to blood-glucose to establish a “stable inner milieu” via homeostatic mechanisms may have been an important factor in the evolution of a more complex glucose-dependent brain in vertebrates, protected from hyper- and hypoglycaemia[7–9]. However, the fact that insulin-like peptides in insects seem to fulfil similar roles in glucose metabolism and other physiological processes such as growth and reproduction suggests that at least some elements of these mechanisms may have a more ancient origin[10].Figure 1

Bottom Line: Conservation of pancreatic hormones and genes encoding digestive proteins support the single, early evolution of a distinct pancreatic gland with endocrine and exocrine functions in jawed vertebrates.In addition, we demonstrate that chondrichthyes lack pancreatic polypeptide (PP) and that reports of PP in the literature are likely due cross-reaction with PYY and/or NPY in the pancreas.A three hormone islet organ is therefore the ancestral jawed vertebrate condition, later elaborated upon only in the tetrapod lineage.

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, Bangor University, Brambell Building, Deiniol Road, Bangor, Gwynedd LL57 2UW, United Kingdom. j.mulley@bangor.ac.uk.

ABSTRACT

Background: Understanding the evolution of the vertebrate pancreas is key to understanding its functions. The chondrichthyes (cartilaginous fish such as sharks and rays) have often been suggested to possess the most ancient example of a distinct pancreas with both hormonal (endocrine) and digestive (exocrine) roles. The lack of genetic, genomic and transcriptomic data for cartilaginous fish has hindered a more thorough understanding of the molecular-level functions of the chondrichthyan pancreas, particularly with respect to their "unusual" energy metabolism (where ketone bodies and amino acids are the main oxidative fuel source) and their paradoxical ability to both maintain stable blood glucose levels and tolerate extensive periods of hypoglycemia. In order to shed light on some of these processes, we carried out the first large-scale comparative transcriptomic survey of multiple cartilaginous fish tissues: the pancreas, brain and liver of the lesser spotted catshark, Scyliorhinus canicula.

Results: We generated a mutli-tissue assembly comprising 86,006 contigs, of which 44,794 were assigned to a particular tissue or combination of tissues based on mapping of sequencing reads. We have characterised transcripts encoding genes involved in insulin regulation, glucose sensing, transcriptional regulation, signaling and digestion, as well as many peptide hormone precursors and their receptors for the first time. Comparisons to mammalian pancreas transcriptomes reveals that mechanisms of glucose sensing and insulin regulation used to establish and maintain a stable internal environment are conserved across jawed vertebrates and likely pre-date the vertebrate radiation. Conservation of pancreatic hormones and genes encoding digestive proteins support the single, early evolution of a distinct pancreatic gland with endocrine and exocrine functions in jawed vertebrates. In addition, we demonstrate that chondrichthyes lack pancreatic polypeptide (PP) and that reports of PP in the literature are likely due cross-reaction with PYY and/or NPY in the pancreas. A three hormone islet organ is therefore the ancestral jawed vertebrate condition, later elaborated upon only in the tetrapod lineage.

Conclusions: The cartilaginous fish are a great untapped resource for the reconstruction of patterns and processes of vertebrate evolution and new approaches such as those described in this paper will greatly facilitate their incorporation into the rank of "model organism".

Show MeSH
Related in: MedlinePlus