Distribution of a Y1 receptor mRNA in the brain of two lamprey species, the sea lamprey (Petromyzon marinus) and the river lamprey (Lampetra fluviatilis)

Abstract

The neuropeptide Y system consists of several neuropeptides acting through a broad number of receptor subtypes, the NPY family of receptors. NPY receptors are divided into three subfamilies (Y1, Y2, and Y5) that display a complex evolutionary history due to local and large-scale gene duplication events and gene losses. Lampreys emerged from a basal branch of the tree of vertebrates and they are in a key position to shed light on the evolutionary history of the NPY system. One member of the Y1 subfamily has been reported in agnathans, but the phylogenetic tree of the Y1 subfamily is not yet clear. We cloned the sequences of the Y1-subtype receptor of Petromyzon marinus and Lampetra fluviatilis to study the expression pattern of this receptor in lampreys by in situ hybridization and to analyze the phylogeny of the Y1-subfamily receptors in vertebrates. The phylogenetic study showed that the Y1 receptor of lampreys is basal to the Y1/6 branch of the Y1-subfamily receptors. In situ hybridization showed that the Y1 receptor is widely expressed throughout the brain of lampreys, with some regions showing numerous positive neurons, as well as the presence of numerous cerebrospinal fluid-contacting cells in the spinal cord. This broad distribution of the lamprey Y1 receptor is more similar to that found in other vertebrates for the Y1 receptor than that of the other members of the Y1 subfamily: Y4, Y8, and Y6 receptors. Both phylogenetic relationship and expression pattern suggest that this receptor is a Y1 receptor.

Cloning, phylogeny, and regional expression of a Y5 receptor mRNA in the brain of the sea lamprey (Petromyzon marinus)

“…Our results, including phylogenetic analysis and in situ hybridization studies, indicate that this receptor belongs to the Y5 subfamily described for other vertebrates. Furthermore, our results demonstrate that its expression pattern in the sea lamprey brain extensively overlaps with that of the Y1 receptor subtype previously reported (Pérez‐Fernández et al, ); therefore, it is likely that the Y5 subtype is conserved throughout vertebrate evolution.…”

“…It also supports the branching of the lamprey lineage from the common trunk of vertebrates to have occurred between the two whole‐genome duplications (see discussion). Apart from the P. marinus Y1‐subtype receptor (Pérez‐Fernández et al, ), a partial sequence of a putative lamprey Y8 receptor, retrieved from BLAT tool of the UCSC Genome Bioinformatics web site (data not shown), was also included in the phylogenetic tree.…”

“…The size, brightness, and contrast of the images were adjusted with GIMP (GNU image manipulator program). The nomenclature for brain nuclei and structures used in this study is the same followed in our previous work on the Y1‐subtype receptor (Pérez‐Fernández et al, ).…”

Neuropeptide Y family receptors Y1 and Y2 from sea lamprey, Petromyzon marinus

“…Thus it would be necessary to study the expression pattern of these two newly cloned receptors, Y1 and Y2, and compare these with the previously reported Y4 and Y5 (Perez-Fernandez et al, 2013, 2014 to understand their functions. One limitation of our functional analysis in cell culture is that we only investigated the Gai signaling pathway via the chimaeric G protein that connects to the Gaq pathway, but other signaling pathways might be involved.…”

“…Previously, we also identified a Y2-like sequence in L. fluviatilis Xu et al, 2013) although it was uncertain whether it was an ortholog of gnathostome Y2 or Y7. Two of these receptors have also been characterized in detail with regard to mRNA distribution in P. marinus brain using in situ hybridization, namely Y4 and Y5, both of which were found to have broad distribution with only minor differences (Perez-Fernandez et al, 2013, 2014.…”