Tryptophan hydroxylase and serotonin receptor 1A expression in the retina of the sea lamprey.
The dual development of the retina of lampreys is exceptional among vertebrates and offers an interesting EvoDevo (evolutionary developmental biology) model for understanding the origin and evolution of the vertebrate retina. Only a single type of photoreceptor, ganglion cell and bipolar cell are present in the early-differentiated central retina of lamprey prolarvae. A lateral retina appears later in medium-sized larvae (about 3 years after hatching in the sea lamprey), growing and remaining largely neuroblastic until metamorphosis. In this lateral retina, only ganglion cells and optic fibers differentiate in larvae, whereas differentiation of amacrine, horizontal, photoreceptor and bipolar cells mainly takes place during metamorphosis, which gives rise to the adult retina. Serotonin (5-hydroxytryptamine, 5-HT) is a neurotransmitter found in the retina of vertebrates whose synthesis is mediated by the rate-limiting enzyme tryptophan hydroxylase (TPH). TPH is also the first enzyme in the biosynthetic pathways of melatonin in photoreceptor cells. The serotonin 1A receptor (5-HT1A) is a major determinant of the activity of both serotonergic cells and their targets due to its pre- and post-synaptic location. Here, we report the developmental pattern of expression of tph and 5-ht1a transcripts in the sea lamprey retina by means of in situ hybridization. In larvae, strong tph mRNA signal was observed in photoreceptors and putative ganglion cells of the central retina, and in some neuroblasts of the lateral retina. In adults, strong tph expression was observed in bipolar, amacrine and ganglion cells and in photoreceptors. In the prolarval (central) retina, all the differentiated retinal cells expressed 5-ht1a transcripts, which were not observed in undifferentiated cells. In larvae, photoreceptors, bipolar cells and ganglion cells in the central retina, and neuroblasts in the lateral retina, showed 5-ht1a expression. In the adult retina, expression of 5-ht1a transcript was mainly observed in the myoid region of both short and long photoreceptors, and was also observed in bipolar, amacrine and ganglion cells. Some 5-HT-immunoreactive amacrine cells have already been reported in the adult lamprey retina. Our study supports the serotonergic phenotype of these amacrine cells of lampreys and also suggests that other retinal neurons could synthesize serotonin at levels not detectable by immunohistochemistry. The expression of the tph transcript in retinal photoreceptors of lampreys strongly suggests that they synthesize melatonin and that this pathway appeared early and has been conserved throughout evolution in vertebrates. The expression of tph and 5-ht1a in neuroblasts also indicates that serotonin might be playing developmental roles in the larval lamprey retina.
Department of Cell Biology and Ecology, CIBUS, Faculty of Biology, University of Santiago de Compostela, 15782 Santiago de Compostela, Spain.
María Eugenia
ME
Cornide-Petronio
Department of Cell Biology and Ecology, CIBUS, Faculty of Biology, University of Santiago de Compostela, 15782 Santiago de Compostela, Spain.
Ramón
R
Anadón
Department of Cell Biology and Ecology, CIBUS, Faculty of Biology, University of Santiago de Compostela, 15782 Santiago de Compostela, Spain. Electronic address: anton.barreiro@gmail.com.
Antón
A
Barreiro-Iglesias
Department of Cell Biology and Ecology, CIBUS, Faculty of Biology, University of Santiago de Compostela, 15782 Santiago de Compostela, Spain. Electronic address: mcelina.rodicio@usc.es.
María Celina
MC
Rodicio
D025042:Amacrine Cells / Q000378:metabolism; D000818:Animals; D007150:Immunohistochemistry; D017403:In Situ Hybridization; D007814:Larva / Q000378:metabolism; D058953:Neural Stem Cells / Q000378:metabolism; D048428:Petromyzon / Q000378:metabolism*; D020419:Photoreceptor Cells, Vertebrate; D012333:RNA, Messenger / Q000378:metabolism; D044282:Receptor, Serotonin, 5-HT1A / Q000378:metabolism*; D012160:Retina / Q000254:growth & development / Q000378:metabolism*; D012165:Retinal Ganglion Cells / Q000378:metabolism; D014365:Tryptophan Hydroxylase / Q000378:metabolism*
D012333:RNA, Messenger; D044282:Receptor, Serotonin, 5-HT1A; D014365:Tryptophan Hydroxylase
Agnathans; Amacrine cells; Neuroblasts; Retinal development; Sea lamprey; Serotonin 1A receptor; Tryptophan hydroxylase