RRC ID 19685
Author Razy-Krajka F, Brown ER, Horie T, Callebert J, Sasakura Y, Joly JS, Kusakabe TG, Vernier P.
Title Monoaminergic modulation of photoreception in ascidian: evidence for a proto-hypothalamo-retinal territory.
Journal BMC Biol.
Abstract BACKGROUND:The retina of craniates/vertebrates has been proposed to derive from a photoreceptor prosencephalic territory in ancestral chordates, but the evolutionary origin of the different cell types making the retina is disputed. Except for photoreceptors, the existence of homologs of retinal cells remains uncertain outside vertebrates.
METHODS:The expression of genes expressed in the sensory vesicle of the ascidian Ciona intestinalis including those encoding components of the monoaminergic neurotransmission systems, was analyzed by in situ hybridization or in vivo transfection of the corresponding regulatory elements driving fluorescent reporters. Modulation of photic responses by monoamines was studied by electrophysiology combined with pharmacological treatments.
RESULTS:We show that many molecular characteristics of dopamine-synthesizing cells located in the vicinity of photoreceptors in the sensory vesicle of the ascidian Ciona intestinalis are similar to those of amacrine dopamine cells of the vertebrate retina. The ascidian dopamine cells share with vertebrate amacrine cells the expression of the key-transcription factor Ptf1a, as well as that of dopamine-synthesizing enzymes. Surprisingly, the ascidian dopamine cells accumulate serotonin via a functional serotonin transporter, as some amacrine cells also do. Moreover, dopamine cells located in the vicinity of the photoreceptors modulate the light-off induced swimming behavior of ascidian larvae by acting on alpha2-like receptors, instead of dopamine receptors, supporting a role in the modulation of the photic response. These cells are located in a territory of the ascidian sensory vesicle expressing genes found both in the retina and the hypothalamus of vertebrates (six3/6, Rx, meis, pax6, visual cycle proteins).
CONCLUSION:We propose that the dopamine cells of the ascidian larva derive from an ancestral multifunctional cell population located in the periventricular, photoreceptive field of the anterior neural tube of chordates, which also gives rise to both anterior hypothalamus and the retina in craniates/vertebrates. It also shows that the existence of multiple cell types associated with photic responses predates the formation of the vertebrate retina.
Volume 10
Pages 45
Published 2012-5-29
DOI 10.1186/1741-7007-10-45
PII 1741-7007-10-45
PMID 22642675
PMC PMC3414799
MeSH Adrenergic alpha-2 Receptor Agonists / pharmacology Adrenergic alpha-2 Receptor Antagonists / pharmacology Amacrine Cells / cytology Amacrine Cells / drug effects Amacrine Cells / metabolism Amacrine Cells / radiation effects Animals Biological Evolution Biomarkers / metabolism Ciona intestinalis / cytology Ciona intestinalis / embryology Ciona intestinalis / metabolism* Ciona intestinalis / radiation effects Dopamine / metabolism* Embryo, Nonmammalian / cytology Embryo, Nonmammalian / drug effects Embryo, Nonmammalian / metabolism Embryo, Nonmammalian / radiation effects Hypothalamus / cytology Hypothalamus / drug effects Hypothalamus / metabolism* Hypothalamus / radiation effects Larva / cytology Larva / drug effects Larva / radiation effects Light Models, Biological Motor Activity / drug effects Motor Activity / radiation effects Neurons / cytology Neurons / drug effects Neurons / metabolism Neurons / radiation effects Photoreceptor Cells, Invertebrate / cytology Photoreceptor Cells, Invertebrate / drug effects Photoreceptor Cells, Invertebrate / metabolism* Photoreceptor Cells, Invertebrate / radiation effects Promoter Regions, Genetic / genetics Receptors, Adrenergic, alpha-2 / metabolism Serotonin / metabolism Swimming Synaptic Transmission / drug effects Synaptic Transmission / radiation effects Vertebrates / metabolism
IF 6.723
Times Cited 4
C.intestinalis / (O.japonicus) Wild C. int