Comparative analysis of monoaminergic cerebrospinal fluid‐contacting cells in Osteichthyes (bony vertebrates)

Abstract

Cerebrospinal fluid-contacting (CSF-c) cells containing monoamines such as dopamine (DA) and serotonin (5-HT) occur in the periventricular zones of the hypothalamic region of most vertebrates except for placental mammals. Here we compare the organization of the CSF-c cells in chicken, Xenopus, and zebrafish, by analyzing the expression of synthetic enzymes of DA and 5-HT, respectively, tyrosine hydroxylase (TH) and tryptophan hydroxylase (TPH), and draw an evolutionary scenario for this cell population. Due to the lack of TH immunoreactivity in this region, the hypothalamic CSF-c cells have been thought to take up DA from the ventricle instead of synthesizing it. We demonstrate that a second TH gene (TH2) is expressed in the CSF-c cells of all the three species, suggesting that these cells do indeed synthetize DA. Furthermore, we found that many CSF-c cells coexpress TH2 and TPH1 and contain both DA and 5-HT, a dual neurotransmitter phenotype hitherto undescribed in the brain of any vertebrate. The similarities of CSF-c cells in chicken, Xenopus, and zebrafish suggest that these characteristics are inherited from the common ancestor of the Osteichthyes. A significant difference between tetrapods and teleosts is that teleosts possess an additional CSF-c cell population around the posterior recess (PR) that has emerged in specific groups of Actinopterygii. Our comparative analysis reveals that the hypothalamus in mammals and teleosts has evolved in a divergent manner: placental mammals have lost the monoaminergic CSF-c cells, while teleosts have increased their relative number. K E Y W O R D S

Organization of the catecholaminergic systems in two basal actinopterygian fishes, Polypterus senegalus and Erpetoichthys calabaricus (Actinopterygii: Cladistia)

“…This CA population in the preoptic area is dopaminergic, although some cells appeared labeled with DA and not with TH antibodies. The latter observation suggests that these cells synthesize dopamine through TH2, whereas the double‐labeled preoptic cells express TH1, enzyme that is detected with the used antibodies, in line with data reported in other vertebrates (Filippi et al, ; Xavier et al, ; Yamamoto et al, ). In mammals, the preoptic dopaminergic cells are included in the A15 group and represent a highly conserved group across vertebrates (Table ).…”

“…Similar to cladistians, the lack of TH‐ir in the PVO was also reported in teleosts, lungfishes, amphibians, and birds, where its cells are not labeled with the generally used antibodies that detect TH1 (López & González, ; Smeets & González, ; Xavier et al, ; Yamamoto et al, ). Initially it was thought that these cells might accumulate extracellular DA by a mechanism of uptake from the ventricular CSF (Smeets & González, ; Smeets & Steinbusch, ), but new data soundly support that the PVO cells are actual DA‐synthesizing cells that use TH2 as the first enzyme instead of TH1 (Xavier et al, ; Yamamoto et al, ). This fact is shared by all vertebrates with the only exception of placental mammals, which have lost the TH2 gene and lack CSF‐contacting cells in the hypothalamus (Yamamoto & Vernier, ).…”

Organization of the catecholaminergic systems in the brain of lungfishes, the closest living relatives of terrestrial vertebrates

“…Suprachiasmatic cells labeled with the DA antibody but not with the TH antibody in Protopterus suggest that these cells synthesize catecholamines through TH2, the enzyme that is not detected with the used antibodies (Yamamoto et al, ). It should be noted that when this situation has been observed in other vertebrate groups, the DA positive cells were CSF‐contacting cells (Xavier et al, ; Yamamoto, Bloch, & Vernier, ), different from the observation in lungfishes. In addition, we observed TH positive but DA negative cells in the suprachiasmatic nucleus.…”

“…Basically, the DA‐ir cell group found in the NPv is mainly constituted by CSF‐contacting cells and matches that of 5‐HT‐ir cells (López & González, ). Like in teleosts, amphibians and birds, these cells are not labeled with the generally used antibodies that detect TH1 (Smeets & González, ; Yamamoto et al, ; Xavier et al, ). A possibility was raised that these cells accumulate extracellular DA by a mechanism of uptake from the ventricular CSF rather than synthesizing it (Smeets & González, ; Smeets & Steinbusch, ), but recent data strongly support that the NPv cells are actual DA‐synthesizing cells that use TH2 as first enzyme instead of TH1 (Yamamoto et al, ; Xavier et al, ).…”

“…It was further confirmed by preadsorbation of the antiserum with DA coupled to sepharose beads via glutaraldehyde‐lysine bridge, which blocked all positive staining from brain sections. This antibody has been previously used in different species of amniote and anamniote vertebrates to reveal a detailed picture of the DA system in the brain (Yamamoto et al, ; Xavier et al, ).…”