Comparative analysis of monoaminergic cerebrospinal fluid-contacting cells in Osteichthyes (bony vertebrates)
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Comparative analysis of monoaminergic cerebrospinal fluid-contacting cells in Osteichthyes (bony vertebrates). / Xavier, Anna L.; Fontaine, Romain; Bloch, Solal; Affaticati, Pierre; Jenett, Arnim; Demarque, Michaël; Vernier, Philippe; Yamamoto, Kei.
In: Journal of Comparative Neurology, Vol. 525, No. 9, 06.2017, p. 2265-2283.Research output: Contribution to journal › Journal article › Research › peer-review
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TY - JOUR
T1 - Comparative analysis of monoaminergic cerebrospinal fluid-contacting cells in Osteichthyes (bony vertebrates)
AU - Xavier, Anna L.
AU - Fontaine, Romain
AU - Bloch, Solal
AU - Affaticati, Pierre
AU - Jenett, Arnim
AU - Demarque, Michaël
AU - Vernier, Philippe
AU - Yamamoto, Kei
PY - 2017/6
Y1 - 2017/6
N2 - 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.
AB - 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.
KW - CSF-contacting cells
KW - dopamine
KW - evolution
KW - hypothalamus
KW - monoamine
KW - paraventricular organ
KW - RRID: AB_10000240
KW - RRID: AB_2201528
KW - RRID: AB_221448
KW - RRID: AB_2314334
KW - RRID: AB_2314655
KW - RRID: AB_477522
KW - RRID: AB_87181
KW - RRID: AB_94865
KW - serotonin
KW - ventricle
U2 - 10.1002/cne.24204
DO - 10.1002/cne.24204
M3 - Journal article
C2 - 28295297
AN - SCOPUS:85016783167
VL - 525
SP - 2265
EP - 2283
JO - The Journal of Comparative Neurology
JF - The Journal of Comparative Neurology
SN - 0021-9967
IS - 9
ER -
ID: 196882269