XB-ART-53508
J Comp Neurol
June 15, 2017;
525
(9):
2265-2283.
Comparative analysis of monoaminergic cerebrospinal fluid-contacting cells in Osteichthyes (bony vertebrates).
Xavier AL
,
Fontaine R
,
Bloch S
,
Affaticati P
,
Jenett A
,
Demarque M
,
Vernier P
,
Yamamoto K
.
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.
PubMed ID: 28295297
PMC ID: PMC6585609
Article link: J Comp Neurol
Species referenced: Xenopus laevis
Genes referenced: elavl3 slc18a2 th th2 tph1 tph2
Antibodies: Elavl3 Ab1 Th Ab5
Article Images: [+] show captions
References [+] :
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Sánchez-Camacho, Descending supraspinal pathways in amphibians. II. Distribution and origin of the catecholaminergic innervation of the spinal cord. 2001, Pubmed , Xenbase
Tay, Comprehensive catecholaminergic projectome analysis reveals single-neuron integration of zebrafish ascending and descending dopaminergic systems. 2019, Pubmed
Treweek, Whole-body tissue stabilization and selective extractions via tissue-hydrogel hybrids for high-resolution intact circuit mapping and phenotyping. 2016, Pubmed
Ueda, Immunohistochemical demonstration of the serotonin neuron system in the central nervous system of the bullfrog, Rana catesbeiana. 1984, Pubmed
Vigh, Nonvisual photoreceptors of the deep brain, pineal organs and retina. 2002, Pubmed
Vígh, The system of cerebrospinal fluid-contacting neurons. Its supposed role in the nonsynaptic signal transmission of the brain. 2004, Pubmed
Wakamatsu, Sequential expression and role of Hu RNA-binding proteins during neurogenesis. 1997, Pubmed
Walther, Synthesis of serotonin by a second tryptophan hydroxylase isoform. 2003, Pubmed
Walther, A unique central tryptophan hydroxylase isoform. 2003, Pubmed
Wen, Visualization of monoaminergic neurons and neurotoxicity of MPTP in live transgenic zebrafish. 2008, Pubmed
Xavier, Comparative analysis of monoaminergic cerebrospinal fluid-contacting cells in Osteichthyes (bony vertebrates). 2017, Pubmed , Xenbase
Yamamoto, Two tyrosine hydroxylase genes in vertebrates New dopaminergic territories revealed in the zebrafish brain. 2010, Pubmed
Yamamoto, Differential expression of dopaminergic cell markers in the adult zebrafish forebrain. 2011, Pubmed
Yamamoto, The evolution of dopamine systems in chordates. 2011, Pubmed
Yoshida, Monoaminergic neurons in the brain of goldfish as observed by immunohistochemical techniques. 1983, Pubmed
Zhang, Establishment of a neuroepithelial barrier by Claudin5a is essential for zebrafish brain ventricular lumen expansion. 2010, Pubmed
Alunni, Notch3 signaling gates cell cycle entry and limits neural stem cell amplification in the adult pallium. 2013, Pubmed
Bellipanni, Cloning of two tryptophan hydroxylase genes expressed in the diencephalon of the developing zebrafish brain. 2016, Pubmed
Biran, Role of developmental factors in hypothalamic function. 2015, Pubmed
Björklund, Evidence for a major spinal cord projection from the diencephalic A11 dopamine cell group in the rat using transmitter-specific fluorescent retrograde tracing. 1980, Pubmed
Bosco, Development of hypothalamic serotoninergic neurons requires Fgf signalling via the ETS-domain transcription factor Etv5b. 2013, Pubmed
Chen, Complementary developmental expression of the two tyrosine hydroxylase transcripts in zebrafish. 2010, Pubmed
Chung, Structural and molecular interrogation of intact biological systems. 2013, Pubmed
Corio, Distribution of catecholaminergic and serotoninergic systems in forebrain and midbrain of the newt, Triturus alpestris (Urodela). 1992, Pubmed
Ekström, Distribution of dopamine-immunoreactive neuronal perikarya and fibres in the brain of a teleost, Gasterosteus aculeatus L. comparison with tyrosine hydroxylase- and dopamine-beta-hydroxylase-immunoreactive neurons. 1990, Pubmed
Filippi, vglut2 and gad expression reveal distinct patterns of dual GABAergic versus glutamatergic cotransmitter phenotypes of dopaminergic and noradrenergic neurons in the zebrafish brain. 2015, Pubmed
Filippi, Expression of the paralogous tyrosine hydroxylase encoding genes th1 and th2 reveals the full complement of dopaminergic and noradrenergic neurons in zebrafish larval and juvenile brain. 2010, Pubmed
Fontaine, Dopamine inhibits reproduction in female zebrafish (Danio rerio) via three pituitary D2 receptor subtypes. 2013, Pubmed
Fontaine, Dopaminergic Neurons Controlling Anterior Pituitary Functions: Anatomy and Ontogenesis in Zebrafish. 2015, Pubmed
Gaspar, Probing the diversity of serotonin neurons. 2012, Pubmed
Hirunagi, Immunocytochemical demonstration of serotonin-immunoreactive cerebrospinal fluid-contacting neurons in the paraventricular organ of pigeons and domestic chickens. 1992, Pubmed
Hornby, Localization of immunoreactive tyrosine hydroxylase in the goldfish brain. 1987, Pubmed
Kang, Dopamine-melatonin neurons in the avian hypothalamus controlling seasonal reproduction. 2008, Pubmed
Kang, Melanopsin expression in dopamine-melatonin neurons of the premammillary nucleus of the hypothalamus and seasonal reproduction in birds. 2011, Pubmed
Kaslin, Comparative anatomy of the histaminergic and other aminergic systems in zebrafish (Danio rerio). 2002, Pubmed
Kawakami, A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. 2004, Pubmed
Kotrschal, Distribution of aminergic neurons in the brain of the sterlet, Acipenser ruthenus (Chondrostei, Actinopterygii). 1985, Pubmed
López, Organization of the serotonergic system in the central nervous system of two basal actinopterygian fishes: the Cladistians Polypterus senegalus and Erpetoichthys calabaricus. 2014, Pubmed
Mayrhofer, A novel brain tumour model in zebrafish reveals the role of YAP activation in MAPK- and PI3K-induced malignant growth. 2017, Pubmed
McPherson, Motor Behavior Mediated by Continuously Generated Dopaminergic Neurons in the Zebrafish Hypothalamus Recovers after Cell Ablation. 2016, Pubmed
Medina, Development of catecholamine systems in the brain of the lizard Gallotia galloti. 1995, Pubmed
Meek, Distribution of dopamine immunoreactivity in the brain of the mormyrid teleost Gnathonemus petersii. 1989, Pubmed
Meek, Distribution of serotonin in the brain of the mormyrid teleost Gnathonemus petersii. 1989, Pubmed
Meek, Distribution of noradrenaline-immunoreactivity in the brain of the mormyrid teleost Gnathonemus petersii. 1993, Pubmed
Meneghelli, Distribution of tryptophan hydroxylase-immunoreactive neurons in the brainstem and diencephalon of the pigeon (Columba livia). 2009, Pubmed
Nakane, A mammalian neural tissue opsin (Opsin 5) is a deep brain photoreceptor in birds. 2010, Pubmed , Xenbase
Neary, Nuclear organization of the bullfrog diencephalon. 1983, Pubmed
Okano, A hierarchy of Hu RNA binding proteins in developing and adult neurons. 1997, Pubmed
Parent, The monoamine-containing neurons in the brain of the garfish, Lepisosteus osseus. 1983, Pubmed
Parent, The organization of monoamine-containing neurons in the brain of the sunfish (Lepomis gibbosus) as revealed by fluorescence microscopy. 1979, Pubmed
Puelles, Forebrain gene expression domains and the evolving prosomeric model. 2003, Pubmed
Puelles, Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. 1994, Pubmed
Ren, Zebrafish tyrosine hydroxylase 2 gene encodes tryptophan hydroxylase. 2013, Pubmed
Rink, The teleostean (zebrafish) dopaminergic system ascending to the subpallium (striatum) is located in the basal diencephalon (posterior tuberculum). 2001, Pubmed
Semenova, The tyrosine hydroxylase 2 (TH2) system in zebrafish brain and stress activation of hypothalamic cells. 2015, Pubmed
Skagerberg, Origin and termination of the diencephalo-spinal dopamine system in the rat. 1983, Pubmed
Smeets, Are putative dopamine-accumulating cell bodies in the hypothalamic periventricular organ a primitive brain character of non-mammalian vertebrates? 1990, Pubmed
Sánchez-Camacho, Descending supraspinal pathways in amphibians. II. Distribution and origin of the catecholaminergic innervation of the spinal cord. 2001, Pubmed , Xenbase
Tay, Comprehensive catecholaminergic projectome analysis reveals single-neuron integration of zebrafish ascending and descending dopaminergic systems. 2019, Pubmed
Treweek, Whole-body tissue stabilization and selective extractions via tissue-hydrogel hybrids for high-resolution intact circuit mapping and phenotyping. 2016, Pubmed
Ueda, Immunohistochemical demonstration of the serotonin neuron system in the central nervous system of the bullfrog, Rana catesbeiana. 1984, Pubmed
Vigh, Nonvisual photoreceptors of the deep brain, pineal organs and retina. 2002, Pubmed
Vígh, The system of cerebrospinal fluid-contacting neurons. Its supposed role in the nonsynaptic signal transmission of the brain. 2004, Pubmed
Wakamatsu, Sequential expression and role of Hu RNA-binding proteins during neurogenesis. 1997, Pubmed
Walther, Synthesis of serotonin by a second tryptophan hydroxylase isoform. 2003, Pubmed
Walther, A unique central tryptophan hydroxylase isoform. 2003, Pubmed
Wen, Visualization of monoaminergic neurons and neurotoxicity of MPTP in live transgenic zebrafish. 2008, Pubmed
Xavier, Comparative analysis of monoaminergic cerebrospinal fluid-contacting cells in Osteichthyes (bony vertebrates). 2017, Pubmed , Xenbase
Yamamoto, Two tyrosine hydroxylase genes in vertebrates New dopaminergic territories revealed in the zebrafish brain. 2010, Pubmed
Yamamoto, Differential expression of dopaminergic cell markers in the adult zebrafish forebrain. 2011, Pubmed
Yamamoto, The evolution of dopamine systems in chordates. 2011, Pubmed
Yoshida, Monoaminergic neurons in the brain of goldfish as observed by immunohistochemical techniques. 1983, Pubmed
Zhang, Establishment of a neuroepithelial barrier by Claudin5a is essential for zebrafish brain ventricular lumen expansion. 2010, Pubmed