Brain asymmetry is encoded at the level of axon terminal morphology

Bianco, Isaac H.; Carl, Michael; Russell, Claire; Clarke, Jon; Wilson, Stephen W.

doi:10.1186/1749-8104-3-9

Cited by 84 publications

(158 citation statements)

References 35 publications

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“…3P). This asymmetrical expression of tac3a in the habenula is consistent with previous findings that the habenula in zebrafish displayed left-right asymmetries in gene expression (18,19). Interestingly, it was shown that neurons appear sooner in the left than in the right habenula (20).…”

Section: Localization Of Embryonic Tac3asupporting

confidence: 80%

Neurokinin Bs and neurokinin B receptors in zebrafish-potential role in controlling fish reproduction

Biran

Palevitch

Ben‐Dor

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

116

172

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The endocrine regulation of vertebrate reproduction is achieved by the coordinated actions of several peptide neurohormones, tachykinin among them. To study the evolutionary conservation and physiological functions of neurokinin B (NKB), we identified tachykinin (tac) and tac receptor (NKBR) genes from many fish species, and cloned two cDNA forms from zebrafish. Phylogenetic analysis showed that piscine Tac3s and mammalian neurokinin genes arise from one lineage. High identity was found among different fish species in the region encoding the NKB; all shared the common Cterminal sequence. Although the piscine Tac3 gene encodes for two putative tachykinin peptides, the mammalian ortholog encodes for only one. The second fish putative peptide, referred to as neurokinin F (NKF), is unique and found to be conserved among the fish species when tested in silico. tac3a was expressed asymmetrically in the habenula of embryos, whereas in adults zebrafish tac3a-expressing neurons were localized in specific brain nuclei that are known to be involved in reproduction. Zebrafish tac3a mRNA levels gradually increased during the first few weeks of life and peaked at pubescence. Estrogen treatment of prepubertal fish elicited increases in tac3a, kiss1, kiss2, and kiss1ra expression. The synthetic zebrafish peptides (NKBa, NKBb, and NKF) activated Tac3 receptors via both PKC/Ca 2+ and PKA/cAMP signal-transduction pathways in vitro. Moreover, a single intraperitoneal injection of NKBa and NKF significantly increased leuteinizing hormone levels in mature female zebrafish. These results suggest that the NKB/NKBR system may participate in neuroendocrine control of fish reproduction.gonadotropin-releasing hormone | kisspeptin | teleost | gonadotropin R eproduction is a highly integrated and complex function that requires synchronized production of gametes by both sexes at an optimum time for offspring survival. Fish show an enormous variety of reproductive strategies (1), and were recently chosen as models for the study of growth, metabolism, and human diseases. The hypothalamic regulation of gonadotropin secretion in fish is different from that of mammals, from both endocrinal and anatomical aspects. In teleosts, the pituitary is innervated directly by neurons projecting to the vicinity of the pituitary gonadotrophs (2). Among the neuropeptides released by these nerve endings are gonadotrophin-releasing hormones (GnRHs) and dopamine, which act as stimulatory and inhibitory factors on the release of luteinizing hormone (LH) and follicle-stimulating hormone (3). However, new actors have recently entered the field of reproductive physiology: kisspeptins, neurokinin, and dynorphin have all been implicated in controlling GnRH (4).Topaloglu et al. (5) found that humans bearing loss-of-function mutations of the genes encoding either neurokinin B (NKB) or its cognate receptor, neurokinin receptor 3 (NKBR, Tac3r) displayed hypogonadotropic hypogonadism; this seminal report implicated NKB signaling as an essential factor in the onset of puberty...

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Section: Localization Of Embryonic Tac3asupporting

confidence: 80%

Neurokinin Bs and neurokinin B receptors in zebrafish-potential role in controlling fish reproduction

Biran

Palevitch

Ben‐Dor

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

116

172

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“…In zebrafish larvae, efferent connectivity from left and right habenular nuclei forms distinct and segregated ring-shaped domains within dorsal and ventral regions of the IPN, respectively (figure 1a(vi),(vii); Aizawa et al 2005;Gamse et al 2005;Bianco et al 2008). A similar pattern of habenular efferent connectivity is observed in the larval IPN of medaka (see figure 1b (vi),(vii); Carl et al 2007).…”

Section: Results (A)supporting

confidence: 50%

“…The red arrowhead points to a neuropil domain that is detected exclusively in the left habenula of medaka. efferents are segregated along the dorsoventral axis of the interpeduncular nucleus (IPN) in the ventral midbrain (Aizawa et al 2005;Gamse et al 2005;Bianco et al 2008). Three main aspects are important to highlight about the development of epithalamic asymmetries.…”

Section: Introductionmentioning

confidence: 99%

Zebrafish and medaka: model organisms for a comparative developmental approach of brain asymmetry

Signore

Guerrero

Loosli

et al. 2008

Phil. Trans. R. Soc. B

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Comparison between related species is a successful approach to uncover conserved and divergent principles of development. Here, we studied the pattern of epithalamic asymmetry in zebrafish (Danio rerio) and medaka (Oryzias latipes), two related teleost species with 115-200 Myr of independent evolution. We found that these species share a strikingly conserved overall pattern of asymmetry in the parapineal-habenular-interpeduncular system. Nodal signalling exhibits comparable spatial and temporal asymmetric expressions in the presumptive epithalamus preceding the development of morphological asymmetries. Neuroanatomical asymmetries consist of left-sided asymmetric positioning and connectivity of the parapineal organ, enlargement of neuropil in the left habenula compared with the right habenula and segregation of left-right habenular efferents along the dorsoventral axis of the interpeduncular nucleus. Despite the overall conservation of asymmetry, we observed heterotopic changes in the topology of parapineal efferent connectivity, heterochronic shifts in the timing of developmental events underlying the establishment of asymmetry and divergent degrees of canalization of embryo laterality. We offer new tools for developmental time comparison among species and propose, for each of these transformations, novel hypotheses of ontogenic mechanisms that explain interspecies variations that can be tested experimentally. Together, these findings highlight the usefulness of zebrafish and medaka as comparative models to study the developmental mechanisms of epithalamic asymmetry in vertebrates.

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“…These asymmetries are PpO-independent in the three species, although by different ontogenic mechanisms: (i) catsharks do not form a recognizable PpO [22], (ii) lampreys do have a midline PpO, but habenular asymmetries develop before the PpO is formed [22] and (iii) zebrafish have an asymmetrically positioned PpO but a sub-type of habenular asymmetries develops even in the absence of PpO, i.e. when the PpO is physically ablated [40,41,52]. In zebrafish, PpO-independent asymmetries of the Hb are very subtle and are frequently masked by the second type of epithalamic asymmetry, which is more conspicuous and dependent on the PpO (figure 4).…”

Section: Nodal As Laterality Modulator In Midlineunpaired Structuresmentioning

confidence: 99%

“…This first morphological asymmetry of the zebrafish epithalamus is followed by the development of prominent structural and functional asymmetries of the Hb ( figure 4a(v-viii)) [40,42]. Experiments of PpO ablation and mutant conditions that delay the onset of PpO asymmetric translocation reveal a requirement of an asymmetrically positioned PpO for the subsequent development of a sub-type of asymmetries in the Hb ( figure 4a(iii)) [40][41][42]58]. These asymmetries result from L-R differences in cell fate decisions towards two main neuronal identities, and it is possible that the PpO modulates these fate decisions as well as the timing of asymmetric habenular neurogenesis by acting on the Notch and Wnt signalling pathways [43,44].…”

Section: Nodal As Laterality Modulator In Midlineunpaired Structuresmentioning

confidence: 99%

Nodal signalling and asymmetry of the nervous system

Signore

Palma

Concha

2016

Phil. Trans. R. Soc. B

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One contribution of 17 to a theme issue 'Provocative questions in left -right asymmetry'. The role of Nodal signalling in nervous system asymmetry is still poorly understood. Here, we review and discuss how asymmetric Nodal signalling controls the ontogeny of nervous system asymmetry using a comparative developmental perspective. A detailed analysis of asymmetry in ascidians and fishes reveals a critical context-dependency of Nodal function and emphasizes that bilaterally paired and midline-unpaired structures/organs behave as different entities. We propose a conceptual framework to dissect the developmental function of Nodal as asymmetry inducer and laterality modulator in the nervous system, which can be used to study other types of body and visceral organ asymmetries. Using insights from developmental biology, we also present novel evolutionary hypotheses on how Nodal led the evolution of directional asymmetry in the brain, with a particular focus on the epithalamus. We intend this paper to provide a synthesis on how Nodal signalling controls left-right asymmetry of the nervous system. This article is part of the themed issue 'Provocative questions in leftright asymmetry'.

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Brain asymmetry is encoded at the level of axon terminal morphology

Abstract: Background: Functional lateralization is a conserved feature of the central nervous system (CNS). However, underlying left-right asymmetries within neural circuitry and the mechanisms by which they develop are poorly described.

Cited by 84 publications

References 35 publications

Neurokinin Bs and neurokinin B receptors in zebrafish-potential role in controlling fish reproduction

Neurokinin Bs and neurokinin B receptors in zebrafish-potential role in controlling fish reproduction

Zebrafish and medaka: model organisms for a comparative developmental approach of brain asymmetry

Nodal signalling and asymmetry of the nervous system

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