Sonic hedgehog expression in zebrafish forebrain identifies the teleostean pallidal signaling center and shows preglomerular complex and posterior tubercular dopamine cells to arise from shh cells.

Mario F Wullimann,Kosisochukwu E Umeasalugo

doi:10.1002/cne.24825

Mario F Wullimann, Kosisochukwu E Umeasalugo

Open Access

https://doi.org/10.1002/cne.24825

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Abstract

Ventralization, a major patterning process in the developing vertebrate neural tube (central nervous system, CNS), depends on Sonic hedgehog (SHH) as a main signaling morphogen. We studied the CNS of late larval and young adult zebrafish in a transgenic shh-GFP line revealing increased neuroanatomical detail due to the progressed differentiation state compared to earlier stages. Some major findings emerge from the present study. (a) shh -GFP is still expressed along the adult zebrafish CNS neuraxis in most locations seen in larvae. (b) We newly identify a ventroposterior shh pallidal domain representing the basal telencephalic signaling center important for basal ganglia development known in other vertebrates (i.e., the anterior entopeduncular area-basal medial ganglionic eminence of mammals). (c) We further show late-emerging shh-GFP positive radial glia cells in the medial zone of the dorsal telencephalon (i.e., the teleostan pallial amygdala). (d) Immunostains for tyrosine hydroxylase demonstrate that there is selective colocalization in adult dopamine cells with shh-GFP in the posterior tuberculum, including in projection cells to striatum, which represents a striking parallel to amniote mesodiencephalic dopamine cell origin from shh expressing floor plate cells. (e) There is no colocalization of shh and islet1 as shown by respective shh-GFP and islet1-GFP lines. (f) The only radially far migrated shh-GFP cells are located in the preglomerular area. (g) There are no adult cerebellar and tectal shh-GFP cells confirming their exclusive role during early development as previously reported by our laboratory.

Highlights

Since teleosts lack midbrain dopamine cells and only possess basal diencephalic dopamine cells—which contribute to the SN/VT in mammals—that project to the fish basal ganglia, we wanted to verify whether these zebrafish diencephalic ascending dopamine cells are produced by shh expressing cells
The shh-Green fluorescent protein (GFP) is generally still expressed in early adult zebrafish brains in most locations along the neuraxis as seen in larval zebrafish brains of 4/5 days postfertilization. These shh domains include classical floor plate cells defining the ventral midline of the neuraxis from spinal cord into the posterior diencephalon
We will focus on data directly relevant to forebrain ventralization, in particular, the telencephalon, for which we report new results in the zebrafish