Segment-specific generation of Drosophila Capability neuropeptide neurons by multi-faceted Hox cues

Anke Suska,Irene Miguel-Aliaga,Stefan Thor

doi:10.1016/j.ydbio.2011.02.015

Anke Suska, Irene Miguel-Aliaga + Show 1 more

Open Access

https://doi.org/10.1016/j.ydbio.2011.02.015

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Abstract

In the Drosophila ventral nerve cord, the three pairs of Capability neuropeptide-expressing Va neurons are exclusively found in the second, third and fourth abdominal segments (A2–A4). To address the underlying mechanisms behind such segment-specific cell specification, we followed the developmental specification of these neurons. We find that Va neurons are initially generated in all ventral nerve cord segments and progress along a common differentiation path. However, their terminal differentiation only manifests itself in A2–A4, due to two distinct mechanisms: segment-specific programmed cell death (PCD) in posterior segments, and differentiation to an alternative identity in segments anterior to A2. Genetic analyses reveal that the Hox homeotic genes are involved in the segment-specific appearance of Va neurons. In posterior segments, the Hox gene Abdominal-B exerts a pro-apoptotic role on Va neurons, which involves the function of several RHG genes. Strikingly, this role of Abd-B is completely opposite to its role in the segment-specific apoptosis of other classes of neuropeptide neurons, the dMP2 and MP1 neurons, where Abd-B acts in an anti-apoptotic manner. In segments A2–A4 we find that abdominal A is important for the terminal differentiation of Va cell fate. In the A1 segment, Ultrabithorax acts to specify an alternate Va neuron fate. In contrast, in thoracic segments, Antennapedia suppresses the Va cell fate. Thus, Hox genes act in a multi-faceted manner to control the segment-specific appearance of the Va neuropeptide neurons in the ventral nerve cord.

Highlights

A common feature of most nervous systems is the appearance of unique neuronal subtypes only within certain segments
Their terminal differentiation only manifests itself in A2-A4, due to two distinct mechanisms: segment-specific programmed cell death (PCD) in posterior segments, and differentiation to an alternative identity in segments anterior to A2
The Hox gene Abdominal-B exerts a pro-apoptotic role on Va neurons, which involves the function of several RHG genes

Summary

Introduction

A common feature of most nervous systems is the appearance of unique neuronal subtypes only within certain segments. Studies have shown that this may result from several developmental mechanisms, the first of which is the segment-specific generation of unique sets of progenitor cells – for example, certain segments of the Drosophila developing CNS (tritocerebrum (B3) and suboesophageal 1 (S1)) appear to contain fewer progenitor cells (neuroblasts)(Urbach and Technau, 2004). Segment-specific lineage size control has been described, such that equivalent neuroblasts may generate different sized lineages in different segments (Schmid et al, 1999; Schmidt et al, 1997). This may be due either to differences in lineage progression (by apoptosis or cell cycle exit) or to early changes in asymmetric cell division by segment-specific control of genes affecting progenitor behavior (Berger et al, 2005a). The Hox homeotic genes have been found to be involved in several of these events, but our understanding of Hox gene involvement in these processes is still rudimentary

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