Surprising gene expression patterns within and between PDF-containing circadian neurons in Drosophila

Jul 14, 2010Proceedings of the National Academy of Sciences of the United States of America

Unexpected gene activity patterns inside and between time-keeping neurons in fruit flies

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Abstract

The l-LNvs contain at least a 10-fold higher fraction of oscillating mRNAs compared to previous analyses of head RNA.

Circadian neurons show distinct gene expression patterns, with specific mRNAs unique to either s-LNvs or l-LNvs.
The s-LNvs serve as principal circadian pacemakers, while l-LNvs are implicated in sleep and light-mediated arousal.
Half of the mRNA population in l-LNvs overlaps with that of s-LNvs, but the other half is specific to each type.
An octopamine receptor mRNA is selectively enriched in l-LNvs, which respond to octopamine application.
RNA cycling in l-LNvs is significantly more pronounced than in other neurons within the head.

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To compare circadian gene expression within highly discrete neuronal populations, we separately purified and characterized two adjacent but distinct groups of Drosophila adult circadian neurons: the 8 small and 10 large PDF-expressing ventral lateral neurons (s-LNvs and l-LNvs, respectively). The s-LNvs are the principal circadian pacemaker cells, whereas recent evidence indicates that the l-LNvs are involved in sleep and light-mediated arousal. Although half of the l-LNv-enriched mRNA population, including core clock mRNAs, is shared between the l-LNvs and s-LNvs, the other half is l-LNv- and s-LNv-specific. The distribution of four specific mRNAs is consistent with prior characterization of the four encoded proteins, and therefore indicates successful purification of the two neuronal types. Moreover, an octopamine receptor mRNA is selectively enriched in l-LNvs, and only these neurons respond to in vitro application of octopamine. Dissection and purification of l-LNvs from flies collected at different times indicate that these neurons contain cycling clock mRNAs with higher circadian amplitudes as well as at least a 10-fold higher fraction of oscillating mRNAs than all previous analyses of head RNA. Many of these cycling l-LNv mRNAs are well expressed but do not cycle or cycle much less well elsewhere in heads. The results suggest that RNA cycling is much more prominent in circadian neurons than elsewhere in heads and may be particularly important for the functioning of these neurons.

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Surprising gene expression patterns within and between PDF-containing circadian neurons in Drosophila

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