Temporal patterning of Drosophila medulla neuroblasts controls neural fates

Li, Xin; Erclik, Ted; Bertet, Claire; Chen, Zhenqing; Voutev, Roumen; Venkatesh, Srinidhi; Morante, Javier; Çelik, Arzu; Desplan, Claude

doi:10.1038/nature12319

Cited by 266 publications

(422 citation statements)

References 48 publications

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“…1C,D). hth expression is detected in medulla neuroblasts and neurons, in the NE progenitors (Reddy et al, 2010;Hasegawa et al, 2011;Morante et al, 2011;Li et al, 2013;Suzuki et al, 2013) and also within the posterior slope of the LF (Fig. 1D,E,F).…”

Section: Resultsmentioning

confidence: 99%

A conserved transcriptional network regulates lamina development in the Drosophila visual system

2014

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The visual system of insects is a multilayered structure composed externally by the compound eye and internally by the three ganglia of the optic lobe: lamina, medulla and the lobula complex. The differentiation of lamina neurons depends heavily on Hedgehog (Hh) signaling, which is delivered by the incoming photoreceptor axons, and occurs in a wave-like fashion. Despite the primary role of lamina neurons in visual perception, it is still unclear how these neurons are specified from neuroepithelial (NE) progenitors. Here we show that a homothorax (hth)-eyes absent (eya)-sine oculis (so)-dachshund (dac) gene regulatory cassette is involved in this specification. Lamina neurons differentiate from NE progenitors that express hth, eya and so. One of the first events in the differentiation of lamina neurons is the upregulation of dac expression in response to Hh signaling. We show that this dac upregulation, which marks the transition from NE progenitors into lamina precursors, also requires Eya/So, the expression of which is locked in by mutual feedback. dac expression is crucial for lamina differentiation because it ensures repression of hth, a negative regulator of single-minded, and thus dac allows further lamina neuron differentiation. Therefore, the specification of lamina neurons is controlled by coupling the cell-autonomous hth-eya-so-dac regulatory cassette to Hh signaling.

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Section: Resultsmentioning

confidence: 99%

A conserved transcriptional network regulates lamina development in the Drosophila visual system

2014

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“…By contrast, Tll is abundant in the offspring of MB NBs (Kurusu et al, 2009) (Fig. 6C, arrows) and the developing optic lobe (Li et al, 2013), but could not be detected within the AL lineages (Fig. 6C,C′, green).…”

Section: Tfs Differentially Expressed In Distinct Nbsmentioning

confidence: 93%

Transcriptomes of lineage-specific Drosophila neuroblasts profiled via genetic targeting and robotic sorting

Yang

Sugino

et al. 2015

Development

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A brain consists of numerous distinct neurons arising from a limited number of progenitors, called neuroblasts in Drosophila. Each neuroblast produces a specific neuronal lineage. To unravel the transcriptional networks that underlie the development of distinct neuroblast lineages, we marked and isolated lineage-specific neuroblasts for RNA sequencing. We labeled particular neuroblasts throughout neurogenesis by activating a conditional neuroblast driver in specific lineages using various intersection strategies. The targeted neuroblasts were efficiently recovered using a custom-built device for robotic single-cell picking. Transcriptome analysis of mushroom body, antennal lobe and type II neuroblasts compared with non-selective neuroblasts, neurons and glia revealed a rich repertoire of transcription factors expressed among neuroblasts in diverse patterns. Besides transcription factors that are likely to be pan-neuroblast, many transcription factors exist that are selectively enriched or repressed in certain neuroblasts. The unique combinations of transcription factors present in different neuroblasts may govern the diverse lineage-specific neuron fates.

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“…S2, for examples); such experiments can validate or extend emergent information on the origins of neuronal diversity in the optic lobe (33).…”

Section: Mcfo Facilitates Visualization Of Complex Arrangements Of Nementioning

confidence: 99%

“…The use of multiple stop-cassette reporters can greatly aid the interpretation of such experiments by revealing the relative positions of independent clones labeled with different colors. This can be particularly useful in the optic lobes where the large number of neuroblasts, as well as extensive cell migration during development, can make clonal patterns difficult to interpret (32,33). To illustrate this approach, we studied the origins of C2 and C3, two related columnar medulla neurons that send centrifugal projections from the medulla to the lamina (3, 30) (Fig.…”

Section: Mcfo Facilitates Visualization Of Complex Arrangements Of Nementioning

confidence: 99%

Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system

Nern

Pfeiffer

Rubin

2015

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

522

691

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We describe the development and application of methods for high-throughput neuroanatomy in Drosophila using light microscopy. These tools enable efficient multicolor stochastic labeling of neurons at both low and high densities. Expression of multiple membrane-targeted and distinct epitope-tagged proteins is controlled both by a transcriptional driver and by stochastic, recombinase-mediated excision of transcription-terminating cassettes. This MultiColor FlpOut (MCFO) approach can be used to reveal cell shapes and relative cell positions and to track the progeny of precursor cells through development. Using two different recombinases, the number of cells labeled and the number of color combinations observed in those cells can be controlled separately. We demonstrate the utility of MCFO in a detailed study of diversity and variability of Distal medulla (Dm) neurons, multicolumnar local interneurons in the adult visual system. Similar to many brain regions, the medulla has a repetitive columnar structure that supports parallel information processing together with orthogonal layers of cell processes that enable communication between columns. We find that, within a medulla layer, processes of the cells of a given Dm neuron type form distinct patterns that reflect both the morphology of individual cells and the relative positions of their arbors. These stereotyped cell arrangements differ between cell types and can even differ for the processes of the same cell type in different medulla layers. This unexpected diversity of coverage patterns provides multiple independent ways of integrating visual information across the retinotopic columns and implies the existence of multiple developmental mechanisms that generate these distinct patterns.neuroanatomy | Drosophila | interneuron diversity | light microscopy | recombinase N ervous systems contain numerous and diverse cells displaying complex anatomical relationships. The specification and patterning of these cells must be generated by the execution of a much smaller set of instructions encoded in the genome. How many different genetic algorithms are needed? How precise are their outcomes? What types of rules do they follow? Answering such questions requires knowledge of the anatomy of neuronal processes for many different cell types, for numerous cells of the same type, and in multiple individuals. We describe here the development of a set of methods for collecting such data by light microscopy and their application in the adult visual system of Drosophila.Neuronal morphology is often sufficiently stereotyped to identify cell types. For example, many cell populations in vertebrate and invertebrate visual systems can be reliably distinguished on the basis of cell shape (1-3). In at least some cases, these anatomical cell types have been shown to correlate well with classifications based on genetic marker expression or functional properties. Important anatomical features are not limited to cell shape, but also include the spatial relationships between cells. One critical ...

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Temporal patterning of Drosophila medulla neuroblasts controls neural fates

Cited by 266 publications

References 48 publications

A conserved transcriptional network regulates lamina development in the Drosophila visual system

A conserved transcriptional network regulates lamina development in the Drosophila visual system

Transcriptomes of lineage-specific Drosophila neuroblasts profiled via genetic targeting and robotic sorting

Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system

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