Bithorax-complex genes sculpt the pattern of leucokinergic neurons in the<i>Drosophila</i>central nervous system

Estacio-Gómez, Alicia; Moris-Sanz, Marta; Schäfer, Anne-Kathrin; Perea, Daniel; Herrero, Pilar; Díaz-Benjumea, Fernando J.

doi:10.1242/dev.090423

Cited by 27 publications

(40 citation statements)

References 75 publications

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“…1D, E). During pupal development a set of 8 additional LK neurons appear anteriorly in the abdominal ganglia [37], [39]; these have far larger cell bodies than the 14 posterior ABLKs (Fig. 1D, E).…”

Section: Resultsmentioning

confidence: 99%

Insulin/IGF-Regulated Size Scaling of Neuroendocrine Cells Expressing the bHLH Transcription Factor Dimmed in Drosophila

2013

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Neurons and other cells display a large variation in size in an organism. Thus, a fundamental question is how growth of individual cells and their organelles is regulated. Is size scaling of individual neurons regulated post-mitotically, independent of growth of the entire CNS? Although the role of insulin/IGF-signaling (IIS) in growth of tissues and whole organisms is well established, it is not known whether it regulates the size of individual neurons. We therefore studied the role of IIS in the size scaling of neurons in the Drosophila CNS. By targeted genetic manipulations of insulin receptor (dInR) expression in a variety of neuron types we demonstrate that the cell size is affected only in neuroendocrine cells specified by the bHLH transcription factor DIMMED (DIMM). Several populations of DIMM-positive neurons tested displayed enlarged cell bodies after overexpression of the dInR, as well as PI3 kinase and Akt1 (protein kinase B), whereas DIMM-negative neurons did not respond to dInR manipulations. Knockdown of these components produce the opposite phenotype. Increased growth can also be induced by targeted overexpression of nutrient-dependent TOR (target of rapamycin) signaling components, such as Rheb (small GTPase), TOR and S6K (S6 kinase). After Dimm-knockdown in neuroendocrine cells manipulations of dInR expression have significantly less effects on cell size. We also show that dInR expression in neuroendocrine cells can be altered by up or down-regulation of Dimm. This novel dInR-regulated size scaling is seen during postembryonic development, continues in the aging adult and is diet dependent. The increase in cell size includes cell body, axon terminations, nucleus and Golgi apparatus. We suggest that the dInR-mediated scaling of neuroendocrine cells is part of a plasticity that adapts the secretory capacity to changing physiological conditions and nutrient-dependent organismal growth.

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Section: Resultsmentioning

confidence: 99%

Insulin/IGF-Regulated Size Scaling of Neuroendocrine Cells Expressing the bHLH Transcription Factor Dimmed in Drosophila

2013

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“…Much of our current understanding of how Hox genes impact neuronal development comes from studies on mouse MNs in the hindbrain and spinal cord, as well as leg MNs, neuroblasts and peptidergic ventral nerve cord neurons in Drosophila (Baek et al, 2013; Catela et al, 2016; Estacio-Gómez and Díaz-Benjumea, 2014; Estacio-Gómez et al, 2013; Karlsson et al, 2010; Mendelsohn et al, 2017; Miguel-Aliaga and Thor, 2004; Moris-Sanz et al, 2015; Philippidou and Dasen, 2013; Suska et al, 2011). In C. elegans , Hox genes have also been recently shown to diversify touch receptor neuron identity (Zheng et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

An intersectional gene regulatory strategy defines subclass diversity of C. elegans motor neurons

Kratsios

Kerk

Catela

et al. 2017

eLife

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A core principle of nervous system organization is the diversification of neuron classes into subclasses that share large sets of features but differ in select traits. We describe here a molecular mechanism necessary for motor neurons to acquire subclass-specific traits in the nematode Caenorhabditis elegans. Cholinergic motor neuron classes of the ventral nerve cord can be subdivided into subclasses along the anterior-posterior (A-P) axis based on synaptic connectivity patterns and molecular features. The conserved COE-type terminal selector UNC-3 not only controls the expression of traits shared by all members of a neuron class, but is also required for subclass-specific traits expressed along the A-P axis. UNC-3, which is not regionally restricted, requires region-specific cofactors in the form of Hox proteins to co-activate subclass-specific effector genes in post-mitotic motor neurons. This intersectional gene regulatory principle for neuronal subclass diversification may be conserved from nematodes to mice.DOI: http://dx.doi.org/10.7554/eLife.25751.001

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“…1C). 21 ABLKs are generated during embryonic neurogenesis by NB5-5 in the first to the seventh abdominal segments of the VNC, producing a fixed number of 7 ABLKs per hemiganglion (embryonic ABLKs: eABLKs). 37 We observed that the number of ABLKs increased during pupal stages, reaching an average of 11 in 4-day-old adults.…”

Section: Actions Of Hox Genes In Controlling Segment Diversity Througmentioning

confidence: 99%

“…39 Similar variability can be observed in the number of postembryonic neurons that produce neuropeptides, for instance, in the number of neurons producing the neuropeptide leucokinin or bursicon in the adult fly. 21,40 Thus, the number of Lk-expressing neurons in the adult CNS varies depending on the environmental conditions and on the number of copies of Abd-B. This has led us to suggest that the level of expression of Abd-B might be affected by the environmental conditions of the larva and so control the number of neurons that produce leukoquinin.…”

Section: Role Of Abd-b As a Sensor Of The Enviromental Conditions Of mentioning

confidence: 99%

“…This has led us to suggest that the level of expression of Abd-B might be affected by the environmental conditions of the larva and so control the number of neurons that produce leukoquinin. 21 Phenotypic plasticity (polyphenism) as a result of changes in the environmental conditions is widely reported in insects. 41 Environmental effects on the expression of patterning genes are also suggested by the variation in the number of segments found in populations of some species of centipedes.…”

Section: Role Of Abd-b As a Sensor Of The Enviromental Conditions Of mentioning

confidence: 99%

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Roles ofHoxgenes in the patterning of the central nervous system ofDrosophila

Estacio-Gómez

Díaz-Benjumea

2013

Fly

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One of the key aspects of functional nervous systems is the restriction of particular neural subtypes to specific regions, which permits the establishment of differential segment-specific neuromuscular networks. Although Hox genes play a major role in shaping the anterior-posterior body axis during animal development, our understanding of how they act in individual cells to determine particular traits at precise developmental stages is rudimentary. We have used the abdominal leucokinergic neurons (ABLKs) to address this issue. These neurons are generated during both embryonic and postembryonic neurogenesis by the same progenitor neuroblast, and are designated embryonic and postembryonic ABLKs, respectively. We report that the genes of the Bithorax-Complex, Ultrabithorax (Ubx) and abdominal-A (abd-A) are redundantly required to specify the embryonic ABLKs. Moreover, the segment-specific pattern of the postembryonic ABLKs, which are restricted to the most anterior abdominal segments, is controlled by the absence of Abdominal-B (Abd-B), which we found was able to repress the expression of the neuropeptide leucokinin. We discuss this and other examples of how Hox genes generate diversity within the central nervous system of Drosophila.

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Bithorax-complex genes sculpt the pattern of leucokinergic neurons in theDrosophilacentral nervous system

Cited by 27 publications

References 75 publications

Insulin/IGF-Regulated Size Scaling of Neuroendocrine Cells Expressing the bHLH Transcription Factor Dimmed in Drosophila

Insulin/IGF-Regulated Size Scaling of Neuroendocrine Cells Expressing the bHLH Transcription Factor Dimmed in Drosophila

An intersectional gene regulatory strategy defines subclass diversity of C. elegans motor neurons

Roles ofHoxgenes in the patterning of the central nervous system ofDrosophila

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