Multiple enhancers contribute to spatial but not temporal complexity in the expression of the proneural gene, amos

Holohan, Eimear E.; Lage, Petra I. zur; Jarman, Andrew P.

doi:10.1186/1471-213x-6-53

Cited by 11 publications

(9 citation statements)

References 38 publications

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“…while present in the proneural genes for neuroblasts and sensory hair cells, achaete and scute , it is not found in amos , the proneural gene for olfactory sensilla (Van Doren et al, 1991 and 1992; Martinez et al, 1993; zur Lage et al, 2003; Holohan et al, 2006). Similarly, among vertebrate proneural homologues, direct auto-regulation is present in Math1 but not in Mash1 or Neurogenin (Helms et al, 2000; Meredith and Johnson, 2000; Bertrand et al, 2002).…”

Section: Discussionmentioning

confidence: 99%

Distinct regulation of atonal in a visual organ of Drosophila : Organ-specific enhancer and lack of autoregulation in the larval eye

Zhou

Friedrich

et al. 2017

Developmental Biology

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Drosophila has three types of visual organs, the larval eyes or Bolwig’s organs (BO), the ocelli (OC) and the compound eyes (CE). In all, the bHLH protein Atonal (Ato) functions as the proneural factor for photoreceptors and effects the transition from progenitor cells to differentiating neurons. In this work, we investigate the regulation of ato expression in the BO primordium (BOP). Surprisingly, we find that ato transcription in the BOP is entirely independent of the shared regulatory DNA for the developing CE and OC. The core enhancer for BOP expression, atoBO, lies ~6 kb upstream of the ato gene, in contrast to the downstream location of CE and OC regulatory elements. Moreover, maintenance of ato expression in the neuronal precursors through autoregulation-a common and ancient feature of ato expression that is well-documented in eyes, ocelli and chordotonal organs-does not occur in the BO. We also show that the atoBO enhancer contains two binding sites for the transcription factor Sine oculis (So), a core component of the progenitor specification network in all three visual organs. These binding sites function in vivo and are specifically bound by So in vitro. Taken together, our findings reveal that the control of ato transcription in the evolutionarily derived BO has diverged considerably from ato regulation in the more ancestral compound eyes and ocelli, to the extent of acquiring what appears to be a distinct and evolutionarily novel cis-regulatory module.

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Section: Discussionmentioning

confidence: 99%

Distinct regulation of atonal in a visual organ of Drosophila : Organ-specific enhancer and lack of autoregulation in the larval eye

Zhou

Friedrich

et al. 2017

Developmental Biology

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“…Could other mechanisms thus be used to replace autoregulation to maintain stable neural fate? Positive autoregulation has not been found in studies of some Drosophila neurons, indicating that although the segregation of initiation and autoregulation provides an important conceptual insight into mechanisms of fate specification, similar outcomes might also be achieved by other regulatory mechanisms (Holohan et al, 2006;Zhou et al, 2017). It is possible that transcription factors further downstream are responsible.…”

Section: Coding Mutationmentioning

confidence: 99%

All in the family: proneural bHLH genes and neuronal diversity

Baker

Brown

2018

Development

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Proneural basic Helix-Loop-Helix (bHLH) proteins are required for neuronal determination and the differentiation of most neural precursor cells. These transcription factors are expressed in vastly divergent organisms, ranging from sponges to primates. Here, we review proneural bHLH gene evolution and function in the and vertebrate nervous systems, arguing that the gene provides a useful platform for understanding proneural gene structure and regulation. We also discuss how functional equivalency experiments using distinct proneural genes can reveal how proneural gene duplication and divergence are interwoven with neuronal complexity.

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“…Combined, these changes allow a spatially and temporally discrete regulation of both atonal paralogs in vertebrates thus tying them into very different functions (ear development for Atoh1 and eye development for Atoh7 ) that are served by the single atonal gene in flies (both ‘ears’ and eyes). Similar to Atoh1 , fly atonal also has an autoregulatory enhancer [39, 40], but amos appears to lack such autoregulation [41]. The presence of such auto-regulatory enhancers in fly atonal and mouse Atoh1 suggests that this may be the ancestral condition.…”

Section: Evolution Of Bhlh Genes For Differentiation Regulation Of Nementioning

confidence: 99%

The role of bHLH genes in ear development and evolution: revisiting a 10-year-old hypothesis

Fritzsch

Eberl

Beisel

2010

Cell. Mol. Life Sci.

106

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In mouse ear development, two bHLH genes, Atoh1 and Neurog1, are essential for hair cell and sensory neuron differentiation. Evolution converted the original simple atonal-dependent neurosensory cell formation program of diploblasts into the derived developmental program of vertebrates that generates two neurosensory cell types, the sensory neuron and the sensory hair cell. This transformation was achieved through gene multiplication in ancestral triploblasts resulting in the expansion of the atonal bHLH gene family. Novel genes of the Neurogenin and NeuroD families are upregulated prior to the expression of Atoh1. Recent data suggest that NeuroD and Neurogenin were lost or their function in neuronal specification reduced in flies, thus changing our perception of the evolution of these genes. This sequence of expression changes was accompanied by modification of the E-box binding sites of these genes to regulate different downstream genes and to form inhibitory loops among each other, thus fine-tuning expression transitions.

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Multiple enhancers contribute to spatial but not temporal complexity in the expression of the proneural gene, amos

Cited by 11 publications

References 38 publications

Distinct regulation of atonal in a visual organ of Drosophila : Organ-specific enhancer and lack of autoregulation in the larval eye

Distinct regulation of atonal in a visual organ of Drosophila : Organ-specific enhancer and lack of autoregulation in the larval eye

All in the family: proneural bHLH genes and neuronal diversity

The role of bHLH genes in ear development and evolution: revisiting a 10-year-old hypothesis

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