Subtype-specific neuronal remodeling during<i>Drosophila</i>metamorphosis

Veverytsa, Lyubov; Allan, Douglas W.

doi:10.4161/fly.23969

Cited by 24 publications

(29 citation statements)

References 85 publications

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“…Instead, remarkably diverse cellular events take place for sculpturing the adult CNS. These in general include production of new cells, remodeling of persistent larval neurons, and apoptosis of obsolete neurons (Veverytsa and Allan, 2013). To gain insight into a role for MsHid in the neuronal apoptosis, the expression of MsHid was analyzed with RNA derived from the dissected CNS.…”

Section: Resultsmentioning

confidence: 99%

“…Specific groups of larval neurons in the CNS are also programmed to die to sculpture functional adult CNS (Robinow et al, 1993; Draizen et al, 1999; Winbush and Weeks, 2011; Lee et al, 2013a, 2013b; Veverytsa and Allan, 2013). Based on prominent expression of MsHid in the CNS, we propose that MsHid functions as an essential apoptogenic factor for metamorphic neuronal cell death in the CNS.…”

Section: Discussionmentioning

confidence: 99%

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Cloning and functional characterizations of an apoptogenic Hid gene in the Scuttle Fly, Megaselia scalaris (Diptera; Phoridae)

Yoo

Lam

Lee

et al. 2017

Gene

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Although the mechanisms of apoptotic cell death have been well studied in the fruit fly, Drosophila melanogaster, it is unclear whether such mechanisms are conserved in other distantly related species. Using degenerate primers and PCR, we cloned a proapoptotic gene homologous to Head involution defective (Hid) from the Scuttle fly, Megaselia scalaris (MsHid). MsHid cDNA encodes a 197-amino acid-long polypeptide, which so far is the smallest HID protein. PCR analyses revealed that the MsHid gene consists of four exons and three introns. Ectopic expression of MsHid in various peptidergic neurons and non-neuronal tissues in Drosophila effectively induced apoptosis of these cells. However, deletion of either conserved domain, N-terminal IBM or C-terminal MTS, abolished the apoptogenic activity of MsHID, indicating that these two domains are indispensable. Expression of MsHid was found in all life stages, but more prominently in embryos and pupae. MsHid is actively expressed in the central nervous system (CNS), indicating its important role in CNS development. Together MsHID is likely to be an important cell death inducer during embryonic and post-embryonic development in this species. In addition, we found 2-fold induction of MsHid expression in UV-irradiated embryos, indicating a possible role for MsHid in UV-induced apoptosis.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Cloning and functional characterizations of an apoptogenic Hid gene in the Scuttle Fly, Megaselia scalaris (Diptera; Phoridae)

Yoo

Lam

Lee

et al. 2017

Gene

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“…4A). These neuronal genes may be developmentally regulated, because insects, like Drosophila, go through metamorphosis in which the nervous system is remarkably remodeled from larva stage to adult stage (20). Therefore, we compared expression levels of 10 genes between third-instar larvae and 1-d adult in the brain.…”

Section: Heterochromatin Enrichment Predominantly Occurs In Long Genesmentioning

confidence: 99%

Heterochromatin remodeling by CDK12 contributes to learning in Drosophila

Pan

Xie

et al. 2015

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

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Dynamic regulation of chromatin structure is required to modulate the transcription of genes in eukaryotes. However, the factors that contribute to the plasticity of heterochromatin structure are elusive. Here, we report that cyclin-dependent kinase 12 (CDK12), a transcription elongation-associated RNA polymerase II (RNAPII) kinase, antagonizes heterochromatin enrichment in Drosophila chromosomes. Notably, loss of CDK12 induces the ectopic accumulation of heterochromatin protein 1 (HP1) on euchromatic arms, with a prominent enrichment on the X chromosome. Furthermore, ChIP and sequencing analysis reveals that the heterochromatin enrichment on the X chromosome mainly occurs within long genes involved in neuronal functions. Consequently, heterochromatin enrichment reduces the transcription of neuronal genes in the adult brain and results in a defect in Drosophila courtship learning. Taken together, these results define a previously unidentified role of CDK12 in controlling the epigenetic transition between euchromatin and heterochromatin and suggest a chromatin regulatory mechanism in neuronal behaviors.A ppropriate regulation of gene transcription is essential throughout the life of an organism. In eukaryotes, DNA and histone octamers are assembled into nucleosomes and further compacted into higher-order structures (1). Dynamic changes in the chromatin architecture affect gene transcription in many aspects of developmental and physiological processes, such as neural plasticity, memory formation, and cognition (2, 3). Eukaryotic genomes are composed of two basic forms, euchromatin and heterochromatin, which are originally characterized by their cytological chromatin packaging levels. Euchromatic regions are generally associated with a relatively open chromatin configuration and mainly contain transcriptionally active genes, whereas heterochromatin is highly compacted and less accessible to the transcriptional machinery (4). Drosophila heterochromatin is mainly localized at the pericentric and subtelomeric regions and enriched for methylation of histone H3 on Lys9 (H3K9me), which provides a docking site for heterochromatin protein 1 (HP1) (5, 6), a highly conserved protein involved in heterochromatin formation (7). Previous studies also show that HP1 and H3K9me associate with a subset of loci on euchromatic regions, and they presumably serve to fine tune the level of gene transcription (8-10). One significant question that comes up is how the chromatin structure is dynamically regulated to impact expression of genes in complex neuronal processes, such as learning and memory. Our earlier study on chromatin domain mapping of chromosome 4 suggests that heterochromatic domains may be regulated by the activities of RNA polymerase II (RNAPII) complexes, which form a "barrier" to prevent heterochromatin spreading and transcriptional gene silencing (11). However, the mechanism underlying such a mode of regulation and the consequence on reprogrammed transcription remain to be investigated. ResultsCyclin-Dependent Kinase 12 ...

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“…During this migration process, the PG undergoes degeneration, as the CC and CA form separate structures (Dai & Gilbert, ). The central nervous system (CNS) also undergoes extensive reorganization, including the remodeling of axonal and dendritic arbors, PCD of some larval neurons, and differentiation of adult‐specific neurons (Lacin & Truman, ; Tissot & Stocker, ; Truman, ; Veverytsa & Allan, ; Williams & Truman, ). As a result, adults have distinct morphological features that enable adult‐specific behaviors such as flight, mating, and periodical feeding.…”

Section: Introductionmentioning

confidence: 99%

Adult‐specific insulin‐producing neurons in Drosophila melanogaster

Ohhara

Kobayashi

Yamakawa‐Kobayashi

et al. 2018

J of Comparative Neurology

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Holometabolous insects undergo metamorphosis to reorganize their behavioral and morphological features into adult-specific ones. In the central nervous system (CNS), some larval neurons undergo programmed cell death, whereas others go through remodeling of axonal and dendritic arbors to support functions of re-established adult organs. Although there are multiple neuropeptides that have stage-specific roles in holometabolous insects, the reorganization pattern of the entire neuropeptidergic system through metamorphosis still remains largely unclear. In this study, we conducted a mapping and lineage tracing of peptidergic neurons in the larval and adult CNS by using Drosophila genetic tools. We found that Diuretic hormone 44-producing median neurosecretory cells start expressing Insulin-like peptide 2 in the pharate adult stage. This neuronal cluster projects to the corpora cardiaca and dorsal vessel in both larval and adult stages, and also innervates an adult-specific structure in the digestive tract, the crop. We propose that the adult-specific insulin-producing cells may regulate functions of the digestive system in a stage-specific manner. Our study provides a neuroanatomical basis for understanding remodeling of the neuropeptidergic system during insect development and evolution.

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Subtype-specific neuronal remodeling duringDrosophilametamorphosis

Cited by 24 publications

References 85 publications

Cloning and functional characterizations of an apoptogenic Hid gene in the Scuttle Fly, Megaselia scalaris (Diptera; Phoridae)

Cloning and functional characterizations of an apoptogenic Hid gene in the Scuttle Fly, Megaselia scalaris (Diptera; Phoridae)

Heterochromatin remodeling by CDK12 contributes to learning in Drosophila

Adult‐specific insulin‐producing neurons in Drosophila melanogaster

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