Limits...
miR-965 controls cell proliferation and migration during tissue morphogenesis in the Drosophila abdomen.

Verma P, Cohen SM - Elife (2015)

Bottom Line: During pupal development, the abdominal histoblast cells proliferate and migrate to replace the larval epidermis.Ecdysone signaling downregulates miR-965 at the onset of pupariation, linking activation of the histoblast nests to the hormonal control of metamorphosis.By regulating both cell proliferation and cell migration, miR-965 contributes to the robustness of this morphogenetic system.

View Article: PubMed Central - PubMed

Affiliation: Institute of Molecular and Cell Biology, Singapore, Singapore.

ABSTRACT
Formation of the Drosophila adult abdomen involves a process of tissue replacement in which larval epidermal cells are replaced by adult cells. The progenitors of the adult epidermis are specified during embryogenesis and, unlike the imaginal discs that make up the thoracic and head segments, they remain quiescent during larval development. During pupal development, the abdominal histoblast cells proliferate and migrate to replace the larval epidermis. Here, we provide evidence that the microRNA, miR-965, acts via string and wingless to control histoblast proliferation and migration. Ecdysone signaling downregulates miR-965 at the onset of pupariation, linking activation of the histoblast nests to the hormonal control of metamorphosis. Replacement of the larval epidermis by adult epidermal progenitors involves regulation of both cell-intrinsic events and cell communication. By regulating both cell proliferation and cell migration, miR-965 contributes to the robustness of this morphogenetic system.

No MeSH data available.


Related in: MedlinePlus

Mature miR-965 miRNA regulation by EcR.miRNA quantitative RT-PCR showing the levels of mature miR-965 in RNA extracted from 0 hr pupae. esg-GAL4 was used to direct UAS-EcRRNAi expression in histoblasts. Data were normalized to U27 and snoR422 and to the esg-GAL4/+ control sample. Data represent the average of three independent biological samples ± SD. Refers to Figure 6A.DOI:http://dx.doi.org/10.7554/eLife.07389.032
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4538364&req=5

fig6s1: Mature miR-965 miRNA regulation by EcR.miRNA quantitative RT-PCR showing the levels of mature miR-965 in RNA extracted from 0 hr pupae. esg-GAL4 was used to direct UAS-EcRRNAi expression in histoblasts. Data were normalized to U27 and snoR422 and to the esg-GAL4/+ control sample. Data represent the average of three independent biological samples ± SD. Refers to Figure 6A.DOI:http://dx.doi.org/10.7554/eLife.07389.032

Mentions: Ecdysone pulses at the beginning of pupariation have been shown to induce string expression in order to reactive histoblast proliferation (Ninov et al., 2009). In light of the relationship between miR-965 and string, we asked whether miR-965 expression might be under Ecdysone control at this stage. We made use of a UAS-EcRRNAi transgene expressed under esg-Gal4 to reduce Ecdysone receptor levels in the histoblasts. RNAi-mediated depletion of EcR mRNA led to an increase in the level of the miR-965 primary transcript and mature miRNA (Figure 6A, Figure 6—figure supplement 1), and to reduced string mRNA levels in RNA samples isolated from early pupae (Figure 6A). EcR binding sites have been identified near the host gene, kismet (Gauhar et al., 2009), consistent with the possibility that ecdysone regulates expression of both kismet and miR-965. When miR-965 was overexpressed in the histoblast cells using esg-GAL4, string transcript levels were reduced (Figure 6B) and histoblast cell divisions were arrested (Figure 6C, Video 12). This phenotype resembles EcR-B mutants, in which histoblast division is compromised (Bender et al., 1997). Pupae overexpressing miR-965 in histoblast cells did not survive beyond ∼12 APF, so it was not possible to monitor the later stages of histoblast migration in this genotype.10.7554/eLife.07389.031Figure 6.Regulation of miR-965 by ecdysone at the beginning of pupariation.


miR-965 controls cell proliferation and migration during tissue morphogenesis in the Drosophila abdomen.

Verma P, Cohen SM - Elife (2015)

Mature miR-965 miRNA regulation by EcR.miRNA quantitative RT-PCR showing the levels of mature miR-965 in RNA extracted from 0 hr pupae. esg-GAL4 was used to direct UAS-EcRRNAi expression in histoblasts. Data were normalized to U27 and snoR422 and to the esg-GAL4/+ control sample. Data represent the average of three independent biological samples ± SD. Refers to Figure 6A.DOI:http://dx.doi.org/10.7554/eLife.07389.032
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4538364&req=5

fig6s1: Mature miR-965 miRNA regulation by EcR.miRNA quantitative RT-PCR showing the levels of mature miR-965 in RNA extracted from 0 hr pupae. esg-GAL4 was used to direct UAS-EcRRNAi expression in histoblasts. Data were normalized to U27 and snoR422 and to the esg-GAL4/+ control sample. Data represent the average of three independent biological samples ± SD. Refers to Figure 6A.DOI:http://dx.doi.org/10.7554/eLife.07389.032
Mentions: Ecdysone pulses at the beginning of pupariation have been shown to induce string expression in order to reactive histoblast proliferation (Ninov et al., 2009). In light of the relationship between miR-965 and string, we asked whether miR-965 expression might be under Ecdysone control at this stage. We made use of a UAS-EcRRNAi transgene expressed under esg-Gal4 to reduce Ecdysone receptor levels in the histoblasts. RNAi-mediated depletion of EcR mRNA led to an increase in the level of the miR-965 primary transcript and mature miRNA (Figure 6A, Figure 6—figure supplement 1), and to reduced string mRNA levels in RNA samples isolated from early pupae (Figure 6A). EcR binding sites have been identified near the host gene, kismet (Gauhar et al., 2009), consistent with the possibility that ecdysone regulates expression of both kismet and miR-965. When miR-965 was overexpressed in the histoblast cells using esg-GAL4, string transcript levels were reduced (Figure 6B) and histoblast cell divisions were arrested (Figure 6C, Video 12). This phenotype resembles EcR-B mutants, in which histoblast division is compromised (Bender et al., 1997). Pupae overexpressing miR-965 in histoblast cells did not survive beyond ∼12 APF, so it was not possible to monitor the later stages of histoblast migration in this genotype.10.7554/eLife.07389.031Figure 6.Regulation of miR-965 by ecdysone at the beginning of pupariation.

Bottom Line: During pupal development, the abdominal histoblast cells proliferate and migrate to replace the larval epidermis.Ecdysone signaling downregulates miR-965 at the onset of pupariation, linking activation of the histoblast nests to the hormonal control of metamorphosis.By regulating both cell proliferation and cell migration, miR-965 contributes to the robustness of this morphogenetic system.

View Article: PubMed Central - PubMed

Affiliation: Institute of Molecular and Cell Biology, Singapore, Singapore.

ABSTRACT
Formation of the Drosophila adult abdomen involves a process of tissue replacement in which larval epidermal cells are replaced by adult cells. The progenitors of the adult epidermis are specified during embryogenesis and, unlike the imaginal discs that make up the thoracic and head segments, they remain quiescent during larval development. During pupal development, the abdominal histoblast cells proliferate and migrate to replace the larval epidermis. Here, we provide evidence that the microRNA, miR-965, acts via string and wingless to control histoblast proliferation and migration. Ecdysone signaling downregulates miR-965 at the onset of pupariation, linking activation of the histoblast nests to the hormonal control of metamorphosis. Replacement of the larval epidermis by adult epidermal progenitors involves regulation of both cell-intrinsic events and cell communication. By regulating both cell proliferation and cell migration, miR-965 contributes to the robustness of this morphogenetic system.

No MeSH data available.


Related in: MedlinePlus