Drosophila retinal pigment cell death is regulated in a position-dependent manner by a cell memory gene

Dos-Santos, Nicolas; Rubin, Thomas; Chalvet, Fabienne; Gandille, Pierre; Crémazy, Frédéric; Leroy, Jacqueline; Boissonneau, Elisabeth; Théodore, Laurent

doi:10.1387/ijdb.072406nd

Cited by 13 publications

(7 citation statements)

References 46 publications

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“…These analyses identified several transcription factors, including Trl, which may contribute to transcriptional regulation during pupal eye development ( Supplementary Table S13 ) ( McLeay and Bailey 2010 ). In a previous study of the role of Trl in the apoptosis of lattice cells, patterning defects are also evident in Trl mutant clones, underscoring a role for Trl in pupal eye morphogenesis ( Dos-Santos et al 2008 ). Trl can influence transcription by functioning as either a transcriptional activator ( Biggin and Tjian 1988 ; Soeller et al 1993 ; Farkas et al 1994 ) or a repressor ( Farkas et al 1994 ; Horard et al 2000 ; Busturia et al 2001 ; Poux et al 2001 ; Mahmoudi et al 2003 ; Mishra et al 2003 ), and interestingly, our analyses indicated that Trl expression declined significantly at 40 h relative to 21 h APF ( Supplementary Tables S12 and S13 ).…”

Section: Resultsmentioning

confidence: 79%

Comparative transcriptome analyses of theDrosophilapupal eye

DeAngelis

Coolon

Johnson

2020

G3 Genes|Genomes|Genetics

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Tissue function is dependent on correct cellular organization and behavior. As a result, the identification and study of genes that contribute to tissue morphogenesis is of paramount importance to the fields of cell and developmental biology. Many of the genes required for tissue patterning and organization are highly conserved between phyla. This has led to the emergence of several model organisms and developmental systems that are used to study tissue morphogenesis. One such model is the Drosophila melanogaster pupal eye that has a highly stereotyped arrangement of cells. In addition, the pupal eye is postmitotic that allows for the study of tissue morphogenesis independent from any effects of proliferation. While the changes in cell morphology and organization that occur throughout pupal eye development are well documented, less is known about the corresponding transcriptional changes that choreograph these processes. To identify these transcriptional changes, we dissected wild-type Canton S pupal eyes and performed RNA-sequencing. Our analyses identified differential expression of many loci that are documented regulators of pupal eye morphogenesis and contribute to multiple biological processes including signaling, axon projection, adhesion, and cell survival. We also identified differential expression of genes not previously implicated in pupal eye morphogenesis such as components of the Toll pathway, several non-classical cadherins, and components of the muscle sarcomere, which could suggest these loci function as novel patterning factors.

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Section: Resultsmentioning

confidence: 79%

Comparative transcriptome analyses of theDrosophilapupal eye

DeAngelis

Coolon

Johnson

2020

G3 Genes|Genomes|Genetics

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“…Анализ Trl-мутантов продемонстрировал, что GAF необходим для эмбриогенеза, развития глаза и крыла дрозофилы (Bhat et al, 1996;Dos-Santos et al, 2008;Omelina et al, 2011;Bayarmagnai et al, 2012).…”

Section: Introductionunclassified

Lack of GAGA protein in Trl mutants causes massive cell death in Drosophila spermatogenesis and oogenesis

et al. 2021

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Drosophila protein GAGA (GAF) is a factor of epigenetic transcription regulation of a large group of genes with a wide variety of cellular functions. GAF is encoded by the Trithorax-like (Trl) gene, which is important for the formation of various organs and tissues at all stages of ontogenesis. In our previous works, we showed that this protein is necessary for the development of the reproductive system, both in males and females of Drosophila. Decreased expression of the Trl gene led to multiple disorders of spermatogenesis and oogenesis. One of the significant disorders was associated with massive degradation and loss of cells in the germline. In this work, we carried out a more detailed cytological study to determine what type of germ cell death is characteristic of Trl mutants, and whether there are disturbances or changes in this process compared to the norm. The results obtained showed that the lack of GAF protein causes massive germ cell death in both females and males of Drosophila, but this death manifests itself in different ways, depending on the sex. In Trl females, this process does not differ phenotypically from the norm. In the dying egg chambers, signs of apoptosis and autophagy were revealed, as well as morphological features that are characteristic of the wild type. In males, Trl mutations induce mass germ cell death through autophagy, which is not typical of Drosophila spermatogenesis, and has not been previously described, neither in the norm nor in other genes’ mutations. Thus, GAF lack in Trl mutants leads to increased germ cell death through apoptosis and autophagy. Ectopic cell death and germ line atrophy are probably associated with impaired expression of the GAGA factor target genes, among which there are genes that regulate both apoptosis and autophagy.

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“…In Drosophila , in addition to Hox genes, GAF regulates a wide‐range of genes that are important for the formation of various organs and tissues at all stages of ontogenesis. It has been shown that GAF is necessary for embryogenesis, oogenesis, spermatogenesis, and eye and wing development (Bayarmagnai, Nicolay, Islam, Lopez‐Bigas, & Frolov, ; Bhat et al, ; Dos‐Santos et al, ; Ogienko et al, ; Ogienko et al, ; Omelina, Pavlova, Ogienko, & Baricheva, ). GAF is also involved in processes responsible for cellular memory, migration, and programmed cell death (Cavalli & Paro, ; Dorogova, Fedorova, Bolobolova, Ogienko, & Baricheva, ; Dorogova, Khrushcheva, Fedorova, Ogienko, & Baricheva, ; Mishra, Chopra, Srinivasan, & Mishra, ; Ogienko et al, ; Poux, Horard, Sigrist, & Pirrotta, ).…”

Section: Introductionmentioning

confidence: 99%

GAGA protein is required for multiple aspects of Drosophila oogenesis and female fertility

Федорова

Дорогова

Болоболова

et al. 2018

Genesis

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Summary Investigation of Drosophila oogenesis provides the opportunity to understand conservative genetic mechanisms underlying fertile female gamete development. In this study, we showed that the Drosophila DNA‐binding protein GAGA factor (GAF) had a multifunctional role in oogenesis and it is involved in the regulation of this process genetic program. We studied the influence on Drosophila oogenesis of a number of mutations in the 5′ region of the Trl gene that encodes GAF. We found that our originally generated Trl mutations lead to a decrease in transcriptional gene activity and levels of GAF expression in both germline and follicular cells. Cytological (fluorescence and electron microscopy) analysis showed that GAF loss resulted in multiple oogenesis defects. Mutations affected the actin cytoskeleton, leading to decrease of cytoplasmic filaments in nurse cells and basal actin in follicular cells. GAF depletion also leads to abnormal follicular cells migration, both border and centripetal. In addition, mutant ovaries demonstrated abnormalities in germ cells, including mitochondria, endoplasmic reticulum, karyosome organization, yolk granule formation and selective transport. Loss of GAF also promoted excessive cell death and egg chamber degradation. In sum, these defects caused very high or full female sterility. Since one of the main GAF activities is regulation of transcription, the complex phenotypes of the Trl mutants might be the consequence of its multiple target genes misexpression.

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Drosophila retinal pigment cell death is regulated in a position-dependent manner by a cell memory gene

Cited by 13 publications

References 46 publications

Comparative transcriptome analyses of theDrosophilapupal eye

Comparative transcriptome analyses of theDrosophilapupal eye

Lack of GAGA protein in Trl mutants causes massive cell death in Drosophila spermatogenesis and oogenesis

GAGA protein is required for multiple aspects of Drosophila oogenesis and female fertility

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