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Drosophila eggshell production: identification of new genes and coordination by Pxt.

Tootle TL, Williams D, Hubb A, Frederick R, Spradling A - PLoS ONE (2011)

Bottom Line: Mutations in pxt, encoding a putative Drosophila cyclooxygenase, cause many transcripts to begin expression prematurely, and are associated with eggshell defects.One of the temporally regulated genes, cyp18a1, which encodes a cytochromome P450 protein mediating ecdysone turnover, is downregulated in pxt mutant follicles, and cyp18a1 mutation itself alters eggshell gene expression.These studies further define the molecular program of Drosophila follicle maturation and support the idea that it is coordinated by lipid and steroid hormonal signals.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy and Cell Biology, Roy J. and Lucille Carver College of Medicine, University of Iowa, Iowa City, Iowa, United States of America. tina-tootle@uiowa.edu

ABSTRACT
Drosophila ovarian follicles complete development using a spatially and temporally controlled maturation process in which they resume meiosis and secrete a multi-layered, protective eggshell before undergoing arrest and/or ovulation. Microarray analysis revealed more than 150 genes that are expressed in a stage-specific manner during the last 24 hours of follicle development. These include all 30 previously known eggshell genes, as well as 19 new candidate chorion genes and 100 other genes likely to participate in maturation. Mutations in pxt, encoding a putative Drosophila cyclooxygenase, cause many transcripts to begin expression prematurely, and are associated with eggshell defects. Somatic activity of Pxt is required, as RNAi knockdown of pxt in the follicle cells recapitulates both the temporal expression and eggshell defects. One of the temporally regulated genes, cyp18a1, which encodes a cytochromome P450 protein mediating ecdysone turnover, is downregulated in pxt mutant follicles, and cyp18a1 mutation itself alters eggshell gene expression. These studies further define the molecular program of Drosophila follicle maturation and support the idea that it is coordinated by lipid and steroid hormonal signals.

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Temporally regulated expression of known eggshell protein transcripts.(A) An ovariole containing sequentially developing ovarian follicles ranging between stage 1 and stage 14 is depicted in cross section, revealing germline (yellow) cells comprising 15 nurse cells and an oocyte, surrounded after stage 7 by about 700 epithelial follicle cells. (B–D) Images of hand dissected stage 10B (B), stage 12 (C) or stage 14 (D) follicles, used for RNA isolation and microarray analyses. (E) The expression patterns determined from the microarray data of all 30 previously known eggshell (and 3 yolk) protein transcripts are depicted graphically. Adjacent genes with the same color are clustered in the genome. The full dynamic range of these changes is underestimated by the diagram, but can be found in Table S1. Accession numbers are listed in Table S1.
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pone-0019943-g001: Temporally regulated expression of known eggshell protein transcripts.(A) An ovariole containing sequentially developing ovarian follicles ranging between stage 1 and stage 14 is depicted in cross section, revealing germline (yellow) cells comprising 15 nurse cells and an oocyte, surrounded after stage 7 by about 700 epithelial follicle cells. (B–D) Images of hand dissected stage 10B (B), stage 12 (C) or stage 14 (D) follicles, used for RNA isolation and microarray analyses. (E) The expression patterns determined from the microarray data of all 30 previously known eggshell (and 3 yolk) protein transcripts are depicted graphically. Adjacent genes with the same color are clustered in the genome. The full dynamic range of these changes is underestimated by the diagram, but can be found in Table S1. Accession numbers are listed in Table S1.

Mentions: Drosophila ovarian follicles mature during their final day of development into a functional oocyte encased in a multi-layered shell capable of protecting and nurturing the developing embryo [1], [2], [3]. The oocyte, 15 germline-derived nurse cells and more than 700 somatic follicle cells work together during these stages, termed stages 8–14, to complete the egg (Figure 1A–D). Triggered by an internally generated steroid hormone signal, each follicle during stage 8 begins to take up yolk and to synthesize the first eggshell layer known as the vitelline membrane. Production of the chorion commences in stage 10B with follicle cell-specific amplification of several chorion structural gene clusters followed, during stages 11–14, by precisely programmed gene-specific transcriptional activation. Precise cell movements and intercellular signals during this period shape the main body of the eggshell, as well as its micropyle and dorsal respiratory appendages [4], [5]. In a process that is closely tied to eggshell production, the egg transmits anterior-posterior and dorsal-ventral patterning information from mother to embryo [6], [7]. For example, the Nudel serine protease is required both to cross-link the vitelline membrane [8], and to cleave Gastrulation Defective protein, an essential step in transmitting maternal dorsal-ventral patterning information [8]. Because of its cellular simplicity, sophisticated information content and exquisite patterning, the maturing follicle has become an attractive system for analyzing differentiation, gene regulation and morphogenesis [9], [10].


Drosophila eggshell production: identification of new genes and coordination by Pxt.

Tootle TL, Williams D, Hubb A, Frederick R, Spradling A - PLoS ONE (2011)

Temporally regulated expression of known eggshell protein transcripts.(A) An ovariole containing sequentially developing ovarian follicles ranging between stage 1 and stage 14 is depicted in cross section, revealing germline (yellow) cells comprising 15 nurse cells and an oocyte, surrounded after stage 7 by about 700 epithelial follicle cells. (B–D) Images of hand dissected stage 10B (B), stage 12 (C) or stage 14 (D) follicles, used for RNA isolation and microarray analyses. (E) The expression patterns determined from the microarray data of all 30 previously known eggshell (and 3 yolk) protein transcripts are depicted graphically. Adjacent genes with the same color are clustered in the genome. The full dynamic range of these changes is underestimated by the diagram, but can be found in Table S1. Accession numbers are listed in Table S1.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3102670&req=5

pone-0019943-g001: Temporally regulated expression of known eggshell protein transcripts.(A) An ovariole containing sequentially developing ovarian follicles ranging between stage 1 and stage 14 is depicted in cross section, revealing germline (yellow) cells comprising 15 nurse cells and an oocyte, surrounded after stage 7 by about 700 epithelial follicle cells. (B–D) Images of hand dissected stage 10B (B), stage 12 (C) or stage 14 (D) follicles, used for RNA isolation and microarray analyses. (E) The expression patterns determined from the microarray data of all 30 previously known eggshell (and 3 yolk) protein transcripts are depicted graphically. Adjacent genes with the same color are clustered in the genome. The full dynamic range of these changes is underestimated by the diagram, but can be found in Table S1. Accession numbers are listed in Table S1.
Mentions: Drosophila ovarian follicles mature during their final day of development into a functional oocyte encased in a multi-layered shell capable of protecting and nurturing the developing embryo [1], [2], [3]. The oocyte, 15 germline-derived nurse cells and more than 700 somatic follicle cells work together during these stages, termed stages 8–14, to complete the egg (Figure 1A–D). Triggered by an internally generated steroid hormone signal, each follicle during stage 8 begins to take up yolk and to synthesize the first eggshell layer known as the vitelline membrane. Production of the chorion commences in stage 10B with follicle cell-specific amplification of several chorion structural gene clusters followed, during stages 11–14, by precisely programmed gene-specific transcriptional activation. Precise cell movements and intercellular signals during this period shape the main body of the eggshell, as well as its micropyle and dorsal respiratory appendages [4], [5]. In a process that is closely tied to eggshell production, the egg transmits anterior-posterior and dorsal-ventral patterning information from mother to embryo [6], [7]. For example, the Nudel serine protease is required both to cross-link the vitelline membrane [8], and to cleave Gastrulation Defective protein, an essential step in transmitting maternal dorsal-ventral patterning information [8]. Because of its cellular simplicity, sophisticated information content and exquisite patterning, the maturing follicle has become an attractive system for analyzing differentiation, gene regulation and morphogenesis [9], [10].

Bottom Line: Mutations in pxt, encoding a putative Drosophila cyclooxygenase, cause many transcripts to begin expression prematurely, and are associated with eggshell defects.One of the temporally regulated genes, cyp18a1, which encodes a cytochromome P450 protein mediating ecdysone turnover, is downregulated in pxt mutant follicles, and cyp18a1 mutation itself alters eggshell gene expression.These studies further define the molecular program of Drosophila follicle maturation and support the idea that it is coordinated by lipid and steroid hormonal signals.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy and Cell Biology, Roy J. and Lucille Carver College of Medicine, University of Iowa, Iowa City, Iowa, United States of America. tina-tootle@uiowa.edu

ABSTRACT
Drosophila ovarian follicles complete development using a spatially and temporally controlled maturation process in which they resume meiosis and secrete a multi-layered, protective eggshell before undergoing arrest and/or ovulation. Microarray analysis revealed more than 150 genes that are expressed in a stage-specific manner during the last 24 hours of follicle development. These include all 30 previously known eggshell genes, as well as 19 new candidate chorion genes and 100 other genes likely to participate in maturation. Mutations in pxt, encoding a putative Drosophila cyclooxygenase, cause many transcripts to begin expression prematurely, and are associated with eggshell defects. Somatic activity of Pxt is required, as RNAi knockdown of pxt in the follicle cells recapitulates both the temporal expression and eggshell defects. One of the temporally regulated genes, cyp18a1, which encodes a cytochromome P450 protein mediating ecdysone turnover, is downregulated in pxt mutant follicles, and cyp18a1 mutation itself alters eggshell gene expression. These studies further define the molecular program of Drosophila follicle maturation and support the idea that it is coordinated by lipid and steroid hormonal signals.

Show MeSH