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Trafficking through COPII stabilises cell polarity and drives secretion during Drosophila epidermal differentiation.

Norum M, Tång E, Chavoshi T, Schwarz H, Linke D, Uv A, Moussian B - PLoS ONE (2010)

Bottom Line: We are studying the molecular mechanisms that Drosophila tracheal and epidermal cells deploy to form their specific apical ECM during differentiation.In this work we demonstrate that the two genetically identified factors haunted and ghost are essential for polarity maintenance, membrane topology as well as for secretion of the tracheal luminal matrix and the cuticle.Taken together, epithelial differentiation during Drosophila embryogenesis is a concerted action of ECM formation, plasma membrane remodelling and maintenance of cell polarity that all three rely mainly, if not absolutely, on the canonical secretory pathway from the ER over the Golgi apparatus to the plasma membrane.

View Article: PubMed Central - PubMed

Affiliation: Interfaculty Institute for Cell Biology, University of Tübingen, Tübingen, Germany.

ABSTRACT

Background: The differentiation of an extracellular matrix (ECM) at the apical side of epithelial cells implies massive polarised secretion and membrane trafficking. An epithelial cell is hence engaged in coordinating secretion and cell polarity for a correct and efficient ECM formation.

Principal findings: We are studying the molecular mechanisms that Drosophila tracheal and epidermal cells deploy to form their specific apical ECM during differentiation. In this work we demonstrate that the two genetically identified factors haunted and ghost are essential for polarity maintenance, membrane topology as well as for secretion of the tracheal luminal matrix and the cuticle. We show that they code for the Drosophila COPII vesicle-coating components Sec23 and Sec24, respectively, that organise vesicle transport from the ER to the Golgi apparatus.

Conclusion: Taken together, epithelial differentiation during Drosophila embryogenesis is a concerted action of ECM formation, plasma membrane remodelling and maintenance of cell polarity that all three rely mainly, if not absolutely, on the canonical secretory pathway from the ER over the Golgi apparatus to the plasma membrane. Our results indicate that COPII vesicles constitute a central hub for these processes.

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Hau and Gho are needed for the formation of the tracheal cuticle.In the wild-type tracheal cuticle of the dorsal trunk and the primary branches of late stage 17 embryos, chitin is organised in a spiral running perpendicular to the length of the tube (A). Remnants of the luminal chitin are visible (arrow). These chitin cables constitute the taenidial folds (tae), which are bulges of the larval cuticle (B). At the larval stage, the lumen (lum) of the tracheal tubes does not contain any solid material. In hau late stage 17 mutant embryos, the chitin cables of the dorsal trunk and the primary branches are properly formed (C). The tracheal lumen, however, is much narrower compared to the wild-type lumen. The hau larval tracheal cuticle dilates and the taenidial folds are sloppy (D). The lumen of the hau mutant larval tracheae is not completely cleared. In gho stage 17 mutant embryos, chitin cables are largely disorganised and often absent (E). The tracheal tubes have an irregular diameter. The gho mutant larval tracheae have shallow taenidiae and their lumen fails to be cleared (F). (B,D,F) Electronmicrographs. Scale bars are 500nm. (A,C,E) Fluorescence microscopy.
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pone-0010802-g006: Hau and Gho are needed for the formation of the tracheal cuticle.In the wild-type tracheal cuticle of the dorsal trunk and the primary branches of late stage 17 embryos, chitin is organised in a spiral running perpendicular to the length of the tube (A). Remnants of the luminal chitin are visible (arrow). These chitin cables constitute the taenidial folds (tae), which are bulges of the larval cuticle (B). At the larval stage, the lumen (lum) of the tracheal tubes does not contain any solid material. In hau late stage 17 mutant embryos, the chitin cables of the dorsal trunk and the primary branches are properly formed (C). The tracheal lumen, however, is much narrower compared to the wild-type lumen. The hau larval tracheal cuticle dilates and the taenidial folds are sloppy (D). The lumen of the hau mutant larval tracheae is not completely cleared. In gho stage 17 mutant embryos, chitin cables are largely disorganised and often absent (E). The tracheal tubes have an irregular diameter. The gho mutant larval tracheae have shallow taenidiae and their lumen fails to be cleared (F). (B,D,F) Electronmicrographs. Scale bars are 500nm. (A,C,E) Fluorescence microscopy.

Mentions: The tracheal cuticle covers the apical (luminal) surface of the tracheal epithelium, and forms a specialized spiral-like structure called the taenidiae. The taenidiae are chitin-containing cuticular folds that are thought to support an open lumen while allowing flexibility along the tubular axis (Figure 6A,B). Detection of chitin by CBP highlights remnants of the taenidiae in hau mutant embryos, whereas gho mutant embryos seem not to form these structures (Figure 6C and E). Ultrastructural analysis of the trachea confirms the presence of taenidiae in hau mutant larvae (Figure 6D), however, their size is variable and their spacing is irregular. In gho mutant larvae traces of shallow taenidia can be distinguished at the ultrastructural level (Figure 6F).


Trafficking through COPII stabilises cell polarity and drives secretion during Drosophila epidermal differentiation.

Norum M, Tång E, Chavoshi T, Schwarz H, Linke D, Uv A, Moussian B - PLoS ONE (2010)

Hau and Gho are needed for the formation of the tracheal cuticle.In the wild-type tracheal cuticle of the dorsal trunk and the primary branches of late stage 17 embryos, chitin is organised in a spiral running perpendicular to the length of the tube (A). Remnants of the luminal chitin are visible (arrow). These chitin cables constitute the taenidial folds (tae), which are bulges of the larval cuticle (B). At the larval stage, the lumen (lum) of the tracheal tubes does not contain any solid material. In hau late stage 17 mutant embryos, the chitin cables of the dorsal trunk and the primary branches are properly formed (C). The tracheal lumen, however, is much narrower compared to the wild-type lumen. The hau larval tracheal cuticle dilates and the taenidial folds are sloppy (D). The lumen of the hau mutant larval tracheae is not completely cleared. In gho stage 17 mutant embryos, chitin cables are largely disorganised and often absent (E). The tracheal tubes have an irregular diameter. The gho mutant larval tracheae have shallow taenidiae and their lumen fails to be cleared (F). (B,D,F) Electronmicrographs. Scale bars are 500nm. (A,C,E) Fluorescence microscopy.
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2875407&req=5

pone-0010802-g006: Hau and Gho are needed for the formation of the tracheal cuticle.In the wild-type tracheal cuticle of the dorsal trunk and the primary branches of late stage 17 embryos, chitin is organised in a spiral running perpendicular to the length of the tube (A). Remnants of the luminal chitin are visible (arrow). These chitin cables constitute the taenidial folds (tae), which are bulges of the larval cuticle (B). At the larval stage, the lumen (lum) of the tracheal tubes does not contain any solid material. In hau late stage 17 mutant embryos, the chitin cables of the dorsal trunk and the primary branches are properly formed (C). The tracheal lumen, however, is much narrower compared to the wild-type lumen. The hau larval tracheal cuticle dilates and the taenidial folds are sloppy (D). The lumen of the hau mutant larval tracheae is not completely cleared. In gho stage 17 mutant embryos, chitin cables are largely disorganised and often absent (E). The tracheal tubes have an irregular diameter. The gho mutant larval tracheae have shallow taenidiae and their lumen fails to be cleared (F). (B,D,F) Electronmicrographs. Scale bars are 500nm. (A,C,E) Fluorescence microscopy.
Mentions: The tracheal cuticle covers the apical (luminal) surface of the tracheal epithelium, and forms a specialized spiral-like structure called the taenidiae. The taenidiae are chitin-containing cuticular folds that are thought to support an open lumen while allowing flexibility along the tubular axis (Figure 6A,B). Detection of chitin by CBP highlights remnants of the taenidiae in hau mutant embryos, whereas gho mutant embryos seem not to form these structures (Figure 6C and E). Ultrastructural analysis of the trachea confirms the presence of taenidiae in hau mutant larvae (Figure 6D), however, their size is variable and their spacing is irregular. In gho mutant larvae traces of shallow taenidia can be distinguished at the ultrastructural level (Figure 6F).

Bottom Line: We are studying the molecular mechanisms that Drosophila tracheal and epidermal cells deploy to form their specific apical ECM during differentiation.In this work we demonstrate that the two genetically identified factors haunted and ghost are essential for polarity maintenance, membrane topology as well as for secretion of the tracheal luminal matrix and the cuticle.Taken together, epithelial differentiation during Drosophila embryogenesis is a concerted action of ECM formation, plasma membrane remodelling and maintenance of cell polarity that all three rely mainly, if not absolutely, on the canonical secretory pathway from the ER over the Golgi apparatus to the plasma membrane.

View Article: PubMed Central - PubMed

Affiliation: Interfaculty Institute for Cell Biology, University of Tübingen, Tübingen, Germany.

ABSTRACT

Background: The differentiation of an extracellular matrix (ECM) at the apical side of epithelial cells implies massive polarised secretion and membrane trafficking. An epithelial cell is hence engaged in coordinating secretion and cell polarity for a correct and efficient ECM formation.

Principal findings: We are studying the molecular mechanisms that Drosophila tracheal and epidermal cells deploy to form their specific apical ECM during differentiation. In this work we demonstrate that the two genetically identified factors haunted and ghost are essential for polarity maintenance, membrane topology as well as for secretion of the tracheal luminal matrix and the cuticle. We show that they code for the Drosophila COPII vesicle-coating components Sec23 and Sec24, respectively, that organise vesicle transport from the ER to the Golgi apparatus.

Conclusion: Taken together, epithelial differentiation during Drosophila embryogenesis is a concerted action of ECM formation, plasma membrane remodelling and maintenance of cell polarity that all three rely mainly, if not absolutely, on the canonical secretory pathway from the ER over the Golgi apparatus to the plasma membrane. Our results indicate that COPII vesicles constitute a central hub for these processes.

Show MeSH
Related in: MedlinePlus