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Genetic control of cell morphogenesis during Drosophila melanogaster cardiac tube formation.

Medioni C, Astier M, Zmojdzian M, Jagla K, Sémériva M - J. Cell Biol. (2008)

Bottom Line: Our study of cell behavior using three-dimensional and time-lapse imaging and the distribution of cell polarity markers reveals a new mechanism of tubulogenesis in which repulsion of prepatterned luminal domains with basal membrane properties and cell shape remodeling constitute the main driving forces.From these data we propose a model for D. melanogaster cardiac lumen formation, which differs, both at a cellular and molecular level, from current models of epithelial tubulogenesis.We suggest that this new example of tube formation may be helpful in studying vertebrate heart tube formation and primary vasculogenesis.

View Article: PubMed Central - PubMed

Affiliation: Institut de Biologie du Développement de Marseille-Luminy, Centre National de la Recherche Scientifique UMR 6216, Université de la Méditerranée, 13288 Marseille, Cedex 9, France.

ABSTRACT
Tubulogenesis is an essential component of organ development, yet the underlying cellular mechanisms are poorly understood. We analyze here the formation of the Drosophila melanogaster cardiac lumen that arises from the migration and subsequent coalescence of bilateral rows of cardioblasts. Our study of cell behavior using three-dimensional and time-lapse imaging and the distribution of cell polarity markers reveals a new mechanism of tubulogenesis in which repulsion of prepatterned luminal domains with basal membrane properties and cell shape remodeling constitute the main driving forces. Furthermore, we identify a genetic pathway in which roundabout, slit, held out wings, and dystroglycan control cardiac lumen formation by establishing nonadherent luminal membranes and regulating cell shape changes. From these data we propose a model for D. melanogaster cardiac lumen formation, which differs, both at a cellular and molecular level, from current models of epithelial tubulogenesis. We suggest that this new example of tube formation may be helpful in studying vertebrate heart tube formation and primary vasculogenesis.

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Characterization of distinct CB membrane domains involved in lumen formation. Dorsal XY views of wild-type cardiac tubes (A–C and D–D″) and reconstructed Z views of wild-type CBs (A′–C′, E-–J, E′–J′, and E″–J″). (A and A′) Dg (green) and How (blue, showing CB nuclei) staining. (B and B′) Trol expression revealed using Trol-GFP reporter. (C and C′) Slit expression. Notice that Dg, Trol, and Slit are expressed at the basal side (arrowheads) and at the luminal side (double-sided arrows) of the CBs in the membrane domain forming the lumen (L domain). (D–D″) Wild-type embryo stained with antibodies against Arm (red), Dg (green), and How (blue) at stage 16. (D′, arrowhead) Arm is localized in the basolateral membranes involved in cell–cell contact between CBs of the same row. (E–J) Merged Z views of wild-type CBs from stages 13–14 in E to stage 16 in J, stained with antibodies against Arm (red), Dg (green), and How (blue). (E′–J′ and E″–J″) The same views as E–J showing Arm and How (E′–J′) or Dg and How staining (E″–J″). Arm is localized at the future contact between the two CBs (arrowheads), at the dorsal leading edge, and at the ventral side. Arm is excluded from Dg-positive domain (basal and luminal faces), before (E–E″, arrowheads), during (F–I, F′–I′, and F″–I″, arrowheads), and after CB migration (J–J″, arrowheads). When CBs join dorsally, Arm is strongly expressed at the site of contact between the two CBs (G–J, G′–J′, and G″–J″, arrowheads). When the ventral sides join to close the tube, Arm is specifically localized at the site of cell–cell contacts (dorsal and ventral; J and J′, arrowheads) and excluded from the lumen domain where Dg is expressed (J″). The Arm-positive domains and forming adherens junctions between CBs of opposite rows are called J domains. (K) Schematic representation of CB morphogenesis during cardiac tube formation. Gray, CBs; red, Arm; green, Dg; blue dashed lines, Z section positions; purple arrows, CB shape changes. (1) Before CB migration, CBs are rather round and already express Arm in the J domains and Dg in the L domains. (2) CBs constrict and form a leading edge dorsally. (3) They join first dorsally, then adopt a crescentlike shape (4), and finally meet ventrally and close the tube (5). Bars, 4 μm.
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fig4: Characterization of distinct CB membrane domains involved in lumen formation. Dorsal XY views of wild-type cardiac tubes (A–C and D–D″) and reconstructed Z views of wild-type CBs (A′–C′, E-–J, E′–J′, and E″–J″). (A and A′) Dg (green) and How (blue, showing CB nuclei) staining. (B and B′) Trol expression revealed using Trol-GFP reporter. (C and C′) Slit expression. Notice that Dg, Trol, and Slit are expressed at the basal side (arrowheads) and at the luminal side (double-sided arrows) of the CBs in the membrane domain forming the lumen (L domain). (D–D″) Wild-type embryo stained with antibodies against Arm (red), Dg (green), and How (blue) at stage 16. (D′, arrowhead) Arm is localized in the basolateral membranes involved in cell–cell contact between CBs of the same row. (E–J) Merged Z views of wild-type CBs from stages 13–14 in E to stage 16 in J, stained with antibodies against Arm (red), Dg (green), and How (blue). (E′–J′ and E″–J″) The same views as E–J showing Arm and How (E′–J′) or Dg and How staining (E″–J″). Arm is localized at the future contact between the two CBs (arrowheads), at the dorsal leading edge, and at the ventral side. Arm is excluded from Dg-positive domain (basal and luminal faces), before (E–E″, arrowheads), during (F–I, F′–I′, and F″–I″, arrowheads), and after CB migration (J–J″, arrowheads). When CBs join dorsally, Arm is strongly expressed at the site of contact between the two CBs (G–J, G′–J′, and G″–J″, arrowheads). When the ventral sides join to close the tube, Arm is specifically localized at the site of cell–cell contacts (dorsal and ventral; J and J′, arrowheads) and excluded from the lumen domain where Dg is expressed (J″). The Arm-positive domains and forming adherens junctions between CBs of opposite rows are called J domains. (K) Schematic representation of CB morphogenesis during cardiac tube formation. Gray, CBs; red, Arm; green, Dg; blue dashed lines, Z section positions; purple arrows, CB shape changes. (1) Before CB migration, CBs are rather round and already express Arm in the J domains and Dg in the L domains. (2) CBs constrict and form a leading edge dorsally. (3) They join first dorsally, then adopt a crescentlike shape (4), and finally meet ventrally and close the tube (5). Bars, 4 μm.

Mentions: To better understand the cellular mechanisms regulating cardiac lumen formation, we analyzed the distribution of cell polarity markers in developing wild-type CBs. CB precursors originate from nonpolarized mesenchymal cells of the dorsal mesoderm. After germ band retraction, they form two bilateral rows of polarized cells sharing some polarity features with epithelial cells (Fremion et al., 1999). CBs possess a basal domain adjacent to the overlying ectoderm, expressing classical markers of basement membranes; extracellular matrix proteins, including laminin A (Yarnitzky and Volk, 1995), perlecan (Terribly reduced optic lobes [Trol] in D. melanogaster; Fig. 4 B; Voigt et al., 2002), pericardin (a type IV collagenlike protein; Chartier et al., 2002), Slit (Fig. 4 C; Rothberg et al., 1988), and their receptors, Dg (Fig. 4 A); integrins; and Robo (Stark et al., 1997; Qian et al., 2005). CBs also contain basal-lateral domains expressing Discs large (Dlg; Fig. S2, A and C, available at http://www.jcb.org/cgi/content/full/jcb.200801100/DC1), α-spectrin, and adherens junction markers such as β-catenin (Armadillo [Arm] in D. melanogaster), and DE-Cadherin (DE-Cad; or Shotgun [Shg] in D. melanogaster; Fremion et al., 1999; Haag et al., 1999), from which adherens junctions among cells of the same CB rows are formed (Fig. 4 D′, arrowheads).


Genetic control of cell morphogenesis during Drosophila melanogaster cardiac tube formation.

Medioni C, Astier M, Zmojdzian M, Jagla K, Sémériva M - J. Cell Biol. (2008)

Characterization of distinct CB membrane domains involved in lumen formation. Dorsal XY views of wild-type cardiac tubes (A–C and D–D″) and reconstructed Z views of wild-type CBs (A′–C′, E-–J, E′–J′, and E″–J″). (A and A′) Dg (green) and How (blue, showing CB nuclei) staining. (B and B′) Trol expression revealed using Trol-GFP reporter. (C and C′) Slit expression. Notice that Dg, Trol, and Slit are expressed at the basal side (arrowheads) and at the luminal side (double-sided arrows) of the CBs in the membrane domain forming the lumen (L domain). (D–D″) Wild-type embryo stained with antibodies against Arm (red), Dg (green), and How (blue) at stage 16. (D′, arrowhead) Arm is localized in the basolateral membranes involved in cell–cell contact between CBs of the same row. (E–J) Merged Z views of wild-type CBs from stages 13–14 in E to stage 16 in J, stained with antibodies against Arm (red), Dg (green), and How (blue). (E′–J′ and E″–J″) The same views as E–J showing Arm and How (E′–J′) or Dg and How staining (E″–J″). Arm is localized at the future contact between the two CBs (arrowheads), at the dorsal leading edge, and at the ventral side. Arm is excluded from Dg-positive domain (basal and luminal faces), before (E–E″, arrowheads), during (F–I, F′–I′, and F″–I″, arrowheads), and after CB migration (J–J″, arrowheads). When CBs join dorsally, Arm is strongly expressed at the site of contact between the two CBs (G–J, G′–J′, and G″–J″, arrowheads). When the ventral sides join to close the tube, Arm is specifically localized at the site of cell–cell contacts (dorsal and ventral; J and J′, arrowheads) and excluded from the lumen domain where Dg is expressed (J″). The Arm-positive domains and forming adherens junctions between CBs of opposite rows are called J domains. (K) Schematic representation of CB morphogenesis during cardiac tube formation. Gray, CBs; red, Arm; green, Dg; blue dashed lines, Z section positions; purple arrows, CB shape changes. (1) Before CB migration, CBs are rather round and already express Arm in the J domains and Dg in the L domains. (2) CBs constrict and form a leading edge dorsally. (3) They join first dorsally, then adopt a crescentlike shape (4), and finally meet ventrally and close the tube (5). Bars, 4 μm.
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fig4: Characterization of distinct CB membrane domains involved in lumen formation. Dorsal XY views of wild-type cardiac tubes (A–C and D–D″) and reconstructed Z views of wild-type CBs (A′–C′, E-–J, E′–J′, and E″–J″). (A and A′) Dg (green) and How (blue, showing CB nuclei) staining. (B and B′) Trol expression revealed using Trol-GFP reporter. (C and C′) Slit expression. Notice that Dg, Trol, and Slit are expressed at the basal side (arrowheads) and at the luminal side (double-sided arrows) of the CBs in the membrane domain forming the lumen (L domain). (D–D″) Wild-type embryo stained with antibodies against Arm (red), Dg (green), and How (blue) at stage 16. (D′, arrowhead) Arm is localized in the basolateral membranes involved in cell–cell contact between CBs of the same row. (E–J) Merged Z views of wild-type CBs from stages 13–14 in E to stage 16 in J, stained with antibodies against Arm (red), Dg (green), and How (blue). (E′–J′ and E″–J″) The same views as E–J showing Arm and How (E′–J′) or Dg and How staining (E″–J″). Arm is localized at the future contact between the two CBs (arrowheads), at the dorsal leading edge, and at the ventral side. Arm is excluded from Dg-positive domain (basal and luminal faces), before (E–E″, arrowheads), during (F–I, F′–I′, and F″–I″, arrowheads), and after CB migration (J–J″, arrowheads). When CBs join dorsally, Arm is strongly expressed at the site of contact between the two CBs (G–J, G′–J′, and G″–J″, arrowheads). When the ventral sides join to close the tube, Arm is specifically localized at the site of cell–cell contacts (dorsal and ventral; J and J′, arrowheads) and excluded from the lumen domain where Dg is expressed (J″). The Arm-positive domains and forming adherens junctions between CBs of opposite rows are called J domains. (K) Schematic representation of CB morphogenesis during cardiac tube formation. Gray, CBs; red, Arm; green, Dg; blue dashed lines, Z section positions; purple arrows, CB shape changes. (1) Before CB migration, CBs are rather round and already express Arm in the J domains and Dg in the L domains. (2) CBs constrict and form a leading edge dorsally. (3) They join first dorsally, then adopt a crescentlike shape (4), and finally meet ventrally and close the tube (5). Bars, 4 μm.
Mentions: To better understand the cellular mechanisms regulating cardiac lumen formation, we analyzed the distribution of cell polarity markers in developing wild-type CBs. CB precursors originate from nonpolarized mesenchymal cells of the dorsal mesoderm. After germ band retraction, they form two bilateral rows of polarized cells sharing some polarity features with epithelial cells (Fremion et al., 1999). CBs possess a basal domain adjacent to the overlying ectoderm, expressing classical markers of basement membranes; extracellular matrix proteins, including laminin A (Yarnitzky and Volk, 1995), perlecan (Terribly reduced optic lobes [Trol] in D. melanogaster; Fig. 4 B; Voigt et al., 2002), pericardin (a type IV collagenlike protein; Chartier et al., 2002), Slit (Fig. 4 C; Rothberg et al., 1988), and their receptors, Dg (Fig. 4 A); integrins; and Robo (Stark et al., 1997; Qian et al., 2005). CBs also contain basal-lateral domains expressing Discs large (Dlg; Fig. S2, A and C, available at http://www.jcb.org/cgi/content/full/jcb.200801100/DC1), α-spectrin, and adherens junction markers such as β-catenin (Armadillo [Arm] in D. melanogaster), and DE-Cadherin (DE-Cad; or Shotgun [Shg] in D. melanogaster; Fremion et al., 1999; Haag et al., 1999), from which adherens junctions among cells of the same CB rows are formed (Fig. 4 D′, arrowheads).

Bottom Line: Our study of cell behavior using three-dimensional and time-lapse imaging and the distribution of cell polarity markers reveals a new mechanism of tubulogenesis in which repulsion of prepatterned luminal domains with basal membrane properties and cell shape remodeling constitute the main driving forces.From these data we propose a model for D. melanogaster cardiac lumen formation, which differs, both at a cellular and molecular level, from current models of epithelial tubulogenesis.We suggest that this new example of tube formation may be helpful in studying vertebrate heart tube formation and primary vasculogenesis.

View Article: PubMed Central - PubMed

Affiliation: Institut de Biologie du Développement de Marseille-Luminy, Centre National de la Recherche Scientifique UMR 6216, Université de la Méditerranée, 13288 Marseille, Cedex 9, France.

ABSTRACT
Tubulogenesis is an essential component of organ development, yet the underlying cellular mechanisms are poorly understood. We analyze here the formation of the Drosophila melanogaster cardiac lumen that arises from the migration and subsequent coalescence of bilateral rows of cardioblasts. Our study of cell behavior using three-dimensional and time-lapse imaging and the distribution of cell polarity markers reveals a new mechanism of tubulogenesis in which repulsion of prepatterned luminal domains with basal membrane properties and cell shape remodeling constitute the main driving forces. Furthermore, we identify a genetic pathway in which roundabout, slit, held out wings, and dystroglycan control cardiac lumen formation by establishing nonadherent luminal membranes and regulating cell shape changes. From these data we propose a model for D. melanogaster cardiac lumen formation, which differs, both at a cellular and molecular level, from current models of epithelial tubulogenesis. We suggest that this new example of tube formation may be helpful in studying vertebrate heart tube formation and primary vasculogenesis.

Show MeSH
Related in: MedlinePlus