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doi: 10.1242/10.1242/dev.00488

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pannier and pointedP2 act sequentially to regulate Drosophila heart development

Alejandra D. Alvarez1, Weiyang Shi2, Beth A. Wilson1 and James B. Skeath1,*

1 Department of Genetics, Washington University School of Medicine, 4566 Scott Avenue, St Louis, MO 63110, USA
2 Program in Developmental Biology, Washington University School of Medicine, 4566 Scott Avenue, St Louis, MO 63110, USA



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  		Fig. 7. Heart cells and their lineages, and a model for pnt and pnr function in the heart. (Top) The heart and heart cell lineages. In the whole heart schematic, Tin-positive pericardial cells are not shown in the posterior domain because in this region they reside beneath the cardioblasts. Segment names are provided above the schematic. The lineages of all anterior domain heart cells (left) and all heart cells found within one segment of the posterior heart domain (right) are shown below the whole heart schematic. Owing to sample size, Tin expression in pericardial cells 1-9 in the anterior domain should be considered preliminary. (Bottom) Cardioblasts and pericardial cells develop from the dorsalmost region of the mesoderm: the cardiac mesoderm (CM). Initially, all dorsal mesodermal cells express Tin (top). Tin expression then resolves into two stripes of cells: a dorsal stripe that defines the cardiac mesoderm and a ventral undulating stripe that labels the primordium of the visceral mesoderm (VM). As development proceeds, cardioblasts and pericardial cells develop from the cardiac mesoderm with pericardial cells residing interior and slightly ventral to cardioblasts. In the absence of pnr function, most of the cardiac mesoderm does not form; however, when cardiac mesoderm forms, the subsequent development of cardioblasts and pericardial cells is normal. In the absence of pnt, cardiac mesoderm forms normally but the subsequent development of pericardial cells is perturbed such that cardioblasts appear to develop in their place.

 


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  		Fig. 1. Cell lineages of Eve- and Tin-positive pericardial cells and anterior Tin-positive cardioblasts. High-magnification dorsal views of stage 15-16 embryos labeled for ß-galactosidase (brown) to identify clones and Eve (A) or Tin (B-D) (black). (A) Clone that contains two Eve-positive pericardial cells (arrows). (B) Clone that contains two Tin-positive pericardial cells (arrows). (C) Anterior heart clone that contains one Tin-positive cardioblast (arrow) and one Tin-positive pericardial cell (arrowhead). (D) Anterior heart clone that contains one Tin-positive cardioblast (arrow) and one Tin-negative pericardial cell (arrowhead). Anterior is towards the left.

 


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  		Fig. 2. pointed represses cardioblast development. (Top) The pointed locus, highlighting the intron-exon structure of pntP1 and pntP2. (Bottom) High-magnification dorsal views of stage 16 wild-type (A), l(3)012309 (B), pnt{triangleup}88 (C) and pntRR112 (D) embryos labeled for Mef2. (A) In wild-type embryos, the heart is formed by two single rows of cardioblasts that meet at the dorsal midline (white arrow). In embryos that contain a P element insert in pnt (B), a deletion of the pntP1 locus and the shared exons of pntP2 (C) or a mutation in the splice donor site of a pntP2-specific exon (D), ectopic cardioblasts develop and form enlarged hearts comprising disorganized rows of cardioblasts (arrows, B-D). Anterior is towards the left; white arrow indicates the dorsal midline.

 


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  		Fig. 3. pointed embryos exhibit a significant increase in Svp-positive cardioblasts. Dorsal views of stage 16 wild-type (A,B) and pnt (C,D) embryos labeled for Svp-lacZ (A,C), and Svp-lacZ and Mef-2 (B,D). (A,B) In wild-type embryos, 12 Svp-negative cardioblasts arise anterior to the first Svp-positive cardioblast (broken white line), seven of these cardioblasts are visible in A and B. Posterior to this location, there is a reiterative pattern of two Svp-lacZ positive cardioblasts (yellow/orange) and four Svp-lacZ negative cardioblasts (green) per hemisegment. (C,D) In pnt embryos, cardioblast development anterior to the first Svp-positive cardioblast (broken white line) appears normal. However, many ectopic cardioblasts are found posterior to this location and the majority of these cells express Svp-lacZ at high (arrow) or moderate levels (arrowhead). The broken white line separates the anterior heart domain from the posterior seven heart segments; anterior is towards the left.

 


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  		Fig. 4. pointed promotes pericardial cell development. Dorsal (A,B) and high magnification lateral (C,D) views of stage 16 (A,B) and early stage 13 (C,D) wild-type (A,C) and pnt (B,D) embryos labeled for ZFH1 to mark pericardial cells (A-C; red in C) and Mef2 (C,D; green). (A) In wild-type embryos, two bilateral stripes of pericardial cells (arrows) develop lateral to the cardioblasts (position of cardioblasts indicated by asterisks). (B) pnt embryos exhibit a severe reduction in pericardial cell number (arrows). (C) In early stage 13 wild-type embryos, pericardial cells (red cells; arrowheads) develop ventral and slightly interior to cardioblasts (green cells; arrows). (D) In early stage 13 pnt embryos, ectopic cardioblasts (arrowheads) arise in the location normally occupied by pericardial cells just ventral to the position of the endogenous cardioblasts (arrows). Anterior is towards the left.

 


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  		Fig. 5. PointedP2 is necessary and sufficient to repress cardioblast development. Dorsal whole heart views of stage 15 wild-type (A), PntP2 RNAi embryos (B-D) and pnt012309 embryos in which either pntP1 (E) or pntP2 (F) was expressed throughout the mesoderm labeled for Mef2 (A,B,D-F) or PntP1 (C). (A) Wild-type embryo showing the two bilateral rows of cardioblasts (arrows). (B) PntP2 RNAi-treated embryo exhibiting a significant increase in cardioblasts (arrows). (C,D) pntP2 RNAi-treated embryo double-labeled for pntP1 (C) and Mef2 (D). This embryo expresses PntP1 in essentially a wild-type pattern (C) and exhibits a significant increase in cardioblasts (arrows, D). (E) pnt012309 embryo in which pntP1 has been expressed ubiquitously throughout the mesoderm exhibits a drastic loss of cardioblasts (arrows indicate cardioblasts). (F) pnt012309 embryo in which PntP2 has been expressed ubiquitously throughout the mesoderm exhibits wild-type cardioblast development (arrows). Anterior is towards the left.

 


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  		Fig. 6. pannier promotes the development of all heart cells. Lateral views of stage 15 (A-F) and stage 11 (G-I) embryos as well as high-magnification dorsal views of stage 16 (J-L) embryos of the indicated genotypes labeled for the indicated proteins. (A) Wild-type embryo showing two bilateral rows of cardioblasts (arrow). (B) In pnr1 embryos, most cardioblasts do not develop, although short stretches of cardioblasts still arise in this background (arrow). (C) In pnrVX6 embryos, cardioblasts almost never develop (arrow indicates normal position of the cardioblast row). (D) Wild-type embryo showing one of the two bilateral rows of pericardial cells (arrow). (E) In pnr1 embryos, there is a strong decrease in pericardial cells (arrow). (F) pnrVX6 embryos exhibit a more severe loss of pericardial cells (arrow). (G) In wild-type embryos Tin expression marks the cardiac mesoderm (arrowheads) and the presumptive visceral mesoderm (arrows). In (H) pnr1 and (I) pnrVX6 embryos, Tin expression is almost completely absent from the cardiac mesoderm (arrowheads) but is essentially wild type in the visceral mesoderm. (J) Wild-type embryo labeled for Mef2 (green) and Svp-lacZ (red) showing the normal reiterative pattern of four Svp-lacZ negative cardioblasts and two Svp-lacZ positive cardioblasts per hemisegment. (K) pnr1 embryos retain the 2:1 ratio of Svp-lacZ-negative to Svp-lacZ-positive cardioblasts although the precise alignment of these cardioblasts is perturbed (arrowheads indicate cardioblasts). (L) pnr1 pnt012309 embryos exhibit localized overproduction of cardioblasts (arrowheads) and the majority of these cardioblasts express Svp-lacZ (yellow or orange cells). Broken white lines in K and L separate images taken from two different embryos of the indicated genotype. Anterior is towards the left.

 

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