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Role of kinesin heavy chain in Crumbs localization along the rhabdomere elongation in Drosophila photoreceptor.

League GP, Nam SC - PLoS ONE (2011)

Bottom Line: Because a genetic interaction was found between crb and khc, Crb localization was examined in the developing photoreceptors of khc mutants. khc was dispensable during early eye differentiation and development.In summary, we examined the role of khc in the regulation of the apical Crb domain in developing photoreceptors.Since the rhabdomeres in developing pupal eyes grow along the distal-proximal axis, these phenotypes suggest that Khc is essential for the microtubule structures and apical membrane domains during the distal-proximal elongation of photoreceptors, but is dispensable for early eye development.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Baylor University, Waco, Texas, United States of America.

ABSTRACT

Background: Crumbs (Crb), a cell polarity gene, has been shown to provide a positional cue for the extension of the apical membrane domain, adherens junction (AJ), and rhabdomere along the growing proximal-distal axis during Drosophila photoreceptor morphogenesis. In developing Drosophila photoreceptors, a stabilized microtubule structure was discovered and its presence was linked to polarity protein localization. It was therefore hypothesized that the microtubules may provide trafficking routes for the polarity proteins during photoreceptor morphogenesis. This study has examined whether Kinesin heavy chain (Khc), a subunit of the microtubule-based motor Kinesin-1, is essential in polarity protein localization in developing photoreceptors.

Methodology/principal findings: Because a genetic interaction was found between crb and khc, Crb localization was examined in the developing photoreceptors of khc mutants. khc was dispensable during early eye differentiation and development. However, khc mutant photoreceptors showed a range of abnormalities in the apical membrane domain depending on the position along the proximal-distal axis in pupal photoreceptors. The khc mutant showed a progressive mislocalization in the apical domain along the distal-proximal axis during rhabdomere elongation. The khc mutation also led to a similar progressive defect in the stabilized microtubule structures, strongly suggesting that Khc is essential for microtubule structure and Crb localization during distal to proximal rhabdomere elongation in pupal morphogenesis. This role of Khc in apical domain control was further supported by khc's gain-of-function phenotype. Khc overexpression in photoreceptors caused disruption of the apical membrane domain and the stabilized microtubules in the developing photoreceptors.

Conclusions/significance: In summary, we examined the role of khc in the regulation of the apical Crb domain in developing photoreceptors. Since the rhabdomeres in developing pupal eyes grow along the distal-proximal axis, these phenotypes suggest that Khc is essential for the microtubule structures and apical membrane domains during the distal-proximal elongation of photoreceptors, but is dispensable for early eye development.

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Acetylated microtubules of Drosophila pupal photoreceptors.(A) Side view of developing photoreceptors at mid-stage pupal development. The photoreceptors elongate along the distal-proximal axis (arrow). (B) Cross-section of mid-stage pupal photoreceptors. Apical domain (green) localizes apical to AJ (red) in the center of a photoreceptor cluster. E-cad localizes at AJ (red), which are more basal to the apical domain. The acetylated-tubulin (blue) localizes just basal to the AJs (red) and the basolateral domains (black) are more basal to both the AJ (red) and the acetylated-tubulin (blue).
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pone-0021218-g001: Acetylated microtubules of Drosophila pupal photoreceptors.(A) Side view of developing photoreceptors at mid-stage pupal development. The photoreceptors elongate along the distal-proximal axis (arrow). (B) Cross-section of mid-stage pupal photoreceptors. Apical domain (green) localizes apical to AJ (red) in the center of a photoreceptor cluster. E-cad localizes at AJ (red), which are more basal to the apical domain. The acetylated-tubulin (blue) localizes just basal to the AJs (red) and the basolateral domains (black) are more basal to both the AJ (red) and the acetylated-tubulin (blue).

Mentions: The compound eye of Drosophila is made up of about 800 ommatidia, each of which is comprised of a cluster of eight elongated columnar photoreceptor cells covered by a thin layer of pigment cells [1], [2]. These clusters of 8 photoreceptor cells (R1–R8) are made in the eye disc epithelium during the third instar larval stage, before photoreceptor morphogenesis takes place. Along the length of each ommatidial column extends a light sensitive, tightly packed array of 60,000 microvilli called a rhabdomere [1], [2], [3]. At 37% pupal development (pd) stage, the apical region of each of the photoreceptor cells is involuted by 90°, reorienting the apical domains towards the center of the cluster (Fig. 1) [1], [2]. At this time, the apical membrane domain, having been localized at the center of the photoreceptor cluster, is now surrounded immediately by the AJs, followed by the basolateral domains (Fig. 1) [4], [5]. The formation of the rhabdomere from the apical surface of the photoreceptor cells begins at 55% pd and involves a series of complex cell-cell signaling interactions and the rapid expansion of the plasma membrane [1], [2], [3]. Because of the enormity of this extension and the rapidity with which it occurs, even small signaling defects can cause dramatic phenotypic consequences in the developing eye.


Role of kinesin heavy chain in Crumbs localization along the rhabdomere elongation in Drosophila photoreceptor.

League GP, Nam SC - PLoS ONE (2011)

Acetylated microtubules of Drosophila pupal photoreceptors.(A) Side view of developing photoreceptors at mid-stage pupal development. The photoreceptors elongate along the distal-proximal axis (arrow). (B) Cross-section of mid-stage pupal photoreceptors. Apical domain (green) localizes apical to AJ (red) in the center of a photoreceptor cluster. E-cad localizes at AJ (red), which are more basal to the apical domain. The acetylated-tubulin (blue) localizes just basal to the AJs (red) and the basolateral domains (black) are more basal to both the AJ (red) and the acetylated-tubulin (blue).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3117887&req=5

pone-0021218-g001: Acetylated microtubules of Drosophila pupal photoreceptors.(A) Side view of developing photoreceptors at mid-stage pupal development. The photoreceptors elongate along the distal-proximal axis (arrow). (B) Cross-section of mid-stage pupal photoreceptors. Apical domain (green) localizes apical to AJ (red) in the center of a photoreceptor cluster. E-cad localizes at AJ (red), which are more basal to the apical domain. The acetylated-tubulin (blue) localizes just basal to the AJs (red) and the basolateral domains (black) are more basal to both the AJ (red) and the acetylated-tubulin (blue).
Mentions: The compound eye of Drosophila is made up of about 800 ommatidia, each of which is comprised of a cluster of eight elongated columnar photoreceptor cells covered by a thin layer of pigment cells [1], [2]. These clusters of 8 photoreceptor cells (R1–R8) are made in the eye disc epithelium during the third instar larval stage, before photoreceptor morphogenesis takes place. Along the length of each ommatidial column extends a light sensitive, tightly packed array of 60,000 microvilli called a rhabdomere [1], [2], [3]. At 37% pupal development (pd) stage, the apical region of each of the photoreceptor cells is involuted by 90°, reorienting the apical domains towards the center of the cluster (Fig. 1) [1], [2]. At this time, the apical membrane domain, having been localized at the center of the photoreceptor cluster, is now surrounded immediately by the AJs, followed by the basolateral domains (Fig. 1) [4], [5]. The formation of the rhabdomere from the apical surface of the photoreceptor cells begins at 55% pd and involves a series of complex cell-cell signaling interactions and the rapid expansion of the plasma membrane [1], [2], [3]. Because of the enormity of this extension and the rapidity with which it occurs, even small signaling defects can cause dramatic phenotypic consequences in the developing eye.

Bottom Line: Because a genetic interaction was found between crb and khc, Crb localization was examined in the developing photoreceptors of khc mutants. khc was dispensable during early eye differentiation and development.In summary, we examined the role of khc in the regulation of the apical Crb domain in developing photoreceptors.Since the rhabdomeres in developing pupal eyes grow along the distal-proximal axis, these phenotypes suggest that Khc is essential for the microtubule structures and apical membrane domains during the distal-proximal elongation of photoreceptors, but is dispensable for early eye development.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Baylor University, Waco, Texas, United States of America.

ABSTRACT

Background: Crumbs (Crb), a cell polarity gene, has been shown to provide a positional cue for the extension of the apical membrane domain, adherens junction (AJ), and rhabdomere along the growing proximal-distal axis during Drosophila photoreceptor morphogenesis. In developing Drosophila photoreceptors, a stabilized microtubule structure was discovered and its presence was linked to polarity protein localization. It was therefore hypothesized that the microtubules may provide trafficking routes for the polarity proteins during photoreceptor morphogenesis. This study has examined whether Kinesin heavy chain (Khc), a subunit of the microtubule-based motor Kinesin-1, is essential in polarity protein localization in developing photoreceptors.

Methodology/principal findings: Because a genetic interaction was found between crb and khc, Crb localization was examined in the developing photoreceptors of khc mutants. khc was dispensable during early eye differentiation and development. However, khc mutant photoreceptors showed a range of abnormalities in the apical membrane domain depending on the position along the proximal-distal axis in pupal photoreceptors. The khc mutant showed a progressive mislocalization in the apical domain along the distal-proximal axis during rhabdomere elongation. The khc mutation also led to a similar progressive defect in the stabilized microtubule structures, strongly suggesting that Khc is essential for microtubule structure and Crb localization during distal to proximal rhabdomere elongation in pupal morphogenesis. This role of Khc in apical domain control was further supported by khc's gain-of-function phenotype. Khc overexpression in photoreceptors caused disruption of the apical membrane domain and the stabilized microtubules in the developing photoreceptors.

Conclusions/significance: In summary, we examined the role of khc in the regulation of the apical Crb domain in developing photoreceptors. Since the rhabdomeres in developing pupal eyes grow along the distal-proximal axis, these phenotypes suggest that Khc is essential for the microtubule structures and apical membrane domains during the distal-proximal elongation of photoreceptors, but is dispensable for early eye development.

Show MeSH
Related in: MedlinePlus