Abstract
The spectrin cytoskeleton crosslinks actin to the membrane, and although it has been greatly studied in erythrocytes, much is unknown about its function in epithelia. We have studied the role of spectrins during epithelia morphogenesis using the Drosophila follicular epithelium (FE). As previously described, we show that α-Spectrin and β-Spectrin are essential to maintain a monolayered FE, but, contrary to previous work, spectrins are not required to control proliferation. Furthermore, spectrin mutant cells show differentiation and polarity defects only in the ectopic layers of stratified epithelia, similar to integrin mutants. Our results identify α-Spectrin and integrins as novel regulators of apical constriction-independent cell elongation, as α-Spectrin and integrin mutant cells fail to columnarize. Finally, we show that increasing and reducing the activity of the Rho1-Myosin II pathway enhances and decreases multilayering of α-Spectrin cells, respectively. Similarly, higher Myosin II activity enhances the integrin multilayering phenotype. This work identifies a primary role for α-Spectrin in controlling cell shape, perhaps by modulating actomyosin. In summary, we suggest that a functional spectrin-integrin complex is essential to balance adequate forces, in order to maintain a monolayered epithelium.
Highlights
Monolayered epithelia are sheets of adherent, polarized cells that act as physical barriers and constitute structural components of organs and tissues
Fasciclin 3 (Fas3) is expressed at high levels in immature FCs, but its expression becomes gradually restricted to the polar cells as oogenesis proceeds (Bai, 2002; Muzzopappa and Wappner, 2005) (Fig. 1Ai), whereas Hnt is upregulated from S6 (Sun and Deng, 2007)
In all cases, the defects are only observed in α-Spec cells located in the ectopic layers of the multilayered epithelium (Fig. 1A,C), and not in mutant cells that are either adjacent to the oocyte (Fig. 1Aiii, yellow arrow) or forming a monolayer (Fig. 5)
Summary
Monolayered epithelia are sheets of adherent, polarized cells that act as physical barriers and constitute structural components of organs and tissues. Loss of epithelial architecture leads to the formation of multilayered epithelia, disorganized cell masses and increased tumorigenic potential. Each egg chamber is composed of 16 germline cells (including the oocyte), and a layer of somatic cells (the follicle cells, FCs) forming a monolayered epithelium termed the follicular epithelium (FE) (Fig. 1A). The factors important for formation of a monolayered FE are not yet fully understood, but mutations in genes controlling polarity and mitosis lead to FE multilayering, such as aPKC (Abdelilah-Seyfried et al, 2003), Notch and the Hippo pathway (Meignin et al, 2007; Polesello and Tapon, 2007; Yu et al, 2008). Integrins and spectrins (Spec) are important for maintaining a monolayer
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