Kinesin-directed secretion of basement membrane proteins to a subdomain of the basolateral surface in Drosophila epithelial cells

Zajac, Allison L.; Horne‐Badovinac, Sally

doi:10.1016/j.cub.2021.12.025

Cited by 30 publications

(43 citation statements)

References 91 publications

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“…Given that epithelial cells express Dlg but not Inscuteable, the possibility that this rescue pathway is the default in epithelia is particularly attractive. We tested it in follicle cells using 1) flies transheterozygous for the null alleles Khc-73 149 and Khc-73 193 , 2) expression of Khc73 shRNA in the follicular epithelium; and 3) mitotic clones mutant for the null allele Khc73 3-3 (Liao et al, 2018; Zajac and Horne-Badovinac, 2022). Spindle angles were normal in all of these conditions (Figure 5A,C).…”

Section: Resultsmentioning

confidence: 99%

The spindle orienting machinery requires activation, not just localization

Neville

Finegan

Lowe

et al. 2022

Preprint

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The orientation of the mitotic spindle at metaphase determines the placement of the daughter cells. Spindle orientation in animals typically relies on an evolutionarily conserved biological machine comprised of at least four proteins - called Partner of Inscuteable (Pins), Gαi, Mushroom body defective (Mud), and Dynein in flies - that exert a pulling force on astral microtubules and reels the spindle into alignment. The canonical model for spindle orientation holds that the direction of pulling is determined by asymmetric placement of this machinery at the cell cortex. In most cell types, this placement is thought to be mediated by Pins, and a substantial body of literature is therefore devoted to identifying polarized cues that govern localized cortical enrichment of Pins. In Drosophila neuroblasts, for example, this cue is thought to be Inscuteable, which helps recruit Pins to the apical cell surface. In this study we revisit the canonical model. We find that spindle orientation in the follicular epithelium requires not only Pins localization but also activation, which relies on direct interaction between Pins and the multifunctional protein Discs large. This mechanism is distinct from the one mediated by Inscuteable, which we find also has an activating step. Together our results show that the canonical model is incomplete. Local enrichment of Pins is not sufficient to determine spindle orientation; an activation step is also necessary.

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Section: Resultsmentioning

confidence: 99%

The spindle orienting machinery requires activation, not just localization

Neville

Finegan

Lowe

et al. 2022

Preprint

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“…In several rod-shaped bacteria, the synthesis of peptidoglycans is guided by MreB, an actin homologue, following membrane curvature 10,11 and driving bacterial elongation. In Drosophila oocytes, microtubules guide the polar secretion of collagen in the surrounding epithelium 8,9 . Collagen deposition is associated with a global rotation of the oocyte inside the matrix, which yields a circumferential arrangement of fibrils and a mechanically anisotropic extracellular matrix, which is required for oocyte elongation 7,12 .…”

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

“…more growth along one axis of the organ. Elongated forms may result from coordinated cell rearrangements such as intercalation 1,2 , from patterned heterogeneity in the physical properties of cells [3][4][5][6] , or from guidance of growth by a matrix surrounding cells or tissues, usually a material reinforced by fibrils [7][8][9] . Here, we consider the link between fibril arrangement and elongation.…”

Section: Introductionmentioning

confidence: 99%

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Spatial consistency of cell growth direction during organ morphogenesis requires CELLULOSE-SYNTHASE INTERACTIVE1

Mollier

Skrzydeł

Borowska-Wykręt

et al. 2022

Preprint

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Extracellular matrices generally contain fibril-like polymers that may be organized in parallel arrays. Although their role in morphogenesis has been recognized, it is still unclear how the subcellular control of fibril synthesis translates into well-defined organ shape. Here, we addressed this question using the Arabidopsis sepal as a model organ. In plants, cell growth is driven by turgor pressure and restrained by the extracellular matrix known as the cell wall. Cellulose is the main load-bearing component of the plant cell wall and cellulose microfibrils are thought to channel growth perpendicularly to their main orientation. We investigated the role of the guidance of cellulose synthesis by CELLULOSE SYNTHASE INTERACTIVE 1 (CSI1) in sepal morphogenesis. We observed that sepals are shorter in csi1 mutants, although the newest cellulose microfibrils are more aligned in csi1. Surprisingly, cell growth anisotropy was similar in csi1 and wild-type plants. We resolved this apparent paradox using polarized Raman microspectroscopy and live imaging of growing sepals. We found that CSI1 is required for spatial consistency of growth direction across the sepal and for the maintenance of overall organ elongation. We confirmed our conclusions at sepal scale, notably using bespoke mechanical assays. Our work illustrates how the subcellular regulation of the extracellular matrix may control morphogenesis at multiple scales.

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“…The follicle cells migrate as a collective orthogonal to the anterior-posterior axis of the egg chamber, spinning the egg chamber along its axis as the follicle cells secrete proteins that reinforce the nascent basement membrane. The result of this tissue behavior is a polarized basement membrane that coils around the egg chamber like thread on a spool, which helps the egg achieve its final elongated shape (Haigo and Bilder, 2011; Isabella and Horne-Badovinac, 2016; Lerner et al, 2013; Zajac and Horne-Badovinac, 2022).…”

Section: Introductionmentioning

confidence: 99%

Rap1 promotes epithelial integrity and cell viability in a growing tissue

Messer

McDonald

2022

Preprint

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Having intact epithelial tissues is critical for embryonic development and adult homeostasis. How epithelia respond to damaging insults or tissue growth while still maintaining intercellular connections and barrier integrity during development is poorly understood. The conserved small GTPase Rap1 is critical for establishing cell polarity and regulating cadherin-catenin cell junctions. Here, we identified a new role for Rap1 in maintaining epithelial integrity and tissue shape of a growing tissue, theDrosophilaegg chamber during oogenesis. Loss of Rap1 activity disrupted the follicle cell epithelium and shape of egg chambers. While Rap1 did not control the localization of non-muscle myosin II (Myo-II), it was required for the apical enrichment of E-Cadherin in some cells. Both Myo-II and the adherens junction-cytoskeletal linker protein α-Catenin were required for normal egg chamber shape. Further, we found that Rap1 promoted epithelial cell survival. Follicle cells deficient for Rap1 had increased caspase activity and underwent apoptosis. Loss of Myo-II did not affect cell survival, though loss of α-Catenin resulted in a mild increase in cells undergoing apoptosis. Blocking the apoptotic cascade failed to rescue the cell shape defects caused by Rap1inhibition. One consequence of increased cell death caused by Rap1 inhibition was the preferential loss of the polar cells, which later in development led to fewer cells forming a properly migrating border cell cluster. Our results thus indicate dual roles for Rap1 in controlling epithelial morphogenesis and cell survival of a growing tissue during development.

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Kinesin-directed secretion of basement membrane proteins to a subdomain of the basolateral surface in Drosophila epithelial cells

Cited by 30 publications

References 91 publications

The spindle orienting machinery requires activation, not just localization

The spindle orienting machinery requires activation, not just localization

Spatial consistency of cell growth direction during organ morphogenesis requires CELLULOSE-SYNTHASE INTERACTIVE1

Rap1 promotes epithelial integrity and cell viability in a growing tissue

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