An Axon-Pathfinding Mechanism Preserves Epithelial Tissue Integrity

Cammarota, Christian; Finegan, Tara M.; Wilson, Tyler J.; Yang, Sifan; Bergstralh, Daniel T.

doi:10.1016/j.cub.2020.09.061

Cited by 21 publications

(48 citation statements)

References 66 publications

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“…It has been shown that, similar to Dg, integrins play important roles during brain morphogenesis, and defects in their functions result in the development of congenital muscular dystrophies ( Barraza-Flores et al, 2020 ). The other factors critical for nervous system development are the cadherin family and the immunoglobulin-related superfamily of cell adhesion molecules, NCAMs ( Cammarota et al, 2020 ; Dumstrei et al, 2003 ; Fung et al, 2009 ; Neuert et al, 2020 ). Cadherins connect cells with each other via adherens junctions, while NCAMs act as neuronal recognition molecules in the regulation of selective axon fasciculation.…”

Section: Resultsmentioning

confidence: 99%

Exocyst-mediated membrane trafficking of the lissencephaly-associated ECM receptor dystroglycan is required for proper brain compartmentalization

Yatsenko

Kucherenko

Xie

et al. 2021

eLife

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To assemble a brain, differentiating neurons must make proper connections and establish specialized brain compartments. Abnormal levels of cell adhesion molecules disrupt these processes. Dystroglycan (Dg) is a major non-integrin cell adhesion receptor, deregulation of which is associated with dramatic neuroanatomical defects such as lissencephaly type II, or cobblestone brain. The previously established Drosophila model for cobblestone encephaly was used to understand how Dg is regulated in the brain. During development, Dg has a spatiotemporally dynamic expression pattern, fine-tuning of which is crucial for accurate brain assembly. In addition, mass spectrometry analyses identified numerous components associated with Dg in neurons, including several proteins of the exocyst complex. Data show that exocyst-based membrane trafficking of Dg allows its distinct expression pattern, essential for proper brain morphogenesis. Further studies of the Dg neuronal interactome will allow identification of new factors involved in the development of dystroglycanopathies and advance disease diagnostics in humans.

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Section: Resultsmentioning

confidence: 99%

Exocyst-mediated membrane trafficking of the lissencephaly-associated ECM receptor dystroglycan is required for proper brain compartmentalization

Yatsenko

Kucherenko

Xie

et al. 2021

eLife

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“…adhaerens, which contain epithelial cells but not neural, strongly suggests that the epithelial pathway was co-opted for axon growth and pathfinding when nervous tissue evolved from epithelia (Cammarota et al, 2020).…”

Section: The Interaction Between Dlg and Pins/lgn/gpsm2 May Be Required For Proper Neural But Not Epithelial Tissue Developmentmentioning

confidence: 99%

Interaction between Discs large and Pins/LGN/GPSM2: a comparison across species

Schiller

Bergstralh

2021

Biology Open

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The orientation of the mitotic spindle determines the direction of cell division, and therefore contributes to tissue shape and cell fate. Interaction between the multifunctional scaffolding protein Discs large (Dlg) and the canonical spindle orienting factor GPSM2 (called Pins in Drosophila and LGN in vertebrates) has been established in bilaterian models, but its function remains unclear. We used a phylogenetic approach to test whether the interaction is obligate in animals, and in particular whether Pins/LGN/GPSM2 evolved in multicellular organisms as a Dlg-binding protein. We show that Dlg diverged in C. elegans and the syncytial sponge O. minuta and propose that this divergence may correspond to differences in spindle orientation requirements between these organisms and the canonical pathways described in bilaterians. We also demonstrate that Pins/LGN/GPSM2 is present in basal animals, but the established Dlg-interaction site cannot be found in either Placozoa or Porifera. Our results suggest that the interaction between Pins/LGN/GPSM2 and Dlg appeared in Cnidaria, and we therefore speculate that it may have evolved to promote accurate division orientation in the nervous system. This work reveals the evolutionary history of the Pins/LGN/GPSM2-Dlg interaction and suggests new possibilities for its importance in spindle orientation during epithelial and neural tissue development.

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“…Both proteins are immunoglobulin-containing adhesion molecules, and act synergistically through a mechanism that seeks to maximize cell-cell adhesion along the lateral membrane. Full activity also requires the cytoplasmic domain of Nrg that interacts with the cytoskeletal-membrane linker protein Ankyrin [ 111 ]. Notably, this process does not happen in the imaginal disc epithelium, where instead misoriented divisions lead to basal extrusion and cell death [ 112 ].…”

Section: Cellular Functions Of Sj Genesmentioning

confidence: 99%

“…One key difference between these developmental contexts is that in the early embryonic ectoderm and early-stage follicular epithelium (cell divisions cease in stage 6 egg chambers), SJs have not formed and Nrg and FasII are strongly expressed all along the lateral membrane, whereas the SJ has formed and these proteins are tightly linked to the apical lateral junction in imaginal tissues. Interestingly, reintegration (at least in the follicular epithelium) does not appear to require the full complement of SJ proteins, as knockdown of Nrx-IV does not lead to reintegration failure [ 111 ].…”

Section: Cellular Functions Of Sj Genesmentioning

confidence: 99%

Expanding the Junction: New Insights into Non-Occluding Roles for Septate Junction Proteins during Development

Rice

Alhadyian

et al. 2021

JDB

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The septate junction (SJ) provides an occluding function for epithelial tissues in invertebrate organisms. This ability to seal the paracellular route between cells allows internal tissues to create unique compartments for organ function and endows the epidermis with a barrier function to restrict the passage of pathogens. Over the past twenty-five years, numerous investigators have identified more than 30 proteins that are required for the formation or maintenance of the SJs in Drosophila melanogaster, and have determined many of the steps involved in the biogenesis of the junction. Along the way, it has become clear that SJ proteins are also required for a number of developmental events that occur throughout the life of the organism. Many of these developmental events occur prior to the formation of the occluding junction, suggesting that SJ proteins possess non-occluding functions. In this review, we will describe the composition of SJs, taking note of which proteins are core components of the junction versus resident or accessory proteins, and the steps involved in the biogenesis of the junction. We will then elaborate on the functions that core SJ proteins likely play outside of their role in forming the occluding junction and describe studies that provide some cell biological perspectives that are beginning to provide mechanistic understanding of how these proteins function in developmental contexts.

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An Axon-Pathfinding Mechanism Preserves Epithelial Tissue Integrity

Cited by 21 publications

References 66 publications

Exocyst-mediated membrane trafficking of the lissencephaly-associated ECM receptor dystroglycan is required for proper brain compartmentalization

Exocyst-mediated membrane trafficking of the lissencephaly-associated ECM receptor dystroglycan is required for proper brain compartmentalization

Interaction between Discs large and Pins/LGN/GPSM2: a comparison across species

Expanding the Junction: New Insights into Non-Occluding Roles for Septate Junction Proteins during Development

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