The basement membrane is a thin but dense, sheet-like specialized type of extracellular matrix that has remarkably diverse functions tailored to individual tissues and organs. Tightly controlled spatial and temporal changes in its composition and structure contribute to the diversity of basement membrane functions. These different basement membranes undergo dynamic transformations throughout animal life, most notably during development. Numerous developmental mechanisms are regulated or mediated by basement membranes, often by a combination of molecular and mechanical processes. A particularly important process involves cell transmigration through a basement membrane because of its link to cell invasion in disease. While developmental and disease processes share some similarities, what clearly distinguishes the two is dysregulation of cells and extracellular matrices in disease. With its relevance to many developmental and disease processes, the basement membrane is a vitally important area of research that may provide novel insights into biological mechanisms and development of innovative therapeutic approaches. Here we present a review of developmental and disease dynamics of basement membranes in Caenorhabditis elegans, Drosophila, and vertebrates.

/pdf/basement-membranes-in-development-and-disease-1ba39cl6ni.pdf

Basement Membranes in Development and Disease.

Highly regulated cell migration events are crucial during animal tissue formation and the trafficking of cells to sites of infection and injury. Misregulation of cell movement underlies numerous human diseases, including cancer. Although originally studied primarily in two-dimensional in vitro assays, most cell migrations in vivo occur in complex three-dimensional tissue environments that are difficult to recapitulate in cell culture or ex vivo Further, it is now known that cells can mobilize a diverse repertoire of migration modes and subcellular structures to move through and around tissues. This review provides an overview of three distinct cellular movement events in Caenorhabditis elegans-cell invasion through basement membrane, leader cell migration during organ formation, and individual cell migration around tissues-which together illustrate powerful experimental models of diverse modes of movement in vivo We discuss new insights into migration that are emerging from these in vivo studies and important future directions toward understanding the remarkable and assorted ways that cells move in animals.

https://www.genetics.org/content/genetics/208/1/53.full.pdf

Invading, Leading and Navigating Cells in Caenorhabditis elegans: Insights into Cell Movement in Vivo.

Cell invasion through basement membrane (BM) barriers is crucial in development, leukocyte trafficking and the spread of cancer. The mechanisms that direct invasion, despite their importance in normal and disease states, are poorly understood, largely because of the inability to visualize dynamic cell-BM interactions in vivo. This protocol describes multichannel time-lapse confocal imaging of anchor-cell invasion in live Caenorhabditis elegans. Methods presented include outline-slide preparation and worm growth synchronization (15 min), mounting (20 min), image acquisition (20-180 min), image processing (20 min) and quantitative analysis (variable timing). The acquired images enable direct measurement of invasive dynamics including formation of invadopodia and cell-membrane protrusions, and removal of BM. This protocol can be combined with genetic analysis, molecular-activity probes and optogenetic approaches to uncover the molecular mechanisms underlying cell invasion. These methods can also be readily adapted by any worm laboratory for real-time analysis of cell migration, BM turnover and cell-membrane dynamics.

/pdf/live-cell-confocal-microscopy-and-quantitative-4d-image-1kppstjw4x.pdf

Live-cell confocal microscopy and quantitative 4D image analysis of anchor-cell invasion through the basement membrane in Caenorhabditis elegans.

Biological tubes must develop and maintain their proper diameter to transport materials efficiently. These tubes are molded and protected in part by apical extracellular matrices (aECMs) that line their lumens. Despite their importance, aECMs are difficult to image in vivo and therefore poorly understood. The Caenorhabditis elegans vulva has been a paradigm for understanding many aspects of organogenesis. Here we describe the vulva luminal matrix, which contains chondroitin proteoglycans, Zona Pellucida (ZP) domain proteins, and other glycoproteins and lipid transporters related to those in mammals. Confocal and transmission electron microscopy revealed, with unprecedented detail, a complex and dynamic aECM. Different matrix factors assemble on the apical surfaces of each vulva cell type, with clear distinctions seen between Ras-dependent (1°) and Notch-dependent (2°) cell types. Genetic perturbations suggest that chondroitin and other aECM factors together generate a structured scaffold that both expands and constricts lumen shape.

A multi-layered and dynamic apical extracellular matrix shapes the vulva lumen in Caenorhabditis elegans.

Breaking down barriers: the evolution of cell invasion.

Epithelial cells and their underlying basement membranes (BMs) slide along each other to renew epithelia, shape organs, and enlarge BM openings. How BM sliding is controlled, however, is poorly understood. Using genetic and live cell imaging approaches during uterine-vulval attachment in C. elegans, we have discovered that the invasive uterine anchor cell activates Notch signaling in neighboring uterine cells at the boundary of the BM gap through which it invades to promote BM sliding. Through an RNAi screen, we found that Notch activation upregulates expression of ctg-1, which encodes a Sec14-GOLD protein, a member of the Sec14 phosphatidylinositol-transfer protein superfamily that is implicated in vesicle trafficking. Through photobleaching, targeted knockdown, and cell-specific rescue, our results suggest that CTG-1 restricts BM adhesion receptor DGN-1 (dystroglycan) trafficking to the cell-BM interface, which promotes BM sliding. Together, these studies reveal a new morphogenetic signaling pathway that controls BM sliding to remodel tissues.

Boundary cells restrict dystroglycan trafficking to control basement membrane sliding during tissue remodeling

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Boundary cells restrict dystroglycan trafficking to control basement membrane sliding during tissue remodeling