Laminin Levels Regulate Tissue Migration and Anterior-Posterior Polarity during Egg Morphogenesis in Drosophila

Abstract

SummaryBasement membranes (BMs) are specialized extracellular matrices required for tissue organization and organ formation. We study the role of laminin and its integrin receptor in the regulation of tissue migration during Drosophila oogenesis. Egg production in Drosophila involves the collective migration of follicle cells (FCs) over the BM to shape the mature egg. We show that laminin content in the BM increases with time, whereas integrin amounts in FCs do not vary significantly. Manipulation of integrin and laminin levels reveals that a dynamic balance of integrin-laminin amounts determines the onset and speed of FC migration. Thus, the interplay of ligand-receptor levels regulates tissue migration in vivo. Laminin depletion also affects the ultrastructure and biophysical properties of the BM and results in anterior-posterior misorientation of developing follicles. Laminin emerges as a key player in the regulation of collective cell migration, tissue stiffness, and the organization of anterior-posterior polarity in Drosophila.

The genetics of egg retention and fertilization success inDrosophila: One step closer to understanding the transition from facultative to obligate viviparity

“…Laminins have been found to be necessary for tissue morphogenesis (reviewed in Miner and Yurchenco ) and function in developmental processes such as egg chamber elongation, egg shape determination (Andersen and Horne‐Badovinac ), cell migration, induction, and maintenance of cell polarity (Diaz de la Loza et al. ) and glial cell development (Yu et al. ; Petley‐Ragan et al.…”

“…Ovaries of LanB2 depleted mutant flies contain aberrant follicle cells and rounded eggs (Diaz de la Loza et al. ), which might have an impact on egg laying rate and thus egg retention. We further found that 5/15 associated genes have highest adult expression in ovaries (Table S3A, B), and are functioning as early gene expression regulators ( vfl ), in repair mechanisms ( spel1 ), and oligosaccharide biosynthesis ( Pgant35A ).…”

“…Laminins are protein constituents of the extracellular matrix in all metazoans, with most forms being essential for embryonic development (Smyth et al 1999;Urbano et al 2009). A recent study in Drosophila showed that the onset and rate of follicle cell migration in the ovary was determined by the level of laminins in the extracellular matrix (Diaz de la Loza et al 2017). Alteration of follicle cell migration, while directly impacting egg morphology, could potentially also impact the rate of egg maturation in the ovaries, thereby affecting the egg-laying rate.…”

Gradient in cytoplasmic pressure in the germline cells controls overlying epithelial cell morphogenesis

“…Several studies have shown the importance of the BM membrane structure and stiffness to elongate the follicle and the egg (Denef et al, 2008;Díaz de la Loza et al, 2017;Haigo and Bilder, 2011;He et al, 2010;Horne-Badovinac, 2015, 2016;Lerner et al, 2013;Schneider et al, 2006;Viktorinová and Dahmann, 2013). Two non-exclusive models have been proposed.…”

In-silicodefinition of theDrosophila melanogastermatrisome

“…BM is an ancient and highly conserved ECM that lines the basal surface of epithelial and endothelial tissues and surrounds muscles, adipose tissue, and nerves [26, 28,29]. Studies using Drosophila have made particularly strong contributions to our understanding of BM secretion and assembly [30][31][32][33][34][35][36][37][38][39][40][41][42][43][44][45], and the role BMs play in shaping tissues during development [35,42,[46][47][48][49][50][51][52][53]. They have also shown how BMs heal after injury [54,55] and how they regulate the immune response [56][57][58][59][60].…”