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

Acaimo González-Reyes,Kristian Franze,María D. Martín-Bermudo,María C. Díaz de la Loza,Alfonsa Díaz-Torres,Alicia E. Rosales-Nieves,Emad Moeendarbary,Federico Zurita

doi:10.1016/j.celrep.2017.06.031

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.

Highlights

Basement membranes (BMs) are specialized types of extracellular matrix (ECM) that coat the basal side of epithelial and endothelial tissues, surround muscles and fat cells, and play an active role in tissue and organ morphogenesis (Morrissey and Sherwood, 2015)
Basement 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

Summary

Introduction

Basement membranes (BMs) are specialized types of extracellular matrix (ECM) that coat the basal side of epithelial and endothelial tissues, surround muscles and fat cells, and play an active role in tissue and organ morphogenesis (Morrissey and Sherwood, 2015). The oocyte is placed posterior to the nurse cells, a step necessary to polarize the developing egg chamber and to allow proper egg fertilization in the final stages of oogenesis (Gonzalez-Reyes et al, 1997). Follicle elongation is generally linked to FC collective migration, a process termed ‘‘global tissue rotation’’ (Cetera et al, 2014; Gates, 2012; Haigo and Bilder, 2011). During this process, FCs project lamellipodia so that the entire egg chamber rotates in a circular trajectory perpendicular to the AP axis without a discernable leading edge and without affecting the AP alignment of follicles. Rotation is accompanied by the polarized secretion of new ECM material, part of which is eventually deposited in fibrils oriented

Results

Discussion

Conclusion