An extracellular matrix protein promotes anillin-dependent processes in the Caenorhabditis elegans germline.

Hongxia Lan,Yu Chung Tse,Xinyan Wang,Ling Jiang,Xuan Wan,Lidan Zeng,Shian Wu,Yiyan Lin,Jianjian Wu,Dandan Zhang,Chunhui Hou

doi:10.26508/lsa.201800152

Abstract

Cell division requires constriction of an actomyosin ring to segregate the genetic material equally into two daughter cells. The spatial and temporal regulation of the contractile ring at the division plane primarily depends on intracellular signals mediated by the centralspindlin complex and astral microtubules. Although much investigative work has elucidated intracellular factors and mechanisms controlling this process, the extracellular regulation of cytokinesis remains unclear. Thus far, the extracellular matrix protein Hemicentin (HIM-4) has been proposed to be required for cleavage furrow stabilization. The underlying molecular mechanism, however, has remained largely unknown. Here, we show that HIM-4 and anillin (ANI-1) genetically act in the same pathway to maintain the rachis bridge stability in the germline. Our FRAP experiments further reveal that HIM-4 restricts the motility of ANI-1. In addition, we demonstrate that HIM-4 is recruited to the cleavage site in dividing germ cells and promotes the proper ingression of the cleavage membrane. Collectively, we propose that HIM-4 is an extracellular factor that regulates ANI-1 for germ cell membrane stabilization and contractile ring formation in Caenorhabditis elegans germline cells.

Highlights

The ECM is a tissue-specific assembly of molecules that reside and function outside of the cell
In this study, using C. elegans germline as a model system, we show that HIM-4 localizes to the rachis bridge and the cleavage plane of dividing germ cells, and this localization is necessary to recruit anillin (ANI-1)
Membrane retraction and resultant binucleation were observed in the meiotic transition zone cells (Fig 2A, cell iii and iv and Video 1). These results indicate that HIM-4 affects C. elegans germline compartmentation in both the mitotic and transition regions

Summary

Introduction

The ECM is a tissue-specific assembly of molecules that reside and function outside of the cell. Knockdown or targeted inactivation of Hemicentin-1 in mouse embryos caused membrane destabilization, cleavage furrow retraction, and cytokinesis failure, which resulted in a large number of embryos arrested at the one- to four-cell stage (Xu & Vogel, 2011b). These results indicate that HIM-4 is required for proper cytokinesis, perhaps with a direct role. Depletion of ANI-1 and HIM-4 phenocopies the single depletion of each for germline compartmentation, rachis bridge size, and cleavage furrow constriction rate of the dividing germ cells This suggests that HIM-4 regulates ANI-1 for membrane stabilization and contractile ring formation. Demonstrates that the ECM protein HIM-4 mediates two biological events: (1) stabilization of germ cell membrane and (2) promotion of contractile ring constriction

Results

Discussion

Experimental procedures