Tension modulation of actomyosin ring assembly and RhoGTPases activity: Perspectives from the Xenopus oocyte wound healing model

Abstract

Cells are remarkably resilient structures; they are able to recover from injuries to their plasma membrane (PM) and cytoskeleton that would normally constitute existential threats. This capacity is exemplified by Xenopus laevis oocytes which can recover from very large PM defects through exocytotic and endocytic events and can repair damaged cortical cytoskeleton structures through the formation of a contractile actomyosin ring (AMR). Formation of the AMR involves the localized Ca2+ -dependent activation of RhoA and Cdc42, and the pre-patterning of guanine nucleotide exchange factors (GEFs) and GTPase-activating proteins (GAPs). However, this model fails to account for observations that suggest a link between cytoskeletal dynamics, intracellular tension, and AMR formation. It also does not explain why the formation of an AMR is not involved in the cytoskeletal repair program of adherent cells. We show here evidence for the support of tension as an essential regulatory signal for the formation of AMR. Indeed, oocytes in which global tension has been experimentally reduced were unable to form a functional AMR following injury, showing severely diminished RhoA activity at the wound site. These new insights place the cytoskeleton at the center of events involving changes in cell shape such as cytokinesis which also involves the formation and closure of an AMR.