C‐Jun N‐terminal Kinase (JNK) maintains tissue integrity during cell rearrangement in the gut

Abstract

Tissue elongation is a fundamental morphogenetic process that generates the proper anatomical topology of the body plan and vital organs. In vertebrates, c‐Jun N‐terminal Kinase (JNK) is a downstream effector of Wnt/PCP signaling that is required for tissue elongation, but the precise cellular role of JNK in this context has remained elusive. Here, we show that JNK activity is indispensable for the rearrangement of endoderm cells that underlies the elongation of the Xenopus gut tube. Whereas other Wnt/PCP mediators, such as Rho, are necessary to induce cell intercalation and remodel adhesive contacts, we found that JNK is required to maintain cell‐cell adhesion and establish parallel microtubule arrays; without JNK activity, the reorganizing endoderm dissociates. Depleting microtubules phenocopies JNK inhibition, consistent with a model in which JNK regulates microtubule architecture to preserve adhesive contacts between rearranging cells. Thus, in contrast to Rho, which generates actomyosin‐based tension and cell movement, JNK signaling is required to establish cytoskeletal stability and maintain tissue cohesion; both factors are required to achieve proper cell rearrangement and gut extension. Our results shed new light on the means by which intra‐ and intercellular forces are balanced to promote topological change, while preserving structural integrity, in numerous morphogenetic contexts.