Tissue/planar cell polarity in vertebrates: new insights and new questions

Abstract

This review focuses on the tissue/planar cell polarity (PCP) pathway and its role in generating spatial patterns in vertebrates. Current evidence suggests that PCP integrates both global and local signals to orient diverse structures with respect to the body axes. Interestingly, the system acts on both subcellular structures, such as hair bundles in auditory and vestibular sensory neurons, and multicellular structures, such as hair follicles. Recent work has shown that intriguing connections exist between the PCP-based orienting system and left-right asymmetry, as well as between the oriented cell movements required for neural tube closure and tubulogenesis. Studies in mice, frogs and zebrafish have revealed that similarities, as well as differences, exist between PCP in Drosophila and vertebrates. IntroductionThe genetic and molecular dissection of what is now referred to as planar cell polarity (PCP) began 25 years ago with the realization by Gubb and Garcia-Bellido (Gubb and Garcia-Bellido, 1982) that a small set of genes controls the polarity of cuticular hairs and bristles in Drosophila. Morphologists and embryologists had long appreciated the precise orientation of cuticular structures with respect to the body axes, but Gubb and Garcia-Bellido's work represented a conceptual departure in that it suggested the existence of a genetically defined system dedicated to coordinating these patterns. The genes that they studied are now known to be players in a complex system of developmental regulation that governs cell and tissue movements and patterns in both invertebrates and vertebrates. Although this phenomenon is now commonly referred to as PCP, Gubb and Garcia-Bellido's original and somewhat more general name 'tissue polarity' might ultimately prove more appropriate as its role is revealed in ever more diverse developmental processes.As is often the case in developmental biology, the vertebrate PCP field owes a large debt to its Drosophila counterpart, which has served as the source for many of the components and concepts in this system. However, the numerous differences between vertebrates and invertebrates in anatomy, tissue types and morphogenetic processes, together with the existence of a number of distinct PCP components in vertebrates, have made the study of vertebrate PCP uniquely interesting. In this review, we highlight recent work on vertebrate PCP and discuss several developmental processes in which there is suggestive, but still incomplete, evidence for PCP signaling or for the activity of a subset of PCP components. We have not attempted to cover the PCP field in a comprehensive manner because many excellent and detailed reviews have recently been published in this area [reviews with an emphasis on Drosophila PCP (Adler, 2002;Strutt, 2002;Tree et al., 2002;Klein and Mlodzik, 2005;Strutt and Strutt, 2005); reviews on various aspects of vertebrate PCP (Wallingford et al., 2002;Barrow, 2006;Karner et al., 2006;Montcouquiol et al., 2006a); a review on the very different mechanisms of planar polarit...

Role of chromatin remodeling gene Cecr2 in neurulation and inner ear development

“…Most PCP genes cause the more severe NTD craniorachischisis (Wang and Nathans, 2007). However, there are also several PCP mutants that do show exencephaly.…”

“…Examples of PCP can be observed throughout vertebrate embryogenesis, most notably in the convergent extension (CE) movements required to elongate and shape the neural epithelium during early neurulation, as well as the highly organized epithelium within the cochlear sensory structures (Park and Moon, 2002;Wang et al, 2005). PCP has also been implicated in the cell movements that form the eyelid (Murdoch et al, 2001;Wang and Nathans, 2007). Defects in PCP genes constitute approximately 5% of all known murine NTD mutations and are usually associated with craniorachischisis (a lack of neural tube closure throughout its length), open eyelids, and rotational defects of the cochlear sensory cells (Kibar et al, 2001;Murdoch et al, 2001;Hamblet et al, 2002;Curtin et al, 2003;Montcouquiol et al, 2003;Lu et al, 2004;Wang et al, 2006b;Harris and Juriloff, 2007;Torban et al, 2008).…”

Controlled levels of canonical Wnt signaling are required for neural crest migration

“…The atypical cadherin, Fmi resides on both distal and proximal edges, where it binds neighboring cells through heomophilic interactions (Usui et al, 1999;Shimada et al, 2001). Xenopus, zebrafish and the mouse, the same set of 'core PCP' proteins has been shown to regulate a plethora of early developmental events ranging from convergent extension movements during gastrulation, orientation of cochlear hair cell in the ear, neural tube closure, oriented cell division, lung branching, hair follicle alignment and polarized ciliary beating in the trachea and brain ventricles (Goodrich andStrutt, 2011, Gray et al, 2011;Zallen, 2007;Bosoi et al, 2011;De Marco et al, 2012;Kibar et al, 2009;Kibar et al, 2007;Rida and Chen, 2009;Wang and Nathans, 2007;Yates and Dean, 2007;Segalen and Bellaïche, 2009;Vladar et al, 2012) ( Fig.1.6.4.1). In all cases local modulation of cytoskeleton is crucial for the proper conduct of these processes.…”

Far from solved: A perspective on what we know about early mechanisms of left–right asymmetry

“…We recently proposed that the early blastoderm's planar polarization (Wang and Nathans, 2007;Zallen, 2007) also plays a key role in coordinating LR asymmetry (Aw and Levin, 2009;Vandenberg and Levin, 2009). We note that planar cell polarity (PCP) and LR orientation have many similarities, including the need to amplify a patterning signal across large numbers of cells, and the ability of proteins to segregate and orient themselves with respect to each other in a consistently biased manner, generating a large scale signal that originates intracellularly.…”