Reciprocal and dynamic polarization of planar cell polarity core components and myosin

Newman-Smith, Erin; Kourakis, Matthew J.; Reeves, Wendy; Veeman, Michael; Smith, William C.

doi:10.7554/elife.05361

Cited by 35 publications

(33 citation statements)

References 46 publications

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“…PCP proteins were first found to drive the phosphorylation of Myosin in Drosophila (Winter et al, 2001), and more recently the same has been shown for cell intercalation in Xenopus and mice (Lienkamp et al, 2012;McGreevy et al, 2015;Nishimura et al, 2012;Shindo and Wallingford, 2014;Williams et al, 2014), as well as in the cochlea of mice (Lee et al, 2012). Interestingly, two recent studies in Xenopus and ascidians suggest that myosin also acts upstream of PCP protein localization (Newman-Smith et al, 2015;Ossipova et al, 2015) and may involve a reciprocal relationship in their polarized functions, and this notion is supported by our data here.…”

Section: Discussionsupporting

confidence: 90%

Spatial and temporal PCP protein dynamics coordinate cell intercalation during neural tube closure

Butler

Wallingford

2018

Preprint

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Planar cell polarity (PCP) controls the convergent extension cell movements that drive axis elongation in all vertebrates. Though asymmetric localization of core PCP proteins is central to their function, we currently understand little about PCP protein localization as it relates to the subcellular behaviors that drive convergent extension. Here, we have used high magnification time-lapse imaging to simultaneously monitor cell intercalation behaviors and the localization of the PCP proteins Prickle2 and Vangl2. We observed the expected asymmetric enrichment of PCP proteins, but more interestingly, we also observed tight temporal and spatial correlation of PCP protein enrichment with contractile behavior in cell-cell junctions. These patterns of localization were associated with similar pattern of protein turnover at junctions as assessed by FRAP. In fact, dynamic enrichment of PCP proteins was linked more strongly to junction behavior than to spatial orientation. Finally, recruitment of Prickle2 and Vangl2 to cell-cell junctions was temporally and spatially coordinated with planar polarized oscillations of actomyosin enrichment, and all of these dynamic relationships were disrupted when PCP signaling was manipulated. Together, these results provide a dynamic and quantitative view of PCP protein localization during convergent extension and suggest a complex and intimate link between the dynamic localization of core PCP proteins, actomyosin assembly, and polarized junction shrinking during cell intercalation of the closing vertebrate neural tube.

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Section: Discussionsupporting

confidence: 90%

Spatial and temporal PCP protein dynamics coordinate cell intercalation during neural tube closure

Butler

Wallingford

2018

Preprint

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“…In addition, recent studies note the possibility of a feedback mechanism in which actomyosin also regulates the distribution of PCP proteins. This is supported by evidence showing that inhibition of actomyosin activation causes a disturbed localization of PCP proteins in the X. laevis neural plate and C. intestinalis notochord development (Figure (f)).…”

Section: Main Topics and Questions Discussed In This Reviewsupporting

confidence: 63%

Models of convergent extension during morphogenesis

Shindo

2017

WIREs Developmental Biology

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Convergent extension (CE) is a fundamental and conserved collective cell movement that forms elongated tissues during embryonic development. Thus far, studies have demonstrated two different mechanistic models of collective cell movements during CE. The first, termed the crawling mode, was discovered in the process of notochord formation in Xenopus laevis embryos, and has been the established model of CE for decades. The second model, known as the contraction mode, was originally reported in studies of germband extension in Drosophila melanogaster embryos and was recently demonstrated to be a conserved mechanism of CE among tissues and stages of development across species. This review summarizes the two modes of CE by focusing on the differences in cytoskeletal behaviors and relative expression of cell adhesion molecules. The upstream molecules regulating these machineries are also discussed. There are abundant studies of notochord formation in X. laevis embryos, as this was one of the pioneering model systems in this field. Therefore, the present review discusses these findings as an approach to the fundamental biological question of collective cell regulation. WIREs Dev Biol 2018, 7:e293. doi: 10.1002/wdev.293This article is categorized under: Early Embryonic Development > Gastrulation and NeurulationComparative Development and Evolution > Model Systems

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“…Finally, the coordinated pulsing of actomyosin and Pk2 is consistent with recent reports that indicate a reciprocal relationship in which actomyosin controls PCP protein localization and PCP proteins in turn control Myosin activity (Newman-Smith et al, 2015, Ossipova et al, 2015. Because we found that pulses of Pk2 were synchronized with those of actomyosin, we tested the effect of Pk2 loss of function on the several parameters of actomyosin oscillation defined above (i.e.…”

Section: Prickle2 Controls the Frequency Of Actomyosin Oscillationssupporting

confidence: 85%

Frequency and synchrony of actomyosin oscillation during PCP-dependent convergent extension

Shindo

Inoue

Kinoshita

et al. 2018

Preprint

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Oscillatory actomyosin flows play a key role in single cell migration and in collective cell movements that shape invertebrates embryos, but the role of such oscillations in vertebrate morphogenesis remains poorly defined. Here, data from mathematical modeling and in vivo 4D imaging of actomyosin in the Xenopus gastrula suggest that oscillatory actomyosin contractions are a general feature of convergent extension by junction shrinking. We show that synchronous intracellular flows link two spatially distinct populations of actomyosin within individual cells, but that oscillations are asynchronous between neighboring cells that share a shrinking cell-cell junction. We also show that the core PCP protein Prickle2 displays a parallel oscillatory behavior and is required for tuning the frequency of actomyosin contractions, indicating that PCP signaling controls not only the orientation of actomyosin contractions, but also their frequency. Together, these data provide new insights into the function and control of oscillatory actomyosin contractions in collective cell movement.

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Reciprocal and dynamic polarization of planar cell polarity core components and myosin

Cited by 35 publications

References 46 publications

Spatial and temporal PCP protein dynamics coordinate cell intercalation during neural tube closure

Spatial and temporal PCP protein dynamics coordinate cell intercalation during neural tube closure

Models of convergent extension during morphogenesis

Frequency and synchrony of actomyosin oscillation during PCP-dependent convergent extension

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