Tissue polarity and PCP protein function: C. elegans as an emerging model

Cravo, Janine; Heuvel, Sander van den

doi:10.1016/j.ceb.2019.11.004

Cited by 7 publications

(8 citation statements)

References 55 publications

(71 reference statements)

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“…One of the earliest examples of proteins that regulate asymmetric cell division are the Partitioning defective (PAR) polarity proteins. PAR proteins were initially discovered in C. elegans as proteins that polarize the zygote by forming two opposing protein domains (Kemphues et al, 1988), but are now known to be evolutionarily conserved, acting as universal regulators of apical-basal polarity (Boxem and Heuvel, 2019;Cravo and van den Heuvel, 2019). During asymmetric cell division of Drosophila neuroblasts, apicalbasal polarity is determined when the PAR complex proteins Par-3 (BAZ), PAR-6 and atypical protein kinase C (aPKC) form an apical polarity cap.…”

Section: Proteinsmentioning

confidence: 99%

Principles and mechanisms of asymmetric cell division

Sunchu

Cabernard

2020

Development

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Asymmetric cell division (ACD) is an evolutionarily conserved mechanism used by prokaryotes and eukaryotes alike to control cell fate and generate cell diversity. A detailed mechanistic understanding of ACD is therefore necessary to understand cell fate decisions in health and disease. ACD can be manifested in the biased segregation of macromolecules, the differential partitioning of cell organelles, or differences in sibling cell size or shape. These events are usually preceded by and influenced by symmetry breaking events and cell polarization. In this Review, we focus predominantly on cell intrinsic mechanisms and their contribution to cell polarization, ACD and binary cell fate decisions. We discuss examples of polarized systems and detail how polarization is established and, whenever possible, how it contributes to ACD. Established and emerging model organisms will be considered alike, illuminating both welldocumented and underexplored forms of polarization and ACD.

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Section: Proteinsmentioning

confidence: 99%

Principles and mechanisms of asymmetric cell division

Sunchu

Cabernard

2020

Development

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“…The asymmetrical distribution of potassium channels and DAPC proteins within each muscle cell therefore translates into a prototypical planar polarity pattern. Most planar cell polarity genes are conserved in the C. elegans genome 31 . The role of VANG-1, PRKL-1, and FMI-1 in cell migration-related processes have been well established.…”

Section: Discussionmentioning

confidence: 99%

“…For instance, PCP proteins regulate the orientation of hair follicles and sensory cells, the shape and movement of cells during gastrulation (e.g., convergent-extension processes) and neural tube closure, or the positioning of cell extensions, such as cilia and axons [2][3][4][5][6] . These non-canonical Wnt signalling pathways are also conserved in the nematode Caenorhabditis elegans [7][8][9][10][11] . They have been shown to control directional polarity processes, including convergent extension movements during gastrulation 12 , migration of neuronal precursors 13,14 , and the extension, guidance, and branching of neuronal projections [15][16][17][18] .…”

Section: Introductionmentioning

confidence: 99%

Wnt-Ror-Dvl signalling and the dystrophin complex organize planar-polarized membrane compartments inC. elegansmuscles

Peysson

Zariohi

Gendrel

et al. 2023

Preprint

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The plasma membrane of excitable cells is highly structured and molecular scaffolds recruit proteins to specific membrane compartments. Here, we show that potassium channels and proteins belonging to the dystrophin-associated protein complex define multiple types of planar-polarized membrane compartments at the surface of C. elegans muscle cells. Surprisingly, conserved planar cell polarity proteins are not required for this process. However, we implicate a Wnt signaling module involving the Wnt ligand EGL-20, the Wnt receptor CAM-1, and the intracellular effector DSH-1/disheveled in the formation of this cell polarity pattern. Moreover, using time-resolved and tissue-specific protein degradation, we demonstrate that muscle cell polarity is a dynamic state, requiring continued presence of DSH-1 throughout post-embryonic life. Our results reveal the intricate, highly reproducible, and entirely unsuspected complexity of the worm's sarcolemma. This novel case of planar cell polarity in a tractable genetic model organism may provide valuable insight into the molecular and cellular mechanisms that regulate cellular organization, allowing specific functions to be compartmentalized within distinct plasma membrane domains.

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“…In terms of the flexibility of the PCP pathway, previous studies in C. elegans indicated that even the so-called core interactions between Frizzled and Van Gogh may be partially replaced (Cravo and van den Heuvel, 2020). Regulation of spindle orientation in the early C. elegans embryo depends on polarized localization of MOM-5/Frizzled to the posterior of the dividing cell.…”

Section: Discussionmentioning

confidence: 99%

A compound PCP scheme underlies sequential rosettes-based cell intercalation

Cheng

Chen

et al. 2022

Preprint

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Sequential rosettes are a type of collective cell behavior recently discovered in the C. elegans embryo to mediate directional cell migration through sequential formation and resolution of multicellular rosettes involving the migrating cell and its neighboring cells along the way. Here we show that a Planar Cell Polarity (PCP)-related polarity scheme regulates sequential rosettes, which is distinct from the known mode of how PCP regulates multicellular rosettes in the process of convergent extension. Specifically, non-muscle myosin (NMY) localization and edge contraction are perpendicular to that of Van Gogh as opposed to colocalizing with Van Gogh. Further analyses suggest a two-component polarity scheme: one being the canonical PCP pathway with MIG-1/Frizzled and VANG-1/Van Gogh localized to the vertical edges, the other being MIG-1/Frizzled and NMY-2 localized to the midline/contracting edges. Both MIG-1/Frizzled and VANG-1/Van Gogh are required for NMY-2 localization and contraction of the midline edges, but in redundancy with LAT-1/Latrophilin, an adhesion GPCR which has not been shown to regulate multicellular rosettes. Our results establish a distinct mode of PCP-mediated cell intercalation and shed light on the versatile nature of PCP pathway.

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Tissue polarity and PCP protein function: C. elegans as an emerging model

Cited by 7 publications

References 55 publications

Principles and mechanisms of asymmetric cell division

Principles and mechanisms of asymmetric cell division

Wnt-Ror-Dvl signalling and the dystrophin complex organize planar-polarized membrane compartments inC. elegansmuscles

A compound PCP scheme underlies sequential rosettes-based cell intercalation

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