Planar cell polarity regulators in asymmetric organogenesis during development and disease

Shi, De-Li

doi:10.1016/j.jgg.2022.06.007

Cited by 15 publications

(7 citation statements)

References 136 publications

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“…Mutations of VANGL and other PCP components have been implicated in human diseases, including NTDs, cystic renal disease, congenital heart disease, and lung disease ( 23 ). Both gain of function and loss of function of Wnt/PCP signaling, which dampen CEMs because of loss of the asymmetric distribution of FZD-DVL and VANGL-PK complexes, provoke deregulation of a variety of cellular processes, such as cell differentiation, migration, hair alignment, and cilia localization.…”

Section: Introductionmentioning

confidence: 99%

The Helicobacter pylori CagA oncoprotein disrupts Wnt/PCP signaling and promotes hyperproliferation of pyloric gland base cells

Takahashi-Kanemitsu

Knight

et al. 2023

Sci. Signal.

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Helicobacter pylori strains that deliver the oncoprotein CagA into gastric epithelial cells are the major etiologic agents of upper gastric diseases including gastric cancer. CagA promotes gastric carcinogenesis through interactions with multiple host proteins. Here, we show that CagA also disrupts Wnt-dependent planar cell polarity (Wnt/PCP), which orients cells within the plane of an epithelium and coordinates collective cell behaviors such as convergent extension to enable epithelial elongation during development. Ectopic expression of CagA in Xenopus laevis embryos impaired gastrulation, neural tube formation, and axis elongation, processes driven by convergent extension movements that depend on the Wnt/PCP pathway. Mice specifically expressing CagA in the stomach epithelium had longer pyloric glands and mislocalization of the tetraspanin proteins VANGL1 and VANGL2 (VANGL1/2), which are critical components of Wnt/PCP signaling. The increased pyloric gland length was due to hyperproliferation of cells at the gland base, where Lgr5 + stem and progenitor cells reside, and was associated with fewer differentiated enteroendocrine cells. In cultured human gastric epithelial cells, the N terminus of CagA interacted with the C-terminal cytoplasmic tails of VANGL1/2, which impaired Wnt/PCP signaling by inducing the mislocalization of VANGL1/2 from the plasma membrane to the cytoplasm. Thus, CagA may contribute to the development of gastric cancer by subverting a Wnt/PCP-dependent mechanism that restrains pyloric gland stem cell proliferation and promotes enteroendocrine differentiation.

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Section: Introductionmentioning

confidence: 99%

The Helicobacter pylori CagA oncoprotein disrupts Wnt/PCP signaling and promotes hyperproliferation of pyloric gland base cells

Takahashi-Kanemitsu

Knight

et al. 2023

Sci. Signal.

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“…It is well documented that "core" PCP proteins display polarized localization within the cell of various organs undergoing asymmetric morphogenesis [20]. This feature seems to be also conserved in cells undergoing mediolateral and radial intercalations during gastrulation and neurulation.…”

Section: Discussionmentioning

confidence: 94%

“…The Wnt/PCP pathway functions in a wide variety of morphogenetic processes and instructs cells with positional cues for directed movements [17]. Particularly, Wnt/PCP signaling is required for cell intercalations during gastrulation, neurulation, and asymmetric organogenesis [6,18,19,20]. Although Wnt/PCP signaling mostly contributes to mediolateral cell intercalation [21],…”

Section: Introductionmentioning

confidence: 99%

Wnt/planar cell polarity signaling controls morphogenetic movements of gastrulation and neural tube closure

Shi

2022

Cell. Mol. Life Sci.

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Gastrulation and neurulation are successive morphogenetic processes that play key roles in shaping the basic embryonic body plan. Importantly, they operate through common cellular and molecular mechanisms to set up the three spatially organized germ layers and to close the neural tube. During gastrulation and neurulation, convergent extension movements driven by cell intercalation and oriented cell division generate major forces to narrow the germ layers along the mediolateral axis and elongate the embryo in the anteroposterior direction. Apical constriction also makes an important contribution to promote the formation of the blastopore and the bending of the neural plate. Planar cell polarity proteins are major regulators of asymmetric cell behaviors and critically involved in a wide variety of developmental processes, from gastrulation and neurulation to organogenesis. Mutations of planar cell polarity genes can lead to general defects in the morphogenesis of different organs and the co-existence of distinct congenital diseases, such as spina bifida, hearing deficits, kidney diseases, and limb elongation defects. This review outlines our current understanding of non-canonical Wnt signaling, commonly known as Wnt/planar cell polarity signaling, in regulating morphogenetic movements of gastrulation and neural tube closure during development and disease. It also attempts to identify unanswered questions that deserve further investigations.

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“… Expression of Rbm24 protein in cochlear hair cells. ( A ) Schema shows the planar cell polarity-dependent organization of hair cells in the organ of Corti [ 47 ]. One row of inner hair cells (IHC) and three rows of outer hair cells (OHC1-3) display uniform orientation of arrow-shaped stereocilia, and are rigorously aligned with surrounding supporting cells (represented by different forms and colors).…”

Section: Figurementioning

confidence: 99%

Emerging Roles of RNA-Binding Proteins in Inner Ear Hair Cell Development and Regeneration

Shi

Cheng

Saquet

et al. 2022

IJMS

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RNA-binding proteins (RBPs) regulate gene expression at the post-transcriptional level. They play major roles in the tissue- and stage-specific expression of protein isoforms as well as in the maintenance of protein homeostasis. The inner ear is a bi-functional organ, with the cochlea and the vestibular system required for hearing and for maintaining balance, respectively. It is relatively well documented that transcription factors and signaling pathways are critically involved in the formation of inner ear structures and in the development of hair cells. Accumulating evidence highlights emerging functions of RBPs in the post-transcriptional regulation of inner ear development and hair cell function. Importantly, mutations of splicing factors of the RBP family and defective alternative splicing, which result in inappropriate expression of protein isoforms, lead to deafness in both animal models and humans. Because RBPs are critical regulators of cell proliferation and differentiation, they present the potential to promote hair cell regeneration following noise- or ototoxin-induced damage through mitotic and non-mitotic mechanisms. Therefore, deciphering RBP-regulated events during inner ear development and hair cell regeneration can help define therapeutic strategies for treatment of hearing loss. In this review, we outline our evolving understanding of the implications of RBPs in hair cell formation and hearing disease with the aim of promoting future research in this field.

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Planar cell polarity regulators in asymmetric organogenesis during development and disease

Cited by 15 publications

References 136 publications

The Helicobacter pylori CagA oncoprotein disrupts Wnt/PCP signaling and promotes hyperproliferation of pyloric gland base cells

The Helicobacter pylori CagA oncoprotein disrupts Wnt/PCP signaling and promotes hyperproliferation of pyloric gland base cells

Wnt/planar cell polarity signaling controls morphogenetic movements of gastrulation and neural tube closure

Emerging Roles of RNA-Binding Proteins in Inner Ear Hair Cell Development and Regeneration

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