Planar Cell Polarity Signaling: Coordinated Crosstalk for Cell Orientation
Abstract
:1. Introduction
2. Historical Notes
3. Molecular/Cellular Mechanisms—PCP Signaling Pathway
4. Core Components
5. PCP Complex
6. Role of Cell Adhesion Molecules
7. Tissue Morphogenesis—Planar Cell Polarity
8. Neural Tube Closure
9. Tissue Regeneration
10. Developmental Process
- (i)
- Convergent Extension Process: It is the first process that is found to be associated with PCP [56]. MSCs stretch and produce mediolateral protrusions during the convergent extension process. These protrusions incorporate mediolaterally, restricting the mediolateral axis and lengthening the AP axis (Figure 3) [101]. Depletion of PCP components has been linked to mediolateral intercalation, polarization, and elongation, according to several experimental findings [54,56,59,102]. Only two discoveries provide direct mechanistic links between convergent extension behaviors and asymmetrically localized core components of PCP, even though many PCP-dependent mechanisms have been hypothesized to mediate convergent extension movements. On the A-P sites of intercalating cells in neuro-epithelial cells, PCP determines the region of myosin localization. Dvl and Fmi/Celsr1 recruit formin-DAAM1 to A-P sites, where it interacts with PDZ-RhoGEF, activates RhoA, and increases myosin contractility, bending the neural plate and mediating directed intercalation of cells [103]. A comparable mechanism has been observed to propel the convergent extension movements of MSCs during the gastrulation process of Xenopus laevis. In Xenopus laevis gastrulation, Dsh and Fritz induce localization of septin towards the mediolateral vertices, where they restrict junctional shrinkage and cortical contractility of cortical actomyosin spatially to the margins of A-P cell ends [104,105]. Collectively, these investigations demonstrate how spatial cytoskeleton modification resulting from asymmetric PCP localization leads to collectively polarized cell behaviors.
- (ii)
- Positioning—Cilia and Centrosome: PCP controls the orientation of microtubule-based structures such as cilia and the mitotic spindle by regulating the positioning of the mitotic spindle along the plane of epithelial cells through interaction with the SOC (spindle orientation complex), followed by binding of microtubules astral to the cell periphery with the help of dynein complex [106]. To orient the spindle posteriorly, astral microtubules and the dynein complex are brought to the posterior cortex through the interaction of Dsh with Mud/NuMA, and Mud/NuMA is recruited by Pins/LGN on the anterior side, which causes the spindle to orient A-P. A non-dividing inner ear cell’s kinocilium is orientated by PCP in conjunction with its spindle orientation machinery [107,108]. The mPins/LGN and Gai localize in vestibular hair cells to the abneural periphery, which is located across from Vangl2; they are necessary for the positioning of kinocilia, followed by subsequent stereocilia bundle alignment [107]. Dynein and the plus ends of microtubules also exhibit an abneural bias, indicating that Gai-mPins/LGN pull on microtubules through a process akin to that because it is responsible for centrosome positioning during spindle orientation. According to one study, Vangl2 is needed for Gai-Pins/LGN-crescent to properly align between cells that coordinate the positioning and polarity of kinocilia and stereocilia, respectively, throughout the tissue [107]. Studies have observed that PCP is needed for asymmetric positioning of cilia in a wide range of cells [67,68,69,109]. Hence, PCP determines both the plane of cell division in dividing cells and specifies cilia positioning in non-dividing cells.
- (iii)
- Distal Positioning—Wing Hairs: Every Drosophila wing blade cell has a distal end with an actin-rich protrusion. The locations of wing hair and the Fz-Dsh-Fmi positions are closely correlated, which implies that core proteins may be responsible for localizing cytoskeletal regulators to certain areas of cells [110]. A group of proteins known as Fuzzy, Fritz, and Inturned is recruited by Vang to the proximal junction, which negatively regulates the formation of actin pre-hairs [103,104]. Actin polymerization is thought to be repressed by Fuzzy, Fritz, and Inturned proteins by regulating multiple wing hairs, a GBD/FH (GTP-binding/formin homology)-3 domain protein [110,111,112]. As a result, actin nucleation occurs at distant positions within the cell, and ectopic actin bundles grow over the apical surface in the absence of multiple wing hairs [113]. The pre-hair nucleation process precedes distal nucleation, and casein kinase 1g CK1/gilamesh is required for further vesicle trafficking coordination with Rab11 [114]. Rho and Drok (Rho–kinase complex) also play a role in wing-hair formation, but the precise role of Rho is tedious to explore because of its involvement in various functions in cells, including cell division and cell shape [115,116].
11. Cochlea
12. Skin
13. Other Signaling Pathways
- (i)
- Wnt Signaling: The Wnt protein activates the PCP signaling pathway through the activation of a transmembrane protein called Fz [9]. Data from multiple vertebrate investigations showed that Wnt11 and Wnt5a are involved in the induction of PCP [142,143,144,145]. Wing experiments on Drosophila reported that dWnt4 and Wg exhibit a crucial instructive role in positioning the PCP axis [146]. It has been demonstrated that Wnt5a interacts with complex receptors in PCP signaling that contain Ryk, Fz, Ror2, and Vangl2 [146,147,148]. In vertebrates, Wnt5a and Wnt11 also play an instructive role in activating PCP [147,149]. Studies on mutants (silberblick and pipetail) observed that mutations in Wnt11 and Wnt5a exhibit defective A-P axis (shortened and broadened) because of disrupted convergent extension movements, indicating that a Wnt signaling pathway is needed to control the convergent extension process via PCP [90,147]. Wnt signaling is not only involved in the regulation of PCP-mediated convergent extension processes but also mediates limb elongation by regulating PCP. Outcomes obtained from the Wnt5a mutant mice model showed that Wnt5a is implicated in the regulation of PCP-mediated limb elongation [150]. Genetic studies on the Wnt5a null mice models found that Wnt5a is very crucial for the establishment of PCP in the developing limb [151].
- (ii)
- Hippo Signaling: Hippo signaling is considered as a key regulator of organ size by regulating cell apoptosis and proliferation in mammals and flies [152]. Several lines of experimental evidence have reported the crosstalk between Hippo and PCP signaling pathways [152,153]. The relationship between Hippo and PCP signaling may be crucial for regulating the orientation of cell division during embryonic development, which is crucial for defining the form of tissues [154]. Ft, a proto-cadherin molecule of the Hippo signaling pathway, is needed for proper PCP in multiple developing tissues in Drosophila like fate choice positioning during the development of ommatidia, hair positioning in the abdomen and wings, and larval denticle orientation [30,48,155,156]. Through the regulation of Ft activity, patterned Ds serve as a cue for PCP orientation and the formation of imaginal discs in Drosophila [30,49,157,158]. While depletion of Fj and Ds causes partial changes in the growth of wings, PCP is engaged in the normal development of wings with uniform expression of Fj and Ds [50,51,153]. The study on the Ft mutant showed that the absence of the ECD (extracellular domain) greatly improved the PCP defects in the abdomen and wings of the ft mutant [157]. An in vivo study conducted on mammals observed that depletion of Fat4 is associated with PCP defects owing to loss of Ds1 [158,159,160]. It has been proposed that there is an overlap between PCP and Hippo functions since the Hippo pathway controls Fj expression [152]. Atrophine/Grunge (a transcriptional co-regulator) is also involved in the regulation of PCP by interacting with the ICD (intracellular domain) of Ft [52].
- (iii)
- Notch Signaling: Notch signaling is a highly conserved signaling cascade involved in the coordination of multiple developmental processes [161,162,163]. It has been demonstrated that Notch signaling is regulated by PCP, like in the development of Drosophila legs and eyes [163,164]. Studies observed the interplay of Notch signaling and PCP in ommatidial rotation in the eyes of insects [164,165,166]. One study on PCP mutant legs showed that ectopic Notch activity is associated with ectopic joints, indicating that PCP regulates Notch signaling [167]. In the Drosophila eye, PCP/Fz signaling determines the R3 fate from the precursor while inducing Notch-mediated signaling in adjacent cells to determine the R4 fate [164,165,166]. Genetic alterations in PCP result in random location of the ommatidial, R3/R4 specification, and related chirality [168].
- (iv)
- Sonic Hedgehog (Shh) signaling: The complex signal transduction mechanisms that control the finely tuned developmental processes of multicellular animals include the Sonic Hedgehog (Shh) signaling cascade. It also has a significant part in the processes of post-embryonic tissue regeneration and repair in addition to setting the patterns of cellular differentiation that control the creation of complex organs. The development of diverse neuronal populations in the central nervous system is specifically linked to Shh signaling [169]. The Shh signaling pathway involves a series of molecular events that occur when the Shh protein binds to its receptor, Patched (Ptch), relieving its inhibition on another receptor called Smoothened (Smo). This activation of Smo triggers a cascade of intracellular events, ultimately leading to the activation of transcription factors such as Gli proteins. These Gli proteins then regulate the expression of target genes involved in cell fate determination, proliferation, and differentiation. The Shh signaling pathway is essential for the development of various tissues and organs, including the central nervous system, limbs, and organs such as the lungs and gastrointestinal tract. Dysregulation of this pathway can lead to developmental defects and diseases, including various types of cancer. Therefore, understanding the mechanisms of Shh signaling holds great promise for both developmental biology and clinical applications.
14. Negative Regulation
15. Genetic Disorders
16. CRISPR/Cas9
17. Challenges in Planar Cell Polarity (PCP)
18. Conclusion and Future Perspectives
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Drosophila | Vertebrates | Type of Protein |
---|---|---|
Fz (Frizzled) | Fz3, Fz2, Fz7, Fz6 | Extracellular-rich cysteine domain, |
VII-pass trans-membrane receptor | ||
Stan/Fmi (Starry night/Flamingo) | Celsr3, Celsr2, and Celsr1 | VII-pass trans-membrane receptor, |
Extracellular cadherin-repeat | ||
Pk (Prickle) | Pk2 and Pk1 | PET-domain, Triple-LIM domains, |
Cytoplasmic | ||
Dsh (Dishevelled) | Dvl3, Dvl1, and Dvl2 | PDZ, DIX, DEP, Cytoplasmic domains |
Vang Gogh/Strabismus | Vangl2 and Vangl1 | PDZ-binding domains, IV-pass |
Trans-membrane receptor | ||
Dgo (Diego) | Inv (Inversin) | Ankyrin-repeats, Cytoplasmic |
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Kacker, S.; Parsad, V.; Singh, N.; Hordiichuk, D.; Alvarez, S.; Gohar, M.; Kacker, A.; Rai, S.K. Planar Cell Polarity Signaling: Coordinated Crosstalk for Cell Orientation. J. Dev. Biol. 2024, 12, 12. https://doi.org/10.3390/jdb12020012
Kacker S, Parsad V, Singh N, Hordiichuk D, Alvarez S, Gohar M, Kacker A, Rai SK. Planar Cell Polarity Signaling: Coordinated Crosstalk for Cell Orientation. Journal of Developmental Biology. 2024; 12(2):12. https://doi.org/10.3390/jdb12020012
Chicago/Turabian StyleKacker, Sandeep, Varuneshwar Parsad, Naveen Singh, Daria Hordiichuk, Stacy Alvarez, Mahnoor Gohar, Anshu Kacker, and Sunil Kumar Rai. 2024. "Planar Cell Polarity Signaling: Coordinated Crosstalk for Cell Orientation" Journal of Developmental Biology 12, no. 2: 12. https://doi.org/10.3390/jdb12020012
APA StyleKacker, S., Parsad, V., Singh, N., Hordiichuk, D., Alvarez, S., Gohar, M., Kacker, A., & Rai, S. K. (2024). Planar Cell Polarity Signaling: Coordinated Crosstalk for Cell Orientation. Journal of Developmental Biology, 12(2), 12. https://doi.org/10.3390/jdb12020012