The role of prickle proteins in vertebrate development and pathology

. 2024 May ; 479 (5) : 1199-1221. [epub] 20230626

Jazyk angličtina Země Nizozemsko Médium print-electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid37358815

Grantová podpora
GA22-06405S Grantová Agentura, Univerzita Karlova
MUNI/J/0004/2021 Grantová agentura. Masaryk University

Odkazy

PubMed 37358815
PubMed Central PMC11116189
DOI 10.1007/s11010-023-04787-z
PII: 10.1007/s11010-023-04787-z
Knihovny.cz E-zdroje

Prickle is an evolutionarily conserved family of proteins exclusively associated with planar cell polarity (PCP) signalling. This signalling pathway provides directional and positional cues to eukaryotic cells along the plane of an epithelial sheet, orthogonal to both apicobasal and left-right axes. Through studies in the fruit fly Drosophila, we have learned that PCP signalling is manifested by the spatial segregation of two protein complexes, namely Prickle/Vangl and Frizzled/Dishevelled. While Vangl, Frizzled, and Dishevelled proteins have been extensively studied, Prickle has been largely neglected. This is likely because its role in vertebrate development and pathologies is still being explored and is not yet fully understood. The current review aims to address this gap by summarizing our current knowledge on vertebrate Prickle proteins and to cover their broad versatility. Accumulating evidence suggests that Prickle is involved in many developmental events, contributes to homeostasis, and can cause diseases when its expression and signalling properties are deregulated. This review highlights the importance of Prickle in vertebrate development, discusses the implications of Prickle-dependent signalling in pathology, and points out the blind spots or potential links regarding Prickle, which could be studied further.

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Ives PJDIS. Melanogaster new mutants. 1945;19:46.

Adler PN. The frizzled/stan Pathway and Planar Cell Polarity in the Drosophila Wing. Curr Top Dev Biol. 2012;101:1–31. doi: 10.1016/B978-0-12-394592-1.00001-6. PubMed DOI PMC

Butler MT, Wallingford JB. Planar cell polarity in development and disease. Nat Rev Mol Cell Biol. 2017;18(6):375–388. doi: 10.1038/nrm.2017.11. PubMed DOI PMC

Fisher SE, Ciccodicola A, Tanaka K, Curci A, Desicato S, D'Urso M, et al. Sequence-based exon prediction around the synaptophysin locus reveals a gene-rich area containing novel genes in human proximal Xp. Genomics. 1997;45(2):340–347. doi: 10.1006/geno.1997.4941. PubMed DOI

Nishikawa S, Kawamoto T. Localization of Core Planar Cell Polarity Proteins, PRICKLEs, in Ameloblasts of Rat Incisors: Possible Regulation of Enamel Rod Decussation. Acta Histochem Cytochem. 2015;48(2):37–45. doi: 10.1267/ahc.14046. PubMed DOI PMC

Ossipova O, Chu CW, Fillatre J, Brott BK, Itoh K, Sokol SY. The involvement of PCP proteins in radial cell intercalations during Xenopus embryonic development. Dev Biol. 2015;408(2):316–327. doi: 10.1016/j.ydbio.2015.06.013. PubMed DOI PMC

Katoh M, Katoh M. Identification and characterization of human PRICKLE1 and PRICKLE2 genes as well as mouse Prickle1 and Prickle2 genes homologous to Drosophila tissue polarity gene prickle. Int J Mol Med. 2003;11(2):249–256. PubMed

Teufel A, Weinmann A, Galle PR, Lohse AW. Characterization of OEBT, a LIM protein. Int J Mol Med. 2005;15(3):513–518. PubMed

Zallen JA. Planar polarity and tissue morphogenesis. Cell. 2007;129(6):1051–1063. doi: 10.1016/j.cell.2007.05.050. PubMed DOI

Jenny A, Darken RS, Wilson PA, Mlodzik M. Prickle and Strabismus form a functional complex to generate a correct axis during planar cell polarity signaling. Embo J. 2003;22(17):4409–4420. doi: 10.1093/emboj/cdg424. PubMed DOI PMC

Tang DD, Gerlach BD. The roles and regulation of the actin cytoskeleton, intermediate filaments and microtubules in smooth muscle cell migration. Respir Res. 2017;18(1):54. doi: 10.1186/s12931-017-0544-7. PubMed DOI PMC

Dreyer CA, VanderVorst K, Carraway KL., 3rd Vangl as a Master Scaffold for Wnt/Planar Cell Polarity Signaling in Development and Disease. Front Cell Dev Biol. 2022;10:887100. doi: 10.3389/fcell.2022.887100. PubMed DOI PMC

Sala S, Catillon M, Hadzic E, Schaffner-Reckinger E, Van Troys M, Ampe C. The PET and LIM1-2 domains of testin contribute to intramolecular and homodimeric interactions. PLoS ONE. 2017;12(5):e0177879. doi: 10.1371/journal.pone.0177879. PubMed DOI PMC

Sweede M, Ankem G, Chutvirasakul B, Azurmendi HF, Chbeir S, Watkins J, et al. Structural and membrane binding properties of the prickle PET domain. Biochemistry. 2008;47(51):13524–13536. doi: 10.1021/bi801037h. PubMed DOI

Anderson CA, Kovar DR, Gardel ML, Winkelman JD. LIM domain proteins in cell mechanobiology. Cytoskeleton (Hoboken) 2021;78(6):303–311. doi: 10.1002/cm.21677. PubMed DOI PMC

Kadrmas JL, Beckerle MC. The LIM domain: from the cytoskeleton to the nucleus. Nat Rev Mol Cell Biol. 2004;5(11):920–931. doi: 10.1038/nrm1499. PubMed DOI

Shi DL. Planar cell polarity regulators in asymmetric organogenesis during development and disease. J Genet Genomics. 2022. PubMed

Dawid IB, Breen JJ, Toyama R. LIM domains: multiple roles as adapters and functional modifiers in protein interactions. Trends Genet. 1998;14(4):156–162. doi: 10.1016/S0168-9525(98)01424-3. PubMed DOI

Maurer-Stroh S, Washietl S, Eisenhaber F. Protein prenyltransferases. Genome Biol. 2003;4(4):212. doi: 10.1186/gb-2003-4-4-212. PubMed DOI PMC

Choy E, Chiu VK, Silletti J, Feoktistov M, Morimoto T, Michaelson D, et al. Endomembrane trafficking of ras: the CAAX motif targets proteins to the ER and Golgi. Cell. 1999;98(1):69–80. doi: 10.1016/S0092-8674(00)80607-8. PubMed DOI

Carr D, Sanchez-Alvarez L, Imai JH, Slatculescu C, Noblett N, Mao L, et al. A Farnesyltransferase Acts to Inhibit Ectopic Neurite Formation in C. elegans. Plos One. 2016;11(6):e0157537. PubMed PMC

Cho B, Pierre-Louis G, Sagner A, Eaton S, Axelrod JD. Clustering and negative feedback by endocytosis in planar cell polarity signaling is modulated by ubiquitinylation of prickle. PLoS Genet. 2015;11(5):e1005259. doi: 10.1371/journal.pgen.1005259. PubMed DOI PMC

Iakoucheva LM, Radivojac P, Brown CJ, O'Connor TR, Sikes JG, Obradovic Z, et al. The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res. 2004;32(3):1037–1049. doi: 10.1093/nar/gkh253. PubMed DOI PMC

Collu GM, Jenny A, Gaengel K, Mirkovic I, Chin ML, Weber U, et al. Prickle is phosphorylated by Nemo and targeted for degradation to maintain Prickle/Spiny-legs isoform balance during planar cell polarity establishment. PLoS Genet. 2018;14(5):e1007391. doi: 10.1371/journal.pgen.1007391. PubMed DOI PMC

Daulat AM, Luu O, Sing A, Zhang L, Wrana JL, McNeill H, et al. Mink1 regulates beta-catenin-independent Wnt signaling via Prickle phosphorylation. Mol Cell Biol. 2012;32(1):173–185. doi: 10.1128/MCB.06320-11. PubMed DOI PMC

Strutt H, Gamage J, Strutt D. Reciprocal action of Casein Kinase Iepsilon on core planar polarity proteins regulates clustering and asymmetric localisation. Elife. 2019;8. PubMed PMC

Agajanian MJ, Potjewyd FM, Bowman BM, Solomon S, LaPak KM, Bhatt DP, et al. Protein proximity networks and functional evaluation of the casein kinase 1 gamma family reveal unique roles for CK1gamma3 in WNT signaling. J Biol Chem. 2022;298(6):101986. doi: 10.1016/j.jbc.2022.101986. PubMed DOI PMC

Butler MT, Wallingford JB. Control of vertebrate core planar cell polarity protein localization and dynamics by Prickle 2. Development. 2015;142(19):3429–3439. PubMed PMC

Dorrego-Rivas A, Ezan J, Moreau MM, Poirault-Chassac S, Aubailly N, De Neve J, et al. The core PCP protein Prickle2 regulates axon number and AIS maturation by binding to AnkG and modulating microtubule bundling. Sci Adv. 2022;8(36):eabo6333. PubMed PMC

Vladar EK, Nayak JV, Milla CE, Axelrod JD. Airway epithelial homeostasis and planar cell polarity signaling depend on multiciliated cell differentiation. JCI Insight. 2016;1(13). PubMed PMC

Yu J, Liang X, Ji Y, Ai C, Liu J, Zhu L, et al. PRICKLE3 linked to ATPase biogenesis manifested Leber's hereditary optic neuropathy. J Clin Invest. 2020;130(9):4935–4946. doi: 10.1172/JCI134965. PubMed DOI PMC

Shimojo M, Hersh LB. REST/NRSF-interacting LIM domain protein, a putative nuclear translocation receptor. Mol Cell Biol. 2003;23(24):9025–9031. doi: 10.1128/MCB.23.24.9025-9031.2003. PubMed DOI PMC

Tao H, Inoue K, Kiyonari H, Bassuk AG, Axelrod JD, Sasaki H, et al. Nuclear localization of Prickle2 is required to establish cell polarity during early mouse embryogenesis. Dev Biol. 2012;364(2):138–148. doi: 10.1016/j.ydbio.2012.01.025. PubMed DOI PMC

UniProt C. UniProt: the Universal Protein Knowledgebase in 2023. Nucleic Acids Res. 2022. PubMed PMC

Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC

Truszkowski J, Goldman N. Maximum Likelihood Phylogenetic Inference is Consistent on Multiple Sequence Alignments, with or without Gaps. Syst Biol. 2016;65(2):328–333. doi: 10.1093/sysbio/syv089. PubMed DOI PMC

Capra JA, Singh M. Predicting functionally important residues from sequence conservation. Bioinformatics. 2007;23(15):1875–1882. doi: 10.1093/bioinformatics/btm270. PubMed DOI

Ciruna B, Jenny A, Lee D, Mlodzik M, Schier AF. Planar cell polarity signalling couples cell division and morphogenesis during neurulation. Nature. 2006;439(7073):220–224. doi: 10.1038/nature04375. PubMed DOI PMC

Chu CW, Sokol SY. Wnt proteins can direct planar cell polarity in vertebrate ectoderm. Elife. 2016;5. PubMed PMC

Antic D, Stubbs JL, Suyama K, Kintner C, Scott MP, Axelrod JD. Planar cell polarity enables posterior localization of nodal cilia and left-right axis determination during mouse and Xenopus embryogenesis. PLoS ONE. 2010;5(2):e8999. doi: 10.1371/journal.pone.0008999. PubMed DOI PMC

Yin C, Kiskowski M, Pouille PA, Farge E, Solnica-Krezel L. Cooperation of polarized cell intercalations drives convergence and extension of presomitic mesoderm during zebrafish gastrulation. J Cell Biol. 2008;180(1):221–232. doi: 10.1083/jcb.200704150. PubMed DOI PMC

Deans MR, Antic D, Suyama K, Scott MP, Axelrod JD, Goodrich LV. Asymmetric distribution of prickle-like 2 reveals an early underlying polarization of vestibular sensory epithelia in the inner ear. J Neurosci. 2007;27(12):3139–3147. doi: 10.1523/JNEUROSCI.5151-06.2007. PubMed DOI PMC

Huang Y, Winklbauer R. Cell cortex regulation by the planar cell polarity protein Prickle1. J Cell Biol. 2022;221(7). PubMed PMC

Mapp OM, Walsh GS, Moens CB, Tada M, Prince VE. Zebrafish Prickle1b mediates facial branchiomotor neuron migration via a farnesylation-dependent nuclear activity. Development. 2011;138(10):2121–2132. doi: 10.1242/dev.060442. PubMed DOI PMC

Sowers LP, Yin T, Mahajan VB, Bassuk AG. Defective motile cilia in Prickle2-deficient mice. J Neurogenet. 2014;28(1–2):146–152. doi: 10.3109/01677063.2014.885966. PubMed DOI

Chu CW, Ossipova O, Ioannou A, Sokol SY. Prickle3 synergizes with Wtip to regulate basal body organization and cilia growth. Sci Rep. 2016;6:24104. doi: 10.1038/srep24104. PubMed DOI PMC

Jakobsen L, Vanselow K, Skogs M, Toyoda Y, Lundberg E, Poser I, et al. Novel asymmetrically localizing components of human centrosomes identified by complementary proteomics methods. EMBO J. 2011;30(8):1520–1535. doi: 10.1038/emboj.2011.63. PubMed DOI PMC

Piel M, Nordberg J, Euteneuer U, Bornens M. Centrosome-dependent exit of cytokinesis in animal cells. Science. 2001;291(5508):1550–1553. doi: 10.1126/science.1057330. PubMed DOI

Yamashita YM, Mahowald AP, Perlin JR, Fuller MT. Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science. 2007;315(5811):518–521. doi: 10.1126/science.1134910. PubMed DOI PMC

Nie Z, Wang C, Chen J, Ji Y, Zhang H, Zhao F, et al. Abnormal morphology and function in retinal ganglion cells derived from patients-specific iPSCs generated from individuals with Leber's hereditary optic neuropathy. Hum Mol Genet. 2022. PubMed PMC

Tao H, Suzuki M, Kiyonari H, Abe T, Sasaoka T, Ueno N. Mouse prickle1, the homolog of a PCP gene, is essential for epiblast apical-basal polarity. Proc Natl Acad Sci U S A. 2009;106(34):14426–14431. doi: 10.1073/pnas.0901332106. PubMed DOI PMC

Etheridge SL, Ray S, Li S, Hamblet NS, Lijam N, Tsang M, et al. Murine dishevelled 3 functions in redundant pathways with dishevelled 1 and 2 in normal cardiac outflow tract, cochlea, and neural tube development. PLoS Genet. 2008;4(11):e1000259. doi: 10.1371/journal.pgen.1000259. PubMed DOI PMC

Adler PN. Planar signaling and morphogenesis in Drosophila. Dev Cell. 2002;2(5):525–535. doi: 10.1016/S1534-5807(02)00176-4. PubMed DOI

Chien YH, Keller R, Kintner C, Shook DR. Mechanical strain determines the axis of planar polarity in ciliated epithelia. Current biology : CB. 2015;25(21):2774–2784. doi: 10.1016/j.cub.2015.09.015. PubMed DOI PMC

Groza T, Gomez FL, Mashhadi HH, Munoz-Fuentes V, Gunes O, Wilson R, et al. The International Mouse Phenotyping Consortium: comprehensive knockout phenotyping underpinning the study of human disease. Nucleic Acids Res. 2023;51(D1):D1038–D1045. doi: 10.1093/nar/gkac972. PubMed DOI PMC

Wallingford JB, Harland RM. Xenopus Dishevelled signaling regulates both neural and mesodermal convergent extension: parallel forces elongating the body axis. Development. 2001;128(13):2581–2592. doi: 10.1242/dev.128.13.2581. PubMed DOI

Wallingford JB. Neural tube closure and neural tube defects: studies in animal models reveal known knowns and known unknowns. Am J Med Genet C Semin Med Genet. 2005;135C(1):59–68. doi: 10.1002/ajmg.c.30054. PubMed DOI

Keller R, Davidson L, Edlund A, Elul T, Ezin M, Shook D, et al. Mechanisms of convergence and extension by cell intercalation. Philos Trans R Soc Lond B Biol Sci. 2000;355(1399):897–922. doi: 10.1098/rstb.2000.0626. PubMed DOI PMC

Wallingford JB, Harland RM. Neural tube closure requires Dishevelled-dependent convergent extension of the midline. Development. 2002;129(24):5815–5825. doi: 10.1242/dev.00123. PubMed DOI

Butler MT, Wallingford JB. Spatial and temporal analysis of PCP protein dynamics during neural tube closure. Elife. 2018;7. PubMed PMC

Shindo A, Inoue Y, Kinoshita M, Wallingford JB. PCP-dependent transcellular regulation of actomyosin oscillation facilitates convergent extension of vertebrate tissue. Dev Biol. 2019;446(2):159–167. doi: 10.1016/j.ydbio.2018.12.017. PubMed DOI PMC

Chuykin I, Ossipova O, Sokol SY. Par3 interacts with Prickle3 to generate apical PCP complexes in the vertebrate neural plate. Elife. 2018;7. PubMed PMC

Dady A, Havis E, Escriou V, Catala M, Duband JL. Junctional neurulation: a unique developmental program shaping a discrete region of the spinal cord highly susceptible to neural tube defects. J Neurosci. 2014;34(39):13208–13221. doi: 10.1523/JNEUROSCI.1850-14.2014. PubMed DOI PMC

Carreira-Barbosa F, Concha ML, Takeuchi M, Ueno N, Wilson SW, Tada M. Prickle 1 regulates cell movements during gastrulation and neuronal migration in zebrafish. Development. 2003;130(17):4037–4046. doi: 10.1242/dev.00567. PubMed DOI

Veeman MT, Slusarski DC, Kaykas A, Louie SH, Moon RT. Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Current biology : CB. 2003;13(8):680–685. doi: 10.1016/S0960-9822(03)00240-9. PubMed DOI

Yang T, Bassuk AG, Fritzsch B. Prickle1 stunts limb growth through alteration of cell polarity and gene expression. Dev Dyn. 2013;242(11):1293–1306. doi: 10.1002/dvdy.24025. PubMed DOI PMC

Liu D, Ban HJ, El Sergani AM, Lee MK, Hecht JT, Wehby GL, et al. PRICKLE1 x FOCAD Interaction Revealed by Genome-Wide vQTL Analysis of Human Facial Traits. Front Genet. 2021;12:674642. doi: 10.3389/fgene.2021.674642. PubMed DOI PMC

Liu C, Lin C, Gao C, May-Simera H, Swaroop A, Li T. Null and hypomorph Prickle1 alleles in mice phenocopy human Robinow syndrome and disrupt signaling downstream of Wnt5a. Biol Open. 2014;3(9):861–870. doi: 10.1242/bio.20148375. PubMed DOI PMC

Chen YT, Liu P, Bradley A. Inducible gene trapping with drug-selectable markers and Cre/loxP to identify developmentally regulated genes. Mol Cell Biol. 2004;24(22):9930–9941. doi: 10.1128/MCB.24.22.9930-9941.2004. PubMed DOI PMC

Gao B, Yang Y. Planar cell polarity in vertebrate limb morphogenesis. Curr Opin Genet Dev. 2013;23(4):438–444. doi: 10.1016/j.gde.2013.05.003. PubMed DOI PMC

Galea GL, Meakin LB, Savery D, Taipaleenmaki H, Delisser P, Stein GS, et al. Planar cell polarity aligns osteoblast division in response to substrate strain. J Bone Miner Res. 2015;30(3):423–435. doi: 10.1002/jbmr.2377. PubMed DOI PMC

Nishikawa S. Cytoskeleton, intercellular junctions, planar cell polarity, and cell movement in amelogenesis. J Oral Biosci. 2017;59(4):197–204. doi: 10.1016/j.job.2017.07.002. DOI

Wan Y, Lantz B, Cusack BJ, Szabo-Rogers HL. Prickle1 regulates differentiation of frontal bone osteoblasts. Sci Rep. 2018;8(1):18021. doi: 10.1038/s41598-018-36742-0. PubMed DOI PMC

Putnova I, Dosedelova H, Bryja V, Landova M, Buchtova M, Stembirek J. Angled Growth of the Dental Lamina Is Accompanied by Asymmetrical Expression of the WNT Pathway Receptor Frizzled 6. Front Physiol. 2017;8:29. doi: 10.3389/fphys.2017.00029. PubMed DOI PMC

Guo D, Yuan Z, Ru J, Gu X, Zhang W, Mao F, et al. A Spatiotemporal Requirement for Prickle 1-Mediated PCP Signaling in Eyelid Morphogenesis and Homeostasis. Invest Ophthalmol Vis Sci. 2018;59(2):952–966. doi: 10.1167/iovs.17-22947. PubMed DOI

Mei X, Westfall TA, Zhang Q, Sheffield VC, Bassuk AG, Slusarski DC. Functional characterization of Prickle2 and BBS7 identify overlapping phenotypes yet distinct mechanisms. Dev Biol. 2014;392(2):245–255. doi: 10.1016/j.ydbio.2014.05.020. PubMed DOI PMC

Mei X, Wu S, Bassuk AG, Slusarski DC. Mechanisms of prickle1a function in zebrafish epilepsy and retinal neurogenesis. Dis Model Mech. 2013;6(3):679–688. PubMed PMC

Tarchini B, Lu X. New insights into regulation and function of planar polarity in the inner ear. Neurosci Lett. 2019;709:134373. doi: 10.1016/j.neulet.2019.134373. PubMed DOI PMC

Copley CO, Duncan JS, Liu C, Cheng H, Deans MR. Postnatal refinement of auditory hair cell planar polarity deficits occurs in the absence of Vangl2. J Neurosci. 2013;33(35):14001–14016. doi: 10.1523/JNEUROSCI.1307-13.2013. PubMed DOI PMC

Yin H, Copley CO, Goodrich LV, Deans MR. Comparison of phenotypes between different vangl2 mutants demonstrates dominant effects of the Looptail mutation during hair cell development. PLoS ONE. 2012;7(2):e31988. doi: 10.1371/journal.pone.0031988. PubMed DOI PMC

Yang T, Kersigo J, Wu S, Fritzsch B, Bassuk AG. Prickle1 regulates neurite outgrowth of apical spiral ganglion neurons but not hair cell polarity in the murine cochlea. PLoS ONE. 2017;12(8):e0183773. doi: 10.1371/journal.pone.0183773. PubMed DOI PMC

Vladar EK, Konigshoff M. Noncanonical Wnt planar cell polarity signaling in lung development and disease. Biochem Soc Trans. 2020;48(1):231–243. doi: 10.1042/BST20190597. PubMed DOI PMC

Vladar EK, Bayly RD, Sangoram AM, Scott MP, Axelrod JD. Microtubules enable the planar cell polarity of airway cilia. Current biology : CB. 2012;22(23):2203–2212. doi: 10.1016/j.cub.2012.09.046. PubMed DOI PMC

Kunimoto K, Weiner AT, Axelrod JD, Vladar EK. Distinct overlapping functions for Prickle1 and Prickle2 in the polarization of the airway epithelium. Front Cell Dev Biol. 2022;10:976182. doi: 10.3389/fcell.2022.976182. PubMed DOI PMC

Gibbs BC, Damerla RR, Vladar EK, Bishwanath C, Chatterjee B, Wan Y, et al. Prickle1 mutation causes planar cell polarity and directional cell migration defects associated with cardiac outflow tract anomalies and other structural birth defects. Biol Open. 2016;5(3):323–335. doi: 10.1242/bio.015750. PubMed DOI PMC

Oteiza P, Koppen M, Krieg M, Pulgar E, Farias C, Melo C, et al. Planar cell polarity signalling regulates cell adhesion properties in progenitors of the zebrafish laterality organ. Development. 2010;137(20):3459–3468. doi: 10.1242/dev.049981. PubMed DOI

Cui S, Capecci LM, Matthews RP. Disruption of planar cell polarity activity leads to developmental biliary defects. Dev Biol. 2011;351(2):229–241. doi: 10.1016/j.ydbio.2010.12.041. PubMed DOI PMC

Gibbs BC, Damerla RR, Vladar EK, Chatterjee B, Wan Y, Liu X, et al. Prickle1 mutation causes planar cell polarity and directional cell migration defects associated with cardiac outflow tract anomalies and other structural birth defects. Biol Open. 2016;5(3):323–335. doi: 10.1242/bio.015750. PubMed DOI PMC

Yuan J, Cha J, Deng W, Bartos A, Sun X, Ho HH, et al. Planar cell polarity signaling in the uterus directs appropriate positioning of the crypt for embryo implantation. Proc Natl Acad Sci U S A. 2016;113(50):E8079–E8088. doi: 10.1073/pnas.1614946113. PubMed DOI PMC

Torban E, Sokol SY. Planar cell polarity pathway in kidney development, function and disease. Nat Rev Nephrol. 2021;17(6):369–385. doi: 10.1038/s41581-021-00395-6. PubMed DOI PMC

Wallingford JB. We Are All Developmental Biologists. Dev Cell. 2019;50(2):132–137. doi: 10.1016/j.devcel.2019.07.006. PubMed DOI

Wen S, Zhu H, Lu W, Mitchell LE, Shaw GM, Lammer EJ, et al. Planar cell polarity pathway genes and risk for spina bifida. Am J Med Genet A. 2010;152A(2):299–304. doi: 10.1002/ajmg.a.33230. PubMed DOI PMC

Bosoi CM, Capra V, Allache R, Trinh VQ, De Marco P, Merello E, et al. Identification and characterization of novel rare mutations in the planar cell polarity gene PRICKLE1 in human neural tube defects. Hum Mutat. 2011;32(12):1371–1375. doi: 10.1002/humu.21589. PubMed DOI PMC

Karczewski KJ, Francioli LC, Tiao G, Cummings BB, Alfoldi J, Wang Q, et al. The mutational constraint spectrum quantified from variation in 141,456 humans. Nature. 2020;581(7809):434–443. doi: 10.1038/s41586-020-2308-7. PubMed DOI PMC

Prasad CP, Chaurasiya SK, Guilmain W, Andersson T. WNT5A signaling impairs breast cancer cell migration and invasion via mechanisms independent of the epithelial-mesenchymal transition. J Exp Clin Cancer Res. 2016;35(1):144. doi: 10.1186/s13046-016-0421-0. PubMed DOI PMC

Jiang W, Crossman DK, Mitchell EH, Sohn P, Crowley MR, Serra R. WNT5A inhibits metastasis and alters splicing of Cd44 in breast cancer cells. Plos One. 2013;8(3). PubMed PMC

Pessoa J, Martins M, Casimiro S, Perez-Plasencia C, Shoshan-Barmatz V. Editorial: Altered Expression of Proteins in Cancer: Function and Potential Therapeutic Targets. Front Oncol. 2022;12:949139. doi: 10.3389/fonc.2022.949139. PubMed DOI PMC

Daulat AM, Borg J-P. When mTORC2-AKT signaling meets cell polarity. Cell Cycle. 2016;15(22):3003–3004. doi: 10.1080/15384101.2016.1214037. PubMed DOI PMC

Ding Y, Chen Y, Wu M, Li L, Huang Y, Huang Y, et al. Identification of genes associated with gastric cancer survival and construction of a nomogram to improve risk stratification for patients with gastric cancer. Oncol Lett. 2020;20(1):215–225. PubMed PMC

Zhou R, Tang Z, Li H, Wang X, Sun Y. PRICKLE1 promotes gastric cancer metastasis by activating mTOR signaling. Am J Transl Res. 2021;13(5):4266–4280. PubMed PMC

Kaucka M, Markéta K, Plevová K, Pavlová Š, Janovská P, Mishra A, et al. The Planar Cell Polarity Pathway Drives Pathogenesis of Chronic Lymphocytic Leukemia by the Regulation of B-Lymphocyte Migration. Can Res. 2013;73(5):1491–1501. doi: 10.1158/0008-5472.CAN-12-1752. PubMed DOI

Jiang D, He Y, He Y, Mo Q, Liu E, Li X, et al. PRICKLE1, a Wnt/PCP signaling component, is overexpressed and associated with inferior prognosis in acute myeloid leukemia. J Transl Med. 2021;19(1):1–17. doi: 10.1186/s12967-021-02873-8. PubMed DOI PMC

Asad M, Asad M, Wong MMK, Tan TZ, Choolani M, Jeffrey L, et al. FZD7 drives in vitro aggressiveness in Stem-A subtype of ovarian cancer via regulation of non-canonical Wnt/PCP pathway. Cell Death and Disease. 2014;5(7). PubMed PMC

Chan DW, Chan CY, Yam JWP, Ching Y-P, Ng IO-L. Prickle-1 Negatively Regulates Wnt/β-Catenin Pathway by Promoting Dishevelled Ubiquitination/Degradation in Liver Cancer. Gastroenterology. 2006;131(4):1218–27. PubMed

Dyberg C, Papachristou P, Haug B, Lagercrantz H, Kogner P, Ringstedt T, et al. Planar cell polarity gene expression correlates with tumor cell viability and prognostic outcome in neuroblastoma. BMC Cancer. 2016;16(1):259-. PubMed PMC

Rudenko EE, Gerashchenko GV, Lapska YV, Vozianov SO, Zgonnyk YM, Zgonnyk YM, et al. PPM1M and PRICKLE2 are potential tumor suppressor genes in human clear-cell renal cell carcinoma. Biopolymers & Cell. 2014;30(3):229–233. doi: 10.7124/bc.00089A. DOI

Senchenko VN, Kisseljova NP, Ivanova TA, Dmitriev AA, Krasnov GS, Kudryavtseva AV, et al. Novel tumor suppressor candidates on chromosome 3 revealed by NotI-microarrays in cervical cancer. Epigenetics. 2013;8(4):409–420. doi: 10.4161/epi.24233. PubMed DOI PMC

Felipe Lima J, Nofech-Mozes S, Bayani J, Bartlett JM. EMT in Breast Carcinoma-A Review. J Clin Med. 2016;5(7). PubMed PMC

Zhang L, Luga V, Armitage SK, Musiol M, Won A, Yip CM, et al. A lateral signalling pathway coordinates shape volatility during cell migration. Nat Commun. 2016;7:11714. doi: 10.1038/ncomms11714. PubMed DOI PMC

Lim BC, Matsumoto S, Hideki Y, Yamamoto H, Mizuno H, Kikuta J, et al. Prickle1 promotes focal adhesion disassembly in cooperation with the CLASP-LL5β complex in migrating cells. J Cell Sci. 2016;129(16):3115–3129. PubMed

Daulat AM, François B, Bertucci F, Audebert S, Sergé A, Finetti P, et al. PRICKLE1 Contributes to Cancer Cell Dissemination through Its Interaction with mTORC2. Dev Cell. 2016;37(4):311–325. doi: 10.1016/j.devcel.2016.04.011. PubMed DOI

Pankova K, Rosel D, Novotny M, Brabek J. The molecular mechanisms of transition between mesenchymal and amoeboid invasiveness in tumor cells. Cell Mol Life Sci. 2010;67(1):63–71. doi: 10.1007/s00018-009-0132-1. PubMed DOI PMC

Luga V, Zhang L, Viloria-Petit A, Ogunjimi AA, Inanlou MR, Mohammad RI, et al. Exosomes Mediate Stromal Mobilization of Autocrine Wnt-PCP Signaling in Breast Cancer Cell Migration. Cell. 2012;151(7):1542–1556. doi: 10.1016/j.cell.2012.11.024. PubMed DOI

Anastas JN, Biechele TL, Robitaille M, Muster J, Allison KH, Angers S, et al. A protein complex of SCRIB, NOS1AP and VANGL1 regulates cell polarity and migration, and is associated with breast cancer progression. Oncogene. 2012;31(32):3696–3708. doi: 10.1038/onc.2011.528. PubMed DOI PMC

Kaucka M, Petersen J, Janovska P, Radaszkiewicz T, Smyckova L, Daulat AM, et al. Asymmetry of VANGL2 in migrating lymphocytes as a tool to monitor activity of the mammalian WNT/planar cell polarity pathway. Cell Commun Signal. 2015;13:2. doi: 10.1186/s12964-014-0079-1. PubMed DOI PMC

Davey CF, Moens CB. Planar cell polarity in moving cells: think globally, act locally. Development. 2017;144(2):187–200. doi: 10.1242/dev.122804. PubMed DOI PMC

Sibasish M, Pallavi M, Omprakash S, Shamima Azma A, Manashi P, Swatismita P, et al. CRISPR-based kinome-screening revealed MINK1 as a druggable player to rewire 5FU-resistance in OSCC through AKT/MDM2/p53 axis. Oncogene. 2022. PubMed PMC

Machacek M, Hodgson L, Welch C, Elliott H, Pertz O, Nalbant P, et al. Coordination of Rho GTPase activities during cell protrusion. Nature. 2009;461(7260):99–103. doi: 10.1038/nature08242. PubMed DOI PMC

Martin K, Reimann A, Fritz RD, Ryu H, Jeon NL, Pertz O. Spatio-temporal co-ordination of RhoA, Rac1 and Cdc42 activation during prototypical edge protrusion and retraction dynamics. Sci Rep. 2016;6:21901. doi: 10.1038/srep21901. PubMed DOI PMC

Daulat AM, Finetti P, Revinski D, Silveira Wagner M, Camoin L, Audebert S, et al. ECT2 associated to PRICKLE1 are poor-prognosis markers in triple-negative breast cancer. Br J Cancer. 2019;120(9):931–940. doi: 10.1038/s41416-019-0448-z. PubMed DOI PMC

Narimatsu M, Bose R, Pye M, Zhang L, Miller BW, Ching P, et al. Regulation of Planar Cell Polarity by Smurf Ubiquitin Ligases. Cell. 2009;137(2):295–307. doi: 10.1016/j.cell.2009.02.025. PubMed DOI

Vicente-Manzanares M, Ma XF, Adelstein RS, Horwitz AR. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Bio. 2009;10(11):778–790. doi: 10.1038/nrm2786. PubMed DOI PMC

Bakker ERM, Raghoebir L, Franken P, Helvensteijn W, van Gurp L, Frits M, et al. Induced Wnt5a expression perturbs embryonic outgrowth and intestinal elongation, but is well-tolerated in adult mice. Dev Biol. 2012;369(1):91–100. doi: 10.1016/j.ydbio.2012.06.007. PubMed DOI

Reynolds A, McDearmid JR, Lachance S, De Marco P, Merello E, Capra V, et al. VANGL1 rare variants associated with neural tube defects affect convergent extension in zebrafish. Mech Dev. 2010;127(7):385–392. doi: 10.1016/j.mod.2009.12.002. PubMed DOI PMC

Justilien V, Jameison L, Channing JD, Der CJ, Rossman KL, Fields AP, et al. Oncogenic Activity of Ect2 Is Regulated through Protein. Journal of Biological Chemistry. 2011. PubMed PMC

Ridley AJ. Rho GTPase signalling in cell migration. Curr Opin Cell Biol. 2015;36:103–112. doi: 10.1016/j.ceb.2015.08.005. PubMed DOI PMC

Kechagia JZ, Ivaska J, Roca-Cusachs P. Integrins as biomechanical sensors of the microenvironment. Nat Rev Mol Cell Bio. 2019;20(8):457–473. doi: 10.1038/s41580-019-0134-2. PubMed DOI

Avais MD, Mônica SW, Audebert S, Malgorzata K, Ariey-Bonnet J, Pascal F, et al. The serine/threonine kinase MINK1 directly regulates the function of promigratory proteins. J Cell Sci. 2022;135(17). PubMed

Stehbens SJ, Paszek MJ, Pemble H, Ettinger A, Gierke S, Wittmann T. CLASPs link focal adhesion-associated microtubule capture to localized exocytosis and adhesion site turnover. Nat Cell Biol. 2014;16(6):558–570. doi: 10.1038/ncb2975. PubMed DOI PMC

Lansbergen G, Grigoriev I, Mimori-Kiyosue Y, Ohtsuka T, Higa S, Kitajima I, et al. CLASPs Attach Microtubule Plus Ends to the Cell Cortex through a Complex with LL5β. Dev Cell. 2006;11(1):21–32. doi: 10.1016/j.devcel.2006.05.012. PubMed DOI

Lamming DW. Inhibition of the Mechanistic Target of Rapamycin (mTOR)–Rapamycin and Beyond. Cold Spring Harbor Perspectives in Medicine. 2016;6(5). PubMed PMC

Jacinto E, Loewith R, Schmidt A, Lin S, Rüegg MA, Hall A, et al. Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat Cell Biol. 2004;6(11):1122–1128. doi: 10.1038/ncb1183. PubMed DOI

Hernández-Negrete I, Carretero-Ortega J, Rosenfeldt H, Hernández-García R, Calderon-Salinas JV, Reyes-Cruz G, et al. P-Rex1 Links Mammalian Target of Rapamycin Signaling to Rac Activation and Cell Migration. J Biol Chem. 2007;282(32):23708–23715. doi: 10.1074/jbc.M703771200. PubMed DOI

Sarbassov DD, Ali SM, Ali SM, Kim D-h, Do-Hyung K, Kim H, et al. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Current Biology. 2004;14(14):1296–302. PubMed

Lamouille S, Connolly EC, Smyth JW, Akhurst RJ, Derynck R. TGF-β-induced activation of mTOR complex 2 drives epithelial-mesenchymal transition and cell invasion. J Cell Sci. 2012;125(5):1259–1273. doi: 10.1242/jcs.095299. PubMed DOI PMC

Guertin DA, Deanna MS, Stevens D, Thoreen CC, Burds AA, Kalaany NY, et al. Ablation in Mice of the mTORC Components raptor, rictor, or mLST8 Reveals that mTORC2 Is Required for Signaling to Akt-FOXO and PKCα, but Not S6K1. Dev Cell. 2006;11(6):859–871. doi: 10.1016/j.devcel.2006.10.007. PubMed DOI

Jacinto E, Facchinetti V, Liu D, Soto N, Wei S, Jung SY, et al. SIN1/MIP1 Maintains rictor-mTOR Complex Integrity and Regulates Akt Phosphorylation and Substrate Specificity. Cell. 2006;127(1):125–137. doi: 10.1016/j.cell.2006.08.033. PubMed DOI

He Y, Sun MM, Zhang GG, Yang J, Chen KS, Xu WW, et al. Targeting PI3K/Akt signal transduction for cancer therapy. Signal Transduct Target Ther. 2021;6(1):425. doi: 10.1038/s41392-021-00828-5. PubMed DOI PMC

Landin Malt A, Hogan AK, Smith CD, Madani MS, Lu X. Wnts regulate planar cell polarity via heterotrimeric G protein and PI3K signaling. J Cell Biol. 2020;219(10). PubMed PMC

Tian T, Lai X, Xiang K, Han X, Yin S, Cabrera RM, et al. Hypermethylation of PI3K-AKT signalling pathway genes is associated with human neural tube defects. Epigenetics. 2022;17(2):133–146. doi: 10.1080/15592294.2021.1878725. PubMed DOI PMC

Delgado-Escueta AV, Enrile-Bacsal F. Juvenile myoclonic epilepsy of Janz. Neurology. 1984;34(3):285–294. doi: 10.1212/WNL.34.3.285. PubMed DOI

Bassuk AG, Wallace RH, Buhr A, Buller AR, Afawi Z, Shimojo M, et al. A homozygous mutation in human PRICKLE1 causes an autosomal-recessive progressive myoclonus epilepsy-ataxia syndrome. Am J Hum Genet. 2008;83(5):572–581. doi: 10.1016/j.ajhg.2008.10.003. PubMed DOI PMC

Algahtani H, Al-Hakami F, Al-Shehri M, Shirah B, Al-Qahtani MH, Abdulkareem AA, et al. A very rare form of autosomal dominant progressive myoclonus epilepsy caused by a novel variant in the PRICKLE1 gene. Seizure. 2019;69:133–139. doi: 10.1016/j.seizure.2019.04.016. PubMed DOI

Tao H, Manak JR, Sowers L, Mei X, Kiyonari H, Abe T, et al. Mutations in prickle orthologs cause seizures in flies, mice, and humans. Am J Hum Genet. 2011;88(2):138–149. doi: 10.1016/j.ajhg.2010.12.012. PubMed DOI PMC

Paemka L, Mahajan VB, Ehaideb SN, Skeie JM, Tan MC, Wu S, et al. Seizures are regulated by ubiquitin-specific peptidase 9 X-linked (USP9X), a de-ubiquitinase. PLoS Genet. 2015;11(3):e1005022. doi: 10.1371/journal.pgen.1005022. PubMed DOI PMC

Sowers LP, Loo L, Wu Y, Campbell E, Ulrich JD, Wu S, et al. Disruption of the non-canonical Wnt gene PRICKLE2 leads to autism-like behaviors with evidence for hippocampal synaptic dysfunction. Mol Psychiatry. 2013;18(10):1077–1089. doi: 10.1038/mp.2013.71. PubMed DOI PMC

Okumura A, Yamamoto T, Miyajima M, Shimojima K, Kondo S, Abe S, et al. 3p interstitial deletion including PRICKLE2 in identical twins with autistic features. Pediatr Neurol. 2014;51(5):730–733. doi: 10.1016/j.pediatrneurol.2014.07.025. PubMed DOI

Paemka L, Mahajan VB, Skeie JM, Sowers LP, Ehaideb SN, Gonzalez-Alegre P, et al. PRICKLE1 interaction with SYNAPSIN I reveals a role in autism spectrum disorders. PLoS ONE. 2013;8(12):e80737. doi: 10.1371/journal.pone.0080737. PubMed DOI PMC

Cukier HN, Dueker ND, Slifer SH, Lee JM, Whitehead PL, Lalanne E, et al. Exome sequencing of extended families with autism reveals genes shared across neurodevelopmental and neuropsychiatric disorders. Mol Autism. 2014;5(1):1. doi: 10.1186/2040-2392-5-1. PubMed DOI PMC

Voineagu I, Wang X, Johnston P, Lowe JK, Tian Y, Horvath S, et al. Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature. 2011;474(7351):380–384. doi: 10.1038/nature10110. PubMed DOI PMC

Fassio A, Patry L, Congia S, Onofri F, Piton A, Gauthier J, et al. SYN1 loss-of-function mutations in autism and partial epilepsy cause impaired synaptic function. Hum Mol Genet. 2011;20(12):2297–2307. doi: 10.1093/hmg/ddr122. PubMed DOI

Megagiannis P, Suresh R, Rouleau GA, Zhou Y. Reversibility and therapeutic development for neurodevelopmental disorders, insights from genetic animal models. Adv Drug Deliv Rev. 2022;191:114562. doi: 10.1016/j.addr.2022.114562. PubMed DOI

Mei Y, Monteiro P, Zhou Y, Kim JA, Gao X, Fu Z, et al. Adult restoration of Shank3 expression rescues selective autistic-like phenotypes. Nature. 2016;530(7591):481–484. doi: 10.1038/nature16971. PubMed DOI PMC

Sun F, Jiang F, Zhang N, Li H, Tian W, Liu W. Upregulation of Prickle2 Ameliorates Alzheimer's Disease-Like Pathology in a Transgenic Mouse Model of Alzheimer's Disease. Front Cell Dev Biol. 2020;8:565020. doi: 10.3389/fcell.2020.565020. PubMed DOI PMC

Smolen JS, Aletaha D, Barton A, Burmester GR, Emery P, Firestein GS, et al. Rheumatoid arthritis Nat Rev Dis Primers. 2018;4:18001. doi: 10.1038/nrdp.2018.1. PubMed DOI

Yang L, Cao N, Miao Y, Dai Y, Wei Z. Morin Acts as a USP7 Inhibitor to Hold Back the Migration of Rheumatoid Arthritis Fibroblast-Like Synoviocytes in a "Prickle1-mTORC2" Dependent Manner. Mol Nutr Food Res. 2021;65(19):e2100367. doi: 10.1002/mnfr.202100367. PubMed DOI

Ross PJ, Mok RSF, Smith BS, Rodrigues DC, Mufteev M, Scherer SW, et al. Modeling neuronal consequences of autism-associated gene regulatory variants with human induced pluripotent stem cells. Mol Autism. 2020;11(1):33. doi: 10.1186/s13229-020-00333-6. PubMed DOI PMC

Russo FB, Brito A, de Freitas AM, Castanha A, de Freitas BC, Beltrao-Braga PCB. The use of iPSC technology for modeling Autism Spectrum Disorders. Neurobiol Dis. 2019;130:104483. doi: 10.1016/j.nbd.2019.104483. PubMed DOI

Hong D, Iakoucheva LM. Therapeutic strategies for autism: targeting three levels of the central dogma of molecular biology. Transl Psychiatry. 2023;13(1):58. doi: 10.1038/s41398-023-02356-y. PubMed DOI PMC

Silverman JL, Thurm A, Ethridge SB, Soller MM, Petkova SP, Abel T, et al. Reconsidering animal models used to study autism spectrum disorder: Current state and optimizing future. Genes Brain Behav. 2022;21(5):e12803. doi: 10.1111/gbb.12803. PubMed DOI PMC

Tippmann HF. Analysis for free: comparing programs for sequence analysis. Brief Bioinform. 2004;5(1):82–87. doi: 10.1093/bib/5.1.82. PubMed DOI

Lefort V, Longueville JE, Gascuel O. SMS: Smart Model Selection in PhyML. Mol Biol Evol. 2017;34(9):2422–2424. doi: 10.1093/molbev/msx149. PubMed DOI PMC

Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 1992;8(3):275–282. PubMed

Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59(3):307–21. PubMed

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