References
- Holstein TW. The evolution of the Wnt pathway. Cold Spring Harb Perspect Biol 2012;4:a007922
- Nusslein-Volhard C, Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature 1980;287:795-801 https://doi.org/10.1038/287795a0
- Sharma RP, Chopra VL. Effect of the wingless (wg1) mutation on wing and haltere development in Drosophila melanogaster. Dev Biol 1976;48:461-465 https://doi.org/10.1016/0012-1606(76)90108-1
- Noordermeer J, Klingensmith J, Perrimon N, Nusse R. Dishevelled and armadillo act in the Wingless signalling pathway in Drosophila. Nature 1994;367:80-83 https://doi.org/10.1038/367080a0
- Peifer M, Sweeton D, Casey M, Wieschaus E. Wingless signal and zeste-white 3 kinase trigger opposing changes in the intracellular distribution of armadillo. Development 1994;120:369-380 https://doi.org/10.1242/dev.120.2.369
- Siegfried E, Chou TB, Perrimon N. Wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell 1992;71:1167-1179 https://doi.org/10.1016/S0092-8674(05)80065-0
- Sokol S, Christian JL, Moon RT, Melton DA. Injected Wnt RNA induces a complete body axis in Xenopus embryos. Cell 1991;67:741-752 https://doi.org/10.1016/0092-8674(91)90069-B
- Steinhart Z, Angers S. Wnt signaling in development and tissue homeostasis. Development 2018;145:dev146589
- Zhan T, Rindtorff N, Boutros M. Wnt signaling in cancer. Oncogene 2017;36:1461-1473 https://doi.org/10.1038/onc.2016.304
- Markowitz SD, Bertagnolli MM. Molecular origins of cancer: molecular basis of colorectal cancer. N Engl J Med 2009;361:2449-2460 https://doi.org/10.1056/NEJMra0804588
- Groenewald W, Lund AH, Gay DM. The role of WNT pathway mutations in cancer development and an overview of therapeutic options. Cells 2023;12:990
- Jung YS, Park JI. Wnt signaling in cancer: therapeutic targeting of Wnt signaling beyond β-catenin and the destruction complex. Exp Mol Med 2020;52:183-191 https://doi.org/10.1038/s12276-020-0380-6
- ClinicalTrials.gov. A study of LGK974 in patients with malignancies dependent on Wnt ligands [Internet]. Bethesda: U.S. National Library of Medicine; Year Mon date [cited 2023 May 22]. Available from: https://clinicaltrials.gov/ct2/show/NCT01351103
- Krishnamurthy N, Kurzrock R. Targeting the Wnt/beta-catenin pathway in cancer: update on effectors and inhibitors. Cancer Treat Rev 2018;62:50-60 https://doi.org/10.1016/j.ctrv.2017.11.002
- Koo BK, Spit M, Jordens I, Low TY, Stange DE, van de Wetering M, van Es JH, Mohammed S, Heck AJ, Maurice MM, Clevers H. Tumour suppressor RNF43 is a stem-cell E3 ligase that induces endocytosis of Wnt receptors. Nature 2012;488:665-669 https://doi.org/10.1038/nature11308
- Hao HX, Jiang X, Cong F. Control of Wnt receptor turnover by R-spondin-ZNRF3/RNF43 signaling module and its dysregulation in cancer. Cancers (Basel) 2016;8:54
- Qin K, Yu M, Fan J, Wang H, Zhao P, Zhao G, Zeng W, Chen C, Wang Y, Wang A, Schwartz Z, Hong J, Song L, Wagstaff W, Haydon RC, Luu HH, Ho SH, Strelzow J, Reid RR, He TC, Shi LL. Canonical and noncanonical Wnt signaling: multilayered mediators, signaling mechanisms and major signaling crosstalk. Genes Dis 2023 doi: 10.1016/j.gendis.2023.01.030 [Epub ahead of print]
- Chae WJ, Bothwell ALM. Canonical and non-canonical Wnt signaling in immune cells. Trends Immunol 2018;39:830-847 https://doi.org/10.1016/j.it.2018.08.006
- Bugter JM, Fenderico N, Maurice MM. Mutations and mechanisms of Wnt pathway tumour suppressors in cancer. Nat Rev Cancer 2021;21:5-21 https://doi.org/10.1038/s41568-020-00307-z
- Munemitsu S, Albert I, Souza B, Rubinfeld B, Polakis P. Regulation of intracellular beta-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc Natl Acad Sci U S A 1995;92:3046-50 https://doi.org/10.1073/pnas.92.7.3046
- Rubinfeld B, Albert I, Porfiri E, Fiol C, Munemitsu S, Polakis P. Binding of GSK3β to the APC-β-catenin complex and regulation of complex assembly. Science 1996;272:1023-1026 https://doi.org/10.1126/science.272.5264.1023
- Rubinfeld B, Souza B, Albert I, Muller O, Chamberlain SH, Masiarz FR, Munemitsu S, Polakis P. Association of the APC gene product with β-catenin. Science 1993;262:1731-1734 https://doi.org/10.1126/science.8259518
- Liu C, Li Y, Semenov M, Han C, Baeg GH, Tan Y, Zhang Z, Lin X, He X. Control of β-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 2002;108:837-847 https://doi.org/10.1016/S0092-8674(02)00685-2
- Hart M, Concordet JP, Lassot I, Albert I, del los Santos R, Durand H, Perret C, Rubinfeld B, Margottin F, Benarous R, Polakis P. The F-box protein β-TrCP associates with phosphorylated β-catenin and regulates its activity in the cell. Curr Biol 1999;9:207-210 https://doi.org/10.1016/S0960-9822(99)80091-8
- Amit S, Hatzubai A, Birman Y, Andersen JS, Ben-Shushan E, Mann M, Ben-Neriah Y, Alkalay I. Axin-mediated CKI phosphorylation of β-catenin at Ser 45: a molecular switch for the Wnt pathway. Genes Dev 2002;16:1066-1076 https://doi.org/10.1101/gad.230302
- Tamai K, Semenov M, Kato Y, Spokony R, Liu C, Katsuyama Y, Hess F, Saint-Jeannet JP, He X. LDL-receptor-related proteins in Wnt signal transduction. Nature 2000;407:530-535 https://doi.org/10.1038/35035117
- Nusse R, Clevers H. Wnt/β-catenin signaling, disease, and emerging therapeutic modalities. Cell 2017;169:985-999 https://doi.org/10.1016/j.cell.2017.05.016
- Giannakis M, Hodis E, Jasmine Mu X, Yamauchi M, Rosenbluh J, Cibulskis K, Saksena G, Lawrence MS, Qian ZR, Nishihara R, Van Allen EM, Hahn WC, Gabriel SB, Lander ES, Getz G, Ogino S, Fuchs CS, Garraway LA. RNF43 is frequently mutated in colorectal and endometrial cancers. Nat Genet 2014;46:1264-1266 https://doi.org/10.1038/ng.3127
- Sugiura T, Yamaguchi A, Miyamoto K. A cancer-associated RING finger protein, RNF43, is a ubiquitin ligase that interacts with a nuclear protein, HAP95. Exp Cell Res 2008;314:1519-1528 https://doi.org/10.1016/j.yexcr.2008.01.013
- Hao HX, Xie Y, Zhang Y, Charlat O, Oster E, Avello M, Lei H, Mickanin C, Liu D, Ruffner H, Mao X, Ma Q, Zamponi R, Bouwmeester T, Finan PM, Kirschner MW, Porter JA, Serluca FC, Cong F. ZNRF3 promotes Wnt receptor turnover in an R-spondin-sensitive manner. Nature 2012;485:195-200 https://doi.org/10.1038/nature11019
- Bian J, Dannappel M, Wan C, Firestein R. Transcriptional regulation of Wnt/β-catenin pathway in colorectal cancer. Cells 2020;9:2125
- Tsukiyama T, Koo BK, Hatakeyama S. Post-translational Wnt receptor regulation: is the fog slowly clearing?: the molecular mechanism of RNF43/ZNRF3 ubiquitin ligases is not yet fully elucidated and still controversial. Bioessays 2021;43:e2000297
- Tsukiyama T, Fukui A, Terai S, Fujioka Y, Shinada K, Takahashi H, Yamaguchi TP, Ohba Y, Hatakeyama S. Molecular role of RNF43 in canonical and noncanonical Wnt signaling. Mol Cell Biol 2015;35:2007-2023 https://doi.org/10.1128/MCB.00159-15
- Carmon KS, Gong X, Lin Q, Thomas A, Liu Q. R-spondins function as ligands of the orphan receptors LGR4 and LGR5 to regulate Wnt/β-catenin signaling. Proc Natl Acad Sci U S A 2011;108:11452-11457 https://doi.org/10.1073/pnas.1106083108
- de Lau W, Barker N, Low TY, Koo BK, Li VS, Teunissen H, Kujala P, Haegebarth A, Peters PJ, van de Wetering M, Stange DE, van Es JE, Guardavaccaro D, Schasfoort RB, Mohri Y, Nishimori K, Mohammed S, Heck AJ, Clevers H. Lgr5 homologues associate with Wnt receptors and mediate R-spondin signalling. Nature 2011;476:293-297 https://doi.org/10.1038/nature10337
- Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, Clevers H. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007;449:1003-1007 https://doi.org/10.1038/nature06196
- Barker N, Rookmaaker MB, Kujala P, Ng A, Leushacke M, Snippert H, van de Wetering M, Tan S, Van Es JH, Huch M, Poulsom R, Verhaar MC, Peters PJ, Clevers H. Lgr5(+ve) stem/progenitor cells contribute to nephron formation during kidney development. Cell Rep 2012;2:540-552 https://doi.org/10.1016/j.celrep.2012.08.018
- de Visser KE, Ciampricotti M, Michalak EM, Tan DW, Speksnijder EN, Hau CS, Clevers H, Barker N, Jonkers J. Developmental stage-specific contribution of LGR5(+) cells to basal and luminal epithelial lineages in the postnatal mammary gland. J Pathol 2012;228:300-309 https://doi.org/10.1002/path.4096
- Snippert HJ, Haegebarth A, Kasper M, Jaks V, van Es JH, Barker N, van de Wetering M, van den Born M, Begthel H, Vries RG, Stange DE, Toftgard R, Clevers H. Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science 2010;327:1385-1389 https://doi.org/10.1126/science.1184733
- Wang Y, Dong J, Li D, Lai L, Siwko S, Li Y, Liu M. Lgr4 regulates mammary gland development and stem cell activity through the pluripotency transcription factor Sox2. Stem Cells 2013;31:1921-1931 https://doi.org/10.1002/stem.1438
- Xie Y, Zamponi R, Charlat O, Ramones M, Swalley S, Jiang X, Rivera D, Tschantz W, Lu B, Quinn L, Dimitri C, Parker J, Jeffery D, Wilcox SK, Watrobka M, LeMotte P, Granda B, Porter JA, Myer VE, Loew A, Cong F. Interaction with both ZNRF3 and LGR4 is required for the signalling activity of R-spondin. EMBO Rep 2013;14:1120-1126 https://doi.org/10.1038/embor.2013.167
- Kim KA, Kakitani M, Zhao J, Oshima T, Tang T, Binnerts M, Liu Y, Boyle B, Park E, Emtage P, Funk WD, Tomizuka K. Mitogenic influence of human R-spondin1 on the intestinal epithelium. Science 2005;309:1256-1259 https://doi.org/10.1126/science.1112521
- Kazanskaya O, Glinka A, del Barco Barrantes I, Stannek P, Niehrs C, Wu W. R-Spondin2 is a secreted activator of Wnt/β-catenin signaling and is required for Xenopus myogenesis. Dev Cell 2004;7:525-534 https://doi.org/10.1016/j.devcel.2004.07.019
- de Lau W, Peng WC, Gros P, Clevers H. The R-spondin/Lgr5/Rnf43 module: regulator of Wnt signal strength. Genes Dev 2014;28:305-316 https://doi.org/10.1101/gad.235473.113
- Peng WC, de Lau W, Madoori PK, Forneris F, Granneman JC, Clevers H, Gros P. Structures of Wnt-antagonist ZNRF3 and its complex with R-spondin 1 and implications for signaling. PLoS One 2013;8:e83110
- Zebisch M, Xu Y, Krastev C, MacDonald BT, Chen M, Gilbert RJ, He X, Jones EY. Structural and molecular basis of ZNRF3/RNF43 transmembrane ubiquitin ligase inhibition by the Wnt agonist R-spondin. Nat Commun 2013;4:2787
- Jiang X, Charlat O, Zamponi R, Yang Y, Cong F. Dishevelled promotes Wnt receptor degradation through recruitment of ZNRF3/RNF43 E3 ubiquitin ligases. Mol Cell 2015;58:522-533 https://doi.org/10.1016/j.molcel.2015.03.015
- Lebensohn AM, Rohatgi R. R-spondins can potentiate WNT signaling without LGRs. Elife 2018;7:e33126
- Szenker-Ravi E, Altunoglu U, Leushacke M, Bosso-Lefevre C, Khatoo M, Thi Tran H, Naert T, Noelanders R, Hajamohideen A, Beneteau C, de Sousa SB, Karaman B, Latypova X, Basaran S, Yucel EB, Tan TT, Vlaminck L, Nayak SS, Shukla A, Girisha KM, Le Caignec C, Soshnikova N, Uyguner ZO, Vleminckx K, Barker N, Kayserili H, Reversade B. RSPO2 inhibition of RNF43 and ZNRF3 governs limb development independently of LGR4/5/6. Nature 2018;557:564-569 https://doi.org/10.1038/s41586-018-0118-y
- Schulte G, Bryja V. The frizzled family of unconventional G-protein-coupled receptors. Trends Pharmacol Sci 2007;28:518-525 https://doi.org/10.1016/j.tips.2007.09.001
- Bhanot P, Brink M, Samos CH, Hsieh JC, Wang Y, Macke JP, Andrew D, Nathans J, Nusse R. A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature 1996;382:225-230 https://doi.org/10.1038/382225a0
- Tauriello DV, Jordens I, Kirchner K, Slootstra JW, Kruitwagen T, Bouwman BA, Noutsou M, Rudiger SG, Schwamborn K, Schambony A, Maurice MM. Wnt/β-catenin signaling requires interaction of the Dishevelled DEP domain and C terminus with a discontinuous motif in Frizzled. Proc Natl Acad Sci U S A 2012;109:E812-E820 https://doi.org/10.1073/pnas.1114802109
- Umbhauer M, Djiane A, Goisset C, Penzo-Mendez A, Riou JF, Boucaut JC, Shi DL. The C-terminal cytoplasmic Lys-thr-X-X-X-Trp motif in frizzled receptors mediates Wnt/beta-catenin signalling. EMBO J 2000;19:4944-4954 https://doi.org/10.1093/emboj/19.18.4944
- Ko SB, Mihara E, Park Y, Roh K, Kang C, Takagi J, Bang I, Choi HJ. Functional role of the frizzled linker domain in the Wnt signaling pathway. Commun Biol 2022;5:421
- Spit M, Fenderico N, Jordens I, Radaszkiewicz T, Lindeboom RG, Bugter JM, Cristobal A, Ootes L, van Osch M, Janssen E, Boonekamp KE, Hanakova K, Potesil D, Zdrahal Z, Boj SF, Medema JP, Bryja V, Koo BK, Vermeulen M, Maurice MM. RNF43 truncations trap CK1 to drive niche-independent self-renewal in cancer. EMBO J 2020;39:e103932
- Tsukiyama T, Zou J, Kim J, Ogamino S, Shino Y, Masuda T, Merenda A, Matsumoto M, Fujioka Y, Hirose T, Terai S, Takahashi H, Ishitani T, Nakayama KI, Ohba Y, Koo BK, Hatakeyama S. A phospho-switch controls RNF43-mediated degradation of Wnt receptors to suppress tumorigenesis. Nat Commun 2020;11:4586
- Ci Y, Li X, Chen M, Zhong J, North BJ, Inuzuka H, He X, Li Y, Guo J, Dai X. SCFβ-TRCP E3 ubiquitin ligase targets the tumor suppressor ZNRF3 for ubiquitination and degradation. Protein Cell 2018;9:879-889 https://doi.org/10.1007/s13238-018-0510-2
- Chang LS, Kim M, Glinka A, Reinhard C, Niehrs C. The tumor suppressor PTPRK promotes ZNRF3 internalization and is required for Wnt inhibition in the Spemann organizer. Elife 2020;9:e51248
- Kim M, Reinhard C, Niehrs C. A MET-PTPRK kinasephosphatase rheostat controls ZNRF3 and Wnt signaling. Elife 2021;10:e70885
- Martin BL, Kimelman D. Wnt signaling and the evolution of embryonic posterior development. Curr Biol 2009;19:R215-R219 https://doi.org/10.1016/j.cub.2009.01.052
- Loh KM, van Amerongen R, Nusse R. Generating cellular diversity and spatial form: Wnt signaling and the evolution of multicellular animals. Dev Cell 2016;38:643-655 https://doi.org/10.1016/j.devcel.2016.08.011
- Eichinger L, Pachebat JA, Glockner G, Rajandream MA, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, Tunggal B, Kummerfeld S, Madera M, Konfortov BA, Rivero F, Bankier AT, Lehmann R, Hamlin N, Davies R, Gaudet P, Fey P, Pilcher K, Chen G, Saunders D, Sodergren E, Davis P, Kerhornou A, Nie X, Hall N, Anjard C, Hemphill L, Bason N, Farbrother P, Desany B, Just E, Morio T, Rost R, Churcher C, Cooper J, Haydock S, van Driessche N, Cronin A, Goodhead I, Muzny D, Mourier T, Pain A, Lu M, Harper D, Lindsay R, Hauser H, James K, Quiles M, Madan Babu M, Saito T, Buchrieser C, Wardroper A, Felder M, Thangavelu M, Johnson D, Knights A, Loulseged H, Mungall K, Oliver K, Price C, Quail MA, Urushihara H, Hernandez J, Rabbinowitsch E, Steffen D, Sanders M, Ma J, Kohara Y, Sharp S, Simmonds M, Spiegler S, Tivey A, Sugano S, White B, Walker D, Woodward J, Winckler T, Tanaka Y, Shaulsky G, Schleicher M, Weinstock G, Rosenthal A, Cox EC, Chisholm RL, Gibbs R, Loomis WF, Platzer M, Kay RR, Williams J, Dear PH, Noegel AA, Barrell B, Kuspa A. The genome of the social amoeba Dictyostelium discoideum. Nature 2005;435:43-57 https://doi.org/10.1038/nature03481
- Prabhu Y, Eichinger L. The Dictyostelium repertoire of seven transmembrane domain receptors. Eur J Cell Biol 2006;85:937-946 https://doi.org/10.1016/j.ejcb.2006.04.003
- Harwood AJ. Dictyostelium development: a prototypic Wnt pathway? Methods Mol Biol 2008;469:21-32 https://doi.org/10.1007/978-1-60327-469-2_2
- Cai C, Tang YD, Zhai J, Zheng C. The RING finger protein family in health and disease. Signal Transduct Target Ther 2022;7:300
- Anandasabapathy N, Ford GS, Bloom D, Holness C, Paragas V, Seroogy C, Skrenta H, Hollenhorst M, Fathman CG, Soares L. GRAIL: an E3 ubiquitin ligase that inhibits cytokine gene transcription is expressed in anergic CD4+ T cells. Immunity 2003;18:535-547 https://doi.org/10.1016/S1074-7613(03)00084-0
- Wang H, Rogers JC, Jiang L. Plant RMR proteins: unique vacuolar sorting receptors that couple ligand sorting with membrane internalization. FEBS J 2011;278:59-68 https://doi.org/10.1111/j.1742-4658.2010.07923.x
- Zebisch M, Jones EY. ZNRF3/RNF43--a direct linkage of extracellular recognition and E3 ligase activity to modulate cell surface signalling. Prog Biophys Mol Biol 2015;118:112-118 https://doi.org/10.1016/j.pbiomolbio.2015.04.006