TMEM98 is a negative regulator of FRAT mediated Wnt/ß-catenin signalling
Autoři:
Tanne van der Wal aff001; Jan-Paul Lambooij aff003; Renée van Amerongen aff001
Působiště autorů:
Section of Molecular Cytology, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, the Netherlands
aff001; Van Leeuwenhoek Centre for Advanced Microscopy, University of Amsterdam, Amsterdam, the Netherlands
aff002; Division of Molecular Genetics, Netherlands Cancer Institute, Amsterdam, the Netherlands
aff003
Vyšlo v časopise:
PLoS ONE 15(1)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0227435
Souhrn
Wnt/ß-catenin signalling is crucial for maintaining the balance between cell proliferation and differentiation, both during tissue morphogenesis and in tissue maintenance throughout postnatal life. Whereas the signalling activities of the core Wnt/ß-catenin pathway components are understood in great detail, far less is known about the precise role and regulation of the many different modulators of Wnt/ß-catenin signalling that have been identified to date. Here we describe TMEM98, a putative transmembrane protein of unknown function, as an interaction partner and regulator of the GSK3-binding protein FRAT2. We show that TMEM98 reduces FRAT2 protein levels and, accordingly, inhibits the FRAT2-mediated induction of ß-catenin/TCF signalling. We also characterize the intracellular trafficking of TMEM98 in more detail and show that it is recycled between the plasma membrane and the Golgi. Together, our findings not only reveal a new layer of regulation for Wnt/ß-catenin signalling, but also a new biological activity for TMEM98.
Klíčová slova:
Cell membranes – Confocal microscopy – Endosomes – Golgi apparatus – Lysosomes – Membrane proteins – Messenger RNA – Wnt signaling cascade
Zdroje
1. Biechele S, Cox BJ, Rossant J. Porcupine homolog is required for canonical Wnt signaling and gastrulation in mouse embryos. Dev Biol. 2011. doi: 10.1016/j.ydbio.2011.04.029 21554866
2. Summerhurst K, Stark M, Sharpe J, Davidson D, Murphy P. 3D representation of Wnt and Frizzled gene expression patterns in the mouse embryo at embryonic day 11.5 (Ts19). Gene Expr Patterns. 2008;8: 331–48. doi: 10.1016/j.gep.2008.01.007 18364260
3. Janda CY, Waghray D, Levin AM, Thomas C, Garcia KC. Structural basis of Wnt recognition by frizzled. Science (80-). 2012. doi: 10.1126/science.1222879 22653731
4. Tamai K, Semenov M, Kato Y, Spokony R, Liu C, Katsuyama Y, et al. LDL-receptor-related proteins in Wnt signal transduction. Nature. 2000. doi: 10.1038/35035117 11029007
5. Inoue T, Oz HS, Wiland D, Gharib S, Deshpande R, Hill RJ, et al. C. elegans LIN-18 is a Ryk ortholog and functions in parallel to LIN-17/Frizzled in Wnt signaling. Cell. 2004. doi: 10.1016/j.cell.2004.09.001 15369677
6. Oishi I, Suzuki H, Onishi N, Takada R, Kani S, Ohkawara B, et al. The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes to Cells. 2003. doi: 10.1046/j.1365-2443.2003.00662.x 12839624
7. Bilić J, Huang YL, Davidson G, Zimmermann T, Cruciat CM, Bienz M, et al. Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science (80-). 2007. doi: 10.1126/science.1137065 17569865
8. Li VSW, Ng SS, Boersema PJ, Low TY, Karthaus WR, Gerlach JP, et al. Wnt Signaling through Inhibition of β-Catenin Degradation in an Intact Axin1 Complex. Cell. 2012;149: 1245–1256. doi: 10.1016/j.cell.2012.05.002 22682247
9. DeBruine ZJ, Xu HE, Melcher K. Assembly and architecture of the Wnt/β-catenin signalosome at the membrane. British Journal of Pharmacology. 2017. doi: 10.1111/bph.14048 28941231
10. Gammons M, Bienz M. Multiprotein complexes governing Wnt signal transduction. Current Opinion in Cell Biology. 2018. doi: 10.1016/j.ceb.2017.10.008 29153704
11. Jonkers J, Van Amerongen R, Van Der Valk M, Robanus-Maandag E, Molenaar M, Destrée O, et al. In vivo analysis of Frat1 deficiency suggests compensatory activity of Frat3. Mech Dev. 1999;88: 183–194. doi: 10.1016/s0925-4773(99)00187-2 10534617
12. van Amerongen R, van der Gulden H, Bleeker F, Jonkers J, Berns A. Characterization and functional analysis of the murine Frat2 gene. J Biol Chem. 2004;279: 26967–26974. doi: 10.1074/jbc.M400439200 15073180
13. Yost C, Farr GH, Pierce SB, Ferkey DM, Chen MM, Kimelman D. GBP, an inhibitor of GSK-3, is implicated in Xenopus development and oncogenesis. Cell. 1998;93: 1031–1041. doi: 10.1016/s0092-8674(00)81208-8 9635432
14. Fraser E, Young N, Dajani R, Franca-Koh J, Ryves J, Williams RSB, et al. Identification of the Axin and Frat Binding Region of Glycogen Synthase Kinase-3. J Biol Chem. 2002;277: 2176–2185. doi: 10.1074/jbc.M109462200 11707456
15. Dajani R, Fraser E, Roe SM, Yeo M, Good VM, Thompson V, et al. Structural basis for recruitment of glycogen synthase kinase 3B to the axin-APC scaffold complex. EMBO J. 2003. doi: 10.1093/emboj/cdg068 12554650
16. Jonkers J, Korswagen HC, Acton D, Breuer M, Berns A. Activation of a novel proto-oncogene, Frat1, contributes to progression of mouse T-cell lymphomas. EMBO J. 1997. doi: 10.1093/emboj/16.3.441 9034327
17. Wang Y, Liu S, Zhu H, Zhang W, Zhang G, Zhou X, et al. FRAT1 overexpression leads to aberrant activation of β-catenin/TCF pathway in esophageal squamous cell carcinoma. Int J Cancer. 2008;123: 561–568. doi: 10.1002/ijc.23600 18498136
18. Zhang Y, Han Y, Zheng R, Yu JH, Miao Y, Wang L, et al. Expression of Frat1 correlates with expression of β-catenin and is associated with a poor clinical outcome in human SCC and AC. Tumor Biol. 2012;33: 1437–1444. doi: 10.1007/s13277-012-0394-3 22528942
19. Guo G, Zhong C-L, Liu Y, Mao X-G, Zhang Z, Jin J, et al. Overexpression of FRAT1 is associated with malignant phenotype and poor prognosis in human gliomas. Dis Markers. 2015. doi: 10.1155/2015/289750 25922553
20. Zhang Y, Yu J-H, Lin X-Y, Miao Y, Han Y, Fan C-F, et al. Overexpression of Frat1 correlates with malignant phenotype and advanced stage in human non-small cell lung cancer. Virchows Arch. 2011. doi: 10.1007/s00428-011-1135-5 21818639
21. Wang Y, Hewitt SM, Liu S, Zhou X, Zhu H, Zhou C, et al. Tissue microarray analysis of human FRAT1 expression and its correlation with the subcellular localisation of beta-catenin in ovarian tumours. Br J Cancer. 2006;94: 686–91. doi: 10.1038/sj.bjc.6602988 16479254
22. Van Amerongen R, Nawijn M, Franca-Koh J, Zevenhoven J, Van Der Gulden H, Jonkers J, et al. Frat is dispensable for canonical Wnt signaling in mammals. Genes Dev. 2005;19: 425–430. doi: 10.1101/gad.326705 15681612
23. Walf-Vorderwülbecke V, De Boer J, Horton SJ, Van Amerongen R, Proost N, Berns A, et al. Frat2 mediates the oncogenic activation of Rac by MLL fusions. Blood. 2012;120: 4819–4828. doi: 10.1182/blood-2012-05-432534 23074275
24. Van Amerongen R, Nawijn MC, Lambooij JP-P, Proost N, Jonkers J, Berns A. Frat oncoproteins act at the crossroad of canonical and noncanonical Wnt-signaling pathways. Oncogene. 2010;29: 93–104. doi: 10.1038/onc.2009.310 19802005
25. Awadalla MS, Burdon KP, Souzeau E, Landers J, Hewitt AW, Sharma S, et al. Mutation in TMEM98 in a large white kindred with autosomal dominant nanophthalmos linked to 17p12-q12. JAMA Ophthalmol. 2014;132: 970–7. doi: 10.1001/jamaophthalmol.2014.946 24852644
26. Khorram D, Choi M, Roos BR, Stone EM, Kopel T, Allen R, et al. Novel TMEM98 mutations in pedigrees with autosomal dominant nanophthalmos. Mol Vis. 2015.
27. Mehrle A, Rosenfelder H, Schupp I, del Val C, Arlt D, Hahne F, et al. The LIFEdb database in 2006. Nucleic Acids Res. 2006;34: D415–8. doi: 10.1093/nar/gkj139 16381901
28. Bannasch D, Mehrle A, Glatting K-H, Pepperkok R, Poustka A, Wiemann S. LIFEdb: a database for functional genomics experiments integrating information from external sources, and serving as a sample tracking system. Nucleic Acids Res. 2004;32: D505–8. doi: 10.1093/nar/gkh022 14681468
29. Simpson JC, Wellenreuther R, Poustka A, Pepperkok R, Wiemann S. Systematic subcellular localization of novel proteins identified by large-scale cDNA sequencing. EMBO Rep. 2000;1: 287–292. doi: 10.1093/embo-reports/kvd058 11256614
30. Fu W, Cheng Y, Zhang Y, Mo X, Li T, Liu Y, et al. The Secreted Form of Transmembrane Protein 98 Promotes the Differentiation of T Helper 1 Cells. J Interferon Cytokine Res. 2015;35: 720–733. doi: 10.1089/jir.2014.0110 25946230
31. Stark C. BioGRID: a general repository for interaction datasets. Nucleic Acids Res. 2006. doi: 10.1093/nar/gkj109 16381927
32. Chatr-Aryamontri A, Oughtred R, Boucher L, Rust J, Chang C, Kolas NK, et al. The BioGRID interaction database: 2017 update. Nucleic Acids Res. 2017. doi: 10.1093/nar/gkw1102 27980099
33. Vinayagam A, Stelzl U, Foulle R, Plassmann S, Zenkner M, Timm J, et al. A directed protein interaction network for investigating intracellular signal transduction. Sci Signal. 2011. doi: 10.1126/scisignal.2001699 21900206
34. Díaz E, Schimmöller F, Pfeffer SR. A novel Rab9 effector required for endosome-to-TGN transport. J Cell Biol. 1997. doi: 10.1083/jcb.138.2.283 9230071
35. Simonsen A, Lippé R, Christoforidis S, Gaullier JM, Brech A, Callaghan J, et al. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature. 1998. doi: 10.1038/28879 9697774
36. Simonsen A, Gaullier JM, D’Arrigo A, Stenmark H. The Rab5 effector EEA1 interacts directly with syntaxin-6. J Biol Chem. 1999. doi: 10.1074/jbc.274.41.28857 10506127
37. Goedhart J, Von Stetten D, Noirclerc-Savoye M, Lelimousin M, Joosen L, Hink MA, et al. Structure-guided evolution of cyan fluorescent proteins towards a quantum yield of 93%. Nat Commun. 2012;3. doi: 10.1038/ncomms1738 22434194
38. Delevoye C, Miserey-Lenkei S, Montagnac G, Gilles-Marsens F, Paul-Gilloteaux P, Giordano F, et al. Recycling endosome tubule morphogenesis from sorting endosomes requires the kinesin motor KIF13A. Cell Rep. 2014. doi: 10.1016/j.celrep.2014.01.002 24462287
39. Puthenveedu MA, Lauffer B, Temkin P, Vistein R, Carlton P, Thorn K, et al. Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell. 2010. doi: 10.1016/j.cell.2010.10.003 21111236
40. Huotari J, Helenius A. Endosome maturation. EMBO Journal. 2011. doi: 10.1038/emboj.2011.286 21878991
41. Barbero P, Bittova L, Pfeffer SR. Visualization of Rab9-mediated vesicle transport from endosomes to the trans-Golgi in living cells. J Cell Biol. 2002. doi: 10.1083/jcb.200109030 11827983
42. Glinka A, Wu W, Delius H, Monaghan AP, Blumenstock C, Niehrs C. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature. 1998;391: 357–362. doi: 10.1038/34848 9450748
43. Szenker-Ravi E, Altunoglu U, Leushacke M, Bosso-Lefèvre C, Khatoo M, Thi Tran H, et al. RSPO2 inhibition of RNF43 and ZNRF3 governs limb development independently of LGR4/5/6. Nature. 2018. doi: 10.1038/s41586-018-0118-y 29769720
44. 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. doi: 10.1016/j.devcel.2004.07.019 15469841
45. Lebensohn AM, Rohatgi R. R-spondins can potentiate WNT signaling without LGRs. Elife. 2018. doi: 10.7554/eLife.33126 29405118
46. De Lau W, Barker N, Low TY, Koo BK, Li VSW, Teunissen H, et al. Lgr5 homologues associate with Wnt receptors and mediate R-spondin signalling. Nature. 2011. doi: 10.1038/nature10337 21727895
47. 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/ -catenin signaling. Proc Natl Acad Sci. 2011. doi: 10.1073/pnas.1106083108 21693646
48. Glinka A, Dolde C, Kirsch N, Huang YL, Kazanskaya O, Ingelfinger D, et al. LGR4 and LGR5 are R-spondin receptors mediating Wnt/β-catenin and Wnt/PCP signalling. EMBO Rep. 2011. doi: 10.1038/embor.2011.175 21909076
49. Jho E, Zhang T, Domon C, Joo C-K, Freund J-N, Costantini F. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol. 2002;22: 1172–83. doi: 10.1128/MCB.22.4.1172-1183.2002 11809808
50. Lustig B, Jerchow B, Sachs M, Weiler S, Pietsch T, Karsten U, et al. Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol Cell Biol. 2002;22: 1184–93. doi: 10.1128/MCB.22.4.1184-1193.2002 11809809
51. Fu W, Cheng Y, Zhang Y, Mo X, Li T, Liu Y, et al. The Secreted Form of Transmembrane Protein 98 Promotes the Differentiation of T Helper 1 Cells. J Interf Cytokine Res. 2015. doi: 10.1089/jir.2014.0110 25946230
52. Hsu VW, Bai M, Li J. Getting active: protein sorting in endocytic recycling. Nat Rev Mol Cell Biol. 2012;13: 323–328. doi: 10.1038/nrm3332 22498832
53. Rink J, Ghigo E, Kalaidzidis Y, Zerial M. Rab Conversion as a Mechanism of Progression from Early to Late Endosomes. Cell. 2005;122: 735–749. doi: 10.1016/j.cell.2005.06.043 16143105
54. Villaseñor R, Kalaidzidis Y, Zerial M. Signal processing by the endosomal system. Curr Opin Cell Biol. 2016;39: 53–60. doi: 10.1016/j.ceb.2016.02.002 26921695
55. Woodman PG, Futter CE. Multivesicular bodies: co-ordinated progression to maturity. Curr Opin Cell Biol. 2008;20: 408–414. doi: 10.1016/j.ceb.2008.04.001 18502633
56. Chairoungdua A, Smith DL, Pochard P, Hull M, Caplan MJ. Exosome release of β-catenin: A novel mechanism that antagonizes Wnt signaling. J Cell Biol. 2010. doi: 10.1083/jcb.201002049 20837771
57. Taelman VF, Dobrowolski R, Plouhinec JL, Fuentealba LC, Vorwald PP, Gumper I, et al. Wnt signaling requires sequestration of Glycogen Synthase Kinase 3 inside multivesicular endosomes. Cell. 2010. doi: 10.1016/j.cell.2010.11.034 21183076
58. Snyder JC, Rochelle LK, Lyerly HK, Caron MG, Barak LS. Constitutive Internalization of the Leucine-rich G Protein-coupled Receptor-5 (LGR5) to the Trans-Golgi Network. J Biol Chem. 2013;288: 10286–10297. doi: 10.1074/jbc.M112.447540 23439653
59. Weaver C. GBP binds kinesin light chain and translocates during cortical rotation in Xenopus eggs. Development. 2003. doi: 10.1242/dev.00737 14507779
60. Loubéry S, Wilhelm C, Hurbain I, Neveu S, Louvard D, Coudrier E. Different microtubule motors move early and late endocytic compartments. Traffic. 2008. doi: 10.1111/j.1600-0854.2008.00704.x 18194411
61. Vitrac H, Bogdanov M, Dowhan W. In vitro reconstitution of lipid-dependent dual topology and postassembly topological switching of a membrane protein. Proc Natl Acad Sci. 2013. doi: 10.1073/pnas.1304375110 23690595
62. Mao M, Chen J, Li X, Wu Z. siRNA-TMEM98 inhibits the invasion and migration of lung cancer cells. Int J Clin Exp Pathol. 2015;8: 15661–9. Available: http://www.ncbi.nlm.nih.gov/pubmed/26884835 26884835
63. Ng KT-P, Lo CM, Guo DY, Qi X, Li CX, Geng W, et al. Identification of Transmembrane Protein 98 as a Novel Chemoresistance-Conferring Gene in Hepatocellular Carcinoma. Mol Cancer Ther. 2014;13: 1285–1297. doi: 10.1158/1535-7163.MCT-13-0806 24608572
64. Huang H, Teng P, Du J, Meng J, Hu X, Tang T, et al. Interactive Repression of MYRF Self-Cleavage and Activity in Oligodendrocyte Differentiation by TMEM98 Protein. J Neurosci. 2018. doi: 10.1523/JNEUROSCI.0154-18.2018 30249802
65. Garnai SJ, Brinkmeier ML, Emery B, Aleman TS, Pyle LC, Veleva-Rotse B, et al. Variants in myelin regulatory factor (MYRF) cause autosomal dominant and syndromic nanophthalmos in humans and retinal degeneration in mice. PLoS Genet. 2019;15: e1008130. doi: 10.1371/journal.pgen.1008130 31048900
66. Cross SH, Mckie L, Keighren M, West K, Thaung C, Davey T, et al. Missense Mutations in the Human Nanophthalmos Gene TMEM98 Cause Retinal Defects in the Mouse. bioRxiv. 2019. doi: 10.1101/513846
67. Fromont-Racine M, Rain J-CC, Legrain P. Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nat Genet. 1997;16: 277–282. doi: 10.1038/ng0797-277 9207794
68. Rain JC, Selig L, De Reuse H, Battaglia V, Reverdy C, Simon S, et al. The protein-protein interaction map of Helicobacter pylori. Nature. 2001;409: 211–215. doi: 10.1038/35051615 11196647
69. Formstecher E, Aresta S, Collura V, Hamburger A, Meil A, Trehin A, et al. Protein interaction mapping: A Drosophila case study. Genome Res. 2005;15: 376–384. doi: 10.1101/gr.2659105 15710747
70. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research. 1997. pp. 3389–3402. doi: 10.1093/nar/25.17.3389 9254694
71. Cranfill PJ, Sell BR, Baird MA, Allen JR, Lavagnino Z, De Gruiter HM, et al. Quantitative assessment of fluorescent proteins. Nat Methods. 2016. doi: 10.1038/nmeth.3891 27240257
72. Lee J-G, Takahama S, Zhang G, Tomarev SI, Ye Y. Unconventional secretion of misfolded proteins promotes adaptation to proteasome dysfunction in mammalian cells. Nat Cell Biol. 2016;18: 765–776. doi: 10.1038/ncb3372 27295555
73. Chang KT, Guo J, Di Ronza A, Sardiello M. Aminode: Identification of Evolutionary Constraints in the Human Proteome. Sci Rep. 2018. doi: 10.1038/s41598-018-19744-w 29358731
Článek vyšel v časopise
PLOS One
2020 Číslo 1
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Proč při poslechu některé muziky prostě musíme tančit?
- Je libo čepici místo mozkového implantátu?
- Chůze do schodů pomáhá prodloužit život a vyhnout se srdečním chorobám
- Pomůže v budoucnu s triáží na pohotovostech umělá inteligence?
Nejčtenější v tomto čísle
- Severity of misophonia symptoms is associated with worse cognitive control when exposed to misophonia trigger sounds
- Chemical analysis of snus products from the United States and northern Europe
- Calcium dobesilate reduces VEGF signaling by interfering with heparan sulfate binding site and protects from vascular complications in diabetic mice
- Effect of Lactobacillus acidophilus D2/CSL (CECT 4529) supplementation in drinking water on chicken crop and caeca microbiome
Zvyšte si kvalifikaci online z pohodlí domova
Všechny kurzy