Cholesterol selectively activates canonical Wnt signalling over non-canonical Wnt signalling

Nature Communications

Volumn 5, Issue , 2014, Pages

  Sheng, Ren ^a   Kim, Hyunjoon ^b   Lee, Hyeyoon ^b   Xin, Yao ^a   Chen, Yong ^a   Tian, Wen ^a   Cui, Yang ^a   Choi, Jong Cheol ^c   Doh, Junsang ^c   Han, Jin Kwan ^b   Cho, Wonhwa ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b Department of Life Science   (South Korea)

^c Pohang University of Science and Technology (POSTECH)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CHOLESTEROL; DISHEVELLED PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; WNT PROTEIN; DISHEVELLED PROTEINS; PHOSPHOPROTEIN; PROTEIN BINDING; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ARTICLE; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOLECULAR IMAGING; MOLECULAR MECHANICS; PDZ DOMAIN; SIGNAL TRANSDUCTION; ANIMAL; HELA CELL LINE; IN SITU HYBRIDIZATION; METABOLISM; PHYSIOLOGY; WESTERN BLOTTING; WNT SIGNALING PATHWAY; XENOPUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLOTTING, WESTERN; CHOLESTEROL; HELA CELLS; HUMANS; IN SITU HYBRIDIZATION; PHOSPHOPROTEINS; PROTEIN BINDING; SIGNAL TRANSDUCTION; WNT PROTEINS; WNT SIGNALING PATHWAY; XENOPUS;

EID: 84904489367     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5393     Document Type: Article

References (70)

1. Logan, C. Y. & Nusse, R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810 (2004).
2. Clevers, H. Wnt/beta-catenin signaling in development and disease. Cell 127, 469-480 (2006).
3. Klaus, A. & Birchmeier, W. Wnt signalling and its impact on development and cancer. Nat. Rev. Cancer 8, 387-398 (2008).
4. MacDonald, B. T., Tamai, K. & He, X. Wnt/beta-catenin signaling: Components, mechanisms, and diseases. Dev. Cell 17, 9-26 (2009).
5. Gao, C. & Chen, Y. G. Dishevelled: the hub of Wnt signaling. Cell. Signal. 22, 717-727 (2010).
6. Kim, S. E. et al. Wnt stabilization of beta-catenin reveals principles for morphogen receptor-scaffold assemblies. Science 340, 867-870 (2013).
7. Simons, M. & Mlodzik, M. Planar cell polarity signaling: From fly development to human disease. Annu. Rev. Genet. 42, 517-540 (2008).
8. Anastas, J. N. & Moon, R. T. WNT signalling pathways as therapeutic targets in cancer. Nat. Rev. Cancer 13, 11-26 (2013).
9. Chen, B. et al. Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat. Chem. Biol. 5, 100-107 (2009).
10. Thorne, C. A. et al. Small-molecule inhibition of Wnt signaling through activation of casein kinase 1alpha. Nat. Chem. Biol. 6, 829-836 (2010).
11. Grossmann, T. N. et al. Inhibition of oncogenic Wnt signaling through direct targeting of beta-catenin. Proc. Natl Acad. Sci. USA 109, 17942-17947 (2012).
12. Wang, S. et al. Small-molecule modulation of Wnt signaling via modulating the Axin-LRP5/6 interaction. Nat. Chem. Biol. 9, 579-585 (2013).
13. Zhang, Y. et al. Inhibition of Wnt signaling by Dishevelled PDZ peptides. Nat. Chem. Biol. 5, 217-219 (2009).
14. Grandy, D. et al. Discovery and characterization of a small molecule inhibitor of the PDZ domain of dishevelled. J. Biol. Chem. 284, 16256-16263 (2009).
15. Schwarz-Romond, T. et al. The DIX domain of Dishevelled confers Wnt signaling by dynamic polymerization. Nat. Struct. Mol. Biol. 14, 484-492 (2007).
16. Bilic, J. et al. Wnt induces LRP6 signalosomes and promotes dishevelleddependent LRP6 phosphorylation. Science 316, 1619-1622 (2007).
17. Wong, H. C. et al. Direct binding of the PDZ domain of Dishevelled to a conserved internal sequence in the C-terminal region of Frizzled. Mol. Cell 12, 1251-1260 (2003).
18. Wong, H. C. et al. Structural basis of the recognition of the dishevelled DEP domain in the Wnt signaling pathway. Nat. Struct. Biol. 7, 1178-1184 (2000).
19. Tauriello, D. V. et al. Wnt/beta-catenin signaling requires interaction of the Dishevelled DEP domain and C terminus with a discontinuous motif in Frizzled. Proc. Natl Acad. Sci. USA 109, E812-E820 (2012).
20. Maxfield, F. R. & Tabas, I. Role of cholesterol and lipid organization in disease. Nature 438, 612-621 (2005).
21. Lingwood, D. & Simons, K. Lipid rafts as a membrane-organizing principle. Science 327, 46-50 (2010).
22. Levitan, I., Fang, Y., Rosenhouse-Dantsker, A. & Romanenko, V. Cholesterol and ion channels. Subcell. Biochem. 51, 509-549 (2010).
23. Hulce, J. J., Cognetta, A. B., Niphakis, M. J., Tully, S. E. & Cravatt, B. F. Proteome-wide mapping of cholesterol-interacting proteins in mammalian cells. Nat. Methods 10, 259-264 (2013).
24. Wallingford, J. B. & Habas, R. The developmental biology of Dishevelled: an enigmatic protein governing cell fate and cell polarity. Development 132, 4421-4436 (2005).
25. Zimmermann, P. et al. PIP(2)-PDZ domain binding controls the association of syntenin with the plasma membrane. Mol. Cell 9, 1215-1225 (2002).
26. Wu, H. et al. PDZ domains of Par-3 as potential phosphoinositide signaling integrators. Mol. Cell 28, 886-898 (2007).
27. Chen, Y. et al. Genome-wide functional annotation of dual-specificity proteinand lipid-binding modules that regulate protein interactions. Mol. Cell 46, 226-237 (2012).
28. Sheng, R. et al. Cholesterol modulates cell signaling and protein networking by specifically interacting with PDZ domain-containing scaffold proteins. Nat. Commun. 3, 1249 (2012).
29. Di Paolo, G. & De Camilli, P. Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657 (2006).
30. McLaughlin, S. & Murray, D. Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438, 605-611 (2005).
31. Cho, W. & Stahelin, R. V. Membrane-protein interactions in cell signaling and membrane trafficking. Annu. Rev. Biophys. Biomol. Struct. 34, 119-151 (2005).
32. Heo, W. D. et al. PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314, 1458-1461 (2006).
33. Yeung, T. et al. Membrane phosphatidylserine regulates surface charge and protein localization. Science 319, 210-213 (2008).
34. Epand, R. M. Cholesterol and the interaction of proteins with membrane domains. Prog. Lipid Res. 45, 279-294 (2006).
35. Hanson, M. A. et al. A specific cholesterol binding site is established by the 2.8 A structure of the human beta2-adrenergic receptor. Structure 16, 897-905 (2008).
36. Silkov, A. et al. Genome-wide structural analysis reveals novel membrane binding properties of AP180 N-terminal homology (ANTH) domains. J. Biol. Chem. 286, 34155-34163 (2011).
37. Zeng, X. et al. Initiation of Wnt signaling: Control of Wnt coreceptor Lrp6 phosphorylation/activation via frizzled, dishevelled and axin functions. Development 135, 367-375 (2008).
38. Tamai, K. et al. A mechanism for Wnt coreceptor activation. Mol. Cell 13, 149-156 (2004).
39. Taelman, V. F. et al. Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell 143, 1136-1148 (2010).
40. Vinyoles, M. et al. Multivesicular GSK3 sequestration upon Wnt signaling is controlled by p120-catenin/cadherin interaction with LRP5/6. Mol. Cell 53, 444-457 (2014).
41. Li, V. S. et al. Wnt signaling through inhibition of beta-catenin degradation in an intact Axin1 complex. Cell 149, 1245-1256 (2012).
42. van Amerongen, R. Alternative Wnt pathways and receptors. Cold Spring Harb. Perspect. Biol. 4, a007914 (2012).
43. Koyama-Honda, I. et al. Fluorescence imaging for monitoring the colocalization of two single molecules in living cells. Biophys. J. 88, 2126-2136 (2005).
44. Schambony, A. & Wedlich, D. Wnt-5A/Ror2 regulate expression of XPAPC through an alternative noncanonical signaling pathway. Dev. Cell 12, 779-792 (2007).
45. Green, J., Nusse, R. & van Amerongen, R. The role of Ryk and Ror receptor tyrosine kinases in Wnt signal transduction. Cold Spring Harb. Perspect. Biol. 6, a009175 (2013).
46. Kim, G. H., Her, J. H. & Han, J. K. Ryk cooperates with Frizzled 7 to promote Wnt11-mediated endocytosis and is essential for Xenopus laevis convergent extension movements. J. Cell Biol. 182, 1073-1082 (2008).
47. Lin, S., Baye, L. M., Westfall, T. A. & Slusarski, D. C. Wnt5b-Ryk pathway provides directional signals to regulate gastrulation movement. J. Cell Biol. 190, 263-278 (2010).
48. Habas, R., Kato, Y. & He, X. Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell 107, 843-854 (2001).
49. Liu, W. et al. Mechanism of activation of the Formin protein Daam1. Proc. Natl Acad. Sci. USA 105, 210-215 (2008).
50. Huang, B., Bates, M. & Zhuang, X. Super-resolution fluorescence microscopy. Annu. Rev. Biochem. 78, 993-1016 (2009).
51. Ramachandran, R., Heuck, A. P., Tweten, R. K. & Johnson, A. E. Structural insights into the membrane-anchoring mechanism of a cholesterol-dependent cytolysin. Nat. Struct. Biol. 9, 823-827 (2002).
52. Shimada, Y., Maruya, M., Iwashita, S. & Ohno-Iwashita, Y. The C-terminal domain of perfringolysin O is an essential cholesterol-binding unit targeting to cholesterol-rich microdomains. Eur. J. Biochem. 269, 6195-6203 (2002).
53. Farrand, A. J., LaChapelle, S., Hotze, E. M., Johnson, A. E. & Tweten, R. K. Only two amino acids are essential for cytolytic toxin recognition of cholesterol at the membrane surface. Proc. Natl Acad. Sci. USA 107, 4341-4346 (2010).
54. Yamamoto, H., Komekado, H. & Kikuchi, A. Caveolin is necessary for Wnt-3adependent internalization of LRP6 and accumulation of beta-catenin. Dev. Cell 11, 213-223 (2006).
55. Yamamoto, H., Sakane, H., Yamamoto, H., Michiue, T. & Kikuchi, A. Wnt3a and Dkk1 regulate distinct internalization pathways of LRP6 to tune the activation of beta-catenin signaling. Dev. Cell 15, 37-48 (2008).
56. Simons, M. et al. Electrochemical cues regulate assembly of the Frizzled/ Dishevelled complex at the plasma membrane during planar epithelial polarization. Nat. Cell Biol. 11, 286-294 (2009).
57. van Amerongen, R. & Nusse, R. Towards an integrated view of Wnt signaling in development. Development 136, 3205-3214 (2009).
58. Florian, M. C. et al. A canonical to non-canonical Wnt signalling switch in haematopoietic stem-cell ageing. Nature 503, 392-396 (2013).
59. Goldstein, J. L., DeBose-Boyd, R. A. & Brown, M. S. Protein sensors for membrane sterols. Cell 124, 35-46 (2006).
60. Chang, T. Y., Chang, C. C., Ohgami, N. & Yamauchi, Y. Cholesterol sensing, trafficking, and esterification. Annu. Rev. Cell Dev. Biol. 22, 129-157 (2006).
61. Ikonen, E. Cellular cholesterol trafficking and compartmentalization. Nat. Rev. Mol. Cell Biol. 9, 125-138 (2008).
62. Fang, Y. et al. Hypercholesterolemia suppresses inwardly rectifying K channels in aortic endothelium in vitro and in vivo. Circ. Res. 98, 1064-1071 (2006).
63. Moore, K. J. et al. Loss of receptor-mediated lipid uptake via scavenger receptor A or CD36 pathways does not ameliorate atherosclerosis in hyperlipidemic mice. J. Clin. Invest. 115, 2192-2201 (2005).
64. Yoon, Y., Zhang, X. & Cho, W. Phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) specifically induces membrane penetration and deformation by Bin/amphiphysin/Rvs (BAR) domains. J. Biol. Chem. 287, 34078-34090 (2012).
65. Choi, S. C. & Han, J. K. Rap2 is required for Wnt/beta-catenin signaling pathway in Xenopus early development. EMBO J. 24, 985-996 (2005).
66. Manna, D. et al. Differential roles of phosphatidylserine, PtdIns(4,5)P2, and PtdIns(3,4,5)P3 in plasma membrane targeting of C2 domains. Molecular dynamics simulation, membrane binding, and cell translocation studies of the PKCalpha C2 domain. J. Biol. Chem. 283, 26047-26058 (2008).
67. Petrey, D., Fischer, M. & Honig, B. Structural relationships among proteins with different global topologies and their implications for function annotation strategies. Proc. Natl Acad. Sci. USA 106, 17377-17382 (2009).
68. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
69. Kim, G. H. & Han, J. K. Essential role for beta-arrestin 2 in the regulation of Xenopus convergent extension movements. EMBO J. 26, 2513-2526 (2007).
70. Hsieh, J. C. et al. Mesd encodes an LRP5/6 chaperone essential for specification of mouse embryonic polarity. Cell 112, 355-367 (2003).