Wnt Signal Production, Secretion, and Diffusion

Wnt Signaling in Development and Disease: Molecular Mechanisms and Biological Functions

Volumn , Issue , 2014, Pages 3-14

  Maurice, Madelon M ^a   Korswagen, Hendrik C ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Diffusion; Morphogen gradient formation; Posttranslational modification; Wnt binding protein; Wnt secretion pathway; Wnt signal production

Indexed keywords

EID: 84926429221     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781118444122.ch1     Document Type: Chapter

References (82)

1. Baeg, G.H., Lin, X., Khare, N. et al. (2001) Heparan sulfate proteoglycans are critical for the organization of the extracellular distribution of Wingless. Development, 128, 87-94.
2. Banziger, C., Soldini, D., Schutt, C. et al. (2006) Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell, 125, 509-522.
3. Bartscherer, K. and Boutros, M. (2008) Regulation of Wnt protein secretion and its role in gradient formation. EMBO Reports, 9, 977-982.
4. Bartscherer, K., Pelte, N., Ingelfinger, D., and Boutros, M. (2006) Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. Cell, 125, 523-533.
5. Beckett, K., Monier, S., Palmer, L. et al. (2013) Drosophila S2 cells secrete wingless on exosomelike vesicles but the wingless gradient forms independently of exosomes. Traffic, 14, 82-96.
6. Belenkaya, T.Y., Wu, Y., Tang, X. et al. (2008) The retromer complex influences Wnt secretion by recycling Wntless from endosomes to the trans-Golgi network. Developmental Cell, 14, 120-131.
7. Binari, R.C., Staveley, B.E., Johnson, W.A. et al. (1997) Genetic evidence that heparin-like glycosaminoglycans are involved in wingless signaling. Development, 124, 2623-2632.
8. Buechling, T., Chaudhary, V., Spirohn, K. et al. (2011) p24 proteins are required for secretion of Wnt ligands. EMBO Reports, 12, 1265-1272.
9. Cadigan, K.M., Fish, M.P., Rulifson, E.J., and Nusse, R. (1998) Wingless repression of Drosophila frizzled 2 expression shapes the Wingless morphogen gradient in the wing. Cell, 93, 767-777.
10. Castillon, G.A., Aguilera-Romero, A., Manzano-Lopez, J. et al. (2011) The yeast p24 complex regulates GPI-anchored protein transport and quality control by monitoring anchor remodeling. Molecular Biology of the Cell, 22, 2924-2936.
11. Ching, W., Hang, H.C., and Nusse, R. (2008) Lipidindependent secretion of a Drosophila Wnt protein. The Journal of Biological Chemistry, 283, 17092-17098.
12. Coombs, G.S., Yu, J., Canning, C.A. et al. (2010) WLSdependent secretion of WNT3A requires Ser209 acylation and vacuolar acidification. Journal of Cell Science, 123, 3357-3367.
13. Coudreuse, D. and Korswagen, H.C. (2007) The making of Wnt: new insights into Wnt maturation, sorting and secretion. Development, 134, 3-12.
14. Coudreuse, D.Y., Roel, G., Betist, M.C. et al. (2006) Wnt gradient formation requires retromer function in Wnt-producing cells. Science, 312, 921-924.
15. Cruciat, C.M. and Niehrs, C. (2013) Secreted and transmembrane wnt inhibitors and activators. Cold Spring Harbor Perspectives in Biology, 5 (3), a015081.
16. Cullen, P.J. and Korswagen, H.C. (2012) Sorting nexins provide diversity for retromer-dependent trafficking events. Nature Cell Biology, 14, 29-37.
17. Doubravska, L., Krausova, M., Gradl, D. et al. (2011) Fatty acid modification of Wnt1 and Wnt3a at serine is prerequisite for lipidation at cysteine and is essential for Wnt signalling. Cell Signal, 23, 837-848.
18. Flower, D.R. (2000) Beyond the superfamily: the lipocalin receptors. Biochimica et Biophysica Acta, 1482, 327-336.
19. Franch-Marro, X., Marchand, O., Piddini, E. et al. (2005) Glypicans shunt the Wingless signal between local signalling and further transport. Development, 132, 659-666.
20. Franch-Marro, X., Wendler, F., Guidato, S. et al. (2008) Wingless secretion requires endosome-to-Golgi retrieval of Wntless/Evi/Sprinter by the retromer complex. Nature Cell Biology, 10, 170-177.
21. Fu, J., Jiang, M., Mirando, A.J. et al. (2009) Reciprocal regulation of Wnt and Gpr177/mouse Wntless is required for embryonic axis formation. Proceedings of the National Academy of Sciences of the United States of America, 106, 18598-18603.
22. Fujise, M., Izumi, S., Selleck, S.B., and Nakato, H. (2001) Regulation of Dally, an integral membrane proteoglycan, and its function during adult sensory organ formation of Drosophila. Developmental Biology, 235, 433-448.
23. Gallet, A., Staccini-Lavenant, L., and Therond, P.P. (2008) Cellular trafficking of the glypican Dallylike is required for full-strength Hedgehog signaling and Wingless transcytosis. Developmental Cell, 14, 712-725.
24. Galli, L.M., Barnes, T.L., Secrest, S.S. et al. (2007) Porcupine-mediated lipid-modification regulates the activity and distribution of Wnt proteins in the chick neural tube. Development, 134, 3339-3348.
25. Ganfornina, M.D., Gutierrez, G., Bastiani, M., and Sanchez, D. (2000) A phylogenetic analysis of the lipocalin protein family. Molecular Biology and Evolution, 17, 114-126.
26. Gasnereau, I., Herr, P., Chia, P.Z. et al. (2011) Identification of an endocytosis motif in an intracellular loop of Wntless protein, essential for its recycling and the control of Wnt protein signaling. The Journal of Biological Chemistry, 286, 43324-43333.
27. Goodman, R.M., Thombre, S., Firtina, Z. et al. (2006) Sprinter: a novel transmembrane protein required for Wg secretion and signaling. Development, 133, 4901-4911.
28. Greco, V., Hannus, M., and Eaton, S. (2001) Argosomes: a potential vehicle for the spread of morphogens through epithelia. Cell, 106, 633-645.
29. Gross, J.C., Chaudhary, V., Bartscherer, K., and Boutros, M. (2012) Active Wnt proteins are secreted on exosomes. Nature Cell Biology, 14, 1036-1045.
30. Hacker, U., Lin, X., and Perrimon, N. (1997) The Drosophila sugarless gene modulates Wingless signaling and encodes an enzyme involved in polysaccharide biosynthesis. Development, 124, 3565-3573.
31. Hacker, U., Nybakken, K., and Perrimon, N. (2005) Heparan sulphate proteoglycans: the sweet side of development. Nature Reviews Molecular Cell Biology, 6, 530-541.
32. Haerry, T.E., Heslip, T.R., Marsh, J.L., and O'Connor, M.B. (1997) Defects in glucuronate biosynthesis disrupt Wingless signaling in Drosophila. Development, 124, 3055-3064.
33. Han, C., Belenkaya, T.Y., Khodoun, M. et al. (2004) Distinct and collaborative roles of Drosophila EXT family proteins in morphogen signalling and gradient formation. Development, 131, 1563-1575.
34. Han, C., Yan, D., Belenkaya, T.Y., and Lin, X. (2005) Drosophila glypicans Dally and Dally-like shape the extracellular Wingless morphogen gradient in the wing disc. Development, 132, 667-679.
35. Harris, J., Honigberg, L., Robinson, N., and Kenyon, C. (1996) Neuronal cell migration in C. elegans: regulation of Hox gene expression and cell position. Development, 122, 3117-3131.
36. Harterink, M., Port, F., Lorenowicz, M.J. et al. (2011) A SNX3-dependent retromer pathway mediates retrograde transport of the Wnt sorting receptor Wntless and is required for Wnt secretion. Nature Cell Biology, 13, 914-923.
37. Herr, P. and Basler, K. (2012) Porcupine-mediated lipidation is required for Wnt recognition by Wls. Developmental Biology, 361, 392-402.
38. Hufnagel, L., Kreuger, J., Cohen, S.M., and Shraiman, B.I. (2006) On the role of glypicans in the process of morphogen gradient formation. Developmental Biology, 300, 512-522.
39. Janda, C.Y., Waghray, D., Levin, A.M. et al. (2012) Structural basis of Wnt recognition by Frizzled. Science, 337, 59-64.
40. Katanaev, V.L., Solis, G.P., Hausmann, G. et al. (2008) Reggie-1/flotillin-2 promotes secretion of the long-range signalling forms of Wingless and Hedgehog in Drosophila. The EMBO Journal, 27, 509-521.
41. Kirkpatrick, C.A., Dimitroff, B.D., Rawson, J.M., and Selleck, S.B. (2004) Spatial regulation of Wingless morphogen distribution and signaling by Dallylike protein. Developmental Cell, 7, 513-523.
42. Koles, K., Nunnari, J., Korkut, C. et al. (2012) Mechanism of evenness interrupted (Evi)-exosome release at synaptic boutons. The Journal of Biological Chemistry, 287, 16820-16834.
43. Komekado, H., Yamamoto, H., Chiba, T., and Kikuchi, A. (2007) Glycosylation and palmitoylation of Wnt-3a are coupled to produce an active form of Wnt-3a. Genes to Cells, 12, 521-534.
44. Korkut, C., Ataman, B., Ramachandran, P. et al. (2009) Trans-synaptic transmission of vesicular Wnt signals through Evi/Wntless. Cell, 139, 393-404.
45. Kreuger, J., Perez, L., Giraldez, A.J., and Cohen, S.M. (2004) Opposing activities of Dally-like glypican at high and low levels of Wingless morphogen activity. Developmental Cell, 7, 503-512.
46. Kurayoshi, M., Yamamoto, H., Izumi, S., and Kikuchi, A. (2007) Post-translational palmitoylation and glycosylation of Wnt5a are necessary for its signalling. The Biochemical Journal, 402, 515-523.
47. Lander, A.D. (2007) Morpheus unbound: reimagining the morphogen gradient. Cell, 128, 245-256.
48. Lin, X. (2004) Functions of heparan sulfate proteoglycans in cell signaling during development. Development, 131, 6009-6021.
49. Lin, X. and Perrimon, N. (1999) Dally cooperates with Drosophila Frizzled 2 to transduce Wingless signalling. Nature, 400, 281-284.
50. Lorenowicz, M.J. and Korswagen, H.C. (2009) Sailing with the Wnt: charting the Wnt processing and secretion route. Experimental Cell Research, 315, 2683-2689.
51. Luders, F., Segawa, H., Stein, D. et al. (2003) Slalom encodes an adenosine 3'-phosphate 5'-phosphosulfate transporter essential for development in Drosophila. The EMBO Journal, 22, 3635-3644.
52. Miura, G.I. and Treisman, J.E. (2006) Lipid modification of secreted signaling proteins. Cell Cycle, 5, 1184-1188.
53. Mulligan, K.A., Fuerer, C., Ching, W. et al. (2012) Secreted Wingless-interacting molecule (Swim) promotes long-range signaling by maintaining Wingless solubility. Proceedings of the National Academy of Sciences of the United States of America, 109, 370-377.
54. Neumann, C.J. and Cohen, S.M. (1997) Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing. Development, 124, 871-880.
55. Neumann, S., Coudreuse, D.Y., van der Westhuyzen, D.R. et al. (2009) Mammalian Wnt3a is released on lipoprotein particles. Traffic, 10, 334-343.
56. Otto, G.P. and Nichols, B.J. (2011) The roles of flotillin microdomains-endocytosis and beyond. Journal of Cell Science, 124, 3933-3940.
57. Pan, C.L., Baum, P.D., Gu, M. et al. (2008) Caenorhabditis elegans AP-2 and retromer control Wnt signaling by regulating mig-14/Wntless. Developmental Cell, 14, 132-139.
58. Panakova, D., Sprong, H., Marois, E. et al. (2005) Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature, 435, 58-65.
59. Port, F. and Basler, K. (2010) Wnt trafficking: new insights into Wnt maturation, secretion and spreading. Traffic, 11, 1265-1271.
60. Port, F., Hausmann, G., and Basler, K. (2011) A genome-wide RNA interference screen uncovers two p24 proteins as regulators of Wingless secretion. EMBO Reports, 12, 1144-1152.
61. Port, F., Kuster, M., Herr, P. et al. (2008) Wingless secretion promotes and requires retromer-dependent cycling of Wntless. Nature Cell Biology, 10, 178-185.
62. Prasad, B.C. and Clark, S.G. (2006) Wnt signaling establishes anteroposterior neuronal polarity and requires retromer in C. elegans. Development, 133, 1757-1766.
63. Sarrazin, S., Lamanna, W.C., and Esko, J.D. (2011) Heparan sulfate proteoglycans. Cold Spring Harbor Perspectives in Biology, 3 (7), pii, a004952.
64. Sato, T., van Es, J.H., Snippert, H.J. et al. (2011) Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature, 469, 415-418.
65. Seaman, M.N. (2005) Recycle your receptors with retromer. Trends in Cell Biology, 15, 68-75.
66. Selva, E.M., Hong, K., Baeg, G.H. et al. (2001) Dual role of the fringe connection gene in both heparan sulphate and fringe-dependent signalling events. Nature Cell Biology, 3, 809-815.
67. Silhankova, M., Port, F., Harterink, M. et al. (2010) Wnt signalling requires MTM-6 and MTM-9 myotubularin lipid-phosphatase function in Wntproducing cells. The EMBO Journal, 29, 4094-4105.
68. Simons, M. and Raposo, G. (2009) Exosomes-vesicular carriers for intercellular communication. Current Opinion in Cell Biology, 21, 575-581.
69. Strigini, M. and Cohen, S.M. (2000) Wingless gradient formation in the Drosophila wing. Current Biology, 10, 293-300.
70. Takada, R., Satomi, Y., Kurata, T. et al. (2006) Monounsaturated fatty acid modification of Wnt protein: its role in Wnt secretion. Developmental Cell, 11, 791-801.
71. Takei, Y., Ozawa, Y., Sato, M. et al. (2004) Three Drosophila EXT genes shape morphogen gradients through synthesis of heparan sulfate proteoglycans. Development, 131, 73-82.
72. Tang, X., Wu, Y., Belenkaya, T.Y. et al. (2012) Roles of N-glycosylation and lipidation in Wg secretion and signaling. Developmental Biology, 364, 32-41.
73. Thorpe, C.J., Schlesinger, A., Carter, J.C., and Bowerman, B. (1997) Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm. Cell, 90, 695-705.
74. Tsuda, M., Kamimura, K., Nakato, H. et al. (1999) The cell-surface proteoglycan Dally regulates Wingless signalling in Drosophila. Nature, 400, 276-280.
75. Vincent, J.P. and Briscoe, J. (2001) Morphogens. Current Biology, 11, R851-R854.
76. Willert, K. and Nusse, R. (2012) Wnt proteins. Cold Spring Harbor Perspectives in Biology, 4, a007864.
77. Willert, K., Brown, J.D., Danenberg, E. et al. (2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature, 423, 448-452.
78. Yan, D., Wu, Y., Feng, Y. et al. (2009) The core protein of glypican Dally-like determines its biphasic activity in wingless morphogen signaling. Developmental Cell, 17, 470-481.
79. Yang, P.T., Lorenowicz, M.J., Silhankova, M. et al. (2008) Wnt signaling requires retromer-dependent recycling of MIG-14/Wntless in Wnt-producing cells. Developmental Cell, 14, 140-147.
80. Zecca, M., Basler, K., and Struhl, G. (1996) Direct and long-range action of a Wingless morphogen gradient. Cell, 87, 833-844.
81. Zhai, L., Chaturvedi, D., and Cumberledge, S. (2004) Drosophila Wnt-1 undergoes a hydrophobic modification and is targeted to lipid rafts, a process that requires porcupine. The Journal of Biological Chemistry, 279, 33220-33227.
82. Zhang, X., Abreu, J.G., Yokota, C. et al. (2012) Tiki1 is required for head formation via Wnt cleavageoxidation and inactivation. Cell, 149, 1565-1577.