Wntless in Wnt secretion: molecular, cellular and genetic aspects
Received date: 02 Dec 2011
Accepted date: 04 Feb 2012
Published date: 01 Dec 2012
Copyright
Throughout the animal kingdom, Wnt-triggered signal transduction pathways play fundamental roles in embryonic development and tissue homeostasis. Wnt proteins are modified as glycolipoproteins and are secreted into the extracellular environment as morphogens. Recent studies on the intracellular trafficking of Wnt proteins demonstrate multiple layers of regulation along its secretory pathway. These findings have propelled a great deal of interest among researchers to further investigate the molecular mechanisms that control the release of Wnts and hence the level of Wnt signaling. This review is dedicated to Wntless, a putative G-protein coupled receptor that transports Wnts intracellularly for secretion. Here, we highlight the conclusions drawn from the most recent cellular, molecular and genetic studies that affirm the role of Wntless in the secretion of Wnt proteins.
Soumyashree DAS , Shiyan YU , Ryotaro SAKAMORI , Ewa Stypulkowski , Nan GAO . Wntless in Wnt secretion: molecular, cellular and genetic aspects[J]. Frontiers in Biology, 2012 , 7(6) : 587 -593 . DOI: 10.1007/s11515-012-1200-8
1 |
Attar N, Cullen P J (2010). The retromer complex. Adv Enzyme Regul, 50(1): 216–236
|
2 |
Bänziger C, Soldini D, Schütt C, Zipperlen P, Hausmann G, Basler K (2006). Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell, 125(3): 509–522
|
3 |
Bartscherer K, Pelte N, Ingelfinger D, Boutros M (2006). Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. Cell, 125(3): 523–533
|
4 |
Belenkaya T Y, Wu Y, Tang X, Zhou B, Cheng L, Sharma Y V, Yan D, Selva E M, Lin X (2008). The retromer complex influences Wnt secretion by recycling wntless from endosomes to the trans-Golgi network. Dev Cell, 14(1): 120–131
|
5 |
Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch D H, McMahon A P, Sommer L, Boussadia O, Kemler R (2001). Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development, 128(8): 1253–1264
|
6 |
Carlton J, Bujny M, Peter B J, Oorschot V M, Rutherford A, Mellor H, Klumperman J, McMahon H T, Cullen P J (2004). Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high- curvature membranes and 3-phosphoinositides. Curr Biol, 14(20): 1791–1800
|
7 |
Carlton J G, Bujny M V, Peter B J, Oorschot V M, Rutherford A, Arkell R S, Klumperman J, McMahon H T, Cullen P J (2005). Sorting nexin-2 is associated with tubular elements of the early endosome, but is not essential for retromer-mediated endosome-to-TGN transport. J Cell Sci, 118(19): 4527–4539
|
8 |
Carpenter A C, Rao S, Wells J M, Campbell K, Lang R A (2010). Generation of mice with a conditional null allele for Wntless. Genesis, 48(9): 554–558
|
9 |
Ching W, Hang H C, Nusse R (2008). Lipid-independent secretion of a Drosophila Wnt protein. J Biol Chem, 283(25): 17092–17098
|
10 |
Clevers H (2006). Wnt/beta-catenin signaling in development and disease. Cell, 127(3): 469–480
|
11 |
Coombs G S, Yu J, Canning C A, Veltri C A, Covey T M, Cheong J K, Utomo V, Banerjee N, Zhang Z H, Jadulco R C, Concepcion G P, Bugni T S, Harper M K, Mihalek I, Jones C M, Ireland C M, Virshup D M (2010). WLS-dependent secretion of WNT3A requires Ser209 acylation and vacuolar acidification. J Cell Sci, 123(19): 3357–3367
|
12 |
Franch-Marro X, Wendler F, Guidato S, Griffith J, Baena-Lopez A, Itasaki N, Maurice M M, Vincent J P (2008). Wingless secretion requires endosome-to-Golgi retrieval of Wntless/Evi/Sprinter by the retromer complex. Nat Cell Biol, 10(2): 170–177
|
13 |
Fu J, Ivy Yu H M, Maruyama T, Mirando A J, Hsu W (2011). Gpr177/mouse Wntless is essential for Wnt-mediated craniofacial and brain development. Dev Dyn, 240(2): 365–371
|
14 |
Fu J, Jiang M, Mirando A J, Yu H M, Hsu W (2009). Reciprocal regulation of Wnt and Gpr177/mouse Wntless is required for embryonic axis formation. Proc Natl Acad Sci USA, 106(44): 18598–18603
|
15 |
Galli L M, Barnes T L, Secrest S S, Kadowaki T, Burrus L W (2007). Porcupine-mediated lipid-modification regulates the activity and distribution of Wnt proteins in the chick neural tube. Development, 134(18): 3339–3348
|
16 |
Gasnereau I, Herr P, Chia P Z, Basler K, Gleeson PA (2011). Identification of an endocytosis motif in an intracellular loop of Wntless, essential for its recycling and the control of Wnt signalling. J Biol Chem, 286: 43324–43333
|
17 |
Goodman R M, Thombre S, Firtina Z, Gray D, Betts D, Roebuck J, Spana E P, Selva E M (2006). Sprinter: a novel transmembrane protein required for Wg secretion and signaling. Development, 133(24): 4901–4911
|
18 |
Harterink M, Port F, Lorenowicz M J, McGough I J, Silhankova M, Betist M C, van Weering J R, van Heesbeen R G, Middelkoop T C, Basler K, Cullen P J, Korswagen H C (2011). A SNX3-dependent retromer pathway mediates retrograde transport of the Wnt sorting receptor Wntless and is required for Wnt secretion. Nat Cell Biol, 13(8): 914–923
|
19 |
Herr P, Basler K (2011). Porcupine-mediated lipidation is required for Wnt recognition by Wls. Dev Biol, 361(2): 392–402
|
20 |
Ikeya M, Lee S M, Johnson J E, McMahon A P, Takada S (1997). Wnt signalling required for expansion of neural crest and CNS progenitors. Nature, 389(6654): 966–970
|
21 |
Jin J, Kittanakom S, Wong V, Reyes B A, Van Bockstaele E J, Stagljar I, Berrettini W, Levenson R (2010). Interaction of the mu-opioid receptor with GPR177 (Wntless) inhibits Wnt secretion: potential implications for opioid dependence. BMC Neurosci, 11(1): 33
|
22 |
Komekado H, Yamamoto H, Chiba T, Kikuchi A (2007). Glycosylation and palmitoylation of Wnt-3a are coupled to produce an active form of Wnt-3a. Genes Cells, 12(4): 521–534
|
23 |
Korkut C, Ataman B, Ramachandran P, Ashley J, Barria R, Gherbesi N, Budnik V (2009). Trans-synaptic transmission of vesicular Wnt signals through Evi/Wntless. Cell, 139(2): 393–404
|
24 |
Kurayoshi M, Yamamoto H, Izumi S, Kikuchi A (2007). Post-translational palmitoylation and glycosylation of Wnt-5a are necessary for its signalling. Biochem J, 402(3): 515–523
|
25 |
Liu P, Wakamiya M, Shea M J, Albrecht U, Behringer R R, Bradley A (1999). Requirement for Wnt3 in vertebrate axis formation. Nat Genet, 22(4): 361–365
|
26 |
Logan C Y, Nusse R (2004). The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol, 20(1): 781–810
|
27 |
MacDonald B T, Tamai K, He X (2009). Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell, 17(1): 9–26
|
28 |
McMahon A P, Bradley A (1990). The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell, 62(6): 1073–1085
|
29 |
Pan C L, Baum P D, Gu M, Jorgensen E M, Clark S G, Garriga G (2008). C. elegans AP-2 and retromer control Wnt signaling by regulating mig-14/Wntless. Dev Cell, 14(1): 132–139
|
30 |
Port F, Kuster M, Herr P, Furger E, Bänziger C, Hausmann G, Basler K (2008). Wingless secretion promotes and requires retromer-dependent cycling of Wntless. Nat Cell Biol, 10(2): 178–185
|
31 |
Rojas R, van Vlijmen T, Mardones G A, Prabhu Y, Rojas A L, Mohammed S, Heck A J, Raposo G, van der Sluijs P, Bonifacino J S (2008). Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J Cell Biol, 183(3): 513–526
|
32 |
Seaman M N (2005). Recycle your receptors with retromer. Trends Cell Biol, 15(2): 68–75
|
33 |
Silhankova M, Port F, Harterink M, Basler K, Korswagen H C (2010). Wnt signalling requires MTM-6 and MTM-9 myotubularin lipid-phosphatase function in Wnt-producing cells. EMBO J, 29(24): 4094–4105
|
34 |
Stefater J A 3rd, Lewkowich I, Rao S, Mariggi G, Carpenter A C, Burr A R, Fan J, Ajima R, Molkentin J D, Williams B O, Wills-Karp M, Pollard J W, Yamaguchi T, Ferrara N, Gerhardt H, Lang R A (2011). Regulation of angiogenesis by a non-canonical Wnt-Flt1 pathway in myeloid cells. Nature, 474(7352): 511–515
|
35 |
Takada R, Satomi Y, Kurata T, Ueno N, Norioka S, Kondoh H, Takao T, Takada S (2006). Monounsaturated fatty acid modification of Wnt protein: its role in Wnt secretion. Dev Cell, 11(6): 791–801
|
36 |
Tanaka K, Kitagawa Y, Kadowaki T (2002). Drosophila segment polarity gene product porcupine stimulates the posttranslational N-glycosylation of wingless in the endoplasmic reticulum. J Biol Chem, 277(15): 12816–12823
|
37 |
Tanaka K, Okabayashi K, Asashima M, Perrimon N, Kadowaki T (2000). The evolutionarily conserved porcupine gene family is involved in the processing of the Wnt family. Eur J Biochem, 267(13): 4300–4311
|
38 |
Tang X, Fan X, Lin X (2011). Regulation of Wnt Secretion and Distribution. Springer Science+Business Media, LLC 2011, 19–33
|
39 |
Temkin P, Lauffer B, Jäger S, Cimermancic P, Krogan N J, von Zastrow M (2011). SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Nat Cell Biol, 13(6): 717–721
|
40 |
Thomas K R, Capecchi M R (1990). Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development. Nature, 346(6287): 847–850
|
41 |
van den Heuvel M, Harryman-Samos C, Klingensmith J, Perrimon N, Nusse R (1993). Mutations in the segment polarity genes wingless and porcupine impair secretion of the wingless protein. EMBO J, 12(13): 5293–5302
|
42 |
Wassmer T, Attar N, Bujny M V, Oakley J, Traer C J, Cullen P J (2007). A loss-of-function screen reveals SNX5 and SNX6 as potential components of the mammalian retromer. J Cell Sci, 120(1): 45–54
|
43 |
Willert K, Brown J D, Danenberg E, Duncan A W, Weissman I L, Reya T, Yates J R 3rd, Nusse R (2003). Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature, 423(6938): 448–452
|
44 |
Yang P T, Lorenowicz M J, Silhankova M, Coudreuse D Y, Betist M C, Korswagen H C (2008). Wnt signaling requires retromer-dependent recycling of MIG-14/Wntless in Wnt-producing cells. Dev Cell, 14(1): 140–147
|
45 |
Zhai L, Chaturvedi D, Cumberledge S (2004). Drosophila wnt-1 undergoes a hydrophobic modification and is targeted to lipid rafts, a process that requires porcupine. J Biol Chem, 279(32): 33220– 33227
|
46 |
Zhang P, Wu Y, Belenkaya T Y, and Lin X (2011). SNX3 controls Wingless/Wnt secretion through regulating retromer-dependent recycling of Wntless. Cell Res, 21(12):1677–1690
|
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