ARF6-Regulated Endocytosis of Growth Factor Receptors Links Cadherin-Based Adhesion to Canonical Wnt Signaling in Epithelia

REFERENCES

• Perez-Moreno M, Jamora C, Fuchs E. 2003. Sticky business: orchestrating cellular signals at adherens junctions. Cell 112:535–548.
   PubMed Web of Science ®Google Scholar
• Hebner C, Weaver VM, Debnath J. 2008. Modeling morphogenesis and oncogenesis in three-dimensional breast epithelial cultures. Annu. Rev. Pathol. 3:313–339.
   PubMed Web of Science ®Google Scholar
• Moon RT, Kohn AD, Ferrari GVD, Kaykas A. 2004. WNT and [beta]-catenin signalling: diseases and therapies. Nat. Rev. Genet. 5:691–701.
   PubMed Web of Science ®Google Scholar
• Klaus A, Birchmeier W. 2008. Wnt signalling and its impact on development and cancer. Nat. Rev. Cancer 8:387–398.
   PubMed Web of Science ®Google Scholar
• Miller RK, McCrea PD. 2010. Wnt to build a tube: contributions of Wnt signaling to epithelial tubulogenesis. Dev. Dyn. 239:77–93.
   PubMedGoogle Scholar
• Cadigan KM, Peifer M. 2009. Wnt signaling from development to disease: insights from model systems. Cold Spring Harb. Perspect. Biol. 1:a002881. doi:10.1101/cshperspect.a002881.
   PubMed Web of Science ®Google Scholar
• Pasca di Magliano M, Biankin AV, Heiser PW, Cano DA, Gutierrez PJA, Deramaudt T, Segara D, Dawson AC, Kench JG, Henshall SM, Sutherland RL, Dlugosz A, Rustgi AK, Hebrok M. 2007. Common activation of canonical Wnt signaling in pancreatic adenocarcinoma. PLoS One 2:e1155. doi:10.1371/journal.pone.0001155.
   PubMed Web of Science ®Google Scholar
• Reya T, Clevers H. 2005. Wnt signalling in stem cells and cancer. Nature 434:843–850.
   PubMed Web of Science ®Google Scholar
• Schepers A, Clevers H. 2012. Wnt signaling, stem cells, and cancer of the gastrointestinal tract. Cold Spring Harb. Perspect. Biol. 4:a007989.
   PubMed Web of Science ®Google Scholar
• Polakis P. 2007. The many ways of Wnt in cancer. Curr. Opin. Genet. Dev. 17:45–51.
   PubMed Web of Science ®Google Scholar
• Polk DB, Peek RM. 2010. Helicobacter pylori: gastric cancer and beyond. Nat. Rev. Cancer 10:403–414.
   PubMed Web of Science ®Google Scholar
• Tomita M, Dewan MZ, Yamamoto N, Kikuchi A, Mori N. 2009. Epstein-Barr virus-encoded latent membrane protein 1 activates β-catenin signaling in B lymphocytes. Cancer Sci. 100:807–812. (Retraction in 102:500.)
   PubMedGoogle Scholar
• Lancaster MA, Gleeson JG. 2010. Cystic kidney disease: the role of Wnt signaling. Trends Mol. Med. 16:349–360.
   PubMedGoogle Scholar
• Gottardi CJ, Gumbiner BM. 2004. Distinct molecular forms of β-catenin are targeted to adhesive or transcriptional complexes. J. Cell Biol. 167:339–349.
   PubMed Web of Science ®Google Scholar
• Cadigan KM, Nusse R. 1997. Wnt signaling: a common theme in animal development. Genes Dev. 11:3286–3305.
   PubMed Web of Science ®Google Scholar
• Liu C, Kato Y, Zhang Z, Do VM, Yankner BA, He X. 1999. beta-Trcp couples beta-catenin phosphorylation-degradation and regulates Xenopus axis formation. Proc. Natl. Acad. Sci. U. S. A. 96:6273–6278.
   PubMed Web of Science ®Google Scholar
• Liu C, Li Y, Semenov M, Han C, Baeg Tan G-HY, Zhang Z, Lin X, He X. 2002. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108:837–847.
   PubMed Web of Science ®Google Scholar
• Aberle H, Bauer A, Stappert J, Kispert A, Kemler R. 1997. beta-Catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16:3797–3804.
   PubMed Web of Science ®Google Scholar
• MacDonald BT, Tamai K, He X. 2009. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17:9–26.
   PubMed Web of Science ®Google Scholar
• Verheyen EM, Gottardi CJ. 2010. Regulation of Wnt/β-catenin signaling by protein kinases. Dev. Dyn. 239:34–44.
   PubMedGoogle Scholar
• Maher MT, Mo R, Flozak AS, Peled ON, Gottardi CJ. 2010. Beta-Catenin phosphorylated at serine 45 is spatially uncoupled from beta-catenin phosphorylated in the GSK3 domain: implications for signaling. PLoS One 5:e10184. doi:10.1371/journal.pone.0010184.
   PubMedGoogle Scholar
• Schramp M, Thapa N, Heck J, Anderson R. 2011. PIPKIgamma regulates beta-catenin transcriptional activity downstream of growth factor receptor signaling. Cancer Res. 71:1282–1291.
   PubMedGoogle Scholar
• Hendriksen J, Jansen M, Brown CM, van der Velde H, van Ham M, Galjart N, Offerhaus GJ, Fagotto F, Fornerod M. 2008. Plasma membrane recruitment of dephosphorylated beta-catenin upon activation of the Wnt pathway. J. Cell Sci. 121:1793–1802.
   PubMedGoogle Scholar
• Staal FJT, van Noort M, Strous GJ, Clevers HC. 2002. Wnt signals are transmitted through N-terminally dephosphorylated beta-catenin. EMBO Rep. 3:63–68.
   PubMed Web of Science ®Google Scholar
• Maher MT, Flozak AS, Stocker AM, Chenn A, Gottardi CJ. 2009. Activity of the beta-catenin phosphodestruction complex at cell-cell contacts is enhanced by cadherin-based adhesion. J. Cell Biol. 186:219–228.
   PubMedGoogle Scholar
• Somorjai IML, Martinez-Arias A. 2008. Wingless signalling alters the levels, subcellular distribution and dynamics of armadillo and E-cadherin in third instar larval wing imaginal discs. PLoS One 3:e2893. doi:10.1371/journal.pone.0002893.
   PubMedGoogle Scholar
• Kam Y, Quaranta V. 2009. Cadherin-bound beta-catenin feeds into the Wnt pathway upon adherens junctions dissociation: evidence for an intersection between beta-catenin pools. PLoS One 4:e4580. doi:10.1371/journal.pone.0004580.
   PubMed Web of Science ®Google Scholar
• Ji H, Wang J, Nika H, Hawke D, Keezer S, Ge Q, Fang B, Fang X, Fang D, Litchfield DW, Aldape K, Lu Z. 2009. EGF-induced ERK activation promotes CK2-mediated disassociation of alpha-catenin from beta-catenin and transactivation of beta-catenin. Mol. Cell 36:547–559.
   PubMed Web of Science ®Google Scholar
• Howard S, Deroo T, Fujita Y, Itasaki N. 2011. A positive role of cadherin in Wnt/beta-catenin signalling during epithelial-mesenchymal transition. PLoS One 6:e23899. doi:10.1371/journal.pone.0023899.
   PubMed Web of Science ®Google Scholar
• Perez-Moreno M, Fuchs E. 2006. Catenins: keeping cells from getting their signals crossed. Dev. Cell 11:601–612.
   PubMed Web of Science ®Google Scholar
• D'Souza-Schorey C, Chavrier P. 2006. ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7:347–358.
   PubMed Web of Science ®Google Scholar
• Schweitzer JK, Sedgwick AE, D'Souza-Schorey C. 2011. ARF6-mediated endocytic recycling impacts cell movement, cell division and lipid homeostasis. Semin. Cell Dev. Biol. 22:39–47.
   PubMed Web of Science ®Google Scholar
• Hu B, Shi B, Jarzynka MJ, Yiin JJ, D'Souza-Schorey C, Cheng SY. 2009. ADP-ribosylation factor 6 regulates glioma cell invasion through the IQ-domain GTPase-activating protein 1-Rac1-mediated pathway. Cancer Res. 69:794–801.
   PubMed Web of Science ®Google Scholar
• Muralidharan-Chari V, Hoover H, Clancy J, Schweitzer J, Suckow MA, Schroeder V, Castellino FJ, Schorey JS, D'Souza-Schorey C. 2009. ADP-ribosylation factor 6 regulates tumorigenic and invasive properties in vivo. Cancer Res. 69:2201–2209.
   PubMed Web of Science ®Google Scholar
• Palacios F, Price L, Schweitzer J, Collard JG, D'Souza-Schorey C. 2001. An essential role for ARF6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. EMBO J. 20:4973–4986.
   PubMed Web of Science ®Google Scholar
• D'Souza-Schorey C. 2005. Disassembling adherens junctions: breaking up is hard to do. Trends Cell Biol. 15:19–26.
   PubMed Web of Science ®Google Scholar
• Hiroi T, Someya A, Thompson W, Moss J, Vaughan M. 2006. GEP100/BRAG2: activator of ADP-ribosylation factor 6 for regulation of cell adhesion and actin cytoskeleton via E-cadherin and alpha-catenin. Proc. Natl. Acad. Sci. U. S. A. 103:10672–10677.
   PubMed Web of Science ®Google Scholar
• Kon S, Tanabe K, Watanabe T, Sabe H, Satake M. 2008. Clathrin dependent endocytosis of E-cadherin is regulated by the Arf6GAP isoform SMAP1. Exp. Cell Res. 314:1415–1428.
   PubMed Web of Science ®Google Scholar
• Schweitzer JK, D'Souza-Schorey C. 2002. Localization and activation of the ARF6 GTPase during cleavage furrow ingression and cytokinesis. J. Biol. Chem. 277:27210–27216.
   PubMed Web of Science ®Google Scholar
• Tushir J, D'Souza-Schorey C. 2007. ARF6-dependent activation of ERK and Rac1 modulates epithelial tubule development. EMBO J. 26:1806–1819.
   PubMedGoogle Scholar
• Monteleon CL, Sedgwick A, Hartsell A, Dai M, Whittington C, Voytik-Harbin S, D'Souza-Schorey C. 2012. Establishing epithelial glandular polarity: interlinked roles for ARF6, Rac1, and the matrix microenvironment. Mol. Biol. Cell 23:4495–4505.
   PubMed Web of Science ®Google Scholar
• Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL, Reya T, Yates JR, Nusse R. 2003. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423:448–452.
   PubMed Web of Science ®Google Scholar
• Tushir JS, Clancy J, Warren A, Wrobel C, Brugge JS, D'Souza-Schorey C. 2010. Unregulated ARF6 activation in epithelial cysts generates hyperactive signaling endosomes and disrupts morphogenesis. Mol. Biol. Cell 21:2355–2366.
   PubMed Web of Science ®Google Scholar
• Wu X, Tu X, Joeng KS, Hilton MJ, Williams DA, Long F. 2008. Rac1 activation controls nuclear localization of beta-catenin during canonical Wnt signaling. Cell 133:340–353.
   PubMed Web of Science ®Google Scholar
• Le TL, Yap AS, Stow JL. 1999. Recycling of E-cadherin. J. Cell Biol. 146:219–232.
   PubMed Web of Science ®Google Scholar
• Kim S-E, Choi K-Y. 2007. EGF receptor is involved in WNT3a-mediated proliferation and motility of NIH3T3 cells via ERK pathway activation. Cell. Signal. 19:1554–1564.
   PubMed Web of Science ®Google Scholar
• Tseng A-S, Engel FB, Keating MT. 2006. The GSK-3 inhibitor BIO promotes proliferation in mammalian cardiomyocytes. Chem. Biol. 13:957–963.
   PubMed Web of Science ®Google Scholar
• Dudley DT, Pang L, Decker SJ, Bridges AJ, Saltiel AR. 1995. A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. U. S. A. 92:7686–7689.
   PubMed Web of Science ®Google Scholar
• Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T. 2006. Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10:839–850.
   PubMed Web of Science ®Google Scholar
• Krejci P, Aklian A, Kaucka M, Sevcikova E, Prochazkova J, Masek JK, Mikolka P, Pospisilova T, Spoustova T, Weis M, Paznekas WA, Wolf JH, Gutkind JS, Wilcox WR, Kozubik A, Jabs EW, Bryja V, Salazar L, Vesela I, Balek L. 2012. Receptor tyrosine kinases activate canonical WNT/Œ≤-catenin signaling via MAP kinase/LRP6 pathway and direct beta-catenin phosphorylation. PLoS One 7:e35826. doi:10.1371/journal.pone.0035826.
   PubMed Web of Science ®Google Scholar
• Niehrs C, Shen J. 2010. Regulation of Lrp6 phosphorylation. Cell. Mol. Life Sci. 67:2551–2562.
   PubMedGoogle Scholar
• Debnath J, Brugge JS. 2005. Modelling glandular epithelial cancers in three-dimensional cultures. Nat. Rev. Cancer 5:675–688.
   PubMed Web of Science ®Google Scholar
• Yu X, Wang Y, DeGraff DJ, Wills ML, Matusik RJ. 2011. Wnt/beta-catenin activation promotes prostate tumor progression in a mouse model. Oncogene 30:1868–1879.
   PubMed Web of Science ®Google Scholar
• Khalil S, Tan GA, Giri DD, Zhou XK, Howe LR. 2012. Activation status of Wnt/ss-catenin signaling in normal and neoplastic breast tissues: relationship to HER2/neu expression in human and mouse. PLoS One 7:e33421. doi:10.1371/journal.pone.0033421.
   PubMedGoogle Scholar
• Ahmad I, Morton JP, Singh LB, Radulescu SM, Ridgway RA, Patel S, Woodgett J, Winton DJ, Taketo MM, Wu XR, Leung HY, Sansom OJ. 2011. beta-Catenin activation synergizes with PTEN loss to cause bladder cancer formation. Oncogene 30:178–189.
   PubMed Web of Science ®Google Scholar
• Zeng G, Germinaro M, Micsenyi A, Monga NK, Bell A, Sood A, Malhotra V, Sood N, Midda V, Monga DK, Kokkinakis DM, Monga SP. 2006. Aberrant Wnt/beta-catenin signaling in pancreatic adenocarcinoma. Neoplasia 8:279–289.
   PubMed Web of Science ®Google Scholar
• He T-C, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW. 1998. Identification of c-MYC as a target of the APC pathway. Science 281:1509–1512.
   PubMed Web of Science ®Google Scholar
• Youle RJ, Strasser A. 2008. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9:47–59.
   PubMed Web of Science ®Google Scholar
• van Amerongen R, Nusse R. 2009. Towards an integrated view of Wnt signaling in development. Development 136:3205–3214.
   PubMed Web of Science ®Google Scholar
• Palacios F, D'Souza-Schorey C. 2003. Modulation of Rac1 and ARF6 activation during epithelial cell scattering. J. Biol. Chem. 278:17395–17400.
   PubMedGoogle Scholar
• Murphy JE, Padilla BE, Hasdemir B, Cottrell GS, Bunnett NW. 2009. Endosomes: a legitimate platform for the signaling train. Proc. Natl. Acad. Sci. U. S. A. 106:17615–17622.
   PubMed Web of Science ®Google Scholar
• Sadowski L, Pilecka I, Miaczynska M. 2009. Signaling from endosomes: location makes a difference. Exp. Cell Res. 315:1601–1609.
   PubMedGoogle Scholar
• Kermorgant S, Zicha D, Parker PJ. 2004. PKC controls HGF-dependent c-Met traffic, signalling and cell migration. EMBO J. 23:3721–3734.
   PubMedGoogle Scholar
• Seto ES, Bellen HJ. 2006. Internalization is required for proper Wingless signaling in Drosophila melanogaster. J. Cell Biol. 173:95–106.
   PubMedGoogle Scholar
• Seto ES, Bellen HJ, Lloyd TE. 2002. When cell biology meets development: endocytic regulation of signaling pathways. Genes Dev. 16:1314–1336.
   PubMedGoogle Scholar
• Blitzer JT, Nusse R. 2006. A critical role for endocytosis in Wnt signaling. BMC Cell Biol. 7:28. doi:10.1186/1471-2121-7-28.
   PubMed Web of Science ®Google Scholar
• Reginato MJ, Mills KR, Paulus JK, Lynch DK, Sgroi DC, Debnath J, Muthuswamy SK, Brugge JS. 2003. Integrins and EGFR coordinately regulate the pro-apoptotic protein Bim to prevent anoikis. Nat. Cell Biol. 5:733–740.
   PubMed Web of Science ®Google Scholar
• Tapia JC, Torres VA, Rodriguez DA, Leyton L, Quest AFG. 2006. Casein kinase 2 (CK2) increases survivin expression via enhanced beta-catenin-T cell factor/lymphoid enhancer binding factor-dependent transcription. Proc. Natl. Acad. Sci. U. S. A. 103:15079–15084.
   PubMed Web of Science ®Google Scholar
• Debnath J, Mills KR, Collins NL, Reginato MJ, Muthuswamy SK, Brugge JS. 2002. The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 111:29–40.
   PubMed Web of Science ®Google Scholar
• Weeraratna AT, Jiang Y, Hostetter G, Rosenblatt K, Duray P, Bittner M, Trent JM. 2002. Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma. Cancer Cell 1:279–288.
   PubMed Web of Science ®Google Scholar
• Mikels AJ, Nusse R. 2006. Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol. 4:e115. doi:10.1371/journal.pbio.0040115.
   PubMed Web of Science ®Google Scholar
• Cha SW, Tadjuidje E, Tao Q, Wylie C, Heasman J. 2008. Wnt5a and Wnt11 interact in a maternal Dkk1-regulated fashion to activate both canonical and non-canonical signaling in Xenopus axis formation. Development 135:3719–3729.
   PubMed Web of Science ®Google Scholar
• Grossmann AH, Yoo JH, Clancy J, Sorensen LK, Sedgwick A, Tong Z, Ostanin K, Rogers A, Grossmann KF, Tripp SR, Thomas KR, D'Souza-Schorey C, Odelberg SJ, Li DY. 2013. The small GTPase ARF6 stimulates beta-catenin transcriptional activity during WNT5A-mediated melanoma invasion and metastasis. Sci. Signal. 6:ra14. doi:10.1126/scisignal.2003398.
   PubMed Web of Science ®Google Scholar
• Morishige M, Hashimoto S, Ogawa E, Toda Y, Kotani H, Hirose M, Wei S, Hashimoto A, Yamada A, Yano H, Mazaki Y, Kodama H, Nio Y, Manabe T, Wada H, Kobayashi H, Sabe H. 2008. GEP100 links epidermal growth factor receptor signalling to Arf6 activation to induce breast cancer invasion. Nat. Cell Biol. 10:85–92.
   PubMed Web of Science ®Google Scholar