When pathways collide: collaboration and connivance among signalling proteins in development (original) (raw)

• Cohen, P. The role of protein phosphorylation in neural and hormonal control of cellular activity. Nature 296, 613–620 (1982).
  Article CAS PubMed Google Scholar
• van Amerongen, R. & Nusse, R. Towards an integrated view of Wnt signaling in development. Development 136, 3205–3214 (2009).
  Article CAS PubMed Google Scholar
• MacDonald, B. T., Tamai, K. & He, X. Wnt/β-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9–26 (2009). References 2 and 3 provide excellent and up-to-date reviews of Wnt signalling.
  Article CAS PubMed PubMed Central Google Scholar
• Zhao, B., Lei, Q. Y. & Guan, K. L. The Hippo-YAP pathway: new connections between regulation of organ size and cancer. Curr. Opin. Cell Biol. 20, 638–646 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Zeng, Q. & Hong, W. The emerging role of the Hippo pathway in cell contact inhibition, organ size control, and cancer development in mammals. Cancer Cell 13, 188–192 (2008). References 4 and 5 provide excellent and up-to-date reviews of Hippo signalling.
  Article CAS PubMed Google Scholar
• Klingensmith, J. & Nusse, R. Signaling by Wingless in Drosophila. Dev. Biol. 166, 396–414 (1994).
  Article CAS PubMed Google Scholar
• Major, M. B. et al. Wilms tumor suppressor WTX negatively regulates WNT/β-catenin signaling. Science 316, 1043–1046 (2007).
  Article CAS PubMed Google Scholar
• Miller, B. W. et al. Application of an integrated physical and functional screening approach to identify inhibitors of the Wnt pathway. Mol. Syst. Biol. 5, 315 (2009). References 7 and 8 provide excellent examples of the power of proteomic approaches for the unbiased assessment of pathway topology and interactions.
  Article PubMed PubMed Central CAS Google Scholar
• Mosimann, C., Hausmann, G. & Basler, K. β-catenin hits chromatin: regulation of Wnt target gene activation. Nature Rev. Mol. Cell Biol. 10, 276–286 (2009).
  Article CAS Google Scholar
• Jho, E. H. et al. Wnt/β-catenin/TCF signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell. Biol. 22, 1172–1183 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Lee, E., Salic, A., Kruger, R., Heinrich, R. & Kirschner, M. W. The roles of APC and Axin derived from experimental and theoretical analysis of the Wnt pathway. PLoS Biol. 1, E10 (2003).
  Article PubMed PubMed Central CAS Google Scholar
• Benchabane, H., Hughes, E. G., Takacs, C. M., Baird, J. R. & Ahmed, Y. Adenomatous polyposis coli is present near the minimal level required for accurate graded responses to the Wingless morphogen. Development 135, 963–971 (2008).
  Article CAS PubMed Google Scholar
• Polakis, P. The many ways of Wnt in cancer. Curr. Opin. Genet. Dev. 17, 45–51 (2007).
  Article CAS PubMed Google Scholar
• Doble, B. W., Patel, S., Wood, G. A., Kockeritz, L. K. & Woodgett, J. R. Functional redundancy of GSK-3α and GSK-3β in Wnt/β-catenin signaling shown by using an allelic series of embryonic stem cell lines. Dev. Cell 12, 957–971 (2007). Describes the insensitivity to the loss of GSK3 alleles in embryonic stem cells and reveals a requirement for GSK3 in differentiation.
  Article CAS PubMed PubMed Central Google Scholar
• Cohen, P. & Frame, S. The renaissance of GSK3. Nature Rev. Mol. Cell Biol. 2, 769–776 (2001).
  Article CAS Google Scholar
• Davidson, G. et al. Casein kinase 1γ couples Wnt receptor activation to cytoplasmic signal transduction. Nature 438, 867–872 (2005).
  Article CAS PubMed Google Scholar
• Zeng, X. et al. A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation. Nature 438, 873–877 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• 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). References 16–18 describe the positive roles of two protein kinases in Wnt signalling that had previously been ascribed negative functions.
  Article CAS PubMed Google Scholar
• Takacs, C. M. et al. Dual positive and negative regulation of Wingless signaling by Adenomatous polyposis coli. Science 319, 333–336 (2008).
  Article CAS PubMed Google Scholar
• McManus, E. J. et al. Role that phosphorylation of GSK3 plays in insulin and Wnt signalling defined by knockin analysis. EMBO J. 24, 1571–1583 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Ng, S. S. et al. Phosphatidylinositol 3-kinase signaling does not activate the Wnt cascade. J. Biol. Chem. 284, 35308–35313 (2009). Provides compelling evidence to debunk the link between PI3K signals and Wnt responses, demonstrating signal authenticity.
  Article CAS PubMed PubMed Central Google Scholar
• Orsulic, S. & Peifer, M. An in vivo structure-function study of Armadillo, the β-catenin homologue, reveals both separate and overlapping regions of the protein required for cell adhesion and for Wingless signaling. J. Cell Biol. 134, 1283–300 (1996).
  Article CAS PubMed Google Scholar
• Simons, M. & Mlodzik, M. Planar cell polarity signaling: from fly development to human disease. Annu. Rev. Genet. 42, 517–540 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Chen, W. S. et al. Asymmetric homotypic interactions of the atypical cadherin Flamingo mediate intercellular polarity signaling. Cell 133, 1093–1105 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Lawrence, P. A., Casal, J. & Struhl, G. Towards a model of the organisation of planar polarity and pattern in the Drosophila abdomen. Development 129, 2749–2760 (2002).
  Article CAS PubMed Google Scholar
• Casal, J., Struhl, G. & Lawrence, P. A. Developmental compartments and planar polarity in Drosophila. Curr. Biol. 12, 1189–1198 (2002).
  Article CAS PubMed Google Scholar
• Rawls, A. S., Guinto, J. B. & Wolff, T. The cadherins Fat and Dachsous regulate dorsal/ventral signaling in the Drosophila eye. Curr. Biol. 12, 1021–1026 (2002).
  Article CAS PubMed Google Scholar
• Yang, C. H., Axelrod, J. D. & Simon, M. A. Regulation of Frizzled by Fat-like cadherins during planar polarity signaling in the Drosophila compound eye. Cell 108, 675–688 (2002).
  Article CAS PubMed Google Scholar
• Saburi, S. et al. Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nature Genet. 40, 1010–1015 (2008). Provides evidence for conserved roles of D. melanogaster Fat and mammalian FAT4 in PCP pathways.
  Article CAS PubMed Google Scholar
• Casal, J., Lawrence, P. A. & Struhl, G. Two separate molecular systems, Dachsous/Fat and Starry night/Frizzled, act independently to confer planar cell polarity. Development 133, 4561–4572 (2006).
  Article CAS PubMed Google Scholar
• Sopko, R. & McNeill, H. The skinny on Fat: an enormous cadherin that regulates cell adhesion, tissue growth, and planar cell polarity. Curr. Opin. Cell Biol. 21, 717–723 (2009).
  Article CAS PubMed Google Scholar
• Fanto, M. et al. The tumor-suppressor and cell adhesion molecule Fat controls planar polarity via physical interactions with Atrophin, a transcriptional co-repressor. Development 130, 763–774 (2003).
  Article CAS PubMed Google Scholar
• Matakatsu, H. & Blair, S. S. Interactions between Fat and Dachsous and the regulation of planar cell polarity in the Drosophila wing. Development 131, 3785–3794 (2004).
  Article CAS PubMed Google Scholar
• Simon, M. A. Planar cell polarity in the Drosophila eye is directed by graded Four-jointed and Dachsous expression. Development 131, 6175–6184 (2004).
  Article CAS PubMed Google Scholar
• Yin, C., Ciruna, B. & Solnica-Krezel, L. Convergence and extension movements during vertebrate gastrulation. Curr. Top. Dev. Biol. 89, 163–192 (2009).
  Article CAS PubMed Google Scholar
• Du, S. J., Purcell, S. M., Christian, J. L., McGrew, L. L. & Moon, R. T. Identification of distinct classes and functional domains of Wnts through expression of wild-type and chimeric proteins in Xenopus embryos. Mol. Cell. Biol. 15, 2625–2634 (1995). This analysis provides an effective classification schema and structure–function analysis of the Wnt family of ligands.
  Article CAS PubMed PubMed Central Google Scholar
• Wong, G. T., Gavin, B. J. & McMahon, A. P. Differential transformation of mammary epithelial cells by Wnt genes. Mol. Cell. Biol. 14, 6278–6286 (1994).
  CAS PubMed PubMed Central Google Scholar
• Angers, S. & Moon, R. T. Proximal events in Wnt signal transduction. Nature Rev. Mol. Cell Biol. 10, 468–477 (2009).
  Article CAS Google Scholar
• Torres, M. A. et al. Activities of the Wnt-1 class of secreted signaling factors are antagonized by the Wnt-5A class and by a dominant negative cadherin in early Xenopus development. J. Cell Biol. 133, 1123–37 (1996).
  Article CAS PubMed Google Scholar
• Ishitani, T. et al. The TAK1-NLK-MAPK-related pathway antagonizes signalling between β-catenin and transcription factor TCF. Nature 399, 798–802 (1999).
  Article CAS PubMed Google Scholar
• Meneghini, M. D. et al. MAP kinase and Wnt pathways converge to downregulate an HMG-domain repressor in Caenorhabditis elegans. Nature 399, 793–797 (1999).
  Article CAS PubMed Google Scholar
• Rousset, R. et al. Naked cuticle targets Dishevelled to antagonize Wnt signal transduction. Genes Dev. 15, 658–671 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Yan, D. et al. Cell autonomous regulation of multiple Dishevelled-dependent pathways by mammalian Nkd. Proc. Natl Acad. Sci. USA 98, 3802–3807 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Lee, J. M. et al. RORα attenuates Wnt/β-catenin signaling by PKCα-dependent phosphorylation in colon cancer. Mol. Cell 37, 183–195 (2010).
  Article CAS PubMed Google Scholar
• Minami, Y., Oishi, I., Endo, M. & Nishita, M. Ror-family receptor tyrosine kinases in noncanonical Wnt signaling: their implications in developmental morphogenesis and human diseases. Dev. Dyn. 239, 1–15 (2010).
  CAS PubMed Google Scholar
• Sato, A., Yamamoto, H., Sakane, H., Koyama, H. & Kikuchi, A. Wnt5a regulates distinct signalling pathways by binding to Frizzled2. EMBO J. 29, 41–54 (2010).
  Article CAS PubMed Google Scholar
• Matsumoto, S., Fumoto, K., Okamoto, T., Kaibuchi, K. & Kikuchi, A. Binding of APC and dishevelled mediates Wnt5a-regulated focal adhesion dynamics in migrating cells. EMBO J. 29, 1192–1204 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Rusan, N. M. & Peifer, M. Original CIN: reviewing roles for APC in chromosome instability. J. Cell Biol. 181, 719–726 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• O'Connell, M. P. et al. The orphan tyrosine kinase receptor, ROR2, mediates Wnt5A signaling in metastatic melanoma. Oncogene 29, 34–44 (2010).
  Article CAS PubMed Google Scholar
• Roman-Gomez, J. et al. WNT5A, a putative tumour suppressor of lymphoid malignancies, is inactivated by aberrant methylation in acute lymphoblastic leukaemia. Eur. J. Cancer 43, 2736–46 (2007).
  Article CAS PubMed Google Scholar
• Oishi, I. et al. The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells 8, 645–654 (2003).
  Article CAS PubMed Google Scholar
• Mikels, A. J. & Nusse, R. Purified Wnt5a protein activates or inhibits β-catenin-TCF signaling depending on receptor context. PLoS Biol. 4, e115 (2006).
  Article PubMed PubMed Central CAS Google Scholar
• He, X. et al. A member of the Frizzled protein family mediating axis induction by Wnt-5A. Science 275, 1652–4 (1997).
  Article CAS PubMed Google Scholar
• Green, J. L., Kuntz, S. G. & Sternberg, P. W. Ror receptor tyrosine kinases: orphans no more. Trends Cell Biol. 18, 536–544 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Yamamoto, S. et al. Cthrc1 selectively activates the planar cell polarity pathway of Wnt signaling by stabilizing the Wnt-receptor complex. Dev. Cell 15, 23–36 (2008).
  Article CAS PubMed Google Scholar
• Clevers, H. Wnt signaling: Ig-norrin the dogma. Curr. Biol. 14, R436–R437 (2004).
  Article CAS PubMed Google Scholar
• Badouel, C. et al. The FERM-domain protein Expanded regulates Hippo pathway activity via direct interactions with the transcriptional activator Yorkie. Dev. Cell 16, 411–420 (2009).
  Article CAS PubMed Google Scholar
• Goulev, Y. et al. Scalloped interacts with Yorkie, the nuclear effector of the Hippo tumor-suppressor pathway in Drosophila. Curr. Biol. 18, 435–441 (2008).
  Article CAS PubMed Google Scholar
• Wu, S., Liu, Y., Zheng, Y., Dong, J. & Pan, D. The TEAD/TEF family protein Scalloped mediates transcriptional output of the Hippo growth-regulatory pathway. Dev. Cell 14, 388–398 (2008).
  Article CAS PubMed Google Scholar
• Zhang, L. et al. The TEAD/TEF family of transcription factor Scalloped mediates Hippo signaling in organ size control. Dev. Cell 14, 377–387 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Bennett, F. C. & Harvey, K. F. Fat cadherin modulates organ size in Drosophila via the Salvador/Warts/Hippo signaling pathway. Curr. Biol. 16, 2101–2110 (2006).
  Article CAS PubMed Google Scholar
• Cho, E. et al. Delineation of a Fat tumor suppressor pathway. Nature Genet. 38, 1142–1150 (2006).
  Article CAS PubMed Google Scholar
• Silva, E., Tsatskis, Y., Gardano, L., Tapon, N. & McNeill, H. The tumor-suppressor gene fat controls tissue growth upstream of Expanded in the Hippo signaling pathway. Curr. Biol. 16, 2081–2089 (2006).
  Article CAS PubMed Google Scholar
• Willecke, M. et al. The Fat cadherin acts through the Hippo tumor-suppressor pathway to regulate tissue size. Curr. Biol. 16, 2090–2100 (2006). References 62–64 position and characterize the key molecules associated with Fat signalling into a pathway.
  Article CAS PubMed Google Scholar
• Yu, J., Poulton, J., Huang, Y. C. & Deng, W. M. The Hippo pathway promotes Notch signaling in regulation of cell differentiation, proliferation, and oocyte polarity. PLoS One 3, e1761 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Meignin, C., Alvarez-Garcia, I., Davis, I. & Palacios, I. M. The Salvador-Warts-Hippo pathway is required for epithelial proliferation and axis specification in Drosophila. Curr. Biol. 17, 1871–1878 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Polesello, C. & Tapon, N. Salvador-Warts-Hippo signaling promotes Drosophila posterior follicle cell maturation downstream of Notch. Curr. Biol. 17, 1864–1870 (2007).
  Article CAS PubMed Google Scholar
• Hamaratoglu, F. et al. The tumour-suppressor genes NF2/Merlin and Expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nature Cell Biol. 8, 27–36 (2006).
  Article CAS PubMed Google Scholar
• Sopko, R. et al. Phosphorylation of the tumor suppressor fat is regulated by its ligand Dachsous and the kinase Discs overgrown. Curr. Biol. 19, 1112–1117 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Feng, Y. & Irvine, K. D. Processing and phosphorylation of the Fat receptor. Proc. Natl Acad. Sci. USA 106, 11989–11994 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Yu, J. et al. Kibra functions as a tumor suppressor protein that regulates Hippo signaling in conjunction with Merlin and Expanded. Dev. Cell 18, 288–299 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Baumgartner, R., Poernbacher, I., Buser, N., Hafen, E. & Stocker, H. The WW domain protein Kibra acts upstream of Hippo in Drosophila. Dev. Cell 18, 309–316 (2010).
  Article CAS PubMed Google Scholar
• Genevet, A., Wehr, M. C., Brain, R., Thompson, B. J. & Tapon, N. Kibra is a regulator of the Salvador/Warts/Hippo signaling network. Dev. Cell 18, 300–308 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Oh, H., Reddy, B. V. & Irvine, K. D. Phosphorylation-independent repression of Yorkie in Fat-Hippo signaling. Dev. Biol. 335, 188–197 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Rogulja, D., Rauskolb, C. & Irvine, K. D. Morphogen control of wing growth through the Fat signaling pathway. Dev. Cell 15, 309–321 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Baena-Lopez, L. A., Rodriguez, I. & Baonza, A. The tumor suppressor genes dachsous and fat modulate different signalling pathways by regulating Dally and Dally-like. Proc. Natl Acad. Sci. USA 105, 9645–9650 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Herranz, H. & Milan, M. Signalling molecules, growth regulators and cell cycle control in Drosophila. Cell Cycle 7, 3335–3337 (2008).
  Article CAS PubMed Google Scholar
• Peng, H. W., Slattery, M. & Mann, R. S. Transcription factor choice in the Hippo signaling pathway: Homothorax and Yorkie regulation of the microRNA bantam in the progenitor domain of the Drosophila eye imaginal disc. Genes Dev. 23, 2307–2319 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Alarcon, C. et al. Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-β pathways. Cell 139, 757–769 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Fernandez, L. A. et al. YAP1 is amplified and up-regulated in Hedgehog-associated medulloblastomas and mediates Sonic hedgehog-driven neural precursor proliferation. Genes Dev. 23, 2729–2741 (2009).
  Article CAS Google Scholar
• Varelas, X. et al. The Hippo pathway regulates Wnt/β-catenin signalling. Dev. Cell 18, 579–591 (2010).
  Article CAS PubMed Google Scholar
• Yuan, Z. et al. Phosphoinositide 3-kinase/Akt inhibits MST1-mediated pro-apoptotic signaling through phosphorylation of threonine 120. J. Biol. Chem. 285, 3815–3824 (2010).
  Article CAS PubMed Google Scholar
• Zhang, J. et al. YAP-dependent induction of amphiregulin identifies a non-cell-autonomous component of the Hippo pathway. Nature Cell Biol. 11, 1444–1450 (2009).
  Article CAS PubMed Google Scholar
• Zhou, D. et al. Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 16, 425–438 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Owens, D. M. & Keyse, S. M. Differential regulation of MAP kinase signalling by dual-specificity protein phosphatases. Oncogene 26, 3203–3213 (2007).
  Article CAS PubMed Google Scholar
• Huang, S. M. et al. Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 461, 614–620 (2009). Reveals a new level of regulation of Wnt signalling through the tankyrase-mediated destabilization of axin 1.
  Article CAS PubMed Google Scholar
• Albeck, J. G. et al. Quantitative analysis of pathways controlling extrinsic apoptosis in single cells. Mol. Cell 30, 11–25 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Arnold, H. K. et al. The Axin1 scaffold protein promotes formation of a degradation complex for c-Myc. EMBO J. 28, 500–512 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Goentoro, L. & Kirschner, M. W. Evidence that fold-change, and not absolute level, of β-catenin dictates Wnt signaling. Mol. Cell 36, 872–884 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Buchert, M. et al. Genetic dissection of differential signaling threshold requirements for the Wnt/β-catenin pathway in vivo. PLoS Genet. 6, e1000816 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Yokota, Y. et al. The adenomatous polyposis coli protein is an essential regulator of radial glial polarity and construction of the cerebral cortex. Neuron 61, 42–56 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Goentoro, L., Shoval, O., Kirschner, M. W. & Alon, U. The incoherent feedforward loop can provide fold-change detection in gene regulation. Mol. Cell 36, 894–899 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Kim, W. Y. et al. GSK-3 is a master regulator of neural progenitor homeostasis. Nature Neurosci. 12, 1390–1397 (2009).
  Article CAS PubMed Google Scholar