Competition between TIAM1 and Membranes Balances Endophilin A3 Activity in Cancer Metastasis

Ahmed, 2013, Epigenetic and genetic features of 24 colon cancer cell lines, Oncogenesis, 2, e71, 10.1038/oncsis.2013.35 Amado, 2008, Wild-type KRAS is required for panitumumab efficacy in patients with metastatic colorectal cancer, J. Clin. Oncol., 26, 1626, 10.1200/JCO.2007.14.7116 Anderson, 2016, MYC-nick promotes cell migration by inducing fascin expression and Cdc42 activation, Proc. Natl. Acad. Sci. USA, 113, E5481, 10.1073/pnas.1610994113 Aramaki, 2005, Direct interaction between metastasis-associated protein 1 and endophilin 3, FEBS Lett., 579, 3731, 10.1016/j.febslet.2005.05.069 Bagrodia, 1998, A novel regulator of p21-activated kinases, J. Biol. Chem., 273, 23633, 10.1074/jbc.273.37.23633 Bai, 2010, Endophilin functions as a membrane-bending molecule and is delivered to endocytic zones by exocytosis, Cell, 143, 430, 10.1016/j.cell.2010.09.024 Ben-Chetrit, 2015, Synaptojanin 2 is a druggable mediator of metastasis and the gene is overexpressed and amplified in breast cancer, Sci. Signal., 8, ra7, 10.1126/scisignal.2005537 Bendris, 2016, Sorting nexin 9 negatively regulates invadopodia formation and function in cancer cells, J. Cell Sci., 129, 2804, 10.1242/jcs.188045 Betz, 1996, Imaging exocytosis and endocytosis, Curr. Opin. Neurobiol., 6, 365, 10.1016/S0959-4388(96)80121-8 Bonner, 2003, Molecular profiling of mouse lung tumors: association with tumor progression, lung development, and human lung adenocarcinomas, Oncogene, 23, 1166, 10.1038/sj.onc.1207234 Boucrot, 2015, Endophilin marks and controls a clathrin-independent endocytic pathway, Nature, 517, 460, 10.1038/nature14067 Boulakirba, 2014, Arf6 exchange factor EFA6 and endophilin directly interact at the plasma membrane to control clathrin-mediated endocytosis, Proc. Natl. Acad. Sci. USA, 111, 9473, 10.1073/pnas.1401186111 Burdisso, 2013, PTP1B promotes focal complex maturation, lamellar persistence and directional migration, J. Cell Sci., 126, 1820, 10.1242/jcs.118828 2012, Comprehensive molecular characterization of human colon and rectal cancer, Nature, 487, 330, 10.1038/nature11252 2014, Comprehensive molecular profiling of lung adenocarcinoma, Nature, 511, 543, 10.1038/nature13385 Kandoth, 2013, Integrated genomic characterization of endometrial carcinoma, Nature, 497, 67, 10.1038/nature12113 Cestra, 1999, The SH3 domains of endophilin and amphiphysin bind to the proline-rich region of Synaptojanin 1 at distinct sites that display an unconventional binding specificity, J. Biol. Chem., 274, 32001, 10.1074/jbc.274.45.32001 Chuang, 2004, Role of Synaptojanin 2 in glioma cell migration and invasion, Cancer Res., 64, 8271, 10.1158/0008-5472.CAN-04-2097 Conacci-Sorrell, 2014, Stress-induced cleavage of Myc promotes cancer cell survival, Genes Dev., 28, 689, 10.1101/gad.231894.113 Delic, 2012, Identification and functional validation of CDH11, PCSK6 and SH3GL3 as novel glioma invasion-associated candidate genes, Neuropathol. Appl. Neurobiol., 38, 201, 10.1111/j.1365-2990.2011.01207.x DeVay, 2009, Coassembly of Mgm1 isoforms requires cardiolipin and mediates mitochondrial inner membrane fusion, J. Cell Biol., 186, 793, 10.1083/jcb.200906098 Dong, 2015, Synaptojanin cooperates in vivo with endophilin through an unexpected mechanism, Elife, 4, e05660, 10.7554/eLife.05660 Doyle, 2012, Micro-environmental control of cell migration—myosin IIA is required for efficient migration in fibrillar environments through control of cell adhesion dynamics, J. Cell Sci., 125, 2244, 10.1242/jcs.098806 Eppinga, 2012, Increased expression of the large GTPase dynamin 2 potentiates metastatic migration and invasion of pancreatic ductal carcinoma, Oncogene, 31, 1228, 10.1038/onc.2011.329 Etienne-Manneville, 2002, Rho GTPases in cell biology, Nature, 420, 629, 10.1038/nature01148 Farsad, 2003, Mechanisms of membrane deformation, Curr. Opin. Cell Biol., 15, 372, 10.1016/S0955-0674(03)00073-5 Frittoli, 2014, A RAB5/RAB4 recycling circuitry induces a proteolytic invasive program and promotes tumor dissemination, J. Cell Biol., 206, 307, 10.1083/jcb.201403127 Frost, 2009, The BAR domain superfamily: membrane-molding macromolecules, Cell, 137, 191, 10.1016/j.cell.2009.04.010 Gad, 2000, Fission and uncoating of synaptic clathrin-coated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin, Neuron, 27, 301, 10.1016/S0896-6273(00)00038-6 Gallop, 2006, Mechanism of endophilin N-BAR domain-mediated membrane curvature, EMBO J., 25, 2898, 10.1038/sj.emboj.7601174 García-Mata, 2006, Analysis of activated GAPs and GEFs in cell lysates, Methods Enzymol., 406, 425, 10.1016/S0076-6879(06)06031-9 Geladopoulos, 1991, A malachite green colorimetric assay for protein phosphatase activity, Anal. Biochem., 192, 112, 10.1016/0003-2697(91)90194-X Ghosh, 2009, SH3GL2 and CDKN2A/2B loci are independently altered in early dysplastic lesions of head and neck: correlation with HPV infection and tobacco habit, J. Pathol., 217, 408, 10.1002/path.2464 Giordani, 2002, Two regions of deletion in 9p22∼p24 in neuroblastoma are frequently observed in favorable tumors, Cancer Genet. Cytogenet., 135, 42, 10.1016/S0165-4608(01)00640-9 Guichet, 2002, Essential role of endophilin A in synaptic vesicle budding at the Drosophila neuromuscular junction, EMBO J., 21, 1661, 10.1093/emboj/21.7.1661 Guo, 2013, Balanced Tiam1-Rac1 and RhoA drives proliferation and invasion of pancreatic cancer cells, Mol. Cancer Res., 11, 230, 10.1158/1541-7786.MCR-12-0632 Hall, 1998, Rho GTPases and the actin cytoskeleton, Science, 279, 509, 10.1126/science.279.5350.509 Hanahan, 2000, The hallmarks of cancer, Cell, 100, 57, 10.1016/S0092-8674(00)81683-9 Hodis, 2012, A landscape of driver mutations in melanoma, Cell, 150, 251, 10.1016/j.cell.2012.06.024 Hoopmann, 2012, Imaging synaptic vesicle recycling by staining and destaining vesicles with FM dyes, Cold Spring Harb. Protoc., 2012, 77, 10.1101/pdb.prot067603 Hu, 2011, Transducer of Cdc42-dependent actin assembly promotes epidermal growth factor-induced cell motility and invasiveness, J. Biol. Chem., 286, 2261, 10.1074/jbc.M110.157974 Huang, 2013, Tiam1 is associated with hepatocellular carcinoma metastasis, Int. J. Cancer, 132, 90, 10.1002/ijc.27627 Hui, 2006, Ca2+-triggered simultaneous membrane penetration of the tandem C2-domains of synaptotagmin I, Biophys. J., 91, 1767, 10.1529/biophysj.105.080325 Jorissen, 2009, Metastasis-associated gene expression changes predict poor outcomes in patients with Dukes stage B and C colorectal cancer, Clin. Cancer Res., 15, 7642, 10.1158/1078-0432.CCR-09-1431 Kimmel, 1995, Stages of embryonic development of the zebrafish, Dev. Dyn., 203, 253, 10.1002/aja.1002030302 Kjaerulff, 2011, The structure and function of endophilin proteins, Cell Biochem. Biophys, 60, 137, 10.1007/s12013-010-9137-5 de Kreuk, 2012, Control of Rho GTPase function by BAR-domains, Small GTPases, 3, 45, 10.4161/sgtp.18960 Lanzetii, 2017, Behind the scenes: endo/exocytosis in the acquistion of metastatic traits, Cancer Res., 77, 1813, 10.1158/0008-5472.CAN-16-3403 Lanzetti, 2008, Endocytosis and cancer: an “insider” network with dangerous liaisons, Traffic, 9, 2011, 10.1111/j.1600-0854.2008.00816.x Van Leeuwen, 1997, The guanine nucleotide exchange factor Tiam1 affects neuronal morphology; opposing roles for the small GTPases Rac and Rho, J. Cell Biol., 139, 797, 10.1083/jcb.139.3.797 Li, 2016, EphA3 promotes malignant transformation of colorectal epithelial cells by upregulating oncogenic pathways, Cancer Lett., 383, 195, 10.1016/j.canlet.2016.10.004 Lua, 2005, Activation of EGF receptor endocytosis and ERK1/2 signaling by BPGAP1 requires direct interaction with EEN/endophilin II and a functional RhoGAP domain, J. Cell Sci., 118, 2707, 10.1242/jcs.02383 Malecz, 2000, Synaptojanin 2, a novel Rac1 effector that regulates clathrin-mediated endocytosis, Curr. Biol., 10, 1383, 10.1016/S0960-9822(00)00778-8 Malliri, 2002, Mice deficient in the Rac activator Tiam1 are resistant to Ras-induced skin tumours, Nature, 417, 867, 10.1038/nature00848 Markowitz, 1995, Inactivation of the type II TGF-beta receptor in colon cancer cells with microsatellite instability, Science, 268, 1336, 10.1126/science.7761852 Masuda, 2006, Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms, EMBO J., 25, 2889, 10.1038/sj.emboj.7601176 Matta, 2012, LRRK2 controls an EndoA phosphorylation cycle in synaptic endocytosis, Neuron, 75, 1008, 10.1016/j.neuron.2012.08.022 Mellman, 2013, Endocytosis and cancer, Cold Spring Harb. Perspect. Biol., 5, a016949, 10.1101/cshperspect.a016949 Metz, 2016, Insulin receptor substrate-1 deficiency drives a proinflammatory phenotype in KRAS mutant lung adenocarcinoma, Proc. Natl. Acad. Sci. USA, 113, 8795, 10.1073/pnas.1601989113 Meyers, 2003, Lighting up the senses: FM1-43 loading of sensory cells through nonselective ion channels, J. Neurosci., 23, 4054, 10.1523/JNEUROSCI.23-10-04054.2003 Miaczynska, 2004, Not just a sink: endosomes in control of signal transduction, Curr. Opin. Cell Biol., 16, 400, 10.1016/j.ceb.2004.06.005 Milosevic, 2011, Recruitment of endophilin to clathrin-coated pit necks is required for efficient vesicle uncoating after fission, Neuron, 72, 587, 10.1016/j.neuron.2011.08.029 Minard, 2004, The role of the guanine nucleotide exchange factor Tiam1 in cellular migration, invasion, adhesion and tumor progression, Breast Cancer Res. Treat., 84, 21, 10.1023/B:BREA.0000018421.31632.e6 Minard, 2006, Tiam1 regulates cell adhesion, migration and apoptosis in colon tumor cells, Clin. Exp. Metastasis, 23, 301, 10.1007/s10585-006-9040-z Morin, 1997, Activation of β-catenin-Tcf signaling in colon cancer by mutations in β-catenin or APC, Science, 275, 1787, 10.1126/science.275.5307.1787 Mosesson, 2008, Derailed endocytosis: an emerging feature of cancer, Nat. Rev. Cancer, 8, 835, 10.1038/nrc2521 Nguyen, 2007, Identification of a predictive gene expression signature of cervical lymph node metastasis in oral squamous cell carcinoma, Cancer Sci., 98, 740, 10.1111/j.1349-7006.2007.00454.x Osterberg, 2009, Potential predictive markers of chemotherapy resistance in stage III ovarian serous carcinomas, BMC Cancer, 9, 368, 10.1186/1471-2407-9-368 Petrelli, 2002, The endophilin-CIN85-Cbl complex mediates ligand-dependent downregulation of c-Met, Nature, 416, 187, 10.1038/416187a Poudel, 2016, A time-course of orchestrated endophilin action in sensing, bending, and stabilizing curved membranes, Mol. Biol. Cell, 27, 2119, 10.1091/mbc.E16-04-0264 Raftopoulou, 2004, Cell migration: Rho GTPases lead the way, Dev. Biol., 265, 23, 10.1016/j.ydbio.2003.06.003 Razidlo, 2013, Dynamin 2 potentiates invasive migration of pancreatic tumor cells through stabilization of the Rac1 GEF Vav1, Dev. Cell, 24, 573, 10.1016/j.devcel.2013.02.010 Renard, 2015, Endophilin-A2 functions in membrane scission in clathrin-independent endocytosis, Nature, 517, 493, 10.1038/nature14064 Riedl, 2008, Lifeact: a versatile marker to visualize F-actin, Nat. Methods, 5, 605, 10.1038/nmeth.1220 Rikhy, 2002, Endophilin is critically required for synapse formation and function in Drosophila melanogaster, J. Neurosci., 22, 7478, 10.1523/JNEUROSCI.22-17-07478.2002 Rikova, 2007, Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer, Cell, 131, 1190, 10.1016/j.cell.2007.11.025 Ringstad, 1999, Endophilin/SH3p4 is required for the transition from early to late stages in clathrin-mediated synaptic vesicle endocytosis, Neuron, 24, 143, 10.1016/S0896-6273(00)80828-4 Roh-Johnson, 2017, Macrophage-dependent cytoplasmic transfer during melanoma invasion in vivo, Dev. Cell, 43, 549, 10.1016/j.devcel.2017.11.003 Rolland, 2014, The CDC42-interacting protein 4 controls epithelial cell cohesion and tumor dissemination, Dev. Cell, 30, 553, 10.1016/j.devcel.2014.08.006 Ruifrok, 2001, Quantification of histochemical staining by color deconvolution, Anal. Quant. Cytol. Histol., 23, 291 Schmitz, 2000, Rho GTPases: signaling, migration, and invasion, Exp. Cell Res., 261, 1, 10.1006/excr.2000.5049 Schuske, 2003, Endophilin is required for synaptic vesicle endocytosis by localizing Synaptojanin, Neuron, 40, 749, 10.1016/S0896-6273(03)00667-6 Sidani, 2007, Cofilin determines the migration behavior and turning frequency of metastatic cancer cells, J. Cell Biol., 179, 777, 10.1083/jcb.200707009 Sinha, 2008, Frequent deletion and methylation in SH3GL2 and CDKN2A loci are associated with early-and late-onset breast carcinoma, Ann. Surg. Oncol., 15, 1070, 10.1245/s10434-007-9790-0 Soubeyran, 2002, Cbl-CIN85-endophilin complex mediates ligand-induced downregulation of EGF receptors, Nature, 416, 183, 10.1038/416183a Soukup, 2016, A LRRK2-dependent EndophilinA phosphoswitch is critical for macroautophagy at presynaptic terminals, Neuron, 92, 829, 10.1016/j.neuron.2016.09.037 Sparks, 1998, Mutational analysis of the APC/β-catenin/Tcf pathway in colorectal cancer, Cancer Res., 58, 1130 Sporn, 1996, The war on cancer, Lancet, 347, 1377, 10.1016/S0140-6736(96)91015-6 Timmins, 2007, Generation of multicellular tumor spheroids by the hanging-drop method, Methods Mol. Med., 140, 141, 10.1007/978-1-59745-443-8_8 Worthylake, 2000, Crystal structure of Rac1 in complex with the guanine nucleotide exchange region of Tiam1, Nature, 408, 682, 10.1038/35047014 Wu, 2005, FAK-mediated Src phosphorylation of endophilin A2 inhibits endocytosis of MT1-MMP and promotes ECM degradation, Dev. Cell, 9, 185, 10.1016/j.devcel.2005.06.006 Xu, 2010, The role of fibroblast Tiam1 in tumor cell invasion and metastasis, Oncogene, 29, 6533, 10.1038/onc.2010.385 Yam, 2004, Identification and characterization of EBP, a novel EEN binding protein that inhibits Ras signaling and is recruited into the nucleus by the MLL-EEN fusion protein, Blood, 103, 1445, 10.1182/blood-2003-07-2452 Zhao, 2011, I-BAR domain proteins: linking actin and plasma membrane dynamics, Curr. Opin. Cell Biol., 23, 14, 10.1016/j.ceb.2010.10.005