Interplay of Endosomal pH and Ligand Occupancy in Integrin α5β1 Ubiquitination, Endocytic Sorting, and Cell Migration

Agromayor, 2012, The UBAP1 subunit of ESCRT-I interacts with ubiquitin via a SOUBA domain, Structure, 20, 414, 10.1016/j.str.2011.12.013 Ali, 2013, Recruitment of UBPY and ESCRT exchange drive HD-PTP-dependent sorting of EGFR to the MVB, Curr. Biol., 23, 453, 10.1016/j.cub.2013.02.033 Apaja, 2010, Quality control for unfolded proteins at the plasma membrane, J. Cell Biol., 191, 553, 10.1083/jcb.201006012 Apaja, 2013, Ubiquitination-dependent quality control of hERG K+ channel with acquired and inherited conformational defect at the plasma membrane, Mol. Biol. Cell, 24, 3787, 10.1091/mbc.e13-07-0417 Arjonen, 2012, Distinct recycling of active and inactive β1 integrins, Traffic, 13, 610, 10.1111/j.1600-0854.2012.01327.x Barriere, 2008, Analysis of endocytic trafficking by single-cell fluorescence ratio imaging, Curr. Protoc. Cell Biol., Chapter 15 Barriere, 2006, Molecular basis of oligoubiquitin-dependent internalization of membrane proteins in Mammalian cells, Traffic, 7, 282, 10.1111/j.1600-0854.2006.00384.x Barriere, 2007, Plasticity of polyubiquitin recognition as lysosomal targeting signals by the endosomal sorting machinery, Mol. Biol. Cell, 18, 3952, 10.1091/mbc.e07-07-0678 Böttcher, 2012, Sorting nexin 17 prevents lysosomal degradation of β1 integrins by binding to the β1-integrin tail, Nat. Cell Biol., 14, 584, 10.1038/ncb2501 Caswell, 2007, Rab25 associates with alpha5beta1 integrin to promote invasive migration in 3D microenvironments, Dev. Cell, 13, 496, 10.1016/j.devcel.2007.08.012 Caswell, 2008, Rab-coupling protein coordinates recycling of alpha5beta1 integrin and EGFR1 to promote cell migration in 3D microenvironments, J. Cell Biol., 183, 143, 10.1083/jcb.200804140 Davis, 1987, Acid-dependent ligand dissociation and recycling of LDL receptor mediated by growth factor homology region, Nature, 326, 760, 10.1038/326760a0 Doyotte, 2008, The Bro1-related protein HD-PTP/PTPN23 is required for endosomal cargo sorting and multivesicular body morphogenesis, Proc. Natl. Acad. Sci. USA, 105, 6308, 10.1073/pnas.0707601105 Dozynkiewicz, 2012, Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes/lysosomes and drive cancer progression, Dev. Cell, 22, 131, 10.1016/j.devcel.2011.11.008 Elia, 2011, Dynamics of endosomal sorting complex required for transport (ESCRT) machinery during cytokinesis and its role in abscission, Proc. Natl. Acad. Sci. USA, 108, 4846, 10.1073/pnas.1102714108 Gingras, 2009, HD-PTP is a catalytically inactive tyrosine phosphatase due to a conserved divergence in its phosphatase domain, PLoS ONE, 4, e5105, 10.1371/journal.pone.0005105 Harford, 1983, Intracellular dissociation of receptor-bound asialoglycoproteins in cultured hepatocytes. A pH-mediated nonlysosomal event, J. Biol. Chem., 258, 3191, 10.1016/S0021-9258(18)32848-5 Henne, 2013, Molecular mechanisms of the membrane sculpting ESCRT pathway, Cold Spring Harb. Perspect. Biol., 5, a016766, 10.1101/cshperspect.a016766 Hicke, 1999, Gettin’ down with ubiquitin: turning off cell-surface receptors, transporters and channels, Trends Cell Biol., 9, 107, 10.1016/S0962-8924(98)01491-3 Homan, 2014, Mutations in USP9X are associated with X-linked intellectual disability and disrupt neuronal cell migration and growth, Am. J. Hum. Genet., 94, 470, 10.1016/j.ajhg.2014.02.004 Hynes, 2002, Integrins: bidirectional, allosteric signaling machines, Cell, 110, 673, 10.1016/S0092-8674(02)00971-6 Katzmann, 2001, Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I, Cell, 106, 145, 10.1016/S0092-8674(01)00434-2 Kulka, 1988, A Chinese hamster cell cycle mutant arrested at G2 phase has a temperature-sensitive ubiquitin-activating enzyme, E1, J. Biol. Chem., 263, 15726, 10.1016/S0021-9258(19)37648-3 Lobert, 2010, Ubiquitination of α-integrin cytoplasmic tails, Commun. Integr. Biol., 3, 583, 10.4161/cib.3.6.13176 Lobert, 2012, The ESCRT machinery mediates polarization of fibroblasts through regulation of myosin light chain, J. Cell Sci., 125, 29, 10.1242/jcs.088310 Lobert, 2010, Ubiquitination of alpha 5 beta 1 integrin controls fibroblast migration through lysosomal degradation of fibronectin-integrin complexes, Dev. Cell, 19, 148, 10.1016/j.devcel.2010.06.010 Magnifico, 2003, WW domain HECT E3s target Cbl RING finger E3s for proteasomal degradation, J. Biol. Chem., 278, 43169, 10.1074/jbc.M308009200 Martin-Serrano, 2001, HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress, Nat. Med., 7, 1313, 10.1038/nm1201-1313 Marx, 2010, ErbB2 trafficking and degradation associated with K48 and K63 polyubiquitination, Cancer Res., 70, 3709, 10.1158/0008-5472.CAN-09-3768 McCullough, 2004, AMSH is an endosome-associated ubiquitin isopeptidase, J. Cell Biol., 166, 487, 10.1083/jcb.200401141 Mouchantaf, 2006, The ubiquitin ligase itch is auto-ubiquitylated in vivo and in vitro but is protected from degradation by interacting with the deubiquitylating enzyme FAM/USP9X, J. Biol. Chem., 281, 38738, 10.1074/jbc.M605959200 Murray, 2004, The FAM deubiquitylating enzyme localizes to multiple points of protein trafficking in epithelia, where it associates with E-cadherin and beta-catenin, Mol. Biol. Cell, 15, 1591, 10.1091/mbc.e03-08-0630 Murtaza, 2015, La FAM fatale: USP9X in development and disease. Cellular and molecular life sciences, Cell. Mol. Life Sci., 72, 2075, 10.1007/s00018-015-1851-0 Nagae, 2012, Crystal structure of α5β1 integrin ectodomain: atomic details of the fibronectin receptor, J. Cell Biol., 197, 131, 10.1083/jcb.201111077 Pashkova, 2013, The yeast Alix homolog Bro1 functions as a ubiquitin receptor for protein sorting into multivesicular endosomes, Dev. Cell, 25, 520, 10.1016/j.devcel.2013.04.007 Piper, 2014, Ubiquitin-dependent sorting in endocytosis, Cold Spring Harb. Perspect. Biol., 6, 6, 10.1101/cshperspect.a016808 Rainero, 2013, Late endosomal and lysosomal trafficking during integrin-mediated cell migration and invasion: cell matrix receptors are trafficked through the late endosomal pathway in a way that dictates how cells migrate, Bioessays, 35, 523, 10.1002/bies.201200160 Rajan, 1985, Evidence that dissociation, not intracellular degradation, is the major pathway for removal of receptor-bound 125I-human chorionic gonadotropin in cultured rat luteal cells, Biol. Reprod., 33, 60, 10.1095/biolreprod33.1.60 Ridley, 2003, Cell migration: integrating signals from front to back, Science, 302, 1704, 10.1126/science.1092053 Stefani, 2011, UBAP1 is a component of an endosome-specific ESCRT-I complex that is essential for MVB sorting, Curr. Biol., 21, 1245, 10.1016/j.cub.2011.06.028 Steinberg, 2012, SNX17 protects integrins from degradation by sorting between lysosomal and recycling pathways, J. Cell Biol., 197, 219, 10.1083/jcb.201111121 Takagi, 2003, Structure of integrin alpha5beta1 in complex with fibronectin, EMBO J., 22, 4607, 10.1093/emboj/cdg445 Théard, 2010, USP9x-mediated deubiquitination of EFA6 regulates de novo tight junction assembly, EMBO J., 29, 1499, 10.1038/emboj.2010.46 Thelen, 2008, Ubiquitination and endocytosis of cell adhesion molecule DM-GRASP regulate its cell surface presence and affect its role for axon navigation, J. Biol. Chem., 283, 32792, 10.1074/jbc.M805896200 Tiwari, 2011, Endothelial cell migration on fibronectin is regulated by syntaxin 6-mediated alpha5beta1 integrin recycling, J. Biol. Chem., 286, 36749, 10.1074/jbc.M111.260828 Tu, 2010, Endosomal-sorting complexes required for transport (ESCRT) pathway-dependent endosomal traffic regulates the localization of active Src at focal adhesions, Proc. Natl. Acad. Sci. USA, 107, 16107, 10.1073/pnas.1009471107 White, 2007, alpha v beta3 and alpha5beta1 integrin recycling pathways dictate downstream Rho kinase signaling to regulate persistent cell migration, J. Cell Biol., 177, 515, 10.1083/jcb.200609004 Wobst, 2012, UCHL1 regulates ubiquitination and recycling of the neural cell adhesion molecule NCAM, FEBS J., 279, 4398, 10.1111/febs.12029 Wunderley, 2014, The molecular basis for selective assembly of the UBAP1-containing endosome-specific ESCRT-I complex, J. Cell Sci., 127, 663 Xie, 2013, Deubiquitinase FAM/USP9X interacts with the E3 ubiquitin ligase SMURF1 protein and protects it from ligase activity-dependent self-degradation, J. Biol. Chem., 288, 2976, 10.1074/jbc.M112.430066