A membrane fusion protein, Ykt6, regulates epithelial cell migration via microRNA-mediated suppression of Junctional Adhesion Molecule A

References

• Bryant DM,Mostov KE. From cells to organs: building polarized tissue. Nat Rev Mol Cell Biol. 2008;9:887–901.
   PubMed Web of Science ®Google Scholar
• Fletcher SJ, Rappoport JZ. The role of vesicle trafficking in epithelial cell motility. Biochem Soc Trans. 2009;37:1072–1076.
   PubMed Web of Science ®Google Scholar
• Wirtz-Peitz F, Zallen JA. Junctional trafficking and epithelial morphogenesis. Curr Opin Gen Develop. 2009;19:350–356.
   PubMed Web of Science ®Google Scholar
• Ridley AJ, Schwartz MA, Burridge K, et al. Cell migration: integrating signals from front to back. Science. 2003;302:1704–1709.
   PubMed Web of Science ®Google Scholar
• Luftman K, Hasan N, Day P, et al. Silencing of VAMP3 inhibits cell migration and integrin-mediated adhesion. Biochem Biophys Res Commun. 2009;380:65–70.
   PubMed Web of Science ®Google Scholar
• Mendoza P, Diaz J, Torres VA. On the role of Rab5 in cell migration. Curr Mol Med. 2014;14:235–245.
   PubMed Web of Science ®Google Scholar
• Naydenov NG, Feygin A, Wang L, et al. N-ethylmaleimide-sensitive factor attachment protein alpha (αSNAP) regulates matrix adhesion and integrin processing in human epithelial cells. J Biol Chem. 2014;289:2424–2439.
   PubMed Web of Science ®Google Scholar
• Williams KC, Cappolino MG. Phosphorylation of membrane type 1-matrix metalloproteinase (MT1-MMP) and its vesicle-associated membrane protein 7 (VAMP7)-dependent trafficking facilitate cell invasion and migration. J Biol Chem. 2011;286:43405–43416.
   PubMed Web of Science ®Google Scholar
• Williams KC, Cappolino MG. SNARE-dependent interaction of Src, EGFR and beta1 integrin regulates invadopodia formation and tumor cell invasion. J Cell Sci. 2014;127:1712–1725.
   PubMed Web of Science ®Google Scholar
• Williamson RC, Cowell CA, Hammond CL, et al. Coronin-1C and RCC2 guide mesenchymal migration by trafficking Rac1 and controlling GEF exposure. J Cell Sci. 2014;127:4292–4307.
   PubMed Web of Science ®Google Scholar
• Lanzetti L, Di Fiore PP. Behind the Scenes: endo/Exocytosis in the Acquisition of Metastatic Traits. Cancer Res. 2017;77:1813–1817.
   PubMed Web of Science ®Google Scholar
• Bonifacino JS, Glick BS. The mechanisms of vesicle budding and fusion. Cell. 2004;116:153–166.
   PubMed Web of Science ®Google Scholar
• Hong W. SNAREs and traffic. Biochim Biophys Acta. 2005;1744:493–517.
   PubMed Web of Science ®Google Scholar
• Malsam J, Kreye S, Sollner TH. Membrane fusion: sNAREs and regulation. Cell Mol Life Sci. 2008;65:2814–2832.
   PubMed Web of Science ®Google Scholar
• Malsam J, Sollner TH. Organization of SNAREs within the Golgi stack. Cold Spring Harb Perspect Biol. 2011;3:a005249.
   PubMed Web of Science ®Google Scholar
• Day P, Riggs KA, Hasan N, et al. Syntaxins 3 and 4 mediate vesicular trafficking of α5β1 and α3β1 integrins and cancer cell migration. Int J Oncol. 2011;39:863–871.
   PubMed Web of Science ®Google Scholar
• Kean MJ, Williams KC, Skalski M, et al. VAMP3, syntaxin-13 and SNAP23 are involved in secretion of matrix metalloproteinases, degradation of the extracellular matrix and cell invasion. J Cell Sci. 2009;122:4089–4098.
   PubMed Web of Science ®Google Scholar
• Garcia-Melero A, Reverter M, Hoque M, et al. Annexin A6 and Late Endosomal Cholesterol Modulate Integrin Recycling and Cell Migration. J Biol Chem. 2016;291:1320–1335.
   PubMed Web of Science ®Google Scholar
• Tiwari A, Jung JJ, Inamdar SM, et al. Endothelial cell migration on fibronectin is regulated by syntaxin 6-mediated α5β1 integrin recycling. J Biol Chem. 2011;286:36749–36761.
   PubMed Web of Science ®Google Scholar
• Fukasawa M, Varlamov O, Eng WS, et al. Localization and activity of the SNARE Ykt6 determined by its regulatory domain and palmitoylation. Proc Natl Acad Sci U S A. 2004;101:4815–4820.
   PubMed Web of Science ®Google Scholar
• McNew JA, Sogaard M, Lampen NM, et al. Ykt6p, a prenylated SNARE essential for endoplasmic reticulum-Golgi transport. J Biol Chem. 1997;272:17776–17783.
   PubMed Web of Science ®Google Scholar
• Hasegawa H, Zinsser S, Rhee Y, et al. Mammalian ykt6 is a neuronal SNARE targeted to a specialized compartment by its profilin-like amino terminal domain. Mol Biol Cell. 2003;14:698–720.
   PubMed Web of Science ®Google Scholar
• Tochio H, Tsui MM, Banfield DK, et al. An autoinhibitory mechanism for nonsyntaxin SNARE proteins revealed by the structure of Ykt6p. Science. 2001;293:698–702.
   PubMed Web of Science ®Google Scholar
• Wen W, Yu J, Pan L, et al. Lipid-Induced conformational switch controls fusion activity of longin domain SNARE Ykt6. Mol Cell. 2010;37:383–395.
   PubMed Web of Science ®Google Scholar
• Parlati F, Varlamov O, Paz K, et al. Distinct SNARE complexes mediating membrane fusion in Golgi transport based on combinatorial specificity. Proc Natl Acad Sci U S A. 2002;99:5424–5429.
   PubMed Web of Science ®Google Scholar
• Santos AJ, Raote I, Scarpa M, et al. TANGO1 recruits ERGIC membranes to the endoplasmic reticulum for procollagen export. Elife. 2015;4:e10982.
   Web of Science ®Google Scholar
• Volchuk A, Ravazzola M, Perrelet A, et al. Countercurrent distribution of two distinct SNARE complexes mediating transport within the Golgi stack. Mol Biol Cell. 2004;15:1506–1518.
   PubMed Web of Science ®Google Scholar
• Zhang T, Hong W. Ykt6 forms a SNARE complex with syntaxin 5, GS28, and Bet1 and participates in a late stage in endoplasmic reticulum-Golgi transport. J Biol Chem. 2001;276:27480–27487.
   PubMedGoogle Scholar
• Hasegawa H, Yang Z, Oltedal L, et al. Intramolecular protein-protein and protein-lipid interactions control the conformation and subcellular targeting of neuronal Ykt6. J Cell Sci. 2004;117:4495–4508.
   PubMed Web of Science ®Google Scholar
• Peltan A, Briggs L, Matthews G, et al. Identification of Drosophila gene products required for phagocytosis of Leishmania donovani. PLoS ONE. 2012;7:e51831.
   PubMed Web of Science ®Google Scholar
• Gross JC, Chaudhary V, Bartscherer K, et al. Active Wnt proteins are secreted on exosomes. Nat Cell Biol. 2012;14:1036–1045.
   PubMed Web of Science ®Google Scholar
• Gordon DE, Chia J, Jayawardena K, et al. VAMP3/Syb and YKT6 are required for the fusion of constitutive secretory carriers with the plasma membrane. PLoS Genetics. 2017;13:e1006698.
   PubMed Web of Science ®Google Scholar
• Naydenov NG, Brown B, Harris G, et al. A membrane fusion protein αSNAP is a novel regulator of epithelial apical junctions. PLoS ONE. 2012;7:e34320.
   PubMed Web of Science ®Google Scholar
• Ivanov AI, Pero RS, Scheck AC, et al. Prostaglandin E(2)-synthesizing enzymes in fever: differential transcriptional regulation. Am J Physiol Regul Integr Comp Physiol. 2002;283:R1104–17.
   PubMed Web of Science ®Google Scholar
• Naydenov NG, Harris G, Morales V, et al. Loss of a membrane trafficking protein αSNAP induces non-canonical autophagy in human epithelia. Cell Cycle. 2012;11:4613–4625.
   PubMed Web of Science ®Google Scholar
• Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9:671–675.
   PubMed Web of Science ®Google Scholar
• Friedl P, Mayor R. Tuning collective cell migration by cell-cell junction regulation. Cold Spring Harb Perspect Biol. 2017;9:a029199.
   Web of Science ®Google Scholar
• McSherry EA, Brennan K, Hudson L, et al. Breast cancer cell migration is regulated through junctional adhesion molecule-A-mediated activation of Rap1 GTPase. Breast Cancer Res. 2011;13:R31.
   PubMed Web of Science ®Google Scholar
• McSherry EA, McGee SF, Jirstrom K, et al. JAM-A expression positively correlates with poor prognosis in breast cancer patients. Int J Cancer. 2009;125:1343–1351.
   PubMed Web of Science ®Google Scholar
• Severson EA, Jiang L, Ivanov AI, et al. Cis-dimerization mediates function of junctional adhesion molecule A. Mol Biol Cell. 2008;19:1862–1872.
   PubMed Web of Science ®Google Scholar
• Severson EA, Lee WY, Capaldo CT, et al. Junctional adhesion molecule A interacts with Afadin and PDZ-GEF2 to activate Rap1A, regulate β1 integrin levels, and enhance cell migration. Mol Biol Cell. 2009;20:1916–1925.
   PubMed Web of Science ®Google Scholar
• Courilleau D, Bisserier M, Jullian JC, et al. Identification of a tetrahydroquinoline analog as a pharmacological inhibitor of the cAMP-binding protein Epac. J Biol Chem. 2012;287:44192–44202.
   PubMed Web of Science ®Google Scholar
• Arthur WT, Quilliam LA, Cooper JA. Rap1 promotes cell spreading by localizing Rac guanine nucleotide exchange factors. J Cell Biol. 2004;167:111–122.
   PubMed Web of Science ®Google Scholar
• Takahashi M, Rikitake Y, Nagamatsu Y, et al. Sequential activation of Rap1 and Rac1 small G proteins by PDGF locally at leading edges of NIH3T3 cells. Genes Cells. 2008;13:549–569.
   PubMed Web of Science ®Google Scholar
• Shutes A, Onesto C, Picard V, et al. Specificity and mechanism of action of EHT 1864, a novel small molecule inhibitor of Rac family small GTPases. J Biol Chem. 2007;282:35666–35678.
   PubMed Web of Science ®Google Scholar
• Mathonnet G, Fabian MR, Svitkin YV, et al. MicroRNA inhibition of translation initiation in vitro by targeting the cap-binding complex eIF4F. Science. 2007;317:1764–1767.
   PubMed Web of Science ®Google Scholar
• Pillai RS, Bhattacharyya SN, Artus CG, et al. Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science. 2005;309:1573–1576.
   PubMed Web of Science ®Google Scholar
• Alvarado AG, Turaga SM, Sathyan P, et al. Coordination of self-renewal in glioblastoma by integration of adhesion and microRNA signaling. Neuro Oncol. 2016;18:656–666.
   PubMed Web of Science ®Google Scholar
• Cao M, Nie W, Li J, et al. MicroRNA-495 induces breast cancer cell migration by targeting JAM-A. Protein Cell. 2014;5:862–872.
   PubMed Web of Science ®Google Scholar
• Gotte M, Mohr C, Koo CY, et al. miR-145-dependent targeting of junctional adhesion molecule A and modulation of fascin expression are associated with reduced breast cancer cell motility and invasiveness. Oncogene. 2010;29:6569–6580.
   PubMed Web of Science ®Google Scholar
• Miyata R, Kakuki T, Nomura K, et al. Poly(I:C) induced microRNA-146a regulates epithelial barrier and secretion of proinflammatory cytokines in human nasal epithelial cells. Eur J Pharmacol. 2015;761:375–382.
   PubMed Web of Science ®Google Scholar
• Kim YJ, Maizel A, Chen X. Traffic into silence: endomembranes and post-transcriptional RNA silencing. EMBO J. 2014;33:968–980.
   PubMed Web of Science ®Google Scholar
• Smalheiser NR. Regulation of mammalian microRNA processing and function by cellular signaling and subcellular localization. Biochim Biophys Acta. 2008;1779:678–681.
   PubMed Web of Science ®Google Scholar
• Gordon DE, Bond LM, Sahlender DA, et al. A targeted siRNA screen to identify SNAREs required for constitutive secretion in mammalian cells. Traffic. 2010;11:1191–1204.
   PubMed Web of Science ®Google Scholar
• Ikari A, Tonegawa C, Sanada A, et al. Tight junctional localization of claudin-16 is regulated by syntaxin 8 in renal tubular epithelial cells. J Biol Chem. 2014;289:13112–13123.
   PubMed Web of Science ®Google Scholar
• Jung JJ, Inamdar SM, Tiwari A, et al. Syntaxin 16 regulates lumen formation during epithelial morphogenesis. PLoS ONE. 2013;8:e61857.
   PubMed Web of Science ®Google Scholar
• Sharma N, Low SH, Misra S, et al. Apical targeting of syntaxin 3 is essential for epithelial cell polarity. J Cell Biol. 2006;173:937–948.
   PubMed Web of Science ®Google Scholar
• Luissint AC, Nusrat A, Parkos CA. JAM-related proteins in mucosal homeostasis and inflammation. Semin Immunopathol. 2014;36:211–226.
   PubMed Web of Science ®Google Scholar
• Severson EA, Parkos CA. Structural determinants of Junctional Adhesion Molecule A (JAM-A) function and mechanisms of intracellular signaling. Curr Opin Cell Biol. 2009;21:701–707.
   PubMed Web of Science ®Google Scholar
• Naik MU, Naik UP. Junctional adhesion molecule-A-induced endothelial cell migration on vitronectin is integrin αv β3 specific. J Cell Sci. 2006;119:490–499.
   PubMed Web of Science ®Google Scholar
• Peddibhotla SS, Brinkmann BF, Kummer D, et al. Tetraspanin CD9 links junctional adhesion molecule-A to αvβ3 integrin to mediate basic fibroblast growth factor-specific angiogenic signaling. Mol Biol Cell. 2013;24:933–944.
   PubMed Web of Science ®Google Scholar
• Schmitt MM, Megens RT, Zernecke A, et al. Endothelial junctional adhesion molecule-a guides monocytes into flow-dependent predilection sites of atherosclerosis. Circulation. 2014;129:66–76.
   PubMed Web of Science ®Google Scholar
• Ikemura K, Yamamoto M, Miyazaki S, et al. MicroRNA-145 post-transcriptionally regulates the expression and function of P-glycoprotein in intestinal epithelial cells. Mol Pharmacol. 2013;83:399–405.
   PubMed Web of Science ®Google Scholar
• Wu H, Xiao Z, Wang K, et al. MiR-145 is downregulated in human ovarian cancer and modulates cell growth and invasion by targeting p70S6K1 and MUC1. Biochem Biophys Res Commun. 2013;441:693–700.
   PubMed Web of Science ®Google Scholar
• Zhang J, Guo H, Zhang H, et al. Putative tumor suppressor miR-145 inhibits colon cancer cell growth by targeting oncogene Friend leukemia virus integration 1 gene. Cancer. 2011;117:86–95.
   PubMed Web of Science ®Google Scholar
• Carthew RW, Sontheimer EJ. Origins and Mechanisms of miRNAs and siRNAs. Cell. 2009;136:642–655.
   PubMed Web of Science ®Google Scholar
• Barbato C, Ciotti MT, Serafino A, et al. Dicer expression and localization in post-mitotic neurons. Brain Res. 2007;1175:17–27.
   PubMed Web of Science ®Google Scholar
• Barman B, Bhattacharyya SN. MRNA targeting to endoplasmic reticulum precedes ago protein interaction and MicroRNA (miRNA)-mediated translation repression in mammalian cells. J Biol Chem. 2015;290:24650–24656.
   PubMed Web of Science ®Google Scholar
• Lee YS, Pressman S, Andress AP, et al. Silencing by small RNAs is linked to endosomal trafficking. Nat Cell Biol. 2009;11:1150–1156.
   PubMed Web of Science ®Google Scholar
• Pepin G, Perron MP, Provost P. Regulation of human Dicer by the resident ER membrane protein CLIMP-63. Nucl Acids Res. 2012;40:11603–11617.
   PubMed Web of Science ®Google Scholar
• Stalder L, Heusermann W, Sokol L, et al. The rough endoplasmatic reticulum is a central nucleation site of siRNA-mediated RNA silencing. EMBO J. 2013;32:1115–1127.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Holmgren BT, Hinas A. The conserved SNARE SEC-22 localizes to late endosomes and negatively regulates RNA interference in Caenorhabditis elegans. RNA. 2017;23:297–307.
   PubMed Web of Science ®Google Scholar
• Thayanidhi N, Liang Y, Hasegawa H, et al.. R-SNARE ykt6 resides in membrane-associated protease-resistant protein particles and modulates cell cycle progression when over-expressed. Biol Cell. 2012;104:397–417.
   PubMed Web of Science ®Google Scholar
• Ruiz-Martinez M, Navarro A, Marrades RM, et al. YKT6 expression, exosome release, and survival in non-small cell lung cancer. Oncotarget. 2016;7:51515–51524.
   PubMedGoogle Scholar
• Choi JW, Moon S, Jang EJ, et al. Association of prediabetes-associated single nucleotide polymorphisms with microalbuminuria. PLoS One. 2017;12:e0171367.
   PubMed Web of Science ®Google Scholar