Endocytic Trafficking of Membrane-Bound Cargo: A Flotillin Point of View
Abstract
:1. Lipid Microdomains and Endocytosis
2. The Flotillin Protein Family
3. Discovery of the Putative Flotillin Dependent Endocytosis Pathway
Sorting Process | References |
---|---|
Flotillin assisted endocytosis | [37,41,50,57,58] |
Polarized sorting | [59,60,61,62,63,64,65] |
Exosomes | [27,44,46,66] |
Endosomal sorting | [42,67,68,69] |
Flotillin oligomerization | [11,12,26,32] |
Flotillin dependent endocytosis | [20,21] |
4. Flotillin Dependent Cargo Trafficking and Sorting: Beyond Endocytosis
4.1. Flotillins in Sorting Events within Endosomes
4.2. An Indirect Role of Flotillins in Endocytosis: Pre-Endocytic Clustering at the Plasma Membrane
5. Flotillins as Endocytic Cargo during Signaling
6. A New Era: From Flotillin Dependent to Flotillin Assisted Endocytosis
7. Conclusions: Flotillins in Membrane Trafficking–Getting the Bigger Picture
Acknowledgments
Authors Contributions
Conflicts of Interest
References
- Brown, D.A.; Rose, J.K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 1992, 68, 533–544. [Google Scholar]
- Simons, K.; Ikonen, E. Functional rafts in cell membranes. Nature 1997, 387, 569–572. [Google Scholar] [CrossRef]
- Simons, K.; Sampaio, J.L. Membrane organization and lipid rafts. Cold Spring Harb. Perspect. Biol. 2011, 3. [Google Scholar] [CrossRef]
- Brown, D.; Waneck, G.L. Glycosyl-phosphatidylinositol-anchored membrane proteins. J. Am. Soc. Nephrol. 1992, 3, 895–906. [Google Scholar]
- Fra, A.M.; Williamson, E.; Simons, K.; Parton, R.G. Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J. Biol. Chem. 1994, 269, 30745–30748. [Google Scholar]
- Sargiacomo, M.; Sudol, M.; Tang, Z.; Lisanti, M.P. Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J. Cell Biol. 1993, 122, 789–807. [Google Scholar] [CrossRef]
- Resh, M.D. Myristylation and palmitylation of Src family members: The fats of the matter. Cell 1994, 76, 411–413. [Google Scholar] [CrossRef]
- Casey, P.J. Protein lipidation in cell signaling. Science 1995, 268, 221–225. [Google Scholar]
- Levental, I.; Grzybek, M.; Simons, K. Greasing their way: Lipid modifications determine protein association with membrane rafts. Biochemistry 2010, 49, 6305–6316. [Google Scholar] [CrossRef]
- Dietrich, C.; Volovyk, Z.N.; Levi, M.; Thompson, N.L.; Jacobson, K. Partitioning of Thy-1, GM1, and cross-linked phospholipid analogs into lipid rafts reconstituted in supported model membrane monolayers. Proc. Natl. Acad. Sci. USA 2001, 98, 10642–10647. [Google Scholar]
- Neumann-Giesen, C.; Falkenbach, B.; Beicht, P.; Claasen, S.; Luers, G.; Stuermer, C.A.; Herzog, V.; Tikkanen, R. Membrane and raft association of reggie-1/flotillin-2: Role of myristoylation, palmitoylation and oligomerization and induction of filopodia by overexpression. Biochem. J. 2004, 378, 509–518. [Google Scholar] [CrossRef]
- Babuke, T.; Ruonala, M.; Meister, M.; Amaddii, M.; Genzler, C.; Esposito, A.; Tikkanen, R. Hetero-oligomerization of reggie-1/flotillin-2 and reggie-2/flotillin-1 is required for their endocytosis. Cell Signal. 2009, 21, 1287–1297. [Google Scholar] [CrossRef]
- Donaldson, J.G.; Porat-Shliom, N.; Cohen, L.A. Clathrin-independent endocytosis: A unique platform for cell signaling and PM remodeling. Cell Signal. 2009, 21, 1–6. [Google Scholar]
- Doherty, G.J.; McMahon, H.T. Mechanisms of endocytosis. Annu Rev. Biochem. 2009, 78, 857–902. [Google Scholar] [CrossRef]
- McMahon, H.T.; Boucrot, E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 2011, 12, 517–533. [Google Scholar] [CrossRef]
- Sandvig, K.; Pust, S.; Skotland, T.; van Deurs, B. Clathrin-independent endocytosis: Mechanisms and function. Curr. Opin. Cell Biol. 2011, 23, 413–420. [Google Scholar] [CrossRef]
- Parton, R.G.; del Pozo, M.A. Caveolae as plasma membrane sensors, protectors and organizers. Nat. Rev. Mol. Cell Biol. 2013, 14, 98–112. [Google Scholar] [CrossRef]
- Henley, J.R.; Krueger, E.W.; Oswald, B.J.; McNiven, M.A. Dynamin-mediated internalization of caveolae. J. Cell Biol. 1998, 141, 85–99. [Google Scholar] [CrossRef]
- Oh, P.; McIntosh, D.P.; Schnitzer, J.E. Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J. Cell Biol. 1998, 141, 101–114. [Google Scholar] [CrossRef]
- Glebov, O.O.; Bright, N.A.; Nichols, B.J. Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nat. Cell Biol. 2006, 8, 46–54. [Google Scholar] [CrossRef]
- Frick, M.; Bright, N.A.; Riento, K.; Bray, A.; Merrified, C.; Nichols, B.J. Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr. Biol. 2007, 17, 1151–1156. [Google Scholar] [CrossRef]
- Meister, M.; Zuk, A.; Tikkanen, R. Role of dynamin and clathrin in the cellular trafficking of flotillins. FEBS J. 2014, 281, 2956–2976. [Google Scholar] [CrossRef]
- Otto, G.P.; Nichols, B.J. The roles of flotillin microdomains—Endocytosis and beyond. J. Cell Sci. 2012, 124, 3933–3940. [Google Scholar] [CrossRef]
- Morrow, I.C.; Rea, S.; Martin, S.; Prior, I.A.; Prohaska, R.; Hancock, J.F.; James, D.E.; Parton, R.G. Flotillin-1/reggie-2 traffics to surface raft domains via a novel golgi-independent pathway. Identification of a novel membrane targeting domain and a role for palmitoylation. J. Biol. Chem. 2002, 277, 48834–48841. [Google Scholar] [CrossRef]
- Li, Y.; Martin, B.R.; Cravatt, B.F.; Hofmann, S.L. DHHC5 protein palmitoylates flotillin-2 and is rapidly degraded on induction of neuronal differentiation in cultured cells. J. Biol. Chem. 2012, 287, 523–530. [Google Scholar] [CrossRef]
- Solis, G.P.; Hoegg, M.; Munderloh, C.; Schrock, Y.; Malaga-Trillo, E.; Rivera-Milla, E.; Stuermer, C.A. Reggie/flotillin proteins are organized into stable tetramers in membrane microdomains. BioChem. J. 2007, 403, 313–322. [Google Scholar] [CrossRef]
- Strauss, K.; Goebel, C.; Runz, H.; Mobius, W.; Weiss, S.; Feussner, I.; Simons, M.; Schneider, A. Exosome secretion ameliorates lysosomal storage of cholesterol in Niemann-Pick type C disease. J. Biol. Chem. 2010, 285, 26279–26288. [Google Scholar]
- Bickel, P.E.; Scherer, P.E.; Schnitzer, J.E.; Oh, P.; Lisanti, M.P.; Lodish, H.F. Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J. Biol. Chem. 1997, 272, 13793–13802. [Google Scholar]
- Volonte, D.; Galbiati, F.; Li, S.; Nishiyama, K.; Okamoto, T.; Lisanti, M.P. Flotillins/cavatellins are differentially expressed in cells and tissues and form a hetero-oligomeric complex with caveolins in vivo. Characterization and epitope-mapping of a novel flotillin-1 monoclonal antibody probe. J. Biol. Chem. 1999, 274, 12702–12709. [Google Scholar]
- Fernow, I.; Icking, A.; Tikkanen, R. Reggie-1 and reggie-2 localize in non-caveolar rafts in epithelial cells: Cellular localization is not dependent on the expression of caveolin proteins. Eur. J. Cell Biol. 2007, 86, 345–352. [Google Scholar] [CrossRef]
- Liu, J.; Deyoung, S.M.; Zhang, M.; Dold, L.H.; Saltiel, A.R. The stomatin/prohibitin/flotillin/HflK/C domain of flotillin-1 contains distinct sequences that direct plasma membrane localization and protein interactions in 3T3-L1 adipocytes. J. Biol. Chem. 2005, 280, 16125–16134. [Google Scholar] [CrossRef]
- Neumann-Giesen, C.; Fernow, I.; Amaddii, M.; Tikkanen, R. Role of EGF-induced tyrosine phosphorylation of reggie-1/flotillin-2 in cell spreading and signaling to the actin cytoskeleton. J. Cell Sci. 2007, 120, 395–406. [Google Scholar] [CrossRef]
- Riento, K.; Frick, M.; Schafer, I.; Nichols, B.J. Endocytosis of flotillin-1 and flotillin-2 is regulated by Fyn kinase. J. Cell Sci. 2009, 122, 912–918. [Google Scholar]
- Kurrle, N.; John, B.; Meister, M.; Tikkanen, R. Function of Flotillins in Receptor Tyrosine Kinase Signaling and Endocytosis: Role of Tyrosine Phosphorylation and Oligomerization. In Protein Phosphorylation in Human Health; Huang, C., Ed.; InTech Publisher: Rijeka, Croatia, 2012. [Google Scholar]
- Edgar, A.J.; Polak, J.M. Flotillin-1: Gene structure: CDNA cloning from human lung and the identification of alternative polyadenylation signals. Int. J. BioChem. Cell Biol. 2001, 33, 53–64. [Google Scholar]
- Rivera-Milla, E.; Stuermer, C.A.; Malaga-Trillo, E. Ancient origin of reggie (flotillin), reggie-like, and other lipid-raft proteins: Convergent evolution of the SPFH domain. Cell Mol. Life Sci. 2006, 63, 343–357. [Google Scholar]
- Amaddii, M.; Meister, M.; Banning, A.; Tomasovic, A.; Mooz, J.; Rajalingam, K.; Tikkanen, R. Flotillin-1/reggie-2 protein plays dual role in activation of receptor-tyrosine kinase/mitogen-activated protein kinase signaling. J. Biol. Chem. 2012, 287, 7265–7278. [Google Scholar]
- Banning, A.; Regenbrecht, C.R.; Tikkanen, R. Increased activity of mitogen activated protein kinase pathway in flotillin-2 knockout mouse model. Cell Signal. 2014, 26, 198–207. [Google Scholar]
- Banning, A.; Kurrle, N.; Meister, M.; Tikkanen, R. Flotillins in receptor tyrosine kinase signaling and cancer. Cells 2014, 3, 129–149. [Google Scholar]
- Meister, M.; Tomasovic, A.; Banning, A.; Tikkanen, R. Mitogen-Activated Protein (MAP) Kinase Scaffolding Proteins: A Recount. Int. J. Mol. Sci. 2013, 14, 4854–4884. [Google Scholar] [CrossRef]
- Stuermer, C.A.; Lang, D.M.; Kirsch, F.; Wiechers, M.; Deininger, S.O.; Plattner, H. Glycosylphosphatidyl inositol-anchored proteins and fyn kinase assemble in noncaveolar plasma membrane microdomains defined by reggie-1 and -2. Mol. Biol. Cell 2001, 12, 3031–3045. [Google Scholar] [CrossRef]
- Solis, G.P.; Hulsbusch, N.; Radon, Y.; Katanaev, V.L.; Plattner, H.; Stuermer, C.A. Reggies/flotillins interact with Rab11a and SNX4 at the tubulovesicular recycling compartment and function in transferrin receptor and E-cadherin trafficking. Mol. Biol. Cell 2013, 24, 2689–2702. [Google Scholar]
- Gagescu, R.; Demaurex, N.; Parton, R.G.; Hunziker, W.; Huber, L.A.; Gruenberg, J. The recycling endosome of Madin-Darby canine kidney cells is a mildly acidic compartment rich in raft components. Mol. Biol. Cell 2000, 11, 2775–2791. [Google Scholar]
- de Gassart, A.; Geminard, C.; Fevrier, B.; Raposo, G.; Vidal, M. Lipid raft-associated protein sorting in exosomes. Blood 2003, 102, 4336–4344. [Google Scholar] [CrossRef]
- Dermine, J.F.; Duclos, S.; Garin, J.; St-Louis, F.; Rea, S.; Parton, R.G.; Desjardins, M. Flotillin-1-enriched lipid raft domains accumulate on maturing phagosomes. J. Biol. Chem. 2001, 276, 18507–18512. [Google Scholar]
- Phuyal, S.; Hessvik, N.P.; Skotland, T.; Sandvig, K.; Llorente, A. Regulation of exosome release by glycosphingolipids and flotillins. FEBS J. 2014, 281, 2214–2227. [Google Scholar]
- Tomasovic, A.; Traub, S.; Tikkanen, R. Molecular networks in FGF signaling: Flotillin-1 and cbl-associated protein compete for the binding to fibroblast growth factor receptor substrate 2. PLoS ONE 2012, 7, e29739. [Google Scholar] [CrossRef]
- Vercauteren, D.; Piest, M.; van der Aa, L.J.; Al Soraj, M.; Jones, A.T.; Engbersen, J.F.; de Smedt, S.C.; Braeckmans, K. Flotillin-dependent endocytosis and a phagocytosis-like mechanism for cellular internalization of disulfide-based poly(amido amine)/DNA polyplexes. Biomaterials 2011, 32, 3072–3084. [Google Scholar]
- Payne, C.K.; Jones, S.A.; Chen, C.; Zhuang, X. Internalization and trafficking of cell surface proteoglycans and proteoglycan-binding ligands. Traffic 2007, 8, 389–401. [Google Scholar]
- Ge, L.; Qi, W.; Wang, L.J.; Miao, H.H.; Qu, Y.X.; Li, B.L.; Song, B.L. Flotillins play an essential role in Niemann-Pick C1-like 1-mediated cholesterol uptake. Proc. Natl. Acad. Sci. USA 2011, 108, 551–556. [Google Scholar]
- Ford, M.G.; Pearse, B.M.; Higgins, M.K.; Vallis, Y.; Owen, D.J.; Gibson, A.; Hopkins, C.R.; Evans, P.R.; McMahon, H.T. Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 2001, 291, 1051–1055. [Google Scholar] [CrossRef]
- Al Soraj, M.; He, L.; Peynshaert, K.; Cousaert, J.; Vercauteren, D.; Braeckmans, K.; de Smedt, S.C.; Jones, A.T. siRNA and pharmacological inhibition of endocytic pathways to characterize the differential role of macropinocytosis and the actin cytoskeleton on cellular uptake of dextran and cationic cell penetrating peptides octaarginine (R8) and HIV-Tat. J. Control. Release 2012, 161, 132–141. [Google Scholar]
- Hansen, G.H.; Dalskov, S.M.; Rasmussen, C.R.; Immerdal, L.; Niels-Christiansen, L.L.; Danielsen, E.M. Cholera toxin entry into pig enterocytes occurs via a lipid raft- and clathrin-dependent mechanism. Biochemistry 2005, 44, 873–882. [Google Scholar]
- Nichols, B.J. GM1-containing lipid rafts are depleted within clathrin-coated pits. Curr. Biol. 2003, 13, 686–690. [Google Scholar]
- Kusumi, A.; Koyama-Honda, I.; Suzuki, K. Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic 2004, 5, 213–230. [Google Scholar] [CrossRef]
- Brameshuber, M.; Weghuber, J.; Ruprecht, V.; Gombos, I.; Horvath, I.; Vigh, L.; Eckerstorfer, P.; Kiss, E.; Stockinger, H.; Schutz, G.J. Imaging of mobile long-lived nanoplatforms in the live cell plasma membrane. J. Biol. Chem. 2010, 285, 41765–41771. [Google Scholar] [CrossRef]
- Schneider, A.; Rajendran, L.; Honsho, M.; Gralle, M.; Donnert, G.; Wouters, F.; Hell, S.W.; Simons, M. Flotillin-dependent clustering of the amyloid precursor protein regulates its endocytosis and amyloidogenic processing in neurons. J. NeuroSci. 2008, 28, 2874–2882. [Google Scholar]
- Cremona, M.L.; Matthies, H.J.; Pau, K.; Bowton, E.; Speed, N.; Lute, B.J.; Anderson, M.; Sen, N.; Robertson, S.D.; Vaughan, R.A.; et al. Flotillin-1 is essential for PKC-triggered endocytosis and membrane microdomain localization of DAT. Nat. NeuroSci. 2011, 14, 469–477. [Google Scholar] [CrossRef]
- Gorgens, A.; Beckmann, J.; Ludwig, A.K.; Mollmann, M.; Durig, J.; Horn, P.A.; Rajendran, L.; Giebel, B. Lipid raft redistribution and morphological cell polarization are separable processes providing a basis for hematopoietic stem and progenitor cell migration. Int. J. BioChem. Cell Biol. 2012, 44, 1121–1132. [Google Scholar] [CrossRef]
- Rajendran, L.; Beckmann, J.; Magenau, A.; Boneberg, E.M.; Gaus, K.; Viola, A.; Giebel, B.; Illges, H. Flotillins are involved in the polarization of primitive and mature hematopoietic cells. PLoS ONE 2009, 4, e8290. [Google Scholar]
- Rajendran, L.; Masilamani, M.; Solomon, S.; Tikkanen, R.; Stuermer, C.A.; Plattner, H.; Illges, H. Asymmetric localization of flotillins/reggies in preassembled platforms confers inherent polarity to hematopoietic cells. Proc. Natl. Acad. Sci. USA 2003, 100, 8241–8246. [Google Scholar]
- Langhorst, M.F.; Reuter, A.; Luxenhofer, G.; Boneberg, E.M.; Legler, D.F.; Plattner, H.; Stuermer, C.A. Preformed reggie/flotillin caps: Stable priming platforms for macrodomain assembly in T cells. FASEB J. 2006, 20, 711–713. [Google Scholar]
- Affentranger, S.; Martinelli, S.; Hahn, J.; Rossy, J.; Niggli, V. Dynamic reorganization of flotillins in chemokine-stimulated human T-lymphocytes. BMC Cell Biol. 2011, 12, 28. [Google Scholar] [CrossRef] [Green Version]
- Rossy, J.; Schlicht, D.; Engelhardt, B.; Niggli, V. Flotillins interact with PSGL-1 in neutrophils and, upon stimulation, rapidly organize into membrane domains subsequently accumulating in the uropod. PLoS ONE 2009, 4, e5403. [Google Scholar]
- Ludwig, A.; Otto, G.P.; Riento, K.; Hams, E.; Fallon, P.G.; Nichols, B.J. Flotillin microdomains interact with the cortical cytoskeleton to control uropod formation and neutrophil recruitment. J. Cell Biol. 2010, 191, 771–781. [Google Scholar] [CrossRef]
- Mathivanan, S.; Simpson, R.J. ExoCarta: A compendium of exosomal proteins and RNA. Proteomics 2009, 9, 4997–5000. [Google Scholar]
- Saslowsky, D.E.; Cho, J.A.; Chinnapen, H.; Massol, R.H.; Chinnapen, D.J.; Wagner, J.S.; de Luca, H.E.; Kam, W.; Paw, B.H.; Lencer, W.I. Intoxication of zebrafish and mammalian cells by cholera toxin depends on the flotillin/reggie proteins but not Derlin-1 or -2. J. Clin. Invest. 2010, 120, 4399–4409. [Google Scholar] [CrossRef]
- Pust, S.; Dyve, A.B.; Torgersen, M.L.; van Deurs, B.; Sandvig, K. Interplay between toxin transport and flotillin localization. PLoS ONE 2010, 5, e8844. [Google Scholar]
- John, B.A.; Meister, M.; Banning, A.; Tikkanen, R. Flotillins bind to the dileucine sorting motif of beta-site amyloid precursor protein-cleaving enzyme 1 and influence its endosomal sorting. FEBS J. 2014, 281, 2074–2087. [Google Scholar] [CrossRef]
- Raposo, G.; Stoorvogel, W. Extracellular vesicles: Exosomes, microvesicles, and friends. J. Cell Biol. 2013, 200, 373–383. [Google Scholar] [CrossRef]
- Raposo, G.; Nijman, H.W.; Stoorvogel, W.; Liejendekker, R.; Harding, C.V.; Melief, C.J.; Geuze, H.J. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 1996, 183, 1161–1172. [Google Scholar] [CrossRef]
- Staubach, S.; Razawi, H.; Hanisch, F.G. Proteomics of MUC1-containing lipid rafts from plasma membranes and exosomes of human breast carcinoma cells MCF-7. Proteomics 2009, 9, 2820–2835. [Google Scholar]
- Baietti, M.F.; Zhang, Z.; Mortier, E.; Melchior, A.; Degeest, G.; Geeraerts, A.; Ivarsson, Y.; Depoortere, F.; Coomans, C.; Vermeiren, E.; Zimmermann, P.; David, G. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat. Cell. Biol. 2012, 14, 677–685. [Google Scholar] [CrossRef]
- He, X.; Chang, W.P.; Koelsch, G.; Tang, J. Memapsin 2 (beta-secretase) cytosolic domain binds to the VHS domains of GGA1 and GGA2: Implications on the endocytosis mechanism of memapsin 2. FEBS Lett. 2002, 524, 183–187. [Google Scholar] [CrossRef]
- Pastorino, L.; Ikin, A.F.; Nairn, A.C.; Pursnani, A.; Buxbaum, J.D. The carboxyl-terminus of BACE contains a sorting signal that regulates BACE trafficking but not the formation of total A(beta). Mol. Cell NeuroSci. 2002, 19, 175–185. [Google Scholar]
- Walter, J.; Fluhrer, R.; Hartung, B.; Willem, M.; Kaether, C.; Capell, A.; Lammich, S.; Multhaup, G.; Haass, C. Phosphorylation regulates intracellular trafficking of beta-secretase. J. Biol. Chem. 2001, 276, 14634–14641. [Google Scholar] [CrossRef]
- Kang, E.L.; Cameron, A.N.; Piazza, F.; Walker, K.R.; Tesco, G. Ubiquitin regulates GGA3-mediated degradation of BACE1. J. Biol. Chem. 2010, 285, 24108–24119. [Google Scholar]
- Tesco, G.; Koh, Y.H.; Kang, E.L.; Cameron, A.N.; Das, S.; Sena-Esteves, M.; Hiltunen, M.; Yang, S.H.; Zhong, Z.; Shen, Y.; et al. Depletion of GGA3 stabilizes BACE and enhances beta-secretase activity. Neuron 2007, 54, 721–737. [Google Scholar] [CrossRef]
- Solis, G.P.; Schrock, Y.; Hulsbusch, N.; Wiechers, M.; Plattner, H.; Stuermer, C.A. Reggies/flotillins regulate E-cadherin-mediated cell contact formation by affecting EGFR trafficking. Mol. Biol. Cell 2012, 23, 1812–1825. [Google Scholar]
- Sorkina, T.; Caltagarone, J.; Sorkin, A. Flotillins regulate membrane mobility of the dopamine transporter but are not required for its protein kinase C dependent endocytosis. Traffic 2013, 14, 709–724. [Google Scholar]
- Koo, E.H.; Squazzo, S.L. Evidence that production and release of amyloid beta-protein involves the endocytic pathway. J. Biol. Chem. 1994, 269, 17386–17389. [Google Scholar]
- Koo, E.H.; Squazzo, S.L.; Selkoe, D.J.; Koo, C.H. Trafficking of cell-surface amyloid beta-protein precursor. I. Secretion, endocytosis and recycling as detected by labeled monoclonal antibody. J. Cell Sci. 1996, 109, 991–998. [Google Scholar]
- Perez, R.G.; Soriano, S.; Hayes, J.D.; Ostaszewski, B.; Xia, W.; Selkoe, D.J.; Chen, X.; Stokin, G.B.; Koo, E.H. Mutagenesis identifies new signals for beta-amyloid precursor protein endocytosis, turnover, and the generation of secreted fragments, including Abeta42. J. Biol. Chem. 1999, 274, 18851–18856. [Google Scholar] [CrossRef]
- Sorkina, T.; Hoover, B.R.; Zahniser, N.R.; Sorkin, A. Constitutive and protein kinase C-induced internalization of the dopamine transporter is mediated by a clathrin-dependent mechanism. Traffic 2005, 6, 157–170. [Google Scholar] [CrossRef]
- Sigismund, S.; Argenzio, E.; Tosoni, D.; Cavallaro, E.; Polo, S.; di Fiore, P.P. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev. Cell 2008, 15, 209–219. [Google Scholar]
- Sigismund, S.; Woelk, T.; Puri, C.; Maspero, E.; Tacchetti, C.; Transidico, P.; di Fiore, P.P.; Polo, S. Clathrin-independent endocytosis of ubiquitinated cargos. Proc. Natl. Acad. Sci. USA 2005, 102, 2760–2765. [Google Scholar] [CrossRef]
- Puri, C.; Tosoni, D.; Comai, R.; Rabellino, A.; Segat, D.; Caneva, F.; Luzzi, P.; di Fiore, P.P.; Tacchetti, C. Relationships between EGFR signaling-competent and endocytosis-competent membrane microdomains. Mol. Biol. Cell 2005, 16, 2704–2718. [Google Scholar] [CrossRef]
- Roitbak, T.; Ward, C.J.; Harris, P.C.; Bacallao, R.; Ness, S.A.; Wandinger-Ness, A. A polycystin-1 multiprotein complex is disrupted in polycystic kidney disease cells. Mol. Biol. Cell 2004, 15, 1334–1346. [Google Scholar]
- Ge, L.; Wang, J.; Qi, W.; Miao, H.H.; Cao, J.; Qu, Y.X.; Li, B.L.; Song, B.L. The cholesterol absorption inhibitor ezetimibe acts by blocking the sterol-induced internalization of NPC1L1. Cell Metab. 2008, 7, 508–519. [Google Scholar] [CrossRef]
- Abrami, L.; Bischofberger, M.; Kunz, B.; Groux, R.; van der Goot, F.G. Endocytosis of the anthraxtoxin is mediated by clathrin, actin and unconventional adaptors. PLoS Pathog. 2010, 6, e1000792. [Google Scholar] [CrossRef]
- Abrami, L.; Kunz, B.; van der Goot, F.G. Anthrax toxin triggers the activation of src-like kinases to mediate its own uptake. Proc. Natl. Acad. Sci. USA 2010, 107, 1420–1424. [Google Scholar] [CrossRef]
- Abrami, L.; Liu, S.; Cosson, P.; Leppla, S.H.; van der Goot, F.G. Anthrax toxin triggers endocytosisof its receptor via a lipid raft-mediated clathrin-dependent process. J. Cell Biol. 2003, 160, 321–328. [Google Scholar] [CrossRef]
- Deinhardt, K.; Berninghausen, O.; Willison, H.J.; Hopkins, C.R.; Schiavo, G. Tetanus toxin is internalized by a sequential clathrin-dependent mechanism initiated within lipid microdomains and independent of epsin1. J. Cell Biol. 2006, 174, 459–471. [Google Scholar] [CrossRef]
- Van Dam, E.M.; Stoorvogel, W. Dynamin-dependent transferrin receptor recycling by endosome-derived clathrin-coated vesicles. Mol. Biol. Cell 2002, 13, 169–182. [Google Scholar] [CrossRef]
- Van Dam, E.M.; Ten Broeke, T.; Jansen, K.; Spijkers, P.; Stoorvogel, W. Endocytosed transferrin receptors recycle via distinct dynamin and phosphatidylinositol 3-kinase-dependent pathways. J. Biol. Chem. 2002, 277, 48876–48883. [Google Scholar]
© 2014 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/3.0/).
Share and Cite
Meister, M.; Tikkanen, R. Endocytic Trafficking of Membrane-Bound Cargo: A Flotillin Point of View. Membranes 2014, 4, 356-371. https://doi.org/10.3390/membranes4030356
Meister M, Tikkanen R. Endocytic Trafficking of Membrane-Bound Cargo: A Flotillin Point of View. Membranes. 2014; 4(3):356-371. https://doi.org/10.3390/membranes4030356
Chicago/Turabian StyleMeister, Melanie, and Ritva Tikkanen. 2014. "Endocytic Trafficking of Membrane-Bound Cargo: A Flotillin Point of View" Membranes 4, no. 3: 356-371. https://doi.org/10.3390/membranes4030356
APA StyleMeister, M., & Tikkanen, R. (2014). Endocytic Trafficking of Membrane-Bound Cargo: A Flotillin Point of View. Membranes, 4(3), 356-371. https://doi.org/10.3390/membranes4030356