Skip to main content
SpringerLink
Log in

Shaping Membranes for Endocytosis

  • Chapter
  • First Online:
Reviews of Physiology, Biochemistry and Pharmacology 161

Part of the book series: Reviews of Physiology, Biochemistry and Pharmacology ((REVIEWS,volume 161))

Abstract

Endocytosis is essential for virtually all eukaryotic cells to internalize nutrients, antigens, pathogens, and cell surface receptors from the plasma membrane into membrane-bounded, endocytic vesicles to regulate cell homeostasis, cell signaling, and development. Distinct mechanisms mediate endocytic uptake of a large variety of distinctly sized cargoes ranging from small molecules to viruses or bacteria. Common to all of these endocytic pathways is the deformation of the plasma membrane by intracellular factors including scaffolding proteins, amphipathic peripheral membrane proteins, and lipid-modifying enzymes. In this review we summarize how different cargoes exploit distinct pathways for cell entry, and how proteins assist the generation of curved membrane domains during internalization.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

ALPS::

ArfGAP1 lipid-packing sensor;

Arf:

ADP-ribosylation factor;

BAR:

Bin-amphiphysin-Rvs;

CLASP:

Clathrin-associated sorting protein;

CME:

Clathrin-mediated endocytosis;

ENTH:

Epsin N-terminal homology;

FCH:

Fes/CIP4 homology;

GAP:

GTPase-activating protein;

GPI:

Glycosyl phosphatidylinositol;

PI:

Phosphoinositide;

PI(4,5)P2 :

Phosphatidylinositol 4,5-bisphosphate;

PIPK I:

Phosphatidylinositol 4-phosphate 5-kinase;

PLD:

Phospholipase D;

PX:

Phox: homology;

SNX9:

Sorting nexin 9;

STx:

Shiga toxin;

SV40:

Simian virus 40;

TIRF:

Total internal reflection fluorescence

References

  • Antonny B, Beraud-Dufour S, Chardin P, Chabre M (1997) N-terminal hydrophobic residues of the G-protein ADP-ribosylation factor-1 insert into membrane phospholipids upon GDP to GTP exchange. Biochemistry 36:4675–4684

    Google Scholar 

  • Bairstow SF, Ling K, Su X, Firestone AJ, Carbonara C, Anderson RA (2006) Type Igamma661 phosphatidylinositol phosphate kinase directly interacts with AP2 and regulates endocytosis. J Biol Chem 281:20632–20642

    Google Scholar 

  • Beck R, Sun Z, Adolf F, Rutz C, Bassler J, Wild K, Sinning I, Hurt E, Brügger B, Béthune J, Wieland F (2008) Membrane curvature induced by Arf1-GTP is essential for vesicle formation. Proc Natl Acad Sci U S A 105:11731–11736

    Google Scholar 

  • Behnia R, Munro S (2005) Organelle identity and the signposts for membrane traffic. Nature 438:597–604

    Google Scholar 

  • Bigay J, Gounon P, Robineau S, Antonny B (2003) Lipid packing sensed by ArfGAP1 couples COPI coat disassembly to membrane bilayer curvature. Nature 426:563–566

    Google Scholar 

  • Bonazzi M, Cossart P (2006) Bacterial entry into cells: a role for the endocytic machinery. FEBS Lett 580:2962–2967

    Google Scholar 

  • Bonifacino JS, Traub LM (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72:395–447

    Google Scholar 

  • Casanova JE (2007) Regulation of Arf activation: the Sec7 family of guanine nucleotide exchange factors. Traffic 8:1476–1485

    Google Scholar 

  • Chimini G, Chavrier P (2000) Function of Rho family proteins in actin dynamics during phagocytosis and engulfment. Nat Cell Biol 2:E191–196

    Google Scholar 

  • Cohen AW, Hnasko R, Schubert W, Lisanti MP (2004) Role of caveolae and caveolins in health and disease. Physiol Rev 84:1341–1379

    Google Scholar 

  • Damm EM, Pelkmans L, Kartenbeck J, Mezzacasa A, Kurzchalia T, Helenius A (2005) Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J Cell Biol 168:477–488

    Google Scholar 

  • Dance AL, Miller M, Seragaki S, Aryal P, White B, Aschenbrenner L, Hasson T (2004) Regulation of myosin-VI targeting to endocytic compartments. Traffic 5:798–813

    Google Scholar 

  • Delaney KA, Murph MM, Brown LM, Radhakrishna H (2002) Transfer of M2 muscarinic acetylcholine receptors to clathrin-derived early endosomes following clathrin-independent endocytosis. J Biol Chem 277:33439–33446

    Google Scholar 

  • Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651–657

    Google Scholar 

  • Donaldson JG (2003) Multiple roles for Arf6: sorting, structuring, and signaling at the plasma membrane. J Biol Chem 278:41573–41576

    Google Scholar 

  • Donaldson JG (2005) Arfs, phosphoinositides and membrane traffic. Biochem Soc Trans 33:1276–1278

    Google Scholar 

  • Drab M, Verkade P, Elger M et al (2001) Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293:2449–2452

    Google Scholar 

  • Drin G, Casella JF, Gautier R, Boehmer T, Schwartz TU, Antonny B (2007) A general amphipathic alpha-helical motif for sensing membrane curvature. Nat Struct Mol Biol 14:138–146

    Google Scholar 

  • Edeling MA, Smith C, Owen D (2006) Life of a clathrin coat: insights from clathrin and AP structures. Nat Rev Mol Cell Biol 7:32–44

    Google Scholar 

  • Edidin M (2001) Shrinking patches and slippery rafts: scales of domains in the plasma membrane. Trends Cell Biol 11:492–496

    Google Scholar 

  • Farge E, Ojcius DM, Subtil A, Dautry-Varsat A (1999) Enhancement of endocytosis due to aminophospholipid transport across the plasma membrane of living cells. Am J Physiol 276:C725–733

    Google Scholar 

  • Ford MG, Mills IG, Peter BJ, Vallis Y, Praefcke GJ, Evans PR, McMahon HT (2002) Curvature of clathrin-coated pits driven by epsin. Nature 419:361–366

    Google Scholar 

  • Fotin A, Cheng Y, Grigorieff N, Walz T, Harrison SC, Kirchhausen T (2004a) Structure of an auxilin-bound clathrin coat and its implications for the mechanism of uncoating. Nature 432:649–653

    Google Scholar 

  • Fotin A, Cheng Y, Sliz P, Grigorieff N, Harrison SC, Kirchhausen T, Walz T (2004b) Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432:573–579

    Google Scholar 

  • Frick M, Bright NA, Riento K, Bray A, Merrified C, Nichols BJ (2007) Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr Biol 17:1151–1156

    Google Scholar 

  • Frost A, Perera R, Roux A, Spasov K, Destaing O, Egelman EH, De Camilli P, Unger VM (2008) Structural basis of membrane invagination by F-BAR domains. Cell 132:807–817

    Google Scholar 

  • Gad H, Ringstad N, Löw P et al (2000) Fission and uncoating of synaptic clathrin-coated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin. Neuron 27:301–312

    Google Scholar 

  • Gallop JL, Jao CC, Kent HM, Butler PJ, Evans PR, Langen R, McMahon HT (2006) Mechanisms of endophilin N-BAR domain-mediated membrane curvature. EMBO J 25:2898–2910

    Google Scholar 

  • Gillingham AK, Munro S (2007) The small G proteins of the Arf family and their regulators. Annu Rev Cell Dev Biol 23:579–611

    Google Scholar 

  • Glebov OO, Bright NA, Nichols BJ (2006) Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nat Cell Biol 8:46–54

    Google Scholar 

  • Godi A, Di Campli A, Konstantakopoulos A et al (2004) FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P. Nat Cell Biol 6:393–404

    Google Scholar 

  • Gold ES, Underhill DM, Morrissette NS, Guo J, McNiven MA, Aderem A (1999) Dynamin 2 is required for phagocytosis in macrophages. J Exp Med 190:1849–1856

    Google Scholar 

  • Grabs D, Slepnev VI, Songyang Z, David C, Lynch M, Cantley LC, De Camilli P (1997) The SH3 domain of amphiphysin binds the proline-rich domain of dynamin at a single site that defines a new SH3 binding consensus sequence. J Biol Chem 272:13419–13425

    Google Scholar 

  • Grass I, Thiel S, Honing S, Haucke V (2004) Recognition of a basic AP-2 binding motif within the C2B domain of synaptotagmin is dependent on multimerization. J Biol Chem 279:54872–54880

    Google Scholar 

  • Habermann B (2004) The BAR-domain family of proteins: a case of bending and binding? EMBO Rep 5:250–255

    Google Scholar 

  • Harder T (2004) Lipid raft domains and protein networks in T-cell receptor signal transduction. Curr Opin Immunol 16:353–359

    Google Scholar 

  • Haucke V (2005) Phosphoinositide regulation of clathrin-mediated endocytosis. Biochem Soc Trans 33:1285–1289

    Google Scholar 

  • Heuser J (1980) Three-dimensional visualization of coated vesicle formation in fibroblasts. J Cell Biol 84:560–583

    Google Scholar 

  • de Heuvel E, Bell AW, Ramjaun AR, Wong K, Sossin WS, McPherson PS (1997) Identification of the major synaptojanin-binding proteins in brain. J Biol Chem 272:8710–8716

    Google Scholar 

  • Hicke L, Dunn R (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 19:141–172

    Google Scholar 

  • Hinrichsen L, Meyerholz A, Groos S, Ungewickell EJ (2006) Bending a membrane: how clathrin affects budding. Proc Natl Acad Sci USA 103:8715–8720

    Google Scholar 

  • Hinshaw JE (2000) Dynamin and its role in membrane fission. Annu Rev Cell Dev Biol 16:483–519

    Google Scholar 

  • Honda A, Nogami M, Yokozeki T et al (1999) Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99:521–532

    Google Scholar 

  • Honing S, Ricotta D, Krauss M et al (2005) Phosphatidylinositol-(4,5)-bisphosphate regulates sorting signal recognition by the clathrin-associated adaptor complex AP2. Mol Cell 18:519–531

    Google Scholar 

  • Huynh KK, Kay JG, Stow JL, Grinstein S (2007) Fusion, fission, and secretion during phagocytosis. Physiology (Bethesda) 22:366–372

    Google Scholar 

  • Itoh T, De Camilli P (2006) BAR, F-BAR (EFC) and ENTH/ANTH domains in the regulation of membrane-cytosol interfaces and membrane curvature. Biochim Biophys Acta 1761:897–912

    Google Scholar 

  • Jung N,Wienisch M, Gu M et al (2007) Molecular basis of synaptic vesicle cargo recognition by the endocytic sorting adaptor stonin 2. J Cell Biol 179:1497–1510

    Google Scholar 

  • Keyel PA, Mishra SK, Roth, R, Heuser JE, Watkins SC, Traub LM (2006) A single common portal for clathrin-mediated endocytosis of distinct cargo governed by cargo-selective adaptors. Mol Biol Cell 17:4300–4317

    Google Scholar 

  • Kirkham M, Fujita A, Chadda R et al (2005) Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J Cell Biol 168:465–476

    Google Scholar 

  • Kooijman EE, Chupin V, Fuller NL, Kozlov MM, de Kruijff B, Burger KN, Rand PR (2005) Spontaneous curvature of phosphatidic acid and lysophosphatidic acid. Biochemistry 44:2097–2102

    Google Scholar 

  • Krendel M, Osterweil EK, Mooseker MS (2007) Myosin 1E interacts with synaptojanin-1 and dynamin and is involved in endocytosis. FEBS Lett 581:644–650

    Google Scholar 

  • Krauss M, Haucke V (2007) Phosphoinositide-metabolizing enzymes at the interface between membrane traffic and cell signalling. EMBO Rep 8:241–246

    Google Scholar 

  • Krauss M, Kinuta M, Wenk MR, De Camilli P, Takei K, Haucke V (2003) ARF6 stimulates clathrin/AP-2 recruitment to synaptic membranes by activating phosphatidylinositol phosphate kinase type Igamma. J Cell Biol 162:113–124

    Google Scholar 

  • Krauss M, Kukhtina V, Pechstein A, Haucke V (2006) Stimulation of phosphatidylinositol kinase type I-mediated phosphatidylinositol (4,5)-bisphosphate synthesis by AP-2mu-cargo complexes. Proc Natl Acad Sci USA 103:11934–11939

    Google Scholar 

  • Krauss M, Jia JY, Roux A, Beck R, Wieland FT, De Camili P, Haucke V (2008) Arf1-GTP-induced tubule formation suggests a function of Arf family proteins in curvature acquisition at sites of vesicle budding. J Biol Chem 283:27717–27723

    Google Scholar 

  • Kumari S, Mayor S (2008) ARF1 is directly involved in dynamin-independent endocytosis. Nat Cell Biol 10:30–41

    Google Scholar 

  • Lakadamyali M, Rust MJ, Zhuang X (2006) Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 124:997–1009

    Google Scholar 

  • Lamaze C, Dujeancourt A, Baba T, Lo CG, Benmerah A, Dautry-Varsat A (2001) Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol Cell 7:661–671

    Google Scholar 

  • Le PU, Guay G, Altschuler Y, Nabi IR (2002) Caveolin-1 is a negative regulator of caveolae-mediated endocytosis to the endoplasmic reticulum. J Biol Chem 277:3371–3379

    Google Scholar 

  • Lecuit M, Hurme R, Pizarro-Cerda J, Ohayon H, Geiger B, Cossart P (2000) A role for alpha-and beta-catenins in bacterial uptake. Proc Natl Acad Sci USA 97, 10008–10013

    Google Scholar 

  • Lencer WI, Hirst TR, Holmes RK (1999) Membrane traffic and the cellular uptake of cholera toxin. Biochim Biophys Acta 1450:177–190

    Google Scholar 

  • Lundmark R, Carlsson SR (2002) The beta-appendages of the four adaptor-protein (AP) complexes: structure and binding properties, and identification of sorting nexin 9 as an accessory protein to AP-2. Biochem J 362:597–607

    Google Scholar 

  • Lundmark R, Carlsson SR (2003) Sorting nexin 9 participates in clathrin-mediated endocytosis through interactions with the core components. J Biol Chem 278:46772–46781

    Google Scholar 

  • Lundmark R, Carlsson SR (2004) Regulated membrane recruitment of dynamin-2 mediated by sorting nexin 9. J Biol Chem 279:42694–42702

    Google Scholar 

  • Masuda M, Takeda S, Sone M, Ohki T, Mori H, Kamioka Y, Mochizuki N (2006) Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms. EMBO J 25:2889–2897

    Google Scholar 

  • May RC, Machesky LM (2001) Phagocytosis and the actin cytoskeleton. J Cell Sci 114:1061–1077

    Google Scholar 

  • Mayor S, Pagano RE (2007) Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 8:603–612

    Google Scholar 

  • McMahon HT, Gallop JL (2005) Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438:590–596

    Google Scholar 

  • Monier S, Parton RG, Vogel F, Behlke J, Henske A, Kurzchalia TV (1995) VIP21-caveolin, a membrane protein constituent of the caveolar coat, oligomerizes in vivo and in vitro. Mol Biol Cell 6:911–927

    Google Scholar 

  • Musacchio A, Smith CJ, Roseman AM, Harrison SC, Kirchhausen T, Pearse BM (1999) Functional organization of clathrin in coats: combining electron cryomicroscopy and X-ray crystallography. Mol Cell 3:761–770

    Google Scholar 

  • Myers KR, Casanova JE (2008) Regulation of actin cytoskeleton dynamics by Arf-family GTPases. Trends Cell Biol 18:184–192

    Google Scholar 

  • Nakano-Kobayashi A, Yamazaki M, Unoki T et al (2007) Role of activation of PIP5Kgamma661 by AP-2 complex in synaptic vesicle endocytosis. EMBO J 26:1105–1116

    Google Scholar 

  • Naslavsky N, Weigert R, Donaldson JG (2004) Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol Biol Cell 15:3542–3552

    Google Scholar 

  • Niedergang F, Chavrier P (2004) Signaling and membrane dynamics during phagocytosis: many roads lead to the phagos(R)ome. Curr Opin Cell Biol 16:422–428

    Google Scholar 

  • Orth JD, McNiven MA (2003) Dynamin at the actin-membrane interface. Curr Opin Cell Biol 15:31–39

    Google Scholar 

  • Orth JD, Krueger EW, Cao H, McNiven MA (2002) The large GTPase dynamin regulates actin comet formation and movement in living cells. Proc Natl Acad Sci USA 99:167–172

    Google Scholar 

  • Palade GE, Bruns RR (1968) Structural modulations of plasmalemmal vesicles. J Cell Biol 37:633–649

    Google Scholar 

  • Pasqualato S, Menetrey J, Franco M, Cherfils J (2001) The structural GDP/GTP cycle of human Arf6. EMBO Rep 2:234–238

    Google Scholar 

  • Pelkmans L, Helenius A (2002) Endocytosis via caveolae. Traffic 3:311–320

    Google Scholar 

  • Pelkmans L, Zerial M (2005) Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae. Nature 436:128–133

    Google Scholar 

  • Pelkmans L, Kartenbeck J, Helenius A (2001) Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 3:473–483

    Google Scholar 

  • Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, Evans PR, McMahon HT (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303:495–499

    Google Scholar 

  • Pomorski T, Lombardi R, Riezman H, Devaux PF, van Meer G, Holthuis JC (2003) Drs2p-related P-type ATPases Dnf1p and Dnf2p are required for phospholipid translocation across the yeast plasma membrane and serve a role in endocytosis. Mol Biol Cell 14:1240–1254

    Google Scholar 

  • Powner DJ, Wakelam MJ (2002) The regulation of phospholipase D by inositol phospholipids and small GTPases. FEBS Lett 531:62–64

    Google Scholar 

  • Presley JF, Ward TH, Pfeifer AC, Siggia ED, Phair RD, Lippincott-Schwartz J (2002) Dissection of COPI and Arf1 dynamics in vivo and role in Golgi membrane transport. Nature 417:187–193

    Google Scholar 

  • Puthenveedu MA, von Zastrow M (2006) Cargo regulates clathrin-coated pit dynamics. Cell 127:113–124

    Google Scholar 

  • Pylypenko O, Lundmark R, Rasmuson E, Carlsson SR, Rak A (2007) The PX-BAR membrane-remodeling unit of sorting nexin 9. EMBO J 26:4788–4800

    Google Scholar 

  • Radhakrishna H, Klausner RD, Donaldson JG (1996) Aluminum fluoride stimulates surface protrusions in cells overexpressing the ARF6 GTPase. J Cell Biol 134:935–947

    Google Scholar 

  • Razani B, Woodman SE, Lisanti MP (2002) Caveolae: from cell biology to animal physiology. Pharmacol Rev 54:431–467

    Google Scholar 

  • Ringstad N, Gad H, Low P, Di Paolo G, Brodin L, Shupliakov O, De Camilli P (1999) Endophilin/SH3p4 is required for the transition from early to late stages in clathrin-mediated synaptic vesicle endocytosis. Neuron 24:143–154

    Google Scholar 

  • Romer W, Berland L, Chambon V et al (2007) Shiga toxin induces tubular membrane invaginations for its uptake into cells. Nature 450:670–675

    Google Scholar 

  • Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG (1992) Caveolin, a protein component of caveolae membrane coats. Cell 68:673–682

    Google Scholar 

  • Roux A, Uyhazi K, Frost A, De Camilli P (2006) GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission. Nature 441:528–531

    Google Scholar 

  • Sabharanjak S, Sharma P, Parton RG, Mayor S (2002) GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell 2:411–423

    Google Scholar 

  • Santarius M, Lee CH, Anderson RA (2006) Supervised membrane swimming: small G-protein lifeguards regulate PIPK signalling and monitor intracellular PtdIns(4,5)P2 pools. Biochem J 398:1–13

    Google Scholar 

  • Schafer DA, D’Souza-Schorey C, Cooper JA (2000) Actin assembly at membranes controlled by ARF6. Traffic 1:892–903

    Google Scholar 

  • Schuske KR, Richmond JE, Matthies DS, Davis WS, Runz S, Rube DA, van der Bliek AM, Jorgensen EM (2003) Endophilin is required for synaptic vesicle endocytosis by localizing synaptojanin. Neuron 40:749–762

    Google Scholar 

  • Shimada A, Niwa H, Tsujita K et al (2007) Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129:761–772

    Google Scholar 

  • Shin N, Ahn N, Chang-Ileto B et al (2008) SNX9 regulates tubular invagination of the plasma membrane through interaction with actin cytoskeleton and dynamin 2. J Cell Sci 121:1252–1263

    Google Scholar 

  • Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569–572

    Google Scholar 

  • Slepnev VI, Ochoa GC, Butler MH, De Camilli P (2000) Tandem arrangement of the clathrin and AP-2 binding domains in amphiphysin 1 and disruption of clathrin coat function by amphiphysin fragments comprising these sites. J Biol Chem 275:17583–17589

    Google Scholar 

  • Soldati T, Schliwa M (2006) Powering membrane traffic in endocytosis and recycling. Nat Rev Mol Cell Biol 7:897–908

    Google Scholar 

  • Spudich G, Chibalina MV, Au JS, Arden SD, Buss F, Kendrick-Jones J (2007) Myosin VI targeting to clathrin-coated structures and dimerization is mediated by binding to Disabled-2 and PtdIns(4,5)P2. Nat Cell Biol 9:176–183

    Google Scholar 

  • Takei K, Slepnev VI, Haucke V, De Camilli P (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol 1:33–39

    Google Scholar 

  • Thomsen P, Roepstorff K, Stahlhut M, van Deurs B (2002) Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. Mol Biol Cell 13:238–250

    Google Scholar 

  • Varnai P, Thyagarajan B, Rohacs T, Balla T (2006) Rapidly inducible changes in phosphatidylinositol 4,5-bisphosphate levels influence multiple regulatory functions of the lipid in intact living cells. J Cell Biol 175:377–382

    Google Scholar 

  • Veiga E, Cossart P (2005) Listeria hijacks the clathrin-dependent endocytic machinery to invade mammalian cells. Nat Cell Biol 7:894–900

    Google Scholar 

  • Verstreken P, Koh TW, Schulze KL et al (2003) Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron 40:733–748

    Google Scholar 

  • Vicente-Manzanares M, Sanchez-Madrid F (2004) Role of the cytoskeleton during leukocyte responses. Nat Rev Immunol 4:110–122

    Google Scholar 

  • Walseng E, Bakke O, Roche PA (2008) Major histocompatibility complex class II-peptide complexes internalize using a clathrin- and dynamin-independent endocytosis pathway. J Biol Chem 283:14717–14727

    Google Scholar 

  • Wolfe BL, Trejo J (2007) Clathrin-dependent mechanisms of G protein-coupled receptor endocytosis. Traffic 8:462–470

    Google Scholar 

  • Yarar D, Waterman-Storer CM, Schmid SL (2005) A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol Biol Cell 16:964–975

    Google Scholar 

  • Zoncu R, Perera RM, Sebastian R et al (2007) Loss of endocytic clathrin-coated pits upon acute depletion of phosphatidylinositol 4,5-bisphosphate. Proc Natl Acad Sci USA 104:3793–3798

    Google Scholar 

Download references

Acknowledgements

Acknowledgements: The authors acknowledge support from the Deutsche Forschungsgemein schaft (DFG) (HA2686/3-1/FOR806; HA2686/4-1/SFB740).

Author information

Authors and Affiliations

  1. Institute of Chemistry and Biochemistry, Department of Membrane Biochemistry, Freie Universität Berlin, Takustraße 6, 14195, Berlin, Germany

    M. Krauss

Authors
  1. M. Krauss
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. Haucke
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Krauss .

Editor information

Editors and Affiliations

  1. School of Medicine, Deptartment of Neurobiology, University of Pittsburgh, Fifth Avenue 3501, Pittsburgh, 15261, Pennsylvania, USA

    Susan G. Amara

  2. MPI für Biophysik, Max-von-Laue-Straße 3, Frankfurt, 60438, Germany

    Ernst Bamberg

  3. Institut für Physiologie I, Universität Bonn, Sigmund-Freud-Str. 25, Bonn, 53105, Germany

    Bernd K. Fleischmann

  4. Medizinische Fakultät, Walther-Straub-Institut für Pharmakologi, Ludwig-Maximilians-Universität München, Goethestr. 33, München, 80336, Germany

    Thomas Gudermann

  5. Abt. Neurobiologie, MPI für Biophysikalische Chemie, Am Faßberg 11, Göttingen, 37077, Germany

    Reinhard Jahn

  6. Center for Biomedical Engineering and Te, University of Maryland Baltimore, West Lombard Street 725, Baltimore, 21201, Maryland, USA

    William J. Lederer

  7. Inst. Zytobiologie und, Zytopathologie, Universität Marburg, Robert-Koch-Str. 5, Marburg, 35033, Germany

    Roland Lill

  8. Lab. Fysiologie, Katholieke Universiteit Leuven, Herestraat 49, Leuven, 3000, Belgium

    Bernd Nilius

  9. , Abteilung II, Max-Planck-Institut für Herz- und Lungen, Ludwigstr. 43, Bad Nauheim, 61231, Germany

    Stefan Offermanns

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Krauss, M., Haucke, V. (2009). Shaping Membranes for Endocytosis. In: Amara, S., et al. Reviews of Physiology, Biochemistry and Pharmacology 161. Reviews of Physiology, Biochemistry and Pharmacology, vol 161. Springer, Berlin, Heidelberg. https://doi.org/10.1007/112_2008_2

Download citation

Publish with us

Policies and ethics

Search

Navigation