CALM Regulates Clathrin-Coated Vesicle Size and Maturation by Directly Sensing and Driving Membrane Curvature

Developmental Cell

Volumn 33, Issue 2, 2015, Pages 163-175

  Miller, Sharon E ^a   Mathiasen, Signe ^b   Bright, Nicholas A ^a   Pierre, Fabienne ^c   Kelly, Bernard T ^a   Kladt, Nikolay ^d   Schauss, Astrid ^d   Merrifield, Christien J ^c   Stamou, Dimitrios ^b   Höning, Stefan ^e   Owen, David J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^d UNIVERSITY OF COLOGNE   (Germany)

^e UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AP2 PROTEIN; CLATHRIN ASSEMBLY LYMPHOID MYELOID LEUKEMIA PROTEIN; EPIDERMAL GROWTH FACTOR; PROTEIN; TRANSFERRIN; UNCLASSIFIED DRUG; CLATHRIN ASSEMBLY PROTEIN; FABP4 PROTEIN, HUMAN; FATTY ACID BINDING PROTEIN; LIPOSOME; PICALM PROTEIN, HUMAN; SMALL INTERFERING RNA; SYNAPTOBREVIN; VAMP8 PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL MATURATION; CELL MEMBRANE; CELL SIZE; COATED VESICLE; CONTROLLED STUDY; ENDOCYTOSIS; IN VITRO STUDY; INTERNALIZATION; MEMBRANE STRUCTURE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; WILD TYPE; CELL SHAPE; CLATHRIN-COATED VESICLE; COATED PIT; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; RNA INTERFERENCE; TUMOR CELL LINE;

MAMMALIA;

CELL LINE, TUMOR; CELL MEMBRANE; CELL SHAPE; CLATHRIN-COATED VESICLES; COATED PITS, CELL-MEMBRANE; ENDOCYTOSIS; EPIDERMAL GROWTH FACTOR; FATTY ACID-BINDING PROTEINS; HELA CELLS; HUMANS; LIPOSOMES; MONOMERIC CLATHRIN ASSEMBLY PROTEINS; PROTEIN STRUCTURE, TERTIARY; R-SNARE PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSFERRIN;

EID: 84928015584     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.03.002     Document Type: Article

References (68)

1. Aguet F., Antonescu C.N., Mettlen M., Schmid S.L., Danuser G. Advances in analysis of low signal-to-noise images link dynamin and AP2 to the functions of an endocytic checkpoint. Dev. Cell 2013, 26:279-291.
2. Antonny B. Mechanisms of membrane curvature sensing. Annu. Rev. Biochem. 2011, 80:101-123.
3. Bao H., Daniels R.W., MacLeod G.T., Charlton M.P., Atwood H.L., Zhang B. AP180 maintains the distribution of synaptic and vesicle proteins in the nerve terminal and indirectly regulates the efficacy of Ca2+-triggered exocytosis. J.Neurophysiol. 2005, 94:1888-1903.
4. Baumgart T., Capraro B.R., Zhu C., Das S.L. Thermodynamics and mechanics of membrane curvature generation and sensing by proteins and lipids. Annu. Rev. Phys. Chem. 2011, 62:483-506.
5. Beck R., Sun Z., Adolf F., Rutz C., Bassler J., Wild K., Sinning I., Hurt E., Brügger B., Béthune J., Wieland F. Membrane curvature induced by Arf1-GTP is essential for vesicle formation. Proc. Natl. Acad. Sci. USA 2008, 105:11731-11736.
6. Bhatia V.K., Madsen K.L., Bolinger P.Y., Kunding A., Hedegård P., Gether U., Stamou D. Amphipathic motifs in BAR domains are essential for membrane curvature sensing. EMBO J. 2009, 28:3303-3314.
7. Bigay J., Gounon P., Robineau S., Antonny B. Lipid packing sensed by ArfGAP1 couples COPI coat disassembly to membrane bilayer curvature. Nature 2003, 426:563-566.
8. Blondeau F., Ritter B., Allaire P.D., Wasiak S., Girard M., Hussain N.K., Angers A., Legendre-Guillemin V., Roy L., Boismenu D., et al. Tandem MS analysis of brain clathrin-coated vesicles reveals their critical involvement in synaptic vesicle recycling. Proc. Natl. Acad. Sci. USA 2004, 101:3833-3838.
9. Borner G.H.H., Antrobus R., Hirst J., Bhumbra G.S., Kozik P., Jackson L.P., Sahlender D.A., Robinson M.S. Multivariate proteomic profiling identifies novel accessory proteins of coated vesicles. J.Cell Biol. 2012, 197:141-160.
10. Boucrot E., Pick A., Çamdere G., Liska N., Evergren E., McMahon H.T., Kozlov M.M. Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell 2012, 149:124-136.
11. Cocucci E., Aguet F., Boulant S., Kirchhausen T. The first five seconds in the life of a clathrin-coated pit. Cell 2012, 150:495-507.
12. Copic A., Latham C.F., Horlbeck M.A., D'Arcangelo J.G., Miller E.A. ER cargo properties specify a requirement for COPII coat rigidity mediated by Sec13p. Science 2012, 335:1359-1362.
13. Dannhauser P.N., Ungewickell E.J. Reconstitution of clathrin-coated bud and vesicle formation with minimal components. Nat. Cell Biol. 2012, 14:634-639.
14. Drin G., Casella J.F., Gautier R., Boehmer T., Schwartz T.U., Antonny B. A general amphipathic α-helical motif for sensing membrane curvature. Nat. Struct. Mol. Biol. 2007, 14:138-146.
15. 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.
16. Ford M.G.J., Mills I.G., Peter B.J., Vallis Y., Praefcke G.J.K., Evans P.R., McMahon H.T. Curvature of clathrin-coated pits driven by epsin. Nature 2002, 419:361-366.
17. Gage R.M., Matveeva E.A., Whiteheart S.W., von Zastrow M. Type I PDZ ligands are sufficient to promote rapid recycling of G protein-coupled receptors independent of binding to N-ethylmaleimide-sensitive factor. J.Biol. Chem. 2005, 280:3305-3313.
18. Gallop J.L., Jao C.C., Kent H.M., Butler P.J., Evans P.R., Langen R., McMahon H.T. Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J. 2006, 25:2898-2910.
19. Harold D., Abraham R., Hollingworth P., Sims R., Gerrish A., Hamshere M.L., Pahwa J.S., Moskvina V., Dowzell K., Williams A., et al. Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease. Nat. Genet. 2009, 41:1088-1093.
20. Hatzakis N.S., Bhatia V.K., Larsen J., Madsen K.L., Bolinger P.Y., Kunding A.H., Castillo J., Gether U., Hedegård P., Stamou D. How curved membranes recruit amphipathic helices and protein anchoring motifs. Nat. Chem. Biol. 2009, 5:835-841.
21. Heuser J. Three-dimensional visualization of coated vesicle formation in fibroblasts. J.Cell Biol. 1980, 84:560-583.
22. Hollopeter G., Lange J.J., Zhang Y., Vu T.N., Gu M., Ailion M., Lambie E.J., Slaughter B.D., Unruh J.R., Florens L., Jorgensen E.M. The membrane-associated proteins FCHo and SGIP are allosteric activators of the AP2 clathrin adaptor complex. eLife 2014, 3:3.
23. Honing S., Ricotta D., Krauss M., Spate K., Spolaore B., Motley A., Robinson M., Robinson C., Haucke V., Owen D.J. Phosphatidylinositol-(4,5)-bisphosphate regulates sorting signal recognition by the clathrin-associated adaptor complex AP2 (vol 19, pg 577, 2005). Mol. Cell 2005, 19. 577-577.
24. Hopkins C.R., Miller K., Beardmore J.M. Receptor-mediated endocytosis of transferrin and epidermal growth factor receptors: a comparison of constitutive and ligand-induced uptake. J.Cell Sci. Suppl. 1985, 3:173-186.
25. Huang F., Khvorova A., Marshall W., Sorkin A. Analysis of clathrin-mediated endocytosis of epidermal growth factor receptor by RNA interference. J.Biol. Chem. 2004, 279:16657-16661.
26. Ishikawa Y., Maeda M., Pasham M., Aguet F., Tacheva-Grigorova S.K., Masuda T., Yi H., Lee S.U., Xu J., Teruya-Feldstein J., et al. Role of the clathrin adaptor PICALM in normal hematopoiesis and polycythemia vera pathophysiology. Haematologica 2014.
27. Itoh T., Erdmann K.S., Roux A., Habermann B., Werner H., De Camilli P. Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev. Cell 2005, 9:791-804.
28. Jensen M.B., Bhatia V.K., Jao C.C., Rasmussen J.E., Pedersen S.L., Jensen K.J., Langen R., Stamou D. Membrane curvature sensing by amphipathic helices: a single liposome study using α-synuclein and annexin B12. J.Biol. Chem. 2011, 286:42603-42614.
29. Jiang X., Huang F., Marusyk A., Sorkin A. Grb2 regulates internalization of EGF receptors through clathrin-coated pits. Mol. Biol. Cell 2003, 14:858-870.
30. Kelly B.T., Graham S.C., Liska N., Dannhauser P.N., Höning S., Ungewickell E.J., Owen D.J. Clathrin adaptors. AP2 controls clathrin polymerization with a membrane-activated switch. Science 2014, 345:459-463.
31. Klebig M.L., Wall M.D., Potter M.D., Rowe E.L., Carpenter D.A., Rinchik E.M. Mutations in the clathrin-assembly gene Picalm are responsible for the hematopoietic and iron metabolism abnormalities in fit1 mice. Proc. Natl. Acad. Sci. USA 2003, 100:8360-8365.
32. Koo S.J., Markovic S., Puchkov D., Mahrenholz C.C., Beceren-Braun F., Maritzen T., Dernedde J., Volkmer R., Oschkinat H., Haucke V. SNARE motif-mediated sorting of synaptobrevin by the endocytic adaptors clathrin assembly lymphoid myeloid leukemia (CALM) and AP180 at synapses. Proc. Natl. Acad. Sci. USA 2011, 108:13540-13545.
33. Kozlov M.M., Campelo F., Liska N., Chernomordik L.V., Marrink S.J., McMahon H.T. Mechanisms shaping cell membranes. Curr. Opin. Cell Biol. 2014, 29:53-60.
34. Krauss M., Jia J.Y., Roux A., Beck R., Wieland F.T., De Camilli P., Haucke V. Arf1-GTP-induced tubule formation suggests a function of Arf family proteins in curvature acquisition at sites of vesicle budding. J.Biol. Chem. 2008, 283:27717-27723.
35. Kunding A.H., Mortensen M.W., Christensen S.M., Stamou D. A fluorescence-based technique to construct size distributions from single-object measurements: application to the extrusion of lipid vesicles. Biophys. J. 2008, 95:1176-1188.
36. Lee M.C., Orci L., Hamamoto S., Futai E., Ravazzola M., Schekman R. Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell 2005, 122:605-617.
37. Loerke D., Mettlen M., Yarar D., Jaqaman K., Jaqaman H., Danuser G., Schmid S.L. Cargo and dynamin regulate clathrin-coated pit maturation. PLoS Biol. 2009, 7:e57.
38. Lohr C., Kunding A.H., Bhatia V.K., Stamou D. Constructing size distributions of liposomes from single-object fluorescence measurements. Methods Enzymol. 2009, 465:143-160.
39. Mao Y., Chen J., Maynard J.A., Zhang B., Quiocho F.A. A novel all helix fold of the AP180 amino-terminal domain for phosphoinositide binding and clathrin assembly in synaptic vesicle endocytosis. Cell 2001, 104:433-440.
40. Mengel-From J., Christensen K., McGue M., Christiansen L. Genetic variations in the CLU and PICALM genes are associated with cognitive function in the oldest old. Neurobiol. Aging 2011, 32. 554.e557-11.
41. Meyerholz A., Hinrichsen L., Groos S., Esk P.C., Brandes G., Ungewickell E.J. Effect of clathrin assembly lymphoid myeloid leukemia protein depletion on clathrin coat formation. Traffic 2005, 6:1225-1234.
42. Miller S.E., Sahlender D.A., Graham S.C., Höning S., Robinson M.S., Peden A.A., Owen D.J. The molecular basis for the endocytosis of small R-SNAREs by the clathrin adaptor CALM. Cell 2011, 147:1118-1131.
43. Montagnac G., de Forges H., Smythe E., Gueudry C., Romao M., Salamero J., Chavrier P. Decoupling of activation and effector binding underlies ARF6 priming of fast endocytic recycling. Curr. Biol. 2011, 21:574-579.
44. Motley A., Bright N.A., Seaman M.N., Robinson M.S. Clathrin-mediated endocytosis in AP-2-depleted cells. J.Cell Biol. 2003, 162:909-918.
45. Motley A.M., Berg N., Taylor M.J., Sahlender D.A., Hirst J., Owen D.J., Robinson M.S. Functional analysis of AP-2 alpha and mu2 subunits. Mol. Biol. Cell 2006, 17:5298-5308.
46. Nonet M.L., Holgado A.M., Brewer F., Serpe C.J., Norbeck B.A., Holleran J., Wei L., Hartwieg E., Jorgensen E.M., Alfonso A. UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles. Mol. Biol. Cell 1999, 10:2343-2360.
47. Peter B.J., Kent H.M., Mills I.G., Vallis Y., Butler P.J., Evans P.R., McMahon H.T. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 2004, 303:495-499.
48. Petralia R.S., Wang Y.X., Indig F.E., Bushlin I., Wu F., Mattson M.P., Yao P.J. Reduction of AP180 and CALM produces defects in synaptic vesicle size and density. Neuromolecular Med. 2013, 15:49-60.
49. Pinot M., Vanni S., Pagnotta S., Lacas-Gervais S., Payet L.A., Ferreira T., Gautier R., Goud B., Antonny B., Barelli H. Lipid cell biology. Polyunsaturated phospholipids facilitate membrane deformation and fission by endocytic proteins. Science 2014, 345:693-697.
50. Rappoport J.Z., Taha B.W., Lemeer S., Benmerah A., Simon S.M. The AP-2 complex is excluded from the dynamic population of plasma membrane-associated clathrin. J.Biol. Chem. 2003, 278:47357-47360.
51. Reynolds E.S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J.Cell Biol. 1963, 17:208-212.
52. Ritter B., Murphy S., Dokainish H., Girard M., Gudheti M.V., Kozlov G., Halin M., Philie J., Jorgensen E.M., Gehring K., McPherson P.S. NECAP 1 regulates AP-2 interactions to control vesicle size, number, and cargo during clathrin-mediated endocytosis. PLoS Biol. 2013, 11:e1001670.
53. Saffarian S., Kirchhausen T. Differential evanescence nanometry: live-cell fluorescence measurements with 10-nm axial resolution on the plasma membrane. Biophys. J. 2008, 94:2333-2342.
54. Scheve C.S., Gonzales P.A., Momin N., Stachowiak J.C. Steric pressure between membrane-bound proteins opposes lipid phase separation. J.Am. Chem. Soc. 2013, 135:1185-1188.
55. Scotland P.B., Heath J.L., Conway A.E., Porter N.B., Armstrong M.B., Walker J.A., Klebig M.L., Lavau C.P., Wechsler D.S. The PICALM protein plays a key role in iron homeostasis and cell proliferation. PLoS ONE 2012, 7:e44252.
56. Settles E.I., Loftus A.F., McKeown A.N., Parthasarathy R. The vesicle trafficking protein Sar1 lowers lipid membrane rigidity. Biophys. J. 2010, 99:1539-1545.
57. Slot J.W., Geuze H.J. Cryosectioning and immunolabeling. Nat. Protoc. 2007, 2:2480-2491.
58. Stachowiak J.C., Schmid E.M., Ryan C.J., Ann H.S., Sasaki D.Y., Sherman M.B., Geissler P.L., Fletcher D.A., Hayden C.C. Membrane bending by protein-protein crowding. Nat. Cell Biol. 2012, 14:944-949.
59. Stahelin R.V., Long F., Peter B.J., Murray D., De Camilli P., McMahon H.T., Cho W. Contrasting membrane interaction mechanisms of AP180 N-terminal homology (ANTH) and epsin N-terminal homology (ENTH) domains. J.Biol. Chem. 2003, 278:28993-28999.
60. Suzuki M., Tanaka H., Tanimura A., Tanabe K., Oe N., Rai S., Kon S., Fukumoto M., Takei K., Abe T., et al. The clathrin assembly protein PICALM is required for erythroid maturation and transferrin internalization in mice. PLoS ONE 2012, 7:e31854.
61. Taylor M.J., Perrais D., Merrifield C.J. A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol. 2011, 9:e1000604.
62. Taylor M.J., Lampe M., Merrifield C.J. A feedback loop between dynamin and actin recruitment during clathrin-mediated endocytosis. PLoS Biol. 2012, 10:e1001302.
63. Tebar F., Bohlander S.K., Sorkin A. Clathrin assembly lymphoid myeloid leukemia (CALM) protein: localization in endocytic-coated pits, interactions with clathrin, and the impact of overexpression on clathrin-mediated traffic. Mol. Biol. Cell 1999, 10:2687-2702.
64. Traub L.M. Regarding the amazing choreography of clathrin coats. PLoS Biol. 2011, 9:e1001037.
65. Umasankar P.K., Sanker S., Thieman J.R., Chakraborty S., Wendland B., Tsang M., Traub L.M. Distinct and separable activities of the endocytic clathrin-coat components Fcho1/2 and AP-2 in developmental patterning. Nat. Cell Biol. 2012, 14:488-501.
66. Umasankar P.K., Ma L., Thieman J.R., Jha A., Doray B., Watkins S.C., Traub L.M. A clathrin coat assembly role for the muniscin protein central linker revealed by TALEN-mediated gene editing. eLife 2014, 3:3.
67. van Weering J.R., Verkade P., Cullen P.J. SNX-BAR-mediated endosome tubulation is co-ordinated with endosome maturation. Traffic 2012, 13:94-107.
68. Zhang B., Koh Y.H., Beckstead R.B., Budnik V., Ganetzky B., Bellen H.J. Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron 1998, 21:1465-1475.