Life of a clathrin coat: insights from clathrin and AP structures (original) (raw)
Ehrlich, M. et al. Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell118, 591–605 (2004). ArticleCASPubMed Google Scholar
Merrifield, C. J., Perrais, D. & Zenisek, D. Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell121, 593–606 (2005). ArticleCASPubMed Google Scholar
Owen, D. J., Collins, B. M. & Evans, P. R. Adaptors for clathrin coats: structure and function. Annu. Rev. Cell Dev. Biol.20, 153–191 (2004). ArticleCASPubMed Google Scholar
Bonifacino, J. S. & Traub, L. M. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem.72, 395–447 (2003). ArticleCASPubMed Google Scholar
Traub, L. M. Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection. J. Cell Biol.163, 203–208 (2003). Introduces the concept of and provides a mechanistic explanation for the function of CLASPs. ArticleCASPubMedPubMed Central Google Scholar
Kanaseki, T. & Kadota, K. The 'vesicle in a basket': a morphological study of the coated vesicle isolated from the nerve endings of the guinea pig brain, with special reference to the mechanism of membrane movements. J. Cell Biol.42, 202–220 (1969). ArticleCASPubMedPubMed Central Google Scholar
Vigers, G. P., Crowther, R. A. & Pearse, B. M. Location of the 100 kd–50 kd accessory proteins in clathrin coats. EMBO J.5, 2079–2085 (1986). ArticleCASPubMedPubMed Central Google Scholar
Vigers, G. P., Crowther, R. A. & Pearse, B. M. Three-dimensional structure of clathrin cages in ice. EMBO J.5, 529–534 (1986). Presents the first 3D reconstruction of a clathrin barrel, on which all subsequent work has been based. ArticleCASPubMedPubMed Central Google Scholar
Heuser, J. E. & Keen, J. Deep-etch visualization of proteins involved in clathrin assembly. J. Cell Biol.107, 877–886 (1988). ArticleCASPubMed Google Scholar
Kirchhausen, T. Adaptors for clathrin-mediated traffic. Annu. Rev. Cell Dev. Biol.15, 705–732 (1999). ArticleCASPubMed Google Scholar
Brodsky, F. M., Chen, C. Y., Knuehl, C., Towler, M. C. & Wakeham, D. E. Biological basket weaving: formation and function of clathrin-coated vesicles. Annu. Rev. Cell Dev. Biol.17, 517–568 (2001). ArticleCASPubMed Google Scholar
Ybe, J. A. et al. Clathrin self-assembly is mediated by a tandemly repeated superhelix. Nature399, 371–375 (1999). ArticleCASPubMed Google Scholar
ter Haar, E., Harrison, S. C. & Kirchhausen, T. Peptide-in-groove interactions link target proteins to the β-propeller of clathrin. Proc. Natl Acad. Sci. USA97, 1096–1100 (2000). Describes the molecular details of peptide binding to clathrin using a clathrin-box motif. ArticleCASPubMedPubMed Central Google Scholar
Miele, A. E., Watson, P. J., Evans, P. R., Traub, L. M. & Owen, D. J. Two distinct interaction motifs in amphiphysin bind two independent sites on the clathrin terminal domain β-propeller. Nature Struct. Mol. Biol.11, 242–248 (2004). ArticleCAS Google Scholar
Smith, C. J., Grigorieff, N. & Pearse, B. M. Clathrin coats at 21 Å resolution: a cellular assembly designed to recycle multiple membrane receptors. EMBO J.17, 4943–4953 (1998). ArticleCASPubMedPubMed Central Google Scholar
Fotin, A. et al. Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature432, 573–579 (2004). ArticleCASPubMed Google Scholar
Fotin, A. et al. Structure of an auxilin-bound clathrin coat and its implications for the mechanism of uncoating. Nature432, 649–653 (2004). References 17 and 18 describe the molecular details of a clathrin coat at 8-Å resolution and provide a molecular explanation for auxilin/HSC70-catalysed clathrin-coat disassembly. ArticleCASPubMed Google Scholar
Heymann, J. B. et al. Visualization of the binding of Hsc70 ATPase to clathrin baskets: implications for an uncoating mechanism. J. Biol. Chem.280, 7156–7161 (2005). ArticleCASPubMed Google Scholar
Crowther, R. A., Finch, J. T. & Pearse, B. M. On the structure of coated vesicles. J. Mol. Biol.103, 785–798 (1976). ArticleCASPubMed Google Scholar
Crowther, R. A. & Pearse, B. M. Assembly and packing of clathrin into coats. J. Cell Biol.91, 790–797 (1981). ArticleCASPubMed Google Scholar
Musacchio, A. et al. Functional organization of clathrin in coats: combining electron cryomicroscopy and X-ray crystallography. Mol. Cell3, 761–770 (1999). ArticleCASPubMed Google Scholar
Chen, C. Y. et al. Clathrin light and heavy chain interface: α-helix binding superhelix loops via critical tryptophans. EMBO J.21, 6072–6082 (2002). ArticleCASPubMedPubMed Central Google Scholar
Chen, C. Y. & Brodsky, F. M. Huntingtin-interacting protein 1 (Hip1) and Hip1-related protein (Hip1R) bind the conserved sequence of clathrin light chains and thereby influence clathrin assembly in vitro and actin distribution in vivo. J. Biol. Chem.280, 6109–6117 (2005). ArticleCASPubMed Google Scholar
Legendre-Guillemin, V. et al. Huntingtin interacting protein 1 (HIP1) regulates clathrin assembly through direct binding to the regulatory region of the clathrin light chain. J. Biol. Chem.280, 6101–6108 (2005). ArticleCASPubMed Google Scholar
Gruschus, J. M. et al. Structure of the functional fragment of auxilin required for catalytic uncoating of clathrin-coated vesicles. Biochemistry43, 3111–3119 (2004). ArticleCASPubMed Google Scholar
Scheele, U., Kalthoff, C. & Ungewickell, E. Multiple interactions of auxilin 1 with clathrin and the AP-2 adaptor complex. J. Biol. Chem.276, 36131–36138 (2001). ArticleCASPubMed Google Scholar
Scheele, U. et al. Molecular and functional characterization of clathrin- and AP-2-binding determinants within a disordered domain of auxilin. J. Biol. Chem.278, 25357–25368 (2003). ArticleCASPubMed Google Scholar
Takenaka, I. M., Leung, S. M., McAndrew, S. J., Brown, J. P. & Hightower, L. E. Hsc70-binding peptides selected from a phage display peptide library that resemble organellar targeting sequences. J. Biol. Chem.270, 19839–19844 (1995). ArticleCASPubMed Google Scholar
Heuser, J. & Steer, C. J. Trimeric binding of the 70-kD uncoating ATPase to the vertices of clathrin triskelia: a candidate intermediate in the vesicle uncoating reaction. J. Cell Biol.109, 1457–1466 (1989). ArticleCASPubMed Google Scholar
Smith, C. J. et al. Location of auxilin within a clathrin cage. J. Mol. Biol.336, 461–471 (2004). ArticleCASPubMed Google Scholar
Keen, J. H., Willingham, M. C. & Pastan, I. H. Clathrin coated vesicles: isolation, dissociation and factor dependent reassociation of clathrin baskets. Cell16, 303–312 (1979). ArticleCASPubMed Google Scholar
Zaremba, S. & Keen, J. H. Limited proteolytic digestion of coated vesicle assembly polypeptides abolishes reassembly activity. J. Cell. Biochem.28, 47–58 (1985). ArticleCASPubMed Google Scholar
Schroder, S. & Ungewickell, E. Subunit interaction and function of clathrin-coated vesicle adaptors from the Golgi and the plasma membrane. J. Biol. Chem.266, 7910–7918 (1991). ArticleCASPubMed Google Scholar
Peden, A. A. et al. Localization of the AP-3 adaptor complex defines a novel endosomal exit site for lysosomal membrane proteins. J. Cell Biol.164, 1065–1076 (2004). ArticleCASPubMedPubMed Central Google Scholar
Peden, A. A., Rudge, R. E., Lui, W. W. & Robinson, M. S. Assembly and function of AP-3 complexes in cells expressing mutant subunits. J. Cell Biol.156, 327–336 (2002). ArticleCASPubMedPubMed Central Google Scholar
Collins, B. M., McCoy, A. J., Kent, H. M., Evans, P. R. & Owen, D. J. Molecular architecture and functional model of the endocytic AP2 complex. Cell109, 523–535 (2002). ArticleCASPubMed Google Scholar
Heldwein, E. E. et al. Crystal structure of the clathrin adaptor protein 1 core. Proc. Natl Acad. Sci. USA101, 14108–14113 (2004). Describes the molecular architecture of AP1 and gives insights into the functional mechanisms of AP1. ArticleCASPubMedPubMed Central Google Scholar
Pauloin, A. & Thurieau, C. The 50 kDa protein subunit of assembly polypeptide (AP) AP-2 adaptor from clathrin-coated vesicles is phosphorylated on threonine-156 by AP-1 and a soluble AP50 kinase which copurifies with the assembly polypeptides. Biochem. J.296, 409–415 (1993). ArticleCASPubMedPubMed Central Google Scholar
Olusanya, O., Andrews, P. D., Swedlow, J. R. & Smythe, E. Phosphorylation of threonine 156 of the μ2 subunit of the AP2 complex is essential for endocytosis in vitro and in vivo. Curr. Biol.11, 896–900 (2001). ArticleCASPubMed Google Scholar
Conner, S. & Schmid, S. Identification of an adaptor-associated kinase, AAK1, as a regulator of clathrin-mediated endocytosis. J. Cell Biol.156, 921–929 (2002). ArticleCASPubMedPubMed Central Google Scholar
Conner, S. D., Schroter, T. & Schmid, S. L. AAK1-mediated μ2 phosphorylation is stimulated by assembled clathrin. Traffic4, 885–890 (2003). ArticleCASPubMed Google Scholar
Jackson, A. P. et al. Clathrin promotes incorporation of cargo into coated pits by activation of the AP2 adaptor μ2 kinase. J. Cell Biol.163, 231–236 (2003). ArticleCASPubMedPubMed Central Google Scholar
Ricotta, D., Conner, S. D., Schmid, S. L., von Figura, K. & Honing, S. Phosphorylation of the AP2 μ subunit by AAK1 mediates high affinity binding to membrane protein sorting signals. J. Cell Biol.156, 791–795 (2002). Establishes a role for μ2-subunit phosphorylation in AP2 function. ArticleCASPubMedPubMed Central Google Scholar
Fingerhut, A., von Figura, K. & Honing, S. Binding of AP2 to sorting signals is modulated by AP2 phosphorylation. J. Biol. Chem.276, 5476–5482 (2001). ArticleCASPubMed Google Scholar
Honing, S. et al. Phosphatidylinositol-(4,5)-bisphosphate regulates sorting signal recognition by the clathrin-associated adaptor complex AP2. Mol. Cell18, 519–531 (2005). ArticlePubMedCAS Google Scholar
Ghosh, P. & Kornfeld, S. AP-1 binding to sorting signals and release from clathrin-coated vesicles is regulated by phosphorylation. J. Cell Biol.160, 699–708 (2003). ArticleCASPubMedPubMed Central Google Scholar
Umeda, A., Meyerholz, A. & Ungewickell, E. Identification of the universal cofactor (auxilin 2) in clathrin coat dissociation. Eur. J. Cell Biol.79, 336–342 (2000). ArticleCASPubMed Google Scholar
Korolchuk, V. & Banting, G. CK2 and GAK/auxilin2 are major protein kinases in clathrin-coated vesicles. Traffic3, 428–439 (2002). ArticleCASPubMed Google Scholar
Simonsen, A., Wurmser, A. E., Emr, S. D. & Stenmark, H. The role of phosphoinositides in membrane transport. Curr. Opin. Cell Biol.13, 485–492 (2001). ArticleCASPubMed Google Scholar
Chung, J. K. et al. Synaptojanin inhibition of phospholipase D activity by hydrolysis of phosphatidylinositol 4,5-biphosphate. J. Biol. Chem.272, 15980–15985 (1997). ArticleCASPubMed Google Scholar
Padron, D., Wang, Y., Yamamoto, M., Yin, H. & Roth, M. Phosphatidylinositol phosphate 5-kinase Iβ recruits AP-2 to the plasma membrane and regulates rates of constitutive endocytosis. J. Cell Biol.162, 693–701 (2003). ArticleCASPubMedPubMed Central Google Scholar
Gaidarov, I., Chen, Q., Falck, J., Reddy, K. & Keen, J. A functional phosphatidylinositol 3,4,5-triphosphate/phosphoinositide binding domain in the clathrin adaptor AP-2 α subunit. J. Biol. Chem.271, 20922–20929 (1996). ArticleCASPubMed Google Scholar
Gaidarov, I. & Keen, J. H. Phosphoinositide–AP-2 interactions required for targeting to plasma membrane clathrin-coated pits. J. Cell Biol.146, 755–764 (1999). ArticleCASPubMedPubMed Central Google Scholar
Gaidarov, I., Smith, M. E., Domin, J. & Keen, J. The class II phosphoinositide 3-kinase C2α is activated by clathrin and regulated clathrin-mediated membrane trafficking. Mol. Cell7, 443–449 (2001). ArticleCASPubMed Google Scholar
Rohde, G., Wenzel, D. & Haucke, V. A phosphatidylinositol (4,5)-bisphosphate binding site within μ2-adaptin regulates clathrin mediated endocytosis. J. Cell Biol.158, 209–214 (2002). ArticleCASPubMedPubMed Central Google Scholar
Munro, S. Organelle identity and the targeting of peripheral membrane proteins. Curr. Opin. Cell Biol.14, 506–514 (2002). ArticleCASPubMed Google Scholar
Crottet, P., Meyer, D. M., Rohrer, J. & Spiess, M. ARF1•GTP, tyrosine-based signals, and phosphatidylinositol 4,5-bisphosphate constitute a minimal machinery to recruit the AP-1 clathrin adaptor to membranes. Mol. Biol. Cell13, 3672–3682 (2002). ArticleCASPubMedPubMed Central Google Scholar
Traub, L. M., Ostrom, J. A. & Kornfeld, S. Biochemical dissection of AP-1 recruitment onto Golgi membranes. J. Cell Biol.123, 561–573 (1993). ArticleCASPubMed Google Scholar
Wang, Y. J. et al. Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell114, 299–310 (2003). ArticleCASPubMed Google Scholar
Austin, C., Hinners, I. & Tooze, S. Direct and GTP-dependent interaction of ADP-ribosylation factor 1 with clathrin adaptor protein AP-1 on immature secretory granules. J. Biol. Chem.275, 21862–21869 (2000). ArticleCASPubMed Google Scholar
Boehm, M., Aguilar, R. C. & Bonifacino, J. S. Functional and physical interactions of the adaptor protein complex AP-4 with ADP-ribosylation factors (ARFs). EMBO J.20, 6265–6276 (2001). ArticleCASPubMedPubMed Central Google Scholar
Robinson, M. S. & Kreis, T. E. Recruitment of coat proteins onto Golgi membranes in intact and permeabilized cells: effects of brefeldin A and G protein activators. Cell69, 129–138 (1992). ArticleCASPubMed Google Scholar
Wong, D. H. & Brodsky, F. M. 100-kD proteins of Golgi- and trans-Golgi network-associated coated vesicles have related but distinct membrane binding properties. J. Cell Biol.117, 1171–1179 (1992). ArticleCASPubMed Google Scholar
Paleotti, O. et al. The small G-protein Arf6GTP recruits the AP-2 adaptor complex to membranes. J. Biol. Chem.280, 21661–21666 (2005). ArticleCASPubMed Google Scholar
Krauss, M. et al. ARF6 stimulates clathrin/AP-2 recruitment to synaptic membranes by activating phosphatidylinositol phosphate kinase type Iγ. J. Cell Biol.162, 113–124 (2003). ArticleCASPubMedPubMed Central Google Scholar
Tanabe, K. et al. A novel GTPase-activating protein for ARF6 directly interacts with clathrin and regulates clathrin-dependent endocytosis. Mol. Biol. Cell16, 1617–1628 (2005). ArticleCASPubMedPubMed Central Google Scholar
Traub, L. M. Common principles in clathrin-mediated sorting at the Golgi and the plasma membrane. Biochim. Biophys. Acta1744, 415–437 (2005). ArticleCASPubMed Google Scholar
Praefcke, G. et al. Evolving nature of the AP2 α-appendage hub during clathrin-coated vesicle endocytosis. EMBO J.23, 4371–4383 (2004). ArticleCASPubMedPubMed Central Google Scholar
Owen, D., Vallis, Y., Noble, M., Hunter, J. & McMahon, H. A structural explanation for the binding of multiple ligands by the α-adaptin appendage domain. Cell97, 805–815 (1999). ArticleCASPubMed Google Scholar
Traub, L., Downs, M., Westrich, J. & Fremont, D. Crystal structure of the α appendage of AP-2 reveals a recruitment platform for clathrin-coat assembly. Proc. Natl Acad. Sci. USA96, 8907–8912 (1999). ArticleCASPubMedPubMed Central Google Scholar
Brett, T., Traub, L. & Fremont, D. Accessory protein recruitment motifs in clathrin-mediated endocytosis. Structure10, 797–809 (2002). ArticleCASPubMed Google Scholar
Ritter, B. et al. Two WXXF-based motifs in NECAPs define the specificity of accessory protein binding to AP-1 and AP-2. EMBO J.23, 3701–3710 (2004). ArticleCASPubMedPubMed Central Google Scholar
Nogi, T. et al. Structural basis for the accessory protein recruitment by the γ-adaptin ear domain. Nature Struct. Biol.9, 527–531 (2002). CASPubMed Google Scholar
Kent, H., McMahon, H., Evans, P., Benmerah, A. & Owen, D. γ-adaptin appendage domain: structure and binding site for eps15 and γ-synergin. Structure10, 1139–1148 (2002). ArticleCASPubMed Google Scholar
Mishra, S. K. et al. Dual engagement regulation of protein interactions with the AP-2 adaptor α appendage. J. Biol. Chem.279, 46191–46203 (2004). ArticleCASPubMed Google Scholar
Owen, D., Vallis, Y., Pearse, B., McMahon, H. & Evans, P. The structure and function of the β2-adaptin appendage domain. EMBO J.19, 4216–4227 (2000). ArticleCASPubMedPubMed Central Google Scholar
Mishra, S. K. et al. Functional dissection of an AP-2 β2 appendage-binding sequence within the autosomal recessive hypercholesterolemia (ARH) protein. J. Biol. Chem.280, 19270–19280 (2005). ArticleCASPubMed Google Scholar
Miller, G. J., Mattera, R., Bonifacino, J. S. & Hurley, J. H. Recognition of accessory protein motifs by the γ-adaptin ear domain of GGA3. Nature Struct. Biol.10, 599–606 (2003). ArticleCASPubMed Google Scholar
Collins, B. M., Praefcke, G. J., Robinson, M. S. & Owen, D. J. Structural basis for binding of accessory proteins by the appendage domain of GGAs. Nature Struct. Biol.10, 607–613 (2003). ArticleCASPubMed Google Scholar
Duden, R., Allan, V. & Kreis, T. Involvement of β-COP in membrane traffic through the Golgi complex. Trends Cell Biol.1, 14–19 (1991). ArticleCASPubMed Google Scholar
Schledzewski, K., Brinkmann, H. & Mendel, R. R. Phylogenetic analysis of components of the eukaryotic vesicle transport system reveals a common origin of adaptor protein complexes 1, 2, and 3 and the F subcomplex of the coatomer COPI. J. Mol. Evol.48, 770–778 (1999). ArticleCASPubMed Google Scholar
Hoffman, G. R., Rahl, P. B., Collins, R. N. & Cerione, R. A. Conserved structural motifs in intracellular trafficking pathways: structure of the γCOP appendage domain. Mol. Cell12, 615–625 (2003). ArticleCASPubMed Google Scholar
Watson, P. J., Frigerio, G., Collins, B. M., Duden, R. & Owen, D. J. γ-COP appendage domain — structure and function. Traffic5, 79–88 (2004). ArticleCASPubMed Google Scholar
McMahon, H. T. & Mills, I. G. COP and clathrin-coated vesicle budding: different pathways, common approaches. Curr. Opin. Cell Biol.16, 379–391 (2004). ArticleCASPubMed Google Scholar
Eugster, A., Frigerio, G., Dale, M. & Duden, R. COP I domains required for coatomer integrity, and novel interactions with ARF and ARF-GAP. EMBO J.19, 3905–3917 (2000). ArticleCASPubMedPubMed Central Google Scholar
Devos, D. et al. Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol.2, e380 (2004). ArticlePubMedPubMed CentralCAS Google Scholar
Gonzalez, L. J., Weis, W. & Scheller, R. A novel SNARE N-terminal domain revealed by the crystal structure of Sec22b. J. Biol. Chem.276, 24203–24221 (2001). ArticleCASPubMed Google Scholar
Tochio, H., Tsui, M., Bandfield, D. & Zhang, M. An autoinhibitory mechanism for non syntaxin SNARE proteins revealed by the structure of Ykt6p. Science293, 698–702 (2001). ArticleCASPubMed Google Scholar
Schwartz, T. & Blobel, G. Structural basis for the function of the β subunit of the eukaryotic signal recognition particle receptor. Cell112, 793–803 (2003). Provides a possible structural mechanism for the interaction between two widely conserved protein folds — the σ/N-μ2 fold and that of an ARF-family GTPase. ArticleCASPubMed Google Scholar
Wilbur, J. D., Hwang, P. K. & Brodsky, F. M. New faces of the familiar clathrin lattice. Traffic6, 346–350 (2005). ArticleCASPubMed Google Scholar