Auxilin-dynamin interactions link the uncoating ATPase chaperone machinery with vesicle formation

Developmental Cell

Volumn 4, Issue 6, 2003, Pages 929-940

  Newmyer, Sherri L ^a   Christensen, Arne ^b,c   Sever, Sanja ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AUXILIN; CHAPERONE; CLATHRIN; DYNAMIN; GUANOSINE TRIPHOSPHATASE; HEAT SHOCK PROTEIN 70; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOGENESIS; CELL ASSAY; CELL MEMBRANE; CELLULAR DISTRIBUTION; COATED VESICLE; CONTROLLED STUDY; ENDOCYTOSIS; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM;

ADENOSINE TRIPHOSPHATASES; ADENOVIRIDAE; AUXILINS; BINDING SITES; CARRIER PROTEINS; CLATHRIN-COATED VESICLES; DYNAMINS; ENDOCYTOSIS; GLUTATHIONE TRANSFERASE; GTP-BINDING PROTEINS; GUANOSINE TRIPHOSPHATE; HELA CELLS; HSC70 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; KINETICS; MODELS, BIOLOGICAL; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS;

ANIMALIA;

EID: 0038617815     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1534-5807(03)00157-6     Document Type: Article

References (58)

1. Altschuler Y. Barbas S. Terlecky L. Mostov K. Schmid S.L. Common and distinct functions for dynamin-1 and dynamin-2 isoforms J. Cell Biol. 143 1998 1871-1881
2. Baba T. Damke H. Hinshaw J.E. Ikeda K. Schmid S.L. Warnock D.E. Role of dynamin in clathrin-coated vesicle formation Cold Spring Harb. Symp. Quant. Biol. 60 1995 235-242
3. Bourne H.R. Sanders D.A. McCormick F. The GTPase superfamily: conserved structure and molecular mechanism Nature 349 1991 117-127
4. Cao H. Garcia F. McNiven M. Differential distribution of dynamin isoforms in mammalian cells Mol. Biol. Cell 9 1998 2595-2609
5. Carr J.F. Hinshaw J.E. Dynamin assembles into spirals under physiological salt conditions upon the addition of GDP and gamma-phosphate analogues J. Biol. Chem. 272 1997 28030-28035
6. Carter L.L. Redelmeier T.E. Woollenweber L.A. Schmid S.L. Multiple GTP-binding proteins participate in clathrin-coated vesicle-mediated endocytosis J. Cell Biol. 120 1993 37-45
7. Chang H.C. Newmyer S.L. Hull M.J. Ebersold M. Schmid S.L. Mellman I. Hsc70 is required for endocytosis and clathrin function in Drosophila J. Cell Biol. 159 2002 477-487
8. Damke H. Baba T. Warnock D.E. Schmid S.L. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation J. Cell Biol. 127 1994 915-934
9. Damke H. Binns D.D. Ueda H. Schmid S.L. Baba T. Dynamin GTPase domain mutants block endocytic vesicle formation at morphologically distinct stages Mol. Biol. Cell 12 2001a 2578-2589
10. Damke H. Muhlberg A.B. Sever S. Sholly S. Warnock D.E. Schmid S.L. Expression, purification, and functional assays for self-association of dynamin-1 Methods Enzymol. 329 2001b 447-457
11. Danino D. Hinshaw J.E. Dynamin family of mechanoenzymes Curr. Opin. Cell Biol. 13 2001 454-460
12. De Camilli P. Takei K. Molecular mechanisms in synaptic vesicle endocytosis and recycling Neuron 16 1996 481-486
13. Fish K.N. Schmid S.L. Damke H. Evidence that dynamin-2 functions as signal-transducing GTPase J. Cell Biol. 150 2000 145-154
14. Fukushima N.H. Brisch E. Keegan B.R. Bleazard W. Shaw J.M. The GTPase effector domain sequence of the Dnm1p GTPase regulates self-assembly and controls a rate-limiting step in mitochondrial fission Mol. Biol. Cell 12 2001 2756-2766
15. Greener T. Zhao X. Nojima H. Eisenberg E. Greene L.E. Role of cyclin G-associated kinase in uncoating clathrin-coated vesicles from non-neuronal cells J. Biol. Chem. 275 2000 1365-1370
16. Greener T. Grant B. Zhang Y. Wu X. Greene L.E. Hirsh D. Eisenberg E. Caenorhabditis elegans auxilin: a J-domain protein essential for clathrin-mediated endocytosis in vivo Nat. Cell Biol. 3 2001 215-219
17. Hannan L.A. Newmyer S.L. Schmid S.L. ATP- and cytosol-dependent release of adaptor proteins from clathrin-coated vesicles: a dual role for hsc70 Mol. Biol. Cell 9 1998 2217-2229
18. Hardy S. Kitamura M. Harris-Stansil T. Dai Y. Phipps M.L. Construction of adenovirus vectors through Cre-lox recombination J. Virol. 71 1997 1842-1849
19. Hill E. van der Kaay J. Downes C.P. Smythe E. The role for dynamin and its binding partners in coated pit invagination and scission J. Cell Biol. 152 2001 309-324
20. Hinshaw J.E. Schmid S.L. Dynamin self assembles into rings suggesting a mechanism for coated vesicle budding Nature 374 1995 190-192
21. Holstein S.E.H. Ungewickell H. Ungewickell E. Mechanism of clathrin basket dissociation: separate functions of protein domains of the DnaJ-homologue auxilin J. Cell Biol. 135 1996 925-937
22. Höning S. Kreimer G. Robenek H. Jockusch B.M. Receptor-mediated endocytosis is sensitive to antibodies against the uncoating ATPase (hsc70) J. Cell Sci. 107 1994 1185-1196
23. Janzen C. Kochs G. Haller O. A monomeric GTPase-negative MxA mutant with antiviral activity J. Virol. 74 2000 8202-8206
24. Jones S.M. Howell K.E. Henley J.R. Cao H. McNiven M.A. Role of dynamin in the formation of transport vesicles from the trans-Golgi network Science 279 1998 573-577
25. Kelley W.L. The J-domain family and the recruitment of chaperone power Trends Biochem. Sci. 23 1998 222-227
26. Kirchhausen T. Three ways to make a vesicle Nat. Rev. Mol. Cell Biol. 1 2000 187-198
27. Maeda K. Nakata T. Noda Y. Sato-Yoshitake R. Hirokawa N. Interaction of dynamin with microtubules: its structure and GTPase activity investigated by using highly purified dynamin Mol. Biol. Cell 3 1992 1181-1194
28. Marks B. Stowell M.H. Vallis J. Mills I.G. Gobson A. Hopkins C.R. McMahon H.T. GTPase activity of dynamin and resulting conformational change are essential for endocytosis Nature 410 2001 231-235
29. McNiven M.A. Dynamin: a molecular motor with pinchase action Cell 94 1998 151-154
30. Mittal R. Ahmadian M.R. Goody R.S. Wittinghofer A. Formation of a transition-state analog of the Ras GTPase reaction by Rad-GDP, tetrafluoroaluminate and GTPase-activating proteins Science 273 1996 115-117
31. Morgan J.R. Prasad K. Jin S. Augustine G.J. Lafer E.M. Uncoating of clathrin-coated vesicles in presynaptic terminals: roles for Hsc70 and auxilin Neuron 32 2001 289-300
32. Mu F.T. Callaghan J.M. Steele-Mortimer O. Stenmark H. Parton R.G. Campbell P.L. McCluskey J. Yeo J.P. Tock E.P. Toh B.H. EEA1, an early endosome-associated protein. EEA1 is a conserved alpha-helical peripheral membrane protein flanked by cysteine "fingers" and contains a calmodulin-binding IQ motif J. Biol. Chem. 270 1995 13503-13511
33. Muhlberg A.B. Warnock D.E. Schmid S.L. Domain structure and intramolecular regulation of dynamin GTPase EMBO J. 16 1997 6676-6683
34. Neimann H.H. Knetsch M.L.W. Scherer A. Manstein D.J. Kull F.J. Crystal structure of a dynamin GTPase domain in both nucleotide-free and GDP-bound forms EMBO J. 20 2001 5813-5821
35. Newmyer S.L. Schmid S.L. Dominant-interfering hsc70 mutants disrupt multiple stages of the clathrin-coated vesicle cycle in vivo J. Cell Biol. 152 2001 607-620
36. Owen D.J. Vallis Y. Noble M.E. Hunter J.B. Dafforn T.R. Evans P.R. McMahon H.T. A structural explanation for the binding of multiple ligands by the alpha-adaptin appendage domain Cell 97 1999 805-815
37. Scheele U. Kalthoff C. Ungewickell E. Multiple interactions of auxilin 1 with clathrin and the AP-2 adaptor complex J. Biol. Chem. 276 2001 36131-36138
38. Scheffzek K. Ahmadian R. Wittinghofer A. GTPase-activating proteins: helping hands to complement an active site Trends Biochem. Sci. 23 1998 257-262
39. Schlossman D.M. Schmid S.L. Braell W.A. Rothman J.E. An enzyme that removes clathrin coats: purification of an uncoating ATPase J. Cell Biol. 99 1984 723-733
40. Schmid S.L. Clathrin-coated vesicle formation and protein sorting: an integrated process Annu. Rev. Biochem. 66 1997 511-548
41. Schmid S.L. McNiven M.A. De Camilli P. Dynamin and its partners: a progress report Curr. Opin. Cell Biol. 10 1998 504-512
42. Schmidt A. Wolde M. Thiele C. Fest W. Kratzin H. Podtelejnikov A.V. Witke W. Huttner W.B. Söling H.-D. Endophilin I mediates synaptic vesicle formation by transfer of arachidonate to lysophosphatidic acid Nature 401 1999 133-141
43. Sever S. Dynamin and endocytosis Curr. Opin. Cell Biol. 14 2002 463-467
44. Sever S. Muhlberg A.B. Schmid S.L. Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis Nature 398 1999 481-486
45. Sever S. Damke H. Schmid S.L. Dynamin:GTP controls formation of constricted coated pits, the rate limiting step in clathrin-mediated endocytosis J. Cell Biol. 150 2000 1137-1147
46. Shpetner H.S. Vallee R.B. Identification of dynamin, a novel mechanochemical enzyme that mediates interactions between microtubules Cell 59 1989 421-432
47. Simpson F. Hussain N.K. Qualmann B. Kelly R.B. Kay B.K. McPherson P.S. Schmid S.L. SH3-domain-containing proteins function at distinct steps in clathrin-coated vesicle formation Nat. Cell Biol. 1 1999 119-124
48. Slepnev V.I. Ochoa G.C. Butler M.H. Grabs D. Camilli P.D. Role of phosphorylation in regulation of the assembly of endocytic coat complexes Science 281 1998 821-824
49. Smythe E. Pypaert M. Lucocq J. Warren G. Formation of coated vesicles from coated pits in broken A431 cells J. Cell Biol. 108 1989 843-853
50. Smythe E. Redelmeier T.E. Schmid S.L. Receptor-mediated endocytosis in semiintact cells Methods Enzymol. 219 1992 223-234
51. Sweitzer S. Hinshaw J. Dynamin undergoes a GTP-dependent conformational change causing vesiculation Cell 93 1998 1021-1029
52. Takei K. Haucke V. Slepnev V. Farsad K. Salazar M. Chen H. De Camilli P. Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes Cell 94 1998 131-141
53. Tuma P.L. Collins C.A. Activation of dynamin GTPase is a result of positive cooperativity J. Biol. Chem. 269 1994 30842-30847
54. Ungewickell E. Ungewickell H. Holstein S.E. Lindner R. Prasad K. Barouch W. Martin B. Greene L.E. Eisenberg E. Role of auxilin in uncoating clathrin-coated vesicles Nature 378 1995 632-635
55. Warnock D.E. Schmid S.L. Dynamin GTPase, a force generating molecular switch Bioessays 18 1996 885-893
56. Warnock D.E. Hinshaw J.E. Schmid S.L. Dynamin self assembly stimulates its GTPase activity J. Biol. Chem. 271 1996 22310-22314
57. Wu X. Zhao X. Baylor L. Kaushal S. Eisenberg E. Greene L.E. Clathrin exchange during clathrin-mediated endocytosis J. Cell Biol. 155 2001 291-300
58. Zhao X. Greener T. Al-Hasani H. Cushman S.W. Eisenberg E. Greene L.E. Expression of auxilin or AP180 inhibits endocytosis by mislocalizing clathrin: evidance for formation of nascent pits containing AP1 or AP2 but not clathrin J. Cell Sci. 114 2001 353-356