Dynamin and endocytosis

Current Opinion in Cell Biology

Volumn 14, Issue 4, 2002, Pages 463-467

  Sever, Sanja ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; DYNAMIN; GUANOSINE TRIPHOSPHATASE; MITOGEN ACTIVATED PROTEIN KINASE;

ACTIN FILAMENT; APOPTOSIS; ENDOCYTOSIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE;

ANIMALS; DYNAMINS; ENDOCYTOSIS; GTP PHOSPHOHYDROLASES; HUMANS; MOLECULAR STRUCTURE; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY;

EID: 0036701910     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(02)00347-2     Document Type: Review

References (44)

1. Schmid S.L., McNiven M.A., De Camilli P. Dynamin and its partners: a progress report. Curr Opin Cell Biol. 10:1998;504-512.
2. Hinshaw J.E., Schmid S.L. Dynamin self-assembles into rings, suggesting a mechanism for coated vesicle budding. Nature. 374:1995;190-192.
3. Tuma P.L., Collins C.A. Activation of dynamin GTPase is a result of positive cooperativity. J Biol Chem. 269:1994;30842-30847.
4. Warnock D.E., Terlecky L.J., Schmid S.L. Dynamin GTPase is stimulated by crosslinking through the C-terminal proline-rich domain. EMBO J. 14:1995;1322-1328.
5. Danino D., Hinshaw J.E. Dynamin family of mechanoenzymes. Curr Opin Cell Biol. 13:2001;454-460. This is a timely review that summarizes the roles of dynamin family members in cells. It emphasizes their ability to self-assemble into higher-order molecular structures, and suggests that their role in the cell is to act as mechanochemical enzymes.
6. Warnock D.E., Schmid S.L. Dynamin GTPase, a force generating molecular switch. Bioessays. 18:1996;885-893.
7. McNiven M.A. Dynamin: a molecular motor with pinchase action. Cell. 94:1998;151-154.
8. Sever S., Muhlberg A.B., Schmid S.L. Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature. 398:1999;481-486.
9. 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. This describes the first high-resolution three-dimensional structure of the dynamin A GTPase domain in both nucleotide-free and GDP-bound forms. Until this work, only the structure of the PH domain of dynamin had been solved at high resolution.
10. Pai E.F., Krengel U., Petsko G.A., Goody R.S., Kabsch W., Wittinghofer A. Refined crystal structure of the triphosphate conformation of H-Ras p21 at 1.35 Å resolution: implications for the mechanism of GTP hydrolysis. EMBO J. 9:1990;2351-2359.
11. Muhlberg A.B., Warnock D.E., Schmid S.L. Domain structure and intramolecular regulation of dynamin GTPase. EMBO J. 16:1997;6676-6683.
12. Smirnova E., Shurland D.L., Newman-Smith E.D., Pishvaee B., van der Bliek A.M. A model for dynamin self-assembly based on binding between three different protein domains. J Biol Chem. 274:1999;14942-14947.
13. Okamoto P.M., Tripet B., Litowski J., Hodges R.S., Vallee R.B. Multiple distinct coiled-coils are involved in dynamin self-assembly. J Biol Chem. 274:1999;10277-10286.
14. Sweitzer S., Hinshaw J. Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell. 93:1998;1021-1029.
15. 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.
16. Stowell M.H.B., Marks B., Wigge P., McMahon H.T. Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring. Nature Cell Biol. 1:1999;27-32.
17. Kosaka T., Ikeda K. Possible temperature-dependent blockage of synaptic vesicle recycling induced by a single gene mutation in Drosophila. J Neurobiol. 14:1983;207-225.
18. Takei K., McPherson P.S., Schmid S.L., De Camilli P. Tubular membrane invaginations coated by dynamin rings are induced by GTPγS in nerve terminals. Nature. 374:1995;186-190.
19. Kim Y., Park D., Park S., Kim S., Cheong G., Hwang I. Arabidopsis dynamin-like 2 that binds specifically to phosphatidylinositol 4-phosphate assembles into a high-molecular weight complex in vivo and in vitro. Plant Physiol. 127:2001;1243-1255. Electron microscopy studies revealed that the purified recombinant ADL2 (Arabidopsis dynamin-like 2) forms spiral-coiled structures or rings. In addition, sucrose gradient and gel filtration experiments demonstrated that the membrane-bound protein exists as a higher molecular weight complex, suggesting ADL2 self-assembles in vivo.
20. 4-. This study is equivalent to that by Yoon et al. (2001) [21•] .
21. Yoon Y., Pitts K.R., McNiven M.A. Mammalian dynamin-like protein DLP1 tubulates membranes. Mol Biol Cell. 12:2001;2894-2905. This study shows that expression of a GFP-tagged dominant-negative mutant of DLP1 (Drp1) led to accumulation of membrane tubules inside the cell. Although the same mutant was used in [20•], this study used high-magnification electron microscopy and immunogold labeling to confirm DLP1 association with membrane tubules. The authors also show that purified DLP1 self-assembles into stacked helical rings in the presence of GTPγS and tubulates membranes.
22. Kochs G., Haener M., Aebi U., Haller O. Self-assembly of human MxA GTPase into highly ordered dynamin-like oligomers. J Biol Chem. 277:2002;14172-14176. Sedimentation assays and electron microscopy were used to demonstrate that recombinant MxA protein assembles into long filamentous structures at physiological salt concentrations in the absence of guanine nucleotides.
23. Okamoto P.M., Gamby C., Wells D., Fallon J., Vallee R.B. Dynamin isoform-specific interaction with the Shank/ProSAP scaffolding proteins of the postsynaptic density and actin cytoskeleton. J Biol Chem. 276:2001;48458-48465. Shank/ProSAP was identified as a dynamin 2 interacting protein in a yeast two-hybrid assay. Co-fractionation and localization of dynamin 2 with postsynaptic density, a site to which Shank 1 almost exclusively localizes, suggests that these interactions are physiological important. It also places dynamin 2 in a novel cellular location.
24. Farsad K., Ringstad N., Takei K., Floyd S.R., Rose K., De Camilli P. Generation of high-curvature membranes mediated by direct endophilin bilayer interactions. J Cell Biol. 155:2001;193-200. Purified endophilin was shown to directly bind and evaginate lipid bilayers into narrow tubules, independently of its putative enzymatic activity. With this study, endophilin joins dynamin and amphiphysin as another endocytic protein that can deform membranes in vitro.
25. Janzen C., Kochs G., Haller O. A monomeric GTPase-negative MxA mutant with antiviral activity. J Virol. 74:2000;8202-8206.
26. Zhang P., Hinshaw J.E. Three-dimensional reconstitution of dynamin in the constricted state. Nature Cell Biol. 3:2001;1-5. An elegant study showing for the first time the three-dimensional structure of assembled dynamin at a resolution of 20 Å. The map was obtained from dynaminΔPRD fully assembled onto lipid tubules in the presence of the nonhydrolysable nucleotide analogue GMP-PCP, and reveals a role of the GTPase, middle and GED domains in assembly.
27. Klockow B., Tichelaar W., Madden D., Neimann H.H., Akiba T., Hirose K., Manstein D. The dynamin A ring complex: molecular organization and nucleotide-dependent conformational changes. EMBO J. 21:2002;240-250. Comparison of the three-dimensional maps of the dynamin A ring complex obtained by single-particle analysis in the presence versus absence of the nucleotide analogue GppNHp further supports the importance of the GTPase and GTPase effector domains in self-assembly and nucleotide-dependent conformational changes.
28. 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. 12:2001;2578-2589. In contrast to existing views, this study shows that it is impossible to block dynamin in GDP-bound or GTP-bound forms by making mutations within the GTPase domain based on known mutations in other GTPases. Specifically, mutations within the GTPase domain destabilized binding of GTP and GDP, resulting in nucleotide-unoccupied enzymes. The paper also provides a superb discussion section that compares biochemical properties of tested dynamin GTPase mutants and their in vivo phenotypes with other GTPase superfamily members.
29. 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.
30. Wittinghofer A. The functioning of molecular switches in three dimensions. Hall A., GTPases. 2000;244-310 Oxford University Press, New York.
31. Fukushima N.H., Brisch E., Keegan B.R., Bleazard W., Shaw J.M. The GTPase effector domain sequence of the Dnm1 GTPase regulates self-assembly and controls a rate-limiting step in mitochondrial fission. Mol Bio Cell. 12:2001;2756-2766. Consistent with work on dynamin (Sever et al. [2000] [32] ), this study shows that expression of mutant Dnm1p with mutations in the GTPase effector domain that are equivalent to those made in dynamin exhibit specific phenotypes in yeast. Specifically, expression of Dnm1p Lys705→Ala stimulates a rate-limiting step in mitochondrial fission, while Dnm1p Arg736→Ala exhibited a Δdnm1-null phenotype, further demonstrating the importance of the arginine residue within the GTPase effector domain for efficient GTP hydrolysis. The data directly contradict with the conclusions made by Marks et al. (2001) [34•] on the role of this arginine residue.
32. 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.
33. Krishnan K.S., Rikhy R., Rao S., Shivalkar M., Mosko M., Narayanan R., Etter P., Estes P.S., Ramaswami M. Nucleoside diphosphate kinase, a source of GTP, is required for dynamin-dependent synaptic vesicle recycling. Neuron. 1:2001;197-210. Drosophila genetics is used to place the roles of dynamin and abnormal wing disc (Awd), a nucleoside diphosphate kinase that converts nucleoside diphosphates to nucleoside triphosphates, on the same pathway in recycling synaptic vesicles at the plasma membrane. Awd is homologous to the product of the tumor suppressor gene nm23, suggesting that dynamin or endocytosis, or both, might be involved in tumorigenesis.
34. 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. Using the same mutations described in Sever et al. (1999) [8] and Sever et al. (2000) [32], the authors suggest that GTPase effector domain mutants have GTPase activity that is stimulated in a normal fashion and undergo normal endocytosis. But these mutants have the phenotypic characteristics of mutants expressing the same mutations in Dnm1p [31••] . In addition, the authors argue that the Thr65→Ala mutant, which contains a mutation in the dynamin GTPase domain, blocks dynamin in its GTP-bound conformation. A detailed biochemical analysis of the same mutant in Damke et al. (2001) [28••] is described.
35. Seewald M.J., Korner C., Wittinghofer A., Vetter I. RanGAP mediates GTP hydrolysis without an arginine finger. Nature. 415:2002;662-666. This is an important breakthrough study, providing novel insights into the mechanism of GTPase-activating protein (GAP)-stimulated GTP hydrolysis. Three-dimensional structure of a Ran-RanGAP-RanBP (Ran-binding protein) ternary complex in a transition state demonstrates for the first time that GAPs can increase the rate of GTP hydrolysis without providing a catalytically active 'arginine finger'. The catalytic machinery provided solely by the Ran GTPase is correctly positioned by the interactions with the RanGAP, demonstrating a novel mechanism for GAP function.
36. Hillig R.C., Renault L., Vetter I.R., Drell T., Wittinghofer A., Becker J. The crystal structure of RNA1p: a new fold for a GTPase-activating protein. Mol Cell. 6:1999;781-791.
37. Fish K.N., Schmid S.L., Damke H. Evidence that dynamin-2 functions as signal-transducing GTPase. J Cell Biol. 150:2000;145-154.
38. Frank S., Gaume B., Bergmann-Leitner E.S., Leitner W.W., Robert E.G., Catez F., Smith C.L., Youle R.J. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev Cell. 4:2001;515-525. The remarkable finding in this paper is that expression of a dominant-negative mutant of Drp1 inhibited apoptosis in COS cells. This finding is complementary to that of Fish et al. (2000) [37], suggesting multiple roles for dynamin family members in the cell.
39. Hislop J.N., Everest H.M., Flynn A., Harding T., Uney J.B., Troskie B.E., Millar R.P., McArdle C.A. Differential internalization of mammalian and non-mammalian gonadotropin-releasing hormone receptors. Uncoupling of dynamin-dependent internalization form mitogen-activated protein kinase signaling. J Biol Chem. 276:2001;39685-39694. In this study, the authors followed internalization of human and Xenopus gonadotropin-releasing hormone (GnRG) receptor in cells expressing the dominant-negative dynamin mutant (dynamin Lys44→Arg), and showed that while internalization of human receptor was not abolished, internalization of Xenopus GnRG receptor as well as EGF receptor was potently inhibited. In contrast to these differences, none of the receptors mediated phosphory-lation of ERK-2, placing the role of dynamin in mitogen-activated protein kinase signaling.
40. Kranenburg O., Verlaan I., Moolenaar W.H. Dynamin is required for the activation of mitogen-activated protein (MAP) kinase by MAP kinase kinase. J Biol Chem. 274:1999;35301-35304.
41. McNiven M.A., Kim L., Krueger E.W., Orth J.D., Cao H., Wong T.W. Regulated interactions between dynamin and the actin-binding protein modulate cell shape. J Cell Biol. 151:2000;187-198.
42. Lee E., De Camilli P. Dynamin at actin tails. Proc Natl Acad Sci USA. 99:2002;161-166. See annotation Orth et al. (2002) [43•] .
43. Orth J.D., Krueger E.W., Cao H., McNiven M.A. The large GTPase dynamin regulates actin comet formation and movement in living cells. Proc Natl Acad Sci USA. 99:2002;167-172. This and Lee et al. (2002) [42•] show, using live-cell imaging, confocal microscopy immunocytochemistry and particle-tracking analysis, that green fluorescent protein tagged dynamin 2 is a component of actin comets associated with macropinosomes. Dynamin localization to actin tails required the proline/arginine-rich domain, and a dominant-negative dynamin mutant decreased comet formation, reduced comet velocity and induced irregular comet movements. This suggests a role for dynamin in actin dynamics.
44. Hoepfner D., van der Berg M., Philippsen P., Tabak H.F., Hettema E.H. A role for Vps1p, actin, and the Myo2p motor in peroxisome abundance and inheritance in Saccharomyces cerevisiae. J Cell Biol. 155:2001;979-990. Superb in vivo time-lapse microscopy reveals a novel role of the GTPase Vps1p in controlling the number of peroxisomes in yeast. Under conditions of growth, cells maintained nine peroxisomes on average, whereas in Δvps1 mutants only one of two giant peroxisomes remained, implicating vps1 in the membrane fission event that is required for regulation of peroxisome abundance. Efficient segregation of peroxisomes from mother to bud was dependent on the actin cytoskeleton.