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Real‐time imaging of plasma membrane deformations reveals pre‐fusion membrane curvature changes and a role for dynamin in the regulation of fusion pore expansion
dc.contributor.authorAnantharam, Arunen_US
dc.contributor.authorAxelrod, Danielen_US
dc.contributor.authorHolz, Ronald W.en_US
dc.date.accessioned2012-08-09T14:55:16Z
dc.date.available2013-10-01T17:06:31Zen_US
dc.date.issued2012-08en_US
dc.identifier.citationAnantharam, Arun; Axelrod, Daniel; Holz, Ronald W. (2012). "Real‐time imaging of plasma membrane deformations reveals pre‐fusion membrane curvature changes and a role for dynamin in the regulation of fusion pore expansion." Journal of Neurochemistry 122(4). <http://hdl.handle.net/2027.42/92384>en_US
dc.identifier.issn0022-3042en_US
dc.identifier.issn1471-4159en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/92384
dc.description.abstractAssays for real‐time investigation of exocytosis typically measure what is released from the granule. From this, inferences are made about the dynamics of membrane remodeling as fusion progresses from start to finish. We have recently undertaken a different approach to investigate the fusion process, by focusing not primarily on the granule, but rather its partner in exocytosis – the plasma membrane. We have been guided by the idea that biochemical interactions between the granule and plasma membranes before and during fusion, cause changes in membrane conformation. To enable study of membrane conformation, a novel imaging technique was developed combining polarized excitation of an oriented membrane probe 1,1′‐dioctadecyl‐3,3,3′,3′‐tetramethylindocarbocyanine perchlorate (diI) with total internal reflection fluorescence microscopy (pTIRFM). Because this technique measures changes in membrane conformation (or deformations) directly, its usefulness persists even after granule cargo reporter (catecholamine, or protein), is no longer present. In this mini‐review, we first summarize the workings of pTIRFM. We then discuss the application of the technique to investigate deformations in the membrane preceding fusion, and later, during fusion pore expansion. Finally, we discuss how expansion of the fusion pore may be regulated by the GTPase activity of dynamin.en_US
dc.publisherWiley Periodicals, Inc.en_US
dc.publisherBlackwell Publishing Ltden_US
dc.subject.otherDynaminen_US
dc.subject.otherExocytosisen_US
dc.subject.otherGranuleen_US
dc.subject.otherPolarizationen_US
dc.subject.otherTIRFMen_US
dc.subject.otherChromaffin Cellsen_US
dc.titleReal‐time imaging of plasma membrane deformations reveals pre‐fusion membrane curvature changes and a role for dynamin in the regulation of fusion pore expansionen_US
dc.typeArticleen_US
dc.rights.robotsIndexNoFollowen_US
dc.subject.hlbsecondlevelNeurosciencesen_US
dc.subject.hlbtoplevelHealth Sciencesen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumDepartment of Pharmacology, University of Michigan, Ann Arbor, Michigan, USAen_US
dc.contributor.affiliationumDepartment of Physics and LSA Biophysics, University of Michigan, Ann Arbor, Michigan, USAen_US
dc.contributor.affiliationotherDepartment of Biological Sciences, Wayne State University, Detroit, Michigan, USAen_US
dc.identifier.pmid22671293en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/92384/1/j.1471-4159.2012.07816.x.pdf
dc.identifier.doi10.1111/j.1471-4159.2012.07816.xen_US
dc.identifier.sourceJournal of Neurochemistryen_US
dc.identifier.citedreferenceRamachandran R. and Schmid S. L. ( 2008 ) Real‐time detection reveals that effectors couple dynamin’s GTP‐dependent conformational changes to the membrane. EMBO J. 27, 27 – 37.en_US
dc.identifier.citedreferenceLee E. and De Camilli P. ( 2002 ) Dynamin at actin tails. Proc. Natl. Acad. Sci. U S A 99, 161 – 166.en_US
dc.identifier.citedreferenceLynch K. L., Gerona R. R. L., Kielar D. M., Martens S., McMahon H. T. and Martin T. F. J. ( 2008 ) Synaptotagmin‐1 utilizes membrane bending and SNARE binding to drive fusion pore expansion. Mol. Biol. Cell 19, 5093 – 5103.en_US
dc.identifier.citedreferenceMacia E., Ehrlich M., Massol R., Boucrot E., Brunner C. and Kirchhausen T. ( 2006 ) Dynasore, a cell‐permeable inhibitor of dynamin. Dev. Cell 10, 839 – 850.en_US
dc.identifier.citedreferenceMarks B., Stowell M. H., Vallis Y., Mills I. G., Gibson A., Hopkins C. R. and McMahon H. T. ( 2001 ) GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410, 231 – 235.en_US
dc.identifier.citedreferenceNgatchou A. N., Kisler K., Fang Q., Walter A. M., Zhao Y., Bruns D., Sorensen J. B. and Lindau M. ( 2010 ) Role of the synaptobrevin C terminus in fusion pore formation. Proc. Natl. Acad. Sci. USA 107, 18463 – 18468.en_US
dc.identifier.citedreferenceOkamoto M., Schoch S. and Sudhof T. C. ( 1999 ) EHSH1/Intersectin, a protein that contains EH and SH3 domains and binds to dynamin and SNAP‐25. A protein connection between exocytosis and endocytosis? J. Biol. Chem. 274, 18446 – 18454.en_US
dc.identifier.citedreferencePalade G. ( 1975 ) Intracellular aspects of the process of protein synthesis. Science 189, 347 – 358.en_US
dc.identifier.citedreferencePerrais D., Kleppe I. C., Taraska J. W. and Almers W. ( 2004 ) Recapture after exocytosis causes differential retention of protein in granules of bovine chromaffin cells. J. Physiol. Online. 560, 413 – 428.en_US
dc.identifier.citedreferencePlattner H., Artalejo A. R. and Neher E. ( 1997 ) Ultrastructural organization of bovine chromaffin cell cortex‐ analysis by cryofixation and morphometry of aspects pertinent to exocytosis [In process citation]. J. Cell Biol. 139, 1709 – 1717.en_US
dc.identifier.citedreferencePucadyil T. J. and Schmid S. L. ( 2009 ) Conserved functions of membrane active GTPases in coated vesicle formation. Science 325, 1217 – 1220.en_US
dc.identifier.citedreferenceRichard J. P., Leikina E., Langen R., Henne W. M., Popova M., Balla T., McMahon H. T., Kozlov M. M. and Chernomordik L. V. ( 2011 ) Intracellular curvature‐generating proteins in cell‐to‐cell fusion. Biochem. J. 440, 185 – 193.en_US
dc.identifier.citedreferenceRobinson M. S. and Bonifacino J. S. ( 2001 ) Adaptor‐related proteins. Curr. Opin. Cell Biol. 13, 444 – 453.en_US
dc.identifier.citedreferenceSchmid S. L. and Frolov V. A. ( 2011 ) Dynamin: functional design of a membrane fission catalyst. Annu. Rev. Cell Dev. Biol. 27, 79 – 105.en_US
dc.identifier.citedreferenceSong B. D., Leonard M. and Schmid S. L. ( 2004 ) Dynamin GTPase domain mutants that differentially affect GTP binding, GTP hydrolysis, and clathrin‐mediated endocytosis. J. Biol. Chem. 279, 40431 – 40436.en_US
dc.identifier.citedreferenceSund S. E., Swanson J. A. and Axelrod D. ( 1999 ) Cell membrane orientation visualized by polarized total internal reflection fluorescence. Biophys. J. 77, 2266 – 2283.en_US
dc.identifier.citedreferenceTakei K., McPherson P. S., Schmid S. L. and De Camilli P. ( 1995 ) Tubular membrane invaginations coated by dynamin rings are induced by GTP‐gamma S in nerve terminals. Nature 374, 186 – 190.en_US
dc.identifier.citedreferenceTaraska J. W., Perrais D., Ohara‐Imaizumi M., Nagamatsu S. and Almers W. ( 2003 ) Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells. Proc. Nat. Acad. Sci. USA 100, 2070 – 2075.en_US
dc.identifier.citedreferenceTsuboi T. and Rutter G. A. ( 2003 ) Multiple forms of “Kiss‐and‐Run” exocytosis revealed by evanescent wave microscopy. Curr. Biol. 13, 563 – 567.en_US
dc.identifier.citedreferenceTsuboi T., McMahon H. T. and Rutter G. A. ( 2004 ) Mechanisms of dense core vesicle recapture following “Kiss and Run” (“Cavicapture”) exocytosis in insulin‐secreting cells. J. Biol. Chem. 279, 47115 – 47124.en_US
dc.identifier.citedreferenceWang C. T., Grishanin R., Earles C. A., Chang P. Y., Martin T. F. J., Chapman E. R. and Jackson M. B. ( 2001 ) Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense‐core vesicles. Science 294, 1111 – 1115.en_US
dc.identifier.citedreferenceWarnock D. E., Hinshaw J. E. and Schmid S. L. ( 1996 ) Dynamin self‐assembly stimulates its GTPase activity. J. Biol. Chem. 271, 22310 – 22314.en_US
dc.identifier.citedreferenceWitke W., Podtelejnikov A. V., Di Nardo A., Sutherland J. D., Gurniak C. B., Dotti C. and Mann M. ( 1998 ) In mouse brain profilin I and profilin II associate with regulators of the endocytic pathway and actin assembly. EMBO J. 17, 967 – 976.en_US
dc.identifier.citedreferenceWolf D. E. ( 1985 ) Determination of the sidedness of carbocyanine dye labeling of membranes. Biochemistry 24, 582 – 586.en_US
dc.identifier.citedreferenceZhang Z., Wu Y., Wang Z., Dunning F. M., Rehfuss J., Ramanan D., Chapman E. R. and Jackson M. B. ( 2011 ) Release mode of large and small dense‐core vesicles specified by different synaptotagmin isoforms in PC12 cells. Mol. Biol. Cell 22, 2324 – 2336.en_US
dc.identifier.citedreferenceZhou Z., Misler S. and Chow R. H. ( 1996 ) Rapid fluctuations in transmitter release from single vesicles in bovine adrenal chromaffin cells. Biophys. J. 70, 1543 – 1552.en_US
dc.identifier.citedreferenceZimmerberg J., Curran M., Cohen F. S. and Brodwick M. ( 1987 ) Simultaneous electrical and optical measurements show that membrane fusion precedes secretory granule swelling during exocytosis of beige mouse mast cells. Proc. Nat. Acad. Sci. U S A 84, 1585 – 1589.en_US
dc.identifier.citedreferenceAlbillos A. G., Dernick H., Horstmann W., Almers G., Alvarez de Toledo and Lindau M. ( 1997 ) The exocytotic event in chromaffin cells revealed by patch amperometry. Nature 389, 509 – 512.en_US
dc.identifier.citedreferenceAllersma M. W., Wang L., Axelrod D. and Holz R. W. ( 2004 ) Visualization of regulated exocytosis with a granule‐membrane probe using total internal reflection microscopy. Mol. Biol. Cell 15, 4658 – 4668.en_US
dc.identifier.citedreferenceAnantharam A., Axelrod D. and Holz R. W. ( 2010a ) Polarized TIRFM reveals changes in plasma membrane topology before and during granule fusion. Cell. Mol. Neurobiol. 30, 1343 – 1349.en_US
dc.identifier.citedreferenceAnantharam A., Onoa B., Edwards R. H., Holz R. W. and Axelrod D. ( 2010b ) Localized topological changes of the plasma membrane upon exocytosis visualized by polarized TIRFM. J. Cell Biol. 188, 415 – 428.en_US
dc.identifier.citedreferenceAnantharam A., Bittner M. A., Aikman R. L., Stuenkel E. L., Schmid S. L., Axelrod D. and Holz R. W. ( 2011 ) A new role for the dynamin GTPase in the regulation of fusion pore expansion. Mol. Biol. Cell 22, 1907 – 1918.en_US
dc.identifier.citedreferenceArtalejo C. R., Henley J. R., McNivan M. A. and Palfrey H. C. ( 1995 ) Rapid endocytosis coupled to excocytosis in adrenal chromaffin cells involves Ca 2 + , GTP, and dynamin but not clathrin. Proc. Nat. Acad. Sci. U S A 92, 8328 – 8332.en_US
dc.identifier.citedreferenceAxelrod D. ( 1979 ) Carbocyanine dye orientation in red cell membrane studied by microscopic fluorescence polarization. Biophys. J. 26, 557 – 574.en_US
dc.identifier.citedreferenceBashkirov P. V., Akimov S. A., Evseev A. I., Schmid S. L., Zimmerberg J. and Frolov V. A. ( 2008 ) GTPase cycle of dynamin is coupled to membrane squeeze and release, leading to spontaneous fission. Cell 135, 1276 – 1286.en_US
dc.identifier.citedreferenceBerberian K., Torres A. J., Fang Q., Kisler K. and Lindau M. ( 2009 ) F‐Actin and Myosin II accelerate catecholamine release from chromaffin granules. J. Neurosci. 29, 863 – 870.en_US
dc.identifier.citedreferenceBreckenridge L. J. and Almers W. ( 1987a ) Currents through the fusion pore that forms during exocytosis of a secretory vesicle. Nature 328, 814 – 817.en_US
dc.identifier.citedreferenceBreckenridge L. J. and Almers W. ( 1987b ) Final steps in exocytosis observed in a cell with giant secretory granules. Proc. Nat. Acad. Sci. U S A 84, 1945 – 1949.en_US
dc.identifier.citedreferenceDoherty G. J. and McMahon H. T. ( 2009 ) Mechanisms of endocytosis. Annu. Rev. Biochem. 78, 857 – 902.en_US
dc.identifier.citedreferenceDoreian B. W., Fulop T. G. and Smith C. B. ( 2008 ) Myosin II activation and actin reorganization regulate the mode of quantal exocytosis in mouse adrenal chromaffin cells. J. Neurosci. 28, 4470 – 4478.en_US
dc.identifier.citedreferenceEthier M. F., Wolf D. E. and Melchior D. L. ( 1983 ) Calorimetric investigation of the phase partitioning of the fluorescent carbocyanine probes in phosphatidylcholine bilayers. Biochemistry 22, 1178 – 1182.en_US
dc.identifier.citedreferenceFulop T., Radabaugh S. and Smith C. ( 2005 ) Activity‐dependent differential transmitter release in mouse adrenal chromaffin cells. J. Neurosci. 25, 7324 – 7332.en_US
dc.identifier.citedreferenceFulop T., Doreian B. and Smith C. ( 2008 ) Dynamin I plays dual roles in the activity‐dependent shift in exocytic mode in mouse adrenal chromaffin cells. Arch. Biochem. Biophys. 477, 146 – 154.en_US
dc.identifier.citedreferenceGalas M. C., Chasserot‐Golaz S., Dirrig‐Grosch S. and Bader M. F. ( 2000 ) Presence of dynamin‐‐syntaxin complexes associated with secretory granules in adrenal chromaffin cells. J. Neurochem. 75, 1511 – 1519.en_US
dc.identifier.citedreferenceGonzalez‐Jamett A. M., Baez‐Matus X., Hevia M. A., Guerra M. J., Olivares M. J., Martinez A. D., Neely A. and Cardenas A. M. ( 2010 ) The association of dynamin with synaptophysin regulates quantal size and duration of exocytotic events in chromaffin cells. J. Neurosci.: Official J. Soc. Neurosci. 30, 10683 – 10691.en_US
dc.identifier.citedreferenceGraham M. E., O’Callaghan D. W., McMahon H. T. and Burgoyne R. D. ( 2002 ) Dynamin‐dependent and dynamin‐independent processes contribute to the regulation of single vesicle release kinetics and quantal size. Proc. Nat. Acad. Sci. 99, 7124 – 7129.en_US
dc.identifier.citedreferenceGu C., Yaddanapudi S., Weins A., Osborn T., Reiser J., Pollak M., Hartwig J. and Sever S. ( 2010 ) Direct dynamin‐actin interactions regulate the actin cytoskeleton. EMBO J. 29, 3593 – 3606.en_US
dc.identifier.citedreferenceHan X., Wang C. T., Bai J., Chapman E. R. and Jackson M. B. ( 2004 ) Transmembrane segments of syntaxin line the fusion pore of ca 2+ ‐triggered exocytosis. Science 304, 289 – 292.en_US
dc.identifier.citedreferenceHenkel A. W. and Almers W. ( 1996 ) Fast steps in exocytosis and endocytosis studied by capacitance measurements in endocrine cells. Curr. Opin. Neurobiol. 6, 350 – 357.en_US
dc.identifier.citedreferenceHinshaw J. E. and Schmid S. L. ( 1995 ) Dynamin self‐assembles into rings suggesting a mechanism for coated vesicle budding. Nature 374, 190 – 192.en_US
dc.identifier.citedreferenceHolroyd P., Lang T., Wenzel D., De Camilli P. and Jahn R. ( 2002 ) Imaging direct, dynamin‐dependent recapture of fusing secretory granules on plasma membrane lawns from PC12 cells. Proc. Nat. Acad. Sci. 99, 16806 – 16811.en_US
dc.identifier.citedreferenceJaiswal J. K., Rivera V. M. and Simon S. M. ( 2009 ) Exocytosis of post‐Golgi vesicles is regulated by components of the endocytic machinery. Cell 137, 1308 – 1319.en_US
dc.identifier.citedreferenceJuhasz J., Davis J. H. and Sharom F. J. ( 2010 ) Fluorescent probe partitioning in giant unilamellar vesicles of ‘lipid raft’ mixtures. Biochem. J. 430, 415 – 423.en_US
dc.identifier.citedreferenceLam A. D., Tryoen‐Toth P., Tsai B., Vitale N. and Stuenkel E. L. ( 2008 ) SNARE‐catalyzed fusion events are regulated by Syntaxin1A‐lipid interactions. Mol. Biol. Cell 19, 485 – 497.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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