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PLOS ONE  2014 

A New Role for Myosin II in Vesicle Fission

DOI: 10.1371/journal.pone.0100757

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Abstract:

An endocytic vesicle is formed from a flat plasma membrane patch by a sequential process of invagination, bud formation and fission. The scission step requires the formation of a tubular membrane neck (the fission pore) that connects the endocytic vesicle with the plasma membrane. Progress in vesicle fission can be measured by the formation and closure of the fission pore. Live-cell imaging and sensitive biophysical measurements have provided various glimpses into the structure and behaviour of the fission pore. In the present study, the role of non-muscle myosin II (NM-2) in vesicle fission was tested by analyzing the kinetics of the fission pore with perforated-patch clamp capacitance measurements to detect single vesicle endocytosis with millisecond time resolution in peritoneal mast cells. Blebbistatin, a specific inhibitor of NM-2, dramatically increased the duration of the fission pore and also prevented closure during large endocytic events. Using the fluorescent markers FM1-43 and pHrodo Green dextran, we found that NM-2 inhibition greatly arrested vesicle fission in a late phase of the scission event when the pore reached a final diameter of ~ 5 nm. Our results indicate that loss of the ATPase activity of myosin II drastically reduces the efficiency of membrane scission by making vesicle closure incomplete and suggest that NM-2 might be especially relevant in vesicle fission during compound endocytosis.

References

[1]  Metcalfe DD, Baram D, Mekori YA (1997) Mast cells. Physiol Rev 77: 1033–79.
[2]  Alvarez de Toledo G, Fernandez JM (1990) Compound versus multigranular exocytosis in peritoneal mast cells. J Gen Physiol 95: 397–409. doi: 10.1085/jgp.95.3.397
[3]  Rohlich P, Anderson P, Uvnas B (1971) Electron microscope observations on compounds 48-80-induced degranulation in rat mast cells. Evidence for sequential exocytosis of storage granules. J Cell Biol 51: 465–83. doi: 10.1083/jcb.51.2.465
[4]  Cabeza JM, Acosta J, Ales E (2013) Mechanisms of granule membrane recapture following exocytosis in intact mast cells. J Biol Chem 288: 20293–305. doi: 10.1074/jbc.m113.459065
[5]  Kaksonen M, Toret CP, Drubin DG (2006) Harnessing actin dynamics for clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 7: 404–14. doi: 10.1038/nrm1940
[6]  Galletta BJ, Mooren OL, Cooper JA (2010) Actin dynamics and endocytosis in yeast and mammals. Curr Opin Biotechnol 21: 604–10. doi: 10.1016/j.copbio.2010.06.006
[7]  Taylor MJ, Lampe M, Merrifield CJ (2012) A feedback loop between dynamin and actin recruitment during clathrin-mediated endocytosis. PLoS Biol 10: e1001302. doi: 10.1371/journal.pbio.1001302
[8]  Merrifield CJ, Porrais D, Zenisek D (2005) Direct visualization of single membrane scission events at clathrin-coated pits using a novel optical assay and evanescent field microscopy. Microsc Microanal 11 Suppl 2240–1. doi: 10.1017/s1431927605505282
[9]  Yarar D, Waterman-Storer CM, Schmid SL (2005) A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol Biol Cell 16: 964–75. doi: 10.1091/mbc.e04-09-0774
[10]  Yao LH, Rao Y, Bang C, Kurilova S, Varga K, et al. (2013) Actin polymerization does not provide direct mechanical forces for vesicle fission during clathrin-mediated endocytosis. J Neurosci 33: 15793–8. doi: 10.1523/jneurosci.2171-13.2013
[11]  Neco P, Giner D, Viniegra S, Borges R, Villarroel A, et al. (2004) New roles of myosin II during vesicle transport and fusion in chromaffin cells. J Biol Chem 279: 27450–7. doi: 10.1074/jbc.m311462200
[12]  Neco P, Fernandez-Peruchena C, Navas S, Gutierrez LM, de Toledo GA, et al. (2008) Myosin II contributes to fusion pore expansion during exocytosis. J Biol Chem 283: 10949–57. doi: 10.1074/jbc.m709058200
[13]  Doreian BW, Fulop TG, Smith CB (2008) Myosin II activation and actin reorganization regulate the mode of quantal exocytosis in mouse adrenal chromaffin cells. J Neurosci 28: 4470–8. doi: 10.1523/jneurosci.0008-08.2008
[14]  Berberian K, Torres AJ, Fang Q, Kisler K, Lindau M (2009) F-actin and myosin II accelerate catecholamine release from chromaffin granules. J Neurosci 29: 863–70. doi: 10.1523/jneurosci.2818-08.2009
[15]  Gutierrez LM (2012) New insights into the role of the cortical cytoskeleton in exocytosis from neuroendocrine cells. Int Rev Cell Mol Biol 295: 109–37. doi: 10.1016/b978-0-12-394306-4.00009-5
[16]  Miserey-Lenkei S, Chalancon G, Bardin S, Formstecher E, Goud B, et al. (2010) Rab and actomyosin-dependent fission of transport vesicles at the Golgi complex. Nat Cell Biol 12: 645–54. doi: 10.1038/ncb2067
[17]  Chandrasekar I, Huettner JE, Turney SG, Bridgman PC (2013) Myosin II regulates activity dependent compensatory endocytosis at central synapses. J Neurosci 33: 16131–45. doi: 10.1523/jneurosci.2229-13.2013
[18]  Yue HY, Xu J (2014) Myosin light chain kinase accelerates vesicle endocytosis at the calyx of held synapse. J Neurosci 34: 295–304. doi: 10.1523/jneurosci.3744-13.2014
[19]  Artalejo CR, Elhamdani A, Palfrey HC (2002) Sustained stimulation shifts the mechanism of endocytosis from dynamin-1-dependent rapid endocytosis to clathrin- and dynamin-2-mediated slow endocytosis in chromaffin cells. Proc Natl Acad Sci U S A 99: 6358–63. doi: 10.1073/pnas.082658499
[20]  Taraska JW, Perrais D, Ohara-Imaizumi M, Nagamatsu S, Almers W (2003) Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells. Proc Natl Acad Sci U S A 100: 2070–5. doi: 10.1073/pnas.0337526100
[21]  Perrais D, Kleppe IC, Taraska JW, Almers W (2004) Recapture after exocytosis causes differential retention of protein in granules of bovine chromaffin cells. J Physiol 560: 413–28. doi: 10.1113/jphysiol.2004.064410
[22]  Fulop T, Radabaugh S, Smith C (2005) Activity-dependent differential transmitter release in mouse adrenal chromaffin cells. J Neurosci 25: 7324–32. doi: 10.1523/jneurosci.2042-05.2005
[23]  Straight AF, Cheung A, Limouze J, Chen I, Westwood NJ, et al. (2003) Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 299: 1743–7. doi: 10.1126/science.1081412
[24]  Kovacs M, Toth J, Hetenyi C, Malnasi-Csizmadia A, Sellers JR (2004) Mechanism of blebbistatin inhibition of myosin II. J Biol Chem 279: 35557–63. doi: 10.1074/jbc.m405319200
[25]  Breckenridge LJ, Almers W (1987) Currents through the fusion pore that forms during exocytosis of a secretory vesicle. Nature 328: 814–7. doi: 10.1038/328814a0
[26]  Spruce AE, Breckenridge LJ, Lee AK, Almers W (1990) Properties of the fusion pore that forms during exocytosis of a mast cell secretory vesicle. Neuron 4: 643–54. doi: 10.1016/0896-6273(90)90192-i
[27]  Aoki R, Kitaguchi T, Oya M, Yanagihara Y, Sato M, et al. (2010) Duration of fusion pore opening and the amount of hormone released are regulated by myosin II during kiss-and-run exocytosis. Biochem J 429: 497–504. doi: 10.1042/bj20091839
[28]  Cabeza JM, Acosta J, Ales E (2010) Dynamics and regulation of endocytotic fission pores: role of calcium and dynamin. Traffic 11: 1579–90. doi: 10.1111/j.1600-0854.2010.01120.x
[29]  Angleson JK, Cochilla AJ, Kilic G, Nussinovitch I, Betz WJ (1999) Regulation of dense core release from neuroendocrine cells revealed by imaging single exocytic events. Nat Neurosci 2: 440–6. doi: 10.1038/8107
[30]  Cochilla AJ, Angleson JK, Betz WJ (1999) Monitoring secretory membrane with FM1-43 fluorescence. Annu Rev Neurosci 22: 1–10. doi: 10.1146/annurev.neuro.22.1.1
[31]  Brumback AC, Lieber JL, Angleson JK, Betz WJ (2004) Using FM1-43 to study neuropeptide granule dynamics and exocytosis. Methods 33: 287–94. doi: 10.1016/j.ymeth.2004.01.002
[32]  Cochilla AJ, Angleson JK, Betz WJ (2000) Differential regulation of granule-to-granule and granule-to-plasma membrane fusion during secretion from rat pituitary lactotrophs. J Cell Biol 150: 839–48. doi: 10.1083/jcb.150.4.839
[33]  Wu Y, Ma L, Cheley S, Bayley H, Cui Q, et al. (2011) Permeation of styryl dyes through nanometer-scale pores in membranes. Biochemistry 50: 7493–502. doi: 10.1021/bi2006288
[34]  Babich V, Meli A, Knipe L, Dempster JE, Skehel P, et al. (2008) Selective release of molecules from Weibel-Palade bodies during a lingering kiss. Blood 111: 5282–90. doi: 10.1182/blood-2007-09-113746
[35]  Yu HY, Bement WM (2007) Multiple myosins are required to coordinate actin assembly with coat compression during compensatory endocytosis. Mol Biol Cell 18: 4096–105. doi: 10.1091/mbc.e06-11-0993
[36]  Merrifield CJ, Moss SE, Ballestrem C, Imhof BA, Giese G, et al. (1999) Endocytic vesicles move at the tips of actin tails in cultured mast cells. Nat Cell Biol 1: 72–4.
[37]  Gu C, Yaddanapudi S, Weins A, Osborn T, Reiser J, et al. (2010) Direct dynamin-actin interactions regulate the actin cytoskeleton. Embo J 29: 3593–606. doi: 10.1038/emboj.2010.249
[38]  Henkel AW, Meiri H, Horstmann H, Lindau M, Almers W (2000) Rhythmic opening and closing of vesicles during constitutive exo- and endocytosis in chromaffin cells. Embo J 19: 84–93. doi: 10.1093/emboj/19.1.84
[39]  Benesch S, Polo S, Lai FP, Anderson KI, Stradal TE, et al. (2005) N-WASP deficiency impairs EGF internalization and actin assembly at clathrin-coated pits. J Cell Sci 118: 3103–15. doi: 10.1242/jcs.02444
[40]  Merrifield CJ, Feldman ME, Wan L, Almers W (2002) Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4: 691–8. doi: 10.1038/ncb837
[41]  Spudich G, Chibalina MV, Au JS, Arden SD, Buss F, et al. (2007) Myosin VI targeting to clathrin-coated structures and dimerization is mediated by binding to Disabled-2 and PtdIns(4,5)P2. Nat Cell Biol 9: 176–83. doi: 10.1038/ncb1531
[42]  Krendel M, Osterweil EK, Mooseker MS (2007) Myosin 1E interacts with synaptojanin-1 and dynamin and is involved in endocytosis. FEBS Lett 581: 644–50. doi: 10.1016/j.febslet.2007.01.021
[43]  Bananis E, Nath S, Gordon K, Satir P, Stockert RJ, et al. (2004) Microtubule-dependent movement of late endocytic vesicles in vitro: requirements for Dynein and Kinesin. Mol Biol Cell 15: 3688–97. doi: 10.1091/mbc.e04-04-0278
[44]  Chandrasekar I, Goeckeler ZM, Turney SG, Wang P, Wysolmerski RB, et al.. (2014) Nonmuscle Myosin II is a Critical Regulator of Clathrin Mediated Endocytosis. Traffic.
[45]  Alvarez de Toledo G, Fernandez-Chacon R, Fernandez JM (1993) Release of secretory products during transient vesicle fusion. Nature 363: 554–8. doi: 10.1038/363554a0
[46]  Bhat P, Thorn P (2009) Myosin 2 maintains an open exocytic fusion pore in secretory epithelial cells. Mol Biol Cell 20: 1795–803. doi: 10.1091/mbc.e08-10-1048
[47]  Monck JR, Alvarez de Toledo G, Fernandez JM (1990) Tension in secretory granule membranes causes extensive membrane transfer through the exocytotic fusion pore. Proc Natl Acad Sci U S A 87: 7804–8. doi: 10.1073/pnas.87.20.7804
[48]  Fawcett DW (1954) Cytological and pharmacological observations on the release of histamine by mast cells. J Exp Med 100: 217–24. doi: 10.1084/jem.100.2.217
[49]  Kobayashi S, Kojidani T, Osakada H, Yamamoto A, Yoshimori T, et al. (2010) Artificial induction of autophagy around polystyrene beads in nonphagocytic cells. Autophagy 6: 36–45. doi: 10.4161/auto.6.1.10324
[50]  Chen M, Van Hook MJ, Zenisek D, Thoreson WB (2013) Properties of ribbon and non-ribbon release from rod photoreceptors revealed by visualizing individual synaptic vesicles. J Neurosci 33: 2071–86. doi: 10.1523/jneurosci.3426-12.2013
[51]  Debus K, Lindau M (2000) Resolution of patch capacitance recordings and of fusion pore conductances in small vesicles. Biophys J 78: 2983–97. doi: 10.1016/s0006-3495(00)76837-8
[52]  Lollike K, Lindau M (1999) Membrane capacitance techniques to monitor granule exocytosis in neutrophils. J Immunol Methods 232: 111–20. doi: 10.1016/s0022-1759(99)00169-6
[53]  Neher E, Marty A (1982) Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc Natl Acad Sci U S A 79: 6712–6. doi: 10.1073/pnas.79.21.6712
[54]  Lindau M, Neher E (1988) Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflugers Arch 411: 137–46. doi: 10.1007/bf00582306
[55]  Rosenboom H, Lindau M (1994) Exo-endocytosis and closing of the fission pore during endocytosis in single pituitary nerve terminals internally perfused with high calcium concentrations. Proc Natl Acad Sci U S A 91: 5267–71. doi: 10.1073/pnas.91.12.5267

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