Role of Microtubules in Fusion of Post-Golgi Vesicles to the Plasma Membrane

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2003 Apr 11

PMID 12686609

Citations 27

Authors

Jan Schmoranzer

Sanford M Simon

Affiliations

Soon will be listed here.

Abstract

Biosynthetic cargo is transported away from the Golgi in vesicles via microtubules. In the cell periphery the vesicles are believed to engage actin and then dock to fusion sites at the plasma membrane. Using dual-color total internal reflection fluorescence microscopy, we observed that microtubules extended within 100 nm of the plasma membrane and post-Golgi vesicles remained on microtubules up to the plasma membrane, even as fusion to the plasma membrane initiated. Disruption of microtubules eliminated the tubular shapes of the vesicles and altered the fusion events: vesicles required multiple fusions to deliver all of their membrane cargo to the plasma membrane. In contrast, the effects of disrupting actin on fusion behavior were subtle. We conclude that microtubules, rather than actin filaments, are the cytoskeletal elements on which post-Golgi vesicles are transported until they fuse to the plasma membrane.

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References

Polishchuk R, Polishchuk E, Marra P, Alberti S, Buccione R, Luini A . Correlative light-electron microscopy reveals the tubular-saccular ultrastructure of carriers operating between Golgi apparatus and plasma membrane. J Cell Biol. 2000; 148(1):45-58. PMC: 2156208. DOI: 10.1083/jcb.148.1.45. View

Brown S . Cooperation between microtubule- and actin-based motor proteins. Annu Rev Cell Dev Biol. 1999; 15:63-80. DOI: 10.1146/annurev.cellbio.15.1.63. View

Schmoranzer J, Goulian M, Axelrod D, Simon S . Imaging constitutive exocytosis with total internal reflection fluorescence microscopy. J Cell Biol. 2000; 149(1):23-32. PMC: 2175105. DOI: 10.1083/jcb.149.1.23. View

Toomre D, Steyer J, Keller P, Almers W, Simons K . Fusion of constitutive membrane traffic with the cell surface observed by evanescent wave microscopy. J Cell Biol. 2000; 149(1):33-40. PMC: 2175107. DOI: 10.1083/jcb.149.1.33. View

Lang T, Wacker I, Wunderlich I, Rohrbach A, Giese G, Soldati T . Role of actin cortex in the subplasmalemmal transport of secretory granules in PC-12 cells. Biophys J. 2000; 78(6):2863-77. PMC: 1300873. DOI: 10.1016/S0006-3495(00)76828-7. View

McNew J, Parlati F, Fukuda R, Johnston R, Paz K, Paumet F . Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature. 2000; 407(6801):153-9. DOI: 10.1038/35025000. View

Lippincott-Schwartz J, Roberts T, Hirschberg K . Secretory protein trafficking and organelle dynamics in living cells. Annu Rev Cell Dev Biol. 2000; 16:557-89. PMC: 4781643. DOI: 10.1146/annurev.cellbio.16.1.557. View

Morris C, Homann U . Cell surface area regulation and membrane tension. J Membr Biol. 2001; 179(2):79-102. DOI: 10.1007/s002320010040. View

Stephens D, Pepperkok R . Illuminating the secretory pathway: when do we need vesicles?. J Cell Sci. 2001; 114(Pt 6):1053-9. DOI: 10.1242/jcs.114.6.1053. View

10.

Zerial M, McBride H . Rab proteins as membrane organizers. Nat Rev Mol Cell Biol. 2001; 2(2):107-17. DOI: 10.1038/35052055. View

11.

Rusan N, Fagerstrom C, Yvon A, Wadsworth P . Cell cycle-dependent changes in microtubule dynamics in living cells expressing green fluorescent protein-alpha tubulin. Mol Biol Cell. 2001; 12(4):971-80. PMC: 32280. DOI: 10.1091/mbc.12.4.971. View

12.

Rudolf R, Salm T, Rustom A, Gerdes H . Dynamics of immature secretory granules: role of cytoskeletal elements during transport, cortical restriction, and F-actin-dependent tethering. Mol Biol Cell. 2001; 12(5):1353-65. PMC: 34589. DOI: 10.1091/mbc.12.5.1353. View

13.

Humeau Y, Doussau F, Vitiello F, Greengard P, Benfenati F, Poulain B . Synapsin controls both reserve and releasable synaptic vesicle pools during neuronal activity and short-term plasticity in Aplysia. J Neurosci. 2001; 21(12):4195-206. PMC: 6762736. View

14.

Seitz A, Kojima H, Oiwa K, Mandelkow E, Song Y, Mandelkow E . Single-molecule investigation of the interference between kinesin, tau and MAP2c. EMBO J. 2002; 21(18):4896-905. PMC: 126299. DOI: 10.1093/emboj/cdf503. View

15.

Huttner W, Schiebler W, Greengard P, De Camilli P . Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J Cell Biol. 1983; 96(5):1374-88. PMC: 2112660. DOI: 10.1083/jcb.96.5.1374. View

16.

Saxton W, Stemple D, Leslie R, Salmon E, Zavortink M, McIntosh J . Tubulin dynamics in cultured mammalian cells. J Cell Biol. 1984; 99(6):2175-86. PMC: 2113582. DOI: 10.1083/jcb.99.6.2175. View

17.

Mitchison T, Kirschner M . Dynamic instability of microtubule growth. Nature. 1984; 312(5991):237-42. DOI: 10.1038/312237a0. View

18.

Schulze E, Kirschner M . Microtubule dynamics in interphase cells. J Cell Biol. 1986; 102(3):1020-31. PMC: 2114101. DOI: 10.1083/jcb.102.3.1020. View

19.

Sammak P, Borisy G . Direct observation of microtubule dynamics in living cells. Nature. 1988; 332(6166):724-6. DOI: 10.1038/332724a0. View

20.

Axelrod D . Total internal reflection fluorescence microscopy. Methods Cell Biol. 1989; 30:245-70. DOI: 10.1016/s0091-679x(08)60982-6. View