Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton

Dorothy I. Mundy, Thomas Machleidt, Yun Shu Ying, Richard G W Anderson, George S. Bloom

Research output: Contribution to journalArticle

239 Citations (Scopus)

Abstract

Live cell, time-lapse microscopy was used to study trafficking of caveolin-1-GFP in stably expressing CHO cells. Multiple cytological and biochemical tests verified that caveolin-1-GFP was a reliable marker for endogenous caveolin-1. At steady state, most caveolin-1-GFP was either at the cell surface associated with invaginated caveolae or near the centrosome in caveosomes. Live cell fluorescence imaging indicated that while much of the caveolin-1-GFP in caveolae at the cell surface was relatively sessile, numerous, highly motile caveolin-1-GFP-positive vesicles were present within the cell interior. These vesicles moved at speeds ranging from 0.3-2 μm/second and movement was abolished when microtubules were depolymerized with nocodazole. In the absence of microtubules, cell surface invaginated caveolae increased more than twofold and they became organized into linear arrays. Complete depolymerization of the actin cytoskeleton with latrunculin A, by contrast, triggered rapid and massive movements of caveolin-positive structures towards the centrosomal region of the cell. The caveolar membrane system of CHO cells therefore appears to be comprised of three caveolin-1-containing compartments. These include caveolae that are confined to the cell surface by cortical actin filaments, the peri-centrosomal caveosomes and caveolar vesicles, which we call 'cavicles', that move constitutively and bi-directionally along microtubules between the cell surface and caveosomes. The behavior of cavicles suggests that they function as transport intermediates between caveolae and caveosomes.

Original languageEnglish (US)
Pages (from-to)4327-4339
Number of pages13
JournalJournal of Cell Science
Volume115
Issue number22
DOIs
StatePublished - Nov 15 2002

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Caveolin 1
Actin Cytoskeleton
Microtubules
Caveolae
Membranes
CHO Cells
Caveolins
Nocodazole
Centrosome
Optical Imaging
Microscopy

Keywords

  • Caveolae
  • Caveolin
  • Caveosome
  • Recycling endosome

ASJC Scopus subject areas

  • Cell Biology

Cite this

Mundy, D. I., Machleidt, T., Ying, Y. S., Anderson, R. G. W., & Bloom, G. S. (2002). Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton. Journal of Cell Science, 115(22), 4327-4339. https://doi.org/10.1242/jcs.00117

Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton. / Mundy, Dorothy I.; Machleidt, Thomas; Ying, Yun Shu; Anderson, Richard G W; Bloom, George S.

In: Journal of Cell Science, Vol. 115, No. 22, 15.11.2002, p. 4327-4339.

Research output: Contribution to journalArticle

Mundy, DI, Machleidt, T, Ying, YS, Anderson, RGW & Bloom, GS 2002, 'Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton', Journal of Cell Science, vol. 115, no. 22, pp. 4327-4339. https://doi.org/10.1242/jcs.00117
Mundy, Dorothy I. ; Machleidt, Thomas ; Ying, Yun Shu ; Anderson, Richard G W ; Bloom, George S. / Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton. In: Journal of Cell Science. 2002 ; Vol. 115, No. 22. pp. 4327-4339.
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