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Membrane expansion increases endocytosis rate during mitosis.

Raucher D, Sheetz MP - J. Cell Biol. (1999)

Bottom Line: Mitosis in mammalian cells is accompanied by a dramatic inhibition of endocytosis.We have found that the addition of amphyphilic compounds to metaphase cells increases the endocytosis rate even to interphase levels.Detergents and solvents all increased endocytosis rate, and the extent of increase was in direct proportion to the concentration added.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell Biology, Duke University Medical Center, Durham, North Carolina 27710, USA.

ABSTRACT
Mitosis in mammalian cells is accompanied by a dramatic inhibition of endocytosis. We have found that the addition of amphyphilic compounds to metaphase cells increases the endocytosis rate even to interphase levels. Detergents and solvents all increased endocytosis rate, and the extent of increase was in direct proportion to the concentration added. Although the compounds could produce a variety of different effects, we have found a strong correlation with a physical alteration in the membrane tension as measured by the laser tweezers. Plasma membrane tethers formed by latex beads pull back on the beads with a force that was related to the in-plane bilayer tension and membrane- cytoskeletal adhesion. We found that as cells enter mitosis, the membrane tension rises as the endocytosis rate decreases; and as cells exited mitosis, the endocytosis rate increased as the membrane tension decreased. The addition of amphyphilic compounds decreased membrane tension and increased the endocytosis rate. With the detergent, deoxycholate, the endocytosis rate was restored to interphase levels when the membrane tension was restored to interphase levels. Although biochemical factors are clearly involved in the alterations in mitosis, we suggest that endocytosis is blocked primarily by the increase in apparent plasma membrane tension. Higher tensions inhibit both the binding of the endocytic complex to the membrane and mechanical deformation of the membrane during invagination. We suggest that membrane tension is an important regulator of the endocytosis rate and alteration of tension is sufficient to modify endocytosis rates during mitosis. Further, we postulate that the rise in membrane tension causes cell rounding and the inhibition of motility, characteristic of mitosis.

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Tether force in interphase and mitotic HeLa  cells. (a) Average tether  force in different mitotic  stages. While previous studies of membrane properties  were not capable of resolving  each phase, the laser optical  tweezers enabled us to directly measure tether force in  each cell phase and to follow  the same cell through mitosis.  (b) Tether force in interphase  and metaphase of NIH-3T3  mouse fibroblast cells. Error  bars represents SEM for 10– 25 measurements. (c) Uptake  of FM1-43 labeled vesicles by  interphase and metaphase  cells.
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Figure 4: Tether force in interphase and mitotic HeLa cells. (a) Average tether force in different mitotic stages. While previous studies of membrane properties were not capable of resolving each phase, the laser optical tweezers enabled us to directly measure tether force in each cell phase and to follow the same cell through mitosis. (b) Tether force in interphase and metaphase of NIH-3T3 mouse fibroblast cells. Error bars represents SEM for 10– 25 measurements. (c) Uptake of FM1-43 labeled vesicles by interphase and metaphase cells.

Mentions: As cells entered into mitosis, there was a nearly twofold increase in the static tether force in prometaphase (Fig. 4 a). In metaphase, the tether force peaked at a level threefold greater than interphase cells. With progression through anaphase, the tether force dropped to twice that of interphase. Finally, as cells reached cytokinesis, tether force returned to the interphase value.


Membrane expansion increases endocytosis rate during mitosis.

Raucher D, Sheetz MP - J. Cell Biol. (1999)

Tether force in interphase and mitotic HeLa  cells. (a) Average tether  force in different mitotic  stages. While previous studies of membrane properties  were not capable of resolving  each phase, the laser optical  tweezers enabled us to directly measure tether force in  each cell phase and to follow  the same cell through mitosis.  (b) Tether force in interphase  and metaphase of NIH-3T3  mouse fibroblast cells. Error  bars represents SEM for 10– 25 measurements. (c) Uptake  of FM1-43 labeled vesicles by  interphase and metaphase  cells.
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2132908&req=5

Figure 4: Tether force in interphase and mitotic HeLa cells. (a) Average tether force in different mitotic stages. While previous studies of membrane properties were not capable of resolving each phase, the laser optical tweezers enabled us to directly measure tether force in each cell phase and to follow the same cell through mitosis. (b) Tether force in interphase and metaphase of NIH-3T3 mouse fibroblast cells. Error bars represents SEM for 10– 25 measurements. (c) Uptake of FM1-43 labeled vesicles by interphase and metaphase cells.
Mentions: As cells entered into mitosis, there was a nearly twofold increase in the static tether force in prometaphase (Fig. 4 a). In metaphase, the tether force peaked at a level threefold greater than interphase cells. With progression through anaphase, the tether force dropped to twice that of interphase. Finally, as cells reached cytokinesis, tether force returned to the interphase value.

Bottom Line: Mitosis in mammalian cells is accompanied by a dramatic inhibition of endocytosis.We have found that the addition of amphyphilic compounds to metaphase cells increases the endocytosis rate even to interphase levels.Detergents and solvents all increased endocytosis rate, and the extent of increase was in direct proportion to the concentration added.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell Biology, Duke University Medical Center, Durham, North Carolina 27710, USA.

ABSTRACT
Mitosis in mammalian cells is accompanied by a dramatic inhibition of endocytosis. We have found that the addition of amphyphilic compounds to metaphase cells increases the endocytosis rate even to interphase levels. Detergents and solvents all increased endocytosis rate, and the extent of increase was in direct proportion to the concentration added. Although the compounds could produce a variety of different effects, we have found a strong correlation with a physical alteration in the membrane tension as measured by the laser tweezers. Plasma membrane tethers formed by latex beads pull back on the beads with a force that was related to the in-plane bilayer tension and membrane- cytoskeletal adhesion. We found that as cells enter mitosis, the membrane tension rises as the endocytosis rate decreases; and as cells exited mitosis, the endocytosis rate increased as the membrane tension decreased. The addition of amphyphilic compounds decreased membrane tension and increased the endocytosis rate. With the detergent, deoxycholate, the endocytosis rate was restored to interphase levels when the membrane tension was restored to interphase levels. Although biochemical factors are clearly involved in the alterations in mitosis, we suggest that endocytosis is blocked primarily by the increase in apparent plasma membrane tension. Higher tensions inhibit both the binding of the endocytic complex to the membrane and mechanical deformation of the membrane during invagination. We suggest that membrane tension is an important regulator of the endocytosis rate and alteration of tension is sufficient to modify endocytosis rates during mitosis. Further, we postulate that the rise in membrane tension causes cell rounding and the inhibition of motility, characteristic of mitosis.

Show MeSH
Related in: MedlinePlus