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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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Relative tether force and relative endocytosis rate in  interphase and metaphase cells for: (a) different concentrations  of deoxycholate; (b) different concentrations of deoxycholate,  DMSO, ethanol, and cells arrested with taxol or vinblastine.  Tether force and endocytosis rate are expressed as a percentage  of the value of interphase cells. Line represents linear least  square fit of the data points.
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Figure 7: Relative tether force and relative endocytosis rate in interphase and metaphase cells for: (a) different concentrations of deoxycholate; (b) different concentrations of deoxycholate, DMSO, ethanol, and cells arrested with taxol or vinblastine. Tether force and endocytosis rate are expressed as a percentage of the value of interphase cells. Line represents linear least square fit of the data points.

Mentions: To further clarify the relationship between tether force and endocytosis we have plotted relative tether force and relative endocytosis rate in for different concentrations of deoxycholate, DMSO, ethanol, and cells arrested with taxol or vinblastine. With different concentrations of deoxycholate there is a linear correlation between membrane endocytosis rate and tether force for both mitotic and interphase cells (Fig. 7 a; R2 = 0.95). When we plot the values for the other conditions on the same graph (Fig. 7 b), there is more scatter but the linear correlation is still very good (R2 = 0.82). The major deviation from the linear trend is DMSO. DMSO is known to affect actin polymerization (Sanger et al., 1980), which may explain higher inhibition of endocytosis rate in that case. We conclude that there is a roughly linear correlation between membrane tension and endocytosis rate in both metaphase and interphase cells. Different agents are expected to have different secondary effects on cell endocytosis which may cause greater scatter in the plot and indicates that other factors than membrane tension can significantly affect endocytosis rate.


Membrane expansion increases endocytosis rate during mitosis.

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

Relative tether force and relative endocytosis rate in  interphase and metaphase cells for: (a) different concentrations  of deoxycholate; (b) different concentrations of deoxycholate,  DMSO, ethanol, and cells arrested with taxol or vinblastine.  Tether force and endocytosis rate are expressed as a percentage  of the value of interphase cells. Line represents linear least  square fit of the data points.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 7: Relative tether force and relative endocytosis rate in interphase and metaphase cells for: (a) different concentrations of deoxycholate; (b) different concentrations of deoxycholate, DMSO, ethanol, and cells arrested with taxol or vinblastine. Tether force and endocytosis rate are expressed as a percentage of the value of interphase cells. Line represents linear least square fit of the data points.
Mentions: To further clarify the relationship between tether force and endocytosis we have plotted relative tether force and relative endocytosis rate in for different concentrations of deoxycholate, DMSO, ethanol, and cells arrested with taxol or vinblastine. With different concentrations of deoxycholate there is a linear correlation between membrane endocytosis rate and tether force for both mitotic and interphase cells (Fig. 7 a; R2 = 0.95). When we plot the values for the other conditions on the same graph (Fig. 7 b), there is more scatter but the linear correlation is still very good (R2 = 0.82). The major deviation from the linear trend is DMSO. DMSO is known to affect actin polymerization (Sanger et al., 1980), which may explain higher inhibition of endocytosis rate in that case. We conclude that there is a roughly linear correlation between membrane tension and endocytosis rate in both metaphase and interphase cells. Different agents are expected to have different secondary effects on cell endocytosis which may cause greater scatter in the plot and indicates that other factors than membrane tension can significantly affect endocytosis rate.

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