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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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Model for regulation of endocytosis during mitosis.  The formation of endocytic vesicles requires substantial force to  bend the membrane and to overcome the membrane tension.  The magnitude of membrane tension is denoted by the thickness  of the arrow and endocytosis is represented by the small vesicles  inside the cell. Low membrane tension in interphase allows bending of the membrane, formation of endocytic vesicles and endocytosis proceed. During the transition from interphase to mitosis membrane tension increases dramatically preventing the  invagination of endocytic vesicles and resulting in inhibition of  endocytosis. However, as shown in this study, if the membrane  tension in mitotic cells is decreased to interphase levels by addition of tension reducing reagents, endocytosis is restored to interphase levels.
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Figure 8: Model for regulation of endocytosis during mitosis. The formation of endocytic vesicles requires substantial force to bend the membrane and to overcome the membrane tension. The magnitude of membrane tension is denoted by the thickness of the arrow and endocytosis is represented by the small vesicles inside the cell. Low membrane tension in interphase allows bending of the membrane, formation of endocytic vesicles and endocytosis proceed. During the transition from interphase to mitosis membrane tension increases dramatically preventing the invagination of endocytic vesicles and resulting in inhibition of endocytosis. However, as shown in this study, if the membrane tension in mitotic cells is decreased to interphase levels by addition of tension reducing reagents, endocytosis is restored to interphase levels.

Mentions: In previous analyses, the relationship between tether force and apparent membrane tension was established. The two components of membrane tension, bilayer in-plane tension, and membrane-cytoskeleton adhesion are linked for animal cells because the adhesive forces mold the shape of the membrane to the cytoskeleton (see Sheetz and Dai, 1996 for further clarification). We consequently suggest a very simple model for regulation of endocytosis during mitosis (see Fig. 8). Relatively low membrane tension in interphase cells allows rapid invagination of vesicles. During the transition from interphase to mitosis, membrane tension increases dramatically preventing the invagination of endocytic vesicles. However, endocytosis in mitotic cells may be restored by reducing the membrane tension with membrane expanding reagents, indicating that membrane tension is an important factor in regulating cellular endocytosis rate.


Membrane expansion increases endocytosis rate during mitosis.

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

Model for regulation of endocytosis during mitosis.  The formation of endocytic vesicles requires substantial force to  bend the membrane and to overcome the membrane tension.  The magnitude of membrane tension is denoted by the thickness  of the arrow and endocytosis is represented by the small vesicles  inside the cell. Low membrane tension in interphase allows bending of the membrane, formation of endocytic vesicles and endocytosis proceed. During the transition from interphase to mitosis membrane tension increases dramatically preventing the  invagination of endocytic vesicles and resulting in inhibition of  endocytosis. However, as shown in this study, if the membrane  tension in mitotic cells is decreased to interphase levels by addition of tension reducing reagents, endocytosis is restored to interphase levels.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 8: Model for regulation of endocytosis during mitosis. The formation of endocytic vesicles requires substantial force to bend the membrane and to overcome the membrane tension. The magnitude of membrane tension is denoted by the thickness of the arrow and endocytosis is represented by the small vesicles inside the cell. Low membrane tension in interphase allows bending of the membrane, formation of endocytic vesicles and endocytosis proceed. During the transition from interphase to mitosis membrane tension increases dramatically preventing the invagination of endocytic vesicles and resulting in inhibition of endocytosis. However, as shown in this study, if the membrane tension in mitotic cells is decreased to interphase levels by addition of tension reducing reagents, endocytosis is restored to interphase levels.
Mentions: In previous analyses, the relationship between tether force and apparent membrane tension was established. The two components of membrane tension, bilayer in-plane tension, and membrane-cytoskeleton adhesion are linked for animal cells because the adhesive forces mold the shape of the membrane to the cytoskeleton (see Sheetz and Dai, 1996 for further clarification). We consequently suggest a very simple model for regulation of endocytosis during mitosis (see Fig. 8). Relatively low membrane tension in interphase cells allows rapid invagination of vesicles. During the transition from interphase to mitosis, membrane tension increases dramatically preventing the invagination of endocytic vesicles. However, endocytosis in mitotic cells may be restored by reducing the membrane tension with membrane expanding reagents, indicating that membrane tension is an important factor in regulating cellular 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