Membrane Tension Inhibits Rapid and Slow Endocytosis in Secretory Cells

被引:39
|
作者
Wu, Xin-Sheng [1 ]
Elias, Sharon [2 ]
Liu, Huisheng [1 ]
Heureaux, Johanna [3 ]
Wen, Peter J. [1 ]
Liu, Allen P. [3 ]
Kozlov, Michael M. [2 ]
Wu, Ling-Gang [1 ]
机构
[1] NINDS, Bldg 36,Rm 4D04, Bethesda, MD 20892 USA
[2] Tel Aviv Univ, Dept Physiol & Pharmacol, Sackler Fac Med, Tel Aviv, Israel
[3] Univ Michigan, Dept Mech Engn, Ann Arbor, MI 48109 USA
基金
美国国家科学基金会; 以色列科学基金会;
关键词
SYNAPTIC VESICLE ENDOCYTOSIS; NERVE-TERMINALS; PLASMA-MEMBRANE; EXOCYTOSIS; FISSION; ACTIN; SHAPE; MECHANISM; SYNAPSES; CALYX;
D O I
10.1016/j.bpj.2017.09.035
中图分类号
Q6 [生物物理学];
学科分类号
071011 ;
摘要
Endocytosis generates spherical or ellipsoid-like vesicles from the plasma membrane, which recycles vesicles that fuse with the plasma member during exocytosis in neurons and endocrine secretory cells. Although tension in the plasma membrane is generally considered to be an important factor in regulating endocytosis, whether membrane tension inhibits or facilitates endocytosis remains debated in the endocytosis field, and has been rarely studied for vesicular endocytosis in secretory cells. Here we report that increasing membrane tension by adjusting osmolarity inhibited both the rapid (a few seconds) and slow (tens of seconds) endocytosis in calyx-type nerve terminals containing conventional active zones and in neuroendocrine chromaffin cells. We address the mechanism of this phenomenon by computational modeling of the energy barrier that the system must overcome at the stage of membrane budding by an assembling protein coat. We show that this barrier grows with increasing tension, which may slow down or prevent membrane budding. These results suggest that in live secretory cells, membrane tension exerts inhibitory action on endocytosis.
引用
收藏
页码:2406 / 2414
页数:9
相关论文
共 50 条
  • [21] Membrane cycling after the excess retrieval mode of rapid endocytosis in mouse chromaffin cells
    Perez Bay, A. E.
    Belingheri, A. V.
    Alvarez, Y. D.
    Marengo, F. D.
    ACTA PHYSIOLOGICA, 2012, 204 (03) : 403 - 418
  • [22] Synaptic vesicle endocytosis: fast and slow modes of membrane retrieval
    Smith, Stephen M.
    Renden, Robert
    von Gersdorff, Henrique
    TRENDS IN NEUROSCIENCES, 2008, 31 (11) : 559 - 568
  • [23] Enhancement of the secretory cycle by glucocorticoid differentiation of PC12 cells: Characteristics of rapid exocytosis and endocytosis.
    Elhamdani, A
    Brown, ME
    Palfrey, CH
    Artalejo, CR
    BIOPHYSICAL JOURNAL, 2000, 78 (01) : 316A - 316A
  • [24] Membrane Mechanics of Endocytosis in Cells with Turgor
    Dmitrieff, S.
    Nedelec, F.
    MOLECULAR BIOLOGY OF THE CELL, 2015, 26
  • [25] Membrane Mechanics of Endocytosis in Cells with Turgor
    Dmitrieff, Serge
    Nedelec, Francois
    PLOS COMPUTATIONAL BIOLOGY, 2015, 11 (10)
  • [26] RAPID SELECTION OF CULTURED-CELLS WITH INCREASED EXPRESSION OF A MEMBRANE MARKER (SECRETORY COMPONENT)
    KVALE, D
    BARTEK, J
    SOLLID, LM
    BRANDTZAEG, P
    INTERNATIONAL JOURNAL OF CANCER, 1988, 42 (04) : 638 - 641
  • [27] Sustained stimulation shifts the mechanism of endocytosis from dynamin-1-dependent rapid endocytosis to clathrin- and dynamin-2-mediated slow endocytosis in chromaffin cells
    Artalejo, CR
    Elhamdani, A
    Palfrey, HC
    PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2002, 99 (09) : 6358 - 6363
  • [28] Rapid and slow endocytosis in calf chromaffin cells are mechanistically distinct and occur in response to different stimulation patterns.
    Artalejo, CR
    Elhamdani, A
    Palfrey, CH
    BIOPHYSICAL JOURNAL, 2000, 78 (01) : 147A - 147A
  • [29] TORC2 controls endocytosis through plasma membrane tension
    Riggi, Margot
    Bourgoint, Clelia
    Macchione, Mariano
    Matile, Stefan
    Loewith, Robbie
    Roux, Aurelien
    JOURNAL OF CELL BIOLOGY, 2019, 218 (07): : 2265 - 2276
  • [30] Rapid Endocytosis and Vesicle Recycling in Neuroendocrine Cells
    Maria Cardenas, Ana
    Marengo, Fernando D.
    CELLULAR AND MOLECULAR NEUROBIOLOGY, 2010, 30 (08) : 1365 - 1370