Architecture and dynamic remodelling of the septin cytoskeleton during the cell cycle

被引:109
作者
Ong, Katy [1 ]
Wloka, Carsten [1 ,2 ]
Okada, Satoshi [1 ]
Svitkina, Tatyana [3 ]
Bi, Erfei [1 ]
机构
[1] Univ Penn, Perelman Sch Med, Dept Cell & Dev Biol, Philadelphia, PA 19104 USA
[2] Free Univ Berlin, Inst Biol, D-14195 Berlin, Germany
[3] Univ Penn, Dept Biol, Philadelphia, PA 19104 USA
基金
美国国家卫生研究院;
关键词
SACCHAROMYCES-CEREVISIAE; BUDDING YEAST; CYTOKINESIS; ORGANIZATION; RING; FILAMENTS; PROTEINS; ROLES; MORPHOGENESIS; MICROSCOPY;
D O I
10.1038/ncomms6698
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Septins perform diverse functions through the formation of filaments and higher-order structures. However, the exact architecture of septin structures remains unclear. In the budding yeast Saccharomyces cerevisiae, septins form an 'hourglass' at the mother-bud neck before cytokinesis, which is converted into a 'double ring' during cytokinesis. Here, using platinum-replica electron microscopy, we find that the early hourglass consists of septin double filaments oriented along the mother-bud axis. In the late hourglass, these double filaments are connected by periodic circumferential single filaments on the membrane-proximal side and are associated with centrally located, circumferential, myosin-II thick filaments on the membrane-distal side. The double ring consists of exclusively circumferential septin filaments. Live-cell imaging studies indicate that the hourglass-to-double ring transition is accompanied by loss of septin subunits from the hourglass and reorganization of the remaining subunits into the double ring. This work provides an unparalleled view of septin structures within cells and defines their remodelling dynamics during the cell cycle.
引用
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页数:10
相关论文
共 38 条
[1]   Saccharomyces cerevisiae septins:: Supramolecular organization of heterooligomers and the mechanism of filament assembly [J].
Bertin, Aurelie ;
McMurray, Michael A. ;
Grob, Patricia ;
Park, Sang-Shin ;
Garcia, Galo, III ;
Patanwala, Insiyyah ;
Ng, Ho-leung ;
Alber, Tom ;
Thorner, Jeremy ;
Nogales, Eva .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2008, 105 (24) :8274-8279
[2]   Three-dimensional ultrastructure of the septin filament network in Saccharomyces cerevisiae [J].
Bertin, Aurelie ;
McMurray, Michael A. ;
Piersonb, Jason ;
Thai, Luong ;
McDonald, Kent L. ;
Zehr, Elena A. ;
Garcia, Galo, III ;
Peters, Peter ;
Thorner, Jeremy ;
Nogales, Eva .
MOLECULAR BIOLOGY OF THE CELL, 2012, 23 (03) :423-432
[3]   Phosphatidylinositol-4,5-bisphosphate Promotes Budding Yeast Septin Filament Assembly and Organization [J].
Bertin, Aurelie ;
McMurray, Michael A. ;
Thai, Luong ;
Garcia, Galo, III ;
Votin, Violet ;
Grob, Patricia ;
Allyn, Theresa ;
Thorner, Jeremy ;
Nogales, Eva .
JOURNAL OF MOLECULAR BIOLOGY, 2010, 404 (04) :711-731
[4]   Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis [J].
Bi, E ;
Maddox, P ;
Lew, DJ ;
Salmon, ED ;
McMillan, JN ;
Yeh, E ;
Pringle, JR .
JOURNAL OF CELL BIOLOGY, 1998, 142 (05) :1301-1312
[5]   HIGHLY ORDERED RING OF MEMBRANE-ASSOCIATED FILAMENTS IN BUDDING YEAST [J].
BYERS, B ;
GOETSCH, L .
JOURNAL OF CELL BIOLOGY, 1976, 69 (03) :717-721
[6]   Septins have a dual role in controlling mitotic exit in budding yeast [J].
Castillon, GA ;
Adames, NR ;
Rosello, CH ;
Seidel, HS ;
Longtine, MS ;
Cooper, JA ;
Heil-Chapdelaine, RA .
CURRENT BIOLOGY, 2003, 13 (08) :654-658
[7]   The role of Cdc42p GTPase-activating proteins in assembly of the septin ring in yeast [J].
Caviston, JP ;
Longtine, M ;
Pringle, JR ;
Bi, E .
MOLECULAR BIOLOGY OF THE CELL, 2003, 14 (10) :4051-4066
[8]   Septin filaments exhibit a dynamic, paired organization that is conserved from yeast to mammals [J].
DeMay, Bradley S. ;
Bai, Xiaobo ;
Howard, Louisa ;
Occhipinti, Patricia ;
Meseroll, Rebecca A. ;
Spiliotis, Elias T. ;
Oldenbourg, Rudolf ;
Gladfelter, Amy S. .
JOURNAL OF CELL BIOLOGY, 2011, 193 (06) :1065-1081
[9]   Phosphorylation-dependent regulation of septin dynamics during the cell cycle [J].
Dobbelaere, J ;
Gentry, MS ;
Hallberg, RL ;
Barral, Y .
DEVELOPMENTAL CELL, 2003, 4 (03) :345-357
[10]   Septin functions in organ system physiology and pathology [J].
Dolat, Lee ;
Hu, Qicong ;
Spiliotis, Elias T. .
BIOLOGICAL CHEMISTRY, 2014, 395 (02) :123-141