A Comparative Analysis of Spindle Morphometrics across Metazoans

被引:76
作者
Crowder, Marina E. [1 ]
Strzelecka, Magdalena [1 ]
Wilbur, Jeremy D. [1 ]
Good, Matthew C. [1 ]
von Dassow, George [2 ]
Heald, Rebecca [1 ]
机构
[1] Univ Calif Berkeley, Dept Mol & Cellular Biol, Berkeley, CA 94720 USA
[2] Oregon Inst Marine Biol, Charleston, OR 97420 USA
关键词
MITOTIC SPINDLE; CENTROSOME REDUCTION; CYTOPLASMIC VOLUME; MEIOTIC SPINDLE; ELEGANS EMBRYOS; MOUSE OOCYTES; IN-VITRO; LENGTH; MICROTUBULE; SIZE;
D O I
10.1016/j.cub.2015.04.036
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Cell division in all eukaryotes depends on function of the spindle, a microtubule-based structure that segregates chromosomes to generate daughter cells in mitosis or haploid gametes in meiosis. Spindle size adapts to changes in cell size and shape, which vary dramatically across species and within a multicellular organism, but the nature of scaling events and their underlying mechanisms are poorly understood. Cell size variations are most pronounced in early animal development, as egg diameters range from tens of microns up to millimeters across animal phyla, and decrease several orders of magnitude during rapid reductive divisions. During early embryogenesis in the model organisms X. laevis and C. elegans, the spindle scales with cell size [1, 2], a phenomenon regulated by molecules that modulate microtubule dynamics [3-6], as well as by limiting cytoplasmic volume [7, 8]. However, it is not known to what extent spindle scaling is conserved across organisms and among different cell types. Here we show that in a range of metazoan phyla, mitotic spindle length decreased with cell size across an similar to 30-fold difference in zygote size. Maximum spindle length varied, but linear spindle scaling occurred similarly in all species once embryonic cell diameter reduced to 140 mm. In contrast, we find that the female meiotic spindle does not scale as closely to egg size, adopting a more uniform size across species that most likely reflects its specialized function. Our analysis reveals that spindle morphometrics change abruptly, within one cell cycle, at the transition from meiosis to mitosis in most animals.
引用
收藏
页码:1542 / 1550
页数:9
相关论文
共 38 条
  • [1] Conserved Functions for Mos in Eumetazoan Oocyte Maturation Revealed by Studies in a Cnidarian
    Amiel, Aldine
    Leclere, Lucas
    Robert, Lucie
    Chevalier, Sandra
    Houliston, Evelyn
    [J]. CURRENT BIOLOGY, 2009, 19 (04) : 305 - 311
  • [2] MICROTUBULE CONFIGURATIONS IN OOCYTES, ZYGOTES, AND EARLY EMBRYOS OF A MARSUPIAL, MONODELPHIS-DOMESTICA
    BREED, WG
    SIMERLY, C
    NAVARA, CS
    VANDEBERG, JL
    SCHATTEN, G
    [J]. DEVELOPMENTAL BIOLOGY, 1994, 164 (01) : 230 - 240
  • [3] Kinetochore fibers are not involved in the formation of the first meiotic spindle in mouse oocytes, but control the exit from the first meiotic M phase
    Brunet, S
    Maria, AS
    Guillaud, P
    Dujardin, D
    Kubiak, JZ
    Maro, B
    [J]. JOURNAL OF CELL BIOLOGY, 1999, 146 (01) : 1 - 11
  • [4] Meiotic Regulation of TPX2 Protein Levels Governs Cell Cycle Progression in Mouse Oocytes
    Brunet, Stephane
    Dumont, Julien
    Lee, Karen W.
    Kinoshita, Kazuhisa
    Hikal, Pascale
    Gruss, Oliver J.
    Maro, Bernard
    Verlhac, Marie-Helene
    [J]. PLOS ONE, 2008, 3 (10):
  • [5] Mechanistic foundations of the metaphase II spindle of human oocytes matured in vivo and in vitro
    Coticchio, Giovanni
    Guglielmo, Maria Cristina
    Dal Canto, Mariabeatrice
    Fadini, Rubens
    Renzini, Mario Mignini
    De Ponti, Elena
    Brambillasca, Fausta
    Albertini, David F.
    [J]. HUMAN REPRODUCTION, 2013, 28 (12) : 3271 - 3282
  • [6] The transition from meiotic to mitotic spindle assembly is gradual during early mammalian development
    Courtois, Aurelien
    Schuh, Melina
    Ellenberg, Jan
    Hiiragi, Takashi
    [J]. JOURNAL OF CELL BIOLOGY, 2012, 198 (03) : 357 - 370
  • [7] Limiting Amounts of Centrosome Material Set Centrosome Size in C. elegans Embryos
    Decker, Markus
    Jaensch, Steffen
    Pozniakovsky, Andrei
    Zinke, Andrea
    O'Connell, Kevin F.
    Zachariae, Wolfgang
    Myers, Eugene
    Hyman, Anthony A.
    [J]. CURRENT BIOLOGY, 2011, 21 (15) : 1259 - 1267
  • [8] The maternal-effect gene futile cycle is essential for pronuclear congression and mitotic spindle assembly in the zebrafish zygote
    Dekens, MPS
    Pelegri, FJ
    Maischein, HM
    Nüsslein-Volhard, C
    [J]. DEVELOPMENT, 2003, 130 (17): : 3907 - 3916
  • [9] Variations of chromatin, tubulin and actin structures in primate oocytes arrested during in vitro maturation and fertilization-what is this telling us about the relationships between cytoskeletal and chromatin meiotic defects?
    Delimitreva, S.
    Tkachenko, O. Y.
    Berenson, A.
    Nayudu, P. L.
    [J]. THERIOGENOLOGY, 2012, 77 (07) : 1297 - 1311
  • [10] Chromatin Shapes the Mitotic Spindle
    Dinarina, Ana
    Pugieux, Celine
    Corral, Maria Mora
    Loose, Martin
    Spatz, Joachim
    Karsenti, Eric
    Nedelec, Francois
    [J]. CELL, 2009, 138 (03) : 502 - 513