Distinct mechanisms eliminate mother and daughter centrioles in meiosis of starfish oocytes

被引:41
作者
Borrego-Pinto, Joana [1 ]
Somogyi, Kalman [1 ]
Karreman, Matthia A. [1 ]
Koenig, Julia [2 ]
Mueller-Reichert, Thomas [2 ]
Bettencourt-Dias, Monica [3 ]
Goenczy, Pierre [4 ]
Schwab, Yannick [1 ]
Lenart, Peter [1 ]
机构
[1] European Mol Biol Lab, Cell Biol & Biophys Unit, D-69117 Heidelberg, Germany
[2] Tech Univ Dresden, Expt Ctr, Med Fac Carl Gustav Carus, D-01307 Dresden, Germany
[3] Inst Gulbenkian Ciencias, P-2780156 Oeiras, Portugal
[4] Swiss Fed Inst Technol, Swiss Inst Expt Canc Res, Sch Life Sci, CH-1015 Lausanne, Switzerland
关键词
POLAR BODY EXTRUSION; CENTROSOME INHERITANCE; CAENORHABDITIS-ELEGANS; MATERNAL CENTROSOME; GERMINAL VESICLE; CELL-CYCLE; RNA-SEQ; CILIA; FERTILIZATION; MATURATION;
D O I
10.1083/jcb.201510083
中图分类号
Q2 [细胞生物学];
学科分类号
071013 [干细胞生物学];
摘要
Centriole elimination is an essential process that occurs in female meiosis of metazoa to reset centriole number in the zygote at fertilization. How centrioles are eliminated remains poorly understood. Here we visualize the entire elimination process live in starfish oocytes. Using specific fluorescent markers, we demonstrate that the two older, mother centrioles are selectively removed from the oocyte by extrusion into polar bodies. We show that this requires specific positioning of the second meiotic spindle, achieved by dynein-driven transport, and anchorage of the mother centriole to the plasma membrane via mother-specific appendages. In contrast, the single daughter centriole remaining in the egg is eliminated before the first embryonic cleavage. We demonstrate that these distinct elimination mechanisms are necessary because if mother centrioles are artificially retained, they cannot be inactivated, resulting in multipolar zygotic spindles. Thus, our findings reveal a dual mechanism to eliminate centrioles: mothers are physically removed, whereas daughters are eliminated in the cytoplasm, preparing the egg for fertilization.
引用
收藏
页码:815 / 827
页数:13
相关论文
共 69 条
[1]
Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans [J].
Albertson, Donna G. ;
Thomson, J. Nichol .
CHROMOSOME RESEARCH, 1993, 1 (01) :15-26
[2]
BASIC LOCAL ALIGNMENT SEARCH TOOL [J].
ALTSCHUL, SF ;
GISH, W ;
MILLER, W ;
MYERS, EW ;
LIPMAN, DJ .
JOURNAL OF MOLECULAR BIOLOGY, 1990, 215 (03) :403-410
[3]
Centrosomes as signalling centres [J].
Arquint, Christian ;
Gabryjonczyk, Anna-Maria ;
Nigg, Erich A. .
PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 2014, 369 (1650)
[4]
SUBCELLULAR-DISTRIBUTION OF ASTER-NUCLEATED MICROTUBULE LENGTH - A MORE-OR-LESS MITOTIC STATUS OF CYTOPLASMIC AREAS DURING MEIOSIS-I OF STARFISH OOCYTES [J].
BARAKAT, H ;
GENEVIEREGARRIGUES, AM ;
SCHATT, P ;
PICARD, A .
BIOLOGY OF THE CELL, 1994, 81 (03) :205-213
[5]
Deconstructing the centriole: structure and number control [J].
Brito, Daniela A. ;
Gouveia, Susana Montenegro ;
Bettencourt-Dias, Monica .
CURRENT OPINION IN CELL BIOLOGY, 2012, 24 (01) :4-13
[6]
Chibby promotes ciliary vesicle formation and basal body docking during airway cell differentiation [J].
Burke, Michael C. ;
Li, Feng-Qian ;
Cyge, Benjamin ;
Arashiro, Takeshi ;
Brechbuhl, Heather M. ;
Chen, Xingwang ;
Siller, Saul S. ;
Weiss, Matthew A. ;
O'Connell, Christopher B. ;
Love, Damon ;
Westlake, Christopher J. ;
Reynolds, Susan D. ;
Kuriyama, Ryoko ;
Takemaru, Ken-Ichi .
JOURNAL OF CELL BIOLOGY, 2014, 207 (01) :123-137
[7]
Tracing the origins of centrioles, cilia, and flagella [J].
Carvalho-Santos, Zita ;
Azimzadeh, Juliette ;
Pereira-Leal, Jose B. ;
Bettencourt-Dias, Monica .
JOURNAL OF CELL BIOLOGY, 2011, 194 (02) :165-175
[8]
Small organelle, big responsibility: the role of centrosomes in development and disease [J].
Chavali, Pavithra L. ;
Puetz, Monika ;
Gergely, Fanni .
PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 2014, 369 (1650)
[9]
A Comparative Analysis of Spindle Morphometrics across Metazoans [J].
Crowder, Marina E. ;
Strzelecka, Magdalena ;
Wilbur, Jeremy D. ;
Good, Matthew C. ;
von Dassow, George ;
Heald, Rebecca .
CURRENT BIOLOGY, 2015, 25 (11) :1542-1550
[10]
DAVRING L, 1973, HEREDITAS, V73, P51