Promotion and Suppression of Centriole Duplication Are Catalytically Coupled through PLK4 to Ensure Centriole Homeostasis

被引:17
作者
Kim, Minhee [1 ,2 ]
O'Rourke, Brian P. [1 ]
Soni, Rajesh Kumar [3 ]
Jallepalli, Prasad V. [4 ]
Hendrickson, Ronald C. [3 ]
Tsou, Meng-Fu Bryan [1 ,2 ]
机构
[1] Mem Sloan Kettering Canc Ctr, Cell Biol Program, New York, NY 10065 USA
[2] Cornell Univ, Weill Cornell Grad Sch Med Sci, New York, NY 10065 USA
[3] Mem Sloan Kettering Canc Ctr, Microchem & Prote Core Facil, New York, NY 10065 USA
[4] Mem Sloan Kettering Canc Ctr, Program Mol Biol, New York, NY 10065 USA
关键词
KINASE-ACTIVITY; STIL; PROCENTRIOLE; CENTROSOMES; RECRUITMENT; MECHANISM; ASTERLESS; SCAFFOLD; SUGGEST; BINDING;
D O I
10.1016/j.celrep.2016.06.069
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
PLK4 is the major kinase driving centriole duplication. Duplication occurs only once per cell cycle, forming one new (or daughter) centriole that is tightly engaged to the preexisting (or mother) centriole. Centriole engagement is known to block the reduplication of mother centrioles, but the molecular identity responsible for the block remains unclear. Here, we show that the centriolar cartwheel, the geometric scaffold for centriole assembly, forms the identity of daughter centrioles essential for the block, ceasing further duplication of the mother centriole to which it is engaged. To ensure a steady block, we found that the cartwheel requires constant maintenance by PLK4 through phosphorylation of the same substrate that drives centriole assembly, revealing a parsimonious control in which "assembly'' and "block for new assembly'' are linked through the same catalytic reaction to achieve homeostasis. Our results support a recently deduced model that the cartwheel-bound PLK4 directly suppresses centriole reduplication.
引用
收藏
页码:1195 / 1203
页数:9
相关论文
共 33 条
[1]   STIL binding to Polo-box 3 of PLK4 regulates centriole duplication [J].
Arquint, Christian ;
Gabryjonczyk, Anna-Maria ;
Imseng, Stefan ;
Boehm, Raphael ;
Sauer, Evelyn ;
Hiller, Sebastian ;
Nigg, Erich A. ;
Maier, Timm .
ELIFE, 2015, 4
[2]   STIL Microcephaly Mutations Interfere with APC/C-Mediated Degradation and Cause Centriole Amplification [J].
Arquint, Christian ;
Nigg, Erich A. .
CURRENT BIOLOGY, 2014, 24 (04) :351-360
[3]  
Berdougo E, 2009, METHODS MOL BIOL, V545, P21, DOI 10.1007/978-1-60327-993-2_2
[4]   Cep152 acts as a scaffold for recruitment of Plk4 and CPAP to the centrosome [J].
Cizmecioglu, Onur ;
Arnold, Marc ;
Bahtz, Ramona ;
Settele, Florian ;
Ehret, Lena ;
Haselmann-Weiss, Uta ;
Antony, Claude ;
Hoffmann, Ingrid .
JOURNAL OF CELL BIOLOGY, 2010, 191 (04) :731-739
[5]   Regulation of Autophosphorylation Controls PLK4 Self-Destruction and Centriole Number [J].
Cunha-Ferreira, Ines ;
Bento, Ines ;
Pimenta-Marques, Ana ;
Jana, Swadhin Chandra ;
Lince-Faria, Mariana ;
Duarte, Paulo ;
Borrego-Pinto, Joana ;
Gilberto, Samuel ;
Amado, Tiago ;
Brito, Daniela ;
Rodrigues-Martins, Ana ;
Debski, Janusz ;
Dzhindzhev, Nikola ;
Bettencourt-Dias, Monica .
CURRENT BIOLOGY, 2013, 23 (22) :2245-2254
[6]   Plk4 Phosphorylates Ana2 to Trigger Sas6 Recruitment and Procentriole Formation [J].
Dzhindzhev, Nikola S. ;
Tzolovsky, George ;
Lipinszki, Zoltan ;
Schneider, Sandra ;
Lattao, Ramona ;
Fu, Jingyan ;
Debski, Janusz ;
Dadlez, Michal ;
Glover, David M. .
CURRENT BIOLOGY, 2014, 24 (21) :2526-2532
[7]   Asterless is a scaffold for the onset of centriole assembly [J].
Dzhindzhev, Nikola S. ;
Yu, Quan D. ;
Weiskopf, Kipp ;
Tzolovsky, George ;
Cunha-Ferreira, Ines ;
Riparbelli, Maria ;
Rodrigues-Martins, Ana ;
Bettencourt-Dias, Monica ;
Callaini, Giuliano ;
Glover, David M. .
NATURE, 2010, 467 (7316) :714-U104
[8]   The centriole duplication cycle [J].
Firat-Karalar, Elif Nur ;
Stearns, Tim .
PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 2014, 369 (1650)
[9]   Conserved molecular interactions in centriole-to-centrosome conversion [J].
Fu, Jingyan ;
Lipinszki, Zoltan ;
Rangone, Helene ;
Min, Mingwei ;
Mykura, Charlotte ;
Chao-Chu, Jennifer ;
Schneider, Sandra ;
Dzhindzhev, Nikola S. ;
Gottardo, Marco ;
Riparbelli, Maria Giovanna ;
Callaini, Giuliano ;
Glover, David M. .
NATURE CELL BIOLOGY, 2016, 18 (01) :87-+
[10]   The Centrosome and Its Duplication Cycle [J].
Fu, Jingyan ;
Hagan, Iain M. ;
Glover, David M. .
COLD SPRING HARBOR PERSPECTIVES IN BIOLOGY, 2015, 7 (02)