Literature DB >> 23222841

Pivoting of microtubules around the spindle pole accelerates kinetochore capture.

Iana Kalinina1, Amitabha Nandi, Petrina Delivani, Mariola R Chacón, Anna H Klemm, Damien Ramunno-Johnson, Alexander Krull, Benjamin Lindner, Nenad Pavin, Iva M Tolić-Nørrelykke.   

Abstract

During cell division, spindle microtubules attach to chromosomes through kinetochores, protein complexes on the chromosome. The central question is how microtubules find kinetochores. According to the pioneering idea termed search-and-capture, numerous microtubules grow from a centrosome in all directions and by chance capture kinetochores. The efficiency of search-and-capture can be improved by a bias in microtubule growth towards the kinetochores, by nucleation of microtubules at the kinetochores and at spindle microtubules, by kinetochore movement, or by a combination of these processes. Here we show in fission yeast that kinetochores are captured by microtubules pivoting around the spindle pole, instead of growing towards the kinetochores. This pivoting motion of microtubules is random and independent of ATP-driven motor activity. By introducing a theoretical model, we show that the measured random movement of microtubules and kinetochores is sufficient to explain the process of kinetochore capture. Our theory predicts that the speed of capture depends mainly on how fast microtubules pivot, which was confirmed experimentally by speeding up and slowing down microtubule pivoting. Thus, pivoting motion allows microtubules to explore space laterally, as they search for targets such as kinetochores.

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Year:  2012        PMID: 23222841     DOI: 10.1038/ncb2640

Source DB:  PubMed          Journal:  Nat Cell Biol        ISSN: 1465-7392            Impact factor:   28.824


  36 in total

1.  Generation of GTP-bound Ran by RCC1 is required for chromatin-induced mitotic spindle formation.

Authors:  R E Carazo-Salas; G Guarguaglini; O J Gruss; A Segref; E Karsenti; I W Mattaj
Journal:  Nature       Date:  1999-07-08       Impact factor: 49.962

2.  Efficient chromosome capture requires a bias in the 'search-and-capture' process during mitotic-spindle assembly.

Authors:  R Wollman; E N Cytrynbaum; J T Jones; T Meyer; J M Scholey; A Mogilner
Journal:  Curr Biol       Date:  2005-05-10       Impact factor: 10.834

3.  Making microtubules and mitotic spindles in cells without functional centrosomes.

Authors:  Nicole M Mahoney; Gohta Goshima; Adam D Douglass; Ronald D Vale
Journal:  Curr Biol       Date:  2006-03-21       Impact factor: 10.834

4.  50 ways to build a spindle: the complexity of microtubule generation during mitosis.

Authors:  Tommy Duncan; James G Wakefield
Journal:  Chromosome Res       Date:  2011-04       Impact factor: 5.239

5.  Microtubule depolymerization can drive poleward chromosome motion in fission yeast.

Authors:  Ekaterina L Grishchuk; J Richard McIntosh
Journal:  EMBO J       Date:  2006-10-12       Impact factor: 11.598

6.  A new method reveals microtubule minus ends throughout the meiotic spindle.

Authors:  Kendra S Burbank; Aaron C Groen; Zachary E Perlman; Daniel S Fisher; Timothy J Mitchison
Journal:  J Cell Biol       Date:  2006-11-06       Impact factor: 10.539

7.  Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe.

Authors:  J Bähler; J Q Wu; M S Longtine; N G Shah; A McKenzie; A B Steever; A Wach; P Philippsen; J R Pringle
Journal:  Yeast       Date:  1998-07       Impact factor: 3.239

8.  Kinetochores generate microtubules with distal plus ends: their roles and limited lifetime in mitosis.

Authors:  Etsushi Kitamura; Kozo Tanaka; Shinya Komoto; Yoko Kitamura; Claude Antony; Tomoyuki U Tanaka
Journal:  Dev Cell       Date:  2010-02-16       Impact factor: 12.270

9.  Origin of kinetochore microtubules in Chinese hamster ovary cells.

Authors:  P L Witt; H Ris; G G Borisy
Journal:  Chromosoma       Date:  1980       Impact factor: 4.316

10.  Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast.

Authors:  H Funabiki; I Hagan; S Uzawa; M Yanagida
Journal:  J Cell Biol       Date:  1993-06       Impact factor: 10.539

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  34 in total

1.  Theory of Cytoskeletal Reorganization during Cross-Linker-Mediated Mitotic Spindle Assembly.

Authors:  Adam R Lamson; Christopher J Edelmaier; Matthew A Glaser; Meredith D Betterton
Journal:  Biophys J       Date:  2019-04-13       Impact factor: 4.033

2.  Search and Capture Efficiency of Dynamic Microtubules for Centrosome Relocation during IS Formation.

Authors:  Apurba Sarkar; Heiko Rieger; Raja Paul
Journal:  Biophys J       Date:  2019-04-13       Impact factor: 4.033

Review 3.  Mitotic spindle assembly in animal cells: a fine balancing act.

Authors:  Suzanna L Prosser; Laurence Pelletier
Journal:  Nat Rev Mol Cell Biol       Date:  2017-02-08       Impact factor: 94.444

4.  Minus-end-directed Kinesin-14 motors align antiparallel microtubules to control metaphase spindle length.

Authors:  Austin J Hepperla; Patrick T Willey; Courtney E Coombes; Breanna M Schuster; Maryam Gerami-Nejad; Mark McClellan; Soumya Mukherjee; Janet Fox; Mark Winey; David J Odde; Eileen O'Toole; Melissa K Gardner
Journal:  Dev Cell       Date:  2014-10-13       Impact factor: 12.270

Review 5.  Mitosis.

Authors:  J Richard McIntosh
Journal:  Cold Spring Harb Perspect Biol       Date:  2016-09-01       Impact factor: 10.005

6.  3D rotational motion of an endocytic vesicle on a complex microtubule network in a living cell.

Authors:  Seohyun Lee; Hideo Higuchi
Journal:  Biomed Opt Express       Date:  2019-11-27       Impact factor: 3.732

7.  The microtubule-associated protein HURP recruits the centrosomal protein TACC3 to regulate K-fiber formation and support chromosome congression.

Authors:  Yajun Zhang; Lora Tan; Qiaoyun Yang; Chenyu Li; Yih-Cherng Liou
Journal:  J Biol Chem       Date:  2018-07-27       Impact factor: 5.157

8.  Fission yeast myosin I facilitates PI(4,5)P2-mediated anchoring of cytoplasmic dynein to the cortex.

Authors:  Jerrin Mathew Thankachan; Stephen Sukumar Nuthalapati; Nireekshit Addanki Tirumala; Vaishnavi Ananthanarayanan
Journal:  Proc Natl Acad Sci U S A       Date:  2017-03-14       Impact factor: 11.205

9.  Mechanisms of chromosome biorientation and bipolar spindle assembly analyzed by computational modeling.

Authors:  Christopher Edelmaier; Adam R Lamson; Zachary R Gergely; Saad Ansari; Robert Blackwell; J Richard McIntosh; Matthew A Glaser; Meredith D Betterton
Journal:  Elife       Date:  2020-02-13       Impact factor: 8.140

10.  Contributions of Microtubule Dynamic Instability and Rotational Diffusion to Kinetochore Capture.

Authors:  Robert Blackwell; Oliver Sweezy-Schindler; Christopher Edelmaier; Zachary R Gergely; Patrick J Flynn; Salvador Montes; Ammon Crapo; Alireza Doostan; J Richard McIntosh; Matthew A Glaser; Meredith D Betterton
Journal:  Biophys J       Date:  2016-09-28       Impact factor: 4.033

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