Aurora B–INCENP localization at centromeres/inner kinetochores is required for chromosome bi-orientation in budding yeast

Luis J. García-Rodríguez, Taciana Kasciukovic, Viola Denninger, Tomoyuki Tanaka (Lead / Corresponding author)

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Abstract

For proper chromosome segregation in mitosis, sister kinetochores must interact with microtubules from opposite spindle poles (chromosome bi-orientation) [1, 2]. To promote bi-orientation, Aurora B kinase disrupts aberrant kinetochore-microtubule interactions [3–6]. It has long been debated how Aurora B halts this action when bi-orientation is established and tension is applied across sister kinetochores. A popular explanation for it is that, upon bi-orientation, sister kinetochores are pulled in opposite directions, stretching the outer kinetochores [7, 8] and moving Aurora B substrates away from Aurora-B-localizing sites at centromeres (spatial separation model) [3, 5, 9]. This model predicts that Aurora B localization at centromeres is required for bi-orientation. However, this notion was challenged by the observation that Bir1 (yeast survivin), which recruits Ipl1-Sli15 (yeast Aurora B-INCENP) to centromeres, can become dispensable for bi-orientation [10]. This raised the possibility that Aurora B localization at centromeres is dispensable for bi-orientation. Alternatively, there might be a Bir1-independent mechanism for recruiting Ipl1-Sli15 to centromeres or inner kinetochores [5, 9]. Here, we show that the COMA inner kinetochore sub-complex physically interacts with Sli15, recruits Ipl1-Sli15 to the inner kinetochore, and promotes chromosome bi-orientation, independently of Bir1, in budding yeast. Moreover, using an engineered recruitment of Ipl1-Sli15 to the inner kinetochore when both Bir1 and COMA are defective, we show that localization of Ipl1-Sli15 at centromeres or inner kinetochores is required for bi-orientation. Our results give important insight into how Aurora B disrupts kinetochore-microtubule interaction in a tension-dependent manner to promote chromosome bi-orientation. García-Rodríguez et al. show that the COMA inner kinetochore sub-complex physically interacts with Sli15, recruits Ipl1-Sli15 to the inner kinetochore, and promotes chromosome bi-orientation, independently of Bir1, in budding yeast. They conclude that localization of Ipl1-Sli15 at centromeres/inner kinetochores is required for bi-orientation.

Original languageEnglish
Pages (from-to)1536-1544.e4
Number of pages13
JournalCurrent Biology
Volume29
Issue number9
Early online date18 Apr 2019
DOIs
Publication statusPublished - 6 May 2019

Fingerprint

Kinetochores
kinetochores
Saccharomycetales
Centromere
centromeres
Chromosomes
Yeast
yeasts
chromosomes
Aurora Kinase B
Microtubules
microtubules
Stretching
Poles
Yeasts
Substrates
Spindle Poles
Chromosome Segregation
chromosome segregation
Mitosis

Keywords

  • Aurora B
  • Bir1
  • COMA
  • INCENP
  • Ipl1
  • Mcm21
  • Sli15
  • chromosome bi-orientation
  • kinetochore
  • survivin

Cite this

@article{91229bd9aab34b5f92312f43cf26de43,
title = "Aurora B–INCENP localization at centromeres/inner kinetochores is required for chromosome bi-orientation in budding yeast",
abstract = "For proper chromosome segregation in mitosis, sister kinetochores must interact with microtubules from opposite spindle poles (chromosome bi-orientation) [1, 2]. To promote bi-orientation, Aurora B kinase disrupts aberrant kinetochore-microtubule interactions [3–6]. It has long been debated how Aurora B halts this action when bi-orientation is established and tension is applied across sister kinetochores. A popular explanation for it is that, upon bi-orientation, sister kinetochores are pulled in opposite directions, stretching the outer kinetochores [7, 8] and moving Aurora B substrates away from Aurora-B-localizing sites at centromeres (spatial separation model) [3, 5, 9]. This model predicts that Aurora B localization at centromeres is required for bi-orientation. However, this notion was challenged by the observation that Bir1 (yeast survivin), which recruits Ipl1-Sli15 (yeast Aurora B-INCENP) to centromeres, can become dispensable for bi-orientation [10]. This raised the possibility that Aurora B localization at centromeres is dispensable for bi-orientation. Alternatively, there might be a Bir1-independent mechanism for recruiting Ipl1-Sli15 to centromeres or inner kinetochores [5, 9]. Here, we show that the COMA inner kinetochore sub-complex physically interacts with Sli15, recruits Ipl1-Sli15 to the inner kinetochore, and promotes chromosome bi-orientation, independently of Bir1, in budding yeast. Moreover, using an engineered recruitment of Ipl1-Sli15 to the inner kinetochore when both Bir1 and COMA are defective, we show that localization of Ipl1-Sli15 at centromeres or inner kinetochores is required for bi-orientation. Our results give important insight into how Aurora B disrupts kinetochore-microtubule interaction in a tension-dependent manner to promote chromosome bi-orientation. Garc{\'i}a-Rodr{\'i}guez et al. show that the COMA inner kinetochore sub-complex physically interacts with Sli15, recruits Ipl1-Sli15 to the inner kinetochore, and promotes chromosome bi-orientation, independently of Bir1, in budding yeast. They conclude that localization of Ipl1-Sli15 at centromeres/inner kinetochores is required for bi-orientation.",
keywords = "Aurora B, Bir1, COMA, INCENP, Ipl1, Mcm21, Sli15, chromosome bi-orientation, kinetochore, survivin",
author = "Garc{\'i}a-Rodr{\'i}guez, {Luis J.} and Taciana Kasciukovic and Viola Denninger and Tomoyuki Tanaka",
note = "Funding: ERC (322682) and Wellcome Trust (096535/Z/11/Z).",
year = "2019",
month = "5",
day = "6",
doi = "10.1016/j.cub.2019.03.051",
language = "English",
volume = "29",
pages = "1536--1544.e4",
journal = "Current Biology",
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TY - JOUR

T1 - Aurora B–INCENP localization at centromeres/inner kinetochores is required for chromosome bi-orientation in budding yeast

AU - García-Rodríguez, Luis J.

AU - Kasciukovic, Taciana

AU - Denninger, Viola

AU - Tanaka, Tomoyuki

N1 - Funding: ERC (322682) and Wellcome Trust (096535/Z/11/Z).

PY - 2019/5/6

Y1 - 2019/5/6

N2 - For proper chromosome segregation in mitosis, sister kinetochores must interact with microtubules from opposite spindle poles (chromosome bi-orientation) [1, 2]. To promote bi-orientation, Aurora B kinase disrupts aberrant kinetochore-microtubule interactions [3–6]. It has long been debated how Aurora B halts this action when bi-orientation is established and tension is applied across sister kinetochores. A popular explanation for it is that, upon bi-orientation, sister kinetochores are pulled in opposite directions, stretching the outer kinetochores [7, 8] and moving Aurora B substrates away from Aurora-B-localizing sites at centromeres (spatial separation model) [3, 5, 9]. This model predicts that Aurora B localization at centromeres is required for bi-orientation. However, this notion was challenged by the observation that Bir1 (yeast survivin), which recruits Ipl1-Sli15 (yeast Aurora B-INCENP) to centromeres, can become dispensable for bi-orientation [10]. This raised the possibility that Aurora B localization at centromeres is dispensable for bi-orientation. Alternatively, there might be a Bir1-independent mechanism for recruiting Ipl1-Sli15 to centromeres or inner kinetochores [5, 9]. Here, we show that the COMA inner kinetochore sub-complex physically interacts with Sli15, recruits Ipl1-Sli15 to the inner kinetochore, and promotes chromosome bi-orientation, independently of Bir1, in budding yeast. Moreover, using an engineered recruitment of Ipl1-Sli15 to the inner kinetochore when both Bir1 and COMA are defective, we show that localization of Ipl1-Sli15 at centromeres or inner kinetochores is required for bi-orientation. Our results give important insight into how Aurora B disrupts kinetochore-microtubule interaction in a tension-dependent manner to promote chromosome bi-orientation. García-Rodríguez et al. show that the COMA inner kinetochore sub-complex physically interacts with Sli15, recruits Ipl1-Sli15 to the inner kinetochore, and promotes chromosome bi-orientation, independently of Bir1, in budding yeast. They conclude that localization of Ipl1-Sli15 at centromeres/inner kinetochores is required for bi-orientation.

AB - For proper chromosome segregation in mitosis, sister kinetochores must interact with microtubules from opposite spindle poles (chromosome bi-orientation) [1, 2]. To promote bi-orientation, Aurora B kinase disrupts aberrant kinetochore-microtubule interactions [3–6]. It has long been debated how Aurora B halts this action when bi-orientation is established and tension is applied across sister kinetochores. A popular explanation for it is that, upon bi-orientation, sister kinetochores are pulled in opposite directions, stretching the outer kinetochores [7, 8] and moving Aurora B substrates away from Aurora-B-localizing sites at centromeres (spatial separation model) [3, 5, 9]. This model predicts that Aurora B localization at centromeres is required for bi-orientation. However, this notion was challenged by the observation that Bir1 (yeast survivin), which recruits Ipl1-Sli15 (yeast Aurora B-INCENP) to centromeres, can become dispensable for bi-orientation [10]. This raised the possibility that Aurora B localization at centromeres is dispensable for bi-orientation. Alternatively, there might be a Bir1-independent mechanism for recruiting Ipl1-Sli15 to centromeres or inner kinetochores [5, 9]. Here, we show that the COMA inner kinetochore sub-complex physically interacts with Sli15, recruits Ipl1-Sli15 to the inner kinetochore, and promotes chromosome bi-orientation, independently of Bir1, in budding yeast. Moreover, using an engineered recruitment of Ipl1-Sli15 to the inner kinetochore when both Bir1 and COMA are defective, we show that localization of Ipl1-Sli15 at centromeres or inner kinetochores is required for bi-orientation. Our results give important insight into how Aurora B disrupts kinetochore-microtubule interaction in a tension-dependent manner to promote chromosome bi-orientation. García-Rodríguez et al. show that the COMA inner kinetochore sub-complex physically interacts with Sli15, recruits Ipl1-Sli15 to the inner kinetochore, and promotes chromosome bi-orientation, independently of Bir1, in budding yeast. They conclude that localization of Ipl1-Sli15 at centromeres/inner kinetochores is required for bi-orientation.

KW - Aurora B

KW - Bir1

KW - COMA

KW - INCENP

KW - Ipl1

KW - Mcm21

KW - Sli15

KW - chromosome bi-orientation

KW - kinetochore

KW - survivin

UR - http://www.scopus.com/inward/record.url?scp=85064869038&partnerID=8YFLogxK

U2 - 10.1016/j.cub.2019.03.051

DO - 10.1016/j.cub.2019.03.051

M3 - Article

VL - 29

SP - 1536-1544.e4

JO - Current Biology

JF - Current Biology

SN - 0960-9822

IS - 9

ER -