Abstract
Mps1 is an essential component of the spindle assembly checkpoint. In this study, we describe a novel Mps1 inhibitor, AZ3146, and use it to probe the role of Mps1's catalytic activity during mitosis. When Mps1 is inhibited before mitotic entry, subsequent recruitment of Mad1 and Mad2 to kinetochores is abolished. However, if Mps1 is inhibited after mitotic entry, the Mad1-C-Mad2 core complex remains kinetochore bound, but O-Mad2 is not recruited to the core. Although inhibiting Mps1 also interferes with chromosome alignment, we see no obvious effect on aurora B activity. In contrast, kinetochore recruitment of centromere protein E (CENP-E), a kinesin-related motor protein, is severely impaired. Strikingly, inhibition of Mps1 significantly increases its own abundance at kinetochores. Furthermore, we show that Mps1 can dimerize and transphosphorylate in cells. We propose a model whereby Mps1 transphosphorylation results in its release from kinetochores, thus facilitating recruitment of O-Mad2 and CENP-E and thereby simultaneously promoting checkpoint signaling and chromosome congression.
MeSH Terms
Aurora Kinase B
Aurora Kinases
Calcium-Binding Proteins/genetics,metabolism
Cell Cycle Proteins/antagonists & inhibitors,genetics,metabolism
Chromosomal Proteins, Non-Histone/genetics,metabolism
HeLa Cells
Humans
Kinetochores/metabolism
Mad2 Proteins
Mitosis/drug effects,physiology
Multiprotein Complexes/genetics,metabolism
Nuclear Proteins/genetics,metabolism
Phosphorylation/drug effects,physiology
Protein Kinase Inhibitors/pharmacology
Protein Multimerization/drug effects,physiology
Protein Serine-Threonine Kinases/antagonists & inhibitors,genetics,metabolism
Protein-Tyrosine Kinases
Repressor Proteins/genetics,metabolism
Signal Transduction/drug effects,physiology
Chemicals
Calcium-Binding Proteins
Cell Cycle Proteins
Chromosomal Proteins, Non-Histone
MAD1L1 protein, human
MAD2L1 protein, human
Mad2 Proteins
Multiprotein Complexes
Nuclear Proteins
Protein Kinase Inhibitors
Repressor Proteins
centromere protein E
Protein-Tyrosine Kinases
AURKB protein, human
Aurora Kinase B
Aurora Kinases
Protein Serine-Threonine Kinases
TTK protein, human
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Hewitt Laura
Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK.
Tighe Anthony
Santaguida Stefano
White Anne M
Jones Clifford D
Musacchio Andrea
Green Stephen
Taylor Stephen S
References (34)
34 references, click to expand
-
Spindle checkpoint protein dynamics at kinetochores in living cells.
Curr Biol. 2004 Jun 8;14(11):953-64
PMID: 15182668
-
Kinetochore localization of murine Bub1 is required for normal mitotic timing and checkpoint response to spindle damage.
Cell. 1997 May 30;89(5):727-35
PMID: 9182760
-
Crystal structure of the catalytic domain of the mitotic checkpoint kinase Mps1 in complex with SP600125.
J Biol Chem. 2008 Aug 1;283(31):21495-500
PMID: 18480048
-
Human Zw10 and ROD are mitotic checkpoint proteins that bind to kinetochores.
Nat Cell Biol. 2000 Dec;2(12):944-7
PMID: 11146660
-
Autophosphorylation-dependent activation of human Mps1 is required for the spindle checkpoint.
Proc Natl Acad Sci U S A. 2007 Dec 18;104(51):20232-7
PMID: 18083840
-
Truncating APC mutations have dominant effects on proliferation, spindle checkpoint control, survival and chromosome stability.
J Cell Sci. 2004 Dec 15;117(Pt 26):6339-53
PMID: 15561772
-
Mps1 kinase promotes sister-kinetochore bi-orientation by a tension-dependent mechanism.
Curr Biol. 2007 Dec 18;17(24):2175-82
PMID: 18060784
-
Mps1 phosphorylates Borealin to control Aurora B activity and chromosome alignment.
Cell. 2008 Jan 25;132(2):233-46
PMID: 18243099
-
Dissecting the role of MPS1 in chromosome biorientation and the spindle checkpoint through the small molecule inhibitor reversine.
J Cell Biol. 2010 Jul 12;190(1):73-87
PMID: 20624901
-
Mps1 is a kinetochore-associated kinase essential for the vertebrate mitotic checkpoint.
Cell. 2001 Jul 13;106(1):83-93
PMID: 11461704
-
Mps1 kinase activity restrains anaphase during an unperturbed mitosis and targets Mad2 to kinetochores.
J Cell Biol. 2008 Jun 16;181(6):893-901
PMID: 18541701
-
Protein phosphatase 2A and separase form a complex regulated by separase autocleavage.
J Biol Chem. 2007 Aug 24;282(34):24623-32
PMID: 17604273
-
Spindle checkpoint requires Mad1-bound and Mad1-free Mad2.
Mol Biol Cell. 2002 May;13(5):1501-11
PMID: 12006648
-
Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen.
Science. 1999 Oct 29;286(5441):971-4
PMID: 10542155
-
Centromere-associated protein-E is essential for the mammalian mitotic checkpoint to prevent aneuploidy due to single chromosome loss.
J Cell Biol. 2003 Aug 18;162(4):551-63
PMID: 12925705
-
Role of Hec1 in spindle checkpoint signaling and kinetochore recruitment of Mad1/Mad2.
Science. 2002 Sep 27;297(5590):2267-70
PMID: 12351790
-
Nuf2 and Hec1 are required for retention of the checkpoint proteins Mad1 and Mad2 to kinetochores.
Curr Biol. 2003 Dec 2;13(23):2103-9
PMID: 14654001
-
Mitotic checkpoint proteins HsMAD1 and HsMAD2 are associated with nuclear pore complexes in interphase.
J Cell Sci. 2001 Mar;114(Pt 5):953-63
PMID: 11181178
-
Small-molecule kinase inhibitors provide insight into Mps1 cell cycle function.
Nat Chem Biol. 2010 May;6(5):359-68
PMID: 20383151
-
Chromosomes can congress to the metaphase plate before biorientation.
Science. 2006 Jan 20;311(5759):388-91
PMID: 16424343
-
Chromosomal instability by inefficient Mps1 auto-activation due to a weakened mitotic checkpoint and lagging chromosomes.
PLoS One. 2008 Jun 11;3(6):e2415
PMID: 18545697
-
Human MPS1 kinase is required for mitotic arrest induced by the loss of CENP-E from kinetochores.
Mol Biol Cell. 2003 Apr;14(4):1638-51
PMID: 12686615
-
Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores.
J Cell Biol. 2003 Apr 28;161(2):267-80
PMID: 12719470
-
Kinetochore localisation and phosphorylation of the mitotic checkpoint components Bub1 and BubR1 are differentially regulated by spindle events in human cells.
J Cell Sci. 2001 Dec;114(Pt 24):4385-95
PMID: 11792804
-
Dynamics of centromere and kinetochore proteins; implications for checkpoint signaling and silencing.
Curr Biol. 2004 Jun 8;14(11):942-52
PMID: 15182667
-
Phosphate-binding tag, a new tool to visualize phosphorylated proteins.
Mol Cell Proteomics. 2006 Apr;5(4):749-57
PMID: 16340016
-
Chemical genetic inhibition of Mps1 in stable human cell lines reveals novel aspects of Mps1 function in mitosis.
PLoS One. 2010 Apr 22;5(4):e10251
PMID: 20422024
-
In vitro FRAP identifies the minimal requirements for Mad2 kinetochore dynamics.
Curr Biol. 2006 Apr 18;16(8):755-66
PMID: 16631582
-
Bub1 is required for kinetochore localization of BubR1, Cenp-E, Cenp-F and Mad2, and chromosome congression.
J Cell Sci. 2004 Mar 15;117(Pt 8):1577-89
PMID: 15020684
-
CENP-E is a plus end-directed kinetochore motor required for metaphase chromosome alignment.
Cell. 1997 Oct 31;91(3):357-66
PMID: 9363944
-
The Mad2 conformational dimer: structure and implications for the spindle assembly checkpoint.
Cell. 2007 Nov 16;131(4):730-43
PMID: 18022367
-
Bub1 and aurora B cooperate to maintain BubR1-mediated inhibition of APC/CCdc20.
J Cell Sci. 2005 Aug 15;118(Pt 16):3639-52
PMID: 16046481
-
The Saccharomyces cerevisiae spindle pole body duplication gene MPS1 is part of a mitotic checkpoint.
J Cell Biol. 1996 Jan;132(1-2):111-23
PMID: 8567717
-
The spindle-assembly checkpoint in space and time.
Nat Rev Mol Cell Biol. 2007 May;8(5):379-93
PMID: 17426725