Augmin accumulation on long-lived microtubules drives amplification and kinetochore-directed growth.
Journal
The Journal of cell biology
ISSN: 1540-8140
Titre abrégé: J Cell Biol
Pays: United States
ID NLM: 0375356
Informations de publication
Date de publication:
01 07 2019
01 07 2019
Historique:
received:
10
05
2018
revised:
19
12
2018
accepted:
30
04
2019
pubmed:
23
5
2019
medline:
15
5
2020
entrez:
23
5
2019
Statut:
ppublish
Résumé
Dividing cells reorganize their microtubule cytoskeleton into a bipolar spindle, which moves one set of sister chromatids to each nascent daughter cell. Early spindle assembly models postulated that spindle pole-derived microtubules search the cytoplasmic space until they randomly encounter a kinetochore to form a stable attachment. More recent work uncovered several additional, centrosome-independent microtubule generation pathways, but the contributions of each pathway to spindle assembly have remained unclear. Here, we combined live microscopy and mathematical modeling to show that most microtubules nucleate at noncentrosomal regions in dividing human cells. Using a live-cell probe that selectively labels aged microtubule lattices, we demonstrate that the distribution of growing microtubule plus ends can be almost entirely explained by Augmin-dependent amplification of long-lived microtubule lattices. By ultrafast 3D lattice light-sheet microscopy, we observed that this mechanism results in a strong directional bias of microtubule growth toward individual kinetochores. Our systematic quantification of spindle dynamics reveals highly coordinated microtubule growth during kinetochore fiber assembly.
Identifiants
pubmed: 31113824
pii: jcb.201805044
doi: 10.1083/jcb.201805044
pmc: PMC6605806
doi:
Substances chimiques
Cell Cycle Proteins
0
HAUS6 protein, human
0
Microtubule-Associated Proteins
0
augmin protein, human
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2150-2168Subventions
Organisme : European Research Council
ID : 281198
Pays : International
Organisme : NIGMS NIH HHS
ID : R01 GM067230
Pays : United States
Informations de copyright
© 2019 David et al.
Références
Curr Biol. 1999 May 6;9(9):481-4
pubmed: 10322113
Nature. 1999 Jul 8;400(6740):178-81
pubmed: 10408446
J Biol Chem. 2000 Aug 25;275(34):26265-76
pubmed: 10818101
Cell. 2001 Jan 12;104(1):83-93
pubmed: 11163242
Mol Biol Cell. 2001 Apr;12(4):971-80
pubmed: 11294900
J Cell Biol. 2001 Apr 30;153(3):517-27
pubmed: 11331303
Nat Cell Biol. 2002 Nov;4(11):871-9
pubmed: 12389033
Mol Biol Cell. 2002 Dec;13(12):4308-16
pubmed: 12475954
J Cell Biol. 2003 Mar 3;160(5):671-83
pubmed: 12604591
J Neurosci. 2003 Apr 1;23(7):2655-64
pubmed: 12684451
J Cell Biol. 1992 Sep;118(5):1097-108
pubmed: 1387400
Nat Biotechnol. 2004 May;22(5):589-94
pubmed: 15064769
Cell. 2004 Jul 23;118(2):187-202
pubmed: 15260989
Curr Biol. 2005 May 10;15(9):828-32
pubmed: 15886100
J Cell Biol. 1992 Jul;118(2):369-83
pubmed: 1629239
Curr Biol. 2006 Mar 7;16(5):536-41
pubmed: 16527751
Curr Biol. 2006 Mar 21;16(6):564-9
pubmed: 16546079
Nature. 2006 Mar 30;440(7084):697-701
pubmed: 16572176
J Cell Biol. 2006 Dec 18;175(6):881-91
pubmed: 17178907
Science. 2007 Apr 20;316(5823):417-21
pubmed: 17412918
Nat Cell Biol. 2007 Nov;9(11):1233-42
pubmed: 17934454
IEEE Trans Image Process. 1998;7(1):27-41
pubmed: 18267377
J Cell Biol. 2008 Feb 25;180(4):729-37
pubmed: 18283108
J Cell Biol. 2008 May 5;181(3):421-9
pubmed: 18443220
Nat Methods. 2008 Aug;5(8):695-702
pubmed: 18641657
J Cell Biol. 2008 Jul 28;182(2):289-300
pubmed: 18663142
J Cell Biol. 2008 Aug 25;182(4):631-9
pubmed: 18710922
Science. 2008 Nov 21;322(5905):1243-7
pubmed: 18948504
J Cell Biol. 2008 Dec 1;183(5):835-48
pubmed: 19029337
Mol Syst Biol. 2009;5:241
pubmed: 19293826
Proc Natl Acad Sci U S A. 2009 Apr 28;106(17):6998-7003
pubmed: 19369198
Curr Biol. 2009 May 26;19(10):816-26
pubmed: 19427217
Methods Mol Biol. 2009;545:113-34
pubmed: 19475385
Curr Biol. 2009 Jul 28;19(14):1210-5
pubmed: 19540121
Curr Biol. 2009 Nov 17;19(21):1839-45
pubmed: 19836241
Dev Cell. 2009 Oct;17(4):437-8
pubmed: 19853556
Mol Biol Cell. 2010 Jan 15;21(2):323-33
pubmed: 19940016
Curr Opin Cell Biol. 2010 Feb;22(1):96-103
pubmed: 19963362
Nat Rev Mol Cell Biol. 2010 Feb;11(2):91-102
pubmed: 20068571
EMBO J. 2010 Dec 15;29(24):4070-82
pubmed: 21102558
Proc Natl Acad Sci U S A. 2011 Aug 30;108(35):14473-8
pubmed: 21844347
Curr Opin Cell Biol. 2012 Feb;24(1):48-56
pubmed: 22154944
Cell. 2012 Apr 27;149(3):554-64
pubmed: 22541427
J Cell Biol. 1990 Jan;110(1):81-95
pubmed: 2295685
Cell. 2013 Feb 14;152(4):768-77
pubmed: 23415226
J Cell Biol. 2013 Jul 8;202(1):25-33
pubmed: 23816620
Dev Cell. 2013 Aug 12;26(3):279-91
pubmed: 23891661
J Cell Biol. 1990 Sep;111(3):1039-45
pubmed: 2391359
Nat Cell Biol. 2013 Nov;15(11):1370-7
pubmed: 24096243
Dev Cell. 2014 Jan 13;28(1):81-93
pubmed: 24389063
Nat Methods. 2014 Jul;11(7):731-3
pubmed: 24859753
Cell. 2014 Jun 5;157(6):1405-15
pubmed: 24906155
Nat Cell Biol. 2014 Aug;16(8):770-8
pubmed: 24976384
Nat Cell Biol. 2014 Sep;16(9):852-63
pubmed: 25173975
Science. 2014 Oct 24;346(6208):1257998
pubmed: 25342811
Proc Natl Acad Sci U S A. 2014 Dec 16;111(50):17715-22
pubmed: 25468969
Curr Biol. 2015 Jan 19;25(2):131-140
pubmed: 25532896
Elife. 2015 Jun 19;4:null
pubmed: 26090906
Nat Cell Biol. 2015 Sep;17(9):1089-93
pubmed: 26316453
Nat Commun. 2015 Oct 01;6:8497
pubmed: 26423723
Trends Cell Biol. 2016 Feb;26(2):80-87
pubmed: 26475655
J Cell Biol. 2015 Dec 21;211(6):1103-11
pubmed: 26668328
Annu Rev Biochem. 2016 Jun 2;85:659-83
pubmed: 27145846
Nature. 2016 Jun 29;535(7611):308-12
pubmed: 27362226
Proc Natl Acad Sci U S A. 2016 Aug 2;113(31):8729-34
pubmed: 27439876
Cell. 2016 Oct 6;167(2):539-552.e14
pubmed: 27716509
Elife. 2016 Nov 28;5:
pubmed: 27892852
Nat Rev Mol Cell Biol. 2017 Mar;18(3):187-201
pubmed: 28174430
J Cell Sci. 2017 May 15;130(10):1709-1715
pubmed: 28386021
Cell. 2017 Aug 24;170(5):956-972.e23
pubmed: 28841419
Curr Biol. 2017 Dec 4;27(23):R1287-R1292
pubmed: 29207274
Elife. 2018 Jan 11;7:
pubmed: 29323637
IEEE Trans Image Process. 2017 Nov;26(11):5395-5410
pubmed: 29388914
J Cell Biol. 2018 Aug 6;217(8):2647-2659
pubmed: 29907657
Cell. 1986 May 9;45(3):329-42
pubmed: 3516413
Nature. 1984 Nov 15-21;312(5991):237-42
pubmed: 6504138
Chromosoma. 1981;84(1):145-58
pubmed: 7297248
Cell. 1993 Nov 5;75(3):419-29
pubmed: 8221885
J Cell Biol. 1997 Jun 30;137(7):1567-80
pubmed: 9199171