Abstract
A stable cell line expressing EB1-green fluorescent protein was used to image growing microtubule plus ends at the G(2)/M transition. By late prophase growing ends no longer extend to the cell periphery and were not uniformly distributed around each centrosome. Growing ends were much more abundant in the area surrounding the nuclear envelope, and microtubules growing around the nucleus were 1.5 fold longer than those growing in the opposite direction. The growth of longer ends toward the nucleus did not result from a localized faster growth rate, because this rate was approximately 11 microm/min in all directions from the centrosome. Rather, microtubule ends growing toward the nucleus seemed stabilized by dynein/dynactin associated with the nuclear envelope. Injection of p50 into late prophase cells removed dynein from the nuclear envelope, reduced the density of growing ends near the nuclear envelope and resulted in a uniform distribution of growing ends from each centrosome. We suggest that the cell cycle-dependent binding of dynein/dynactin to the nuclear envelope locally stabilizes growing microtubules. Both dynein and microtubules would then be in a position to participate in nuclear envelope breakdown, as described in recent studies.
MeSH Terms
Animals
Cell Line
Dynactin Complex
Dyneins/metabolism
Epithelial Cells/cytology,metabolism
Green Fluorescent Proteins
Luminescent Proteins/genetics,metabolism
Microtubule-Associated Proteins/genetics,metabolism
Microtubules/metabolism
Mitosis/physiology
Nuclear Envelope/metabolism
Protein Binding
Recombinant Fusion Proteins/genetics,metabolism
Swine
Tubulin/metabolism
Chemicals
Dynactin Complex
EB1 microtubule binding proteins
Luminescent Proteins
Microtubule-Associated Proteins
Recombinant Fusion Proteins
Tubulin
Green Fluorescent Proteins
Dyneins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Piehl Michelle
Department of Biological Sciences, Lehigh University, Bethlehem, Pennsylvania 18015, USA. maka@lehigh.edu
Cassimeris Lynne
References (22)
22 references, click to expand
-
Feedback interactions between cell-cell adherens junctions and cytoskeletal dynamics in newt lung epithelial cells.
Mol Biol Cell. 2000 Jul;11(7):2471-83
PMID: 10888682
-
Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis.
J Cell Biol. 1996 Feb;132(4):617-33
PMID: 8647893
-
Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5.
J Cell Biol. 2000 Sep 4;150(5):975-88
PMID: 10973989
-
Cell cycle-dependent changes in microtubule dynamics in living cells expressing green fluorescent protein-alpha tubulin.
Mol Biol Cell. 2001 Apr;12(4):971-80
PMID: 11294900
-
Cytoplasmic dynein/dynactin drives kinetochore protein transport to the spindle poles and has a role in mitotic spindle checkpoint inactivation.
J Cell Biol. 2001 Dec 24;155(7):1159-72
PMID: 11756470
-
Nuclear envelope breakdown proceeds by microtubule-induced tearing of the lamina.
Cell. 2002 Jan 11;108(1):83-96
PMID: 11792323
-
Microtubule dynamics at the G2/M transition: abrupt breakdown of cytoplasmic microtubules at nuclear envelope breakdown and implications for spindle morphogenesis.
J Cell Biol. 1996 Oct;135(1):201-14
PMID: 8858174
-
Dynein and dynactin are localized to astral microtubules and at cortical sites in mitotic epithelial cells.
Curr Biol. 1998 Apr 23;8(9):541-4
PMID: 9560347
-
The adenomatous polyposis coli-binding protein EB1 is associated with cytoplasmic and spindle microtubules.
Proc Natl Acad Sci U S A. 1998 Sep 1;95(18):10596-601
PMID: 9724749
-
Regional regulation of microtubule dynamics in polarized, motile cells.
Cell Motil Cytoskeleton. 1999;42(1):48-59
PMID: 9915584
-
Yeast Bim1p promotes the G1-specific dynamics of microtubules.
J Cell Biol. 1999 May 31;145(5):993-1007
PMID: 10352017
-
The sudden recruitment of gamma-tubulin to the centrosome at the onset of mitosis and its dynamic exchange throughout the cell cycle, do not require microtubules.
J Cell Biol. 1999 Aug 9;146(3):585-96
PMID: 10444067
-
Decreasing oncoprotein 18/stathmin levels reduces microtubule catastrophes and increases microtubule polymer in vivo.
J Cell Sci. 1999 Nov;112 ( Pt 21):3713-22
PMID: 10523507
-
Cytoplasmic dynein as a facilitator of nuclear envelope breakdown.
Cell. 2002 Jan 11;108(1):97-107
PMID: 11792324
-
EB 1 immunofluorescence reveals an increase in growing astral microtubule length and number during anaphase in NRK-52E cells.
Eur J Cell Biol. 2001 Dec;80(12):749-53
PMID: 11831388
-
Tubulin dynamics in cultured mammalian cells.
J Cell Biol. 1984 Dec;99(6):2175-86
PMID: 6501419
-
Sites of microtubule assembly and disassembly in the mitotic spindle.
Cell. 1986 May 23;45(4):515-27
PMID: 3708686
-
Fine structural studies of early mitotic stages in untreated and nocodazole-treated HeLa cells.
Eur J Cell Biol. 1988 Dec;47(2):334-45
PMID: 3243286
-
Real-time visualization of cell cycle-dependent changes in microtubule dynamics in cytoplasmic extracts.
Cell. 1990 Aug 10;62(3):579-89
PMID: 2379239
-
Kinetochores capture astral microtubules during chromosome attachment to the mitotic spindle: direct visualization in live newt lung cells.
J Cell Biol. 1990 Sep;111(3):1039-45
PMID: 2391359
-
Cytoplasmic dynein binds dynactin through a direct interaction between the intermediate chains and p150Glued.
J Cell Biol. 1995 Dec;131(6 Pt 1):1507-16
PMID: 8522607
-
The dynamic behavior of the APC-binding protein EB1 on the distal ends of microtubules.
Curr Biol. 2000 Jul 13;10(14):865-8
PMID: 10899006