Abstract
Dividing cells need to coordinate the separation of chromosomes with the formation of a cleavage plane. There is evidence that microtubule bundles in the interzone region of the anaphase spindle somehow control both the location and the assembly of the cleavage furrow [1-3]. A microtubule motor that concentrates in the interzone, MKLP1, has previously been implicated in the assembly of both the metaphase spindle and the cleavage furrow [4-6]. To gain insight into mechanisms that might underlie interdependence of the spindle and the cleavage furrow, we used RNA-mediated interference (RNAi) to study the effects of eliminating MKLP1 from Caenorhabditis elegans embryos. Surprisingly, in MKLP1(RNAi) embryos, spindle formation appears normal until late anaphase. Microtubule bundles form in the spindle interzone and the cleavage furrow assembles; anaphase and cleavage furrow ingression initially appear normal. The interzone bundles do not gather into a stable midbody, however, and furrow contraction always fails before complete closure. This sequence of relatively normal mitosis and a late failure of cytokinesis continues for many cell cycles. These and additional results suggest that the interzone microtubule bundles need MKLP1 to encourage the advance and stable closure of the cleavage furrow.
MeSH Terms
Animals
Caenorhabditis elegans/cytology,embryology,genetics
Caenorhabditis elegans Proteins
Kinesins/genetics,physiology
Microtubule-Associated Proteins/genetics,physiology
RNA, Antisense
RNA, Small Interfering
Chemicals
Caenorhabditis elegans Proteins
MKLP1 protein, C elegans
Microtubule-Associated Proteins
RNA, Antisense
RNA, Small Interfering
Kinesins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Powers J
Department of Biology, Indiana University, Bloomington, Indiana 47405, USA.
Bossinger O
Rose D
Strome S
Saxton W
References (14)
14 references, click to expand
-
Fluorescence visualization of the distribution of microfilaments in gonads and early embryos of the nematode Caenorhabditis elegans.
J Cell Biol. 1986 Dec;103(6 Pt 1):2241-52
PMID: 3782297
-
Distribution of a matrix component of the midbody during the cell cycle in Chinese hamster ovary cells.
J Cell Biol. 1988 Feb;106(2):431-9
PMID: 2448315
-
A monoclonal antibody to a mitotic microtubule-associated protein blocks mitotic progression.
J Cell Biol. 1990 Aug;111(2):511-22
PMID: 2199459
-
A plus-end-directed motor enzyme that moves antiparallel microtubules in vitro localizes to the interzone of mitotic spindles.
Nature. 1992 Oct 8;359(6395):543-7
PMID: 1406973
-
pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for cytokinesis.
Genes Dev. 1998 May 15;12(10):1483-94
PMID: 9585508
-
Heterogeneity and microtubule interaction of the CHO1 antigen, a mitosis-specific kinesin-like protein. Analysis of subdomains expressed in insect sf9 cells.
J Cell Sci. 1994 Dec;107 ( Pt 12):3485-99
PMID: 7706400
-
The Drosophila kinesin-like protein KLP3A is a midbody component required for central spindle assembly and initiation of cytokinesis.
J Cell Biol. 1995 May;129(3):709-23
PMID: 7730406
-
Signals from the spindle midzone are required for the stimulation of cytokinesis in cultured epithelial cells.
Mol Biol Cell. 1996 Feb;7(2):225-32
PMID: 8688554
-
Midzone microtubule bundles are continuously required for cytokinesis in cultured epithelial cells.
J Cell Biol. 1996 Nov;135(4):981-9
PMID: 8922381
-
Inhibition of a mitotic motor compromises the formation of dendrite-like processes from neuroblastoma cells.
J Cell Biol. 1997 Feb 10;136(3):659-68
PMID: 9024695
-
Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans.
Nature. 1998 Feb 19;391(6669):806-11
PMID: 9486653
-
Cytokinesis and midzone microtubule organization in Caenorhabditis elegans require the kinesin-like protein ZEN-4.
Mol Biol Cell. 1998 Aug;9(8):2037-49
PMID: 9693365
-
Roles of kinesin and kinesin-like proteins in sea urchin embryonic cell division: evaluation using antibody microinjection.
J Cell Biol. 1993 Nov;123(3):681-9
PMID: 8227132
-
Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos.
Cell. 1983 Nov;35(1):15-25
PMID: 6684994