Microtubules in ascidian eggs during meiosis, fertilization, and mitosis

Sawada, Teruo; Schatten, Gerald

doi:10.1002/cm.970090304

Cited by 80 publications

(35 citation statements)

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“…Reliable segregation of meiotic chromosomes depends on the correct assembly of microtubules (MTs) into a bipolar spindle. In most animal systems, female meiotic spindles lack centrosomes and their MT nucleating activity (Sawada and Schatten, 1988;Gard, 1992;Theurkauf and Hawley, 1992;Albertson and Thomson, 1993). Interestingly, vertebrate cultured cells in which centrosomes have been destroyed can use a centrosome-independent pathway to build a functional bipolar spindle (Khodjakov et al, 2000).…”

Section: Introductionmentioning

confidence: 99%

KLP-18, a Klp2 Kinesin, Is Required for Assembly of Acentrosomal Meiotic Spindles inCaenorhabditis elegans

Segbert

Barkus

Powers

et al. 2003

MBoC

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The proper segregation of chromosomes during meiosis or mitosis requires the assembly of well organized spindles. In many organisms, meiotic spindles lack centrosomes. The formation of such acentrosomal spindles seems to involve first assembly or capture of microtubules (MTs) in a random pattern around the meiotic chromosomes and then parallel bundling and bipolar organization by the action of MT motors and other proteins. Here, we describe the structure, distribution, and function of KLP-18, a Caenorhabditis elegans Klp2 kinesin. Previous reports of Klp2 kinesins agree that it concentrates in spindles, but do not provide a clear view of its function. During prometaphase, metaphase, and anaphase, KLP-18 concentrates toward the poles in both meiotic and mitotic spindles. Depletion of KLP-18 by RNAmediated interference prevents parallel bundling/bipolar organization of the MTs that accumulate around female meiotic chromosomes. Hence, meiotic chromosome segregation fails, leading to haploid or aneuploid embryos. Subsequent assembly and function of centrosomal mitotic spindles is normal except when aberrant maternal chromatin is present. This suggests that although KLP-18 is critical for organizing chromosome-derived MTs into a parallel bipolar spindle, the order inherent in centrosome-derived astral MT arrays greatly reduces or eliminates the need for KLP-18 organizing activity in mitotic spindles. INTRODUCTIONIn eukaryotes meiosis allows the exchange of genetic material between parental chromosomes and leads to the formation of haploid gametes. Reliable segregation of meiotic chromosomes depends on the correct assembly of microtubules (MTs) into a bipolar spindle. In most animal systems, female meiotic spindles lack centrosomes and their MT nucleating activity (Sawada and Schatten, 1988;Gard, 1992;Theurkauf and Hawley, 1992;Albertson and Thomson, 1993). Interestingly, vertebrate cultured cells in which centrosomes have been destroyed can use a centrosome-independent pathway to build a functional bipolar spindle (Khodjakov et al., 2000). These and other results suggest that although the diastral mode of spindle assembly dominates when centrosomes are present, chromatin-based spindle assembly can be used when centrosomes are absent. The question of how meiotic MTs become organized into a bipolar structure remains largely unanswered.Studies in Xenopus egg extracts have provided some important insights into acentrosomal spindle assembly. The observation that bipolar spindles can form around DNAcoated beads confirmed that chromatin itself can provide a platform for the nucleation, stabilization, and/or capture of MTs (Heald et al., 1996). Analysis of the effects of inactivating or depleting specific MT motor proteins from Xenopus extracts along with analysis of mutations that affect assembly of acentrosomal meiotic spindles in Drosophila (Merdes and Cleveland, 1997;Walczak et al., 1998;Walczak, 2000) have led to the following model for chromatin-based assembly of bipolar spindles. Chromatin-associated kinesins, e.g., X...

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Section: Introductionmentioning

confidence: 99%

KLP-18, a Klp2 Kinesin, Is Required for Assembly of Acentrosomal Meiotic Spindles inCaenorhabditis elegans

Segbert

Barkus

Powers

et al. 2003

MBoC

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“…However, relatively few studies have examined the detergent-resistant cytoskeleton during early development. Those that have report the presence of an extensive detergent-resistant cytoskeletal network in eggs of a variety of species ranging from fresh water and marine organisms (24,35,37) to mammals (8). Much less, however, is known about the metabolic and structural role of the cytoskeleton during early development.…”

Section: Introductionmentioning

confidence: 99%

A Freeze‐Sectioning Method for Preparation of the Detergent‐Resistant Cytoskeleton Identifies Stage‐Specific Cytoskeleal Proteins and Associated mRNA in Xenopus Oocytes and Embryos

1989

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Proteins of the detergent-resistant cytoskeleton fraction and the detergent-soluble fraction from Xenopus oocytes and embryos are examined using a procedure which allows rapid and uniform extraction of tissues and large, single cells. SDS-polyacrylamide gels reveal only a few prominent cytoskeletal proteins in the early embryo, however qualitatively different proteins begin to appear after gastrulation. Incorporation of [35S]-methionine into newly synthesized proteins indicates that there is synthesis and assembly of proteins into the cytoskeleton, but the amount remains low until after gastrulation. The use of nucleic acid probes for alpha-tubulin and actin mRNA indicates that about 80% of these mRNAs in the oocyte and meiotically mature egg are bound to the detergent-resistant cytoskeleton.

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“…This is commensurat with the idea that segregation of myoplasm-specific molecules is brought about by cytoskeletal movement (24,11). Jeffery (10) reported that some maternal macromolecules, such as mRNAs and polypeptides, bound to the cytoskeletal lattice (12) and segregated to the yellow crescent.…”

Section: Discussionmentioning

confidence: 81%

Characterization of Antigenic Polypeptides Recognized by Monoclonal Antibodies Specific to the Myoplasm of Eggs of the Ascidian Ciona intestinalis

Nishikata

1991

Dev Growth Differ

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The determinants responsible for the differentiation of ascidian larval muscle cells are thought to be contained within the egg myoplasm. To analyze the macromolecules composing the myoplasm, several hybridoma cell lines which secrete monoclonal antibodies specific to myoplasmic components of Ciona eggs have been established (1 7). In the present investigation, seven of these myoplasm-specific antigens were characterized according to their molecular features and distribution patterns within the egg cytoplasm. Four of the seven antigenic polypeptides were shown to be components of the cortical cytoplasm, two were related to mitochondria, and one is likely to be a yolk protein. An antigen recognized by llG6B2 antibody, which inhibited muscle development when injected into fertilized eggs, was a single polypeptide of relative molecular mass about 40,000 and isoelectric point about 5. The antigen was designated myoplasmin-C1 after its characteristic localization. The llF9E9 antigen was a single 35-kDa polypeptide related to mitochondria and was thus designated myoplasmin-M1 . The other five antibodies recognized two or more spots by immunoblotting analysis using two-dimensional gel electrophoresis. All of these myoplasmspecific antigens, except for the llH10D6 antigen, are likely to be produced by the oocyte itself. Synthesis of llH10D6 antigen seems to be associated with test cells.

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Microtubules in ascidian eggs during meiosis, fertilization, and mitosis

Cited by 80 publications

References 11 publications

KLP-18, a Klp2 Kinesin, Is Required for Assembly of Acentrosomal Meiotic Spindles inCaenorhabditis elegans

KLP-18, a Klp2 Kinesin, Is Required for Assembly of Acentrosomal Meiotic Spindles inCaenorhabditis elegans

A Freeze‐Sectioning Method for Preparation of the Detergent‐Resistant Cytoskeleton Identifies Stage‐Specific Cytoskeleal Proteins and Associated mRNA in Xenopus Oocytes and Embryos

Characterization of Antigenic Polypeptides Recognized by Monoclonal Antibodies Specific to the Myoplasm of Eggs of the Ascidian Ciona intestinalis

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