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Microtubules are the only structural constituent of the spindle apparatus required for induction of cell cleavage.

Alsop GB, Zhang D - J. Cell Biol. (2003)

Bottom Line: We show that furrow induction occurs under all circumstances, so long as sufficient microtubules are present.Microtubules, as the only spindle structural constituent, undergo dramatic, stage-specific reorganizations, radiating toward cell cortex in "metaphase," disassembling in "anaphase," and bundling into arrays in "telophase." Furrow induction usually occurs at multisites around microtubule bundles, but only those induced by sustained bundles ingress.We suggest that microtubules, regardless of source, are the only structural constituent of the spindle apparatus essential for cleavage furrow induction.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, Oregon State University, 3029 Cordley Hall, Corvallis, OR 97331, USA.

ABSTRACT
Structural constituents of the spindle apparatus essential for cleavage induction remain undefined. Findings from various cell types using different approaches suggest the importance of all structural constituents, including asters, the central spindle, and chromosomes. In this study, we systematically dissected the role of each constituent in cleavage induction in grasshopper spermatocytes and narrowed the essential one down to bundled microtubules. Using micromanipulation, we produced "cells" containing only asters, a truncated central spindle lacking both asters and chromosomes, or microtubules alone. We show that furrow induction occurs under all circumstances, so long as sufficient microtubules are present. Microtubules, as the only spindle structural constituent, undergo dramatic, stage-specific reorganizations, radiating toward cell cortex in "metaphase," disassembling in "anaphase," and bundling into arrays in "telophase." Furrow induction usually occurs at multisites around microtubule bundles, but only those induced by sustained bundles ingress. We suggest that microtubules, regardless of source, are the only structural constituent of the spindle apparatus essential for cleavage furrow induction.

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Bundled microtubule arrays are required for furrow induction. Cells were manipulated as in Fig. 3 to remove both asters and chromosomes, inducing assembly of bundled microtubules. (A) Partial disassembly of microtubules with nocodazole at furrow initiation (88 min) leads to regression of the furrow (101 onward). The fixed cell (116) retains remnants of bundled microtubule arrays (MT) and actin filaments from the disassembled contractile ring (AF and Overlay, arrow). (B) Complete disassembly of microtubules (MT) with nocodazole before furrow initiation (17) results in formation of a disorganized mitochondrial mass (44 onward). Although random contractions can still occur (101–187), no furrow initiation is observed. Actin filaments (AF and Overlay) are associated primarily with the mitochondrial mass. Bar, 10 μm.
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fig4: Bundled microtubule arrays are required for furrow induction. Cells were manipulated as in Fig. 3 to remove both asters and chromosomes, inducing assembly of bundled microtubules. (A) Partial disassembly of microtubules with nocodazole at furrow initiation (88 min) leads to regression of the furrow (101 onward). The fixed cell (116) retains remnants of bundled microtubule arrays (MT) and actin filaments from the disassembled contractile ring (AF and Overlay, arrow). (B) Complete disassembly of microtubules (MT) with nocodazole before furrow initiation (17) results in formation of a disorganized mitochondrial mass (44 onward). Although random contractions can still occur (101–187), no furrow initiation is observed. Actin filaments (AF and Overlay) are associated primarily with the mitochondrial mass. Bar, 10 μm.

Mentions: Organization of actin filaments and furrow initiation in cells lacking both asters and chromosomes require the presence of bundled microtubule arrays; partial (Fig. 4 A, 101 onward; MT) or complete (Fig. 4 B, 44 onward; MT) disassembly of microtubules with nocodazole in such cells (n = 5) disrupts microtubule-associated distribution of actin filaments and prevents furrow initiation (Fig. 4, A and B, AF and Overlay). Random cell contractions, however, can still occur (Fig. 4 B, 101 onward), as is observed in mammalian cells that lack microtubules (Canman et al., 2000). We do not know how radiating microtubules organize midzones, as one would expect these microtubules to extend continuously from the cell center with their plus ends leading toward the periphery of the cell. A self-assembly process (Bonaccorsi et al., 1998; Bucciarelli et al., 2003) requiring midzone-associated motor proteins (Mishima et al., 2002) is probably involved in defining the midzone. Perhaps microtubules with opposite polarity are assembled at the distal ends of radiating microtubules. The elongation of newly assembled microtubules would shift antiparallel, overlapping microtubules along radiating microtubules to the midzone.


Microtubules are the only structural constituent of the spindle apparatus required for induction of cell cleavage.

Alsop GB, Zhang D - J. Cell Biol. (2003)

Bundled microtubule arrays are required for furrow induction. Cells were manipulated as in Fig. 3 to remove both asters and chromosomes, inducing assembly of bundled microtubules. (A) Partial disassembly of microtubules with nocodazole at furrow initiation (88 min) leads to regression of the furrow (101 onward). The fixed cell (116) retains remnants of bundled microtubule arrays (MT) and actin filaments from the disassembled contractile ring (AF and Overlay, arrow). (B) Complete disassembly of microtubules (MT) with nocodazole before furrow initiation (17) results in formation of a disorganized mitochondrial mass (44 onward). Although random contractions can still occur (101–187), no furrow initiation is observed. Actin filaments (AF and Overlay) are associated primarily with the mitochondrial mass. Bar, 10 μm.
© Copyright Policy
Related In: Results  -  Collection

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fig4: Bundled microtubule arrays are required for furrow induction. Cells were manipulated as in Fig. 3 to remove both asters and chromosomes, inducing assembly of bundled microtubules. (A) Partial disassembly of microtubules with nocodazole at furrow initiation (88 min) leads to regression of the furrow (101 onward). The fixed cell (116) retains remnants of bundled microtubule arrays (MT) and actin filaments from the disassembled contractile ring (AF and Overlay, arrow). (B) Complete disassembly of microtubules (MT) with nocodazole before furrow initiation (17) results in formation of a disorganized mitochondrial mass (44 onward). Although random contractions can still occur (101–187), no furrow initiation is observed. Actin filaments (AF and Overlay) are associated primarily with the mitochondrial mass. Bar, 10 μm.
Mentions: Organization of actin filaments and furrow initiation in cells lacking both asters and chromosomes require the presence of bundled microtubule arrays; partial (Fig. 4 A, 101 onward; MT) or complete (Fig. 4 B, 44 onward; MT) disassembly of microtubules with nocodazole in such cells (n = 5) disrupts microtubule-associated distribution of actin filaments and prevents furrow initiation (Fig. 4, A and B, AF and Overlay). Random cell contractions, however, can still occur (Fig. 4 B, 101 onward), as is observed in mammalian cells that lack microtubules (Canman et al., 2000). We do not know how radiating microtubules organize midzones, as one would expect these microtubules to extend continuously from the cell center with their plus ends leading toward the periphery of the cell. A self-assembly process (Bonaccorsi et al., 1998; Bucciarelli et al., 2003) requiring midzone-associated motor proteins (Mishima et al., 2002) is probably involved in defining the midzone. Perhaps microtubules with opposite polarity are assembled at the distal ends of radiating microtubules. The elongation of newly assembled microtubules would shift antiparallel, overlapping microtubules along radiating microtubules to the midzone.

Bottom Line: We show that furrow induction occurs under all circumstances, so long as sufficient microtubules are present.Microtubules, as the only spindle structural constituent, undergo dramatic, stage-specific reorganizations, radiating toward cell cortex in "metaphase," disassembling in "anaphase," and bundling into arrays in "telophase." Furrow induction usually occurs at multisites around microtubule bundles, but only those induced by sustained bundles ingress.We suggest that microtubules, regardless of source, are the only structural constituent of the spindle apparatus essential for cleavage furrow induction.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, Oregon State University, 3029 Cordley Hall, Corvallis, OR 97331, USA.

ABSTRACT
Structural constituents of the spindle apparatus essential for cleavage induction remain undefined. Findings from various cell types using different approaches suggest the importance of all structural constituents, including asters, the central spindle, and chromosomes. In this study, we systematically dissected the role of each constituent in cleavage induction in grasshopper spermatocytes and narrowed the essential one down to bundled microtubules. Using micromanipulation, we produced "cells" containing only asters, a truncated central spindle lacking both asters and chromosomes, or microtubules alone. We show that furrow induction occurs under all circumstances, so long as sufficient microtubules are present. Microtubules, as the only spindle structural constituent, undergo dramatic, stage-specific reorganizations, radiating toward cell cortex in "metaphase," disassembling in "anaphase," and bundling into arrays in "telophase." Furrow induction usually occurs at multisites around microtubule bundles, but only those induced by sustained bundles ingress. We suggest that microtubules, regardless of source, are the only structural constituent of the spindle apparatus essential for cleavage furrow induction.

Show MeSH
Related in: MedlinePlus