Cytokinesis in eukaryotes - PubMed (original) (raw)

Review

Cytokinesis in eukaryotes

David A Guertin et al. Microbiol Mol Biol Rev. 2002 Jun.

Abstract

Cytokinesis is the final event of the cell division cycle, and its completion results in irreversible partition of a mother cell into two daughter cells. Cytokinesis was one of the first cell cycle events observed by simple cell biological techniques; however, molecular characterization of cytokinesis has been slowed by its particular resistance to in vitro biochemical approaches. In recent years, the use of genetic model organisms has greatly advanced our molecular understanding of cytokinesis. While the outcome of cytokinesis is conserved in all dividing organisms, the mechanism of division varies across the major eukaryotic kingdoms. Yeasts and animals, for instance, use a contractile ring that ingresses to the cell middle in order to divide, while plant cells build new cell wall outward to the cortex. As would be expected, there is considerable conservation of molecules involved in cytokinesis between yeast and animal cells, while at first glance, plant cells seem quite different. However, in recent years, it has become clear that some aspects of division are conserved between plant, yeast, and animal cells. In this review we discuss the major recent advances in defining cytokinesis, focusing on deciding where to divide, building the division apparatus, and dividing. In addition, we discuss the complex problem of coordinating the division cycle with the nuclear cycle, which has recently become an area of intense research. In conclusion, we discuss how certain cells have utilized cytokinesis to direct development.

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Figures

FIG. 1.

FIG. 1.

General mechanisms of cytokinesis in eukaryotes. While the process of cytokinesis results in the physical partition of a mother cell into two daughter cells, the approach to cell division differs between several model organisms. (A) Higher plants, after separating the nuclei, use microtubules to deliver Golgi-derived vesicles to the equatorial region. Vesicles fuse to form the phragmoplast, which, through continued vesicle fusion, grows outward to the cell cortex, ultimately building a physical barrier between daughter cells called the cell plate. (B and C) Yeast and animal cells, unlike plant cells, divide through use of an actomyosin-based contractile ring. (B) In budding yeast cells, the ring is positioned at the interface between the mother cell and daughter bud, termed the bud neck. (C) In fission yeast and animal cells, the contractile ring is centrally placed, as both cell types divide by medial fission. Both budding and fission yeasts synthesize a division septum behind the leading edge of the constricting ring, which is eventually degraded, resulting in physical cell separation. (D) In animals, the ingressing furrow constricts the spindle midzone components into a dense structure called the midbody.

FIG. 2.

FIG. 2.

Positioning the division site. Positioning the division site is one of the least-conserved aspects of cytokinesis. (A) In higher plants, microtubules centrally position the nucleus while condensing in the shortest nucleus-cortex distance to form the phragmosome. Once the nucleus is positioned, the phragmosome appears to mark the position at the cortex for formation of a medial ring structure called the PPB, which marks the division plane. (B) In budding yeast cells, the old or previous bud site is marked on the mother cell cortex by a bud scar. Near the bud scar, a ring containing septins is formed, which marks the site of the new bud. Polarized growth causes the new bud to grow outward from the mother cell cortex. (C) The position of the nucleus in thought to determine the division site in fission yeast. Mid1 protein, which is localized primarily to the nucleus during interphase, exits the nucleus in early mitosis and marks the cortex adjacent to the nucleus. Actin polymers are then recruited to the division site. (D) In animal cells, the spindle midzone determines where the cleavage furrow will form. Many proteins, including the chromosomal passenger proteins, localize to the spindle midzone.

FIG. 3.

FIG. 3.

Vesicle fusion and cytokinesis. (A) In plant cells, Golgi-derived vesicles are targeted by microtubules (MTs) to the cell plate as it grows outward from the cell middle to the cortex. (B) In Xenopus and zebra fish embryos, the FMA is an array of microtubules emanating out from just ahead of the advancing cleavage furrow that is thought to deliver membrane-containing vesicles to the division site. It was recently shown that new membrane accumulation at the cleavage site was also associated with dividing early C. elegans embryos (see text).

FIG. 4.

FIG. 4.

Chromosomal passenger proteins. Chromosomal passenger proteins are so called because they translocate from centromeres to the spindle midzone in anaphase. (A) Aurora-B is localized to centromeres in metaphase in rat NRK cells. During anaphase, Aurora-B translocates to the spindle midzone and subsequently is condensed into the midbody during furrow ingression. (Images courtesy of Maki Murata-Hori and Yu-li Wang.) (B) INCENP, Aurora-B, and Survivin are thought to function as a tripartite chromosomal passenger complex at the spindle midzone. A speculative model suggests that the chromosomal passenger complex interacts with the kinesin MKLP, Polo kinase, and the Rho GAP Cyk-4 to maintain the spindle midzone and promote cytokinesis (see text).

FIG. 5.

FIG. 5.

Model for localization of the SIN proteins in fission yeast. (A) The SPB is a regulatory headquarters for the organization and activation of the SIN pathway. (Panel 1) In interphase Clp1p is in the nucleolus, CDK activity is low, and Sid4p-Cdc11p, Cdc16p-Byr4p, and Spg1-GDP localize to the SPB. (Panel 2) Upon entry into mitosis, CDK activity becomes high, Clp1p leaves the nucleolus, Cdc16p-Byr4p leave both SPBs, and Spg1p converts to the GTP-bound form, which recruits Cdc7p to the SPB. Note that Clp1p also localizes to the SPB, spindle, and actomyosin ring; however, this has been omitted for simplicity. Upon anaphase onset, CDK activity begins to drop (panel 3), and then Cdc16-Byr4p return to one SPB, which results in conversion of Spg1-GTP to Spg1-GDP and loss of Cdc7p from that SPB (panel 4). In addition, Sid1p-Cdc14p are recruited to the Cdc7p-containing SPB. (Panel 5) Just prior to initiation of cytokinesis, the Sid2p-Mob1p complex localizes to the division site and is thought to deliver the signal to divide to the actomyosin ring. (Panel 6) Once the septum has fully formed, the cell returns to the interphase state. (See text for references.) (B and C) SIN proteins and the cytokinesis checkpoint. (B) In cells that have defects in actomyosin ring formation, SIN pathway activation proceeds normally; however, cells undergo a prolonged delay with the SIN “on,” Clp1p out of the nucleus, and CDK activity low, which blocks further nuclear division cycles until cytokinesis is complete. (See text for references.) (C) Sid2p-green fluorescent protein (green) localization in early anaphase (above) and in telophase (below). DNA (blue) and tubulin (red) are also shown.

FIG. 6.

FIG. 6.

Model for activation of the MEN in budding yeast. (A) (Panel 1) In G1 phase Cdc14p localizes to the nucleolus, Lte1p is diffuse, and Nud1p is at the SPB, as is Dbf2p-Mob1p (reports differ [see text] about whether Dbf2p-Mob1p localizes to the SPB in interphase). Also note that because there is no consensus for the Cdc15p localization pattern, it is not shown. (Panel 2) After bud emergence, the nucleolus migrates to the bud neck, Tem1p localizes to the SPB closest to the bud neck, and Lte1p localizes to the bud. (Panel 3) Upon anaphase onset, the spindle elongates into the bud, bringing Tem1p close to its activator, Lte1, causing it to be activated. This leads to activation of the MEN and release of Cdc14p from the nucleolus. (Panel 4) In telophase Cdc14p promotes mitotic exit, localization of Dbf2p-Mob1p to the bud neck, and cytokinesis. (B) The MEN and the spindle orientation checkpoint. Mutants that have defects orienting the mitotic spindle behave normally in G1 (panel 1) but have defects in orienting the mitotic spindle after bud emergence (panel 2). This causes Tem1p not to be brought into contact with its activator Lte1p (panel 3), keeping it in the inactive state, which causes a delay in Cdc14p release from the nucleolus. Thus, cells delay mitotic exit and cytokinesis until the spindle becomes properly oriented.

FIG. 7.

FIG. 7.

Variations of traditional cytokinesis important for development. (A) Many organisms, including C. elegans, reposition the spindle such that cytokinesis will result in unequal-size daughter cell’s. By segregating specific fate determinants (red) into the daughters, an asymmetry is established that is important for determining a cell’s developmental outcome. (B) In Drosophila embryogenesis, incomplete cytokinesis produces a specialized structure called the ring canal. Ring canals (arrow) serve as intracellular bridges in which cytoplasm is shared between adjacent cells and the oocyte. (C) During syncytial divisions in the developing Drosophila embryo, actin (red) ingresses into a pseudocleavage furrow around nuclei during mitosis and is thought to prevent aberrant interactions between adjacent spindles (green). Once mitosis completes, pseudocleavage furrows disassemble and actin is organized into caps between the plasma membrane and centrosomes (see text).

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