Article |
Address correspondence to Fred Chang, Dept. of Microbiology, Columbia University College of Physicians and Surgeons, 701 W. 168th St., New York, NY 10032. Tel.: (212) 305-0252. Fax: (212) 305-1468. E-mail: fc99{at}columbia.edu
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Abstract |
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Key Words: cytokinesis; septin; fission yeast Schizosaccharomyces pombe; contractile ring; FRAP
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Introduction |
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In the fission yeast Schizosaccharomyces pombe, cytokinesis proceeds in multiple phases: in early mitosis (preanaphase), a single contractile ring, consisting of actin, myosin, and other proteins, is assembled and persists through anaphase (2030 min). At the end of anaphase, septation is triggered by the Sin/Sid pathway of cell cycle regulators (McCollum and Gould, 2001). During this process, the contractile ring begins to close, acting to guide the closure of the plasma membrane behind it. At the same time, the cell wall of the septum is synthesized outside the plasma membrane. Upon completion of the cell wall and after the cell membranes are closed, cellcell separation occurs by the digestion of the primary septum. In S. pombe, seven septins have been identified, four of which are localized to the division plane and three of which are involved in sporulation in meiotic cells (J. Pringle, personal communication). S. pombe septin (spn) mutants are viable but have a defect in cellcell separation and accumulate in chains of cells (Longtine et al., 1996) (J. Pringle, personal communication). Consistent with this phenotype, septins appear at the division site only after the contractile ring has been fully assembled. Thus, in contrast to septins in budding yeast, fission yeast septins are not essential for cell viability and may function primarily in late stages of cytokinesis.
Here, we identify a gene that functions in septin organization. Mid2p was identified on the basis of its homology to Mid1p, a protein required for proper positioning of the contractile ring during cytokinesis (Sohrmann et al., 1996; Bahler et al., 1998a; Paoletti and Chang, 2000). The Mid2p sequence also shares similarity with Bud4p, a septin-associated protein required for bud site selection in S. cerevisiae (Sanders and Herskowitz, 1996), and Candida albicans Int1, a protein required for hyphal growth, adhesion, and pathogenesis (Gale et al., 1996, 1998). Our analysis showed that Mid2p associates with and organizes the septin rings. Time-lapse and FRAP analysis of mid2 mutant cells revealed that Mid2p has a specific role in maintaining the integrity and stability of the septin rings during cleavage.
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Results |
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Microscopic examination of mid2 cells revealed a significant defect in cellcell separation in cytokinesis (Fig. 2 A). When grown in rich liquid medium, 16% of asynchronous wild-type cells exhibited a septum, whereas 66% of mid2
cells possessed one septum (Fig. 2 B). A small percentage (<5% of cells) had two or three septa (grown in rich medium in exponential phase) and grew in short chains of cells. No cells were seen with more than three septa. Careful microscopic examination of the septa in multiple focal planes using differential interference contrast (DIC) or calcofluor staining suggested that most of the septa were complete. Chains of cells occasionally contained a cell that had lysed, suggesting that these mutants had rare defects in cellular integrity and that cells in each chain were completely separated by membrane and septum. Robust growth rates suggest that these mutants do not have a significant delay in progression of the nuclear cell cycle but have a specific delay of approximately one generation time in digestion of the septum for cellcell separation.
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Because of this similarity in phenotypes, we tested whether mid2 cells may have defects in septin organization. We examined septin distribution in living wild-type and mid2
cells expressing a Spn4p-GFP fusion construct using time-lapse confocal microscopy. In wild-type cells, septins first appeared in anaphase as a collection of medial dots that were then incorporated into a single medial ring around the circumference of the cell (Fig. 4 A). This single ring then changed into a double ring structure that persisted throughout septation. At the end of septation, septins were present in discrete dots at the new cell ends. During interphase, cells sometimes exhibited small septin dots at the cell ends and also occasionally contained a single bright cytoplasmic motile dot or small ring shaped particle (unpublished data).
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Mid2p affects septin dynamics
This abnormal localization of Spn4p-GFP in mid2 cells suggested that septins may be flowing from the septin rings into the cleavage furrow during ring closure. Alternatively, new septin proteins may be deposited at the membrane in the furrow during this process. To distinguish between these two possibilities, we investigated the dynamics of septin proteins using FRAP. Portions of Spn4p-GFP rings were photobleached, and the rates of recovery of Spn4p-GFP fluorescence were assayed. In mid2+ cells, Spn4p-GFP in well established septin rings recovered relatively slowly with t1/2 = 350 ± 136 s (range 168532 s; n = 7) (Fig. 5; see Materials and methods), showing that Spn4p is relatively stable. In contrast, in mid2
cells Spn4p-GFP fluorescence recovered over 30-fold more rapidly, with t1/2 = 10 ± 4 s (range 517 s; n = 6) (Fig. 5) showing that Spn4p is rapidly exchanging in the ring. Similar FRAP rates were observed in mid2
cells at all different stages of cleavage (n = 18), showing that this large difference between wild-type and mid2
cells was not due to cell cycle stage differences between the datasets. Since the rate of septin exchange is much faster than the rate of invagination, these dynamics show that Spn4p proteins in mid2
cells are not flowing in from the rings at the cell surface into the furrow but may be rapidly binding and exchanging with the invaginating membrane. Thus, Mid2p is required to stabilize septins.
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mid2+ does not share overlapping functions with mid1+
Since Mid2p and Mid1p share significant amino acid similarity, we tested whether they may share overlapping functions. Wild-type, single mid1, and mid2
mutants, and mid1
mid2
double mutants were assayed for growth and cell integrity at multiple temperatures on agar plates containing phloxin, a red dye that stains dead cells. We also assayed for septum placement defects in cells grown in liquid cultures. In these assays, the phenotype of the mid1
mid2
double mutant was not more severe than that of either single mutant (Fig. 8, A and B). Mid1p-GFP was properly localized as a medial broad band of dots at the cell surface and in a tight ring in mid2
mutant cells (Fig. 8 C) (Paoletti and Chang, 2000). Mid2p-GFP was properly localized in single or double rings in the mid1
mutant (Fig. 8 D). Thus, together our data suggest that Mid1p and Mid2p do not have overlapping functions and act in different aspects of cytokinesis.
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Discussion |
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Septins are filament-forming proteins. In vitro, septins assemble into 10-nm filaments (Field et al., 1996; Frazier et al., 1998; Mendoza et al., 2002). In budding yeast, septins appear to be components of the bud neck filaments, although in other organisms analogous septin filaments in vivo have not yet been reported. Little is known about how septin filaments may be regulated by other protein factors, such as factors that promote polymerization, depolymerization, or filament bundling, or affect GTP hydrolysis or exchange. Here we show that in contrast to the contractile ring proteins actin, cdc4p, cdc8p, and myo2p which exchange rapidly (mean t1/2 < 1 min) (Pelham and Chang, 2002; Wong et al., 2002), septins form relatively stable structures in the ring (mean t1/2 = 7 min). We speculate that Mid2p promotes the assembly and/or the stabilization of septin filaments. The abnormally rapid dynamics of septins in mid2 cells may arise from unassembled septin proteins that exchange with binding sites at the membrane of the cleavage furrow. Expression of a nondegradable form of the Mid2p protein has been shown to stabilize septin rings so that they persist into the next cell cycle (K. Gould, personal communication), suggesting that Mid2p can prevent the disassembly of the septin ring at cell division. To our knowledge, our study presents one of the first in vivo analyses of septin dynamics using FRAP identifying a protein required specifically for septin stability.
Although other septin-interacting proteins have not been well characterized yet in S. pombe, a number of proteins have been identified that regulate septins in budding yeast. The GTPase Cdc42p is likely to be a central regulator of septin ring assembly in budding yeast (Gladfelter et al., 2002). Mutants of budding yeast Gin4p, a protein kinase that may directly interact with septins, have septin "bars" rather than rings (Longtine et al., 1998, 2000). elm1 and specific cdc42 mutant alleles display misplacement of septin rings (Bouquin et al., 2000; Gladfelter et al., 2002). Septins have been found to be conjugated with the ubiquitin-related protein SUMO and interact with components of the sumoylation machinery, such as the E3-like factor Siz1p (Johnson and Blobel, 1999; Takahashi et al., 1999; Johnson and Gupta, 2001).
Mid2p and septin function in S. pombe
Septins have been implicated in cytokinesis in several organisms. In budding yeast, septins are essential for cytokinesis and for other important functions such as regulation of the cell cycle and cell shape (Gladfelter et al., 2001). Surprisingly, septin mutants in fission yeast have a much milder phenotype in which many aspects of cytokinesis such as actomyosin ring assembly and contraction and septation are apparently normal, and only the final step in cellcell separation is delayed for about a generation time (23 h). This step in cytokinesis may involve the deposition or activation of factors at the septum that degrade the primary septum, allowing for cell separation. What may be the functions of septins in cytokinesis in S. pombe? Other mutants with a similar cellcell separation phenotype include mutants in the exocyst complex (sec6, sec8, sec10, and exo70), calcineurin (ppb1), a MAPK (pmk1), a MAPK phosphatase (pmp1), and a forkhead transcription factor (sep1) (Sipiczki et al., 1993; Yoshida et al., 1994; Toda et al., 1996; Ribar et al., 1997; Sugiura et al., 1998; Wang et al., 2002). Possible effects of these gene products on Mid2p and septins remain to be determined. In other organisms, septins interact with the exocytosis machinery, such as exocyst components or syntaxins (Hsu et al., 1998; Beites et al., 1999; Kartmann and Roth, 2001). Thus, septins and Mid2p may be required for proper exocytosis of a septum digestive enzyme to the septum.
Septins are still able to localize normally to medial plasma membrane even in the absence of Mid2p. This distribution suggests that there are septin-binding sites in this region. Filipin staining shows that an oxysterol-rich membrane domain is established in a medial band starting in anaphase, and then in the region of the cleavage furrow during cytokinesis (unpublished data). Formation of this membrane domain is independent of septins and Mid2p (unpublished data). Since septins may bind directly to phospholipids (Zhang et al., 1999), they may initially recognize and bind to this membrane domain before cleavage. One function of Mid2p may be to stabilize septins so that they stay in rings at the cell surface and do not associate with the rest of the membrane domain in the interior of the cleavage furrow.
New family of cytokinesis proteins
Mid2p has significant similarity to several other proteins involved in cytokinesis and/or septin association: S. pombe Mid1p, S. cerevisiae Bud4, and C. albicans Int1 (Gale et al., 1996; Sanders and Herskowitz, 1996; Sohrmann et al., 1996). These proteins begin to define a new family of cytokinesis proteins. All share a very COOH-terminal PH domain and have additional areas of similarity at the COOH terminus. Mid1p is a protein involved in the positioning of the actomyosin contractile ring, since mid1 mutants form rings in random locations at the cell surface. No association between Mid1p and septins have been noted. Genetic tests did not reveal any overlapping functions between Mid1p and Mid2p. Rather, Mid1p and Mid2p may function independently at two different parts of the cell cycle: Mid1p acts in early mitosis to organize and position the actomyosin ring, whereas Mid2p acts in late mitosis to organize the septin rings.
Bud4p and Int1p influence the placement of the cell division site and also appear to associate with the septins. Budding yeast Bud4p is located at the septin rings at the bud neck and functions in positioning the future bud site at a site adjacent to the septin ring from the previous cell cycle (Sanders and Herskowitz, 1996). Although septin rings appear normal in bud4 mutants, Bud4p does not appear to be involved in organizing the septin structure but may use septins as a means for localization. C. albicans Int1p is required for hyphal formation, adherence, and pathogenesis (Gale et al., 1998). Overexpression of Int1p in budding yeast causes reorganization of the septins into spiral-like structures, and Int1p coimmunoprecipitates with budding yeast septins (Gale et al., 2001). In Candida, Int1p colocalizes with a septin ring distal to the germ tube neck and is required for bud site selection.
The functional metazoan homologues of these proteins may be anillins, contractile ring proteins identified in flies, Xenopus, and human (Field and Alberts, 1995; Oegema et al., 2000). Anillins also have a COOH-terminal PH domain, but the amino acid similarity outside of the PH domain to the fungal proteins is low. Recent in vivo and in vitro results show that anillin may function directly to link septins to actin bundles (Oegema et al., 2000; Kinoshita et al., 2002). The COOH-terminal region of anillin that encompasses the PH domain is required for this septin recruitment activity and for its localization to the cleavage furrow. Thus, the COOH-terminal portion of all these proteins, including Mid2p, may share a common function in septin interaction. Since anillin associates with both actin and septins, its function may encompass both the roles of Mid1p and Mid2p. Additional proteins related to anillin are also encoded in the genomes of Drosophila, Caenorhabditis elegans, human, and mice, suggesting the possibility that these proteins have diverse or additional molecular functions (Oegema et al., 2000). Therefore, these fungal and metazoan proteins may serve conserved functions in cytokinesis as important organizers of cleavage furrow components.
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Materials and methods |
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Western analysis
Western blotting was performed with yeast extracts prepared using a mortar and pestle method (Glynn et al., 2001). Anti-GFP antibodies (from J. Kahana and P. Silver, Harvard Medical School, Boston, MA, or K. Sawin, University of Edinburgh, Edinburgh, UK) were used at a 1:1,000 dilution. Anti-HA antibodies (Covance) were used at a 1:1,000 dilution.
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Acknowledgments |
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This work was supported by a Research Project grant from the American Cancer Society.
Submitted: 2 December 2002
Revised: 7 February 2003
Accepted: 7 February 2003
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References |
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