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Cell Division: Bud-site selection is only skin deep
SYLVIA L. SANDERS AND CHRISTINE M. FIELD
CELL DIVISION
Bud-site selection isonly skin deep Yeast cells that divide by budding place new buds in predetermined locations. Recent studies of the subcellular localization of the Bud3 protein help to explain how this occurs. Haploid cells of the yeast Saccharomyces cerevisiae grow by budding, and they select the sites at which to build buds using an 'axial' pattern: a cell produces a new bud at a site adjacent to the site of budding in the previous cell cycle (Fig. 1) [1]. Analysis of the subcellular localization of the Bud3 protein (Bud3p), which is required for axial budding, prompted Chant et al. [2] to provide a molecular model for the generation of the axial budding pattern. Their data suggest that Bud3p provides an intracellular landmark for polarity in each new cell cycle by marking the cortex of the cell at the site of the previous cell division. The results presented in two recent papers by Chant and colleagues are the subject of this review. Although growth by budding is peculiar to yeasts, many aspects of bud-site selection are of general interest. First, the choice of a position at which to build a bud is equivalent to the determination of the future plane for cell division (compare Fig. la and Fig. c). Septa or new membrane in all dividing cells must be placed in a position that allows the appropriate distribution of cytoplasm between the daughter cells, be it equitable or asymmetric. Second, a cell's internal polarity is established when it chooses a site at which to build a bud. Internal polarization is a trait common to both prokaryotic and eukaryotic cells, and is manifest in such phenomena as the placement of flagella and directional movement [3,4].
Surface expansion in yeast cells occurs predominantly in the bud, reflecting an asymmetry in the actin cytoskeleton of the mother-bud pair. In addition, a number of conserved molecules - such as GTPases of the Rho family, proteins containing Src homology 3 (SH3) domains, and motor proteins of the myosin family - are thought to assemble specifically at the site of bud emergence (Fig. 1, inset) [5]. Mutations in the BUD3 gene cause the two types of haploid yeast cells, a and ar, to deviate from the axial budding pattern and to select bipolar bud sites, just as a/ot diploid cells normally do [6]. Mutations in BUD4 and AXL1 produce the same phenotype [6,7]. Cells that bud axially place bud sites directly adjacent to the previous bud site (Fig. 1) [1], so these data suggest that wildtype a and a cells contain a morphological landmark, possibly located at the previous bud site (which is also the site of the previous cell division), to facilitate axial budding [6,8]. Such a landmark would be lacking or ignored in a/a diploids [6,8]. The roles of Bud3p, Bud4p and Axllp, then, might be to recognize, or form part of, the morphogenetic landmark. The axial spatial information is transient: starved cells accumulate without buds and arrest in the GO or G1 phases of the cell cycle; when recovering from this arrest, the cells 'forget' where to place new buds [1,9].
Fig. 1. The axial budding pattern of the yeast Saccharomyces cerevisiae. The mother cell (M) produces a bud (B)at the first bud site. The bud grows to become a fully grown daughter cell (D), which itself produces a bud (DB) from a site adjacent to its own bud site, but opposite the new bud (MB) on the mother cell. Adapted from [1]. Inset: Proteins found at the bud site. Bemlp is an SH3 domaincontaining protein thought to organize actin; Cdc42p is a Rho-family GTPase; the myosin is Myo2p, a type V myosin. © Current Biology 1995, Vol 5 No 11
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Fig. 2. The behavior of neck filaments and the Bud3 protein during budding. Adapted from [2]. Additional candidates for components of a morphogenetic landmark are the 10 nm neck filaments. These filaments, found in the 'neck' between mother and bud, are important for cytokinesis and are thought to comprise the products - collectively termed septins - of the CDC3, CDC1O, CDC11 and CDC12 genes [10-14]. The neck filaments reside at the mother-bud neck, a logical place to locate an axial landmark (Fig. 2) [10-12]. Analysis of mutants suggests that the neck filaments are also important for axial budding [2,15]. Septin homologues are also found in larger eukaryotic cells, and the septin-family member Peanut is required for cytokinesis in Drosophila[16]. The localization of Bud3p is consistent with it having a direct role in facilitating axial budding, either by functioning as a morphological landmark, or by recognizing such a landmark, or both [2]. Like the neck filaments, Bud3p is localized in apparent ring structures at the base of the mother-bud neck. Data from asynchronous cultures and from cells arrested at various stages during the cell cycle suggest that Bud3p is present during M phase (mitosis), persists past cytokinesis, disappears, and then reappears at the next M phase (Fig. 2). Like the hypothetical axial landmark, the localization of Bud3p is transient. Localization of Bud3p to the bud neck depends upon the neck filaments. Conditional temperature-sensitive cdc12 mutants shifted to the non-permissive temperature lose neck filament structures, Cdc12 protein localization and Bud3p localization within five minutes of the temperature shift. These data allowed Chant et al. [2] to propose that a temporal and spatial cycle of interactions is necessary for axial budding to occur. According to their model, Bud3p assembles on the neck filaments during mitosis, the neck filaments disassemble around the time of cytokinesis, and Bud3p remains to direct the adjacent assembly of a new ring of neck filaments (Fig. 2). This model offers a pretty explanation of the axial budding pattern.
Mutations in BUD3 confer no obvious disadvantage on yeast cells [6]. Why, then, do cells go to the trouble of specifying a spatial pattern for bud emergence? A predetermined place to build the bud might facilitate assembly of those protein complexes required to build the bud. Protein complexes might be stabilized by the interaction of subunits not only with each other but also with the cortex (Bud3p). Indeed, requirements for the BUD genes can be revealed in yeast strains that are already otherwise impaired for bud assembly [17]. This model does not explain why a and a haploid cells maintain a different budding pattern from that of a/a diploids. Perhaps the different patterns facilitate cell-type-specific behaviors, such as mating in homothallic a and ot cells or pseudohyphal growth in a/a diploids [18,19]. Are there similarities between bud-site selection in yeast and other events of interest to cell biologists? Bud3p marks the position of the previous cell division, and such markers might help cells to establish other aspects of cell polarity. For example, new growth in cells of the fission yeast, Schizosaccharomyces pombe, occurs at the 'old' end of the cell, not at the end created by the previous cytokinesis [20], perhaps suggesting that a landmark left at the cell-division site discourages future growth. Similar and relevant examples of such inhibition can also be found in the prokaryotic world [4]. Might a protein like Bud3p play roles in other cells? In yeast, Bud3p seems to be an intracellular place-marker that links the cell-division site to the downstream event of establishing an axis of polarity. Bud3p might bind directly to septins through one of its domains and to other proteins using another domain. Both yeast and animal cells maintain septins at their cell-division sites, so a Bud3-like protein could function in animal cells by binding to a septin, such as Peanut, while simultaneously interacting with other proteins.
DISPATCH
Choosing a bud-site defines the site for cell division in yeast (Fig. 1). Although we appreciate yeast as a model organism, it would be surprising if yeast and metazoans use a conserved mechanism for selecting a plane of cell division. Plant and animal cells use microtubule-based structures to determine the cleavage site: plants take advantage of a preprophase band of microtubules, and animal cells use spindle asters to position the cleavage furrow [21,22]. Microtubules have not been implicated in yeast cell-polarity decisions however, because mutations in neither nor 3 tubulin, nor disassembly of microtubules with nocodazole, affect bud growth or placement of axial bud sites [23,24]. In addition, assembly of proteins at the presumptive bud site seems to occur prior to the orientation of extranuclear microtubules towards the bud site, consistent with the idea that microtubules do not underlie primary cell-polarity decisions [8]. Taking these results together, there is no evidence for a common mechanism for choosing the plane of cell division in yeast and animal cells. Yeast may be similar to diatoms, however; like yeast, diatoms can choose division sites independent of spindle position, probably by use of cortical sites [25]. Regardless of the mechanism underlying the choice of a plane of cell division, the cortex and the spindle must communicate. Perhaps molecules like Bud3p send signals to the spindle in budding yeast and diatoms, yet receive signals from the spindle in animal cells; such a signal might then be transmitted to a protein resident in the cleavage furrow, such as actin, myosin or septins. In summary, bud-site selection is selection of a site for cell division, and it also represents the determination of an axis for internal cell polarity. Based on the phenotype of loss-of-function mutations in the BUD3 gene and the subcellular localization of Bud3p, it seems as though Bud3p is involved in marking the former site of cell division to encourage new growth and cell division at a new site. Study of bud-site selection in yeast could illuminate how cells grow at particular points on their surfaces and trigger the assembly of structures at specific sites, but will probably not contribute to a general understanding of how the plane for cell division is chosen in other eukaryotic cells. We would not be surprised, though, if Bud3plike molecules are found in animal cells; such proteins might act in concert with the septins, which are found in animal cells. Like Bud3p in yeast cells, the Drosophila septin, Peanut, also lingers at the site of cell division (the midbody). A Bud3p homologue could cooperate with the septins either by participating in cytokinesis or by determining the internal axis for cell polarity. Acknowledgements: We thank T. Mitchison for helpful discussions, and A. Sil, D. Schneider and M. Maxon for helpful comments. References 1. Chant J, Pringle JR: Patterns of bud-site selection in the yeast Saccharomyces cerevisiae. J Cell Biol 1995, 129:751-765.
2. Chant J, Mischke M, Mitchell E, Herskowitz I, Pringle JR: Role of Bud3p in producing the axial budding pattern of yeast. J Cell Biol 1995, 129:767-778. 3. Stossel TP: On the crawling of animal cells. Science 1993, 260:1086-1094. 4. Maddock JR, Alley MRK, Shapiro L: Polarized cells, polar actions. J Bact 1993, 175: 7125-7129. 5. Sanders SL, Field CM: Septins in common? Curr Biol 1994, 4:907-910. 6. Chant J, Herskowitz : Genetic control of bud-site selection in yeast by a set of gene products that comprise a morphogenetic pathway. Cell 1991, 65:1203-1212. 7. Fujita A, Oka C, Arikawa Y, Katagai T, Tonouchi A, Kuhara S, Misumi Y: A yeast gene necessary for bud-site selection encodes a protein similar to insulin-degrading enzymes. Nature 1994, 372: 567-570. 8. Snyder M, Gehrung S, Page BD: Studies concerning the temporal and genetic control of cell polarity in Saccharomyces cerevisiae. J Cell Biol 1991, 114:515-532. 9. Madden K, Snyder M: Specification of sites for polarized growth in Saccharomyces cerevisiae and the influence of external factors on site selection. Mol Biol Cell 1992, 3:1025-1035. 10. Ford SK, Pringle JR: Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC11 gene product and the timing of events at the budding site. Dev Genet 1991, 12:281-292. 11. Haarer BK, Pringle JR: Immunofluorescence localization of the Saccharomyces cerevisiae CDC12 gene product to the vicinity of the 10-nm filaments in the mother-bud neck. Mol Cell Biol 1987, 7:3678-3687. 12. Kim HB, Haarer BK, Pringle JR: Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC3 gene product and the timing of events at the budding site. Cell Biol 1991, 112:535-544. 13. Byers B, Goetsch L: A highly ordered ring of membrane-associated filaments in budding yeast. J Cell Biol 1976, 69:717-721. 14. Byers B, Goetsch L: Loss of the filamentous ring in cytokinesisdefective mutants of budding yeast. J Cell Biol 1976, 70:35a. 15. Flescher EG, Madden K, Snyder M: Components required for cytokinesis are important for bud site selection in yeast. J Cell Biol 1993, 122:373-86. 16. Neufeld TP, Rubin GM: The Drosophila peanut gene is required for cytokinesis and encodes a protein similar to yeast putative bud neck filament proteins. Cell 1994, 77:371-379. 17. Chant J, Corrado K, Pringle JR, Herskowitz : Yeast BUD5, encoding a putative GDP-GTP echange factor, is necessary for bud site selection and interacts with bud formation gene BEM1. Cell 1991, 65:1213-1224. 18. Nasmyth K, Shore D: Transcriptional regulation in the yeast life cycle. Science 1987, 237:1162-1170. 19. Gimeno CJ, Ljungdahl PO, Styles CA, Fink GR: Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 1992, 68:1077-1090. 20. Fankhauser C, Simanis V: Cold fission: splitting the pombe cell at room temperature. Trends Cell Biol 1994, 4:96-101. 21. Strome S: Determination of cleavage planes. Cell 1993, 72:3-6. 22. Wick SM: Spatial aspects of cytokinesis in plant cells. Curr Opin Cell Biol 1991, 3:253-260. 23. Huffaker TC, Thomas JH, Botstein D: Diverse effects of -tubulin mutations on microtubule formation and function. J Cell Biol 1988, 106:1997-2010. 24. Jacobs CW, Adams AEM, Szaniszlo PJ, Pringle JR: Functions of microtubules in the Saccharomyces cerevisiae cell cycle. J Cell Biol 1988, 107:1409-1426. 25. Wordeman L, McDonald KL, Cande WZ: The distribution of cytoplasmic microtubules throughout the cell cycle of the centric diatom Stephanopyxis turris: their role in nuclear migration and positioning the mitotic spindle during cytokinesis. J Cell Biol 1986, 102:1688-1698.
Sylvia L. Sanders and Christine M. Field, Department of Biochemistry and Biophysics, University of California, San Francisco, California 94143-0448, USA.
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CELL DIVISION
Bud-site selection isonly skin deep Yeast cells that divide by budding place new buds in predetermined locations. Recent studies of the subcellular localization of the Bud3 protein help to explain how this occurs. Haploid cells of the yeast Saccharomyces cerevisiae grow by budding, and they select the sites at which to build buds using an 'axial' pattern: a cell produces a new bud at a site adjacent to the site of budding in the previous cell cycle (Fig. 1) [1]. Analysis of the subcellular localization of the Bud3 protein (Bud3p), which is required for axial budding, prompted Chant et al. [2] to provide a molecular model for the generation of the axial budding pattern. Their data suggest that Bud3p provides an intracellular landmark for polarity in each new cell cycle by marking the cortex of the cell at the site of the previous cell division. The results presented in two recent papers by Chant and colleagues are the subject of this review. Although growth by budding is peculiar to yeasts, many aspects of bud-site selection are of general interest. First, the choice of a position at which to build a bud is equivalent to the determination of the future plane for cell division (compare Fig. la and Fig. c). Septa or new membrane in all dividing cells must be placed in a position that allows the appropriate distribution of cytoplasm between the daughter cells, be it equitable or asymmetric. Second, a cell's internal polarity is established when it chooses a site at which to build a bud. Internal polarization is a trait common to both prokaryotic and eukaryotic cells, and is manifest in such phenomena as the placement of flagella and directional movement [3,4].
Surface expansion in yeast cells occurs predominantly in the bud, reflecting an asymmetry in the actin cytoskeleton of the mother-bud pair. In addition, a number of conserved molecules - such as GTPases of the Rho family, proteins containing Src homology 3 (SH3) domains, and motor proteins of the myosin family - are thought to assemble specifically at the site of bud emergence (Fig. 1, inset) [5]. Mutations in the BUD3 gene cause the two types of haploid yeast cells, a and ar, to deviate from the axial budding pattern and to select bipolar bud sites, just as a/ot diploid cells normally do [6]. Mutations in BUD4 and AXL1 produce the same phenotype [6,7]. Cells that bud axially place bud sites directly adjacent to the previous bud site (Fig. 1) [1], so these data suggest that wildtype a and a cells contain a morphological landmark, possibly located at the previous bud site (which is also the site of the previous cell division), to facilitate axial budding [6,8]. Such a landmark would be lacking or ignored in a/a diploids [6,8]. The roles of Bud3p, Bud4p and Axllp, then, might be to recognize, or form part of, the morphogenetic landmark. The axial spatial information is transient: starved cells accumulate without buds and arrest in the GO or G1 phases of the cell cycle; when recovering from this arrest, the cells 'forget' where to place new buds [1,9].
Fig. 1. The axial budding pattern of the yeast Saccharomyces cerevisiae. The mother cell (M) produces a bud (B)at the first bud site. The bud grows to become a fully grown daughter cell (D), which itself produces a bud (DB) from a site adjacent to its own bud site, but opposite the new bud (MB) on the mother cell. Adapted from [1]. Inset: Proteins found at the bud site. Bemlp is an SH3 domaincontaining protein thought to organize actin; Cdc42p is a Rho-family GTPase; the myosin is Myo2p, a type V myosin. © Current Biology 1995, Vol 5 No 11
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Current Biology 1995, Vol 5 No 11
Fig. 2. The behavior of neck filaments and the Bud3 protein during budding. Adapted from [2]. Additional candidates for components of a morphogenetic landmark are the 10 nm neck filaments. These filaments, found in the 'neck' between mother and bud, are important for cytokinesis and are thought to comprise the products - collectively termed septins - of the CDC3, CDC1O, CDC11 and CDC12 genes [10-14]. The neck filaments reside at the mother-bud neck, a logical place to locate an axial landmark (Fig. 2) [10-12]. Analysis of mutants suggests that the neck filaments are also important for axial budding [2,15]. Septin homologues are also found in larger eukaryotic cells, and the septin-family member Peanut is required for cytokinesis in Drosophila[16]. The localization of Bud3p is consistent with it having a direct role in facilitating axial budding, either by functioning as a morphological landmark, or by recognizing such a landmark, or both [2]. Like the neck filaments, Bud3p is localized in apparent ring structures at the base of the mother-bud neck. Data from asynchronous cultures and from cells arrested at various stages during the cell cycle suggest that Bud3p is present during M phase (mitosis), persists past cytokinesis, disappears, and then reappears at the next M phase (Fig. 2). Like the hypothetical axial landmark, the localization of Bud3p is transient. Localization of Bud3p to the bud neck depends upon the neck filaments. Conditional temperature-sensitive cdc12 mutants shifted to the non-permissive temperature lose neck filament structures, Cdc12 protein localization and Bud3p localization within five minutes of the temperature shift. These data allowed Chant et al. [2] to propose that a temporal and spatial cycle of interactions is necessary for axial budding to occur. According to their model, Bud3p assembles on the neck filaments during mitosis, the neck filaments disassemble around the time of cytokinesis, and Bud3p remains to direct the adjacent assembly of a new ring of neck filaments (Fig. 2). This model offers a pretty explanation of the axial budding pattern.
Mutations in BUD3 confer no obvious disadvantage on yeast cells [6]. Why, then, do cells go to the trouble of specifying a spatial pattern for bud emergence? A predetermined place to build the bud might facilitate assembly of those protein complexes required to build the bud. Protein complexes might be stabilized by the interaction of subunits not only with each other but also with the cortex (Bud3p). Indeed, requirements for the BUD genes can be revealed in yeast strains that are already otherwise impaired for bud assembly [17]. This model does not explain why a and a haploid cells maintain a different budding pattern from that of a/a diploids. Perhaps the different patterns facilitate cell-type-specific behaviors, such as mating in homothallic a and ot cells or pseudohyphal growth in a/a diploids [18,19]. Are there similarities between bud-site selection in yeast and other events of interest to cell biologists? Bud3p marks the position of the previous cell division, and such markers might help cells to establish other aspects of cell polarity. For example, new growth in cells of the fission yeast, Schizosaccharomyces pombe, occurs at the 'old' end of the cell, not at the end created by the previous cytokinesis [20], perhaps suggesting that a landmark left at the cell-division site discourages future growth. Similar and relevant examples of such inhibition can also be found in the prokaryotic world [4]. Might a protein like Bud3p play roles in other cells? In yeast, Bud3p seems to be an intracellular place-marker that links the cell-division site to the downstream event of establishing an axis of polarity. Bud3p might bind directly to septins through one of its domains and to other proteins using another domain. Both yeast and animal cells maintain septins at their cell-division sites, so a Bud3-like protein could function in animal cells by binding to a septin, such as Peanut, while simultaneously interacting with other proteins.
DISPATCH
Choosing a bud-site defines the site for cell division in yeast (Fig. 1). Although we appreciate yeast as a model organism, it would be surprising if yeast and metazoans use a conserved mechanism for selecting a plane of cell division. Plant and animal cells use microtubule-based structures to determine the cleavage site: plants take advantage of a preprophase band of microtubules, and animal cells use spindle asters to position the cleavage furrow [21,22]. Microtubules have not been implicated in yeast cell-polarity decisions however, because mutations in neither nor 3 tubulin, nor disassembly of microtubules with nocodazole, affect bud growth or placement of axial bud sites [23,24]. In addition, assembly of proteins at the presumptive bud site seems to occur prior to the orientation of extranuclear microtubules towards the bud site, consistent with the idea that microtubules do not underlie primary cell-polarity decisions [8]. Taking these results together, there is no evidence for a common mechanism for choosing the plane of cell division in yeast and animal cells. Yeast may be similar to diatoms, however; like yeast, diatoms can choose division sites independent of spindle position, probably by use of cortical sites [25]. Regardless of the mechanism underlying the choice of a plane of cell division, the cortex and the spindle must communicate. Perhaps molecules like Bud3p send signals to the spindle in budding yeast and diatoms, yet receive signals from the spindle in animal cells; such a signal might then be transmitted to a protein resident in the cleavage furrow, such as actin, myosin or septins. In summary, bud-site selection is selection of a site for cell division, and it also represents the determination of an axis for internal cell polarity. Based on the phenotype of loss-of-function mutations in the BUD3 gene and the subcellular localization of Bud3p, it seems as though Bud3p is involved in marking the former site of cell division to encourage new growth and cell division at a new site. Study of bud-site selection in yeast could illuminate how cells grow at particular points on their surfaces and trigger the assembly of structures at specific sites, but will probably not contribute to a general understanding of how the plane for cell division is chosen in other eukaryotic cells. We would not be surprised, though, if Bud3plike molecules are found in animal cells; such proteins might act in concert with the septins, which are found in animal cells. Like Bud3p in yeast cells, the Drosophila septin, Peanut, also lingers at the site of cell division (the midbody). A Bud3p homologue could cooperate with the septins either by participating in cytokinesis or by determining the internal axis for cell polarity. Acknowledgements: We thank T. Mitchison for helpful discussions, and A. Sil, D. Schneider and M. Maxon for helpful comments. References 1. Chant J, Pringle JR: Patterns of bud-site selection in the yeast Saccharomyces cerevisiae. J Cell Biol 1995, 129:751-765.
2. Chant J, Mischke M, Mitchell E, Herskowitz I, Pringle JR: Role of Bud3p in producing the axial budding pattern of yeast. J Cell Biol 1995, 129:767-778. 3. Stossel TP: On the crawling of animal cells. Science 1993, 260:1086-1094. 4. Maddock JR, Alley MRK, Shapiro L: Polarized cells, polar actions. J Bact 1993, 175: 7125-7129. 5. Sanders SL, Field CM: Septins in common? Curr Biol 1994, 4:907-910. 6. Chant J, Herskowitz : Genetic control of bud-site selection in yeast by a set of gene products that comprise a morphogenetic pathway. Cell 1991, 65:1203-1212. 7. Fujita A, Oka C, Arikawa Y, Katagai T, Tonouchi A, Kuhara S, Misumi Y: A yeast gene necessary for bud-site selection encodes a protein similar to insulin-degrading enzymes. Nature 1994, 372: 567-570. 8. Snyder M, Gehrung S, Page BD: Studies concerning the temporal and genetic control of cell polarity in Saccharomyces cerevisiae. J Cell Biol 1991, 114:515-532. 9. Madden K, Snyder M: Specification of sites for polarized growth in Saccharomyces cerevisiae and the influence of external factors on site selection. Mol Biol Cell 1992, 3:1025-1035. 10. Ford SK, Pringle JR: Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC11 gene product and the timing of events at the budding site. Dev Genet 1991, 12:281-292. 11. Haarer BK, Pringle JR: Immunofluorescence localization of the Saccharomyces cerevisiae CDC12 gene product to the vicinity of the 10-nm filaments in the mother-bud neck. Mol Cell Biol 1987, 7:3678-3687. 12. Kim HB, Haarer BK, Pringle JR: Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC3 gene product and the timing of events at the budding site. Cell Biol 1991, 112:535-544. 13. Byers B, Goetsch L: A highly ordered ring of membrane-associated filaments in budding yeast. J Cell Biol 1976, 69:717-721. 14. Byers B, Goetsch L: Loss of the filamentous ring in cytokinesisdefective mutants of budding yeast. J Cell Biol 1976, 70:35a. 15. Flescher EG, Madden K, Snyder M: Components required for cytokinesis are important for bud site selection in yeast. J Cell Biol 1993, 122:373-86. 16. Neufeld TP, Rubin GM: The Drosophila peanut gene is required for cytokinesis and encodes a protein similar to yeast putative bud neck filament proteins. Cell 1994, 77:371-379. 17. Chant J, Corrado K, Pringle JR, Herskowitz : Yeast BUD5, encoding a putative GDP-GTP echange factor, is necessary for bud site selection and interacts with bud formation gene BEM1. Cell 1991, 65:1213-1224. 18. Nasmyth K, Shore D: Transcriptional regulation in the yeast life cycle. Science 1987, 237:1162-1170. 19. Gimeno CJ, Ljungdahl PO, Styles CA, Fink GR: Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 1992, 68:1077-1090. 20. Fankhauser C, Simanis V: Cold fission: splitting the pombe cell at room temperature. Trends Cell Biol 1994, 4:96-101. 21. Strome S: Determination of cleavage planes. Cell 1993, 72:3-6. 22. Wick SM: Spatial aspects of cytokinesis in plant cells. Curr Opin Cell Biol 1991, 3:253-260. 23. Huffaker TC, Thomas JH, Botstein D: Diverse effects of -tubulin mutations on microtubule formation and function. J Cell Biol 1988, 106:1997-2010. 24. Jacobs CW, Adams AEM, Szaniszlo PJ, Pringle JR: Functions of microtubules in the Saccharomyces cerevisiae cell cycle. J Cell Biol 1988, 107:1409-1426. 25. Wordeman L, McDonald KL, Cande WZ: The distribution of cytoplasmic microtubules throughout the cell cycle of the centric diatom Stephanopyxis turris: their role in nuclear migration and positioning the mitotic spindle during cytokinesis. J Cell Biol 1986, 102:1688-1698.
Sylvia L. Sanders and Christine M. Field, Department of Biochemistry and Biophysics, University of California, San Francisco, California 94143-0448, USA.
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