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First published online August 24, 2006
doi: 10.1242/10.1242/jcs.03193

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Microtubule dynamics in the budding yeast mating pathway

Department of Biology, University of North Carolina, 622 Fordham Hall, Chapel Hill, NC 27599, USA

^* Author for correspondence (e-mail: kerry_bloom{at}unc.edu)

Accepted 26 July 2006

	Summary

Top Summary Introduction MT dynamics during S.... Formation of the MT-shmoo... MT dynamics during nuclear... Mitosis during the first... Conclusions and future... References

 
In order for haploid gametes to fuse during fertilization, microtubules (MTs) must generate forces that are sufficient to move the nuclei together. Nuclear movements during fertilization rely on microtubule-associated proteins (MAPs), many of which have been characterized extensively during mitosis. A useful model system to study MT-dependent forces before nuclear fusion, or karyogamy, is the mating pathway of budding yeast. Dynamic MTs are guided to the mating projection (shmoo tip) when plus-end-binding proteins interact with polarized actin microfilaments. If two shmoo tips are in proximity they may fuse, dissolving the MT-cortical interactions. Subsequently, oppositely oriented MT plus ends interact and draw the nuclei together. The plus-end-binding proteins in the yeast mating pathway are conserved in metazoan cells and may play a role in higher eukaryotic fertilizaton. Thus, understanding the mechanism of plus end orientation and karyogamy in budding yeast will reveal mechanisms of MT-dependent force generation conserved throughout evolution.

Key words: Kar3p, Bik1p, Kar9p, Nuclear congression, Microtubules

	Introduction

Top Summary Introduction MT dynamics during S.... Formation of the MT-shmoo... MT dynamics during nuclear... Mitosis during the first... Conclusions and future... References

 
Eukaryotic fertilization requires microtubule (MT)-dependent nuclear movements for gamete fusion. MTs are polarized polymers nucleated at centrosomes or spindle pole bodies (SPBs) that are composed primarily of - and ß-tubulin dimers. MTs grow and shorten through rapid tubulin addition and subtraction at their plus ends, a process known as dynamic instability (Inoue and Salmon, 1995; Kirschner and Mitchison, 1986). Dynamic instability is not inhibited when MT plus ends interact with attachment sites or the plus ends of oppositely oriented MTs. Consequently, MTs can facilitate the movement of subcellular structures to which they attach. MT plus ends are linked to cortical sites or oppositely oriented MTs by plus-end-binding proteins, a subset of which are plus-end-tracking proteins (+TIPs) that preferentially accumulate on growing MTs (Akhmanova and Hoogenraad, 2005; Schuyler and Pellman, 2001). When a MT encounters an attachment site, the plus-end-binding proteins act as an adaptor to tether the dynamic plus end to the attachment site. After the MTs attach, growth and shrinkage continues, and because MTs are anchored at microtubule-organizing centers, the attached structures can oscillate, a behavior seen during chromosome directional instability in mitosis (Skibbens et al., 1993). Alternatively, directed movement may dominate as a consequence of persistent MT polymerization or depolymerization, such as during anaphase chromosome movement. A model system that allows us to examine MT attachment, MT-dependent oscillations, and MT-MT interactions is the mating pathway of Saccharomyces cerevisiae. In this pathway, nuclei are oriented towards the site of cell fusion by MTs and attach to the cell cortex. After the two cells fuse, the nuclei are then drawn together by MT-MT interactions. Thus, information about MT dynamics revealed by studies of the mating pathway is relevant to processes ranging from chromosome segregation to metazoan fertilization that are critical for cellular survival.

	MT dynamics during S. cerevisiae mating

Top Summary Introduction MT dynamics during S.... Formation of the MT-shmoo... MT dynamics during nuclear... Mitosis during the first... Conclusions and future... References

 
When budding yeast cells of opposite mating type are mixed, a signal transduction cascade is initiated to induce the mating pathway (Fig. 1A) (Bardwell, 2005). The mating response includes the polarization of the unbudded cell and formation of a mating projection known as the shmoo (MacKay and Manney, 1974; Tkacz and MacKay, 1979). Cells of opposite mating types fuse at the shmoo tips (Rose, 1996).

View larger version (83K): [in this window] [in a new window]   Fig. 1. Microtubule (MT) and plus-end-tracking protein (+TIP) distribution in the budding yeast mating pathway. (A) MT morphologies through the first zygotic division. Upper panel shows fluorescent images of GFP fused to tubulin (GFP-Tub1p) in the mating pathway. Lower panel are corresponding DIC images. (B) +TIP localization in pheromone-treated cells. Schematic of mating cell is shown on the left. Formation of the shmoo after cell polarization allows MT plus ends to interact with the shmoo tip. Bik1p-3xGFP localizes to MT plus ends in the shmoo tip, free MT plus ends, and to the SPB (right, bright-field image is displayed in lower right corner). Bars, 2 µm.

After cell fusion, MTs that were originally attached to the shmoo tip interact with MTs from the other cell to form a bridge between the two nuclei (Hasek et al., 1987; Read et al., 1992). The cross-linked MTs then coordinately depolymerize, drawing the nuclei together for karyogamy (Maddox et al., 1999; Molk et al., 2006; Rose, 1996). Inhibitor studies and genetic analysis of tubulin mutants have demonstrated that MTs are required for karyogamy (Delgado and Conde, 1984; Huffaker et al., 1988). [Class I karyogamy mutants exhibit defective nuclear congression whereas class II karyogamy mutants do not undergo nuclear fusion (Kurihara et al., 1994).] Genetic analyses have similarly demonstrated that plus-end-binding proteins are required for nuclear congression and for karyogamy (Berlin et al., 1990; Meluh and Rose, 1990; Schwartz et al., 1997) (Fig. 1B).

MT dynamics in the mating pathway are thus crucial for orientation of the nucleus to the shmoo tip and nuclear congression. They are also required at mitosis in the first zygotic division. Here, we review what is known about these processes and highlight some outstanding questions.

	Formation of the MT-shmoo tip attachment

Top Summary Introduction MT dynamics during S.... Formation of the MT-shmoo... MT dynamics during nuclear... Mitosis during the first... Conclusions and future... References

 
There are three steps in the formation of the MT-shmoo tip attachment (Fig. 2 and Table 1): (1) polarization of the actin cytoskeleton and formation of the shmoo tip; (2) nuclear orientation - guidance of MT plus ends toward the shmoo tip along actin cables; (3) attachment of MT plus ends to the shmoo tip cell cortex.

View larger version (26K): [in this window] [in a new window]   Fig. 2. Schematic of +TIP function during nuclear orientation to the shmoo tip. (A) In unbudded cells, Kar9p (red) and Bik1p (purple) are transported along the MT (green) by the motor protein Kip2p (brown) to the plus end where Bim1p (blue) binds. Kar3p (cyan) and Cik1p (yellow) form heterodimers that localize near the plus ends. (B) After cell polarization, the MT plus end interacts with actin cables (red) via Myo2p (gray). Myo2p links to Bim1p through Kar9p and moves the nucleus towards the shmoo tip. (C) Once at the shmoo tip, the plus end interacts persistently with the shmoo tip. This interaction could be mediated by proteins at the shmoo tip cortex that act as attachment factors.

Polarization
Cell polarization is initiated when pheromones bind to cell surface receptors that are coupled to a heterotrimeric G-protein signaling cascade (reviewed by Bardwell, 2005). Disassociation of the G subunit, Gpa1p, from the Gß subunits activates Cdc42p, a key component of the cell polarization pathway, and induces the formation of the polarisome, a protein complex that includes Pea2p, Spa2p, Bud6p, and Bni1p (Bardwell, 2005; Etienne-Manneville, 2004; Pruyne and Bretscher, 2000). Gpa1p is required for localization of Bni1p to the future shmoo site, and this event is coupled to Cdc42p activation to polarize the cell (Matheos et al., 2004). As the cell polarizes, new cell-surface materials are synthesized to form the shmoo (Tkacz and MacKay, 1979). After shmoos form, cells polarize towards and mate with the partner expressing the highest pheromone concentration - this process is termed courtship (Jackson and Hartwell, 1990). If cells are treated with synthetic mating pheromone, a default mating pathway is initiated and the shmoo forms next to the bud scar from previous divisions (Dorer et al., 1995). In both cases, the major cytoskeletal component required for cell polarization is actin (Hasek et al., 1987; Read et al., 1992).

Orientation
After the cell polarizes, MT plus ends are transported along actin cables to the shmoo tip; because the minus ends are attached to the SPB, the result is orientation of the nucleus to the shmoo tip (Fig. 2B). Nuclear orientation requires the +TIP Bim1p and Kar9p. Bim1p, the budding yeast EB1 (end binding protein) ortholog, binds to MTs and preferentially localizes to growing plus ends (Maddox et al., 2003; Tirnauer et al., 1999). Bim1p interacts with Kar9p to link MTs to the actin network. Kar9p is transported to MT plus ends and serves as an adaptor protein between Bim1p and the actin-associated type V myosin motor Myo2p (Hwang et al., 2003; Korinek et al., 2000; Lee et al., 2000; Maekawa et al., 2003; Yin et al., 2000). Once Kar9p links the plus end to the actin network, Myo2p moves along polarized actin pulling the nucleus to the shmoo tip. When both mating partners have defects in nuclear orientation, such as kar9 cells, karyogamy can still occur when the plus ends of MTs stochastically interact (Molk et al., 2006). When karyogamy mutants, such as kar9, are mated to a wild-type cell, no defects in nuclear congression occur (Berlin et al., 1990; Kurihara et al., 1994). In this unilateral condition, it is likely that the wild-type protein diffuses quickly into the other cell body after fusion and binds MT plus ends, driving nuclear congression. Therefore, nuclear orientation is not necessary for karyogamy, but proteins such as Kar9p and Myo2p that guide plus ends to the shmoo tip are required for high-fidelity nuclear congression. Because the plus end is the site of MT-MT cross-linking for nuclear congression, guidance of plus ends to the shmoo tip significantly increases the probability that MTs from the different nuclei will interact.

Attachment
After MTs have been transported to the shmoo tip along microfilaments, their plus ends interact with the cell cortex (Maddox et al., 1999; Maddox et al., 2003). Plus-end-binding proteins keep polymerizing and depolymerizing plus ends at the shmoo tip. Thus far, only Bim1p has been proposed to link polymerizing plus ends to the shmoo tip (Maddox et al., 2003). Depolymerizing plus ends attach to the shmoo tip via Kar3p and Bik1p. Kar3p is a kinesin 14 motor protein that has minus-end-directed motility (Endow et al., 1994; Maddox et al., 2003; Meluh and Rose, 1990). Kar3p forms a heterodimer with the light chain Cik1p, and this heterodimer is targeted to the plus end, where Kar3p promotes depolymerization (Barrett et al., 2000; Maddox et al., 2003; Sproul et al., 2005). In kar3 cells, MTs lose their persistent attachment to the shmoo tip when switching to depolymerization and shorten back to the SPB (Maddox et al., 2003). Therefore, Kar3p is proposed to anchor depolymerizing plus ends to the shmoo tip, preventing their detachment and shortening.

Bik1p, the CLIP-170 ortholog in budding yeast, helps maintain depolymerizing MTs at the shmoo tip and is required for nuclear congression (Berlin et al., 1990; Lin et al., 2001; Molk et al., 2006). CLIP-170 is a MT-binding protein that was originally characterized as a linker between MTs and membranes in metazoan cells (Vaughan, 2005). In budding yeast, Bik1p may directly interact with the plasma membrane, anchoring MTs to the shmoo tip. In pheromone-treated kar3 cells, Bik1p localizes to the plus end, which suggests Bik1p localization does not depend on Kar3p (Molk et al., 2006). However, in kar3 cells MTs detach from the shmoo tip when they switch to shortening (Maddox et al., 2003), which demonstrates that Bik1p is necessary but not sufficient for MT interactions with the shmoo tip.

In addition to plus-end-binding proteins, other proteins involved in cell polarization could play a role in MT-shmoo-tip attachments. Kip2p is a plus-end-directed kinesin-like protein that transports both Kar9p and Bik1p along MTs in mitotic cells but kip2 cells do not exhibit karyogamy defects (Carvalho et al., 2004; Maekawa et al., 2003; Miller et al., 1998). It is unknown whether, after nuclear orientation, actin cables are required to maintain MT attachments. In myo2-17, myo2-18 and myo2-20 mutants that lack functional Myo2p myosin motors, MTs appear detached from the shmoo tip but the SPB remains near the base of the mating projection (Hwang et al., 2003). This phenotype is reminiscent of kar3 cells, and Myo2p may play a direct role in attachment of MTs to the shmoo tip. Furthermore, proteins that establish cell polarity and are found at the plasma membrane, such as Gpa1p or polarisome components, may link the MT to the shmoo tip. Thus, it is likely that additional proteins are required to couple MTs to the shmoo tip.

Models for MT attachment to the shmoo tip
How do MTs attach to the cell cortex at the shmoo tip? The leading hypothesis is the cortical anchorage model in which polymerizing MTs have Bim1p on their plus ends and are kept at the shmoo tip by Kar9p that is linked to the actin network or polarity proteins at the cell cortex (Fig. 3A) (Maddox et al., 2003; Miller et al., 1999). When MTs switch to depolymerization, the plus ends are held at the shmoo tip by Bik1p and Kar3p. Kar3p is anchored to the cell cortex by an unknown attachment factor. Candidates for this include a component of the heterotrimeric G-protein complex or the polarisome.

View larger version (28K): [in this window] [in a new window]   Fig. 3. Models for MT interaction with the shmoo tip. (A) As hypothesized by Maddox et al. (Maddox et al., 2003), an unknown binding factor may interact with Kar3p to keep this motor near the cortex. Bim1p may link the plus end to the shmoo tip through Kar9p. During polymerization, Bim1p and Kar9p maintain the interactions between the plus end and the shmoo tip. A switch to depolymerization will cause Bim1p to leave the plus end while Kar3p maintains the attachment of the MT to the tip. (B) Plus end cycling hypothesis. In this model, the MT plus end can detach from the shmoo tip at some frequency governed by the affinity of +TIPs for either the cortex or the ends of actin cables. After detachment, the MT shrinks back to the SPB while a newly nucleated MT grows and interacts with the actin network. The newly nucleated MT is transported by Myo2p along the actin network towards the shmoo tip, generating movement of the nucleus towards the mating projection. Once at the shmoo tip, the MT attaches and begins to polymerize, moving the nucleus away from the shmoo tip. Therefore, the combination of MT transport and MT dynamics at the shmoo tip generates nuclear oscillations.

One way to distinguish between the two models would be an analysis of shmoo tip attachment in tropomyosin mutants in which actin cables are defective. The cortical anchorage model predicts that actin cables are not required once the MT interacts with the shmoo tip. The plus end cycling model requires actin cables for MT-shmoo-tip attachment.

	MT dynamics during nuclear congression

Top Summary Introduction MT dynamics during S.... Formation of the MT-shmoo... MT dynamics during nuclear... Mitosis during the first... Conclusions and future... References

 
After cell fusion, MTs rapidly associate during nuclear congression (Maddox et al., 1999). Nuclear congression requires Bik1p and Kar3p (Fig. 4A) (Berlin et al., 1990; Meluh and Rose, 1990). In early models for nuclear congression based on genetic analysis, Kar3p was proposed to cross-link and slide oppositely oriented MTs, which would result in extensive MT overlap (Fig. 4B) (Rose, 1996). This model predicts that plus ends would be located near the SPBs. However, live cell fluorescence microscopy has demonstrated that MTs do not slide past one another over long distances and that cross-linking occurs only near the plus ends (Molk et al., 2006). Therefore, we favor a new model for nuclear congression that focuses on plus end interactions (Fig. 4B). In this model, the opposing plus ends at the shmoo tip are juxtaposed and cross-linking occurs with a minimum of MT-MT sliding. The cross-linking is initiated by the Kar3p-Cik1p heterodimer and Bik1p could also play a role. Once plus ends interact, we propose that the MTs switch to persistent shortening to drive both nuclei together.

View larger version (70K): [in this window] [in a new window]   Fig. 4. Karyogamy in budding yeast. (A) Models for nuclear congression in budding yeast. (Left) Sliding cross-bridge model for nuclear congression. In this model, Kar3p-Cik1p slides MTs past one another and then depolymerization occurs at the SPBs. (Right) Plus end model for nuclear congression. MTs are linked at the plus end by Kar3p-Cik1p and then depolymerize, drawing both nuclei together for karyogamy. (B) MT dynamics in the wild type and karyogamy mutants. (Left) Wild-type MT dynamics during nuclear congression. (Middle) MT dynamics when nuclear orientation is defective. MTs grow and shrink the cytoplasm and rely on stochastic interactions to cross-link and perform nuclear congression. (Right) MT dynamics when cross-linking is defective. MTs undergo dynamic instability in the cytoplasm but never interact. A failure to undergo karyogamy does not block the zygotic bud from forming, resulting in the assembly of two mitotic spindles within the same cell.

	Mitosis during the first zygotic division

Top Summary Introduction MT dynamics during S.... Formation of the MT-shmoo... MT dynamics during nuclear... Mitosis during the first... Conclusions and future... References

 
Little is known about mitosis during the first zygotic division. Thus far, it appears spindle elongation during the first zygotic division is similar to vegetative divisions (Maddox et al., 1999). A failure to perform karyogamy produces a single cell that has two haploid nuclei, each of which generates its own mitotic spindle. In experiments using kar1 mutants with two spindles, the response to DNA damage was determined to inhibit anaphase onset locally within a single nucleus (Demeter et al., 2000). A similar analysis of other karyogamy mutants may uncover characteristics about how cell division occurs in the presence of multiple spindles.

	Conclusions and future perspectives

Top Summary Introduction MT dynamics during S.... Formation of the MT-shmoo... MT dynamics during nuclear... Mitosis during the first... Conclusions and future... References

 
MT plus ends and plus-end-binding proteins are required for efficient mating in budding yeast. Plus ends are crucial for attachment to the shmoo tip and MT-MT interactions during nuclear congression. Plus-end-binding proteins required for MT dynamics in mating include Bim1p, Bik1p and Kar3p. Bik1p and Kar3p function at the kinetochore in budding yeast (Lin et al., 2001; Middleton and Carbon, 1994; Tanaka et al., 2005), which suggests MT linkages could be similar at the shmoo tip and centromere. Thus, the shmoo tip attachment site could also serve as a model for kinetochore-MT attachments. Future studies of MT-binding proteins may reveal further karyogamy factors that are necessary for nuclear congression. There are some differences between yeast karyogamy, in which dynein is not required, and metazoan fertilization, which does require cytoplasmic dynein (Molk et al., 2006; Payne et al., 2003). However, plus-end-binding proteins may well have conserved functions in yeast and metazoans that facilitate nuclear movements. Therefore, understanding how MT dynamics affect shmoo tip attachment and nuclear congression could reveal underlying mechanisms that apply to a variety of problems in cell biology.

	Acknowledgments

 
We thank David Bouck, Richard Cheney, Julian Haase, Ted Salmon, David Stone and members of the Bloom and Salmon laboratories for helpful discussions and critical reading of the manuscript. We would like to acknowledge Paul Maddox for initiating the live cell studies of karyogamy and his insight into the mechanisms that govern shmoo tip attachment. This work was supported by the National Institutes of Health grant GM-32238 (to K.B.).

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Top Summary Introduction MT dynamics during S.... Formation of the MT-shmoo... MT dynamics during nuclear... Mitosis during the first... Conclusions and future... References

 

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