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First published online October 22, 2003
doi: 10.1242/10.1242/jcs.00835

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Cytoplasmic dynein in fungi: insights from nuclear migration

CREST Research Project, Kansai Advanced Research Center, Communications Research Laboratory, 588-2 Iwaoka, Iwaoka-cho, Nishi-ku, Kobe 651-2492, Japan

View larger version (37K): [in a new window]   Fig. 1. Organization of dynein and dynactin, and their interaction with a microtubule and another cellular organelle. (A) Dynein organization, showing (for simplicity) only two molecules of DIC, DLIC and DLC (B) Dynactin organization. (C) Model for interaction of dynein/dynactin with a microtubule and cellular structure (Karki and Holzbaur, 1995; Holleran et al., 1996). For simplicity, only DHC, DIC, p150Glued, p50 and Arp1 are shown. Dynactin interacts with dynein via association of a middle portion of p150Glued with DIC. Dynein interacts with a microtubule at the tip of the stalk of DHC, whereas dynactin interacts with the microtubule at an N-terminal globular domain of p150Glued. Dynein/dynactin interacts with a cellular structure via an Arp1 filament. Arrow indicates the direction of dynein/dynactin movement. The minus (–) and plus (+) ends of the microtubule are indicated.

View larger version (46K): [in a new window]   Fig. 2. A role of dynein in the budding yeast S. cerevisiae. Dynein mediates attachment of astral microtubules (AMT; purple lines) to the bud cortex and sliding of the microtubules on the attachment site (red arrow). Consequently, the nucleus (blue sphere) moves into the bud neck (black arrow). Dynein also drives cortical sliding of microtubules in the mother cell (red arrow), generating an opposing force on the nucleus. As a result, the nucleus remains at the neck with oscillations between the mother and bud cells (black arrows). The opposing forces also orient the mitotic spindle along the cell axis, and contribute to spindle pole separation.

View larger version (23K): [in a new window]   Fig. 3. Models of dynein-dependent nuclear migration and organelle transport. (A) Dynein-dependent nuclear migration. Microtubules emanate from the SPB, with their plus ends (+) distal to it. Immotile dynein is recruited to the microtubule distal end together with dynactin and LIS1 by CLIP-170. Dynein, dynactin and LIS1 are delivered to the dynein-anchoring factor (Num1 or a Num1-delated factor, ApsA) on the cell cortex by microtubule elongation. The anchoring factor anchors dynein, dynactin and LIS1, and activates dynein motility. The motile dynein moves on the microtubule toward the minus end, driving nuclear migration toward the cortex. (B) Organelle transport. Dynein, dynactin and LIS1 are delivered to the dynein-anchoring factor on the organelle surface by microtubule elongation, as in A. The anchoring factor anchors and activates dynein. The activated dynein moves on the microtubule, transporting the organelle. The plus (+) and minus (–) ends of the microtubule are indicated. Black arrows indicate microtubule elongation, and red arrows indicate dynein movement.

View larger version (51K): [in a new window]   Fig. 4. Roles of dynein in the fission yeast, S. pombe. (A) Nuclear migration. During meiotic prophase, dynein mediates the cortical attachment of astral microtubules (purple lines) emanating from the SPB (red circles) and drives their lateral sliding at the attachment site toward the cell end (red arrow), resulting in movement of the nucleus toward the end (black arrow). The microtubules shorten during the movement and eventually disappear when the nucleus reaches the cortical attachment site of the microtubule. The nucleus moves towards the opposite side (black arrow) when cortical attachment of microtubules is established in the other side of the cell (red arrow). The nucleus moves until it reaches the cortical attachment site of the microtubules. This series is repeated during meiotic prophase. (B) Telomere clustering. During mitotic interphase, centromeres (white circles) are located near the SPB, whereas telomeres (red rectangles) are located away from it, probably in association with nuclear membrane. Upon entering meiosis, telomeres move towards the SPB to form a telomere cluster, which remains near the SPB during meiotic prophase, whereas centromeres dissociate from the SPB. Dynein plays a role in telomere clustering. (C) Nuclear fusion. Upon nitrogen starvation, haploid fission yeast cells with opposite mating types fuse to form a zygote containing a diploid nucleus. Dynein and Klp2 drive fusion of two haploid nuclei in the zygote.

View larger version (35K): [in a new window]   Fig. 5. Roles of dynein in filamentous fungi. (A) Nuclear migration. During the elongation of the hypha by the apical growth (grey arrow), the nuclei migrate towards the growing tip (black arrows) and distribute relatively evenly along the cell length – this migration depends on dynein. Note that the migration distance of each nuclei differs. (B) Organelle transport. In the hyphae, vesicles move in both retrograde (black arrows) and anterograde (blue arrows) directions. It is proposed that dynein drives the retrograde transport of vesicles (blue circles), whereas kinesin drives the anterograde transport (red circles).

View larger version (33K): [in a new window]   Fig. 6. Roles of dynein in the dimorphic fungus, U. maydis. (A) Nuclear migration. In G2 phase, cytoplasmic microtubules (MT) emanate from a pair of two spherical structures located in the bud cell, unlike those in S. cerevisiae (Steinberg et al., 2000). The structures consist of tubulin and are thus called paired tubulin structures (PTS). The microtubules are probably oriented in such a way that the plus ends are distal to the PTS. The nucleus migrates into the bud cell before undergoing mitotic division (black arrow). This migration depends on dynein. After the nucleus moves into the bud cell, astral microtubules are formed exclusively from the SPB and the nucleus undergoes division. (B) Endosome transport. Endosome distribution changes during the cell cycle (Wedlich-Söldner et al., 2000; Wedlich-Söldner et al., 2002b). In particular, in a small-bud stage, endosomes (green circles) accumulate in the small bud. During this stage, microtubules emanate from PTS located in the small bud. Because of this microtubule organization, the minus ends are probably located in the small bud, whereas the plus ends are located at the distal end of the mother cell. Dynein probably transports endosomes in the minus-end direction, causing accumulation of endosomes in the bud. By contrast, Kin3 probably transports endosomes in the plus-end direction.