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Myosin-Independent Cytokinesis in Giardia Utilizes Flagella To Myosin-independent cytokinesis in Giardia utilizes PNAS PLUS flagella to coordinate force generation and direct membrane trafficking William R. Hardina, Renyu Lia, Jason Xub, Andrew M. Sheltona, Germain C. M. Alasa, Vladimir N. Minina,b, and Alexander R. Paredeza,1 aDepartment of Biology, University of Washington, Seattle, WA 98195; and bDepartment of Statistics, University of Washington, Seattle, WA 98195 Edited by Edward D. Korn, National Heart, Lung, and Blood Institute, Bethesda, MD, and approved June 13, 2017 (received for review March 28, 2017) Devoid of all known canonical actin-binding proteins, the prevalent trafficking is used to build a new cell wall, known as the cell plate, parasite Giardia lamblia uses an alternative mechanism for cytokine- between daughter cells. After mitosis, interdigitated spindle mi- sis. Unique aspects of this mechanism can potentially be leveraged crotubules maintain antiparallel organization and transition to a for therapeutic development. Here, live-cell imaging methods were cytokinetic apparatus known as the phragmoplast. Microtubules of developed for Giardia to establish division kinetics and the core di- the phragmoplast guide Golgi-derived vesicles to the center of the vision machinery. Surprisingly, Giardia cytokinesis occurred with a division plane by using plus-end–directed trafficking (13). Intrigu- median time that is ∼60 times faster than mammalian cells. In con- ingly, proteomic analysis has revealed that the phragmoplast shares trast to cells that use a contractile ring, actin was not concentrated in many molecular components with the mammalian midbody, sug- the furrow and was not directly required for furrow progression. gesting that, despite appearances, plant cytokinesis employs a mod- Live-cell imaging and morpholino depletion of axonemal Paralyzed ified midbody mechanism (14). Flagella 16 indicated that flagella-based forces initiated daughter cell Discovery of the diverse strategies that cells use to accom- separation and provided a source for membrane tension. Inhibition plish cell division will provide information on the constraints of of membrane partitioning blocked furrow progression, indicating a eukaryotic cell division. Although the myosin II-based actomyosin contractile ring has a central role in Unikont cytokinesis, cells can requirement for membrane trafficking to support furrow advance- – Dic- CELL BIOLOGY ment. Rab11 was found to load onto the intracytoplasmic axonemes divide without myosin II under specific conditions (15 17). tyostelium and mammalian cells with impaired myosin II function late in mitosis and to accumulate near the ends of nascent axonemes. can complete cytokinesis by using traction to pull daughter cells These developing axonemes were positioned to coordinate traffick- apart (15–17). Hence, the use of myosin II may be implemented ing into the furrow and mark the center of the cell in lieu of a mid- on top of a more ancient mechanism that is dependent on cortical body/phragmoplast. We show that flagella motility, Rab11, and actin tension and a Laplace-like pressure property of cells that serves to coordination are necessary for proper abscission. Organisms repre- minimize the surface area-to-volume ratio (18, 19). Moreover, senting three of the five eukaryotic supergroups lack myosin II of the phylogenetic distribution of myosin II is limited to Unikonts with actomyosin contractile ring. These results support an emerging view one known exception that may be an example of horizontal gene that flagella play a central role in cell division among protists that transfer (20, 21); thus, three of the five eukaryotic supergroups use lack myosin II and additionally implicate the broad use of membrane an alternative to the canonical “purse-string” mechanism of cy- tension as a mechanism to drive abscission. tokinesis, as is the case in plants (22). The number and types of alternative mechanisms remain understudied (23), especially in actin | Rab11 | PF16 | tubulin | mitosis cells that have been difficult to culture and for which molecular and imaging methodologies are lacking. ell division is a fundamental process whereby cellular content is The study of giardial mitosis and cytokinesis has been chal- Cpartitioned for proliferation. Drugs that target this process are lenging because of a lack of effective cell synchronization and live- immensely valuable as cancer therapeutics (1) and have promise cell imaging, which is complicated by Giardia’s lethal sensitivity to for treating infectious disease (2–4). Giardia lamblia (synonymous with Giardia intestinalis and Giardia duodenalis)isacommonwa- Significance terborne pathogen that infects 280 million people each year (5). In Giardia addition to being a major parasite, belongs to possibly the Many protists, including Giardia, lack myosin II and thus are earliest diverging eukaryotic lineage and could provide clues about unlikely to use the canonical contractile mechanism of cell di- early mechanisms of cell division (6, 7). Despite the fundamental vision. Giardia depends solely on its flagella for motility; here, requirement for division to proliferate, the mechanisms underlying we show that flagella function is also required to drive Giardia cytokinesis vary across the evolutionary tree (8). As has daughter cells in opposite directions for cytokinesis. Addition- actin but lacks myosin and all known actin cytoskeletal components ally, just before cytokinesis, Rab11 accumulated in the forming required for amoeboid motility and cytokinesis (9), it is not clear furrow and the nascent intracytoplasmic axonemes were ori- how the division plane is specified, if division involves force gen- ented to deliver Rab11. This mechanism constitutes a means to eration for daughter cell separation, or if division occurs strictly mark the center of the cell and guide trafficking to the furrow. through a membrane remodeling mechanism (8). These results support an emerging view that flagella play a Our most complete mechanistic understanding of cytokinesis central role in cell division among protists that lack myosin II. comes from studies of model organisms that are Unikonts, a group that comprises the supergroups Opisthokonta (e.g., yeast Author contributions: W.R.H. and A.R.P. designed research; W.R.H., R.L., A.M.S., and to man) and Amoebozoa (e.g., Dictyostelium discoideum) (10). G.C.M.A. performed research; W.R.H. contributed new reagents/analytic tools; W.R.H., Animals use an actomyosin contractile ring to pinch the plasma R.L., J.X., A.M.S., V.N.M., and A.R.P. analyzed data; and W.R.H. and A.R.P. wrote the paper. membrane down onto the midbody microtubules (11). Abscis- The authors declare no conflict of interest. sion at the midbody is subsequently completed by plus-end– This article is a PNAS Direct Submission. directed vesicle trafficking to the center of the midbody and 1To whom correspondence should be addressed. Email: [email protected]. – ESCRT-III mediated scission (12). Plants lack myosin II and the This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. pinching down mechanism for scission; instead, extensive membrane 1073/pnas.1705096114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1705096114 PNAS Early Edition | 1of10 Downloaded by guest on September 27, 2021 oxygen concentrations greater than 5% (24). Initial studies com- opposition to each other. We propose that caudal flagella flexion pletely missed the presence of a mitotic spindle, leading to the (i.e., sustained bending) is important for initiating daughter cell proposal of several incompatible mechanisms for cell division (25– separation. As the intracytoplasmic axonemes of the caudal fla- 29). Ultimately, Giardia’s mitotic stages were found to begin sim- gella are nucleated by basal bodies that are intimately associated ilarly to those of plants and animals (30). The spindle, however, is with the nascent ventral discs (40), this arrangement could facili- completely disassembled before cytokinesis, and division occurs tate positioning the daughter ventral discs. Indeed, these intra- across the long rather than the short axis of the cell (30–32). The cytoplasmic axonemes were observed to flex in opposite directions mechanism for coordinating membrane remodeling during cyto- during cytokinesis, and, as the daughter cells moved in opposite kinesis and the timing of major events remain unexplored. Here we directions, the plasma membrane appeared to stretch around the combine the use of a hypoxic stage-top incubator, a newly de- two new discs and the furrow advanced between them (Fig. 1B and veloped low-fluorescence media formulation, and a bright fast- Movies S1 and S2). Abscission occurred after daughter cells folding fluorescent protein tag (33) that allow robust imaging of transitioned into a tail-to-tail orientation and swam in opposite Giardia throughout the cell cycle. We use these technical advances directions, presumably driven by anterior flagella power strokes. to uncover the core division machinery and establish a working After scission, daughter cells quickly attached to the cover glass, model for Giardia’s mechanism of myosin-independent cytokinesis. indicating that the nascent ventral discs are functional upon cy- tokinesis despite the immaturity of the ventral flagella, which have Results been proposed to support attachment (41). Notably, the ventral Giardia Uses a Tubulin Reservoir to Support Rapid Mitosis and Ventral and posterolateral flagella were observed to grow at different rates Disk
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