Organelle Transport: Dynamic Actin Tracks for Myosin Motors
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View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Current Biology Vol 18 No 22 R1066 5. McMahon, T.A., and Cheng, G.C. (1990). The 9. Full, R.J., and Koditschek, D.E. (1999). implications for energy cost. J. Appl. Physiol. mechanics of running: How does stiffness Templates and Anchors: Neuromechanical 97, 2266–2274. couple with speed? J. Biomech. 23, 65–78. hypotheses of legged locomotion on land. 14. McGeer, T. (1993). Dynamics and control of 6. Raibert, M.H., Chepponis, M., and Brown, H. J. Exp. Biol. 202, 3325–3332. bipedal locomotion. J. Theor. Biol. 163, (1986). Running on four legs as though they 10. Seyfarth, A., Geyer, H., and Herr, H. (2003). 277–314. were one. IEEE J. Robotics Automation 2, Swing-leg retraction: a simple control model 15. Muybridge, E. (1887). Muybridge’s Complete 70–82. for stable running. J. Exp. Biol. 206, 2547–2555. Human and Animal Locomotion (Courier Dover 7. 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Muscle mechanical R1022–R1031. advantage of human walking and running: DOI: 10.1016/j.cub.2008.09.050 Organelle Transport: Dynamic Actin actin transport track as the myosin moves [5] (Figure 1B). Tracks for Myosin Motors Extension of actin transport tracks during organelle motility explains an apparent paradox in pigment granule Transport of cargo by molecular motors on microtubule and actin filament movement on actin. The length of tracks is a fundamental property of eukaryotic cells. A new study reports individual actin filaments associated that actin dynamics are required in cells for myosin I and V motor proteins to with pigment granules is short, ranging transport their organelle cargos on actin tracks. from 0.2 to 3 mm for the majority of filaments, with an average of 1.3 mm Louise Cramer respectively, along actin tracks [8,9], yet individual pigment granules in frog pigment cells (known as are transported by myosin V on actin Transport of cargo inside cells was melanophores). The term ‘actin tracks over far greater total distances a landmark discovery over 200 years dynamics’ in this context means that (from 3 to >10 mm) [5,9]. One ago [1]. Intracellular transport is individual actin filaments are rapidly reasonable explanation of this essential for eukaryotes and a variety of polymerizing and depolymerizing. paradox, with no a priori requirement cargo is transported — membrane- Actin and microtubule dynamics are for actin dynamics, is that myosin V bound organelles, such as the already known to be important for other motors switch between static actin nucleus, Golgi, secretory and distinct types of cargo transportation, tracks to increase the total distance endocytic vesicles, as well as such as cargo surfing on the ends of moved by an individual cargo. non-membrane-bound particles such polymerizing microtubules, or actin- However, switching of static tracks is as mRNA, and proteins involved in polymerization-mediated rocketing of not favoured because insufficient signalling and establishing cell polarity. some endosomes and bacterial/viral tracks touch individual organelles [5], In addition, some bacteria and viruses pathogens (Figure 1A). In rocketing and this switching is also not favoured subvert intracellular cargo transport motility, actin dynamics are important in a mathematical model [8]. The systems to infect human and other because actin polymerization is revelation that the actin transport animal cells and to cause disease. directly coupled to providing the force tracks are dynamic [5] adds a new The most widely used system for that drives the movement of the dimension, allowing dynamic extension transporting cargo in eukaryotic cells is endosome or pathogen forwards of actin transport tracks during myosin- directed movement driven by (Figure 1A). However, it is less V-based organelle motility to be molecular motors moving along immediately obvious why actin a rational solution to the paradox transport tracks made of cytoskeletal dynamics should be important for (Figure 1B). Conceivably, actin polymers — kinesin and dynein motors myosin-mediated transport of dynamics can extend the total journey are required for movement along lysosomes and pigment granules an individual pigment granule makes in microtubule tracks [2] and myosins for where, in contrast to rocketing motility, two ways. One is a simple extension of movement along actin filament tracks actin filaments are already polymerized the same track the organelle is moving [3,4]. The expectation is that these before transportation is needed and on (Figure 1B, actin track 1) and the types of transport track are relatively simply provide actin substrate for other is by bridging to a nearby, but stable so that they can support useful myosin to move on (Figure 1B). The not directly touching, second actin cargo movement. It is perhaps authors experimentally exclude the track (Figure 1B, actin track 2), surprising then that new experimental possibility that actin dynamics are although neither scenario has yet been findings [5], reported in a recent issue needed to create spatial openings in directly visualized in cells. Bridging to of Current Biology, show that the the actin meshwork to provide access a nearby actin track of different spatial myosin class I [6] and V [7] motors need for organelle transport on separate orientation in the cell could account actin dynamics to pull their cargo of actin tracks. The likely answer is that for the abrupt directional changes in lysosomes and pigment granules, actin dynamics allow extension of the movement that individual pigment Dispatch R1067 actin filaments within lamellipodial or A B filopodial membrane protrusions at the cell periphery (half-life of 1–2 minutes). Significantly, myosin I motors in yeast directly stimulate actin dynamics during endocytosis [14–18]. This offers the new, though yet unexplored 1 possibility that myosin transport 2 motors like myosin I and V directly stimulate actin polymerization or depolymerization when pulling their cargo on actin tracks, resulting in the extension of their own track for their Current Biology own further advancement. References Figure 1. Actin dynamics and organelle transport. 1. Kuroda, K. (1990). Cytoplasmic streaming in The distinct types of actin-based organelle and particle transport present in cells differ in the plants. Int. Rev. Cytol. 121, 267–307. source of power to move the organelle/particle [19,20]. Two common distinct types of actin- 2. Vale, R.D. (2003). The molecular motor tool based transport require actin dynamics for different purposes. (A) In rocketing motility, poly- box for intracellular transport. Cell 112, 467–480. merization (curved on-arrow) of actin monomer (single pink chevron) between the organelle/ 3. Tuxworth, R.I., and Titus, M.A. (2000). particle cargo (orange sphere) and associated actin filament (chevrons) directly powers for- Unconventional myosins: anchors in the ward movement of cargo. (B) In myosin-driven transport, myosin I and V motors (black stick membrane traffic relay. Traffic 1, 11–18. and ball) pull organelle/particle cargo (green sphere) along a preformed track of actin filaments 4. Krendel, M., and Mooseker, M.S. (2005). (chevrons) towards only one end of the track (for these two motors, the barbed, or plus end). Myosins: tails (and heads) of functional diversity. Physiol. 20, 239–251. During pigment granule and lysosome transport in melanophores [5], ongoing actin polymer- 5. Semenova, I., Burakov, A., Berardone, N., ization (curved on-arrow) either simply extends the original actin track (1), and/or bridges the Zaliapin, I., Slepchenko, B., Svitkina, T.M., original actin track (1) to the next actin track (2); in both cases, the total distance that an indi- Kashina, A., and Rodionov, V. (2008). Actin vidual organelle travels on actin is increased. For these organelles, the measured net organelle dynamics is essential for myosin-based displacement on actin is shorter than the measured total distance travelled [5,9] due to the transport of membrane organelles. Curr. Biol. 18, 1581–1586. known random arrangement of actin-tracks (compare straight arrows) [5,9]. In cells, for both 6. Cordonnier, M.-N., Dauzonne, D., Louvard, D., rocketing transport of cargo [10] and myosin-driven organelle transport [5], actin filament and Coudrier, E. (2001). Actin filaments and depolymerization (curved off-arrow), rather than desequestration of stored actin monomer myosin I alpha cooperate with microtubules for (chevron in a box), at least in part directly provides the required actin monomer (single pink the movement of lysosomes. Mol. Biol. Cell 12, chevron) to fuel ongoing actin polymerization. 4013–4029. 7. Rogers, S.L., and Gelfand, V.I. (1998). Myosin cooperates with microtubule motors during granules make on actin tracks [5,9] migration [10] — that are directly organelle transport in melanophores. Curr. Biol. (Figure 1B, the direction of travel of regulated by controlling actin 8, 161–163. 8. Snider, J., Lin, F., Zahedi, N., Rodionov, V.I., individual cargo changes when actin depolymerization and recycling. This Yu, C.C., and Gross, S.P. (2004). Intracellular track 1 bridges to actin track 2).