Microtubule-Based Transport and the Distribution, Tethering, and Organization of Organelles

Abstract

SUMMARY Microtubules provide long tracks along which a broad range of organelles and vesicles are transported by kinesin and dynein motors. Motor protein complexes also tether cargoes to cytoskeletal filaments, helping facilitate their interaction and communication. The generation of biochemically distinct microtubule subpopulations allows subsets of motors to recognize a given microtubule identity, allowing further organization within the cytoplasm. Both transport and tethering are spatiotemporally regulated through multiple modes, including acute modification of both motor–cargo and motor–track associations by various physiological signals. Strict regulation of intracellular transport is particularly important in specialized cell types such as neurons. Here, we review general mechanisms by which cargo transport is controlled and also highlight examples of transport regulated by multiple mechanisms.

Parental centrioles are dispensable for deuterosome formation and function during basal body amplification

“…Initially, we found that GFP‐positive puncta, presumably deuterosomes, moved rapidly and were difficult to trace over time (Movie EV1). Impairing microtubule‐dependent intracellular transport by treating the cells with nocodazole (0.5 μg/ml), a microtubule‐destabilizing drug, markedly slowed down the deuterosome motilities. In the presence of nocodazole, we captured 15 cells that initiated their deuterosome biogenesis during the imaging (Fig E and Movie EV2) and 16 cells that already contained deuterosomes from the beginning and showed increased numbers of their deuterosomes over time (Movie EV3).…”

Role of actin in organelle trafficking in neurons

“…This intracellular transport is mediated by molecular motors, like kinesins and dyneins on microtubule tracks, and myosins on actin filaments (Hirokawa, Niwa, & Tanaka, ). In neurons, long‐range transport is predominantly mediated by microtubule‐based motor proteins and short‐range transport is typically thought to occur on actin filaments (Barlan & Gelfand, ; Langford, ). Actin‐dependent transport can occur in the following ways (a) myosin‐dependent cargo transport along actin filaments (Arden, Puri, Au, Kendrick‐Jones, & Buss, ; DePina & Langford, ; Semenova et al, ), (b) force‐based propulsion of cargoes by actin polymerization (Boldogh et al, ; Merrifield et al, ; Welch, Iwamatsu, & Mitchison, ), and (c) actin flow mediated organellar movement (Solecki et al, ; Trivedi et al, ).…”

Hitching a Ride: Mechanics of Organelle Transport Through Linker-Mediated Hitchhiking

“…A number of organelles, including mitochondria, melanophores, and peroxisomes are known to become tethered to microtubule tracks by regulatory proteins that are crucial for maintaining their cellular distribution (23,25,28,41,42). Such tethering not only helps localize organelles along extended cell regions (as in neurons) (27,41) but is also thought to facilitate interactions between multiple organelles by restricting their three-dimensional diffusion through the cytoplasm (28). In the case of hitchhiking cargos such as peroxisomes in Aspergillus and Ustilago, tethering to a microtubule has the potential to enhance the rate of hitchhiking initiation by eliminating the time spent out of reach of the microtubule-bound carrier organelles.…”

“…In some cell types, organelles such as peroxisomes and mitochondria have been observed to attach to microtubules when not being actively transported (23)(24)(25). Such tethering allows for regulated placement of organelles within the cell (25)(26)(27)(28). Tethering may also enhance the ability of cargo to interact with the transport machinery, increasing the rate of initiating active runs while restricting short-range diffusion (19).…”