Regulation of cytoplasmic dynein function in vivo by the Drosophila Glued complex.

McGrail, Maura; Gepner, Janice; Silvanovich, Andre; Ludmann, Susan A.; Serr, Madeline; Hays, Thomas S.

doi:10.1083/jcb.131.2.411

Cited by 124 publications

(107 citation statements)

References 58 publications

(114 reference statements)

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“…Dynein heavy chain (Dhc), the motor subunit of the Dynein complex, was enriched at the posterior pole of the oocyte in stage 10 egg chambers (Figure 1C,arrow). This localization pattern is consistent with published findings (McGrail et al 1995). Partial colocalization was observed between Egl and Dhc at the posterior pole and along the oocyte cortex ( Figure 1C).…”

Section: Resultssupporting

confidence: 82%

“…In stage 10 egg chambers expressing a control shRNA, Dhc was enriched at the posterior pole of the oocyte and also along the anterior and lateral cortex ( Figure 5A). A similar pattern was observed in wild-type egg chambers (data not shown) (McGrail et al 1995). In the absence of Egl, Dhc was no longer enriched at the oocyte posterior or along the cortex in stage 10 egg chambers.…”

Section: Egl Regulates the Translation Of Osk And Grk Mrnassupporting

confidence: 59%

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Multiple Roles for Egalitarian in Polarization of the Drosophila Egg Chamber

et al. 2016

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The Drosophila egg chamber provides a useful model for examining mechanisms by which cell fates are specified and maintained in the context of a complex tissue. The egg chamber is also an excellent model for understanding the mechanism by which cytoskeletal filaments are organized and the critical interplay between cytoskeletal organization, polarity establishment, and cell fate specification. Previous work has shown that Egalitarian (Egl) is required for specification and maintenance of oocyte fate. Mutants in egl either completely fail to specify an oocyte, or if specified, the oocyte eventually reverts back to nurse cell fate. Due to this very early role for Egl in egg chamber maturation, it is unclear whether later stages of egg chamber development also require Egl function. In this report, we have depleted Egl at specific stages of egg chamber development. We demonstrate that in early-stage egg chambers, Egl has an additional role in organization of oocyte microtubules. In the absence of Egl function, oocyte microtubules completely fail to reorganize. As such, the localization of microtubule motors and their cargo is disrupted. In addition, Egl also appears to function in regulating the translation of critical polarity determining messenger RNAs (mRNAs). Finally, we demonstrate that in midstage egg chambers, Egl does not appear to be required for microtubule organization, but rather for the correct spatial localization of oskar, bicoid, and gurken mRNAs.

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Section: Resultssupporting

confidence: 82%

Section: Egl Regulates the Translation Of Osk And Grk Mrnassupporting

confidence: 59%

Multiple Roles for Egalitarian in Polarization of the Drosophila Egg Chamber

et al. 2016

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“…First, although the Gl 1 allele produces a truncated protein that acts as a dominant-negative inhibitor of P150 Glued in eye development (McGrail et al, 1995), it might have an aberrant gain of function effect in axonal transport. Second, the increases could reflect an indirect Gl 1 effect that alters axonal transport regulatory signals to axons from glial or other cells.…”

Section: P150 Glued Influences Anterograde and Retrograde Transport Pmentioning

confidence: 99%

Kinesin-1 and Dynein Are the Primary Motors for Fast Transport of Mitochondria inDrosophilaMotor Axons

Pilling

Horiuchi

Lively

et al. 2006

MBoC

615

621

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To address questions about mechanisms of filament-based organelle transport, a system was developed to image and track mitochondria in an intact Drosophila nervous system. Mutant analyses suggest that the primary motors for mitochondrial movement in larval motor axons are kinesin-1 (anterograde) and cytoplasmic dynein (retrograde), and interestingly that kinesin-1 is critical for retrograde transport by dynein. During transport, there was little evidence that force production by the two opposing motors was competitive, suggesting a mechanism for alternate coordination. Tests of the possible coordination factor P150 Glued suggested that it indeed influenced both motors on axonal mitochondria, but there was no evidence that its function was critical for the motor coordination mechanism. Observation of organelle-filled axonal swellings ("organelle jams" or "clogs") caused by kinesin and dynein mutations showed that mitochondria could move vigorously within and pass through them, indicating that they were not the simple steric transport blockades suggested previously. We speculate that axonal swellings may instead reflect sites of autophagocytosis of senescent mitochondria that are stranded in axons by retrograde transport failure; a protective process aimed at suppressing cell death signals and neurodegeneration. INTRODUCTIONOrganelle transport is central to the organization, developmental fate, and functions of asymmetric cells. A bipolar neuron is an extreme case, with the somato-dendritic region and the axon containing different sets of proteins and organelles. In general, much of the machinery for synthesizing and recycling neuronal components is clustered near the nucleus. Because an axon, often with an axial ratio of many thousands, usually contains Ͼ99% of the neuronal cytoplasm, active transport of new components away from the cell body and of spent components and trophic materials back toward the cell body is critical. Disruptions of axonal transport are thought to contribute to the pathologies of Alzheimer's, amyotrophic lateral sclerosis, and other neurodegenerative diseases (reviewed by Mandelkow and Mandelkow, 2002;Hirokawa and Takemura, 2005).Long-distance organelle transport in axons is driven by motor proteins that move along parallel microtubules whose plus ends are mostly oriented toward the axon terminal (reviewed by Hollenbeck and Saxton, 2005). There are multiple types of microtubule motors in postmitotic vertebrate neurons, including kinesins that can move toward either plus-or minus-ends and at least one cytoplasmic dynein that moves toward minus-ends (Martin et al., 1999b;Hirokawa and Takemura, 2005;Hollenbeck and Saxton, 2005). Which motors bind and move which axonal components? When multiple types of motors bind a single cargo, do they collaborate or compete, how are they regulated, and how do their combined activities generate an optimal distribution of that type of cargo?Axonal mitochondria are critical for the physiology of neurons and are particularly well suited for studying active tr...

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“…Preparation of crude dynein by ATP-sensitive affinity to taxol-stabilized microtubules was as described previously . Sedimentation of crude dynein or soluble extracts of tissues through 5-20% sucrose gradients was as described previously (McGrail et al, 1995). Immunoprecipitation experimental procedures were as described previously (Boylan et al, 2000).…”

Section: Antibodies and Protein Analysismentioning

confidence: 99%

TheDrosophilatctex-1 Light Chain Is Dispensable for Essential Cytoplasmic Dynein Functions but Is Required during Spermatid Differentiation

Serr

Newman

et al. 2004

MBoC

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Variations in subunit composition and modification have been proposed to regulate the multiple functions of cytoplasmic dynein. Here, we examine the role of the Drosophila ortholog of tctex-1, the 14-kDa dynein light chain. We show that the 14-kDa light chain is a bona fide component of Drosophila cytoplasmic dynein and use P element excision to generate flies that completely lack this dynein subunit. Remarkably, the null mutant is viable and the only observed defect is complete male sterility. During spermatid differentiation, the 14-kDa light chain is required for the localization of a nuclear "cap" of cytoplasmic dynein and for proper attachment between the sperm nucleus and flagellar basal body. Our results provide evidence that the function of the 14-kDa light chain in Drosophila is distinct from other dynein subunits and is not required for any essential functions in early development or in the adult organism. INTRODUCTIONThe minus-end-directed microtubule motor cytoplasmic dynein has been implicated in a variety of cellular processes, including nuclear envelope breakdown, mitotic spindle assembly and orientation, chromosome movements, intracellular trafficking of organelles and mRNAs, and intraflagellar transport (reviewed in Karki and Holzbaur, 1999). The heavy chain subunit of dynein is known to provide ATPase and microtubule binding functions, and although more than one cytoplasmic dynein heavy chain has been identified, the major cytoplasmic dynein motor contains a homodimer of a single heavy chain. It remains unclear how this single cytoplasmic dynein motor is targeted to distinct organelles and cellular processes. One hypothesis is that the accessory intermediate, light intermediate, and light chain subunits of cytoplasmic dynein mediate its functional specialization. Consistent with this idea, in some eukaryotes these subunits are encoded by multiple genes that are differentially expressed and/or alternatively spliced as distinct transcripts in different tissues and cells (Gill et al., 1994;Pfister et al., 1996a;Bowman et al., 1999;Susalka et al., 2000;Tynan et al., 2000;Tai et al., 2001). In addition, the posttranslational modification of subunits may contribute to the heterogeneity of subunit composition in the dynein complex . Although the mutational analysis of the cytoplasmic dynein heavy chain has revealed a range of motor functions, the functional contribution of other individual subunits is not well understood.The present study addresses the function of the 14-kDa dynein light chain. This light chain was first identified as a cytoplasmic dynein subunit in mammalian brain (King et al., 1996a) and as an axonemal dynein subunit within the specialized inner arm dynein of the Chlamydomonas flagella (Harrison et al., 1998). In Drosophila, a molecular study of the 14-kDa light chain gene reported defective male fertility for hypomorphic alleles, but the nature of the mutations left unresolved the significance of the 14-kDa light chain in cytoplasmic dynein (Caggese et al., 2001). Sequence analysis...

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Regulation of cytoplasmic dynein function in vivo by the Drosophila Glued complex.

Cited by 124 publications

References 58 publications

Multiple Roles for Egalitarian in Polarization of the Drosophila Egg Chamber

Multiple Roles for Egalitarian in Polarization of the Drosophila Egg Chamber

Kinesin-1 and Dynein Are the Primary Motors for Fast Transport of Mitochondria inDrosophilaMotor Axons

TheDrosophilatctex-1 Light Chain Is Dispensable for Essential Cytoplasmic Dynein Functions but Is Required during Spermatid Differentiation

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