Dynein–Dynactin Function and Sensory Axon Growth duringDrosophilaMetamorphosis: A Role for Retrograde Motors

Murphey, R. K.; Caruccio, Phyllis; Getzinger, Michael J.; Westgate, Pamela J.; Phillis, Randall W.

doi:10.1006/dbio.1999.9217

Cited by 29 publications

(25 citation statements)

References 45 publications

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“…Dynein and dynactin are the major components of the retrograde motor system of axonal transport and also mediate the anterograde transport of short axonal microtubules (Ahmad et al, 1998(Ahmad et al, , 2006. In Drosophila mutants of dynactin, the terminal branching of sensory neurons is greatly impaired (Murphey et al, 1999), perhaps reflecting the role of dynein and dynactin in the transport of microtubule fragments into branches.…”

Section: Mechanisms Of Collateral Branch Maturation: Targeting Of Micmentioning

confidence: 99%

The cytoskeletal and signaling mechanisms of axon collateral branching

Gallo

2011

Developmental Neurobiology

168

233

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During development, axons are guided to their appropriate targets by a variety of guidance factors. On arriving at their synaptic targets, or while en route, axons form branches. Branches generated de novo from the main axon are termed collateral branches. The generation of axon collateral branches allows individual neurons to make contacts with multiple neurons within a target and with multiple targets. In the adult nervous system, the formation of axon collateral branches is associated with injury and disease states and may contribute to normally occurring plasticity. Collateral branches are initiated by actin filament– based axonal protrusions that subsequently become invaded by microtubules, thereby allowing the branch to mature and continue extending. This article reviews the current knowledge of the cellular mechanisms of the formation of axon collateral branches. The major conclusions of this review are (1) the mechanisms of axon extension and branching are not identical; (2) active suppression of protrusive activity along the axon negatively regulates branching; (3) the earliest steps in the formation of axon branches involve focal activation of signaling pathways within axons, which in turn drive the formation of actin-based protrusions; and (4) regulation of the microtubule array by microtubule-associated and severing proteins underlies the development of branches. Linking the activation of signaling pathways to specific proteins that directly regulate the axonal cytoskeleton underlying the formation of collateral branches remains a frontier in the field.

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Section: Mechanisms Of Collateral Branch Maturation: Targeting Of Micmentioning

confidence: 99%

The cytoskeletal and signaling mechanisms of axon collateral branching

Gallo

2011

Developmental Neurobiology

168

233

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“…Interestingly, the sensory axons in ctp homozygous adults failed to form proper branches and seemed to grow in altered trajectories. Similar phenotype occurred when a dominant negative Glued gene product was expressed in these neurons (Murphey et al, 1999). All these suggest that DDLC1 could also regulate spectrin-Dynactin-Dynein interaction at the growth cones, and this would maintain cell growth.…”

Section: Role Of Spectrin In Cell Growth At the Distal Endmentioning

confidence: 58%

“…It is required to maintain the retrograde IFT (Pazour et al, 1998), and the assembly of Dynein arms and radial spoke structures of the axoneme (Yang et al, 2001). Studies in Aspergillus have shown that the NUDG/ LC8 is required to maintain nuclear migration, cell growth, and distal end localization of Dynein at higher temperature (Beckwith et al, 1998;Liu et al, 2003), and studies in Drosophila suggested that both DLC1 (ctp) and P150 Dynactin (Glued) are involved in maintaining axonal growth in sensory neurons (Phillis et al, 1996;Murphey et al, 1999). Together, these data suggest that DLC1/LC8 is required for cell growth in a variety of different cell types.…”

Section: Introductionmentioning

confidence: 99%

Cytoplasmic Dynein–Dynactin Complex Is Required for Spermatid Growth but Not Axoneme Assembly inDrosophila

Ghosh-Roy

Kulkarni

Kumar

et al. 2004

MBoC

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Spermatids derived from a single gonial cell remain interconnected within a cyst and elongate by synchronized growth inside the testis in Drosophila. Cylindrical spectrin-rich elongation cones form at their distal ends during the growth. The mechanism underlying this process is poorly understood. We found that developing sperm tails were abnormally coiled at the growing ends inside the cysts in the Drosophila Dynein light chain 1 (ddlc1) hemizygous mutant testis. A quantitative assay showed that average number of elongation cones was reduced, they were increasingly deformed, and average cyst lengths were shortened in ddlc1 hemizygous testes. These phenotypes were further enhanced by additional partial reduction of Dhc64C and Glued and rescued by Myc-PIN/LC8 expression in the gonial cells in ddlc1 backgrounds. Furthermore, DDLC1, DHC, and GLUED were enriched at the distal ends of growing spermatids. Finally, ultrastructure analysis of ddlc1 testes revealed abnormally formed interspermatid membrane, but the 9 ؉ 2 microtubule organization, the radial spoke structures, and the Dynein arms of the axoneme were normal. Together, these findings suggest that axoneme assembly and spermatid growth involve independent mechanisms in Drosophila and DDLC1 interacts with the Dynein-Dynactin complex at the distal ends of spermatids to maintain the spectrin cytoskeleton assembly and cell growth. INTRODUCTIONSpermatogenesis is a complex cell differentiation process that involves both mitotic and meiotic cell divisions followed by dramatic cytoskeletal reorganizations and cell growth. In Drosophila, for example, an undifferentiated gonial cell produces 64 nearly spherical spermatocytes after four rounds of mitosis and a meiosis and then all of them simultaneously grow to form ϳ1.8-mm-long spermatids (Lindsley and Tokuyasu, 1980;Fuller, 1993). Axoneme growth inside each spermatid is synchronized with the cell growth and thus it always fits the length of the spermatid as it grows. Once fully grown, the spermatids inside a cyst are individualized to form motile sperm, which then swim into the seminal vesicle. The mechanism of sperm individualization is understood to some extent (Arama et al., 2003;Noguchi and Miller, 2003). However, the mechanism involved in spermatid growth remained unclear.Intraflagellar transport (IFT) plays an important role in the growth of flagella in unicellular organisms such as Chlamydomonas and in the primary cilia of various other organisms (Rosenbaum and Witman, 2002). Mutations affecting the IFT reduce the length of the flagella/cilia as well as the axoneme (Kozminski et al., 1995;Pazour et al., 1998;Signor et al., 1999;Qin et al., 2001), and a recent study has shown that the components of the radial spoke structure of the axoneme is transported in and out of the flagella by the IFT (Qin et al., 2004). Thus, axoneme growth is intimately linked to that of flagella and cilia. Although the molecular mechanism of flagella formation in mammalian sperm is not so clearly defined, a recent report indicated that t...

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“…Axonal projections from lch5 have been mapped and also show some diversity (Merritt and Whitington, 1995, Smith and Shepherd, 1996, Merritt, 1997, Schrader and Merritt, 2000. In the fCHO, several Gal4 lines (see Brand and Perrimon (1993) and Duffy (2002) for explanation of these genetic tools) express in different subsets of neurons, with different projection patterns into the thoracic ganglia (Phillis et al, 1996, Reddy et al, 1997, Murphey et al, 1999. It is not known whether any of these also express in JO.…”

Section: B Amentioning

confidence: 99%

Development of Johnston's organ in Drosophila

Eberl¹,

Boekhoff-Falk²

2007

Int. J. Dev. Biol.

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Hearing is a specialized mechanosensory modality that is refined during evolution to meet the particular requirements of different organisms. In the fruitfly, Drosophila, hearing is mediated by Johnston's organ, a large chordotonal organ in the antenna that is exquisitely sensitive to the near-field acoustic signal of courtship songs generated by male wing vibration. We summarize recent progress in understanding the molecular genetic determinants of Johnston's organ development and discuss surprising differences from other chordotonal organs that likely facilitate hearing. We outline novel discoveries of active processes that generate motion of the antenna for acute sensitivity to the stimulus. Finally, we discuss further research directions that would probe remaining questions in understanding Johnston's organ development, function and evolution.

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Dynein–Dynactin Function and Sensory Axon Growth duringDrosophilaMetamorphosis: A Role for Retrograde Motors

Cited by 29 publications

References 45 publications

The cytoskeletal and signaling mechanisms of axon collateral branching

The cytoskeletal and signaling mechanisms of axon collateral branching

Cytoplasmic Dynein–Dynactin Complex Is Required for Spermatid Growth but Not Axoneme Assembly inDrosophila

Development of Johnston's organ in Drosophila

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