The polarity of axon growth in the wings of Drosophila melanogaster

doi:10.1016/0012-1606(83)90377-9

Developmental Biology

Volume 98, Issue 2, August 1983, Pages 481-492

https://doi.org/10.1016/0012-1606(83)90377-9 Get rights and content

Abstract

We have analyzed the growth of axons in the wings of the mutants Hairy wing and hairy of Drosophila melanogaster. These mutants produce many supernumerary bristle organs and sensilla campaniformia, whose axons grow between the two wing epithelia and can be visualized in both pupal and adult stages. The sensory axons of wild-type animals follow two paths in the wing, within longitudinal veins L1 and L3, and always grow with a distal to proximal polarity. In the mutants, all axons following these two paths likewise grow with correct polarity. Axons elsewhere in the wing, however, are found to grow in many different directions, including from proximal to distal and hence directly away from the central nervous system. A variety of patterns of axon growth and fasciculation are seen in different individuals. Only if the supernumerary axons encounter the two normal paths do they reliably grow toward the base of the wing. We conclude that these two paths provide polarity information for axon growth, information which is either not used or not available elsewhere in the wing in spite of the obvious morphological polarization of every epithelial cell. The time course of neural differentiation suggests that the normal sensory cells of mutant wings, which grow axons relatively early, may be the source of polarity information for the later-differentiating supernumerary cells.

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Cited by (31)

The dREAM/Myb-MuvB complex and Grim are key regulators of the programmed death of neural precursor cells at the Drosophila posterior wing margin
2012, Developmental Biology
Citation Excerpt :
However, we also made an unexpected observation. In wild-type and control wings that are heterozygous for the mybMH107allele, neuronal innervation of sensory bristles is restricted to the anterior compartment (Palka et al., 1983; and see Fig. 1E-E″). In contrast, labeling with Elav and 22C10 antibodies revealed that mybMH107 clones exhibit ectopic neuronal development at the PWM (ca. 40 neurons; Fig. 1F-F″).
Successful development of a multicellular organism depends on the finely tuned orchestration of cell proliferation, differentiation and apoptosis from embryogenesis through adulthood. The MYB-gene family encodes sequence-specific DNA-binding transcription factors that have been implicated in the regulation of both normal and neoplastic growth. The Drosophila Myb protein, DMyb (and vertebrate B-Myb protein), has been shown to be part of the dREAM/MMB complex, a large multi-subunit complex, which in addition to four Myb-interacting proteins including Mip130, contains repressive E2F and pRB proteins. This complex has been implicated in the regulation of DNA replication within the context of chorion gene amplification and transcriptional regulation of a wide array of genes. Detailed phenotypic analysis of mutations in the Drosophila myb gene, Dm myb, has revealed a previously undiscovered function for the dREAM/MMB complex in regulating programmed cell death (PCD). In cooperation with the pro-apoptotic protein Grim and dREAM/MMB, DMyb promotes the PCD of specified sensory organ precursor daughter cells in at least two different settings in the peripheral nervous system: the pIIIb precursor of the neuron and sheath cells in the posterior wing margin and the glial cell in the thoracic microchaete lineage. Unlike previously analyzed settings, in which the main role of DMyb has been to antagonize the activities of other dREAM/MMB complex members, it appears to be the critical effector in promoting PCD. The finding that Dm myb and grim are both involved in regulating PCD in two distinct settings suggests that these two genes may often work together to mediate PCD.
Larval multidendrite neurons survive metamorphosis and participate in the formation of imaginal sensory axonal pathways in the notum of Drosophila
2000, Developmental Biology
In each hemimesothorax of Drosophila, a cluster of five larval multidendrite neurons that survives metamorphosis is described. The cell bodies of these neurons, initially grouped together, spread out over the medial heminotum during early pupal stages and extend new dendrites. Growing axons from sensory bristle neurons first appear in a defined orientation specific for each macrochaete. They subsequently contact processes from the larval multidendrite neurons and then appear to follow the preestablished axon trajectories of the latter. Ablation of the multidendrite neurons during the larval stage causes bristle axons to adopt abnormal trajectories. We suggest that the persistent larval neurons participate in guiding axons of the bristles on the medial half of the notum to the posterior dorsal mesothoracic nerve leading to the central nervous system.
Multiple Factors Govern Intraretinal Axon Guidance: A Time-Lapse Study
1995, Molecular and Cellular Neuroscience
In this study, the multiple factors that govern the unidirectional path of intraretinal axons, as well as the cellular movements prior to and during early axonogenesis, were investigated using time-lapse videomicroscopy. For several hours prior to overt axon elongation, young retinal ganglion cells send out transient minor processes in all directions at the pial surface. Time-lapse analysis of the chondroitin sulfate (CS)-containing matrix that has been suggested to play an important role in regulating this early differentiative event revealed the dynamic, wavelike properties of this extracellular matrix component. As the CS matrix dissipates across the immature ganglion cells, only one minor process, away from the highest concentration of CS peripherally and in the direction of the optic fissure centrally, is retained and becomes the mature axon. Focal concentrations of L1 appear at points of neurite contact with previously established axons, suggesting that this growth-promoting molecule is also involved with establishing the precise, unidirectional outgrowth pattern of retinal ganglion cell axons. NCAM was diffusely distributed on neural elements and on the neuroepithelial endfeet in the central and peripheral retina and, thus, may not be an essential unidirectional axon growth cue. Growth cones mechanically deflected 180° from the optic fissure after the CS wave had receded from the central retina had morphologies and rates of elongation similar to those oriented in the proper direction. Growth cones deflected obliquely toward the ventral retinal periphery entered a territory of increasing CS-containing proteoglycan matrix and neurons with minor processes. As these deflected axons entered more deeply into this region they slowed down and sent out long transient branchlike processes. These observations illustrate the complex organization of the changing cell surface and matrix components within the retina during axonogenesis and axon outgrowth. The results also elucidate the potential importance of a cell state where immature neurons probe their environment via minor processes. These specialized neurites may provide the neuron with a way to sample a full 360° of terrain around them. This method of exploring the environment could afford the cell a mechanism with which to sample, summate, and respond to physical structures as well as simultaneously occurring negative and positive molecular influences that are distributed unequally on either side of the cell body.
A role for the segment polarity gene shaggy-zeste white 3 in the specification of regional identity in the developing wing of Drosophila
1994, Developmental Biology
The Drosophila segment polarity gene known as shaggy or zeste white 3 encodes a ubiquitously expressed serine-threonine protein kinase which is critical for a number of important developmental processes. In the developing wing blade, clones of cells lacking the normal shaggy-zeste white 3 product form dense tufts of margin-like bristles and bristle precursors. In a previous study I hypothesized that this phenotype could be best explained as a transformation in the regional identity of wing blade cells to one resembling that found along the normal wing margin. A number of genes have recently been identified which are expressed exclusively or at higher levels along the normal wing margin; in this study I will show that two of these genes, vestigial and scalloped, are overexpressed at margin-like levels in shaggy-zeste white 3 clones. This phenotype does not depend upon the formation of ectopic bristle precursors and occurs in clones lacking both shaggy-zeste white 3 and the entire achaete-scute complex. As vestigial and scalloped are both involved in early patterning events prior to the stages of bristle specification, these results strongly suggest that shaggy-zeste white 3 is required for the normal specification or maintenance of regional identity in the developing wing blade. The margin-like transformation is, however, partial, since the expression of apterous (in pupal wings) and wingless and cut (at late third instar) was not reliably altered in shaggy-zeste white 3 clones. It has been suggested that shaggy-zeste white 3 is involved in a wingless signaling pathway in the embryo; a model is discussed in which shaggy-zeste white 3 acts downstream of localized apterous and wingless expression to specify or maintain margin identity in the wing.
shaggy (zeste-white 3) and the formation of supernumerary bristle precursors in the developing wing blade of Drosophila
1992, Developmental Biology
The development of supernumerary bristle precursors induced by the mutation shaggy (sgg; also known as zeste-white 3) was examined in the developing wing blade of imaginal and pupal Drosophila. sgg clones were induced by mitotic recombination; clones were marked using enhancer-trap flies which express β-galactosidase ubiquitously in imaginal tissues, while bristle precursors were identified using sensillum and bristle-specific enhancer-trap lines. It was shown that the precursors of supernumerary sgg bristles in the wing blade mimicked the development of morphologically similar margin bristles, developing in a manner similar to that of anterior sensory bristles in anterior clones and posterior noninnervated bristles in posterior clones. Interestingly, supernumerary anterior sensory bristles appeared outside the normal regions of “proneural” gene activity as identified using anti-achaete. Moreover, sgg could induce the ectopic expression of achaete in anterior clones. Thus, in the anterior wing blade the sgg mutation leads to the formation of ectopic proneural regions.
The development of normal and ectopic sensilla in the wings of hairy and hairy wing mutants of Drosophila
1992, Mechanisms of Development
We have utilized enhancer trap markers to follow the development of ectopic sensillar precursors in the wings of Drosophila induced by the mutations hairy and Hairy wing. Normal sensilla are still present in these mutations, and can be distinguished from ectopic sensilla based upon both the position and the timing of their development. This correlates well with the development of ectopic achaete expression in these mutations: such staining is detected only after the appearance of normal staining. Thus, neither mutation appears to alter the specification of proneural clusters in the wing, as identified with anti-achaete, or the specification of sensillar precursors within these clusters. Rather, both act to induce the formation of a temporally and spatially distinct phase of sensillar development.

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^☆: This work was supported by NIH Research Grant NS-07778 and NSF Grant BNS-8141325.

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Developmental Biology

Abstract

References (24)

Pioneer neurons and pathways in insect appendages

Trends NeuroSci

The projection of sensory neurons in the central nervous system of Drosophila: Choice of the appropriate pathway

Dev. Biol

Neuronal pathfinding in developing wings of the moth Manduca sexta

Dev. Biol

Segments, compartments and axon paths in Drosophila

Trends Neurosci

Neural projection patterns from homeotic tissue of Drosophila studied in bithorax mutants and mosaics

Dev. Biol

Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer

Cell

Development of sensory nerves within the wing of Drosophila melanogaster: A light- and electron-microscope study

Abst. Soc. Neurosci

Pioneer neurons in an insect embryo

Nature (London)

The pattern of campaniform sensilla on the wing and haltere of Drosophila melanogaster and several of its homeotic mutants

J. Embryol. Exp. Morphol

Pathfinding by neuronal growth cones in grasshopper embryos

Peripheral pathways are pioneered by an array of central and peripheral neurones in grasshopper embryos

Nature (London)

Abnormal neural development in Drosophila embryos carrying mutations affecting segmental identity or segment numbers

Abst. Soc. Neurosci

Cited by (31)

The dREAM/Myb-MuvB complex and Grim are key regulators of the programmed death of neural precursor cells at the Drosophila posterior wing margin

Larval multidendrite neurons survive metamorphosis and participate in the formation of imaginal sensory axonal pathways in the notum of Drosophila

Multiple Factors Govern Intraretinal Axon Guidance: A Time-Lapse Study

A role for the segment polarity gene shaggy-zeste white 3 in the specification of regional identity in the developing wing of Drosophila

shaggy (zeste-white 3) and the formation of supernumerary bristle precursors in the developing wing blade of Drosophila

The development of normal and ectopic sensilla in the wings of hairy and hairy wing mutants of Drosophila

Full paperThe polarity of axon growth in the wings of Drosophila melanogaster☆

Abstract

Trends NeuroSci

Dev. Biol

Dev. Biol

Trends Neurosci

Dev. Biol

Cell

Development of sensory nerves within the wing of Drosophila melanogaster: A light- and electron-microscope study

Abst. Soc. Neurosci

Pioneer neurons in an insect embryo

Nature (London)

The pattern of campaniform sensilla on the wing and haltere of Drosophila melanogaster and several of its homeotic mutants

J. Embryol. Exp. Morphol

Pathfinding by neuronal growth cones in grasshopper embryos

Peripheral pathways are pioneered by an array of central and peripheral neurones in grasshopper embryos

Nature (London)

Abnormal neural development in Drosophila embryos carrying mutations affecting segmental identity or segment numbers

Abst. Soc. Neurosci

Full paper
The polarity of axon growth in the wings of Drosophila melanogaster☆