Elsevier

Experimental Eye Research

Volume 144, March 2016, Pages 90-98
Experimental Eye Research

iFly: The eye of the fruit fly as a model to study autophagy and related trafficking pathways

https://doi.org/10.1016/j.exer.2015.06.013Get rights and content

Highlights

  • The fly eye is a popular and excellent model for retinopathies and proteinopathies.

  • Autophagy plays important roles in health and disease.

  • Autophagy is dispensable for eye development and pigment granule formation.

  • Autophagy usually protects from neurodegeneration induced by light or mutant proteins.

Abstract

Autophagy is a process by which eukaryotic cells degrade and recycle their intracellular components within lysosomes. Autophagy is induced by starvation to ensure survival of individual cells, and it has evolved to fulfill numerous additional roles in animals. Autophagy not only provides nutrient supply through breakdown products during starvation, but it is also required for the elimination of damaged or surplus organelles, toxic proteins, aggregates, and pathogens, and is essential for normal organelle turnover. Because of these roles, defects in autophagy have pathological consequences. Here we summarize the current knowledge of autophagy and related trafficking pathways in a convenient model: the compound eye of the fruit fly Drosophila melanogaster. In our review, we present a general introduction of the development and structure of the compound eye. This is followed by a discussion of various neurodegeneration models including retinopathies, with special emphasis on the protective role of autophagy against these diseases.

Section snippets

Overview of autophagy

Autophagy is a highly conserved catabolic process of eukaryotic cells, which is responsible for the turnover of cytoplasmic material via the lysosomal apparatus. Autophagy has three subtypes: macroautophagy, microautophagy, and chaperone mediated autophagy (Mizushima et al., 2008). Of these pathways, the first one is the best characterized, so we will focus on macroautophagy (hereafter simply referred to as autophagy) in this review.

The autophagic process begins with the emergence of a double

The structure and development of the Drosophila compound eye

The compound eye of the fly develops from the larval eye primordium, the so-called eye-antennal disc (Fig. 1A). This small, paired organ belongs to the group of imaginal discs that all consist of two epithelial monolayers opposing each other. One cell layer of a disc is a squamous epithelium and it is called the peripodial membrane, and the other layer is a columnar epithelium, the so-called disc proper. Besides its structural role, the function of the peripodial membrane is to secrete

Studying autophagy in the Drosophila eye

Much of the work on autophagy was carried out in the polyploid larval fat body in Drosophila, as both starvation-induced and developmental forms of this process can be easily studied in that tissue (Mauvezin et al., 2014, Nagy et al., 2014). The level of autophagy is relatively low in larval eye discs or adult eyes, and the loss of autophagy genes does not alter the structure of the compound eye (Juhasz et al., 2007, Velentzas et al., 2013) (Fig. 3D). The precisely controlled activity of

The Drosophila eye as a tool to study the role of autophagy in models of proteinopathy and neurodegeneration

Retinule cells are primary sensory neurons, so the fly eye is widely used to study the mechanisms of neurodegeneration. Most human diseases have a Drosophila model, and as working with fruit flies is faster and often easier than with mammals thanks to the shorter lifecycle and less genetic redundancy, researchers have much more room to maneuver when it comes to examine models of neurodegenerative disorders (Ambegaokar et al., 2010, Rincon-Limas et al., 2012). Neurodegeneration can be relatively

Autophagy prevents light-induced retinal degeneration in Drosophila

The fly eye also proved to be useful to study retinopathies, and many retinal disease model flies are available by now (Knust, 2007). The pathomechanisms of retinal degenerative disorders are extremely diverse, but in most cases it is the misfolded or mutated form of Rhodopsin that causes retinal cell death. One example is the inheritable disease retinitis pigmentosa (RP), a form of retinopathy characterized by progressive photoreceptor loss mostly due to mutations affecting Rhodopsin. The

Connections between pigment granule synthesis and autophagy

Ommatidia in the fly eye are isolated by pigment cells, and pigment granules are lysosome-related organelles, so the Drosophila eye is excellent for the study of biosynthetic lysosomal trafficking (Lloyd et al., 1998, Shoup, 1966). Recent studies show that several genes affecting pigment granule biosynthesis also have a role in lysosome biogenesis, so these are important for autophagic degradation as well. For example, one abnormal eye color phenotype is caused by a mutation in mauve (mv), the

Concluding remarks

To summarize the role of autophagy in the fruit fly eye, we can conclude that while it is dispensable for pigment granule synthesis and eye development, autophagy is important for maintaining retinal homeostasis. Thus, the Drosophila retina provides an ideal tool to study the involvement of autophagy and autophagy-related genes in certain diseases including proteinopathies and retinopathies. Established neurodegeneration model flies can be used for the screening of relevant genes and

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