A Drosophila Protein Specific to Pheromone-Sensing Gustatory Hairs Delays Males' Copulation Attempts

Park, Su K.; Mann, Kevin; Lin, Heping; Starostina, Elena; Kolski-Andreaco, Aaron; Pikielny, Claudio W.

doi:10.1016/j.cub.2006.04.028

Cited by 41 publications

(63 citation statements)

References 32 publications

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“…Consistent with this suggestion, CheB42a and llz showed a similar pattern of expression. Moreover, they both seem to be involved in male courtship behavior (5,30,31), and the two proteins interact (Y.B.-S. and M.J.W., unpublished data).…”

Section: Discussionmentioning

confidence: 97%

Eukaryotic operon-like transcription of functionally related genes in Drosophila

Ben‐Shahar

Nannapaneni²,

Casavant³

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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Complex biological processes require coordinated function of many genes. One evolutionary solution to the problem of coordinately expressing functionally related genes in bacteria and nematodes is organization of genes in operons. Surprisingly, eukaryotic operons are considered rare outside the nematode lineage. In Drosophila melanogaster, we found lounge lizard (llz), which encodes a degenerin/ENaC cation channel, cotranscribed with CheB42a, a nonhomologous gene of unknown function residing <100 bp upstream. These two genes were transcribed from a single promoter as one primary transcript and were processed posttranscriptionally to generate individual mRNAs. The mechanism did not involve alternative splicing, and it differed from the trans splicing used in nematode operons. Both genes were expressed in the same tissues, and previous work suggested that both may be involved in courtship behavior. A bioinformatic approach identified numerous additional loci as potential Drosophila operons. These data reveal eukaryotic operon-like transcription of functionally related genes in Drosophila. The results also suggest that operon-based transcription may be more common in eukaryotes than previously appreciated.degenerin/epithelial Na ϩ channel ͉ fruit fly ͉ ion channels ͉ lounge lizard ͉ CheB42a D egenerin/epithelial Na ϩ channel (DEG/ENaC) proteins form non-voltage-gated cation channels. Their functions vary widely and include mechanosensation, nociception (sensing acidic stimuli), salt sensing, and detecting the peptidergic neurotransmitter FMRFamide (1-4). During our investigation of Drosophila melanogaster DEG/ENaC channels, we discovered a genomic locus containing a DEG/ENaC gene, which we named lounge lizard (llz, CG33349), and a nonhomologous gene of unknown function (CheB42a) (5) that appeared to be transcribed in the same direction with a predicted intergenic distance of Ͻ100 bp. The close proximity of these two genes and the lack of obvious promoter sequences in front of the downstream gene suggested that they might be cotranscribed from a single upstream promoter. This organization would resemble that of the nematode operon, an elegant evolutionary solution for coexpressing genes that are part of the same biochemical pathway or physiological process (6, 7).Although abundant in nematodes, operons are thought to be rare in other eukaryotes. This is despite eukaryote's complicated cellular physiology and the intricacy of their genomes, which might predict that operon-like transcription would solve some of the problem of coordinately regulating genes (8). With this background, we hypothesized that the CheB42a/llz locus might be transcribed as a eukaryotic operon, and, hence, the two genes might be functionally related.

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Section: Discussionmentioning

confidence: 97%

Eukaryotic operon-like transcription of functionally related genes in Drosophila

Ben‐Shahar

Nannapaneni²,

Casavant³

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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“…In the olfactory system, a mutation in one of these proteins, LUSH, has been shown to affect behavioral responses to cis-vaccenyl acetate, a volatile pheromone involved in aggregation behavior [8,30]. Finally, a member of a new class of membrane proteins, CheB42a, is malebiased expressed in support cells of taste bristles also associated with the only known pheromone receptor, Gr68a, and plays a role in male courtship [31,32]. Thus, several lines of evidence indicate that accessory cells of taste bristles and olfactory hairs produce and secrete proteins that may significantly modulate responses of associated neurons.…”

Section: The Drosophila Taste Systemmentioning

confidence: 99%

Taste and pheromone perception in the fruit fly Drosophila melanogaster

Ebbs

Amrein

2007

Pflugers Arch - Eur J Physiol

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Taste is an essential sense for detection of nutrient-rich food and avoidance of toxic substances. The Drosophila melanogaster gustatory system provides an excellent model to study taste perception and taste-elicited behaviors. "The fly" is unique in the animal kingdom with regard to available experimental tools, which include a wide repertoire of molecular-genetic analyses (i.e., efficient production of transgenics and gene knockouts), elegant behavioral assays, and the possibility to conduct electrophysiological investigations. In addition, fruit flies, like humans, recognize sugars as a food source, but avoid bitter tasting substances that are often toxic to insects and mammals alike. This paper will present recent research progress in the field of taste and contact pheromone perception in the fruit fly. First, we shall describe the anatomical properties of the Drosophila gustatory system and survey the family of taste receptors to provide an appropriate background. We shall then review taste and pheromone perception mainly from a molecular genetic perspective that includes behavioral, electrophysiological and imaging analyses of wild type flies and flies with genetically manipulated taste cells. Finally, we shall provide an outlook of taste research in this elegant model system for the next few years.Keywords Drosophila . Gustatory receptor neurons . GTP-binding protein-coupled receptors Like most animals, Drosophila monitor their chemical world with two distinct senses: the olfactory system, which is used for the detection of volatile chemicals, and the gustatory (taste) system, which enables the fly to detect soluble compounds. The olfactory sensory system (or the fly nose) is comprised of two pairwise head appendages, the third segments of the antennae, and the maxillary palps (Fig. 1). These appendages are covered with hundreds of sensory hairs, each of which contains two to four olfactory sensory neurons (OSNs) [1]. In contrast, the gustatory system is widely distributed over the animal's body. The main taste organ, the proboscis or labial palps (i.e., the fly tongue), is located on the distal end of the labellum (also a head appendage), but flies, like many other insects, have taste sensilla on legs and wings and, in females, on the genitalia [1,2].The roles of the olfactory and taste systems are clearly separated with regard to the physical state of chemicals they detect (volatile vs solubilized). However, the two systems often cooperate to fulfill specific functions in related processes and behaviors, the most obvious of them being the location and identification of food. For example, chemical cues such as the specific odor of a flower and the sugar compounds present in its nectar are by nature associated with one another. Thus, the odor cue provides a primary sensory input for an insect such as a honeybee to locate a food source (nectar), whose particular chemical composition is subsequently verified by the taste system. Similarly, the typical odor of yeast, which produces high amounts of t...

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“…In particular, female-specific cuticular hydrocarbons are required for normal stimulation of male courtship behavior (9,10), and even trigger homosexual male courtship when ectopically produced by males (11). Remarkably, whereas these compounds have very low volatility and are only effective over a radius of less than 1 cm (12), their detection may involve both olfactory (13,14) and gustatory organs (15)(16)(17). Although there have been recent breakthroughs in the characterization of the olfactory perception of these cuticular hydrocarbon pheromones (8,18), more is known about the gustatory organs and molecules involved.…”

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confidence: 99%

“…Differences in the number and innervation patterns of taste sensilla between the sexes (19,20), as well as amputation and masking experiments (21,22), provided early evidence that taste sensilla on male forelegs are involved in detection of pheromones. We and others therefore identified genes that are specifically expressed in subsets of gustatory sensilla on male front legs, at least two of which are required for normal male courtship response to female-specific cuticular hydrocarbons (16,17,23). CheA29a and CheB42a, two genes expressed specifically in subsets of gustatory sensilla on male front legs, defined two novel and unrelated families of small secreted proteins (23).…”

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confidence: 99%

A Drosophila Protein Family Implicated in Pheromone Perception Is Related to Tay-Sachs GM2-Activator Protein

Starostina

Lin

et al. 2009

Journal of Biological Chemistry

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Low volatility, lipid-like cuticular hydrocarbon pheromones produced by Drosophila melanogaster females play an essential role in triggering and modulating mating behavior, but the chemosensory mechanisms involved remain poorly understood. Recently, we showed that the CheB42a protein, which is expressed in only 10 pheromone-sensing taste hairs on the front legs of males, modulates progression to late stages of male courtship behavior in response to female-specific cuticular hydrocarbons. Here we report that expression of all 12 genes in the CheB gene family is predominantly or exclusively gustatory-specific, and occurs in many different, often non-overlapping patterns. Only the Gr family of gustatory receptor genes displays a comparable variety of gustatory-specific expression patterns. Unlike Grs, however, expression of all but one CheB gene is sexually dimorphic. Like CheB42a, other CheBs may therefore function specifically in gustatory perception of pheromones. We also show that CheBs belong to the ML superfamily of lipid-binding proteins, and are most similar to human GM2-activator protein (GM2-AP). In particular, GM2-AP residues involved in ligand binding are conserved in CheBs but not in other ML proteins. Finally, CheB42a is specifically secreted into the inner lumen of pheromone-sensing taste hairs, where pheromones interact with membrane-bound receptors. We propose that CheB proteins interact directly with lipid-like Drosophila pheromones and modulate their detection by the gustatory signal transduction machinery. Furthermore, as loss of GM2-AP in Tay-Sachs disease prevents degradation of GM2 gangliosides and results in neurodegeneration, the function of CheBs in pheromone response may involve biochemical mechanisms critical for lipid metabolism in human neurons.

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A Drosophila Protein Specific to Pheromone-Sensing Gustatory Hairs Delays Males' Copulation Attempts

Cited by 41 publications

References 32 publications

Eukaryotic operon-like transcription of functionally related genes in Drosophila

Eukaryotic operon-like transcription of functionally related genes in Drosophila

Taste and pheromone perception in the fruit fly Drosophila melanogaster

A Drosophila Protein Family Implicated in Pheromone Perception Is Related to Tay-Sachs GM2-Activator Protein

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