Transient Receptor Potential-Like Channels Are Essential for Calcium Signaling and Fluid Transport in a Drosophila Epithelium

MacPherson, Matthew; Pollock, Valerie P.; Kean, Laura; Southall, Maria E.; Giannakou, Maria E.; Broderick, Kate E.; Dow, Julian A. T.; Hardie, Roger C.; Davies, Shireen A.

doi:10.1534/genetics.104.035139

Cited by 26 publications

(21 citation statements)

References 60 publications

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“…In the first report describing TRP␥, its expression was shown to specifically occur in Drosophila eyes and the head, but not in the body (17), suggesting a possible sensory function of TRP␥. In contrast, a second report showed that the transcription of TRP␥ mRNA not only occurs in the fruit fly's head but also in the cells of the Malpighian tubules (18). Similarly, our present RT-PCR data support the notion that TRP␥ expression is not restricted to Drosophila head.…”

Section: Discussionsupporting

confidence: 87%

“…Xu et al showed expression of TRP␥ predominantly in Drosophila head (17). In contrast, two recent publications showed a much broader distribution of TRP␥ (18,19). A broad expression pattern of TRP␥ and the fact that there are only three TRPC members (TRP, TRPL, TRP␥) in the genome of Drosophila make it likely that a TRP␥-mediated Ca 2ϩ influx is integrated in many receptor-mediated signaling pathways outside the visual system.…”

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confidence: 99%

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Receptor-induced Activation of Drosophila TRPγ by Polyunsaturated Fatty Acids

Jörs

Kazanski

Foik

et al. 2006

Journal of Biological Chemistry

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Cellular calcium homeostasis is regulated by hormones and neurotransmitters, resulting in the activation of a variety of proteins, in particular, channel proteins of the plasma membrane and of intracellular compartments. Such channels are, for example, TRP channels of the TRPC protein family that are activated by various mediators from receptor-stimulated signaling cascades. In Drosophila, two TRPC channels, TRP and TRPL, are involved in phototransduction. In addition, a third Drosophila TRPC channel, TRP␥, has been identified and described as an auxiliary subunit of TRPL. Beyond it, our data show that heterologously expressed TRP␥ formed a receptor-activated, outwardly rectifying cation channel independent from TRPL coexpression. Analysis of the activation mechanism revealed that TRP␥ is activated by various polyunsaturated fatty acids generated in a phospholipase C-and phospholipase A 2 -dependent manner. The most potent activator of TRP␥, the stable analogue of arachidonic acid, 5,8,11,14-eicosatetraynoic acid, induced currents in single channel recordings. Here we show that upon heterologous expression TRP␥ forms a homomeric channel complex that is activated by polyunsaturated fatty acids as mediators of receptor-dependent signaling pathways. Reverse transcription PCR analysis showed that TRP␥ is expressed in Drosophila heads and bodies. Its body-wide expression pattern and its activation mechanism suggest that TRP␥ forms a fly cation channel responsible for the regulation of intracellular calcium in a variety of hormonal signaling cascades.

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Section: Discussionsupporting

confidence: 87%

mentioning

confidence: 99%

Receptor-induced Activation of Drosophila TRPγ by Polyunsaturated Fatty Acids

Jörs

Kazanski

Foik

et al. 2006

Journal of Biological Chemistry

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“…During the course of the experiment, it was reported that TRPL was expressed not only in Drosophila eyes but also in the Malpighian tubules (29). We therefore tested whether the highly significant difference in TRPL expression was maintained if RNA from heads only was measured.…”

Section: Methodsmentioning

confidence: 99%

Systems-level analysis and evolution of the phototransduction network inDrosophila

Landry¹,

Castillo-Davis

Ogura³

et al. 2007

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

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Networks of interacting genes are responsible for generating life's complexity and for mediating how organisms respond to their environment. Thus, a basic understanding of genetic variation in gene networks in natural populations is important for elucidating how changes at the genetic level map to higher levels of biological organization. Here, using the well-characterized phototransduction network in Drosophila, we analyze variation in gene expression within and between two closely related species, Drosophila melanogaster and Drosophila simulans, under different environmental conditions. Gene expression levels in the pathway are largely conserved between these two sibling species. For most genes in the network, differences in level of gene expression between species are correlated with degree of polymorphism within species. However, one gene encoding the light-induced ion channel TRPL (transient receptor potential-like) shows an excess of expression divergence relative to polymorphism, suggesting a possible role for natural selection in shaping this expression difference between species. Finally, this difference in TRPL expression likely has significant functional consequences, because it is known that a high level of rhabdomeral TRPL leads to increased sensitivity to dim background light and an increased response to a wider range of light intensities. These results provide a preliminary quantification of variation and divergence of gene expression between species in a known gene network and provide a foundation for a system-level understanding of functional and evolutionary change.natural selection ͉ gene expression ͉ network G enes act together in networks to generate important organismal phenotypes. Understanding the general properties of gene networks and how they adapt to environmental changes is of fundamental importance to evolutionary biology. Elucidating the structure of gene networks represents a major goal of systems biology and ecological genomics in the postgenomic era. Recent approaches have primarily exploited genomic and computational methods to focus on distantly related organisms (1). However, very little is known about the basic microevolutionary properties of known genetic networks, information that is crucial for understanding network function, regulation, and evolution, because key adaptations first emerge at the population level. For example, very little is known about natural variation within gene expression networks in different populations, different species, and under different environmental conditions. How much expression variation is present in a gene network within a population? Do genes that show low variation within one species also show low variation in closely related species? To attempt to answer these fundamental questions, we analyzed variation in gene expression in the phototransduction network under two different environmental conditions within and between species of Drosophila melanogaster and its sibling species Drosophila simulans, which diverged Ϸ3 Mya (2).The Drosophi...

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“…PDE1 and PDE11), so this allows for further cross-talk between cAMP and cGMP under physiological conditions. , receptor guanylate cyclase Gyc76c ] and Ca 2+ channels [L-type (MacPherson et al, 2001), transient receptor potential (TRP) and TRP-like (TRPL) (MacPherson et al, 2005) and cyclic nucleotide-gated (CNG) (Broderick et al, 2003)] on the basolateral membrane. Intracellular organelles, i.e.…”

Section: Camp Signallingmentioning

confidence: 99%

Cell signalling mechanisms for insect stress tolerance

Davies

Cabrero

Overend

et al. 2014

Journal of Experimental Biology

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Insects successfully occupy most environmental niches and this success depends on surviving a broad range of environmental stressors including temperature, desiccation, xenobiotic, osmotic and infection stress. Epithelial tissues play key roles as barriers between the external and internal environments and therefore maintain homeostasis and organismal tolerance to multiple stressors. As such, the crucial role of epithelia in organismal stress tolerance cannot be underestimated. At a molecular level, multiple cell-specific signalling pathways including cyclic cAMP, cyclic cGMP and calcium modulate tissue, and hence, organismal responses to stress. Thus, epithelial cell-specific signal transduction can be usefully studied to determine the molecular mechanisms of organismal stress tolerance in vivo. This review will explore cell signalling modulation of stress tolerance in insects by focusing on cell signalling in a fluid transporting epithelium -the Malpighian tubule. Manipulation of specific genes and signalling pathways in only defined tubule cell types can influence the survival outcome in response to multiple environmental stressors including desiccation, immune, salt (ionic) and oxidative stress, suggesting that studies in the genetic model Drosophila melanogaster may reveal novel pathways required for stress tolerance.

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Transient Receptor Potential-Like Channels Are Essential for Calcium Signaling and Fluid Transport in a Drosophila Epithelium

Abstract: ABSTRACT

Cited by 26 publications

References 60 publications

Receptor-induced Activation of Drosophila TRPγ by Polyunsaturated Fatty Acids

Receptor-induced Activation of Drosophila TRPγ by Polyunsaturated Fatty Acids

Systems-level analysis and evolution of the phototransduction network inDrosophila

Cell signalling mechanisms for insect stress tolerance

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