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Logo of jphysiolThe Journal of Physiology SiteMembershipSubmissionJ Physiol
J Physiol. Aug 15, 2005; 567(Pt 1): 45–51.
Published online Jun 16, 2005. doi:  10.1113/jphysiol.2005.092551
PMCID: PMC1474165

TRP channels in Drosophila photoreceptor cells

Abstract

TRP cation channels are conserved throughout animal phylogeny and include many members that function in sensory physiology. The founding TRP is required for Drosophila phototransduction and has served as a paradigm for unravelling the roles and macromolecular organizations of TRP channels in native tissues. Two other TRPC channels, TRPL and TRPγ, are expressed in photoreceptor cells and form heteromultimers with TRP and with each other. TRP is a member of a supramolecular signalling complex, the signalplex, which includes the PDZ scaffold protein, INAD, and two other core members that remain bound and depend on INAD for localization. Other INAD binding proteins are proposed to interact dynamically with INAD, one of which, TRPL, undergoes light-dependent translocation in photoreceptor cells. Surprisingly, TRP has non-channel functions, including an anchoring role necessary for retaining INAD in the rhabdomeres. Loss of TRP function or constitutive TRP activity results in retinal degeneration, which can be suppressed by disruption or overexpression of the Na+/Ca2+ exchanger, CalX, respectively. Given that hypoxia-induced constitutive activity of some mammalian TRPs leads to neuronal cell death, interventions that increase Na+/Ca2+ exchanger or decrease TRP function have the potential to reduce the severity of cell death due to ischaemia.

The superfamily of TRP channels comprises 28 members in mammals and 13 in Drosophila, many of which function in sensory physiology (reviewed in Montell, 2005). These include roles in phototransduction, taste, thermosensation, osmosensation, touch and hearing. Among the many questions in the TRP field are those concerning the activation mechanisms of the channels in vivo, descriptions of their physiological roles, identification of interacting proteins and the relationship of TRPs to human health and disease.

The Drosophila trp mutation was identified on the basis of a defect in visual transduction (Cosens & Manning, 1969). Drosophila phototransduction utilizes a phosphoinositide (PI) signalling cascade and a phospholipase C (PLC), encoded by the norpA locus (reviewed in Montell, 1999). The end result of this cascade is depolarization of the photoreceptor cells due to opening of Na+- and Ca2+-permeable channels. As such, Drosophila phototransduction is distinct from the cascade in mammalian rods and cones, which utilize cGMP as the second messenger and culminate with the closing of cGMP-gated channels. Rather, Drosophila phototransduction bears greater similarity to the cascade that operates in a small subset of intrinsically photosensitive retinal ganglion cells (ipRGCs) that function in circadian rhythm (reviewed in Berson, 2003). As in fly photoreceptor cells, the ipRGCs depolarize upon exposure to light and have been suggested to operate through PI signalling (Berson et al. 2002; Isoldi et al. 2005; Panda et al. 2005; Qiu et al. 2005).

Much of the interest in Drosophila phototransduction stems from the apparent similarities in signalling in fly photoreceptor cells and the wide array of excitable and non-excitable cells in mammals that rely upon PI signalling and conclude with opening of Ca2+-permeable channels. Such cascades appear to be required in processes ranging from the immune response to fluid secretion, apoptosis and cell proliferation (reviewed in Parekh et al. 1997). However, the identities of the Ca2+ influx channels and their modes of activation have been enigmatic.

The Drosophila visual system offers a combination of important approaches to characterize PI-mediated signalling in general and Ca2+ influx in particular. These include the ability to perform forward and reverse genetics, to generate transgenic animals and to employ electrophysiological, cell biological and biochemical techniques. Many of the proteins important in Drosophila phototransduction can be obtained at high levels due to the relatively large size of the fly's compound eyes, and the reiterative structure of 800 basic eye units, referred to as ommatidia.

Identification and mode of activation of Drosophila TRP

In contrast to the sustained light response observed in wild-type flies, in the trp mutant, the light response is transient. The first evidence that trp disrupts a protein required for Ca2+ entry was obtained from an analysis of the light-dependent movement of pigment granules in photoreceptor cells, which comprises a type of pupillary mechanism. The migration of these granules is a Ca2+-dependent phenomenon and in trp flies this movement is transient (Lo & Pak, 1981). More direct evidence that there was a defect in Ca2+ influx required the development and application of patch clamp recordings to a preparation of isolated Drosophila ommatidia. Using whole-cell recordings, it was apparent that there was ~10-fold decrease in Ca2+ influx in the trp flies, suggesting that the mutation disrupted a Ca2+ entry channel or a protein required for its activity (Hardie & Minke, 1992).

At the time that the trp gene was cloned, the predicted protein product did not have significant sequence identity to other proteins in the databanks, but had a predicted topology of multiple transmembrane segments, most likely six (Fig. 1A), reminiscent of members of the superfamily of voltage- and second messenger-gated cation channels (Montell et al. 1985; Montell & Rubin, 1989). Confirmation that Drosophila TRP was a Ca2+-permeable influx channel was obtained upon expressing the protein in heterologous expression systems, such as Sf9 and HEK293T cells (Vaca et al. 1994; Xu et al. 1997). Moreover, TRP had some selectivity for Ca2+ over Na+ (~10: 1), but was not nearly as selective as voltage-gated Ca2+ channels.

Figure 1
Organization of TRP domains and TRP homo- and heteromultimers

A key question concerns the mechanism leading to activation of TRP in vivo. There is a uniform consensus that TRP requires activity of PLC since the light response is eliminated in norpA flies (Bloomquist et al. 1988). However, the link between stimulation of PLC and opening of the TRP channels is not completely resolved. PLC-mediated hydrolysis of phosphatidylinositol 4,5-bisphosphate (PIP2) leads to production of inositol 1,4,5-trisphosphate (IP3) and diacylglycerol (DAG). Thus, there are at least three proposed modes through which PIP2 hydrolysis leads to activation of TRP. According to one model, IP3 causes release of Ca2+ from internal stores, which in turn activates TRP through a store-operated mechanism. However, release of caged IP3 in dark adapted photoreceptor cells does not simulate the light response (Hardie & Raghu, 1998) and elimination of the only IP3 receptor encoded in the fly genome has no impact on phototransduction (Acharya et al. 1997; Raghu et al. 2000a). An in vitro study suggests that PIP2 inhibits a TRP-related channel (TRPL, see below) expressed in photoreceptor cells (Phillips et al. 1992; Estacion et al. 2001); however, in vivo evidence is lacking for both TRP and TRPL.

Currently, the strongest candidates for activating TRP are polyunsaturated fatty acids (PUFAs), which are formed from DAG. In support of this proposal are the findings that PUFAs, such as arachidonic acid and linoleic acid, lead to activation of TRP in photoreceptor cells from isolated ommatidia (Chyb et al. 1999). In addition, both TRP and TRPL are constitutively active in a mutant, rdgA, that eliminates the DAG kinase that functions in fly photoreceptor cells (Raghu et al. 2000b). It has been argued that the effects of PUFAs are indirect since they can act as mitochondrial uncouplers and anoxia can lead to constitutive activation of TRP (Agam et al. 2000). However, this does not appear to be the case as activation of the channels by metabolic inhibitors requires PLC activity (Hardie et al. 2003). Whether PUFAs interact directly with TRP remains to be addressed.

Given that the light response is not eliminated in trp flies, there must be one or more additional channels that function in Drosophila phototransduction. A second such channel is TRPL as trpl; trp double mutant flies are completely unresponsive to light (Niemeyer et al. 1996; Reuss et al. 1997). Nevertheless, elimination of trpl alone has relatively subtle effects on the light response under typical recording conditions (Niemeyer et al. 1996), although during very long light stimulation, trpl photoreceptor cells are unable to sustain a maximal light response (Leung et al. 2000).

TRPL has been expressed in vitro and is a constitutively active non-specific cation channel (Hu et al. 1994; Harteneck et al. 1995; Xu et al. 1997). However, TRPL is not constitutively active in vivo as there is no dark current in trp photoreceptor cells. An apparent resolution to this conundrum is that TRPL requires interaction with other TRP channels for regulated activity. A third TRP-related channel is expressed in fly photoreceptor cells, TRPγ, and TRPL forms obligatory heteromultimers with either TRP or TRPγ (Xu et al. 1997, 2000). TRP is 10-fold more abundant that TRPL or TRPγ and the full composition of TRPC channels in photoreceptor cells are TRP homomultimers and heteromultimers composed of TRP/TRPL and TRPγ/TRPL (Fig. 1B). Neither of these latter heteromultimers is constitutively open, but is activated through stimulation of PLC-dependent signalling. This is particularly notable with respect to the TRPγ/TRPL heteromultimer since in vitro expression of each of the individual channels leads to constitutively activity. Currently, a trpγ loss-of-function mutation is not available, although a dominant negative form of TRPγ suppresses most of the remaining light-dependent conductance in trp photoreceptor cells (Xu et al. 2000).

Light regulated translocation of TRPL

A fascinating feature of TRPL, which is shared by the trimeric G protein (Gq) and the major arrestin (Arr2), is that it undergoes dramatic light-dependent translocation. In dark-adapted flies, most of the TRPL is in the rhabdomeres, whereas after 1 h, the channel is primarily in the cell bodies (Bähner et al. 2002) (Fig. 2). The return to the rhabdomeres occurs over a slightly faster time span. The dynamic transport of TRPL out of the rhabdomeres has been proposed to contribute to long-term adaptation (Bähner et al. 2002).

Figure 2
TRPL undergoes light-dependent translocation from the rhabdomeres

The mechanisms underlying the light-dependent movements of TRPL are not known, although insights have been provided into the translocations of Arr2 and the G subunit. As is the case with TRPL, G shuttles out of the rhabdomeres in response to light (Kosloff et al. 2003), while the translocation of Arr2 occurs in the opposite direction (Kiselev et al. 2000). Similar light-induced transport of arrestin and the transducin occur in rods and cones (reviewed in Arshavsky, 2003). The movement of the Drosophila Arr2 into the rhabdomeres depends on PI mediated interactions with the myosin III, NINAC (Lee et al. 1993). The shuttling of G into the rhabdomeres also requires NINAC, although a role for PIs has not been addressed (Cronin et al. 2004). The reciprocal transport of Arr2 or G out of the rhabdomeres does not depend on NINAC, which is consistent with the orientation of the actin filaments and the presumption that NINAC is a plus-ended motor, based on studies of a vertebrate homolog (Komaba et al. 2003). These findings raise the question as to whether TRPL is also shuttled into the rhabdomeres via a PI and NINAC-dependent mechanism.

The INAD signalplex

The TRP channel and many of the other signalling proteins critical for Drosophila phototransduction associate in a macromolecular assembly, the signalplex. The central player in the signalplex is INAD, a scaffold comprised of five PDZ protein interaction modules. Three proteins, TRP, PLC (NORPA) and a protein kinase C appear to be constitutively bound to INAD and depend on INAD for retention in the microvillar portion of the photoreceptor cells, the rhabdomeres (Huber et al. 1996; Shieh & Zhu, 1996; Chevesich et al. 1997; Tsunoda et al. 1997) (Fig. 3), which is the fly equivalent of the outer segments of mammalian rods and cones. In addition to the three core INAD binding proteins, TRP, PLC and PKC, at least five other proteins appear to associate with INAD. These include the major rhodopsin (Rh1), a myosin III (NINAC), TRPL, calmodulin (Chevesich et al. 1997; Xu et al. 1998; Wes et al. 1999) and the immunophilin, FKBP59, which has been reported to also bind directly to TRPL (Goel et al. 2001). In contrast to the core binding partners, the other INAD binding proteins do not depend on INAD for retention in rhabdomeres (Xu et al. 1998; Wes et al. 1999). It is interesting to speculate that these latter INAD targets may associate dynamically with INAD, perhaps in a light-dependent manner, although, this has not been demonstrated.

Figure 3
The signalplex

A central question concerns the roles of the TRP/INAD interaction. One function as mentioned above, is to retain TRP in the rhabdomeres (Chevesich et al. 1997). An additional possibility is that the association of TRP with INAD may participate in rapid signalling as the fly phototransduction cascade is maximally activated within 20 ms and is the fastest known G protein-coupled signalling cascade. However, mutation of the INAD binding site in TRP does not have a major impact on the light response (Li & Montell, 2000), although, a portion of the TRP pool is presumably interacting indirectly with INAD through TRPL. Consistent with this latter proposal is the observation that TRP channels that are not associated with INAD contribute significantly to signalling only when TRPL is present in the photoreceptor cells (Leung et al. 2000). Thus, indirect interactions between TRP and INAD may be sufficient for proper signalling. Nevertheless, the signalplex is required for rapid termination of the photoresponse, as mutations in NINAC or the PKC, which preclude their association with INAD, result in slow response termination (Adamski et al. 1998; Wes et al. 1999).

Multifunctional roles of TRP

A surprising finding is that TRP is a multifunctional protein with an anchoring role in addition to its more recognized role as a cation channel. Just as the TRP/INAD complex is essential for retention of TRP in rhabdomeres, there is a reciprocal requirement for this interaction for maintaining INAD in the rhabdomeres (Li & Montell, 2000; Tsunoda et al. 2001). In fact, deletion of the C-terminal four residues of TRP (TRPΔ1272), which prevents direct association with INAD, results in mislocalization of the entire core complex (Li & Montell, 2000). The anchoring role of TRP may provide an explanation for the high concentration of TRP in the rhabdomeres and its presence in approximately equal levels with INAD (Huber et al. 1996).

An additional non-channel role for TRP includes a requirement for the light-dependent translocation of TRPL out of the rhabdomeres (Bähner et al. 2002). The shuttling of TRPL does not depend on the PLC encoded by norpA, thus TRP activity is not required. However, elimination of TRP prevents the dynamic transport of TRPL.

Due to the dual channel and non-channel roles of TRP, the question arises as to the phenotypes resulting from disruption of one or the other TRP function. Null mutations in TRP result in a transient response to light, disruption of the core complex and light-dependent retinal degeneration. As described above, the TRPΔ1272 mutation in TRP, which prevents its interaction with INAD and thereby interferes with its anchoring role, has no significant impact on signalling and causes only minor retinal degeneration.

Identification of the consequences resulting from specifically disrupting the channel function of TRP has been difficult since, until recently, the extant TRP alleles obtained through forward genetic screens express greatly reduced concentrations of TRP protein. However, a recently isolated TRP allele (trp14) with a missense mutation just C-terminal to the sixth transmembrane segment is expressed at nearly normal levels and does not disrupt the core complex (T. Wang and C. Montell, unpublished observations). In contrast to flies harbouring null mutations in both trp and trpl, which are blind, trpl; trp14 flies exhibit a transient response to light. Thus, the mutation in TRP14 greatly increases the light-dependent inactivation of the channel. The trp14 flies also exhibit light-induced retinal degeneration similar to that observed in trp null flies. These results demonstrate that an alteration in TRP activity results in greater retinal degeneration than that caused by disruption of the TRP anchoring function.

TRP channels and retinal degeneration

Photoreceptor cell death occurs either from loss-of-function mutations in TRP (Cosens & Perry, 1972) or as a result of constitutive activation of the channel (Yoon et al. 2000). Interestingly, constitutive activity of several mammalian TRPs, such as occurs under ischaemic conditions, leads to cell death in the mammalian brain (Hara et al. 2002; Aarts et al. 2003). Thus, there are parallels in mammals and flies between changes in TRP channel activity and neuronal cell death.

Since the retinal degeneration associated with perturbations in trp channel function is more severe than that resulting from disruption of the TRP anchoring role, it would appear that the basis of the cell death is due to increased or decreased Ca2+ influx. Consistent with this proposal, the cell death associated with trp14 is reduced by eliminating the Na+/Ca2+ exchanger, CalX, which colocalizes with TRP in the rhabdomeres (Fig. 4) and functions in the photoresponse (T. Wang and C. Montell, unpublished observations). Conversely, the profound retinal degeneration occurring from constitutive activity of TRP is suppressed by overexpression of CalX (Wang et al. 2005). These results raise the possibility that the cell death occurring in the mammalian brain, due to hypoxia-induced activation of TRP channels can be suppressed by approaches that increase the activity of the Na+/Ca2+ exchanger or reduce the activity of TRPs.

Figure 4
TRP and CalX

References

  • Aarts M, Iihara K, Wei WL, Xiong ZG, Arundine M, Cerwinski W, MacDonald JF, Tymianski M. A key role for TRPM7 channels in anoxic neuronal death. Cell. 2003;115:863–877. [PubMed]
  • Acharya JK, Jalink K, Hardy RW, Hartenstein V, Zuker CS. InsP3 receptor essential for growth and differentiation but not for vision in Drosophila. Neuron. 1997;18:881–887. [PubMed]
  • Adamski FM, Zhu M-Y, Bahiraei F, Shieh B-H. Interaction of eye protein kinase C and INAD in Drosophila: localization of binding domains and electrophysiological characterization of a loss of association in transgenic flies. J Biol Chem. 1998;273:17713–17719. [PubMed]
  • Agam K, von Campenhausen M, Levy S, Ben-Ami HC, Cook B, Kirschfeld K, Minke B. Metabolic stress reversibly activates the Drosophila light-sensitive channels TRP and TRPL in vivo. J Neurosci. 2000;20:5748–5755. [PubMed]
  • Arshavsky VY. Protein translocation in photoreceptor light adaptation: a common theme in vertebrate and invertebrate vision. Sci STKE 2003. 2003:PE43. [PubMed]
  • Bähner M, Frechter S, Da Silva N, Minke B, Paulsen R, Huber A. Light-regulated subcellular translocation of Drosophila TRPL channels induces long-term adaptation and modifies the light-induced current. Neuron. 2002;34:83–93. [PubMed]
  • Berson DM. Strange vision: ganglion cells as circadian photoreceptors. Trends Neurosci. 2003;26:314–320. [PubMed]
  • Berson DM, Dunn FA, Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science. 2002;295:1070–1073. [PubMed]
  • Bloomquist BT, Shortridge RD, Schneuwly S, Perdew M, Montell C, Steller H, Rubin G, Pak WL. Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell. 1988;54:723–733. [PubMed]
  • Chevesich J, Kreuz AJ, Montell C. Requirement for the PDZ domain protein, INAD, for localization of the TRP store-operated channel to a signaling complex. Neuron. 1997;18:95–105. [PubMed]
  • Chyb S, Raghu P, Hardie RC. Polyunsaturated fatty acids activate the Drosophila light-sensitive channels TRP and TRPL. Nature. 1999;397:255–259. [PubMed]
  • Cosens DJ, Manning A. Abnormal electroretinogram from a Drosophila mutant. Nature. 1969;224:285–287. [PubMed]
  • Cosens D, Perry MM. The fine structure of the eye of a visual mutant, A-type, of Drosophila melanogaster. J Insect Physiol. 1972;18:1773–1786. [PubMed]
  • Cronin MA, Diao F, Tsunoda S. Light-dependent subcellular translocation of Gqα in Drosophila photoreceptors is facilitated by the photoreceptor-specific myosin III NINAC. J Cell Sci. 2004;117:4797–4806. [PubMed]
  • Estacion M, Sinkins WG, Schilling WP. Regulation of Drosophila transient receptor potential-like (TrpL) channels by phospholipase C-dependent mechanisms. J Physiol. 2001;530:1–19. [PMC free article] [PubMed]
  • Goel M, Garcia R, Estacion M, Schilling WP. Regulation of Drosophila TRPL channels by immunophilin FKBP59. J Biol Chem. 2001;276:38762–38773. [PubMed]
  • Hara Y, Wakamori M, Ishii M, Maeno E, Nishida M, Yoshida T, Yamada H, Shimizu S, Mori E, Kudoh J, Shimizu N, Kurose H, Okada Y, Imoto K, Mori Y. LTRPC2 Ca2+-permeable channel activated by changes in redox status confers susceptibility to cell death. Mol Cell. 2002;9:163–173. [PubMed]
  • Hardie RC, Martin F, Chyb S, Raghu P. Rescue of light responses in the Drosophila ‘null’ phospholipase C mutant, norpAP24, by the diacylglycerol kinase mutant, rdgA, and by metabolic inhibition. J Biol Chem. 2003;278:18851–18858. [PubMed]
  • Hardie RC, Minke B. The trp gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors. Neuron. 1992;8:643–651. [PubMed]
  • Hardie RC, Raghu P. Activation of heterologously expressed Drosophila TRPL channels: Ca2+ is not required and InsP3 is not sufficient. Cell Calcium. 1998;24:153–163. [PubMed]
  • Harteneck C, Obukhov AG, Zobel A, Kalkbrenner F, Schultz G. The Drosophila cation channel trpl expressed in Sf9 cells is stimulated by agonists of G-protein-coupled receptors. FEBS Lett. 1995;358:297–300. [PubMed]
  • Hu Y, Vaca L, Zhu X, Birnbaumer L, Kunze DL, Schilling WP. Appearance of a novel Ca2+ influx pathway in Sf9 insect cells following expression of the transient potential-like (trpl) protein of Drosophila. Biochem Biophys Res Commun. 1994;201:1050–1056. [PubMed]
  • Huber A, Sander P, Gobert A, Bähner M, Hermann R, Paulsen R. The transient receptor potential protein (Trp), a putative store-operated Ca2+ channel essential for phosphoinositide-mediated photoreception, forms a signaling complex with NorpA, InaC and InaD. EMBO J. 1996;15:7036–7045. [PMC free article] [PubMed]
  • Isoldi MC, Rollag MD, de Lauro Castrucci AM, Provencio I. Rhabdomeric phototransduction initiated by the vertebrate photopigment melanopsin. Proc Natl Acad Sci U S A. 2005 [PMC free article] [PubMed]
  • Kiselev A, Socolich M, Vinos J, Hardy RW, Zuker CS, Ranganathan R. A molecular pathway for light-dependent photoreceptor apoptosis in Drosophila. Neuron. 2000;28:139–152. [PubMed]
  • Komaba S, Inoue A, Maruta S, Hosoya H, Ikebe M. Determination of human myosin III as a motor protein having a protein kinase activity. J Biol Chem. 2003;278:21352–21360. [PubMed]
  • Kosloff M, Elia N, Joel-Almagor T, Timberg R, Zars TD, Hyde DR, Minke B, Selinger Z. Regulation of light-dependent Gqα translocation and morphological changes in fly photoreceptors. EMBO J. 2003;22:459–468. [PMC free article] [PubMed]
  • Lee K-M, Toscas K, Villereal ML. Inhibition of bradykinin- and thapsigargin-induced Ca2+ entry by tyrosine kinase inhibitors. J Biol Chem. 1993;15:9945–9948. [PubMed]
  • Leung HT, Geng C, Pak WL. Phenotypes of trpl mutants and interactions between the transient receptor potential (TRP) and TRP-like channels in Drosophila. J Neurosci. 2000;20:6797–6803. [PubMed]
  • Li HS, Montell C. TRP and the PDZ protein, INAD, form the core complex required for retention of the signalplex in Drosophila photoreceptor cells. J Cell Biol. 2000;150:1411–1422. [PMC free article] [PubMed]
  • Lo M-VC, Pak WL. Light-induced pigment granule migration in the retinular cells of Drosophila melanogaster. J General Physiol. 1981;77:155–175. [PMC free article] [PubMed]
  • Montell C. Drosophila visual transduction. Ann Rev Cell Dev Biol. 1999;15:231–268. [PubMed]
  • Montell C. The TRP superfamily of cation channels. Sci STKE 2005. 2005:re3. [PubMed]
  • Montell C, Jones K, Hafen E, Rubin G. Rescue of the Drosophila phototransduction mutation trp by germline transformation. Science. 1985;230:1040–1043. [PubMed]
  • Montell C, Rubin GM. Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron. 1989;2:1313–1323. [PubMed]
  • Niemeyer BA, Suzuki E, Scott K, Jalink K, Zuker CS. The Drosophila light-activated conductance is composed of the two channels TRP and TRPL. Cell. 1996;85:651–659. [PubMed]
  • Panda S, Nayak SK, Campo B, Walker JR, Hogenesch JB, Jegla T. Illumination of the melanopsin signaling pathway. Science. 2005;307:600–604. [PubMed]
  • Parekh AB, Fleig A, Penner R. The store-operated calcium current ICRAC: nonlinear activation by InsP3 and dissociation from calcium release. Cell. 1997;89:973–980. [PubMed]
  • Phillips AM, Bull A, Kelly LE. Identification of a Drosophila gene encoding a calmodulin-binding protein with homology to the trp phototransduction gene. Neuron. 1992;8:631–642. [PubMed]
  • Qiu X, Kumbalasiri T, Carlson SM, Wong KY, Krishna V, Provencio I, Berson DM. Induction of photosensitivity by heterologous expression of melanopsin. Nature. 2005;433:745–749. [PubMed]
  • Raghu P, Colley NJ, Webel R, James T, Hasan G, Danin M, Selinger Z, Hardie RC. Normal phototransduction in Drosophila photoreceptors lacking an InsP3 receptor gene. Mol Cell Neurosci. 2000a;15:429–445. [PubMed]
  • Raghu P, Usher K, Jonas S, Chyb S, Polyanovsky A, Hardie RC. Constitutive activity of the light-sensitive channels TRP and TRPL in the Drosophila diacylglycerol kinase mutant. Rdga Neuron. 2000b;26:169–179. [PubMed]
  • Reuss H, Mojet MH, Chyb S, Hardie RC. In vivo analysis of the Drosophila light-sensitive channels, TRP and TRPL. Neuron. 1997;19:1249–1259. [PubMed]
  • Shieh B-H, Zhu M-Y. Regulation of the TRP Ca2+ channel by INAD in Drosophila photoreceptors. Neuron. 1996;16:991–998. [PubMed]
  • Tsunoda S, Sierralta J, Sun Y, Bodner R, Suzuki E, Becker A, Socolich M, Zuker CS. A multivalent PDZ-domain protein assembles signalling complexes in a G-protein-coupled cascade. Nature. 1997;388:243–249. [PubMed]
  • Tsunoda S, Sun Y, Suzuki E, Zuker C. Independent anchoring and assembly mechanisms of INAD signaling complexes in Drosophila photoreceptors. J Neurosci. 2001;21:150–158. [PubMed]
  • Vaca L, Sinkins WG, Hu Y, Kunze DL, Schilling WP. Activation of recombinant trp by thapsigargin in Sf9 insect cells. Am J Physiol. 1994;266:C1501–C1505. [PubMed]
  • Wang T, Xu H, Oberwinkler J, Gu Y, Hardie RC, Montell C. Light activation, adaptation, and cell survival functions of the Na+/Ca2+ exchanger CalX. Neuron. 2005;45:367–378. [PubMed]
  • Wes PD, Xu X-ZS, Li H-S, Chien F, Doberstein SK, Montell C. Termination of phototransduction requires binding of the NINAC myosin III and the PDZ protein INAD. Nat Neurosci. 1999;2:447–453. [PubMed]
  • Xu XZ, Chien F, Butler A, Salkoff L, Montell C. TRPγ, a Drosophila TRP-related subunit, forms a regulated cation channel with TRPL. Neuron. 2000;26:647–657. [PubMed]
  • Xu X-ZS, Choudhury A, Li X, Montell C. Coordination of an array of signaling proteins through homo- and heteromeric interactions between PDZ domains and target proteins. J Cell Biol. 1998;142:545–555. [PMC free article] [PubMed]
  • Xu X-ZS, Li H-S, Guggino WB, Montell C. Coassembly of TRP and TRPL produces a distinct store-operated conductance. Cell. 1997;89:1155–1164. [PubMed]
  • Yoon J, Ben-Ami HC, Hong YS, Park S, Strong LL, Bowman J, Geng C, Baek K, Minke B, Pak WL. Novel mechanism of massive photoreceptor degeneration caused by mutations in the trp gene of Drosophila. J Neurosci. 2000;20:649–659. [PubMed]

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