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1.
PLoS One ; 19(6): e0303882, 2024.
Artigo em Inglês | MEDLINE | ID: mdl-38848405

RESUMO

Activated GPCRs are phosphorylated and internalized mostly via clathrin-mediated endocytosis (CME), which are then sorted for recycling or degradation. We investigated how differential activation of the same GPCR affects its endocytic trafficking in vivo using rhodopsin as a model in pupal photoreceptors of flies expressing mCherry-tagged rhodopsin 1 (Rh1-mC) or GFP-tagged arrestin 1 (Arr1-GFP). Upon blue light stimulation, activated Rh1 recruited Arr1-GFP to the rhabdomere, which became co-internalized and accumulated in cytoplasmic vesicles of photoreceptors. This internalization was eliminated in shits1 mutants affecting dynamin. Moreover, it was blocked by either rdgA or rdgB mutations affecting the PIP2 biosynthesis. Together, the blue light-initiated internalization of Rh1 and Arr1 belongs to CME. Green light stimulation also triggered the internalization and accumulation of activated Rh1-mC in the cytoplasm but with faster kinetics. Importantly, Arr1-GFP was also recruited to the rhabdomere but not co-internalized with Rh1-mC. This endocytosis was not affected in shits1 nor rdgA mutants, indicating it is not CME. We explored the fate of internalized Rh1-mC following CME and observed it remained in cytoplasmic vesicles following 30 min of dark adaptation. In contrast, in the non-CME Rh1-mC appeared readily recycled back to the rhabdomere within five min of dark treatment. This faster recycling may be regulated by rhodopsin phosphatase, RdgC. Together, we demonstrate two distinct endocytic and recycling mechanisms of Rh1 via two light stimulations. It appears that each stimulation triggers a distinct conformation leading to different phosphorylation patterns of Rh1 capable of recruiting Arr1 to rhabdomeres. However, a more stable interaction leads to the co-internalization of Arr1 that orchestrates CME. A stronger Arr1 association appears to impede the recycling of the phosphorylated Rh1 by preventing the recruitment of RdgC. We conclude that conformations of activated rhodopsin determine the downstream outputs upon phosphorylation that confers differential protein-protein interactions.


Assuntos
Endocitose , Rodopsina , Rodopsina/metabolismo , Rodopsina/genética , Animais , Fosforilação , Transporte Proteico , Luz , Mutação , Células Fotorreceptoras de Invertebrados/metabolismo , Drosophila melanogaster/metabolismo , Clatrina/metabolismo
2.
J Insect Physiol ; 155: 104636, 2024 Jun.
Artigo em Inglês | MEDLINE | ID: mdl-38609008

RESUMO

Photic entrainment is an essential function of the circadian clock, which enables organisms to set the appropriate timing of daily behavioral and physiological events. Recent studies have shown that the mechanisms of the circadian clock and photic entrainment vary among insect species. This study aimed to elucidate the circadian photoreceptors necessary for photic entrainment in firebrats Thermobia domestica, one of the most primitive apterygote insects. A homology search of publicly available RNA sequence (RNA-seq) data from T. domestica exhibited a cryptochrome 2 (cry2) gene and three opsin genes, opsin long wavelength 1 (opLW1), opLW2, and opUV, as candidate circadian photoreceptors. We examined the possible involvement of these genes in photic entrainment of firebrat locomotor rhythms. Firebrats had the highest entrainability to the light-dark cycle of green light. Treatment with dsRNA of the candidate genes strongly downregulated the respective targeted genes, and in the case of opsin genes, other untargeted genes were occasionally downregulated to various degrees. Under constant light, most control firebrats became arrhythmic, whereas a fraction of those treated with double RNAi of the two opLWs remained rhythmic. Behavioral experiments revealed that the transient cycles necessary for re-entrainment to shifted light cycles were lengthened when opLW2 expression was reduced. These results suggest that opLW2 is involved in the photic entrainment of circadian rhythm in firebrats.


Assuntos
Ritmo Circadiano , Animais , Proteínas de Insetos/genética , Proteínas de Insetos/metabolismo , Locomoção , Tephritidae/genética , Tephritidae/fisiologia , Opsinas/genética , Opsinas/metabolismo , Luz , Células Fotorreceptoras de Invertebrados/fisiologia , Células Fotorreceptoras de Invertebrados/metabolismo , Relógios Circadianos/genética
3.
Ying Yong Sheng Tai Xue Bao ; 35(3): 858-866, 2024 Mar 18.
Artigo em Inglês | MEDLINE | ID: mdl-38646774

RESUMO

Insect visual electrophysiological techniques are important to study the electrical characteristics of photoreceptor cells and visual neurons in insects, including electroretinography (ERG) and microelectrode intracellular recording (MIR). ERG records the changes of voltage or electric current in the retina of insects in response to different light stimuli, which occurs outside the cell. MIR records the changes in individual photoreceptor cells or visual neurons of an insect exposed to different lights, which occurs inside the cell. Insect visual electrophysiological techniques can explore the mechanism of electrophysiological response of insects' vision to light and reveal their sensitive light spectra and photoreceptor types. This review introduced the basic structure and the principle of ERG and MIR, and summarized their applications in insect researches in the past 20 years, which would provide references for elucidating the mechanism of light perception in insects and the use of insect phototropism to control pests.


Assuntos
Eletrorretinografia , Insetos , Células Fotorreceptoras de Invertebrados , Animais , Insetos/fisiologia , Eletrorretinografia/métodos , Células Fotorreceptoras de Invertebrados/fisiologia , Visão Ocular/fisiologia , Microeletrodos , Fenômenos Eletrofisiológicos , Eletrofisiologia/métodos
4.
Vision Res ; 219: 108403, 2024 06.
Artigo em Inglês | MEDLINE | ID: mdl-38581820

RESUMO

Bioluminescence is a prevalent phenomenon throughout the marine realm and is often the dominant source of light in mesophotic and aphotic depth horizons. Shrimp belonging to the superfamily Oplophoroidea are mesopelagic, perform diel vertical migration, and secrete a bright burst of bioluminescent mucous when threatened. Species in the family Oplophoridae also possess cuticular light-emitting photophores presumably for camouflage via counter-illumination. Many species within the superfamily express a single visual pigment in the retina, consistent with most other large-bodied mesopelagic crustaceans studied to date. Photophore-bearing species have an expanded visual opsin repertoire and dual-sensitivity visual systems, as evidenced by transcriptomes and electroretinograms. In this study, we used immunohistochemistry to describe opsin protein localization in the retinas of four species of Oplophoroidea and non-ocular tissues of Janicella spinicauda. Our results show that Acanthephyra purpurea (Acanthephyridae) retinas possess LWS-only photoreceptors, consistent with the singular peak sensitivity previously reported. Oplophoridae retinas contain two opsin clades (LWS and MWS) consistent with dual-sensitivity. Oplophorus gracilirostris and Systellaspis debilis have LWS in the proximal rhabdom (R1-7 cells) and MWS2 localized in the distal rhabdom (R8 cell). Surprisingly, Janicella spinicauda has LWS in the proximal rhabdom (R1-7) and co-localized MWS1 and MWS2 opsin paralogs in the distal rhabdom, providing the first evidence of co-localization of opsins in a crustacean rhabdomeric R8 cell. Furthermore, opsins were found in multiple non-ocular tissues of J. spinicauda, including nerve, tendon, and photophore. These combined data demonstrate evolutionary novelty and opsin duplication within Oplophoridae, with implications for visual ecology, evolution in mesophotic environments, and a mechanistic understanding of adaptive counter-illumination using photophore bioluminescence.


Assuntos
Opsinas , Animais , Opsinas/metabolismo , Células Fotorreceptoras de Invertebrados/fisiologia , Células Fotorreceptoras de Invertebrados/metabolismo , Retina/metabolismo , Imuno-Histoquímica , Filogenia
5.
Development ; 151(6)2024 Mar 15.
Artigo em Inglês | MEDLINE | ID: mdl-38421315

RESUMO

Vision is mainly based on two different tasks, object detection and color discrimination, carried out by photoreceptor (PR) cells. The Drosophila compound eye consists of ∼800 ommatidia. Every ommatidium contains eight PR cells, six outer cells (R1-R6) and two inner cells (R7 and R8), by which object detection and color vision are achieved, respectively. Expression of opsin genes in R7 and R8 is highly coordinated through the instructive signal from R7 to R8, and two major ommatidial subtypes are distributed stochastically; pale type expresses Rh3/Rh5 and yellow type expresses Rh4/Rh6 in R7/R8. The homeodomain protein Defective proventriculus (Dve) is expressed in yellow-type R7 and in six outer PRs, and it is involved in Rh3 repression to specify the yellow-type R7. dve mutant eyes exhibited atypical coupling, Rh3/Rh6 and Rh4/Rh5, indicating that Dve activity is required for proper opsin coupling. Surprisingly, Dve activity in R1 is required for the instructive signal, whereas activity in R6 and R7 blocks the signal. Our results indicate that functional coupling of two different neurons is established through signaling pathways from adjacent neurons that are functionally different.


Assuntos
Visão de Cores , Proteínas de Drosophila , Animais , Drosophila/genética , Drosophila/metabolismo , Opsinas/genética , Opsinas/metabolismo , Visão de Cores/genética , Proteínas de Drosophila/genética , Proteínas de Drosophila/metabolismo , Neurônios/metabolismo , Transdução de Sinais/genética , Células Fotorreceptoras de Invertebrados/fisiologia , Drosophila melanogaster/genética , Drosophila melanogaster/metabolismo
6.
J Comp Neurol ; 532(2): e25579, 2024 02.
Artigo em Inglês | MEDLINE | ID: mdl-38204156

RESUMO

Extensive analysis of the flower-visiting behavior of a butterfly, Papilio xuthus, has indicated complex interaction between chromatic, achromatic, and motion cues. Their eyes are spectrally rich with six classes of photoreceptors, respectively sensitive in the ultraviolet, violet, blue, green, red, and broad-band wavelength regions. Here, we studied the anatomy and physiology of photoreceptors and second-order neurons of P. xuthus, focusing on their spectral sensitivities and projection terminals to address where the early visual integration takes place. We thus found the ultraviolet, violet, and blue photoreceptors and all second-order neurons terminate in the distal region of the second optic ganglion, the medulla. We identified five types of second-order neurons based on the arborization in the first optic ganglion, the lamina, and the shape of the medulla terminals. Their spectral sensitivity is independent of the morphological types but reflects the combination of pre-synaptic photoreceptors. The results indicate that the distal medulla is the most plausible region for early visual integration.


Assuntos
Borboletas , Animais , Borboletas/fisiologia , Células Fotorreceptoras de Invertebrados/fisiologia , Olho , Neurônios
7.
J Biol Chem ; 300(1): 105484, 2024 Jan.
Artigo em Inglês | MEDLINE | ID: mdl-37992804

RESUMO

Sterols are hydrophobic molecules, known to cluster signaling membrane-proteins in lipid rafts, while methyl-ß-cyclodextrin (MßCD) has been a major tool for modulating membrane-sterol content for studying its effect on membrane proteins, including the transient receptor potential (TRP) channels. The Drosophila light-sensitive TRP channels are activated downstream of a G-protein-coupled phospholipase Cß (PLC) cascade. In phototransduction, PLC is an enzyme that hydrolyzes phosphatidylinositol 4,5-bisphosphate (PIP2) generating diacylglycerol, inositol-tris-phosphate, and protons, leading to TRP and TRP-like (TRPL) channel openings. Here, we studied the effects of MßCD on Drosophila phototransduction using electrophysiology while fluorescently monitoring PIP2 hydrolysis, aiming to examine the effects of sterol modulation on PIP2 hydrolysis and the ensuing light-response in the native system. Incubation of photoreceptor cells with MßCD dramatically reduced the amplitude and kinetics of the TRP/TRPL-mediated light response. MßCD also suppressed PLC-dependent TRP/TRPL constitutive channel activity in the dark induced by mitochondrial uncouplers, but PLC-independent activation of the channels by linoleic acid was not affected. Furthermore, MßCD suppressed a constitutively active TRP mutant-channel, trpP365, suggesting that TRP channel activity is a target of MßCD action. Importantly, whole-cell voltage-clamp measurements from photoreceptors and simultaneously monitored PIP2-hydrolysis by translocation of fluorescently tagged Tubby protein domain, from the plasma membrane to the cytosol, revealed that MßCD virtually abolished the light response when having little effect on the light-activated PLC. Together, MßCD uncoupled TRP/TRPL channel gating from light-activated PLC and PIP2-hydrolysis suggesting the involvement of distinct nanoscopic lipid domains such as lipid rafts and PIP2 clusters in TRP/TRPL channel gating.


Assuntos
Proteínas de Drosophila , Lipídeos de Membrana , Canais de Potencial de Receptor Transitório , Fosfolipases Tipo C , beta-Ciclodextrinas , Animais , beta-Ciclodextrinas/farmacologia , Drosophila/metabolismo , Proteínas de Drosophila/genética , Proteínas de Drosophila/metabolismo , Lipídeos de Membrana/metabolismo , Células Fotorreceptoras de Invertebrados/efeitos dos fármacos , Células Fotorreceptoras de Invertebrados/metabolismo , Esteróis/metabolismo , Canais de Potencial de Receptor Transitório/efeitos dos fármacos , Canais de Potencial de Receptor Transitório/genética , Canais de Potencial de Receptor Transitório/metabolismo , Fosfolipases Tipo C/metabolismo , Transdução de Sinal Luminoso/efeitos dos fármacos
8.
BMC Biol ; 21(1): 291, 2023 12 18.
Artigo em Inglês | MEDLINE | ID: mdl-38110917

RESUMO

BACKGROUND: Rhabdomeric photoreceptors of eyes in the terrestrial slug Limax are the typical invertebrate-type but unique in that three visual opsins (Gq-coupled rhodopsin, xenopsin, Opn5A) and one retinochrome, all belonging to different groups, are co-expressed. However, molecular properties including spectral sensitivity and G protein selectivity of any of them are not determined, which prevents us from understanding an advantage of multiplicity of opsin properties in a single rhabdomeric photoreceptor. To gain insight into the functional role of the co-expression of multiple opsin species in a photoreceptor, we investigated the molecular properties of the visual opsins in the present study. RESULTS: First, we found that the fourth member of visual opsins, Opn5B, is also co-expressed in the rhabdomere of the photoreceptor together with previously identified three opsins. The photoreceptors were also demonstrated to express Gq and Go alpha subunits. We then determined the spectral sensitivity of the four visual opsins using biochemical and spectroscopic methods. Gq-coupled rhodopsin and xenopsin exhibit maximum sensitivity at ~ 456 and 475 nm, respectively, and Opn5A and Opn5B exhibit maximum sensitivity at ~ 500 and 470 nm, respectively, with significant UV sensitivity. Notably, in vitro experiments revealed that Go alpha was activated by all four visual opsins, in contrast to the specific activation of Gq alpha by Gq-coupled rhodopsin, suggesting that the eye photoreceptor of Limax uses complex G protein signaling pathways. CONCLUSIONS: The eye photoreceptor in Limax expresses as many as four different visual opsin species belonging to three distinct classes. The combination of opsins with different spectral sensitivities and G protein selectivities may underlie physiological properties of the ocular photoreception, such as a shift in spectral sensitivity between dark- and light-adapted states. This may be allowed by adjustment of the relative contribution of the four opsins without neural networks, enabling a simple strategy for fine-tuning of vision.


Assuntos
Opsinas , Células Fotorreceptoras de Invertebrados , Animais , Opsinas/genética , Opsinas/análise , Células Fotorreceptoras de Invertebrados/fisiologia , Rodopsina/genética , Moluscos , Proteínas de Ligação ao GTP/análise , Proteínas de Ligação ao GTP/metabolismo
9.
Nature ; 623(7987): 562-570, 2023 Nov.
Artigo em Inglês | MEDLINE | ID: mdl-37880372

RESUMO

Vision enables both image-forming perception, driven by a contrast-based pathway, and unconscious non-image-forming circadian photoentrainment, driven by an irradiance-based pathway1,2. Although two distinct photoreceptor populations are specialized for each visual task3-6, image-forming photoreceptors can additionally contribute to photoentrainment of the circadian clock in different species7-15. However, it is unknown how the image-forming photoreceptor pathway can functionally implement the segregation of irradiance signals required for circadian photoentrainment from contrast signals required for image perception. Here we report that the Drosophila R8 photoreceptor separates image-forming and irradiance signals by co-transmitting two neurotransmitters, histamine and acetylcholine. This segregation is further established postsynaptically by histamine-receptor-expressing unicolumnar retinotopic neurons and acetylcholine-receptor-expressing multicolumnar integration neurons. The acetylcholine transmission from R8 photoreceptors is sustained by an autocrine negative feedback of the cotransmitted histamine during the light phase of light-dark cycles. At the behavioural level, elimination of histamine and acetylcholine transmission impairs R8-driven motion detection and circadian photoentrainment, respectively. Thus, a single type of photoreceptor can achieve the dichotomy of visual perception and circadian photoentrainment as early as the first visual synapses, revealing a simple yet robust mechanism to segregate and translate distinct sensory features into different animal behaviours.


Assuntos
Ritmo Circadiano , Drosophila melanogaster , Células Fotorreceptoras de Invertebrados , Percepção Visual , Animais , Acetilcolina/metabolismo , Relógios Biológicos/fisiologia , Relógios Biológicos/efeitos da radiação , Ritmo Circadiano/fisiologia , Ritmo Circadiano/efeitos da radiação , Drosophila melanogaster/citologia , Drosophila melanogaster/fisiologia , Drosophila melanogaster/efeitos da radiação , Retroalimentação Fisiológica , Histamina/metabolismo , Neurotransmissores/metabolismo , Células Fotorreceptoras de Invertebrados/metabolismo , Células Fotorreceptoras de Invertebrados/efeitos da radiação , Receptores Colinérgicos/metabolismo , Receptores Histamínicos/metabolismo , Percepção Visual/fisiologia , Percepção Visual/efeitos da radiação
10.
Int J Mol Sci ; 24(14)2023 Jul 15.
Artigo em Inglês | MEDLINE | ID: mdl-37511262

RESUMO

Establishing apicobasal polarity, involving intricate interactions among polarity regulators, is key for epithelial cell function. Though phosphatase of regenerating liver (PRL) proteins are implicated in diverse biological processes, including cancer, their developmental role remains unclear. In this study, we explore the role of Drosophila PRL (dPRL) in photoreceptor cell development. We reveal that dPRL, requiring a C-terminal prenylation motif, is highly enriched in the apical membrane of developing photoreceptor cells. Moreover, dPRL knockdown during retinal development results in adult Drosophila retinal degeneration, caused by hid-induced apoptosis. dPRL depletion also mislocalizes cell adhesion and polarity proteins like Armadillo, Crumbs, and DaPKC and relocates the basolateral protein, alpha subunit of Na+/K+-ATPase, to the presumed apical membrane. Importantly, this polarity disruption is not secondary to apoptosis, as suppressing hid expression does not rescue the polarity defect in dPRL-depleted photoreceptor cells. These findings underscore dPRL's crucial role in photoreceptor cell polarity and emphasize PRL's importance in establishing epithelial polarity and maintaining cell survival during retinal development, offering new insights into PRL's role in normal epithelium.


Assuntos
Proteínas de Drosophila , Drosophila , Animais , Drosophila/metabolismo , Proteínas de Drosophila/metabolismo , Monoéster Fosfórico Hidrolases/metabolismo , Células Fotorreceptoras de Invertebrados/metabolismo , Fígado/metabolismo , Polaridade Celular/genética
11.
J Biol Chem ; 299(6): 104822, 2023 06.
Artigo em Inglês | MEDLINE | ID: mdl-37201584

RESUMO

Pkc53E is the second conventional protein kinase C (PKC) gene expressed in Drosophila photoreceptors; it encodes at least six transcripts generating four distinct protein isoforms including Pkc53E-B whose mRNA is preferentially expressed in photoreceptors. By characterizing transgenic lines expressing Pkc53E-B-GFP, we show Pkc53E-B is localized in the cytosol and rhabdomeres of photoreceptors, and the rhabdomeric localization appears dependent on the diurnal rhythm. A loss of function of pkc53E-B leads to light-dependent retinal degeneration. Interestingly, the knockdown of pkc53E also impacted the actin cytoskeleton of rhabdomeres in a light-independent manner. Here the Actin-GFP reporter is mislocalized and accumulated at the base of the rhabdomere, suggesting that Pkc53E regulates depolymerization of the actin microfilament. We explored the light-dependent regulation of Pkc53E and demonstrated that activation of Pkc53 E can be independent of the phospholipase C PLCß4/NorpA as degeneration of norpAP24 photoreceptors was enhanced by a reduced Pkc53E activity. We further show that the activation of Pkc53E may involve the activation of Plc21C by Gqα. Taken together, Pkc53E-B appears to exert both constitutive and light-regulated activity to promote the maintenance of photoreceptors possibly by regulating the actin cytoskeleton.


Assuntos
Proteínas de Drosophila , Drosophila melanogaster , Proteína Quinase C , Animais , Citoesqueleto de Actina/metabolismo , Drosophila melanogaster/metabolismo , Proteínas de Drosophila/genética , Proteínas de Drosophila/metabolismo , Fosfolipases/metabolismo , Células Fotorreceptoras de Invertebrados/metabolismo , Proteína Quinase C/genética , Proteína Quinase C/metabolismo
12.
J Exp Biol ; 226(10)2023 05 15.
Artigo em Inglês | MEDLINE | ID: mdl-37078618

RESUMO

Larval stomatopods have generally been described as having a typical larval crustacean compound eye, which lacks the visual pigment diversity and morphological specializations of the well-studied stomatopod adult eye. However, recent work has suggested that larval stomatopod eyes are more complex than previously described. In this study, we provide physiological and behavioral evidence of at least three distinct photoreceptor classes in three species of larval stomatopods: Gonodactylellus n. sp., Gonodactylaceus falcatus and Pullosquilla n. sp. First, electroretinogram recordings were used to measure the spectral sensitivity of each species. Evidence for at least three spectral classes were identified in each: an ultraviolet, peaking at 340-376 nm; a short-wavelength blue, peaking at 455-464 nm; and a long-wavelength orange, peaking at 576-602 nm. Next, the behavioral response to light was investigated. We found that each species demonstrated positive phototactic responses to monochromatic stimuli across the UV-visible spectrum. In wavelength preference trials, distinct preferences among species were identified when different colored light stimuli were presented simultaneously. All species displayed a strong response to the UV stimulus, as well as responses to blue and orange stimuli, although at different response strengths, but no response to green. The results of this study demonstrate that larval stomatopods not only have multiple physiologically active spectral classes but they also display clear and distinct responses to wavelengths across the spectrum. We propose that the spectral classes demonstrated in each are related to visually guided ecological tasks of the larvae, which may differ between species.


Assuntos
Olho , Células Fotorreceptoras de Invertebrados , Animais , Células Fotorreceptoras de Invertebrados/fisiologia , Larva/anatomia & histologia , Olho/anatomia & histologia , Crustáceos/fisiologia
13.
J Exp Biol ; 226(7)2023 04 01.
Artigo em Inglês | MEDLINE | ID: mdl-36967715

RESUMO

The Australian lycaenid butterfly Jalmenus evagoras has iridescent wings that are sexually dimorphic, spectrally and in their degree of polarization, suggesting that these properties are likely to be important in mate recognition. We first describe the results of a field experiment showing that free-flying individuals of J. evagoras discriminate between visual stimuli that vary in polarization content in blue wavelengths but not in others. We then present detailed reflectance spectrophotometry measurements of the polarization content of male and female wings, showing that female wings exhibit blue-shifted reflectance, with a lower degree of polarization relative to male wings. Finally, we describe a novel method for measuring alignment of ommatidial arrays: by measuring variation of depolarized eyeshine intensity from patches of ommatidia as a function of eye rotation, we show that (a) individual rhabdoms contain mutually perpendicular microvilli; (b) many rhabdoms in the array have their microvilli misaligned with respect to neighboring rhabdoms by as much as 45 deg; and (c) the misaligned ommatidia are useful for robust polarization detection. By mapping the distribution of the ommatidial misalignments in eye patches of J. evagoras, we show that males and females exhibit differences in the extent to which ommatidia are aligned. Both the number of misaligned ommatidia suitable for robust polarization detection and the number of aligned ommatidia suitable for edge detection vary with respect to both sex and eye patch elevation. Thus, J. evagoras exhibits finely tuned ommatidial arrays suitable for perception of polarized signals, likely to match sex-specific life history differences in the utility of polarized signals.


Assuntos
Borboletas , Animais , Masculino , Feminino , Humanos , Austrália , Visão Ocular , Células Fotorreceptoras de Invertebrados
14.
Science ; 379(6633): 695-700, 2023 02 17.
Artigo em Inglês | MEDLINE | ID: mdl-36795838

RESUMO

Many oceanic prey animals use transparent bodies to avoid detection. However, conspicuous eye pigments, required for vision, compromise the organisms' ability to remain unseen. We report the discovery of a reflector overlying the eye pigments in larval decapod crustaceans and show how it is tuned to render the organisms inconspicuous against the background. The ultracompact reflector is constructed from a photonic glass of crystalline isoxanthopterin nanospheres. The nanospheres' size and ordering are modulated to tune the reflectance from deep blue to yellow, enabling concealment in different habitats. The reflector may also function to enhance the acuity or sensitivity of the minute eyes by acting as an optical screen between photoreceptors. This multifunctional reflector offers inspiration for constructing tunable artificial photonic materials from biocompatible organic molecules.


Assuntos
Mimetismo Biológico , Crustáceos , Células Fotorreceptoras de Invertebrados , Visão Ocular , Animais , Crustáceos/fisiologia , Olho/ultraestrutura , Fótons , Mimetismo Biológico/fisiologia , Células Fotorreceptoras de Invertebrados/fisiologia
15.
Proc Natl Acad Sci U S A ; 120(8): e2218948120, 2023 02 21.
Artigo em Inglês | MEDLINE | ID: mdl-36780532

RESUMO

Organisms from cyanobacteria to humans have evolved a wide array of photoreceptive strategies to detect light. Sunlight avoidance behavior is common in animals without vision or known photosensory genes. While indirect light perception via photothermal conversion is a possible scenario, there is no experimental evidence for this hypothesis. Here, we show a nonvisual and extraocular sunlight detection mechanism by identifying the broad-range thermal receptor 1 (BRTNaC1, temperature range = 33 to 48 °C) in centipede antennae. BRTNaC1, a heat-activated cation-permeable ion channel, is structurally related to members of the epithelial sodium channel family. At the molecular level, heat activation of BRTNaC1 exhibits strong pH dependence controlled by two protonatable sites. Physiologically, temperature-dependent activation of BRTNaC1 upon sunlight exposure comes from a striking photothermal effect on the antennae, where a slightly acidic environment (pH 6.1) of the body fluid leads to the protonation of BRTNaC1 and switches on its high thermal sensitivity. Furthermore, testosterone potently inhibits heat activation of BRTNaC1 and the sunlight avoidance behavior of centipedes. Taken together, our study suggests a sophisticated strategy for nonvisual sunlight detection in myriapods.


Assuntos
Artrópodes , Canais Epiteliais de Sódio , Células Fotorreceptoras de Invertebrados , Luz Solar , Animais , Humanos , Artrópodes/genética , Canais Epiteliais de Sódio/genética , Temperatura Alta , Temperatura , Células Fotorreceptoras de Invertebrados/fisiologia
16.
Commun Biol ; 5(1): 1370, 2022 12 14.
Artigo em Inglês | MEDLINE | ID: mdl-36517671

RESUMO

The adult Drosophila eye is a powerful model system for phototransduction and neurodegeneration research. However, single cell resolution transcriptomic data are lacking for this tissue. We present single cell RNA-seq data on 1-day male and female, 3-day and 7-day old male adult eyes, covering early to mature adult eyes. All major cell types, including photoreceptors, cone and pigment cells in the adult eye were captured and identified. Our data sets identified novel cell type specific marker genes, some of which were validated in vivo. R7 and R8 photoreceptors form clusters that reflect their specific Rhodopsin expression and the specific Rhodopsin expression by each R7 and R8 cluster is the major determinant to their clustering. The transcriptomic data presented in this report will facilitate a deeper mechanistic understanding of the adult fly eye as a model system.


Assuntos
Proteínas de Drosophila , Drosophila , Feminino , Masculino , Animais , Drosophila/metabolismo , Células Fotorreceptoras de Invertebrados , Rodopsina/genética , Rodopsina/metabolismo , Proteínas de Drosophila/metabolismo , Análise de Sequência de RNA
17.
J Cell Sci ; 135(24)2022 12 15.
Artigo em Inglês | MEDLINE | ID: mdl-36444566

RESUMO

Polarized transport is essential for constructing multiple plasma membrane domains in the cell. Drosophila photoreceptors are an excellent model system to study the mechanisms of polarized transport. Rab11 is the key factor regulating the post-Golgi transport of rhodopsin 1 (Rh1; also known as NinaE), a photoreceptive protein, to the rhabdomere, a photoreceptive plasma membrane. Here, we found that neuronal Synaptobrevin (nSyb) colocalizes with Rab11 on the trans-side of Golgi stacks and post-Golgi vesicles at the rhabdomere base, and nSyb deficiency impairs rhabdomeric transport and induces accumulation of Rh1 and vesicles in the cytoplasm; this is similar to the effects of Rab11 loss. These results indicate that nSyb acts as a post-Golgi SNARE toward rhabdomeres. Surprisingly, in Rab11-, Rip11- and nSyb-deficient photoreceptors, illumination enhances cytoplasmic accumulation of Rh1, which colocalizes with Rab11, Rabenosyn5, nSyb and Arrestin 1 (Arr1). Arr1 loss, but not Rab5 dominant negative (Rab5DN) protein expression, inhibits the light-enhanced cytoplasmic Rh1 accumulation. Rab5DN inhibits the generation of Rh1-containing multivesicular bodies rather than Rh1 internalization. Overall, these results indicate that exocytic Rh1 mingles with endocytosed Rh1 and is then transported together to rhabdomeres.


Assuntos
Proteínas de Drosophila , Drosophila , Animais , Drosophila/metabolismo , Rodopsina/metabolismo , Células Fotorreceptoras de Invertebrados/metabolismo , Proteínas de Drosophila/metabolismo , Proteínas R-SNARE/metabolismo , Proteínas rab5 de Ligação ao GTP/metabolismo , Drosophila melanogaster/metabolismo
18.
Artigo em Inglês | MEDLINE | ID: mdl-36224473

RESUMO

Photoreceptors with different spectral sensitivities serve different physiological and behavioral roles. We hypothesized that such functional evolutionary optimization could also include differences in phototransduction dynamics. We recorded elementary responses to light, quantum bumps (QBs), of broadband green-sensitive and ultraviolet (UV)-sensitive photoreceptors in the cockroach, Periplaneta americana, compound eyes using intracellular recordings. In addition to control photoreceptors, we used photoreceptors from cockroaches whose green opsin 1 (GO1) or UV opsin expression was suppressed by RNA interference. In the control broadband and UV-sensitive photoreceptors average input resistances were similar, but the membrane capacitance, a proxy for membrane area, was smaller in the broadband photoreceptors. QBs recorded in the broadband photoreceptors had comparatively short latencies, high amplitudes and short durations. Absolute sensitivities of both opsin knockdown photoreceptors were significantly lower than in wild type, and, unexpectedly, their latency was significantly longer while the amplitudes were not changed. Morphologic examination of GO1 knockdown photoreceptors did not find significant differences in rhabdom size compared to wild type. Our results differ from previous findings in Drosophila melanogaster rhodopsin mutants characterized by progressive rhabdomere degeneration, where QB amplitudes were larger but phototransduction latency was not changed compared to wild type.


Assuntos
Baratas , Periplaneta , Animais , Periplaneta/fisiologia , Opsinas/genética , Opsinas/metabolismo , Células Fotorreceptoras de Invertebrados/fisiologia , Drosophila melanogaster/metabolismo , Transdução de Sinal Luminoso
19.
G3 (Bethesda) ; 12(11)2022 11 04.
Artigo em Inglês | MEDLINE | ID: mdl-36218412

RESUMO

Drosophila rhabdomeric terminal photoreceptor differentiation is an extended process taking several days to complete. Following ommatidial patterning by the morphogenetic furrow, photoreceptors are sequentially recruited and specified, and terminal differentiation begins. Key events of terminal differentiation include the establishment of apical and basolateral domains, rhabdomere and stalk formation, inter-rhabdomeral space formation, and expression of phototransduction machinery. While many key regulators of these processes have been identified, the complete network of transcription factors to downstream effector molecules necessary for regulating each of these major events remains incomplete. Here, we report an RNAi screen to identify additional molecules and cellular pathways required for photoreceptor terminal differentiation. First, we tested several eye-specific GAL4 drivers for correct spatial and temporal specificity and identified Pph13-GAL4 as the most appropriate GAL4 line for our screen. We screened lines available through the Transgenic RNAi Project and isolated lines that when combined with Pph13-GAL4 resulted in the loss of the deep pseudopupil, as a readout for abnormal differentiation. In the end, we screened 6,189 lines, representing 3,971 genes, and have identified 64 genes, illuminating potential new regulatory molecules and cellular pathways for the differentiation and organization of Drosophila rhabdomeric photoreceptors.


Assuntos
Proteínas de Drosophila , Drosophila , Animais , Drosophila/genética , Células Fotorreceptoras de Invertebrados , Proteínas de Drosophila/metabolismo , Drosophila melanogaster/metabolismo , Interferência de RNA , Diferenciação Celular/genética
20.
Sci Signal ; 15(755): eabl6179, 2022 10 11.
Artigo em Inglês | MEDLINE | ID: mdl-36219683

RESUMO

Drosophila phototransduction is a model for signaling cascades that culminate in the activation of transient receptor potential (TRP) cation channels. TRP and TRPL are the canonical TRP (TRPC) channels that are regulated by light stimulation of rhodopsin and engagement of Gαq and phospholipase Cß (PLC). Lipid metabolite(s) generated downstream of PLC are essential for the activation of the TRPC channels in photoreceptor cells. We sought to identify the key lipids produced subsequent to PLC stimulation that contribute to channel activation. Here, using genetics, lipid analysis, and Ca2+ imaging, we found that light increased the amount of an abundant endocannabinoid, 2-linoleoyl glycerol (2-LG), in vivo. The increase in 2-LG amounts depended on the PLC and diacylglycerol lipase encoded by norpA and inaE, respectively. This endocannabinoid facilitated TRPC-dependent Ca2+ influx in a heterologous expression system and in dissociated ommatidia from compound eyes. Moreover, 2-LG and mechanical stimulation cooperatively activated TRPC channels in ommatidia. We propose that 2-LG is a physiologically relevant endocannabinoid that activates TRPC channels in photoreceptor cells.


Assuntos
Proteínas de Drosophila , Canais de Potencial de Receptor Transitório , Animais , Cátions/metabolismo , Drosophila/fisiologia , Proteínas de Drosophila/genética , Proteínas de Drosophila/metabolismo , Endocanabinoides/metabolismo , Endocanabinoides/farmacologia , Glicerol/metabolismo , Luz , Lipase Lipoproteica/genética , Lipase Lipoproteica/metabolismo , Fosfolipases/metabolismo , Células Fotorreceptoras de Invertebrados/metabolismo , Rodopsina/metabolismo , Canais de Cátion TRPC/genética , Canais de Cátion TRPC/metabolismo , Canais de Potencial de Receptor Transitório/genética , Canais de Potencial de Receptor Transitório/metabolismo
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