Distinct roles of light-activated channels TRP and TRPL in photoreceptors of <i>Periplaneta americana</i>

Saari, Paulus; French, Andrew S.; Torkkeli, Päivi H.; Liu, Hongxia; Immonen, Esa‐Ville; Frolov, Roman V.

doi:10.1085/jgp.201611737

Cited by 13 publications

(25 citation statements)

References 31 publications

(80 reference statements)

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“…Although decreased quantum efficiency is consistent with our findings of the relatively low absolute sensitivities in both knockdowns, and also with the previous findings in D. melanogaster (Hardie et al 2002), this effect cannot be separated from the loss of absolute sensitivity associated with what we consider the non-specific changes in the photoreceptor, especially with the reduced C m [the relations between absolute sensitivity and C m are discussed at length in Frolov et al (2018)]. These presumably compensatory changes are similar to those documented previously in other cockroach retinal protein knockdown experiments Saari et al 2017). Interestingly, increased ionic permeability of photoreceptor membrane at rest was also described in ion channel mutants in D. melanogaster (Vähäsöyrinki et al 2006), suggesting the presence of intrinsic mechanisms that upregulate leak conductance(s) to substitute for a missing ion channel.…”

Section: Discussionsupporting

confidence: 87%

“…Similar to the previous studies involving RNAi of important photoreceptor proteins Saari et al 2017), we found changes in the photoreceptors of Gq and PLC knockdowns, which could not be directly linked to altered gene expression. We, therefore, refer to such changes as non-specific compensations.…”

Section: Changes In Membrane Resistance Capacitance and Absolute Sensupporting

confidence: 88%

“…However, the relative mRNA expression levels were very low. Previously, knockdown of P. americana TRPL channels using similar methods as described here, dramatically reduced the quantum bump amplitudes within 7-20 days after injection Saari et al 2017). Second, the large changes of membrane capacitance and absolute sensitivity in the knockdown photoreceptors suggest extensive remodelling of the rhabdomeres.…”

Section: Discussionsupporting

confidence: 50%

“…First, ionic permeability of the microvillar membrane was altered to reflect the predominant expression of TRPL channels in the P. americana retina (Immonen et al 2014;Saari et al 2017). These channels are less selective for Ca 2+ than TRP channels.…”

Section: Modifications To the Modelmentioning

confidence: 99%

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Suppression of Gq and PLC gene expression has a small effect on quantum bumps in vivo in Periplaneta americana

et al. 2020

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Visual signal transmission by Drosophila melanogaster photoreceptors is mediated by a Gq protein that activates a phospholipase C (PLC). Mutations and deficiencies in expression of either of these proteins cause severe defects in phototransduction.Here we investigated whether these proteins are also involved in the cockroach, Periplaneta americana, phototransduction by silencing Gq α-subunit (Gqα) and phosphoinositide-specific phospholipase C (PLC) by RNA interference and observing responses to single photons (quantum bumps, QB). We found (1) non-specific decreases in membrane resistance, membrane capacitance and absolute sensitivity in the photoreceptors of both Gqα and PLC knockdowns, and (2) small changes in QB statistics. Despite significant decreases in expressions of Gq and PLC mRNA, the changes in QB properties were surprisingly modest, with mean latencies increasing by ~ 10%, and without significant decrease in their amplitudes. To better understand our results, we used a mathematical model of the phototransduction cascade. By modifying the Gq and PLC abundances, and diffusion rates for Gq, we found that QB latencies and amplitudes deteriorated noticeably only after large decreases in the protein levels, especially when Gq diffusion was slow. Also, reduction in Gq but not PLC lowered quantum efficiency. These results suggest that expression of the proteins may be redundant.

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Section: Discussionsupporting

confidence: 87%

Section: Changes In Membrane Resistance Capacitance and Absolute Sensupporting

confidence: 88%

Section: Discussionsupporting

confidence: 50%

Section: Modifications To the Modelmentioning

confidence: 99%

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Suppression of Gq and PLC gene expression has a small effect on quantum bumps in vivo in Periplaneta americana

et al. 2020

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“…In vivo intracellular single-electrode recordings were performed as described previously (Saari et al 2017).…”

Section: Intracellular Recordingsmentioning

confidence: 99%

Changes in electrophysiological properties of photoreceptors in Periplaneta americana associated with the loss of screening pigment

et al. 2018

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Absence of screening pigment in insect compound eyes has been linked to visual dysfunction. We investigated how its loss in a white-eyed mutant (W-E) alters the photoreceptor electrophysiological properties, opsin gene expression and the behavior of the cockroach, Periplaneta americana. Whole-cell patch-clamp recordings of green-sensitive photoreceptors in WE cockroaches gave reduced membrane capacitance, absolute sensitivity to light and light-induced currents. Decreased low-pass filtering increased voltage bump amplitudes in WE photoreceptors. Intracellular recordings showed that angular sensitivity of WE photoreceptors had two distinct components: a large narrow component with the same acceptance angle as wild-type, plus a relatively small wide component. Information processing was evaluated using Gaussian white-noise modulated light stimulation. In bright light, WE photoreceptors demonstrated higher signal gain and signal power than wild-type photoreceptors. Expression levels of the primary UV-and green-sensitive opsins were lower and of the secondary green-sensitive opsin significantly higher in WE than in wild-type retinae. In behaviour experiments, WE cockroaches were significantly less active in dim green light, consistent with the relatively low light sensitivity of their photoreceptors. Overall, these differences can be related to the loss of screening pigment function and to a compensatory decrease in the rhabdomere size in WE retinae.

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Behavioral responses to visual overstimulation in the cockroach Periplaneta americana L.

et al. 2017

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In the visual systems of insects, different types of photoreceptors contribute to specialized visual channels that mediate distinct functions and behaviors. Large compound eyes of Periplaneta americana contain photoreceptors of two spectral classes, broadband green-sensitive photoreceptors and narrow-band UV-sensitive photoreceptors. Here, we investigated how visual stimulation by UV and green light affects locomotor, resting, and grooming behaviors in P. americana under conditions when light avoidance is not possible. We show that green but not UV light stimulates locomotor activity, inducing paradoxical positive masking. Duration of resting and grooming decreased with increasing light intensity, consistent with development of behavioral stress in response to visual overstimulation. A reaction of full immobility is described under UV light and at higher intensities of green light, with relative periods of immobility and grooming strongly negatively correlated. Low-intensity UV was more effective than low-intensity green light in suppressing grooming and inducing immobility. Our results suggest that locomotor activity in P. americana is mainly regulated by green-sensitive photoreceptors, and that dim UV light can trigger behavioral immobility, whereas both wavelengths induce stress-like reactions at high intensities. Considering the intrinsic UV sensitivity of green-sensitive photoreceptors, the contrasting behavioral responses indicate antagonistic interactions between UV and green visual channels.

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Distinct roles of light-activated channels TRP and TRPL in photoreceptors of Periplaneta americana

Cited by 13 publications

References 31 publications

Suppression of Gq and PLC gene expression has a small effect on quantum bumps in vivo in Periplaneta americana

Suppression of Gq and PLC gene expression has a small effect on quantum bumps in vivo in Periplaneta americana

Changes in electrophysiological properties of photoreceptors in Periplaneta americana associated with the loss of screening pigment

Behavioral responses to visual overstimulation in the cockroach Periplaneta americana L.

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