TRPA1 is selected as a semi-conserved channel during vertebrate evolution due to its involvement in spermatogenesis

Saha, S. K.; Sucharita, Samikshya; Majhi, Rakesh Kumar; Tiwari, Ajay; Ghosh, Arijit; Pradhan, Sunil Kumar; Patra, Bijay Kumar; Dash, Rashmi; Nayak, Rabi Narayan; Giri, Sunil; Routray, P.; Kumar, Abhishek; Kumar, Pratap; Goswami, Chandan

doi:10.1016/j.bbrc.2019.02.121

Cited by 12 publications

(10 citation statements)

References 25 publications

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“…Generally, TRPA1 has higher sequence divergence across vertebrates compared with other TRP genes, particularly in the extracellular loops ( Saha et al 2019 ). It has been hypothesized that these extracellular regions have diverged to adapt to each specific environment ( Saha et al 2019 ). However, we found only one extracellular site under significant diversifying selection in cryonotothenioids.…”

Section: Discussionmentioning

confidence: 99%

Evolution of Transient Receptor Potential (TRP) Ion Channels in Antarctic Fishes (Cryonotothenioidea) and Identification of Putative Thermosensors

York

Zakon

2022

Genome Biology and Evolution

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Animals rely on their sensory systems to inform them of ecologically relevant environmental variation. In the Southern Ocean, the thermal environment has remained between -1.9 and 5 °C for 15 million years, yet we have no knowledge of how an Antarctic marine organism might sense their thermal habitat as we have yet to discover a thermosensitive ion channel that gates (opens/closes) below 10 °C. Here, we investigate the evolutionary dynamics of transient receptor potential (TRP) channels, which are the primary thermosensors in animals, within cryonotothenioid fishes—the dominant fish fauna of the Southern Ocean. We found cryonotothenioids have a similar complement of TRP channels as other teleosts (∼28 genes). Previous work has shown that thermosensitive-gating in a given channel is species specific, and multiple channels act together to sense the thermal environment. Therefore, we combined evidence of changes in selective pressure, gene gain/loss dynamics, and the first sensory ganglion transcriptome in this clade to identify the best candidate TRP channels that might have a functional dynamic range relevant for frigid Antarctic temperatures. We concluded that TRPV1a, TRPA1b, and TRPM4 are the likeliest putative thermosensors, and found evidence of diversifying selection at sites across these proteins. We also put forward hypotheses for molecular mechanisms of other cryonotothenioid adaptations, such as reduced skeletal calcium deposition, sensing oxidative stress, and unusual magnesium homeostasis. By completing a comprehensive and unbiased survey of these genes, we lay the groundwork for functional characterization and answering long-standing thermodynamic questions of thermosensitive gating and protein adaptation to low temperatures.

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Section: Discussionmentioning

confidence: 99%

Evolution of Transient Receptor Potential (TRP) Ion Channels in Antarctic Fishes (Cryonotothenioidea) and Identification of Putative Thermosensors

York

Zakon

2022

Genome Biology and Evolution

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“…Hence, it is also involved in respiratory diseases, such as asthma, chronic obstructive pulmonary disease, and chronic cough [47][48][49][50][51][52] . In addition, a recent study showed that TRPA1 is expressed in mature sperms and testes, which is one of the major target tissues of PA esters 53) . Although it is currently unknown whether TRPA1 is also expressed in human sperms, these results suggest that humans may be more susceptible to testicular toxicity caused by PA esters.…”

Section: Discussionmentioning

confidence: 99%

Species-Specific Activation of Transient Receptor Potential Ankyrin 1 by Phthalic Acid Monoesters

Mori

Aoki

Okamoto

et al. 2022

Biological & Pharmaceutical Bulletin

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Phthalic acid (PA) diesters are widely used in consumer products, as plasticizers, and are ubiquitous environmental pollutants. There is a growing concern about their adjuvant effect on allergic diseases. Although its precise mechanism remains unknown, possible involvement of TRPA1 has been suggested. Hence, in this study, the activation of human and mouse TRPA1s by a series of PA di-and monoesters was investigated using a heterologous expression system in vitro.Consequently, it was found that monoesters activated human TRPA1, where EC50 values were in the order of mono-hexyl > mono-heptyl > mono-n-octyl > mono-2-ethylhexyl > mono-isononyl and mono-isodecyl esters. Significant species differences in TRPA1 activation by PA monoesters were also discovered; PA monoesters activated human TRPA1 but not mouse TRPA1 in a concentrationdependent manner up to 50 μM. These findings suggest that PA esters may exert TRPA1-dependent adverse effects on humans, which have never been demonstrated in experimental animals.

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“…In support of this hypothesis, the transcriptome meta-analysis showed that the seabream ejaculated spermatozoa express a high number of VGCCs and VGKCs, as well as other channels that can also transport Ca 2+ or K + ions, such as TRP channels (Trpv1, -4, -6, Trpa1, Trmp4), Na + /Ca 2+ exchangers, CNGK channels, SACs, or MSCs. We have shown that some of these channels are localized in the head and/or the flagellum of the seabream spermatozoon, and their mammalian and piscine orthologs have been shown to play a role in the control of the spermatozoon motility [ 4 , 5 , 20 , 21 , 33 , 44 , 49 , 50 , 51 , 52 , 53 , 54 , 55 ]. The potential role of some of these ion channels in the preservation of post activated sperm motility in seabream is supported by our pharmacological targeting experiments, where inhibitors of L- and T-type Ca 2+ channels (verapamil and mibefradil, respectively), CNG channels (L-cis diltiazem), TRPV channels (capsazepine), SACs (Gd 3+ ), and MSCs (GsMTx-4), as well as of ATP-sensitive K + channels (glybenclamide) and VGKCs (4-aminopyridine), reduced the motility, progressivity, and velocity, of spermatozoa at 30 and/or 60 s post activation.…”

Section: Discussionmentioning

confidence: 99%

Role of Ion Channels in the Maintenance of Sperm Motility and Swimming Behavior in a Marine Teleost

Castro-Arnau

Chauvigné

Cerdà

2022

IJMS

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In oviparous marine fishes, the hyperosmotic induction of sperm motility in seawater (SW) is well established, however, the potential function of ion channels in the maintenance of post activated spermatozoon swimming performance remains largely unknown. Here, we investigated the influence of ion channels on the spermatozoon swimming parameters using the gilthead seabream (Sparus aurata) as a model for modern marine teleosts. Our data show that the SW-induced activation of seabream sperm motility requires three concomitant processes, the hyperosmotic shock, an ion-flux independent increase of the intracellular concentration of Ca2+ ([Ca2+]i), but not of [K+]i or [Na+]i, and the alkalization of the cytosol. The combination of all three processes is obligatory to trigger flagellar beating. However, the time-course monitoring of sperm motion kinetics and changes in the [Ca2+]i, [K+]i and [Na+]i in SW or in non-ionic activation media, showed that the post activated maintenance of spermatozoa motility is dependent on extracellular Ca2+ and K+. A meta-analysis of a seabream sperm transcriptome uncovered the expression of multiple ion channels, some of which were immunolocalized in the head and/or tail of the spermatozoon. Selective pharmacological inhibition of these ion channel families impaired the long-term motility, progressivity, and velocity of SW-activated spermatozoa. The data further revealed that some antagonists of K+-selective or Ca2+-selective channels, as well as of stretch-activated and mechanosensitive channels, altered the trajectory of spermatozoa, suggesting that these ion channels are likely involved in the control of the swimming pattern of the post activated spermatozoon. These combined findings provide new insight into the signaling pathways regulating spermatozoon activation and swimming performance in marine fishes.

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TRPA1 is selected as a semi-conserved channel during vertebrate evolution due to its involvement in spermatogenesis

Cited by 12 publications

References 25 publications

Evolution of Transient Receptor Potential (TRP) Ion Channels in Antarctic Fishes (Cryonotothenioidea) and Identification of Putative Thermosensors

Evolution of Transient Receptor Potential (TRP) Ion Channels in Antarctic Fishes (Cryonotothenioidea) and Identification of Putative Thermosensors

Species-Specific Activation of Transient Receptor Potential Ankyrin 1 by Phthalic Acid Monoesters

Role of Ion Channels in the Maintenance of Sperm Motility and Swimming Behavior in a Marine Teleost

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