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Targeting TRP Channels for Pain, Itch and Inflammation Relief

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Immunology".

Deadline for manuscript submissions: closed (30 August 2023) | Viewed by 24751

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Dr. Arpad Szallasi

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Guest Editor

Department of Pathology and Experimental Cancer Research, Faculty of Medicine, Semmelweis University, Budapest, Hungary
Interests: the capsaicin (vanilloid) receptor TRPV1; “thermoTRP” expression in cancer; TRP channels as oncotargets; TRP channels as tumor suppressors; sensory nerve-tumor interactions; oncothermia
Special Issues, Collections and Topics in MDPI journals

Dr. Ari-Pekka Koivisto

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Research and Development, Orion Corporation Orion Pharma, 20360 Turku, Finland
Interests: TRPA1; TRP ion channels; drug discovery; cardiac electrophysiology; chronic pain; neuropathic and osteoarthritis pain
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Transient Receptor Potential (TRP) channels are multifunctional signaling molecules with important roles in sensory perception and cellular physiology. More than two decades of intensive preclinical and clinical research supports the involvement of TRP channels in pain, itch, and neurogenic inflammation. In fact, a number of potent small molecule TRPA1 and TRPV1 antagonists have already been advanced into clinical trials for the treatment of inflammatory and neuropathic pain. Other TRP channels (e.g. TRPV2, TRPV3, TRPM2, TRPM3, TRPM8 and TRPC4/C5) are also of significant interest.

This Special Issue will review the preclinical promise and therapeutic value of TRP channel modulators aimed both established and emerging targets, along with the challenges that these compounds may face in clinical practice. Experimental and clinical studies with pain, itch and inflammation will be discussed, along with the emerging roles of TRP gene polymorphism and epigenetic regulation in disease risk and altered sensory perception. Critical review articles of old concepts and new thoughts are also welcome for consideration.

Dr. Árpád Szállási
Dr. Ari-Pekka Koivisto
Guest Editors

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Keywords

TRP channels
“thermoTRP” channels
neuropathic pain
inflammatory pain
cancer pain
pruritic skin iseases
itch
neurogenic inflammation
migraine

Published Papers (12 papers)

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Editorial

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4 pages, 174 KiB

Open AccessEditorial

Targeting TRP Channels for Pain, Itch and Neurogenic Inflammation

by Ari-Pekka Koivisto and Arpad Szallasi

Int. J. Mol. Sci. 2024, 25(1), 320; https://doi.org/10.3390/ijms25010320 - 25 Dec 2023

Viewed by 810

Abstract

Transient receptor potential (TRP) channels are multifunctional signaling molecules with important roles in health and disease [...] Full article

(This article belongs to the Special Issue Targeting TRP Channels for Pain, Itch and Inflammation Relief)

Research

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7 pages, 2202 KiB

Open AccessCommunication

Human Osteoarthritic Chondrocytes Express Nineteen Different TRP-Genes—TRPA1 and TRPM8 as Potential Drug Targets

by Leevi Halonen, Antti Pemmari, Elina Nummenmaa, Mari Hämäläinen, Teemu Moilanen, Katriina Vuolteenaho and Eeva Moilanen

Int. J. Mol. Sci. 2023, 24(12), 10057; https://doi.org/10.3390/ijms241210057 - 13 Jun 2023

Cited by 5 | Viewed by 1662

Abstract

Transient receptor potential (TRP) ion channels are expressed in neuronal and some non-neuronal cells and are involved particularly in pain and thermosensation. We previously showed that TRPA1 is functionally expressed in human osteoarthritic (OA) chondrocytes and mediates inflammation, cartilage degradation, and pain in monosodium-iodoacetate-induced experimental OA. In the present study, we explored the expression of TRP-channels in primary human OA chondrocytes and investigated whether drugs used in the treatment of OA, ibuprofen and glucocorticoids, have effects on TRP-channel expression. OA cartilage was obtained from knee replacement surgery and chondrocytes were isolated with enzyme digestion. NGS analysis showed the expression of 19 TRP-genes in OA chondrocytes, with TRPM7, TRPV4, TRPC1, and TRPM8 having the highest counts in unstimulated cells. These results were verified with RT-PCR in samples from a different group of patients. Interleukin-1β (IL-1β) significantly increased TRPA1 expression, while TRPM8 and TRPC1 expression was decreased, and TRPM7 and TRPV4 expression remained unaffected. Furthermore, dexamethasone attenuated the effect of IL-1β on TRPA1 and TRPM8 expression. The TRPM8 and TRPA1 agonist menthol increased the expression of the cartilage-degrading enzymes MMP-1, MMP-3, and MMP-13 and the inflammatory factors iNOS and IL-6 in OA chondrocytes. In conclusion, human OA chondrocytes express 19 different TRP-genes, of which the significant TRPM8 expression is a novel finding. Dexamethasone attenuated IL-1β-induced TRPA1 expression. Interestingly, the TRPM8 and TRPA1 agonist menthol increased MMP expression. These results support the concept of TRPA1 and TRMP8 as potential novel drug targets in arthritis. Full article

(This article belongs to the Special Issue Targeting TRP Channels for Pain, Itch and Inflammation Relief)

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9 pages, 508 KiB

Open AccessArticle

Activation of TRPV1-Expressing Renal Sensory Nerves of Rats with N-Oleoyldopamine Attenuates High-Fat-Diet-Induced Impairment of Renal Function

by Shuang-Quan Yu, Shuangtao Ma and Donna H. Wang

Int. J. Mol. Sci. 2023, 24(7), 6207; https://doi.org/10.3390/ijms24076207 - 25 Mar 2023

Viewed by 1096

Abstract

Enhanced renal sympathetic nerve activity (RSNA) contributes to obesity-induced renal disease, while the role of afferent renal nerve activity (ARNA) is not fully understood. The present study tested the hypothesis that activating the transient receptor potential vanilloid 1 (TRPV1) channel in afferent renal nerves suppresses RSNA and prevents renal dysfunction and hypertension in obese rats. N-oleoyldopamine (OLDA, 1 ng/kg, daily) was administrated intrathecally (T8-L3) via an indwelled catheter to chronically activate, TRPV1-positive afferent renal nerves in rats fed a chow diet or high-fat diet (HFD) for 8 weeks. HFD intake significantly increased the body weight, impaired glucose and insulin tolerance, decreased creatinine clearance, and elevated systolic blood pressure in rats compared with the levels of the chow-fed rats (all p < 0.05). An intrathecal OLDA treatment for 8 weeks did not affect the fasting glucose level, glucose tolerance, and insulin tolerance in rats fed either chow or HFD. As expected, the chronic OLDA treatment significantly increased the levels of plasma calcitonin gene-related peptide and substance P and ARNA in the HFD-fed rats (all p < 0.05). Interestingly, the OLDA treatment decreased the urinary norepinephrine level and RSNA in rats fed HFD (both p < 0.05). Importantly, the OLDA treatment attenuated HFD-induced decreases in creatinine clearance and urinary Na⁺ excretion and increases in the plasma urea level, urinary albumin level, and systolic blood pressure at the end of an 8-week treatment (all p < 0.05). Taken together, the intrathecal administration of OLDA ameliorates the enhancement of RSNA, renal dysfunction, and hypertension in obese rats. These findings shed light on the roles of TRPV1-positive renal afferent nerves in obesity-related renal dysfunction and hypertension. Full article

(This article belongs to the Special Issue Targeting TRP Channels for Pain, Itch and Inflammation Relief)

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15 pages, 1140 KiB

Open AccessArticle

Inhibition of Canonical Transient Receptor Potential Channels 4/5 with Highly Selective and Potent Small-Molecule HC-070 Alleviates Mechanical Hypersensitivity in Rat Models of Visceral and Neuropathic Pain

by Niina Jalava, Janne Kaskinoro, Hugh Chapman, Miguel Morales, Hanna Metsänkylä, Satu-Maarit Heinonen and Ari-Pekka Koivisto

Int. J. Mol. Sci. 2023, 24(4), 3350; https://doi.org/10.3390/ijms24043350 - 8 Feb 2023

Cited by 2 | Viewed by 1953

Abstract

Transient receptor potential channels C4/C5 are widely expressed in the pain pathway. Here, we studied the putative analgesic efficacy of the highly selective and potent TRPC4/C5 antagonist HC-070 in rats. Inhibitory potency on human TRPC4 was assessed by using the whole-cell manual patch-clamp technique. Visceral pain sensitivity was assessed by the colonic distension test after intra-colonic trinitrobenzene sulfonic acid injection and partial restraint stress. Mechanical pain sensitivity was assessed by the paw pressure test in the chronic constriction injury (CCI) neuropathic pain model. We confirm that HC-070 is a low nanomolar antagonist. Following single oral doses (3–30 mg/kg in male or female rats), colonic hypersensitivity was significantly and dose-dependently attenuated, even fully reversed to baseline. HC-070 also had a significant anti-hypersensitivity effect in the established phase of the CCI model. HC-070 did not have an effect on the mechanical withdrawal threshold of the non-injured paw, whereas the reference compound morphine significantly increased it. Analgesic effects are observed at unbound brain concentrations near the 50% inhibitory concentration (IC₅₀) recorded in vitro. This suggests that analgesic effects reported here are brought about by TRPC4/C5 blocking in vivo. The results strengthen the idea that TRPC4/C5 antagonism is a novel, safe non-opioid treatment for chronic pain. Full article

(This article belongs to the Special Issue Targeting TRP Channels for Pain, Itch and Inflammation Relief)

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21 pages, 4007 KiB

Open AccessArticle

Bipartite Activation of Sensory Neurons by a TRPA1 Agonist Allyl Isothiocyanate Is Reflected by Complex Ca²⁺ Influx and CGRP Release Patterns: Enhancement by NGF and Inhibition with VAMP and SNAP-25 Cleaving Botulinum Neurotoxins

by Mariia Belinskaia, Jiafu Wang, Seshu Kumar Kaza, Caren Antoniazzi, Tomas Zurawski, J. Oliver Dolly and Gary W. Lawrence

Int. J. Mol. Sci. 2023, 24(2), 1338; https://doi.org/10.3390/ijms24021338 - 10 Jan 2023

Cited by 1 | Viewed by 1916

Abstract

The trafficking of transient receptor potential (TRP) channels to the plasma membrane and the release of calcitonin gene-related peptide (CGRP) from trigeminal ganglion neurons (TGNs) are implicated in some aspects of chronic migraines. These exocytotic processes are inhibited by cleavage of SNAREs with botulinum neurotoxins (BoNTs); moreover, type A toxin (/A) clinically reduces the frequency and severity of migraine attacks but not in all patients for unknown reasons. Herein, neonatal rat TGNs were stimulated with allyl isothiocyanate (AITC), a TRPA1 agonist, and dose relationships were established to link the resultant exocytosis of CGRP with Ca²⁺ influx. The CGRP release, quantified by ELISA, was best fit by a two-site model (EC₅₀ of 6 and 93 µM) that correlates with elevations in intracellular Ca²⁺ [Ca²⁺]_i revealed by time-lapse confocal microscopy of fluo-4-acetoxymethyl ester (Fluo-4 AM) loaded cells. These signals were all blocked by two TRPA1 antagonists, HC-030031 and A967079. At low [AITC], [Ca²⁺]_i was limited because of desensitisation to the agonist but rose for concentrations > 0.1 mM due to a deduced non-desensitising second phase of Ca²⁺ influx. A recombinant BoNT chimera (/DA), which cleaves VAMP1/2/3, inhibited AITC-elicited CGRP release to a greater extent than SNAP-25-cleaving BoNT/A. /DA also proved more efficacious against CGRP efflux evoked by a TRPV1 agonist, capsaicin. Nerve growth factor (NGF), a pain-inducing sensitiser of TGNs, enhanced the CGRP exocytosis induced by low [AITC] only. Both toxins blocked NGF-induced neuropeptide secretion and its enhancement of the response to AITC. In conclusion, NGF sensitisation of sensory neurons involves TRPA1, elevated Ca²⁺ influx, and CGRP exocytosis, mediated by VAMP1/2/3 and SNAP-25 which can be attenuated by the BoNTs. Full article

(This article belongs to the Special Issue Targeting TRP Channels for Pain, Itch and Inflammation Relief)

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11 pages, 5531 KiB

Open AccessCommunication

Dihydroceramides Derived from Bacteroidetes Species Sensitize TRPV1 Channels

by Nora Ludwig, Isaac S. Demaree, Chiaki Yamada, Amilia Nusbaum, Frank C. Nichols, Fletcher A. White, Alexandru Movila and Alexander G. Obukhov

Int. J. Mol. Sci. 2023, 24(1), 877; https://doi.org/10.3390/ijms24010877 - 3 Jan 2023

Cited by 1 | Viewed by 1684

Abstract

Bacterial colonization of open wounds is common, and patients with infected wounds often report significantly elevated pain sensitivity at the wound site. Transient Receptor Potential Vanilloid Type 1 (TRPV1) channels are known to play an important role in pain signaling and may be sensitized under pro-inflammatory conditions. Bacterial membrane components, such as phosphoethanolamine dihydroceramide (PEDHC), phosphoglycerol dihydroceramide (PGDHC), and lipopolysaccharide (LPS), are released in the environment from the Gram-negative bacteria of the Bacteroidetes species colonizing the infected wounds. Here, we used intracellular calcium imaging and patch-clamp electrophysiology approaches to determine whether bacterially derived PEDHC, PGDHC, or LPS can modulate the activity of the TRPV1 channels heterologously expressed in HEK cells. We found that PEDHC and PGDHC can sensitize TRPV1 in a concentration-dependent manner, whereas LPS treatment does not significantly affect TRPV1 activity in HEK cells. We propose that sensitization of TRPV1 channels by Bacteroidetes-derived dihydroceramides may at least in part underlie the increased pain sensitivity associated with wound infections. Full article

(This article belongs to the Special Issue Targeting TRP Channels for Pain, Itch and Inflammation Relief)

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19 pages, 4340 KiB

Open AccessArticle

Validation of Six Commercial Antibodies for the Detection of Heterologous and Endogenous TRPM8 Ion Channel Expression

by Pablo Hernández-Ortego, Remedios Torres-Montero, Elvira de la Peña, Félix Viana and Jorge Fernández-Trillo

Int. J. Mol. Sci. 2022, 23(24), 16164; https://doi.org/10.3390/ijms232416164 - 18 Dec 2022

Cited by 2 | Viewed by 1760

Abstract

TRPM8 is a non-selective cation channel expressed in primary sensory neurons and other tissues, including the prostate and urothelium. Its participation in different physiological and pathological processes such as thermoregulation, pain, itch, inflammation and cancer has been widely described, making it a promising target for therapeutic approaches. The detection and quantification of TRPM8 seems crucial for advancing the knowledge of the mechanisms underlying its role in these pathophysiological conditions. Antibody-based techniques are commonly used for protein detection and quantification, although their performance with many ion channels, including TRPM8, is suboptimal. Thus, the search for reliable antibodies is of utmost importance. In this study, we characterized the performance of six TRPM8 commercial antibodies in three immunodetection techniques: Western blot, immunocytochemistry and immunohistochemistry. Different outcomes were obtained for the tested antibodies; two of them proved to be successful in detecting TRPM8 in the three approaches while, in the conditions tested, the other four were acceptable only for specific techniques. Considering our results, we offer some insight into the usefulness of these antibodies for the detection of TRPM8 depending on the methodology of choice. Full article

(This article belongs to the Special Issue Targeting TRP Channels for Pain, Itch and Inflammation Relief)

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10 pages, 1806 KiB

Open AccessArticle

Changes in TRPV1 Expression as Well as Substance P and Vasoactive Intestinal Peptide Levels Are Associated with Recurrence of Pterygium

by Hatice Deniz İlhan, Betül Ünal, Yusuf Ayaz and Nuray Erin

Int. J. Mol. Sci. 2022, 23(24), 15692; https://doi.org/10.3390/ijms232415692 - 10 Dec 2022

Cited by 2 | Viewed by 1261

Abstract

Pterygium, a disease of the ocular surface, is characterized by the proliferation and invasion of fibrovascular tissue. Chronic inflammation contributes to pterygium occurrence. Sensory neuropeptides of TRPV1-positive nerve fibers are involved in inflammation and corneal wound healing. The possible association between TRPV1 in nerve fibers and neuropeptides such as Substance P (SP) and Vasoactive Intestinal Peptide (VIP) in the recurrence of pterygium has not been examined before. The pterygia from 64 patients were used to determine changes in SP and VIP levels using 10 min acetic-acid extraction that yielded mainly neuronal peptides. There was a sufficient amount of pterygium tissues from the 35 patients for further immunohistochemical analysis of TRPV1 and S100, which is a glial marker to visualize nerve fibers. SP and VIP levels increased markedly in cases with primary and secondary recurrences, and there was a close correlation between SP and VIP levels. TRPV1 expression increased in the epithelium, while stromal expression decreased in recurrences. Nerve fibers were demonstrated mainly in the stroma, and serial sections confirmed the localization of TRPV1 with the nerve fibers. These results together with previous findings demonstrated that the increased epithelial expression of TRPV1 in recurrent pterygia might be involved in the pathogenesis, and the inhibition of epithelial TRPV1 activity may prevent recurrence. Full article

(This article belongs to the Special Issue Targeting TRP Channels for Pain, Itch and Inflammation Relief)

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Review

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14 pages, 706 KiB

Open AccessReview

Targeting Nociceptive Neurons and Transient Receptor Potential Channels for the Treatment of Migraine

by Cinder Faith Cohen, Jueun Roh, Sang Hoon Lee, Chul-Kyu Park and Temugin Berta

Int. J. Mol. Sci. 2023, 24(9), 7897; https://doi.org/10.3390/ijms24097897 - 26 Apr 2023

Cited by 2 | Viewed by 3271

Abstract

Migraine is a neurovascular disorder that affects approximately 12% of the global population. While its exact causes are still being studied, researchers believe that nociceptive neurons in the trigeminal ganglia play a key role in the pain signals of migraine. These nociceptive neurons innervate the intracranial meninges and convey pain signals from the meninges to the thalamus. Targeting nociceptive neurons is considered promising due to their accessibility and distinct molecular profile, which includes the expression of several transient receptor potential (TRP) channels. These channels have been linked to various pain conditions, including migraine. This review discusses the role and mechanisms of nociceptive neurons in migraine, the challenges of current anti-migraine drugs, and the evidence for well-studied and emerging TRP channels, particularly TRPC4, as novel targets for migraine prevention and treatment. Full article

(This article belongs to the Special Issue Targeting TRP Channels for Pain, Itch and Inflammation Relief)

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24 pages, 3201 KiB

Open AccessReview

TRP Channels: Recent Development in Translational Research and Potential Therapeutic Targets in Migraine

by Eleonóra Spekker, Tamás Körtési and László Vécsei

Int. J. Mol. Sci. 2023, 24(1), 700; https://doi.org/10.3390/ijms24010700 - 31 Dec 2022

Cited by 7 | Viewed by 2758

Abstract

Migraine is a chronic neurological disorder that affects approximately 12% of the population. The cause of migraine headaches is not yet known, however, when the trigeminal system is activated, neuropeptides such as calcitonin gene-related peptide (CGRP) and substance P (SP) are released, which cause neurogenic inflammation and sensitization. Advances in the understanding of migraine pathophysiology have identified new potential pharmacological targets. In recent years, transient receptor potential (TRP) channels have been the focus of attention in the pathophysiology of various pain disorders, including primary headaches. Genetic and pharmacological data suggest the role of TRP channels in pain sensation and the activation and sensitization of dural afferents. In addition, TRP channels are widely expressed in the trigeminal system and brain regions which are associated with the pathophysiology of migraine and furthermore, co-localize several neuropeptides that are implicated in the development of migraine attacks. Moreover, there are several migraine trigger agents known to activate TRP channels. Based on these, TRP channels have an essential role in migraine pain and associated symptoms, such as hyperalgesia and allodynia. In this review, we discuss the role of the certain TRP channels in migraine pathophysiology and their therapeutic applicability. Full article

(This article belongs to the Special Issue Targeting TRP Channels for Pain, Itch and Inflammation Relief)

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11 pages, 706 KiB

Open AccessReview

Transient Receptor Potential Channels and Itch

by Omar Mahmoud, Georgia Biazus Soares and Gil Yosipovitch

Int. J. Mol. Sci. 2023, 24(1), 420; https://doi.org/10.3390/ijms24010420 - 27 Dec 2022

Cited by 18 | Viewed by 3096

Abstract

Transient Receptor Potential (TRP) channels are multifunctional sensory molecules that are abundant in the skin and are involved in the sensory pathways of itch, pain, and inflammation. In this review article, we explore the complex physiology of different TRP channels, their role in modulating itch sensation, and their contributions to the pathophysiology of acute and chronic itch conditions. We also cover small molecule and topical TRP channel agents that are emerging as potential anti-pruritic treatments; some of which have shown great promise, with a few treatments advancing into clinical trials—namely, TRPV1, TRPV3, TRPA1, and TRPM8 targets. Lastly, we touch on possible ethnic differences in TRP channel genetic polymorphisms and how this may affect treatment response to TRP channel targets. Further controlled studies on the safety and efficacy of these emerging treatments is needed before clinical use. Full article

(This article belongs to the Special Issue Targeting TRP Channels for Pain, Itch and Inflammation Relief)

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11 pages, 277 KiB

Open AccessReview

TRPV3 and Itch: The Role of TRPV3 in Chronic Pruritus according to Clinical and Experimental Evidence

by Ji Young Um, Han Bi Kim, Jin Cheol Kim, Jin Seo Park, So Yeon Lee, Bo Young Chung, Chun Wook Park and Hye One Kim

Int. J. Mol. Sci. 2022, 23(23), 14962; https://doi.org/10.3390/ijms232314962 - 29 Nov 2022

Cited by 9 | Viewed by 2320

Abstract

Itching is a sensory phenomenon characterized by an unpleasant sensation that makes you want to scratch the skin, and chronic itching diminishes the quality of life. In recent studies, multiple transient receptor potential (TRP) channels present in keratinocytes or nerve endings have been shown to engage in the propagation of itch signals in chronic dermatological or pruritic conditions, such as atopic dermatitis (AD) and psoriasis (PS). TRPV3, a member of the TRP family, is highly expressed in the epidermal keratinocytes. Normal TRPV3 signaling is essential for maintaining epidermal barrier homeostasis. In recent decades, many studies have suggested that TRPV3 contributes to detecting pruritus signals. Gain-of-function mutations in TRPV3 in mice and humans are characterized by severe itching, hyperkeratosis, and elevated total IgE levels. These studies suggest that TRPV3 is an important channel for skin itching. Preclinical studies have provided evidence to support the development of TRPV3 antagonists for treating inflammatory skin conditions, itchiness, and pain. This review explores the role of TRPV3 in chronic pruritus, collating clinical and experimental evidence. We also discuss underlying cellular and molecular mechanisms and explore the potential of TRPV3 antagonists as therapeutic agents. Full article

(This article belongs to the Special Issue Targeting TRP Channels for Pain, Itch and Inflammation Relief)

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