Transient Receptor Potential Canonical (TRPC) Channels: Then and Now
Abstract
:1. Introduction and Historical Overview
2. Discovery of TRPC Channels
3. Structure of TRPC Channels
3.1. General Structural Organization of TRPCs
3.2. The Pore Region
3.3. Disulfide Bond
3.4. Cation Binding Sites
3.5. Arg593 Serves as “Molecular Fulcrum” and Is Critical for GPCR-Gq-PLC-Dependent Gating of TRPC5
3.6. The Calmodulin Binding Site on TRPC4
4. Physiological and Pathological Functions of TRPCs Revealed Using Gene Knockout, Knockin and Pharmacological Approaches
4.1. Physiological Activators of TRPC Channels
4.2. TRPC-Mediated Cellular Ca2+ Signaling
4.3. Physiological and Pathophysiological Functions of TRPC Channels
4.3.1. The Cardiovascular System
4.3.2. Cancer
4.3.3. Diabetes Mellitus
4.3.4. Neuronal Function
4.3.5. The Uterus
4.3.6. The Gastrointestinal Tract
4.3.7. The Kidneys
4.3.8. Others
5. A Brief Guide to Small Molecular Modulators for TRPC Channels
Agonists | Chemical Structure | TRPC Channel (EC50/IC50) | Characteristics | Reference |
---|---|---|---|---|
GSK1702934A | TRPC3 (0.08 μm) TRPC6 (0.44 μm) | No effect on TRPV4, TRPA1, TRPM1, TRPM4, CaV1.2, hERG, NaV1.5, or CXCR5 receptors at a concentration of 10 μmol/L | [305] | |
Pyrazolo-pyrimidines | TRPC6 (0.89–6.28 µm) TRPC3 (0.02–0.45 μm) | Potency order: TRPC3 > TRPC7 > TRPC6 | [306] | |
OptoDArG | TRPC6 TRPC3 (30 μm was tested) | Photoswitchable DAG analogue containing two azobenzene photoswitchable moieties; active in cis-form at 365 nm and inactive at 430 nm | [50] | |
OptoBI-1 | TRPC6 TRPC3 TRPC7 (10 and 30 μm were tested) | Photoswitchable azobenzene analogue of GSK1702934 A; active in the cis-form | [307] | |
PhoDAGs | TRPC6 TRPC2 (5 and 50 μm were tested) | Photoswitchable DAG analogues; contain one photoswitchable moiety; active in cis-form at 370 nM and inactive at 460 nm | [308] | |
Hyp9 | TRPC6 (1.26 μm) | A derivative of nonselective activator of TRPC3, TRPC6, and TRPC7 | [305] | |
Artemisinin | TRPC3 (33 µm) | May inhibit TRPC6 | [309] | |
(−)-Englerin A | TRPC4 (11.2 nm) and TRPC5 (7.6 nm) | Selective activator | [296] |
Antagonists | Chemical Structure | TRPC Channel (EC50/IC50) | Characteristics | Reference |
---|---|---|---|---|
Pyrazolo [1,5-a] pyrimidine (14a) | TRPC6 (1 μm) | Inhibits TRPC3/6/7 (TRPC6 > C7 > C3) with a very weak effect on TRPC4 and no effect on other TRP channels. | [197] | |
Pyrazole 3 (Pyr3) | TRPC3 (0.5 μm) TRPC6 (> 10 μm) | Also inhibits STIM/Orai | [274] | |
Pyrazole 10 (Pyr10) | TRPC (0.72 μm) TRPC6 (> 10 μm) | More selective than Pyr3; does not inhibit STIM/Orai | [160] | |
BTDM | TRPC3 (0.01 μm) TRPC6 (0.01 μm) | The exact BTDM binding site in TRPC6 was defined by cryo-EM; wedges between the S5-S6 pore domain and voltage sensor-like domain to inhibit channel opening | [99] | |
GSK503A | TRPC3 (0.003 μm) TRPC6 (0.021 μm) | Anilino thiazoles; good selectivity over other TRPA1,TRPV1, TRPV4, CaV1.2, hERG, and NaV1.5; in rodent models not orally bioavailable; high clearance, more suitable as in vitro tool | [141] | |
DS88790512 | TRPC6 (0.011 μm) | Novel blocker of TRPC6; cyclohexanone derivative; excellent selectivity against hERG and hNaV1.5 channels | [310] | |
larixyl acetate | TRPC6 (0.1–0.6 μm) | Larch-derived labdane-type diterpenes; 12- and 5-fold selectivity compared with TRPC3 and TRPC7 | [177] | |
BI749327 | TRPC6 (13 nm) | BI 749327 is 85-fold more selective for mouse TRPC6 than TRPC3 (IC50 = 1100 nm) and 42-fold versus TRPC7 | [311] | |
Pico145 (HC-608) | TRPC4 (63 pM) TRPC5 (1.3 nm) | Pico145 potency ranges from 9 to 1300 pM depending on the TRPC1/4/5 subtype while a range of other TRPC channels were unaffected | [312] | |
HC-070 | TRPC4 (46.0 ± 3.9 nm) TRPC5 (9.3 ± 0.9 nm) | HC-070 inhibits recombinant TRPC4 and TRPC5 homomultimers in heterologous expression systems with nanomolar potency | [220] | |
AC-1903 | TRPC5 (14.7 μm) | AC1903 selectively blocks TRPC5 ion channels | [265] | |
ML204 | TRPC4 (0.99 μm) TRPC5 (9.2 μm) | ML204 exhibited modest inhibitory effects on TRPC6 | [174] | |
Galangin | TRPC5 (0.45 μm) | Galangin is a natural product from the ginger family and a TRPC5 inhibitor depending on the substitution patterns of both the chromone core and the phenyl ring | [313] | |
SAR7334 | TRPC6 (7.9 nm) | SAR7334 inhibited TRPC3 and TRPC7-mediated Ca2+ influx into cells with IC50 s of 282 nm and 226 nm | [314] | |
SH045 | TRPC6(~5.8 nm) | IC50 for TRPC3 and TRPC7 are 0.84 μm and 0.22 μm, respectively | [315] | |
Bromoenol lactone (BEL) | TRPC5 TRPC6 TRPC1–TRPC5 Cav1.2, SOCE | TRPC5: 10.6 μm TRPC6: 7.2 μm Cav1.2: 7.6 μm | [55] |
6. Conclusions
Funding
Conflicts of Interest
References
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Type | Effects | Authors | Reference |
---|---|---|---|
TRPC1 KO | TRPC1 KO mice exhibited increased mGluR agonist-induced non-selective inward currents in the CA1 neurons of the hippocampus | Kepura et al., 2020 | [287] |
TRPC1 KO mice did not develop pulmonary hypertension under chronic hypoxia and had reduced vascular remodeling; however, right ventricular hypertrophy was similar to that in WT mice | Malczyk et al., 2013 | [163] | |
TRPC1 KO mice showed impairment in spatial working memory and fear memory formation but innate fear behavior was unaffected; activation of mGluR increased inward currents in hippocampal neurons from WT but not from TRPC KO mice | Lepannetier et al., 2018 | [223] | |
TRPC1 KO mice fed a high fat diet exhibited reduced fat mass, fasting glucose concentrations, and autophagy markers, whereas apoptosis markers were increased | Krout et al., 2017 | [200] | |
Tamoxifen-inducible TRPC1 genetic ablation in the hippocampus impaired mGluR-induced ERK1/2 activation, diminished mGluR-LTD, and decreased memory extinction | Yerna et al., 2020 | [224] | |
TRPC1 KO mice exhibited increased cerebral ischemia/reperfusion-induced infarction, neurological severity score, memory impairment, and oxidative stress. | Xu et al., 2018 | [231] | |
TRPC1 KO mice exhibited a reduced airway remodeling following house dust mite challenge with decreases in mucus production, cytokine secretion, and collagen deposition. | Pu et al., 2019 | [286] | |
TRPC1 KO mice exhibited no deficit of learning and memory under physiological conditions, but exacerbated learning and memory deficits induced by amyloid-β (Aβ), associated with Alzheimer’s disease | Li et al., 2018 | [210] | |
TRPC1 KO mice exhibited a reduced endothelial progenitor cell function secondary to calmodulin/endothelial nitric oxide synthase downregulation | Du et al., 2018 | [167] | |
Improved motor performance and an increased density of striatal medium spiny neuron spines in a mouse model of Huntington disease | Wu et al., 2018 | [222] | |
TRPC3 KO | TRPC3 KO mice exhibited ameliorated hypertension through reduction of angiotensin II-induced mitochondrial ROS generation | Wang et al., 2017 | [159] |
TRPC3 KO impaired the pluripotency of undifferentiated mouse embryonic stem cells and repressed their neural differentiation | Hao et al., 2018 | [215] | |
TRPC3 KO mice exhibited reduced pilocarpine-induced seizures and theta activity involved in status epilepticus | Phelan et al., 2017 | [237] | |
Phenylephrine-induced vasoconstriction and endothelium-dependent acetylcholine-induced vasodilation were reduced in TRPC3 KO mouse mesenteric arteries, whereas KCl- or pressure-induced vasoconstriction was unaltered. | Yeon et al., 2014 | [170] | |
Increase of mGluR1-induced slow EPSC by GABABR activation was absent in TRPC3 KO mouse cerebellar Purkinje neurons but unaltered in TRPC1, TRPC4 and TRPC1/4/5/6 KO Purkinje neurons | Tian & Zhu, 2018 | [234] | |
TRPC3 KO mice exhibited a delayed occurrence of inflammation-induced preterm labor | Jing et al., 2018 | [251] | |
TRPC3 KD | TRPC3 KD resulted in a decreased insulin-mediated glucose uptake in adult skeletal muscle cells | Lanner et al., 2009 | [203] |
TRPC3 KD resulted in a reduced angiotensin II-induced Ca2+ influx in VSMC from spontaneously hypertensive rats | Liu et al., 2009 | [157] | |
TRPC4 KO | TRPC4 KO mice exhibited a reduced self-administration of cocaine, but normal learning for natural reward | Klipec et al., 2016 | [226] |
TRPC4 KO mice lack store-operated Ca2+ currents and agonist-dependent vasorelaxation | Freichel et al., 2001 | [165] | |
TRPC5 KO | Compared with WT mice, TRPC5 KO mice had a reduced phosphatidylserine externalization and less apoptosis of cerebral neurons following ischemia-reperfusion | Guo et al., 2020 | [229] |
Cortical neurons from TRPC5 KO mice were resistant to H2O2 toxicity as compared to WT neurons | Park et al., 2019 | [230] | |
Acetylchoine-induced endothelium-dependent contractions were smaller in TRPC5 KO carotid arteries compared to WT mice; TRPC5 contributed by stimulating COX-2-mediatedprostanoid production from carotid artery endothelial cells | Liang et al., 2019 | [185] | |
TRPC5 KO mice fed supplemental cholic acid had less liver enlargement than WT; hepatic bile acid was lower in TRPC5 KO mice | Alawi et al., 2017 | [283] | |
TRPC5 KO mice demonstrated reduced nociceptive thresholds (thermal and mechanical) in a complete Freund’s adjuvant-induced unilateral arthritis model | Alawi et al., 2017 | [243] | |
TRPC5 KO did not alter body temperature but was associated with increased accumulation of peritoneal leukocytes secreting inflammatory mediator in thioredoxin-treated LPS- injected mice. | Pereira et al., 2018 | [275] | |
Isoliquiritigenin from Glycyrrhiza glabra (Licorice) inhibits atherosclerosis by blocking TRPC5 channel expression and lipid serum levels in an apolipoprotein E (ApoE) knockout mouse model and angiotensin II-stimulated vascular smooth muscle cells (VSMCs) | Qi et al., 2020 | [184] | |
TRPC5 KO mice exhibited diminished innate fear levels in response to aversive stimuli and reduced response to metabotropic glutamate receptor activation in amygdala | Riccio et al., 2009 | [218] | |
TRPC5 KD | Knockdown of TRPC5 increased chemosensitivity to temozolomide in glioblastoma | Zou et al., 2019 | [190] |
TRPC6 KO | Compared to Akita mice, TRPC6 KO Akita mice exhibited increased insulin resistance, mesangial expansion, and glomerular injury but reduced albuminuria and tubular injury | Wang et al., 2019 | [202] |
In the unilateral ureter obstruction model, TRPC6 knockout was linked to decreased expression of pro-fibrotic, with pro-inflammatory genes being unaffected | Kong et al., 2019 | [271] | |
Reduces allergic airway response | Sel et al., 2008 | [284] | |
Induction of hypoventilation resulted in severe arterial hypoxemia not found in wild type | Weissmann et al., 2006 | [161] | |
Displayed reduced litter sizes and structural changes of the placenta | Hasna et al., 2019 | [252] | |
Protects mice from mTBI-induced aortic endothelial dysfunction; | Chen et al., 2019 | [176] | |
TRPC6 knockout has reno-protective effects in diabetic kidney disease, protecting the podocytes but not the glomerulus as a whole | Spires et al., 2018 | [205] | |
In TRPC6 KO mice, pancreatic stellate cells (PSCs) exhibited decrease migration as compared to WT PSCs under hypoxic conditions | Nielsen et al., 2017 | [198] | |
TRPC6 KO mice exhibited an elevated blood pressure and enhanced agonist-induced aortic contractility due to upregulation of constitutively active TRPC3-type channels | Dietrich et al., 2005 | [145] | |
TRPC6 KD | Attenuated Ca2+ influx and the stress fiber formation induced by DHPG | Wang et al., 2019 | [269] |
Prevented podocyte permeability increase induced by puromucin aminonucleaside | Sun et al., 2012 | [270] | |
Increased autophagic flux and mitigated oxidative stress-induced apoptosis of proximal tubular cells | Hou et al., 2018 | [272] | |
Decreased hypoxic increases of Ca2+ influx in PASMCs | Malczyk et al., 2017 | [162] | |
Increased TGF-β1-induced Akt phosphorylation at Ser473 in VSMCs | Numaga-Tomita et al., 2019 | [154] | |
Mitochondrial elongation, reduced phosphorylation of dynamin-related protein 1, and extracellular-signal-regulated kinase 1/2 | Ko et al., 2017 | [221] | |
Unaltered ROS production, but increased inflammatory cytokines production compared to WT mice | Oda et al., 2017 | [288] | |
TRPC6 KD | Increased density of striatal medium spiny neuron spines in a mouse model of Huntington disease | Wu et al., 2018 | [222] |
TRPC1 or TRPC3 KD | Asthmatic mouse airway smooth muscle cells exhibited upregulated TRPC1 and TRPC3 and increased proliferation. Knockdown either of the channels reduced proliferation. | Zhang et al., 2018 | [285] |
TRPC6 KO and TRPC5/6 DKO | TRPC6 KO mice and TRPC5/6 double KO mice were protected from H2O2-induced damage in a model of diabetic kidney disease | Ilatovskaya et al., 2018 | [206] |
TRPC1/4 KO TRPC5 KO TRPC1 KO | LTP and pilocarpine-induced seizures are reduced in TRPC5 KO mice, but are unaltered in TRPC1/4 KO mice; mGluR-mediated epileptiform bursting in the hippocampal CA1 area is not affected in TRPC5 KO mice, but is abolished in TRPC1 KO and TRPC1/4 DKO mice; seizure-induced neural cell death in the hippocampus was reduced in both TRPC5 KO and TRPC1/4 DKO mice | Phelan et al., 2013 | [219] |
TRPC1/4/5 KO | TRPC1/4/5 KO mice exhibited deficits in spatial working memory and relearning task, while spatial reference memory was not affected | Bröker-Lai et al., 2017 | [126] |
TRPC1/4/5 KO mice exhibited decreased basal-evoked secretion, reduces readily releasable vesicles pool size, and accelerated synaptic depression during high-frequency stimulation, whereas TRPC5 KI showed short-term enhancement of synaptic strength during high frequency stimulation | Schwarz et al., 2019 | [225] | |
TRPC3/6/7 KO | Compared to WT mice, triple TRPC3/6/7 KO mice had smaller infarct size when subjected to cerebral ischemia-reperfusion | Chen et al., 2017 | [228] |
TRPC1/4/5/6 KO | Tetra-TRPC KO mice are protected from hyperglycemia-evoked vasoregression. In addition, the KO mice are resistant to the STZ-induced reduction in retinal layer thickness | Sachdeva et al., 2018 | [207] |
TRPC1/4/5 or hepta-TRPC-KO | No change in persistent activity in entorhinal cortex neurons of layer V | Egorov et al., 2019 | [227] |
Hepta- TRPC KO | Thapsigargin-induced store-operated Ca2+ entry was absent in Orai1 KO anterior pituitary cells, but was unaffected in hepta TRPC KO; conversely, spontaneous intracellular Ca2+ oscillations related to electrical activity was reduced in hepta TRPC1-7 KO mouse cells and unaffected in Orai1 KO mouse cells | Núñez et al., 2019 | [289] |
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Chen, X.; Sooch, G.; Demaree, I.S.; White, F.A.; Obukhov, A.G. Transient Receptor Potential Canonical (TRPC) Channels: Then and Now. Cells 2020, 9, 1983. https://doi.org/10.3390/cells9091983
Chen X, Sooch G, Demaree IS, White FA, Obukhov AG. Transient Receptor Potential Canonical (TRPC) Channels: Then and Now. Cells. 2020; 9(9):1983. https://doi.org/10.3390/cells9091983
Chicago/Turabian StyleChen, Xingjuan, Gagandeep Sooch, Isaac S. Demaree, Fletcher A. White, and Alexander G. Obukhov. 2020. "Transient Receptor Potential Canonical (TRPC) Channels: Then and Now" Cells 9, no. 9: 1983. https://doi.org/10.3390/cells9091983