Transient Receptor Potential Vanilloid subfamily member 6 (TRPV6) is an epithelial Ca2+ channel that belongs to the transient receptor potential family (TRP) of proteins. The TRP family is a group of channel proteins critical for ionic homeostasis and the perception of various physical and chemical stimuli. TRP channels can detect temperature, osmotic pressure, olfaction, taste, and mechanical forces. The human genome encodes for 28 TRP channels, which include six TRPV channels. The high Ca2+-selectivity of TRPV5 and TRPV6 makes these channels distinct from the other four TRPV channels (TRPV1-TRPV4). TRPV5 and TRPV6 are involved in Ca2+ transport, whereas TRPV1 through TRPV3 are heat sensors with different temperature threshold for activation, and TRPV4 is involved in sensing osmolarity. Genetic defects in TRPV6 gene are linked to transient neonatal hyperparathyroidism and early-onset chronic pancreatitis. Dysregulation of TRPV6 is also involved in hypercalciuria, kidney stone formation, bone disorders, defects in keratinocyte differentiation, skeletal deformities, osteoarthritis, male sterility, Pendred syndrome, and certain sub-types of Cancer.
aTo be verified in different tissues.
Differences in the TRPV6 expression profile have been reported possibly due to variation in assay-dependent such primer design, hybridization probes, PCR vs. northern blotting, semi-quantitative PCR vs. RT-PCR, and antibodies used for immunodetection. TRPV6 expression profile is also influenced by age, gender, Ca2+ and vitamin D3 levels in food, hormonal status, location within the tissue, cellular location, reproductive status, and weaning status (see Section Regulation).
In humans, TRPV6 transcripts have been detected in the placenta, pancreas, prostate cancer, and duodenum and the prostate by northern blotting; and in duodenum, jejunum, placenta, pancreas, testis, kidney, brain, and colon by semi-quantitative PCR. In rodents, TRPV6 expression has been validated in the duodenum, cecum, small intestine, colon, placenta, pancreas, prostate, and epididymis by Northern Blotting. In mouse, TRPV6 transcript abundance measured by RT-PCR is as follows: prostate > stomach, brain > lung > duodenum, cecum, heart, kidney, bone > colon > skeletal muscle > pancreas.
Data from Human Protein Atlas and RNA-Seq based suggest TRPV6 mRNA is low in most tissues except for the placenta, salivary gland, pancreas, and prostate. TRPV6 mRNA is expressed in the apical domain of murine osteoclasts of cortical bone. Cortical and trabecular osteocytes do not express TRPV6 mRNA whereas osteoblasts show weak expression.
Overall, four subunits of TRPV6 arrange to form a tetrameric channel displaying a four-fold symmetry. Beginning from N-terminus and moving towards the C-terminus of the protein, each TRPV6 polypeptide contains: an N-terminal helix, an ankyrin repeat domain (ARD) containing six ankyrin repeats, a β-hairpin structure linker domain made up two β-strands, a helix-turn-helix motif, a pre-SI helix, TM domain made up of six TM helices (S1 through S6), a pore-loop (also called P-loop), amphipathic TRP helix, C-terminal hook, and a six-residue β-strand (β3) (Figure 1).
The TRPV6 channel protein displays four-fold symmetry and contains two main compartments: a 30 Å-tall transmembrane domain with a central ion channel pore and a ~70 Å-tall and a ~110 Å-wide intracellular skirt enclosing a 50 Å × 50 Å cavity wide cavity underneath the ion channel. The clustering of four TRPV6 subunits forms an aqueous pore exhibiting a fourfold symmetry (Figure 2). A pre-SI helix links the intracellular portion of the protein to the TM domain through a linker domain made up of β-hairpin structure and a helix-turn-helix motif. Helices S1 through S4 form a transmembrane helical bundle or TM domain that is inserted almost perpendicularly to the plane of the plasma membrane.
The pore module elements are made up of S5, S6, and the P-loop in TM domains. The pore module from each TRPV6 polypeptide participates in inter-subunit interactions to form a central ion pore (Figure 1). The pore-forming elements of each TRPV6 subunit also interact with S1-S4 domains of the adjacent polypeptide in a domain-swapped arrangement. Intersubunit interactions also occur between S1-S2 extracellular loops and S5-P and S6-P loops of the neighboring TRPV6 subunits. The conserved N-linked glycosylation site on the S1-S2 loop is required for by the Klotho-mediated activation. The intracellular skirt portion of the TRPV6 protein is mainly made up of the ankyrin repeats. The TRP domain is oriented parallel to the membrane and participates in hydrophobic interactions with the TM domain and the hydrophilic interactions in the intracellular skirt. The N-terminal helix, C-terminal hook, and β-sheets (formed by the β-hairpin structure in the linker domain) in the channel participates in intersubunit interactions with the ARDs to provides a framework for holding the elements of the intracellular skirt together.
The TRPV6 pore has four main elements, namely, the extracellular vestibule, a selectivity filter, a hydrophobic cavity, and a lower gate. Facing the central lumen of the channel, a four-residue selectivity filter (538TIID541) containing four Aspartate 541 (D541) side chains (one from each protomer) is critical for Ca2+ selectivity and other biophysical properties of the channel. This filter forms a negatively charged ring that discriminates between ions based on their size and charge. Mutations in the critical pore-forming residue of TRPV6 blocks Ca2+uptake, a strategy has been used to generate TRPV6 loss-of-function models to examine the role of the channel in animal physiology. Four different types of cation binding sites are thought to exist in the TRPV6 channel. Site 1 is located in the central pore and shares the same plane that is occupied by the key selective residues D541. Site 2 is thought to be present about 6-8 Å below Site 1 followed by Site 3 which is located in the central pore axis about 6.8 Å below Site 2. Site 2 and 3 are thought to interact with partially-hydrated to equatorially-hydrated Ca2+ ions. Finally, four symmetrical cation binding sites in the extracellular vestibule mediate the recruitment of cations towards the extracellular vestibule of TRPV6 and are referred to as recruitment sites.
The conformational changes involved in channel opening are hinged around the residue Alanine 566 (A566) and occur in the pore-lining helix S6 (Figure 3). The upper portion of S6 helix undergoes an α-to-π helical transition which forces the lower portion of the helix to turn by 100 degrees and tilt away from the pore axis by 11 degrees. This conformational change moves the lower portion of the helix gating the pore and thereby widens the pore size. The conformational change alters the residues facing the pore axis and triggers the formation of new electrostatic bonds subunit and salt bridges that offset the high energetic cost of unfavorable α-to-π helical transition that occurs during channel opening.
The influx of Ca2+ inside the cell triggers negative feedback mechanisms to suppress TRPV6 activity and prevent Ca2+ overload. TRPV6 channel activity is regulated by the intracellular level of phospholipid phosphatidylinositol 4,5-bisphosphate (PIP2) and interactions with Ca2+-Calmodulin (CaM) complex. The depletion of PIP2 or CaM-binding inactivates TRPV6. The influx of Ca2+ in TRPV6 expressing cells activates phospholipase C (PLC) which in turn hydrolyzes PIP2. Depletion in PIP2 levels results in a decline in channel activity since most TRP channels require this lipid for activation. The lipid PIP2 can override Ca2+-CaM-mediated inhibition of TRPV6. Overall, TRPV6 inactivation by calmodulin is orchestrated by a balance of intracellular Ca2+ and PIP2 concentration.
Among 20+ TRPV6 interactors identified so far, the functional consequences of Ca2+-binding protein Calmodulin (CaM) and Glucuronidase Klotho have been most extensively characterized [36, 37, 41, 42]. Functional consequences of TRPV6 channel activation are summarized in the table below).
TRPV6 Interactors and their Functional ConsequencesBSPRY: B-Box and Spry Domain Containing Protein; FYN: Fyn Kinase Belonging Src Family of Kinases; I-MFA: Myo D Family Inhibitor; NHERF: Na Exchanger Regulatory Factor; NIPSNAP14-Nitrophenylphosphatase Domain and Non-Neuronal SNAP25-Like Protein Homolog 1; Numb: Drosophila mutation that removes most of the sensory neurons in the developing peripheral nervous system; PTP: Protein Tyrosine Phosphatase; Rab11a: Member RAS Oncogene Family; RGS2: Regulator Of G-Protein Signaling 2; RyR1: Ryanodine Receptor 1; TRPC1: Transient receptor potential canonical 1; TRPML3: Transient receptor potential Mucolipin-3.
The Ca2+-selective channel proteins TRPV6 and TRPV5 cooperate to maintain calcium concentration in specific organs. TRPV6 functions as apical Ca2+ entry channels mediating transcellular transport of this ion in the intestine, placenta, and possibly some other exocrine organs. TRPV6 also plays important roles in maternal-fetal calcium transport, keratinocyte differentiation, and Ca2+ homeostasis in the endolymphatic system of the vestibular system, and maintenance of male fertility.
In contrast to the intestine, where TRPV6 is the gatekeeper of Ca2+ absorption, the transcellular reabsorption of this ion in the kidney occurs through TRPV5. Although TRPV5 is a recognized gatekeeper for transcellular reabsorption of Ca2+ ion in the kidney, TRPV6 knockout (KO) mice also struggle to concentrate their urine and display hypercalciuria. TRPV6 is known to co-localize with TRPV5 Calbindin-D28K in apical domains of distal convoluted tubules and connecting tubules [20]. TRPV5 KO mice compensate for Ca2+ loss by increasing TRPV6 expression in the duodenum. Moreover, a recent study analyzing vitamin D responsive genes in ovine, canine and, equine kidney suggested that TRPV6, calD9k/calD28k, and PMCA could be the main pathways orchestrating transcellular Ca2+ transport in the kidney of sheep, dogs, and horses.
Under conditions of sub-optimal dietary Ca2+, normal serum calcium levels in TRPV6 KO mice are maintained at the expense of bone. TRPV6 plays an important role in osteoclasts but not in osteoblasts. In mice, TRPV6 depletion results in increased osteoclasts differentiation whereas TRPV5 is essential for proper osteoclastic bone resorption.
Keratinocytes differentiation is orchestrated by calcium switch, a process that entails an influx of Ca2+ in keratinocyte which induces broad transcriptional changes necessary for desmosome formation, stratification, and cornification. TRPV6 KO mice display thinner layers of stratum corneum and 20% of the mice also show alopecia and dermatitis. The silencing of TRPV6 impairs Ca2+-mediated differentiation of human primary keratinocytes and downregulates differentiation markers such as involucrin, transglutaminase-1, and cytokeratin-10. The hormone 1,25-dihydroxyvitamin-D3 upregulates TRPV6 in keratinocytes and triggers a Ca2+ influx. This in turn induces the expression of keratinocyte differentiation-specific pathways.
Loss of TRPV6 in murine placenta severely impairs Ca2+ transport across trophoblast and reduces embryo growth, induces bone calcification, and impairs bone development. In humans, the insufficient maternal-fetal transport caused by pathogenic genomic variants of TRPV6 is thought to be a cause for skeletal defects observed in selected case reports of transient neonatal hyperparathyroidism (TNHP) cases. These variants are believed to compromise the plasma membrane localization of the protein. Exome sequencing of an infant with severe antenatal onset thoracic insufficiency with accompanying fetal skeletal abnormalities indicates the critical role of TRPV6 in maternal-fetal transport. The study indicated that compound heterozygous variants of TRPV6 result in severe undermineralization and severe dysplasia of the fetal skeleton.
Recent evidence indicates that naturally occurring TRPV6 loss of function variants predisposes certain demographics to chronic pancreatitis (CP) by dysregulating calcium homeostasis in the pancreatic cells. Sequencing studies among chronic pancreatitis patients revealed the presence of 33 missense and 2 nonsense variants predisposed Japanese, German, and French patients to a higher risk of CP. Overall, these studies have shown that disease-inducing TRPV6 loss-of-function genomic variants are over-represented in German, French, Chinese, and Japanese CP patients in comparison to controls in their respective groups. The loss-of-function variants are believed to compromise calcium transport in the pancreas by act by either reducing the total protein level and/or compromising Ca2+ uptake activity by the channel.
The role of TRPV6 in renal stone formation has been suggested through sequencing studies conducted on a cohort of 170 patients in Switzerland. The studies revealed that the frequency of TRPV6 gain-of-function haplotype is significantly higher in Ca2+-stone formers (nephrolithiasis) in comparison to non-formers. The observed hypercalciuria phenotypes from animal studies and studies on TRPV6 single nucleotide polymorphisms (SNPs) suggest that TRPV6 haplotype could be an important risk factor for absorptive and renal hypercalciuria (kidney stones due to impaired intestinal absorption and renal re-absorption respectively). The lower incidence of kidney stone diseases in African-Americans and a relatively higher prevalence of ancestral haplotype suggest theory according to which this haplotype endows an advantage of increased Ca2+ reabsorption in this demographic and reduces the incidence of kidney stones.
The high degree of similarity between Hereditary Vitamin D–Resistant Rickets (HVDRR) disease symptoms and observed phenotypes in TRPV6 KO mice has led some experts to postulate pathological connections between the disease and TRPV6 dysfunction. TRPV6 plays an important chondroprotective role by regulating multiple aspects of chondrocyte function, such as extracellular matrix secretion, the release of matrix-degrading enzymes, cell proliferation, and apoptosis. Furthermore, TRPV6 knockout mice display multiple osteoarthritis (OA) phenotypes such as cartilage fibrillation, eburnation, and loss of proteoglycans.
Expression of TRPV6 is upregulated by estrogen, progesterone, and estradiol in breast cancer cell line T47D. In agreement with these observations, the estrogen receptor antagonist Tamoxifen reduces TRPV6 expression in T47D cells and suppresses Ca2+-uptake of the channel in both ER-positive and ER-negative breast cancer cell lines. The overexpression of TRPV6 is associated with early-stage colon cancer and its silencing in colon cancer induces apoptosis and inhibits cancer cell proliferation. In terms of mechanism, mutations within the calmodulin-binding domains of TRPV6 channels confers invasive properties to colon adenocarcinoma cells. The proteins p38α and GADD45α are believed to upregulate TRPV6 expression signaling in SW480 colon cancer cells by enhancing vitamin D signaling. TRPV6 has been reported to amplify Insulin-like growth factors (IGF)-induced PI3K-PDK1-Akt signaling in human colon cancer and promote colon cancer.
Several chemical inhibitors are known to inhibit TRPV6. Some compounds that have demonstrated inhibitory activity towards TRPV6 include TH-1177, 2-Aminoethoxydiphenyl borate (2-APB), 2-APB derivative 22b, Econazole, Miconazole, Piperazine derivative Cis-22a, Capsaicin, Δ9-tetrahydrocannabivarin, Xestospongin C, Lidocaine, gold-caged nanoparticle (PTX-PP@Au NPs) and Sorcidin C-13 (SOR-C13) synthetic peptide. Among different inhibition strategies tested so far, the 13-amino acid peptide SOR-C13 has shown the most promise. This 13-amino acid peptide derived from 54-amino acid peptide found in the paralytic venom of the northern short-tailed shrew (Blarina brevicauda) reduces cancer growth in cell and animal models. This anti-cancer agent has recently completed a Phase I clinical safety trial that had enrolled 23 patients with advanced solid tumors of epithelial origin non-responsive to all standard-of-care treatments.
The regulation of TRPV6 can be examined mainly in the context of its physiological, hormonal, and molecular factors. The hormonal regulation of TRPV6 has been characterized most extensively. In this regard, its regulation by the hormone vitamin D3 and sex hormones has been examined in considerable detail. Rodent studies suggest that the TRPV6 channel is regulated by a wide range of physiological factors such as diet, age, gender, pregnancy, lactation, sex hormones, exercise, age, and gender. Some biological and pharmacological agents known to regulate TRPV6 include glucocorticoids, immunosuppressive drugs, and diuretics.
Multiple dose-response and time-course experiments in rodents and colon cancer cell lines have conclusively shown TRPV6 mRNA is robustly induced by this vitamin D at extremely low concentrations. At least five vitamin D response elements (VDREs) at positions −1.2, −2.1, −3.5, −4.3, and −5.5 kb relative to transcriptional start site (TSS) have been identified on TRPV6 transcripts. Among these five sites, VDREs at positions −1.2, −2.1, and −4.3 kb are significantly more responsive to 1,25-(OH)2D3 in comparison to VDREs located at −3.5 and −5.5 kb which do not appear to contribute substantially to vitamin D mediated transcriptional regulation in the intestine. Mechanism wise, TRPV6 transcription is initiated in response to vitamin D Receptor (VDR)-mediated signaling, although other non-direct mechanisms cannot be ruled out. Important steps in vitamin D mediated transcriptional regulation include 1) binding of vitamin D on its cognate vitamin D receptor (VDR), 2) the translocation of vitamin D receptor (VDR)-retinoid X receptor heterodimer complex in the nucleus, 3) binding VDR-RXR complex on the TRPV6 gene promoter, 4) recruitment of steroid receptor coactivator 1 and RNA polymerase II on the promoter, and 5) transcriptional activation mediated through histone H4 acetylation events.
Duodenal expression of TRPV6 transcripts is upregulated in WT and VDR KO mice during pregnancy and lactation. The hormone prolactin upregulates TRPV6 transcription and facilitates an increase in intestinal Ca2+ absorption in lactating and pregnant rats, possibly as an adaptive mechanism for overcoming the loss in bone mineralization content during lactation.
The intestinal expression of TRPV6 in mice varies dramatically by age and relative tissue location. The duodenal expression of TRPV6 is undetectable at P1 and increases 6-fold as mice age to P14. Similarly, the expression also varies with age in the jejunum, where TRPV6 levels increases from P1 to P14, become weak at 1-month age and becomes undetectable in older mice. The expression of TRPV6 in older rats (12-months) is at least 50% lower in comparison to younger counterparts (2-months old). In both WT and VDR KO mice, the age-associated decline in intestinal absorption of Ca2+ is accompanied by a decline in duodenal expression of TRPV6.
Sex hormones play an important role in the regulation of TRPV6. In comparison to male mice, female mice exhibit a 2-fold higher increase in duodenal expression of TRPV6 mRNA following vitamin D treatment. Sex hormone-associated differential regulation of TRPV6 across genders is believed to be correlated to differences in relative risk to osteoporosis in older postmenopausal women which have been reported to have lower TRPV6 and VDR expression in comparison to males.
Estrogen treatment upregulates TRPV6 transcripts by 8-fold in VDR KO mice and by 4-fold in ovariectomized mice. Greater than 50% reduction in TRPV6 mRNA has been observed in estrogen receptor α KO mice. It is believed that estrogen could be differentially regulating Ca2+ absorption in the duodenum by increasing TRPV6 expression through ERα. Anti-progesterone agent RU486 and anti-estrogen agent ICI 182,780 suppress TRPV6 expression in rodents by their respective antagonist action on progesterone and estrogen receptors. Estrogen, progesterone, and dexamethasone are known to upregulate TRPV6 expression in the cerebral cortex and hypothalamus of mice suggesting a potential involvement of TRPV6 in calcium absorption in the brain.
Subcutaneous administration of glucocorticoids dexamethasone induces both renal and intestinal expression of TRPV6 in mice within 24 hours of whereas oral application of prednisolone reduction in TRPV6 which is also accompanied by reduced Ca2+ absorption in duodenum. Intestinal regulation of TRPV6 in response to glucocorticoids appears to be VDR-dependent. The enzyme serum and glucocorticoid-regulated kinase 1 (SKG1) regulates TRPV6 expression by enhancing phosphatidylinositol-3-phosphate-5-kinase PIKfyve (PIP5K3). This kinase is critical for the generation of secondary messenger PIP2, a known lipid activator of TRPV6.
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