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REVIEW |
Center for Translational Neuroscience, Duke University, Durham, North Carolina 27710, USA
(Requests for offprints should be addressed to W Liedtke; Email: wolfgang{at}neuro.duke.edu)
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 Top Abstract Introduction: response to...References |
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Introduction: response to osmotic stimuli – a function of TRPV ion channels, apparent since ‘birth’ of this subfamily |
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TopAbstractIntroduction: response to...References |
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). Alluding to their function, TRPV1, TRPV2, TRPV3, and TRPV4 have been named ‘thermo-TRPs’; review articles on ‘thermo-TRPs’ are available for interested readers (Caterina & Julius 1999, Clapham 2003, Tominaga & Caterina 2004, Caterina & Montell 2005, Patapoutian 2005). TRPV5 and TRPV6, possibly function in Ca2+ uptake in the kidney and intestine (Hoenderop et al. 1999, 2003, Peng et al. 1999, 2003, den Dekker et al. 2003). Regarding the invertebrate TRPV channel genes, one invertebrate branch includes C. elegans OSM-9 and Drosophila IAV and the other branch includes OCR-1 to OCR-4 of C. elegans and Drosophila NAN. In case heterologous expression system data were available for TRPV channels, their non-selective conductance of cations with a (slight) preference for Ca2+ was apparent. This means that Ca2+ influx through the respective TPRPV channel is the critical signaling mechanism.
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, guided by the question: do TRPV ion channels function in transduction of osmotic (and mechanical) stimuli, and by which molecular mechanism?
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In heterologous cellular expression systems, there have not been reports on transduction of osmotic and mechanical stimuli involving TRPV1. Genetically engineered trpv1–/– mice, which have previously been shown to lack thermal hyperalgesia following inflammation (Caterina et al. 2000, Davis et al. 2000), also showed an altered response of their magnocellular hypothalamic neurons to tonicity stimuli. Very recently, Reza Sharif Naeini from Charles Bourque’s group reported that trpv1–/– mice failed to express an N-terminal variant of the trpv1 gene in magnocellular neurons of the supraoptic and paraventricular nucleus of the hypothalamus (Naeini et al. 2006). As these neurons are known to secrete vasopressin, the trpv1–/– mice were found to have a profound impairment of antidiuretic hormone (ADH) secretion in response to systemic hypertonicity, and their magnocellular neurons did not show an appropriate bioelectrical response to hypertonicity. These findings led Bourque and colleagues to conclude that this trpv1 N-terminal variant, which could not be identified at the molecular level, is likely involved as (part of) a tonicity sensor of intrinsically osmo-sensitive magnocellular neurons.
trpv1–/– mice also showed an abnormal response of their bladder to stretch (Birder et al. 2002). TRPV1 could be localized to sensory and autonomous ganglia neurons innervating the bladder, and also to urethelial cells. When bladder and urothel-epithelial cells were cultured, their response to mechanical stretch and hypotonicity was different from wild-type controls. Specifically, the TRPV1+ bladders secreted ATP upon stretch and hypotonicity, which, in turn, is known to activate nerve fibers in the urinary bladder. This response to mechanical stimulation was greatly reduced in bladders excised from trpv1–/– mice. It appears likely that this mechanism, functional in mice, also plays a role in human bladder epithelium. Intravesical instillation of TRPV1 activators is used to treat hyperactive bladder in spinal cord disease (Dinis et al. 2004, Lazzeri et al. 2004, Stein et al. 2004, Apostolidis et al. 2005). Another instance of an altered response to mechanical stimuli in trpv1–/– mice relates to the response of the jejunum to stretch (Rong et al. 2004). Afferent jejunal nerve fibers were found to respond with decreased frequency of discharge in trpv1–/– mice when compared with wild type. In humans, in the rectum, TRPV1-positive fibers were found significantly increased in patients suffering from fecal urgency, a condition with rectal hypersensitivity in response to mechanical distension (Chan et al. 2003). Expression of TRPV1+ fibers in rectal biopsy samples from these patients was positively correlated with a decreased threshold to stretch. In addition, the occurrence of TRPV1+ fibers was also correlated with a dysaesthesia, described as a burning sensation by the patients. Another recent study focused on possible mechanisms of signal transduction in response to mechanical stimuli in blood vessels (Scotland et al. 2004). Elevation of luminal pressure in mesenterial arteries was shown to be associated with generation of 20-hydroxyeicosatetraenoic acid, which, in turn, activated TRPV1 expressed on C-fibers leading to nerve depolarization and vasoactive neuropeptide release. With respect to nociception, using trpv1–/– mice, trpv1 was shown to be involved in inflammatory thermal hyperalgesia, but not inflammatory mechanical hyperalgesia (Caterina & Julius 1999, Gunthorpe et al. 2002). However, a specific blocker of TRPV1 was found to reduce mechanical hyperalgesia in rats (Pomonis et al. 2003). This latter result appears contradictory in view of the obvious lack of difference between trpv1–/– and wild-type control mice. This discrepancy is either due to a species difference between mouse and rat or may be due to the different mechanisms that affect signaling in a trpv1 general knockout versus a specific temporal pharmacological blocking of TRPV1 ion channel proteins, which very likely participate in signaling multiplex protein complexes.
Taken together, loss-of-function studies using trpv1–/– mice clearly imply the trpv1 gene as playing a significant role in transduction of osmotic and mechanical stimuli. Despite this phenotypical clarity, the details and molecular mechanisms await further investigation.
Tissue culture cell data implicate TRPV2 in osmo-mechanotransduction
In heterologous cellular expression systems, TRPV2 was initially described as a temperature-gated channel for stimuli >52 °C (Caterina et al. 1999). Recently, TRPV2 was also demonstrated to respond to hypotonicity and mechanical stimuli (Muraki et al. 2003). Arterial smooth muscle cells from various arteries expressed TRPV2. These myocytes responded to hypotonicity with Ca2+ influx. This activation could be reduced by specific downregulation of TRPV2 by an anti-sense method. Heterologously expressed TRPV2 in Chinese hamster ovary (CHO) cells displayed a similar response to hypotonicity. These cells were also subjected to stretch by suction of the recording pipette and by stretching the cell membrane on a mechanical stimulator. Both maneuvers led to Ca2+ influx that was dependent on heterologous TRPV2 expression.
In aggregate, having been discovered as a ‘thermo-TRP’, TRPV2 appears to be an ‘osmo-mechano-TRP’ as well. However, in the absence of reports on TRPV2 null mice, this grouping is based on tissue culture data.
In vivo mouse and tissue culture data implicate the trpv4 gene to function in osmo-mechanotransduction, including hydromineral homeostasis and pain
CHO immortalized tissue culture cells responded to hypotonic solution when they were (stably) transfected with TRPV4 (Liedtke et al. 2000). Human embryonic kidney cell line 293, transformed by large-T antigen (HEK-293T) cells, when maintained by the same authors, were found to express trpv4 cDNA, which was cloned from these cells. However, trpv4 cDNA was not found in other batches of HEK-293T cells, so that this cell line was used for heterologous expression by other groups (Strotmann et al. 2000, Wissenbach et al. 2000). Notably, when comparing the two settings, it was obvious that the single-channel conductance of TRPV4 was different (Liedtke et al. 2000, Strotmann et al. 2000). This underscores the relevance of complimentary gene expression in heterologous cellular systems for the functioning of TRPV4 in response to a basic biophysical stimulation. Also, it was found that the sensitivity of TRPV4 could be modulated by warming of the media. Similar results were found in another investigation when expressing TRPV4 in HEK-293T cells (Gao et al. 2003), reviewed in Mutai & Heller (2003), O’Neil & Heller (2005). In addition, in this investigation, the cells were mechanically stretched (at isotonicity). At room temperature, there was no response to mechanical stress; however, at 37 °C, the response to stretch resulted in the maximum Ca2+ influx of all conditions. In two other investigations, heterologously expressed TRPV4 was found to be responsive to changes in temperature (Guler et al. 2002, Watanabe et al. 2002). Temperature change was accomplished by heating the streaming bath solution. This method of applying a temperature stimulus represents a mechanical stimulus per se. Gating of TRPV4 was found to be amplified when hypotonic solution was used as streaming bath. In one of these investigations, temperature stimuli could not activate the TRPV4 channel in cell-detached inside-out patches (Watanabe et al. 2002).
In regards to maintenance of systemic osmotic pressure in live animals, trpv4–/– mice, when stressed with systemic hypertonicity, did not regulate their systemic tonicity as efficiently as did wild-type controls (Liedtke & Friedman 2003). Their drinking was reduced and systemic tonicity was significantly elevated. Continuous infusion of the ADH analog dDAVP led to systemic hypotonicity, whereas renal water readsorbtion was not changed in both genotypes. ADH synthesis in response to osmotic stimulation was reduced in trpv4–/– mice. Hypertonic stress led to reduced expression of c-FOS+ cells in the sensory circumventricular organ, organum vasculosum laminae terminalis (OVLT), indicating an impaired osmotic activation in this brain area lacking a functional blood–brain barrier. These findings in trpv4–/– mice point towards a deficit in central osmotic sensing. Thus, TRPV4 is necessary for the maintenance of the tonicity equilibrium in mammals. It is conceivable that TRPV4 acts as an osmotic sensor in the central nervous system (CNS). The impaired osmotic regulation in trpv4–/– mice reported differs from that published in another paper. While the author’s own experiments showed that trpv4–/– mice secrete lower amounts of ADH in response to hypertonic stimuli, the results from Mizuno et al.(2003) suggest that there is an increased ADH response to water deprivation and subsequent systemic administration of propylene glycol. The reasons for this discrepancy are not obvious. In the author’s investigation, a blunted ADH response and diminished cFOS response in the OVLT of trpv4–/– mice upon systemic hypertonicity suggests, as one possibility, an activation of TRPV4+ sensory cells in the OVLT by hypertonicity. These data imply that the trpv4 gene plays a significant role in the maintenance of systemic osmotic homeostasis in vivo, and a possible role for it in disorders of hydromineral homeostasis.
In regards to pain-related behavior in mice, Alessandri--Haber et al.(2005) described that hypertonic and hypotonic s.c. solution leads to pain-related behavior in wild-type mice, which is not present in trpv4–/– mice. When sensitizing nociceptors with prostaglandin E2, the pain-related responses to hypertonic and hypotonic stimulation increased in frequency, and were greatly reduced in trpv4–/– mice. The in vivo behavioral data for hypertonicity could not be mirrored in acutely dissociated dorsal root ganglion (DRG) neurons upon stimulation with hypertonicity and subsequent Ca2+ imaging, which was, on the other hand feasible for hypotonic stimulation. Taken together, this study indicates differences in the response of mice to noxious tonicity depending on the presence/absence of TRPV4. Yet at the level of a critical transducer cell, namely the DRG sensory neuron, only hypotonicity led to a rise of intracellular Ca2+, which was dependent on the presence of TRPV4. These data imply that the trpv4 gene plays a significant role in transduction of pain stimuli evoked or amplified by local changes in tonicity.
In aggregate, the trpv4 gene functions critically in regulation of systemic tonicity and in pain transduction of noxious osmotic stimuli in mammals. Heterologous cellular expression studies imply TRPV4 to confer responsiveness to hypotonicity (both aspects also reviewed in Voets et al. (2002), Liedtke & Kim (2005)).
Recent developments pertaining to trpv4 function in osmo-transduction at the cellular level: regulation of TRPV4 channels by N-glycosylation and their critical role in cellular volume regulation
Another recent focus in the field of TRP ion channels is intracellular trafficking, post-translational modification and subsequent functional modulation. For TRPV4, it was reported in heterologous cells (HEK-293T) that N-glycosylation between transmembrane-domain 5 and pore-loop homeostasis (position 651) decreases osmotic activation via decreased plasma membrane insertion (Xu et al. 2006). Interestingly, N-glycosylation between transmembrane domains 1 and 2 had a homeostasis similar effect on TRPV5, and the anti-ageing hormone KLOTHO could function as ß-glucuronidase and subsequently activate TRPV5 (Chang et al. 2005). Thus, it appears feasible that KLOTHO or related, KLOTHO-like hormones function as ß-glucuronidases regulating plasma membrane insertion of TRPV4. How critical this mechanism is in vivo, remains to be determined.
TRPV4 also has been found to play a role in maintenance of cellular osmotic homeostasis. One particular cellular defense mechanism of tonicity homeostasis is regulatory volume change, namely regulatory volume decrease (RVD) in response to hypotonicity. In a recent paper, Bereiter-Hahn’s group demonstrated that CHO immortalized tissue culture cells have a poor RVD which, after transfection with TRPV4, improved strikingly (Becker et al. 2005). In yet another study, Miguel Valverde’s group published that TRPV4 mediates the cell-swelling induced Ca2+ influx into bronchial epithelial cells that triggers RVD via Ca2+-dependent potassium ion channels (Arniges et al. 2004). This cell swelling response did not function in cystic fibrosis transmembrane resistance (CFTR) bronchial epithelia, where, on the other hand, TRPV4 could be activated by 4-ß-PDD, leading to Ca2+ influx. This indicates that TRPV4 is downstream of the signaling step that is genetically defective in cystic fibrosis, the CFTR chloride conductance. These findings raise the intriguing possibility that activation of TRPV4 could be used therapeutically in cystic fibrosis. Yet in another recent investigation, Ambudkar and colleagues found the concerted interaction of the water channel aquaporin-5 (AQP-5) with TRPV4 in hypotonic swelling-induced RVD of salivary gland epithelia (Liu et al. 2006). These findings shed light on molecular mechanisms operative in secretory organs that secrete watery fluids. This basic physiological mechanism appears to be maintained by a concerted interaction of TRPV4 and AQP-5, which was found to be dependent on the cytoskeleton (for interaction AQP-5–TRPV4, see also Sidhaye et al. (2006)). In regards to volume regulation of cells in the CNS, Andrew et al.(2006) reported very recently on neuronal RVD in response to hypotonic stimulation in brain slice culture. Perplexingly, the neurons were resistant to changes in tonicity, yet swelled readily when deprived of oxygen–glucose or when depolarized by potassium. This investigation raises once again the unresolved question of the molecular nature of the neuronal water conductance. The behavior of the neurons appears in sharp contrast to the above AQP-5–TRPV4 interaction described for hypotonic swelling and subsequent RVD by secretory epithelial cells. Taken together, TRPV4 also plays a role in regulatory volume decrease in response to tonicity-induced cell swelling, suggested for epithelial cells in airways and exocrine glands but not in nerve cells. An exciting possibility opens up in which TRPV4 could become a translational target in cystic fibrosis.
Mammalian TRPV4 directs osmotic avoidance behavior in C. elegans
Cloning of the C. elegans gene osm-9, the other founding member of the trpv gene family As referenced in the introduction, the osm-9 mutant line was first reported in 1997 (Colbert et al. 1997). The forward genetics screen in C. elegans applied a confinement assay with a high-molar osmotically active substance. osm-9 mutants did not respect this osmotic barrier, and the mutated gene was found to be a TRP channel. On closer analysis, osm-9 mutants did not respond to aversive tonicity stimuli, they did not respond to aversive mechanical stimuli to their ‘nose’, and they did not respond to (aversive) odorants. The OSM-9 channel protein was found to be expressed in amphid sensory neurons, the worm’s cellular substrate of exteroceptive sensing of chemical, osmotic, and mechanical stimuli. At the subcellular level, the OSM-9 channel was also expressed in the sensory cilia of the AWC and ASH sensory neurons. Bilateral laser ablation of the ASH neuron, referred by some researchers as the worms’ equivalent of the trigeminal ganglion or the ‘nociceptive’ neuron (Bargmann & Kaplan 1998), has been shown to lead to a deficit in osmotic, nose touch, and olfactory avoidance (Kaplan & Horvitz 1993). Next, four more TRPV channels from C. elegans were isolated, named OCR-1 to OCR-4 (Tobin et al. 2002). Out of these four channels, only OCR-2 was expressed in ASH. The ocr-2 mutant phenotype was virtually identical to the osm-9 phenotype with respect to worm ‘nociception’, and there was genetic evidence that the two channels were necessary for proper intracellular trafficking of each other in sensory neurons, indicating an interaction between OSM-9 and OCR-2. When expressing the mammalian capsaicin receptor TRPV1 in the ASH sensory neurons, neither osm-9 nor ocr-2 mutants could be rescued, but osm-9 ash::trpv1 transgenic worms displayed a strong avoidance to capsaicin, which normal worms do not respond to.
TRPV4 expression in ASH rescues osm-9 mechanical and osmotic deficits
Next, TRPV4 was transgenically directed to ASH amphid neurons of osm-9 mutants. Surprisingly, TRPV4 expression in C. elegans ASH rescued osm-9 mutants’defects in avoidance of hypertonicity and nose touch (Liedtke et al. 2003). However, mammalian TRPV4 did not rescue the odorant avoidance defects of osm-9, suggesting that this function of TRPV channels differs between vertebrate and invertebrate. This basic finding of the rescue experiments in osm-9 ash::trpv4 worms has important implications for our understanding of mechanisms of signal transduction (Fig. 2).
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When taken together, these findings suggest that mammalian TRPV4 was functioning as the osmotic and mechanical sensor or at least as a component of it. It should be realized that TRPV4 was expressed functionally only in ASH, a single sensory neuron, where the mammalian protein, with a similarity to OSM-9 of approximately 25%, was trafficked correctly to the ASH sensory cilia, a distance of more than 100 µm. The rescue was specific (not for mutated ocr-2, not by mammalian TRPV1 capsaicin receptor), and it respected genetically defined pathways.
The above OSM-9–TRPV4 study delivers stimulating points to be addressed in future investigations. Whereas TRPV4 restores responsiveness to hypertonicity in C. elegans osm-9 mutants, it is only gated by hypo-osmotic stimuli in transfected mammalian cells. The reasons for this discrepancy are not understood. Related to this study, it was recently reported that TRPV2 could rescue one particular deficit of the ocr-2 mutant, namely the dramatic downregulation of serotonin biosynthesis in the sensory ADF neuron, but mammalian TRPV2, unlike TRPV4 directing behavior in osm-9, did not complement the lack of the osmotic avoidance reaction of ocr-2 (Zhang et al. 2004, Sokolchik et al. 2005). However, common to these two investigations is the conservation of TRPV signaling across phyla that have separated for several hundred million years of molecular evolution, despite low sequence homology.
In reference to the Drosophila TRPV channels, NAN and IAV, the interested reader is directed to original papers (Kim et al. 2003, Gong et al. 2004) and relevant reviews (Vriens et al. 2004a, Liedtke & Kim 2005).
Outlook for future research on TRPV channels In regards to TRP channels, one topic for the future is the investigation of the functional significance of protein–protein interactions of TRPV ion channels with the interaction partners that are to be discovered (a particularly interesting example of protein–protein interactions of TRPV4 splice variants from airway epithelia was reported recently (Arniges et al. 2006), but see also Cuajungco et al.(2006)). In addition, there is the obvious potential for TRP channels as targets for translational efforts (Nilius et al. 2005), such as secretory disorders (e.g., cystic fibrosis), pain, and hydromineral homeostasis.
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TopAbstractIntroduction: response to...References |
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Andrew RD, Labron MW, Boehnke SE, Carnduff L & Kirov SA 2006 Physiological evidence that pyramidal neurons lack functional water channels. Cerebral Cortex. In Press.
Apostolidis A, Brady CM, Yiangou Y, Davis J, Fowler CJ & Anand P 2005 Capsaicin receptor TRPV1 in urothelium of neurogenic human bladders and effect of intravesical resiniferatoxin. Urology 65 400–405.[CrossRef][ISI][Medline]
Arniges M, Vazquez E, Fernandez-Fernandez JM & Valverde MA 2004 Swelling-activated Ca2+ entry via TRPV4 channel is defective in cystic fibrosis airway epithelia. Journal of Biological Chemistry 279 54062–54068.
Arniges M, Fernandez-Fernandez JM, Albrecht N, Schaefer M & Valverde MA 2006 Human TRPV4 channel splice variants revealed a key role of ankyrin domains in multimerization and trafficking. Journal of Biological Chemistry 281 1580–1586.
Bargmann CI & Kaplan JM 1998 Signal transduction in the Caenorhabditis elegans nervous system. Annual Review of Neuroscience 21 279–308.[CrossRef][ISI][Medline]
Becker D, Blase C, Bereiter-Hahn J & Jendrach M 2005 TRPV4 exhibits a functional role in cell-volume regulation. Journal of Cell Science 118 2435–2440.
Birder LA, Nakamura Y, Kiss S, Nealen ML, Barrick S, Kanai AJ, Wang E, Ruiz G, De Groat WC, Apodaca G et al. 2002 Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nature Neuroscience 5 856–860.[CrossRef][ISI][Medline]
Caterina MJ & Julius D 1999 Sense and specificity: a molecular identity for nociceptors. Current Opinion in Neurobiology 9 525–530.[CrossRef][ISI][Medline]
Caterina MJ & Montell C 2005 Take a TRP to beat the heat. Genes and Development 19 415–418.
Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD & Julius D 1997 The capsaicin receptor: a heat-activated ion channel in the pain pathway [see comments]. Nature 389 816–824.[CrossRef][Medline]
Caterina MJ, Rosen TA, Tominaga M, Brake AJ & Julius D 1999 A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398 436–441.[CrossRef][Medline]
Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI & Julius D 2000 Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288 306–313.
Chan CL, Facer P, Davis JB, Smith GD, Egerton J, Bountra C, Williams NS & Anand P 2003 Sensory fibres expressing capsaicin receptor TRPV1 in patients with rectal hypersensitivity and faecal urgency. Lancet 361 385–391.[CrossRef][ISI][Medline]
Chang Q, Hoefs S, van der Kemp AW, Topala CN, Bindels RJ & Hoenderop JG 2005 The beta-glucuronidase klotho hydrolyzes and activates the TRPV5 channel. Science 310 490–493.
Clapham DE 2003 TRP channels as cellular sensors. Nature 426 517–524.[CrossRef][Medline]
Colbert HA, Smith TL & Bargmann CI 1997 OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. Journal of Neuroscience 17 8259–8269.
Corey DP 2003 New TRP channels in hearing and mechanosensation. Neuron 39 585–588.[CrossRef][ISI][Medline]
Cosens DJ & Manning A 1969 Abnormal electroretinogram from a Drosophila mutant. Nature 224 285–287.[CrossRef][Medline]
Cuajungco MP, Grimm C, Oshima K, D’Hoedt D, Nilius B, Mensenkamp AR, Bindels RJ, Plomann M & Heller S 2006 PACSINs bind to the TRPV4 cation channel. PACSIN 3 modulates the subcellular localization of TRPV4. Journal of Biological Chemistry 281 18753–18762.
Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K et al. 2000 Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405 183–187.[CrossRef][Medline]
den Dekker E, Hoenderop JG, Nilius B & Bindels RJ 2003 The epithelial calcium channels, TRPV5 & TRPV6: from identification towards regulation. Cell Calcium 33 497–507.[CrossRef][ISI][Medline]
Dinis P, Charrua A, Avelino A, Yaqoob M, Bevan S, Nagy I & Cruz F 2004 Anandamide-evoked activation of vanilloid receptor 1 contributes to the development of bladder hyperreflexia and nociceptive transmission to spinal dorsal horn neurons in cystitis. Journal of Neuroscience 24 11253–11263.
Gao X, Wu L & O’Neil RG 2003 Temperature-modulated diversity of TRPV4 channel gating: activation by physical stresses and phorbol ester derivatives through protein kinase C-dependent and -independent pathways. Journal of Biological Chemistry 278 27129–27137.
Gong Z, Son W, Chung YD, Kim J, Shin DW, McClung CA, Lee Y, Lee HW, Chang DJ, Kaang BK et al. 2004 Two interdependent TRPV channel subunits, inactive and Nanchung, mediate hearing in Drosophila. Journal of Neuroscience 24 9059–9066.
Guler AD, Lee H, Iida T, Shimizu I, Tominaga M & Caterina M 2002 Heat-evoked activation of the ion channel, TRPV4. Journal of Neuroscience 22 6408–6414.
Gunthorpe MJ, Benham CD, Randall A & Davis JB 2002 The diversity in the vanilloid (TRPV) receptor family of ion channels. Trends in Pharmacological Sciences 23 183–191.[CrossRef][Medline]
Hardie RC & Minke B 1992 The trp gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors. Neuron 8 643–651.[CrossRef][ISI][Medline]
Hoenderop JG, van der Kemp AW, Hartog A, van de Graaf SF, van Os CH, Willems PH & Bindels RJ 1999 Molecular identification of the apical Ca2+ channel in 1, 25- dihydroxyvitamin D3-responsive epithelia. Journal of Biological Chemistry 274 8375–8378.
Hoenderop JG, Nilius B & Bindels RJ 2003 Epithelial calcium channels: from identification to function and regulation. Pflugers Archiv 446 304–308.[ISI][Medline]
Kanzaki M, Zhang YQ, Mashima H, Li L, Shibata H & Kojima I 1999 Translocation of a calcium-permeable cation channel induced by insulin-like growth factor-I. Nature Cell Biology 1 165–170.[CrossRef][ISI][Medline]
Kaplan JM & Horvitz HR 1993 A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. PNAS 90 2227–2231.
Kim J, Chung YD, Park DY, Choi S, Shin DW, Soh H, Lee HW, Son W, Yim J, Park CS et al. 2003 A TRPV family ion channel required for hearing in Drosophila. Nature 424 81–84.[CrossRef][Medline]
Lazzeri M, Vannucchi MG, Zardo C, Spinelli M, Beneforti P, Turini D & Faussone-Pellegrini MS 2004 Immunohistochemical evidence of vanilloid receptor 1 in normal human urinary bladder. European Urology 46 792–798.[CrossRef][ISI][Medline]
Liedtke W & Friedman JM 2003 Abnormal osmotic regulation in trpv4–/– mice. PNAS 100 13698–13703.
Liedtke W & Kim C 2005 Functionality of the TRPV subfamily of TRP ion channels: add mechano-TRP and osmo-TRP to the lexicon!. Cellular and Molecular Life Sciences 62 2985–3001.[CrossRef][ISI][Medline]
Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS, Sali A, Hudspeth AJ, Friedman JM & Heller S 2000 Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103 525–535.[CrossRef][ISI][Medline]
Liedtke W, Tobin DM, Bargmann CI & Friedman JM 2003 Mammalian TRPV4 (VR-OAC) directs behavioral responses to osmotic and mechanical stimuli in Caenorhabditis elegans. PNAS 100 14531–14536.
Liu X, Bandyopadhyay B, Nakamoto T, Singh B, Liedtke W, Melvin JE & Ambudkar I 2006 A role for AQP5 in activation of TRPV4 by hypotonicity: concerted involvement of AQP5 and TRPV4 in regulation of cell volume recovery. Journal of Biological Chemistry 281 15485–15495.
Mizuno A, Matsumoto N, Imai M & Suzuki M 2003 Impaired osmotic sensation in mice lacking TRPV4. American Journal of Physiology. Cell Physiology 285 C96–C101.
Montell C & Rubin GM 1989 Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for photo-transduction. Neuron 2 1313–1323.[CrossRef][ISI][Medline]
Muraki K, Iwata Y, Katanosaka Y, Ito T, Ohya S, Shigekawa M & Imaizumi Y 2003 TRPV2 is a component of osmotically sensitive cation channels in murine aortic myocytes. Circulation Research 93 829–838.
Mutai H & Heller S 2003 Vertebrate and invertebrate TRPV-like mechanoreceptors. Cell Calcium 33 471–478.[CrossRef][ISI][Medline]
Naeini RS, Witty MF, Seguela P & Bourque CW 2006 An N-terminal variant of Trpv1 channel is required for osmosensory transduction. Nature Neuroscience 9 93–98.[CrossRef][ISI][Medline]
Nagata K, Duggan A, Kumar G & Garcia-Anoveros J 2005 Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. Journal of Neuroscience 25 4052–4061.
Nilius B, Voets T & Peters J 2005 TRP channels in disease. Science’s STKE 2005 re8.
O’Neil RG & Heller S 2005 The mechanosensitive nature of TRPV channels. Pflugers Archiv 451 193–203.[CrossRef][ISI][Medline]
Patapoutian A 2005 Channels and thermosensation. Chemical Senses 30 i193–i194.
Peier AM, Reeve AJ, Andersson DA, Moqrich A, Earley TJ, Hergarden AC, Story GM, Colley S, Hogenesch JB, McIntyre P et al. 2002 A heat-sensitive TRP channel expressed in keratinocytes. Science 296 2046–2049.
Peng JB, Chen XZ, Berger UV, Vassilev PM, Tsukaguchi H, Brown EM & Hediger MA 1999 Molecular cloning and characterization of a channel-like transporter mediating intestinal calcium absorption. Journal of Biological Chemistry 274 22739–22746.
Peng JB, Brown EM & Hediger MA 2003 Epithelial Ca2+ entry channels: transcellular Ca2+ transport and beyond. Journal of Physiology 551 729–740.
Pomonis JD, Harrison JE, Mark L, Bristol DR, Valenzano KJ & Walker K 2003 N-(4-Tertiarybutylphenyl)-4-(3-cholorphyridin-2-yl)tetrahydropyrazine -1(2H)-carboxamide (BCTC), a novel, orally effective vanilloid receptor 1 antagonist with analgesic properties: II. in vivo characterization in rat models of inflammatory and neuropathic pain. Journal of Pharmacology and Experimental Therapeutics 306 387–393.
Rong W, Hillsley K, Davis JB, Hicks G, Winchester WJ & Grundy D 2004 Jejunal afferent nerve sensitivity in wild-type and TRPV1 knockout mice. Journal of Physiology 560 867–881.
Scotland RS, Chauhan S, Davis C, De Felipe C, Hunt S, Kabir J, Kotsonis P, Oh U & Ahluwalia A 2004 Vanilloid receptor TRPV1, sensory C-fibers, and vascular autoregulation: a novel mechanism involved in myogenic constriction. Circulation Research 95 1027–1034.
Sidhaye VK, Guler AD, Schweitzer KS, D’Alessio F, Caterina MJ & King LS 2006 Transient receptor potential vanilloid 4 regulates aquaporin-5 abundance under hypotonic conditions. PNAS 103 4747–4752.
Smith GD, Gunthorpe MJ, Kelsell RE, Hayes PD, Reilly P, Facer P, Wright JE, Jerman JC, Walhin JP, Ooi L et al. 2002 TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature 418 186–190.[CrossRef][Medline]
Sokolchik I, Tanabe T, Baldi PF & Sze JY 2005 Polymodal sensory function of the Caenorhabditis elegans OCR-2 channel arises from distinct intrinsic determinants within the protein and is selectively conserved in mammalian TRPV proteins. Journal of Neuroscience 25 1015–1023.
Stein RJ, Santos S, Nagatomi J, Hayashi Y, Minnery BS, Xavier M, Patel AS, Nelson JB, Futrell WJ, Yoshimura N et al. 2004 Cool (TRPM8) and hot (TRPV1) receptors in the bladder and male genital tract. Journal of Urology 172 1175–1178.[CrossRef][ISI][Medline]
Strotmann R, Harteneck C, Nunnenmacher K, Schultz G & Plant TD 2000 OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nature Cell Biology 2 695–702.[CrossRef][ISI][Medline]
Tobin D, Madsen DM, Kahn-Kirby A, Peckol E, Moulder G, Barstead R, Maricq AV & Bargmann CI 2002 Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35 307–318.[CrossRef][ISI][Medline]
Tominaga M & Caterina MJ 2004 Thermosensation and pain. Journal of Neurobiology 61 3–12.[CrossRef][ISI][Medline]
Voets T, Prenen J, Vriens J, Watanabe H, Janssens A, Wissenbach U, Boedding M, Droogmans G & Nilius B 2002 Molecular determinants of permeation through the cation channel TRPV4. Journal of Biological Chemistry 277 33704–33710.
Vriens J, Owsianik G, Voets T, Droogmans G & Nilius B 2004a Invertebrate TRP proteins as functional models for mammalian channels. Pflugers Archiv 449 213–226.[ISI][Medline]
Vriens J, Watanabe H, Janssens A, Droogmans G, Voets T & Nilius B 2004b Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. PNAS 101 396–401.
Walker RG, Willingham AT & Zuker CS 2000 A Drosophila mechanosensory transduction channel. Science 287 2229–2234.
Watanabe H, Vriens J, Suh SH, Benham CD, Droogmans G & Nilius B 2002 Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. Journal of Biological Chemistry 277 47044–47051.
Wissenbach U, Bodding M, Freichel M & Flockerzi V 2000 Trp12, a novel Trp related protein from kidney. FEBS Letters 485 127–134.[CrossRef][ISI][Medline]
Wong F, Schaefer EL, Roop BC, LaMendola JN, Johnson-Seaton D & Shao D 1989 Proper function of the Drosophila trp gene product during pupal development is important for normal visual transduction in the adult. Neuron 3 81–94.[CrossRef][ISI][Medline]
Xu H, Ramsey IS, Kotecha SA, Moran MM, Chong JA, Lawson D, Ge P, Lilly J, Silos-Santiago I, Xie Y et al. 2002 TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 418 181–186.[CrossRef][Medline]
Xu H, Zhao H, Tian W, Yoshida K, Roullet JB & Cohen DM 2003 Regulation of a transient receptor potential (TRP) channel by tyrosine phosphorylation. SRC family kinase-dependent tyrosine phosphorylation of TRPV4 on TYR-253 mediates its response to hypotonic stress. Journal of Biological Chemistry 278 11520–11527.
Xu H, Fu Y, Tian W & Cohen DM 2006 Glycosylation of the osmoresponsive transient receptor potential channel TRPV4 on Asn-651 influences membrane trafficking. American Journal of Physiology. Renal Physiology 290 1103–1109.
Zhang S, Sokolchik I, Blanco G & Sze JY 2004 Caenorhabditis elegans TRPV ion channel regulates 5HT biosynthesis in chemosensory neurons. Development 131 1629–1638.
Zhu X, Chu PB, Peyton M & Birnbaumer L 1995 Molecular cloning of a widely expressed human homologue for the Drosophila trp gene. FEBS Letters 373 193–198.[CrossRef][ISI][Medline]
Received 7 June 2006
Received in final form 2 August 2006
Accepted 15 August 2006
Made available online as an Accepted Preprint 25 August 2006
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