Urothelial lysosomal dysfunction causes bladder hyperactivity and inflammation

Rodriguez R1, Phipps S1, Obidike C1, Daugherty S1, Beckel J1

Research Type

Pure and Applied Science / Translational

Abstract Category

Pelvic Pain Syndromes

Abstract 373
Sensory Function and Fibrosis
Scientific Podium Short Oral Session 24
On-Demand
Painful Bladder Syndrome/Interstitial Cystitis (IC) Molecular Biology Urgency/Frequency Voiding Dysfunction Overactive Bladder
1. University of Pittsburgh, PA USA
Presenter
Links

Abstract

Hypothesis / aims of study
It is well known that the prevalence of bladder pathology increases with age.  For example, increased age is associated with a decrease in bladder capacity, increased bladder sensations, and increases in urinary concentrations of ATP and other pro-inflammatory mediators.  These changes can lead to a clinical manifestation of bladder pathologies such as overactive bladder (OAB) and bladder pain syndrome/interstitial cystitis (BPS/IC), with symptoms such as urgency, frequency and pain.  However, little is known about the cellular mechanisms that drive these pathological changes with age.

One possibility may be defects in the endolysosomal pathway of the urothelium.  It is known that lysosomal function diminishes with age, especially in post-mitotic cells such as differentiated epithelia.  This can lead to a buildup of undigested cellular material and damaged intracellular organelles, leading to disrupted cellular function.  A previous study demonstrated that aged rats (~26 months old) exhibited a marked increase in endolysosomal volume with a concurrent increase in endolysosomal pH [1]. As the function of the lysosome is directly tied to the acidic nature of its luminal pH, cathepsin B activity was also decreased. Additionally, it has been recently demonstrated that the lysosome acts as a significant store of ATP in the urothelium, and that stimulation of urothelial cells with agents such as bacterial lipopolysaccharides (LPS) can induce ATP release through lysosomal exocytosis.  This has led us to hypothesize that defects in lysosomal function may play a role in bladder dysfunction and that increasing lysosomal pH artificially may result in bladder hyperactivity and inflammation in rats.  Thus, alkalization of urothelial lysosomal pH may represent a new model for BPS/IC.
Study design, materials and methods
To increase lysosomal pH, we used chloroquine (CHQ), a lysosomotropic weak base which has been shown to collect in lysosomes.  Once inside the lysosome, chloroquine becomes protonated, preventing it from leaving the lysosome and decreasing lysosomal pH.  To demonstrate the importance of the lysosome to a given effect, we used Gly-Phe β-naphthylamide (GPN), another agent that collects preferentially into lysosomes, where it is cleaved by cathepsin C.  The cleavage product of GPN collects in the lysosome, creating an osmotic gradient that causes the lysosome to swell and eventually lyse.

The cell-based portion of our study used immortalized normal human urothelial cells (TRT-HU1) at passage number 25-35. Cells were used for experiments after 1-2 days when they had reached 50-70% confluency.

To measure extracellular ATP concentrations, TRT-HU1 cells were grown in white-walled 96-well plates.  First, the media supporting the cells was first replaced with 50µl of Krebs solution alone or containing GPN (20µM, 2X final concentration) and incubated at 37°C for 20 minutes.  50µl of Krebs (for non-stimulated controls) or CHQ (200µM, 2X final concentration) was then added and the plate incubated again for 30 minutes at 37°C.  50µl of the luciferin/luciferase assay mix (Sigma-Aldrich) was then added and the luminescence measured using a plate-based luminometer.  Luminescence readings were converted to ATP concentrations using a standard curve with known concentrations of ATP.

To measure lysosomal pH, TRT-Cells were grown in black-walled 96-well plates.  At the time of the experiment, the media was removed and replaced with 50µl of either Krebs solution alone (control) or CHQ (100µM).  After a 30-minute incubation, the extracellular solution was aspirated and the cells incubated with 5 μM LysoSensor Yellow/Blue DND 160 (Invitrogen) for 3 min followed by a 15 min post-incubation in Krebs solution. Lysosomal pH was determined from the ratio of light emitted at 450 nm vs. 510 nm (365 nm ex) using a plate reader (Tecan Spark 20M) and calibrated by exposing cells to 10μM monensin and 20 μM nigericin in a solution containing (in mM) 20 MES, 110 KCl and 20 NaCl at pH 4.0–6.0 for 15 min.

Extracellular IL-1β concentrations were measured using a commercially available ELISA kit (Abcam). Briefly, TRT-HU1 cells, grown on 35mm dishes, were stimulated with CHQ (100µM in Krebs solution) for 2 hours.  To measure IL-1β, 100µl samples of the extracellular solution was used in triplicate according to the manufacturer’s instructions.  

For our in vivo experiments, female Sprague-Dawley rats (~200-250g) were anesthetized using isoflurane and CHQ (100µM in sterile saline, 0.5ml) was instilled in the bladder through a transurethral catheter for 1 hour.  The animals were then used immediately for cystometry or plasma extravasation or allowed to recover for experiments one or three days later. For cystometry, the rats were anesthetized with urethane and catheterized through the bladder dome. Open cystometry was then performed by perfusing Krebs solution into the bladder at a rate of 0.08ml/min.  For plasma extravasation, rats were anesthetized using urethane, and Evans Blue (50mg/kg) was injected through a jugular vein catheter. Fifteen minutes after dye injection, the rats were sacrificed by decapitation, exsanguinated and the bladder removed. After weighing, the bladder was placed in 3 ml formamide for 72 hours.  The dye present in the formamide solution was quantified by measuring optical density and then the concentration was estimated using a standard curve.  

For bladder strip experiments, bladders were removed from female Sprague Dawley rats, cut into strips longitudinally, and attached to a force displacement transducer in a tissue bath containing oxygenated Krebs solution at 37°C.  Agonists and antagonists were bath applied and changes in basal tone and spontaneous contraction amplitude recorded.
Results
Stimulation of TRT-HU1 urothelial cells with CHQ (100µM) increased lysosomal pH from 4.5 to 5.0 and increased extracellular ATP concentrations by 13.6%, which was prevented after pre-incubation with GPN.  Extracellular concentrations of the pro-inflammatory cytokine IL-1β were also increased following CHQ treatment.  During in vitro rat bladder strip experiments, CHQ increased the area of spontaneous detrusor contractions by 30.1% one hour after application.  This increase was also blocked by GPN pre-treatment.  Intravesical instillation of CHQ during cystometry in anesthetized rats showed a small increase in voiding frequency after 2 hours (~25%).  This increase in voiding frequency was greater 24 or 72 hours after CHQ treatment. Plasma extravasation in these animals also showed a time dependent increase in bladder edema, with a maximum increase after 72 hours (~10-fold).
Interpretation of results
Our results demonstrate that alkalization of urothelial lysosomes using chloroquine can induce bladder hyperactivity and inflammation, as demonstrated by increased spontaneous detrusor contractions, increased voiding frequency and increased plasma extravasation in the bladder.  The mechanism of these effects most likely includes the release of ATP through lysosomal exocytosis and release of pro-inflammatory cytokines such as IL-1β.  This suggests that urothelial lysosomal dysfunction may be a plausible etiology for bladder pathology, especially in the aged where lysosomal dysfunction is more common.
Concluding message
Our study indicates that urothelial lysosomal dysfunction may be a plausible etiology for inflammatory bladder disorders such as BPS/IC, especially in the aged population where lysosomal dysfunction is more common.  The effects of one intravesical treatment of chloroquine are long lasting; inducing bladder hyperactivity and inflammation that lasts for at least 3 days.  This makes intravesical chloroquine instillation an easy method for inducing lysosomal dysfunction and may serve as an excellent animal model for BPS/IC.
References
  1. Truschel ST, Clayton DR, Beckel JM, et al. Age-related endolysosome dysfunction in the rat urothelium. PLoS One. 2018;13(6):e0198817. Published 2018 Jun 8. doi:10.1371/journal.pone.0198817
Disclosures
Funding NIH: DK114492 and DK117884 Clinical Trial No Subjects Animal Species Rat Ethics Committee University of Pittsburgh Institutional Animal Care and Use Committee (IACUC)
20/11/2024 00:51:56