Functional role of the transient receptor potential melastatin 8 (TRPM8) ion channel in the urinary bladder assessed by conscious cystometry and ex vivo measurements of single-unit mechanosensitive bladder afferent activities in the rat

BJU International

Volumn 117, Issue 3, 2016, Pages 484-494

  Ito, Hiroki ^a   Aizawa, Naoki ^a   Sugiyama, Rino ^a,b   Watanabe, Shuzo ^c   Takahashi, Nobuyuki ^c   Tajimi, Masaomi ^c   Fukuhara, Hiroshi ^a   Homma, Yukio ^a   Kubota, Yoshinobu ^b   Andersson, Karl Erik ^d   Igawa, Yasuhiko ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c RaQualia Pharma Inc   (Japan)

^d AARHUS UNIVERSITY   (Denmark)

Author keywords

afferent; detrusor function; rat; TRPM8 channel

Indexed keywords

MENTHOL; RQ 00203078; TRANSIENT RECEPTOR POTENTIAL CHANNEL AFFECTING AGENT; TRANSIENT RECEPTOR POTENTIAL CHANNEL M8; UNCLASSIFIED DRUG; ION CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL M; TRPM8 PROTEIN, RAT; URINARY TRACT AGENT;

ANIMAL TISSUE; ARTICLE; BLADDER CAPACITY; BLADDER EXAMINATION; BLADDER FILLING; BLADDER FUNCTION; BLADDER PRESSURE; BODY TEMPERATURE; CHANNEL GATING; CONCENTRATION RESPONSE; CYSTOMETRY; DETRUSOR MUSCLE; EX VIVO STUDY; FEMALE; MUSCLE SPINDLE AFFERENT NERVE; NONHUMAN; POSTVOID RESIDUAL URINE VOLUME; PRIORITY JOURNAL; RAT; URINE VOLUME; ANIMAL; BLADDER; DRUG EFFECTS; PHYSIOLOGY; SENSORY NERVE; SPRAGUE DAWLEY RAT;

AFFERENT PATHWAYS; ANIMALS; BODY TEMPERATURE; FEMALE; ION CHANNELS; MENTHOL; RATS, SPRAGUE-DAWLEY; TRPM CATION CHANNELS; URINARY BLADDER; UROLOGICAL AGENTS;

EID: 84959309695     PISSN: 14644096     EISSN: 1464410X     Source Type: Journal    
DOI: 10.1111/bju.13225     Document Type: Article

References (45)

1. Avelino A, Cruz F. TRPV1 (vanilloid receptor) in the urinary tract: expression, function and clinical applications. Naunyn Schmiedebergs Arch Pharmacol 2006; 373: 287-99
2. Caprodossi S, Lucciarini R, Amantini C, et al. Transient receptor potential vanilloid type 2 (TRPV2) expression in normal urothelium and in urothelial carcinoma of human bladder: correlation with the pathologic stage. Eur Urol 2008; 54: 612-20
3. Yamada T, Ugawa S, Ueda T, Ishida Y, Kajita K, Shimada S. Differential localizations of the transient receptor potential channels TRPV4 and TRPV1 in the mouse urinary bladder. J Histochem Cytochem 2009; 57: 277-87
4. Minagawa T, Aizawa N, Igawa Y, Wyndaele JJ. The role of transient receptor potential ankyrin 1 (TRPA1) channel in activation of single unit mechanosensitive bladder afferent activities in the rat. Neurourol Urodyn 2014; 33: 544-9
5. Smith AC, Parajuli SP, Hristov KL, et al. TRPM4 channel: a new player in urinary bladder smooth muscle function in rats. Am J Physiol Renal Physiol 2013; 304: F918-29
6. Yu W, Hill WG, Apodaca G, Zeidel ML. Expression and distribution of transient receptor potential (TRP) channels in bladder epithelium. Am J Physiol Renal Physiol 2011; 300: F49-59
7. Stein RJ, Santos S, Nagatomi J, et al. Cool (TRPM8) and hot (TRPV1) receptors in the bladder and male genital tract. J Urol 2004; 172: 1175-8
8. Apostolidis A, Brady CM, Yiangou Y, Davis J, Fowler CJ, Anand P. Capsaicin receptor TRPV1 in urothelium of neurogenic human bladders and effect of intravesical resiniferatoxin. Urology 2005; 65: 400-5
9. Brady CM, Apostolidis AN, Harper M, et al. Parallel changes in bladder suburothelial vanilloid receptor TRPV1 and pan-neuronal marker PGP9.5 immunoreactivity in patients with neurogenic detrusor overactivity after intravesical resiniferatoxin treatment. BJU Int 2004; 93: 770-6
10. Deruyver Y, Voets T, De Ridder D, Everaerts W. Transient receptor potential channel modulators as pharmacological treatments for lower urinary tract symptoms (LUTS): myth or reality? BJU Int 2015; 115: 686-97
11. Shabir S, Cross W, Kirkwood LA, et al. Functional expression of purinergic P2 receptors and transient receptor potential channels by the human urothelium. Am J Physiol Renal Physiol 2013; 305: F396-406
12. Streng T, Axelsson HE, Hedlund P, et al. Distribution and function of the hydrogen sulfide-sensitive TRPA1 ion channel in rat urinary bladder. Eur Urol 2008; 53: 391-9
13. Gevaert T, Vriens J, Segal A, et al. Deletion of the transient receptor potential cation channel TRPV4 impairs murine bladder voiding. J Clin Invest 2007; 117: 3453-62
14. Franken J, Uvin P, De Ridder D, Voets T. TRP channels in lower urinary tract dysfunction. Br J Pharmacol 2014; 171: 2537-51
15. Skryma R, Prevarskaya N, Gkika D, Shuba Y. From urgency to frequency: facts and controversies of TRPs in the lower urinary tract. Nat Rev Urol 2011; 8: 617-30
16. Avelino A, Charrua A, Frias B, et al. Transient receptor potential channels in bladder function. Acta Physiol (Oxf) 2013; 207: 110-22
17. Peier AM, Moqrich A, Hergarden AC, et al. A TRP channel that senses cold stimuli and menthol. Cell 2002; 108: 705-15
18. Colburn RW, Lubin ML, Stone DJ Jr, et al. Attenuated cold sensitivity in TRPM8 null mice. Neuron 2007; 54: 379-86
19. Dhaka A, Murray AN, Mathur J, Earley TJ, Petrus MJ, Patapoutian A. TRPM8 is required for cold sensation in mice. Neuron 2007; 54: 371-8
20. Bautista DM, Siemens J, Glazer JM, et al. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 2007; 448: 204-8
21. Almaraz L, Manenschijn JA, de la Pena E, Viana F. TRPM8. Handb Exp Pharmacol 2014; 222: 547-79
22. Gardiner JC, Kirkup AJ, Curry J, et al. The role of TRPM8 in the Guinea-pig bladder-cooling reflex investigated using a novel TRPM8 antagonist. Eur J Pharmacol 2014; 740: 398-409
23. Hayashi T, Kondo T, Ishimatsu M, et al. Function and expression pattern of TRPM8 in bladder afferent neurons associated with bladder outlet obstruction in rats. Auton Neurosci 2011; 164: 27-33
24. Jun JH, Kang HJ, Jin MH, et al. Function of the Cold Receptor (TRPM8) Associated with Voiding Dysfunction in Bladder Outlet Obstruction in Rats. Int Neurourol J 2012; 16: 69-76
25. Geirsson G. Evidence of cold receptors in the human bladder: effect of menthol on the bladder cooling reflex. J Urol 1993; 150: 427-30
26. Mukerji G, Waters J, Chessell IP, Bountra C, Agarwal SK, Anand P. Pain during ice water test distinguishes clinical bladder hypersensitivity from overactivity disorders. BMC Urol 2006; 6: 31
27. Ohmi M, Shishido Y, Inoue T, et al. Identification of a novel 2-pyridyl-benzensulfonamide derivative, RQ-00203078, as a selective and orally active TRPM8 antagonist. Bioorg Med Chem Lett 2014; 24: 5364-8
28. Andersson DA, Chase HW, Bevan S. TRPM8 activation by menthol, icilin, and cold is differentially modulated by intracellular pH. J Neurosci 2004; 24: 5364-9
29. Igawa Y, Kumano S, Aizawa N, et al. Changes in the function and expression of T-type and N-type calcium channels in the rat bladder after bladder outlet obstruction. J Urol 2014; 191: 1159-67
30. Severinsen T, Munch IC. Body core temperature during food restriction in rats. Acta Physiol Scand 1999; 165: 299-305
31. Almeida MC, Hew-Butler T, Soriano RN, et al. Pharmacological blockade of the cold receptor TRPM8 attenuates autonomic and behavioral cold defenses and decreases deep body temperature. J Neurosci 2012; 32: 2086-99
32. Aizawa N, Igawa Y, Nishizawa O, Wyndaele JJ. Effects of CL316,243, a beta 3-adrenoceptor agonist, and intravesical prostaglandin E2 on the primary bladder afferent activity of the rat. Neurourol Urodyn 2010; 29: 771-6
33. Nomoto Y, Yoshida A, Ikeda S, et al. Effect of menthol on detrusor smooth-muscle contraction and the micturition reflex in rats. Urology 2008; 72: 701-5
34. Karashima Y, Damann N, Prenen J, et al. Bimodal action of menthol on the transient receptor potential channel TRPA1. J Neurosci 2007; 27: 9874-84
35. Lashinger ES, Steiginga MS, Hieble JP, et al. AMTB, a TRPM8 channel blocker: evidence in rats for activity in overactive bladder and painful bladder syndrome. Am J Physiol Renal Physiol 2008; 295: F803-10
36. Hills JM, Aaronson PI. The mechanism of action of peppermint oil on gastrointestinal smooth muscle. An analysis using patch clamp electrophysiology and isolated tissue pharmacology in rabbit and guinea pig. Gastroenterology 1991; 101: 55-65
37. Ramos-Filho AC, Shah A, Augusto TM, et al. Menthol inhibits detrusor contractility independently of TRPM8 activation. PLoS ONE 2014; 9: e111616
38. Malkia A, Morenilla-Palao C, Viana F. The emerging pharmacology of TRPM8 channels: hidden therapeutic potential underneath a cold surface. Curr Pharm Biotechnol 2011; 12: 54-67
39. Sherkheli MA, Vogt-Eisele AK, Bura D, Beltran ML, Gisselmann G, Hatt H. Characterization of selective TRPM8 ligands and their structure activity response (S.A.R) relationship. J Pharm Pharm Sci 2010; 13: 242-53.
40. Habler HJ, Janig W, Koltzenburg M. Activation of unmyelinated afferent fibres by mechanical stimuli and inflammation of the urinary bladder in the cat. J Physiol 1990; 425: 545-62
41. Aizawa N, Igawa Y, Nishizawa O, Wyndaele JJ. Effects of nitric oxide on the primary bladder afferent activities of the rat with and without intravesical acrolein treatment. Eur Urol 2011; 59: 264-71
42. Chen Z, Ishizuka O, Imamura T, et al. Stimulation of skin menthol receptors stimulates detrusor activity in conscious rats. Neurourol Urodyn 2010; 29: 506-11
43. Uvin P, Franken J, Pinto S, et al. Essential role of Transient Receptor Potential M8 (TRPM8) in a model of acute cold-induced urinary urgency. Eur Urol 2015; [Epub ahead of print]. DOI: 10.1016/j.eururo.2015.03.037.
44. Shibata Y, Ugawa S, Imura M, et al. TRPM8-expressing dorsal root ganglion neurons project dichotomizing axons to both skin and bladder in rats. Neuroreport 2011; 22: 61-7
45. Everaerts W, Vriens J, Owsianik G, et al. Functional characterization of transient receptor potential channels in mouse urothelial cells. Am J Physiol Renal Physiol 2010; 298: F692-701