Impaired M3 and enhanced M2 muscarinic receptor contractile function in a streptozotocin model of mouse diabetic urinary bladder

Naunyn-Schmiedeberg's Archives of Pharmacology

Volumn 381, Issue 5, 2010, Pages 441-454

  Pak, K J ^a   Ostrom, R S ^b   Matsui, M ^c   Ehlert, F J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c Tokyo west Tokushukai Hospital   (Japan)

Author keywords

Contraction; Diabetes; M2 muscarinic receptor; Smooth muscle; Streptozotocin; Urinary bladder

Indexed keywords

FORSKOLIN; MUSCARINIC AGENT; MUSCARINIC M2 RECEPTOR; MUSCARINIC M3 RECEPTOR; OXOTREMORINE M; POTASSIUM CHLORIDE; DRUG DERIVATIVE; OXOTREMORINE; STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLADDER CONTRACTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; KNOCKOUT MOUSE; MOUSE; NONHUMAN; SMOOTH MUSCLE RELAXATION; STREPTOZOCIN DIABETES; UROTHELIUM; WILD TYPE; ANIMAL; BLADDER; C57BL MOUSE; DISEASE MODEL; DRUG EFFECT; EXPERIMENTAL DIABETES MELLITUS; GENETICS; MALE; METABOLISM; MOUSE MUTANT; MUSCLE CONTRACTION; PATHOPHYSIOLOGY; TIME;

ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; FORSKOLIN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCARINIC AGONISTS; MUSCLE CONTRACTION; OXOTREMORINE; RECEPTOR, MUSCARINIC M2; RECEPTOR, MUSCARINIC M3; STREPTOZOCIN; TIME FACTORS; URINARY BLADDER;

EID: 77953232473     PISSN: 00281298     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00210-010-0509-6     Document Type: Article

References (61)

1. LA Birder WC de Groat 2007 Mechanisms of disease: involvement of the urothelium in bladder dysfunction Nat Clin Pract Urol 4 46 54 10.1038/ncpuro0672 1:CAS:528:DC%2BD2sXhsVSku74%3D 17211425 (Pubitemid 46062986)
2. LA Birder ML Nealen S Kiss WC de Groat MJ Caterina E Wang G Apodaca AJ Kanai 2002 Beta-adrenoceptor agonists stimulate endothelial nitric oxide synthase in rat urinary bladder urothelial cells J Neurosci 22 8063 8070 1:CAS:528:DC%2BD38Xnt12kt74%3D 12223560
3. JW Black P Leff 1983 Operational models of pharmacological agonism Proc R Soc Lond B Biol Sci 220 141 162 10.1098/rspb.1983.0093 1:CAS:528: DyaL2cXmtFaqtA%3D%3D 6141562
4. GT Bolger P Gengo R Klockowski E Luchowski H Siegel RA Janis AM Triggle DJ Triggle 1983 Characterization of binding of the Ca++ channel antagonist, [3H]nitrendipine, to guinea-pig ileal smooth muscle J Pharmacol Exp Ther 225 291 309 1:CAS:528:DyaL3sXksVOmtrg%3D 6842393
5. TB Bolton 1979 Mechanisms of action of transmitters and other substances on smooth muscle Physiol Rev 59 606 718 1:CAS:528:DyaE1MXkvVelt78%3D 37533
6. AS Braverman MR Ruggieri Sr 2003 Hypertrophy changes the muscarinic receptor subtype mediating bladder contraction from M3 toward M2 Am J Physiol Regul Integr Comp Physiol 285 R701 R708 12763741
7. AS Braverman GR Luthin MR Ruggieri 1998 M2 muscarinic receptor contributes to contraction of the denervated rat urinary bladder Am J Physiol 275 R1654 R1660 1:CAS:528:DyaK1cXnsF2msrY%3D 9791087
8. A Braverman J Legos W Young G Luthin M Ruggieri 1999 M2 receptors in genito-urinary smooth muscle pathology Life Sci 64 429 436 10.1016/S0024- 3205(98)00582-7 1:CAS:528:DyaK1MXoslajtw%3D%3D 10069506 (Pubitemid 29066689)
9. T Bschleipfer K Schukowski W Weidner SA Grando U Schwantes W Kummer KS Lips 2007 Expression and distribution of cholinergic receptors in the human urothelium Life Sci 80 2303 2307 10.1016/j.lfs.2007.01.053 1:CAS:528: DC%2BD2sXmtVeht7c%3D 17335853 (Pubitemid 46818274)
10. J-T Cheng B-C Yu Y-C Tong 2007 Changes of M3-muscarinic receptor protein and mRNA expressions in the bladder urothelium and muscle layer of streptozotocin-induced diabetic rats Neurosci Lett 423 1 5 10.1016/j.neulet. 2007.05.062 1:CAS:528:DC%2BD2sXosFKlt7w%3D 17630213 (Pubitemid 47176777)
11. WC Cole KM Sanders 1989 G proteins mediate suppression of Ca2+-activated K current by acetylcholine in smooth muscle cells Am J Physiol 257 C596 C600 1:CAS:528:DyaL1MXlvVyjtb8%3D 2506760
12. WC de Groat N Yoshimura 2001 Pharmacology of the lower urinary tract Annu Rev Pharmacol Toxicol 41 691 721 10.1146/annurev.pharmtox.41.1.691 11264473 (Pubitemid 32385903)
13. FJ Ehlert 2003 Pharmacological analysis of the contractile role of M2 and M3 muscarinic receptors in smooth muscle Receptors Channels 9 261 277 10.1080/10606820308265 1:CAS:528:DC%2BD3sXmtVelsbk%3D 12893538 (Pubitemid 37069447)
14. FJ Ehlert 2003 Contractile role of M2 and M3 muscarinic receptors in gastrointestinal, airway and urinary bladder smooth muscle Life Sci 74 355 366 10.1016/j.lfs.2003.09.023 1:CAS:528:DC%2BD3sXos12qtLk%3D 14607264 (Pubitemid 37357066)
15. FJ Ehlert MT Griffin DM Abe TH Vo MM Taketo T Manabe M Matsui 2005 The M2 muscarinic receptor mediates contraction through indirect mechanisms in mouse urinary bladder J Pharmacol Exp Ther 313 368 378 10.1124/jpet.104.077909 1:CAS:528:DC%2BD2MXjtlSntrg%3D 15608083 (Pubitemid 40411363)
16. FJ Ehlert S Ahn KJ Pak GJ Park MS Sangnil JA Tran M Matsui 2007 Neuronally released acetylcholine acts on the m2 muscarinic receptor to oppose the relaxant effect of isoproterenol on cholinergic contractions in mouse urinary bladder J Pharmacol Exp Ther 322 631 637 10.1124/jpet.107.121756 1:CAS:528:DC%2BD2sXoslSjtbw%3D 17473176 (Pubitemid 47105792)
17. D Gautam S-J Han FF Hamdan J Jeon B Li JH Li Y Cui D Mears H Lu C Deng T Heard J Wess 2006 A critical role for [beta] cell M3 muscarinic acetylcholine receptors in regulating insulin release and blood glucose homeostasis in vivo Cell Metabolism 3 449 461 10.1016/j.cmet.2006.04.009 1:CAS:528: DC%2BD28Xmt1eku7k%3D 16753580 (Pubitemid 43811775)
18. MT Griffin M Matsui RS Ostrom FJ Ehlert 2009 The guinea pig ileum lacks the direct, high-potency, M(2)-muscarinic, contractile mechanism characteristic of the mouse ileum Naunyn Schmiedebergs Arch Pharmacol 380 327 335 10.1007/s00210-009-0434-8 1:CAS:528:DC%2BD1MXhtFOitbbI 19582435
19. MH Hawthorn CR Chapple M Cock R Chess-Williams 2000 Urothelium-derived inhibitory factor(s) influences on detrusor muscle contractility in vitro Br J Pharmacol 129 416 419 10.1038/sj.bjp.0703068 1:CAS:528:DC%2BD3cXht1ynsLY%3D 10711338
20. SS Hegde RM Eglen 1999 Muscarinic receptor subtypes modulating smooth muscle contractility in the urinary bladder Life Sci 64 419 428 10.1016/S0024-3205(98)00581-5 1:CAS:528:DyaK1MXoslWqtw%3D%3D 10069505 (Pubitemid 29066688)
21. SS Hegde A Choppin D Bonhaus S Briaud M Loeb TM Moy D Loury RM Eglen 1997 Functional role of M2 and M3 muscarinic receptors in the urinary bladder of rats in vitro and in vivo Br J Pharmacol 120 1409 1418 10.1038/sj.bjp.0701048 1:CAS:528:DyaK2sXjtVGrsr8%3D 9113359
22. Inoue R (1991) Ion channels involved in responses to muscarinic receptor activation in smooth muscle. In: Sperelakis HKN (ed) Ion channels of vascular smooth muscle cells and endothelial cells. Elsevier Science Publishing Co., Inc, New York, pp 81-91
23. R Inoue G Isenberg 1990 Acetylcholine activates nonselective cation channels in guinea pig ileum through a G protein Am J Physiol 258 C1173 C1178 1:CAS:528:DyaK3cXkslWksbw%3D 1694399
24. T Kitazawa R Hirama K Masunaga T Nakamura K Asakawa J Cao H Teraoka T Unno S Komori M Yamada J Wess T Taneike 2008 Muscarinic receptor subtypes involved in carbachol-induced contraction of mouse uterine smooth muscle Naunyn Schmiedebergs Arch Pharmacol 377 503 513 10.1007/s00210-007-0223-1 1:CAS:528:DC%2BD1cXnsVSqtLg%3D 18071676
25. MG Kolta LJ Wallace MC Gerald 1985 Streptozocin-induced diabetes affects rat urinary bladder response to autonomic agents Diabetes 34 917 921 10.2337/diabetes.34.9.917 1:CAS:528:DyaL2MXlsFyntbc%3D 4029511
26. M Kosan G Hafez B Ozturk O Ozgunes S Gur M Cetinkaya 2005 Effect of urothelium on bladder contractility in diabetic rats Int J Urol 12 677 682 10.1111/j.1442-2042.2005.01098.x 16045562 (Pubitemid 41725495)
27. H Kume K Mikawa K Takagi MI Kotlikoff 1995 Role of G proteins and KCa channels in the muscarinic and beta-adrenergic regulation of airway smooth muscle Am J Physiol 268 L221 L229 1:CAS:528:DyaK2MXktFGnur0%3D 7864143
28. J Latifpour A Gousse S Kondo T Morita RM Weiss 1989 Effects of experimental diabetes on biochemical and functional characteristics of bladder muscarinic receptors J Pharmacol Exp Ther 248 81 88 1:CAS:528:DyaL1MXhsFaitrk%3D 2913290
29. J Lincoln M Crockett AJ Haven G Burnstock 1984 Rat bladder in the early stages of streptozotocin-induced diabetes: adrenergic and cholinergic innervation Diabetologia 26 81 87 1:CAS:528:DyaL2cXhtFyqsr8%3D 6231206 (Pubitemid 14182356)
30. PA Longhurst JA Belis 1986 Abnormalities of rat bladder contractility in streptozotocin-induced diabetes mellitus J Pharmacol Exp Ther 238 773 777 1:STN:280:DyaL28zgslGhsw%3D%3D 3746663
31. M Matsui D Motomura H Karasawa T Fujikawa J Jiang Y Komiya S Takahashi MM Taketo 2000 Multiple functional defects in peripheral autonomic organs in mice lacking muscarinic acetylcholine receptor gene for the M3 subtype Proc Natl Acad Sci USA 97 9579 9584 10.1073/pnas.97.17.9579 1:CAS:528:DC%2BD3cXmtVensbY%3D 10944224
32. M Matsui D Motomura T Fujikawa J Jiang S Takahashi T Manabe MM Taketo 2002 Mice lacking M2 and M3 muscarinic acetylcholine receptors are devoid of cholinergic smooth muscle contractions but still viable J Neurosci 22 10627 10632 1:CAS:528:DC%2BD38XpslCqsb0%3D 12486155
33. M Matsui MT Griffin D Shehnaz MM Taketo FJ Ehlert 2003 Increased relaxant action of forskolin and isoproterenol against muscarinic agonist-induced contractions in smooth muscle from M2 receptor knockout mice J Pharmacol Exp Ther 305 106 113 10.1124/jpet.102.044701 1:CAS:528:DC%2BD3sXis1antbo%3D 12649358 (Pubitemid 36373840)
34. MC Michel MM Barendrecht 2008 Physiological and pathological regulation of the autonomic control of urinary bladder contractility Pharmacol Ther 117 297 312 10.1016/j.pharmthera.2007.12.001 1:CAS:528:DC%2BD1cXisVWit7k%3D 18221785
35. H Mimata MA Wheeler Y Fukomoto H Takigawa T Nishimoto RM Weiss J Latifpour 1995 Enhancement of muscarinic receptor-coupled phosphatidylinositol hydrolysis in diabetic bladder Mol Cell Biochem 152 71 76 1:CAS:528: DyaK2MXpvVWlsb4%3D 8609914
36. ME Molitch RA DeFronzo MJ Franz WF Keane CE Mogensen HH Parving MW Steffes 2004 Nephropathy in diabetes Diabetes Care 27 Suppl 1 S79 S83 14693934
37. Motulsky H, Christopoulos A (2003) Fitting models to biological data using linear and nonlinear regression. GraphPad Software, Inc, San Diego
38. T Nakamura J Kimura O Yamaguchi 2002 Muscarinic M2 receptors inhibit Ca2+-activated K+channels in rat bladder smooth muscle Int J Urol 9 689 696 10.1046/j.1442-2042.2002.00548.x 1:CAS:528:DC%2BD3sXhs12jurk%3D 12492954
39. L Noronha-Blob V Lowe A Patton B Canning D Costello WJ Kinnier 1989 Muscarinic receptors: relationships among phosphoinositide breakdown, adenylate cyclase inhibition, in vitro detrusor muscle contractions and in vivo cystometrogram studies in guinea pig bladder J Pharmacol Exp Ther 249 843 851 1:CAS:528:DyaL1MXksFWjtbg%3D 2543813
40. AM Nsabimana JA Ojewole 2008 Diabetes mellitus and responses of the urinary bladder to acetylcholine: an in vitro study J Smooth Muscle Res 44 143 150 10.1540/jsmr.44.143 18832790
41. RS Ostrom FJ Ehlert 1997 M2 muscarinic receptor inhibition of agonist-induced cyclic adenosine monophosphate accumulation and relaxation in the guinea pig ileum J Pharmacol Exp Ther 280 189 199 1:CAS:528: DyaK2sXntFWmug%3D%3D 8996196
42. RS Ostrom FJ Ehlert 1998 M2 muscarinic receptors inhibit forskolin-but not isoproterenol-mediated relaxation in bovine tracheal smooth muscle J Pharmacol Exp Ther 286 234 242 1:CAS:528:DyaK1cXksFChu7Y%3D 9655865
43. MA Pontari AS Braverman MR Ruggieri Sr 2004 The M2 muscarinic receptor mediates in vitro bladder contractions from patients with neurogenic bladder dysfunction Am J Physiol Regul Integr Comp Physiol 286 R874 R880 1:CAS:528:DC%2BD2cXkt1enurc%3D 14751843
44. MR Ruggieri Sr AS Braverman 2006 Regulation of bladder muscarinic receptor subtypes by experimental pathologies Auton Autacoid Pharmacol 26 311 325 10.1111/j.1474-8673.2006.00377.x 1:CAS:528:DC%2BD28Xot1OrsL8%3D 16879497 (Pubitemid 43898629)
45. T Sakamoto T Unno T Kitazawa T Taneike M Yamada J Wess M Nishimura S Komori 2007 Three distinct muscarinic signalling pathways for cationic channel activation in mouse gut smooth muscle cells J Physiol 582 41 61 10.1113/jphysiol.2007.133165 1:CAS:528:DC%2BD2sXotFamu7Y%3D 17463038 (Pubitemid 46993560)
46. GW Sawyer FJ Ehlert 1999 Muscarinic M3 receptor inactivation reveals a pertussis toxin-sensitive contractile response in the guinea pig colon: evidence for M2/M3 receptor interactions J Pharmacol Exp Ther 289 464 476 1:CAS:528:DyaK1MXit1Khtbs%3D 10087039
47. PW Stengel M Yamada J Wess ML Cohen 2002 M(3)-receptor knockout mice: muscarinic receptor function in atria, stomach fundus, urinary bladder, and trachea Am J Physiol Regul Integr Comp Physiol 282 R1443 R1449 1:CAS:528:DC%2BD38XjslWmu7g%3D 11959688
48. LA Stevens DJ Sellers NG McKay CR Chapple R Chess-Williams 2006 Muscarinic receptor function, density and G-protein coupling in the overactive diabetic rat bladder Auton Autacoid Pharmacol 26 303 309 10.1111/j.1474-8673. 2006.00371.x 1:CAS:528:DC%2BD28Xot1OrsL4%3D 16879496 (Pubitemid 43898628)
49. YC Tay Y Wang L Kairaitis GK Rangan C Zhang DC Harris 2005 Can murine diabetic nephropathy be separated from superimposed acute renal failure? Kidney Int 68 391 398 10.1111/j.1523-1755.2005.00405.x 15954931 (Pubitemid 43181399)
50. GH Tesch TJ Allen 2007 Rodent models of streptozotocin-induced diabetic nephropathy Nephrology (Carlton) 12 261 266 10.1111/j.1440-1797.2007.00796.x (Pubitemid 46718209)
51. GH Tesch DJ Nikolic-Paterson 2006 Recent insights into experimental mouse models of diabetic nephropathy Nephron Exp Nephrol 104 e57 e62 10.1159/000093998 16785742 (Pubitemid 44450472)
52. EA Thomas FJ Ehlert 1994 Pertussis toxin blocks M2 muscarinic receptor-mediated effects on contraction and cyclic AMP in the guinea pig ileum, but not M3-mediated contractions and phosphoinositide hydrolysis J Pharmacol Exp Ther 271 1042 1050 1:CAS:528:DyaK2MXisVyjsLo%3D 7965766
53. EA Thomas SA Baker FJ Ehlert 1993 Functional role for the M2 muscarinic receptor in smooth muscle of guinea pig ileum Mol Pharmacol 44 102 110 1:CAS:528:DyaK3sXlslClsLo%3D 8393516
54. YC Tong JT Cheng 2002 Alteration of M(3) subtype muscarinic receptors in the diabetic rat urinary bladder Pharmacology 64 148 151 10.1159/000056164 1:CAS:528:DC%2BD38XhtVCnsbk%3D 11834891 (Pubitemid 34136856)
55. YC Tong WT Chin JT Cheng 1999 Alterations in urinary bladder M2-muscarinic receptor protein and mRNA in 2-week streptozotocin-induced diabetic rats Neurosci Lett 277 173 176 10.1016/S0304-3940(99)00871-X 1:CAS:528:DyaK1MXnvFentbg%3D 10626841
56. YC Tong JT Cheng WC Wan 2002 Effects of Ba-Wei-Die-Huang-Wan on the cholinergic function and protein expression of M2 muscarinic receptor of the urinary bladder in diabetic rats Neurosci Lett 330 21 24 10.1016/S0304-3940(02) 00713-9 1:CAS:528:DC%2BD38Xms1yhu7Y%3D 12213625 (Pubitemid 35245760)
57. YC Tong WT Chin JT Cheng 2002 Role of sorbitol in the up-regulation of urinary bladder M(2) muscarinic receptors in streptozotocin-induced diabetic rats Neurourol Urodyn 21 154 159 10.1002/nau.10028 1:CAS:528: DC%2BD38XisFOmsbg%3D 11857669 (Pubitemid 34195209)
58. Y-C Tong J-T Cheng C-T Hsu 2006 Alterations of M2-muscarinic receptor protein and mRNA expression in the urothelium and muscle layer of the streptozotocin-induced diabetic rat urinary bladder Neurosci Lett 406 216 221 10.1016/j.neulet.2006.07.065 1:CAS:528:DC%2BD28XpsVOms7k%3D 16935418 (Pubitemid 44311373)
59. JA Tran M Matsui FJ Ehlert 2006 Differential coupling of muscarinic M1, M2, and M3 receptors to phosphoinositide hydrolysis in urinary bladder and longitudinal muscle of the ileum of the mouse J Pharmacol Exp Ther 318 649 656 10.1124/jpet.106.103093 1:CAS:528:DC%2BD28XnslOlsb8%3D 16675640 (Pubitemid 44063465)
60. GR Wade SM Sims 1993 Muscarinic stimulation of tracheal smooth muscle cells activates large-conductance Ca(2+)-dependent K+channel Am J Physiol 265 C658 C665 1:CAS:528:DyaK3sXms1eitbY%3D 8214022
61. Y Wakabayashi Y Kojima Y Makiura T Tomoyoshi T Maeda 1995 Acetylcholinesterase-positive afferent axons in mucosa of urinary bladder of adult cats: retrograde tracing and degeneration studies Histol Histopathol 10 523 530 1:STN:280:DyaK28%2FjtFWjtQ%3D%3D 7579800