Signalling to contractile proteins by muscarinic and purinergic pathways in neurally stimulated bladder smooth muscle

Journal of Physiology

Volumn 590, Issue 20, 2012, Pages 5107-5121

  Tsai, Ming Ho ^a   Kamm, Kristine E ^a   Stull, James T ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA,BETA METHYLENEADENOSINE TRIPHOSPHATE; ATROPINE; CALCIUM ION; CONTRACTILE PROTEIN; CPI 17; ESTERASE INHIBITOR; MUSCARINIC RECEPTOR; MYOSIN; MYOSIN LIGHT CHAIN KINASE; MYOSIN LIGHT CHAIN PHOSPHATASE; MYOSIN REGULATORY LIGHT CHAIN; PROTEIN MYPT1; PURINERGIC RECEPTOR; SURAMIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BLADDER CONTRACTION; BLADDER MUSCLE; CALCIUM SIGNALING; CONTROLLED STUDY; DESENSITIZATION; ELECTRIC FIELD; ENZYME ACTIVATION; ENZYME ANALYSIS; MOUSE; MUSCLE EXCITATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

EID: 84867479200     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.235424     Document Type: Article

References (63)

1. Abrams P, Andersson KE, Buccafusco JJ, Chapple C, de Groat WC, Fryer AD, Kay G, Laties A, Nathanson NM, Pasricha PJ & Wein AJ (2006). Muscarinic receptors: their distribution and function in body systems, and the implications for treating overactive bladder. Br J Pharmacol 148, 565-578.
2. Aita Y, Kurebayashi N, Hirose S & Maturana AD (2011). Protein kinase D regulates the human cardiac L-type voltage-gated calcium channel through serine 1884. FEBS Lett 585, 3903-3906.
3. Andersson KE & Arner A (2004). Urinary bladder contraction and relaxation: physiology and pathophysiology. Physiol Rev 84, 935-986.
4. Brading AF & Mostwin JL (1989). Electrical and mechanical responses of guinea-pig bladder muscle to nerve stimulation. Br J Pharmacol 98, 1083-1090.
5. Brading AF & Williams JH (1990). Contractile responses of smooth muscle strips from rat and guinea-pig urinary bladder to transmural stimulation: effects of atropine and alpha, beta-methylene ATP. Br J Pharmacol 99, 493-498.
6. Caulfield MP & Birdsall NJ (1998). International Union of Pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol Rev 50, 279-290.
7. Colburn JC, Michnoff CH, Hsu LC, Slaughter CA, Kamm KE & Stull JT (1988). Sites phosphorylated in myosin light chain in contracting smooth muscle. J Biol Chem 263, 19166-19173.
8. Ding HL, Ryder JW, Stull JT & Kamm KE (2009). Signaling processes for initiating smooth muscle contraction upon neural stimulation. J Biol Chem 284, 15541-15548.
9. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
10. Durlu-Kandilci NT & Brading AF (2006). Involvement of Rho kinase and protein kinase C in carbachol-induced calcium sensitization in β-escin skinned rat and guinea-pig bladders. Br J Pharmacol 148, 376-384.
11. Felder CC (1995). Muscarinic acetylcholine receptors: signal transduction through multiple effectors. FASEB J 9, 619-625.
12. Fleichman M, Schneider T, Fetscher C & Michel MC (2004). Signal transduction underlying carbachol-induced contraction of rat urinary bladder. II. Protein kinases. J Pharmacol Exp Ther 308, 54-58.
13. 2+ signals in murine urinary bladder smooth muscle. Eur J Pharmacol 610, 106-109.
14. Fry CH, Meng E & Young JS (2010). The physiological function of lower urinary tract smooth muscle. Auton Neurosci 154, 3-13.
15. Fu Y & Rubin CS (2011). Protein kinase D: coupling extracellular stimuli to the regulation of cell physiology. EMBO Rep 12, 785-796.
16. 2+/calmodulin binding and activation of myosin light chain kinase in cells. FEBS Lett 557, 121-124.
17. Hashitani H, Brading AF & Suzuki H (2004). Correlation between spontaneous electrical, calcium and mechanical activity in detrusor smooth muscle of the guinea-pig bladder. Br J Pharmacol 141, 183-193.
18. Hashitani H, Bramich NJ & Hirst GD (2000). Mechanisms of excitatory neuromuscular transmission in the guinea-pig urinary bladder. J Physiol 524, 565-579.
19. He WQ, Peng YJ, Zhang WC, Lv N, Tang J, Chen C, Zhang CH, Gao S, Chen HQ, Zhi G, Feil R, Kamm KE, Stull JT, Gao X & Zhu MS (2008). Myosin light chain kinase is central to smooth muscle contraction and required for gastrointestinal motility in mice. Gastroenterology 135, 610-620.
20. He WQ, Qiao YN, Zhang CH, Peng YJ, Chen C, Wang P, Gao YQ, Chen X, Tao T, Su XH, Li CJ, Kamm KE, Stull JT & Zhu MS (2011). Role of myosin light chain kinase in regulation of basal blood pressure and maintenance of salt-induced hypertension. Am J Physiol Heart Circ Physiol 301, H584-H591.
21. Hegde SS, Choppin A, Bonhaus D, Briaud S, Loeb M, Moy TM, Loury D & Eglen RM (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.
22. 2+ transients evoked by nerve stimulation in rat urinary bladder smooth muscle. J Physiol 564, 201-212.
23. 2+ flashes and contractility evoked by muscarinic receptor activation in mouse urinary bladder smooth muscle. J Physiol 587, 5275-5288.
24. Horman S, Morel N, Vertommen D, Hussain N, Neumann D, Beauloye C, El Najjar N, Forcet C, Viollet B, Walsh MP, Hue L & Rider MH (2008). AMP-activated protein kinase phosphorylates and desensitizes smooth muscle myosin light chain kinase. J Biol Chem 283, 18505-18512.
25. Horowitz A, Menice CB, Laporte R & Morgan KG (1996). Mechanisms of smooth muscle contraction. Physiol Rev 76, 967-1003.
26. V1.2/PKC is involved in muscarinic signalling in smooth muscle. FASEB J 24, 2651-2659.
27. Isotani E, Zhi G, Lau KS, Huang J, Mizuno Y, Persechini A, Geguchadze R, Kamm KE & Stull JT (2004). Real-time evaluation of myosin light chain kinase activation in smooth muscle tissues from a transgenic calmodulin-biosensor mouse. Proc Natl Acad Sci U S A 101, 6279-6284.
28. Kam Y & Exton JH (2004). Role of phospholipase D in the activation of protein kinase D by lysophosphatidic acid. Biochem Biophys Res Commun 315, 139-143.
29. Kamm KE & Stull JT (1985). The function of myosin and myosin light chain kinase phosphorylation in smooth muscle. Annu Rev Pharmacol Toxicol 25, 593-620.
30. Kamm KE & Stull JT (2001). Dedicated myosin light chain kinases with diverse cellular functions. J Biol Chem 276, 4527-4530.
31. Kishii K, Hisayama T & Takayanagi I (1992). Comparison of contractile mechanisms by carbachol and ATP in detrusor strips of rabbit urinary bladder. Jpn J Pharmacol 58, 219-229.
32. 2+ sensitization in rabbit smooth muscle. J Physiol 546, 879-889.
33. 2+ transients during neurogenic contractions of rat mesenteric small arteries. J Physiol 549, 801-808.
34. Matsui M, Motomura D, Karasawa H, Fujikawa T, Jiang J, Komiya Y, Takahashi S & Taketo MM (2000). Multiple functional defects in peripheral autonomic organs in mice lacking muscarinic acetylcholine receptor gene for the M3 subtype. Proc Natl Acad Sci U S A 97, 9579-9584.
35. Matthews SA, Rozengurt E & Cantrell D (1999). Characterization of serine 916 as an in vivo autophosphorylation site for protein kinase D/protein kinase Cμ. J Biol Chem 274, 26543-26549.
36. 3-muscarinic acetylcholine receptor stimulates glucose uptake in L6 skeletal muscle cells by a CaMKK-AMPK-dependent mechanism. Cell Signal 22, 1104-1113.
37. Mizuno Y, Isotani E, Huang J, Ding H, Stull JT & Kamm KE (2008). Myosin light chain kinase activation and calcium sensitization in smooth muscle in vivo. Am J Physiol Cell Physiol 295, C358-C364.
38. 3-mediated calcium release. Am J Physiol Regul Integr Comp Physiol 299, R878-R888.
39. Nomura M, Stull JT, Kamm KE & Mumby MC (1992). Site-specific dephosphorylation of smooth muscle myosin light chain kinase by protein phosphatases 1 and 2A. Biochemistry 31, 11915-11920.
40. Poley RN, Dosier CR, Speich JE, Miner AS & Ratz PH (2008). Stimulated calcium entry and constitutive RhoA kinase activity cause stretch-induced detrusor contraction. Eur J Pharmacol 599, 137-145.
41. Puetz S, Lubomirov LT & Pfitzer G (2009). Regulation of smooth muscle contraction by small GTPases. Physiology (Bethesda) 24, 342-356.
42. Rokolya A & Singer HA (2000). Inhibition of CaM kinase II activation and force maintenance by KN-93 in arterial smooth muscle. Am J Physiol Cell Physiol 278, C537-C545.
43. 12 but not Gq-type G proteins: regulators of G proteins as tools to dissect pertussis toxin-resistant G proteins in receptor-effector coupling. J Biol Chem 276, 2474-2479.
44. Schneider T, Fetscher C, Krege S & Michel MC (2004a). Signal transduction underlying carbachol-induced contraction of human urinary bladder. J Pharmacol Exp Ther 309, 1148-1153.
45. 2+ sources. J Pharmacol Exp Ther 308, 47-53.
46. 2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83, 1325-1358.
47. Streets AJ, Needham AJ, Gill SK & Ong AC (2010). Protein kinase D-mediated phosphorylation of polycystin-2 (TRPP2) is essential for its effects on cell growth and calcium channel activity. Mol Biol Cell 21, 3853-3865.
48. Stull JT, Hsu LC, Tansey MG & Kamm KE (1990). Myosin light chain kinase phosphorylation in tracheal smooth muscle. J Biol Chem 265, 16683-16690.
49. Stull JT, Krueger JK, Kamm KE, Gao ZH & Padre R (1996). Myosin light chain kinase. In Biochemistry of Smooth Muscle, ed. Bárány M, pp. 119-130. Academic, New York.
50. 2+ desensitization. Mol Cell Biochem 127-128, 229-237.
51. 2+ sensitization in contraction of human bladder smooth muscle. J Urol 172, 748-752.
52. Tang DC, Kubota Y, Kamm KE & Stull JT (1993). GTPγS-induced phosphorylation of myosin light chain kinase in smooth muscle. FEBS Lett 331, 272-275.
53. Tansey MG, Word RA, Hidaka H, Singer HA, Schworer CM, Kamm KE & Stull JT (1992). Phosphorylation of myosin light chain kinase by the multifunctional calmodulin-dependent protein kinase II in smooth muscle cells. J Biol Chem 267, 12511-12516.
54. 2+ sensitization in the rat lower urinary tract. Biochem Pharmacol 74, 647-658.
55. 1 receptors for functional P2X receptor responses in the mouse urinary bladder smooth muscle. Br J Pharmacol 131, 1489-1495.
56. Wang QJ (2006). PKD at the crossroads of DAG and PKC signalling. Trends Pharmacol Sci 27, 317-323.
57. Wang T, Kendig DM, Smolock EM & Moreland RS (2009). Carbachol-induced rabbit bladder smooth muscle contraction: roles of protein kinase C and Rho kinase. Am J Physiol Renal Physiol 297, F1534-F1542.
58. v1.2 L-type calcium channel for urinary bladder function. FASEB J 18, 1159-1161.
59. Werner ME, Knorn AM, Meredith AL, Aldrich RW & Nelson MT (2007). Frequency encoding of cholinergic- and purinergic-mediated signalling to mouse urinary bladder smooth muscle: modulation by BK channels. Am J Physiol Regul Integr Comp Physiol 292, R616-R624.
60. 2+ influx to carbachol-induced detrusor contraction is different in human urinary bladder compared to pig and mouse. Eur J Pharmacol 565, 180-189.
61. Young JS, Meng E, Cunnane TC & Brain KL (2008). Spontaneous purinergic neurotransmission in the mouse urinary bladder. J Physiol 586, 5743-5755.
62. Zderic SA, Sillen U, Liu GH, Snyder MC 3rd, Duckett JW, Gong C & Levin RM (1994). Developmental aspects of excitation contraction coupling of rabbit bladder smooth muscle. J Urol 152, 679-681.
63. Zhang WC, Peng YJ, Zhang GS, He WQ, Qiao YN, Dong YY, Gao YQ, Chen C, Zhang CH, Li W, Shen HH, Ning W, Kamm KE, Stull JT, Gao X & Zhu MS (2010). Myosin light chain kinase is necessary for tonic airway smooth muscle contraction. J Biol Chem 285, 5522-5531.