Pressure-dependent contribution of Rho kinase-mediated calcium sensitization in serotonin-evoked vasoconstriction of rat cerebral arteries

Journal of Physiology

Volumn 588, Issue 10, 2010, Pages 1747-1762

  El Yazbi, Ahmed F ^a   Johnson, Rosalyn P ^a   Walsh, Emma J ^a   Takeya, Kosuke ^b   Walsh, Michael P ^b   Cole, William C ^a  

^a Smooth Muscle Research Group   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; BLEBBISTATIN; CALCIUM ION; CPI 17; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN PHOSPHATASE; MYOSIN LIGHT CHAIN PHOSPHATASE TARGETING SUBUNIT 1; PROTEIN KINASE C; PROTEIN KINASE C INHIBITOR; RHO KINASE; SEROTONIN; UNCLASSIFIED DRUG; CALCIUM; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN INHIBITOR;

ARTERIAL PRESSURE; ARTERY DIAMETER; ARTERY RESISTANCE; ARTICLE; COMPETITIVE INHIBITION; CONTROLLED STUDY; ENZYME ACTIVITY; MALE; MIDDLE CEREBRAL ARTERY; MUSCLE CONTRACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SENSITIZATION; VASOCONSTRICTION; WESTERN BLOTTING; ANIMAL CELL; ANIMAL TISSUE; BRAIN ARTERY; CELL MEMBRANE DEPOLARIZATION; CONCENTRATION (PARAMETERS); ENZYME INHIBITION; ENZYME REPRESSION; PROTEIN ANALYSIS; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; BLOOD PRESSURE; BLOTTING, WESTERN; CALCIUM; CEREBRAL ARTERIES; DOSE-RESPONSE RELATIONSHIP, DRUG; MALE; MUSCLE PROTEINS; MYOGRAPHY; PHOSPHOPROTEINS; PHOSPHORYLATION; PRESSURE; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; PROTEIN PHOSPHATASE 1; RATS; RATS, SPRAGUE-DAWLEY; RHO-ASSOCIATED KINASES; SEROTONIN; VASOCONSTRICTION;

EID: 77954079337     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.187146     Document Type: Article

References (73)

1. Akopov SE, Zhang L, Pearce WJ. Regulation of Ca2+ sensitization by PKC and rho proteins in ovine cerebral arteries: effects of artery size and age. Am J Physiol Heart Circ Physiol 1998, 275:H930-H939.
2. Anschütz S, Schubert R. Modulation of the myogenic response by neurogenic influences in rat small arteries. Br J Pharmacol 2005, 146:226-233.
3. Chen TT, Leukenaar KD, Walsh EJ, Walsh MP, Cole WJ. Key role of Kv1 channels in vasoregulation. Circ Res 2006, 99:53-60.
4. Cipolla MJ, Gokina NI, Osol G. Pressure-induced actin polymerization in vascular smooth muscle as a mechanism underlying myogenic behaviour. FASEB J 2002, 16:72-76.
5. Cipolla MJ, Osol G. Vascular smooth muscle actin cytoskeleton in cerebral artery forced dilation. Stroke 1998, 29:1223-1228.
6. Cobine CA, Callaghan BP, Keef KD. Role of L-type calcium channels and PKC in active tone development in rabbit coronary artery. Am J Physiol Heart Circ Physiol 2007, 292:H3079-H3088.
7. Cohen Z, Bonvento G, Lacombe P, Hamel E. Serotonin in the regulation of brain microcirculation. Progress Neurobiol 1996, 50:335-362.
8. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 2000, 351:95-105.
9. Davis MJ, Hill MA. Signalling mechanisms underlying the vascular myogenic response. Physiol Rev 1999, 79:387-423.
10. Dimopoulos GJ, Semba S, Kitazawa K, Eto M, Kitazawa T. Ca2+-dependent rapid Ca2+-sensitization of contraction in arterial smooth muscle. Circ Res 2007, 100:121-129.
11. Drummond GB. Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 2009, 587:713-719.
12. Earley S, Straub SV, Brayden JE. Protein kinase C regulates vascular myogenic tone through activation of TRPM4. Am J Physiol Heart Circ Physiol 2007, 292:H2613-H2622.
13. Eddinger TJ, Meer DP, Miner AS, Meehl J, Rovner AS, Ratz PH. Potent inhibition of arterial smooth muscle tonic contractions by the selective myosin II inhibitor, blebbistatin. J Pharmacol Exp Ther 2007, 320:865-870.
14. Faber JE, Meininger GA. Selective interaction of α-adrenoceptors with myogenic regulation of microvascular smooth muscle. Am J Physiol Heart Circ Physiol 1990, 259:H1126-H1133.
15. Faraci FM, Heistad DD. Regulation of large cerebral arteries and cerebral microvascular pressure. Circ Res 1990, 66:8-17.
16. Feng J, Ito M, Ichikawa K, Isaka N, Nishikawa M, Hartshorne DJ, Nakano T. Inhibitory phosphorylation site for Rho-associated kinase on smooth muscle myosin phosphatase. J Biol Chem 1999, 274:37385-37390.
17. Freitas MR, Eto M, Kirkbride JA, Schott C, Sassard J, Stoclet JC. Y27632, a Rho-activated kinase inhibitor, normalizes dysregulation in α1-adrenergic receptor-induced contraction of Lyon hypertensive rat artery smooth muscle. Fundam Clin Pharmacol 2009, 23:169-178.
18. Garland CJ. The role of membrane depolarization in the contractile response of the rabbit basilar artery to 5-hydroxytryptamine. J Physiol 1987, 392:333-348.
19. Gerthoffer WT. Actin cytoskeletal dynamics in smooth muscle contraction. Can J Physiol Pharmacol 2005, 83:851-856.
20. Gokina NI, Knot HJ, Nelson MT, Osol G. Increased Ca2+ sensitivity as a key mechanism of PKC-induced constriction in pressurized cerebral arteries. Am J Physiol Heart Circ Physiol 1999, 277:H1178-H1188.
21. Gokina NI, Osol G. Temperature and protein kinase C modulate myofilament Ca2+ sensitivity in pressurized rat cerebral arteries. Am J Physiol Heart Circ Physiol 1998, 274:H1920-H1927.
22. Gokina NI, Osol G. Actin cytoskeletal modulation of pressure-induced depolarization and Ca2+ influx in cerebral arteries. Am J Physiol Heart Circ Physiol 2002, 282:H1410-H1420.
23. Gunst SJ, Zhang W. Actin cytoskeletal dynamics in smooth muscle: a new paradigm for the regulation of smooth muscle contraction. Am J Physiol Cell Physiol 2008, 295:C576-C587.
24. Hansen-Schwartz J, Ansar S, Edvinsson L. Cerebral vasoconstriction after subarachnoid hemorrhage: role of changes in vascular receptor phenotype. Front Biosci 2008, 13:2160-2164.
25. Harder DR. Increased sensitivity of cat cerebral arteries to serotonin upon elevation of transmural pressure. Pflügers Arch 1988, 411:698-700.
26. Harder DR, Waters A. Electromechanical coupling in feline basilar artery in response to serotonin. Eur J Pharmacol 1983, 93:95-100.
27. Hayashi Y, Senba S, Yazawa M, Brautigan DL, Eto M. Defining the structural determinants and a mechanism for inhibiton of myosin phosphatase by the protein kinase C-potentiated inhibitor protein of 17 kDa. J Biol Chem 2001, 276:39858-39863.
28. Heistad DD. What's new in the cerebral circulation? Landis Award Lecture. Micorcirculation 2001, 8:365-375.
29. Hill MA, Davis MJ, Song J, Zou H. Calcium dependence of indolactam-mediated contractions in resistance vessels. J Pharmacol Exp Ther 1996, 276:867-874.
30. Hill MA, Falcone JC, Meininger GA. Evidence for protein kinase C involvement in arteriolar myogenic reactivity. Am J Physiol Heart Circ Physiol 1990, 259:H1586-H1594.
31. Hirano K. Current topics in the regulatory mechanism underlying the Ca2+ sensitization of the contractile apparatus in vascular smooth muscle. J Pharmacol Sci 2007, 104:109-115.
32. Iadecola C, Nedergaard M. Glial regulation of the cerebral microvasculature. Nat Neursci 2007, 10:1369-1376.
33. Jin JP, Walsh MP, Sutherland C, Chen W. A role for serine-175 in modulating the molecular conformation of calponin. Biochem J 2000, 350:579-588.
34. Johnson RP, El-Yazbi AF, Takeya K, Walsh EJ, Walsh MP, Cole WC. Ca2+ sensitization via phosphorylation of myosin phosphatase targeting subunit at threonine-855 by Rho kinase contributes to the arterial myogenic response. J Physiol 2009, 587:2537-2553.
35. Kaneko T, Amano M, Maeda A, Goto H, Takahashi K, Ito M, Kaibuchi K. Identification of calponin as a novel substrate of Rho-kinase. Biochem Biophys Res Commun 2000, 273:110-116.
36. Khromov A, Choudhury N, Stevenson AS, Somlyo AV, Eto M. Phosphorylation-dependent autoinhibition of myosin light chain phosphatase accounts for Ca2+ sensitization force of smooth muscle contraction. J Biol Chem 2009, 284:21569-21579.
37. Kitazawa T, Eto M, Woodsome TP, Khalequzzaman M. Phosphorylation of the myosin phosphatase targeting subunit and CPI-17 during Ca2+-sensitization in rabbit smooth muscle. J Physiol 2003, 546:879-889.
38. Knot HJ, Nelson MT. Regulation of arterial diameter and wall [Ca2+] in cerebral arteries of rat by membrane potential and intravascular pressure. J Physiol 1998, 508:199-209.
39. Korzick DH, Laughlin MH, Bowles DK. Alterations in PKC signalling underlie enhanced myogenic tone in exercise-trained porcine coronary resistance arteries. J Appl Physiol 2004, 96:1425-1432.
40. Kulik T, Kusano Y, Aronhime S, Sandler AL, Winn HR. Regulation of cerebral vasculature in normal and ischemic brain. Neuropharmacol 2008, 55:281-288.
41. Lagaud G, Gaudreault N, Moore ED, Van Breemen C, Laher I. Pressure-dependent myogenic constriction of cerebral arteries occurs independently of voltage-dependent activation. Am J Physiol Heart Circ Physiol 2002, 283:H2187-H2195.
42. Liu J, Hill MA, Meininger GA. Mechanism of myogenic enhancement of norepinephrine. Am J Physiol Heart Circ Physiol 1994, 266:H440-H446.
43. Lombard JH, Eskinder H, Kauser K, Osborn JL, Harder DR. Enhanced norepinephrine sensitivity in renal arteries at elevated pressure. Am J Physiol Heart Circ Physiol 1990, 259:H29-H33.
44. MacDonald JA, Borman MA, Murányi A, Somlyo AV, Hartshorne DJ, Haystead TA. Identification of the endogenous smooth muscle phosphatase-associated kinase. Proc Natl Acad Sci USA 2001, 98:2419-2424.
45. Maruko K, Stiffel VM, Gilbert RD. The effect of long term hypoxia on tension and intracellular calcium responses following stimulation of the thromboxane A2 receptor in the left anterior descending coronary artery of fetal sheep. Reprod Sci 2009, 16:364-372.
46. Massett MP, Ungvari Z, Csiszar A, Kaley G, Koller A. Different roles of PKC and MAP kinases in arteriolar constrictions to pressure and agonists. Am J Physiol Heart Circ Physiol 2002, 283:H2282-H2287.
47. McCarron JG, Crichton CA, Langton PD, Mackenzie A, Smith GL. Myogenic contraction by modulation of voltage-dependent calcium currents in isolated rat cerebral arteries. J Physiol 1997, 498:371-379.
48. Meininger GA, Faber JE. Adrenergic facilitation of myogenic response in skeletal muscle arterioles. Am J Physiol Heart Circ Physiol 1991, 260:H1424-H1432.
49. Morgan KG, Gangopadhyay SS. Invited review: Cross-bridge regulation by thin filament-associated proteins. J Appl Physiol 2001, 91:953-962.
50. Murányi A, Derkach D, Erdödi F, Kiss A, Ito M, Hartshorne DJ. Phosphorylation of Thr695 and Thr850 on the myosin phosphatase target subunit: inhibitory effects and occurrence in A7r5 cells. FEBS Lett 2005, 579:6611-6615.
51. Murányi A, MacDonald JA, Deng JT, Wilson DP, Haystead TA, Walsh MP, Erdödi F, Kiss E, Wu Y, Hartshorne DJ. Phosphorylation of the myosin phosphatase target subunit by integrin-linked kinase. Biochem J 2002, 366:211-216.
52. Neppl RL, Lubomirov LT, Momotani K, Pfitzer G, Eto M, Somlyo AV. Thromboxane A2-induced bi-directional regulation of cerebral arterial tone. J Biol Chem 2009, 284:6348-6360.
53. Osol G, Brekke JF, McElroy-Yaggy K, Gokina NI. Myogenic tone, reactivity, and forced dilation: a three phase model of in vitro arterial myogenic behaviour. Am J Physiol Heart Circ Physiol 2002, 283:H2260-H2267.
54. Osol G, Laher I, Cipolla M. Protein kinase C modulates basal myogenic tone in resistance arteries from the cerebral circulation. Circ Res 1991, 68:359-367.
55. Salomone S, Soydan G, Moskowitz MA, Sims JR. Inhibition of cerebral vasoconstriction by dantrolene and nimodipine. Neurocrit Care 2009, 10:93-102.
56. Sandoval RJ, Injeti ER, Gerthoffer WT, Pearce WJ. Postnatal maturaion modulates relationships among cytosolic Ca2+, myosin light chain phosphorylation, and contractile tone in ovine cerebral arteries. Am J Physiol Heart Circ Physiol 2007, 293:H2183-H2192.
57. Sato M, Tani E, Fujikawa H, Kaibuchi K. Involvement of rho-kinase-mediated phosphorylation of myosin light chain in enhancement of cerebral vasospasm. Circ Res 2000, 87:195-200.
58. Shaw L, O'Neill S, Jones CJ, Austin C, Taggart MJ. Comparison of U46619-, endothelin-1- or phenylephrine-induced changes in cellular Ca2+ profiles and Ca2+ sensitisation of constriction of pressurised rat resistance arteries. Br J Pharmacol 2004, 141:678-688.
59. Somlyo AP, Somlyo AV. Ca2+ sensitivity of smooth muscle and non-muscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 2003, 83:1325-1358.
60. Somlyo AP, Somlyo AV. Signal transduction through the RhoA/Rho-kinase pathway in smooth muscle. J Muscle Res Cell Motil 2004, 25:613-615.
61. Stevenson AS, Matthew JD, Eto M, Luo S, Somlyo AP, Somlyo AV. Uncoupling of GPCR and Rho A-induced Ca2+-sensitization of chicken amnion smooth muscle lacking CPI-17. FEBS Lett 2004, 578:73-79.
62. Swärd K, Mita M, Wilson DP, Deng JT, Susnjar M, Walsh MP. The role of Rho A and Rho-associated kinase in vascular smooth muscle contraction. Curr Hypertens Rep 2003, 5:66-72.
63. Takeya K, Loutzenhiser K, Shiraishi M, Loutzenhiser R, Walsh MP. A highly sensitive technique to measure myosin regulatory light chain phosphorylation: the first quantification in renal arterioles. Am J Physiol Renal Physiol 2008, 294:F1487-F1492.
64. Toullec D, Pianetti P, Coste H, Bellevergue P, Grand-Perret T, Ajakane M, Baudet V, Boissin P, Boursier E, Loriolle F, Duhamel L, Charon D, Kirilovsky D. The bisindolemaleimide GF109203X is a potent and selective inhibitor of protein kinase C. J Biol Chem 1991, 266:15771-15781.
65. Tsai MH, Jiang MJ. Rho-kinase-mediated regulation of receptor-agonist-stimulated smooth muscle contraction. Pflugers Arch 2006, 453:223-232.
66. VanBavel E, Mulvany MJ. Role of wall tension in the vasoconstrictor response of cannulated rat mesenteric small arteries. J Physiol 1994, 477:103-115.
67. Velasco G, Armstrong C, Morrice N, Frame S, Cohen P. Phosphorylation of the regulatory subunit of smooth muscle protein phosphatase 1M at Thr850 induces its dissociation from myosin. FEBS Lett 2002, 527:101-104.
68. Watanabe Y, Faraci FM, Heistad DD. Activation of Rho-associated kinase during augmented contraction of the basilar artery to serotonin after subarachnoid hemorrhage. Am J Physiol Heart Circ Physiol 2005, 288:H2653-H2658.
69. Wesselman JP, Spaan JA, van der Meulen ET, VanBavel E. Role of protein kinase C in myogenic calcium-contraction coupling in rat cannulated mesenteric small arteries. Clin Exp Pharmacol Physiol 2001, 28:848-855.
70. Wilson DP, Susnjar M, Kiss E, Sutherland C, Walsh MP. Thromboxane A2-induced contraction of rat caudal arterial smooth muscle involves activation of Ca2+ entry and Ca2+ sensitization: Rho-associated kinase mediated phosphorylation of MYPT1 at Thr-855, but not Thr-697. Biochem J 2005, 389:763-774.
71. Worley JF, Quayle JM, Standen NB, Nelson MT. Regulation of single calcium channels in cerebral arteries by voltage, serotonin and dihydropyridine. Am J Physiol Heart Circ Physiol 1991, 261:H1951-H1960.
72. Yoshino H, Sakurai T, Oizumi XS, Akisaki T, Wang X, Yokono K, Kondoh T, Kohmura E, Umentani K. Dilation of perforating arteries in rat brain in response to systemic hypotension is more sensitive and pronounced than that of pial arterioles: simultaneous visualization of perforating and cortical vessels by in-vivo microangiography. Microvasc Res 2009, 77:230-233.
73. Zou H, Ratz PH, Hill MA. Temporal aspects of Ca2+ and myosin phosphorylation during myogenic and norepinephrine-induced arteriolar constriction. J Vasc Res 2000, 37:556-567.