PKC-mediated cerebral vasoconstriction: Role of myosin light chain phosphorylation versus actin cytoskeleton reorganization

Biochemical Pharmacology

Volumn 95, Issue 4, 2015, Pages 263-278

  El Yazbi, Ahmed F ^a,b   Abd Elrahman, Khaled S ^a   Moreno Dominguez, Alejandro ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b Alexandria University Faculty of Pharmacy   (Egypt)

Author keywords

Actin cytoskeleton polymerization; Ca2+ sensitization; Cerebral arteries; PKC; Thin filament regulation

Indexed keywords

12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; CALDESMON; CALPONIN; G ACTIN; HEAT SHOCK PROTEIN 27; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN PHOSPHATASE; PAXILLIN; PHORBOL DIBUTYRATE; PHOSPHOPROTEIN; PROTEIN CPI 17; PROTEIN KINASE C; PROTEIN MYPT1; SEROTONIN; UNCLASSIFIED DRUG; BLEBBISTATIN; FUSED HETEROCYCLIC RINGS; LATRUNCULIN B; THIAZOLIDINE DERIVATIVE;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL TISSUE; ARTICLE; CEREBRAL VASOCONSTRICTION; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVATION; MALE; MIDDLE CEREBRAL ARTERY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; THIN FILAMENT; VASOCONSTRICTION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; DRUG EFFECTS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; POLYMERIZATION; SPRAGUE DAWLEY RAT; VASCULAR RESISTANCE; VASCULARIZATION;

ACTIN CYTOSKELETON; ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; BRAIN; ENZYME ACTIVATION; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; MALE; MIDDLE CEREBRAL ARTERY; MYOSIN LIGHT CHAINS; PHORBOL 12,13-DIBUTYRATE; PHOSPHORYLATION; POLYMERIZATION; PROTEIN KINASE C; RATS, SPRAGUE-DAWLEY; SEROTONIN; THIAZOLIDINES; VASCULAR RESISTANCE; VASOCONSTRICTION;

EID: 84929705321     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2015.04.011     Document Type: Article

References (90)

1. I.V. Kizub, K.I. Klymenko, and A.I. Soloviev Protein kinase C in enhanced vascular tone in diabetes mellitus Int. J. Cardiol. 174 2014 230 242
2. 2+ sensitivity of contractile elements via protein kinase C in alpha-toxin permeabilized SMA from young spontaneously hypertensive rats Cardiovasc. Res. 36 1997 86 91
3. R.A. Khalil Protein kinase C inhibitors as modulators of vascular function and their application in vascular disease Pharmaceuticals (Basel, Switzerland) 6 2013 407 439
4. Y. Takai, A. Kishimoto, Y. Iwasa, Y. Kawahara, T. Mori, and Y. Nishizuka Calcium-dependent activation of a multifunctional protein kinase by membrane phospholipids J. Biol. Chem. 254 1979 3692 3695
5. A.C. Newton Protein kinase C: structure, function, and regulation J. Biol. Chem. 270 1995 28495 28498
6. S.F. Steinberg Structural basis of protein kinase C isoform function Physiol. Rev. 88 2008 1341 1378
7. D.A. Salamanca, and R.A. Khalil Protein kinase C isoforms as specific targets for modulation of vascular smooth muscle function in hypertension Biochem. Pharmacol. 70 2005 1537 1547
8. 2+ sensitisation of constriction of pressurised rat resistance arteries Br. J. Pharmacol. 141 2004 678 688
9. (2+) and myosin phosphorylation during myogenic and norepinephrine-induced arteriolar constriction J. Vasc. Res. 37 2000 556 567
10. 2+]i in myogenic reactivity and arteriolar tone Am. J. Physiol. 269 1995 H1590 H1596
11. M.J. Davis, and M.A. Hill Signaling mechanisms underlying the vascular myogenic response Physiol. Rev. 79 1999 387 423
12. 2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase Physiol. Rev. 83 2003 1325 1358
13. 2+ sensitization via phosphorylation of myosin phosphatase targeting subunit at threonine-855 by Rho kinase contributes to the arterial myogenic response J. Physiol. 587 2009 2537 2553
14. A.F. El-Yazbi, R.P. Johnson, E.J. Walsh, K. Takeya, M.P. Walsh, and W.C. Cole Pressure-dependent contribution of Rho kinase-mediated calcium sensitization in serotonin-evoked vasoconstriction of rat cerebral arteries J. Physiol. 588 2010 1747 1762
15. S.J. Gunst, and W. Zhang Actin cytoskeletal dynamics in smooth muscle: a new paradigm for the regulation of smooth muscle contraction Am. J. Physiol. Cell Physiol. 295 2008 C576 C587
16. W. Zhang, Y. Wu, L. Du, D.D. Tang, and S.J. Gunst Activation of the Arp2/3 complex by N-WASp is required for actin polymerization and contraction in smooth muscle Am. J. Physiol. Cell Physiol. 288 2005 C1145 C1160
17. A. Moreno-Dominguez, A.F. El-Yazbi, H.L. Zhu, O. Colinas, X.Z. Zhong, and E.J. Walsh Cytoskeletal reorganization evoked by Rho-associated kinase- and protein kinase C-catalyzed phosphorylation of cofilin and heat shock protein 27, respectively, contributes to myogenic constriction of rat cerebral arteries J. Biol. Chem. 289 2014 20939 20952
18. 2+ sensitization due to myosin light chain phosphatase inhibition and cytoskeletal reorganization in the myogenic response of skeletal muscle resistance arteries J. Physiol. 591 2013 1235 1250
19. 2+ sensitization, and contraction activated by protein kinase C in small airway smooth muscle J. Gen. Physiol. 141 2013 165 178
20. M. Huster, E. Frei, F. Hofmann, and J.W. Wegener A complex of Ca(V)1.2/PKC is involved in muscarinic signaling in smooth muscle FASEB J. 24 2010 2651 2659
21. 2+ channels Proc. Natl. Acad. Sci. USA 102 2005 11112 11117
22. Y. Hayashi, S. Senba, M. Yazawa, D.L. Brautigan, and M. Eto Defining the structural determinants and a potential mechanism for inhibition of myosin phosphatase by the protein kinase C-potentiated inhibitor protein of 17 kDa J. Biol. Chem. 276 2001 39858 39863
23. 2+ sensitization of contraction in arterial smooth muscle Circ. Res. 100 2007 121 129
24. (2+)-independent contractions of vascular smooth muscle Biochem. Cell Biol. 74 1996 485 502
25. A. Horowitz, O. Clement-Chomienne, M.P. Walsh, T. Tao, H. Katsuyama, and K.G. Morgan Effects of calponin on force generation by single smooth muscle cells Am. J. Physiol. 270 1996 H1858 H1863
26. K.G. Morgan, and S.S. Gangopadhyay Invited review: cross-bridge regulation by thin filament-associated proteins J. Appl. Physiol. (Bethesda, Md: 1985) 91 2001 953 962
27. M.A. Hill, J.C. Falcone, and G.A. Meininger Evidence for protein kinase C involvement in arteriolar myogenic reactivity Am. J. Physiol. 259 1990 H1586 H1594
28. G. Osol, I. Laher, and M. Cipolla Protein kinase C modulates basal myogenic tone in resistance arteries from the cerebral circulation Circ. Res. 68 1991 359 367
29. M.P. Massett, Z. Ungvari, A. Csiszar, G. Kaley, and A. Koller Different roles of PKC and MAP kinases in arteriolar constrictions to pressure and agonists Am. J. Physiol. Heart Circ. Physiol. 283 2002 H2282 H2287
30. 2+ sensitization in rat arterial smooth muscle J. Physiol. 590 2012 5401 5423
31. F. Plane, R. Johnson, P. Kerr, W. Wiehler, K. Thorneloe, and K. Ishii Heteromultimeric Kv1 channels contribute to myogenic control of arterial diameter Circ. Res. 96 2005 216 224
32. T.T. Chen, K.D. Luykenaar, E.J. Walsh, M.P. Walsh, and W.C. Cole Key role of Kv1 channels in vasoregulation Circ. Res. 99 2006 53 60
33. J. Baik, S.H. Ok, H. Cho, J. Yu, W. Kim, and I.K. Nam Dexmedetomidine-induced contraction involves phosphorylation of caldesmon by JNK in endothelium-denuded rat aortas Int. J. Biol. Sci. 10 2014 1108 1115
34. D. Xiao, R. Zhu, and L. Zhang Gestational hypoxia up-regulates protein kinase C and inhibits calcium-activated potassium channels in ovine uterine arteries Int. J. Med. Sci. 11 2014 886 892
35. D. Xiao, X. Huang, and L. Zhang Chronic hypoxia differentially up-regulates protein kinase C-mediated ovine uterine arterial contraction via actin polymerization signaling in pregnancy Biol. Reprod. 87 2012 142
36. R. Goyal, A. Mittal, N. Chu, R.A. Arthur, L. Zhang, and L.D. Longo Maturation and long-term hypoxia-induced acclimatization responses in PKC-mediated signaling pathways in ovine cerebral arterial contractility Am. J. Physiol. Regul. Integr. Comp. Physiol. 299 2010 R1377 R1386
37. K. Sathishkumar, U. Yallampalli, R. Elkins, and C. Yallampalli Raf-1 kinase regulates smooth muscle contraction in the rat mesenteric arteries J. Vasc. Res. 47 2010 384 398
38. K. Takeya, K. Loutzenhiser, M. Shiraishi, R. Loutzenhiser, and M.P. Walsh A highly sensitive technique to measure myosin regulatory light chain phosphorylation: the first quantification in renal arterioles Am. J. Physiol. Renal Physiol. 294 2008 F1487 F1492
39. R.L. Corteling, S.E. Brett, H. Yin, X.L. Zheng, M.P. Walsh, and D.G. Welsh The functional consequence of RhoA knockdown by RNA interference in rat cerebral arteries Am. J. Physiol. Heart Circ. Physiol. 293 2007 H440 H447
40. M.P. Walsh, K. Thornbury, W.C. Cole, G. Sergeant, M. Hollywood, and N. McHale Rho-associated kinase plays a role in rabbit urethral smooth muscle contraction, but not via enhanced myosin light chain phosphorylation Am. J. Physiol. Renal Physiol. 300 2011 F73 F85
41. S.J. Winder, and M.P. Walsh Smooth muscle calponin. Inhibition of actomyosin MgATPase and regulation by phosphorylation J. Biol. Chem. 265 1990 10148 10155
42. A.X. Wu-Zhang, and A.C. Newton Protein kinase C pharmacology: refining the toolbox Biochem. J. 452 2013 195 209
43. Y. Sasaki, M. Suzuki, and H. Hidaka The novel and specific Rho-kinase inhibitor (S)-(+)-2-methyl-1-[(4-methyl-5-isoquinoline)sulfonyl]-homopiperazine as a probing molecule for Rho-kinase-involved pathway Pharmacol. Ther. 93 2002 225 232
44. L. Shaw, S. Ahmed, C. Austin, and M.J. Taggart Inhibitors of actin filament polymerisation attenuate force but not global intracellular calcium in isolated pressurised resistance arteries J. Vasc. Res. 40 2003 1 10 (discussion)
45. T.J. Eddinger, D.P. Meer, A.S. Miner, J. Meehl, A.S. Rovner, and P.H. Ratz Potent inhibition of arterial smooth muscle tonic contractions by the selective myosin II inhibitor, blebbistatin J. Pharmacol. Exp. Ther. 320 2007 865 870
46. J. Ohanian, M. Pieri, and V. Ohanian Non-receptor tyrosine kinases and the actin cytoskeleton in contractile vascular smooth muscle J. Physiol. 2014 http://dx.doi.org/10.1113/jphysiol.2014.284174
47. W. Zhang, Y. Huang, and S.J. Gunst The small GTPase RhoA regulates the contraction of smooth muscle tissues by catalyzing the assembly of cytoskeletal signaling complexes at membrane adhesion sites J. Biol. Chem. 287 2012 33996 34008
48. H. Wang, R.C. Robinson, and L.D. Burtnick The structure of native G-actin Cytoskeleton (Hoboken, NJ). 67 2010 456 465
49. R. Zhao, L. Du, Y. Huang, Y. Wu, and S.J. Gunst Actin depolymerization factor/cofilin activation regulates actin polymerization and tension development in canine tracheal smooth muscle J. Biol. Chem. 283 2008 36522 36531
50. M. Eto, T. Kitazawa, M. Yazawa, H. Mukai, Y. Ono, and D.L. Brautigan Histamine-induced vasoconstriction involves phosphorylation of a specific inhibitor protein for myosin phosphatase by protein kinase C alpha and delta isoforms J. Biol. Chem. 276 2001 29072 29078
51. 2+ sensitization in triton X-100-demembranated rabbit arterial smooth muscle J. Physiol. 520 Pt 1 1999 139 152
52. S.B. Patil, and K.N. Bitar RhoA- and PKC-alpha-mediated phosphorylation of MYPT and its association with HSP27 in colonic smooth muscle cells Am. J. Physiol. Gastrointest. Liver Physiol. 290 2006 G83 G95
53. K. Shibata, H. Sakai, Q. Huang, H. Kamata, Y. Chiba, and M. Misawa Rac1 regulates myosin II phosphorylation through regulation of myosin light chain phosphatase J. Cell. Physiol. 230 6 2015 1352 1364 http://dx.doi.org/10.1002/jcp.24878
54. P.H. Ratz, C.M. Hai, and R.A. Murphy Dependence of stress on cross-bridge phosphorylation in vascular smooth muscle Am. J. Physiol. 256 1989 C96 C100
55. R.A. Murphy, and C.M. Rembold The latch-bridge hypothesis of smooth muscle contraction Can. J. Physiol. Pharmacol. 83 2005 857 864
56. K. Sato, M. Hori, H. Ozaki, H. Takano-Ohmuro, T. Tsuchiya, and H. Sugi Myosin phosphorylation-independent contraction induced by phorbol ester in vascular smooth muscle J. Pharmacol. Exp. Ther. 261 1992 497 505
57. M.J. Jiang, and K.G. Morgan Intracellular calcium levels in phorbol ester-induced contractions of vascular muscle Am. J. Physiol. 253 1987 H1365 H1371
58. 2+ antagonist-insensitive coronary smooth muscle contraction involves activation of epsilon-protein kinase C-dependent pathway Am. J. Physiol. Cell Physiol. 285 2003 C1454 C1463
59. 2+-independent contraction of pulmonary artery smooth muscle J. Vet. Med. Sci. 67 2005 787 793
60. E.E. Daniel, T. Eteraf, B. Sommer, W.J. Cho, and A. Elyazbi The role of caveolae and caveolin 1 in calcium handling in pacing and contraction of mouse intestine J. Cell. Mol. Med. 13 2009 352 364
61. P.J. Dougherty, Z.V. Nepiyushchikh, S. Chakraborty, W. Wang, M.J. Davis, and D.C. Zawieja PKC activation increases Ca(2)(+) sensitivity of permeabilized lymphatic muscle via myosin light chain 20 phosphorylation-dependent and -independent mechanisms Am. J. Physiol. Heart Circ. Physiol. 306 2014 H674 H683
62. (2+)-independent isoforms of protein kinase C differentially translocate in smooth muscle Am. J. Physiol. 263 1992 C714 C719
63. J. Pohl, S.J. Winder, B.G. Allen, M.P. Walsh, J.R. Sellers, and W.T. Gerthoffer Phosphorylation of calponin in airway smooth muscle Am. J. Physiol. 272 1997 L115 L123
64. S.B. Marston, and C.S. Redwood Inhibition of actin-tropomyosin activation of myosin MgATPase activity by the smooth muscle regulatory protein caldesmon J. Biol. Chem. 267 1992 16796 16800
65. A. Horowitz, C.B. Menice, R. Laporte, and K.G. Morgan Mechanisms of smooth muscle contraction Physiol. Rev. 76 1996 967 1003
66. M.J. Cipolla, N.I. Gokina, and G. Osol Pressure-induced actin polymerization in vascular smooth muscle as a mechanism underlying myogenic behavior FASEB J. 16 2002 72 76
67. N.A. Flavahan, S.R. Bailey, W.A. Flavahan, S. Mitra, and S. Flavahan Imaging remodeling of the actin cytoskeleton in vascular smooth muscle cells after mechanosensitive arteriolar constriction Am. J. Physiol. Heart Circ. Physiol. 288 2005 H660 H669
68. A.D. Tejani, and C.M. Rembold Force augmentation and stimulated actin polymerization in swine carotid artery Am. J. Physiol. Cell Physiol. 298 2010 C182 C190
69. C.M. Rembold, A.D. Tejani, M.L. Ripley, and S. Han Paxillin phosphorylation, actin polymerization, noise temperature, and the sustained phase of swine carotid artery contraction Am. J. Physiol. Cell Physiol. 293 2007 C993 C1002
70. M.K. Meeks, M.L. Ripley, Z. Jin, and C.M. Rembold Heat shock protein 20-mediated force suppression in forskolin-relaxed swine carotid artery Am. J. Physiol. Cell Physiol. 288 2005 C633 C639
71. E.V. Mymrikov, A.S. Seit-Nebi, and N.B. Gusev Large potentials of small heat shock proteins Physiol. Rev. 91 2011 1123 1159
72. N. Mounier, and A.P. Arrigo Actin cytoskeleton and small heat shock proteins: how do they interact? Cell Stress Chaperones 7 2002 167 176
73. R. Srinivasan, S. Forman, R.A. Quinlan, J. Ohanian, and V. Ohanian Regulation of contractility by Hsp27 and Hic-5 in rat mesenteric small arteries Am. J. Physiol. Heart Circ. Physiol. 294 2008 H961 H969
74. E.T. Maizels, C.A. Peters, M. Kline, R.E. Cutler Jr., M. Shanmugam, and M. Hunzicker-Dunn Heat-shock protein-25/27 phosphorylation by the delta isoform of protein kinase C Biochem. J. 332 Pt 3 1998 703 712
75. K. Kato, H. Ito, I. Iwamoto, K. Lida, and Y. Inaguma Protein kinase inhibitors can suppress stress-induced dissociation of Hsp27 Cell Stress Chaperones 6 2001 16 20
76. S. Chakraborti, S. Roy, A. Mandal, K. Dey, A. Chowdhury, and S. Shaikh Role of PKCalpha-p(38)MAPK-G(i)alpha axis in NADPH oxidase derived O(2)(.-)-mediated activation of cPLA(2) under U46619 stimulation in pulmonary artery smooth muscle cells Arch. Biochem. Biophys. 523 2012 169 180
77. D. Stokoe, K. Engel, D.G. Campbell, P. Cohen, and M. Gaestel Identification of MAPKAP kinase 2 as a major enzyme responsible for the phosphorylation of the small mammalian heat shock proteins FEBS Lett 313 1992 307 313
78. M.M. McLaughlin, S. Kumar, P.C. McDonnell, S. Van Horn, J.C. Lee, and G.P. Livi Identification of mitogen-activated protein (MAP) kinase-activated protein kinase-3, a novel substrate of CSBP p38 MAP kinase J. Biol. Chem. 271 1996 8488 8492
79. O. Bernard Lim kinases, regulators of actin dynamics Int. J. Biochem. Cell Biol. 39 2007 1071 1076
80. K. Burridge, and M. Chrzanowska-Wodnicka Focal adhesions, contractility, and signaling Annu. Rev. Cell Dev. Biol. 12 1996 463 518
81. A. Richardson, R.K. Malik, J.D. Hildebrand, and J.T. Parsons Inhibition of cell spreading by expression of the C-terminal domain of focal adhesion kinase (FAK) is rescued by coexpression of Src or catalytically inactive FAK: a role for paxillin tyrosine phosphorylation Mol. Cell. Biol. 17 1997 6906 6914
82. J. Ohanian, V. Ohanian, L. Shaw, C. Bruce, and A.M. Heagerty Involvement of tyrosine phosphorylation in endothelin-1-induced calcium-sensitization in rat small mesenteric arteries Br. J. Pharmacol. 120 1997 653 661
83. F.M. Pavalko, L.P. Adam, M.F. Wu, T.L. Walker, and S.J. Gunst Phosphorylation of dense-plaque proteins talin and paxillin during tracheal smooth muscle contraction Am. J. Physiol. 268 1995 C563 C571
84. D.T. Ward, A.C. Alder, J. Ohanian, and V. Ohanian Noradrenaline-induced paxillin phosphorylation, ERK activation and MEK-regulated contraction in intact rat mesenteric arteries J. Vasc. Res. 39 2002 1 11
85. V. Ohanian, K. Gatfield, and J. Ohanian Role of the actin cytoskeleton in G-protein-coupled receptor activation of PYK2 and paxillin in vascular smooth muscle Hypertension. 46 2005 93 99
86. (2+) on p42/p44 MAPK, Pyk2, and Src activation in rat conjunctival goblet cells Exp. Eye Res. 85 2007 836 844
87. M.Y. Chang, D.Y. Huang, F.M. Ho, K.C. Huang, and W.W. Lin PKC-dependent human monocyte adhesion requires AMPK and Syk activation PLoS ONE 7 2012 e40999
88. Z. Cao, J. George, D.G. Baden, and T.F. Murray Brevetoxin-induced phosphorylation of Pyk2 and Src in murine neocortical neurons involves distinct signaling pathways Brain Res. 1184 2007 17 27
89. M.T. Kunkel, and A.C. Newton Calcium transduces plasma membrane receptor signals to produce diacylglycerol at Golgi membranes J. Biol. Chem. 285 2010 22748 22752
90. K.S. Abd-Elrahman, M.P. Walsh, and W.C. Cole Abnormal Rho-associated kinase activity contributes to the dysfunctional myogenic response of cerebral arteries in type 2 diabetes Can. J. Physiol. Pharmacol. 93 3 2015 177 184 http://dx.doi.org/10.1139/cjpp-2014-0437