Focal adhesion signaling: Vascular smooth muscle cell contractility beyond calcium mechanisms

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art_RIBEIRO-SILVA_Focal_adhesion_signaling_Vascular_smooth_muscle_cell_contractility_2021.PDF (4.99 MB)
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18
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article
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2021
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Scopus
PubMed
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PORTLAND PRESS LTD
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CLINICAL SCIENCE, v.135, n.9, p.1189-1207, 2021
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Unidades Organizacionais
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Resumo
Smooth muscle cell (SMC) contractility is essential to vessel tone maintenance and blood pressure regulation. In response to vasoconstrictors, calcium-dependent mechanisms promote the activation of the regulatory myosin light chain, leading to increased cytoskeleton tension that favors cell shortening. In contrast, SMC maintain an intrinsic level of a contractile force independent of vasoconstrictor stimulation and sustained SMC contraction beyond the timescale of calcium-dependent mechanisms suggesting the involvement of additional players in the contractile response. Focal adhesions (FAs) are conceivable candidates that may influence SMC contraction. They are required for actin-based traction employed by cells to sense and respond to environmental cues in a process termed mechanotransduction. Depletion of FA proteins impairs SMC contractility, producing arteries that are prone to dissection because of a lack of mechanical stability. Here, we discuss the role of calcium-independent FA signaling mechanisms in SMC contractility. We speculate that FA signaling contributes to the genesis of a variety of SMC phenotypes and discuss the potential implications for mechanical homeostasis in normal and diseased states. ©2021 The Author(s).
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https://observatorio.fm.usp.br/handle/OPI/49012
Referências
  1. Wolinsky, H., Glagov, S., A lamellar unit of aortic medial structure and function in mammals (1967) Circ. Res, 20, pp. 99-111. , https://doi.org/10.1161/01.RES.20.1.99, 1
  2. Owens, G.K., Regulation of differentiation of vascular smooth muscle cells (1995) Physiol. Rev, 75, pp. 487-517. , https://doi.org/10.1152/physrev.1995.75.3.487, 2
  3. Majesky, M.W., Neointima formation after acute vascular injury: Role of counteradhesive extracellular matrix proteins (1994) Texas Hear. Inst. J, 21, pp. 78-85. , 3
  4. Jones, J.I., Prevette, T., Gockerman, A., Clemmons, D.R., Ligand occupancy of the alpha-V-beta3 integrin is necessary for smooth muscle cells to migrate in response to insulin-like growth factor (1996) Proc. Natl. Acad. Sci. U.S.A, 93, pp. 2482-2487. , 4
  5. Skinner, M.P., Raines, E.W., Ross, R., Dynamic expression of α1β1 and α2β1 integrin receptors by human vascular smooth muscle cells: α2β1 integrin is required for chemotaxis across type I collagen-coated membranes (1994) Am. J. Pathol, 145, pp. 1070-1081. , 5
  6. Turner, C.E., Pietras, K.M., Taylor, D.S., Molloy, C.J., Angiotensin II stimulation of rapid paxillin tyrosine phosphorylation correlates with the formation of focal adhesions in rat aortic smooth muscle cells (1995) J. Cell Sci, 108, pp. 333-342. , https://doi.org/10.1242/jcs.108.1.333, 6
  7. Schiller, H.B., Friedel, C.C., Boulegue, C., Fä ssler, R., Quantitative proteomics of the integrin adhesome show a myosin II-dependent recruitment of LIM domain proteins (2011) EMBO Rep, 12, pp. 259-266. , https://doi.org/10.1038/embor.2011.5, 7
  8. Zaidel-Bar, R., Cohen, M., Addadi, L., Geiger, B., Hierarchical assembly of cell-matrix adhesion complexes (2004) Biochem. Soc. Trans, 32, pp. 416-420. , https://doi.org/10.1042/bst0320416, 8
  9. Geiger, B., Bershadsky, A., Pankov, R., Yamada, K.M., Transmembrane crosstalk between the extracellular matrix and the cytoskeleton (2001) Nat. Rev. Mol. Cell Biol, 2, pp. 793-805. , https://doi.org/10.1038/35099066, 9
  10. Zargham, R., Thibault, G., α8 Integrin expression is required for maintenance of the smooth muscle cell differentiated phenotype (2006) Cardiovasc. Res, 71, pp. 170-178. , https://doi.org/10.1016/j.cardiores.2006.03.003, 10
  11. Welser, J.V., Lange, N., Singer, C.A., Elorza, M., Scowen, P., Keef, K.D., Loss of the α7 integrin promotes extracellular signal-regulated kinase activation and altered vascular remodeling (2007) Circ. Res, 101, pp. 672-681. , https://doi.org/10.1161/CIRCRESAHA.107.151415, 11
  12. Wynne, B.M., Chiao, C.-W., Webb, R.C., Vascular smooth muscle cell signaling mechanisms for contraction to angiotensin II and endothelin-1 (2009) J. Am. Soc. Hypertens, 3, pp. 84-95. , https://doi.org/10.1016/j.jash.2008.09.002, 35
  13. Michell, R.H., Inositol phospholipids and cell surface receptor function (1975) Biochim. Biophys. Acta Rev. Biomembr, 415, pp. 81-147. , https://doi.org/10.1016/0304-4157(75)90017-9, 36
  14. Mignery, G.A., Sü dhof, T.C., The ligand binding site and transduction mechanism in the inositol-1, 4, 5-triphosphate receptor (1990) EMBO J, 9, pp. 3893-3898. , https://doi.org/10.1002/j.1460-2075.1990.tb07609.x, 37
  15. Malencik, D.A., Anderson, S.R., Bohnert, J.L., Shalitin, Y., Functional interactions between smooth muscle myosin light chain kinase and calmodulin (1982) Biochemistry, 21, pp. 4031-4039. , https://doi.org/10.1021/bi00260a019, 38
  16. Adelstein, R.S., Anne Conti, M., Phosphorylation of platelet myosin increases actin-activated myosin ATPase activity (1975) Nature, 256, pp. 597-598. , https://doi.org/10.1038/256597a0, 39
  17. Ikebe, M., Hartshorne, D.J., Effects of Ca2+ on the conformation and enzymatic activity of smooth muscle myosin (1985) J. Biol. Chem, 260, pp. 13146-13153. , https://doi.org/10.1016/S0021-9258(17)38850-6, 40
  18. Jung, H.S., Billington, N., Thirumurugan, K., Salzameda, B., Cremo, C.R., Chalovich, J.M., Role of the Tail in the regulated state of Myosin 2 (2011) J. Mol. Biol, 408, pp. 863-878. , https://doi.org/10.1016/j.jmb.2011.03.019, 41
  19. Salzameda, B., Facemyer, K.C., Beck, B.W., Cremo, C.R., The N-terminal lobes of both regulatory light chains interact with the tail domain in the 10 S-inhibited conformation of smooth muscle myosin (2006) J. Biol. Chem, 281, pp. 38801-38811. , https://doi.org/10.1074/jbc.M606555200, 42
  20. Applegate, D., Pardee, J., Actin-facilitated assembly of smooth muscle myosin induces formation of actomyosin fibrils (1992) J. Cell Biol, 117, pp. 1223-1230. , https://doi.org/10.1083/jcb.117.6.1223, 43
  21. Gó recka, A., Aksoy, M.O., Hartshorne, D.J., The effect of phosphorylation of gizzard myosin on actin activation (1976) Biochem. Biophys. Res. Commun, 71, pp. 325-331. , https://doi.org/10.1016/0006-291X(76)90286-2, 44
  22. Cipolla, M.J., Osol, G., Vascular smooth muscle actin cytoskeleton in cerebral artery forced dilatation (1998) Stroke, 29, pp. 1223-1228. , https://doi.org/10.1161/01.STR.29.6.1223, 68
  23. Vicente-Manzanares, M., Ma, X., Adelstein, R.S., Horwitz, A.R., Non-muscle myosin II takes centre stage in cell adhesion and migration (2009) Nat. Rev. Mol. Cell Biol, 10, pp. 778-790. , https://doi.org/10.1038/nrm2786, 45
  24. Ikebe, M., Onishi, H., Watanabe, S., Phosphorylation and dephosphorylation of a light chain of the chicken gizzard myosin molecule (1977) J. Biochem, 82, pp. 299-302. , https://doi.org/10.1093/oxfordjournals.jbchem.a131684, 46
  25. Sobieszek, A., Ca-linked phosphorylation of a light chain of vertebrate smooth-muscle myosin (1977) Eur. J. Biochem, 73, pp. 477-483. , https://doi.org/10.1111/j.1432-1033.1977.tb11340.x, 47
  26. Hartshorne, D.J., Ito, M., Erdö di, F., Myosin light chain phosphatase: Subunit composition, interactions and regulation (1998) J. Muscle Res. Cell Motil, 19, pp. 325-341. , https://doi.org/10.1023/A:1005385302064, 48
  27. Woodsome, T.P., Eto, M., Everett, A., Brautigan, D.L., Kitazawa, T., Expression of CPI-17 and myosin phosphatase correlates with Ca 2+ sensitivity of protein kinase C-induced contraction in rabbit smooth muscle (2001) J. Physiol, 535, pp. 553-564. , https://doi.org/10.1111/j.1469-7793.2001.t01-1-00553.x, 49
  28. Eto, M., Kitazawa, T., Matsuzawa, F., Aikawa, S., Kirkbride, J.A., Isozumi, N., Phosphorylation-induced conformational switching of CPI-17 produces a potent myosin phosphatase inhibitor (2007) Structure, 15, pp. 1591-1602. , https://doi.org/10.1016/j.str.2007.10.014, 50
  29. Kitazawa, T., Eto, M., Woodsome, T.P., Brautigan, D.L., Agonists trigger G protein-mediated activation of the CPI-17 inhibitor phosphoprotein of myosin light chain phosphatase to enhance vascular smooth muscle contractility (2000) J. Biol. Chem, 275, pp. 9897-9900. , https://doi.org/10.1074/jbc.275.14.9897, 51
  30. Benham, C.D., Hess, P., Tsien, R.W., Two types of calcium channels in single smooth muscle cells from rabbit ear artery studied with whole-cell and single-channel recordings (1987) Circ. Res, 61, pp. I10-I16. , 52
  31. Collier, M.L., Ji, G., Wang, Y.-X., Kotlikoff, M.I., Calcium-induced calcium release in smooth muscle (2000) J. Gen. Physiol, 115, pp. 653-662. , https://doi.org/10.1085/jgp.115.5.653, 53
  32. Knot, H.J., Nelson, M.T., Regulation of arterial diameter and wall [Ca 2+[ in cerebral arteries of rat by membrane potential and intravascular pressure (1998) J. Physiol, 508, pp. 199-209. , https://doi.org/10.1111/j.1469-7793.1998.199br.x, 54
  33. Cipolla, M.J., Gokina, N.I., Osol, G., Pressure-induced actin polymerization in vascular smooth muscle as a mechanism underlying myogenic behavior (2002) FASEB J, 16, pp. 72-76. , https://doi.org/10.1096/cj.01-0104hyp, 69
  34. Prakriya, M., Lewis, R.S., Store-operated calcium channels (2015) Physiol. Rev, 95, pp. 1383-1436. , https://doi.org/10.1152/physrev.00020.2014, 55
  35. Albert, A.P., Gating mechanisms of canonical transient receptor potential channel proteins: Role of phosphoinositols and diacylglycerol (2011) Advances in Experimental Medicine and Biology, 704, pp. 391-411. , https://doi.org/10.1007/978-94-007-0265-3?22, 56 ISBN 9789400702646
  36. Earley, S., Brayden, J.E., Transient receptor potential channels in the vasculature (2015) Physiol. Rev, 95, pp. 645-690. , https://doi.org/10.1152/physrev.00026.2014, 57
  37. Martinsen, A., Dessy, C., Morel, N., Regulation of calcium channels in smooth muscle: New insights into the role of myosin light chain kinase (2014) Channels, 8, pp. 402-413. , https://doi.org/10.4161/19336950.2014.950537, 58
  38. Hill, M.A., Potocnik, S.J., Martinez-Lemus, L.A., Meininger, G.A., Delayed arteriolar relaxation after prolonged agonist exposure: Functional remodeling involving tyrosine phosphorylation (2003) Am. J. Physiol. Circ. Physiol, 285, pp. H849-H856. , https://doi.org/10.1152/ajpheart.00986.2002, 59
  39. Rembold, C.M., Force suppression and the crossbridge cycle in swine carotid artery (2007) Am. J. Physiol. Cell Physiol, 293, pp. C1003-C1009. , https://doi.org/10.1152/ajpcell.00091.2007, 60
  40. Rasmussen, H., Takuwa, Y., Park, S., Protein kinase C in the regulation of smooth muscle contraction (1987) FASEB J, 1, pp. 177-185. , https://doi.org/10.1096/fasebj.1.3.3040504, 61
  41. Martinez-Lemus, L.A., Persistent agonist-induced vasoconstriction is not required for angiotensin II to mediate inward remodeling of isolated arterioles with myogenic tone (2008) J. Vasc. Res, 45, pp. 211-221. , https://doi.org/10.1159/000112513, 62
  42. Martinez-Lemus, L.A., Hill, M.A., Bolz, S.S., Pohl, U., Meininger, G.A., Acute mechanoadaptation of vascular smooth muscle cells in response to continuous arteriolar vasoconstriction: Implications for functional remodeling (2004) FASEB J, 18, pp. 708-710. , https://doi.org/10.1096/fj.03-0634fje, 63
  43. Fultz, M.E., Li, C., Geng, W., Wright, G.L., Remodeling of the actin cytoskeleton in the contracting A7r5 smooth muscle cell (2000) J. Muscle Res. Cell Motil, 21, pp. 775-787. , https://doi.org/10.1023/A:1010396429297, 64
  44. Adler, K.B., Krill, J., Alberghini, T.V., Evans, J.N., Effect of cytochalasin D on smooth muscle contraction (1983) Cell Motil, 3, pp. 545-551. , https://doi.org/10.1002/cm.970030521, 70
  45. Chen, X., Pavlish, K., Zhang, H.-Y., Benoit, J.N., Effects of chronic portal hypertension on agonist-induced actin polymerization in small mesenteric arteries (2006) Am. J. Physiol. Circ. Physiol, 290, pp. H1915-H1921. , https://doi.org/10.1152/ajpheart.00643.2005, 65
  46. Anfinogenova, Y., Wang, R., Li, Q., Spinelli, A.M., Tang, D.D., Abl silencing inhibits CAS-mediated process and constriction in resistance arteries (2007) Circ. Res, 101, pp. 420-428. , https://doi.org/10.1161/CIRCRESAHA.107.156463, 66
  47. Shaw, L., Ahmed, S., Austin, C., Taggart, M.J., Inhibitors of actin filament polymerisation attenuate force but not global intracellular calcium in isolated pressurised resistance arteries (2003) J. Vasc. Res, 40, pp. 1-10. , https://doi.org/10.1159/000068940, 67
  48. Wright, G., Hurn, E., Cytochalasin inhibition of slow tension increase in rat aortic rings (1994) Am. J. Physiol. Circ. Physiol, 267, pp. H1437-H1446. , https://doi.org/10.1152/ajpheart.1994.267.4.H1437, 71
  49. Cipolla, M.J., Gokina, N.I., Osol, G., Pressure-induced actin polymerization in vascular smooth muscle as a mechanism underlying myogenic behavior (2002) FASEB J, 16, pp. 72-76. , https://doi.org/10.1096/cj.01-0104hyp, 72
  50. Ghosh, S., Kollar, B., Nahar, T., Suresh Babu, S., Wojtowicz, A., Sticht, C., Loss of the mechanotransducer Zyxin promotes a synthetic phenotype of vascular smooth muscle cells (2015) J. Am. Heart Assoc, 4, p. e001712. , https://doi.org/10.1161/JAHA.114.001712, 73
  51. Sun, Z., Huang, S., Li, Z., Meininger, G.A., Zyxin is involved in regulation of mechanotransduction in arteriole smooth muscle cells (2012) Front. Physiol, 3, p. 472. , https://doi.org/10.3389/fphys.2012.00472, 74
  52. Ohanian, V., Gatfield, K., Ohanian, J., Role of the actin cytoskeleton in G-protein-coupled receptor activation of PYK2 and Paxillin in vascular smooth muscle (2005) Hypertension, 46, pp. 93-99. , https://doi.org/10.1161/01.HYP.0000167990.82235.3c, 75
  53. Li, J., Su, Y., Xia, W., Qin, Y., Humphries, M.J., Vestweber, D., Conformational equilibria and intrinsic affinities define integrin activation (2017) EMBO J, 36, pp. 629-645. , https://doi.org/10.15252/embj.201695803, 76
  54. Galbraith, C.G., Yamada, K.M., Sheetz, M.P., The relationship between force and focal complex development (2002) J. Cell Biol, 159, pp. 695-705. , https://doi.org/10.1083/jcb.200204153, 77
  55. Chen, L., Vicente-Manzanares, M., Potvin-Trottier, L., Wiseman, P.W., Horwitz, A.R., The integrin-ligand interaction regulates adhesion and migration through a molecular clutch (2012) PLoS ONE, 7, p. e40202. , https://doi.org/10.1371/journal.pone.0040202, 101
  56. Zaidel-Bar, R., Itzkovitz, S., Ma'ayan, A., Iyengar, R., Geiger, B., Functional atlas of the integrin adhesome (2007) Nat. Cell Biol, 9, pp. 858-867. , https://doi.org/10.1038/ncb0807-858, 78
  57. Horton, E.R., Byron, A., Askari, J.A., Ng, D.H.J., Millon-Frémillon, A., Robertson, J., Definition of a consensus integrin adhesome and its dynamics during adhesion complex assembly and disassembly (2015) Nat. Cell Biol, 17, pp. 1577-1587. , https://doi.org/10.1038/ncb3257, 79
  58. Kanchanawong, P., Shtengel, G., Pasapera, A.M., Ramko, E.B., Davidson, M.W., Hess, H.F., Nanoscale architecture of integrin-based cell adhesions (2010) Nature, 468, pp. 580-584. , https://doi.org/10.1038/nature09621, 80
  59. Case, L.B., Baird, M.A., Shtengel, G., Campbell, S.L., Hess, H.F., Davidson, M.W., Molecular mechanism of vinculin activation and nanoscale spatial organization in focal adhesions (2015) Nat. Cell Biol, 17, pp. 880-892. , https://doi.org/10.1038/ncb3180, 81
  60. Paszek, M.J., DuFort, C.C., Rubashkin, M.G., Davidson, M.W., Thorn, K.S., Liphardt, J.T., Scanning angle interference microscopy reveals cell dynamics at the nanoscale (2012) Nat. Methods, 9, pp. 825-827. , https://doi.org/10.1038/nmeth.2077, 82
  61. del Rio, A., Perez-Jimenez, R., Liu, R., Roca-Cusachs, P., Fernandez, J.M., Sheetz, M.P., Stretching single talin rod molecules activates vinculin binding (2009) Science, 323, pp. 638-641. , https://doi.org/10.1126/science.1162912, 83
  62. Carisey, A., Tsang, R., Greiner, A.M., Nijenhuis, N., Heath, N., Nazgiewicz, A., Vinculin regulates the recruitment and release of core focal adhesion proteins in a force-dependent manner (2013) Curr. Biol, 23, pp. 271-281. , https://doi.org/10.1016/j.cub.2013.01.009, 84
  63. Atherton, P., Stutchbury, B., Wang, D.-Y., Jethwa, D., Tsang, R., Meiler-Rodriguez, E., Vinculin controls talin engagement with the actomyosin machinery (2015) Nat. Commun, 6, p. 10038. , https://doi.org/10.1038/ncomms10038, 85
  64. Yao, M., Goult, B.T., Chen, H., Cong, P., Sheetz, M.P., Yan, J., Mechanical activation of vinculin binding to talin locks talin in an unfolded conformation (2015) Sci. Rep, 4, p. 4610. , https://doi.org/10.1038/srep04610, 86
  65. Elosegui-Artola, A., Oria, R., Chen, Y., Kosmalska, A., Pé rez-Gonzá lez, C., Castro, N., Mechanical regulation of a molecular clutch defines force transmission and transduction in response to matrix rigidity (2016) Nat. Cell Biol, 18, pp. 540-548. , https://doi.org/10.1038/ncb3336, 87
  66. Seong, J., Tajik, A., Sun, J., Guan, J.-L., Humphries, M.J., Craig, S.E., Distinct biophysical mechanisms of focal adhesion kinase mechanoactivation by different extracellular matrix proteins (2013) Proc. Natl. Acad. Sci. U.S.A, 110, pp. 19372-19377. , https://doi.org/10.1073/pnas.1307405110, 102
  67. Zhang, X., Jiang, G., Cai, Y., Monkley, S.J., Critchley, D.R., Sheetz, M.P., Talin depletion reveals independence of initial cell spreading from integrin activation and traction (2008) Nat. Cell Biol, 10, pp. 1062-1068. , https://doi.org/10.1038/ncb1765, 88
  68. Cluzel, C., Saltel, F., Lussi, J., Paulhe, F., Imhof, B.A., Wehrle-Haller, B., The mechanisms and dynamics of αvβ3 integrin clustering in living cells (2005) J. Cell Biol, 171, pp. 383-392. , https://doi.org/10.1083/jcb.200503017, 89
  69. Min, J., Reznichenko, M., Poythress, R.H., Gallant, C.M., Vetterkind, S., Li, Y., Src modulates contractile vascular smooth muscle function via regulation of focal adhesions (2012) J. Cell. Physiol, 227, pp. 3585-3592. , https://doi.org/10.1002/jcp.24062, 90
  70. Gao, Y.Z., Saphirstein, R.J., Yamin, R., Suki, B., Morgan, K.G., Aging impairs smooth muscle-mediated regulation of aortic stiffness: A defect in shock absorption function? (2014) Am. J. Physiol. Circ. Physiol, 307, pp. H1252-H1261. , https://doi.org/10.1152/ajpheart.00392.2014, 91
  71. Lehoux, S., Esposito, B., Merval, R., Tedgui, A., Differential regulation of vascular focal adhesion kinase by steady stretch and pulsatility (2005) Circulation, 111, pp. 643-649. , https://doi.org/10.1161/01.CIR.0000154548.16191.2F, 92
  72. Albinsson, S., Hellstrand, P., Integration of signal pathways for stretch-dependent growth and differentiation in vascular smooth muscle (2007) Am. J. Physiol. Cell Physiol, 293, pp. C772-C782. , https://doi.org/10.1152/ajpcell.00622.2006, 93
  73. Saphirstein, R.J., Gao, Y.Z., Jensen, M.H., Gallant, C.M., Vetterkind, S., Moore, J.R., The focal adhesion: A regulated component of aortic stiffness (2013) PLoS ONE, 8, p. e62461. , https://doi.org/10.1371/journal.pone.0062461, 94
  74. George, E.L., Baldwin, H.S., Hynes, R.O., Fibronectins are essential for heart and blood vessel morphogenesis but are dispensable for initial specification of precursor cells (1997) Blood, 90, pp. 3073-3081. , https://doi.org/10.1182/blood.V90.8.3073, 95
  75. Hong, Z., Sun, Z., Li, Z., Mesquitta, W.-T., Trzeciakowski, J.P., Meininger, G.A., Coordination of fibronectin adhesion with contraction and relaxation in microvascular smooth muscle (2012) Cardiovasc. Res, 96, pp. 73-80. , https://doi.org/10.1093/cvr/cvs239, 96
  76. Hong, Z., Sun, Z., Li, M., Li, Z., Bunyak, F., Ersoy, I., Vasoactive agonists exert dynamic and coordinated effects on vascular smooth muscle cell elasticity, cytoskeletal remodelling and adhesion (2014) J. Physiol, 592, pp. 1249-1266. , https://doi.org/10.1113/jphysiol.2013.264929, 97
  77. Hanks, S.K., Focal adhesion kinase signaling activities and their implications in the control of cell survival and motility (2003) Front. Biosci, 8, p. 1114. , https://doi.org/10.2741/1114, 103
  78. Moraes, J.A., Frony, A.C., Dias, A.M., Renovato-Martins, M., Rodrigues, G., Marcinkiewicz, C., Data in support of alpha1beta1 and integrin-linked kinase interact and modulate angiotensin II effects in vascular smooth muscle cells (2016) Data Brief, 6, pp. 330-340. , https://doi.org/10.1016/j.dib.2015.11.053, 98
  79. Moraes, J.A., Frony, A.C., Dias, A.M., Renovato-Martins, M., Rodrigues, G., Marcinkiewicz, C., Alpha1beta1 and integrin-linked kinase interact and modulate angiotensin II effects in vascular smooth muscle cells (2015) Atherosclerosis, 243, pp. 477-485. , https://doi.org/10.1016/j.atherosclerosis.2015.09.026, 99
  80. Tamura, K., Okazaki, M., Tamura, M., Kanegae, K., Okuda, H., Abe, H., Synergistic interaction of integrin and angiotensin II in activation of extracellular signal-regulated kinase pathways in vascular smooth muscle cells (2001) J. Cardiovasc. Pharmacol, 38, pp. S59-S62. , https://doi.org/10.1097/00005344-200110001-00013, 100
  81. Hu, X.-Q., Singh, N., Mukhopadhyay, D., Akbarali, H.I., Modulation of voltage-dependent Ca2+ channels in rabbit colonic smooth muscle cells by c-Src and focal adhesion kinase (1998) J. Biol. Chem, 273, pp. 5337-5342. , https://doi.org/10.1074/jbc.273.9.5337, 104
  82. Mogford, J.E., Davis, G.E., Platts, S.H., Meininger, G.A., Vascular smooth muscle α v β 3 integrin mediates arteriolar vasodilation in response to RGD peptides (1996) Circ. Res, 79, pp. 821-826. , https://doi.org/10.1161/01.RES.79.4.821, 105
  83. D'Angelo, G., Mogford, J.E., Davis, G.E., Davis, M.J., Meininger, G.A., Integrin-mediated reduction in vascular smooth muscle [Ca2+]i induced by RGD-containing peptide (1997) Am. J. Physiol. Circ. Physiol, 272, pp. H2065-H2070. , https://doi.org/10.1152/ajpheart.1997.272.4.H2065, 106
  84. Wu, X., Mogford, J.E., Platts, S.H., Davis, G.E., Meininger, G.A., Davis, M.J., Modulation of calcium current in arteriolar smooth muscle by αvβ3 and α5β1 integrin ligands (1998) J. Cell Biol, 143, pp. 241-252. , https://doi.org/10.1083/jcb.143.1.241, 107
  85. Callera, G.E., Antunes, T.T., He, Y., Montezano, A.C., Yogi, A., Savoia, C., c-Src inhibition improves cardiovascular function but not remodeling or fibrosis in angiotensin II-induced hypertension (2016) Hypertension, 68, pp. 1179-1190. , https://doi.org/10.1161/HYPERTENSIONAHA.116.07699, 108
  86. Touyz, R.M., Wu, X.-H., He, G., Park, J.B., Chen, X., Vacher, J., Role of c-Src in the regulation of vascular contraction and Ca2+ signaling by angiotensin II in human vascular smooth muscle cells (2001) J. Hypertens, 19, pp. 441-449. , https://doi.org/10.1097/00004872-200103000-00012, 109
  87. Wu, X., Davis, G.E., Meininger, G.A., Wilson, E., Davis, M.J., Regulation of the L-type calcium channel by α 5 β 1 integrin requires signaling between focal adhesion proteins (2001) J. Biol. Chem, 276, pp. 30285-30292. , https://doi.org/10.1074/jbc.M102436200, 110
  88. Zargham, R., Touyz, R.M., Thibault, G., α8 Integrin overexpression in de-differentiated vascular smooth muscle cells attenuates migratory activity and restores the characteristics of the differentiated phenotype (2007) Atherosclerosis, 195, pp. 303-312. , https://doi.org/10.1016/j.atherosclerosis.2007.01.005, 12
  89. Jia, L., Tang, D.D., Abl activation regulates the dissociation of CAS from cytoskeletal vimentin by modulating CAS phosphorylation in smooth muscle (2010) Am. J. Physiol. Cell Physiol, 299, pp. C630-C637. , https://doi.org/10.1152/ajpcell.00095.2010, 111
  90. Ushio-Fukai, M., Zuo, L., Ikeda, S., Tojo, T., Patrushev, N.A., Alexander, R.W., cAbl tyrosine kinase mediates reactive oxygen species- A nd caveolin-dependent AT 1 receptor signaling in vascular smooth muscle (2005) Circ. Res, 97, pp. 829-836. , https://doi.org/10.1161/01.RES.0000185322.46009.F5, 112
  91. Chen, S., Wang, R., Li, Q.-F., Tang, D.D., Abl knockout differentially affects p130 Crk-associated substrate, vinculin, and paxillin in blood vessels of mice (2009) Am. J. Physiol. Circ. Physiol, 297, pp. H533-H539. , https://doi.org/10.1152/ajpheart.00237.2009, 113
  92. Bö ttcher, R.T., Veelders, M., Rombaut, P., Faix, J., Theodosiou, M., Stradal, T.E., Kindlin-2 recruits paxillin and Arp2/3 to promote membrane protrusions during initial cell spreading (2017) J. Cell Biol, 216, pp. 3785-3798. , https://doi.org/10.1083/jcb.201701176, 114
  93. Pasapera, A.M., Schneider, I.C., Rericha, E., Schlaepfer, D.D., Waterman, C.M., Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation (2010) J. Cell Biol, 188, pp. 877-890. , https://doi.org/10.1083/jcb.200906012, 115
  94. Schneider, I.C., Hays, C.K., Waterman, C.M., Epidermal growth factor-induced contraction regulates paxillin phosphorylation to temporally separate traction generation from de-adhesion (2009) Mol. Biol. Cell, 20, pp. 3155-3167. , https://doi.org/10.1091/mbc.e09-03-0219, 116
  95. Zaidel-Bar, R., Milo, R., Kam, Z., Geiger, B., A paxillin tyrosine phosphorylation switch regulates the assembly and form of cell-matrix adhesions (2006) J. Cell Sci, 120, pp. 137-148. , https://doi.org/10.1242/jcs.03314, 117
  96. Friedland, J.C., Lee, M.H., Boettiger, D., Mechanically activated integrin switch controls α5β1 function (2009) Science, 323, pp. 642-644. , https://doi.org/10.1126/science.1168441, 118
  97. Strohmeyer, N., Bharadwaj, M., Costell, M., Fä ssler, R., Mü ller, D.J., Fibronectin-bound α5β1 integrins sense load and signal to reinforce adhesion in less than a second (2017) Nat. Mater, 16, pp. 1262-1270. , https://doi.org/10.1038/nmat5023, 119
  98. Plotnikov, S.V., Pasapera, A.M., Sabass, B., Waterman, C.M., Force fluctuations within focal adhesions mediate ECM-rigidity sensing to guide directed cell migration (2012) Cell, 151, pp. 1513-1527. , https://doi.org/10.1016/j.cell.2012.11.034, 120
  99. Sundberg-Smith, L.J., DiMichele, L.A., Sayers, R.L., Mack, C.P., Taylor, J.M., The LIM protein leupaxin is enriched in smooth muscle and functions as an serum response factor cofactor to induce smooth muscle cell gene transcription (2008) Circ. Res, 102, pp. 1502-1511. , https://doi.org/10.1161/CIRCRESAHA.107.170357, 13
  100. Guilluy, C., Swaminathan, V., Garcia-Mata, R., Timothy O'Brien, E., Superfine, R., Burridge, K., The Rho GEFs LARG and GEF-H1 regulate the mechanical response to force on integrins (2011) Nat. Cell Biol, 13, pp. 722-727. , https://doi.org/10.1038/ncb2254, 121
  101. Tang, D.D., Tan, J., Role of Crk-associated substrate in the regulation of vascular smooth muscle contraction (2003) Hypertension, 42, pp. 858-863. , https://doi.org/10.1161/01.HYP.0000085333.76141.33, 122
  102. Ogden, K., Thompson, J.M., Hickner, Z., Huang, T., Tang, D.D., Watts, S.W., A new signaling paradigm for serotonin: Use of Crk-associated substrate in arterial contraction (2006) Am. J. Physiol. Circ. Physiol, 291, pp. H2857-H2863. , https://doi.org/10.1152/ajpheart.00229.2006, 123
  103. Roca-Cusachs, P., del Rio, A., Puklin-Faucher, E., Gauthier, N.C., Biais, N., Sheetz, M.P., Integrin-dependent force transmission to the extracellular matrix by-actinin triggers adhesion maturation (2013) Proc. Natl. Acad. Sci. U.S.A, 110, pp. E1361-E1370. , https://doi.org/10.1073/pnas.1220723110, 124
  104. Chereau, D., Dominguez, R., Understanding the role of the G-actin-binding domain of Ena/VASP in actin assembly (2006) J. Struct. Biol, 155, pp. 195-201. , https://doi.org/10.1016/j.jsb.2006.01.012, 125
  105. Schirenbeck, A., Arasada, R., Bretschneider, T., Stradal, T.E.B., Schleicher, M., Faix, J., The bundling activity of vasodilator-stimulated phosphoprotein is required for filopodium formation (2006) Proc. Natl. Acad. Sci. U.S.A, 103, pp. 7694-7699. , https://doi.org/10.1073/pnas.0511243103, 126
  106. Hü ttelmaier, S., Harbeck, B., Steffens, N.O., Meßerschmidt, T., Illenberger, S., Jockusch, B.M., Characterization of the actin binding properties of the vasodilator-stimulated phosphoprotein VASP (1999) FEBS Lett, 451, pp. 68-74. , https://doi.org/10.1016/S0014-5793(99)00546-3, 127
  107. Bear, J.E., Svitkina, T.M., Krause, M., Schafer, D.A., Loureiro, J.J., Strasser, G.A., Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility (2002) Cell, 109, pp. 509-521. , https://doi.org/10.1016/S0092-8674(02)00731-6, 128
  108. Barzik, M., Kotova, T.I., Higgs, H.N., Hazelwood, L., Hanein, D., Gertler, F.B., Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins (2005) J. Biol. Chem, 280, pp. 28653-28662. , https://doi.org/10.1074/jbc.M503957200, 129
  109. Bundschu, K., Walter, U., Schuh, K., The VASP-Spred-Sprouty domain puzzle (2006) J. Biol. Chem, 281, pp. 36477-36481. , https://doi.org/10.1074/jbc.R600023200, 130
  110. Staus, D.P., Blaker, A.L., Taylor, J.M., Mack, C.P., Diaphanous 1 and 2 regulate smooth muscle cell differentiation by activating the myocardin-related transcription factors (2007) Arterioscler. Thromb. Vasc. Biol, 27, pp. 478-486. , https://doi.org/10.1161/01.ATV.0000255559.77687.c1, 14
  111. Zhuang, S., Nguyen, G.T., Chen, Y., Gudi, T., Eigenthaler, M., Jarchau, T., Vasodilator-stimulated phosphoprotein activation of serum-response element-dependent transcription occurs downstream of RhoA and is inhibited by cGMP-dependent protein kinase phosphorylation (2004) J. Biol. Chem, 279, pp. 10397-10407. , https://doi.org/10.1074/jbc.M313048200, 131
  112. Blume, C., Benz, P.M., Walter, U., Ha, J., Kemp, B.E., Renné, T., AMP-activated protein kinase impairs endothelial actin cytoskeleton assembly by phosphorylating vasodilator-stimulated phosphoprotein (2007) J. Biol. Chem, 282, pp. 4601-4612. , https://doi.org/10.1074/jbc.M608866200, 132
  113. Defawe, O.D., Kim, S., Chen, L., Huang, D., Kenagy, R.D., Renné, T., VASP phosphorylation at serine239 regulates the effects of NO on smooth muscle cell invasion and contraction of collagen (2010) J. Cell. Physiol, 222, pp. 230-237. , https://doi.org/10.1002/jcp.21942, 133
  114. Tang, D.D., Gunst, S.J., The small GTPase Cdc42 regulates actin polymerization and tension development during contractile stimulation of smooth muscle (2004) J. Biol. Chem, 279, pp. 51722-51728. , https://doi.org/10.1074/jbc.M408351200, 15
  115. Tang, D.D., Zhang, W., Gunst, S.J., The adapter protein CrkII regulates neuronal Wiskott-Aldrich syndrome protein, actin polymerization, and tension development during contractile stimulation of smooth muscle (2005) J. Biol. Chem, 280, pp. 23380-23389. , https://doi.org/10.1074/jbc.M413390200, 16
  116. Pollard, T.D., Blanchoin, L., Mullins, R.D., Molecular mechanisms controlling actin filament dynamics in nonmuscle cells (2000) Annu. Rev. Biophys. Biomol. Struct, 29, pp. 545-576. , https://doi.org/10.1146/annurev.biophys.29.1.545, 17
  117. Takahashi, T., Kawahara, Y., Taniguchi, T., Yokoyama, M., Tyrosine phosphorylation and association of p130 Cas and c-Crk II by ANG II in vascular smooth muscle cells (1998) Am. J. Physiol. Circ. Physiol, 274, pp. H1059-H1065. , https://doi.org/10.1152/ajpheart.1998.274.4.H1059, 18
  118. Rohatgi, R., Nollau, P., Ho, H.-Y.H., Kirschner, M.W., Mayer, B.J., Nck and phosphatidylinositol 4, 5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 pathway (2001) J. Biol. Chem, 276, pp. 26448-26452. , https://doi.org/10.1074/jbc.M103856200, 19
  119. Tang, D.D., Critical role of actin-associated proteins in smooth muscle contraction, cell proliferation, airway hyperresponsiveness and airway remodeling (2015) Respir Res, 16, p. 134. , https://doi.org/10.1186/s12931-015-0296-1, 20
  120. Gunst, S.J., Zhang, W., Actin cytoskeletal in smooth muscle: A new paradigm for the regulation of smooth muscle contraction (2008) Am. J. Physiol. Cell Physiol, 295, pp. C576-C587. , https://doi.org/10.1152/ajpcell.00253.2008, 21
  121. Milewicz, D.M., Michael, K., Fisher, N., Coselli, J.S., Markello, T., Biddinger, A., Fibrillin-1 (FBN1) mutations in patients with thoracic aortic aneurysms (1996) Circulation, 94, pp. 2708-2711. , https://doi.org/10.1161/01.CIR.94.11.2708, 22
  122. Shen, D., Li, J., Lepore, J.J., Anderson, T.J.T., Sinha, S., Lin, A.Y., Aortic aneurysm generation in mice with targeted deletion of integrin-linked kinase in vascular smooth muscle cells (2011) Circ. Res, 109, pp. 616-628. , https://doi.org/10.1161/CIRCRESAHA.110.239343, 23
  123. Arnold, T.D., Zang, K., Vallejo-Illarramendi, A., Deletion of integrin-linked kinase from neural crest cells in mice results in aortic aneurysms and embryonic lethality (2013) Dis. Model Mech, 6, pp. 1205-1212. , https://doi.org/10.1242/dmm.011866, 24
  124. Brozovich, F.V., Nicholson, C.J., Degen, C.V., Gao, Y.Z., Aggarwal, M., Morgan, K.G., Mechanisms of vascular smooth muscle contraction and the basis for pharmacologic treatment of smooth muscle disorders (2016) Pharmacol. Rev, 68, pp. 476-532. , https://doi.org/10.1124/pr.115.010652, 25
  125. Apter, J.T., Marquez, E., Correlation of visco-elastic properties of large arteries with microscopic structure (1968) Circ. Res, 22, pp. 393-404. , https://doi.org/10.1161/01.RES.22.3.393, 26
  126. Bia, D., Zó calo, Y., Cabrera-Fischer, E.I., Wray, S., Armentano, R.L., Quantitative analysis of the relationship between blood vessel wall constituents and viscoelastic properties: Dynamic biomechanical and structural in vitro studies in aorta and carotid arteries (2014) Physiol. J, 2014, pp. 1-9. , https://doi.org/10.1155/2014/142421, 27
  127. Fisher, S.A., Vascular smooth muscle phenotypic diversity and function (2010) Physiol. Genomics, 42A, pp. 169-187. , https://doi.org/10.1152/physiolgenomics.00111.2010, 28
  128. Squire, J.M., Muscle filament structure and muscle contraction (1975) Annu. Rev. Biophys. Bioeng, 4, pp. 137-163. , https://doi.org/10.1146/annurev.bb.04.060175.001033, 29
  129. Liu, J.C.Y., Rottler, J., Wang, L., Zhang, J., Pascoe, C.D., Lan, B., Myosin filaments in smooth muscle cells do not have a constant length (2013) J. Physiol, 591, pp. 5867-5878. , https://doi.org/10.1113/jphysiol.2013.264168, 30
  130. Craig, R., Megerman, J., Assembly of smooth muscle myosin into side-polar filaments (1977) J. Cell Biol, 75, pp. 990-996. , https://doi.org/10.1083/jcb.75.3.990, 31
  131. Cooke, P.H., Fay, F.S., Craig, R., Myosin filaments isolated from skinned amphibian smooth muscle cells are side-polar (1989) J. Muscle Res. Cell Motil, 10, pp. 206-220. , https://doi.org/10.1007/BF01739811, 32
  132. Xu, J.Q., Harder, B.A., Uman, P., Craig, R., Myosin filament structure in vertebrate smooth muscle (1996) J. Cell Biol, 134, pp. 53-66. , https://doi.org/10.1083/jcb.134.1.53, 33
  133. Ingber, D.E., Cellular mechanotransduction: Putting all the pieces together again (2006) FASEB J, 20, pp. 811-827. , https://doi.org/10.1096/fj.05-5424rev, 34

Coleções
Artigos e Materiais de Revistas Científicas - FM/MCP
Artigos e Materiais de Revistas Científicas - HC/InCor
Artigos e Materiais de Revistas Científicas - LIM/13