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Abstract
Vascular smooth muscle cells (VSMCs) are the predominant cell type in the arterial wall and normally adopt a quiescent, contractile phenotype to regulate vascular tone. In the arterial wall, VSMCs are exposed to multiple mechanical cues, including stretch and matrix stiffness, which regulate VSMC contraction. However, during ageing and in vascular disease, such as atherosclerosis, hypertension and vascular calcification, the arterial wall stiffens and VSMC contraction contributes to this process. VSMCs display remarkable plasticity and changes in their mechanical environment promote VSMCs to adopt a proliferative, synthetic phenotype. VSMC phenotypic modulation is associated with altered expression of contractile proteins that generate actomyosin-based force. However, our understanding of precise mechanisms whereby altered mechanical landscape and mechanotransduction influence VSMC contraction remains limited. In this review, we discuss the present literature describing how VSMCs sense and respond to changes in their mechanical environment and how these changes influence VSMC contraction.
Keywords
Matrix stiffness
/
mechanotransduction
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vascular smooth muscle cell
/
contraction
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Sultan Ahmed, Derek T. Warren.
Vascular smooth muscle cell contractile function and mechanotransduction.
Vessel Plus, 2018, 2(1): 36 DOI:10.20517/2574-1209.2018.51
| [1] |
Bhatnagar P,Wilkins E.Trends in the epidemiology of cardiovascular disease in the UK..Heart2016;102:1945-52 PMCID:PMC5256396
|
| [2] |
Islam AM,Paul T.Cardiovascular disease in Bangladesh: a review..Bangladesh Heart J2016;31:80-99
|
| [3] |
Ness AR.Fruit and vegetables, and cardiovascular disease: a review..Int J Epidemiol1997;26:1-13
|
| [4] |
Stewart J,Wilkinson P.Primary prevention of cardiovascular disease: a review of contemporary guidance and literature..JRSM Cardiovasc Dis2017;6:2048004016687211 PMCID:PMC5331469
|
| [5] |
Sun LY,Zahra A.Risk factors of cardiovascular disease and their related socio-economical, environmental and health behavioral factors: focused on low-middle income countries-a narrative review article..Iran J Public Health2015;44:435-44 PMCID:PMC4441956
|
| [6] |
Södergren M.Lifestyle predictors of healthy ageing in men..Maturitas2013;75:113-7
|
| [7] |
Jani B.Ageing and vascular ageing..Postgrad Med J2006;82:357-62 PMCID:PMC2563742
|
| [8] |
Cecelja M.Role of arterial stiffness in cardiovascular disease..JRSM Cardiovasc Dis2012; PMCID:PMC3738327
|
| [9] |
Strait JB.Aging-associated cardiovascular changes and their relationship to heart failure..Heart Fail Clin2012;8:143-64 PMCID:PMC3223374
|
| [10] |
Ungvari Z,de Cabo R,Csiszar A.Mechanisms of vascular aging: new perspectives..J Gerontol A Biol Sci Med Sci2010;65:1028-41 PMCID:PMC2950814
|
| [11] |
Palombo C.Arterial stiffness, atherosclerosis and cardiovascular risk: pathophysiologic mechanisms and emerging clinical indications..Vascul Pharmacol2016;77:1-7
|
| [12] |
Mitchell GF.Arterial stiffness and hypertension..Hypertension2014;64:13-8 PMCID:PMC4063409
|
| [13] |
Safar ME,Blacher J.Obesity, arterial stiffness, and cardiovascular risk..J Am Soc Nephrol2006;17:S109-11
|
| [14] |
Mitchell GF,Vasan RS,Pencina MJ.Arterial stiffness and cardiovascular events: the Framingham heart study..Circulation2010;121:505-11 PMCID:PMC2836717
|
| [15] |
Sethi S,Oliveros R.Aortic stiffness: pathophysiology, clinical implications, and approach to treatment..Integr Blood Press Control2014;7:29-34 PMCID:PMC4046515
|
| [16] |
Shirwany NA.Arterial stiffness: a brief review..Acta Pharmacol Sin2010;31:1267-76 PMCID:PMC3078647
|
| [17] |
DeLoach SS.Vascular stiffness: its measurement and significance for epidemiologic and outcome studies..Clin J Am Soc Nephrol2008;3:184-92
|
| [18] |
Tsamis A,Vorp DA.Elastin and collagen fibre microstructure of the human aorta in ageing and disease: a review..J R Soc Interface2013;10:20121004 PMCID:PMC3645409
|
| [19] |
Belz GG.Elastic properties and windkessel function of the human aorta..Cardiovasc Drugs Ther1995;9:73-83
|
| [20] |
Steed MM,Sen U,Joshua IG.Functional consequences of the collagen/elastin switch in vascular remodeling in hyperhomocysteinemic wild-type, eNOS-/-, and iNOS-/- mice..Am J Physiol Lung Cell Mol Physiol2010;299:L301-11 PMCID:PMC2951073
|
| [21] |
Wagenseil JE.Vascular extracellular matrix and arterial mechanics..Physiol Rev2009;89:957-89 PMCID:PMC2775470
|
| [22] |
Jufri NF,Avolio A.Mechanical stretch: physiological and pathological implications for human vascular endothelial cells..Vasc Cell2015;7:8 PMCID:PMC4575492
|
| [23] |
Humphrey JD.Mechanisms of arterial remodeling in hypertension: coupled roles of wall shear and intramural stress..Hypertension2008;52:195-200 PMCID:PMC2753501
|
| [24] |
Ye GJ,Parker KK.The role of mechanotransduction on vascular smooth muscle myocytes cytoskeleton and contractile function..Anat Rec (Hoboken)2014;297:1758-69 PMCID:PMC4863956
|
| [25] |
Sehgel NL,Meininger GA.“Smooth muscle cell stiffness syndrome”-revisiting the structural basis of arterial stiffness..Front Physiol2015;6:335 PMCID:PMC4649054
|
| [26] |
Qiu H,Sun Z,Gansner M.Short communication: vascular smooth muscle cell stiffness as a mechanism for increased aortic stiffness with aging..Circ Res2010;107:615-9 PMCID:PMC2936100
|
| [27] |
Haga JH,Chien S.Molecular basis of the effects of mechanical stretch on vascular smooth muscle cells..J Biomech2007;40:947-60
|
| [28] |
Brozovich FV,Degen CV,Aggarwal M.Mechanisms of vascular smooth muscle contraction and the basis for pharmacologic treatment of smooth muscle disorders..Pharmacol Rev2016;68:476-532 PMCID:PMC4819215
|
| [29] |
Alexander MR.Epigenetic control of smooth muscle cell differentiation and phenotypic switching in vascular development and disease..Annu Rev Physiol2012;74:13-40
|
| [30] |
Owens GK.Molecular control of vascular smooth muscle cell differentiation and phenotypic plasticity..Novartis Found Symp2007;283:174-91
|
| [31] |
Yamin R.Deciphering actin cytoskeletal function in the contractile vascular smooth muscle cell..J Physiol2012;590:4145-54 PMCID:PMC3473273
|
| [32] |
Skalli O,Trzeciak A,Gillessen D.A monoclonal antibody against alpha-smooth muscle actin: a new probe for smooth muscle differentiation..J Cell Biol1986;103:2787-96
|
| [33] |
Papakonstanti EA.Cell responses regulated by early reorganization of actin cytoskeleton..FEBS Lett2008;582:2120-7
|
| [34] |
Rzucidlo EM,Powell RJ.Regulation of vascular smooth muscle cell differentiation..J Vasc Surg2007;45:A25-32
|
| [35] |
Rensen SS,van Eys GJ.Regulation and characteristics of vascular smooth muscle cell phenotypic diversity..Neth Heart J2007;15:100-8 PMCID:PMC1847757
|
| [36] |
Webb RC.Smooth muscle contraction and relaxation..Adv Physiol Educ2003;27:201-6
|
| [37] |
Eddinger TJ.Myosin II isoforms in smooth muscle: heterogeneity and function..Am J Physiol Cell Physiol2007;293:C493-508
|
| [38] |
Löfgren M,Morano I.Nonmuscle myosin motor of smooth muscle..J Gen Physiol2003;121:301-10 PMCID:PMC2217371
|
| [39] |
Woodrum DA.The paradox of smooth muscle physiology..Mol Cell Endocrinol2001;177:135-43
|
| [40] |
Martinsen A,Morel N.Regulation of calcium channels in smooth muscle: new insights into the role of myosin light chain kinase..Channels (Austin)2014;8:402-13 PMCID:PMC4594426
|
| [41] |
Fridlyand LE.Pancreatic beta cell G-protein coupled receptors and second messenger interactions: a systems biology computational analysis..PloS One2016;11:e0152869 PMCID:PMC4854486
|
| [42] |
Inagami T,Tsuzuki S.Dhalla NS,Dixon IMC.Angiotensin II receptors AT1 and AT2: new mechanisms of signaling and antagonistic effects of AT1 and AT2..Angiotensin II receptor blockade physiological and clinical implications.1998;BostonSpringer129-39
|
| [43] |
Walsh MP.Calmodulin and its roles in skeletal muscle function..Can Anaesth Soc J1983;30:390-8
|
| [44] |
Lee S.Actomyosin stress fiber mechanosensing in 2D and 3D..F1000Res2016; PMCID:PMC5017290
|
| [45] |
Schwartz MA.Integrins and extracellular matrix in mechanotransduction..Cold Spring Harb Perspect Biol2010;2:a005066 PMCID:PMC2982167
|
| [46] |
Bar-Sagi D.Ras and Rho GTPases: a family reunion..Cell2000;103:227-38
|
| [47] |
Fukata Y,Kaibuchi K.Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of non-muscle cells..Trends Pharmacol Sci2001;22:32-9
|
| [48] |
Amano M,Kaibuchi K.Rho-kinase/ROCK: a key regulator of the cytoskeleton and cell polarity..Cytoskeleton (Hoboken)2010;67:545-54 PMCID:PMC3038199
|
| [49] |
Liao JK,Noma K.Rho kinase (ROCK) inhibitors..J Cardiovasc Pharmacol2007;50:17-24 PMCID:PMC2692906
|
| [50] |
Murányi A,Erdodi F,Ito M.Phosphorylation of Thr695 and Thr850 on the myosin phosphatase target subunit: inhibitory effects and occurrence in A7r5 cells..FEBS Lett2005;579:6611-5
|
| [51] |
Burute M.Spatial segregation between cell-cell and cell-matrix adhesions..Curr Opin Cell Biol2012;24:628-36
|
| [52] |
Lodish H,Zipursky SL,Baltimore D.Cell-cell adhesion and communication..Molecular cell biology.2000;New YorkW. H. Freeman
|
| [53] |
Sun Z,Hill MA.N-cadherin, a vascular smooth muscle cell-cell adhesion molecule: function and signaling for vasomotor control..Microcirculation2014;21:208-18
|
| [54] |
Lyon CA,White S,George SJ.EC4, a truncation of soluble N-cadherin, reduces vascular smooth muscle cell apoptosis and markers of atherosclerotic plaque instability..Mol Ther Methods Clin Dev2014;1:14004 PMCID:PMC4362368
|
| [55] |
Lyon CA,George SJ.Soluble N-cadherin: a novel inhibitor of VSMC proliferation and intimal thickening..Vascul Pharmacol2016;78:53-62 PMCID:PMC4749540
|
| [56] |
Lyon CA,Aguilera CM,George SJ.Inhibition of N-cadherin retards smooth muscle cell migration and intimal thickening via induction of apoptosis..J Vasc Surg2010;52:1301-9 PMCID:PMC2977853
|
| [57] |
Perez TD.Cadherin adhesion: mechanisms and molecular interactions..Handb Exp Pharmacol2004; PMCID:PMC3368609
|
| [58] |
Shapiro L.Structure and biochemistry of cadherins and catenins..Cold Spring Harb Perspect Biol2009;1:a003053 PMCID:PMC2773639
|
| [59] |
Weis WI.Re-solving the cadherin-catenin-actin conundrum..J Biol Chem2006;281:35593-7 PMCID:PMC3368706
|
| [60] |
Wozniak MA,Kwong L.Focal adhesion regulation of cell behavior..Biochim Biophys Acta2004;1692:103-19
|
| [61] |
Berrier AL.Cell-matrix adhesion..J Cell Physiol2007;213:565-73
|
| [62] |
Suki B,Imsirovic J.Regulatory roles of fluctuation-driven mechanotransduction in cell function..Physiology (Bethesda)2016;31:346-58 PMCID:PMC5504461
|
| [63] |
Bachir AI,Moissoglu K,Gratton E.Integrin-associated complexes form hierarchically with variable stoichiometry in nascent adhesions..Curr Biol2014;24:1845-53 PMCID:PMC4138543
|
| [64] |
Romer LH,Garcia JG.Focal adhesions: paradigm for a signaling nexus..Circ Res2006;98:606-16
|
| [65] |
Chorev DS,Livne A,Martins B.Conformational states during vinculin unlocking differentially regulate focal adhesion properties..Sci Rep2018;8:2693 PMCID:PMC5807537
|
| [66] |
Mierke CT.The role of vinculin in the regulation of the mechanical properties of cells..Cell Biochem Biophys2009;53:115-26
|
| [67] |
Carisey A.Vinculin, an adapter protein in control of cell adhesion signalling..Eur J Cell Biol2011;90:157-63 PMCID:PMC3526775
|
| [68] |
Burke B.Remodelling the walls of the nucleus..Nat Rev Mol Cell Biol2002;3:487-97
|
| [69] |
Warren DT,Weissberg PL.Nesprins: intracellular scaffolds that maintain cell architecture and coordinate cell function?.Expert Rev Mol Med2005;7:1-15
|
| [70] |
Haque F,Smallwood DT,Shanahan CM.SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton..Mol Cell Biol2006;26:3738-51 PMCID:PMC1488999
|
| [71] |
Crisp M,Roux K,Shanahan C.Coupling of the nucleus and cytoplasm: role of the LINC complex..J Cell Biol2006;172:41-53 PMCID:PMC2063530
|
| [72] |
Guilluy C,Van Landeghem L,Superfine R.Isolated nuclei adapt to force and reveal a mechanotransduction pathway in the nucleus..Nat Cell Biol2014;16:376-81 PMCID:PMC4085695
|
| [73] |
Lombardi ML,Shanahan CM,Roux KJ.The interaction between nesprins and sun proteins at the nuclear envelope is critical for force transmission between the nucleus and cytoskeleton..J Biol Chem2011;286:26743-53 PMCID:PMC3143636
|
| [74] |
Stewart RM,Rosowski KA,Horsley V.Nuclear-cytoskeletal linkages facilitate cross talk between the nucleus and intercellular adhesions..J Cell Biol2015;209:403-18 PMCID:PMC4427780
|
| [75] |
Chambliss AB,Erdenberger N,Hodzic D.The LINC-anchored actin cap connects the extracellular milieu to the nucleus for ultrafast mechanotransduction..Sci Rep2013;3:1087 PMCID:PMC3548190
|
| [76] |
Schwartz C,Mamchaoui K,Lok T.Lamins and nesprin-1 mediate inside-out mechanical coupling in muscle cell precursors through FHOD1..Sci Rep2017;7:1253 PMCID:PMC5430732
|
| [77] |
Chancellor TJ,Thodeti CK.Actomyosin tension exerted on the nucleus through nesprin-1 connections influences endothelial cell adhesion, migration, and cyclic strain-induced reorientation..Biophys J2010;99:115-23 PMCID:PMC2895377
|
| [78] |
Porter LJ,Soong D,Warren DT.Prelamin a accumulation attenuates rac1 activity and increases the intrinsic migrational persistence of aged vascular smooth muscle cells..Cells2016; PMCID:PMC5187525
|
| [79] |
Thakar K,Rogers A.Opposing roles for distinct LINC complexes in regulation of the small GTPase RhoA..Mol Biol Cell2017;28:182-91 PMCID:PMC5221622
|
| [80] |
Alonso JL.Cellular mechanotransduction..AIMS Biophys2016;3:50-62
|
| [81] |
Belaadi N,Guilluy C.Under pressure: mechanical stress management in the nucleus..Cells2016; PMCID:PMC4931676
|
| [82] |
Wrighton KH.Cell adhesion: the ‘ins’ and ‘outs’ of integrin signalling..Nat Rev Mol Cell Biol2013;14:752
|
| [83] |
Anwar MA,Lim CS,Davies AH.The effect of pressure-induced mechanical stretch on vascular wall differential gene expression..J Vasc Res2012;49:463-78
|
| [84] |
Ducret T,Courtois A,Marthan R.Stretch-activated channels in pulmonary arterial smooth muscle cells from normoxic and chronically hypoxic rats..Cell calcium2010;48:251-9
|
| [85] |
Zou H,Tuft RA,Singer JJ.Visualization of Ca2+ entry through single stretch-activated cation channels..Proc Natl Acad Sci U S A2002;99:6404-9 PMCID:PMC122961
|
| [86] |
Humphrey JD,Figueroa CA,Laurent S.Central artery stiffness in hypertension and aging: a problem with cause and consequence..Circ Res2016;118:379-81 PMCID:PMC4745997
|
| [87] |
Tabas I,Owens GK.Recent insights into the cellular biology of atherosclerosis..J Cell Biol2015;209:13-22 PMCID:PMC4395483
|
| [88] |
Kher N.Pathobiology of atherosclerosis--a brief review..Semin Thromb Hemost2004;30:665-72
|
| [89] |
Tracqui P,Toczek J,Ohayon J.Mapping elasticity moduli of atherosclerotic plaque in situ via atomic force microscopy..J Struct Biol2011;174:115-23
|
| [90] |
Bennett MR,Owens GK.Vascular smooth muscle cells in atherosclerosis..Circ Res2016;118:692-702 PMCID:PMC4762053
|
| [91] |
Hytönen VP.Mechanosensing in cell-matrix adhesions - converting tension into chemical signals..Exp Cell Res2016;343:35-41
|
| [92] |
Timraz SBH,Boularaoui SM.Stiffness of extracellular matrix components modulates the phenotype of human smooth muscle cells in vitro and allows for the control of properties of engineered tissues..Procedia Eng2015;110:29-36
|
| [93] |
Sazonova OV,Herrmann J,Purwada A.Extracellular matrix presentation modulates vascular smooth muscle cell mechanotransduction..Matrix Biol2015;41:36-43
|
| [94] |
McDaniel DP,Elliott JT,Meuse C.The stiffness of collagen fibrils influences vascular smooth muscle cell phenotype..Biophys J2007;92:1759-69 PMCID:PMC1796816
|
| [95] |
Chaterji S,Choe SH,Lam CH.Synergistic effects of matrix nanotopography and stiffness on vascular smooth muscle cell function..Tissue Eng Part A2014;20:2115-26 PMCID:PMC4137359
|
| [96] |
Seawright JW,Gibbs HC,Shin SY.Vascular smooth muscle contractile function declines with age in skeletal muscle feed arteries..Front Physiol2018;9:856 PMCID:PMC6079263
|
| [97] |
Kohn JC,Reinhart-King CA.Age-related vascular stiffening: causes and consequences..Front Genet2015;6:112 PMCID:PMC4396535
|
| [98] |
Isenberg BC,Walker M,Wong JY.Vascular smooth muscle cell durotaxis depends on substrate stiffness gradient strength..Biophys J2009;97:1313-22 PMCID:PMC2749749
|
| [99] |
Berry MF,Woo YJ,Bish LT.Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance..Am J Physiol Heart Circ Physiol2006;290:H2196-203
|
| [100] |
Liu F.Micro-mechanical characterization of lung tissue using atomic force microscopy..J Vis Exp2011; PMCID:PMC3217627
|
| [101] |
Lopez JI,You WK,Weaver VM.In situ force mapping of mammary gland transformation..Integr Biol (Camb)2011;3:910-21 PMCID:PMC3564969
|
| [102] |
Plodinec M,Monnier CA,Zanetti-Dallenbach R.The nanomechanical signature of breast cancer..Nat Nanotechnol2012;7:757-65
|
| [103] |
Hartman CD,Chua SG.Vascular smooth muscle cell durotaxis depends on extracellular matrix composition..Proc Natl Acad Sci U S A2016;113:11190-5 PMCID:PMC5056055
|