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Adaptation of active tone in the mouse descending thoracic aorta under acute changes in loading

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Abstract

Arteries can adapt to sustained changes in blood pressure and flow, and it is thought that these adaptive processes often begin with an altered smooth muscle cell activity that precedes any detectable changes in the passive wall components. Yet, due to the intrinsic coupling between the active and passive properties of the arterial wall, it has been difficult to delineate the adaptive contributions of active smooth muscle. To address this need, we used a novel experimental–computational approach to quantify adaptive functions of active smooth muscle in arterial rings excised from the proximal descending thoracic aorta of mice and subjected to short-term sustained circumferential stretches while stimulated with various agonists. A new mathematical model of the adaptive processes was derived and fit to data to describe and predict the effects of active tone adaptation. It was found that active tone was maintained when the artery was adapted close to the optimal stretch for maximal active force production, but it was reduced when adapted below the optimal stretch; there was no significant change in passive behavior in either case. Such active adaptations occurred only upon smooth muscle stimulation with phenylephrine, however, not stimulation with KCl or angiotensin II. Numerical simulations using the proposed model suggested further that active tone adaptation in vascular smooth muscle could play a stabilizing role for wall stress in large elastic arteries.

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References

  • Albinsson S, Nordström I, Hellstrand P (2004) Stretch of the vascular wall induces smooth muscle differentiation by promoting actin polymerization. J Biol Chem 279(33):34849–34855

    Article  Google Scholar 

  • Arner A (1982) Mechanical characteristics of chemically skinned guinea-pig taenia coli. Eur J Physiol 395:277–284

    Article  Google Scholar 

  • Arner A, Malmqvist U, Uvelius B (1984) Structural and mechanical adaptations in rat aorta in response to sustained changes in arterial pressure. Acta Physiol Scand 122(2):119–126

    Article  Google Scholar 

  • Bakker EN, van der Meulen ET, van den Berg BM, Everts V, Spaan JA, VanBavel E (2002) Inward remodeling follows chronic vasoconstriction in isolated resistance arteries. J Vasc Res 39(1):12–20

    Article  Google Scholar 

  • Bakker EN, Buus CL, VanBavel E, Mulvany MJ (2004) Activation of resistance arteries with endothelin-1: from vasoconstriction to functional adaptation and remodeling. J Vasc Res 41(2):174–182

    Article  Google Scholar 

  • Bakker EN, Matlung HL, Bonta P, de Vries CJ, van Rooijen N, Vanbavel E (2008) Blood flow-dependent arterial remodelling is facilitated by inflammation but directed by vascular tone. Cardiovasc Res 78(2):341–348

    Article  Google Scholar 

  • Barclay CJ (1998) Estimation of cross-bridge stiffness from maximum thermodynamic efficiency. J Muscle Res Cell Motil 19(8):855–864

    Article  Google Scholar 

  • Bray D, White JG (1988) Cortical flow in animal cells. Science 239(4842):883–888

    Article  Google Scholar 

  • Buus CL, Pourageaud F, Fazzi GE, Janssen G, Mulvany MJ, De Mey JG (2001) Smooth muscle cell changes during flow-related remodeling of rat mesenteric resistance arteries. Circ Res 89(2):180–186

    Article  Google Scholar 

  • Böl M, Schmitz A, Nowak G, Siebert T (2012) A three-dimensional chemo-mechanical continuum model for smooth muscle contraction. J Mech Behav Biomed Mater 13:215–229

    Article  Google Scholar 

  • Dajnowiec D, Langille BL (2007) Arterial adaptations to chronic changes in haemodynamic function: coupling vasomotor tone to structural remodelling. Clin Sci (Lond) 113(1):15–23

    Article  Google Scholar 

  • Davis B, Rahman A, Arner A (2012) AMP-activated kinase relaxes agonist induced contractions in the mouse aorta via effects on PKC signaling and inhibits NO-induced relaxation. Eur J Pharmacol 695(1–3):88–95

    Article  Google Scholar 

  • Devine CE, Somlyo AP (1971) Thick filaments in vascular smooth muscle. J Cell Biol 49(3):636–649

    Article  Google Scholar 

  • Edman KA (2009) Non-linear myofilament elasticity in frog intact muscle fibres. J Exp Biol 212:1115–1119

    Article  Google Scholar 

  • Ferruzzi J, Bersi MR, Humphrey JD (2013) Biomechanical phenotyping of central arteries in health and disease: advantages of and methods for murine models. Ann Biomed Eng 41:1311–1330

    Article  Google Scholar 

  • Ferruzzi J, Bersi MR, Uman S, Yanagisawa H, Humphrey JD (2015) Decreased elastic energy storage, not increased material stiffness, characterizes central artery dysfunction in fibulin-5 deficiency independent of sex. J Biomech Eng 137(3):031007

    Article  Google Scholar 

  • Hai CM, Murphy RA (1988) Cross-bridge phosphorylation and regulation of latch state in smooth muscle. Am J Physiol 254:C99–106

    Google Scholar 

  • Herrera AM, Kuo KH, Seow CY (2002) Influence of calcium on myosin thick filament formation in intact airway smooth muscle. Am J Physiol Cell Physiol 282(2):C310–C316

    Article  Google Scholar 

  • Holzapfel GA, Gasser TC, Ogden RW (2000) A new constitutive framework for arterial wall mechanics and a comparative study of material models. J Elasticity 61:1–48

    Article  MathSciNet  MATH  Google Scholar 

  • Humphrey JD (2002) Cardiovascular solid mechanics. Cells, tissues and organs. Springer, NY

    Book  Google Scholar 

  • Humphrey JD, Eberth JF, Dye WW, Gleason RL (2009) Fundamental role of axial stress in compensatory adaptations by arteries. J Biomech 42:1–8

    Article  Google Scholar 

  • Huxley AF, Tideswell S (1996) Filament compliance and tension transients in muscle. J Muscle Res Cell Motil 17(4):507–511

    Article  Google Scholar 

  • Langille BL, Dajnowiec D (2005) Cross-linking vasomotor tone and vascular remodeling: a novel function for tissue transglutaminase? Circ Res 96(1):9–11

    Article  Google Scholar 

  • Liu JC-Y, Rottler J, Wang L, Zhang J, Pascoe CD, Lan B, Norris BA, Herrera AM, Paré PD, Seow CY (2013) Myosin filaments in smooth muscle cells do not have a constant length. J Physiol 19(23):5867–5878

    Article  Google Scholar 

  • Martinez-Lemus LA, Hill MA, Bolz SS, Pohl U, Meininger GA (2004) Acute mechanoadaptation of vascular smooth muscle cells in response to continuous arteriolar vasoconstriction: implications for functional remodeling. FASEB J 18(6):708–710

    Google Scholar 

  • Martinez-Lemus LA (2008) Persistent agonist-induced vasoconstriction is not required for angiotensin II to mediate inward remodeling of isolated arterioles with myogenic tone. J Vasc Res 45(3):211–221

    Article  Google Scholar 

  • Martinez-Lemus LA, Hill MA, Meininger GA (2009) The plastic nature of the vascular wall: a continuum of remodelling events contributing to control of arteriolar diameter and structure. Physiology 24:45–57

    Article  Google Scholar 

  • Mijailovich SM, Butler JP, Fredberg JJ (2000) Perturbed equilibria of myosin binding in airway smooth muscle: bond-length distributions, mechanics, and ATP metabolism. Biophys J 79(5):2667–2681

    Article  Google Scholar 

  • Murtada S-I, Kroon M, Holzapfel GA (2010) A calcium-driven mechanochemical model for prediction of force generation in smooth muscle. Biomech Model Mechanobiol 9(6):749–762

    Article  Google Scholar 

  • Murtada S-I, Arner A, Holzapfel GA (2012) Experiments and mechanochemical modeling of smooth muscle contraction: significance of filament overlap. J Theor Biol 297:176–186

    Article  MathSciNet  Google Scholar 

  • Murtada S-I, Holzapfel GA (2014) Investigating the role of smooth muscle cells in large elastic arteries: a finite element analysis. J Theor Biol 358:1–10

    Article  MathSciNet  Google Scholar 

  • Russell A, Watts S (2000) Vascular reactivity of isolated thoracic aorta of the C57BL/6J mouse. J Pharmacol Exp Theor 294(2):598–604

    Google Scholar 

  • Stålhand J, Klarbring A, Holzapfel GA (2008) Smooth muscle contraction: mechanochemical formulation for homogeneous finite strains. Prog Biophys Mol Biol 96(1–3):465–481

    Article  Google Scholar 

  • Sweeney HL, Houdusse A (2010) Structural and functional insights into the Myosin motor mechanism. Annu Rev Biophys 39:539–557

    Article  Google Scholar 

  • Tee SY, Fu J, Chen CS, Janmey PA (2011) Cell shape and substrate rigidity both regulate cell stiffness. Biophys J 100(5):L25–L27

    Article  Google Scholar 

  • Tsoularis A, Wallace J (2002) Analysis of logistic growth models. Math Biosci 179(1):21–55

    Article  MathSciNet  MATH  Google Scholar 

  • Tuna BG, Bakker EN, VanBavel E (2013) Relation between active and passive biomechanics of small mesenteric arteries during remodeling. J Biomech 46(8):1420–1426

    Article  Google Scholar 

  • Valentín A, Cardamone L, Baek S, Humphrey JD (2009) Complementary vasoactivity and matrix remodelling in arterial adaptations to altered flow and pressure. J R Soc Interface 6(32):293–306

    Article  Google Scholar 

  • Xu J-Q, Harder BA, Uman P, Craig R (1996) Myosin filament structure in vertebrate smooth muscle. J Cell Biol 134(1):53–66

    Article  Google Scholar 

  • Zhou Y, Chen Y, Dirksen WP, Morris M, Periasamy M (2003a) AT1b receptor predominantly mediates contractions in major mouse blood vessels. Circ Res 93(11):1089–1094

    Article  Google Scholar 

  • Zhou Y, Dirksen WP, Babu GJ, Periasamy M (2003b) Differential vasoconstrictions induced by angiotensin II: role of AT1 and AT2 receptors in isolated C57BL/6J mouse blood vessels. Am J Physiol Heart Circ Physiol 285(6):H2797–H2803

    Article  Google Scholar 

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Acknowledgments

This work was supported, in part, by a Grant (#2012419) from the ‘Swedish Research Council’ and grants from the US NIH (HL105297 and EB016810).

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Correspondence to S.-I. Murtada.

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Murtada, SI., Lewin, S., Arner, A. et al. Adaptation of active tone in the mouse descending thoracic aorta under acute changes in loading. Biomech Model Mechanobiol 15, 579–592 (2016). https://doi.org/10.1007/s10237-015-0711-z

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  • DOI: https://doi.org/10.1007/s10237-015-0711-z

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