×

zbMATH — the first resource for mathematics

Experiments and mechanochemical modeling of smooth muscle contraction: significance of filament overlap. (English) Zbl 1336.92034
Summary: The main function of smooth muscle is to maintain/regulate the size of different hollow organs through contraction and relaxation. The magnitude of the active force during contraction is dependent on the number of attached cross-bridges, which can be linked to the overlap between the thin and thick filaments. The relevance of filament overlap and the active cross-bridges in smooth muscle is investigated through a mechanical model founded on Hill’s three-element model. The mechanical model describes a sarcomere-equivalent contractile unit supported by structural observations with a distinct filament overlap and a realistic framework for the filament sliding behavior based on force-velocity experiments. The mechanical model is coupled to the four-state latch-model by C.M. Hai and R.A. Murphy [“Cross-bridge phosphorylation and regulation of latch state in smooth muscle”, Am. J. Physiol. 254, No. 1, C99–C106 (1988)] to capture the electromechanical activation from intracellular calcium concentration to load-bearing cross-bridges. The model is fitted to isometric experiments performed on the pig carotid media and on isotonic quick-release experiments found in the literature. The proposed coupled mechanochemical model with the description of the filament overlap, which has a significant influence on the results, is able to predict isometric experimental data performed at different muscle lengths. The relevance of the filament overlap and the load-bearing cross-bridges is investigated through the model by simulating additional scenarios that has been documented in the literature.

MSC:
92C45 Kinetics in biochemical problems (pharmacokinetics, enzyme kinetics, etc.)
92C10 Biomechanics
PDF BibTeX XML Cite
Full Text: DOI
References:
[1] Arner, A., Mechanical characteristics of chemically skinned guinea-pig taenia coli, Eur. J. physiol., 395, 277-284, (1982)
[2] Ashton, F.T.; Somlyo, A.V.; Somlyo, A.P., The contractile apparatus of vascular smooth muscle: intermediate high voltage stereo electron microscopy, J. mol. biol., 98, 17-29, (1975)
[3] Blumenthal, D.K.; Stull, J.T., Activation of skeletal muscle myosin light chain kinase by calcium(2+) and calmodulin, Biochemistry, 19, 5608-5614, (1980)
[4] Bond, M.; Somlyo, A.V., Dense bodies and actin polarity in vertebrate smooth muscle, J. cell biol., 95, 403-413, (1982)
[5] Bursztyn, L.; Eytan, O.; Jaffa, A.J.; Elad, D., Modeling myometrial smooth muscle contraction, Ann. N. Y. acad. sci., 1101, 110-138, (2007)
[6] Dillon, P.F.; Aksoy, M.O.; Driska, S.P.; Murphy, R.A., Myosin phosphorylation and the cross-bridge cycle in arterial smooth muscle, Science, 211, 495-497, (1981)
[7] Ford, L.E.; Seow, C.Y.; Pratusevich, V.R., Plasticity in smooth muscle, a hypothesis, Can. J. physiol. pharmacol., 72, 1320-1324, (1994)
[8] Gillis, J.M.; Cao, M.L.; Godfraind-De Becker, A., Density of myosin filaments in the rat anococcygeus muscle at rest and in contraction. II, J. muscle res. cell motil., 9, 18-29, (1988)
[9] Guilford, W.H.; Warshaw, D.M., The molecular mechanics of smooth muscle myosin, Comp. biochem. physiol., 119, 451-458, (1998)
[10] Hai, C.M., Length-dependent myosin phosphorylation and contraction of arterial smooth muscle, Pflügers arch. eur. J. physiol., 418, 564-571, (1991)
[11] Hai, C.M.; Murphy, R.A., Cross-bridge phosphorylation and regulation of latch state in smooth muscle, J. appl. physiol., 254, C99-C106, (1988)
[12] Hai, C.M.; Murphy, R.A., Regulation of shortening velocity by cross-bridge phosphorylation in smooth muscle, Am. J. physiol., 255, C86-C94, (1988)
[13] Hai, C.M.; Kim, H.R., An expanded latch-bridge model of protein kinase C-mediated smooth muscle contraction, J. appl. physiol., 98, 1356-1365, (2005)
[14] Hanks, B.S.; Stephens, N.L., Mechanics and energetics of lengthening of active airway smooth muscle, Am. J. physiol., 241, C42-C46, (1981)
[15] Hellstrand, P.; Arner, A., Contraction of the rat portal vein in hypertonic and isotonic medium: mechanical properties and effects of mg^2+, Acta physiol. scand., 110, 59-67, (1980)
[16] Herlihy, J.T.; Murphy, R.A., Length-tension relationship of smooth muscle of the hog carotid artery, Circ. res., 33, 275-283, (1973)
[17] Holzapfel, G.A., Nonlinear solid mechanics. A continuum approach for engineering, (2000), John Wiley & Sons Chichester · Zbl 0980.74001
[18] Holzapfel, G.A.; Ogden, R.W., Constitutive modelling of arteries, Proc. R. soc. London A, 466, 1551-1597, (2010) · Zbl 1197.74075
[19] Holzapfel, G.A.; Gasser, T.C.; Ogden, R.W., A new constitutive framework for arterial wall mechanics and a comparative study of material models, J. elasticity, 61, 1-48, (2000) · Zbl 1023.74033
[20] Horowitz, A.; Menice, C.B.; Laporte, R.; Morgan, K.G., Mechanisms of smooth muscle contraction, Physiol. rev., 76, 967-1003, (1996)
[21] Humphrey, J.D.; Taylor, C.A., Intracranial and abdominal aortic aneurysms: similarities, differences, and need for a new class of computational models, Annu. rev. biomed. eng., 10, 221-246, (2008)
[22] Hunter, P.J.; Borg, T.K., Integration from proteins to organs: the physiome project, Nat. rev. mol. cell biol., 4, 237-243, (2003)
[23] Hunter, P.J.; Nielsen, P., A strategy for integrative computational physiology, Physiology (Bethesda), 20, 316-325, (2005)
[24] Hunter, P.J.; Robbins, P.; Noble, D., The IUPS human physiome project, Eur. J. physiol., 445, 1-9, (2002)
[25] Kamm, K.E.; Stull, J.T., Myosin phosphorylation, force, and maximal shortening velocity in neurally stimulated tracheal smooth muscle, Am. J. phys., 249, C238-C247, (1985)
[26] Kamm, K.E.; Gerthoffer, W.H.; Murphy, R.A.; Bohr, D.F., Mechanical properties of carotid arteries from DOCA hypertensive swine, Hypertension, 13, 102-109, (1989)
[27] Kargacin, G.J.; Cooke, P.H.; Abramson, S.B.; Fay, F.S., Periodic organization of the contractile apparatus in smooth muscle revealed by the motion of dense bodies in single cells, J. cell biol., 108, 1465-1475, (1989)
[28] Löfgren, M.; Ekblad, E.; Morano, I.; Arner, A., Nonmuscle myosin motor of smooth muscle, J. gen. physiol., 121, 301-310, (2003)
[29] Murtada, S.; Kroon, M.; Holzapfel, G.A., A calcium-driven mechanochemical model for prediction of force generation in smooth muscle, Biomech. model. mechanobiol., 9, 749-762, (2010)
[30] Murtada, S.; Kroon, M.; Holzapfel, G.A., Modeling the dispersion effects of contractile fibers in smooth muscles, J. mech. phys. solids, 58, 2065-2082, (2010) · Zbl 1225.74057
[31] Offer, G.; Ranatunga, K.W., Crossbridge and filament compliance in muscle: implications for tension generation and lever arm swing, J. muscle res. cell motil., 31, 245-265, (2010)
[32] Rembold, C.M., Modulation of the [ca^2+] sensitivity of myosin phosphorylation in intact swine arterial smooth muscle, J. physiol., 429, 77-94, (1990)
[33] Rembold, C.M.; Murphy, R.A., Myoplasmic [ca^2+] determines myosin phosphorylation in agonist-stimulated swine arterial smooth muscle, Circ. res., 63, 593-603, (1988)
[34] Rembold, C.M.; Murphy, R.A., Muscle length, shortening, myoplasmic [ca^2+] and activation of arterial smooth muscle, Circ. res., 66, 1354-1361, (1990)
[35] Singer, H.A.; Kamm, K.E.; Murphy, R.A., Estimates of activation in arterial smooth muscle, Am. J. physiol., 251, C465-C473, (1986)
[36] Smolensky, A.V.; Ragozzino, J.; Gilbert, S.H.; Seow, S.Y.; Ford, L.E., Length-dependent filament formation assessed from birefringence increases during activation of porcine tracheal muscle, J. physiol., 563, 517-527, (2005)
[37] Somlyo, A.P.; Somlyo, A.V., Signal transduction and regulation in smooth muscle, Nature, 372, 231-236, (1994)
[38] Somlyo, A.P.; Somlyo, A.V., Ca^2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase, Physiol. rev., 83, 1325-1358, (2003)
[39] Stålhand, J.; Klarbring, A.; Holzapfel, G.A., A mechanochemical 3D continuum model for smooth muscle contraction under finite strains, J. theor. biol., 268, 120-130, (2011)
[40] Steffen, W.; Smith, D.; Simmons, R.; Sleep, J., Mapping the actin filament with myosin, Proc. natl. acad. sci. USA, 98, 14949-14954, (2001)
[41] Uvelius, B., Isometric and isotonic length-tension relations and variations in cell length in longitudinal smooth muscle from rabbit urinary bladder, Acta physiol. scand., 97, 1-12, (1976)
[42] Walmsley, J.G.; Murphy, R.A., Force-length dependence of arterial lamellar, smooth muscle, and myofilament orientations, Am. J. physiol. heart circ. physiol., 253, H1141-H1147, (1987)
[43] Woledge, R.C.; Curtin, N.A.; Homsher, E., Energetic aspects of muscle contraction, (1985), Academic Press
[44] Xu, J.Q.; Harder, B.A.; Uman, P.; Craig, R., Myosin filament structure in vertebrate smooth muscle, J. cell biol., 134, 53-66, (1996)
[45] Yu, S.N.; Crago, P.E.; Chiel, H.J., A nonisometric kinetic model for smooth muscle, Am. J. physiol., 272, 3 Pt 1, C1025-C1039, (1997)
[46] Zeinali-Davarani, S., Sheidaei, A., Baek, S., 2011. A finite element model of stress-mediated vascular adaptation: application to abdominal aortic aneurysms. Comput. Methods Biomech. Biomed. Eng. 14, 803-817.
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. It attempts to reflect the references listed in the original paper as accurately as possible without claiming the completeness or perfect precision of the matching.