×

Force distribution and multi-scale mechanics in smooth muscle tissues. (English) Zbl 1461.92007

Summary: The mechanical role of smooth muscle tissue in many physiological processes is vital to their healthy function. In this work, we provide a deeper understanding of the underlying mechanisms that govern the smooth muscle tissue response. Specifically, we model and investigate the distribution and the transmission of passive and active forces throughout the microstructure. Broadly, smooth muscle cells contain a structural network with two types of load carrying structures: (1) contractile units made of actin and myosin filaments, which are capable of generating force, and (2) intermediate filaments. The extracellular matrix comprises elastin and collagen fibers that can sustain stress. We argue that all of the load carrying constituents in the tissue participate in the generation and the transmission of passive and active forces. We begin by modeling the response of the elements in the smooth muscle cell and defining a network of contractile units and intermediate filaments through which forces are transferred. This allows to derive an expression for the stress that develops in the cell. Next, we assume a hyperelastic behavior for the extracellular matrix and determine the stress in the tissue. With appropriate kinematic constraints and equilibrium considerations, we relate the macroscopic deformation to the stretch of the individual load carrying structures. Consequently, the stress on each element in the tissue can be computed. To validate the framework, we consider a simple microstructure of a smooth muscle tissue and fit the model parameters to experimental findings. The framework is also used to delineate experimental evidence which suggests that the suppression of intermediate filaments reduces the active and passive forces in a tissue. We show that the degradation and the reduction of the number of intermediate filaments in the cell fully explains this observation.

MSC:

92C10 Biomechanics
PDFBibTeX XMLCite
Full Text: DOI

References:

[1] Aguilar, H. N.; Mitchell, B., Physiological pathways and molecular mechanisms regulating uterine contractility, Hum. Reprod. Update, 16, 6, 725-744 (2010)
[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, 1, 17-29 (1975)
[3] PMID: 20008114
[4] Burgess, J. K.; Johnson, P. R.A.; Ge, Q.; Au, W. W.; Poniris, M. H.; McParland, B. E.; King, G.; Roth, M.; Black, J. L., Expression of connective tissue growth factor in asthmatic airway smooth muscle cells, Am. J. Respir. Crit. Care Med., 167, 1, 71-77 (2003)
[5] Cohen, N.; Deshpande, V. S.; Holmes, J. W., Biomech. Model. Mechanobiol., 18, 1233 (2019)
[6] Dharmashankar, K.; Widlansky, M. E., Vascular endothelial function and hypertension: insights and directions, Curr. Hypertens. Rep., 12, 6, 448-455 (2010)
[7] Gabella, G., Structural apparatus for force transmission in smooth muscles, Physiol. Rev., 64, 2, 455-477 (1984)
[8] Gunst, S. J., Chapter 104 - airway smooth muscle and asthma, (Hill, J. A.; Olson, E. N., Muscle (2012), Academic Press: Academic Press Boston/Waltham), 1359-1369
[9] PMID: 3337223
[10] PMID: 3389402
[11] Herrera, A. M.; McParland, B. E.; Bienkowska, A.; Tait, R.; Paré, P. D.; Seow, C. Y., ‘Sarcomeres’ of smooth muscle: functional characteristics and ultrastructural evidence, J. Cell. Sci., 118, 11, 2381-2392 (2005)
[12] Horowitz, A.; Menice, C. B.; Laporte, R.; Morgan, K. G., Mechanisms of smooth muscle contraction, Physiol. Rev., 76, 4, 967-1003 (1996)
[13] Kuo, K.-H.; Seow, C. Y., Contractile filament architecture and force transmission in swine airway smooth muscle, J. Cell. Sci., 117, 8, 1503-1511 (2004)
[14] Lavoie, T. L.; Dowell, M. L.; Lakser, O. J.; Gerthoffer, W. T.; Fredberg, J. J.; Seow, C. Y.; Mitchell, R. W.; Solway, J., Disrupting actin-myosin-actin connectivity in airway smooth muscle as a treatment for asthma?, Proc. Am. Thorac. Soc., 6, 19387033, 295-300 (2009)
[15] Li, Q.-F.; Spinelli, A. M.; Wang, R.; Anfinogenova, Y.; Singer, H. A.; Tang, D. D., Critical role of vimentin phosphorylation at Ser-56 by p21-activated kinase in vimentin cytoskeleton signaling, J. Biol. Chem., 281, 45, 34716-34724 (2006)
[16] Liu, J. C.-Y.; Rottler, J.; Wang, L.; Zhang, J.; Pascoe, C. D.; Lan, B.; Norris, B. A.; Herrera, A. M.; Pare, P. D.; Seow, C. Y., Myosin filaments in smooth muscle cells do not have a constant length, J. Physiol., 591, 23, 5867-5878 (2013)
[17] Liu, T., A constitutive model for cytoskeletal contractility of smooth muscle cells, Proc. R. Soc. A, 470, 2164, 20130771 (2014) · Zbl 1371.74212
[18] Lofgren, M.; Ekblad, E.; Morano, I.; Arner, A., Nonmuscle myosin motor of smooth muscle, J. Gen. Physiol., 121, 4, 301 (2003)
[19] Meiss, R. A., An analysis of length-dependent active stiffness in smooth muscle strips, (Moreland, R. S., Regulation of Smooth Muscle Contraction (1991), Springer US: Springer US Boston, MA), 425-434
[20] PMID: 9887107
[21] Milewicz, D. M.; Guo, D.-C.; Tran-Fadulu, V.; Lafont, A. L.; Papke, C. L.; Inamoto, S.; Kwartler, C. S.; Pannu, H., Genetic basis of thoracic aortic aneurysms and dissections: focus on smooth muscle cell contractile dysfunction, Annu. Rev. Genom. Hum. Genet., 9, 1, 283-302 (2008)
[22] PMID: 16333357
[23] Murtada, S. C.; Arner, A.; Holzapfel, G. A., Experiments and mechanochemical modeling of smooth muscle contraction: significance of filament overlap, J. Theor. Biol., 297, 176-186 (2012) · Zbl 1336.92034
[24] Murtada, S.-I.; Humphrey, J. D.; Holzapfel, G. A., Multiscale and multiaxial mechanics of vascular smooth muscle, Biophys. J., 113, 3, 714-727 (2017)
[25] Murtada, S.-I.; Kroon, M.; Holzapfel, G. A., Modeling the dispersion effects of contractile fibers in smooth muscles, J. Mech. Phys. Solids, 58, 12, 2065-2082 (2010) · Zbl 1225.74057
[26] Small, J. V., Structure-function relationships in smooth muscle: the missing links, Bioessays, 17, 9, 785-792 (1995)
[27] Somlyo, A. P.; Somlyo, A. V., Signal transduction and regulation in smooth muscle, Nature, 372, 6503, 231-236 (1994)
[28] Stalhand, J.; Holzapfel, G. A., Length adaptation of smooth muscle contractile filaments in response to sustained activation, J. Theor. Biol., 397, 13-21 (2016) · Zbl 1343.92172
[29] Stalhand, J.; McMeeking, R. M.; Holzapfel, G. A., On the thermodynamics of smooth muscle contraction, J. Mech. Phys. Solids, 94, 490-503 (2016)
[30] Instabilities and Nonlinearities in Soft Systems: From Fluids to Biomaterials
[31] Tang, D. D., Intermediate filaments in smooth muscle, Am. J. Physiol. Cell Physiol., 294, 4, C869-C878 (2008)
[32] Tang, D. D.; Bai, Y.; Gunst, S. J., Silencing of p21-activated kinase attenuates vimentin phosphorylation on Ser-56 and reorientation of the vimentin network during stimulation of smooth muscle cells by 5-hydroxytryptamine, Biochem. J., 388, 3, 773-783 (2005)
[33] Touyz, R. M.; Alves-Lopes, R.; Rios, F. J.; Camargo, L. L.; Anagnostopoulou, A.; Arner, A.; Montezano, A. C., Vascular smooth muscle contraction in hypertension, Cardiovasc. Res., 114, 4, 529-539 (2018)
[34] PMID: 3688257
[35] Wang, R.; Li, Q.; Tang, D. D., Role of vimentin in smooth muscle force development, Am. J. Physiol. Cell Physiol., 291, 3, C483-C489 (2006)
[36] PMID: 15130890
[37] Zuyderduyn, S.; Sukkar, M. B.; Fust, A.; Dhaliwal, S.; Burgess, J. K., Treating asthma means treating airway smooth muscle cells, Eur. Respir. J., 32, 2, 265-274 (2008)
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. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.