Stress and strain in the contractile and cytoskeletal filaments of airway smooth muscle

Pulmonary Pharmacology and Therapeutics

Volumn 22, Issue 5, 2009, Pages 407-416

  Deng, Linhong ^a,b   Bosse, Ynuk ^c   Brown, Nathan ^d   Chin, Leslie Y M ^c   Connolly, Sarah C ^e   Fairbank, Nigel J ^e   King, Greg G ^d   Maksym, Geoffrey N ^e   Paré, Peter D ^c   Seow, Chun Y ^c   Stephen, Newman L ^f  

^a CHONGQING UNIVERSITY   (China)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d ROYAL NORTH SHORE HOSPITAL   (Australia)

^e DALHOUSIE UNIVERSITY   (Canada)

^f UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Airway smooth muscle filaments; Asthma; Cytoskeleton dynamics; Stress and strain

Indexed keywords

ACTIN; DESMIN; MYOSIN; MYOSIN LIGHT CHAIN KINASE; MYOSIN LIGHT CHAIN PHOSPHATASE;

ACTIN FILAMENT; AIRWAY; AIRWAY DYNAMICS; AIRWAY SMOOTH MUSCLE; ARTICLE; ASTHMA; CELL ULTRASTRUCTURE; CYTOSKELETON; ENZYME ACTIVITY; HIGH RESOLUTION COMPUTER TOMOGRAPHY; HUMAN; LUNG VOLUME; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SMOOTH MUSCLE; SMOOTH MUSCLE CONTRACTILITY; STRESS STRAIN RELATIONSHIP; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; ASTHMA; CYTOSKELETON; HUMANS; MODELS, BIOLOGICAL; MUSCLE CELLS; MUSCLE CONTRACTION; MUSCLE PROTEINS; MUSCLE, SMOOTH; RESPIRATORY MECHANICS; RESPIRATORY SYSTEM; STRESS, MECHANICAL;

EID: 69349099104     PISSN: 10945539     EISSN: 15229629     Source Type: Journal    
DOI: 10.1016/j.pupt.2009.04.008     Document Type: Article

References (87)

1. Fredberg J.J. Counterpoint: airway smooth muscle is not useful. J Appl Physiol 102 4 (2007) 1709-1710
2. Mead J. Point: airway smooth muscle is useful. J Appl Physiol 102 4 (2007) 1708-1709
3. Mitzner W. Airway smooth muscle: the appendix of the lung. Am J Respir Crit Care Med 169 7 (2004) 787-790
4. Chen C.S., Ostuni E., Whitesides G.M., and Ingber D.E. Using self-assembled monolayers to pattern ECM proteins and cells on substrates. Meth Mol Biol 139 (2000) 209-219
5. Chien S. Role of shear stress direction in endothelial mechanotransduction. Mol Cell Biomech 5 1 (2008) 1-8
6. Engler A.J., Sen S., Sweeney H.L., and Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 126 4 (2006) 677-689
7. Ingber D.E. Cancer as a disease of epithelial-mesenchymal interactions and extracellular matrix regulation. Differentiation 70 9-10 (2002) 547-560
8. Maksym G.N., Deng L., Fairbank N.J., Lall C.A., and Connolly S.C. Beneficial and harmful effects of oscillatory mechanical strain on airway smooth muscle. Can J Physiol Pharmacol 83 10 (2005) 913-922
9. North A., Gimona M., Lando Z., and Small J. Actin isoform compartments in chicken gizzard smooth muscle cells. J Cell Sci 107 3 (1994) 445-455
10. Small J.V., and Gimona M. The cytoskeleton of the vertebrate smooth muscle cell. Acta Physiol Scand 164 (1998) 341-348
11. Craig R., and Megerman J. Assembly of smooth muscle myosin into side-polar filaments. J Cell Biol 75 3 (1977) 990-996
12. Craig R., and Woodhead J.L. Structure and function of myosin filaments. In: Janin J., Levitt M., Egelman E.H., and Leslie A.G.W. (Eds). Theory and simulation/Macromolecular assemblages. Curr Opin Struct Biol 16 2 (2006) 204-212
13. Xu J.Q., Harder B.A., Uman P., and Craig R. Myosin filament structure in vertebrate smooth muscle. J Cell Biol 134 1 (1996) 53-66
14. Lowy J., and Hanson J. Ultrastructure of invertebrate smooth muscles. Physiol Rev 5 Suppl (1962) 34-47
15. Geiger B., Dutton A.H., Tokuyasu K.T., and Singer S.J. Immunoelectron microscope studies of membrane-microfilament interactions: distributions of alpha-actinin, tropomyosin, and vinculin in intestinal epithelial brush border and chicken gizzard smooth muscle cells. J Cell Biol. 91 3 (1981) 614-628
16. Bai T.R., Cooper J., Koelmeyer T., Pare P.D., and Weir T.D. The effect of age and duration of disease on airway structure in fatal asthma. Am J Respir Crit Care Med 162 2 Pt 1 (2000) 663-669
17. Pratusevich V., Seow C., and Ford L. Plasticity in canine airway smooth muscle. J Gen Physiol 105 1 (1995) 73-94
18. Kuo K.H., Wang L., Pare P.D., Ford L.E., and Seow C.Y. Myosin thick filament lability induced by mechanical strain in airway smooth muscle. J Appl Physiol 90 (2001) 1811
19. Bosse Y., Sobieszek A., Pare P.D., and Seow C.Y. Length adaptation of airway smooth muscle. Proc Am Thorac Soc 5 1 (2008) 62-67
20. Herrera A.M., Martinez E.C., and Seow C.Y. Electron microscopic study of actin polymerization in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 286 6 (2004) L1161-L1168
21. Gunst S.J., and Pisoni J.M. Effects of extracellular calcium on canine tracheal smooth muscle. J Appl Physiol 61 2 (1986) 706-711
22. Gunst S.J., and Tang D.D. The contractile apparatus and mechanical properties of airway smooth muscle. Eur Respir J 15 3 (2000) 600-616
23. Gunst S.J., Meiss R.A., Wu M.F., and Rowe M. Mechanisms for the mechanical plasticity of tracheal smooth muscle. Am J Physiol Cell Physiol 268 5 (1995) C1267-C1276
24. Opazo Saez A., Zhang W., Wu Y., Turner C.E., Tang D.D., and Gunst S.J. Tension development during contractile stimulation of smooth muscle requires recruitment of paxillin and vinculin to the membrane. Am J Physiol Cell Physiol 286 2 (2004) C433-C447
25. Herrera A.M., McParland B.E., Bienkowska A., Tait R., Pare P.D., and Seow C.Y. 'Sarcomeres' of smooth muscle: functional characteristics and ultrastructural evidence. J Cell Sci 118 11 (2005) 2381-2392
26. Zhang W., and Gunst S.J. Dynamic association between {alpha}-actinin and {beta}-integrin regulates contraction of canine tracheal smooth muscle. J Physiol 572 3 (2006) 659-676
27. Wang L., Pare P., and Seow C. Effect of chronic passive length change on airway smooth muscle length-tension relationship. J Appl Physiol 90 (2001) 734-740
28. Silberstein J., and Hai C.M. Dynamics of length-force relations in airway smooth muscle. Respir Physiol Neurobiol 132 2 (2002) 205-221
29. Kuo K.H., Herrera A.M., Wang L., Pare P.D., Ford L.E., Stephens N.L., et al. Structure-function correlation in airway smooth muscle adapted to different lengths. Am J Physiol Cell Physiol 285 (2003) C384-C390
30. Seow C.Y. Myosin filament assembly in an ever-changing myofilament lattice of smooth muscle. Am J Physiol Cell Physiol 289 6 (2005) C1363-C1368
31. Smolensky A.V., Ragozzino J., Gilbert S.H., Seow C.Y., and Ford L.E. Length-dependent filament formation assessed from birefringence increases during activation of porcine tracheal muscle. J Physiol 563 Pt 2 (2005) 517-527
32. 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 (1976) 1-12
33. Smolensky A.V., and Ford L.E. The extensive length-force relationship of porcine airway smooth muscle. J Appl Physiol 102 5 (2007) 1906-1911
34. McParland B.E., Tait R.R., Pare P.D., and Seow C.Y. The role of airway smooth muscle during an attack of asthma simulated in vitro. Am J Respir Cell Mol Biol 33 5 (2005) 500-504
35. Fredberg J.J., and Kamm R.D. Stress transmission in the lung: pathways from organ to molecule. Annu Rev Physiol 68 (2006) 507-541
36. Deng L., Fairbank N.J., Fabry B., Smith P.G., and Maksym G.N. Localized mechanical stress induces time-dependent actin cytoskeletal remodeling and stiffening in cultured airway smooth muscle cells. Am J Physiol Cell Physiol 287 2 (2004) C440-C448
37. Hirshman C.A., and Emala C.W. Actin reorganization in airway smooth muscle cells involves Gq and Gi-2 activation of Rho. Am J Physiol 277 (1999) L653-L661
38. Mehta D., and Gunst S.J. Actin polymerization stimulated by contractile activation regulates force development in canine tracheal smooth muscle. J Physiol 519 Pt 3 (1999) 829-840
39. Smith P.G., Roy C., Fisher S., Huang Q.Q., and Brozovich F. Selected contribution: mechanical strain increases force production and calcium sensitivity in cultured airway smooth muscle cells. J Appl Physiol 89 5 (2000) 2092-2098
40. Smith P.G., Tokui T., and Ikebe M. Mechanical strain increases contractile enzyme activity in cultured airway smooth muscle cells. Am J Physiol 268 6 Pt 1 (1995) L999-1005
41. Smith P.G., Moreno R., and Ikebe M. Strain increases airway smooth muscle contractile and cytoskeletal proteins in vitro. Am J Physiol 272 1 Pt 1 (1997) L20-L27
42. Smith P.G., Roy C., Zhang Y.N., and Chauduri S. Mechanical stress increases RhoA activation in airway smooth muscle cells. Am J Respir Cell Mol Biol 28 4 (2003) 436-442
43. Smith P.G., Roy C., Dreger J., and Brozovich F. Mechanical strain increases velocity and extent of shortening in cultured airway smooth muscle cells. Am J Physiol 277 2 Pt 1 (1999) L343-L348
44. Panettieri R.A., Murray R.K., DePalo L.R., Yadvish P.A., and Kotlikoff M.I. A human airway smooth muscle cell line that retains physiological responsiveness. Am J Physiol Cell Physiol 256 2 (1989) C329-C335
45. Tran M.U., Weir A.J., Fanucchi M.V., Rodriguez A.E., Pantle L.M., Smiley-Jewell S.M., et al. Smooth muscle hypertrophy in distal airways of sensitized infant rhesus monkeys exposed to house dust mite allergen. Clin Exp Allergy 34 10 (2004) 1627-1633
46. An S.S., Bai T.R., Bates J.H.T., Black J.L., Brown R.H., Brusasco V., et al. Airway smooth muscle dynamics: a common pathway of airway obstruction in asthma. Eur Respir J 29 5 (2007) 834-860
47. Ma X., Cheng Z., Kong H., Wang Y., Unruh H., Stephens N.L., et al. Changes in biophysical and biochemical properties of single bronchial smooth muscle cells from asthmatic subjects. Am J Physiol Lung Cell Mol Physiol 283 (2002) L1181-L1189
48. Leguillette R., Laviolette M., Bergeron C., Zitouni N., Kogut P., Solway J., et al. Myosin, transgelin, and myosin light chain kinase: expression and function in asthma. Am J Respir Crit Care Med 179 3 (2009) 194-204
49. Wang L., Liu H.W., McNeill K.D., Stelmack G., Scott J.E., and Halayko A.J. Mechanical strain inhibits airway smooth muscle gene transcription via protein kinase C signaling. Am J Respir Cell Mol Biol 31 1 (2004) 54-61
50. Global Initiative for Asthma (GINA) Report. Global strategy for asthma management and prevention. National Institutes of Health. National Heart, Lung and Blood Institute. NIH Publication no. 02-3659. Available from: http://www.ginasthma.com.
51. Hubmayr R.D., Hill M.J., and Wilson T.A. Nonuniform expansion of constricted dog lungs. J Appl Physiol 80 (1996) 522-530
52. Maksym G.N., Fabry B., Butler J.P., Navajas D., Tschumperlin D.J., Laporte J.D., et al. Mechanical properties of cultured human airway smooth muscle cells from 0.05 to 0.4 Hz. J Appl Physiol 89 4 (2000) 1619-1632
53. Shore S.A., Laporte J., Hall I.P., Hardy E., and Panettieri Jr. R.A. Effect of IL-1beta on responses of cultured human airway smooth muscle cells to bronchodilator agonists. Am J Respir Cell Mol Biol 16 (1997) 702-712
54. Pellegrino R., Wilson O., Jenouri G., and Rodarte J.R. Lung mechanics during induced bronchoconstriction. J Appl Physiol 81 2 (1996) 964-975
55. Salter H. On asthma, its pathology and treatment (1860), Churchill, London XII
56. Kapsali T., Permutt S., Laube B., Scichilone N., and Togias A. Potent bronchoprotective effect of deep inspiration and its absence in asthma. J Appl Physiol 89 (2000) 711-720
57. Fredberg J.J., Inouye D.S., Mijailovich S.M., and Butler J.P. Perturbed equilibrium of myosin binding in airway smooth muscle and its implications in bronchospasm. Am J Respir Crit Care Med 159 (1999) 1-9
58. Pellegrino R., Violante B., and Brusasco V. Maximal bronchoconstriction in humans. Relationship to deep inhalation and airway sensitivity. Am J Respir Crit Care Med 153 1 (1996) 115-121
59. Salome C.M., Thorpe C.W., Diba C., Brown N.J., Berend N., and King G.G. Airway re-narrowing following deep inspiration in asthmatic and nonasthmatic subjects. Eur Respir J 22 1 (2003) 62-68
60. Lim T.K., Pride N.B., and Ingram Jr. R.H. Effects of volume history during spontaneous and acutely induced air-flow obstruction in asthma. Am Rev Respir Dis 135 (1987) 591-596
61. Skloot G., and Togias A. Bronchodilation and bronchoprotection by deep inspiration and their relationship to bronchial hyperresponsiveness. Clin Rev Allergy Immunol 24 1 (2003) 55-72
62. Fredberg J., Inouye D., Miller B., Nathan M., Jafari S., Raboudi S., et al. Airway smooth muscle, tidal stretches, and dynamically determined contractile states. Am J Respir Crit Care Med 156 (1997) 1752-1759
63. Gunst S.J. Contractile force of airway smooth muscle during cyclical length changes. J Appl Physiol 55 (1983) 759-769
64. Gunst S.J., Stropp J.Q., and Service J. Mechanical modulation of pressure-volume characteristics of contracted canine airways in vitro. J Appl Physiol 68 (1990) 2223-2229
65. Sasaki H., and Hoppin F.J. Hysteresis of contracted airway smooth muscle. J Appl Physiol 47 (1979) 1251-1262
66. Fredberg J.J., Jones K.A., Nathan M., Raboudi S., Prakash Y.S., Shore S.A., et al. Friction in airway smooth muscle: mechanism, latch and implications in asthma. J Appl Physiol 81 (1996) 2703-2712
67. Gunst S.J., Tang D.D., and Opazo Saez A. Cytoskeletal remodeling of the airway smooth muscle cell: a mechanism for adaptation to mechanical forces in the lung. Respir Physiol Neurobiol 137 2-3 (2003) 151-168
68. Latourelle J., Fabry B., and Fredberg J.J. Dynamic equilibration of airway smooth muscle contraction during physiological loading. J Appl Physiol 92 2 (2002) 771-779
69. Raboudi S.H., Miller B., Butler J.P., Shore S.A., and Fredberg J.J. Dynamically determined contractile states of airway smooth muscle. Am J Respir Crit Care Med 158 5 Pt 3 (1998) S176-S178
70. Fredberg J.J. Bronchospasm and its biophysical basis in airway smooth muscle. Respir Res 5 1 (2004) 2
71. Snyder L.S., Hertz M.I., Peterson M.S., Harmon K.R., Marinelli W.A., Henke C.A., et al. Acute lung injury. Pathogenesis of intraalveolar fibrosis. J Clin Invest 88 2 (1991) 663-673
72. Seow C.Y., Pratusevich V.R., and Ford L.E. Series-to-parallel transition in the filament lattice of airway smooth muscle. J Appl Physiol 89 (2000) 869-876
73. Fairbank N.J., Connolly S.C., MacKinnon J.D., Wehry K., Deng L., and Maksym G.N. Airway smooth muscle cell tone amplifies contractile function in the presence of chronic cyclic strain. Am J Physiol Lung Cell Mol Physiol 295 3 (2008) L479-L488
74. Gosens R, Bromhaar MMG, Tonkes A, Schaafsma D, Zaagsma J, Nelemans SA, et al: Muscarinic M3 receptor-dependent regulation of airway smooth muscle contractile phenotype. Br J Pharmacol 2004;141(6):943-950.
75. Brown R.H., Zerhouni E.A., and Mitzner W. Variability in the size of individual airways over the course of one year. Am J Respir Crit Care Med 151 4 (1995) 1159-1164
76. Brown R.H., Kaczka D.W., Fallano K., Chen S., and Mitzner W. Temporal variability in the responses of individual canine airways to methacholine. J Appl Physiol 104 5 (2008) 1381-1386
77. Brown N.J., Salome C.M., Berend N., Thorpe C.W., and King G.G. Airway distensibility in adults with asthma and healthy adults, measured by forced oscillation technique. Am J Respir Crit Care Med 176 2 (2007) 129-137
78. Ward C., Pais M., Bish R., Reid D., Feltis B., Johns D., et al. Airway inflammation, basement membrane thickening and bronchial hyperresponsiveness in asthma. Thorax 57 4 (2002) 309-316
79. Kennedy D., and Norman C. What Don't We Know? Introduction to special issue with 125 Questions for the 125 Anniversary of Science Magazine. Science 309 5731 (2005) 75
80. Fabry B., Maksym G.N., Butler J.P., Glogauer M., Navajas D., and Fredberg J.J. Scaling the microrheology of living cells. Phys Rev Lett 87 14 (2001) 148102
81. Fabry B., Maksym G.N., Butler J.P., Glogauer M., Navajas D., Taback N.A., et al. Time scale and other invariants of integrative mechanical behavior in living cells. Phys Rev E Stat Nonlin Soft Matter Phys 68 4 Pt 1 (2003) 041914
82. Deng L., Fairbank N.J., Cole D.J., Fredberg J.J., and Maksym G.N. Airway smooth muscle tone modulates mechanically induced cytoskeletal stiffening and remodeling. J Appl Physiol 99 2 (2005) 634-641
83. Deng L., Trepat X., Butler J.P., Millet E., Morgan K.G., Weitz D.A., et al. Fast and slow dynamics of the cytoskeleton. Nat Mater 5 8 (2006) 636-640
84. Fabry B., Maksym G.N., Shore S.A., Moore P.E., Panettieri Jr. R.A., Butler J.P., et al. Signal transduction in smooth muscle: selected contribution: time course and heterogeneity of contractile responses in cultured human airway smooth muscle cells. J Appl Physiol 91 2 (2001) 986-994
85. Bonn D., Tanaka H., Coussot P., and Meunier J. Ageing, shear rejuvenation and avalanches in soft glassy materials. J Phys Condens Matter 16 No. 42 (2004) S4987-S4991
86. Bursac P, Lenormand G, Fabry B, Oliver M, Weitz DA, Viasnoff V, et al: Cytoskeletal remodelling and slow dynamics in the living cell. Nat Mater 2005;4(7):557-561.
87. Fabry B., and Fredberg J.J. Remodeling of the airway smooth muscle cell: are we built of glass?. Respir Physiol Neurobiol 137 2-3 (2003) 109-124