About this Journal Submit a Manuscript Table of Contents
Journal of Allergy
Volume 2012 (2012), Article ID 768982, 8 pages
http://dx.doi.org/10.1155/2012/768982
Review Article

A Brief History of Airway Smooth Muscle’s Role in Airway Hyperresponsiveness

1James Hogg Research Center, St. Paul’s Hospital Vancouver, University of British Columbia, Vancouver, BC, Canada V6Z 1Y6
2Respiratory Division, Department of Medicine, University of British Columbia, Vancouver, BC, V5Z 1Mg, Canada

Received 10 August 2012; Accepted 21 September 2012

Academic Editor: Michael M. Grunstein

Copyright © 2012 C. D. Pascoe et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Floyer, A Treatise of the Asthma. Divided Into Four Parts, John Churchill, London, UK.
  2. H. H. Salter, On Asthma: Its Pathology and Treatment, John Churchill, London, UK, 1859.
  3. H. L. Huber and K. K. Koessler, “The pathology of bronchial asthma,” Archives of Internal Medicine, vol. 30, pp. 689–760, 1922.
  4. A. L. James, J. G. Elliot, R. L. Jones et al., “Airway smooth muscle hypertrophy and hyperplasia in asthma,” American Journal of Respiratory and Critical Care Medicine, vol. 185, no. 10, pp. 1058–1064, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. H. Alexander and R. Paddock, “Bronchial asthma: response to pilocarpine and epinephrine,” Archives of Internal Medicine, vol. 27, pp. 184–191, 1921.
  6. S. Weiss, G. P. Robb, and L. B. Ellis, “The systematic effects of histamine in man,” Archives of Internal Medicine, vol. 49, pp. 360–396, 1932.
  7. I. Starr Jr., “Acetyl-beta-methylcholin: its action on paroxysmal tachycardia and peripheral vascular disease, with discussion of its action in other conditions,” JAMA, vol. 186, pp. 330–345, 1933.
  8. D. L. Philippot, “Asthmatic crisis produced by aerosols of carbaminolycholine in man treated by aerosols of amphetamine: study of action of these substances by determination of useful respiratory volume,” La Presse Médicale, vol. 49, 1941.
  9. J. J. Curry, “The action of histamine on the respiratory tract in normal and asthmatic subjects,” The Journal of Clinical Investigation, vol. 25, pp. 785–791, 1946.
  10. H. S. Herxheimer and H. S. E, “The effect of slow reacting substance (srs-a) in guinea pigs and asthmatic patients,” Physiol, vol. 165, article 78, 1962.
  11. A. A. Mathé, P. Hedqvist, A. Holmgren, and N. Svanborg, “Bronchial hyperreactivity to prostaglandin F 2 and histamine in patients with asthma,” BMJ, vol. 1, no. 5847, pp. 193–196, 1973. View at Scopus
  12. R. S. McNeill and C. G. Ingram, “Effect of propranolol on ventilatory function,” The American Journal of Cardiology, vol. 18, no. 3, pp. 473–475, 1966. View at Scopus
  13. R. E. Wells J, J. E. Walker, and R. B. Hickler, “Effects of cold air on respiratory airflow resistance in patients with respiratory-tract disease,” The New England Journal of Medicine, vol. 263, pp. 263–268, 1960.
  14. J. A. Nadel, B. Tamplin, and Y. Tokiwa, “Mechanism of bronchoconstriction during inhalation of sulfur dioxide,” Archives of Environmental Health, vol. 10, pp. 175–178, 1965. View at Scopus
  15. A. B. Dubois and L. Dautrebande, “Acute effects of breathing inert dust particles and of carbachol aerosol on mechanical characteristics of lungs in man: changes in response after inhaling sympathomimetic aerosols,” The Journal of Clinical Investigation, vol. 37, pp. 1746–1755, 1958.
  16. R. S. McNeill, J. R. Nairn, J. S. Millar, and C. G. Ingram, “Exercise-induced asthma,” The Quarterly Journal of Medicine, vol. 35, no. 137, pp. 55–67, 1966. View at Scopus
  17. K. Devries, H. Booij-Noord, and J. T. Goei, “Hyperreactivity of the bronchial tree to drugs, chemical and physical agents,” in Bronchitis, N. G. M. Orie and H. G. Sluiter, Eds., p. 167, Royal VanGorcum, Assen, The Netherlands, 1964.
  18. C. D. Parker, R. E. Bilbo, and C. E. Reed, “Methacholine aerosol as test for bronchial asthma,” Archives of Internal Medicine, vol. 115, pp. 452–458, 1965. View at Scopus
  19. B. G. Simonsson, “Clinical and physiological studies on chronic bronchitis. 3. Bronchial reactivity to inhaled acetylcholine,” Acta Allergologica, vol. 20, no. 5, pp. 325–348, 1965. View at Scopus
  20. A. J. Woolcock, S. D. Anderson, J. K. Peat et al., “Characteristics of bronchial hyperresponsiveness in chronic obstructive pulmonary disease and in asthma,” American Review of Respiratory Disease, vol. 143, no. 6, pp. 1438–1443, 1991. View at Scopus
  21. de Vries, J. T. Goei, H. Booy-Noord, and N. G. Orie, “Changes during 24 hours in the lung function and histamine hyperreactivity of the bronchial tree in asthmatic and bronchitic patients,” International Archives of Allergy and Applied Immunology, vol. 20, pp. 93–101, 1962. View at Scopus
  22. K. F. Kerrebijin, “Endogenous factors in childhood (NSLD: methodological aspects in popilation studies),” in Bronchitis III, N. G. H. Orie and R. Lende van der, Eds., pp. 38–48, Royal VanGorcum, Assen, The Netherlands, 1970.
  23. D. W. Cockcroft, R. E. Ruffin, J. Dolovich, and F. E. Hargreave, “Allergen-induced increase in non-allergic bronchial reactivity,” Clinical Allergy, vol. 7, no. 6, pp. 503–513, 1977. View at Scopus
  24. E. F. Juniper, P. A. Frith, and F. E. Hargreave, “Long-term stability of bronchial responsiveness to histamine,” Thorax, vol. 37, no. 4, pp. 288–291, 1982. View at Scopus
  25. H. O. Schild, D. F. Hawkins, J. L. Mongar, and H. Herxheimer, “Reactions of isolated human asthmatic lung and bronchial tissue to a specific antigen; histamine release and muscular contraction,” The Lancet, vol. 258, no. 6679, pp. 376–382, 1951. View at Scopus
  26. M. K. Benson, “Bronchial hyperreactivity,” British Journal of Diseases of the Chest, vol. 69, no. 4, pp. 227–239, 1975. View at Scopus
  27. M. K. Benson, “The influence of bronchomotor tone on bronchial reactivity,” Clinical Science and Molecular Medicine, vol. 47, no. 3, p. 13, 1974. View at Scopus
  28. B. G. Simonsson, F. M. Jacobs, and J. A. Nadel, “Role of autonomic nervous system and the cough reflex in the increased responsiveness of airways in patients with obstructive airway disease,” The Journal of Clinical Investigation, vol. 46, no. 11, pp. 1812–1818, 1967. View at Scopus
  29. A. Szentivanyi, “The beta adrenergic theory of the atopic abnormality in bronchial asthma,” Journal of Allergy, vol. 42, no. 4, pp. 203–232, 1968. View at Scopus
  30. B. J. Freedman, “The functional geometry of the bronchi. The relationship between changes in external diameter and calibre, and a consideration of the passive role played by the mucosa in bronchoconstriction,” Bulletin de Physio-Pathologie Respiratoire, vol. 8, no. 3, pp. 545–552, 1972. View at Scopus
  31. A. J. Woolcock, C. M. Salome, and K. Yan, “The shape of the dose-response curve to histamine in asthmatic and normal subjects,” American Review of Respiratory Disease, vol. 130, no. 1, pp. 71–75, 1984. View at Scopus
  32. T. R. Bai, “Abnormalities in airway smooth muscle in fatal asthma,” American Review of Respiratory Disease, vol. 141, no. 3, pp. 552–557, 1990. View at Scopus
  33. A. M. Bramley, R. J. Thomson, C. R. Roberts, and R. R. Schellenberg, “Hypothesis: excessive bronchoconstriction in asthma is due to decreased airway elastance,” European Respiratory Journal, vol. 7, no. 2, pp. 337–341, 1994. View at Scopus
  34. T. R. Bai, “Abnormalities in airway smooth muscle in fatal asthma: a comparison between trachea and bronchus,” American Review of Respiratory Disease, vol. 143, no. 2, pp. 441–443, 1991. View at Scopus
  35. J. Cerrina, M. Le Roy Ladurie, and C. Labat, “Comparison of human bronchial muscle responses to histamine in vivo with histamine and isoproterenol agonists in vitro,” American Review of Respiratory Disease, vol. 134, no. 1, pp. 57–61, 1986. View at Scopus
  36. J. Cerrina, C. Labat, I. Haye-Legrande, B. Raffestin, J. Benveniste, and C. Brink, “Human isolated bronchial muscle preparations from asthmatic patients: effects of indomethacin and contractile agonists,” Prostaglandins, vol. 37, no. 4, pp. 457–469, 1989. View at Scopus
  37. L. Y. M. Chin, Y. Bosse, C. Pascoe, T. L. Hackett, C. Y. Seow, and P. D. Paré, “Mechanical properties of asthmatic airway smooth muscle,” European Respiratory Journal, vol. 40, no. 1, pp. 45–54, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. S. D. Whicker, C. L. Armour, and J. L. Black, “Responsiveness of bronchial smooth muscle from asthmatic patients to relaxant and contractile agonists,” Pulmonary Pharmacology, vol. 1, no. 1, pp. 25–31, 1988. View at Scopus
  39. R. H. Moreno, J. C. Hogg, and P. D. Pare, “Mechanics of airway narrowing,” American Review of Respiratory Disease, vol. 133, no. 6, pp. 1171–1180, 1986. View at Scopus
  40. A. L. James, P. D. Pare, and J. C. Hogg, “The mechanics of airway narrowing in asthma,” American Review of Respiratory Disease, vol. 139, no. 1, pp. 242–246, 1989. View at Scopus
  41. B. R. Wiggs, C. Bosken, P. D. Paré, A. James, and J. C. Hogg, “A model of airway narrowing in asthma and in chronic obstructive pulmonary disease,” American Review of Respiratory Disease, vol. 145, no. 6, pp. 1251–1258, 1992. View at Scopus
  42. R. K. Lambert, B. R. Wiggs, K. Kuwano, J. C. Hogg, and P. D. Pare, “Functional significance of increased airway smooth muscle in asthma and COPD,” Journal of Applied Physiology, vol. 74, no. 6, pp. 2771–2781, 1993. View at Scopus
  43. M. N. Oliver, B. Fabry, A. Marinkovic, S. M. Mijailovich, J. P. Butler, and J. J. Fredberg, “Airway hyperresponsiveness, remodeling, and smooth muscle mass: right answer, wrong reason?” American Journal of Respiratory Cell and Molecular Biology, vol. 37, no. 3, pp. 264–272, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. X. Ma, Z. Cheng, H. Kong et al., “Changes in biophysical and biochemical properties of single bronchial smooth muscle cells from asthmatic subjects,” American Journal of Physiology, vol. 283, no. 6, pp. L1181–L1189, 2002. View at Scopus
  45. R. Léguillette, M. Laviolette, C. Bergeron et al., “Myosin, transgelin, and myosin light chain kinase expression and function in asthma,” American Journal of Respiratory and Critical Care Medicine, vol. 179, no. 3, pp. 194–204, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. V. R. Pratusevich, C. Y. Seow, and L. E. Ford, “Plasticity in canine airway smooth muscle,” Journal of General Physiology, vol. 105, no. 1, pp. 73–94, 1995. View at Publisher · View at Google Scholar · View at Scopus
  47. G. Skloot, S. Permutt, and A. Togias, “Airway hyperresponsiveness in asthma: a problem of limited smooth muscle relaxation with inspiration,” The Journal of Clinical Investigation, vol. 96, no. 5, pp. 2393–2403, 1995. View at Scopus
  48. L. Wang and P. D. Paré, “Deep inspiration and airway smooth muscle adaptation to length change,” Respiratory Physiology and Neurobiology, vol. 137, no. 2-3, pp. 169–178, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. G. Skloot and A. Togias, “Bronchodilation and bronchoprotection by deep inspiration and their relationship to bronchial hyperresponsiveness,” Clinical Reviews in Allergy and Immunology, vol. 24, no. 1, pp. 55–71, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. X. Shen, M. F. Wu, R. S. Tepper, and S. J. Gunst, “Mechanisms for the mechanical response of airway smooth muscle to length oscillation,” Journal of Applied Physiology, vol. 83, no. 3, pp. 731–738, 1997. View at Scopus
  51. L. Wang, P. D. Paré, and C. Y. Seow, “Effects of length oscillation on the subsequent force development in swine tracheal smooth muscle,” Journal of Applied Physiology, vol. 88, no. 6, pp. 2246–2250, 2000. View at Scopus
  52. J. J. Fredberg, D. S. Inouye, S. M. Mijailovich, and J. P. Butler, “Perturbed equilibrium of myosin binding in airway smooth muscle and its implications in bronchospasm,” American Journal of Respiratory and Critical Care Medicine, vol. 159, no. 3, pp. 959–967, 1999. View at Scopus
  53. T. K. Lim, N. B. Pride, and R. H. Ingram, “Effects of volume history during spontaneous and acutely induced air-flow obstruction in asthma,” American Review of Respiratory Disease, vol. 135, no. 3, pp. 591–596, 1987. View at Scopus
  54. P. Gayrard, J. Orehek, C. Grimaud, and J. Charpin, “Bronchoconstrictor effects of a deep inspiration in patients with asthma,” American Review of Respiratory Disease, vol. 111, no. 4, pp. 433–439, 1975. View at Scopus
  55. P. Malmberg, K. Larsson, B. M. Sundblad, and W. Zhiping, “Importance of the time interval between FEV1 measurements in a methacholine provocation test,” European Respiratory Journal, vol. 6, no. 5, pp. 680–686, 1993. View at Scopus
  56. B. J. Moore, L. M. Verburgt, G. G. King, and P. D. Paré, “The effect of deep inspiration on methacholine dose-response curves in normal subjects,” American Journal of Respiratory and Critical Care Medicine, vol. 156, no. 4, pp. 1278–1281, 1997. View at Scopus
  57. X. Shen RR, S. J. Gunst, and R. S. Tepper, “Effect of timing of deep inspiration on airway response to methacholine challenge in mature and immature rabbits,” American Journal of Respiratory and Critical Care Medicine, vol. 159, pp. 959–967, 1999.
  58. D. C.-B. R. Chandy, E. N. Schachter, and G. S. Skloot, “Differences between the bronchoprotective effect of fast and slow deep inspiration,” American Journal of Respiratory and Critical Care Medicine, vol. 159, article A468, 1999.
  59. N. Scichilone, T. Kapsali, S. Permutt, and A. Togias, “Deep inspiration-induced bronchoprotection is stronger than bronchodilation,” American Journal of Respiratory and Critical Care Medicine, vol. 162, no. 3, pp. 910–916, 2000. View at Scopus
  60. N. Scichilone, S. Permutt, and A. Togias, “The lack of the bronchoprotective and not the bronchodilatory ability of deep inspiration is associated with airway hyperresponsiveness,” American Journal of Respiratory and Critical Care Medicine, vol. 163, no. 2, pp. 413–419, 2001. View at Scopus
  61. T. Kapsali, S. Permutt, B. Laube, N. Scichilone, and A. Togias, “Potent bronchoprotective effect of deep inspiration and its absence in asthma,” Journal of Applied Physiology, vol. 89, no. 2, pp. 711–720, 2000. View at Scopus
  62. J. J. Fredberg, D. Inouye, B. Miller et al., “Airway smooth muscle, tidal stretches, and dynamically determined contractile states,” American Journal of Respiratory and Critical Care Medicine, vol. 156, no. 6, pp. 1752–1759, 1997. View at Scopus
  63. B. E. McParland, R. R. Tait, P. D. Paré, and C. Y. Seow, “The role of airway smooth muscle during an attack of asthma simulated in vitro,” American Journal of Respiratory Cell and Molecular Biology, vol. 33, no. 5, pp. 500–504, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. R. H. Brown, N. Scichilone, B. Mudge, F. B. Diemer, S. Permutt, and A. Togias, “High-resolution computed tomographic evaluation of airway distensibility and the effects of lung inflation on airway caliber in healthy subjects and individuals with asthma,” American Journal of Respiratory and Critical Care Medicine, vol. 163, no. 4, pp. 994–1001, 2001. View at Scopus
  65. A. Jensen, H. Atileh, B. Suki, E. P. Ingenito, and K. R. Lutchen, “Selected contribution: airway caliber in healthy and asthmatic subjects: effects of bronchial challenge and deep inspirations,” Journal of Applied Physiology, vol. 91, no. 1, pp. 506–515, 2001. View at Scopus
  66. L. Wang, P. Chitano, and T. M. Murphy, “Length oscillation induces force potentiation in infant guinea pig airway smooth muscle,” American Journal of Physiology, vol. 289, no. 6, pp. L909–L915, 2005. View at Publisher · View at Google Scholar · View at Scopus
  67. A. Weist, T. Williams, J. Kisling, C. Clem, and R. S. Tepper, “Volume history and effect on airway reactivity in infants and adults,” Journal of Applied Physiology, vol. 93, no. 3, pp. 1069–1074, 2002. View at Scopus
  68. A. Raqeeb, D. Solomon, P. D. Paré, and C. Y. Seow, “Length oscillation mimicking periodic individual deep inspirations during tidal breathing attenuates force recovery and adaptation in airway smooth muscle,” Journal of Applied Physiology, vol. 109, no. 5, pp. 1476–1482, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. G. A. Farkas and C. Roussos, “Diaphragm in emphysematous hamsters: sarcomere adaptability,” Journal of Applied Physiology Respiratory Environmental and Exercise Physiology, vol. 54, no. 6, pp. 1635–1640, 1983. View at Scopus
  70. S. G. Kelsen, T. Wolanski, G. S. Supinski, and U. Roessmann, “The effect of elastase-induced emphysema on diaphragmatic muscle structure in hamsters,” American Review of Respiratory Disease, vol. 127, no. 3, pp. 330–334, 1983. View at Scopus
  71. J. B. Shrager, D. K. Kim, Y. J. Hashmi et al., “Sarcomeres are added in series to emphysematous rat diaphragm after lung volume reduction surgery,” Chest, vol. 121, no. 1, pp. 210–215, 2002. View at Publisher · View at Google Scholar · View at Scopus
  72. L. Wang, P. D. Paré, and C. Y. Seow, “Selected contribution: effect of chronic passive length change on airway smooth muscle length-tension relationship,” Journal of Applied Physiology, vol. 90, no. 2, pp. 734–740, 2001. View at Scopus
  73. J. Naghshin, L. Wang, P. D. Paré, and C. Y. Seow, “Adaptation to chronic length change in explanted airway smooth muscle,” Journal of Applied Physiology, vol. 95, no. 1, pp. 448–453, 2003. View at Scopus
  74. A. S. LaPrad, A. R. West, P. B. Noble, K. R. Lutchen, and H. W. Mitchell, “Maintenance of airway caliber in isolated airways by deep inspiration and tidal strains,” Journal of Applied Physiology, vol. 105, no. 2, pp. 479–485, 2008. View at Publisher · View at Google Scholar · View at Scopus
  75. P. B. Noble, P. K. McFawn, and H. W. Mitchell, “Responsiveness of the isolated airway during simulated deep inspirations: effect of airway smooth muscle stiffness and strain,” Journal of Applied Physiology, vol. 103, no. 3, pp. 787–795, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. P. B. Noble, R. L. Jones, E. T. Needi et al., “Responsiveness of the human airway in vitro during deep inspiration and tidal oscillation,” Journal of Applied Physiology, vol. 110, no. 6, pp. 1510–1518, 2011. View at Publisher · View at Google Scholar · View at Scopus
  77. A. S. LaPrad, T. L. Szabo, B. Suki, and K. R. Lutchen, “Tidal stretches do not modulate responsiveness of intact airways in vitro,” Journal of Applied Physiology, vol. 109, no. 2, pp. 295–304, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. G. G. King, B. J. Moore, C. Y. Seow, and P. D. Paré, “Time course of increased airway narrowing caused by inhibition of deep inspiration during methacholine challenge,” American Journal of Respiratory and Critical Care Medicine, vol. 160, no. 2, pp. 454–457, 1999. View at Scopus
  79. G. G. King, B. J. Moore, C. Y. Seow, and P. D. Paré, “Airway narrowing associated with inhibition of deep inspiration during methacholine inhalation in asthmatics,” American Journal of Respiratory and Critical Care Medicine, vol. 164, no. 2, pp. 216–218, 2001. View at Scopus
  80. D. G. Chapman, N. Berend, G. G. King, B. E. McParland, and C. M. Salome, “Deep inspirations protect against airway closure in nonasthmatic subjects,” Journal of Applied Physiology, vol. 107, no. 2, pp. 564–569, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. E. Crimi, R. Pellegrino, M. Milanese, and V. Brusasco, “Deep breaths, methacholine, and airway narrowing in healthy and mild asthmatic subjects,” Journal of Applied Physiology, vol. 93, no. 4, pp. 1384–1390, 2002. View at Scopus
  82. A. M. Slats, K. Janssen, A. Van Schadewijk et al., “Bronchial inflammation and airway responses to deep inspiration in asthma and chronic obstructive pulmonary disease,” American Journal of Respiratory and Critical Care Medicine, vol. 176, no. 2, pp. 121–128, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. R. S. Wong, A. N. Larcombe, L. B. Fernandes, G. R. Zosky, and P. B. Noble, “The mechanism of deep inspiration induced bronchoprotection: evidence from a mouse model,” European Respiratory Journal, vol. 40, no. 4, pp. 982–989, 2012.
  84. K. H. Kuo, L. Wang, P. D. Paré, L. E. Ford, and C. Y. Seow, “Myosin thick filament lability induced by mechanical strain in airway smooth muscle,” Journal of Applied Physiology, vol. 90, no. 5, pp. 1811–1816, 2001. View at Scopus
  85. Y. Bossé, L. Y. M. Chin, P. D. Paré, and C. Y. Seow, “Adaptation of airway smooth muscle to basal tone relevance to airway hyperresponsiveness,” American Journal of Respiratory Cell and Molecular Biology, vol. 40, no. 1, pp. 13–18, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. C. Pascoe, Y. Jiao, C. Y. Seow, P. D. Paré, and Y. Bossé, “Force oscillations simulating breathing maneuvers do not prevent force adaptation,” American Journal of Respiratory Cell and Molecular Biology, vol. 47, no. 1, pp. 44–49, 2012. View at Publisher · View at Google Scholar · View at Scopus
  87. Y. Bossé, D. G. Chapman, P. D. Paré, G. G. King, and C. M. Salome, “A “good” muscle in a “bad” environment: the importance of airway smooth muscle force adaptation to airway hyperresponsiveness,” Respir Physiol Neurobiol, vol. 179, pp. 269–275, 2011.
  88. Y. Bossé and P. D. Paré, “Histamine and endogenously produced spasmogenic prostaglandins increase the strength of airway smooth muscle,” Journal of Allergy and Clinical Immunology, vol. 129, 2012, Abstract 52.