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Published ahead of print on January 16, 2003, doi:10.1164/rccm.200209-1030OC
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American Journal of Respiratory and Critical Care Medicine Vol 167. pp. 1360-1368, (2003)
© 2003 American Thoracic Society

Airway Structural Alterations Selectively Associated with Severe Asthma

Laurent Benayoun, Anne Druilhe, Marie-Christine Dombret, Michel Aubier and Marina Pretolani

Institut National de la Santé et de la Recherche Médicale Unité 408, Faculté de Médecine Xavier Bichat and Service de Pneumologie, Hôpital Bichat, Paris, France

Correspondence and requests for reprints should be addressed to Marina Pretolani, Ph.D., INSERM U408, Faculté de Médecine Xavier Bichat, 16 rue Henri Huchard, 75018 Paris, France. E-mail: mpretol{at}bichat.inserm.fr

To identify airway pathologic abnormalities selectively associated with severe asthma, we examined 10 control subjects, 10 patients with intermittent asthma, 15 patients with mild-to-moderate persistent asthma, 15 patients with severe persistent asthma, and 10 patients with chronic obstructive pulmonary disease. Bronchial biopsies were assessed for epithelial integrity; subepithelial basement membrane (SBM) thickness; collagen type III deposition; eosinophil, neutrophil, and fibroblast numbers; mucous gland and airway smooth muscle (ASM) areas; SBM-ASM distance; ASM hypertrophy (increased cell size); and the expression of the contractile proteins {alpha}-actin, smooth muscle myosin heavy-chain isoforms, myosin light-chain kinase, and the phosphorylated form of the regulatory light chain of myosin. Neither mucosal eosinophilia nor neutrophilia, epithelial damage, or SBM thickness reflected asthma severity. In contrast, higher numbers of fibroblasts (p < 0.001), an increase in collagen type III deposition (p < 0.020), larger mucous gland (p < 0.040) and ASM (p < 0.001) areas, augmented ASM cell size (p < 0.001), and myosin light-chain kinase expression (p < 0.005) distinguished patients with severe persistent asthma from patients with milder disease or with chronic obstructive pulmonary disease. Stepwise multivariate regression analysis established that fibroblast numbers and ASM cell size were negatively associated with prebronchodilator and postbronchodilator FEV1 values in patients with asthma. We conclude that fibroblast accumulation and ASM hypertrophy in proximal airways are selective determinants of severe persistent asthma.

Key Words: airway smooth muscle • hypertrophy • myosin light chain kinase • fibroblasts • chronic obstructive pulmonary disease




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Airway Smooth Muscle and Mast Cell-derived CC Chemokine Ligand 19 Mediate Airway Smooth Muscle Migration in Asthma
Am. J. Respir. Crit. Care Med., December 1, 2006; 174(11): 1179 - 1188.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
S. Pegorier, L. A. Wagner, G. J. Gleich, and M. Pretolani
Eosinophil-Derived Cationic Proteins Activate the Synthesis of Remodeling Factors by Airway Epithelial Cells
J. Immunol., October 1, 2006; 177(7): 4861 - 4869.
[Abstract] [Full Text] [PDF]

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 ChestHome page
G. W. Canonica
Treating Asthma as an Inflammatory Disease
Chest, July 1, 2006; 130(1_suppl): 21S - 28S.
[Abstract] [Full Text] [PDF]

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 ChestHome page
C. Bergeron and L.-P. Boulet
Structural changes in airway diseases: characteristics, mechanisms, consequences, and pharmacologic modulation.
Chest, April 1, 2006; 129(4): 1068 - 1087.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
W. R. Henderson Jr., G. K. S. Chiang, Y.-t. Tien, and E. Y. Chi
Reversal of Allergen-induced Airway Remodeling by CysLT1 Receptor Blockade
Am. J. Respir. Crit. Care Med., April 1, 2006; 173(7): 718 - 728.
[Abstract] [Full Text] [PDF]

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 ThoraxHome page
J Wicks, H M Haitchi, S T Holgate, D E Davies, and R M Powell
Enhanced upregulation of smooth muscle related transcripts by TGF{beta}2 in asthmatic (myo) fibroblasts
Thorax, April 1, 2006; 61(4): 313 - 319.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Cell Mol. Bio.Home page
A. M. Goldsmith, J. K. Bentley, L. Zhou, Y. Jia, K. N. Bitar, D. C. Fingar, and M. B. Hershenson
Transforming Growth Factor-beta Induces Airway Smooth Muscle Hypertrophy
Am. J. Respir. Cell Mol. Biol., February 1, 2006; 34(2): 247 - 254.
[Abstract] [Full Text] [PDF]

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 Eur Respir JHome page
C. Boxall, S. T. Holgate, and D. E. Davies
The contribution of transforming growth factor-{beta} and epidermal growth factor signalling to airway remodelling in chronic asthma
Eur. Respir. J., January 1, 2006; 27(1): 208 - 229.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
T. Koya, T. Kodama, K. Takeda, N. Miyahara, E.-S. Yang, C. Taube, A. Joetham, J.-W. Park, A. Dakhama, and E. W. Gelfand
Importance of Myeloid Dendritic Cells in Persistent Airway Disease after Repeated Allergen Exposure
Am. J. Respir. Crit. Care Med., January 1, 2006; 173(1): 42 - 55.
[Abstract] [Full Text] [PDF]

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 Proc Am Thorac SocHome page
K. F. Chung
The Role of Airway Smooth Muscle in the Pathogenesis of Airway Wall Remodeling in Chronic Obstructive Pulmonary Disease
Proceedings of the ATS, November 1, 2005; 2(4): 347 - 354.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
E. L. J. van Rensen, J. K. Sont, C. E. Evertse, L. N. A. Willems, T. Mauad, P. S. Hiemstra, P. J. Sterk, and the AMPUL Study Group
Bronchial CD8 Cell Infiltrate and Lung Function Decline in Asthma
Am. J. Respir. Crit. Care Med., October 1, 2005; 172(7): 837 - 841.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
D. A. Kuperman, X. Huang, L. Nguyenvu, C. Holscher, F. Brombacher, and D. J. Erle
IL-4 Receptor Signaling in Clara Cells Is Required for Allergen-Induced Mucus Production
J. Immunol., September 15, 2005; 175(6): 3746 - 3752.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
P. Joubert, S. Lajoie-Kadoch, I. Labonte, A. S. Gounni, K. Maghni, V. Wellemans, J. Chakir, M. Laviolette, Q. Hamid, and B. Lamkhioued
CCR3 Expression and Function in Asthmatic Airway Smooth Muscle Cells
J. Immunol., August 15, 2005; 175(4): 2702 - 2708.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
L. Deng, N. J. Fairbank, D. J. Cole, J. J. Fredberg, and G. N. Maksym
Airway smooth muscle tone modulates mechanically induced cytoskeletal stiffening and remodeling
J Appl Physiol, August 1, 2005; 99(2): 634 - 641.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Cell Mol. Bio.Home page
L. Zhou, A. M. Goldsmith, J. K. Bentley, Y. Jia, M. L. Rodriguez, M. K. Abe, D. C. Fingar, and M. B. Hershenson
4E-Binding Protein Phosphorylation and Eukaryotic Initiation Factor-4E Release Are Required for Airway Smooth Muscle Hypertrophy
Am. J. Respir. Cell Mol. Biol., August 1, 2005; 33(2): 195 - 202.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
S. Wenzel
Severe Asthma in Adults
Am. J. Respir. Crit. Care Med., July 15, 2005; 172(2): 149 - 160.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
R. Gosens, I. S. T. Bos, J. Zaagsma, and H. Meurs
Protective Effects of Tiotropium Bromide in the Progression of Airway Smooth Muscle Remodeling
Am. J. Respir. Crit. Care Med., May 15, 2005; 171(10): 1096 - 1102.
[Abstract] [Full Text] [PDF]

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 PhysiologyHome page
R. J. Homer and J. A. Elias
Airway Remodeling in Asthma: Therapeutic Implications of Mechanisms
Physiology, February 1, 2005; 20(1): 28 - 35.
[Abstract] [Full Text] [PDF]

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 ThoraxHome page
S Guerra
Clinical remission of asthma: what lies beyond?
Thorax, January 1, 2005; 60(1): 5 - 6.
[Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
M. Wahl, T. J. Eddinger, and C.-M. Hai
Sinusoidal length oscillation- and receptor-mediated mRNA expression of myosin isoforms and {alpha}-SM actin in airway smooth muscle
Am J Physiol Cell Physiol, December 1, 2004; 287(6): C1697 - C1708.
[Abstract] [Full Text] [PDF]

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 Proc Am Thorac SocHome page
P. K. Jeffery
Remodeling and Inflammation of Bronchi in Asthma and Chronic Obstructive Pulmonary Disease
Proceedings of the ATS, November 1, 2004; 1(3): 176 - 183.
[Abstract] [Full Text] [PDF]

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 Proc Am Thorac SocHome page
P. Chanez, A. Bourdin, I. Vachier, P. Godard, J. Bousquet, and A. M. Vignola
Effects of Inhaled Corticosteroids on Pathology in Asthma and Chronic Obstructive Pulmonary Disease
Proceedings of the ATS, November 1, 2004; 1(3): 184 - 190.
[Abstract] [Full Text] [PDF]

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 Eur Respir JHome page
A.G. Stewart
Emigration and immigration of mesenchymal cells: a multicultural airway wall
Eur. Respir. J., October 1, 2004; 24(4): 515 - 517.
[Full Text] [PDF]

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 ChestHome page
A. F. Gelb, A. Schein, E. Nussbaum, C. M. Shinar, Y. Aelony, H. Aharonian, and N. Zamel
Risk Factors for Near-Fatal Asthma
Chest, October 1, 2004; 126(4): 1138 - 1146.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
A. ten Brinke, A. H. Zwinderman, P. J. Sterk, K. F. Rabe, and E. H. Bel
"Refractory" Eosinophilic Airway Inflammation in Severe Asthma: Effect of Parenteral Corticosteroids
Am. J. Respir. Crit. Care Med., September 15, 2004; 170(6): 601 - 605.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
J. L. Black
Asthma--More Muscle Cells or More Muscular Cells?
Am. J. Respir. Crit. Care Med., May 1, 2004; 169(9): 980 - 981.
[Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
P. G. Woodruff, G. M. Dolganov, R. E. Ferrando, S. Donnelly, S. R. Hays, O. D. Solberg, R. Carter, H. H. Wong, P. S. Cadbury, and J. V. Fahy
Hyperplasia of Smooth Muscle in Mild to Moderate Asthma without Changes in Cell Size or Gene Expression
Am. J. Respir. Crit. Care Med., May 1, 2004; 169(9): 1001 - 1006.
[Abstract] [Full Text] [PDF]

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 Proc Am Thorac SocHome page
S. T. Holgate, J. Holloway, S. Wilson, F. Bucchieri, S. Puddicombe, and D. E. Davies
Epithelial-Mesenchymal Communication in the Pathogenesis of Chronic Asthma
Proceedings of the ATS, April 1, 2004; 1(2): 93 - 98.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
L. Zhou, J. Li, A. M. Goldsmith, D. C. Newcomb, D. M. Giannola, R. G. Vosk, E. M. Eves, M. R. Rosner, J. Solway, and M. B. Hershenson
Human Bronchial Smooth Muscle Cell Lines Show a Hypertrophic Phenotype Typical of Severe Asthma
Am. J. Respir. Crit. Care Med., March 15, 2004; 169(6): 703 - 711.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
M. Terada, E. A. B. Kelly, and N. N. Jarjour
Increased Thrombin Activity after Allergen Challenge: A Potential Link to Airway Remodeling?
Am. J. Respir. Crit. Care Med., February 1, 2004; 169(3): 373 - 377.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
M. J. Tobin
Asthma, Airway Biology, and Nasal Disorders in AJRCCM 2003
Am. J. Respir. Crit. Care Med., January 15, 2004; 169(2): 265 - 276.
[Full Text] [PDF]

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 Eur Respir JHome page
A.M. Vignola, A. Bonanno, M. Profita, L. Riccobono, N. Scichilone, M. Spatafora, J. Bousquet, G. Bonsignore, and V. Bellia
Effect of age and asthma duration upon elastase and {alpha}1-antitrypsin levels in adult asthmatics
Eur. Respir. J., November 1, 2003; 22(5): 795 - 801.
[Abstract] [Full Text] [PDF]

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 J. Leukoc. Biol.Home page
B. McElhinney, M. E. Poynter, P. Shrivastava, S. L. Hazen, and Y. M. W. Janssen-Heininger
Eosinophil peroxidase catalyzes JNK-mediated membrane blebbing in a Rho kinase-dependent manner
J. Leukoc. Biol., November 1, 2003; 74(5): 897 - 907.
[Abstract] [Full Text] [PDF]


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