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[1]Jenkins MA, JL Hopper, G Bowes, JB Carlin, LB Flander, GG Giles. Factors in childhood as predictors of asthma in adult life. BMJ 309, 90-93 (1994)
[2]Burrows B, MR Sears, EM Flannery, GP Herbison, MD Holdaway. Relationships of Bronchial Responsiveness Assessed by Methacholine to Serum IgE, Lung Function, Symptoms, and Diagnoses in 11-Year-Old New Zealand Children. J Allergy Clin Immunol 90, 376-385 (1992)
[3]Tumas DB, B Chan, W Werther, T Wrin, J Vennari, N Desjardin, RL Shields, P Jardieu. Anti-IgE Efficacy in Murine Asthma Models Is Dependent on the Method of Allergen Sensitization. J Allergy Clin Immunol 107, 1025-1033 (2001)
[4]Saglani S, K Malmstrom, AS Pelkonen, LP Malmberg, H Lindahl, M Kajosaari, M Turpeinen, AV Rogers, DN Payne, A Bush, T Haahtela, MJ Makela, PK Jeffery. Airway Remodeling and Inflammation in Symptomatic Infants With Reversible Airflow Obstruction. Am J Respir Crit Care Med 171, 722-727 (2005)
[5]Tormanen KR, L Uller, CG Persson, JS Erjefalt. Allergen Exposure of Mouse Airways Evokes Remodeling of Both Bronchi and L arge Pulmonary Vessels. Am J Respir Crit Care Med 171, 19-25 (2005)
[6]Saetta M, SA Di, C Rosina, G Thiene, LM Fabbri. Quantitative Structural Analysis of Peripheral Airways and Arteries in Sudden Fatal Asthma. Am Rev Respir Dis 143, 138-143 (1991)
[7]Chetta A, E Marangio, D Olivieri. Inhaled Steroids and Airway Remodelling in Asthma. Acta Biomed Ateneo Parmense 74, 121-125 (2003)
[8]Li X, J Wilson. Increased Vascularity of the Bronchial Mucosa in Mild Asthma. Am J Respir Crit Care Med 156, 229-233 (1997)
[9]Siddiqui S, A Sutcliffe, A Shikotra, L Woodman, C Doe, McKenna S, A Wardlow, P Bradding, I Pavord, C Brightling. Vascular Remodeling Is a Feature of Asthma and Nonasthmatic Eosinophilic Bronchitis. J Allergy Clin Immunol 120, 813-819 (2007)
[10]Chitano P, L Wang, S Degan, CL Worthington, V Pozzato, SH Hussaini, WC Turner, DR Dorscheid, TM Murphy. Ovalbumin Sensitization of Guinea Pig at Birth Prevents the Ontogenetic Decrease in Airway Smooth Muscle Responsiveness. Physiol Rep 2, e12241 (2014)
[11]Aven L, J Paez-Cortez, R Achey, R Krishnan, S Ram-Mohan, WW Cruikshank, A Fine, X Ai. An NT4/TrkB-Dependent Increase in Innervation Links Early-Life Allergen Exposure to Persistent Airway Hyperreactivity. FASEB J 28, 897-907 (2014)
[12]Guerassimov A, Y Hoshino, Y Takubo, A Turcotte, M Yamamoto, H Ghezzo, A Triantafillapoulos, K Whittaker, JR Hoidal, MG Cosio. The Development of Emphysema in Cigarette Smoke-Exposed Mice Is Strain Dependent. Am J Respir Crit Care Med 170, 974-980 (2004)
[13]Lim DH, JY Cho, M Miller, K McElwain, S McElwain, DH Broide. Reduced Peribronchial Fibrosis in Allergen-Challenged MMP-9-Deficient Mice. Am J Physiol Lung Cell Mol Physiol 291, L265-L271 (2006)
[14]Kanazawa H. VEGF, Angiopoietin-1 and -2 in Bronchial Asthma: New Molecular Targets in Airway Angiogenesis and Microvascular Remodeling. Recent Pat Inflamm Allergy Drug Discov 2001, 1-8 (2007)
[15]Coyle AJ, K Wagner, C Bertrand, S Tsuyuki, J Bews, C Heusser. Central Role of Immunoglobulin (Ig) E in the Induction of Lung Eosinophil Infiltration and T Helper 2 Cell Cytokine Production: Inhibition by a Non-Anaphylactogenic Anti-IgE Antibody. J Exp Med 183, 1303-1310 (1996)
[16]Mehlhop PD, M van de Rijn, JP Brewer, AB Kisselgof, RS Geha, HC Oettgen, TR Martin. CD40L, but Not CD40, Is Required for Allergen-Induced Bronchial Hyperresponsiveness in Mice. Am J Respir Cell Mol Biol 23, 646-651 (2000)
[17]Nwaru BI, M Erkkola, S Ahonen, M Kaila, AM Haapala, C Kronberg-Kippila, R Salmelin, R Veijola, J Ilonen, O Simell, M Knip, SM Virtanen. Age at the Introduction of Solid Foods During the First Year and Allergic Sensitization at Age 5 Years. Pediatrics 125, 50-59 (2010)
[18]Mitzner W, W Lee, D Georgakopoulos, E Wagner. Angiogenesis in the Mouse Lung. Am J Pathol 157, 93-101 (2000)
[19]Tillie-Leblond I, J de Blic, F Jaubert, B Wallaert, P Scheinmann, P Gosset. Airway Remodeling Is Correlated With Obstruction in Children With Severe Asthma. Allergy 63, 533-541 (2008)
[20]Bradding P, AF Walls, ST Holgate. The Role of the Mast Cell in the Pathophysiology of Asthma. J Allergy Clin Immunol 117, 1277-1284 (2006)
[21]Su X, N Taniuchi, E Jin, M Fujiwara, L Zhang, M Ghazizadeh, H Tashimo, N Yamashita, K Ohta, O Kawanami. Spatial and Phenotypic Characterization of Vascular Remodeling in a Mouse Model of Asthma. Pathobiology 75, 42-56 (2008)
[22]McDonald D. Angiogenesis and Remodeling of Airway Vasculature in Chronic Inflammation. Am J Respir Crit Care Med 164, S39-S45 (2001)
[23]Watson CJ, NJ Webb, MJ Bottomley, PE Brenchley. Identification of polymorphisms within the vascular endothelial growth fac CJ tor (VEGF) gene: correlation with variation in VEGF protein production. Cytokine 12, 1232-1235 (2000)
[24]Fehrenbach H, M Kasper, H Maase, D Schuh, M Muller. Differential immunolocalization of VEGF in rat and human adult lung, and in experimental rat lung fibrosis: light, fluorescence, and electron microscopy. Anat Rec 254, 61-73 (1999)
[25]Faffe DS, L Flynt, K Bourgeois, RA Panettieri, Jr., SA Shore. Interleukin-13 and Interleukin-4 Induce Vascular Endothelial Growth Factor Release From Airway Smooth Muscle Cells: Role of Vascular Endothelial Growth Factor Genotype. Am J Respir Cell Mol Biol 34, 213-218 (2006)
[26]Cao G, CD O’Brien, Z Zhou, SM Sanders, GN Greenbaum, A Makrigiannakis, HM DeLisser. Involvement of Human PECAM-1 in Angiogenesis and in vitro Endothelial Cell Migration. Am J Physiol Cell Physiol 282, C1181-C1190 (2002)
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Frontiers in Bioscience-Elite (FBE) is published by IMR Press from Volume 13 Issue 2 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.
IgE mediates broncho-vascular remodeling after neonatal sensitization in mice
1 Department of Pediatrics, Floating Hospital for Children, Tufts Medical Center, Boston, MA
*Author to whom correspondence should be addressed.
Abstract
The temporal origins of childhood asthma are incompletely understood. We hypothesize that allergen sensitization which begins in early infancy causes IgE-mediated airway and vascular remodeling, and airway hyper-responsiveness. Mice were sensitized with ovalbumin (OVA) without or with anti-IgE antibody from postnatal day (P) 10 through P42. We studied airway resistance in response to Methacholine (MCh) challenge, bronchoalveolar lavage fluid (BAL) inflammatory cell content, immunohistochemistry for inflammation, alpha-smooth muscle actin (alpha-SMA) and platelet/endothelial cell adhesion molecule (PECAM) proteins, and Western blotting for vascular endothelial growth factor (VEGF) protein. Compared to controls, mice treated with OVA had increased airway resistance (baseline: 192% of control; MCH 12 mg/mL 170% of control; P less than 0.0.5). OVA treatment also increased lung alpha-SMA, VEGF and PECAM compared to controls. Inflammatory cells in the BAL and perivascular and peribronchiolar inflammatory cell infiltrates increased over controls with OVA exposure. These changes were counteracted by anti-IgE treatment. We conclude that mice sensitized in early infancy develop an IgE-mediated hyper-reactive airway disease with airway and vascular remodeling. Preventive approaches in early infancy of at-risk individuals may reduce childhood asthma.
Keywords
- Developing Lung
- Asthma
- Vascular Endothelial Growth Factor
- Alpha-Smooth Muscle Actin
- IgE
References
- [1] Jenkins MA, JL Hopper, G Bowes, JB Carlin, LB Flander, GG Giles. Factors in childhood as predictors of asthma in adult life. BMJ 309, 90-93 (1994)
- [2] Burrows B, MR Sears, EM Flannery, GP Herbison, MD Holdaway. Relationships of Bronchial Responsiveness Assessed by Methacholine to Serum IgE, Lung Function, Symptoms, and Diagnoses in 11-Year-Old New Zealand Children. J Allergy Clin Immunol 90, 376-385 (1992)
- [3] Tumas DB, B Chan, W Werther, T Wrin, J Vennari, N Desjardin, RL Shields, P Jardieu. Anti-IgE Efficacy in Murine Asthma Models Is Dependent on the Method of Allergen Sensitization. J Allergy Clin Immunol 107, 1025-1033 (2001)
- [4] Saglani S, K Malmstrom, AS Pelkonen, LP Malmberg, H Lindahl, M Kajosaari, M Turpeinen, AV Rogers, DN Payne, A Bush, T Haahtela, MJ Makela, PK Jeffery. Airway Remodeling and Inflammation in Symptomatic Infants With Reversible Airflow Obstruction. Am J Respir Crit Care Med 171, 722-727 (2005)
- [5] Tormanen KR, L Uller, CG Persson, JS Erjefalt. Allergen Exposure of Mouse Airways Evokes Remodeling of Both Bronchi and L arge Pulmonary Vessels. Am J Respir Crit Care Med 171, 19-25 (2005)
- [6] Saetta M, SA Di, C Rosina, G Thiene, LM Fabbri. Quantitative Structural Analysis of Peripheral Airways and Arteries in Sudden Fatal Asthma. Am Rev Respir Dis 143, 138-143 (1991)
- [7] Chetta A, E Marangio, D Olivieri. Inhaled Steroids and Airway Remodelling in Asthma. Acta Biomed Ateneo Parmense 74, 121-125 (2003)
- [8] Li X, J Wilson. Increased Vascularity of the Bronchial Mucosa in Mild Asthma. Am J Respir Crit Care Med 156, 229-233 (1997)
- [9] Siddiqui S, A Sutcliffe, A Shikotra, L Woodman, C Doe, McKenna S, A Wardlow, P Bradding, I Pavord, C Brightling. Vascular Remodeling Is a Feature of Asthma and Nonasthmatic Eosinophilic Bronchitis. J Allergy Clin Immunol 120, 813-819 (2007)
- [10] Chitano P, L Wang, S Degan, CL Worthington, V Pozzato, SH Hussaini, WC Turner, DR Dorscheid, TM Murphy. Ovalbumin Sensitization of Guinea Pig at Birth Prevents the Ontogenetic Decrease in Airway Smooth Muscle Responsiveness. Physiol Rep 2, e12241 (2014)
- [11] Aven L, J Paez-Cortez, R Achey, R Krishnan, S Ram-Mohan, WW Cruikshank, A Fine, X Ai. An NT4/TrkB-Dependent Increase in Innervation Links Early-Life Allergen Exposure to Persistent Airway Hyperreactivity. FASEB J 28, 897-907 (2014)
- [12] Guerassimov A, Y Hoshino, Y Takubo, A Turcotte, M Yamamoto, H Ghezzo, A Triantafillapoulos, K Whittaker, JR Hoidal, MG Cosio. The Development of Emphysema in Cigarette Smoke-Exposed Mice Is Strain Dependent. Am J Respir Crit Care Med 170, 974-980 (2004)
- [13] Lim DH, JY Cho, M Miller, K McElwain, S McElwain, DH Broide. Reduced Peribronchial Fibrosis in Allergen-Challenged MMP-9-Deficient Mice. Am J Physiol Lung Cell Mol Physiol 291, L265-L271 (2006)
- [14] Kanazawa H. VEGF, Angiopoietin-1 and -2 in Bronchial Asthma: New Molecular Targets in Airway Angiogenesis and Microvascular Remodeling. Recent Pat Inflamm Allergy Drug Discov 2001, 1-8 (2007)
- [15] Coyle AJ, K Wagner, C Bertrand, S Tsuyuki, J Bews, C Heusser. Central Role of Immunoglobulin (Ig) E in the Induction of Lung Eosinophil Infiltration and T Helper 2 Cell Cytokine Production: Inhibition by a Non-Anaphylactogenic Anti-IgE Antibody. J Exp Med 183, 1303-1310 (1996)
- [16] Mehlhop PD, M van de Rijn, JP Brewer, AB Kisselgof, RS Geha, HC Oettgen, TR Martin. CD40L, but Not CD40, Is Required for Allergen-Induced Bronchial Hyperresponsiveness in Mice. Am J Respir Cell Mol Biol 23, 646-651 (2000)
- [17] Nwaru BI, M Erkkola, S Ahonen, M Kaila, AM Haapala, C Kronberg-Kippila, R Salmelin, R Veijola, J Ilonen, O Simell, M Knip, SM Virtanen. Age at the Introduction of Solid Foods During the First Year and Allergic Sensitization at Age 5 Years. Pediatrics 125, 50-59 (2010)
- [18] Mitzner W, W Lee, D Georgakopoulos, E Wagner. Angiogenesis in the Mouse Lung. Am J Pathol 157, 93-101 (2000)
- [19] Tillie-Leblond I, J de Blic, F Jaubert, B Wallaert, P Scheinmann, P Gosset. Airway Remodeling Is Correlated With Obstruction in Children With Severe Asthma. Allergy 63, 533-541 (2008)
- [20] Bradding P, AF Walls, ST Holgate. The Role of the Mast Cell in the Pathophysiology of Asthma. J Allergy Clin Immunol 117, 1277-1284 (2006)
- [21] Su X, N Taniuchi, E Jin, M Fujiwara, L Zhang, M Ghazizadeh, H Tashimo, N Yamashita, K Ohta, O Kawanami. Spatial and Phenotypic Characterization of Vascular Remodeling in a Mouse Model of Asthma. Pathobiology 75, 42-56 (2008)
- [22] McDonald D. Angiogenesis and Remodeling of Airway Vasculature in Chronic Inflammation. Am J Respir Crit Care Med 164, S39-S45 (2001)
- [23] Watson CJ, NJ Webb, MJ Bottomley, PE Brenchley. Identification of polymorphisms within the vascular endothelial growth fac CJ tor (VEGF) gene: correlation with variation in VEGF protein production. Cytokine 12, 1232-1235 (2000)
- [24] Fehrenbach H, M Kasper, H Maase, D Schuh, M Muller. Differential immunolocalization of VEGF in rat and human adult lung, and in experimental rat lung fibrosis: light, fluorescence, and electron microscopy. Anat Rec 254, 61-73 (1999)
- [25] Faffe DS, L Flynt, K Bourgeois, RA Panettieri, Jr., SA Shore. Interleukin-13 and Interleukin-4 Induce Vascular Endothelial Growth Factor Release From Airway Smooth Muscle Cells: Role of Vascular Endothelial Growth Factor Genotype. Am J Respir Cell Mol Biol 34, 213-218 (2006)
- [26] Cao G, CD O’Brien, Z Zhou, SM Sanders, GN Greenbaum, A Makrigiannakis, HM DeLisser. Involvement of Human PECAM-1 in Angiogenesis and in vitro Endothelial Cell Migration. Am J Physiol Cell Physiol 282, C1181-C1190 (2002)