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Am. J. Respir. Crit. Care Med., Volume 163, Number 3, March 2001, 737-744

Endothelial Cell Death and Decreased Expression of Vascular Endothelial Growth Factor and Vascular Endothelial Growth Factor Receptor 2 in Emphysema

YASUNORI KASAHARA, RUBIN M. TUDER, CARLYNE D. COOL, DAVID A. LYNCH, SONIA C. FLORES, and NORBERT F. VOELKEL

Division of Pulmonary Sciences and Critical Care Medicine, Pulmonary Hypertension Center, Department of Pathology, Department of Radiology, and Webb-Waring Antioxidant Research Institute, University of Colorado Health Sciences Center, Denver, Colorado

Emphysema due to cigarette smoking is characterized by a loss of alveolar structures. We hypothesize that the disappearance of alveoli involves apoptosis of septal endothelial cells and a decreased expression of lung vascular endothelial growth factor (VEGF) and its receptor 2 (VEGF R2). By terminal transferase dUTP nick end labeling (TUNEL) in combination with immunohistochemistry, we found that the number of TUNEL+ septal epithelial and endothelial cells/lung tissue nucleic acid (µg) was increased in the alveolar septa of emphysema lungs (14.2 ± 2.0/µg, n = 6) when compared with normal lungs (6.8 ± 1.3/µg, n = 7) (p < 0.01) and with primary pulmonary hypertensive lungs (2.3 ± 0.8/µg, n = 5) (p < 0.001). The cell death events were not significantly different between healthy nonsmoker (7.4 ± 1.9/µg) and smoker (5.7 ± 0.7/µg) control subjects. The TUNEL results were confirmed by single-stranded DNA and active caspase-3 immunohistochemistry, and by DNA ligation assay. Emphysema lungs (n = 12) had increased levels of oligonucleosomal-length DNA fragmentation when compared with normal lungs (n = 11). VEGF, VEGF R2 protein, and mRNA expression were significantly reduced in emphysema. We propose that epithelial and endothelial alveolar septal death due to a decrease of endothelial cell maintenance factors may be part of the pathogenesis of emphysema.




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One Hundred Years of Research in the Pathogenesis of Pulmonary Hypertension
Am. J. Respir. Cell Mol. Biol., November 1, 2005; 33(5): 425 - 431.
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W. MacNee
Pathogenesis of Chronic Obstructive Pulmonary Disease
Proceedings of the ATS, November 1, 2005; 2(4): 258 - 266.
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C. A. Owen
Proteinases and Oxidants as Targets in the Treatment of Chronic Obstructive Pulmonary Disease
Proceedings of the ATS, November 1, 2005; 2(4): 373 - 385.
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 ChestHome page
H. Kanazawa and J. Yoshikawa
Elevated Oxidative Stress and Reciprocal Reduction of Vascular Endothelial Growth Factor Levels With Severity of COPD
Chest, November 1, 2005; 128(5): 3191 - 3197.
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 ChestHome page
T. L. Petty
Are COPD and Lung Cancer Two Manifestations of the Same Disease?
Chest, October 1, 2005; 128(4): 1895 - 1897.
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 ERRHome page
W. MacNee
Treatment of stable COPD: antioxidants
Eur. Respir. Rev., September 1, 2005; 14(94): 12 - 22.
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 Am. J. Respir. Crit. Care Med.Home page
S. Murakami, N. Nagaya, T. Itoh, T. Iwase, T. Fujisato, K. Nishioka, K. Hamada, K. Kangawa, and H. Kimura
Adrenomedullin Regenerates Alveoli and Vasculature in Elastase-induced Pulmonary Emphysema in Mice
Am. J. Respir. Crit. Care Med., September 1, 2005; 172(5): 581 - 589.
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 J. Immunol.Home page
T. Zheng, M. J. Kang, K. Crothers, Z. Zhu, W. Liu, C. G. Lee, L. A. Rabach, H. A. Chapman, R. J. Homer, D. Aldous, et al.
Role of Cathepsin S-Dependent Epithelial Cell Apoptosis in IFN-{gamma}-Induced Alveolar Remodeling and Pulmonary Emphysema
J. Immunol., June 15, 2005; 174(12): 8106 - 8115.
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 Am. J. Respir. Crit. Care Med.Home page
D. Saey, A. Michaud, A. Couillard, C. H. Cote, M. J. Mador, P. LeBlanc, J. Jobin, and F. Maltais
Contractile Fatigue, Muscle Morphometry, and Blood Lactate in Chronic Obstructive Pulmonary Disease
Am. J. Respir. Crit. Care Med., May 15, 2005; 171(10): 1109 - 1115.
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 Eur Respir JHome page
K. Nagai, T. Betsuyaku, Y. Ito, Y. Nasuhara, and M. Nishimura
Decrease of vascular endothelial growth factor in macrophages from long-term smokers
Eur. Respir. J., April 1, 2005; 25(4): 626 - 633.
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N. Voelkel and L. Taraseviciene-Stewart
Emphysema: An Autoimmune Vascular Disease?
Proceedings of the ATS, April 1, 2005; 2(1): 23 - 25.
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W. MacNee
Pulmonary and Systemic Oxidant/Antioxidant Imbalance in Chronic Obstructive Pulmonary Disease
Proceedings of the ATS, April 1, 2005; 2(1): 50 - 60.
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R. Buhl and S. G. Farmer
Future Directions in the Pharmacologic Therapy of Chronic Obstructive Pulmonary Disease
Proceedings of the ATS, April 1, 2005; 2(1): 83 - 93.
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S. I. Rennard
Clinical Approach to Patients with Chronic Obstructive Pulmonary Disease and Cardiovascular Disease
Proceedings of the ATS, April 1, 2005; 2(1): 94 - 100.
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 Am. J. Respir. Crit. Care Med.Home page
L. Taraseviciene-Stewart, R. Scerbavicius, K.-H. Choe, M. Moore, A. Sullivan, M. R. Nicolls, A. P. Fontenot, R. M. Tuder, and N. F. Voelkel
An Animal Model of Autoimmune Emphysema
Am. J. Respir. Crit. Care Med., April 1, 2005; 171(7): 734 - 742.
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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
L. Plantier, S. Marchand-Adam, J. Marchal-Somme, G. Leseche, M. Fournier, M. Dehoux, M. Aubier, and B. Crestani
Defect of hepatocyte growth factor production by fibroblasts in human pulmonary emphysema
Am J Physiol Lung Cell Mol Physiol, April 1, 2005; 288(4): L641 - L647.
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 CirculationHome page
N. Shigemura, Y. Sawa, S. Mizuno, M. Ono, M. Ohta, T. Nakamura, Y. Kaneda, and H. Matsuda
Amelioration of Pulmonary Emphysema by In Vivo Gene Transfection With Hepatocyte Growth Factor in Rats
Circulation, March 22, 2005; 111(11): 1407 - 1414.
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 Eur Respir JHome page
S. Hodge, G. Hodge, M. Holmes, and P. N. Reynolds
Increased airway epithelial and T-cell apoptosis in COPD remains despite smoking cessation
Eur. Respir. J., March 1, 2005; 25(3): 447 - 454.
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 ThoraxHome page
A R Kranenburg, W I de Boer, V K T Alagappan, P J Sterk, and H S Sharma
Enhanced bronchial expression of vascular endothelial growth factor and receptors (Flk-1 and Flt-1) in patients with chronic obstructive pulmonary disease
Thorax, February 1, 2005; 60(2): 106 - 113.
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 Eur Respir JHome page
B. Bartalesi, E. Cavarra, S. Fineschi, M. Lucattelli, B. Lunghi, P. A. Martorana, and G. Lungarella
Different lung responses to cigarette smoke in two strains of mice sensitive to oxidants
Eur. Respir. J., January 1, 2005; 25(1): 15 - 22.
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 Am. J. Respir. Cell Mol. Bio.Home page
H. A. Golpon, C. D. Coldren, M. R. Zamora, G. P. Cosgrove, M. D. Moore, R. M. Tuder, M. W. Geraci, and N. F. Voelkel
Emphysema Lung Tissue Gene Expression Profiling
Am. J. Respir. Cell Mol. Biol., December 1, 2004; 31(6): 595 - 600.
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 Am. J. Respir. Cell Mol. Bio.Home page
T. Tsuji, K. Aoshiba, and A. Nagai
Cigarette Smoke Induces Senescence in Alveolar Epithelial Cells
Am. J. Respir. Cell Mol. Biol., December 1, 2004; 31(6): 643 - 649.
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 Am. J. Respir. Cell Mol. Bio.Home page
H. Kim, X. Liu, T. Kobayashi, H. Conner, T. Kohyama, F.-Q. Wen, Q. Fang, S. Abe, P. Bitterman, and S. I. Rennard
Reversible Cigarette Smoke Extract-Induced DNA Damage in Human Lung Fibroblasts
Am. J. Respir. Cell Mol. Biol., November 1, 2004; 31(5): 483 - 490.
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 Eur Respir JHome page
O. Holz, I. Zuhlke, E. Jaksztat, K.C. Muller, L. Welker, M. Nakashima, K.D. Diemel, D. Branscheid, H. Magnussen, and R.A. Jorres
Lung fibroblasts from patients with emphysema show a reduced proliferation rate in culture
Eur. Respir. J., October 1, 2004; 24(4): 575 - 579.
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 J. Appl. Physiol.Home page
X. Li, R. Shu, G. Filippatos, and B. D. Uhal
Apoptosis in lung injury and remodeling
J Appl Physiol, October 1, 2004; 97(4): 1535 - 1542.
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 J. Appl. Physiol.Home page
K. Tang, H. B. Rossiter, P. D. Wagner, and E. C. Breen
Lung-targeted VEGF inactivation leads to an emphysema phenotype in mice
J Appl Physiol, October 1, 2004; 97(4): 1559 - 1566.
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 ThoraxHome page
A Boutten, M Bonay, S Laribe, G Leseche, Y Castier, V Lecon-Malas, M Fournier, G Durand, M Aubier, M Dehoux, et al.
Decreased expression of interleukin 13 in human lung emphysema
Thorax, October 1, 2004; 59(10): 850 - 854.
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 Am. J. Respir. Crit. Care Med.Home page
A. Churg, R. D. Wang, H. Tai, X. Wang, C. Xie, and J. L. Wright
Tumor Necrosis Factor-{alpha} Drives 70% of Cigarette Smoke-induced Emphysema in the Mouse
Am. J. Respir. Crit. Care Med., September 1, 2004; 170(5): 492 - 498.
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 Am. J. Respir. Cell Mol. Bio.Home page
I. R. Witherden, E. J. Vanden Bon, P. Goldstraw, C. Ratcliffe, U. Pastorino, and T. D. Tetley
Primary Human Alveolar Type II Epithelial Cell Chemokine Release: Effects of Cigarette Smoke and Neutrophil Elastase
Am. J. Respir. Cell Mol. Biol., April 1, 2004; 30(4): 500 - 509.
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 Am. J. Respir. Crit. Care Med.Home page
P.-N. Tsao, Y.-N. Su, H. Li, P.-H. Huang, C.-T. Chien, Y.-L. Lai, C.-N. Lee, C.-A. Chen, W.-F. Cheng, S.-C. Wei, et al.
Overexpression of Placenta Growth Factor Contributes to the Pathogenesis of Pulmonary Emphysema
Am. J. Respir. Crit. Care Med., February 15, 2004; 169(4): 505 - 511.
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N. Yokohori, K. Aoshiba, and A. Nagai
Increased Levels of Cell Death and Proliferation in Alveolar Wall Cells in Patients With Pulmonary Emphysema
Chest, February 1, 2004; 125(2): 626 - 632.
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 Am. J. Respir. Cell Mol. Bio.Home page
N. C. Smits, A. A. Robbesom, E. M. M. Versteeg, E. M. A. van de Westerlo, P. N. R. Dekhuijzen, and T. H. van Kuppevelt
Heterogeneity of Heparan Sulfates in Human Lung
Am. J. Respir. Cell Mol. Biol., February 1, 2004; 30(2): 166 - 173.
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 Am. J. Respir. Cell Mol. Bio.Home page
S. K. Banerjee, H. W. J. Young, A. Barczak, D. J. Erle, and M. R. Blackburn
Abnormal Alveolar Development Associated with Elevated Adenine Nucleosides
Am. J. Respir. Cell Mol. Biol., January 1, 2004; 30(1): 38 - 50.
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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
C. Liu, M. Ikegami, M. T. Stahlman, C. R. Dey, and J. A. Whitsett
Inhibition of alveolarization and altered pulmonary mechanics in mice expressing GATA-6
Am J Physiol Lung Cell Mol Physiol, December 1, 2003; 285(6): L1246 - L1254.
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 Eur Respir JHome page
N.F. Voelkel and C.D. Cool
Pulmonary vascular involvement in chronic obstructive pulmonary disease
Eur. Respir. J., November 2, 2003; 22(46_suppl): 28s - 32s.
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 JNMHome page
T. Arao, N. Takabatake, M. Sata, S. Abe, Y. Shibata, T. Honma, K. Takahashi, A. Okada, Y. Takeishi, and I. Kubota
In Vivo Evidence of Endothelial Injury in Chronic Obstructive Pulmonary Disease by Lung Scintigraphic Assessment of 123I-Metaiodobenzylguanidine
J. Nucl. Med., November 1, 2003; 44(11): 1747 - 1754.
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 Am. J. Respir. Cell Mol. Bio.Home page
J. A. Wickenden, M. C. H. Clarke, A. G. Rossi, I. Rahman, S. P. Faux, K. Donaldson, and W. MacNee
Cigarette Smoke Prevents Apoptosis through Inhibition of Caspase Activation and Induces Necrosis
Am. J. Respir. Cell Mol. Biol., November 1, 2003; 29(5): 562 - 570.
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