Nonhematopoietic NADPH oxidase regulation of lung eosinophilia and airway hyperresponsiveness in experimentally induced asthma

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 292, Issue 5, 2007, Pages

  Abdala Valencia, Hiam ^a,b   Earwood, Julie ^b   Bansal, Shelly ^b   Jansen, Michael ^c   Babcock, George ^b   Garvy, Beth ^d   Wills Karp, Marsha ^c   Cook Mills, Joan M ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^d UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

Endothelium; Eosinophils; Gp91 phox; VCAM 1

Indexed keywords

CHEMOKINE; EOTAXIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 5; OVALBUMIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; CELL ACTIVATION; CELL INFILTRATION; CONTROLLED STUDY; DISEASE MARKER; DISEASE MODEL; ENDOTHELIUM; ENDOTHELIUM CELL; ENZYME REGULATION; EOSINOPHIL; EXPERIMENTAL STUDY; GENE EXPRESSION; HEMATOPOIETIC CELL; HYPERSENSITIVITY REACTION; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE MIGRATION; LOEFFLER PNEUMONIA; LUNG LAVAGE; MONONUCLEAR CELL; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; WILD TYPE;

ANIMALS; ASTHMA; BRONCHIAL HYPERREACTIVITY; CHEMOKINES, CC; CYTOKINES; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; NADPH OXIDASE; OVALBUMIN; PULMONARY EOSINOPHILIA; VASCULAR CELL ADHESION MOLECULE-1;

EID: 34447554398     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00208.2006     Document Type: Article

References (75)

1. +. Circ Res 83: 730-737, 1998.
2. Bandeira-Melo C, Calheiros AS, Silva PM, Cordeiro RS, Teixeira MM, Martins MA. Suppressive effect of distinct bradykinin B2 receptor antagonist on allergen-evoked exudation and leukocyte infiltration in sensitized rats. Br J Pharmacol 127: 315-320, 1999.
3. Bankers-Fulbright JL, Kita H, Gleich GJ, O'Grady SM. Regulation of human eosinophil NADPH oxidase activity: a central role for PKC delta. J Cell Physiol 189: 306-315, 2001.
4. Baron JL, Madri JA, Ruddle NH, Hashim G, Janeway CA Jr. Surface expression of alpha 4 integrin by CD4 T cells is required for their entry into brain parenchyma. J Exp Med 177: 57-68, 1993.
5. Bjorgvinsdottir H, Ding C, Pech N, Gifford MA, Li LL, Dinauer MC. Retroviral-mediated gene transfer of gp91phox into bone marrow cells rescues defect in host defense against Aspergillus fumigatus in murine X-linked chronic granulomatous disease. Blood 89: 41-48, 1997.
6. Borchers MT, Ansay T, DeSalle R, Daugherty BL, Shen H, Metzger M, Lee NA, Lee JJ. In vitro assessment of chemokine receptor-ligand interactions mediating mouse eosinophil migration. J Leukoc Biol 71: 1033-1041, 2002.
7. Borchers MT, Crosby J, Farmer S, Sypek J, Ansay T, Lee NA, Lee JJ. Blockade of CD49d inhibits allergic airway pathologies independent of effects on leukocyte recruitment. Am J Physiol Lung Cell Mol Physiol 280: L813-L821, 2001.
8. Borchers MT, Crosby J, Justice P, Farmer S, Hines E, Lee JJ, Lee NA. Intrinsic AHR in IL-5 transgenic mice is dependent on CD4(+) cells and CD49d-mediated signaling. Am J Physiol Lung Cell Mol Physiol 281: L653-L659, 2001.
9. Bryce PJ, Mathias CB, Harrison KL, Watanabe T, Geha RS, Oettgen HC. The H1 histamine receptor regulates allergic lung responses. J Clin Invest 116: 1624-1632, 2006.
10. Bryce PJ, Oyoshi MK, Kawamoto S, Oettgen HC, Tsitsikov EN. TRAF1 regulates Th2 differentiation, allergic inflammation and nuclear localization of the Th2 transcription factor, NIP45. Int Immunol 18: 101-111, 2006.
11. Chiba Y, Arimoto T, Yoshikawa T, Misawa M. Elevated nitric oxide synthase activity concurrent with antigen-induced airway hyperresponsiveness in rats. Exp Lung Res 26: 535-549, 2000.
12. Chin JE, Hatfield CA, Winterrowd GE, Brashler JR, Vonderfecht SL, Fidler SF, Griffin RL, Kolbasa KP, Krzesicki RF, Sly LM, Staite ND, Richards IM. Airway recruitment of leukocytes in mice is dependent on α4-integrins and vascular cell adhesion molecule-1. Am J Physiol Lung Cell Mol Physiol 272: L219-L229, 1997.
13. Comhair SA, Bhathena PR, Farver C, Thunnissen FB, Erzurum SC. Extracellular glutathione peroxidase induction in asthmatic lungs: evidence for redox regulation of expression in human airway epithelial cells. FASEB J 15: 70-78, 2001.
14. Comhair SAA, Erzurum SC. Antioxidant responses to oxidant-mediated lung diseases. Am J Physiol Lung Cell Mol Physiol 283: L246-L255, 2002.
15. Cook-Mills JM, Deem TL. Active endothelial cell function during inflammation. J Leukoc Biol 77: 487-495, 2005.
16. Cook-Mills JM, Gallagher JS, Feldbush TL. Isolation and characterization of high endothelial cell lines derived from mouse lymph nodes. In Vitro Cell Dev Biol 32: 167-177, 1996.
17. Cook-Mills JM, Johnson JD, Deem TL, Ochi A, Wang L, Zheng Y. Calcium mobilization and Rac1 activation are required for VCAM-1 (vascular cell adhesion molecule-1) stimulation of NADPH oxidase activity. Biochem J 378: 539-547, 2004.
18. Deem TL, Cook-Mills JM. Vascular cell adhesion molecule-1 (VCAM-1) activation of endothelial cell matrix metalloproteinases: role of reactive oxygen species. Blood 104: 2385-2393, 2004.
19. Eisenbarth SC, Piggott DA, Huleatt JW, Visintin I, Herrick CA, Bottomly K. Lipopolysaccharide-enhanced, toll-like receptor 4-dependent T helper cell type 2 responses to inhaled antigen. J Exp Med 196: 1645-1651, 2002.
20. Ewart SL, Kuperman D, Schadt E, Tankersley C, Grupe A, Shubitowski DM, Peltz G, Wills-Karp M. Quantitative trait loci controlling allergen-induced airway hyperresponsiveness in inbred mice. Am J Respir Cell Mol Biol 23: 537-545, 2000.
21. Foster PS, Mould AW, Yang M, Mackenzie J, Mattes J, Hogan SP, Mahalingam S, McKenzie AN, Rothenberg ME, Young IG, Matthaei KI, Webb DC. Elemental signals regulating eosinophil accumulation in the lung. Immunol Rev 179: 173-181, 2001.
22. Gerhold K, Blumchen K, Bock A, Seib C, Stock P, Kallinich T, Lohning M, Wahn U, Hamelmann E. Endotoxins prevent murine IgE production, T(H)2 immune responses, and development of airway eosinophilia but not airway hyperreactivity. J Allergy Clin Immunol 110: 110-116, 2002.
23. Gopinath R, Nutman TB. Identification of eosinophils in lysed whole blood using side scatter and CD16 negativity. Cytometry 30: 313-316, 1997.
24. Gurtner GC, Davis V, Li H, McCoy MJ, Sharpe A, Cybulsky MI. Targeted disruption of the murine VCAM1 gene: essential role of VCAM-1 in chorioallantoic fusion and placentation. Genes Dev 9: 1-14, 1995.
25. Hakugawa J, Bae SJ, Tanaka Y, Katayama I. The inhibitory effect of anti-adhesion molecule antibodies on eosinophil infiltration in cutaneous late phase response in Balb/c mice sensitized with ovalbumin (OVA). J Dermatol 24: 73-79, 1997.
26. Hisada T, Hellewell PG, Teixeira MM, Malm MG, Salmon M, Huang TJ, Chung KF. α4-Integrin-dependent eotaxin induction of bronchial hyperresponsiveness and eosinophil migration in interleukin-5 transgenic mice. Am J Respir Cell Mol Biol 20: 992-1000, 1999.
27. Humbles AA, Lu B, Friend DS, Okinaga S, Lora J, Al-Garawi A, Martin TR, Gerard NP, Gerard C. The murine CCR3 receptor regulates both the role of eosinophils and mast cells in allergen-induced airway inflammation and hyperresponsiveness. Proc Natl Acad Sci USA 99: 1479-1484, 2002.
28. Iiyama K, Hajra L, Iiyama M, Li H, DiChiara M, Medoff BD, Cybulsky MI. Patterns of vascular cell adhesion molecule-1 and intercellular adhesion molecule-1 expression in rabbit and mouse atherosclerotic lesions and at sites predisposed to lesion formation. Circ Res 85: 199-207, 1999.
29. Keane-Myers A, Wysocka M, Trinchieri G, Wills-Karp M. Resistance to antigen-induced airway hyperresponsiveness requires endogenous production of IL-12. J Immunol 161: 919-926, 1998.
30. Keshavan P, Deem TL, Schwemberger SJ, Babcock GF, Cook-Mills JM, Zucker SD. Unconjugated bilirubin inhibits VCAM-1-mediated transendothelial leukocyte migration. J Immunol 174: 3709-3718, 2005.
31. Kudlacz E, Whitney C, Andresen C, Duplantier A, Beckius G, Chupak L, Klein A, Kraus K, Milici A. Pulmonary eosinophilia in a murine model of allergic inflammation is attenuated by small molecule α4β1 antagonists. J Pharmacol Exp Ther 301: 747-752, 2002.
32. Lassegue B, Sorescu D, Szocs K, Yin Q, Akers M, Zhang Y, Grant SL, Lambeth JD, Griendling KK. Novel gp91(phox) homologues in vascular smooth muscle cells: nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways. Circ Res 88: 888-894, 2001.
33. Lewis CA, Johnson A, Broadley KJ. Early and late phase bronchoconstrictions in conscious sensitized guinea-pigs after macro- and microshock inhalation of allergen and associated airway accumulation of leukocytes. Int J Immunopharmacol 18: 415-422, 1996.
34. Lindsay MA, Haddad EB, Rousell J, Teixeira MM, Hellewell PG, Barnes PJ, Giembycz MA. Role of the mitogen-activated protein kinases and tyrosine kinases during leukotriene B4-induced eosinophil activation. J Leukoc Biol 64: 555-562, 1998.
35. Ma W, Bryce PJ, Humbles AA, Laouini D, Yalcindag A, Alenius H, Friend DS, Oettgen HC, Gerard C, Geha RS. CCR3 is essential for skin eosinophilia and airway hyperresponsiveness in a murine model of allergic skin inflammation. J Clin Invest 109: 621-628, 2002.
36. Macias MP, Fitzpatrick LA, Brenneise I, McGarry MP, Lee JJ. Expression of IL-5 alters bone metabolism and induces ossification of the spleen in transgenic mice. J Clin Invest 107: 949-959, 2001.
37. Matheny HE, Deem TL, Cook-Mills JM. Lymphocyte migration through monolayers of endothelial cell lines involves VCAM-1 signaling via endothelial cell NADPH oxidase. J Immunol 164: 6550-6559, 2000.
38. Matsumoto K, Appiah-Pippim J, Schleimer RP, Bickel CA, Beck LA, Bochner BS. CD44 and CD69 represent different types of cell-surface activation markers for human eosinophils. Am J Respir Cell Mol Biol 18: 860-866, 1998.
39. Meyer JW, Holland JA, Ziegler LM, Chang MM, Beebe G, Schmitt ME. Identification of a functional leukocyte-type NADPH oxidase in human endothelial cells: a potential atherogenic source of reactive oxygen species. Endothelium 7: 11-22, 1999.
40. Mishell BB, Shiigi SM, Henry C, Chan EL, North J, Galliliy R, Slomich M, Miller K, Marbrook J, Parks D, Good AH. Determination of viability by trypan blue exclusion. In: Selected Methods in Cellular Immunology, edited by Mishell BB and Shiigi SM. San Francisco: Freeman, 1980, chapt 1.11, p. 16-17.
41. Mould AW, Ramsay AJ, Matthaei KI, Young IG, Rothenberg ME, Foster PS. The effect of IL-5 and eotaxin expression in the lung on eosinophil trafficking and degranulation and the induction of bronchial hyperreactivity. J Immunol 164: 2142-2150, 2000.
42. Mueller JP, Evans MJ, Cofiell R, Rother RP, Matis LA, Elliott EA. Porcine vascular cell adhesion molecule (VCAM) mediates endothelial cell adhesion to human T cells. Development of blocking antibodies specific for porcine VCAM. Transplantation 60: 1299-1306, 1995.
43. Muijsers RB, van Ark I, Folkerts G, Koster AS, van Oosterhout AJ, Postma DS, Nijkamp FP. Apocynin and 1400 W prevents airway hyperresponsiveness during allergic reactions in mice. Br J Pharmacol 134: 434-440, 2001.
44. Nagata M, Sedgwick JB, Kita H, Busse WW. Granulocyte macrophage colony-stimulating factor augments ICAM-1 and VCAM-1 activation of eosinophil function. Am J Respir Cell Mol Biol 19: 158-166, 1998.
45. Nagata M, Sedgwick JB, Vrtis R, Busse WW. Endothelial cells upregulate eosinophil superoxide generation via VCAM-1 expression. Clin Exp Allergy 29: 550-561, 1999.
46. Pagano PJ, Clark JK, Cifuentes-Pagano ME, Clark SM, Callis GM, Quinn MT. Localization of a constitutively active, phagocyte-like NADPH oxidase in rabbit aortic adventitia: enhancement by angiotensin II. Proc Natl Acad Sci USA 94: 14483-14488, 1997.
47. Pollock JD, Williams DA, Gifford MA, Li LL, Du X, Fisherman J, Orkin SH, Doerschuk CM, Dinauer MC. Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat Genet 9: 202-209, 1995.
48. Ravetch JV, Kinet JP. Fc receptors. Annu Rev Immunol 9: 457-492, 1991.
49. Sagara H, Matsuda H, Wada N, Yagita H, Fukuda T, Okumura K, Makino S, Ra C. A monoclonal antibody against very late activation antigen-4 inhibits eosinophil accumulation and late asthmatic response in a guinea pig model of asthma. Int Arch Allergy Immunol 112: 287-294, 1997.
50. Schneider T, van Velzen D, Moqbel R, Issekutz AC. Kinetics and quantitation of eosinophil and neutrophil recruitment to allergic lung inflammation in a brown Norway rat model. Am J Respir Cell Mol Biol 17: 702-712, 1997.
51. Sedgwick JB, Jansen KJ, Kennedy JD, Kita H, Busse WW. Effects of the very late adhesion molecule 4 antagonist WAY103 on human peripheral blood eosinophil vascular cell adhesion molecule 1-dependent functions. J Allergy Clin Immunol 116: 812-819, 2005.
52. Shen HH, Ochkur SI, McGarry MP, Crosby JR, Hines EM, Borchers MT, Wang H, Biechelle TL, O'Neill KR, Ansay TL, Colbert DC, Cormier SA, Justice JP, Lee NA, Lee JJ. A causative relationship exists between eosinophils and the development of allergic pulmonary pathologies in the mouse. J Immunol 170: 3296-3305, 2003.
53. Shi HZ, Humbles A, Gerard C, Jin Z, Weller PF. Lymph node trafficking and antigen presentation by endobronchial eosinophils. J Clin Invest 105: 945-953, 2000.
54. Singh J, Van Vlijmen H, Liao Y, Lee WC, Cornebise M, Harris M, Shu IH, Gill A, Cuervo JH, Abraham WM, Adams SP. Identification of potent and novel α4β1 antagonists using in silico screening. J Med Chem 45: 2988-2993, 2002.
55. Springer TA. Traffic signals on endothelium for lymphocyte recirculation and leukocyte emigration. Annu Rev Physiol 57: 827-872, 1995.
56. Suto A, Nakajima H, Kagami SI, Suzuki K, Saito Y, Iwamoto I. Role of CD4(+) CD25(+) regulatory T cells in T helper 2 cell-mediated allergic inflammation in the airways. Am J Respir Crit Care Med 164: 680-687, 2001.
57. Szocs K, Lassegue B, Sorescu D, Hilenski LL, Valppu L, Couse TL, Wilcox JN, Quinn MT, Lambeth JD, Griendling KK. Upregulation of Nox-based NAD(P)H oxidases in restenosis after carotid injury. Arterioscler Thromb Vasc Biol 22: 21-27, 2002.
58. Taube C, Dakhama A, Rha YH, Takeda K, Joetham A, Park JW, Balhorn A, Takai T, Poch KR, Nick JA, Gelfand EW. Transient neutrophil infiltration after allergen challenge is dependent on specific antibodies and Fc gamma III receptors. J Immunol 170: 4301-4309, 2003.
59. Thabut G, El-Benna J, Samb A, Corda S, Megret J, Leseche G, Vicaut E, Aubier M, Boczkowski J. Tumor necrosis factor-alpha increases airway smooth muscle oxidants production through a NADPH oxidase-like system to enhance myosin light chain phosphorylation and contractility. J Biol Chem 277: 22814-22821, 2002.
60. Tomkinson A, Cieslewicz G, Duez C, Larson KA, Lee JJ, Gelfand EW. Temporal association between airway hyperresponsiveness and airway eosinophilia in ovalbumin-sensitized mice. Am J Respir Crit Care Med 163: 721-730, 2001.
61. Tsukagoshi H, Haddad EB, Sun J, Barnes PJ, Chung KF. Ozone-induced airway hyperresponsiveness: role of superoxide anions, NEP, and BK receptors. J Appl Physiol 78: 1015-1022, 1995.
62. Tudor KSRS, Deem TL, Cook-Mills JM. Novel α4-integrin ligands on an endothelial cell line. Biochem Cell Biol 78: 99-113, 2000.
63. Tudor KSRS, Hess KL, Cook-Mills JM. Cytokines modulate endothelial cell intracellular signal transduction required for VCAM-1-dependent lymphocyte transendothelial migration. Cytokine 15: 196-211, 2001.
64. Underwood S, Foster M, Raeburn D, Bottoms S, Karlsson JA. Time-course of antigen-induced airway inflammation in the guinea-pig and its relationship to airway hyperresponsiveness. Eur Respir J 8: 2104-2113, 1995.
65. van Buul JD, Voermans C, van den Berg V, Anthony EC, Mul FPJ, van Wetering S, van der Schoot EC, Hordijk PL. Migration of human hematopoietic progenitor cells across bone marrow endothelium is regulated by vascular endothelial cadherin. J Immunol 168: 588-596, 2002.
66. van Klaveren RJ, Roelant C, Boogaerts M, Demedts M, Nemery B. Involvement of an NAD(P)H oxidase-like enzyme in superoxide anion and hydrogen peroxide generation by rat type II cells. Thorax 52: 465-471, 1997.
67. van Wetering S, van Buul JD, Quik S, Mul FPJ, Anthony EC, ten Klooster JP, Collard JG, Hordijk PL. Reactive oxygen species mediate Rac-induced loss of cell-cell adhesion in primary human endothelial cells. J Cell Sci 115: 1837-1846, 2002.
68. Venkayya R, Lam M, Willkom M, Grunig G, Corry DB, Erle DJ. The Th2 lymphocyte products IL-4 and IL-13 rapidly induce airway hyperresponsiveness through direct effects on resident airway cells. Am J Respir Cell Mol Biol 26: 202-208, 2002.
69. Walsh GM, Wardlaw AJ, Hartnell A, Sanderson CJ, Kay AB. Interleukin-5 enhances the in vitro adhesion of human eosinophils, but not neutrophils, in a leukocyte integrin (CD11/18)-dependent manner. Int Arch Allergy Appl Immunol 94: 174-178, 1991.
70. + channel may function as an oxygen sensor complex in airway chemoreceptors and small cell lung carcinoma cell lines. Proc Natl Acad Sci USA 93: 13182-13187, 1996.
71. Wang S, Fan Y, Han X, Yang J, Bilenki L, Yang X. IL-12-dependent vascular cell adhesion molecule-1 expression contributes to airway eosinophilic inflammation in a mouse model of asthma-like reaction. J Immunol 166: 2741-2749, 2001.
72. Wardlaw AJ, Brightling C, Green R, Woltmann G, Pavord I. Eosinophils in asthma and other allergic diseases. Br Med Bull 56: 985-1003, 2000.
73. Yang L, Cohn L, Zhang DH, Homer R, Ray A, Ray P. Essential role of nuclear factor kappaB in the induction of eosinophilia in allergic airway inflammation. J Exp Med 188: 1739-1750, 1998.
74. Youngson C, Nurse C, Yeger H, Cutz E. Oxygen sensing in airway chemoreceptors. Nature 365: 153-155, 1993.
75. Zuany-Amorim C, Haile S, Leduc D, Dumarey C, Huerre M, Vargaftig BB, Pretolani M. Interleukin-10 inhibits antigen-induced cellular recruitment into the airways of sensitized mice. J Clin Invest 95: 2644-2651, 1995.