Allergen-induced, eotaxin-rich, proangiogenic bone marrow progenitors: A blood-borne cellular envoy for lung eosinophilia

Journal of Allergy and Clinical Immunology

Volumn 125, Issue 4, 2010, Pages 918-925

  Asosingh, Kewal ^a   Hanson, Jodi D ^a   Cheng, Georgiana ^a   Aronica, Mark A ^a   Erzurum, Serpil C ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

airway inflammation; allergy; angiogenesis; bone marrow; Eosinophils; eotaxin

Indexed keywords

ALLERGEN; CHEMOATTRACTANT; EOTAXIN; MESSENGER RNA; OVALBUMIN; PROTEIN;

ADULT; AGED; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; CELL CULTURE; CELL ISOLATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENVIRONMENTAL EXPOSURE; ENZYME LINKED IMMUNOSORBENT ASSAY; EOSINOPHIL; EXPOSURE; FEMALE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; HYPOTHESIS; IMMUNOFLUORESCENCE; IN VIVO STUDY; INFLAMMATION; LOEFFLER PNEUMONIA; LUNG ENDOTHELIUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SMOOTH MUSCLE FIBER;

ADULT; AIRWAY REMODELING; ALLERGENS; ANIMALS; ASTHMA; BONE MARROW CELLS; CHEMOKINE CCL11; ENDOTHELIUM; EOSINOPHILS; FEMALE; HUMANS; MALE; MICE; MICE, INBRED BALB C; NEOVASCULARIZATION, PHYSIOLOGIC; OVALBUMIN; PULMONARY EOSINOPHILIA; STEM CELLS;

EID: 77950298928     PISSN: 00916749     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jaci.2010.01.017     Document Type: Article

References (60)

1. Kuwano K., Bosken C.H., Pare P.D., Bai T.R., Wiggs B.R., and Hogg J.C. Small airways dimensions in asthma and in chronic obstructive pulmonary disease. Am Rev Respir Dis 148 (1993) 1220-1225
2. Dunnill M.S. The pathology of asthma, with special reference to changes in the bronchial mucosa. J Clin Pathol 13 (1960) 27-33
3. Li X., and Wilson J.W. Increased vascularity of the bronchial mucosa in mild asthma. Am J Respir Crit Care Med 156 (1997) 229-233
4. Salvato G. Quantitative and morphological analysis of the vascular bed in bronchial biopsy specimens from asthmatic and non-asthmatic subjects. Thorax 56 (2001) 902-906
5. Vrugt B., Wilson S., Bron A., Holgate S.T., Djukanovic R., and Aalbers R. Bronchial angiogenesis in severe glucocorticoid-dependent asthma. Eur Respir J 15 (2000) 1014-1021
6. Lee C.G., Link H., Baluk P., Homer R.J., Chapoval S., Bhandari V., et al. Vascular endothelial growth factor (VEGF) induces remodeling and enhances TH2-mediated sensitization and inflammation in the lung. Nat Med 10 (2004) 1095-1103
7. Asosingh K., Swaidani S., Aronica M., and Erzurum S.C. Th1- and Th2-dependent endothelial progenitor cell recruitment and angiogenic switch in asthma. J Immunol 178 (2007) 6482-6494
8. Qin G., Ii M., Silver M., Wecker A., Bord E., Ma H., et al. Functional disruption of alpha4 integrin mobilizes bone marrow-derived endothelial progenitors and augments ischemic neovascularization. J Exp Med 203 (2006) 153-163
9. Kerbel R.S., Benezra R., Lyden D.C., Hattori K., Heissig B., Nolan D.J., et al. Endothelial progenitor cells are cellular hubs essential for neoangiogenesis of certain aggressive adenocarcinomas and metastatic transition but not adenomas. Proc Natl Acad Sci U S A 105 (2008) e54-e55
10. Zacchigna S., Pattarini L., Zentilin L., Moimas S., Carrer A., Sinigaglia M., et al. Bone marrow cells recruited through the neuropilin-1 receptor promote arterial formation at the sites of adult neoangiogenesis in mice. J Clin Invest 118 (2008) 2062-2075
11. Ritter M.R., Banin E., Moreno S.K., Aguilar E., Dorrell M.I., and Friedlander M. Myeloid progenitors differentiate into microglia and promote vascular repair in a model of ischemic retinopathy. J Clin Invest 116 (2006) 3266-3276
12. Jin D.K., Shido K., Kopp H.G., Petit I., Shmelkov S.V., Young L.M., et al. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemangiocytes. Nat Med 12 (2006) 557-567
13. Fazel S., Cimini M., Chen L., Li S., Angoulvant D., Fedak P., et al. Cardioprotective c-kit+ cells are from the bone marrow and regulate the myocardial balance of angiogenic cytokines. J Clin Invest 116 (2006) 1865-1877
14. Stellos K., Langer H., Daub K., Schoenberger T., Gauss A., Geisler T., et al. Platelet-derived stromal cell-derived factor-1 regulates adhesion and promotes differentiation of human CD34+ cells to endothelial progenitor cells. Circulation 117 (2008) 206-215
15. Prater D.N., Case J., Ingram D.A., and Yoder M.C. Working hypothesis to redefine endothelial progenitor cells. Leukemia 21 (2007) 1141-1149
16. Pearson J.D. Endothelial progenitor cells-hype or hope?. J Thromb Haemost 7 (2009) 255-262
17. Shantsila E., Watson T., Tse H.F., and Lip G.Y. New insights on endothelial progenitor cell subpopulations and their angiogenic properties. J Am Coll Cardiol 51 (2008) 669-671
18. Sieveking D.P., Buckle A., Celermajer D.S., and Ng M.K. Strikingly different angiogenic properties of endothelial progenitor cell subpopulations: insights from a novel human angiogenesis assay. J Am Coll Cardiol 51 (2008) 660-668
19. Hirschi K.K., Ingram D.A., and Yoder M.C. Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler Thromb Vasc Biol 28 (2008) 1584-1595
20. Jacobsen E.A., Ochkur S.I., Lee N.A., and Lee J.J. Eosinophils and asthma. Curr Allergy Asthma Rep 7 (2007) 18-26
21. Rothenberg M.E., and Hogan S.P. The eosinophil. Annu Rev Immunol 24 (2006) 147-174
22. Fulkerson P.C., Fischetti C.A., McBride M.L., Hassman L.M., Hogan S.P., and Rothenberg M.E. A central regulatory role for eosinophils and the eotaxin/CCR3 axis in chronic experimental allergic airway inflammation. Proc Natl Acad Sci U S A 103 (2006) 16418-16423
23. Humbles A.A., Conroy D.M., Marleau S., Rankin S.M., Palframan R.T., Proudfoot A.E., et al. Kinetics of eotaxin generation and its relationship to eosinophil accumulation in allergic airways disease: analysis in a guinea pig model in vivo. J Exp Med 186 (1997) 601-612
24. Ying S., Robinson D.S., Meng Q., Rottman J., Kennedy R., Ringler D.J., et al. Enhanced expression of eotaxin and CCR3 mRNA and protein in atopic asthma. Association with airway hyperresponsiveness and predominant co-localization of eotaxin mRNA to bronchial epithelial and endothelial cells. Eur J Immunol 27 (1997) 3507-3516
25. Komiya A., Nagase H., Yamada H., Sekiya T., Yamaguchi M., Sano Y., et al. Concerted expression of eotaxin-1, eotaxin-2, and eotaxin-3 in human bronchial epithelial cells. Cell Immunol 225 (2003) 91-100
26. Blanchard C., Wang N., Stringer K.F., Mishra A., Fulkerson P.C., Abonia J.P., et al. Eotaxin-3 and a uniquely conserved gene-expression profile in eosinophilic esophagitis. J Clin Invest 116 (2006) 536-547
27. Rothenberg M.E. Eotaxin. An essential mediator of eosinophil trafficking into mucosal tissues. Am J Respir Cell Mol Biol 21 (1999) 291-295
28. Pope S.M., Fulkerson P.C., Blanchard C., Akei H.S., Nikolaidis N.M., Zimmermann N., et al. Identification of a cooperative mechanism involving interleukin-13 and eotaxin-2 in experimental allergic lung inflammation. J Biol Chem 280 (2005) 13952-13961
29. Garcia-Zepeda E.A., Rothenberg M.E., Ownbey R.T., Celestin J., Leder P., and Luster A.D. Human eotaxin is a specific chemoattractant for eosinophil cells and provides a new mechanism to explain tissue eosinophilia. Nat Med 2 (1996) 449-456
30. Smit J.J., and Lukacs N.W. A closer look at chemokines and their role in asthmatic responses. Eur J Pharmacol 533 (2006) 277-288
31. Palframan R.T., Collins P.D., Williams T.J., and Rankin S.M. Eotaxin induces a rapid release of eosinophils and their progenitors from the bone marrow. Blood 91 (1998) 2240-2248
32. Mould A.W., Matthaei K.I., Young I.G., and Foster P.S. Relationship between interleukin-5 and eotaxin in regulating blood and tissue eosinophilia in mice. J Clin Invest 99 (1997) 1064-1071
33. Jose P.J., Griffiths-Johnson D.A., Collins P.D., Walsh D.T., Moqbel R., Totty N.F., et al. Eotaxin: a potent eosinophil chemoattractant cytokine detected in a guinea pig model of allergic airways inflammation. J Exp Med 179 (1994) 881-887
34. Tenscher K., Metzner B., Schopf E., Norgauer J., and Czech W. Recombinant human eotaxin induces oxygen radical production, Ca(2+)-mobilization, actin reorganization, and CD11b upregulation in human eosinophils via a pertussis toxin-sensitive heterotrimeric guanine nucleotide-binding protein. Blood 88 (1996) 3195-3199
35. Ponath P.D., Qin S., Ringler D.J., Clark-Lewis I., Wang J., Kassam N., et al. Cloning of the human eosinophil chemoattractant, eotaxin. Expression, receptor binding, and functional properties suggest a mechanism for the selective recruitment of eosinophils. J Clin Invest 97 (1996) 604-612
36. Campbell E.M., Kunkel S.L., Strieter R.M., and Lukacs N.W. Temporal role of chemokines in a murine model of cockroach allergen-induced airway hyperreactivity and eosinophilia. J Immunol 161 (1998) 7047-7053
37. Gonzalo J.A., Lloyd C.M., Wen D., Albar J.P., Wells T.N., Proudfoot A., et al. The coordinated action of CC chemokines in the lung orchestrates allergic inflammation and airway hyperresponsiveness. J Exp Med 188 (1998) 157-167
38. Rothenberg M.E., MacLean J.A., Pearlman E., Luster A.D., and Leder P. Targeted disruption of the chemokine eotaxin partially reduces antigen-induced tissue eosinophilia. J Exp Med 185 (1997) 785-790
39. Yang Y., Loy J., Ryseck R.P., Carrasco D., and Bravo R. Antigen-induced eosinophilic lung inflammation develops in mice deficient in chemokine eotaxin. Blood 92 (1998) 3912-3923
40. Ochkur S.I., Jacobsen E.A., Protheroe C.A., Biechele T.L., Pero R.S., McGarry M.P., et al. Coexpression of IL-5 and eotaxin-2 in mice creates an eosinophil-dependent model of respiratory inflammation with characteristics of severe asthma. J Immunol 178 (2007) 7879-7889
41. Brown J.R., Kleimberg J., Marini M., Sun G., Bellini A., and Mattoli S. Kinetics of eotaxin expression and its relationship to eosinophil accumulation and activation in bronchial biopsies and bronchoalveolar lavage (BAL) of asthmatic patients after allergen inhalation. Clin Exp Immunol 114 (1998) 137-146
42. Ying S., Meng Q., Zeibecoglou K., Robinson D.S., Macfarlane A., Humbert M., et al. Eosinophil chemotactic chemokines (eotaxin, eotaxin-2, RANTES, monocyte chemoattractant protein-3 (MCP-3 and MCP-4), and C-C chemokine receptor 3 expression in bronchial biopsies from atopic and nonatopic (Intrinsic) asthmatics. J Immunol 163 (1999) 6321-6329
43. National Asthma Education and Prevention Program. 1997. Expert Panel Report II: Guidelines for the Diagnosis and Management of Asthma, National Institutes of Health Publication 97-4051. National Heart, Lung, and Blood Institute, Bethesda, MD.
44. Aronica M.A., McCarthy S., Swaidani S., Mitchell D., Goral M., Sheller J.R., et al. Recall helper T cell response: T helper 1 cell-resistant allergic susceptibility without biasing uncommitted CD4 T cells. Am J Respir Crit Care Med 169 (2004) 587-595
45. Aronica M.A., Swaidani S., Zhang Y.H., Mitchell D., Mora A.L., McCarthy S., et al. Susceptibility to allergic lung disease regulated by recall responses of dual-receptor memory T cells. J Allergy Clin Immunol 114 (2004) 1441-1448
46. Urbich C., and Dimmeler S. Endothelial progenitor cells: characterization and role in vascular biology. Circ Res 95 (2004) 343-353
47. Urbich C., Heeschen C., Aicher A., Dernbach E., Zeiher A.M., and Dimmeler S. Relevance of monocytic features for neovascularization capacity of circulating endothelial progenitor cells. Circulation 108 (2003) 2511-2516
48. Chavakis E., Aicher A., Heeschen C., Sasaki K., Kaiser R., El Makhfi N., et al. Role of beta2-integrins for homing and neovascularization capacity of endothelial progenitor cells. J Exp Med 201 (2005) 63-72
49. Rossig L., Urbich C., Bruhl T., Dernbach E., Heeschen C., Chavakis E., et al. Histone deacetylase activity is essential for the expression of HoxA9 and for endothelial commitment of progenitor cells. J Exp Med 201 (2005) 1825-1835
50. Hill J.M., Zalos G., Halcox J.P., Schenke W.H., Waclawiw M.A., Quyyumi A.A., et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 348 (2003) 593-600
51. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25 (2001) 402-408
52. Lee J.J., Dimina D., Macias M.P., Ochkur S.I., McGarry M.P., O'Neill K.R., et al. Defining a link with asthma in mice congenitally deficient in eosinophils. Science 305 (2004) 1773-1776
53. Marsboom G., Pokreisz P., Gheysens O., Vermeersch P., Gillijns H., Pellens M., et al. Sustained endothelial progenitor cell dysfunction after chronic hypoxia-induced pulmonary hypertension. Stem Cells 26 (2008) 1017-1026
54. Asahara T., Murohara T., Sullivan A., Silver M., van der Zee R., Li T., et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275 (1997) 964-967
55. Kalka C., Masuda H., Takahashi T., Gordon R., Tepper O., Gravereaux E., et al. Vascular endothelial growth factor(165) gene transfer augments circulating endothelial progenitor cells in human subjects. Circ Res 86 (2000) 1198-1202
56. Oynebraten I., Bakke O., Brandtzaeg P., Johansen F.E., and Haraldsen G. Rapid chemokine secretion from endothelial cells originates from 2 distinct compartments. Blood 104 (2004) 314-320
57. Justice J.P., Borchers M.T., Crosby J.R., Hines E.M., Shen H.H., Ochkur S.I., et al. Ablation of eosinophils leads to a reduction of allergen-induced pulmonary pathology. Am J Physiol Lung Cell Mol Physiol 284 (2003) L169-L178
58. Grimaldi J.C., Yu N.X., Grunig G., Seymour B.W., Cottrez F., Robinson D.S., et al. Depletion of eosinophils in mice through the use of antibodies specific for C-C chemokine receptor 3 (CCR3). J Leukoc Biol 65 (1999) 846-853
59. Pascual R.M., and Peters S.P. Airway remodeling contributes to the progressive loss of lung function in asthma: an overview. J Allergy Clin Immunol 116 (2005) 477-487
60. Ganzalo J.A., Jia G.Q., Aguirre V., Friend D., Coyle A.J., Jenkins N.A., et al. Mouse eotaxin expression parallels eosinophil accumulation during lung allergic inflammation but it is not restricted to a Th2-type response. Immunity 4 (1996) 1-14