IL-5 triggers a cooperative cytokine network that promotes eosinophil precursor maturation

Journal of Immunology

Volumn 193, Issue 8, 2014, Pages 4043-4052

  Fulkerson, Patricia C ^a   Schollaert, Kaila L ^a   Bouffi, Carine ^a   Rothenberg, Marc E ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR CCR1; CYTOKINE; CYTOKINE RECEPTOR; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR ALPHA; INTERLEUKIN 5; CCL3 PROTEIN, MOUSE; CCR1 PROTEIN, MOUSE; CELL SURFACE RECEPTOR; IL4RA PROTEIN, MOUSE; INTERLEUKIN 5 RECEPTOR ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOCRINE EFFECT; BONE MARROW CELL; CELL DIFFERENTIATION; CELL MATURATION; CELL STIMULATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEVELOPMENTAL STAGE; EOSINOPHIL; FEMALE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STEM CELL; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL CULTURE; CELL LINEAGE; CYTOLOGY; DRUG EFFECTS; EOSINOPHILIA; IMMUNOLOGY;

ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; CHEMOKINE CCL3; EOSINOPHILIA; EOSINOPHILS; FEMALE; INTERLEUKIN-4; INTERLEUKIN-5; INTERLEUKIN-5 RECEPTOR ALPHA SUBUNIT; MALE; MICE; MICE, INBRED BALB C; RECEPTORS, CCR1; RECEPTORS, CELL SURFACE;

EID: 84907485545     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400732     Document Type: Article

References (35)

1. Iwasaki, H., S. Mizuno, R. Mayfield, H. Shigematsu, Y. Arinobu, B. Seed, M. F. Gurish, K. Takatsu, and K. Akashi. 2005. Identification of eosinophil lineage-committed progenitors in the murine bone marrow. J. Exp. Med. 201: 1891-1897.
2. Mori, Y., H. Iwasaki, K. Kohno, G. Yoshimoto, Y. Kikushige, A. Okeda, N. Uike, H. Niiro, K. Takenaka, K. Nagafuji, et al. 2009. Identification of the human eosinophil lineage-committed progenitor: revision of phenotypic definition of the human common myeloid progenitor. J. Exp. Med. 206: 183-193.
3. Inman, M. D., R. Ellis, J. Wattie, J. A. Denburg, and P. M. O'Byrne. 1999. Allergen-induced increase in airway responsiveness, airway eosinophilia, and bone-marrow eosinophil progenitors in mice. Am. J. Respir. Cell Mol. Biol. 21: 473-479.
4. Gaspar Elsas, M. I., D. Joseph, P. X. Elsas, and B. B. Vargaftig. 1997. Rapid increase in bone-marrow eosinophil production and responses to eosinopoietic interleukins triggered by intranasal allergen challenge. Am. J. Respir. Cell Mol. Biol. 17: 404-413.
5. Robinson, D. S., R. Damia, K. Zeibecoglou, S. Molet, J. North, T. Yamada, A. B. Kay, and Q. Hamid. 1999. CD34(+)/interleukin-5Ralpha messenger RNA+ cells in the bronchial mucosa in asthma: potential airway eosinophil progenitors. Am. J. Respir. Cell Mol. Biol. 20: 9-13.
6. Cameron, L., P. Christodoulopoulos, F. Lavigne, Y. Nakamura, D. Eidelman, A. McEuen, A. Walls, J. Tavernier, E. Minshall, R. Moqbel, and Q. Hamid. 2000. Evidence for local eosinophil differentiation within allergic nasal mucosa: inhibition with soluble IL-5 receptor. J. Immunol. 164: 1538-1545.
7. Allakhverdi, Z., M. R. Comeau, D. E. Smith, D. Toy, L. M. Endam, M. Desrosiers, Y. J. Liu, K. J. Howie, J. A. Denburg, G. M. Gauvreau, and G. Delespesse. 2009. CD34+ hemopoietic progenitor cells are potent effectors of allergic inflammation. J. Allergy Clin. Immunol. 123: 472-478.
8. Kouro, T., and K. Takatsu. 2009. IL-5-and eosinophil-mediated inflammation: from discovery to therapy. Int. Immunol. 21: 1303-1309.
9. Clutterbuck, E. J., E. M. Hirst, and C. J. Sanderson. 1989. Human interleukin-5 (IL-5) regulates the production of eosinophils in human bone marrow cultures: comparison and interaction with IL-1, IL-3, IL-6, and GMCSF. Blood 73: 1504-1512.
10. Dent, L. A., M. Strath, A. L. Mellor, and C. J. Sanderson. 1990. Eosinophilia in transgenic mice expressing interleukin 5. J. Exp. Med. 172: 1425-1431.
11. Lee, N. A., M. P. McGarry, K. A. Larson, M. A. Horton, A. B. Kristensen, and J. J. Lee. 1997. Expression of IL-5 in thymocytes/T cells leads to the development of a massive eosinophilia, extramedullary eosinophilopoiesis, and unique histopathologies. J. Immunol. 158: 1332-1344.
12. Kopf, M., F. Brombacher, P. D. Hodgkin, A. J. Ramsay, E. A. Milbourne, W. J. Dai, K. S. Ovington, C. A. Behm, G. Köhler, I. G. Young, and K. I. Matthaei. 1996. IL-5-deficient mice have a developmental defect in CD5+ B-1 cells and lack eosinophilia but have normal antibody and cytotoxic T cell responses. Immunity 4: 15-24.
13. Busse, W. W., J. Ring, J. Huss-Marp, and J. E. Kahn. 2010. A review of treatment with mepolizumab, an anti-IL-5 mAb, in hypereosinophilic syndromes and asthma. J. Allergy Clin. Immunol. 125: 803-813.
14. Haldar, P., C. E. Brightling, B. Hargadon, S. Gupta, W. Monteiro, A. Sousa, R. P. Marshall, P. Bradding, R. H. Green, A. J. Wardlaw, and I. D. Pavord. 2009. Mepolizumab and exacerbations of refractory eosinophilic asthma. N. Engl. J. Med. 360: 973-984.
15. Flood-Page, P. T., A. N. Menzies-Gow, A. B. Kay, and D. S. Robinson. 2003. Eosinophil's role remains uncertain as anti-interleukin-5 only partially depletes numbers in asthmatic airway. Am. J. Respir. Crit. Care Med. 167: 199-204.
16. Plö tz, S. G., H. U. Simon, U. Darsow, D. Simon, E. Vassina, S. Yousefi, R. Hein, T. Smith, H. Behrendt, and J. Ring. 2003. Use of an anti-interleukin-5 antibody in the hypereosinophilic syndrome with eosinophilic dermatitis. N. Engl. J. Med. 349: 2334-2339.
17. Straumann, A., S. Conus, P. Grzonka, H. Kita, G. Kephart, C. Bussmann, C. Beglinger, D. A. Smith, J. Patel, M. Byrne, and H. U. Simon. 2010. Antiinterleukin-5 antibody treatment (mepolizumab) in active eosinophilic oesophagitis: a randomised, placebo-controlled, double-blind trial. Gut 59: 21-30.
18. Assa'ad, A. H., S. K. Gupta, M. H. Collins, M. Thomson, A. T. Heath, D. A. Smith, T. L. Perschy, C. H. Jurgensen, H. G. Ortega, and S. S. Aceves. 2011. An antibody against IL-5 reduces numbers of esophageal intraepithelial eosinophils in children with eosinophilic esophagitis. Gastroenterology 141: 1593-1604.
19. Alam, R., J. York, M. Boyars, S. Stafford, J. A. Grant, J. Lee, P. Forsythe, T. Sim, and N. Ida. 1996. Increased MCP-1, RANTES, and MIP-1alpha in bronchoalveolar lavage fluid of allergic asthmatic patients. Am. J. Respir. Crit. Care Med. 153: 1398-1404.
20. Fulkerson, P. C., N. Zimmermann, L. M. Hassman, F. D. Finkelman, and M. E. Rothenberg. 2004. Pulmonary chemokine expression is coordinately regulated by STAT1, STAT6, and IFN-gamma. J. Immunol. 173: 7565-7574.
21. McKenzie, G. J., P. G. Fallon, C. L. Emson, R. K. Grencis, and A. N. McKenzie. 1999. Simultaneous disruption of interleukin (IL)-4 and IL-13 defines individual roles in T helper cell type 2-mediated responses. J. Exp. Med. 189: 1565-1572.
22. Mohrs, M., K. Shinkai, K. Mohrs, and R. M. Locksley. 2001. Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter. Immunity 15: 303-311.
23. Bouffi, C., M. Rochman, C. B. Zust, E. M. Stucke, A. Kartashov, P. C. Fulkerson, A. Barski, and M. E. Rothenberg. 2013. IL-33 markedly activates murine eosinophils by an NF-kB-dependent mechanism differentially dependent upon an IL-4-driven autoinflammatory loop. J. Immunol. 191: 4317-4325.
24. Edgar, R., M. Domrachev, and A. E. Lash. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30: 207-210.
25. Menzies-Gow, A., P. Flood-Page, R. Sehmi, J. Burman, Q. Hamid, D. S. Robinson, A. B. Kay, and J. Denburg. 2003. Anti-IL-5 (mepolizumab) therapy induces bone marrow eosinophil maturational arrest and decreases eosinophil progenitors in the bronchial mucosa of atopic asthmatics. J. Allergy Clin. Immunol. 111: 714-719.
26. Conus, S., A. Straumann, E. Bettler, and H. U. Simon. 2010. Mepolizumab does not alter levels of eosinophils, T cells, and mast cells in the duodenal mucosa in eosinophilic esophagitis. J. Allergy Clin. Immunol. 126: 175-177.
27. Byström, J., T. A. Wynn, J. B. Domachowske, and H. F. Rosenberg. 2004. Gene microarray analysis reveals interleukin-5-dependent transcriptional targets in mouse bone marrow. Blood 103: 868-877.
28. Elsner, J., Y. Dulkys, S. Gupta, S. E. Escher, W. G. Forssmann, A. Kapp, and U. Forssmann. 2005. Differential pattern of CCR1 internalization in human eosinophils: prolonged internalization by CCL5 in contrast to CCL3. Allergy 60: 1386-1393.
29. Phillips, R. M., V. E. Stubbs, M. R. Henson, T. J. Williams, J. E. Pease, and I. Sabroe. 2003. Variations in eosinophil chemokine responses: an investigation of CCR1 and CCR3 function, expression in atopy, and identification of a functional CCR1 promoter. J. Immunol. 170: 6190-6201.
30. Oliveira, S. H., S. Lira, C. Martinez-A, M. Wiekowski, L. Sullivan, and N. W. Lukacs. 2002. Increased responsiveness of murine eosinophils to MIP-1beta (CCL4) and TCA-3 (CCL1) is mediated by their specific receptors, CCR5 and CCR8. J. Leukoc. Biol. 71: 1019-1025.
31. Borchers, M. T., T. Ansay, R. DeSalle, B. L. Daugherty, H. Shen, M. Metzger, N. A. Lee, and J. J. Lee. 2002. In vitro assessment of chemokine receptor-ligand interactions mediating mouse eosinophil migration. J. Leukoc. Biol. 71: 1033-1041.
32. Gaga, M., Y. E. Ong, F. Benyahia, M. Aizen, J. Barkans, and A. B. Kay. 2008. Skin reactivity and local cell recruitment in human atopic and nonatopic subjects by CCL2/MCP-1 and CCL3/MIP-1alpha. Allergy 63: 703-711.
33. Domachowske, J. B., C. A. Bonville, J. L. Gao, P. M. Murphy, A. J. Easton, and H. F. Rosenberg. 2000. The chemokine macrophage-inflammatory protein-1 alpha and its receptor CCR1 control pulmonary inflammation and antiviral host defense in paramyxovirus infection. J. Immunol. 165: 2677-2682.
34. Broxmeyer, H. E., S. Cooper, G. Hangoc, J. L. Gao, and P. M. Murphy. 1999. Dominant myelopoietic effector functions mediated by chemokine receptor CCR1. J. Exp. Med. 189: 1987-1992.
35. Leckie, M. J., A. ten Brinke, J. Khan, Z. Diamant, B. J. O'Connor, C. M. Walls, A. K. Mathur, H. C. Cowley, K. F. Chung, R. Djukanovic, et al. 2000. Effects of an interleukin-5 blocking monoclonal antibody on eosinophils, airway hyperresponsiveness, and the late asthmatic response. Lancet 356: 2144-2148.