Myeloid hypoxia-inducible factor 1α prevents airway allergy in mice through macrophage-mediated immunoregulation

Mucosal Immunology

Volumn 6, Issue 3, 2013, Pages 485-497

  Toussaint, M ^a   Fievez, L ^a   Drion, P V ^a   Cataldo, D ^a   Bureau, F ^a   Lekeux, P ^a   Desmet, C J ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; HOUSE DUST ALLERGEN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 10; MYELOID DIFFERENTIATION FACTOR 88; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CELL ACTIVATION; CELL MIGRATION; CELL SELECTION; CONTROLLED STUDY; DENDRITIC CELL; DISEASE EXACERBATION; EXPOSURE; FEMALE; FLOW CYTOMETRY; IMMUNOREGULATION; LUNG ALVEOLUS MACROPHAGE; LYMPHOCYTE ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY TRACT ALLERGY; SENSITIZATION; T LYMPHOCYTE; UPREGULATION;

EID: 84876384409     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2012.88     Document Type: Article

References (58)

1. Eder, W., Ege, M. J. & von Mutius, E. The asthma epidemic. N. Engl. J. Med. 355, 2226-2235 (2006).
2. Barrett, N. A. & Austen, K. F. Innate cells and T helper 2 cell immunity in airway infl ammation. Immunity 31, 425-437 (2009).
3. Lambrecht, B. N. & Hammad, H. Biology of lung dendritic cells at the origin of asthma. Immunity 31, 412-424 (2009).
4. Locksley, R. M. Asthma and allergic infl ammation. Cell 140, 777-783 (2010).
5. Robinson, D. S. Regulatory T cells and asthma. Clin. Exp. Allergy 39, 1314-1323 (2009).
6. Arnold, I. C. et al. Helicobacter pylori infection prevents allergic asthma in mouse models through the induction of regulatory T cells. J. Clin. Invest. 121, 3088-3093 (2011).
7. Franke-Ullmann, G., Pfortner, C., Walter, P., Steinmuller, C., Lohmann- Matthes, M. L. & Kobzik, L. Characterization of murine lung interstitial macrophages in comparison with alveolar macrophages in vitro. J. Immunol. 157, 3097-3104 (1996).
8. Hoppstadter, J. et al. Differential cell reaction upon Toll-like receptor 4 and 9 activation in human alveolar and lung interstitial macrophages. Respir. Res. 11, 124 (2010).
9. Thepen, T., Van Rooijen, N. & Kraal, G. Alveolar macrophage elimination in vivo is associated with an increase in pulmonary immune response in mice. J. Exp. Med. 170, 499-509 (1989).
10. Holt, P. G. et al. Downregulation of the antigen presenting cell function(s) of pulmonary dendritic cells in vivo by resident alveolar macrophages. J. Exp. Med. 177, 397-407 (1993).
11. Bedoret, D. et al. Lung interstitial macrophages alter dendritic cell functions to prevent airway allergy in mice. J. Clin. Invest. 119, 3723-3738 (2009).
12. King, C., Brennan, S., Thompson, P. J. & Stewart, G. A. Dust mite proteolytic allergens induce cytokine release from cultured airway epithelium. J. Immunol. 161, 3645-3651 (1998).
13. Hammad, H., Chieppa, M., Perros, F., Willart, M. A., Germain, R. N. & Lambrecht, B. N. House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat. Med. 15, 410-416 (2009).
14. Bilyk, N. & Holt, P. G. Inhibition of the immunosuppressive activity of resident pulmonary alveolar macrophages by granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 177, 1773-1777 (1993).
15. Michel, O. et al. Severity of asthma is related to endotoxin in house dust. Am. J. Respir. Crit. Care Med. 154 (6 part 1), 1641-1646 (1996).
16. Thorn, J. & Rylander, R. Airways infl ammation and glucan in a rowhouse area. Am. J. Respir. Crit. Care Med. 157, 1798-1803 (1998).
17. Douwes, J. et al. Does early indoor microbial exposure reduce the risk of asthma? The Prevention and Incidence of Asthma and Mite Allergy Birth Cohort Study. J. Allergy Clin. Immunol. 117, 1067-1073 (2006).
18. Weidemann, A. & Johnson, R. S. Biology of HIF-1alpha. Cell. Death Differ. 15, 621-627 (2008).
19. Wang, G. L., Jiang, B. H., Rue, E. A. & Semenza, G. L. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. USA 92, 5510-5514 (1995).
20. Bruick, R. K. & McKnight, S. L. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294, 1337-1340 (2001).
21. Jaakkola, P. et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292, 468-472 (2001).
22. Sitkovsky, M. & Lukashev, D. Regulation of immune cells by local-tissue oxygen tension: HIF1 alpha and adenosine receptors. Nat. Rev. Immunol. 5, 712-721 (2005).
23. Cramer, T. et al. HIF-1alpha is essential for myeloid cell-mediated infl ammation. Cell 112, 645-657 (2003).
24. Walmsley, S. R. et al. Hypoxia-induced neutrophil survival is mediated by HIF-1alpha-dependent NF-kappaB activity. J. Exp. Med. 201, 105-115 (2005).
25. Elks, P. M. et al. Activation of hypoxia-inducible factor-1alpha (Hif-1alpha) delays infl ammation resolution by reducing neutrophil apoptosis and reverse migration in a zebrafi sh infl ammation model. Blood 118, 712-722 (2011).
26. Rius, J. et al. NF-kappaB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1alpha. Nature 453, 807-811 (2008).
27. Peyssonnaux, C., Cejudo-Martin, P., Doedens, A., Zinkernagel, A. S., Johnson, R. S. & Nizet, V. Cutting edge: essential role of hypoxia inducible factor-1alpha in development of lipopolysaccharide-induced sepsis. J. Immunol. 178, 7516-7519 (2007).
28. Peyssonnaux, C. et al. HIF-1alpha expression regulates the bactericidal capacity of phagocytes. J. Clin. Invest. 115, 1806-1815 (2005).
29. Jantsch, J. et al. Toll-like receptor activation and hypoxia use distinct signaling pathways to stabilize hypoxia-inducible factor 1alpha (HIF1A) and result in differential HIF1A-dependent gene expression. J. Leukoc. Biol. 90, 551-562 (2011).
30. Mahabeleshwar, GH. et al. The myeloid transcription factor KLF2 regulates the host response to polymicrobial infection and endotoxic shock. Immunity 34, 715-728 (2011).
31. Blouin, C. C., Page, E. L., Soucy, G. M. & Richard, D. E. Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1alpha. Blood 103, 1124-1130 (2004).
32. Landsman, L., Varol, C. & Jung, S. Distinct differentiation potential of blood monocyte subsets in the lung. J. Immunol. 178, 2000-2007 (2007).
33. Cates, E. C. et al. Intranasal exposure of mice to house dust mite elicits allergic airway infl ammation via a GM-CSF-mediated mechanism. J. Immunol. 173, 6384-6392 (2004).
34. Marichal, T. et al. Interferon response factor 3 is essential for house dust mite-induced airway allergy. J. Allergy Clin. Immunol. 126, 836-844 (2010).
35. Hammad, H. et al. Infl ammatory dendritic cells-not basophils-are necessary and suffi cient for induction of Th2 immunity to inhaled house dust mite allergen. J. Exp. Med. 207, 2097-2111 (2010).
36. Trompette, A. et al. Allergenicity resulting from functional mimicry of a Toll-like receptor complex protein. Nature 457, 585-588 (2009).
37. Shi, LZ. et al. HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J. Exp. Med. 208, 1367-1376 (2011).
38. Dang, E. V. et al. Control of TH17/Treg balance by hypoxia-inducible factor 1. Cell 146, 772-784 (2011).
39. Thiel, M. et al. Oxygenation inhibits the physiological tissue-protecting mechanism and thereby exacerbates acute infl ammatory lung injury. PLoS. Biol. 3, e174 (2005).
40. Rosenberger, P. et al. Hypoxia-inducible factor-dependent induction of netrin-1 dampens infl ammation caused by hypoxia. Nat. Immunol. 10, 195-202 (2009).
41. Corzo, CA. et al. HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J. Exp. Med. 207, 2439-2453 (2010).
42. Doedens, A. L. et al. Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression. Cancer Res. 70, 7465-7475 (2010).
43. Huerta-Yepez, S. et al. Hypoxia inducible factor promotes murine allergic airway infl ammation and is increased in asthma and rhinitis. Allergy 66, 909-918 (2011).
44. Kim, S. R. et al. HIF-1alpha inhibition ameliorates an allergic airway disease via VEGF suppression in bronchial epithelium. Eur. J. Immunol. 40, 2858-2869 (2010).
45. Jantsch, J. et al. Hypoxia and hypoxia-inducible factor-1alpha modulate lipopolysaccharide-induced dendritic cell activation and function. J. Immunol. 180, 4697-4705 (2008).
46. Mancino, A. et al. Divergent effects of hypoxia on dendritic cell functions. Blood 112, 3723-3734 (2008).
47. Yang, M. et al. HIF-dependent induction of adenosine receptor A2b skews human dendritic cells to a Th2-stimulating phenotype under hypoxia. Immunol. Cell. Biol. 88, 165-171 (2010).
48. Tang, C. et al. Th type 1-stimulating activity of lung macrophages inhibits Th2-mediated allergic airway infl ammation by an IFN-gamma-dependent mechanism. J. Immunol. 166, 1471-1481 (2001).
49. Careau, E. & Bissonnette, E. Y. Adoptive transfer of alveolar macrophages abrogates bronchial hyperresponsiveness. Am. J. Respir. Cell. Mol. Biol. 31, 22-27 (2004).
50. Gasser, O. & Schifferli, A. Jr Activated polymorphonuclear neutrophils disseminate anti-infl ammatory microparticles by ectocytosis. Blood 104, 2543-2548 (2004).
51. Maffi a, P. C. et al. Neutrophil elastase converts human immature dendritic cells into transforming growth factor-beta1-secreting cells and reduces allostimulatory ability. Am. J. Pathol. 171, 928-937 (2007).
52. Eken, C., Gasser, O., Zenhaeusern, G., Oehri, I., Hess, C. & Schifferli, J. A. Polymorphonuclear neutrophil-derived ectosomes interfere with the maturation of monocyte-derived dendritic cells. J. Immunol. 180, 817-824 (2008).
53. Lamblin, C. et al. Bronchial neutrophilia in patients with noninfectious status asthmaticus. Am. J. Respir. Crit. Care Med. 157, 394-402 (1998).
54. Foley, S. C. & Hamid, Q. Images in allergy and immunology: neutrophils in asthma. J. Allergy Clin. Immunol. 119, 1282-1286 (2007).
55. Nabe, T. et al. Important role of neutrophils in the late asthmatic response in mice. Life Sci. 88, 1127-1135 (2011).
56. Denning, T. L., Wang, Y.-C., Patel, S. R., W illiams, I. R. & Pulendran, B. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat. Immunol. 8, 1086-1094 (2007).
57. Ryan, H. E. et al. Hypoxia-inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res. 60, 4010-4015 (2000).
58. Clausen, B. E., Burkhardt, C., Reith, W., Renkawitz, R. & Forster, I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8, 265-277 (1999).