Lung-resident eosinophils represent a distinct regulatory eosinophil subset

Journal of Clinical Investigation

Volumn 126, Issue 9, 2016, Pages 3279-3295

  Mesnil, Claire ^a   Raulier, Stéfanie ^a   Paulissen, Geneviève ^a   Xiao, Xue ^a   Birrell, Mark A ^b   Pirottin, Dimitri ^a   Janss, Thibaut ^a   Starkl, Philipp ^c   Ramery, Eve ^a   Henket, Monique ^d   Schleich, Florence N ^d   Radermecker, Marc ^d   Thielemans, Kris ^e   Gillet, Laurent ^a   Thiry, Marc ^a   Belvisi, Maria G ^b   Louis, Renaud ^d   Desmet, Christophe ^a   Marichal, Thomas ^a   Bureau, Fabrice ^a,f  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

^d UNIVERSITY OF LIÈGE   (Belgium)

^e VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^f Walloon Excellence in Life Sciences and Biotechnology (Welbio)   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

HOUSE DUST ALLERGEN; INTERLEUKIN 5; L SELECTIN; SIALIC ACID BINDING IMMUNOGLOBULIN LIKE LECTIN; ALLERGEN; CD101 ANTIGEN, HUMAN; LEUKOCYTE ANTIGEN; MEMBRANE PROTEIN; TRANSCRIPTOME;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SHAPE; CLINICAL FEATURE; CONTROLLED STUDY; DERMATOPHAGOIDES; EOSINOPHIL; EOSINOPHIL COUNT; FEMALE; GENETIC ANALYSIS; HOUSE DUST ALLERGY; HUMAN; HUMAN CELL; LUNG PARENCHYMA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEADY STATE; TH2 CELL; AGED; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CYTOLOGY; DENDRITIC CELL; HOMEOSTASIS; HYPERSENSITIVITY; IMMUNOLOGY; INFLAMMATION; LUNG; METABOLISM; MIDDLE AGED; PHAGOCYTOSIS; PYROGLYPHIDAE;

ADULT; AGED; ALLERGENS; ANIMALS; ANTIGENS, CD; DENDRITIC CELLS; EOSINOPHILS; FEMALE; HOMEOSTASIS; HUMANS; HYPERSENSITIVITY; INFLAMMATION; INTERLEUKIN-5; L-SELECTIN; LUNG; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MIDDLE AGED; PHAGOCYTOSIS; PYROGLYPHIDAE; TH2 CELLS; TRANSCRIPTOME;

EID: 84987786714     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI85664     Document Type: Article

References (83)

1. Rothenberg ME, Hogan SP. The eosinophil. Annu Rev Immunol. 2006;24:147-174
2. Travers J, Rothenberg ME. Eosinophils in mucosal immune responses. Mucosal Immunol. 2015;8(3):464-475
3. Nerlov C, Graf T. PU.1 induces myeloid lineage commitment in multipotent hematopoietic progenitors. Genes Dev. 1998;12(15):2403-2412
4. Nerlov C, McNagny KM, Döderlein G, Kowenz-Leutz E, Graf T. Distinct C/EBP functions are required for eosinophil lineage commitment and maturation. Genes Dev. 1998;12(15):2413-2423
5. Hirasawa R, et al. Essential and instructive roles of GATA factors in eosinophil development. J Exp Med. 2002;195(11):1379-1386
6. Bettigole SE, et al. The transcription factor XBP1 is selectively required for eosinophil differentiation. Nat Immunol. 2015;16(8):829-837
7. Grouls V, Helpap B. Selective staining of eosinophils and their immature precursors in tissue sections and autoradiographs with Congo red. Stain Technol. 1981;56(5):323-325
8. Rosenberg HF, Dyer KD, Foster PS. Eosinophils: changing perspectives in health and disease. Nat Rev Immunol. 2013;13(1):9-22
9. Lopez AF, Sanderson CJ, Gamble JR, Campbell HD, Young IG, Vadas MA. Recombinant human interleukin 5 is a selective activator of human eosinophil function. J Exp Med. 1988;167(1):219-224
10. de Graauw E, Beltraminelli H, Simon HU, Simon D. Eosinophilia in Dermatologic Disorders. Immunol Allergy Clin North Am. 2015;35(3):545-560
11. Padigel UM, et al. Eosinophils act as antigen-presenting cells to induce immunity to Strongyloides stercoralis in mice. J Infect Dis. 2007;196(12):1844-1851
12. Shi HZ, Humbles A, Gerard C, Jin Z, Weller PF. Lymph node trafficking and antigen presentation by endobronchial eosinophils. J Clin Invest. 2000;105(7):945-953
13. Wang HB, Ghiran I, Matthaei K, Weller PF. Airway eosinophils: allergic inflammation recruited professional antigen-presenting cells. J Immunol. 2007;179(11):7585-7592
14. Chu DK, et al. Indigenous enteric eosinophils control DCs to initiate a primary Th2 immune response in vivo. J Exp Med. 2014;211(8):1657-1672
15. Jacobsen EA, Zellner KR, Colbert D, Lee NA, Lee JJ. Eosinophils regulate dendritic cells and Th2 pulmonary immune responses following allergen provocation. J Immunol. 2011;187(11):6059-6068
16. Lee JJ, Jacobsen EA, McGarry MP, Schleimer RP, Lee NA. Eosinophils in health and disease: the LIAR hypothesis. Clin Exp Allergy. 2010;40(4):563-575
17. Chu VT, et al. Eosinophils promote generation and maintenance of immunoglobulin-A-expressing plasma cells and contribute to gut immune homeostasis. Immunity. 2014;40(4):582-593
18. Jung Y, et al. IL-1β in eosinophil-mediated small intestinal homeostasis and IgA production. Mucosal Immunol. 2015;8(4):930-942
19. Wu D, et al. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science. 2011;332(6026):243-247
20. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest. 2007;117(1):175-184
21. Enerbäck S. Human brown adipose tissue. Cell Metab. 2010;11(4):248-252
22. Throsby M, Herbelin A, Pléau JM, Dardenne M. CD11c+ eosinophils in the murine thymus: devel-opmental regulation and recruitment upon MHC class I-restricted thymocyte deletion. J Immunol. 2000;165(4):1965-1975
23. Gouon-Evans V, Pollard JW. Eotaxin is required for eosinophil homing into the stroma of the pubertal and cycling uterus. Endocrinology. 2001;142(10):4515-4521
24. Gouon-Evans V, Rothenberg ME, Pollard JW. Postnatal mammary gland development requires macrophages and eosinophils. Development. 2000;127(11):2269-2282
25. Abdala Valencia H, Loffredo LF, Misharin AV, Berdnikovs S. Phenotypic plasticity and targeting of Siglec-F(high) CD11c(low) eosinophils to the airway in a murine model of asthma. Allergy. 2016;71(2):267-271
26. Carlens J, Wahl B, Ballmaier M, Bulfone-Paus S, Förster R, Pabst O. Common gamma-chaindependent signals confer selective survival of eosinophils in the murine small intestine. J Immunol. 2009;183(9):5600-5607
27. Rose CE, Lannigan JA, Kim P, Lee JJ, Fu SM, Sung SS. Murine lung eosinophil activation and chemokine production in allergic airway inflammation. Cell Mol Immunol. 2010;7(5):361-374
28. Dyer KD, Garcia-Crespo KE, Killoran KE, Rosenberg HF. Antigen profiles for the quantitative assessment of eosinophils in mouse tissues by flow cytometry. J Immunol Methods. 2011;369(1-2):91-97
29. Stevens WW, Kim TS, Pujanauski LM, Hao X, Braciale TJ. Detection and quantitation of eosinophils in the murine respiratory tract by flow cytometry. J Immunol Methods. 2007; 327(1-2):63-74
30. Takatsu K. Interleukin 5 (IL-5) and its receptor. Microbiol Immunol. 1991;35(8):593-606
31. Zhang JQ, Biedermann B, Nitschke L, Crocker PR. The murine inhibitory receptor mSiglec-E is expressed broadly on cells of the innate immune system whereas mSiglec-F is restricted to eosinophils. Eur J Immunol. 2004;34(4):1175-1184
32. McGarry MP, Stewart CC. Murine eosinophil granulocytes bind the murine macrophage-monocyte specific monoclonal antibody F4/80. J Leukoc Biol. 1991;50(5):471-478
33. Gao JL, et al. Identification of a mouse eosinophil receptor for the CC chemokine eotaxin. Biochem Biophys Res Commun. 1996;223(3):679-684
34. Malm-Erjefält M, Persson CG, Erjefält JS. Degranulation status of airway tissue eosinophils in mouse models of allergic airway inflammation. Am J Respir Cell Mol Biol. 2001;24(3):352-359
35. Melo RC, Dvorak AM, Weller PF. Contributions of electron microscopy to understand secretion of immune mediators by human eosinophils. Microsc Microanal. 2010;16(6):653-660
36. Jacobsen EA, Ochkur SI, Lee NA, Lee JJ. Eosinophils and asthma. Curr Allergy Asthma Rep. 2007;7(1):18-26
37. Wegmann M. Targeting eosinophil biology in asthma therapy. Am J Respir Cell Mol Biol. 2011;45(4):667-674
38. Marichal T, et al. Interferon response factor 3 is essential for house dust mite-induced airway allergy. J Allergy Clin Immunol. 2010;126(4):836-844.e13
39. Xue FM, et al. CD98 positive eosinophils contribute to T helper 1 pattern inflammation. PLoS ONE. 2012;7(12):e51830
40. McAlees JW, et al. Distinct Tlr4-expressing cell compartments control neutrophilic and eosinophilic airway inflammation. Mucosal Immunol. 2015;8(4):863-873
41. Drouin SM, Corry DB, Hollman TJ, Kildsgaard J, Wetsel RA. Absence of the complement anaphylatoxin C3a receptor suppresses Th2 effector functions in a murine model of pulmonary allergy. J Immunol. 2002;169(10):5926-5933
42. Niebuhr M, Bäumer W, Kietzmann M, Wichmann K, Heratizadeh A, Werfel T. Participation of complement 3a receptor (C3aR) in the sensitization phase of Th2 mediated allergic contact dermatitis. Exp Dermatol. 2012;21(1):52-56
43. Mitchell J, Dimov V, Townley RG. IL-13 and the IL-13 receptor as therapeutic targets for asthma and allergic disease. Curr Opin Investig Drugs. 2010;11(5):527-534
44. Chu DK, et al. Therapeutic potential of anti-IL-6 therapies for granulocytic airway inflammation in asthma. Allergy Asthma Clin Immunol. 2015;11(1):14
45. Kamal AM, Smith SF, Wijayasinghe M, Solito E, Corrigan CJ. An annexin 1 (ANXA1)-derived peptide inhibits prototype antigen-driven human T cell Th1 and Th2 responses in vitro. Clin Exp Allergy. 2001;31(7):1116-1125
46. Ng FS, et al. Annexin-1-deficient mice exhibit spontaneous airway hyperresponsiveness and exacerbated allergen-specific antibody responses in a mouse model of asthma. Clin Exp Allergy. 2011;41(12):1793-1803
47. Oliver PM, et al. Ndfip1 protein promotes the function of itch ubiquitin ligase to prevent T cell activation and T helper 2 cell-mediated inflammation. Immunity. 2006;25(6):929-940
48. Fainaru O, et al. Runx3 regulates mouse TGFbeta-mediated dendritic cell function and its absence results in airway inflammation. EMBO J. 2004;23(4):969-979
49. Benarafa C, Priebe GP, Remold-O'Donnell E. The neutrophil serine protease inhibitor serpinb1 preserves lung defense functions in Pseudomonas aeruginosa infection. J Exp Med. 2007;204(8):1901-1909
50. Yao X, et al. Apolipoprotein E negatively regulates house dust mite-induced asthma via a low-density lipoprotein receptor-mediated pathway. Am J Respir Crit Care Med. 2010;182(10):1228-1238
51. Collins PD, Marleau S, Griffiths-Johnson DA, Jose PJ, Williams TJ. Cooperation between interleukin-5 and the chemokine eotaxin to induce eosinophil accumulation in vivo. J Exp Med. 1995;182(4):1169-1174
52. Kopf M, et al. 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. 1996;4(1):15-24
53. Furuta GT, Atkins FD, Lee NA, Lee JJ. Changing roles of eosinophils in health and disease. Ann Allergy Asthma Immunol. 2014;113(1):3-8
54. Yu C, et al. Targeted deletion of a high-affinity GATA-binding site in the GATA-1 promoter leads to selective loss of the eosinophil lineage in vivo. J Exp Med. 2002;195(11):1387-1395
55. Bedoret D, et al. Lung interstitial macrophages alter dendritic cell functions to prevent airway allergy in mice. J Clin Invest. 2009;119(12):3723-3738
56. DeKruyff RH, Yu S, Kim HY, Umetsu DT. Innate immunity in the lung regulates the development of asthma. Immunol Rev. 2014;260(1):235-248
57. Hammad H, Lambrecht BN. Barrier Epithelial Cells and the Control of Type 2 Immunity. Immunity. 2015;43(1):29-40
58. Lambrecht BN, Hammad H. The immunology of asthma. Nat Immunol. 2015;16(1):45-56
59. Jacobsen EA, et al. Eosinophil activities modulate the immune/inflammatory character of allergic respiratory responses in mice. Allergy. 2014;69(3):315-327
60. Fattouh R, et al. Eosinophils are dispensable for allergic remodeling and immunity in a model of house dust mite-induced airway disease. Am J Respir Crit Care Med. 2011;183(2):179-188
61. Barnig C, et al. Circulating Human Eosinophils Share a Similar Transcriptional Profile in Asthma and Other Hypereosinophilic Disorders. PLoS ONE. 2015;10(11):e0141740
62. Hitoshi Y, et al. Distribution of IL-5 receptor-positive B cells. Expression of IL-5 receptor on Ly-1(CD5)+ B cells. J Immunol. 1990;144(11):4218-4225
63. Miyajima A, Mui AL, Ogorochi T, Sakamaki K. Receptors for granulocyte-macrophage colony-stimulating factor, interleukin-3, and interleukin-5. Blood. 1993;82(7):1960-1974
64. Yoshida T, et al. Defective B-1 cell development and impaired immunity against Angiostrongylus cantonensis in IL-5R alpha-deficient mice. Immunity. 1996;4(5):483-494
65. Håkansson L, Venge P. Priming of eosinophil and neutrophil migratory responses by interleukin 3 and interleukin. APMIS. 1994;102(4):308-316
66. el-Cheikh MC, Borojevic R. Extramedullar proliferation of eosinophil granulocytes in chronic schistosomiasis mansoni is mediated by a factor secreted by inflammatory macrophages. Infect Immun. 1990;58(3):816-821
67. Lee JJ, et al. Human versus mouse eosinophils: "that which we call an eosinophil, by any other name would stain as red". J Allergy Clin Immunol. 2012;130(3):572-584
68. Barnes PJ. Immunology of asthma and chronic obstructive pulmonary disease. Nat Rev Immunol. 2008;8(3):183-192
69. The Jackson Laboratory. Hematological survey of 11 strains of mice. MPD:Jaxpheno4. Mouse Phenome Database web site. The Jackson Laboratory. http://http://phenome.jax.org/db/q?rtn=projects/ projdetandreqprojid=229. Accessed: June 23, 2016
70. Riches AC, Sharp JG, Thomas DB, Smith SV. Blood volume determination in the mouse. J Physiol (Lond). 1973;228(2):279-284
71. Bentley AM, et al. Identification of T lymphocytes, macrophages, and activated eosinophils in the bronchial mucosa in intrinsic asthma. Relationship to symptoms and bronchial responsiveness. Am Rev Respir Dis. 1992;146(2):500-506
72. Robinson DS, et al. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N Engl J Med. 1992;326(5):298-304
73. Horikawa K, Takatsu K. Interleukin-5 regulates genes involved in B-cell terminal maturation. Immunology. 2006;118(4):497-508
74. Foster PS, Hogan SP, Ramsay AJ, Matthaei KI, Young IG. Interleukin 5 deficiency abolishes eosinophilia, airways hyperreactivity, and lung damage in a mouse asthma model. J Exp Med. 1996;183(1):195-201
75. Flood-Page PT, Menzies-Gow AN, Kay AB, Robinson DS. Eosinophil's role remains uncertain as anti-interleukin-5 only partially depletes numbers in asthmatic airway. Am J Respir Crit Care Med. 2003;167(2):199-204
76. Conus S, Straumann A, Bettler E, Simon HU. Mepolizumab does not alter levels of eosinophils, T cells, and mast cells in the duodenal mucosa in eosinophilic esophagitis. J Allergy Clin Immunol. 2010;126(1):175-177
77. Kips JC, et al. Effect of SCH55700, a humanized anti-human interleukin-5 antibody, in severe persistent asthma: a pilot study. Am J Respir Crit Care Med. 2003;167(12):1655-1659
78. Leckie MJ, et al. Effects of an interleukin-5 blocking monoclonal antibody on eosinophils, airway hyper-responsiveness, and the late asthmatic response. Lancet. 2000;356(9248):2144-2148
79. Jacobsen EA, et al. Allergic pulmonary inflammation in mice is dependent on eosinophil-induced recruitment of effector T cells. J Exp Med. 2008;205(3):699-710
80. de Heer HJ, et al. Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J Exp Med. 2004;200(1):89-98
81. Haley KJ, et al. Immunolocalization of leukotriene C4 synthase in normal and asthmatic lung. Am J Respir Crit Care Med. 2000;161(3):A926
82. Kraft M, Martin RJ, Wilson S, Djukanovic R, Holgate ST. Lymphocyte and eosinophil influx into alveolar tissue in nocturnal asthma. Am J Respir Crit Care Med. 1999;159(1):228-234
83. Willetts L, et al. Immunodetection of occult eosinophils in lung tissue biopsies may help predict survival in acute lung injury. Respir Res. 2011;12:116