Eosinophil activities modulate the immune/inflammatory character of allergic respiratory responses in mice

Allergy: European Journal of Allergy and Clinical Immunology

Volumn 69, Issue 3, 2014, Pages 315-327

  Jacobsen, E A ^a   LeSuer, W E ^a   Willetts, L ^a,b   Zellner, K R ^a   Mazzolini, K ^a   Antonios, N ^a   Beck, B ^a   Protheroe, C ^a   Ochkur, S I ^a   Colbert, D ^a   Lacy, P ^b   Moqbel, R ^c   Appleton, J ^d   Lee, N A ^a   Lee, J J ^a  

^a MAYO GRADUATE SCHOOL   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

^c UNIVERSITY OF MANITOBA   (Canada)

^d Department of Obstetrics Gynecology   (United States)

Author keywords

asthma; eosinophil deficient; neutrophil; steroid resistant

Indexed keywords

ASTHMA; EOSINOPHIL DEFICIENT; NEUTROPHIL; STEROID RESISTANT;

ALLERGENS; ANIMALS; ASTHMA; CYTOTOXICITY, IMMUNOLOGIC; DIPHTHERIA TOXIN; DISEASE MODELS, ANIMAL; DRUG RESISTANCE; EOSINOPHILS; GENE KNOCK-IN TECHNIQUES; GRANULOCYTE PRECURSOR CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; OVALBUMIN; PHENOTYPE; PNEUMONIA; RESPIRATORY HYPERSENSITIVITY; STEROIDS; TH2 CELLS;

EID: 84894278821     PISSN: 01054538     EISSN: 13989995     Source Type: Journal    
DOI: 10.1111/all.12321     Document Type: Article

References (41)

1. Gonem S, Desai D, Siddiqui S, Brightling CC,. Evidence for phenotype-driven treatment in asthmatic patients. Curr Opin Allergy Clin Immunol 2011; 11: 381-385.
2. Wenzel SE,. Asthma phenotypes: the evolution from clinical to molecular approaches. Nat Med 2012; 18: 716-725.
3. Lee JJ, Rosenberg HF, editors. Eosinophils in Health and Disease. Waltham: MA Elsevier, 2012.
4. Lee JJ, Dimina D, Macias MP, Ochkur SI, McGarry MP, O'Neill KR, et al. Defining a link with asthma in mice congenitally deficient in eosinophils. Science 2004; 305: 1773-1776.
5. Humbles AA, Lloyd CM, McMillan SJ, Friend DS, Xanthou G, McKenna EE, et al. A critical role for eosinophils in allergic airways remodeling. Science 2004; 305: 1776-1779.
6. Jacobsen EA, Ochkur SI, Pero RS, Taranova AG, Protheroe CA, Colbert DC, et al. Allergic pulmonary inflammation in mice is dependent on eosinophil-induced recruitment of effector T cells. J Exp Med 2008; 205: 699-710.
7. Walsh ER, Sahu N, Kearley J, Benjamin E, Kang BH, Humbles A, et al. Strain-specific requirement for eosinophils in the recruitment of T cells to the lung during the development of allergic asthma. J Exp Med 2008; 205: 1285-1292.
8. 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: 6059-6068.
9. Fattouh R, Al-Garawi A, Fattouh M, Arias K, Walker TD, Goncharova S, 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: 179-188.
10. Willis-Owen SA, Valdar W,. Deciphering gene-environment interactions through mouse models of allergic asthma. J Allergy Clin Immunol 2009; 123: 14-23
11. Ma BW, Bokulich NA, Castillo PA, Kananurak A, Underwood MA, Mills DA, et al. Routine habitat change: a source of unrecognized transient alteration of intestinal microbiota in laboratory mice. PLoS ONE 2012; 7: e47416.
12. Tulic MK, Sly PD, Andrews D, Crook M, Davoine F, Odemuyiwa SO, et al. Thymic indoleamine 2,3-dioxygenase-positive eosinophils in young children: potential role in maturation of the naive immune system. Am J Pathol 2009; 175: 2043-2052.
13. Chu VT, Frohlich A, Steinhauser G, Scheel T, Roch T, Fillatreau S, et al. Eosinophils are required for the maintenance of plasma cells in the bone marrow. Nat Immunol 2011; 12: 1512-1519.
14. Lee JJ, Jacobsen EA, McGarry MP, Schleimer RP, Lee NA,. Eosinophils in health and disease: the LIAR hypothesis. Clin Exp Allergy 2010; 40: 563-575.
15. Jacobsen EA, Helmers RA, Lee JJ, Lee NA,. The expanding role(s) of eosinophils in health and disease. Blood 2012; 120: 3882-3890.
16. Fahy JV,. Eosinophilic and neutrophilic inflammation in asthma: insights from clinical studies. Proc Am Thorac Soc 2009; 6: 256-259.
17. Denzler KL, Levin WJ, Lee JJ, Lee NA,. The murine eosinophil peroxidase gene (Epx) maps to chromosome 11. Mamm Genome 1997; 8: 381-382.
18. McGarry MP, Protheroe CA, Lee JJ,. Mouse Hematology. A Laboratory Manual with Accompanying CD of Training Videos and Poster of Mouse Peripheral Blood Cells, 1st edn. New York: Cold Spring Harbor Laboratory Press, 2010.
19. Doyle AD, Jacobsen EA, Ochkur SI, McGarry MP, Shim KG, Nguyen DTC, et al. Expression of the Secondary Granule Proteins Major Basic Protein (MBP)-1 and Eosinophil Peroxidase (EPX) is Required for Eosinophilopoiesis in Mice. Blood 2013; 122: 781-790.
20. Dyer KD, Moser JM, Czapiga M, Siegel SJ, Percopo CM, Rosenberg HF,. Functionally competent eosinophils differentiated ex vivo in high purity from normal mouse bone marrow. J Immunol 2008; 181: 4004-4009.
21. Lee NA, McGarry MP, Larson KA, Horton MA, Kristensen AB, Lee JJ,. Expression of IL-5 in thymocytes/T cells leads to the development of a massive eosinophilia, extramedullary eosinophilopoiesis, and unique histopathologies. J Immunol 1997; 158: 1332-1344.
22. Masterson JC, McNamee EN, Jedlicka P, Fillon S, Ruybal J, Hosford L, et al. CCR3 blockade attenuates eosinophilic ileitis and associated remodeling. Am J Pathol 2011; 179: 2302-2314.
23. Ochkur SI, Jacobsen EA, Protheroe CA, Biechele TL, Pero RS, McGarry MP, et al. Co-expression of IL-5 and eotaxin-2 in mice creates an eosinophil-dependent model of respiratory inflammation with characteristics of severe asthma. J Immunol 2007; 178: 7879-7889.
24. Ochkur SI, Protheroe CA, Li W, Colbert DC, Zellner KR, Shen H, et al. Cys-Leukotrienes Promote Fibrosis in a Mouse Model of Eosinophil-mediated Respiratory Inflammation. Am J Respir Cell Mol Biol 2013; 49: 1074-1084.
25. Buch T, Heppner FL, Tertilt C, Heinen TJ, Kremer M, Wunderlich FT, et al. A cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat Methods 2005; 2: 419-426.
26. Fulkerson PC, Rothenberg ME,. Targeting eosinophils in allergy, inflammation and beyond. Nat Rev Drug Discovery 2013; 12: 117-129.
27. Lambrecht BN, De Veerman M, Coyle AJ, Gutierrez-Ramos JC, Thielemans K, Pauwels RA,. Myeloid dendritic cells induce Th2 responses to inhaled antigen, leading to eosinophilic airway inflammation. J Clin Invest 2000; 106: 551-559.
28. McKee AS, Munks MW, MacLeod MK, Fleenor CJ, Van Rooijen N, Kappler JW, et al. Alum induces innate immune responses through macrophage and mast cell sensors, but these sensors are not required for alum to act as an adjuvant for specific immunity. J Immunol 2009; 183: 4403-4414.
29. Kool M, Soullie T, van Nimwegen M, Willart MA, Muskens F, Jung S, et al. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J Exp Med 2008; 205: 869-882.
30. Wang HB, Weller PF,. Pivotal advance: eosinophils mediate early alum adjuvant-elicited B cell priming and IgM production. J Leukoc Biol 2008; 83: 817-821.
31. Fulkerson PC, Fischetti CA, McBride ML, Hassman LM, Hogan SP, Rothenberg ME,. A central regulatory role for eosinophils and the eotaxin/CCR3 axis in chronic experimental allergic airway inflammation. Proc Natl Acad Sci USA 2006; 103: 16418-16423.
32. Hansen CH, Nielsen DS, Kverka M, Zakostelska Z, Klimesova K, Hudcovic T, et al. Patterns of early gut colonization shape future immune responses of the host. PLoS ONE 2012; 7: e34043.
33. Sczesnak A, Segata N, Qin X, Gevers D, Petrosino JF, Huttenhower C, et al. The genome of th17 cell-inducing segmented filamentous bacteria reveals extensive auxotrophy and adaptations to the intestinal environment. Cell Host Microbe 2011; 10: 260-272.
34. Herbst T, Sichelstiel A, Schar C, Yadava K, Burki K, Cahenzli J, et al. Dysregulation of allergic airway inflammation in the absence of microbial colonization. Am J Respir Crit Care Med 2011; 184: 198-205.
35. Isobe Y, Kato T, Arita M,. Emerging roles of eosinophils and eosinophil-derived lipid mediators in the resolution of inflammation. Front immunol 2012; 3: 270.
36. Justice JP, Borchers MT, Lee JJ, Rowan WH, Shibata Y, Scott MRV,. Ragweed-induced expression of GATA-3, IL-4, and IL-5 by eosinophils in the lungs of allergic C57BL/6 mice. Am J Physiol Lung Cell Mol Physiol 2002; 282: L302-L309.
37. Spencer LA, Melo RC, Perez SA, Bafford SP, Dvorak AM, Weller PF,. Cytokine receptor-mediated trafficking of preformed IL-4 in eosinophils identifies an innate immune mechanism of cytokine secretion. Proc Natl Acad Sci USA 2006; 103: 3333-3338.
38. Wang YH, Angkasekwinai P, Lu N, Voo KS, Arima K, Hanabuchi S, et al. IL-25 augments type 2 immune responses by enhancing the expansion and functions of TSLP-DC-activated Th2 memory cells. J Exp Med 2007; 204: 1837-1847.
39. McKinley L, Alcorn JF, Peterson A, Dupont RB, Kapadia S, Logar A, et al. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J Immunol 2008; 181: 4089-4097.
40. Lyakh L, Trinchieri G, Provezza L, Carra G, Gerosa F,. Regulation of interleukin-12/interleukin-23 production and the T-helper 17 response in humans. Immunol Rev 2008; 226: 112-131.
41. Wenzel SE,. Complex phenotypes in asthma: current definitions. Pulm Pharmacol Ther 2013; 26: 710-715.