IL-4 engagement of the type I IL-4 receptor complex enhances mouse eosinophil migration to eotaxin-1 in vitro

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Heller, Nicola M ^a   Gwinn, William M ^b   Donnelly, Raymond P ^c   Constant, Stephanie L ^b   Keegan, Achsah D ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR; EOTAXIN; INSULIN RECEPTOR SUBSTRATE 2; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR TYPE I; INTERLEUKIN 4 RECEPTOR TYPE II; STAT6 PROTEIN; TYROSINE;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL INFILTRATION; CELL ISOLATION; CELL MIGRATION; CHEMOTAXIS; CONTROLLED STUDY; EOSINOPHIL; GENETIC TRANSCRIPTION; LOEFFLER PNEUMONIA; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; CHEMOKINE CCL11; DNA PRIMERS; EOSINOPHILS; INTERLEUKIN-4; MICE; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, INTERLEUKIN-4; SIGNAL TRANSDUCTION;

EID: 84863004070     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039673     Document Type: Article

References (65)

1. Trivedi SG, Lloyd CM, (2007) Eosinophils in the pathogenesis of allergic airways disease. Cell Mol Life Sci 64: 1269-1289.
2. Hogan SP, Rosenberg HF, Moqbel R, Phipps S, Foster PS, et al. (2008) Eosinophils: biological properties and role in health and disease. Clin Exp Allergy 38: 709-750.
3. Foster PS, Rosenberg HF, Asquith KL, Kumar RK, (2008) Targeting eosinophils in asthma. Curr Mol Med 8: 585-590.
4. Klion AD, Nutman TB, (2004) The role of eosinophils in host defense against helminth parasites. J Allergy Clin Immunol 113: 30-37.
5. Anthony RM, Rutitzky LI, Urban JF Jr, Stadecker MJ, Gause WC, (2007) Protective immune mechanisms in helminth infection. Nat Rev Immunol 7: 975-987.
6. Ackerman SJ, Bochner BS, (2007) Mechanisms of eosinophilia in the pathogenesis of hypereosinophilic disorders. Immunol Allergy Clin North Am 27: 357-375.
7. Gessner A, Mohrs K, Mohrs M, (2005) Mast cells, basophils, and eosinophils acquire constitutive IL-4 and IL-13 transcripts during lineage differentiation that are sufficient for rapid cytokine production. J Immunol 174: 1063-1072.
8. Nakajima H, Takatsu K, (2007) Role of cytokines in allergic airway inflammation. Int Arch Allergy Immunol 142: 265-273.
9. Dubois GR, Schweizer RC, Versluis C, Bruijnzeel-Koomen CA, Bruijnzeel PL, (1998) Human eosinophils constitutively express a functional interleukin-4 receptor: interleukin-4-induced priming of chemotactic responses and induction of PI-3 kinase activity. Am J Respir Cell Mol Biol 19: 691-699.
10. Spencer LA, Melo RC, Perez SA, Bafford SP, Dvorak AM, et al. (2006) Cytokine receptor-mediated trafficking of preformed IL-4 in eosinophils identifies an innate immune mechanism of cytokine secretion. Proc Natl Acad Sci U S A 103: 3333-3338.
11. Kuperman DA, Schleimer RP, (2008) Interleukin-4, interleukin-13, signal transducer and activator of transcription factor 6, and allergic asthma. Curr Mol Med 8: 384-392.
12. Heller NM, Qi X, Junttila IS, Shirey KA, Vogel SN, et al. (2008) Type I IL-4Rs selectively activate IRS-2 to induce target gene expression in macrophages. Sci Signal 1: ra17.
13. Ramalingam TR, Pesce JT, Sheikh F, Cheever AW, Mentink-Kane MM, et al. (2008) Unique functions of the type II interleukin 4 receptor identified in mice lacking the interleukin 13 receptor alpha1 chain. Nat Immunol 9: 25-33.
14. Munitz A, Brandt EB, Mingler M, Finkelman FD, Rothenberg ME, (2008) Distinct roles for IL-13 and IL-4 via IL-13 receptor alpha1 and the type II IL-4 receptor in asthma pathogenesis. Proc Natl Acad Sci U S A 105: 7240-7245.
15. Kelly-Welch AE, Melo ME, Smith E, Ford AQ, Haudenschild C, et al. (2004) Complex role of the IL-4 receptor alpha in a murine model of airway inflammation: expression of the IL-4 receptor alpha on nonlymphoid cells of bone marrow origin contributes to severity of inflammation. J Immunol 172: 4545-4555.
16. Lee NA, McGarry MP, Larson KA, Horton MA, Kristensen AB, et al. (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.
17. Borchers MT, Ansay T, DeSalle R, Daugherty BL, Shen H, et al. (2002) In vitro assessment of chemokine receptor-ligand interactions mediating mouse eosinophil migration. J Leukoc Biol 71: 1033-1041.
18. Gwinn WM, Damsker JM, Falahati R, Okwumabua I, Kelly-Welch A, et al. (2006) Novel approach to inhibit asthma-mediated lung inflammation using anti-CD147 intervention. J Immunol 177: 4870-4879.
19. Malm-Erjefalt M, Stevens TR, Persson CG, Erjefalt JS, (2004) Discontinuous Percoll gradient centrifugation combined with immunomagnetic separation obviates the need for erythrocyte lysis and yields isolated eosinophils with minimal granule abnormalities. J Immunol Methods 288: 99-109.
20. Dyer KD, Moser JM, Czapiga M, Siegel SJ, Percopo CM, et al. (2008) Functionally competent eosinophils differentiated ex vivo in high purity from normal mouse bone marrow. J Immunol 181: 4004-4009.
21. Wang J, Homer RJ, Hong L, Cohn L, Lee CG, et al. (2000) IL-11 selectively inhibits aeroallergen-induced pulmonary eosinophilia and Th2 cytokine production. J Immunol 165: 2222-2231.
22. Hilton DJ, Zhang JG, Metcalf D, Alexander WS, Nicola NA, et al. (1996) Cloning and characterization of a binding subunit of the interleukin 13 receptor that is also a component of the interleukin 4 receptor. Proc Natl Acad Sci U S A 93: 497-501.
23. Myrtek D, Knoll M, Matthiesen T, Krause S, Lohrmann J, et al. (2004) Expression of interleukin-13 receptor alpha 1-subunit on peripheral blood eosinophils is regulated by cytokines. Immunology 112: 597-604.
24. Nelms K, Keegan AD, Zamorano J, Ryan JJ, Paul WE, (1999) The IL-4 receptor: signaling mechanisms and biologic functions. Annu Rev Immunol 17: 701-738.
25. Dubois GR, Bruijnzeel-Koomen CA, Bruijnzeel PL, (1994) IL-4 induces chemotaxis of blood eosinophils from atopic dermatitis patients, but not from normal individuals. J Invest Dermatol 102: 843-846.
26. Horie S, Okubo Y, Hossain M, Sato E, Nomura H, et al. (1997) Interleukin-13 but not interleukin-4 prolongs eosinophil survival and induces eosinophil chemotaxis. Intern Med 36: 179-185.
27. Moser R, Groscurth P, Carballido JM, Bruijnzeel PL, Blaser K, et al. (1993) Interleukin-4 induces tissue eosinophilia in mice: correlation with its in vitro capacity to stimulate the endothelial cell-dependent selective transmigration of human eosinophils. J Lab Clin Med 122: 567-575.
28. Bracke M, Coffer PJ, Lammers JW, Koenderman L, (1998) Analysis of signal transduction pathways regulating cytokine-mediated Fc receptor activation on human eosinophils. J Immunol 161: 6768-6774.
29. Kudlacz E, Whitney C, Andresenl C, Conklyn M, (2002) Functional effects of eotaxin are selectively upregulated on IL-5 transgenic mouse eosinophils. Inflammation 26: 111-119.
30. Coffer PJ, Schweizer RC, Dubois GR, Maikoe T, Lammers JW, et al. (1998) Analysis of signal transduction pathways in human eosinophils activated by chemoattractants and the T-helper 2-derived cytokines interleukin-4 and interleukin-5. Blood 91: 2547-2557.
31. Boehme SA, Sullivan SK, Crowe PD, Santos M, Conlon PJ, et al. (1999) Activation of mitogen-activated protein kinase regulates eotaxin-induced eosinophil migration. J Immunol 163: 1611-1618.
32. Kampen GT, Stafford S, Adachi T, Jinquan T, Quan S, et al. (2000) Eotaxin induces degranulation and chemotaxis of eosinophils through the activation of ERK2 and p38 mitogen-activated protein kinases. Blood 95: 1911-1917.
33. Dubois GR, Bruijnzeel PL, (1994) IL-4-induced migration of eosinophils in allergic inflammation. Ann N Y Acad Sci 725: 268-273.
34. Dulkys Y, Kluthe C, Buschermohle T, Barg I, Knoss S, et al. (2001) IL-3 induces down-regulation of CCR3 protein and mRNA in human eosinophils. J Immunol 167: 3443-3453.
35. Luttmann W, Matthiesen T, Matthys H, Virchow JC Jr, (1999) Synergistic effects of interleukin-4 or interleukin-13 and tumor necrosis factor-alpha on eosinophil activation in vitro. Am J Respir Cell Mol Biol 20: 474-480.
36. Justice JP, Borchers MT, Lee JJ, Rowan WH, Shibata Y, et al. (2002) Ragweed-induced expression of GATA-3, IL-4, and IL-5 by eosinophils in the lungs of allergic C57BL/6J mice. Am J Physiol Lung Cell Mol Physiol 282: L302-309.
37. Tomkinson A, Cieslewicz G, Duez C, Larson KA, Lee JJ, et al. (2001) Temporal association between airway hyperresponsiveness and airway eosinophilia in ovalbumin-sensitized mice. Am J Respir Crit Care Med 163: 721-730.
38. Simson L, Foster PS, (2000) Chemokine and cytokine cooperativity: eosinophil migration in the asthmatic response. Immunol Cell Biol 78: 415-422.
39. Walsh ER, August A, (2010) Eosinophils and allergic airway disease: there is more to the story. Trends Immunol 31: 39-44.
40. Spencer LA, Weller PF, (2010) Eosinophils and Th2 immunity: contemporary insights. Immunol Cell Biol 88: 250-256.
41. LaPorte SL, Juo ZS, Vaclavikova J, Colf LA, Qi X, et al. (2008) Molecular and structural basis of cytokine receptor pleiotropy in the interleukin-4/13 system. Cell 132: 259-272.
42. Andrews AL, Holloway JW, Holgate ST, Davies DE, (2006) IL-4 receptor alpha is an important modulator of IL-4 and IL-13 receptor binding: implications for the development of therapeutic targets. J Immunol 176: 7456-7461.
43. Junttila IS, Mizukami K, Dickensheets H, Meier-Schellersheim M, Yamane H, et al. (2008) Tuning sensitivity to IL-4 and IL-13: Differential expression of IL-4Rα, IL-13Rα1 and γc regulates relative cytokine sensitivity. Journal of Experimental Medicine 205(11): 2595-2608.
44. Khodoun M, Lewis CC, Yang JQ, Orekov T, Potter C, et al. (2007) Differences in expression, affinity, and function of soluble (s)IL-4Ralpha and sIL-13Ralpha2 suggest opposite effects on allergic responses. J Immunol 179: 6429-6438.
45. Thomas M, Edwards MJ, Sawicka E, Duggan N, Hirsch E, et al. (2009) Essential role of phosphoinositide 3-kinase gamma in eosinophil chemotaxis within acute pulmonary inflammation. Immunology 126: 413-422.
46. Pinho V, Souza DG, Barsante MM, Hamer FP, De Freitas MS, et al. (2005) Phosphoinositide-3 kinases critically regulate the recruitment and survival of eosinophils in vivo: importance for the resolution of allergic inflammation. J Leukoc Biol 77: 800-810.
47. Maghazachi AA, al-Aoukaty A, Schall TJ, (1994) C-C chemokines induce the chemotaxis of NK and IL-2-activated NK cells. Role for G proteins. J Immunol 153: 4969-4977.
48. Hirsch E, Katanaev VL, Garlanda C, Azzolino O, Pirola L, et al. (2000) Central role for G protein-coupled phosphoinositide 3-kinase gamma in inflammation. Science 287: 1049-1053.
49. Li Z, Jiang H, Xie W, Zhang Z, Smrcka AV, et al. (2000) Roles of PLC-beta2 and-beta3 and PI3Kgamma in chemoattractant-mediated signal transduction. Science 287: 1046-1049.
50. Sasaki T, Irie-Sasaki J, Jones RG, Oliveira-dos-Santos AJ, Stanford WL, et al. (2000) Function of PI3Kgamma in thymocyte development, T cell activation, and neutrophil migration. Science 287: 1040-1046.
51. Hasan AM, Mourtada-Maarabouni M, Hameed MS, Williams GT, Dent G, (2010) Phosphoinositide 3-kinase gamma mediates chemotactic responses of human eosinophils to platelet-activating factor. Int Immunopharmacol 10: 1017-1021.
52. Wang LM, Keegan AD, Paul WE, Heidaran MA, Gutkind JS, et al. (1992) IL-4 activates a distinct signal transduction cascade from IL-3 in factor-dependent myeloid cells. EMBO J 11: 4899-4908.
53. Sotsios Y, Whittaker GC, Westwick J, Ward SG, (1999) The CXC chemokine stromal cell-derived factor activates a Gi-coupled phosphoinositide 3-kinase in T lymphocytes. J Immunol 163: 5954-5963.
54. Tilton B, Andjelkovic M, Didichenko SA, Hemmings BA, Thelen M, (1997) G-Protein-coupled receptors and Fcgamma-receptors mediate activation of Akt/protein kinase B in human phagocytes. J Biol Chem 272: 28096-28101.
55. Murga C, Laguinge L, Wetzker R, Cuadrado A, Gutkind JS, (1998) Activation of Akt/protein kinase B by G protein-coupled receptors. A role for alpha and beta gamma subunits of heterotrimeric G proteins acting through phosphatidylinositol-3-OH kinasegamma. J Biol Chem 273: 19080-19085.
56. Thornhill MH, Haskard DO, (1990) IL-4 regulates endothelial cell activation by IL-1, tumor necrosis factor, or IFN-gamma. J Immunol 145: 865-872.
57. Schleimer RP, Sterbinsky SA, Kaiser J, Bickel CA, Klunk DA, et al. (1992) IL-4 induces adherence of human eosinophils and basophils but not neutrophils to endothelium. Association with expression of VCAM-1. J Immunol 148: 1086-1092.
58. Patel KD, (1998) Eosinophil tethering to interleukin-4-activated endothelial cells requires both P-selectin and vascular cell adhesion molecule-1. Blood 92: 3904-3911.
59. Davey EJ, Thyberg J, Conrad DH, Severinson E, (1998) Regulation of cell morphology in B lymphocytes by IL-4: evidence for induced cytoskeletal changes. J Immunol 160: 5366-5373.
60. Jay SM, Skokos E, Laiwalla F, Krady MM, Kyriakides TR, (2007) Foreign body giant cell formation is preceded by lamellipodia formation and can be attenuated by inhibition of Rac1 activation. Am J Pathol 171: 632-640.
61. Girard D, Paquin R, Beaulieu AD, (1997) Responsiveness of human neutrophils to interleukin-4: induction of cytoskeletal rearrangements, de novo protein synthesis and delay of apoptosis. Biochem J 325 (Pt 1): 147-153.
62. Davey EJ, Greicius G, Thyberg J, Severinson E, (2000) STAT6 is required for the regulation of IL-4-induced cytoskeletal events in B cells. Int Immunol 12: 995-1003.
63. Westerberg L, Greicius G, Snapper SB, Aspenstrom P, Severinson E, (2001) Cdc42, Rac1, and the Wiskott-Aldrich syndrome protein are involved in the cytoskeletal regulation of B lymphocytes. Blood 98: 1086-1094.
64. Welham MJ, Bone H, Levings M, Learmonth L, Wang LM, et al. (1997) Insulin receptor substrate-2 is the major 170-kDa protein phosphorylated on tyrosine in response to cytokines in murine lymphohemopoietic cells. J Biol Chem 272: 1377-1381.
65. Patti ME, Sun XJ, Bruening JC, Araki E, Lipes MA, et al. (1995) 4PS/insulin receptor substrate (IRS)-2 is the alternative substrate of the insulin receptor in IRS-1-deficient mice. J Biol Chem 270: 24670-24673.