Eosinophil-derived cytokines in health and disease: Unraveling novel mechanisms of selective secretion

Allergy: European Journal of Allergy and Clinical Immunology

Volumn 68, Issue 3, 2013, Pages 274-284

  Melo, R C N ^a,b   Liu, L ^b   Xenakis, J J ^b   Spencer, L A ^b  

^a FEDERAL UNIVERSITY OF JUIZ DE FORA   (Brazil)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

asthma; basic immunology; chemokines; eosinophils; innate immunity

Indexed keywords

CELL ADHESION MOLECULE; CHEMOKINE RECEPTOR CCR3; CXCL9 CHEMOKINE; CYTOKINE; CYTOKINE RECEPTOR; EOSINOPHIL DERIVED CYTOKINE; EOTAXIN; G PROTEIN COUPLED RECEPTOR; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GELATINASE B; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 13 RECEPTOR ALPHA1; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR ALPHA; INTERLEUKIN 5; INTERLEUKIN 6 RECEPTOR ALPHA; MACROPHAGE DERIVED CHEMOKINE; MAJOR BASIC PROTEIN; RANTES; SNARE PROTEIN; SYNAPTOBREVIN 2; THYMUS AND ACTIVATION REGULATED CHEMOKINE; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG;

CELL MIGRATION; CYTOKINE RELEASE; CYTOLYSIS; ENDOPLASMIC RETICULUM; EOSINOPHIL; EXOCYTOSIS; FLOW CYTOMETRY; HUMAN; IMMUNOELECTRON MICROSCOPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SECRETORY VESICLE; TH1 CELL; TH2 CELL; WESTERN BLOTTING;

CELL DEGRANULATION; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; EOSINOPHILS; HUMANS; IMMUNITY, INNATE; SECRETORY VESICLES; SIGNAL TRANSDUCTION;

EID: 84873702479     PISSN: 01054538     EISSN: 13989995     Source Type: Journal    
DOI: 10.1111/all.12103     Document Type: Review

References (91)

1. Voehringer D, Shinkai K, Locksley RM,. Type 2 immunity reflects orchestrated recruitment of cells committed to IL-4 production. Immunity 2004; 20: 267-277.
2. Sabin EA, Kopf MA, Pearce EJ,. Schistosoma mansoni egg-induced early IL-4 production is dependent upon IL-5 and eosinophils. J Exp Med 1996; 184: 1871-1878.
3. Voehringer D, Reese TA, Huang X, Shinkai K, Locksley RM,. Type 2 immunity is controlled by IL-4/IL-13 expression in hematopoietic non-eosinophil cells of the innate immune system. J Exp Med 2006; 203: 1435-1446.
4. 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.
5. 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.
6. Rose CE Jr, 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: 361-374.
7. Nouri-Aria KT, O'Brien F, Noble W, Jabcobson MR, Rajakulasingam K, Durham SR,. Cytokine expression during allergen-induced late nasal responses: IL-4 and IL-5 mRNA is expressed early (at 6 h) predominantly by eosinophils. Clin Exp Allergy 2000; 30: 1709-1716.
8. Spencer LA, Szela CT, Perez SA, Kirchhoffer CL, Neves JS, Radke AL, et al. Human eosinophils constitutively express multiple Th1, Th2, and immunoregulatory cytokines that are secreted rapidly and differentially. J Leukoc Biol 2009; 85: 117-123.
9. Woerly G, Roger N, Loiseau S, Capron M,. Expression of Th1 and Th2 immunoregulatory cytokines by human eosinophils. Int Arch Allergy Immunol 1999; 118: 95-97.
10. Woerly G, Roger N, Loiseau S, Dombrowicz D, Capron A, Capron M,. Expression of CD28 and CD86 by human eosinophils and role in the secretion of type 1 cytokines (interleukin 2 and interferon gamma): inhibition by immunoglobulin a complexes. J Exp Med 1999; 190: 487-495.
11. Todd R, Donoff BR, Chiang T, Chou MY, Elovic A, Gallagher GT, et al. The eosinophil as a cellular source of transforming growth factor alpha in healing cutaneous wounds. Am J Pathol 1991; 138: 1307-1313.
12. Aceves SS, Broide DH,. Airway fibrosis and angiogenesis due to eosinophil trafficking in chronic asthma. Curr Mol Med 2008; 8: 350-358.
13. Detoraki A, Granata F, Staibano S, Rossi FW, Marone G, Genovese A,. Angiogenesis and lymphangiogenesis in bronchial asthma. Allergy 2010; 65: 946-958.
14. Puxeddu I, Alian A, Piliponsky AM, Ribatti D, Panet A, Levi-Schaffer F,. Human peripheral blood eosinophils induce angiogenesis. Int J Biochem Cell Biol 2005; 37: 628-636.
15. Hoshino M, Takahashi M, Aoike N,. Expression of vascular endothelial growth factor, basic fibroblast growth factor, and angiogenin immunoreactivity in asthmatic airways and its relationship to angiogenesis. J Allergy Clin Immunol 2001; 107: 295-301.
16. Hoshino M, Nakamura Y, Hamid QA,. Gene expression of vascular endothelial growth factor and its receptors and angiogenesis in bronchial asthma. J Allergy Clin Immunol 2001; 107: 1034-1038.
17. Kay AB,. The role of eosinophils in the pathogenesis of asthma. Trends Mol Med 2005; 11: 148-152.
18. Minshall EM, Leung DY, Martin RJ, Song YL, Cameron L, Ernst P, et al. Eosinophil-associated TGF-beta1 mRNA expression and airways fibrosis in bronchial asthma. Am J Respir Cell Mol Biol 1997; 17: 326-333.
19. Gharaee-Kermani M, Phan SH,. Molecular mechanisms of and possible treatment strategies for idiopathic pulmonary fibrosis. Curr Pharm Des 2005; 11: 3943-3971.
20. Aceves SS, Newbury RO, Dohil R, Bastian JF, Broide DH,. Esophageal remodeling in pediatric eosinophilic esophagitis. J Allergy Clin Immunol 2007; 119: 206-212.
21. Varga J, Kahari VM,. Eosinophilia-myalgia syndrome, eosinophilic fasciitis, and related fibrosing disorders. Curr Opin Rheumatol 1997; 9: 562-570.
22. Bataller R, Brenner DA,. Liver fibrosis. J Clin Invest 2005; 115: 209-218.
23. Spry CJ,. The pathogenesis of endomyocardial fibrosis: the role of the eosinophil. Springer Semin Immunopathol 1989; 11: 471-477.
24. Jordan MB, Mills DM, Kappler J, Marrack P, Cambier JC,. Promotion of B cell immune responses via an alum-induced myeloid cell population. Science 2004; 304: 1808-1810.
25. 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.
26. 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: 151-159.
27. Wu D, Molofsky AB, Liang HE, Ricardo-Gonzalez RR, Jouihan HA, Bando JK, et al. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 2011; 332: 243-247.
28. Gouon-Evans V, Rothenberg ME, Pollard JW,. Postnatal mammary gland development requires macrophages and eosinophils. Development 2000; 127: 2269-2282.
29. Robertson SA, Mau VJ, Hudson SN, Tremellen KP,. Cytokine-leukocyte networks and the establishment of pregnancy. Am J Reprod Immunol 1997; 37: 438-442.
30. Dyer KD, Percopo CM, Xie Z, Yang Z, Kim JD, Davoine F, et al. Mouse and human eosinophils degranulate in response to platelet-activating factor (PAF) and lysoPAF via a PAF-receptor-independent mechanism: evidence for a novel receptor. J Immunol 2010; 184: 6327-6334.
31. Shamri R, Melo RCN, Young KM, Bivas-Benita M, Xenakis JJ, Spencer LA, et al. CCL11 elicits secretion of RNases from mouse eosinophils and their cell-free granules. FASEB J 2012; 26: 2084-2093.
32. Clark K, Simson L, Newcombe N, Koskinen AM, Mattes J, Lee NA, et al. Eosinophil degranulation in the allergic lung of mice primarily occurs in the airway lumen. J Leukoc Biol 2004; 75: 1001-1009.
33. Denzler KL, Borchers MT, Crosby JR, Cieslewicz G, Hines EM, Justice JP, et al. Extensive eosinophil degranulation and peroxidase-mediated oxidation of airway proteins do not occur in a mouse ovalbumin-challenge model of pulmonary inflammation. J Immunol 2001; 167: 1672-1682.
34. Malm-Erjefalt M, Persson CG, Erjefalt JS,. Degranulation status of airway tissue eosinophils in mouse models of allergic airway inflammation. Am J Respir Cell Mol Biol 2001; 24: 352-359.
35. Persson CG, Erjefalt JS,. Degranulation in eosinophils in human, but not in mouse, airways. Allergy 1999; 54: 1230-1232.
36. Bandeira-Melo C, Sugiyama K, Woods LJ, Weller PF,. Cutting edge: eotaxin elicits rapid vesicular transport-mediated release of preformed IL-4 from human eosinophils. J Immunol 2001; 166: 4813-4817.
37. Miyamasu M, Hirai K, Takahashi Y, Iida M, Yamaguchi M, Koshino T, et al. Chemotactic agonists induce cytokine generation in eosinophils. J Immunol 1995; 154: 1339-1349.
38. Abu-Ghazaleh RI, Fujisawa T, Mestecky J, Kyle RA, Gleich GJ,. IgA-induced eosinophil degranulation. J Immunol 1989; 142: 2393-2400.
39. Wong CK, Cheung PF, Ip WK, Lam CW,. Intracellular signaling mechanisms regulating toll-like receptor-mediated activation of eosinophils. Am J Respir Cell Mol Biol 2007; 37: 85-96.
40. Bruijnzeel PL, Rihs S, Virchow JC Jr, Warringa RA, Moser R, Walker C,. Early activation or "priming" of eosinophils in asthma. Schweiz Med Wochenschr 1992; 122: 298-301.
41. Bates ME, Green VL, Bertics PJ,. ERK1 and ERK2 activation by chemotactic factors in human eosinophils is interleukin 5-dependent and contributes to leukotriene C(4) biosynthesis. J Biol Chem 2000; 275: 10968-10975.
42. Pazdrak K, Young TW, Straub C, Stafford S, Kurosky A,. Priming of eosinophils by GM-CSF is mediated by protein kinase CbetaII-phosphorylated L-plastin. J Immunol 2011; 186: 6485-6496.
43. Yamashita N, Koizumi H, Murata M, Mano K, Ohta K,. Nuclear factor kappa B mediates interleukin-8 production in eosinophils. Int Arch Allergy Immunol 1999; 120: 230-236.
44. Liu LY, Bates ME, Jarjour NN, Busse WW, Bertics PJ, Kelly EA,. Generation of Th1 and Th2 chemokines by human eosinophils: evidence for a critical role of TNF-alpha. J Immunol 2007; 179: 4840-4848.
45. Kelly EA, Liu LY, Esnault S, Quinchia Johnson BH, Jarjour NN,. Potent synergistic effect of IL-3 and TNF on matrix metalloproteinase 9 generation by human eosinophils. Cytokine 2012; 58: 199-206.
46. Bandeira-Melo C, Sugiyama K, Woods LJ, Phoofolo M, Center DM, Cruikshank WW, et al. IL-16 promotes leukotriene C(4) and IL-4 release from human eosinophils via CD4- and autocrine CCR3-chemokine-mediated signaling. J Immunol 2002; 168: 4756-4763.
47. Kato M, Kimura H, Tachibana A, Motegi Y, Tokuyama K, Kita H, et al. Intracellular signaling pathways in human eosinophil activation: role of a beta2 integrin, alphaMbeta2. Int Arch Allergy Immunol 1999; 120 (Suppl 1): 51-53.
48. Pazdrak K, Young TW, Stafford S, Olszewska-Pazdrak B, Straub C, Starosta V, et al. Cross-talk between ICAM-1 and granulocyte-macrophage colony-stimulating factor receptor signaling modulates eosinophil survival and activation. J Immunol 2008; 180: 4182-4190.
49. Stanley AC, Lacy P,. Pathways for cytokine secretion. Physiology (Bethesda) 2010; 25: 218-229.
50. Shen ZJ, Esnault S, Malter JS,. The peptidyl-prolyl isomerase Pin1 regulates the stability of granulocyte-macrophage colony-stimulating factor mRNA in activated eosinophils. Nat Immunol 2005; 6: 1280-1287.
51. Shen ZJ, Esnault S, Rosenthal LA, Szakaly RJ, Sorkness RL, Westmark PR, et al. Pin1 regulates TGF-beta1 production by activated human and murine eosinophils and contributes to allergic lung fibrosis. J Clin Invest 2008; 118: 479-490.
52. McLaren DJ, Mackenzie CD, Ramalho-Pinto FJ,. Ultrastructural observations on the in vitro interaction between rat eosinophils and some parasitic helminths (Schistosoma mansoni, Trichinella spiralis and Nippostrongylus brasiliensis). Clin Exp Immunol 1977; 30: 105-118.
53. Dvorak HF, Dvorak AM,. Basophilic leucocytes: structure, function and role in disease. Clin Haematol 1975; 4: 651-683.
54. Melo RCN, Perez SA, Spencer LA, Dvorak AM, Weller PF,. Intragranular vesiculotubular compartments are involved in piecemeal degranulation by activated human eosinophils. Traffic 2005; 6: 866-879.
55. Melo RCN, Spencer LA, Dvorak AM, Weller PF,. Mechanisms of eosinophil secretion: large vesiculotubular carriers mediate transport and release of granule-derived cytokines and other proteins. J Leukoc Biol 2008; 83: 229-236.
56. Melo RCN, Spencer LA, Perez SA, Ghiran I, Dvorak AM, Weller PF,. Human eosinophils secrete preformed, granule-stored interleukin-4 through distinct vesicular compartments. Traffic 2005; 6: 1047-1057.
57. Lacy P, Logan MR, Bablitz B, Moqbel R,. Fusion protein vesicle-associated membrane protein 2 is implicated in IFN-gamma-induced piecemeal degranulation in human eosinophils from atopic individuals. J Allergy Clin Immunol 2001; 107: 671-678.
58. Logan MR, Lacy P, Odemuyiwa SO, Steward M, Davoine F, Kita H, et al. A critical role for vesicle-associated membrane protein-7 in exocytosis from human eosinophils and neutrophils. Allergy 2006; 61: 777-784.
59. Hoffmann HJ, Bjerke T, Karawajczyk M, Dahl R, Knepper MA, Nielsen S,. SNARE proteins are critical for regulated exocytosis of ECP from human eosinophils. Biochem Biophys Res Commun 2001; 282: 194-199.
60. Logan MR, Odemuyiwa SO, Moqbel R,. Understanding exocytosis in immune and inflammatory cells: the molecular basis of mediator secretion. J Allergy Clin Immunol 2003; 111: 923-932; quiz 933.
61. Melo RCN, Spencer LA, Perez SA, Neves JS, Bafford SP, Morgan ES, et al. Vesicle-mediated secretion of human eosinophil granule-derived major basic protein. Lab Invest 2009; 89: 769-781.
62. Feng D, Flaumenhaft R, Bandeira-Melo C, Weller P, Dvorak A,. Ultrastructural localization of vesicle-associated membrane protein(s) to specialized membrane structures in human pericytes, vascular smooth muscle cells, endothelial cells, neutrophils, and eosinophils. J Histochem Cytochem 2001; 49: 293-304.
63. Spencer LA, Melo RCN, 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.
64. Elbim C, Reglier H, Fay M, Delarche C, Andrieu V, El Benna J, et al. Intracellular pool of IL-10 receptors in specific granules of human neutrophils: differential mobilization by proinflammatory mediators. J Immunol 2001; 166: 5201-5207.
65. Price KS, Friend DS, Mellor EA, De Jesus N, Watts GF, Boyce JA,. CC chemokine receptor 3 mobilizes to the surface of human mast cells and potentiates immunoglobulin E-dependent generation of interleukin 13. Am J Respir Cell Mol Biol 2003; 28: 420-427.
66. Mortier E, Woo T, Advincula R, Gozalo S, Ma A,. IL-15Ralpha chaperones IL-15 to stable dendritic cell membrane complexes that activate NK cells via trans presentation. J Exp Med 2008; 205: 1213-1225.
67. Duitman EH, Orinska Z, Bulanova E, Paus R, Bulfone-Paus S,. How a cytokine is chaperoned through the secretory pathway by complexing with its own receptor: lessons from interleukin-15 (IL-15)/IL-15 receptor alpha. Mol Cell Biol 2008; 28: 4851-4861.
68. Lacy P,. The role of Rho GTPases and SNAREs in mediator release from granulocytes. Pharmacol Ther 2005; 107: 358-376.
69. Logan MR, Lacy P, Bablitz B, Moqbel R,. Expression of eosinophil target SNAREs as potential cognate receptors for vesicle-associated membrane protein-2 in exocytosis. J Allergy Clin Immunol 2002; 109: 299-306.
70. Straumann A, Kristl J, Conus S, Vassina E, Spichtin HP, Beglinger C, et al. Cytokine expression in healthy and inflamed mucosa: probing the role of eosinophils in the digestive tract. Inflamm Bowel Dis 2005; 11: 720-726.
71. Hingorani M, Calder V, Jolly G, Buckley RJ, Lightman SL,. Eosinophil surface antigen expression and cytokine production vary in different ocular allergic diseases. J Allergy Clin Immunol 1998; 102: 821-830.
72. Roth N, Stadler S, Lemann M, Hosli S, Simon HU, Simon D,. Distinct eosinophil cytokine expression patterns in skin diseases-the possible existence of functionally different eosinophil subpopulations. Allergy 2011; 66: 1477-1486.
73. Persson CG, Erjefalt JS,. Eosinophil lysis and free granules: an in vivo paradigm for cell activation and drug development. Trends Pharmacol Sci 1997; 18: 117-123.
74. Erjefalt JS, Andersson M, Greiff L, Korsgren M, Gizycki M, Jeffery PK, et al. Cytolysis and piecemeal degranulation as distinct modes of activation of airway mucosal eosinophils. J Allergy Clin Immunol 1998; 102: 286-294.
75. Uller L, Andersson M, Greiff L, Persson CG, Erjefalt JS,. Occurrence of apoptosis, secondary necrosis, and cytolysis in eosinophilic nasal polyps. Am J Respir Crit Care Med 2004; 170: 742-747.
76. Persson CG, Erjefalt JS,. "Ultimate activation" of eosinophils in vivo: lysis and release of clusters of free eosinophil granules (Cfegs). Thorax 1997; 52: 569-574.
77. Fukuda T, Ackerman SJ, Reed CE, Peters MS, Dunnette SL, Gleich GJ,. Calcium ionophore A23187 calcium-dependent cytolytic degranulation in human eosinophils. J Immunol 1985; 135: 1349-1356.
78. Cheng JF, Ott NL, Peterson EA, George TJ, Hukee MJ, Gleich GJ, et al. Dermal eosinophils in atopic dermatitis undergo cytolytic degeneration. J Allergy Clin Immunol 1997; 99: 683-692.
79. Watanabe K, Misu T, Inoue S, Edamatsu H,. Cytolysis of eosinophils in nasal secretions. Ann Otol Rhinol Laryngol 2003; 112: 169-173.
80. Greiff L, Erjefalt JS, Andersson M, Svensson C, Persson CG,. Generation of clusters of free eosinophil granules (Cfegs) in seasonal allergic rhinitis. Allergy 1998; 53: 200-203.
81. Ponikau JU, Sherris DA, Kephart GM, Kern EB, Congdon DJ, Adolphson CR, et al. Striking deposition of toxic eosinophil major basic protein in mucus: implications for chronic rhinosinusitis. J Allergy Clin Immunol 2005; 116: 362-369.
82. Toyoda M, Maruyama T, Morohashi M, Bhawan J,. Free eosinophil granules in urticaria: a correlation with the duration of wheals. Am J Dermatopathol 1996; 18: 49-57.
83. Gutierrez-Pena EJ, Knab J, Buttner DW,. Immunoelectron microscopic evidence for release of eosinophil granule matrix protein onto microfilariae of Onchocerca volvulus in the skin after exposure to amocarzine. Parasitol Res 1998; 84: 607-615.
84. Caruso RA, Ieni A, Fedele F, Zuccala V, Riccardo M, Parisi E, et al. Degranulation patterns of eosinophils in advanced gastric carcinoma: an electron microscopic study. Ultrastruct Pathol 2005; 29: 29-36.
85. Tajirian A, Ross R, Zeikus P, Robinson-Bostom L,. Subcutaneous fat necrosis of the newborn with eosinophilic granules. J Cutan Pathol 2007; 34: 588-590.
86. Neves JS, Weller PF,. Functional extracellular eosinophil granules: novel implications in eosinophil immunobiology. Curr Opin Immunol 2009; 21: 694-699.
87. Neves JS, Radke AL, Weller PF,. Cysteinyl leukotrienes acting via granule membrane expressed receptors elicit secretion from within cell-free human eosinophil granules. J. Allergy Clin. Immunol. 2010; 125: 477-482.
88. Neves JS, Perez SA, Spencer LA, Melo RCN, Reynolds L, Ghiran I, et al. Eosinophil granules function extracellularly as receptor-mediated secretory organelles. Proc Natl Acad Sci USA 2008; 105: 18478-18483.
89. Shamri R, Xenakis JJ, Spencer LA,. Eosinophils in innate immunity: an evolving story. Cell Tissue Res 2011; 343: 57-83.
90. Hogan SP, Rosenberg HF, Moqbel R, Phipps S, Foster PS, Lacy P, et al. Eosinophils: biological properties and role in health and disease. Clin Exp Allergy 2008; 38: 709-750.
91. Melo RCN, Dvorak AM, Weller PF,. Contributions of electron microscopy to understand secretion of immune mediators by human eosinophils. Microsc Microanal 2010; 16: 653-660.