Therapeutic strategies for harnessing human eosinophils in allergic inflammation, hypereosinophilic disorders, and cancer

Current Allergy and Asthma Reports

Volumn 12, Issue 5, 2012, Pages 402-412

  Amini Vaughan, Zhaleh J ^a   Martinez Moczygemba, Margarita ^a   Huston, David P ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

Allergic inflammation; Anti IL 5 antibodies; Anti IL 5R antibodies; Asthma; Cancer; Eosinophil; Eosinophilic syndromes; Hypereosinophilic disorders; IL 5 receptor (IL 5R); Interleukin 5 (IL 5); Therapeutic; Treatment

Indexed keywords

ANTIASTHMATIC AGENT; BENRALIZUMAB; CD18 ANTIGEN; CINQUIL; CORTICOSTEROID; EOTAXIN; INTERLEUKIN 5; INTERLEUKIN 5 RECEPTOR; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MATRIX METALLOPROTEINASE; MEPOLIZUMAB; PATTERN RECOGNITION RECEPTOR; PLACEBO; PREDNISONE; RANTES; RESLIZUMAB; SCLEROPROTEIN; TENASCIN; TPI ASM 8; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ALLERGIC ASTHMA; ALLERGY; ARTICLE; ASTHMA; ATOPIC DERMATITIS; BINDING AFFINITY; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL INFILTRATION; CELL SURVIVAL; CHRONIC OBSTRUCTIVE LUNG DISEASE; CHURG STRAUSS SYNDROME; COUGHING; CRYSTALLOGRAPHY; CYTOKINE PRODUCTION; CYTOTOXICITY; DEGRANULATION; DRUG ACTIVITY; DRUG DOSE COMPARISON; DRUG DOSE REDUCTION; DRUG EFFICACY; DRUG HALF LIFE; DRUG INDUCED HEADACHE; DRUG SAFETY; ENZYME DEGRADATION; EOSINOPHIL; EOSINOPHILIC ESOPHAGITIS; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; HOST PARASITE INTERACTION; HUMAN; HYPEREOSINOPHILIA; HYPEREOSINOPHILIC SYNDROME; IMMUNE RESPONSE; IMMUNOBIOLOGY; LOIASIS; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; NOSE OBSTRUCTION; NOSE POLYP; OUTCOME ASSESSMENT; PERISTALSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RESPIRATORY TRACT INFECTION; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; TH2 CELL;

ANTIBODIES, MONOCLONAL, HUMANIZED; ASTHMA; CHURG-STRAUSS SYNDROME; CLINICAL TRIALS AS TOPIC; CYTOTOXICITY, IMMUNOLOGIC; DERMATITIS, ATOPIC; EOSINOPHILS; HUMANS; HYPEREOSINOPHILIC SYNDROME; HYPERSENSITIVITY; INFLAMMATION; INTERLEUKIN-5; NASAL POLYPS; NEOPLASMS; PHOSPHOROTHIOATE OLIGONUCLEOTIDES; RECEPTORS, INTERLEUKIN-5;

EID: 84870482467     PISSN: 15297322     EISSN: 15346315     Source Type: Journal    
DOI: 10.1007/s11882-012-0290-3     Document Type: Article

References (99)

1. Rothenberg ME, Hogan SP. The eosinophil. Annu Rev Immunol. 2006;24:147-74.
2. Hogan SP, Rosenberg HF, Moqbel R, et al. Eosinophils: biological properties and role in health and disease. Clin Exp Allergy. 2008;38(5):709-50.
3. Blanchard C, Rothenberg ME. Biology of the eosinophil. Adv Immunol. 2009;101:81-121.
4. Shamri R, Xenakis JJ, Spencer LA. Eosinophils in innate immunity: an evolving story. Cell Tissue Res. 2011;343 (1):57-83.
5. Gleich GJ, Adolphson CR, Leiferman KM. The biology of the eosinophilic leukocyte. Annu Rev Med. 1993;44:85-101.
6. Arai KI, Lee F, Miyajima A, et al. Cytokines: coordinators of immune and inflammatory responses. Annu Rev Biochem. 1990;59:783-836.
7. Miyajima AT, Kitamura N, Harada T, Yokota T, Arai K. Cytokine receptors and signal transduction. Annu Rev Immunol. 1992;10:295-331.
8. Komiya A, Nagase H, Yamada H, et al. Concerted expression of eotaxin-1, eotaxin-2, and eotaxin-3 in human bronchial epithelial cells. Cell Immunol. 2003;225(2):91-100.
9. Amerio P, Frezzolini A, Feliciani C, et al. Eotaxins and CCR3 receptor in inflammatory and allergic skin diseases: therapeutical implications. Curr Drug Targets Inflamm Allergy. 2003;2 (1):81-94.
10. Halwani R, Al-Muhsen S, Al-Jahdali H, Hamid Q. Role of transforming growth factor-β in airway remodeling in asthma. Am J Respir Cell Mol Biol. 2011;44:127-33.
11. Moore B, Murphy RF, Agrawal DK. Interaction of tgf-beta with immune cells in airway disease. Curr Mol Med. 2008;8(5):427-36.
12. Klion AD, Nutman TB. The role of eosinophils in host defense against helminth parasites. J Allergy Clin Immunol. 2004;113(1):30-7.
13. Lotfi R, Lee JJ, Lotze MT. Eosinophilic granulocytes and damageassociated molecular pattern molecules (DAMPs): role in the inflammatory response within tumors. J Immunother. 2007;30:16-28.
14. Shin MH, Lee YA, Min DY. Eosinophil-mediated tissue inflammatory responses in helminth infection. Korean J Parasitol. 2009;47(Suppl):S125-31.
15. Kvarnhammar AM, Cardell LO. Pattern recognition receptors in human eosinophils. Immunology. 2012;136(1):11-20.
16. Cohn L, Elias JA, Chupp GL. Asthma: mechanisms of disease persistence and progression. Annu Rev Immunol. 2004;22:789-815.
17. Foster PS, Mould AW, Yang M, et al. Elemental Signals regulating eosinophil accumulation in the lung. Immunol Rev. 2001;179:173-81.
18. Lee JJ, Dimina D, Macias MP, et al. Defining a link with asthma in mice congenitally deficient in eosinophils. Science. 2004;305 (5691):1773-76.
19. Humbles AA, Lloyd CM, McMillan SJ, et al. A critical role for eosinophils in allergic airway remodeling. Science. 2004;305 (5691):1776-79.
20. Cho JY, Miller M, Baek KJ, et al. Inhibition of airway remodeling in IL-5-deficient mice. J Clin Invest. 2004;113:551-60.
21. Robinson DS, Hamid Q, Ying S, et al. Predominant TH2-like brochoalveolar T-lymphocyte population in atopic asthma. N Engl J Med. 1992;326:298-304.
22. Hamelmann E, Oshiba A, Loader J, et al. Antiinterleukin-5 antibody prevents airway hyperresponsiveness in a murine model of airway sensitization. Am J Respir Crit Care Med. 1997;155:819-25.
23. 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;183:195-201.
24. Lee JJ, McGarry MP, Farmer SC, et al. Interleukin-5 expression in the lung epithelium of transgenic mice leads to pulmonary changes pathognomonic of asthma. J Exp Med. 1997;185:2143-56.
25. Klion AD. Hypereosinophilic syndrome: current approach to diagnosis and treatment. Annu Rev Med. 2009;60:293-306.
26. Simon HU, Rothenberg ME, Bochner BS, et al. Refining the definition of hypereosinophilic syndrome. J Allergy Clin Immunol. 2010;126(1):45-9.
27. Valent P, Klion AD, Horny HP, et al. Contemporary consensus proposal on criteria and classification of eosinophilic disorders and related syndromes. J Allergy Clin Immunol. 2012;
28. Hogan SP, Rothenberg ME. Eosinophil function in eosinophilassociated gastrointestinal disorders. Curr Allergy Asthma Rep. 2006;6(1):65-71.
29. DeBrosse CW, Rothenberg ME. Allergy and eosinophil-associated gastrointestinal disorders (EGID). Curr Opin Immunol. 2008;20 (6):703-8.
30. Dellon ES. Eosinophilic esophagitis: diagnostic tests and criteria. Curr Opin Gastroenterol. 2012;28(4):382-8.
31. Mishra A, Hogan SP, Brandt EB, Rothenberg ME. An etiological role for aeroallergens and eosinophils in experimental esophagitis. J Clin Invest. 2001;107(1):83-90.
32. Pagnoux C, Guilpain P, Guillevin L. Churg-Strauss syndrome. Curr Opin Rheumatol. 2007;19(1):25-32.
33. Baldini C, Talarico R, Della Rossa A, Bombardieri S. Clinical manifestations and treatment of Churg-Strauss syndrome. Rheum Dis Clin North Am. 2010;36:527-43.
34. Blaiss MS. Expanding the evidence base for the medical treatment of nasal polyposis. J Allergy Clin Immunol. 2005;116:1272-4.
35. Palm NW, Rosenstein RK, Medzhitov R. Allergic host defences. Nature. 2012;484(7395):465-72.
36. Lee JJ, Jacobsen EA, McGarry MP, Schleimer RP, Lee NA. Eosinophils in health and disease: the LIAR hypothesis. Clin Exp Allergy. 2010;40(4):563-75.
37. Mattes J, Foster PS. Regulation of eosinophil migration and Th2 cell function by IL-5 and eotaxin. Curr Drug Targets Inflamm Allergy. 2003;2(2):169-74.
38. Bazan JF. Haemopoetic receptors and helical cytokines. Immunol Today. 1990;10:350-54.
39. Dickason RR, Huston MM, Huston DP. Delineation of IL-5 domains, predicted to engage the IL-5 receptor complex. J Immunol. 1996;156:1030-7.
40. Carr PD, Conlan F, Ford S, Ollis DL, Young IG. An improved resolution structure of the human β common receptor involved in IL-3, IL-5 and GM-CSF signaling which gives better definition of the high-affinity binding epitope. Acta Crystallogr F Struct Biol Crystallogr Commun. 2006;62 (6):509-13.
41. Patino E, Kotzsch A, Saremba S, et al. Structure analysis of the IL-5 ligand-receptor complex reveals a wrench-like architecture for IL-5Rα. Structure 2011, 19(12):1864-75.
42. Hansen G, Hercus TR, McClure BJ, et al. The structure of the GMCSF receptor complex reveals a distinct mode of cytokine receptor activation. Cell. 2008;134(3):496-507.
43. Kolbeck R, Kozhich A, Koike M, et al. MEDI-563, a humanized anti-IL-5 receptor α mAb with enhanced antibody-dependent cellmediated cytotoxicity function. J Allergy Clin Immunol. 2010;125 (6):1344-53.
44. Martinez-Moczygemba M, Huston DP. Biology of Common β receptor-signalling cytokine: IL-3, IL-5 and GM-CSF. J Allergy Clin Immunol. 2003;112:653-65.
45. Shardonofsky FR, Venzor 3rd J, Barrios R, et al. Therapeutic efficacy of an anti-IL-5 monoclonal antibody delivered into the respiratory tract in a murine model of asthma. J Allergy Clin Immunol. 1999;104:215-21.
46. Zhang JI, Kuvelkar R, Murgolo J, et al. Mapping and characterization of the epitopes of Sch 55700, a humanized mAb, that inhibits human IL-5. Int Immunol. 1999;11(12):1935-43.
47. Hart TK, Cook RM, Zia-Amirhosseini P, et al. Preclinical efficacy and safety of mepolizumab (SB-240563), a humanized monoclonal antibody to IL-5, in cynomolgus monkeys. J Allergy Clinical Immunol. 2001;108(2):250-7.
48. Egan RW, Athwahl D, Chou CC, et al. Pulmonary biology of anti-interleukin 5 antibodies. Mem Inst Oswaldo Cruz. 1997;92:69-73.
49. Flood-Page P, Swenson C, Faiferman I, et al. A study to evaluate safety and efficacy of mepolizumab in patients with moderate persistent asthma. Am J Respir Crit Care Med. 2007;176 (11):1062-71.
50. Leckie MJ, ten Brinke A, Khan J, et al. Effects of an interleukin-5 blocking monoclonal antibody on eosinophils, airway hyperresponsiveness, and the late asthmatic response. Lancet. 2000;356(9248):2144-8.
51. Nair P, Pizzichini MMM, Kjarsgaard M, et al. Mepolizumab for prednisone-dependent asthma with sputum eosinophilia. NEJM. 2009;360:985-93.
52. Haldar P, Brightling CE, Hargadon B, et al. Mepolizumab and exacerbations of refractory eosinophilic asthma. NEJM. 2009;360:973-84.
53. Gevaert P, Van Bruaene N, Cattaert T, et al. Mepolizumab, a humanized anti-IL-5 mAb, as a treatment option for severe nasal polyposis. J Allergy Clin Immunol. 2011;128(5):989-95.
54. Rothenberg ME, Klion AD, Roufosse FE, et al. Treatment of patients with the hypereosinophilic syndrome with mepolizumab. NEJM. 2008;358(12):1215-28.
55. Roufosse F, de Lavareille A, Schandené L, et al. Mepolizumab as a corticosteroid-sparing agent in lymphocytic variant hypereosinophilic syndrome. J Allergy Clin Immunol. 2010;126 (4):826-35.
56. Stein ML, Collins MH, Villanueva JM, et al. Anti-IL-5 (mepolizumab) therapy for eosinophilic esophagitis. J Allergy CLin Immunol. 2006;118(6):1312-9.
57. Straumann A, Conus S, Grzonka P, et al. Anti-interleukin-5 antibody treatment (mepolizumab) in active eosinophilic oesophagitis: a randomized, placebo-controlled, double-blind trial. Gut. 2010;59:21-30.
58. Assa'ad AH, Gupta SK, Collins MH, et al. An antibody against IL- 5 reduces numbers of esophageal intraepithelial eosinophils in children with eosinophilic esophagitis. Gastroenterology. 2011;141(5):1593-604.
59. Kahn JE, Grandpeix-Guyodo C, Marroun I, et al. Sustained response to mepolizumab in refractory Churg-Strauss syndrome. J Allergy Clin Immunol. 2010;125:267-70.
60. Kim S, Marigowda G, Oren E, Israel E, Wechsler M. Mepolizumab as a steroid-sparing treatment option in patients with Churg-Strauss syndrome. J Allergy Clin Immunol. 2010;125:1336-43.
61. Oldhoff JM, Darsow U, Werfel T, et al. Anti-IL-5 recombinant humanized monoclonal antibody (mepolizumab) for the treatment of atopic dermatitis. Allergy. 2005;60(5):693-6.
62. Oldhoff JM, Darsow U, Werfel T, et al. No effect of antiinterleukin-5 therapy (mepolizumab) on the atopy patch test in atopic dermatitis patients. Int Arch Allergy Immunol. 2006;141:290-4.
63. Kips JC, O'Conner BJ, Langley SJ, Woodcock A. Effect of SCH55700, a humanized anti-human interleukin-5 antibody, in severe persistent asthma: A pilot study. Am J Resp Crit Med. 2003;167(12):1655-59.
64. Castro M, Mathur S, Hargreave F, et al. Reslizumab for poorly controlled, eosinophilic asthma: A randomized, placebo controlled study. Am J Resp Crit Med. 2011;184:1125-32.
65. Klion AD, Law MA, Noel P, et al. Safety and efficacy of the monoclonal anti-interleukin-% antibody SCH55700 in the treatment of patients with hypereosinophilic syndrome. Blood. 2004;103:2939-41.
66. Spergel JM, Rothenberg ME, Collins MH, et al. Reslizumab in children and adolescents with eosinophilic esophagitis: Results of a double blind, randomized, placebo-controlled trial. J Allergy Clin Immunol. 2012;129(2):456-63.
67. NIAID. A randomized, placebo-controlled, double-blind pilot study of single-dose humanized anti-IL5 antibody (reslizumab) for the reduction of eosinophilia following diethylcarbamazine treatment of Loa Loa infection. In: ClinicalTrials.gov [Internet]. Bethesda (MD): National Library of Medicine (US). 2000- [cited 2012 May 17]. Available from: http://clinicaltrials.gov/ct2/show/ NCT01111305?term0reslizumab&rank09 NLM Identifier: NCT01111305.
68. Devos R, Guisez Y, Plaetinck G, et al. Covalent modification of the interleukin-5 receptor by isothiazolones leads to inhibition of the binding of interleukin-5. Eur J Biochem. 1994;225(2):635-40.
69. Busse WW, Katial R, Gossage D, et al. Safety profile, pharmacokinetics, and biologic activity of MEDI-563, and anti-IL-5 receptor alpha antibody, in a phase I study of subjects with mild asthma. J Allergy Clin Immunol. 2010;125:1237-44.
70. Gauvreau GM, Pageau R, Seguin R, et al. Dose-response effects of TPI ASM8 in asthmatics after allergen. Allergy. 2011;66:1242-8.
71. MedImmune LLC. A Study to Evaluate the Effectiveness of a Drug (MEDI-563) in Subjects With Chronic Obstructive Pulmonary Disease (COPD). In: ClinicalTrials.gov [Internet]. Bethesda (MD): National Library of Medicine (US). 2000- [cited 2012 May 17]. Available from: http://clinicaltrials.gov/ct2/show/ NCT01227278?term0MEDI-563&rank05 NLM Identifier: NCT01227278.
72. Asquith KL, Ramshaw HS, Hansbro PM, et al. The IL-3/IL-5/GMCSF common receptor plays a pivotal role in the regulation of Th2 immunity and allergic airway inflammation. J Immunol. 2008;180:1199-206.
73. Martinez-Moczygemba M, Huston DP. Immune dysregulation in the pathogenesis of pulmonary alveolar proteinosis. Cur Allergy Asthma Rep. 2010;10:320-5.
74. Dorta RG, Landman G, Kowalski LP, et al. Tumour-associated tissue eosinophilia as a prognostic factor in oral squamous cell carcinomas. Histopathology. 2002;41(2):152-7.
75. Pretlow TP, Keith EF, Cryar AK, et al. Eosinophil infiltration of human colonic carcinomas as a prognostic indicator. Cancer Res. 1983;43:2997-3000.
76. Goldsmith MM, Belchis DA, Cresson DH, Merritt WD III, Askin FB. The importance of the eosinophil in head and neck cancer. Otolaryngol Head Neck Surg. 1992;106:27-33.
77. Ownby HE, Roi LD, Isenberg RR, Brennan MJ. Peripheral lymphocyte and eosinophil counts as indicators of prognosis in primary breast cancer. Cancer. 1983;52:126-30.
78. Leighton SE, Teo JG, Leung SF, et al. Prevalence and prognostic significance of tumor-associated tissue eosinophilia in nasopharyngeal carcinoma. Cancer. 1996;77(3):436-40.
79. Fernandez-Acenero MJ, Galindo-Gallego M, Sanz J, Aljama A. Prognostic influence of tumor-associated eosinophilic infiltrate in colorectal carcinoma. Cancer. 2000;88:1544-8.
80. Iwasaki K, Torisu M, Fujimura T. Malignant tumor and eosinophils. I. Prognostic significance in gastric cancer. Cancer. 1986;58:1321-7.
81. van Driel WJ, Kievit-Tyson P, van den Broek, et al. Presence of an eosinophilic infiltrate in cervical squamous carcinoma results from a type 2 immune response. Gynecol Oncol. 1999;74:188-95.
82. Ishibashi S, Ohashi Y, Suzuki T, et al. Tumor-associated tissue eosinophilia in human esophageal squamous cell carcinoma. Anticancer Res. 2006;26:1419-24.
83. Wong DTW, Bowen SM, Elovic A, Gallagher GT, Weller PF. Eosinophil ablation and tumor development. Oral Oncol. 1999;35:496-501.
84. Gordon S, Martinez FO. Alternative activation of macrophages: mechanisms and functions. Nat Rev Immunol. 2003;3(1):23-5.
85. Sica A, Mantovani A. Macrophage diversity and polarization: in vivo veritas. J Am Soc Hemat. 2006;108(2):408-9.
86. Murdoch C, Muthana M, Coffelt SB, Lewis CE. The role of myeloid cells in tumour angiogenesis. Nature Rev Cancer. 2008;8:618-31.
87. Puxeddu I, Alian A, Piliponsky AM, et al. Human peripheral blood eosinophils induce angiogenesis. Int J Biochem Cell Biol. 2005;37:628-36.
88. Wong DT, Weller PF, Galli SJ, et al. Human eosinophils express transforming growth factor alpha. J Exp Med. 1990;172:673-81.
89. 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.
90. Kita H, Ohnishi T, Okubo Y, et al. Granulocyte/macrophage colony-stimulating factor and interleukin 3 release from human peripheral blood eosinophils and neutrophils. J Exp Med. 1991;174:745-8.
91. Ohno I, Ohtani H, Nitta Y, et al. Eosinophils as a source of matrix metalloproteinase-9 in asthmatic airway inflammation. Am J Respir Cell Mol Biol. 1997;16(3):212-9.
92. Mattes J, Hulett M, Xie W, et al. Immunotherapy of cytotoxic T cell resistant tumors by T helper 2 cells: an eotaxin and STAT 6-dependent process. J Exp Med. 2003;197:387-93.
93. Simson L, Ellyard JI, Dent LA, et al. Regulation of carcinogenesis by IL-5 and CCL11: a potential role for eosinophils in tumor surveillance. J Immunol. 2007;178(7):4222-9.
94. Cormier SA, Taranova AG, Bedient C, et al. Pivotal advance: eosinophil infiltration of solid tumors is an early and persistent inflammatory host response. J Leukoc Biol. 2006; 9:1131-9.
95. Legrand F, Driss V, Delbeke M, et al. Human Eosinophils exert TNFa and Granzyme A-mediated tumorcidal activity toward colon carcinoma cells. J Immunol. 2010;185(12):7443-51.
96. Wasserman SI, Goetzl EJ, Ellman L, Austen KF. Tumor associated eosinophilotactic factor. NEJM. 1974;290:420-4.
97. Cherry BW, Yoon J, Bartemes KR, Iijima K, Kita H. A novel IL-1 family cytokine, IL-33, potently activates human eosinophils. J Allergy Clin Immunol. 2008;121(6):1484.
98. Carlson M, Peterson C, Venge P. The influence of IL-3, IL-5, and GM-CSF on normal human eosinophil and neutrophil C3binduced degranulation. Allergy. 1993;48(6):437-42.
99. Pleass RJ, Lang ML, Kerr MA, Woof JM. IgA is a more potent inducer of NADPH oxidase activation and degranulation in blood eosinophils than IgE. Mol Immunol. 2007;44:1401-8.