CSL311, a novel, potent, therapeutic monoclonal antibody for the treatment of diseases mediated by the common β chain of the IL-3, GM-CSF and IL-5 receptors

mAbs

Volumn 8, Issue 3, 2016, Pages 436-453

  Panousis, Con ^a,b   Dhagat, Urmi ^c   Edwards, Kirsten M ^a,b   Rayzman, Veronika ^a,b   Hardy, Matthew P ^a,b   Braley, Hal ^a,b   Gauvreau, Gail M ^d   Hercus, Timothy R ^e   Smith, Steven ^d   Sehmi, Roma ^d   McMillan, Laura ^a,b   Dottore, Mara ^e   McClure, Barbara J ^e   Fabri, Louis J ^a,b   Vairo, Gino ^a,b   Lopez, Angel F ^e   Parker, Michael W ^b,c   Nash, Andrew D ^a,b   Wilson, Nicholas J ^a,b   Wilson, Michael J ^a,b   Owczarek, Catherine M ^a,b   more..

^a CSL LIMITED   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d MCMASTER UNIVERSITY   (Canada)

^e UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

Affinity maturation; asthma; cytokine; eosinophil; GM CSF; IL 3; IL 5; myeloid; phage display; therapeutic antibody; common receptor

Indexed keywords

ALLERGEN; CD131 ANTIGEN; CD34 ANTIGEN; CELL SURFACE RECEPTOR; COMPLEMENTARY DNA; EPITOPE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 3; INTERLEUKIN 5 RECEPTOR; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CSL311; UNCLASSIFIED DRUG; ANTIGEN ANTIBODY COMPLEX; CSF2RB PROTEIN, HUMAN; IL3 PROTEIN, HUMAN; IL5 PROTEIN, HUMAN; INTERLEUKIN 5;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN BINDING; ARTICLE; ASTHMA; BINDING AFFINITY; BINDING SITE; BONE MARROW CELL; CELL CULTURE; CELL PROLIFERATION ASSAY; CELL SIGNALING ASSAY; CELL SURVIVAL; CONTROLLED STUDY; DRUG STRUCTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; EOSINOPHIL; EPITOPE MAPPING; HUMAN; HUMAN CELL; HYBRIDOMA; IN VITRO STUDY; INFLAMMATORY CELL; MOUSE; NEUTROPHIL; NONHUMAN; PHAGE DISPLAY; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PROTEIN PURIFICATION; SITE DIRECTED MUTAGENESIS; SIZE EXCLUSION CHROMATOGRAPHY; TRANSIENT TRANSFECTION; X RAY CRYSTALLOGRAPHY; ANIMAL; ANTAGONISTS AND INHIBITORS; ANTIGEN ANTIBODY COMPLEX; CHEMISTRY; IMMUNOLOGY; PATHOLOGY;

ANIMALS; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ANTIGEN-ANTIBODY COMPLEX; ASTHMA; CRYSTALLOGRAPHY, X-RAY; CYTOKINE RECEPTOR COMMON BETA SUBUNIT; EOSINOPHILS; EPITOPES; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; INTERLEUKIN-3; INTERLEUKIN-5; MICE;

EID: 84961566827     PISSN: 19420862     EISSN: 19420870     Source Type: Journal    
DOI: 10.1080/19420862.2015.1119352     Document Type: Article

References (93)

1. M.Martinez-Moczygemba, D.P.Huston. Biology of common β receptor-signaling cytokines: IL-3, IL-5, and GM-CSF. J Allergy Clin Immunol 2003; 112:653-65; PMID:14564341; http://dx.doi.org/10.1016/j.jaci.2003.08.015
2. E.Hamelmann, E.W.Gelfand. IL-5-induced airway eosinophilia–the key to asthma? Immunol Rev 2001; 179:182-91; PMID:11292022; http://dx.doi.org/10.1034/j.1600-065X.2001.790118.x
3. F.L.Dente, S.Carnevali, M.L.Bartoli, S.Cianchetti, E.Bacci, A.Di Franco, B.Vagaggini, P.Paggiaro. Profiles of proinflammatory cytokines in sputum from different groups of severe asthmatic patients. Ann Allergy Asthma Immunol 2006; 97:312-20; PMID:17042136; http://dx.doi.org/10.1016/S1081-1206(10)60795-8
4. N.N.Jarjour, S.C.Erzurum, E.R.Bleecker, W.J.Calhoun, M.Castro, S.A.Comhair, K.F.Chung, D.Curran-Everett, R.A.Dweik, S.B.Fain, et al. Severe asthma: lessons learned from the National Heart, Lung, and Blood Institute Severe Asthma Research Program. Am J Respir Crit Care Med 2012; 185:356-62; PMID:22095547; http://dx.doi.org/10.1164/rccm.201107-1317PP
5. M.J.Schuijs, M.A.Willart, H.Hammad, B.N.Lambrecht. Cytokine targets in airway inflammation. Curr Opin Pharmacol 2013; 13:351-61; PMID:23643194; http://dx.doi.org/10.1016/j.coph.2013.03.013
6. S.Saha, C.Doe, V.Mistry, S.Siddiqui, D.Parker, M.Sleeman, E.S.Cohen, C.E.Brightling. Granulocyte-macrophage colony-stimulating factor expression in induced sputum and bronchial mucosa in asthma and COPD. Thorax 2009; 64:671-6; PMID:19213775; http://dx.doi.org/10.1136/thx.2008.108290
7. A.Hoskins, J.L.Roberts, 2nd, G.Milne, L.Choi, R.Dworski. Natural-source d-α-tocopheryl acetate inhibits oxidant stress and modulates atopic asthma in humans in vivo. Allergy 2012; 67:676-82; PMID:22435735; http://dx.doi.org/10.1111/j.1398-9995.2012.02810.x
8. C.Walker, W.Bauer, R.K.Braun, G.Menz, P.Braun, F.Schwarz, T.T.Hansel, B.Villiger. Activated T cells and cytokines in bronchoalveolar lavages from patients with various lung diseases associated with eosinophilia. Am J Respir Crit Care Med 1994; 150:1038-48; PMID:7921434; http://dx.doi.org/10.1164/ajrccm.150.4.7921434
9. H.Z.Shi, C.Q.Xiao, D.Zhong, S.M.Qin, Y.Liu, G.R.Liang, H.Xu, Y.Q.Chen, X.M.Long, Z.F.Xie. Effect of inhaled interleukin-5 on airway hyperreactivity and eosinophilia in asthmatics. Am J Respir Crit Care Med 1998; 157:204-9; PMID:9445301; http://dx.doi.org/10.1164/ajrccm.157.1.9703027
10. J.Tavernier, J.Van der Heyden, A.Verhee, G.Brusselle, X.Van Ostade, J.Vandekerckhove, J.North, S.M.Rankin, A.B.Kay, D.S.Robinson. Interleukin 5 regulates the isoform expression of its own receptor α-subunit. Blood 2000; 95:1600-7; PMID:10688814
11. R.Sehmi, L.J.Wood, R.Watson, R.Foley, Q.Hamid, P.M.O'Byrne, J.A.Denburg. Allergen-induced increases in IL-5 receptor α-subunit expression on bone marrow-derived CD34+ cells from asthmatic subjects. A novel marker of progenitor cell commitment towards eosinophilic differentiation. J Clin Invest 1997; 100:2466-75; PMID:9366561; http://dx.doi.org/10.1172/JCI119789
12. T.R.Hercus, S.E.Broughton, P.G.Ekert, H.S.Ramshaw, M.Perugini, M.Grimbaldeston, J.M.Woodcock, D.Thomas, S.Pitson, T.Hughes, et al. The GM-CSF receptor family: Mechanism of activation and implications for disease. Growth Factors 2012; 30:63-75; PMID:22257375; http://dx.doi.org/10.3109/08977194.2011.649919
13. K.L.Asquith, H.S.Ramshaw, P.M.Hansbro, K.W.Beagley, A.F.Lopez, P.S.Foster. The IL-3/IL-5/GM-CSF common receptor plays a pivotal role in the regulation of Th2 immunity and allergic airway inflammation. J Immunol 2008; 180:1199-206; PMID:18178860; http://dx.doi.org/10.4049/jimmunol.180.2.1199
14. A.Trifilieff, Y.Fujitani, A.J.Coyle, M.Kopf, C.Bertrand. IL-5 deficiency abolishes aspects of airway remodelling in a murine model of lung inflammation. Clin Exp Allergy 2001; 31:934-42; PMID:11422160; http://dx.doi.org/10.1046/j.1365-2222.2001.01084.x
15. I.D.Pavord, S.Korn, P.Howarth, E.R.Bleecker, R.Buhl, O.N.Keene, H.Ortega, P.Chanez. Mepolizumab for severe eosinophilic asthma (DREAM): a multicentre, double-blind, placebo-controlled trial. Lancet 2012; 380:651-9; PMID:22901886; http://dx.doi.org/10.1016/S0140-6736(12)60988-X
16. A.Ghazi, A.Trikha, W.J.Calhoun. Benralizumab-a humanized mAb to IL-5Ralpha with enhanced antibody-dependent cell-mediated cytotoxicity-a novel approach for the treatment of asthma. Expert Opin Biol Ther 2012; 12:113-8; PMID:22136436; http://dx.doi.org/10.1517/14712598.2012.642359
17. G.M.Walsh. Profile of reslizumab in eosinophilic disease and its potential in the treatment of poorly controlled eosinophilic asthma. Biologics 2013; 7:7-11; PMID:23326187
18. J.A.Hamilton. GM-CSF as a target in inflammatory/autoimmune disease: current evidence and future therapeutic potential. Expert Rev Clin Immunol 2015; 11:457-65; PMID:25748625; http://dx.doi.org/10.1586/1744666X.2015.1024110
19. B.Hilvering, L.Xue, I.D.Pavord. Evidence for the efficacy and safety of anti-interleukin-5 treatment in the management of refractory eosinophilic asthma. Ther Adv Respir Dis 2015; 9:135-45; PMID:25900924; http://dx.doi.org/10.1177/1753465815581279
20. N.A.Molfino. Targeting of eosinophils in asthma. Expert Opin Biol Ther 2012; 12:807-9; PMID:22500988; http://dx.doi.org/10.1517/14712598.2012.674938
21. Kalobios Pharmaceuticals Inc. KaloBios Reports Top Line Data for Phase 2 Study of KB003 in Severe Asthma. Study Does Not Meet Primary Endpoint. Media release, January 29, 2014 2014:http://www.kalobios.com/.
22. H.G.Ortega, M.C.Liu, I.D.Pavord, G.G.Brusselle, J.M.FitzGerald, A.Chetta, M.Humbert, L.E.Katz, O.N.Keene, S.W.Yancey, et al. Mepolizumab treatment in patients with severe eosinophilic asthma. N Engl J Med 2014; 371:1198-207; PMID:25199059; http://dx.doi.org/10.1056/NEJMoa1403290
23. E.H.Bel, S.E.Wenzel, P.J.Thompson, C.M.Prazma, O.N.Keene, S.W.Yancey, H.G.Ortega, I.D.Pavord; SIRIUS Investigators. Oral glucocorticoid-sparing effect of mepolizumab in eosinophilic asthma. N Engl J Med 2014; 371:1189-97; PMID:25199060; http://dx.doi.org/10.1056/NEJMoa1403291
24. P.Nair. Anti-interleukin-5 monoclonal antibody to treat severe eosinophilic asthma. N Engl J Med 2014; 371:1249-51; PMID:25197762; http://dx.doi.org/10.1056/NEJMe1408614
25. Q.Sun, K.Jones, B.McClure, B.Cambareri, B.Zacharakis, P.O.Iversen, F.Stomski, J.M.Woodcock, C.J.Bagley, R.D'Andrea, et al. Simultaneous antagonism of interleukin-5, granulocyte-macrophage colony-stimulating factor, and interleukin-3 stimulation of human eosinophils by targetting the common cytokine binding site of their receptors. Blood 1999; 94:1943-51; PMID:10477723
26. M.E.Wechsler, P.C.Fulkerson, B.S.Bochner, G.M.Gauvreau, G.J.Gleich, T.Henkel, R.Kolbeck, S.K.Mathur, H.Ortega, J.Patel, et al. Novel targeted therapies for eosinophilic disorders. J Allergy Clin Immunol 2012; 130:563-71; PMID:22935585; http://dx.doi.org/10.1016/j.jaci.2012.07.027
27. G.Hansen, T.R.Hercus, B.J.McClure, F.C.Stomski, M.Dottore, J.Powell, H.Ramshaw, J.M.Woodcock, Y.Xu, M.Guthridge, et al. The structure of the GM-CSF receptor complex reveals a distinct mode of cytokine receptor activation. Cell 2008; 134:496-507; PMID:18692472; http://dx.doi.org/10.1016/j.cell.2008.05.053
28. T.Kitamura, T.Tange, T.Terasawa, S.Chiba, T.Kuwaki, K.Miyagawa, Y.F.Piao, K.Miyazono, A.Urabe, F.Takaku. Establishment and characterization of a unique human cell line that proliferates dependently on GM-CSF, IL-3, or erythropoietin. J Cell Physiol 1989; 140:323-34; PMID:2663885; http://dx.doi.org/10.1002/jcp.1041400219
29. S.Angal, D.J.King, M.W.Bodmer, A.Turner, A.D.Lawson, G.Roberts, B.Pedley, J.R.Adair. A single amino acid substitution abolishes the heterogeneity of chimeric mouse/human (IgG4) antibody. Mol Immunol 1993; 30:105-8; PMID:8417368; http://dx.doi.org/10.1016/0161-5890(93)90432-B
30. L.Sautina, Y.Sautin, E.Beem, Z.Zhou, A.Schuler, J.Brennan, S.I.Zharikov, Y.Diao, J.Bungert, M.S.Segal. Induction of nitric oxide by erythropoietin is mediated by the β common receptor and requires interaction with VEGF receptor 2. Blood 2010; 115:896-905; PMID:19965681; http://dx.doi.org/10.1182/blood-2009-04-216432
31. I.A.Wilson, R.L.Stanfield. Antibody-antigen interactions. Curr Op Struct Biol 1993; 3:113-8; http://dx.doi.org/10.1016/0959-440X(93)90210-C
32. A.F.Lopez, M.A.Vadas, J.M.Woodcock, S.E.Milton, A.Lewis, M.J.Elliott, D.Gillis, R.Ireland, E.Olwell, L.S.Park. Interleukin-5, interleukin-3, and granulocyte-macrophage colony-stimulating factor cross-compete for binding to cell surface receptors on human eosinophils. J Biol Chem 1991; 266:24741-7; PMID:1761568
33. T.R.Hercus, D.Thomas, M.A.Guthridge, P.G.Ekert, J.King-Scott, M.W.Parker, A.F.Lopez. The granulocyte-macrophage colony-stimulating factor receptor: linking its structure to cell signaling and its role in disease. Blood 2009; 114:1289-98; PMID:19436055; http://dx.doi.org/10.1182/blood-2008-12-164004
34. J.M.Murphy, S.C.Ford, U.M.Wiedemann, P.D.Carr, D.L.Ollis, I.G.Young. A novel functional epitope formed by domains 1 and 4 of the human common β-subunit is involved in receptor activation by granulocyte macrophage colony-stimulating factor and interleukin 5. J Biol Chem 2003; 278:10572-7; PMID:12525483; http://dx.doi.org/10.1074/jbc.M211664200
35. J.J.Scibek, E.Evergren, S.Zahn, G.A.Canziani, D.Van Ryk, I.M.Chaiken. Biosensor analysis of dynamics of interleukin 5 receptor subunit β(c) interaction with IL5:IL5R(α) complexes. Anal Biochem 2002; 307:258-65; PMID:12202242; http://dx.doi.org/10.1016/S0003-2697(02)00043-X
36. J.M.Murphy, S.C.Ford, J.E.Olsen, S.E.Gustin, P.D.Jeffrey, D.L.Ollis, I.G.Young. Interleukin-3 binding to the murine betaIL-3 and human betac receptors involves functional epitopes formed by domains 1 and 4 of different protein chains. J Biol Chem 2004; 279:26500-8; PMID:15060062; http://dx.doi.org/10.1074/jbc.M402705200
37. J.M.Woodcock, C.J.Bagley, B.Zacharakis, A.F.Lopez. A single tyrosine residue in the membrane-proximal domain of the granulocyte-macrophage colony-stimulating factor, interleukin (IL)-3, and IL-5 receptor common β-chain is necessary and sufficient for high affinity binding and signaling by all three ligands. J Biol Chem 1996; 271:25999-6006; PMID:8824238; http://dx.doi.org/10.1074/jbc.271.42.25999
38. P.Lock, D.Metcalf, N.A.Nicola. Histidine-367 of the human common β chain of the receptor is critical for high-affinity binding of human granulocyte-macrophage colony-stimulating factor. Proc Natl Acad Sci USA 1994; 91:252-6; PMID:8278375; http://dx.doi.org/10.1073/pnas.91.1.252
39. J.M.Woodcock, B.Zacharakis, G.Plaetinck, C.J.Bagley, S.Qiyu, T.R.Hercus, J.Tavernier, A.F.Lopez. Three residues in the common β chain of the human GM-CSF, IL-3 and IL-5 receptors are essential for GM-CSF and IL-5 but not IL-3 high affinity binding and interact with Glu21 of GM-CSF. EMBOJ 1994; 13:5176-85.
40. M.C.Lawrence, P.M.Colman. Shape complementarity at protein/protein interfaces. J Mol Biol 1993; 234:946-50; PMID:8263940; http://dx.doi.org/10.1006/jmbi.1993.1648
41. P.Haldar, C.E.Brightling, B.Hargadon, S.Gupta, W.Monteiro, A.Sousa, R.P.Marshall, P.Bradding, R.H.Green, A.J.Wardlaw, et al. Mepolizumab and exacerbations of refractory eosinophilic asthma. N Engl J Med 2009; 360:973-84; PMID:19264686; http://dx.doi.org/10.1056/NEJMoa0808991
42. P.Nair, M.M.Pizzichini, M.Kjarsgaard, M.D.Inman, A.Efthimiadis, E.Pizzichini, F.E.Hargreave, P.M.O'Byrne. Mepolizumab for prednisone-dependent asthma with sputum eosinophilia. N Engl J Med 2009; 360:985-93; PMID:19264687; http://dx.doi.org/10.1056/NEJMoa0805435
43. A.Lindemann, A.Ganser, F.Herrmann, J.Frisch, G.Seipelt, G.Schulz, D.Hoelzer, R.Mertelsmann. Biologic effects of recombinant human interleukin-3 in vivo. J Clin Oncol 1991; 9:2120-7; PMID:1960553
44. E.Nievergall, H.S.Ramshaw, A.S.Yong, M.Biondo, S.J.Busfield, G.Vairo, A.F.Lopez, T.P.Hughes, D.L.White, D.K.Hiwase. Monoclonal antibody targeting of IL-3 receptor α with CSL362 effectively depletes CML progenitor and stem cells. Blood 2014; 123:1218-28; PMID:24363400; http://dx.doi.org/10.1182/blood-2012-12-475194
45. G.R.Burmester, E.Feist, M.A.Sleeman, B.Wang, B.White, F.Magrini. Mavrilimumab, a human monoclonal antibody targeting GM-CSF receptor-α, in subjects with rheumatoid arthritis: a randomised, double-blind, placebo-controlled, phase I, first-in-human study. Ann Rheum Dis 2011; 70:1542-9; PMID:21613310; http://dx.doi.org/10.1136/ard.2010.146225
46. M.Koike, A.Furuya, K.Nakamura, A.Iida, H.Anazawa, N.Hanai, et al. Antibody against human interleukin-5-receptor α chain. United States: US patent 6,018,032, 1997.
47. Z.Diamant, G.M.Gauvreau, D.W.Cockcroft, L.P.Boulet, P.J.Sterk, F.H.de Jongh, B.Dahlén, P.M.O'Byrne. Inhaled allergen bronchoprovocation tests. J Allergy Clin Immunol 2013; 132:1045-55 e6; PMID:24119772; http://dx.doi.org/10.1016/j.jaci.2013.08.023
48. G.M.Gauvreau, A.K.Ellis, J.A.Denburg. Haemopoietic processes in allergic disease: eosinophil/basophil development. Clin Exp Allergy 2009; 39:1297-306; PMID:19622087; http://dx.doi.org/10.1111/j.1365-2222.2009.03325.x
49. J.Tavernier, R.Devos, S.Cornelis, T.Tuypens, J.Van der Heyden, W.Fiers, G.Plaetinck. A human high affinity interleukin-5 receptor (IL5R) is composed of an IL5-specific α chain and a β chain shared with the receptor for GM-CSF. Cell 1991; 66:1175-84; PMID:1833065; http://dx.doi.org/10.1016/0092-8674(91)90040-6
50. K.Hayashida, T.Kitamura, D.M.Gorman, K.Arai, T.Yokota, A.Miyajima. Molecular cloning of a second subunit of the receptor for human granulocyte-macrophage colony-stimulating factor (GM-CSF): reconstitution of a high-affinity GM-CSF receptor. Proc Natl Acad Sci USA 1990; 87:9655-9; PMID:1702217; http://dx.doi.org/10.1073/pnas.87.24.9655
51. T.Kitamura, K.Hayashida, K.Sakamaki, T.Yokota, K.Arai, A.Miyajima. Reconstitution of functional receptors for human granulocyte/macrophage colony-stimulating factor (GM-CSF): evidence that the protein encoded by the AIC2B cDNA is a subunit of the murine GM-CSF receptor. Proc Natl Acad Sci USA 1991; 88:5082-6; PMID:1828890; http://dx.doi.org/10.1073/pnas.88.12.5082
52. T.Kitamura, N.Sato, K.Arai, A.Miyajima. Expression cloning of the human IL-3 receptor cDNA reveals a shared β subunit for the human IL-3 and GM-CSF receptors. Cell 1991; 66:1165-74; PMID:1833064; http://dx.doi.org/10.1016/0092-8674(91)90039-2
53. T.Kitamura, A.Miyajima. Functional reconstitution of the human interleukin-3 receptor. Blood 1992; 80:84-90; PMID:1377056
54. H.Kankaanranta, M.A.Lindsay, M.A.Giembycz, X.Zhang, E.Moilanen, P.J.Barnes. Delayed eosinophil apoptosis in asthma. J Allergy Clin Immunol 2000; 106:77-83; PMID:10887309; http://dx.doi.org/10.1067/mai.2000.107038
55. W.C.Moore, A.M.Fitzpatrick, X.Li, A.T.Hastie, H.Li, D.A.Meyers, E.R.Bleecker. Clinical heterogeneity in the severe asthma research program. Ann Am Thorac Soc 2013; 10 Suppl:S118-24; PMID:24313761; http://dx.doi.org/10.1513/AnnalsATS.201309-307AW
56. R.Sehmi, A.J.Baatjes, J.A.Denburg. Hemopoietic progenitor cells and hemopoietic factors: potential targets for treatment of allergic inflammatory diseases. Curr Drug Targets Inflamm Allergy 2003; 2:271-8; PMID:14561146; http://dx.doi.org/10.2174/1568010033484007
57. A.Menzies-Gow, P.Flood-Page, R.Sehmi, J.Burman, Q.Hamid, D.S.Robinson, A.B.Kay, J.Denburg. Anti-IL-5 (mepolizumab) therapy induces bone marrow eosinophil maturational arrest and decreases eosinophil progenitors in the bronchial mucosa of atopic asthmatics. J Allergy Clin Immunol 2003; 111:714-9; PMID:12704348; http://dx.doi.org/10.1067/mai.2003.1382
58. L.Y.Liu, J.B.Sedgwick, M.E.Bates, R.F.Vrtis, J.E.Gern, H.Kita, N.N.Jarjour, W.W.Busse, E.A.Kelly. Decreased expression of membrane IL-5 receptor α on human eosinophils: II. IL-5 down-modulates its receptor via a proteinase-mediated process. J Immunol 2002; 169:6459-66; PMID:12444155; http://dx.doi.org/10.4049/jimmunol.169.11.6459
59. B.Gregory, A.Kirchem, S.Phipps, P.Gevaert, C.Pridgeon, S.M.Rankin, D.S.Robinson. Differential regulation of human eosinophil IL-3, IL-5, and GM-CSF receptor α-chain expression by cytokines: IL-3, IL-5, and GM-CSF down-regulate IL-5 receptor α expression with loss of IL-5 responsiveness, but up-regulate IL-3 receptor α expression. J Immunol 2003; 170:5359-66; PMID:12759409; http://dx.doi.org/10.4049/jimmunol.170.11.5359
60. P.T.Flood-Page, A.N.Menzies-Gow, A.B.Kay, D.S.Robinson. Eosinophil's role remains uncertain as anti-interleukin-5 only partially depletes numbers in asthmatic airway. Am J Respir Crit Care Med 2003; 167:199-204; PMID:12406833; http://dx.doi.org/10.1164/rccm.200208-789OC
61. T.K.Hart, R.M.Cook, P.Zia-Amirhosseini, E.Minthorn, T.S.Sellers, B.E.Maleeff, S.Eustis, L.W.Schwartz, P.Tsui, E.R.Appelbaum, et al. Preclinical efficacy and safety of mepolizumab (SB-240563), a humanized monoclonal antibody to IL-5, in cynomolgus monkeys. J Allergy Clin Immunol 2001; 108:250-7; PMID:11496242; http://dx.doi.org/10.1067/mai.2001.116576
62. P.C.Fulkerson, M.E.Rothenberg. Targeting eosinophils in allergy, inflammation and beyond. Nat Rev Drug Discov 2013; 12:117-29; PMID:23334207; http://dx.doi.org/10.1038/nrd3838
63. R.Kolbeck, A.Kozhich, M.Koike, L.Peng, C.K.Andersson, M.M.Damschroder, J.L.Reed, R.Woods, W.W.Dall'acqua, G.L.Stephens, et al. MEDI-563, a humanized anti-IL-5 receptor α mAb with enhanced antibody-dependent cell-mediated cytotoxicity function. J Allergy Clin Immunol 2010; 125:1344-53 e2; PMID:20513525; http://dx.doi.org/10.1016/j.jaci.2010.04.004
64. D.A.Smith, E.A.Minthorn, M.Beerahee. Pharmacokinetics and pharmacodynamics of mepolizumab, an anti-interleukin-5 monoclonal antibody. Clin Pharmacokinet 2011; 50:215-27; PMID:21348536; http://dx.doi.org/10.2165/11584340-000000000-00000
65. G.M.Gauvreau, R.Pageau, R.Seguin, D.Carballo, J.Gauthier, H.D'Anjou, H.Campbell, R.Watson, M.Mistry, M.Parry-Billings, et al. Dose-response effects of TPI ASM8 in asthmatics after allergen. Allergy 2011; 66:1242-8; PMID:21605124; http://dx.doi.org/10.1111/j.1398-9995.2011.02638.x
66. L.Robb, C.C.Drinkwater, D.Metcalf, R.Li, F.Kontgen, N.A.Nicola, C.G.Begley. Hematopoietic and lung abnormalities in mice with a null mutation of the common β subunit of the receptors for granulocyte-macrophage colony-stimulating factor and interleukins 3 and 5. Proc Natl Acad Sci USA 1995; 92:9565-9; PMID:7568173; http://dx.doi.org/10.1073/pnas.92.21.9565
67. T.R.Hercus, C.J.Bagley, B.Cambareri, M.Dottore, J.M.Woodcock, M.A.Vadas, M.F.Shannon, A.F.Lopez. Specific human granulocyte-macrophage colony-stimulating factor antagonists. Proc Natl Acad Sci USA 1994; 91:5838-42; PMID:8016076; http://dx.doi.org/10.1073/pnas.91.13.5838
68. T.R.Hercus, E.F.Barry, M.Dottore, B.J.McClure, A.I.Webb, A.F.Lopez, I.G.Young, J.M.Murphy. High yield production of a soluble human interleukin-3 variant from E. coli with wild-type bioactivity and improved radiolabeling properties. PLoS One 2013; 8:e74376; PMID:23991218; http://dx.doi.org/10.1371/journal.pone.0074376
69. R.R.Minter, E.S.Cohen, B.Wang, M.Liang, I.Vainshtein, G.Rees, L.Eghobamien, P.Harrison, D.A.Sims, C.Matthews, et al. Protein engineering and preclinical development of a GM-CSF receptor antibody for the treatment of rheumatoid arthritis. Br J Pharmacol 2013; 168:200-11.
70. M.Kozak. An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucl Acids Res 1987; 15:8125-48; PMID:3313277; http://dx.doi.org/10.1093/nar/15.20.8125
71. M.Koike, K.Nakamura, A.Furuya, A.Iida, H.Anazawa, K.Takatsu, N.Hanai. Establishment of humanized anti-interleukin-5 receptor α chain monoclonal antibodies having a potent neutralizing activity. Hum Antibodies 2009; 18:17-27; PMID:19478395
72. M.D.Spanevello, S.I.Tajouri, C.Mirciov, N.Kurniawan, M.J.Pearse, L.J.Fabri, C.M.Owczarek, M.P.Hardy, R.A.Bradford, M.L.Ramunno, et al. Acute delivery of EphA4-Fc improves functional recovery after contusive spinal cord injury in rats. J Neurotrauma 2013; 30:1023-34; PMID:23557244; http://dx.doi.org/10.1089/neu.2012.2729
73. U.Ritzen, J.Rotticci-Mulder, P.Stromberg, S.R.Schmidt. Endotoxin reduction in monoclonal antibody preparations using arginine. J Chromatogr B Analyt Technol Biomed Life Sci 2007; 856:343-7; PMID:17644450; http://dx.doi.org/10.1016/j.jchromb.2007.06.020
74. R.M.Hoet, E.H.Cohen, R.B.Kent, K.Rookey, S.Schoonbroodt, S.Hogan, L.Rem, N.Frans, M.Daukandt, H.Pieters, et al. Generation of high-affinity human antibodies by combining donor-derived and synthetic complementarity-determining-region diversity. Nature Biotechnol 2005; 23:344-8; http://dx.doi.org/10.1038/nbt1067
75. C.F.Barbas, 3rd, A.S.Kang, R.A.Lerner, S.J.Benkovic. Assembly of combinatorial antibody libraries on phage surfaces: the gene III site. Proc Natl Acad Sci USA 1991; 88:7978-82; PMID:1896445; http://dx.doi.org/10.1073/pnas.88.18.7978
76. T.Jostock, M.Vanhove, E.Brepoels, R.Van Gool, M.Daukandt, A.Wehnert, R.Van Hegelsom, D.Dransfield, D.Sexton, M.Devlin, et al. Rapid generation of functional human IgG antibodies derived from Fab-on-phage display libraries. J Immunol Methods 2004; 289:65-80; PMID:15251413; http://dx.doi.org/10.1016/j.jim.2004.03.014
77. S.S.Sidhu, H.B.Lowman, B.C.Cunningham, J.A.Wells. Phage display for selection of novel binding peptides. Methods Enzymol 2000; 328:333-63; PMID:11075354; http://dx.doi.org/10.1016/S0076-6879(00)28406-1
78. T.A.Kunkel, J.D.Roberts, R.A.Zakour. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol 1987; 154:367-82; PMID:3323813; http://dx.doi.org/10.1016/0076-6879(87)54085-X
79. T.M.McPhillips, S.E.McPhillips, H.J.Chiu, A.E.Cohen, A.M.Deacon, P.J.Ellis, E.Garman, A.Gonzalez, N.K.Sauter, R.P.Phizackerley, et al. Blu-Ice and the Distributed Control System: software for data acquisition and instrument control at macromolecular crystallography beamlines. J Synchrotron Radiat 2002; 9:401-6; PMID:12409628; http://dx.doi.org/10.1107/S0909049502015170
80. W.Kabsch. Xds. Acta Crystallogr D Biol Crystallogr 2010; 66:125-32; PMID:20124692; http://dx.doi.org/10.1107/S0907444909047337
81. P.R.Evans, G.N.Murshudov. How good are my data and what is the resolution? Acta Crystallogr D Biol Crystallogr 2013; 69:1204-14; PMID:23793146; http://dx.doi.org/10.1107/S0907444913000061
82. A.J.McCoy, R.W.Grosse-Kunstleve, P.D.Adams, M.D.Winn, L.C.Storoni, R.J.Read. Phaser crystallographic software. J Appl Crystallogr 2007; 40:658-74; PMID:19461840; http://dx.doi.org/10.1107/S0021889807021206
83. P.D.Carr, F.Conlan, S.Ford, D.L.Ollis, I.G.Young. An improved resolution structure of the human β common receptor involved in IL-3, IL-5 and GM-CSF signalling which gives better definition of the high-affinity binding epitope. Acta Crystallogr Sect F Struct Biol Cryst Commun 2006; 62:509-13; PMID:16754968; http://dx.doi.org/10.1107/S1744309106016812
84. H.Zhang, J.H.Liu, W.Yang, T.Springer, M.Shimaoka, J.H.Wang. Structural basis of activation-dependent binding of ligand-mimetic antibody AL-57 to integrin LFA-1. Proc Natl Acad Sci U S A 2009; 106:18345-50; PMID:19805116; http://dx.doi.org/10.1073/pnas.0909301106
85. Collaborative Computational Project N. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 1994; 50:760-3; PMID:15299374; http://dx.doi.org/10.1107/S0907444994003112
86. P.D.Adams, P.V.Afonine, G.Bunkoczi, V.B.Chen, I.W.Davis, N.Echols, J.J.Headd, L.W.Hung, G.J.Kapral, R.W.Grosse-Kunstleve, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 2010; 66:213-21; PMID:20124702; http://dx.doi.org/10.1107/S0907444909052925
87. P.Emsley, K.Cowtan. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 2004; 60:2126-32; PMID:15572765; http://dx.doi.org/10.1107/S0907444904019158
88. V.B.Chen, W.B.Arendall, 3rd, J.J.Headd, D.A.Keedy, R.M.Immormino, G.J.Kapral, L.W.Murray, J.S.Richardson, D.C.Richardson. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 2010; 66:12-21; PMID:20057044; http://dx.doi.org/10.1107/S0907444909042073
89. P.J.Munson, D.Rodbard. Ligand: a versatile computerized approach for characterization of ligand-binding systems. Anal Biochem 1980; 107:220-39; PMID:6254391; http://dx.doi.org/10.1016/0003-2697(80)90515-1
90. P.M.O'Byrne, J.Dolovich, F.E.Hargreave. Late asthmatic responses. Am Rev Resp Dis 1987; 136:740-51; PMID:3115156; http://dx.doi.org/10.1164/ajrccm/136.3.740
91. L.J.Wood, R.Sehmi, G.M.Gauvreau, R.M.Watson, R.Foley, J.A.Denburg, P.M.O'byrne. An inhaled corticosteroid, budesonide, reduces baseline but not allergen-induced increases in bone marrow inflammatory cell progenitors in asthmatic subjects. Am J Respir Crit Care Med 1999; 159:1457-63; PMID:10228111; http://dx.doi.org/10.1164/ajrccm.159.5.9808123
92. M.M.Cyr, A.J.Baatjes, S.C.Dorman, L.Crawford, R.Sehmi, R.Foley, R.Alam, P.O.Byrne, J.A.Denburg. In vitro effects of budesonide on eosinophil-basophil lineage commitment. Open Respir Med J 2008; 2:60-6; PMID:19343093; http://dx.doi.org/10.2174/1874306400802010060
93. DeLano, W.L. 2002. DeLano Scientific (San Carlos, CA, USA). http://pymol.sourceforge.net/.