Engineering of a functional interleukin-5 monomer: A paradigm for redesigning helical bundle cytokines with therapeutic potential in allergy and asthma

Journal of Molecular Medicine

Volumn 74, Issue 9, 1996, Pages 535-546

  Dickason, R R ^a   English, J D ^a   Huston, D P ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Allergy and asthma; Helical bundle proteins; Interleukin 5; Redesigning cytokines; Signal transduction

Indexed keywords

CYTOKINE; INTERLEUKIN 5; MITOGEN ACTIVATED PROTEIN KINASE; MONOCLONAL ANTIBODY; MONOMER; MUTANT PROTEIN; TYROSINE;

ALLERGY; ARTICLE; ASTHMA; CELL DIFFERENTIATION; CONTROLLED STUDY; DISULFIDE BOND; DRUG DESIGN; ERYTHROLEUKEMIA CELL; GENETIC ENGINEERING; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 0029793706     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF00204980     Document Type: Article

References (68)

1. Enokihara H, Furusawa S, Nakakubo H, Kajitani H, Nagashima S, Saito K, Shishido H, Hitoshi Y, Takatsu K, Noma T et al (1989) T cells from eosinophilic patients produce interleukin-5 with interleukin-2 stimulation. Blood 73:1809-1813
2. Schrezenmeier H, Thome S, Tewald F, Fleischer B, Raghavachar A (1993) Interleukin-5 is the predominant eosinophilopoietin produced by cloned T lymphocytes in hypereosinophilic syndrome. Exp Hematol 21:358-365
3. Dubucquoi S, Desreaumaux P, Janin A, Klein O, Goldman M, Tavernier J, Capron A, Capron M (1994) Interleukin 5 synthesis by eosinophils: Association with granules and immunoglobulin-dependent secretion. J Exp Med 179:703-708
4. Kay A, Hamid Q, Robinson D, Bentley A, Tsicopoulos A, Ying S, Moqbel R, Corrigan C, Durham S (1993) Asthma, eosinophils, and interleukin-5. In: Gleich, Kay (ed) Eosinophils in allergy and inflammation. Dekker, New York
5. Bradding P, Okayama Y, Howarth P, Church M, Holgate S (1995) Heterogeneity of human mast cells based on cytokine content. J Immunol 155:297-307
6. Bradding P, Roberts J, Britten K, Montefort S, Djukanovic R, Mueller R, Huesser C, Howarth P, Holgate S (1994) Interleukin-4, -5, -6 and tumour necrosis factor-alpha in normal and asthmatic airway: evidence for the human mast cell as a source of these cytokines. Am J Respir Cell Mol Biol 10:471-480
7. Dutton R, Wetzel G, Swain S (1984) Partial purification and characterization of a BCGFII from EL4 culture supernatants. J Immunol 132:2451-2456
8. Huston M, Moore J, Mettes H, Tavana G, Huston D (1996) Human B cells express IL-5 receptor mRNA and respond to IL-5 with enhanced IgM production after mitogenic stimulation with Moraxella catarrhalis. 156:1392-1401
9. Takatsu K, Kikuchi Y, Takahashi T, Honjo T, Matsumoto M, Harada N, Yamaguchi N, Tominaga A (1987) Interleukin 5, a T-cell-derived B-cell differentiation factor also induces cytoloxic T lymphocytes. Proc Natl Acad Sci USA 84:4234-4238
10. Bischoff S, Brunner T, De-Week A, Dahinden C (1990) Interleukin 5 modifies histamine release and leukotriene generation by human basophils in response to diverse agonists. J Exp Med 172:1577-1582
11. Hirai K, Yamaguchi M, Misaki Y, Takaishi T, Ohta K, Morita Y, Ito K, Miyamoto T (1990) Enhancement of human basophil histamine release by interleukin 5. J Exp Med 172:1525-1528
12. Campbell H, Tucker W, Hort Y, Martinson M, Mayo G, Clutterbuck E, Sanderson C, Young I (1987) Molecular cloning, nucleotide sequence, and expression of the gene encoding human eosinophil differentiation factor (interleukin-5). Proc Natl Acad Sci USA 84:6629-6633
13. Yamaguchi Y, Suda T, Ohta S, Tominaga K, Miura Y, Kasahara T (1991) Analysis of the survival of mature human eosinophils: interleukin-5 prevents apoptosis in mature human eosinophils. Blood 78:2542-2547
14. Yamaguchi Y, Hayashi Y, Sugama Y, Miura Y, Kasahara T, Kitamura S, Torisii M, Mita S, Tominaga A, Takatsu K (1988) Highly purified murine interleukin 5 (IL-5) stimulates eosinophil function and prolongs in vitro survival. IL-5 as an eosinophil chemotactic factor. J Exp Med 167:1737-1742
15. Walsh G, Hartnell A, Wardlaw A, Kurihara K, Sanderson C, Kay A (1990) IL-5 enhances the in vitro adhesion of human eosinophils, but not neutrophils, in a leucocyte integrin (CD11/18)-dependent manner. Immunol 71:258-265
16. Lopez A, Sanderson C, Gamble J, Campbell H, Young I, Vadas M (1988) Recombinant human interleukin 5 is a selective activator of human eosinophil function. J Exp Med 167:219-224
17. Fujisawa T, Abu-Ghazaleh R, Kita H, Sanderson C, Gleich G (1990) Regulatory effect of cytokines on eosinophil degranulation. J Immunol 144:642-646
18. Coffman R, Seymour B, Hudak S, Jackson J, Rennick D (1989) Antibody to interleukin-5 inhibits helminth-induced eosinophilia in mice. Science 245:308-310
19. Nakashima Y, Mita S, Takatsu K, Ogawa M (1993) Interleukin-5 induces tumor suppression by peritoneal exudate cells in mice. Cancer Immunol Immunother 37:227-232
20. Wu H, Hirai H, Inamori K, Kitamura K, Takaku F (1992) Anti-tumor effects of interleukin-4 and interleukin-5 against mouse B cell lymphoma and possible mechanisms of their action. Jpn J Cancer Res 83:200-210
21. Ying S, Durham S, Barkans J, Masuyama K, Jacobson M, Rak S, Lowhagen O, Moqbel R, Kay A, Hamid Q (1993) T cells are the principal source of interleukin-5 mRNA in allergen-induced rhinitis. Am J Respir Cell Mol Biol 9:356-360
22. Owen W, Rothenberg M, Petersen J, Weller P, Silberstein D, Sheffer A, Stevens R, Soberman R, Austen K (1989) Interleukin 5 and phenotypically altered eosinophils in the blood of patients with the idiopathic hypereosinophilic syndrome. J Exp Med 170:343-348
23. Kay A, Ying S, Varney V, Gaga M, Durham S, Moqbel R, Wardlaw A, Hamid Q (1991) Messenger RNA expression of the cytokine gene cluster, interleukin 3 (IL-3), IL-4, IL-5, and granulocyte/macrophage colony-stimulating factor, in allergen-induced late-phase cutaneous reactions in atopic subjects. J Exp Med 173:775-778
24. Bradding P, Feather I, Wilson S, Bardin P, Heusser C, Holgate S, Howarth P (1993) Immunolocalization of cytokines in the nasal mucosa of normal and perennial rhinitic subjects. The mast cell as a source of IL-4, IL-5, and IL-6 in human allergic mucosal inflammation. J Immunol 151:3853-3865
25. Bentley A, Meng Q, Robinson D, Hamid Q, Kay A, Durham S (1993) Increases in activated T lymphocytes, eosinophils, and cytokine mRNA expression for interleukin-5 and granulocyte/macrophage colony-stimulating factor in bronchial biopsies after allergen inhalation challenge in atopic asthmatics. Am J Respir Cell Mol Biol 8:35-42
26. Hamid Q, Azzawi M, Ying S, Moqbel R, Wardlaw A, Corrigan C, Bradley B, Durham S, Collins J, Jeffery P et al (1991) Expression of mRNA for interleukin-5 in mucosal bronchial biopsies from asthma. J Clin Invest 87:1541-1546
27. + T cell lines in atopic asthmatics and atopic and non-atopic controls. Eur J Immunol 25:2727-2731
28. Chand N, Harrison J, Rooney S, Pillar J, Jakubicki R, Nolan K, Diamantis W, Sofia R (1992) Anti-IL-5 monoclonal antibody inhibits allergic late phase bronchial eosinophilia in guinea pigs: a therapeutic approach. Eur J Pharmacol 211:121-123
29. Mauser P, Pitman A, Witt A, Fernandez X, Zurcher J, Kung T, Jones H, Watnick A, Egan R, Kreutner W (1993) Inhibitory effect of the TRFK-5 anti-IL-5 antibody in a guinea pig model of asthma. Am Rev Respir Dis 148:1623-1627
30. Mauser P, Pitman A, Fernandez X, Foran S, Adams III G, Kreutner W, Egan R, Chapman R (1995) Effects of an antibody to IL-5 in a monkey model of asthma. Am J Respir Crit Care Med 152:467-472
31. Nagai H, Yamaguchi S, Inagaki N, Tsuruoka N, Hitoshi Y, Takatsu K (1993) Effect of anti-IL-5 monoclonal antibody on allergic bronchial eosinophilia and airway hyperresponsiveness in mice. Life Sci 53:PL243-PL247
32. Kung T, Stelts D, Zurcher J, Adams G, Egan R, Kreutner W, Watnick A, Jones H, Chapman R (1995). Involvement of IL-5 in a murine model of allergic pulmonary inflammation: prophylactic and therapeutic effect of an anti-IL-5 antibody. Am J Respir Cell Mol Biol 13:360-365
33. Van Oosterhout A, Van Ark I, Folkerts G, Van der Linde H, Savelkoul H, Verheyen K, Nijkamp F (1995) Antibody to interleukin-5 inhibits virus-induced airway hyperresponsiveness to histamine in guinea pigs. Am J Respir Crit Care Med 151:177-183
34. Foster P, Hogan S, Ramsay A, Matthaei K, Young I (1996) Interleukin 5 deficiency abolishes eosinophilia, airways hyperreactivity, and lung damaae in a mouse asthma model. J Exp Med 183:195-201
35. Milburn M, Hassell A., Lambert M, Jordan S, Proudfoot A, Graber P, Wells T (1993) A novel dimer configuration revealed by the crystal structure at 2.4 A resolution of human interleukin-5. Nature 363:172-176
36. Rozwarski D, Gronenborn A, Clore G, Bazan J, Bohm A, Wlodawer A, Hatada M, Karplus P (1994) Structural comparison among the short-chain helical cytokines. Structure 2:159-173
37. Mita S, Tominaga A, Hitoshi Y, Sakamoto K, Honjo T, Akagi M, Kikuchi Y, Yamaguchi N, Takatsu K (1989) Characterization of high-affinity receptors for interleukin 5 on interleukin 5-dependent cell lines. Proc Natl Acad Sci USA 86:2311-2315
38. Tavernier J, Devos R, Cornelis S, Tuypens T, Van-der-Heyden J, Fiers W, Plaetinck G (1991) A human high affinity interleukin-5 receptor (IL5R) is composed of an IL5-specific alpha chain and a beta chain shared with the receptor for GM-CSF. Cell 66:1175-1184
39. Johanson K, Appelbaum E, Doyle M, Hensley P, Zhao B, Abdel-Meguid S, Yonne P, Cook R, Carr S, Matico R, Cusimano D, Dul E, Angelichio M, Brooks I, Winborne E, McDonnell P, Morton T, Bennett D, Sokoloski T, McNulty D, Rosenberg M, Chaiken I (1995) Binding interactions of human interleukin 5 with its receptor alpha subunit. J Biol Chem 270:9459-9471
40. Devos R, Guisez Y, Cornelis S, Verhee A, Van-der-Heyden J, Manneberg M, Lahm H, Fiers W, Tavernier J, Plaetinck G (1993) Recombinant soluble human interleukin-5 (hIL-5) receptor molecules. Cross-linking and stoichiometry of binding to IL-5. J Biol Chem 268:6581-6587
41. Dickason R, Huston D (1996) Creation of a functional interleukin-5 monomer. Nature 379:652-655
42. Dickason R, Huston M, Huston D (1996) Delineation of IL-5 domains predicted to engage the IL-5 receptor complex. J Immunol 156:1030-1037
43. Cornelis S, Plaetinck G, Devos R, Van der Heyden J, Tavernier J, Sanderson C, Guisez Y, Fiers W (1995) Detailed analysis of the IL-5-IL-5R alpha interaction characterization of crucial residues on the ligand and the receptor. EMBO J 14:3395-3402
44. Graber P, Proudfoot A, Talabot R, Bernard A, McKinnon M, Banks M, Fattah D, Solari R, Peitsch M, Wells T (1995) Identification of key charged residues of human interleukin-5 in receptor binding and cellular activitation. J Biol Chem 270:15762-15769
45. Tavernier J, Tuypens T, Verhee A, Plaetinck G, Devos R, Van der Heyden J, Guisez Y, Oefner C (1995) Identication of receptor-binding domains on human interleukin 5 and design of an interleukin 5-derived receptor antagonist. Proc Natl Acad Sci USA 92:5194-5198
46. Morton T, Li J, Cook R, Chaiken I (1995) Mutagenesis in the C-terminal region of human interleukin-5 reveals a central patch for receptor alpha chain recognition. Proc Natl Acad Sci USA 92:10879-10883
47. Li J, Cook R, Dede K, Chaiken I (1996) Single chain human interleukin 5 and its asymmetric mutagenesis for mapping receptor binding sites. J Biol Chem 271:1817-1820
48. Kitamura T, Tange T, Terasawa T, Chiba S, Kuwaki K, Miyagawa K, Piao Y, Miyazano K, Urabe A, Takaku F (1989) Establishment and characterization of a unique human cell line that proliferates dependently on GM-CSF, IL-3, or erythropoietin. J Cell Physiol 140:323-334
49. Dickason R, Huston M, Huston D (1994) Enhanced detection of human IL-5 in biological fluids utilizing murine monoclonal antibodies which delineate distinct neutralizing epitopes. Cytokine 6:647-656
50. Murata Y, Yamaguchi N, Hitoshi Y, Tominaga A, Takatsu K (1990) Interleukin 5 and interleukin 3 induce serine and tyrosine phosphorylations of several cellular proteins in an interleukin 5-dependent cell line. Biochem Biophys Res Commun 173:1102-1108
51. Takaki S, Kanazawa H, Shiiba M, Takatsu K (1994) A critical cytoplasmic domain of the interleukin-5 (IL-5) receptor alpha chain and its function in IL-5-mediated growth signal transduction. Mol Cell Biol 14:7404-7413
52. Sato S, Katagiri T, Takaki S, Kikuchi Y, Hitoshi Y, Yonehara S, Tsukadu S, Kitamura D, Watanabe T, Witte O, Takatsu K (1994) IL-5 receptor-mediated tyrosine phosphorylation of SH2/SH3-containing proteins and activation of Bruton's tyrosine and Janus 2 kinases. J Exp Med 180:2101-2111
53. Sakamaki K, Miyajima I, Kitamura T, Miyajima A (1992) Critical cytoplasmic domains of the common beta subunit of the human GM-CSF, IL-3 and IL-5 receptors for growth signal transduction and tyrosine phosphorylation. EMBO J 11:3541-3549
54. Van der Brugger T, Caldenhover E, Kanters D, Coffer P, Raaijimakers J, Lammers J, Koenderman L (1995) IL-5 signaling in human eosinophils involves JAK2 tyrosine kinase and Stat1a. Blood 85:1442-1448
55. Pazdrak K, Stafford S, Alam R (1995) The activation of the Jak-STAT1 signaling pathway by IL-5 in eosinophils. J Immunol 155:397-402
56. Sato N, Sakamaki K, Terada N, Arai K, Miyajima A (1993) Signal transduction by the high-affinity GM-CSF receptor: two distinct cytoplasmic regions of the common β subunit responsible for different signaling. EMBO J 12:4181-4189
57. Bates M, Bertics P, Busse W (1996) IL-5 activates a 45-kilodalton mitogen-activated protein (MAP) kinase and Jak-2 tyrosine kinase in human eosinophils. J Immunol 156:711-718
58. McKenzie A, Ely B, Sanderson C (1991) Mutated interleukin-5 monomers are biologically inactive. Mol Immunol 28:155-158
59. Windsor W, Syto R, Tsarbopoulos A, Zhang R, Durkin J, Baldwin S, Paliwal S, Mui P, Pramanik B, Trotta P et al (1993) Disulfide bond assignments and secondary structure analysis of human and murine interleukin 10. Biochem 32:8807-8815
60. Halick S, Cook W, Vijay-Kumar S, Carson M, Nagabhushan T, Trotta P, Bugg C (1991) Three-dimensional structure of recombinant human interferon-gamma. Science 252:698-702
61. Mita S, Takaki S, Tominage A, Takatsu K (1993) Comparative analysis of kinetics of binding and internalization of IL-5 murine IL-5 receptor of high and low affinity. J Immunol 151:6924-6932
62. Zdanov A, Schalk-Hili C, Gustchina A, Tsang M, Weatherbee J, Wlodawer A (1995) Crystal structure of interleukin-10 reveals the functional dimer with an unexpected topological similarity to interferon gamma. Structure 3:591-601
63. Fountoulakis M, Zulauf M, Lustig A, Garotta G (1992) Stoichiometry of interaction between interferon gamma and its receptor. Eur J Biochem 208:781-787
64. Tan J, Indelicato S, Narula S, Zavodny P, Chou C (1993) Characterization of interleukin-10 receptors on human and mouse cells. J Biol Chem 268:21053-21059
65. Montaner L, Griffin P, Gordon S (1994) Interleukin-10 inhibits initial reverse transcription of human immunodeficiency virus type 1 and mediates a virostatic latent state in primary blood-derived human macrophages in vitro. J Gen Virol 75:3393-3400
66. Mosmann T (1994) Properties and functions of interleukin-10. Adv Immunol 56:1-27
67. Masood R, Lunardi-Iskandar Y, Moudgil T, Zhang V, Law R, Huang C, Puri R, Levine A, Gill P (1994) IL-10 inhibits HIV-1 replication and is induced by Tat. Biochem Biophys Res Commun 202:374-383
68. Sprang S, Bazan J (1993) Cytokine structural taxonomy and mechanisms of receptor engagement. Curr Op Struct Biol 3:815-827