A modular interface of IL-4 allows for scalable affinity without affecting specificity for the IL-4 receptor

BMC Biology

Volumn 4, Issue , 2006, Pages

  Kraich, Michael ^a   Klein, Markus ^a   Patiño, Edwin ^a   Harrer, Henning ^a   Nickel, Joachim ^a   Sebald, Walter ^a,b   Mueller, Thomas D ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; GLUTAMIC ACID; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR; INTERLEUKIN 4 RECEPTOR ALPHA; LIGAND; PHENYLALANINE; RECEPTOR SUBUNIT; THREONINE; ISOPROTEIN; PORIN; PROTEIN BINDING; PROTEIN IIIA, RHIZOBIUM LEGUMINOSARUM;

ARTICLE; CONTROLLED STUDY; IN VITRO STUDY; MOLECULAR INTERACTION; MUTAGENESIS; NONHUMAN; RECEPTOR AFFINITY; RECEPTOR BINDING; AGONISTS; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; GENETICS; HUMAN; METABOLISM; MUTATION; SIGNAL TRANSDUCTION;

BINDING SITES; HUMANS; INTERLEUKIN-13; INTERLEUKIN-4; MODELS, MOLECULAR; MUTATION; PORINS; PROTEIN BINDING; PROTEIN ISOFORMS; RECEPTORS, INTERLEUKIN-4; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY;

EID: 33745227715     PISSN: 17417007     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-4-13     Document Type: Article

References (70)

1. Paul WE: Interleukin-4: a prototypic immunoregulatory lymphokine. Blood 1991, 77(9):1859-1870.
2. Paul WE, Seder RA: Lymphocyte responses and cytokines. Cell 1994, 76(2):241-251.
3. Bacharier LB, Jabara H, Geha RS: Molecular mechanisms of immunoglobulin E regulation. Int Arch Allergy Immunol 1998, 115(4):257-269.
4. Worm M, Henz BM: Molecular regulation of human IgE synthesis. J Mol Med 1997, 75(6):440-447.
5. Doucet C, Brouty-Boye D, Pottin-Clemenceau C, Canonica GW, Jasmin C, Azzarone B: Interleukin (IL) 4 and IL-13 act on human lung fibroblasts. Implication in asthma. J Clin Invest 1998, 101(10):2129-2139.
6. Mochizuki M, Bartels J, Mallet Al, Christophers E, Schroder JM: IL-4 induces eotaxin: a possible mechanism of selective eosinophil recruitment in helminth infection and atopy. J Immunol 1998, 160(1):60-68.
7. Hoeck J, Woisetschlager M: STAT6 mediates eotaxin-I expression in IL-4 or TNF-alpha-induced fibroblasts. J Immunol 2001, 166(7):4507-4515.
8. Zimmermann N, Hogan SP, Mishra A, Brandt EB, Bodette TR, Pope SM, Finkelman FD, Rothenberg ME: Murine eotaxin-2: a constitutive eosinophil chemokine induced by allergen challenge and IL-4 overexpression. J Immunol 2000, 165(10):5839-5846.
9. Bischoff SC, Sellge G, Lorentz A, Sebald W, Raab R, Manns MP: IL-4 enhances proliferation and mediator release in mature human mast cells. Proc Natl Acad Sci U S A 1999, 96(14):8080-8085.
10. Hara T, Yamada K, Tachibana H: Basophilic differentiation of the human leukemia cell line KU812 upon treatment with interleukin-4. Biochem Biophys Res Commun 1998, 247(3):542-548.
11. Maggi E: The TH1/TH2 paradigm in allergy. Immunotechnology 1998, 3(4):233-244.
12. Leonard WJ: The defective gene in X-linked severe combined immunodeficiency encodes a shared interleukin receptor subunit: implications for cytokine pleiotropy and redundancy. Curr Opin Immunol 1994, 6(4):631-635.
13. Sugamura K, Asao H, Kondo M, Tanaka N, Ishii N, Nakamura M, Takeshita T: The common gamma-chain for multiple cytokine receptors. Adv Immunol 1995, 59:225-277.
14. Gauchat JF, Schlagenhauf E, Feng NP, Moser R, Yamage M, Jeannin P, Alouani S, Elson G, Notarangelo LD, Wells T, Eugster HP, Bonnefoy JY: A novel 4-kb interleukin-13 receptor alpha mRNA expressed in human B, T, and endothelial cells encoding an alternate type-II interleukin-4/ interleukin-13 receptor. Eur J Immunol 1997, 27(4):971-978.
15. Miloux B, Laurent P, Bonnin O, Lupker J, Caput D, Vita N, Ferrara P: Cloning of the human IL-13R alpha 1 chain and reconstitution with the IL4R alpha of a functional IL-4/IL-13 receptor complex. FEBS Lett 1997, 401(2-3):163-166.
16. Nelms K, Keegan AD, Zamorano J, Ryan JJ, Paul WE: The IL-4 receptor: signaling mechanisms and biologic functions. Annu Rev Immunol 1999, 17:701-738.
17. Minty A, Chalon P, Derocq JM, Dumont X, Guillemot JC, Kaghad M, Labit C, Leplatois P, Liauzun P, Miloux B, et al.: Interleukin-13 is a new human lymphokine regulating inflammatory and immune responses. Nature 1993, 362(6417):248-250.
18. Kruse N, Shen BJ, Arnold S, Tony HP, Muller T, Sebald W: Two distinct functional sites of human interleukin 4 are identified by variants impaired in either receptor binding or receptor activation. Embo J 1993, 12(13):5121-5129.
19. Shen BJ, Hage T, Sebald W: Global and local determinants for the kinetics of interleukin-4/interleukin-4 receptor alpha chain interaction. A biosensor study employing recombinant interleukin-4-binding protein. Eur J Biochem 1996, 240(1):252-261.
20. Letzelter F, Wang Y, Sebald W: The interleukin-4 site-2 epitope determining binding of the common receptor gamma chain. Eur J Biochem 1998, 257(1):11-20.
21. Andrews AL, Holloway JW, Puddicombe SM, Holgate ST, Davies DE: Kinetic analysis of the interleukin-13 receptor complex. J Biol Chem 2002, 277(48):46073-46078.
22. Eisenmesser EZ, Horita DA, Altieri AS, Byrd RA: Solution structure of interleukin-13 and insights into receptor engagement. J Mol Biol 2001, 310(1):231-241.
23. Moy FJ, Diblasio E, Wilhelm J, Powers R: Solution structure of human IL-13 and implication for receptor binding. J Mol Biol 2001, 310(1):219-230.
24. Powers R, Garrett DS, March CJ, Frieden EA. Gronenborn AM, Clore GM: Three-dimensional solution structure of human interleukin-4 by multidimensional heteronuclear magnetic resonance spectroscopy. Science 1992, 256(5064):1673-1677.
25. Smith LJ, Redfield C, Boyd J, Lawrence GM, Edwards RG, Smith RA, Dobson CM: Human interleukin 4. The solution structure of a four-helix bundle protein. J Mol Biol 1992, 224(4):899-904.
26. Walter MR, Cook WJ, Zhao BG, Cameron RP Jr, Ealick SE, Walter RL, Reichert P Jr, Nagabhushan TL, Trotta PP, Bugg CE: Crystal structure of recombinant human interleukin-4. J Biol Chem 1992, 267(28):20371-20376.
27. Wlodaver A, Pavlovsky A, Gustchina A: Crystal structure of human recombinant interleukin-4 at 2.25 A resolution. FEBS Lett 1992,309(1):59-64.
28. Kruse N, Lehrnbecher T, Sebald W. Site-directed mutagenesis reveals the importance of disulfide bridges and aromatic residues for structure and proliferative activity of human interleukin-4. FEBS Lett 1991, 286(1-2):58-60.
29. Kruse N, Tony HP, Sebald W: Conversion of human interleukin-4 into a high affinity antagonist by a single amino acid replacement EMBO J 1992, 11(9):3237-3244.
30. Wang Y, Shen BJ, Sebald W: A mixed-charge pair in human interleukin 4 dominates high-affinity interaction with the receptor alpha chain. Proc Natl Acad Sci U S A 1997, 94(5):1657-1662.
31. Muller T, Dieckmann T, Sebald W, Oschkinat H: Aspects of receptor binding and signalling of interleukin-4 investigated by site-directed mutagenesis and NMR spectroscopy. J Mol Biol 1994, 237(4):423-436.
32. Muller T, Oehlenschlager F, Buehner M: Human interleukin-4 and variant R88Q: phasing X-ray diffraction data by molecular replacement using X-ray and nuclear magnetic resonance models. J Mol Biol 1995, 247(2):360-372.
33. Hage T, Sebald W, Reinemer P: Crystal structure of the interleukin-4/ receptor alpha chain complex reveals a mosaic binding interface. Cell 1999, 97(2):271-281.
34. Mueller TD, Zhang JL, Sebald W, Duschl A: Structure, binding, and antagonists in the IL-4/IL-13 receptor system. Biochim Biophys Acta 2002, 1592(3):237-250.
35. Madhankumar AB, Mintz A, Debinski W: Alanine-scanning mutagenesis of alpha-helix D segment of interleukin-13 reveals new functionally important residues of the cytokine. J Biol Chem 2002, 277(45):43194-43205.
36. Oshima Y, Joshi BH, Puri RK: Conversion of interleukin-13 into a high affinity agonist by a single amino acid substitution. J Biol Chem 2000, 275(19):14375-14380.
37. Thompson JP, Debinski W: Mutants of interleukin 13 with altered reactivity toward interleukin 13 receptors. J Biol Chem 1999, 274(42):29944-29950.
38. Redfield C, Smith LJ, Boyd J, Lawrence GM, Edwards RG, Gershater CJ, Smith RA, Dobson CM: Analysis of the solution structure of human interleukin-4 determined by heteronuclear three-dimensional nuclear magnetic resonance techniques. J Mol Biol 1994. 238(1):23-41.
39. Zhang JL, Simeonowa I, Wang Y, Sebald W: The high-affinity interaction of human IL-4 and the receptor alpha chain is constituted by two independent binding clusters. J Mol Biol 2002, 315(3):399-407.
40. Obiri NI, Debinski W, Leonard WJ, Puri RK: Receptor for interleukin 13. Interaction with interleukin 4 by a mechanism that does not involve the common gamma chain shared by receptors for interleukins 2, 4, 7, 9, and 15. J Biol Chem 1995, 270(15):8797-8804.
41. Vita N, Lefort S, Laurent P, Caput D, Ferrara P: Characterization and comparison of the interleukin 13 receptor with the interleukin 4 receptor on several cell types. J Biol Chem 1995, 270(8):3512-3517.
42. Arima K, Sato K. Tanaka G, Kanali S, Terada T, Honjo E, Kuroki R, Matsuo Y, Izuhara K: Characterization of the interaction between interleukin-13 and interleukin-13 receptors. J Biol Chem 2005, 280(26):24915-24922.
43. Boulanger MJ, Garcia KC: Shared cytokine signaling receptors: structural insights from the gp 130 system. Adv Protein Chem 2004, 68:107-146.
44. Kovanen PE, Leonard WJ: Cytokines and immunodeficiency diseases: critical roles of the gamma(c)-dependent cytokines interleukins 2, 4, 7, 9, 15, and 21, and their signaling pathways. Immunol Rev 2004, 202:67-83.
45. Nickel J, Kotzsch A, Sebald W, Mueller TD: A single residue of GDF-5 defines binding specificity to BMP receptor IB. J Mol Biol 2005, 349(5):933-947.
46. Sebald W, Nickel J, Zhang JL, Mueller TD: Molecular recognition in bone morphogenetic protein (BMP)/receptor interaction. Biol Chem 2004, 385(8):697-710.
47. Souchelnytskyi S, Moustakas A. Heldin CH: TGF-beta signaling from a three-dimensional perspective: insight into selection of partners. Trends Cell Biol 2002, 12(7):304-307.
48. Patapoutian A, Reichardt LF: Trk receptors: mediators of neurotrophin action. Curr Opin Neurobiol 2001, 11(3):272-280.
49. Bazan JF: Emerging families of cytokines and receptors. Curr Biol 1993, 3(9):603-606.
50. Janin J: Principles of protein-protein recognition from structure to thermodynamics. Biochimie 1995, 77:7-8.
51. Lo Conte L, Chothia C, Janin J: The atomic structure of protein-protein recognition sites. J Mol Biol 1999, 285(5):2177-2198.
52. Goh CS, Bogan AA, Joachimiak M, Walther D, Cohen FE: Co-evolution of proteins with their interaction partners. J Mol Biol 2000, 299(2):283-293.
53. Ma B, Elkayam T, Wolfson H, Nussinov R: Protein-protein interactions: structurally conserved residues distinguish between binding sites and exposed protein surfaces. Proc Natl Acad Sci U S A 2003, 100(10):5772-5777.
54. Clackson T, Wells JA: A hot spot of binding energy in a hormone-receptor interface. Science 1995, 267(5196):383-386.
55. Cunningham BC, Wells JA: Comparison of a structural and a functional epitope. J Mol Biol 1993, 234(3):554-563.
56. Kossiakoff AA: The structural basis for biological signaling, regulation, and specificity in the growth hormone-prolactin system of hormones and receptors. Adv Protein Chem 2004, 68:147-169.
57. Donaldson DD, Whitters MJ, Fitz LJ, Neben TY, Finnerty H, Henderson SL, O'Hara RM Jr, Beier DR, Turner KJ, Wood CK, et al.: The murine IL-13 receptor alpha 2: molecular cloning, characterization, and comparison with murine IL-13 receptor alpha 1, J Immunol 1998, 161 (5):2317-2324.
58. Leonard WJ, Shores EW, Love PE: Role of the common cytokine receptor gamma chain in cytokine signaling and lymphoid development. Immunol Rev 1995, 148:97-114.
59. Boulanger MJ, Bankovich AJ, Kortemme T, Baker D, Garcia KC: Convergent mechanisms for recognition of divergent cytokines by the shared signaling receptor gp130. Mol Cell 2003, 12(3):577-589.
60. Zhang JL, Foster D, Sebald W: Human IL-21 and IL-4 bind to partially overlapping epitopes of common gamma-chain. Biochem Biophys Res Commun 2003, 300(2):291-296.
61. Li W, Hamill SJ, Hemmings AM, Moore GR, James R, Kleanthous C: Dual recognition and the role of specificity-determining residues in colicin E9 DNase-immunity protein interactions. Biochemistry 1998, 37(34):11771-11779.
62. Li W, Keeble AH, Giffard C, James R, Moore GR. Kleanthous C: Highly discriminating protein-protein interaction specificities in the context of a conserved binding energy hotspot. J Mol Biol 2004, 337(3):743-759.
63. Shanafelt AB, Forte CP, Kasper JJ, Sanchez-Pescador L, Wetzel M, Gundel R, Greve JM: An immune cell-selective interleukin 4 agonist. Proc Natl Acad Sci U S A 1998, 95(16):9454-9458.
64. Srivannaboon K, Shanafelt AB, Todisco E, Forte CP, Behm FG, Raimondi SC, Pui CH, Campana D: Interleukin-4 variant (BAY 361677) selectively induces apoptosis in acute lymphoblastic leukemia cells. Blood 2001, 97(3):752-758.
65. Kawakami K, Kawakami M, Puri RK: Specifically targeted killing of interleukin-13 (IL-13) receptor-expressing breast cancer by IL-13 fusion cytotoxin in animal model of human disease. Mol Cancer Ther 2004, 3(2):137-147.
66. Kawakami K, Kioi M, Liu Q, Kawakami M, Puri RK: Evidence that IL-13R alpha2 chain in human glioma cells is responsible for the antitumor activity mediated by receptor-directed cytotoxin therapy. J Immunother 2005, 28(3):193-202.
67. Weigel U, Meyer M, Sebald W: Mutant proteins of human interleukin 2. Renaturation yield, proliferative activity and receptor binding. Eur J Biochem 1989, 180(2):295-300.
68. Eisenmesser EZ, Kapust RB, Nawrocki JP, Mazzulla MJ, Pannell LK, Waugh DS, Byrd RA: Expression, purification, refolding, and characterization of recombinant human interleukin-13: utilization of intracellular processing. Protein Expr Purif 2000, 20(2):186-195.
69. Kitamura T, Tange T, Terasawa T, Chiba S, Kuwaki T, Miyagawa K, Piao YF, Miyazono K, Urabe A, Takaku F: Establishment and characterization of a unique human cell line that proliferates dependently on GM-CSF, IL-3, or erythropoietin. J Cell Physiol 1989, 140(2):323-334.
70. Lakkis FG, Cruet EN, Nassar GM, Badr KF, Pascual DW: Expression of recombinant rat interleukin-13 (IL-13) and generation of a neutralizing rat IL-13 antiserum. Biochem Biophys Res Commun 1997, 235(3):529-532.