Ligand-binding sites in Ig-like domains of receptor tyrosine kinases

Journal of Molecular Medicine

Volumn 78, Issue 5, 2000, Pages 247-260

  Wiesmann, Christian ^a,c   Muller, Yves A ^b   De Vos, Abraham M ^a  

^a GENENTECH INC   (United States)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c Sunesis Pharmaceuticals Inc   (United States)

Author keywords

Binding and specificity; Crystal structure; Flt 1; Ig like domain; Ligand receptor complex; TrkA

Indexed keywords

IMMUNOGLOBULIN; PLATELET DERIVED GROWTH FACTOR; PROTEIN TYROSINE KINASE; VASCULOTROPIN; VASCULOTROPIN RECEPTOR;

BINDING SITE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME SPECIFICITY; LIGAND BINDING; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION;

EID: 0033915675     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s001090000082     Document Type: Review

References (86)

1. 1. van der Geer P, Hunter T, Lindberg RA (1994) Receptor protein-tyrosine kinases and their signal transduction pathways. Annu Rev Cell Biol 10:251-337
2. 2. Schlessinger J, Ullrich A (1992) Growth factor signaling by receptor tyrosine kinases. Neuron 9:383-391
3. 3. Levitzki A (1999) Protein tyrosine kinase inhibitors as novel therapeutic agents. Pharmacol Ther 82:231-239
4. 4. Hubbard SR, Wei L, Ellis L, Hendrickson WA (1994) Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature 372:746-754
5. 5. Hubbard SR (1997) Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analog. EMBO J 16:5572-5581
6. 6. Mohammadi M, Schlessinger J, Hubbard SR (1996) Structure of the FGF receptor tyrosine kinase domain reveals a novel autoinhibitory mechanism. Cell 86:577-587
7. 7. Mohammadi M, McMahon G, Sun L, Tang C, Hirth P, Yeh BK, Hubbard SR, Schlessinger J (1997) Structures of the tyrosine kinase domain of fibroblast growth factor receptor in complex with inhibitors. Science 276:955-960
8. 8. Mohammadi M, Froum S, Hamby JM, Schroeder MC, Panek RL, Lu GH, Eliseenkova AV, Green D, Schlessinger J, Hubbard SR (1998) Crystal structure of an angiogenesis inhibitor bound to the FGF receptor tyrosine kinase domain. EMBO J 17:5896-5904
9. 9. McTigue MA, Wickersham JA, Pinko C, Showalter RE, Parast CV, Tempczyk-Russell A, Gehring MR, Mroczkowski B, Kan CC, Villafranca JE, Appelt K (1999) Crystal structure of the kinase domain of human vascular endothelial growth factor receptor 2: a key enzyme in angiogenesis. Struct Fold Des 7:319-330
10. 10. Hubbard SR (1999) Structural analysis of receptor tyrosine kinases. Prog Biophys Mol Biol 71:343-358
11. 11. Kossiakoff AA, de Vos AM (1998) Structural basis for cytokine hormone-receptor recognition and receptor activation. Adv Protein Chem 52:67-108
12. 12. Wells JA, de Vos AM (1996) Hematopoietic receptor complexes. Annu Rev Biochem 65:609-634
13. 13. Himanen JP, Henkemeyer M, Nikolov DB (1998) Crystal structure of the ligand-binding domain of the receptor tyrosine kinase EphB2. Nature 396:486-491
14. 14. Wiesmann C, Fuh G, Christinger HW, Eigenbrot C, Wells JA, de Vos AM (1997) Crystal structure at 1.7 Å resolution of VEGF in complex with domain 2 of the Flt-1 receptor. Cell 91:695-704
15. 15. Ultsch M, Wiesmann C, Simmons LC, Henrich J, Yang M, Reilly D, Bass SH, de Vos AM (1999) Crystal structures of the neurotrophin-binding domain of TrkA, TrkB and TrkC. J Mol Biol 290:149-159
16. 16. Plotnikov AN, Schlessinger J, Hubbard SR, Mohammadi M (1999) Structural basis for FGF receptor dimerization and activation. Cell 98:641-650
17. 17. Garrett TP, McKern NM, Lou M, Frenkel MJ, Bentley JD, Lovrecz GO, Elleman TC, Cosgrove LJ, Ward CW (1998) Crystal structure of the first three domains of the type-1 insulin-like growth factor receptor. Nature 394:395-399
18. 18. Murray-Rust J, McDonald NQ, Blundell TL, Hosang M, Oefner C, Winkler F, Bradshaw RA (1993) Topological similarities in TGF-β2, PDGF-BB and NGF define a superfamily of polypeptide growth factors. Structure 1:153-159
19. 19. Sun PD, Davies DR (1995) The cystine-knot growth-factor superfamily. Annu Rev Biophys Biomol Struct 24:269-291
20. 20. MacDonald JI, Meakin SO (1996) Deletions in the extracellular domain of rat trkA lead to an altered differentiative phenotype in neurotrophin responsive cells. Mol Cell Neurosci 7:371-390
21. 21. Ferrara N (1995) The role of vascular endothelial growth factor in pathological angiogenesis. Breast Cancer Res Treat 36:127-137
22. 22. Houck KA, Ferrara N, Winer J, Cachianes G, Li B, Leung DW (1991) The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol Endocrinol 5:1806-1814
23. 23. Fairbrother WJ, Champe MA, Christinger HW, Keyt BA, Starovasnik MA (1998) Solution structure of the heparin-binding domain of vascular endothelial growth factor. Structure 6:637-648
24. 24. Chirgadze DY, Hepple JP, Zhou H, Byrd RA, Blundell TL, Gherardi E (1999) Crystal structure of the NK1 fragment of HGF/SF suggests a novel mode for growth factor dimerization and receptor binding. Nat Struct Biol 6:72-79
25. 25. Ultsch M, Lokker NA, Godowski PJ, de Vos AM (1998) Crystal structure of the NK1 fragment of human hepatocyte growth factor at 2.0 A resolution. Structure 6:1383-1393
26. 26. Muller YA, Christinger HW, Keyt BA, de Vos AM (1997) The crystal structure of vascular endothelial growth factor (VEGF) refined to 1.93 A resolution: multiple copy flexibility and receptor binding. Structure 5:1325-1338
27. 27. Muller YA, Li B, Christinger HW, Wells JA, Cunningham BC, de Vos AM (1997) Vascular endothelial growth factor: crystal structure and functional mapping of the kinase domain receptor binding site. Proc Natl Acad Sci USA 94:7192-7197
28. 28. Muller YA, Chen Y, Christinger HW, Li B, Cunningham BC, Lowman HB, de Vos AM (1998) VEGF and the Fab fragment of a humanized neutralizing antibody: crystal structure of the complex at 2.4 A resolution and mutational analysis of the interface. Structure 6:1153-1167
29. 29. Presta LG, Chen H, O'Connor SJ, Chisholm V, Meng YG, Krummen L, Winkler M, Ferrara N (1997) Humanization of an anti-vascular endothelial growth factor monoclonal antibody for the therapy of solid tumors and other disorders. Cancer Res 57:4593-4599
30. 30. Kim KJ, Li B, Winer J, Armanini M, Gillet N, Phillips HS, Ferrara N (1993) Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature 362:841-844
31. 31. Wrighton NC, Farrell FX, Chang R, Kashyap AK, Barbone FP, Mulcahy LS, Johnson DL, Barrett RW, Jolliffe LK, Dower WJ (1996) Small peptides as potent mimetics of the protein hormone erythropoietin. Science 273:458-464
32. 32. Fairbrother WJ, Christinger HW, Cochran AG, Fuh G, Keenan CJ, Quan C, Shriver SK, Tom JY, Wells JA, Cunningham BC (1998) Novel peptides selected to bind vascular endothelial growth factor target the receptor-binding site. Biochemistry 37:17754-17764
33. 33. Wiesmann C, Christinger HW, Cochran AG, Cunningham BC, Fairbrother WJ, Keenan CJ, Meng G, de Vos AM (1998) Crystal structure of the complex between VEGF and a receptor-blocking peptide. Biochemistry 37:17765-17772
34. 34. Pandit J, Bohm A, Jancarik J, Halenbeck R, Koths K, Kim SH (1992) Three-dimensional structure of dimeric human recombinant macrophage colony-stimulating factor. Science 258: 1358-1362
35. 35. Savvides SN, Boone T, Karplus PA (1998) A new, early-acting hematopoietic cytokine: structure of the Flt-3 ligand. Protein Sci 8 [Suppl 1]:117-117
36. 36. Graddis TJ, Brasel K, Friend D, Srinivasan S, Wee S, Lyman SD, March CJ, McGrew JT (1998) Structure-function analysis of FLT3 ligand-FLT3 receptor interactions using a rapid functional screen. J Biol Chem 273:17626-17633
37. 37. Taylor EW, Fear AL, Bohm A, Kim SH, Koths K (1994) Structure-function studies on recombinant human macrophage colony-stimulating factor (M-CSF). J Biol Chem 269:31171-31177
38. 38. Lemmon MA, Pinchasi D, Zhou M, Lax I, Schlessinger J (1997) Kit receptor dimerization is driven by bivalent binding of stem cell factor. J Biol Chem 272:6311-6317
39. 39. Zhu X, Komiya H, Chirino A, Faham S, Fox GM, Arakawa T, Hsu BT, Rees DC (1991) Three-dimensional structures of acidic and basic fibroblast growth factors. Science 251:90-93
40. 40. Springer BA, Pantoliano MW, Barbera FA, Gunyuzlu PL, Thompson LD, Herblin WF, Rosenfeld SA, Book GW (1994) Identification and concerted function of two receptor binding surfaces on basic fibroblast growth factor required for mitogenesis. J Biol Chem 269:26879-26884
41. 41. Yayon A, Aviezer D, Safran M, Gross JL, Heldman Y, Cabilly S, Givol D, Katchalski-Katzir E (1993) Isolation of peptides that inhibit binding of basic fibroblast growth factor to its receptor from a random phage-epitope library. Proc Natl Acad Sci USA 90:10643-10647
42. 42. DiGabriele AD, Lax I, Chen DI, Svahn CM, Jaye M, Schlessinger J, Hendrickson WA (1998) Structure of a heparin-linked biologically active dimer of fibroblast growth factor. Nature 393:812-817
43. 43. Faham S, Hileman RE, Fromm JR, Linhardt RJ, Rees DC (1996) Heparin structure and interactions with basic fibroblast growth factor. Science 271:1116-1120
44. 44. Ornitz DM, Herr AB, Nilsson M, Westman J, Svahn CM, Waksman G (1995) FGF binding and FGF receptor activation by synthetic heparan-derived di-and trisaccharides. Science 268:432-436
45. 45. Lemmon MA, Schlessinger J (1994) Regulation of signal transduction and signal diversity by receptor oligomerization. Trends Biochem Sci 19:459-463
46. 46. Heldin CH, Ernlund A, Rorsman C, Ronnstrand L (1989) Dimerization of B-type platelet-derived growth factor receptors occurs after ligand binding and is closely associated with receptor kinase activation. J Biol Chem 264:8905-8912
47. 47. Williams AF, Barclay AN (1988) The immunoglobulin superfamily-domains for cell surface recognition. Annu Rev Immunol 6:381-405
48. 48. Harpaz Y, Chothia C (1994) Many of the immunoglobulin superfamily domains in cell adhesion molecules and surface receptors belong to a new structural set which is close to that containing variable domains. J Mol Biol 238:528-539
49. 49. Chothia C, Jones EY (1997) The molecular structure of cell adhesion molecules. Annu Rev Biochem 66:823-862
50. 50. Casasnovas JM, Stehle T, Liu JH, Wang JH, Springer TA (1998) A dimeric crystal structure for the N-terminal two domains of intercellular adhesion molecule-1. Proc Natl Acad Sci USA 95:4134-4139
51. 51. Ferrara N (1999) Vascular endothelial growth factor: molecular and biological aspects. Curr Top Microbiol Immunol 237:1-30
52. 52. Korpelainen EI, Alitalo K (1998) Signaling angiogenesis and lymphangiogenesis. Curr Opin Cell Biol 10:159-164
53. 53. Kondo K, Hiratsuka S, Subbalakshmi E, Matsushime H, Shibuya M (1998) Genomic organization of the flt-1 gene encoding for vascular endothelial growth factor (VEGF) receptor-1 suggests an intimate evolutionary relationship between the 7-Ig and the 5-Ig tyrosine kinase receptors. Gene 208:297-305
54. 54. Mahadevan D, Yu JC, Saldanha JW, Thanki N, McPhie P, Uren A, LaRochelle WJ, Heidaran MA (1995) Structural role of extracellular domain 1 of alpha-platelet-derived growth factor (PDGF) receptor for PDGF-AA and PDGF-BB binding. J Biol Chem 270:27595-27600
55. 55. Blechman JM, Lev S, Barg J, Eisenstein M, Vaks B, Vogel Z, Givol D, Yarden Y (1995) The fourth immunoglobulin domain of the stem cell factor receptor couples ligand binding to signal transduction. Cell 80:103-113
56. 56. Davis-Smyth T, Chen H, Park J, Presta LG, Ferrara N (1996) The second immunoglobulin-like domain of the VEGF tyrosine kinase receptor Flt-1 determines ligand binding and may initiate a signal transduction cascade. EMBO J 15:4919-4927
57. 57. Barleon B, Totzke F, Herzog C, Blanke S, Kremmer E, Siemeister G, Marme D, Martiny-Baron G (1997) Mapping of the sites for ligand binding and receptor dimerization at the extracellular domain of the vascular endothelial growth factor receptor FLT-1. J Biol Chem 272:10382-10388
58. 58. Cunningham SA, Stephan CC, Arrate MP, Ayer KG, Brock TA (1997) Identification of the extracellular domains of Flt-1 that mediate ligand interactions. Biochem Biophys Res Commun 231:596-599
59. 59. Fuh G, Li B, Crowley C, Cunningham B, Wells JA (1998) Requirements for binding and signaling of the kinase domain receptor for vascular endothelial growth factor. J Biol Chem 273:11197-11204
60. 60. Miyazawa K, Backstrom G, Leppanen O, Persson C, Wernstedt C, Hellman U, Heldin CH, Ostman A (1998) Role of immuno-globulin-like domains 2-4 of the platelet-derived growth factor alpha-receptor in ligand-receptor complex assembly. J Biol Chem 273:25495-25502
61. 61. Starovasnik MA, Christinger HW, Wiesmann C, Champe MA, de Vos AM, Skelton NJ (1999) Solution structure of the VEGF-binding domain of Flt-1: comparison of its free and bound states. J Mol Biol 293:531-544
62. 62. Holden HM, Ito M, Hartshorne DJ, Rayment I (1992) X-ray structure determination of telokin, the C-terminal domain of myosin light chain kinase, at 2.8 A resolution. J Mol Biol 227:840-851
63. 63. Cordon-Cardo C, Tapley P, Jing SQ, Nanduri V, O'Rourke E, Lamballe F, Kovary K, Klein R, Jones KR, Reichardt LF, Barbacid M (1991) The trk tyrosine protein kinase mediates the mitogenic properties of nerve growth factor and neurotrophin-3. Cell 66:173-183
64. 64. Kaplan DR, Hempstead BL, Martin-Zanca D, Chao MV, Parada LF (1991) The trk proto-oncogene product: a signal transducing receptor for nerve growth factor. Science 252: 554-558
65. 65. Klein R, Nanduri V, Jing SA, Lamballe F, Tapley P, Bryant S, Cordon-Cardo C, Jones KR, Reichardt LF, Barbacid M (1991) The trkB tyrosine protein kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3. Cell 66:395-403
66. 66. Klein R, Jing SQ, Nanduri V, O'Rourke E, Barbacid M (1991) The trk proto-oncogene encodes a receptor for nerve growth factor. Cell 65:189-197
67. 67. Berkemeier LR, Winslow JW, Kaplan DR, Nikolics K, Goeddel DV, Rosenthal A (1991) Neurotrophin-5: a novel neurotrophic factor that activates trk and trkB. Neuron 7:857-866
68. 68. Soppet D, Escandon E, Maragos J, Middlemas DS, Reid SW, Blair J, Burton LE, Stanton BR, Kaplan DR, Hunter T, et al (1991) The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell 65:895-903
69. 69. Lamballe F, Klein R, Barbacid M (1991) trkC, a new member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3. Cell 66:967-979
70. 70. Tannahill L, Klein R, Schachner M (1995) The neurotrophin receptors TrkA and TrkB are inhibitory for neurite outgrowth. Europ. J Neurosci 7:1424-1428
71. 71. Holden PH, Asopa V, Robertson AG, Clarke AR, Tyler S, Bennett GS, Brain SD, Wilcock GK, Allen SJ, Smith SK, Dawbarn D (1997) Immunoglobulin-like domains define the nerve growth factor binding site of the TrkA receptor. Nat Biotechnol 15:668-872
72. 72. Pérez P, Coll PM, Hempstead BL, Martin-Zanca D, Chao MV (1995) NGF binding to the trk tyrosine kinase receptor requires the extracellular immunoglobulin-like domains. Mol Cell Neurosci 6:97-105
73. 73. Urfer R, Tsoulfas P, O'Connell L, Shelton DL, Parada LF, Presta LG (1995) An immunoglobulin-like domain determines the specificity of neurotrophin receptors. EMBO J 14:2795-2805
74. 74. Windisch JM, Marksteiner R, Schneider R (1995) Nerve growth factor binding site on TrkA mapped to a single 24-amino acid leucine-rich motif. J Biol Chem 270:28133-28138
75. 75. Windisch JM, Marksteiner R, Lang ME, Auer B, Schneider R (1995) Brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4 bind to a single leucine-rich motif of TrkB. Biochemistry 34:11256-11263
76. 76. Haniu M, Montestruque S, Bures EJ, Talvenheimo J, Toso R, Lewis-Sandy S, Welcher AA, Rohde MF (1997) Interactions between brain-derived neurotrophic factor and the TRKB receptor. Identification of two ligand binding domains in soluble TRKB by affinity separation and chemical cross-linking. J Biol Chem 272:25296-25303
77. 77. Wiesmann C, Ultsch MH, Bass SH, de Vos AM (1999) Crystal structure of nerve growth factor in complex with the ligand-binding domain of the TrkA receptor. Nature 401:184-188
78. 78. Urfer R, Tsoulfas P, O'Connell L, Hongo JA, Zhao W, Presta LG (1998) High resolution mapping of the binding site of TrkA for nerve growth factor and TrkC for neurotrophin-3 on the second immunoglobulin-like domain of the Trk receptors. J Biol Chem 273:5829-5840
79. 79. Kahle P, Burton LE, Schmelzer CH, Hertel C (1992) The amino terminus of nerve growth factor is involved in the interaction with the receptor tyrosine kinase p140trkA. J Biol Chem 267:22707-22710
80. 80. McDonald NQ, Lapatto R, Murray-Rust J, Gunning J, Wlodawer A, Blundell TL (1991) New protein fold revealed by a 2.3-A resolution crystal structure of nerve growth factor. Nature 354:411-414
81. 81. Holland DR, Cousens LS, Meng W, Matthews BW (1994) Nerve growth factor in different crystal forms displays structural flexibility and reveals zinc binding sites. J Mol Biol 239:385-400
82. 82. Bax B, Blundell TL, Murray-Rust J, McDonald NQ (1997) Structure of mouse 7S NGF: a complex of nerve growth factor with four binding proteins. Structure 5:1275-1285
83. 83. Kullander K, Ebendal T (1994) Neurotrophin-3 acquires NGF-like activity after exchange to five NGF amino acid residues: molecular analysis of the sites in NGF mediating the specific interaction with the NGF high affinity receptor. J Neurosci Res 39:195-210
84. 84. Ibáñez CF, Ilag LL, Murray-Rust J, Persson H (1993) An extended surface of binding to Trk tyrosine kinase receptors in NGF and BDNF allows the engineering of a multifunctional pan-neurotrophin. EMBO J 12:2281-2293
85. 85. O'Leary PD, Hughes RA (1998) Structure-activity relationships of conformationally constrained peptide analogues of loop 2 of brain-derived neurotrophic factor. J Neurochem 70:1712-1721
86. 86. Bateman A, Chothia C (1995) Outline structures for the extracellular domains of the fibroblast growth factor receptors. Nat Struct Biol 2:1068-1074