Receptor tyrosine kinases: Legacy of the first two decades

Cold Spring Harbor Perspectives in Biology

Volumn 6, Issue 3, 2014, Pages

  Schlessinger, Joseph ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR RECEPTOR; PROTEIN TYROSINE KINASE;

ARTICLE; BIOLOGICAL MODEL; DIMERIZATION; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION;

DIMERIZATION; MODELS, BIOLOGICAL; PHOSPHORYLATION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 84897584347     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a008912     Document Type: Article

References (85)

1. Alvarado D, Klein DE, Lemmon MA. 2010. Structural basis for the negative cooperativity in growth factor binding to an EGF receptor. Cell 142: 568-579.
2. Antoniades HN, Scher CD, Stiles CD. 1979. Purification of human platelet-derived growth factor. Proc Natl Acad Sci 76: 1809-1813.
3. Bae JH, Boggon TJ, Tomé F, Mandiyan V, Lax I, Schlessinger J. 2010. Asymmetric receptor contact is required for tyrosine autophosphorylation of fibroblast growth factor receptor in living cells. Proc Natl Acad Sci 107: 2866-2871.
4. Bae JH, Lew ED, Yuzawa S, Tomé F, Lax I, Schlessinger J. 2009. The selectivity of receptor tyrosine kinase signaling is controlled by a secondary SH2 domain binding site. Cell 138: 514-524.
5. Basu M, Frick K, Sen-Majumdar A, Scher CD, Das M. 1985. EGF receptor-associatedDNA-nicking activity is due to a Mr-100,000 dissociable protein. Nature 316: 640-641.
6. Bertics PJ, Weber W, Cochet C, Gill CN. 1985. Regulation of the epidermal growth factor by phosphorylation. J Cell Biochem 29: 195-208.
7. Bottaro DP, Rubin JS, Faletto DL, Chan AM, Kmiecik TE, Vande Woude GF, Aaronson SA. 1991. Identification of the hepatocyte growth factor receptor as the c-met protooncogene product. Science 251: 802-804.
8. Boucher J, Kleinridders A, Kahn CR. 2014. Insulin receptor signaling in normal and insulin-resistant states. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect. a009191.
9. Brugge JS, Erikson RL. 1977. Identification of a transformation- specific antigen induced by an avian sarcoma virus. Nature 269: 346-348.
10. Burgess AW, Cho HS, Eigenbrot C, Ferguson KM, Garrett TP, Leahy DJ, Lemmon MA, Sliwkowski MX, Ward CW, Yokoyama S. 2003. An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors. Mol Cell 12: 541-542.
11. Carpenter G, Cohen S. 1976. 125I-labeled human epidermal growth factor. Binding, internalization, and degradation in human fibroblasts. J Cell Biol 71: 159-171.
12. Carpenter G, King L Jr, Cohen S. 1978. Epidermal growth factor stimulates phosphorylation in membrane preparations in vitro. Nature 276: 409-410.
13. Carpenter G, Lembach KJ, Morrison MM, Cohen S. 1975. Characterization of the binding of 125I-labeled epidermal growth factor to human fibroblasts. J Biol Chem 250: 4297-4304.
14. Carpentier JL, Gorden P, Barazzone P, Freychet P, Le Cam A, Orci L. 1979. Intracellular localization of 125I-labeled insulin in hepatocytes from intact rat liver. Proc Natl Acad Sci 76: 2803-2807.
15. Chung I, Akita R, Vandlen R, Toomre D, Schlessinger J, Mellman I. 2010. Spatial control of EGF receptor activation by reversible dimerization on living cells. Nature 464: 783-787.
16. Cohen S. 1962. Isolation of a mouse submaxillary gland protein accelerating incisor eruption and eyelid opening in the new-born animal. J Biol Chem 237: 1555-1562.
17. Collett MS, Erikson RL. 1978. Protein kinase activity associatedwith the avian sarcomavirus src gene product. Proc Natl Acad Sci 75: 2021-2024.
18. Das M. 1980. Mitogenic hormone-induced intracellular message: Assay and partial characterization of an activator of DNA replication induced by epidermal growth factor. Proc Natl Acad Sci 77: 112-116.
19. De Meyts P. 2008. The insulin receptor: A prototype for dimeric, allosteric membrane receptor? Trends Biochem Sci 33: 376-384.
20. DeMeyts P, Roth J, Neville DM Jr, Gavin JR III, Lesniak MA. 1973. Insulin interactions with its receptors: Experimental evidence for negative cooperativity. Biochem Biophys Res Commun 55: 154-161.
21. Doolittle RF, Hunkapiller MW, Hood LE, Devare SG, Robbins KC, Aaronson SA, Antoniades HN. 1983. Simian sarcoma virus onc gene, v-sis, is derived from the gene (or genes) encoding a platelet-derived growth factor. Science 221: 275-277.
22. Downward J, Yarden Y, Mayes E, Scrace G, Totty N, Stockwell P, Ullrich A, Schlessinger J, Waterfield MD. 1984. Close similarity of epidermal growth factor receptor and v-erb- B oncogene sequences. Nature 307: 521-527.
23. Ek B, Westermark B, Wasteson A, Heldin CH. 1982. Stimulation of tyrosine-specific phosphorylation by plateletderived growth factor. Nature 295: 419-420.
24. Flier JS, Kahn CR, Jarrett DB, Roth J. 1977. Autoantibodies to the insulin receptor. Effect of the insulin-receptor interaction in IM-9 lymphocytes. J Clin Invest 60: 784-794.
25. Gill GN, Santon FB, Bertics PJ. 1987. Regulatory features of the epidermal growth factor receptor. J Cell Physiol 5: 35-41.
26. Gordon P, Carpentier JL, Freychet P, LeCam A, Orci L. 1978, Intracellular translocation of iodine-125 labeled insulin: Direct demonstration in isolated hepatocytes. Science 200: 782-785.
27. Gospodarowicz D, Bialecki H, Greenburg G. 1978. Purification of the fibroblast growth activity from bovine brain. J Biol Chem 253: 3736-3743.
28. Haigler HT, McKanna JA, Cohen S. 1979. Direct visualization of the binding and internalization of a ferritin conjugate of epidermal growth factor in human carcinoma cells A-431. J Cell Biol 81: 382-395.
29. Heldin CH, Westermark B, Wasteson A. 1979. Plateletderived growth factor: Purification and partial characterization. Proc Natl Acad Sci 76: 3722-3726.
30. Honegger AM, Kris RM, Ullrich A, Schlessinger J. 1989. Evidence that autophosphorylation of solubilized receptors for epidermal growth factor is mediated by intermolecular cross-phosphorylation. Proc Natl Acad Sci 86: 925-929.
31. 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.
32. Hunter T, Sefton BM. 1980. Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc Natl Acad Sci 77: 1311-1315.
33. Jiang LW, Schindler M. 1990. Nucleocytoplasmic transport is enhanced concomitant with nuclear accumulation of epidermal growth factor (EGF) binding activity in both 3T3-1 and EGF receptor reconstituted NR-6 fibroblasts. J Cell Biol 110: 559-568.
34. Jura N, Endres NF, Engel K, Deindl S, Das R, Lamers MH, Wemmer DE, Zheng X, Kuriyan J. 2009. Mechanism for activation of the EGF receptor catalytic domain by the juxtamembrane segment. Cell 137: 1293-1307.
35. Kahn CR, Baird KL, Jarrett DB, Flier JS. 1978. Direct demonstration that receptor crosslinking or aggregation is important to insulin action. Proc Natl Acad Sci 75: 4209-4213.
36. Kashles O, Yarden Y, Fischer R, Ullrich A, Schlessinger J. 1991. A dominant negative mutation suppresses the function of normal epidermal growth factors by heterodimerization. Mol Cell Biol 11: 1454-1463.
37. Kasuga M, Zick Y, Blithe DL, Crettaz M, Kahn CR. 1982. Insulin stimulates tyrosine phosphorylation of the insulin receptor in a cell-free system. Nature 298: 667-669.
38. 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.
39. Koland JG, Cerione RA. 1988. Growth factor control of epidermal growth factor receptor kinase activity via an intramolecular mechanism. J Biol Chem 263: 2230-2237.
40. Kris RM, Lax I, Gullick W, Waterfield MD, Ullrich A, Fridkin M, Schlessinger J. 1985. Antibodies against a synthetic peptide as a probe for the kinase activity of the avian EGF receptor and v-erbB protein. Cell 40: 619-625.
41. Larner J, Galasko G, Cheng K, DePaoli-Roach AA, Huang L, Daggy P, Kellogg J. 1979. Generation by insulin of a chemical mediator that controls protein phosphorylation and dephosphorylation. Science 206: 1408-1410.
42. Lax I, Bar-Eli M, Yarden Y, Libermann TA, Schlessinger J. 1984. Antibodies of two defined regions of the transforming protein pp60src interact specifically with the epidermal growth factor receptor kinase system. Proc Natl Acad Sci 81: 5911-5915.
43. Lee DC, Rose TM, Webb NR, Todaro GJ. 1985. Cloning and sequence analysis of a cDNA for rat transformation growth factor-a. Nature 313: 489-491.
44. Lemmon MA, Schlessinger J. 2010. Cell signaling by receptor tyrosine kinases. Cell 141: 1117-1134.
45. Levi-Montalcini R, Booker B. 1960. Excessive growth of sympathetic ganglia evoked by a protein isolated from mouse salivary gland. Proc Natl Acad Sci 46: 373-384.
46. Libermann TA, Nusbaum HR, Razon N, Kris R, Lax I, Soreg H, Whittle N, Waterfield MD, Ullrich A, Schlessinger J. 1985. Amplification, enhanced expression and possible rearrangement of EGF receptor gene in primary human brain tumours of glial origin. Nature 313: 144-147.
47. Margolis B, Bellot F, Honegger AM, Ullrich A, Schlessinger J, Zilberstein A. 1990. Tyrosine kinase activity is essential for the association of phospholipase C-g with the epidermal growth factor receptor. Mol Cell Biol 10: 435-441.
48. Margolis B, Li N, Kock A, Mohammadi M, Hurwitz DR, Zilberstein A, Ullrich A, Pawson T, Schlessinger J. 1990. The tyrosine phosphorylated carboxyterminus of the EGF receptor is a binding site for GAP and PLC-g. EMBO J 9: 4375-4380.
49. Margolis B, Rhee SG, Felder S, Mervic M, Lyall R, Levitzki A, Ullrich A, Zilberstein A, Schlessinger J. 1989. EGF induces tyrosine phosphorylation of phospholipase C-II: A potential mechanism for EGF receptor signaling. Cell 57: 1101-1107.
50. Matsuda M, Mayer BJ, Fukui Y, Hanafusa H. 1990. Binding of transforming protein, P47gag-crk, to a broad range of phosphotyrosine-containing proteins. Science 248: 1537-1539.
51. Matsuda M, Mayer BJ, Hanafusa H. 1991. Identification of domains of the v-crk oncogene product sufficient for association with phosphotyrosine-containing proteins. Mol Cell Biol 11: 1607-1613.
52. Mayer BJ, Hanafusa H. 1990. Association of the v-crk oncogene product with phosphotyrosine-containing proteins and protein kinase activity. Proc Natl Acad Sci 87: 2642-2648.
53. Meisenhelder J, Suh PG, Rhee SG, Hunter T. 1989. Phospholipase C-g is a substrate for the PDGF and EGF receptor protein-tyrosine kinases in vivo and in vitro. Cell 57: 1109-1122.
54. Miskimins R, Miskimins WK, Bernstein H, Shimizu N. 1983. Epidermal growth factor-induced topoisomerase(s). Intracellular translocation and relation to DNA synthesis. Exp Cell Res 146: 53-62.
55. Mroczkowski B, Mosig G, Cohen S. 1984. ATP-stimulated interaction between epidermal growth factor receptor and supercoiled DNA. Nature 309: 270-273.
56. Nakamura T, Teramoto H, Ichihara A. 1986. Purification and characterization of a growth factor from rat platelets for mature parenchymal hepatocytes in primary cultures. Proc Natl Acad Sci 83: 6489-6493.
57. Northwood IC, Davis RJ. 1988. Activation of the epidermal growth factor receptor tyrosine protein kinase in the absence of receptor oligermerization. J Biol Chem 263: 7450-7453.
58. Pawson T. 1995. Protein modules and signaling networks. Nature 373: 573-580.
59. Pawson T. 2004. Specificity in signal transduction: From phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 116: 191-203.
60. Pike LJ. 2012. Negative co-operativity in the EGF receptor. Biochem Soc Trans 40: 15-19.
61. Podlecki DA, Smith RM, Kao M, Tsai P, Huecksteadt T, Brandenburg D, Lasher RS, Jarett L, Olefsky JM. 1986. Nuclear translocation of the insulin receptor. J Biol Chem 262: 3362-3368.
62. Red Brewer M, Choi SH, Alvarado D, Moravcevic K, Pozzi A, Lemmon MA, Carpenter G. 2009. The juxtamembrane region of the EGF receptor functions as an activation domain. Mol Cell 34: 641-651.
63. Roberts AB, Anzano MA, Lamb LC, Smith JM, Frolik CA, Marquadt H, Todaro GJ, Sporn MB. 1982. Isolation from murine sarcoma cells of novel transforming growth factors potentiated by EGF. Nature 295: 417-419.
64. Roberts AB, Lamb LC, Newton DL, Sporn MB, De Larco JE, Todaro GJ. 1980. Transforming growth factors: Isolation of polypeptides from virally and chemically transformed cells by acid/ethanol extraction. Proc Natl Acad Sci 77: 3494-3498.
65. Sadowski I, Stone JC, Pawson T. 1986. A noncatalytic domain conserved among cytoplasmic protein-tyrosine kinases modifies the kinase function and transforming activity of Fujinami sarcoma virus P130gag-fps. Mol Cell Biol 6: 4396-4408.
66. Saltiel AR, Cuatrecasas P. 1986. Insulin stimulates the generation from hepatic plasma membranes of modulators derived froman inositol glycolipid. ProcNatl Acad Sci 83: 5793-5797.
67. Schlessinger J. 2000. Cell signaling by receptor tyrosine kinases. Cell 103: 211-225.
68. Schlessinger J, Plotnikov AN, Ibrahimi OA, Eliseenkova AV, Yeh BK, Yayon A, Linhardt RJ, Mohammadi M. 2000. Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol Cell 6: 743-750.
69. Schlessinger J, Shechter Y, Cuatrecasas P, Willingham MC, Pastan I. 1978a. Quantitative determination of the lateral diffusion coefficients of the hormone-receptor complexes of insulin and epidermal growth factor on the plasma membrane of cultured fibroblasts. Proc Natl Acad Sci 75: 5353-5357.
70. Schlessinger J, Shechter Y, Willingham MC, Pastan I. 1978b. Direct visualization of binding, aggregation and internalization of insulin and epidermal growth factor on living fibroblastic cells. Proc Natl Acad Sci 75: 2659-2663.
71. Schreiber AB, Lax I, Yarden Y, Eshhar Z, Schlessinger J. 1981.Monoclonal antibodies against receptor for epidermal growth factor induce early and delayed effects of epidermal growth factor. Proc Natl Acad Sci 78: 7535-7539.
72. Schreiber AB, Libermann TA, Lax I, Yarden Y, Schlessinger J. 1983. Biological role of epidermal growth factor-receptor clustering. Investigation with monoclonal anti-receptor antibodies. J Biol Chem 258: 846-853.
73. Temin HM. 1966. Studies on carcinogenesis by avian sarcoma viruses. III: The differential effect of serum and polyanions on multiplication of uninfected and converted cells. J Natl Cancer Inst 37: 167-175.
74. Temin HM. 1967. Studies on carcinogenesis by avian sarcoma viruses. VI. Differential multiplication of uninfected and of converted cells in response to insulin. J Cell Physiol 69: 377-384.
75. Todaro GJ, De Larco JE, Cohen S. 1976. Transformation by murine and feline sarcoma viruses blocks binding of epidermal growth factor to cells. Nature 264: 26-31.
76. Ullrich A, Coussens L, Hayflick JS, Dull TJ, Gray A, Tam AW, Lee J, Yarden Y, Libermann TA, Schlessinger J, et al. 1984. Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. Nature 309: 418-425.
77. Ushiro H, Cohen S. 1980. Identification of phosphotyrosine as a product of epidermal growth factor-activated protein kinase in A-431 cell membranes. J Biol Chem 255: 8363-8365.
78. Van Obberghen E, Spooner PM, Kahn CR, Chernick SS, Garrison MM, Karlsson FA, Grunfeld C. 1979. Insulinreceptor antibodies mimic a late insulin effect. Nature 280: 500-502.
79. Vigneri R, Goldfine ID, Wong KY, Smith GJ, Pezzino V. 1978. The nuclear envelope. The major site of insulin binding in rat liver nuclei. J Biol Chem 253: 2098-2103.
80. Waksman G, Kuriyan J. 2004. Structure and specificity of the SH2 domain. Cell 116: S45-S48.
81. Waterfield MD, Scrace FT, Whittle N, Stroobant P, Johnsson A, Wasteson A, Westermark B, Heldin CH, Huang JS, Deuel TF. 1983. Platelet-derived growth factor is structurally related to the putative transforming protein p28sis of simian sarcoma virus. Nature 304: 35-39.
82. Witte ON, Dasgupta A, Baltimore D. 1980. Abelson murine leukaemia virus protein is phosphorylated in vitro to form phosphotyrosine. Nature 283: 826-831.
83. Yarden Y, Schlessinger J. 1987. Self-phosphorylation of epidermal growth factor receptor: Evidence for a model of intermolecular allosteric activation. Biochemistry 26: 1434-1442.
84. Yuzawa S, Opatowsky Y, Zhang Z, Mandiyan V, Lax I, Schlessinger J. 2007. Structural basis for activation of the receptor tyrosine kinase KIT by stem cell factor. Cell 130: 323-334.
85. Zhang X, Gureasko J, Shen K, Cole PA, Kuriyan J. 2006. An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 125: 1137-1149.