1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Cell and Developmental Biology
  4. Volume 36, 2020
  5. Article

Annual Review of Cell and Developmental Biology

Volume 36, 2020

Processing Temporal Growth Factor Patterns by an Epidermal Growth Factor Receptor Network Dynamically Established in Space

Abstract

The proto-oncogenic epidermal growth factor (EGF) receptor (EGFR) is a tyrosine kinase whose sensitivity and response to growth factor signals that vary over time and space determine cellular behavior within a developing tissue. The molecular reorganization of the receptors on the plasma membrane and the enzyme-kinetic mechanisms of phosphorylation are key determinants that couple growth factor binding to EGFR signaling. To enable signal initiation and termination while simultaneously accounting for suppression of aberrant signaling, a coordinated coupling of EGFR kinase and protein tyrosine phosphatase activity is established through space by vesicular dynamics. The dynamical operation mode of this network enables not only time-varying growth factor sensing but also adaptation of the response depending on cellular context. By connecting spatially coupled enzymatic kinase/phosphatase processes and the corresponding dynamical systems description of the EGFR network, we elaborate on the general principles necessary for processing complex growth factor signals.

Keyword(s): collective computing, nonlinear dynamics, receptor tyrosine kinases, spatial cycles, spatially organized signaling, time-varying growth factors
Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-013020-103810
2020-10-06
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/36/1/annurev-cellbio-013020-103810.html?itemId=/content/journals/10.1146/annurev-cellbio-013020-103810&mimeType=html&fmt=ahah

Literature Cited

  1. Abo A, Pick E, Hall A, Totty N, Teahan CG, Segal AW 1991. Activation of the NADPH oxidase involves the small GTP-binding protein p21rac1. Nature 353:668–70
     [Google Scholar]
  2. Agazie YM, Hayman MJ. 2003. Molecular mechanism for a role of SHP2 in epidermal growth factor receptor signaling. Mol. Cell Biol. 23:7875–86
     [Google Scholar]
  3. Alonso A, Sasin J, Bottini N, Friedberg I, Friedberg I et al. 2004. Protein tyrosine phosphatases in the human genome. Cell 117:699–711
     [Google Scholar]
  4. Alvarado D, Klein DE, Lemmon MA 2010. Structural basis for negative cooperativity in growth factor binding to an EGF receptor. Cell 142:568–79
     [Google Scholar]
  5. Andersen JN, Mortensen OH, Peters GH, Drake PG, Iversen LF et al. 2001. Structural and evolutionary relationships among protein tyrosine phosphatase domains. Mol. Cell Biol. 21:7117–36
     [Google Scholar]
  6. Aoki K, Kondo Y, Naoki H, Hiratsuka T, Itoh RE, Matsuda M 2017. Propagating wave of ERK activation orients collective cell migration. Dev. Cell 43:305–17.e5
     [Google Scholar]
  7. Arteaga CL, Engelman JA. 2014. ERBB receptors: from oncogene discovery to basic science to mechanism-based cancer therapeutics. Cancer Cell 25:282–303
     [Google Scholar]
  8. Baass PC, Diguglielmo GM, Authier F, Posner BI, Bergeron JJM 1995. Compartmentalized signal transduction by receptor tyrosine kinases. Trends Cell Biol 5:465–70
     [Google Scholar]
  9. Bae YS, Kang SW, Seo MS, Baines IC, Tekle E et al. 1997. Epidermal growth factor (EGF)-induced generation of hydrogen peroxide: role in EGF receptor-mediated tyrosine phosphorylation. J. Biol. Chem. 272:217–21
     [Google Scholar]
  10. Bae YS, Sung JY, Kim OS, Kim YJ, Hur KC et al. 2000. Platelet-derived growth factor-induced H2O2 production requires the activation of phosphatidylinositol 3-kinase. J. Biol. Chem. 275:10527–31
     [Google Scholar]
  11. Bakker J, Spits M, Neefjes J, Berlin I 2017. The EGFR odyssey—from activation to destruction in space and time. J. Cell Sci. 130:4087–96
     [Google Scholar]
  12. Barr AJ, Ugochukwu E, Lee WH, King ON, Filippakopoulos P et al. 2009. Large-scale structural analysis of the classical human protein tyrosine phosphatome. Cell 136:352–63
     [Google Scholar]
  13. Baumdick M, Bruggemann Y, Schmick M, Xouri G, Sabet O et al. 2015. EGF-dependent re-routing of vesicular recycling switches spontaneous phosphorylation suppression to EGFR signaling. eLife 4:12223
     [Google Scholar]
  14. Baumdick M, Gelleri M, Uttamapinant C, Beranek V, Chin JW, Bastiaens PIH 2018. A conformational sensor based on genetic code expansion reveals an autocatalytic component in EGFR activation. Nat. Commun. 9:3847
     [Google Scholar]
  15. Bellot F, Moolenaar W, Kris R, Mirakhur B, Verlaan I et al. 1990. High-affinity epidermal growth factor binding is specifically reduced by a monoclonal antibody, and appears necessary for early responses. J. Cell Biol. 110:491–502
     [Google Scholar]
  16. Bennett AM, Hausdorff SF, O'Reilly AM, Freeman RM, Neel BG 1996. Multiple requirements for SHPTP2 in epidermal growth factor-mediated cell cycle progression. Mol. Cell. Biol. 16:1189–202
     [Google Scholar]
  17. Bienert GP, Schjoerring JK, Jahn TP 2006. Membrane transport of hydrogen peroxide. Biochim. Biophys. Acta Biomembr. 1758:994–1003
     [Google Scholar]
  18. Blum Y, Mikelson J, Dobrzynski M, Ryu H, Jacques MA et al. 2019. Temporal perturbation of ERK dynamics reveals network architecture of FGF2/MAPK signaling. Mol. Syst. Biol. 15:e8947
     [Google Scholar]
  19. Bohmer FD, Bohmer A, Obermeier A, Ullrich A 1995. Use of selective tyrosine kinase blockers to monitor growth-factor receptor dephosphorylation in intact cells. Anal. Biochem. 228:267–73
     [Google Scholar]
  20. Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K et al. 1992. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70:715–28
     [Google Scholar]
  21. Burgess AW. 2008. EGFR family: structure physiology signalling and therapeutic targets. Growth Factors 26:263–74
     [Google Scholar]
  22. Burgess AW, Cho HS, Eigenbrot C, Ferguson KM, Garrett TP et al. 2003. An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors. Mol. Cell 12:541–52
     [Google Scholar]
  23. Ceresa BP. 2006. Regulation of EGFR endocytic trafficking by rab proteins. Histol. Histopathol. 21:987–93
     [Google Scholar]
  24. Chen YR, Fu YN, Lin CH, Yang ST, Hu SF et al. 2006. Distinctive activation patterns in constitutively active and gefitinib-sensitive EGFR mutants. Oncogene 25:1205–15
     [Google Scholar]
  25. Choi SH, Mendrola JM, Lemmon MA 2007. EGF-independent activation of cell-surface EGF receptors harboring mutations found in gefitinib-sensitive lung cancer. Oncogene 26:1567–76
     [Google Scholar]
  26. 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 464:783–87
     [Google Scholar]
  27. Clayton AHA, Walker F, Orchard SG, Henderson C, Fuchs D et al. 2005. Ligand-induced dimer-tetramer transition during the activation of the cell surface epidermal growth factor receptor—a multidimensional microscopy analysis. J. Biol. Chem. 280:30392–99
     [Google Scholar]
  28. Coban O, Zanetti-Dominguez LC, Matthews DR, Rolfe DJ, Weitsman G et al. 2015. Effect of phosphorylation on EGFR dimer stability probed by single-molecule dynamics and FRET/FLIM. Biophys. J. 108:1013–26
     [Google Scholar]
  29. Collinet C, Stoter M, Bradshaw CR, Samusik N, Rink JC et al. 2010. Systems survey of endocytosis by multiparametric image analysis. Nature 464:243–49
     [Google Scholar]
  30. Conte A, Sigismund S. 2016. The ubiquitin network in the control of EGFR endocytosis and signaling. Prog. Mol. Biol. Transl. Sci. 141:225–76
     [Google Scholar]
  31. Cool DE, Tonks NK, Charbonneau H, Walsh KA, Fischer EH, Krebs EG 1989. cDNA isolated from a human T-cell library encodes a member of the protein-tyrosine-phosphatase family. PNAS 86:5257–61
     [Google Scholar]
  32. de Melker AA, van der Horst G, Borst J 2004. Ubiquitin ligase activity of c-Cbl guides the epidermal growth factor receptor into clathrin-coated pits by two distinct modes of Eps15 recruitment. J. Biol. Chem. 279:55465–73
     [Google Scholar]
  33. Defize LHK, Boonstra J, Meisenhelder J, Kruijer W, Tertoolen LGJ et al. 1989. Signal transduction by epidermal growth factor occurs through the subclass of high affinity receptors. J. Cell Biol. 109:2495–507
     [Google Scholar]
  34. Dehmelt L, Bastiaens PIH. 2010. Spatial organization of intracellular communication: insights from imaging. Nat. Rev. Mol. Cell Biol. 11:440–52
     [Google Scholar]
  35. den Hartigh JC, van Bergen en Henegouwen PM, Verkleij AJ, Boonstra J 1992. The EGF receptor is an actin-binding protein. J. Cell Biol. 119:349–55
     [Google Scholar]
  36. Dykes SS, Steffan JJ, Cardelli JA 2017. Lysosome trafficking is necessary for EGF-driven invasion and is regulated by p38 MAPK and Na+/H+ exchangers. BMC Cancer 17:672
     [Google Scholar]
  37. Ekstrand AJ, Sugawa N, James CD, Collins VP 1992. Amplified and rearranged epidermal growth factor receptor genes in human glioblastomas reveal deletions of sequences encoding portions of the N- and/or C-terminal tails. PNAS 89:4309–13
     [Google Scholar]
  38. Er EE, Mendoza MC, Mackey AM, Rameh LE, Blenis J 2013. AKT facilitates EGFR trafficking and degradation by phosphorylating and activating PIKfyve. Sci. Signal. 6:ra45
     [Google Scholar]
  39. Falls DL. 2003. Neuregulins: functions, forms, and signaling strategies. Exp. Cell Res. 284:14–30
     [Google Scholar]
  40. Ferguson KM, Berger MB, Mendrola JM, Cho HS, Leahy DJ, Lemmon MA 2003. EGF activates its receptor by removing interactions that autoinhibit ectodomain dimerization. Mol. Cell 11:507–17
     [Google Scholar]
  41. Fischer E, Charbonneau H, Tonks N 1991. Protein tyrosine phosphatases: a diverse family of intracellular and transmembrane enzymes. Science 253:401–6
     [Google Scholar]
  42. Freed DM, Bessman NJ, Kiyatkin A, Salazar-Cavazos E, Byrne PO et al. 2017. EGFR ligands differentially stabilize receptor dimers to specify signaling kinetics. Cell 171:683–95.e18
     [Google Scholar]
  43. Fujiwara TK, Iwasawa K, Kalay Z, Tsunoyama TA, Watanabe Y et al. 2016. Confined diffusion of transmembrane proteins and lipids induced by the same actin meshwork lining the plasma membrane. Mol. Biol. Cell 27:1101–19
     [Google Scholar]
  44. Garrett TP, McKern NM, Lou M, Elleman TC, Adams TE et al. 2002. Crystal structure of a truncated epidermal growth factor receptor extracellular domain bound to transforming growth factor α. Cell 110:763–73
     [Google Scholar]
  45. Goh LK, Huang F, Kim W, Gygi S, Sorkin A 2010. Multiple mechanisms collectively regulate clathrin-mediated endocytosis of the epidermal growth factor receptor. J. Cell Biol. 189:871–83
     [Google Scholar]
  46. Goh LK, Sorkin A. 2013. Endocytosis of receptor tyrosine kinases. Cold Spring Harb. Perspect. Biol. 5:a017459
     [Google Scholar]
  47. Grecco HE, Schmick M, Bastiaens PI 2011. Signaling from the living plasma membrane. Cell 144:897–909
     [Google Scholar]
  48. Grimes ML, Zhou J, Beattie EC, Yuen EC, Hall DE et al. 1996. Endocytosis of activated TrkA: evidence that nerve growth factor induces formation of signaling endosomes. J. Neurosci. 16:7950–64
     [Google Scholar]
  49. Gusenbauer S, Vlaicu P, Ullrich A 2013. HGF induces novel EGFR functions involved in resistance formation to tyrosine kinase inhibitors. Oncogene 32:3846–56
     [Google Scholar]
  50. Haglund K, Shimokawa N, Szymkiewicz I, Dikic I 2002. Cbl-directed monoubiquitination of CIN85 is involved in regulation of ligand-induced degradation of EGF receptors. PNAS 99:12191–96
     [Google Scholar]
  51. Haj FG, Verveer PJ, Squire A, Neel BG, Bastiaens PI 2002. Imaging sites of receptor dephosphorylation by PTP1B on the surface of the endoplasmic reticulum. Science 295:1708–11
     [Google Scholar]
  52. Hanafusa H, Ishikawa K, Kedashiro S, Saigo T, Iemura S et al. 2011. Leucine-rich repeat kinase LRRK1 regulates endosomal trafficking of the EGF receptor. Nat. Commun. 2:158
     [Google Scholar]
  53. Haque A, Andersen JN, Salmeen A, Barford D, Tonks NK 2011. Conformation-sensing antibodies stabilize the oxidized form of PTP1B and inhibit its phosphatase activity. Cell 147:185–98
     [Google Scholar]
  54. Haslekås C, Breen K, Pedersen KW, Johannessen LE, Stang E, Madshus IH 2005. The inhibitory effect of ErbB2 on epidermal growth factor-induced formation of clathrin-coated pits correlates with retention of epidermal growth factor receptor-ErbB2 oligomeric complexes at the plasma membrane. Mol. Biol. Cell 16:5832–42
     [Google Scholar]
  55. Henne WM, Buchkovich NJ, Emr SD 2011. The ESCRT pathway. Dev. Cell 21:77–91
     [Google Scholar]
  56. Hiratsuka T, Fujita Y, Naoki H, Aoki K, Kamioka Y, Matsuda M 2015. Intercellular propagation of extracellular signal-regulated kinase activation revealed by in vivo imaging of mouse skin. eLife 4:e05178
     [Google Scholar]
  57. Holowka D, Baird B. 2017. Mechanisms of epidermal growth factor receptor signaling as characterized by patterned ligand activation and mutational analysis. Biochim. Biophys. Acta Biomembr. 1859:1430–35
     [Google Scholar]
  58. Huang F, Kirkpatrick D, Jiang X, Gygi S, Sorkin A 2006. Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol. Cell 21:737–48
     [Google Scholar]
  59. Huang YJ, Bharill S, Karandur D, Peterson SM, Marita M et al. 2016. Molecular basis for multimerization in the activation of the epidermal growth factor receptor. eLife 5:e14107
     [Google Scholar]
  60. Ibach J, Radon Y, Gelleri M, Sonntag MH, Brunsveld L et al. 2015. Single particle tracking reveals that EGFR signaling activity is amplified in clathrin-coated pits. PLOS ONE 10:e0143162
     [Google Scholar]
  61. Ichinose J, Murata M, Yanagida T, Sako Y 2004. EGF signalling amplification induced by dynamic clustering of EGFR. Biochem. Biophys. Res. Commun. 324:1143–49
     [Google Scholar]
  62. Jiang X, Huang F, Marusyk A, Sorkin A 2003. Grb2 regulates internalization of EGF receptors through clathrin-coated pits. Mol. Biol. Cell 14:858–70
     [Google Scholar]
  63. Jura N, Endres NF, Engel K, Deindl S, Das R et al. 2009. Mechanism for activation of the EGF receptor catalytic domain by the juxtamembrane segment. Cell 137:1293–307
     [Google Scholar]
  64. Kim Y, Li ZM, Apetri M, Luo BB, Settleman JE, Anderson KS 2012. Temporal resolution of autophosphorylation for normal and oncogenic forms of EGFR and differential effects of gefitinib. Biochemistry 51:5212–22
     [Google Scholar]
  65. Kleiman LB, Maiwald T, Conzelmann H, Lauffenburger DA, Sorger PK 2011. Rapid phospho-turnover by receptor tyrosine kinases impacts downstream signaling and drug binding. Mol. Cell 43:723–37
     [Google Scholar]
  66. Konturek JW, Bielanski W, Konturek SJ, Bogdal J, Oleksy J 1989. Distribution and release of epidermal growth factor in man. Gut 30:1194–200
     [Google Scholar]
  67. Koseska A, Bastiaens PI. 2017. Cell signaling as a cognitive process. EMBO J 36:568–82
     [Google Scholar]
  68. Kovacs E, Das R, Wang Q, Collier TS, Cantor A et al. 2015. Analysis of the role of the C-terminal tail in the regulation of the epidermal growth factor receptor. Mol. Cell. Biol. 35:3083–102
     [Google Scholar]
  69. Kusumi A, Nakada C, Ritchie K, Murase K, Suzuki K et al. 2005. Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu. Rev. Biophys. Biomol. Struct. 34:351–78
     [Google Scholar]
  70. Kusumi A, Sako Y. 1996. Cell surface organization by the membrane skeleton. Curr. Opin. Cell Biol. 8:566–74
     [Google Scholar]
  71. Laketa V, Zarbakhsh S, Traynor-Kaplan A, MacNamara A, Subramanian D et al. 2014. PIP3 induces the recycling of receptor tyrosine kinases. Sci. Signal. 7:ra5
     [Google Scholar]
  72. Lax I, Bellot F, Howk R, Ullrich A, Givol D, Schlessinger J 1989. Functional analysis of the ligand binding site of EGF-receptor utilizing chimeric chicken/human receptor molecules. EMBO J 8:421–27
     [Google Scholar]
  73. Lechleider RJ, Sugimoto S, Bennett AM, Kashishian AS, Cooper JA et al. 1993. Activation of the SH2-containing phosphotyrosine phosphatase SH-PTP2 by its binding site, phosphotyrosine 1009, on the human platelet-derived growth factor receptor. J. Biol. Chem. 268:21478–81
     [Google Scholar]
  74. Lee SR, Kwon KS, Kim SR, Rhee SG 1998. Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. J. Biol. Chem. 273:15366–72
     [Google Scholar]
  75. Lemmon MA, Schlessinger J, Ferguson KM 2014. The EGFR family: not so prototypical receptor tyrosine kinases. Cold Spring Harb. Perspect. Biol. 6:a020768
     [Google Scholar]
  76. Levkowitz G, Waterman H, Ettenberg SA, Katz M, Tsygankov AY et al. 1999. Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol. Cell 4:1029–40
     [Google Scholar]
  77. Liang SI, van Lengerich B, Eichel K, Cha M, Patterson DM et al. 2018. Phosphorylated EGFR dimers are not sufficient to activate Ras. Cell Rep 22:2593–600
     [Google Scholar]
  78. Liu F, Chernoff J. 1997. Protein tyrosine phosphatase 1B interacts with and is tyrosine phosphorylated by the epidermal growth factor receptor. Biochem. J. 327:139–45
     [Google Scholar]
  79. Liu P, Cleveland TE, Bouyain S, Byrne PO, Longo PA, Leahy DJ 2012. A single ligand is sufficient to activate EGFR dimers. PNAS 109:10861–66
     [Google Scholar]
  80. Macdonald JL, Pike LJ. 2008. Heterogeneity in EGF-binding affinities arises from negative cooperativity in an aggregating system. PNAS 105:112–17
     [Google Scholar]
  81. Macdonald-Obermann JL, Pike LJ. 2014. Different epidermal growth factor (EGF) receptor ligands show distinct kinetics and biased or partial agonism for homodimer and heterodimer formation. J. Biol. Chem. 289:26178–88
     [Google Scholar]
  82. Marmor MD, Yarden Y. 2004. Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene 23:2057–70
     [Google Scholar]
  83. Masip ME, Huebinger J, Christmann J, Sabet O, Wehner F et al. 2016. Reversible cryo-arrest for imaging molecules in living cells at high spatial resolution. Nat. Methods 13:665–72
     [Google Scholar]
  84. Meng TC, Buckley DA, Galic S, Tiganis T, Tonks NK 2004. Regulation of insulin signaling through reversible oxidation of the protein-tyrosine phosphatases TC45 and PTP1B. J. Biol. Chem. 279:37716–25
     [Google Scholar]
  85. Mettlen M, Chen PH, Srinivasan S, Danuser G, Schmid SL 2018. Regulation of clathrin-mediated endocytosis. Annu. Rev. Biochem. 87:871–96
     [Google Scholar]
  86. Miaczynska M, Pelkmans L, Zerial M 2004. Not just a sink: endosomes in control of signal transduction. Curr. Opin. Cell Biol. 16:400–6
     [Google Scholar]
  87. Miettinen PJ, Berger JE, Meneses J, Phung Y, Pedersen RA et al. 1995. Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature 376:337–41
     [Google Scholar]
  88. Miettinen PJ, Chin JR, Shum L, Slavkin HC, Shuler CF et al. 1999. Epidermal growth factor receptor function is necessary for normal craniofacial development and palate closure. Nat. Genet. 22:69–73
     [Google Scholar]
  89. Needham SR, Roberts SK, Arkhipov A, Mysore VP, Tynan CJ et al. 2016. EGFR oligomerization organizes kinase-active dimers into competent signalling platforms. Nat. Commun. 7:13307
     [Google Scholar]
  90. Nomura M, Shigematsu H, Li L, Suzuki M, Takahashi T et al. 2007. Polymorphisms, mutations, and amplification of the EGFR gene in non-small cell lung cancers. PLOS Med 4:e125
     [Google Scholar]
  91. Odaka M, Kohda D, Lax I, Schlessinger J, Inagaki F 1997. Ligand-binding enhances the affinity of dimerization of the extracellular domain of the epidermal growth factor receptor. J. Biochem. 122:116–21
     [Google Scholar]
  92. Offterdinger M, Bastiaens PI. 2008. Prolonged EGFR signaling by ERBB2-mediated sequestration at the plasma membrane. Traffic 9:147–55
     [Google Scholar]
  93. Offterdinger M, Georget V, Girod A, Bastiaens PIH 2004. Imaging phosphorylation dynamics of the epidermal growth factor receptor. J. Biol. Chem. 279:36972–81
     [Google Scholar]
  94. Ogiso H, Ishitani R, Nureki O, Fukai S, Yamanaka M et al. 2002. Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains. Cell 110:775–87
     [Google Scholar]
  95. Osherov N, Levitzki A. 1994. Epidermal-growth-factor-dependent activation of the src-family kinases. Eur. J. Biochem. 225:1047–53
     [Google Scholar]
  96. Ozer BH, Wiepz GJ, Bertics PJ 2010. Activity and cellular localization of an oncogenic glioblastoma multiforme-associated EGF receptor mutant possessing a duplicated kinase domain. Oncogene 29:855–64
     [Google Scholar]
  97. Pasquale EB. 2010. Eph receptors and ephrins in cancer: bidirectional signalling and beyond. Nat. Rev. Cancer 10:165–80
     [Google Scholar]
  98. Paulsen CE, Truong TH, Garcia FJ, Homann A, Gupta V et al. 2012. Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity. Nat. Chem. Biol. 8:57–64
     [Google Scholar]
  99. Pike LJ. 2012. Negative co-operativity in the EGF receptor. Biochem. Soc. Trans. 40:15–19
     [Google Scholar]
  100. Pines G, Kostler WJ, Yarden Y 2010. Oncogenic mutant forms of EGFR: lessons in signal transduction and targets for cancer therapy. FEBS Lett 584:2699–706
     [Google Scholar]
  101. Rahi SJ, Larsch J, Pecani K, Katsov AY, Mansouri N et al. 2017. Oscillatory stimuli differentiate adapting circuit topologies. Nat. Methods 14:1010–16
     [Google Scholar]
  102. Rappoport JZ, Simon SM. 2009. Endocytic trafficking of activated EGFR is AP-2 dependent and occurs through preformed clathrin spots. J. Cell Sci. 122:1301–5
     [Google Scholar]
  103. Rashid S, Pilecka I, Torun A, Olchowik M, Bielinska B, Miaczynska M 2009. Endosomal adaptor proteins APPL1 and APPL2 are novel activators of β-catenin/TCF-mediated transcription. J. Biol. Chem. 284:18115–28
     [Google Scholar]
  104. Red Brewer M, Yun CH, Lai D, Lemmon MA, Eck MJ, Pao W 2013. Mechanism for activation of mutated epidermal growth factor receptors in lung cancer. PNAS 110: E3595–604. Erratum. 2013 PNAS 110.20344
     [Google Scholar]
  105. Reynolds AR, Tischer C, Verveer PJ, Rocks O, Bastiaens PI 2003. EGFR activation coupled to inhibition of tyrosine phosphatases causes lateral signal propagation. Nat. Cell Biol. 5:447–53
     [Google Scholar]
  106. Rhee SG, Bae YS, Lee S-R, Kwon J 2000. Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Sci. Signal.2000:pe1
     [Google Scholar]
  107. Rink J, Ghigo E, Kalaidzidis Y, Zerial M 2005. Rab conversion as a mechanism of progression from early to late endosomes. Cell 122:735–49
     [Google Scholar]
  108. Rowinsky EK. 2004. The erbB family: targets for therapeutic development against cancer and therapeutic strategies using monoclonal antibodies and tyrosine kinase inhibitors. Annu. Rev. Med. 55:433–57
     [Google Scholar]
  109. Ruff SJ, Chen K, Cohen S 1997. Peroxovanadate induces tyrosine phosphorylation of multiple signaling proteins in mouse liver and kidney. J. Biol. Chem. 272:1263–67
     [Google Scholar]
  110. Ryu H, Chung M, Dobrzyński M, Fey D, Blum Y et al. 2015. Frequency modulation of ERK activation dynamics rewires cell fate. Mol. Syst. Biol 11:838 Erratum. 2016 Mol. Syst. Biol 12:866
     [Google Scholar]
  111. Salazar G, Gonzalez A. 2002. Novel mechanism for regulation of epidermal growth factor receptor endocytosis revealed by protein kinase A inhibition. Mol. Biol. Cell 13:1677–93
     [Google Scholar]
  112. Salazar-Cavazos E, Nitta CF, Mitra ED, Wilson BS, Lidke KA et al. 2020. Multisite EGFR phosphorylation is regulated by adaptor protein abundances and dimer lifetimes. Mol. Biol. Cell 31:7695–708
     [Google Scholar]
  113. Salmeen A, Andersen JN, Myers MP, Meng TC, Hinks JA et al. 2003. Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423:769–73
     [Google Scholar]
  114. Sato K, Sato A, Aoto M, Fukami Y 1995. c-Src phosphorylates epidermal growth factor receptor on tyrosine 845. Biochem. Biophys. Res. Commun. 215:1078–87
     [Google Scholar]
  115. Schenck A, Goto-Silva L, Collinet C, Rhinn M, Giner A et al. 2008. The endosomal protein Appl1 mediates Akt substrate specificity and cell survival in vertebrate development. Cell 133:486–97
     [Google Scholar]
  116. Schieber M, Chandel NS. 2014. ROS function in redox signaling and oxidative stress. Curr. Biol. 24:R453–62
     [Google Scholar]
  117. Schmidt MHH, Dikic I. 2005. The Cbl interactome and its functions. Nat. Rev. Mol. Cell Biol. 6:907–18
     [Google Scholar]
  118. Shan Y, Eastwood MP, Zhang X, Kim ET, Arkhipov A et al. 2012. Oncogenic mutations counteract intrinsic disorder in the EGFR kinase and promote receptor dimerization. Cell 149:860–70
     [Google Scholar]
  119. Sharma SV, Bell DW, Settleman J, Haber DA 2007. Epidermal growth factor receptor mutations in lung cancer. Nat. Rev. Cancer 7:169–81
     [Google Scholar]
  120. Sibilia M, Kroismayr R, Lichtenberger BM, Natarajan A, Hecking M, Holcmann M 2007. The epidermal growth factor receptor: from development to tumorigenesis. Differentiation 75:770–87
     [Google Scholar]
  121. Sibilia M, Wagner EF. 1995. Strain-dependent epithelial defects in mice lacking the Egf receptor. Science 269:234–38
     [Google Scholar]
  122. Singh AB, Harris RC. 2005. Autocrine, paracrine and juxtacrine signaling by EGFR ligands. Cell Signal 17:1183–93
     [Google Scholar]
  123. Sorkin A, Mazzotti M, Sorkina T, Scotto L, Beguinot L 1996. Epidermal growth factor receptor interaction with clathrin adaptors is mediated by the Tyr974-containing internalization motif. J. Biol. Chem. 271:13377–84
     [Google Scholar]
  124. Sorkin A, McClure M, Huang FT, Carter R 2000. Interaction of EGF receptor and Grb2 in living cells visualized by fluorescence resonance energy transfer (FRET) microscopy. Curr. Biol. 10:1395–98
     [Google Scholar]
  125. Spencer NY, Engelhardt JF. 2014. The basic biology of redoxosomes in cytokine-mediated signal transduction and implications for disease-specific therapies. Biochemistry 53:1551–64
     [Google Scholar]
  126. Stallaert W, Bruggemann Y, Sabet O, Baak L, Gattiglio M, Bastiaens PIH 2018. Contact inhibitory Eph signaling suppresses EGF-promoted cell migration by decoupling EGFR activity from vesicular recycling. Sci. Signal. 11:eaat0114
     [Google Scholar]
  127. Stang E, Johannessen LE, Knardal SL, Madshus IH 2000. Polyubiquitination of the epidermal growth factor receptor occurs at the plasma membrane upon ligand-induced activation. J. Biol. Chem. 275:13940–47
     [Google Scholar]
  128. Stanoev A, Mhamane A, Schuermann KC, Grecco HE, Stallaert W et al. 2018. Interdependence between EGFR and phosphatases spatially established by vesicular dynamics generates a growth factor sensing and responding network. Cell Syst 7:295–309.e11
     [Google Scholar]
  129. Stanoev A, Nandan AP, Koseska A 2020. Organization at criticality enables processing of time-varying signals by receptor networks. Mol. Syst. Biol. 16:e8870
     [Google Scholar]
  130. Strogatz SH. 2018. Nonlinear Dynamics and Chaos: With Applications to Physics, Biology, Chemistry, and Engineering Boca Raton, FL: CRC Press
  131. Sugimoto S, Lechleider RJ, Shoelson SE, Neel BG, Walsh CT 1993. Expression, purification, and characterization of SH2-containing protein-tyrosine-phosphatase, SH-PTP2. J. Biol. Chem. 268:22771–76
     [Google Scholar]
  132. Suh YA, Arnold RS, Lassegue B, Shi J, Xu XX et al. 1999. Cell transformation by the superoxide-generating oxidase Mox1. Nature 401:79–82
     [Google Scholar]
  133. Sweeney C, Carraway KL. 2000. Ligand discrimination by ErbB receptors: differential signaling through differential phosphorylation site usage. Oncogene 19:5568–73
     [Google Scholar]
  134. Tarcic G, Boguslavsky SK, Wakim J, Kiuchi T, Liu A et al. 2009. An unbiased screen identifies DEP-1 tumor suppressor as a phosphatase controlling EGFR endocytosis. Curr. Biol. 19:1788–98
     [Google Scholar]
  135. Thien CB, Langdon WY. 2001. Cbl: many adaptations to regulate protein tyrosine kinases. Nat. Rev. Mol. Cell Biol. 2:294–307
     [Google Scholar]
  136. Threadgill DW, Dlugosz AA, Hansen LA, Tennenbaum T, Lichti U et al. 1995. Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269:230–34
     [Google Scholar]
  137. Tiganis T, Bennett AM, Ravichandran KS, Tonks NK 1998. Epidermal growth factor receptor and the adaptor protein p52Shc are specific substrates of T-cell protein tyrosine phosphatase. Mol. Cell Biol. 18:1622–34
     [Google Scholar]
  138. Tischer C, Bastiaens PI. 2003. Lateral phosphorylation propagation: an aspect of feedback signalling. Nat. Rev. Mol. Cell Biol. 4:971–74
     [Google Scholar]
  139. Tonks NK. 2006. Protein tyrosine phosphatases: from genes, to function, to disease. Nat. Rev. Mol. Cell Biol. 7:833–46
     [Google Scholar]
  140. Tonks NK, Diltz CD, Fischer EH 1988. Characterization of the major protein-tyrosine-phosphatases of human placenta. J. Biol. Chem. 263:6731–37
     [Google Scholar]
  141. Tonks NK, Neel BG. 1996. From form to function: signaling by protein tyrosine phosphatases. Cell 87:365–68
     [Google Scholar]
  142. Tsutsumi R, Harizanova J, Stockert R, Schroder K, Bastiaens PIH, Neel BG 2017. Assay to visualize specific protein oxidation reveals spatio-temporal regulation of SHP2. Nat. Commun. 8:466
     [Google Scholar]
  143. Valley CC, Arndt-Jovin DJ, Karedla N, Steinkamp MP, Chizhik AI et al. 2015. Enhanced dimerization drives ligand-independent activity of mutant epidermal growth factor receptor in lung cancer. Mol. Biol. Cell 26:4087–99
     [Google Scholar]
  144. Vanlandingham PA, Ceresa BP. 2009. Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration. J. Biol. Chem. 284:12110–24
     [Google Scholar]
  145. Vieira AV, Lamaze C, Schmid SL 1996. Control of EGF receptor signaling by clathrin-mediated endocytosis. Science 274:2086–89
     [Google Scholar]
  146. Villasenor R, Kalaidzidis Y, Zerial M 2016. Signal processing by the endosomal system. Curr. Opin. Cell Biol. 39:53–60
     [Google Scholar]
  147. Villasenor R, Nonaka H, Del Conte-Zerial P, Kalaidzidis Y, Zerial M 2015. Regulation of EGFR signal transduction by analogue-to-digital conversion in endosomes. eLife 4:e06156
     [Google Scholar]
  148. Wang J, Ren J, Wu B, Feng S, Cai G et al. 2015. Activation of Rab8 guanine nucleotide exchange factor Rabin8 by ERK1/2 in response to EGF signaling. PNAS 112:148–53
     [Google Scholar]
  149. Waterman H, Katz M, Rubin C, Shtiegman K, Lavi S et al. 2002. A mutant EGF-receptor defective in ubiquitylation and endocytosis unveils a role for Grb2 in negative signaling. EMBO J 21:303–13
     [Google Scholar]
  150. Wilson KJ, Gilmore JL, Foley J, Lemmon MA, Riese DJ 2009. Functional selectivity of EGF family peptide growth factors: implications for cancer. Pharmacol. Ther. 122:1–8
     [Google Scholar]
  151. Wofsy C, Goldstein B, Lund K, Wiley HS 1992. Implications of epidermal growth factor (EGF) induced egf receptor aggregation. Biophys. J. 63:98–110
     [Google Scholar]
  152. Wouters FS, Bastiaens PIH. 1999. Fluorescence lifetime imaging of receptor tyrosine kinase activity in cells. Curr. Biol. 9:1127–30
     [Google Scholar]
  153. Yao Z, Darowski K, St-Denis N, Wong V, Offensperger F et al. 2017. A global analysis of the receptor tyrosine kinase-protein phosphatase interactome. Mol. Cell 65:347–60
     [Google Scholar]
  154. Yarden Y, Sliwkowski MX. 2001. Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2:127–37
     [Google Scholar]
  155. Yu FS, Yin J, Xu K, Huang J 2010. Growth factors and corneal epithelial wound healing. Brain Res. Bull. 81:229–35
     [Google Scholar]
  156. Yuan T, Wang Y, Zhao ZJ, Gu H 2010. Protein-tyrosine phosphatase PTPN9 negatively regulates ErbB2 and epidermal growth factor receptor signaling in breast cancer cells. J. Biol. Chem. 285:14861–70
     [Google Scholar]
  157. Yudushkin IA, Schleifenbaum A, Kinkhabwala A, Neel BG, Schultz C, Bastiaens PI 2007. Live-cell imaging of enzyme-substrate interaction reveals spatial regulation of PTP1B. Science 315:115–19
     [Google Scholar]
  158. Yun CH, Boggon TJ, Li Y, Woo MS, Greulich H et al. 2007. Structures of lung cancer-derived EGFR mutants and inhibitor complexes: mechanism of activation and insights into differential inhibitor sensitivity. Cancer Cell 11:217–27
     [Google Scholar]
  159. Zanetti-Domingues LC, Korovesis D, Needham SR, Tynan CJ, Sagawa S et al. 2018. The architecture of EGFR's basal complexes reveals autoinhibition mechanisms in dimers and oligomers. Nat. Commun. 9:4325
     [Google Scholar]
  160. 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 125:1137–49
     [Google Scholar]
/content/journals/10.1146/annurev-cellbio-013020-103810
Loading
Processing Temporal Growth Factor Patterns by an Epidermal Growth Factor Receptor Network Dynamically Established in Space
Annual Review of Cell and Developmental Biology 36, 359 (2020); https://doi.org/10.1146/annurev-cellbio-013020-103810
/content/journals/10.1146/annurev-cellbio-013020-103810
/content/journals/10.1146/annurev-cellbio-013020-103810
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error