The Complexity of Complexes in Signal Transduction

Biotechnology and Bioengineering

Volumn 84, Issue 7, 2003, Pages 783-794

  Hlavacek, William S ^a   Faeder, James R ^a   Blinov, Michael L ^a   Perelson, Alan S ^a   Goldstein, Byron ^a  

^a LOS ALAMOS NATIONAL LABORATORY   (United States)

Author keywords

Mathematical model; Multivalent binding; Receptor; Regulated recruitment; Signal transduction

Indexed keywords

CELLS; ENZYMES; MATHEMATICAL MODELS; NUCLEATION;

SIGNAL TRANSDUCTION;

BIOTECHNOLOGY;

CELL SURFACE RECEPTOR; PHOSPHOTRANSFERASE;

CHEMICAL MODIFICATION; COMPLEX FORMATION; DOWN REGULATION; LIGAND BINDING; MATHEMATICAL MODEL; PROTEIN PHOSPHORYLATION; REACTION ANALYSIS; REVIEW; SIGNAL TRANSDUCTION;

MODELS, BIOLOGICAL; PROTEIN BINDING; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, CELL SURFACE; RECEPTORS, IGE; SIGNAL TRANSDUCTION;

EID: 0346502078     PISSN: 00063592     EISSN: None     Source Type: Journal    
DOI: 10.1002/bit.10842     Document Type: Review

References (100)

1. Aebersold R, Mann M. 2003. Mass spectrometry-based proteomics. Nature 422:198-207.
2. Arkin AP. 2001. Synthetic cell biology. Curr Opinion Biotechnol 12:638-644.
3. Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer ELL. 2002. The Pfam protein families database. Nucleic Acids Res 30:276-280.
4. Batzer AG, Rotin D, Ureña JM, Skolnik EY, Schlessinger J. 1994. Hierarchy of binding sites for Grb2 and Shc on the epidermal growth factor receptor. Mol Cell Biol 14:5192-5201.
5. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. 2000. The protein data bank. Nucleic Acids Res 28:235-242.
6. Bhalla US, Iyengar R. 1999. Emergent properties of networks of biological signaling pathways. Science 283:381-387.
7. Blagoev B, Kratchmarova I, Ong S-E, Nielsen M, Foster LJ, Mann M. 2003. A proteomics strategy to elucidate functional protein-protein interáctions applied to EGF signaling. Nat Biotechnol 21:315-318.
8. Boguski MS, McCormick F. 1993. Proteins regulating Ras and its relatives. Nature 366:643-654.
9. Bonneau R, Strauss CEM, Rohl CA, Chivian D, Bradley P, Malmström L, Robertson T, Baker D. 2002. De novo prediction of three-dimensional structures for major protein families. J Mol Biol 322:65-78.
10. Bray D. 2003. Molecular prodigality. Science 299:1189-1190.
11. Bray D, Lay S. 1997. Computer-based analysis of the binding steps in protein complex formation. Proc Natl Acad Sci USA 94:13493-13498.
12. Bunnell SC, Hong DI, Kardon JR, Yamazaki T, McGlade CJ, Barr VA, Samelson LE. 2002. T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J Cell Biol 158:1263-1275.
13. Burack WR, Shaw AS. 2000. Signal transduction: Hanging on a scaffold. Curr Opinion Cell Biol 12:211-216.
14. Burack WR, Cheng AM, Shaw AS. 2002. Scaffolds, adaptors and linkers of TCR signaling: Theory and practice. Curr Opinion Immunol 14:312-316.
15. Cambier JC. 1995. Antigen and Fc receptor signaling: The awesome power of the immunoreceptor tyrosine-based activation motif (ITAM). J Immunol 155:3281-3285.
16. Chang L, Karin M. 2001. Mammalian MAP kinase signalling cascades. Nature 410:37-40.
17. 2+ or antibody activation. J Biol Chem 276:48670-48678.
18. Day ED. 1990. Advanced immunochemistry. 2nd edition. New York: Wiley-Liss.
19. DeLisi C. 1980. The biophysics of ligand-receptor interactions. Q Rev Biophys 13:201-230.
20. Dembo M, Golstein B. 1978. Theory of equilibrium binding of symmetric bivalent haptens to cell surface antibody: Application to histamine release from basophils. J Immunol 121:345-353.
21. Egan SE, Giddings BW, Brooks MW, Buday L, Sizeland AM, Weinberg RA. 1993. Association of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation. Nature 363:45-51.
22. Elion EA. 2001. The Ste5p scaffold. J Cell Sci 114:3967-3978.
23. Endy D, Brent R. 2001. Modelling cellular behaviour. Nature 409:391-395.
24. Faeder JR, Hlavacek WS, Reischl I, Blinov ML, Metzger H, Redondo A, Wofsy C, Goldstein B. 2003. Investigation of early events in FcεRI-mediated signaling using a detailed mathematical model. J Immunol 170:3769-3781.
25. Faulon J-L, Sault AG. 2001. Stochastic generator of chemical structure. 3. Reaction network generation. J Chem Inf Comput Sci 41:894-908.
26. Ferguson KM, Berger MB, Mendrola JM, Cho H-S, Leahy DJ, Lemmon MA. 2003. EGF activates its receptor by removing interactions that autoinhibit ectodomain dimerization. Mol Cell 11:507-517.
27. Ferrell JE Jr. 1998. How regulated protein translocation can produce switch-like responses. Trends Biochem Sci 23:461-465.
28. Fong DC, Brauweiler A, Minskoff SA, Bruhns P, Tamir I, Mellman I, Daeron M, Cambier JC. 2000. Mutational analysis reveals multiple distinct sites within Fcγ receptor IIB that function in inhibitory signaling. J Immunol 165:4453-4462.
29. Garrett TPJ, McKern NM, Lou M, Elleman TC, Adams TE, Lovrecz GO, Zhu H-J, Walker F, Frenkel MJ, Hoyne PA, Jorissen RN, Nice EC, Burgess AW, Ward CW. 2002. Crystal struture of a truncated epidermal growth factor receptor extracellular domain bound to transforming growth factor α. Cell 110:763-773.
30. Gillespie DT. 1976. General method for numerically simulating stochastic time evolution of coupled chemical reactions. J Comput Physics 22:403-434.
31. Gillespie DT. 1977. Exact stochastic simulation of coupled chemical reactions. J Phys Chem 81:2340-2361.
32. Gilman A, Arkin AP. 2002. Genetic "code": Representations and dynamical models of genetic components and networks. Ann Rev Genomics Hum Genet 3:341-369.
33. Goldstein B, Faeder JR, Hlavacek WS, Blinov ML, Redondo A, Wofsy C. 2002. Modeling the early signaling events mediated by FcεRI. Mol Immunol 38:1213-1219.
34. Goldstein B, Perelson AS. 1984. Equilibrium theory for the clustering of bivalent cell surface receptors by trivalent ligands: application to histamine release from basophils. Biophys J 45:1109-1123.
35. Harris NT, Goldstein B, Holowka D, Baird B. 1997. Altered patterns of tyrosine phosphorylation and Syk activation for sterically restricted cyclic dimers of IgE-FcεRI. Biochemistry 36:2237-2242.
36. Haugh JM, Lauffenburger DA. 1997. Physical modulation of intracellular signaling processes by locational regulation. Biophys J 72:2014-2031.
37. Haugh JM, Schooler K, Wells A, Wiley HS, Lauffenburger DA. 1999. Effect epidermanl growth factor receptor internalization on regulation of the phospholipase C-γ1 signaling pathway. J Biol Chem 274:8958-8965.
38. Hlavacek WS, Redondo A, Metzger H, Wofsy C, Goldstein B. 2001. Kinetic proofreading models for cell signaling predict ways to escape kinetic proofreading. Proc Natl Acad Sci USA 98:7295-7300.
39. Hlavacek WS, Redondo A, Wofsy C, Goldstein B. 2002. Kinetic proofreading in receptor-mediated transduction of cellular signals: Receptor aggregation, partially activated receptors, and cytosolic messengers. Bull Math Biol 64:887-911.
40. Hunter T. 1995. Protein kinases and phosphatases: The Yin and Yang of protein phosphorylation and signaling. Cell 80:225-236.
41. Hunter T. 2000. Signaling - 2000 and beyond. Cell 100:113-127.
42. Husi H, Ward MA, Choudhary JS, Blackstock WP, Grant SGN. 2000. Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat Neurosci 3:661-669.
43. Jamshidi N, Edwards JS, Fahland T, Church GM, Palsson BO. 2001. Dynamic simulation of the human red blood cell metabolic network. Bioinformatics 17:286-287.
44. Jiang X, Sorkin A. 2002. Coordinated traffic of Grb2 and Ras during epidermal growth factor receptor endocytosis visualized in living cells. Mol Biol Cell 13:1522-1535.
45. Jorissen RN, Walker F, Pouliot N, Garrett TPJ, Ward CW, Burgess AW. 2003. Epidermal growth factor receptor: Mechanisms of activation and signalling. Exp Cell Res 284:31-53.
46. Kersh EN, Shaw AS, Allen PM. 1998. Fidelity of T cell activation through multistep T cell receptor ζ phosphorylation. Science 281:572-575.
47. Kholodenko BN, Demin OV, Moehren G, Hoek JB. 1999. Quantification of short term signaling by the epidermal growth factor receptor. J Biol Chem 274:30169-30181.
48. Kholodenko BN, Hoek JB, Westerhoff HV. 2000. Why cytoplasmic signalling proteins should be recruited to cell membranes. Trends Cell Biol 10:173-178.
49. Kinet J-P. 1999. The high-affinity IgE receptor (FcεRI): from physiology to pathology. Ann Rev Immunol 17:931-972.
50. Kitano H. 2002. Computational systems biology. Nature 420:206-210.
51. Lanzavecchia A, Iezzi G, Viola A. 1999. From TCR engagement to T cell activation: A kinetic view of T cell behavior. Cell 96:1-4.
52. Le Novère N, Shimizu TS. 2001. STOCHSIM: Modelling of stochastic biomolecular processes. Bioinformatics 17:575-576.
53. Levchenko A, Bruck J, Sternberg PW. 2000. Scaffold proteins may biphasically affect the levels of mitogen-activated protein kinase signaling and reduce its threshold properties. Proc Natl Acad Sci USA 97:5818-5823.
54. Li N, Batzer A, Daly R, Yajnik V, Skolnik E, Chardin P, Bar-Sagi D, Margolis B, Schlessinger J. 1993. Guanine-nucleotide-releasing factor hSos1 binds to Grb2 and links receptor tyrosine kinase to Ras signalling. Nature 363:85-88.
55. Lin S, Cicala C, Scharenberg AM, Kinet J-P. 1996. The FcεRI subunit functions as an amplifier of FcεR-γ-mediated cell activation signals. Cell 85:985-995.
56. Liu Z-J, Haleem-Smith H, Chen H, Metzger H. 2001. Unexpected signals in a system subject to kinetic proofreading. Proc Natl Acad Sci USA 98:7289-7294.
57. Lowenstein EJ, Daly RJ, Batzer AG, Li W, Margolis B, Lammers R, Ullrich A, Skolnik EY, Bar-Sagi D, Schlessinger J. 1992. The SH2 and SH3 domain containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 70:431-442.
58. Macken CA, Perelson AS. 1985. Branching processes applied to cell surface aggregation phenomena. New York: Springer-Verlag.
59. Mann M, Jensen ON. 2003. Proteomic analysis of post-translational modifications. Nat Biotechnol 21:255-261.
60. March ME, Ravichandran K. 2002. Regulation of the immune response by SHIP. Semin Immunol 14:37-47.
61. McKeithan TW. 1995. Kinetic proofreading in T-cell receptor signal transduction. Proc Natl Acad Sci USA 92:5042-5046.
62. Meyer T, Teruel MN. 2003. Fluorescence imaging of signaling networks. Trends Cell Biol 13:101-106.
63. Morton-Firth CJ, Bray D. 1998. Predicting temporal fluctuations in an intracellular signalling pathway. J Theor Biol 192:117-128.
64. Nishimura R, Li W, Kashishian A, Mondino A, Zhou M, Cooper J, Schlessinger J. 1993. Two signaling molecules share a phosphotyrosine-containing binding site in the platelet-derived growth factor receptor. Mol Cell Biol 13:6889-6896.
65. Ogiso H, Ishitani R, Nureki O, Fukai S, Yamanaka M, Kim J-H, Saito K, Sakamoto A, Inoue M, Shirouzu M, Yokoyama S. 2002. Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains. Cell 110:775-787.
66. Okabayashi Y, Kido Y, Okutani T, Sugimoto Y, Sakaguchi K, Kasuga M. 1994. Tyrosines 1148 and 1173 of activated human epidermal growth factor receptors are binding sites of Shc in intact cells. J Biol Chem 269:18674-18678.
67. O'Rourke L, Ladbury JE. 2003. Specificity is complex and time consuming: Mutual exclusivity in tyrosine kinase-mediated signaling. Acc Chem Res 36:410-416.
68. Osborne MA, Zenner G, Lubinus M, Zhang X, Songyang Z, Cantley LC, Majerus P, Burn P, Kochan JP. 1996. The inositol 5′-phosphatase SHIP binds to immunoreceptor signaling motifs and responds to high affinity IgE receptor aggregation. J Biol Chem 271:29271-29278.
69. Paar JM, Harris NT, Holowka D, Baird B. 2002. Bivalent ligands with rigid double-stranded DNA spacers reveal structural constraints on signaling by FcεRI. J Immunol 169:856-864.
70. Pacini S, Valensin S, Telford JL, Ladbury J, Baldari CT. 2000. Temporally regulated assembly of a dynamic signaling complex associated with the activated TCR. Eur J Immunol 30:2620-2631.
71. Park S-H, Zarrinpar A, Lim WA. 2003. Rewiring MAP kinase pathways using alternative scaffold assembly mechanisms. Science 299:1061-1064.
72. Pawson T, Nash P. 2003. Assembly of cell regulatory systems through protein interaction domains. Science 300:445-452.
73. Pelicci G, Lanfrancone L, Grignani F, McGlade J, Cavallo F, Forni G, Nicoletti I, Grignani F, Pawson T, Pelicci PG. 1992. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 70:93-104.
74. Perelson AS. 1984. Some mathematical models of receptor clustering by multivalent ligands. In: Perelson AS, DeLisi C, Wiegel FW, editors. Cell surface dynamics: concepts and models. New York: Marcel Dekker. p 223-276.
75. Perelson AS, DeLisi C. 1980. Receptor clustering on a cell surface. I. Theory of receptor cross-linking by ligands bearing two chemically identical functional groups. Math Biosci 48:71-110.
76. Posner RG, Subramanian K, Goldstein B, Thomas J, Feder T, Holowka D, Baird B. 1995a. Simultaneous cross-linking by two nontriggering bivalent ligands causes synergistic signaling of IgE FcεRI complexes. J Immunol 155:3601-3609.
77. Posner RG, Wofsy C, Goldstein B. 1995b. The kinetics of bivalent ligand-bivalent receptor aggregation: Ring formation and the breakdown of the equivalent site approximation. Math Biosci 126:171-190.
78. Prehoda KE, Lim WA. 2002. How signaling proteins integrate multiple inputs: A comparison of N-WASP and Cdk2. Curr Opinion Cell Biol 14:149-154.
79. Priami C, Regev A, Shapiro E, Silverman W. 2001. Application of a stochastic name-passing calculus to representation and simulation of molecular processes. Inf Process Lett 80:25-31.
80. Ptashne M, Gann A. 2002. Genes & Signals. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
81. Rozakis-Adcock M, Fernley R, Wade J, Pawson T, Bowtell D. 1993. The SH2 and SH3 domains of mammalian Grb2 couple the EGF receptor to the Ras activator mSos1. Nature 363:83-85.
82. Rozakis-Adcock M, McGlade J, Mbamalu G, Pelicci G, Daly R, Li W, Batzer A, Thomas S, Brugge J, Pelicci PG, Schlessinger J, Pawson T. 1992. Association of the Shc and Grb2/Sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature 360:689-692.
83. ras. J Biol Chem 269:32621-32625.
84. Schlessinger J. 2000. Cell signaling by receptor tyrosine kinases. Cell 103:211-225.
85. Schoeberl B, Eichler-Jonsson C, Gilles ED, Müller G. 2002. Computational modeling of the dynamics of the MAP kinase cascade activated by surface and internalized EGF receptors. Nat Biotechnol 20:370-375.
86. Shen-Orr SS, Milo R, Mangan S, Alon U. 2002. Network motifs in the transcriptional regulation network of Escherichia coli. Nat Genet 31:64-68.
87. Shimaoka M, Xiao T, Liu J-H, Yang Y, Dong Y, Jun C-D, McCormack A, Zhang R, Joachimiak A, Takagi J, Wang J-H, Springer TA. 2003. Structures of the αL I domain and its complex with ICAM-1 reveal a shape-shifting pathway for integrin regulation. Cell 112:99-111.
88. Smith GR, Sternberg MJE. 2002. Prediction of protein-protein interactions by docking methods. Curr Opinion Struct Biol 12:28-35.
89. Taussig R, Ranganathan R, Ross EM, Gilman AG. 2002. Overview of the alliance for cellular signaling. Nature 420:703-706.
90. Thieffry D, Huerta AM, Pérez-Rueda E, Collado-Vides J. 1998. From specific gene regulation to genomic networks: A global analysis of transcriptional regulation in Escherichia coli. BioEssays 20:433-440.
91. Torigoe C, Goldstein B, Wofsy C, Metzger H. 1997. Shuttling of initiating kinase between discrete aggregates of the high affinity receptor for IgE regulates the cellular response. Proc Natl Acad Sci USA 94:1372-1377.
92. Torigoe C, Inman JK, Metzger H. 1998. An unusual mechanism for ligand antagonism. Science 281:568-572.
93. Tovchigrechko A, Wells CA, Vakser IA. 2002. Docking of protein models. Protein Sci 11:1888-1896.
94. Treisman R. 1996. Regulation of transcription by MAP kinase cascades. Curr Opinion Cell Biol 8:205-215.
95. Turner H, Kinet J-P. 1999. Signalling through the high-affinity IgE receptor FcεRI. Nature 402(suppl):B24-B30.
96. Ugi I, Bauer J, Bley K, Dengler A, Dietz A, Fontain E, Gruber B, Herges R, Knauer M, Reitsam K, Stein N. 1993. Computer-assisted solution of chemical problems - The historical development and the present state of the art of a new discipline of chemistry. Angew Chem Int Ed Engl 32:201-227.
97. Vogelstein B, Lane D, Levine AJ. 2000. Surfing the p53 network. Nature 408:307-310.
98. Wiley HS, Shvartsman SY, Lauffenburger DA. 2003. Computational modeling of the EGF-receptor system: A paradigm for systems biology. Trends Cell Biol 13:43-50.
99. Wofsy C, Torigoe C, Kent UM, Metzger H, Goldstein B. 1997. Exploiting the difference between intrinsic and extrinsic kinases: Implications for regulation of signaling by immunoreceptors. J Immunol 159:5984-5992.
100. Zhang J, Billingsley ML, Kincaid RL, Siraganian RP. 2000. Phosphorylation of Syk activation loop tyrosines is essential for Syk function: An in vivo study using a specific anti-Syk activation loop phosphotyrosine antibody. J Biol Chem 275:35442-35447.