A Bipolar Clamp Mechanism for Activation of Jak-Family Protein Tyrosine Kinases

PLoS Computational Biology

Volumn 5, Issue 4, 2009, Pages

  Barua, Dipak ^a   Faeder, James R ^b   Haugh, Jason M ^a  

^a North Carolina State University   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL MEMBRANES; CHEMICAL ACTIVATION; DIMERS; ENZYMES; SIGNAL TRANSDUCTION;

CELL SURFACE RECEPTORS; CYTOKINES; GROWTH FACTOR; JANUS KINASE; KINASE FAMILY; PROTEIN TYROSINE KINASE; RECEPTOR COMPLEX; RECEPTORS PROTEINS; SRC HOMOLOGY 2; SRC HOMOLOGY 2 DOMAINS;

PHOSPHORYLATION;

GROWTH HORMONE RECEPTOR; JANUS KINASE; PROTEIN TYROSINE PHOSPHATASE SHP; SH2BPSM1 PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ARTICLE; CLAMP; COMBINATORIAL CHEMISTRY; DIMERIZATION; KINETICS; MOLECULE; PHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSACTIVATION; BINDING SITE; BIOLOGICAL MODEL; CHEMICAL MODEL; CHEMISTRY; COMPUTER SIMULATION; ENZYME ACTIVATION; METABOLISM; PHYSIOLOGY; PROTEIN BINDING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BINDING SITES; COMPUTER SIMULATION; ENZYME ACTIVATION; JANUS KINASES; MODELS, BIOLOGICAL; MODELS, CHEMICAL; PHOSPHORYLATION; PROTEIN BINDING; SIGNAL TRANSDUCTION;

EID: 66249114051     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000364     Document Type: Article

References (36)

1. Lanning NJ, Carter-Su C (2006) Recent advances in growth hormone signaling. Rev Endocr Metab Disord 7: 225-235.
2. Argetsinger LS, Campbell GS, Yang XN, Witthuhn BA, Silvennoinen O, et al. (1993) Identification of Jak2 as a growth-hormone receptor-associated tyrosine kinase. Cell 74: 237-244.
3. Van der Kuur JA, Wang XY, Zhang LY, Campbell GS, Allevato G, et al. (1994) Domains of the growth-hormone receptor required for association and activation of Jak2 tyrosine kinase. J Biol Chem 269: 21709-21717.
4. Frank SJ, Yi W, Zhao Y, Goldsmith JF, Gilliland G, et al. (1995) Regions of the JAK2 tyrosine kinase required for coupling to the growth hormone receptor. J Biol Chem 270: 14776-14785.
5. Wells JA (1996) Binding in the growth hormone receptor complex. Proc Natl Acad Sci U S A 93: 1-6.
6. Smit LS, Meyer DJ, Billestrup N, Norstedt G, Schwartz J, et al. (1996) The role of the growth hormone (GH) receptor and JAK1 and JAK2 kinases in the activation of Stats 1, 3, and 5 by GH. Mol Endocrinol 10: 519-533.
7. Yasukawa H, Misawa H, Sakamoto H, Masuhara M, Sasaki A, et al. (1999) The JAK-binding protein JAB inhibits Janus tyrosine kinase activity through binding in the activation loop. EMBO J 18: 1309-1320.
8. Ungureanu D, Saharinen P, Junttila I, Hilton DJ, Silvennoinen O (2002) Regulation of Jak2 through the ubiquitin-proteasome pathway involves phosphorylation of Jak2 on Y1007 and interaction with SOCS-1. Mol Cell Biol 22: 3316-3326.
9. Rui L, Mathews L, Hotta K, Gustafson T, Carter-Su C (1997) Identification of SH2-Bb as a substrate of the tyrosine kinase JAK2 involved in growth hormone signaling. Mol Cell Biol 17: 6633-6644.
10. Rui L, Carter-Su C (1999) Identification of SH2-Bb as a potent cytoplasmic activator of the tyrosine kinase Janus kinase 2. Proc Natl Acad Sci U S A 96: 7172-7177.
11. Yousaf N, Deng YP, Kang YH, Riedel H (2001) Four PSM/SH2-B alternative splice variants and their differential roles in mitogenesis. J Biol Chem 276: 40940-40948.
12. O'Brien KB, O'Shea JJ, Carter-Su C (2002) SH2-B family members differentially regulate JAK family tyrosine kinases. J Biol Chem 277: 8673-8681.
13. Kurzer JH, Argetsinger LS, Zhou Y-J, Kouadio J-LK, O'Shea JJ, et al. (2004) Tyrosine 813 is a site of JAK2 autophosphorylation critical for activation of JAK2 by SH2-Bb. Mol Cell Biol 24: 4557-4570.
14. Nishi M, Werner ED, Oh B-C, Frantz JD, Dhe-Paganon S, et al. (2005) Kinase activation through dimerization by human SH2-B. Mol Cell Biol 25: 2607-2621.
15. Rui L, Gunter DR, Herrington J, Carter-Su C (2000) Differential binding to and regulation of JAK2 by the SH2 domain and N-terminal region of SH2-Bb. Mol Cell Biol 20: 3168-3177.
16. Kurzer JH, Saharinen P, Silvennoinen O, Carter-Su C (2006) Binding of SH2-B family members within a potential negative regulatory region maintains JAK2 in an active state. Mol Cell Biol 26: 6381-6394.
17. Barua D, Faeder JR, Haugh JM (2007) Structure-based kinetic models of modular signaling protein function: Focus on Shp2. Biophys J 92: 2290-2300.
18. Barua D, Faeder JR, Haugh JM (2008) Computational models of tandem Src homology 2 domain interactions and application to phosphoinositide 3-kinase. J Biol Chem 283: 7338-7345.
19. Hlavacek WS, Faeder JR, Blinov ML, Posner RG, Hucka M, et al. (2006) Rules for modeling signal-transduction systems. Sci STKE 2006 344: re6.
20. Ladbury JE, Lemmon MA, Zhou M, Green J, Botfield MC, et al. (1995) Measurement of the binding of tyrosyl phosphopeptides to SH2 domains: a reappraisal. Proc Natl Acad Sci U S A 92: 3199-3203.
21. Ottinger EA, Botfield MC, Shoelson SE (1998) Tandem SH2 domains confer high specificity in tyrosine kinase signaling. J Biol Chem 273: 729-735.
22. Yang P, Whelan RJ, Jameson EE, Kurzer JH, Argetsinger LS, et al. (2005) Capillary electrophoresis and fluorescence anisotropy for quantitative analysis of peptide-protein interactions using JAK2 and SH2-Bb as a model system. Anal Chem 77: 2482-2489.
23. Hu J, Hubbard SR (2006) Structural basis for phosphotyrosine recognition by the Src homology-2 domains of the adapter proteins SH2-B and APS. J Mol Biol 361: 69-79.
24. Haugh JM (2004) Mathematical model of human growth hormone (hGH) - stimulated cell proliferation explains the efficacy of hGH variants as receptor agonists or antagonists. Biotechnol Prog 20: 1337-1344.
25. Rui L, Herrington J, Carter-Su C (1999) SH2-B, a membrane-associated adapter, is phosphorylated on multiple serines/threonines in response to nerve growth factor by kinases within the MEK/ERK cascade. J Biol Chem 274: 26485-26492.
26. Pawson T (2004) Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 116: 191-203.
27. Bhattacharyya RP, Remenyi A, Yeh BJ, Lim WA (2006) Domains, motifs, and scaffolds: the role of modular interactions in the evolution and wiring of cell signaling circuits. Annu Rev Biochem 75: 655-680.
28. Hlavacek WS, Faeder JR, Blinov ML, Perelson AS, Goldstein B (2003) The complexity of complexes in signal transduction. Biotechnol Bioeng 84: 783-794.
29. Blinov ML, Faeder JR, Goldstein B, Hlavacek WS (2006) A network model of early events in epidermal growth factor receptor signaling that accounts for combinatorial complexity. Biosystems 83: 136-151.
30. Constantinescu SN, Ghaffari S, Lodish HF (1999) The erythropoietin receptor: Structure, activation, and intracellular signal transduction. Trends Endocrinol Metab 10: 18-23.
31. Morrison DK (2009) The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development. Trends Cell Biol 19: 16-23.
32. Rushworth LK, Hindley AD, O'Neill E, Kolch W (2006) Regulation and role of Raf-1/B-Raf heterodimerization. Mol Cell Biol 26: 2262-2272.
33. Northrup SH, Erickson HP (1992) Kinetics of protein-protein association explained by Brownian dynamics computer simulation. Proc Natl Acad Sci U S A 89: 3338-3342.
34. Haugh JM, Lauffenburger DA (1997) Physical modulation of intracellular signaling processes by locational regulation. Biophys J 72: 2014-2031.
35. Haugh JM, Schneider IC, Lewis JM (2004) On the cross-regulation of protein tyrosine phosphatases and receptor tyrosine kinases in intracellular signaling. J Theor Biol 230: 119-132.
36. Faeder JR, Blinov ML, Hlavacek WS (in press) Rule-based modeling of biochemical systems with BioNetGen. In: Methods in Molecular Biology: Systems Biology. Maly IV, ed. Totowa, NJ: Humana Press.