SH2 Domains Serve as Lipid-Binding Modules for pTyr-Signaling Proteins

Molecular Cell

Volumn 62, Issue 1, 2016, Pages 7-20

  Park, Mi Jeong ^a   Sheng, Ren ^b   Silkov, Antonina ^c   Jung, Da Jung ^a   Wang, Zhi Gang ^b   Xin, Yao ^b   Kim, Hyunjin ^b   Thiagarajan Rosenkranz, Pallavi ^b   Song, Seohyeon ^a   Yoon, Youngdae ^b,e   Nam, Wonhee ^a   Kim, Ilshin ^d   Kim, Eui ^a   Lee, Dong Gyu ^a   Chen, Yong ^b   Singaram, Indira ^b   Wang, Li ^b   Jang, Myoung Ho ^d   Hwang, Cheol Sang ^a   Honig, Barry ^c   Ryu, Sungho ^a   Lorieau, Justin ^b   Kim, You Me ^a   Cho, Wonhwa ^b   more..

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c Columbia University ^*  (United States)

^d Institute for Basic Science   (South Korea)

^e Konkuk University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID BINDING PROTEIN; MEMBRANE LIPID; PHOSPHATIDYLINOSITIDE; PROTEIN KINASE ZAP 70; PROTEIN SH2; PHOSPHOTYROSINE; PROTEIN BINDING; ZAP70 PROTEIN, HUMAN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CELL FUNCTION; CELL MEMBRANE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; LIPID COMPOSITION; MEMBRANE BINDING; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; T LYMPHOCYTE; CELL CULTURE; CHEMISTRY; DRUG EFFECTS; JURKAT CELL LINE; LIPID METABOLISM; METABOLISM; MOLECULAR DOCKING; MOLECULAR MODEL; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN;

BINDING SITES; CELLS, CULTURED; HUMANS; JURKAT CELLS; LIPID METABOLISM; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; PHOSPHOTYROSINE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; T-LYMPHOCYTES; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 84962393747     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.01.027     Document Type: Article

References (52)

1. Bae Y.S., Cantley L.G., Chen C.S., Kim S.R., Kwon K.S., Rhee S.G. Activation of phospholipase C-gamma by phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 1998, 273:4465-4469.
2. Bae J.H., Lew E.D., Yuzawa S., Tomé F., Lax I., Schlessinger J. The selectivity of receptor tyrosine kinase signaling is controlled by a secondary SH2 domain binding site. Cell 2009, 138:514-524.
3. Brauer P.M., Tyner A.L. RAKing in AKT: a tumor suppressor function for the intracellular tyrosine kinase FRK. Cell Cycle 2009, 8:2728-2732.
4. Bray D. Signaling complexes: biophysical constraints on intracellular communication. Annu. Rev. Biophys. Biomol. Struct. 1998, 27:59-75.
5. Chen Y., Sheng R., Källberg M., Silkov A., Tun M.P., Bhardwaj N., Kurilova S., Hall R.A., Honig B., Lu H., Cho W. Genome-wide functional annotation of dual-specificity protein- and lipid-binding modules that regulate protein interactions. Mol. Cell 2012, 46:226-237.
6. Cho W. Building signaling complexes at the membrane. Sci. STKE 2006, 2006:pe7.
7. Cho W., Stahelin R.V. Membrane-protein interactions in cell signaling and membrane trafficking. Annu. Rev. Biophys. Biomol. Struct. 2005, 34:119-151.
8. Di Paolo G., De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature 2006, 443:651-657.
9. Feng W., Zhang M. Organization and dynamics of PDZ-domain-related supramodules in the postsynaptic density. Nat. Rev. Neurosci. 2009, 10:87-99.
10. Good M.C., Zalatan J.G., Lim W.A. Scaffold proteins: hubs for controlling the flow of cellular information. Science 2011, 332:680-686.
11. Graves A.P., Shivakumar D.M., Boyce S.E., Jacobson M.P., Case D.A., Shoichet B.K. Rescoring docking hit lists for model cavity sites: predictions and experimental testing. J. Mol. Biol. 2008, 377:914-934.
12. Groesch T.D., Zhou F., Mattila S., Geahlen R.L., Post C.B. Structural basis for the requirement of two phosphotyrosine residues in signaling mediated by Syk tyrosine kinase. J. Mol. Biol. 2006, 356:1222-1236.
13. Hatada M.H., Lu X., Laird E.R., Green J., Morgenstern J.P., Lou M., Marr C.S., Phillips T.B., Ram M.K., Theriault K., et al. Molecular basis for interaction of the protein tyrosine kinase ZAP-70 with the T-cell receptor. Nature 1995, 377:32-38.
14. Heo W.D., Inoue T., Park W.S., Kim M.L., Park B.O., Wandless T.J., Meyer T. PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 2006, 314:1458-1461.
15. Hong Y., Chalkia D., Ko K.D., Bhardwaj G., Chang G.S., van Rossum D.B., Patterson R.L. Phylogenetic Profiles Reveal Structural and Functional Determinants of Lipid-binding. J. Proteomics Bioinform. 2009, 2:139-149.
16. Huby R.D., Iwashima M., Weiss A., Ley S.C. ZAP-70 protein tyrosine kinase is constitutively targeted to the T cell cortex independently of its SH2 domains. J. Cell Biol. 1997, 137:1639-1649.
17. Inoue T., Meyer T. Synthetic activation of endogenous PI3K and Rac identifies an AND-gate switch for cell polarization and migration. PLoS ONE 2008, 3:e3068.
18. Inoue T., Heo W.D., Grimley J.S., Wandless T.J., Meyer T. An inducible translocation strategy to rapidly activate and inhibit small GTPase signaling pathways. Nat. Methods 2005, 2:415-418.
19. Kim J., Huh J., Hwang M., Kwon E.H., Jung D.J., Brinkmann M.M., Jang M.H., Ploegh H.L., Kim Y.M. Acidic amino acid residues in the juxtamembrane region of the nucleotide-sensing TLRs are important for UNC93B1 binding and signaling. J. Immunol. 2013, 190:5287-5295.
20. Koyama-Honda I., Ritchie K., Fujiwara T., Iino R., Murakoshi H., Kasai R.S., Kusumi A. Fluorescence imaging for monitoring the colocalization of two single molecules in living cells. Biophys. J. 2005, 88:2126-2136.
21. Kraskouskaya D., Duodu E., Arpin C.C., Gunning P.T. Progress towards the development of SH2 domain inhibitors. Chem. Soc. Rev. 2013, 42:3337-3370.
22. Ladbury J.E., Arold S. Searching for specificity in SH domains. Chem. Biol. 2000, 7:R3-R8.
23. Lemmon M.A. Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 2008, 9:99-111.
24. Lim W.A., Pawson T. Phosphotyrosine signaling: evolving a new cellular communication system. Cell 2010, 142:661-667.
25. Liu B.A., Nash P.D. Evolution of SH2 domains and phosphotyrosine signalling networks. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2012, 367:2556-2573.
26. Liu S.L., Sheng R., O'Connor M.J., Cui Y., Yoon Y., Kurilova S., Lee D., Cho W. Simultaneous in situ quantification of two cellular lipid pools using orthogonal fluorescent sensors. Angew. Chem. Int. Ed. Engl. 2014, 53:14387-14391.
27. Machida K., Mayer B.J. The SH2 domain: versatile signaling module and pharmaceutical target. Biochim. Biophys. Acta 2005, 1747:1-25.
28. MacKerell A.D., Bashford D., Bellott M., Dunbrack R.L., Evanseck J.D., Field M.J., Fischer S., Gao J., Guo H., Ha S., et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 1998, 102:3586-3616.
29. Manna D., Albanese A., Park W.S., Cho W. Mechanistic basis of differential cellular responses of phosphatidylinositol 3,4-bisphosphate- and phosphatidylinositol 3,4,5-trisphosphate-binding pleckstrin homology domains. J. Biol. Chem. 2007, 282:32093-32105.
30. McLaughlin S., Murray D. Plasma membrane phosphoinositide organization by protein electrostatics. Nature 2005, 438:605-611.
31. McLaughlin S., Wang J., Gambhir A., Murray D. PIP(2) and proteins: interactions, organization, and information flow. Annu. Rev. Biophys. Biomol. Struct. 2002, 31:151-175.
32. Pawson T. Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 2004, 116:191-203.
33. Petrey D., Honig B. GRASP2: visualization, surface properties, and electrostatics of macromolecular structures and sequences. Methods Enzymol. 2003, 374:492-509.
34. Pollizzi K.N., Powell J.D. Integrating canonical and metabolic signalling programmes in the regulation of T cell responses. Nat. Rev. Immunol. 2014, 14:435-446.
35. Rameh L.E., Chen C.S., Cantley L.C. Phosphatidylinositol (3,4,5)P3 interacts with SH2 domains and modulates PI 3-kinase association with tyrosine-phosphorylated proteins. Cell 1995, 83:821-830.
36. Rocchia W., Alexov E., Honig B. Extending the applicability of the nonlinear Poisson-Boltzmann equation: multiple dielectric constants and multivalent ions. J. Phys. Chem. B 2001, 105:6507-6514.
37. Sadowski I., Stone J.C., Pawson T. 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. 1986, 6:4396-4408.
38. Sali A., Blundell T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 1993, 234:779-815.
39. Scott J.D., Pawson T. Cell signaling in space and time: where proteins come together and when they're apart. Science 2009, 326:1220-1224.
40. Sheng R., Chen Y., Yung Gee H., Stec E., Melowic H.R., Blatner N.R., Tun M.P., Kim Y., Källberg M., Fujiwara T.K., et al. Cholesterol modulates cell signaling and protein networking by specifically interacting with PDZ domain-containing scaffold proteins. Nat. Commun. 2012, 3:1249.
41. Sheng R., Kim H., Lee H., Xin Y., Chen Y., Tian W., Cui Y., Choi J.C., Doh J., Han J.K., Cho W. Cholesterol selectively activates canonical Wnt signalling over non-canonical Wnt signalling. Nat. Commun. 2014, 5:4393.
42. Stahelin R.V., Cho W. Differential roles of ionic, aliphatic, and aromatic residues in membrane-protein interactions: a surface plasmon resonance study on phospholipases A2. Biochemistry 2001, 40:4672-4678.
43. Surdo P.L., Bottomley M.J., Arcaro A., Siegal G., Panayotou G., Sankar A., Gaffney P.R., Riley A.M., Potter B.V., Waterfield M.D., Driscoll P.C. Structural and biochemical evaluation of the interaction of the phosphatidylinositol 3-kinase p85alpha Src homology 2 domains with phosphoinositides and inositol polyphosphates. J. Biol. Chem. 1999, 274:15678-15685.
44. Tokonzaba E., Capelluto D.G., Kutateladze T.G., Overduin M. Phosphoinositide, phosphopeptide and pyridone interactions of the Abl SH2 domain. Chem. Biol. Drug Des. 2006, 67:230-237.
45. Varnai P., Thyagarajan B., Rohacs T., Balla T. Rapidly inducible changes in phosphatidylinositol 4,5-bisphosphate levels influence multiple regulatory functions of the lipid in intact living cells. J. Cell Biol. 2006, 175:377-382.
46. Waksman G., Shoelson S.E., Pant N., Cowburn D., Kuriyan J. Binding of a high affinity phosphotyrosyl peptide to the Src SH2 domain: crystal structures of the complexed and peptide-free forms. Cell 1993, 72:779-790.
47. Wang H., Kadlecek T.A., Au-Yeung B.B., Goodfellow H.E., Hsu L.Y., Freedman T.S., Weiss A. ZAP-70: an essential kinase in T-cell signaling. Cold Spring Harb. Perspect. Biol. 2010, 2:a002279.
48. Winters M.J., Lamson R.E., Nakanishi H., Neiman A.M., Pryciak P.M. A membrane binding domain in the ste5 scaffold synergizes with gbetagamma binding to control localization and signaling in pheromone response. Mol. Cell 2005, 20:21-32.
49. Wu H., Feng W., Chen J., Chan L.N., Huang S., Zhang M. PDZ domains of Par-3 as potential phosphoinositide signaling integrators. Mol. Cell 2007, 28:886-898.
50. Yoon Y., Lee P.J., Kurilova S., Cho W. In situ quantitative imaging of cellular lipids using molecular sensors. Nat. Chem. 2011, 3:868-874.
51. Zheng Y., Asara J.M., Tyner A.L. Protein-tyrosine kinase 6 promotes peripheral adhesion complex formation and cell migration by phosphorylating p130 CRK-associated substrate. J. Biol. Chem. 2012, 287:148-158.
52. Zimmermann P., Meerschaert K., Reekmans G., Leenaerts I., Small J.V., Vandekerckhove J., David G., Gettemans J. PIP(2)-PDZ domain binding controls the association of syntenin with the plasma membrane. Mol. Cell 2002, 9:1215-1225.