A comprehensive immunoreceptor phosphotyrosine-based signaling network revealed by reciprocal protein-peptide array screening

Molecular and Cellular Proteomics

Volumn 14, Issue 7, 2015, Pages 1846-1858

  Liu, Huadong ^a   Li, Lei ^a   Voss, Courtney ^a   Wang, Feng ^b   Liu, Juewen ^b   Li, Shawn Shun Cheng ^a  

^a WESTERN UNIVERSITY   (Canada)

^b UNIVERSITY OF WATERLOO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD22 ANTIGEN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; IMMUNORECEPTOR PHOSPHOTYROSINE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOTYROSINE; PROTEIN KINASE FYN; PROTEIN KINASE LYN; PROTEIN KINASE SYK; PROTEIN SH2; PROTEIN SHC; PROTEIN TYROSINE PHOSPHATASE SHP 1; UNCLASSIFIED DRUG; IMMUNOGLOBULIN RECEPTOR; PEPTIDE; PROTEIN BINDING;

ARTICLE; ENZYME LINKED IMMUNOSORBENT ASSAY; FAST PROTEIN LIQUID CHROMATOGRAPHY; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN MICROARRAY; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING ASSAY; SIGNAL TRANSDUCTION; WESTERN BLOTTING; CHEMISTRY; HUMAN; METABOLISM; PROTEIN MOTIF; SRC HOMOLOGY DOMAIN; U-937 CELL LINE;

AMINO ACID MOTIFS; HUMANS; PEPTIDES; PHOSPHOTYROSINE; PROTEIN ARRAY ANALYSIS; PROTEIN BINDING; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; U937 CELLS;

EID: 84936770806     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M115.047951     Document Type: Article

References (49)

1. Guy, C. S., Vignali, K. M., Temirov, J., Bettini, M. L., Overacre, A. E., Smeltzer, M., Zhang, H., Huppa, J. B., Tsai, Y. H., Lobry, C., Xie, J., Dempsey, P. J., Crawford, H. C., Aifantis, I., Davis, M. M., and Vignali, D. A. (2013) Distinct TCR signaling pathways drive proliferation and cytokine production in T cells. Nat. Immunol. 14, 262-270.
2. van Leeuwen, J. E., and Samelson, L. E. (1999) T cell antigen-receptor signal transduction. Current Opinion Immunol. 11, 242-248.
3. Ravetch, J. V., and Lanier, L. L. (2000) Immune inhibitory receptors. Science 290, 84-89.
4. Dong, Z., and Veillette, A. (2010) How do SAP family deficiencies compromise immunity? Trends Immunol. 31, 295-302.
5. Ostrakhovitch, E. A., and Li, S. S. (2006) The role of SLAM family receptors in immune cell signaling. Biochem. Cell Biol. 84, 832-843.
6. Steevels, T. A., and Meyaard, L. (2011) Immune inhibitory receptors: Essential regulators of phagocyte function. Eur. J. Immunol. 41, 575-587.
7. Bezbradica, J. S., and Medzhitov, R. (2012) Role of ITAM signaling module in signal integration. Current Opinion Immunol. 24, 58-66.
8. Hamerman, J. A., and Lanier, L. L. (2006) Inhibition of immune responses by ITAM-bearing receptors. Science's STKE 2006, re1.
9. Pumphrey, N. J., Taylor, V., Freeman, S., Douglas, M. R., Bradfield, P. F., Young, S. P., Lord, J. M., Wakelam, M. J., Bird, I. N., Salmon, M., and Buckley, C. D. (1999) Differential association of cytoplasmic signalling molecules SHP-1, SHP-2, SHIP and phospholipase C-gamma1 with PECAM-1/CD31. FEBS Lett. 450, 77-83.
10. Bonnerot, C., Briken, V., and Amigorena, S. (1997) Intracellular signaling and endosomal trafficking of immunoreceptors. Shared effectors underlying MHC class II-restricted antigen presentation. Immunology Lett. 57, 1-4.
11. Daeron, M., Jaeger, S., Du Pasquier, L., and Vivier, E. (2008) Immunoreceptor tyrosine-based inhibition motifs: A quest in the past and future. Immunol. Rev. 224, 11-43.
12. Verbrugge, A., Rijkers, E. S., de Ruiter, T., and Meyaard, L. (2006) Leukocyte- Associated Ig-like receptor-1 has SH2 domain-containing phosphatase- independent function and recruits C-terminal Src kinase. Eur. J. Immunol. 36, 190-198.
13. Zhu, M., Janssen, E., Leung, K., and Zhang, W. (2002) Molecular cloning of a novel gene encoding a membrane-associated adaptor protein (LAX) in lymphocyte signaling. The J. Biol. Chem. 277, 46151-46158.
14. Fusaki, N., Tomita, S., Wu, Y., Okamoto, N., Goitsuka, R., Kitamura, D., and Hozumi, N. (2000) BLNK is associated with the CD72/SHP-1/Grb2 complex in the WEHI231 cell line after membrane IgM cross-linking. Eur. J. Immunol. 30, 1326-1330.
15. Lamesch, P., Li, N., Milstein, S., Fan, C., Hao, T., Szabo, G., Hu, Z., Venkatesan, K., Bethel, G., Martin, P., Rogers, J., Lawlor, S., McLaren, S., Dricot, A., Borick, H., Cusick, M. E., Vandenhaute, J., Dunham, I., Hill, D. E., and Vidal, M. (2007) hORFeome v3.1: A resource of human open reading frames representing over 10, 000 human genes. Genomics 89, 307-315.
16. Brettner, L. M., and Masel, J. (2012) Protein stickiness, rather than number of functional protein-protein interactions, predicts expression noise and plasticity in yeast. BMC Syst. Biol. 6, 128.
17. Kim, T., Tyndel, M. S., Huang, H., Sidhu, S. S., Bader, G. D., Gfeller, D., and Kim, P. M. (2012) MUSI: An integrated system for identifying multiple specificity from very large peptide or nucleic acid data sets. Nucleic Acids Res. 40, e47.
18. Melton, L. (2004) Protein arrays: proteomics in multiplex. Nature 429, 101-107.
19. Huang, H., Li, L., Wu, C., Schibli, D., Colwill, K., Ma, S., Li, C., Roy, P., Ho, K., Songyang, Z., Pawson, T., Gao, Y., and Li, S. S. (2008) Defining the specificity space of the human SRC homology 2 domain. Mol. Cell. Proteomics 7, 768-784.
20. Liu, H., Galka, M., Iberg, A., Wang, Z., Li, L., Voss, C., Jiang, X., Lajoie, G., Huang, Z., Bedford, M. T., and Li, S. S. (2010) Systematic identification of methyllysine-driven interactions for histone and nonhistone targets. J. Proteome Res. 9, 5827-5836.
21. Chuang, S. S., Kumaresan, P. R., and Mathew, P. A. (2001) 2B4 (CD244)- mediated activation of cytotoxicity and IFN-gamma release in human NK cells involves distinct pathways. J. Immunol. 167, 6210-6216.
22. Aksoy, S., and Haralick, R. M. (2001) Feature normalization and likelihoodbased similarity measures for image retrieval. Pattern Recogn. Lett. 22, 563-582.
23. Haso, W., Lee, D. W., Shah, N. N., Stetler-Stevenson, M., Yuan, C. M., Pastan, I. H., Dimitrov, D. S., Morgan, R. A., Fitzgerald, D. J., Barrett, D. M., Wayne, A. S., Mackall, C. L., and Orentas, R. J. (2012) Anti-CD22- chimeric antigen receptors targeting B cell precursor acute lymphoblastic leukemia. Blood. 121, 1165-1174.
24. Nitschke, L. (2009) CD22 and Siglec-G: B-cell inhibitory receptors with distinct functions. Immunol. Rev. 230, 128-143.
25. Fujimoto, M., Kuwano, Y., Watanabe, R., Asashima, N., Nakashima, H., Yoshitake, S., Okochi, H., Tamaki, K., Poe, J. C., Tedder, T. F., and Sato, S. (2006) B cell antigen receptor and CD40 differentially regulate CD22 tyrosine phosphorylation. J. Immunol. 176, 873-879.
26. Poe, J. C., Fujimoto, M., Jansen, P. J., Miller, A. S., and Tedder, T. F. (2000) CD22 forms a quaternary complex with SHIP, Grb2, and Shc. A pathway for regulation of B lymphocyte antigen receptor-induced calcium flux. J. Biol. Chem. 275, 17420-17427.
27. Tolar, P., Hanna, J., Krueger, P. D., and Pierce, S. K. (2009) The Constant Region of the Membrane Immunoglobulin Mediates B Cell-Receptor Clustering and Signaling in Response to Membrane Antigens. Immunity 30, 44-55.
28. Bjorge, J. D., Jakymiw, A., and Fujita, D. J. (2000) Selected glimpses into the activation and function of Src kinase. Oncogene 19, 5620-5635.
29. Tourdot, B. E., Brenner, M. K., Keough, K. C., Holyst, T., Newman, P. J., and Newman, D. K. (2013) Immunoreceptor tyrosine-based inhibitory motif (ITIM)-mediated inhibitory signaling is regulated by sequential phosphorylation mediated by distinct nonreceptor tyrosine kinases: A case study involving PECAM-1. Biochemistry 52, 2597-2608.
30. Apweiler, R., Martin, M. J., O'Donovan, C., Magrane, M., Alam-Faruque, Y., Antunes, R., Barrell, D., Bely, B., Bingley, M., Binns, D., Bower, L., Browne, P., Chan, W. M., Dimmer, E., Eberhardt, R., Fazzini, F., Fedotov, A., Foulger, R., Garavelli, J., Castro, L. G., Huntley, R., Jacobsen, J., Kleen, M., Laiho, K., Legge, D., Lin, Q. A., Liu, W. D., Luo, J., Orchard, S., Patient, S., Pichler, K., Poggioli, D., Pontikos, N., Pruess, M., Rosanoff, S., Sawford, T., Sehra, H., Turner, E., Corbett, M., Donnelly, M., van Rensburg, P., Xenarios, I., Bougueleret, L., Auchincloss, A., Argoud-Puy, G., Axelsen, K., Bairoch, A., Baratin, D., Blatter, M. C., Boeckmann, B., Bolleman, J., Bollondi, L., Boutet, E., Quintaje, S. B., Breuza, L., Bridge, A., deCastro, E., Coudert, E., Cusin, I., Doche, M., Dornevil, D., Duvaud, S., Estreicher, A., Famiglietti, L., Feuermann, M., Gehant, S., Ferro, S., Gasteiger, E., Gateau, A., Gerritsen, V., Gos, A., Gruaz-Gumowski, N., Hinz, U., Hulo, C., Hulo, N., James, J., Jimenez, S., Jungo, F., Kappler, T., Keller, G., Lara, V., Lemereier, P., Lieberherr, D., Martin, X., Masson, P., Moinat, M., Morgat, A., Paesano, S., Pedruzzi, I., Pilbout, S., Poux, S., Pozzato, M., Redaschi, N., Rivoire, C., et al.(2011) Ongoing and future developments at the Universal Protein Resource. Nucleic Acids Res. 39, D214-D219.
31. Franceschini, A., Szklarczyk, D., Frankild, S., Kuhn, M., Simonovic, M., Roth, A., Lin, J., Minguez, P., Bork, P., von Mering, C., and Jensen, L. J. (2013) STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 41, D808-815.
32. Du, J., Yuan, Z., Ma, Z., Song, J., Xie, X., and Chen, Y. (2014) KEGG-PATH: Kyoto encyclopedia of genes and genomes-based pathway analysis using a path analysis model. Mol. Biosyst. 10, 2441-2447.
33. Bloch-Queyrat, C., Fondaneche, M. C., Chen, R., Yin, L., Relouzat, F., Veillette, A., Fischer, A., and Latour, S. (2005) Regulation of natural cytotoxicity by the adaptor SAP and the Src-related kinase Fyn. J. Exp. Med. 202, 181-192.
34. Clarkson, N. G., Simmonds, S. J., Puklavec, M. J., and Brown, M. H. (2007) Direct and indirect interactions of the cytoplasmic region of CD244 (2B4) in mice and humans with FYN kinase. J. Biol. Chem. 282, 25385-25394.
35. Clarkson, N. G., and Brown, M. H. (2009) Inhibition and activation by CD244 depends on CD2 and phospholipase C-gamma1. J. Biol. Chem. 284, 24725-24734.
36. Lowin-Kropf, B., Kunz, B., Schneider, P., and Held, W. (2002) A role for the src family kinase Fyn in NK cell activation and the formation of the repertoire of Ly49 receptors. Eur. J. Immunol. 32, 773-782.
37. Charvet, C., Canonigo, A. J., Billadeau, D. D., and Altman, A. (2005) Membrane localization and function of Vav3 in T cells depend on its association with the adapter SLP-76. J. Biol. Chem. 280, 15289-15299.
38. Tsai, D. H., DelRio, F. W., Keene, A. M., Tyner, K. M., MacCuspie, R. I., Cho, T. J., Zachariah, M. R., and Hackley, V. A. (2011) Adsorption and conformation of serum albumin protein on gold nanoparticles investigated using dimensional measurements and in situ spectroscopic methods. Langmuir 27, 2464-2477.
39. Lanier, L. L. (2008) Up on the tightrope: Natural killer cell activation and inhibition. Nat. Immunol. 9, 495-502.
40. Kathiriya, J. J., Pathak, R. R., Clayman, E., Xue, B., Uversky, V. N., and Dave, V. (2014) Presence and utility of intrinsically disordered regions in kinases. Mol. Biosyst. 10, 2876-2888.
41. Deng, Y., Alicea-Velazquez, N. L., Bannwarth, L., Lehtonen, S. I., Boggon, T. J., Cheng, H. C., Hytonen, V. P., and Turk, B. E. (2014) Global analysis of human nonreceptor tyrosine kinase specificity using high-density peptide microarrays. J. Proteome Res. 13, 4339-4346.
42. Jones, R. B., Gordus, A., Krall, J. A., and MacBeath, G. (2006) A quantitative protein interaction network for the ErbB receptors using protein microarrays. Nature 439, 168-174.
43. Tong, A. H. Y., Drees, B., Nardelli, G., Bader, G. D., Brannetti, B., Castagnoli, L., Evangelista, M., Ferracuti, S., Nelson, B., Paoluzi, S., Quondam, M., Zucconi, A., Hogue, C. W. V., Fields, S., Boone, C., and Cesareni, G. (2002) A combined experimental and computational strategy to define protein interaction networks for peptide recognition modules. Science 295, 321-324.
44. Kyle K., Biggar, S. S.-C. L. (2014) Non-histone protein methylation as a regulator of cellular signalling and function. Nat. Rev. 1, 5-17.
45. Pfirsch-Maisonnas, S., Aloulou, M., Xu, T., Claver, J., Kanamaru, Y., Tiwari, M., Launay, P., Monteiro, R. C., and Blank, U. (2011) Inhibitory ITAM signaling traps activating receptors with the phosphatase SHP-1 to form polarized "inhibisome" clusters. Sci. Signaling 4, ra24.
46. Barrow, A. D., and Trowsdale, J. (2006) You say ITAM and I say ITIM, let's call the whole thing off: The ambiguity of immunoreceptor signalling. Eur. J. Immunol. 36, 1646-1653.
47. Van Roey, K., Gibson, T. J., and Davey, N. E. (2012) Motif switches: decision-making in cell regulation. Current Opin. Structural Biol. 22, 378-385.
48. Pawson, T., and Scott, J. D. (1997) Signaling through scaffold, anchoring, and adaptor proteins. Science 278, 2075-2080.
49. Horejsi, V., and Hrdinka, M. (2014) Membrane microdomains in immunoreceptor signaling. FEBS Lett. 588, 2392-2397.