In-depth analyses of B cell signaling through tandem mass spectrometry of phosphopeptides enriched by PolyMAC

International Journal of Mass Spectrometry

Volumn 377, Issue 1, 2015, Pages 744-753

  Iliuk, Anton ^a,b   Jayasundera, Keerthi ^a   Wang, Wen Horng ^c   Schluttenhofer, Rachel ^a   Geahlen, Robert L ^c   Tao, W Andy ^a,b,c  

^a PURDUE UNIVERSITY   (United States)

^b Tymora Analytical Operations   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

Kinase; Protein phosphorylation; Proteomics; Tandem mass spectrometry

Indexed keywords

EID: 85027918783     PISSN: 13873806     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijms.2014.08.032     Document Type: Article

References (50)

1. R. W. Kondrat, R. G. Cooks, Direct analysis of mixtures by mass-spectrometry, Anal. Chem. 50 (1978) A81-A92.
2. M. Kruger, M. Moser, S. Ussar, I. Thievessen, C. A. Luber, F. Forner, S. Schmidt, S. Zanivan, R. Fassler, M. Mann, SILAC mouse for quantitative proteomics uncovers kindlin-3 as an essential factor for red blood cell function, Cell 134 (2008) 353-364.
3. M. Q. Dong, J. D. Venable, N. Au, T. Xu, S. K. Park, D. Cociorva, J. R. Johnson, A. Dillin, J. R. Yates 3rd, Quantitative mass spectrometry identifies insulin signaling targets in C. elegans, Science 317 (2007) 660-663.
4. D. A. Wolters, M. P. Washburn, J. R. Yates 3rd, An automated multidimensional protein identification technology for shotgun proteomics, Anal. Chem. 73 (2001) 5683-5690.
5. J. V. Olsen, B. Blagoev, F. Gnad, B. Macek, C. Kumar, P. Mortensen, M. Mann, Global, in vivo, and site-specific phosphorylation dynamics in signaling networks, Cell 127 (2006) 635-648.
6. C. S. Tan, B. Bodenmiller, A. Pasculescu, M. Jovanovic, M. O. Hengartner, C. Jorgensen, G. D. Bader, R. Aebersold, T. Pawson, R. Linding, Comparative analysis reveals conserved protein phosphorylation networks implicated in multiple diseases, Sci. Signal 2 (2009) ra39.
7. J. Porath, High-performance immobilized-metal-ion affinity chromatography of peptides and proteins, J. Chromatogr. 443 (1988) 3-11.
8. S. B. Ficarro, M. L. McCleland, P. T. Stukenberg, D. J. Burke, M. M. Ross, J. Shabanowitz, D. F. Hunt, F. M. White, Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae, Nat. Biotechnol. 20 (2002) 301-305.
9. M. W. Pinkse, P. M. Uitto, M. J. Hilhorst, B. Ooms, A. J. Heck, Selective isolation at the femtomole level of phosphopeptides from proteolytic digests using 2D-NanoLC-ESI-MS/MS and titanium oxide precolumns, Anal. Chem. 76 (2004) 3935-3943.
10. M. R. Larsen, T. E. Thingholm, O. N. Jensen, P. Roepstorff, T. J. Jorgensen, Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns, Mol. Cell Proteomics 4 (2005) 873-886.
11. H. Zhou, S. Xu, M. Ye, S. Feng, C. Pan, X. Jiang, X. Li, G. Han, Y. Fu, H. Zou, Zirconium phosphonate-modified porous silicon for highly specific capture of phosphopeptides and MALDI-TOF MS analysis, J. Proteome Res. 5 (2006) 2431-2437.
12. H. K. Kweon, K. Hakansson, Selective zirconium dioxide-based enrichment of phosphorylated peptides for mass spectrometric analysis, Anal. Chem. 78 (2006) 1743-1749.
13. F. Wolschin, S. Wienkoop, W. Weckwerth, Enrichment of phosphorylated proteins and peptides from complex mixtures using metal oxide/hydroxide affinity chromatography (MOAC), Proteomics 5 (2005) 4389-4397.
14. A. B. Iliuk, V. A. Martin, B. M. Alicie, R. L. Geahlen, W. A. Tao, In-depth analyses of kinase-dependent tyrosine phosphoproteomes based on metal ion functionalized soluble nanopolymers, Mol. Cell. Proteomics 9 (2010) 2162-2172.
15. A. Iliuk, K. Jayasundera, R. Schluttenhofer, W. A. Tao, Functionalized soluble nanopolymers for phosphoproteome analysis, Methods Mol. Biol. 790 (2011) 277-285.
16. N. Munagala, S. Nguyen, W. Lam, J. Lee, A. Joly, K. McMillan, W. Zhang, Identification of small molecule ceramide kinase inhibitors using a homogeneous chemiluminescence high throughput assay, Assay Drug Dev. Technol. 5 (2007) 65-73.
17. T. Kurosaki, Regulation of BCR signaling, Mol. Immunol. 48 (2011) 1287-1291.
18. R. J. Brezski, J. G. Monroe, B-cell receptor, Adv. Exp. Med. Biol. 640 (2008) 12-21.
19. S. Gobessi, L. Laurenti, P. G. Longo, L. Carsetti, V. Berno, S. Sica, G. Leone, D. G. Efremov, Inhibition of constitutive and BCR-induced Syk activation downregulates Mcl-1 and induces apoptosis in chronic lymphocytic leukemia B cells, Leukemia 23 (2009) 686-697.
20. P. G. Longo, L. Laurenti, S. Gobessi, S. Sica, G. Leone, D. G. Efremov, The Akt/Mcl-1 pathway plays a prominent role in mediating antiapoptotic signals downstream of the B-cell receptor in chronic lymphocytic leukemia B cells, Blood 111 (2008) 846-855.
21. A. Franke, G. J. Niederfellner, C. Klein, H. Burtscher, Antibodies against CD20 or B-cell receptor induce similar transcription patterns in human lymphoma cell lines, PLoS One 6 (2011) e16596.
22. M. Matsumoto, K. Oyamada, H. Takahashi, T. Sato, S. Hatakeyama, K. I. Nakayama, Large-scale proteomic analysis of tyrosine-phosphorylation induced by T-cell receptor or B-cell receptor activation reveals new signaling pathways, Proteomics 9 (2009) 3549-3563.
23. K. Xiao, J. Sun, J. Kim, S. Rajagopal, B. Zhai, J. Villen, W. Haas, J. J. Kovacs, A. K. Shukla, M. R. Hara, M. Hernandez, A. Lachmann, S. Zhao, Y. Lin, Y. Cheng, K. Mizuno, A. Ma'ayan, S. P. Gygi, R. J. Lefkowitz, Global phosphorylation analysis of beta-arrestin-mediated signaling downstream of a seven transmembrane receptor (7TMR), Proc. Natl. Acad. Sci. U. S. A. 107 (2010) 15299-15304.
24. S. B. Ficarro, Y. Zhang, Y. Lu, A. R. Moghimi, M. Askenazi, E. Hyatt, E. D. Smith, L. Boyer, T. M. Schlaeger, C. J. Luckey, J. A. Marto, Improved electrospray ionization efficiency compensates for diminished chromatographic resolution and enables proteomics analysis of tyrosine signaling in embryonic stem cells, Anal. Chem. 81 (2009) 3440-3447.
25. N. Nagaraj, R. C. D'Souza, J. Cox, J. V. Olsen, M. Mann, Feasibility of large-scale phosphoproteomics with higher energy collisional dissociation fragmentation, J. Proteome Res. 9 (2010) 6786-6794.
26. L. Xue, W. H. Wang, A. Iliuk, L. Hu, J. A. Galan, S. Yu, M. Hans, R. L. Geahlen, W. Tao, A., Sensitive kinase assay linked with phosphoproteomics for identifying direct kinase substrates, Proc. Natl. Acad. Sci. U. S. A. 109 (2012) 5615-5620.
27. 2 surfaces used in the study of regulated, dynamic protein phosphorylation, J. Am. Soc. Mass Spectrom. 18 (2007) 1932-1944.
28. D. S. Kalinowski, D. R. Richardson, Theevolutionofironchelatorsforthetreatment of iron overload disease and cancer, Pharmacol. Rev. 57 (2005) 547-583.
29. M. d'Hardemare Adu, S. Torelli, G. Serratrice, J. L. Pierre, Design of iron chelators: syntheses and iron (III) complexing abilities of tripodal trisbidentate ligands, Biometals 19 (2006) 349-366.
30. 2 from aqueous solutions: an in situ internal reflection infrared spectroscopic study, Langmuir 15 (1999) 2916-2921.
31. K. M. Buettner, J. M. Collins, A. M. Valentine, Titanium (IV) and vitamin C: aqueous complexes of a bioactive form of Ti (IV), Inorg. Chem. 51 (2012) 11030-11039.
32. D. L. Swaney, G. C. McAlister, J. J. Coon, Decision tree-driven tandem mass spectrometry for shotgun proteomics, Nat. Methods 5 (2008) 959-964.
33. J. V. Olsen, B. Macek, O. Lange, A. Makarov, S. Horning, M. Mann, Higher-energy C-trap dissociation for peptide modification analysis, Nat. Methods 4 (2007) 709-712.
34. T. E. Thingholm, O. N. Jensen, P. J. Robinson, M. R. Larsen, SIMAC (sequential elution from IMAC), a phosphoproteomics strategy for the rapid separation of monophosphorylated from multiply phosphorylated peptides, Mol. Cell Proteomics 7 (2008) 661-671.
35. N. E. Harwood, F. D. Batista, Early events in B cell activation, Annu. Rev. Immunol. 28 (2010) 185-210.
36. S. E. Ong, B. Blagoev, I. Kratchmarova, D. B. Kristensen, H. Steen, A. Pandey, M. Mann, Stable isotope labeling by amino acids in cell culture SILAC, as a simple and accurate approach to expression proteomics, Mol. Cell Proteomics 1 (2002) 376-386.
37. M. Gilar, P. Olivova, A. E. Daly, J. C. Gebler, Two-dimensional separation of peptides using RP-RP-HPLC system with different pH in first and second separation dimensions, J. Sep. Sci. 28 (2005) 1694-1703.
38. R. L. Geahlen, Syk and pTyr'd: signaling through the B cell antigen receptor, Biochim. Biophys. Acta 1793 (2009) 1115-1127.
39. S. Richards, C. Watanabe, L. Santos, A. Craxton, E. A. Clark, Regulation of B-cell entry into the cell cycle, Immunol. Rev. 224 (2008) 183-200.
40. F. Huang, H. Gu, Negative regulation of lymphocyte development and function by the Cbl family of proteins, Immunol. Rev. 224 (2008) 229-238.
41. A. Mocsai, J. Ruland, V. L. Tybulewicz, The SYK tyrosine kinase: a crucial player in diverse biological functions, Nat. Rev. Immunol. 10 (2010) 387-402.
42. S. K. Pierce, W. Liu, The tipping points in the initiation of B cell signalling: how small changes make big differences, Nat. Rev. Immunol. 10 (2010) 767-777.
43. F. D. Batista, B. Treanor, N. E. Harwood, Visualizing a role for the actin cytoskeleton in the regulation of B-cell activation, Immunol. Rev. 237 (2014) 191-204.
44. F. Mackay, W. A. Figgett, D. Saulep, M. Lepage, M. L. Hibbs, B-cell stage and context-dependent requirements for survival signals from BAFF and the B-cell receptor, Immunol. Rev. 237 (2014) 205-225.
45. E. Takada, K. Hata, J. Mizuguchi, Requirement for JNK-dependent upregulation of BimLinanti-IgM-induced apoptosisin murineBlymphoma cell lines WEHI-231 and CH31, Exp. Cell Res. 312 (2006) 3728-3738.
46. A. Jiang, A. Craxton, T. Kurosaki, E. A. Clark, Different protein tyrosine kinases are required for B cell antigen receptor-mediated activation of extracellular signal-regulated kinase c-Jun. NH2-terminal kinase 1, and p38 mitogenactivated protein kinase, J. Exp. Med. 188 (1998) 1297-1306.
47. S. Herzog, M. Reth, H. Jumaa, Regulation of B-cell proliferation and differentiation by pre-B-cell receptor signalling, Nat. Rev. Immunol. 9 (2009) 195-205.
48. H. Shinohara, T. Kurosaki, Comprehending the complex connection between PKCbeta, TAK1, and IKK in BCR signaling, Immunol. Rev. 232 (2009) 300-318.
49. T. Yasuda, H. Sanjo, G. Pages, Y. Kawano, H. Karasuyama, J. Pouyssegur, M. Ogata, T. Kurosaki, Erk kinases link pre-B cell receptor signaling to transcriptional events required for early B cell expansion, Immunity 28 (2008) 499-508.
50. A. D. Baudot, P. Y. Jeandel, X. Mouska, U. Maurer, S. Tartare-Deckert, S. D. Raynaud, J. P. Cassuto, M. Ticchioni, M. Deckert, The tyrosine kinase Syk regulates the survival of chronic lymphocytic leukemia B cells through PKCdelta and proteasome-dependent regulation of Mcl-1 expression, Oncogene 28 (2009) 3261-3273.