Machine learning-based classification of diffuse large B-cell lymphoma patients by their protein expression profiles

Molecular and Cellular Proteomics

Volumn 14, Issue 11, 2015, Pages 2947-2960

  Deeb, Sally J ^a   Tyanova, Stefka ^a   Hummel, Michael ^b   Schmidt Supprian, Marc ^c   Cox, Juergen ^a   Mann, Matthias ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ 1; B LYMPHOCYTE RECEPTOR; FORMALDEHYDE; GLUCOSE TRANSPORTER 4; INTERFERON REGULATORY FACTOR 4; MATRIX METALLOPROTEINASE; MME PROTEIN; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 4; MYELOID DIFFERENTIATION FACTOR 88; PALD1 PROTEIN; PARAFFIN; PROTEIN KINASE LCK; PROTEIN P53; SCLEROPROTEIN; SMALL INTERFERING RNA; TBC1D4 PROTEIN; TNFAIP8 PROTEIN; TOLL LIKE RECEPTOR 9; TRANSCRIPTION FACTOR; TUMOR ANTIGEN; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; MEMBRANE METALLOENDOPEPTIDASE; PALADIN PROTEIN, HUMAN; PHOSPHOPROTEIN PHOSPHATASE; PROTEOME; TBC1D4 PROTEIN, HUMAN; TNFAIP8 PROTEIN, HUMAN; TUMOR MARKER; TUMOR PROTEIN;

ACCURACY; ACUTE MYELOBLASTIC LEUKEMIA; ANION EXCHANGE CHROMATOGRAPHY; ARTICLE; B LYMPHOCYTE; CANCER CLASSIFICATION; CANCER PATIENT; CANCER TISSUE; CELL LYSATE; CELL PROLIFERATION; CONTROLLED STUDY; CROSS LINKING; DNA REPLICATION; EMBEDDING; EXTRACELLULAR MATRIX; FRACTIONATION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; HOUSEKEEPING GENE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LARGE CELL LYMPHOMA; MACHINE LEARNING; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEOMICS; REGULATORY MECHANISM; RNA SPLICING; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SUPPORT VECTOR MACHINE; TANDEM MASS SPECTROMETRY; TISSUE PRESERVATION; TUMOR MICROENVIRONMENT; UPREGULATION; GENE EXPRESSION REGULATION; GENETICS; HISTOLOGY; ISOTOPE LABELING; LYMPHOMA, LARGE B-CELL, DIFFUSE; METABOLISM; PATHOLOGY; PRINCIPAL COMPONENT ANALYSIS; PROCEDURES; TISSUE FIXATION; TUMOR CELL LINE;

APOPTOSIS REGULATORY PROTEINS; BIOMARKERS, TUMOR; CELL LINE, TUMOR; FORMALDEHYDE; GENE EXPRESSION REGULATION, NEOPLASTIC; GTPASE-ACTIVATING PROTEINS; HUMANS; ISOTOPE LABELING; LYMPHOMA, LARGE B-CELL, DIFFUSE; MACHINE LEARNING; NEOPLASM PROTEINS; NEPRILYSIN; PHOSPHOPROTEIN PHOSPHATASES; PRINCIPAL COMPONENT ANALYSIS; PROTEOME; PROTEOMICS; SIGNAL TRANSDUCTION; TISSUE EMBEDDING; TISSUE FIXATION;

EID: 84946063277     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M115.050245     Document Type: Article

References (63)

1. Van Dijk, E. L., Auger, H., Jaszczyszyn, Y., and Thermes, C. (2014) Ten years of next-generation sequencing technology. Trends Genet. 30, 418-426
2. Schilsky, R. L. (2010) Personalized medicine in oncology: the future is now. Nat. Rev. Drug Discov. 9, 363-366
3. Alizadeh, A. A., Eisen, M. B., Davis, R. E., Ma, C., Lossos, I. S., Rosenwald, A., Boldrick, J. C., Sabet, H., Tran, T., Yu, X., Powell, J. I., Yang, L., Marti, G. E., Moore, T., Hudson, J., Jr., Lu, L., Lewis, D. B., Tibshirani, R., Sherlock, G., Chan, W. C., Greiner, T. C., Weisenburger, D. D., Armitage, J. O., Warnke, R., Levy, R., Wilson, W., Grever, M. R., Byrd, J. C., Botstein, D., Brown, P. O., and Staudt, L. M. (2000) Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 403, 503-511
4. Wright, G., Tan, B., Rosenwald, A., Hurt, E. H., Wiestner, A., and Staudt, L. M. (2003) A gene expression-based method to diagnose clinically distinct subgroups of diffuse large B cell lymphoma. Proc. Natl. Acad. Sci. U. S. A. 100, 9991-9996
5. Roschewski, M., Staudt, L. M., and Wilson, W. H. (2014) Diffuse large B-cell lymphoma-treatment approaches in the molecular era. Nat. Rev. Clin. Oncol. 11, 12-23
6. Lenz, G., Wright, G., Dave, S. S., Xiao, W., Powell, J., Zhao, H., Xu, W., Tan, B., Goldschmidt, N., Iqbal, J., Vose, J., Bast, M., Fu, K., Weisenburger, D. D., Greiner, T. C., Armitage, J. O., Kyle, A., May, L., Gascoyne, R. D., Connors, J. M., Troen, G., Holte, H., Kvaloy, S., Dierickx, D., Verhoef, G., Delabie, J., Smeland, E. B., Jares, P., Martinez, A., Lopez-Guillermo, A., Montserrat, E., Campo, E., Braziel, R. M., Miller, T. P., Rimsza, L. M., Cook, J. R., Pohlman, B., Sweetenham, J., Tubbs, R. R., Fisher, R. I., Hartmann, E., Rosenwald, A., Ott, G., Muller-Hermelink, H.-K., Wrench, D., Lister, T. A., Jaffe, E. S., Wilson, W. H., Chan, W. C., and Staudt, L. M.; Lymphoma/Leukemia Molecular Profiling Project (2008) Stromal gene signatures in large-B-cell lymphomas. N. Engl. J. Med. 359, 2313-2323
7. Van't Veer, L. J., Dai, H., Van De Vijver, M. J., He, Y. D., Hart, A. A., Mao, M., Peterse, H. L., Van Der Kooy, K., Marton, M. J., Witteveen, A. T., Schreiber, G. J., Kerkhoven, R. M., Roberts, C., Linsley, P. S., Bernards, R., and Friend, S. H. (2002) Gene expression profiling predicts clinical outcome of breast cancer. Nature 415, 530-536
8. Cancer Genome Atlas Network (2012) Comprehensive molecular characterization of human colon and rectal cancer. Nature 487, 330-337
9. Raspe, E., Decraene, C., and Berx, G. (2012) Gene expression profiling to dissect the complexity of cancer biology: pitfalls and promise. Semin. Cancer Biol. 22, 250-260
10. Perry, A. M., Cardesa-Salzmann, T. M., Meyer, P. N., Colomo, L., Smith, L. M., Fu, K., Greiner, T. C., Delabie, J., Gascoyne, R. D., Rimsza, L., Jaffe, E. S., Ott, G., Rosenwald, A., Braziel, R. M., Tubbs, R., Cook, J. R., Staudt, L. M., Connors, J. M., Sehn, L. H., Vose, J. M., López-Guillermo, A., Campo, E., Chan, W. C., and Weisenburger, D. D. (2012) A new biologic prognostic model based on immunohistochemistry predicts survival in patients with diffuse large B-cell lymphoma. Blood 120, 2290-2296
11. Gutiérrez-García, G., Cardesa-Salzmann, T., Climent, F., González-Barca, E., Mercadal, S., Mate, J. L., Sancho, J. M., Arenillas, L., Serrano, S., Escoda, L., Martínez, S., Valera, A., Martínez, A., Jares, P., Pinyol, M., García-Herrera, A., Martínez-Trillos, A., Giné, E., Villamor, N., Campo, E., Colomo, L., López-Guillermo, A., and Grup per l'Estudi dels Limfomes de Catalunya I Balears (GELCAB) (2011) Gene-expression profiling and not immunophenotypic algorithms predicts prognosis in patients with diffuse large B-cell lymphoma treated with immunochemotherapy. Blood 117, 4836-4843
12. Scott, D. W., Wright, G. W., Williams, P. M., Lih, C.-J., Walsh, W., Jaffe, E. S., Rosenwald, A., Campo, E., Chan, W. C., Connors, J. M., Smeland, E. B., Mottok, A., Braziel, R. M., Ott, G., Delabie, J., Tubbs, R. R., Cook, J. R., Weisenburger, D. D., Greiner, T. C., Glinsmann-Gibson, B. J., Fu, K., Staudt, L. M., Gascoyne, R. D., and Rimsza, L. M. (2014) Determining cell-of-origin subtypes of diffuse large B-cell lymphoma using gene expression in formalin-fixed paraffin-embedded tissue. Blood 123, 1214-1217
13. Nagaraj, N., Wisniewski, J. R., Geiger, T., Cox, J., Kircher, M., Kelso, J., Pääbo, S., and Mann, M. (2011) Deep proteome and transcriptome mapping of a human cancer cell line. Mol. Syst. Biol. 7, 548
14. Beck, M., Schmidt, A., Malmstroem, J., Claassen, M., Ori, A., Szymborska, A., Herzog, F., Rinner, O., Ellenberg, J., and Aebersold, R. (2011) The quantitative proteome of a human cell line. Mol. Syst. Biol. 7, 549
15. Nagaraj, N., Kulak, N. A., Cox, J., Neuhauser, N., Mayr, K., Hoerning, O., Vorm, O., and Mann, M. (2012) System-wide perturbation analysis with nearly complete coverage of the yeast proteome by single-shot ultra HPLC runs on a bench top Orbitrap. Mol. Cell. Proteomics 11, M111-013722
16. Mann, M., Kulak, N. A., Nagaraj, N., and Cox, J. (2013) The coming age of complete, accurate, and ubiquitous proteomes. Mol. Cell 49, 583-590
17. Ostasiewicz, P., Zielinska, D. F., Mann, M., and Wisńiewski, J. R. (2010) Proteome, phosphoproteome, and N-glycoproteome are quantitatively preserved in formalin-fixed paraffin-embedded tissue and analyzable by high-resolution mass spectrometry. J. Proteome Res. 9, 3688-3700
18. Deeb, S. J., D'Souza, R. C., Cox, J., Schmidt-Supprian, M., and Mann, M. (2012) Super-SILAC allows classification of diffuse large B-cell lymphoma subtypes by their protein expression profiles. Mol. Cell. Proteomics 11, 77-89
19. Deeb, S. J., Cox, J., Schmidt-Supprian, M., and Mann, M. (2014) N-Linked glycosylation enrichment for in-depth cell surface proteomics of diffuse large B-cell lymphoma subtypes. Mol. Cell. Proteomics 13, 240-251
20. Geiger, T., Cox, J., Ostasiewicz, P., Wisniewski, J. R., and Mann, M. (2010) Super-SILAC mix for quantitative proteomics of human tumor tissue. Nat. Methods 7, 383-385
21. Wisńiewski, J. R., Zougman, A., Nagaraj, N., and Mann, M. (2009) Universal sample preparation method for proteome analysis. Nat. Methods 6, 359-362
22. Wisńiewski, J. R., Zougman, A., and Mann, M. (2009) Combination of FASP and StageTip-based fractionation allows in-depth analysis of the hippocampal membrane proteome. J. Proteome Res. 8, 5674-5678
23. Rappsilber, J., Ishihama, Y., and Mann, M. (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663-670
24. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p. p. b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
25. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V., and Mann, M. (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res. 10, 1794-1805
26. Segal, E., Friedman, N., Koller, D., and Regev, A. (2004) A module map showing conditional activity of expression modules in cancer. Nat. Genet. 36, 1090-1098
27. Cox, J., and Mann, M. (2012) 1D and 2D annotation enrichment: a statistical method integrating quantitative proteomics with complementary highthroughput data. BMC Bioinformatics 13, Suppl. 16, S12
28. Tusher, V. G., Tibshirani, R., and Chu, G. (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U. S. A. 98, 5116-5121
29. Hewitt, S. M., Lewis, F. A., Cao, Y., Conrad, R. C., Cronin, M., Danenberg, K. D., Goralski, T. J., Langmore, J. P., Raja, R. G., Williams, P. M., Palma, J. F., and Warrington, J. A. (2008) Tissue handling and specimen preparation in surgical pathology: issues concerning the recovery of nucleic acids from formalin-fixed, paraffin-embedded tissue. Arch. Pathol. Lab. Med. 132, 1929-1935
30. Shi, S.-R., Liu, C., Balgley, B. M., Lee, C., and Taylor, C. R. (2006) Protein extraction from formalin-fixed, paraffin-embedded tissue sections: quality evaluation by mass spectrometry. J. Histochem. Cytochem. 54, 739-743
31. Hood, B. L., Darfler, M. M., Guiel, T. G., Furusato, B., Lucas, D. A., Ringeisen, B. R., Sesterhenn, I. A., Conrads, T. P., Veenstra, T. D., and Krizman, D. B. (2005) Proteomic analysis of formalin-fixed prostate cancer tissue. Mol. Cell. Proteomics 4, 1741-1753
32. Cox, J., Hein, M. Y., Luber, C. A., Paron, I., Nagaraj, N., and Mann, M. (2014) MaxLFQ allows accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction. Mol. Cell. Proteomics. 13, 2513-2526
33. Michalski, A., Damoc, E., Hauschild, J. P., Lange, O., Wieghaus, A., Makarov, A., Nagaraj, N., Cox, J., Mann, M., and Horning, S. (2011) Mass spectrometry-based proteomics using Q Exactive, a high-performance benchtop quadrupole Orbitrap mass spectrometer. Mol. Cell. Proteomics 10, M111-011015
34. Pfeifer, M., Grau, M., Lenze, D., Wenzel, S.-S., Wolf, A., Wollert-Wulf, B., Dietze, K., Nogai, H., Storek, B., Madle, H., Dörken, B., Janz, M., Dirnhofer, S., Lenz, P., Hummel, M., Tzankov, A., and Lenz, G. (2013) PTEN loss defines a PI3K/AKT pathway-dependent germinal center subtype of diffuse large B-cell lymphoma. Proc. Natl. Acad. Sci. U. S. A. 110, 12420-12425
35. Davis, R. E., Brown, K. D., Siebenlist, U., and Staudt, L. M. (2001) Constitutive nuclear factor κB activity is required for survival of activated B cell-like diffuse large B cell lymphoma cells. J. Exp. Med. 194, 1861-1874
36. Yang, Y., Shaffer, A. L., 3rd, Emre, N. C., Ceribelli, M., Zhang, M., Wright, G., Xiao, W., Powell, J., Platig, J., Kohlhammer, H., Young, R. M., Zhao, H., Yang, Y., Xu, W., Buggy, J. J., Balasubramanian, S., Mathews, L. A., Shinn, P., Guha, R., Ferrer, M., Thomas, C., Waldmann, T. A., and Staudt, L. M. (2012) Exploiting synthetic lethality for the therapy of ABC diffuse large B cell lymphoma. Cancer Cell 21, 723-737
37. Dent, A. L., Yewdell, J., Puvion-Dutilleul, F., Koken, M. H., De The, H., and Staudt, L. M. (1996) LYSP100-associated nuclear domains (LANDs): description of a new class of subnuclear structures and their relationship to PML nuclear bodies. Blood 88, 1423-1426
38. Bloch, D. B., De La Monte, S. M., Guigaouri, P., Filippov, A., and Bloch, K. D. (1996) Identification and characterization of a leukocyte-specific component of the nuclear body. J. Biol. Chem. 271, 29198-29204
39. Zucchelli, C., Tamburri, S., Quilici, G., Palagano, E., Berardi, A., Saare, M., Peterson, P., Bachi, A., and Musco, G. (2014) Structure of human Sp140 PHD finger: an atypical fold interacting with Pin1. FEBS J. 281, 216-231
40. Di Bernardo, M. C., Crowther-Swanepoel, D., Broderick, P., Webb, E., Sellick, G., Wild, R., Sullivan, K., Vijayakrishnan, J., Wang, Y., Pittman, A. M., Sunter, N. J., Hall, A. G., Dyer, M. J., Matutes, E., Dearden, C., Mainou-Fowler, T., Jackson, G. H., Summerfield, G., Harris, R. J., Pettitt, A. R., Hillmen, P., Allsup, D. J., Bailey, J. R., Pratt, G., Pepper, C., Fegan, C., Allan, J. M., Catovsky, D., and Houlston, R. S. (2008) A genome-wide association study identifies six susceptibility loci for chronic lymphocytic leukemia. Nat. Genet. 40, 1204-1210
41. Miranda, R. N., Briggs, R. C., Shults, K., Kinney, M. C., Jensen, R. A., and Cousar, J. B. (1999) Immunocytochemical analysis of MNDA in tissue sections and sorted normal bone marrow cells documents expression only in maturing normal and neoplastic myelomonocytic cells and a subset of normal and neoplastic B lymphocytes. Hum. Pathol. 30, 1040-1049
42. Joshi, A. D., Hegde, G. V., Dickinson, J. D., Mittal, A. K., Lynch, J. C., Eudy, J. D., Armitage, J. O., Bierman, P. J., Bociek, R. G., Devetten, M. P., Vose, J. M., and Joshi, S. S. (2007) ATM, CTLA4, MNDA, and HEM1 in high versus low CD38-expressing B-cell chronic lymphocytic leukemia. Clin. Cancer Res. 13, 5295-5304
43. Kanellis, G., Roncador, G., Arribas, A., Mollejo, M., Montes-Moreno, S., Maestre, L., Campos-Martin, Y., Ríos Gonzalez, J. L., Martinez-Torrecuadrada, J. L., Sanchez-Verde, L., Pajares, R., Cigudosa, J. C., Martin, M. C., and Piris, M. A. (2009) Identification of MNDA as a new marker for nodal marginal zone lymphoma. Leukemia 23, 1847-1857
44. Richmond, J., Tuzova, M., Cruikshank, W., and Center, D. (2014) Regulation of cellular processes by interleukin-16 in homeostasis and cancer. J. Cell. Physiol. 229, 139-147
45. Sano, H., Kane, S., Sano, E., Mîinea, C. P., Asara, J. M., Lane, W. S., Garner, C. W., and Lienhard, G. E. (2003) Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J. Biol. Chem. 278, 14599-14602
46. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
47. Yu, C. L., Jove, R., and Burakoff, S. J. (1997) Constitutive activation of the Janus kinase-STAT pathway in T lymphoma overexpressing the Lck protein tyrosine kinase. J. Immunol. 159, 5206-5210
48. Majolini, M. B., D'Elios, M. M., Galieni, P., Boncristiano, M., Lauria, F., Del Prete, G., Telford, J. L., and Baldari, C. T. (1998) Expression of the T-cell-specific tyrosine kinase Lck in normal B-1 cells and in chronic lymphocytic leukemia B cells. Blood 91, 3390-3396
49. Talab, F., Allen, J. C., Thompson, V., Lin, K., and Slupsky, J. R. (2013) LCK is an important mediator of B-cell receptor signaling in chronic lymphocytic leukemia cells. Mol. Cancer Res. 11, 541-554
50. Paterson, J. C., Tedoldi, S., Craxton, A., Jones, M., Hansmann, M. L., Collins, G., Roberton, H., Natkunam, Y., Pileri, S., Campo, E., Clark, E. A., Mason, D. Y., and Marafioti, T. (2006) The differential expression of LCK and BAFF-receptor and their role in apoptosis in human lymphomas. Haematologica 91, 772-780
51. Rosenwald, A., Wright, G., Chan, W. C., Connors, J. M., Campo, E., Fisher, R. I., Gascoyne, R. D., Muller-Hermelink, H. K., Smeland, E. B., Giltnane, J. M., Hurt, E. M., Zhao, H., Averett, L., Yang, L., Wilson, W. H., Jaffe, E. S., Simon, R., Klausner, R. D., Powell, J., Duffey, P. L., Longo, D. L., Greiner, T. C., Weisenburger, D. D., Sanger, W. G., Dave, B. J., Lynch, J. C., Vose, J., Armitage, J. O., Montserrat, E., López-Guillermo, A., Grogan, T. M., Miller, T. P., LeBlanc, M., Ott, G., Kvaloy, S., Delabie, J., Holte, H., Krajci, P., Stokke, T., Staudt, L. M., and Lymphoma/Leukemia Molecular Profiling Project (2002) The Use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. N. Engl. J. Med. 346, 1937-1947
52. Ramuz, O., Bouabdallah, R., Devilard, E., Borie, N., Groulet-Martinec, A., Bardou, V. J., Brousset, P., Bertucci, F., Birg, F., Birnbaum, D., and Xerri, L. (2005) Identification of TCL1A as an immunohistochemical marker of adverse outcome in diffuse large B-cell lymphomas. Int. J. Oncol. 26, 151-157
53. Banham, A. H., Connors, J. M., Brown, P. J., Cordell, J. L., Ott, G., Sreenivasan, G., Farinha, P., Horsman, D. E., and Gascoyne, R. D. (2005) Expression of the FOXP1 transcription factor is strongly associated with inferior survival in patients with diffuse large B-cell lymphoma. Clin. Cancer Res. 11, 1065-1072
54. Barrans, S. L., Fenton, J. A., Ventura, R., Smith, A., Banham, A. H., and Jack, A. S. (2007) Deregulated over expression of FOXP1 protein in diffuse large B-cell lymphoma does not occur as a result of gene rearrangement. Haematologica 92, 863-864
55. Weng, J., Rawal, S., Chu, F., Park, H. J., Sharma, R., Delgado, D. A., Fayad, L., Fanale, M., Romaguera, J., Luong, A., Kwak, L. W., and Neelapu, S. S. (2012) TCL1: a shared tumor-associated antigen for immunotherapy against B-cell lymphomas. Blood 120, 1613-1623
56. Wang, J. Q., Jeelall, Y. S., Beutler, B., Horikawa, K., and Goodnow, C. C. (2014) Consequences of the recurrent MYD88L265P somatic mutation for B cell tolerance. J. Exp. Med. 211, 413-426
57. Scott, D. W., and Gascoyne, R. D. (2014) The tumour microenvironment in B cell lymphomas. Nat. Rev. Cancer 14, 517-534
58. Hans, C. P., Weisenburger, D. D., Greiner, T. C., Gascoyne, R. D., Delabie, J., Ott, G., Müller-Hermelink, H. K., Campo, E., Braziel, R. M., Jaffe, E. S., Pan, Z., Farinha, P., Smith, L. M., Falini, B., Banham, A. H., Rosenwald, A., Staudt, L. M., Connors, J. M., Armitage, J. O., and Chan, W. C. (2004) Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood 103, 275-282
59. Hara, H., Wada, T., Bakal, C., Kozieradzki, I., Suzuki, S., Suzuki, N., Nghiem, M., Griffiths, E. K., Krawczyk, C., Bauer, B., D'Acquisto, F., Ghosh, S., Yeh, W.-C., Baier, G., Rottapel, R., and Penninger, J. M. (2003) The MAGUK family protein CARD11 is essential for lymphocyte activation. Immunity 18, 763-775
60. Tauzin, S., Ding, H., Burdevet, D., Borisch, B., and Hoessli, D. C. (2011) Membrane-associated signaling in human B-lymphoma lines. Exp. Cell Res. 317, 151-162
61. Rifai, N., Gillette, M. A., and Carr, S. A. (2006) Protein biomarker discovery and validation: the long and uncertain path to clinical utility. Nat. Biotechnol. 24, 971-983
62. Kulak, N. A., Pichler, G., Paron, I., Nagaraj, N., and Mann, M. (2014) Minimal, encapsulated proteomic-sample processing applied to copynumber estimation in eukaryotic cells. Nat. Methods 11, 319-324
63. Vizcaíno, J. A., Deutsch, E. W., Wang, R., Csordas, A., Reisinger, F., Ríos, D., Dianes, J. A., Sun, Z., Farrah, T., Bandeira, N., Binz, P.-A., Xenarios, I., Eisenacher, M., Mayer, G., Gatto, L., Campos, A., Chalkley, R. J., Kraus, H.-J., Albar, J. P., Martinez-Bartolomé, S., Apweiler, R., Omenn, G. S., Martens, L., Jones, A. R., and Hermjakob, H. (2014) ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol. 32, 223-226