Phospho-proteomic analysis of mantle cell lymphoma cells suggests a pro-survival role of B-cell receptor signaling

Cellular Oncology

Volumn 34, Issue 2, 2011, Pages 141-153

  Pighi, Chiara ^a   Gu, Ting Lei ^b   Dalai, Irene ^a   Barbi, Stefano ^a   Parolini, Claudia ^a   Bertolaso, Anna ^a   Pedron, Serena ^a   Parisi, Alice ^a   Ren, Jianmin ^b   Cecconi, Daniela ^a   Chilosi, Marco ^a   Menestrina, Fabio ^a   Zamò, Alberto ^a,c  

^a UNIVERSITY OF VERONA   (Italy)

^b CELL SIGNALING TECHNOLOGY   (United States)

^c Sezione di Anatomia Patologica   (Italy)

Author keywords

BCR signaling; Mantle cell lymphoma; PhosphoScan; Piceatannol; Proteomics; Syk

Indexed keywords

B LYMPHOCYTE RECEPTOR; CYCLIN D1; PICEATANNOL; 3,3',4,5'-TETRAHYDROXYSTILBENE; ISOENZYME; LYMPHOCYTE ANTIGEN RECEPTOR; PHOSPHOPROTEIN; PROTEIN TYROSINE KINASE; STILBENE DERIVATIVE; TYRO3 PROTEIN, HUMAN; TYROSINE;

ARTICLE; CANCER SURVIVAL; CONTROLLED STUDY; FLOW CYTOMETRY; HIGH THROUGHPUT PHOSPHO PROTEOMICS; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPHOMA CELL LINE; MANTLE CELL LYMPHOMA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEOMICS; SIGNAL TRANSDUCTION; VALIDATION PROCESS; WESTERN BLOTTING; BIOLOGICAL MODEL; CELL SURVIVAL; DRUG ANTAGONISM; DRUG EFFECT; ENZYME ACTIVATION; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; METHODOLOGY; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

BLOTTING, WESTERN; CELL LINE, TUMOR; CELL SURVIVAL; ENZYME ACTIVATION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; ISOENZYMES; LYMPHOMA, MANTLE-CELL; MODELS, BIOLOGICAL; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEOMICS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, ANTIGEN, B-CELL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STILBENES; TYROSINE;

EID: 79960917689     PISSN: 22113428     EISSN: 22113436     Source Type: Journal    
DOI: 10.1007/s13402-011-0019-7     Document Type: Article

References (61)

1. S.H. Swerdlow, E. Campo, M. Seto, H.K. Muller-Hermelink, in Mantle cell lymphoma, in: WHO classification of tumours of haematopoietic and lymphoid tissues, ed. by S.H. Swerdlow, E. Campo, N.L. Harris, E.S. Jaffe, S. Pileri, H. Stein, J. Thiele, J. Vardiman (IARC Press, Lyon, 2008)
2. W.K. Hofmann, S. de Vos, K. Tsukasaki, W. Wachsman, G.S. Pinkus, J.W. Said, H.P. Koeffler, Altered apoptosis pathways in mantle cell lymphoma detected by oligonucleotide microarray. Blood 98, 787-794 (2001)
3. N. Martinez, F.I. Camacho, P. Algara, A. Rodriguez, A. Dopazo, E. Ruiz-Ballesteros, P. Martin, J.A. Martinez-Climent, J. Garcia-Conde, J. Menarguez, F. Solano, M. Mollejo, M.A. Piris, The molecular signature of mantle cell lymphoma reveals multiple signals favoring cell survival. Cancer Res. 63, 8226-8232 (2003) (Pubitemid 37549472)
4. E. Ortega-Paino, J. Fransson, S. Ek, C.A. Borrebaeck, Functionally associated targets in mantle cell lymphoma as defined by DNA microarrays and RNA interference. Blood 111, 1617-1624 (2008) (Pubitemid 351213453)
5. M. Pinyol, S. Bea, L. Pla, V. Ribrag, J. Bosq, A. Rosenwald, E. Campo, P. Jares, Inactivation of RB1 in mantle-cell lymphoma detected by nonsense-mediated mRNA decay pathway inhibition and microarray analysis. Blood 109, 5422-5429 (2007) (Pubitemid 46890565)
6. A. Rinaldi, I. Kwee, M. Taborelli, C. Largo, S. Uccella, V. Martin, G. Poretti, G. Gaidano, G. Calabrese, G. Martinelli, L. Baldini, G. Pruneri, C. Capella, E. Zucca, F.E. Cotter, J.C. Cigudosa, C.V. Catapano, M.G. Tibiletti, F. Bertoni, Genomic and expression profiling identifies the B-cell associated tyrosine kinase Syk as a possible therapeutic target in mantle cell lymphoma. Br. J. Haematol. 132, 303-316 (2006) (Pubitemid 43381537)
7. E.G. Rizzatti, R.P. Falcao, R.A. Panepucci, R. Proto-Siqueira, W. T. Anselmo-Lima, O.K. Okamoto, M.A. Zago, Gene expression profiling of mantle cell lymphoma cells reveals aberrant expression of genes from the PI3K-AKT, WNT and TGFbeta signalling pathways. Br. J. Haematol. 130, 516-526 (2005) (Pubitemid 43899754)
8. A. Rosenwald, G. Wright, A. Wiestner, W.C. Chan, J.M. Connors, E. Campo, R.D. Gascoyne, T.M. Grogan, H.K. Muller-Hermelink, E.B. Smeland, M. Chiorazzi, J.M. Giltnane, E.M. Hurt, H. Zhao, L. Averett, S. Henrickson, L. Yang, J. Powell, W.H. Wilson, E.S. Jaffe, R. Simon, R.D. Klausner, E. Montserrat, F. Bosch, T.C. Greiner, D.D. Weisenburger, W.G. Sanger, B.J. Dave, J.C. Lynch, J. Vose, J.O. Armitage, R.I. Fisher, T.P. Miller, M. LeBlanc, G. Ott, S. Kvaloy, H. Holte, J. Delabie, L.M. Staudt, The proliferation gene expression signature is a quantitative integrator of oncogenic events that predicts survival in mantle cell lymphoma. Cancer Cell 3, 185-197 (2003) (Pubitemid 37443390)
9. C. Thieblemont, V. Nasser, P. Felman, K. Leroy, S. Gazzo, E. Callet-Bauchu, B. Loriod, S. Granjeaud, P. Gaulard, C. Haioun, A. Traverse-Glehen, L. Baseggio, F. Bertucci, D. Birnbaum, F. Magrangeas, S. Minvielle, H. Avet-Loiseau, G. Salles, B. Coiffier, F. Berger, R. Houlgatte, Small lymphocytic lymphoma, marginal zone B-cell lymphoma, and mantle cell lymphoma exhibit distinct gene-expression profiles allowing molecular diagnosis. Blood 103, 2727-2737 (2004) (Pubitemid 38393031)
10. F. Antonucci, M. Chilosi, C. Parolini, M. Hamdan, H. Astner, P.G. Righetti, Two-dimensional molecular profiling of mantle cell lymphoma. Electrophoresis 24, 2376-2385 (2003) (Pubitemid 38089023)
11. D. Cecconi, A. Zamó, A. Parisi, E. Bianchi, C. Parolini, A.M. Timperio, L. Zolla, M. Chilosi, Induction of apoptosis in Jeko-1 mantle cell lymphoma cell line by resveratrol: A proteomic analysis. J. Proteome Res. 7, 2670-2680 (2008)
12. I.M. Ghobrial, D.J. McCormick, S.H. Kaufmann, A.A. Leontovich, D.A. Loegering, N.T. Dai, K.L. Krajnik, M.J. Stenson, M.F. Melhem, A.J. Novak, S.M. Ansell, T.E. Witzig, Proteomic analysis of mantle-cell lymphoma by protein microarray. Blood 105, 3722- 3730 (2005) (Pubitemid 40628222)
13. M. Weinkauf, Y. Zimmermann, E. Hartmann, A. Rosenwald, M. Rieken, A. Pastore, G. Hutter, W. Hiddemann, M. Dreyling, 2-D PAGE-based comparison of proteasome inhibitor bortezomib in sensitive and resistant mantle cell lymphoma. Electrophoresis 30, 974-986 (2009)
14. C. Jansen, K.M. Hebeda, M. Linkels, J.M. Grefte, J.M. Raemaekers, J.H. van Krieken, P.J. Groenen, Protein profiling of B-cell lymphomas using tissue biopsies: A potential tool for small samples in pathology. Cell. Oncol. 30, 27-38 (2008) (Pubitemid 351161035)
15. C. Jansen, T. Feuth, J.M.M. Raemaekers, J. Rijntjes, J.W. Meijer, P.J. Westenend, J. van Baarlen, J.H.J.M. van Krieken, K.M. Hebeda, P.J.T.A. Groenen, Protein profiling in pathology: Analysis and evaluation of 239 frozen tissue biopsies for diagnosis of Bcell lymphomas. Proteomics: Clin. Appl. 4, 519-527 (2010)
16. H. Stranneheim, L.M. Orre, J. Lehtio, J. Flygare, A comparison between protein profiles of B cell subpopulations and mantle cell lymphoma cells. Proteome Sci. 7, 43 (2009)
17. L. Miguet, G. Bechade, L. Fornecker, E. Zink, C. Felden, C. Gervais, R. Herbrecht, A. Van Dorsselaer, L. Mauvieux, S. Sanglier-Cianferani, Proteomic analysis of malignant B-cell derived microparticles reveals CD148 as a potentially useful antigenic biomarker for mantle cell lymphoma diagnosis. J. Proteome Res. 8, 3346-3354 (2009)
18. M. Weinkauf, M. Christopeit, W. Hiddemann, M. Dreyling, Proteome-and microarray-based expression analysis of lymphoma cell lines identifies a p53-centered cluster of differentially expressed proteins in mantle cell and follicular lymphoma. Electrophoresis 28, 4416-4426 (2007) (Pubitemid 350259043)
19. R.S. Boyd, R. Jukes-Jones, R. Walewska, D. Brown, M.J. Dyer, K. Cain, Protein profiling of plasma membranes defines aberrant signaling pathways in mantle cell lymphoma. Mol. Cell. Proteomics 8, 1501-1515 (2009)
20. D. Cecconi, A. Zamo, E. Bianchi, A. Parisi, S. Barbi, A. Milli, S. Rinalducci, A. Rosenwald, E. Hartmann, L. Zolla, M. Chilosi, Signal transduction pathways of mantle cell lymphoma: A phosphoproteome-based study. Proteomics 8, 4495-4506 (2008)
21. M. Weinkauf, W. Hiddemann, M. Dreyling, Sample pooling in 2-D gel electrophoresis: A new approach to reduce nonspecific expression background. Electrophoresis 27, 4555-4558 (2006) (Pubitemid 44869610)
22. J. Rush, A. Moritz, K.A. Lee, A. Guo, V.L. Goss, E.J. Spek, H. Zhang, X.M. Zha, R.D. Polakiewicz, M.J. Comb, Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol. 23, 94-101 (2005) (Pubitemid 41724631)
23. K. Rikova, A. Guo, Q. Zeng, A. Possemato, J. Yu, H. Haack, J. Nardone, K. Lee, C. Reeves, Y. Li, Y. Hu, Z. Tan, M. Stokes, L. Sullivan, J. Mitchell, R. Wetzel, J. Macneill, J.M. Ren, J. Yuan, C. E. Bakalarski, J. Villen, J.M. Kornhauser, B. Smith, D. Li, X. Zhou, S.P. Gygi, T.L. Gu, R.D. Polakiewicz, J. Rush, M.J. Comb, Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 131, 1190-1203 (2007) (Pubitemid 350235027)
24. J. Carretero, T. Shimamura, K. Rikova, A.L. Jackson, M.D. Wilkerson, C.L. Borgman, M.S. Buttarazzi, B.A. Sanofsky, K.L. McNamara, K.A. Brandstetter, Z.E. Walton, T.L. Gu, J.C. Silva, K. Crosby, G.I. Shapiro, S.M. Maira, H. Ji, D.H. Castrillon, C.F. Kim, C. Garcia-Echeverria, N. Bardeesy, N.E. Sharpless, N.D. Hayes, W.Y. Kim, J.A. Engelman, K.K. Wong, Integrative genomic and proteomic analyses identify targets for Lkb1-deficient metastatic lung tumors. Cancer Cell 17 547-559
25. D.K.Walters, V.L. Goss, E.P. Stoffregen, T.L. Gu, K. Lee, J. Nardone, L. McGreevey, M.C. Heinrich, M.W. Deininger, R. Polakiewicz, B.J. Druker, Phosphoproteomic analysis of AML cell lines identifies leukemic oncogenes. Leuk. Res. 30, 1097-1104 (2006) (Pubitemid 44055977)
26. V.L. Goss, K.A. Lee, A. Moritz, J. Nardone, E.J. Spek, J. MacNeill, J. Rush, M.J. Comb, R.D. Polakiewicz, A common phosphotyrosine signature for the Bcr-Abl kinase. Blood 107, 4888-4897 (2006) (Pubitemid 43882642)
27. T.L. Gu, V.L. Goss, C. Reeves, L. Popova, J. Nardone, J. Macneill, D.K. Walters, Y. Wang, J. Rush, M.J. Comb, B.J. Druker, R.D. Polakiewicz, Phosphotyrosine profiling identifies the KG-1 cell line as a model for the study of FGFR1 fusions in acute myeloid leukemia. Blood 108, 4202-4204 (2006) (Pubitemid 44913294)
28. T.L. Gu, J. Cherry, M. Tucker, J. Wu, C. Reeves, R.D. Polakiewicz, Identification of activated Tnk1 kinase in Hodgkin's lymphoma. Leukemia 24 861-865.
29. S. Bea, I. Salaverria, L. Armengol, M. Pinyol, V. Fernandez, E. M. Hartmann, P. Jares, V. Amador, L. Hernandez, A. Navarro, G. Ott, A. Rosenwald, X. Estivill, E. Campo, Uniparental disomies, homozygous deletions, amplifications, and target genes in mantle cell lymphoma revealed by integrative highresolution whole-genome profiling. Blood 113, 3059-3069 (2009)
30. F. Rubio-Moscardo, J. Climent, R. Siebert, M.A. Piris, J.I. Martin-Subero, I. Nielander, J. Garcia-Conde, M.J. Dyer, M.J. Terol, D. Pinkel, J.A. Martinez-Climent, Mantle-cell lymphoma genotypes identified with CGH to BAC microarrays define a leukemic subgroup of disease and predict patient outcome. Blood 105, 4445-4454 (2005) (Pubitemid 40720793)
31. I. Vater, F. Wagner, M. Kreuz, H. Berger, J.I. Martin-Subero, C. Pott, J.A. Martinez-Climent, W. Klapper, K. Krause, M.J. Dyer, S. Gesk, L. Harder, A. Zamo, M. Dreyling, D. Hasenclever, N. Arnold, R. Siebert, GeneChip analyses point to novel pathogenetic mechanisms in mantle cell lymphoma. Br. J. Haematol. 144, 317-331 (2009)
32. D. Hui, T. Reiman, J. Hanson, R. Linford, W. Wong, A. Belch, R. Lai, Immunohistochemical detection of cdc2 is useful in predicting survival in patients with mantle cell lymphoma. Mod. Pathol. 18, 1223-1231 (2005) (Pubitemid 43079922)
33. F. Jardin, J.M. Picquenot, F. Parmentier, P. Ruminy, M. Cornic, D. Penther, P. Bertrand, H. Lanic, O. Cassuto, C. Humbrecht, E. Lemasle, A. Wautier, C. Bastard, H. Tilly, Detection of gene copy number aberrations in mantle cell lymphoma by a single quantitative multiplex PCR assay: Clinicopathological relevance and prognosis value. Br. J. Haematol. (2009)
34. H. Tagawa, S. Karnan, R. Suzuki, K. Matsuo, X. Zhang, A. Ota, Y. Morishima, S. Nakamura, M. Seto, Genome-wide array-based CGH for mantle cell lymphoma: Identification of homozygous deletions of the proapoptotic gene. BIM Oncogene 24, 1348-1358 (2005) (Pubitemid 40343115)
35. Y.Y. Cho, F. Tang, K. Yao, C. Lu, F. Zhu, D. Zheng, A. Pugliese, A.M. Bode, Z. Dong, Cyclin-dependent kinase-3-mediated c-Jun phosphorylation at Ser63 and Ser73 enhances cell transformation. Cancer Res. 69, 272-281 (2009)
36. D. Zheng, Y.Y. Cho, A.T. Lau, J. Zhang, W.Y. Ma, A.M. Bode, Z. Dong, Cyclin-dependent kinase 3-mediated activating transcription factor 1 phosphorylation enhances cell transformation. Cancer Res. 68, 7650-7660 (2008)
37. H. Ogata, S. Goto, K. Sato, W. Fujibuchi, H. Bono, M. Kanehisa, KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 27, 29-34 (1999) (Pubitemid 29209394)
38. L. Chen, S. Monti, P. Juszczynski, J. Daley, W. Chen, T.E. Witzig, T.M. Habermann, J.L. Kutok, M.A. Shipp, SYK-dependent tonic B-cell receptor signaling is a rational treatment target in diffuse large B-cell lymphoma. Blood 111, 2230-2237 (2008) (Pubitemid 351451430)
39. R.E. Davis, V.N. Ngo, G. Lenz, P. Tolar, R.M. Young, P.B. Romesser, H. Kohlhammer, L. Lamy, H. Zhao, Y. Yang, W. Xu, A.L. Shaffer, G. Wright, W. Xiao, J. Powell, J.K. Jiang, C.J. Thomas, A. Rosenwald, G. Ott, H.K. Muller-Hermelink, R.D. Gascoyne, J.M. Connors, N.A. Johnson, L.M. Rimsza, E. Campo, E.S. Jaffe, W.H. Wilson, J. Delabie, E.B. Smeland, R.I. Fisher, R. M. Braziel, R.R. Tubbs, J.R. Cook, D.D. Weisenburger, W.C. Chan, S.K. Pierce, L.M. Staudt, Chronic active B-cell-receptor signalling in diffuse large B-cell lymphoma. Nature 463 88-92
40. 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 downregulatesMcl-1 and induces apoptosis in chronic lymphocytic leukemia B cells. Leukemia 23, 686-697 (2009)
41. J.W. Friedberg, J. Sharman, J. Sweetenham, P.B. Johnston, J.M. Vose, A. Lacasce, J. Schaefer-Cutillo, S. De Vos, R. Sinha, J.P. Leonard, L.D. Cripe, S.A. Gregory, M.P. Sterba, A.M. Lowe, R. Levy, M.A. Shipp, Inhibition of Syk with fostamatinib disodium has significant clinical activity in non-Hodgkin lymphoma and chronic lymphocytic leukemia. Blood 115 2578-2585
42. J.M. Oliver, D.L. Burg, B.S. Wilson, J.L. McLaughlin, R.L. Geahlen, Inhibition of mast cell Fc epsilon R1-mediated signaling and effector function by the Syk-selective inhibitor, piceatannol. J. Biol. Chem. 269, 29697-29703 (1994)
43. L. Leseux, S.M. Hamdi, T. Al Saati, F. Capilla, C. Recher, G. Laurent, C. Bezombes, Syk-dependent mTOR activation in follicular lymphoma cells. Blood 108, 4156-4162 (2006) (Pubitemid 44913287)
44. A. Rinaldi, I. Kwee, M. Taborelli, C. Largo, S. Uccella, V. Martin, G. Poretti, G. Gaidano, G. Calabrese, G. Martinelli, L. Baldini, G. Pruneri, C. Capella, E. Zucca, F.E. Cotter, J.C. Cigudosa, C.V. Catapano, M.G. Tibiletti, F. Bertoni, Genomic and expression profiling identifies the B-cell associated tyrosine kinase Syk as a possible therapeutic target in mantle cell lymphoma. Br. J. Haematol. 132, 303-316 (2006) (Pubitemid 43381537)
45. J. Ennaciri, D. Girard, IL-4R(alpha), a new member that associates with Syk kinase: Implication in IL-4-induced human neutrophil functions. J. Immunol. 183, 5261-5269 (2009)
46. L. Wang, E. Devarajan, J. He, S.P. Reddy, J.L. Dai, Transcription repressor activity of spleen tyrosine kinase mediates breast tumor suppression. Cancer Res. 65, 10289-10297 (2005) (Pubitemid 41743721)
47. F.M. Uckun, S. Qazi, H. Ma, L. Tuel-Ahlgren, Z. Ozer, STAT3 is a substrate of SYK tyrosine kinase in B-lineage leukemia/ lymphoma cells exposed to oxidative stress. Proc. Natl. Acad. Sci. U S A 107 2902-2907.
48. F. Baran-Marszak, M. Boukhiar, S. Harel, C. Laguillier, C. Roger, R. Gressin, A. Martin, R. Fagard, N. Varin-Blank, F. Ajchenbaum-Cymbalista, D. Ledoux, Constitutive and B-cell receptor-induced activation of STAT3 are important signaling pathways targeted by bortezomib in leukemic mantle cell lymphoma. Haematologica 95, 1865-1872 (2010)
49. L.V. Pham, A.T. Tamayo, C. Li, W. Bornmann, W. Priebe, R.J. Ford, Degrasyn potentiates the antitumor effects of bortezomib in mantle cell lymphoma cells in vitro and in vivo: Therapeutic implications. Mol. Cancer Ther. 9, 2026-2036 (2010)
50. S. Tauzin, H. Ding, K. Khatib, I. Ahmad, D. Burdevet, G. van Echten-Deckert, J.A. Lindquist, B. Schraven, N.U. Din, B. Borisch, D.C. Hoessli, Oncogenic association of the Cbp/PAG adaptor protein with the Lyn tyrosine kinase in human B-NHL rafts. Blood 111, 2310-2320 (2008) (Pubitemid 351451439)
51. M.A. Yared, J.D. Khoury, L.J. Medeiros, G.Z. Rassidakis, R. Lai, Activation status of the JAK/STAT3 pathway in mantle cell lymphoma. Arch. Pathol. Lab. Med. 129, 990-996 (2005) (Pubitemid 41060635)
52. R. Lai, G.Z. Rassidakis, L.J. Medeiros, V. Leventaki, M. Keating, T.J. McDonnell, Expression of STAT3 and its phosphorylated forms in mantle cell lymphoma cell lines and tumours. J. Pathol. 199, 84-89 (2003) (Pubitemid 36054732)
53. J.A. Diehl, M. Cheng, M.F. Roussel, C.J. Sherr, Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev. 12, 3499-3511 (1998) (Pubitemid 28553242)
54. J. Camps, I. Salaverria, M.J. Garcia, E. Prat, S. Bea, J.C. Pole, L. Hernandez, J. Del Rey, J.C. Cigudosa, M. Bernues, C. Caldas, D. Colomer, R. Miro, E. Campo, Genomic imbalances and patterns of karyotypic variability in mantle-cell lymphoma cell lines. Leuk. Res. 30, 923-934 (2006) (Pubitemid 43831180)
55. S.W. Tait, D.R. Green, Mitochondria and cell death: Outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 11, 621-632 (2010)
56. T. Miyashita, J.C. Reed, Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80, 293- 299 (1995)
57. F. Zhou, J. Hu, H. Ma, M.L. Harrison, R.L. Geahlen, Nucleocytoplasmic trafficking of the Syk protein tyrosine kinase. Mol. Cell. Biol. 26, 3478-3491 (2006)
58. L. Wang, L. Duke, P.S. Zhang, R.B. Arlinghaus, W.F. Symmans, A. Sahin, R. Mendez, J.L. Dai, Alternative splicing disrupts a nuclear localization signal in spleen tyrosine kinase that is required for invasion suppression in breast cancer. Cancer Res. 63, 4724-4730 (2003) (Pubitemid 36951053)
59. L. Bordin, C. Fiore, M. Bragadin, A.M. Brunati, G. Clari, Regulation of membrane band 3 Tyr-phosphorylation by proteolysis of p72(Syk) and possible involvement in senescence process. Acta. Biochim. Biophys. Sin. (Shanghai) 41, 846-851 (2009)
60. A. Zamo, G. Ott, T. Katzenberger, P. Adam, C. Parolini, A. Scarpa, M. Lestani, F.Menestrina,M. Chilosi, Establishment of theMAVER-1 cell line, a model for leukemic and aggressive mantle cell lymphoma. Haematologica 91, 40-47 (2006) (Pubitemid 43235384)
61. G. Dennis Jr., B.T. Sherman, D.A. Hosack, J. Yang, W. Gao, H.C. Lane, R.A. Lempicki, DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4, P3 (2003)