Dynamic mathematical modeling of IL13-induced signaling in Hodgkin and primary mediastinal B-cell lymphoma allows prediction of therapeutic targets

Cancer Research

Volumn 71, Issue 3, 2011, Pages 693-704

  Raia, Valentina ^a   Schilling, Marcel ^a   Böhm, Martin ^b   Hahn, Bettina ^b   Kowarsch, Andreas ^c   Raue, Andreas ^d   Sticht, Carsten ^e   Bohl, Sebastian ^a   Saile, Maria ^e   Möller, Peter ^f   Gretz, Norbert ^e   Timmer, Jens ^d   Theis, Fabian ^c   Lehmann, Wolf Dieter ^b   Lichter, Peter ^b   Klingmüller, Ursula ^a  

^a GERMAN CANCER RESEARCH CENTER   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d UNIVERSITY OF FREIBURG   (Germany)

^e UNIVERSITY OF HEIDELBERG   (Germany)

^f UNIVERSITY HOSPITAL ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 13; INTERLEUKIN RECEPTOR; JANUS KINASE 2; STAT2 PROTEIN; STAT6 PROTEIN;

ARTICLE; B CELL LYMPHOMA; B LYMPHOCYTE; BACTERIAL GENE; CANCER CELL CULTURE; CLASSICAL HODGKIN LYMPHOMA; GENE EXPRESSION; GENOME; HODGKIN DISEASE; HUMAN; HUMAN CELL; INFORMATION; LYMPHOMA CELL LINE; MATHEMATICAL MODEL; MEDIASTINUM TUMOR; MOLECULE; PREDICTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; SENSITIVITY ANALYSIS; UPREGULATION;

CELL LINE, TUMOR; HODGKIN DISEASE; HUMANS; INTERLEUKIN-13; JANUS KINASE 2; LYMPHOMA, B-CELL; MEDIASTINAL NEOPLASMS; MODELS, BIOLOGICAL; MOLECULAR TARGETED THERAPY; PHOSPHORYLATION; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; STAT6 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 79551508997     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-2987     Document Type: Article

References (44)

1. Guiter C, Dusanter-Fourt I, Copie-Bergman C, Boulland ML, Le Gouvello S, Gaulard P, et al. Constitutive STAT6 activation in primary mediastinal large B-cell lymphoma. Blood 2004;104:543-9. (Pubitemid 38900039)
2. Skinnider BF, Elia AJ, Gascoyne RD, Patterson B, Trumper L, Kapp U, et al. Signal transducer and activator of transcription 6 is frequently activated in Hodgkin and Reed-Sternberg cells of Hodgkin lymphoma. Blood 2002;99:618-26.
3. Melzner I, Bucur AJ, Bruderlein S , Dorsch K, Hasel C, Barth TF, et al. Biallelic mutation of SOCS-1 impairs JAK2 degradation and sustains phospho-JAK2 action in the MedB-1 mediastinal lymphoma line. Blood 2005;105:2535-42.
4. Weniger MA, Melzner I, Menz CK, Wegener S, Bucur AJ, Dorsch K, et al. Mutations of the tumor suppressor gene SOCS-1 in classical Hodgkin lymphoma are frequent and associated with nuclear phospho-STAT5 accumulation. Oncogene 2006;25:2679-84.
5. Meier C, Hoeller S, Bourgau C, Hirschmann P, Schwaller J, Went P, et al. Recurrent numerical aberrations of JAK2 and deregulation of the JAK2-STAT cascade in lymphomas. Mod Pathol 2009;22:476-87.
6. Martini M, Hohaus S, Petrucci G, Cenci T, Pierconti F, Massini G, et al. Phosphorylated STAT5 represents a new possible prognostic marker in Hodgkin lymphoma. Am J Clin Pathol 2008;129:472-7.
7. Rolling C, Treton D, Pellegrini S, Galanaud P, Richard Y. IL4 and IL13 receptors share the gamma c chain and activate STAT6, STAT3 and STAT5 proteins in normal human B cells. FEBS Lett 1996;393:53-6.
8. Murata T, Puri RK. Comparison of IL-13- and IL-4-induced signaling in EBV-immortalized human B cells. Cell Immunol 1997;175:33-40. (Pubitemid 27041841)
9. Kapp U, Yeh WC, Patterson B, Elia AJ, Kagi D, Ho A, et al. Interleukin 13 is secreted by and stimulates the growth of Hodgkin and Reed-Sternberg cells. J Exp Med 1999;189:1939-46.
10. Scheeren FA, Diehl SA, Smit LA, Beaumont T, Naspetti M, Bende RJ, et al. IL-21 is expressed in Hodgkin lymphoma and activates STAT5: evidence that activated STAT5 is required for Hodgkin lymphomagenesis. Blood 2008;111:4706-15.
11. Zi Z, Cho KH, Sung MH, Xia X, Zheng J, Sun Z. In silico identification of the key components and steps in IFN-gamma induced JAK-STAT signaling pathway. FEBS Lett 2005;579:1101-8.
12. Guerriero ML, Dudka A, Underhill-Day N, Heath JK, Priami C. Narrative-based computational modelling of the Gp130/JAK/STAT signalling pathway. BMC Syst Biol 2009;3:40.
13. Papin JA, Palsson BO. The JAK-STAT signaling network in the human B-cell: an extreme signaling pathway analysis. Biophys J 2004;87:37-46.
14. Yamada S, Shiono S, Joo A, Yoshimura A. Control mechanism of JAK/STAT signal transduction pathway. FEBS Lett 2003;534:190-6.
15. Singh A, Jayaraman A, Hahn J. Modeling regulatory mechanisms in IL-6 signal transduction in hepatocytes. Biotechnol Bioeng 2006;95: 850-62. (Pubitemid 44863203)
16. Swameye I, Muller TG, Timmer J, Sandra O, Klingmuller U. Identification of nucleocytoplasmic cycling as a remote sensor in cellular signaling by databased modeling. Proc Natl Acad Sci U S A 2003;100:1028-33.
17. Won HH, Park I, Lee E, Kim JW, Lee D. Comparative analysis of the JAK/STAT signaling through erythropoietin receptor and thrombopoietin receptor using a systems approach. BMC Bioinformatics 2009;10Suppl 1:S53.
18. Martelli M, Ferreri AJ, Johnson P. Primary mediastinal large B-cell lymphoma. Crit Rev Oncol Hematol 2008;68:256-63.
19. Hamilton A, Gallipoli P, Nicholson E, Holyoake TL. Targeted therapy in haematological malignancies. J Pathol 2010;220:404-18.
20. Möller P, Bruderlein S, Strater J, Leithauser F, Hasel C, Bataille F, et al. MedB-1, a human tumor cell line derived from a primary mediastinal large B-cell lymphoma. Int J Cancer 2001;92:348-53.
21. Schilling M, Maiwald T, Hengl S, Winter D, Kreutz C, Kolch W, et al. Theoretical and experimental analysis links isoform-specific ERK signalling to cell fate decisions. Mol Syst Biol 2009;5:334.
22. Vera J, Bachmann J, Pfeifer AC, Becker V, Hormiga JA, Darias NV, et al. A systems biology approach to analyse amplification in the JAK2-STAT5 signalling pathway. BMC Syst Biol 2008;2:38.
23. Schilling M, Maiwald T, Bohl S, Kollmann M, Kreutz C, Timmer J, et al. Quantitative data generation for systems biology: the impact of randomisation, calibrators and normalisers. Syst Biol (Stevenage) 2005;152:193-200. (Pubitemid 43125136)
24. Seidler J, Adal M, Kubler D, Bossemeyer D, Lehmann WD. Analysis of autophosphorylation sites in the recombinant catalytic subunit alpha of cAMP-dependent kinase by nano-UPLC-ESI-MS/MS. Anal Bioanal Chem 2009;395:1713-20.
25. Seidler J, Zinn N, Haaf E, Böhm ME, Winter D, Schlosser A, et al. Metal ion-mobilizing additives for comprehensive detection of femtomole amounts of phosphopeptides by reversed phase LC-MS. Amino Acids 2010. Jun 16. [Epub ahead of print].
26. Kowarsch A, Blöchl F, Bohl S, Saile M, Gretz N, Klingmüller U, et al. Knowledge-based matrix factorization temporally resolves the cellular responses to Il-6 stimulation. BMC Bioinformatics 2010;11-585.
27. Maiwald T, Timmer J. Dynamical modeling and multi-experiment fitting with PottersWheel. Bioinformatics 2008;24:2037-43.
28. Hengl S, Kreutz C, Timmer J, Maiwald T. Data-based identifiability analysis of non-linear dynamical models. Bioinformatics 2007;23:2612-8. (Pubitemid 350048365)
29. Kreutz C, Timmer J. Systems biology: experimental design. FEBS J 2009;276:923-42.
30. Xiao W, Hong H, Kawakami Y, Kato Y, Wu D, Yasudo H, et al. Tumor suppression by phospholipase C-beta3 via SHP-1-mediated dephosphorylation of Stat5. Cancer Cell 2009;16:161-71.
31. Kim YS, Seo DW, Kong SK, Lee JH, Lee ES, Stetler-Stevenson M, et al. TIMP1 induces CD44 expression and the activation and nuclear translocation of SHP1 during the late centrocyte/post-germinal center B cell differentiation. Cancer Lett 2008;269:37-45.
32. Hagner PR, Schneider A, Gartenhaus RB. Targeting the translational machinery as a novel treatment strategy for hematologic malignancies. Blood 2010;115:2127-35.
33. Nasim MT, Ghouri A, Patel B, James V, Rudarakanchana N, Morrell NW, et al. Stoichiometric imbalance in the receptor complex contributes to dysfunctional BMPR-II mediated signalling in pulmonary arterial hypertension. Hum Mol Genet 2008;17:1683-94.
34. Daines MO, Tabata Y, Walker BA, Chen W, Warrier MR, Basu S, et al. Level of expression of IL-13R alpha 2 impacts receptor distribution and IL-13 signaling. J Immunol 2006;176:7495-501.
35. Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 2005;5:263-74.
36. Matsumoto A, Masuhara M, Mitsui K, Yokouchi M, Ohtsubo M, Misawa H, et al. CIS, a cytokine inducible SH2 protein, is a target of the JAK-STAT5 pathway and modulates STAT5 activation. Blood 1997;89:3148-54.
37. Davey HW, McLachlan MJ, Wilkins RJ, Hilton DJ, Adams TE. STAT5b mediates the GH-induced expression of SOCS-2 and SOCS-3 mRNA in the liver. Mol Cell Endocrinol 1999;158:111-6.
38. Kitano H, Funahashi A, Matsuoka Y, Oda K. Using process diagrams for the graphical representation of biological networks. Nat Biotechnol 2005;23:961-6.
39. Joos S, Granzow M, Holtgreve-Grez H, Siebert R, Harder L, Martin-Subero JI, et al. Hodgkin's lymphoma cell lines are characterized by frequent aberrations on chromosomes 2p and 9p including REL and JAK2. Int J Cancer 2003;103:489-95.
40. Feys T, Poppe B, De Preter K, Van Roy N, Verhasselt B, De Paepe P, et al. A detailed inventory of DNA copy number alterations in four commonly used Hodgkin's lymphoma cell lines. Haematologica 2007;92:913-20.
41. Delibrias CC, Floettmann JE, Rowe M, Fearon DT. Downregulated expression of SHP-1 in Burkitt lymphomas and germinal center B lymphocytes. J Exp Med 1997;186:1575-83. (Pubitemid 27479817)
42. Renné C, Willenbrock K, Martin-Subero JI, Hinsch N, Döring C, Tiacci E, et al. High expression of several tyrosine kinases and activation of the PI3K/AKT pathway in mediastinal large B cell lymphoma reveals further similarities to Hodgkin lymphoma. Leukemia 2007;21:780-7.
43. Hinz M, Lemke P, Anagnostopoulos I, Hacker C, Krappmann D, Mathas S, et al. Nuclear factor kappaB-dependent gene expression profiling of Hodgkin's disease tumor cells, pathogenetic significance, and link to constitutive signal transducer and activator of transcription 5a activity. J Exp Med 2002; 196:605-17.
44. Nagy ZS, LeBaron MJ, Ross JA, Mitra A, Rui H, Kirken RA. STAT5 regulation of BCL10 parallels constitutive NFkappaB activation in lymphoid tumor cells. Mol Cancer 2009;8:67.