STAT6 and STAT1 are essential antagonistic regulators of cell survival in classical Hodgkin lymphoma cell line

Leukemia

Volumn 23, Issue 10, 2009, Pages 1885-1893

  Baus, D ^a   Nonnenmacher, F ^a,b   Jankowski, S ^a,b   Doring C ^c   Brautigam C ^b   Frank, M ^c   Hansmann, M L ^c   Pfitzner, E ^a,b  

^a INSTITUTE FOR TUMOR BIOLOGY AND EXPERIMENTAL THERAPY   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 4; LENTIVIRUS VECTOR; SHORT HAIRPIN RNA; STAT1 PROTEIN; STAT6 PROTEIN;

APOPTOSIS; ARTICLE; B LYMPHOCYTE; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL PROLIFERATION; CELL SURVIVAL; CLASSICAL HODGKIN LYMPHOMA; CONTROLLED STUDY; DOWN REGULATION; DRUG ACTIVITY; GENE ACTIVATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE TARGETING; GENETIC IDENTIFICATION; GENETIC TRANSFORMATION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MICROARRAY ANALYSIS; PRIORITY JOURNAL; RAMOS B LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; VIRAL GENE DELIVERY SYSTEM;

EID: 70350123881     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2009.103     Document Type: Article

References (48)

1. Kuppers R, Hansmann ML, Rajewsky K. Clonality and germinal centre B-cell derivation of Hodgkin/Reed-Sternberg cells in Hodgkin's disease. Ann Oncol 1998; 9: S17-S20.
2. Thomas RK, Re D, Wolf J, Diehl V. Part I: Hodgkin's lymphoma - molecular biology of Hodgkin and Reed-Sternberg cells. Lancet Oncol 2004; 5: 11-18.
3. Kuppers R, Rajewsky K, Zhao M, Simons G, Laumann R, Fischer R et al Hodgkin disease: Hodgkin and Reed-Sternberg cells picked from histological sections show clonal immunoglobulin gene rearrangements and appear to be derived from B cells at various stages of development. Proc Natl Acad Sci USA 1994; 91: 10962-10966.
4. Kanzler H, Hansmann ML, Kapp U, Wolf J, Diehl V, Rajewsky K et al. Molecular single cell analysis demonstrates the derivation of a peripheral blood-derived cell line (L1236) from the Hodgkin/ Reed-Sternberg cells of a Hodgkin's lymphoma patient. Blood 1996; 87: 3429-3436.
5. Schwering I, Brauninger A, Distler V, Jesdinsky J, Diehl V, Hansmann ML et al. Profiling of Hodgkin's lymphoma cell line L1236 and germinal center B cells: Identification of Hodgkin's lymphoma-specific genes. Mol Med 2003; 9: 85-95.
6. Mathas S, Janz M, Hummel F, Hummel M, Wollert-Wulf B, Lusatis S et al Intrinsic inhibition of transcription factor E2A by HLH proteins ABF-1 and Id2 mediates reprogramming of neoplastic B cells in Hodgkin lymphoma. Nat Immunol 2006; 7: 207-215.
7. Skinnider BF, Kapp U, Mak TW. Interleukin 13: A growth factor in Hodgkin lymphoma. Int Arch Allergy Immunol 2001; 126: 267-276.
8. Skinnider BF, Mak TW. The role of cytokines in classical Hodgkin lymphoma. Blood 2002; 99: 4283-4297.
9. Baus D, Pfitzner E. Specific function of STAT3, SOCS1, and SOCS3 in the regulation of proliferation and survival of classical Hodgkin lymphoma cells. Int J Cancer 2006; 118: 1404-1413.
10. 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: 2679-2684.
11. 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: 489-495.
12. Kube D, Holtick U, Vockerodt M, Ahmadi T, Haier B, Behrmann I et al STAT3 is constitutively activated in Hodgkin cell lines. Blood 2001; 98: 762-770.
13. 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: 605-617.
14. Skinnider BF, Elia AJ, Gascoyne RD, Trumper LH, von Bonin F, Kapp U et al. Interleukin 13 and interleukin 13 receptor are frequently expressed by Hodgkin and Reed-Sternberg cells of Hodgkin lymphoma. Blood 2001; 97: 250-255.
15. Benekli M, Baer MR, Baumann H, Wetzler M. Signal transducer and activator of transcription proteins in leukemias. Blood 2003; 101: 2940-2954.
16. Bowman T, Garcia R, Turkson J, Jove R. STATs in oncogenesis. Oncogene 2000; 19: 2474-2488.
17. Holtick U, Vockerodt M, Pinkert D, Schoof N, Sturzenhofecker B, Kussebi N et al. STAT3 is essential for Hodgkin lymphoma cell proliferation and is a target of tyrphostin AG17 which confers sensitization for apoptosis. Leukemia 2005; 19: 936-944.
18. 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: 4706-4715.
19. 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: 1939-1946.
20. 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: 53-56.
21. Schaadt M, Fonatsch C, Kirchner H, Diehl V. Establishment of a malignant, Epstein-Barr-virus (EBV)-negative cell-line from the pleura effusion of a patient with Hodgkin's disease. Blut 1979; 38: 185-190.
22. Wolf J, Kapp U, Bohlen H, Kornacker M, Schoch C, Stahl B et al. Peripheral blood mononuclear cells of a patient with advanced Hodgkin's lymphoma give rise to permanently growing Hodgkin-Reed Sternberg cells. Blood 1996; 87: 3418-3428.
23. Klein G, Giovanella B, Westman A, Stehlin JS, Mumford D. An EBV-genome-negative cell line established from an American Burkitt lymphoma; receptor characteristics. EBV infectibility and permanent conversion into EBV-positive sublines by in vitro infection. Intervirology 1975; 5: 319-334.
24. Schnell T, Foley P, Wirth M, Munch J, Uberla K. Development of a self-inactivating, minimal lentivirus vector based on simian immunodeficiency virus. Hum Gene Ther 2000; 11: 439-447.
25. Fouchier RA, Meyer BE, Simon JH, Fischer U, Malim MH. HIV-1 infection of non-dividing cells: Evidence that the amino-terminal basic region of the viral matrix protein is important for Gag processing but not for post-entry nuclear import. EMBO J 1997; 16: 4531-4539.
26. Rippmann JF, Andreas S, Andreas W, Silke H. Gene silencing with STAT6 specific siRNAs blocks eotaxin release in IL-4/TNFα stimulated human epithelial cells. FEBS letters 2005; 579: 173-178.
27. Catlett-Falcone R, Landowski TH, Oshiro MM, Turkson J, Levitzki A, Savino R et al. Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 1999; 10: 105-115.
28. Mi H, Lazareva-Ulitsky B, Loo R, Kejariwal A, Vandergriff J, Rabkin S et al. The PANTHER database of protein families, subfamilies, functions and pathways. Nucleic Acids Res 2005; 33: D284-D288.
29. 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: 618-626.
30. Trieu Y, Wen XY, Skinnider BF, Bray MR, Li Z, Claudio JO et al. Soluble interleukin-13Ralpha2 decoy receptor inhibits Hodgkin's lymphoma growth in vitro and in vivo. The role of cytokines in classical Hodgkin lymphoma. Cancer Res 2004; 64: 3271-3275.
31. Schroder AJ, Pavlidis P, Arimura A, Capece D, Rothman PB. Cutting edge: STAT6 serves as a positive and negative regulator of gene expression in IL-4-stimulated B lymphocytes. J Immunol 2002; 168: 996-1000.
32. Lu X, Nechushtan H, Ding F, Rosado MF, Singal R, Alizadeh AA et al Distinct IL-4-induced gene expression, proliferation, and intracellular signaling in germinal center B-cell-like and activated B-cell-like diffuse large-cell lymphomas. Blood 2005; 105: 2924-2932.
33. Conrad DJ, Lu M. Regulation of human 12/15-lipoxygenase by Stat6-dependent transcription. Am J Respir Cell Mol Biol 2000; 22: 226-234.
34. Suto A, Nakajima H, Hirose K, Suzuki K, Kagami S, Seto Y et al. Interleukin 21 prevents antigen-induced IgE production by inhibiting germ line C(epsilon) transcription of IL-4-stimulated B cells. Blood 2002; 100: 4565-4573.
35. Zamorano J, Mora AL, Boothby M, Keegan AD. NF-kappa B activation plays an important role in the IL-4-induced protection from apoptosis. Int Immunol 2001; 13: 1479-1487.
36. Renne C, Willenbrock K, Kuppers R, Hansmann ML, Brauninger A. Autocrine and paracrine activated receptor tyrosine kinases in classical Hodgkin lymphoma. Blood 2005; 105: 4051-4059.
37. Irie-Sasaki J, Sasaki T, Matsumoto W, Opavsky A, Cheng M, Welstead G et al. CD45 is a JAK phosphatase and negatively regulates cytokine receptor signalling. Nature 2001; 409: 349-354.
38. Zhao X, Qiu W, Kung J, Peng X, Yegappan M, Yen-Lieberman B et al. Bortezomib induces caspase-dependent apoptosis in Hodgkin lymphoma cell lines and is associated with reduced c-FLIP expression: A gene expression profiling study with implications for potential combination therapies. Leuk Res 2008; 32: 275-285.
39. Drexler HG. Recent results on the biology of Hodgkin and Reed-Sternberg cells. II. Continuous cell lines. Leuk Lymphoma 1993; 9: 1-25.
40. Pesu M, Aittomaki S, Takaluoma K, Lagerstedt A, Silvennoinen O. p38 Mitogen-activated protein kinase regulates interleukin-4-induced gene expression by stimulating STAT6-mediated transcription. J Biol Chem 2002; 277: 38254-38261.
41. Bargou RC, Emmerich F, Krappmann D, Bommert K, Mapara MY, Arnold W et al. Constitutive nuclear factor-kappaB-RelA activation is required for proliferation and survival of Hodgkin's disease tumor cells. J Clin Invest 1997; 100: 2961-2969.
42. Mathas S, Hinz M, Anagnostopoulos I, Krappmann D, Lietz A, Jundt F et al. Aberrantly expressed c-Jun and JunB are a hallmark of Hodgkin lymphoma cells, stimulate proliferation and synergize with NF-kappa B. EMBO J 2002; 21: 4104-4113.
43. Bromberg JF, Horvath CM, Wen Z, Schreiber RD, Darnell Jr JE. Transcriptionally active Stat1 is required for the antiproliferative effects of both interferon alpha and interferon gamma. Proc Natl Acad Sci USA 1996; 93: 7673-7678.
44. Kim HS, Lee MS. STAT1 as a key modulator of cell death. Cell Signal 2007; 19: 454-465.
45. Garcia JF, Camacho FI, Morente M, Fraga M, Montalban C, Alvaro T et al. Hodgkin and Reed-Sternberg cells harbor alterations in the major tumor suppressor pathways and cell-cycle checkpoints: Analyses using tissue microarrays. Blood 2003; 101: 681-689.
46. Ohmori Y, Hamilton TA. Interleukin-4/STAT6 represses STAT1 and NF-kappa B-dependent transcription through distinct mechanisms. J Biol Chem 2000; 275: 38095-38103.
47. Venkataraman C, Leung S, Salvekar A, Mano H, Schindler U. Repression of IL-4-induced gene expression by IFN-gamma requires Stat1 activation. J Immunol 1999; 162: 4053-4061.
48. Naka T, Tsutsui H, Fujimoto M, Kawazoe Y, Kohzaki H, Morita Y et al SOCS-1/SSI-1-deficient NKT cells participate in severe hepatitis through dysregulated cross-talk inhibition of IFN-gamma and IL-4 signaling in vivo. Immunity 2001; 14: 535-545.