The rGel/BLyS fusion toxin inhibits STAT3 signaling via down-regulation of interleukin-6 receptor in diffuse large B-cell lymphoma

Biochemical Pharmacology

Volumn 80, Issue 9, 2010, Pages 1335-1342

  Lyu, Mi Ae ^a   Sung, Bokyung ^a   Cheung, Lawrence H ^a   Marks, John W ^a   Aggarwal, Bharat B ^a   Aguiar, Ricardo C T ^b   Rosenblum, Michael G ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b University of Texas Health Science Center at San Antonio   (United States)

Author keywords

Apoptosis; Diffuse large B cell lymphoma; Fusion toxin; Interleukin 6 receptor; STAT3

Indexed keywords

B CELL ACTIVATING FACTOR; CYTOTOXIC AGENT; INTERLEUKIN 6 RECEPTOR; MYC PROTEIN; PROTEIN BCL XL; PROTEIN KINASE SYK; PROTEIN MCL 1; PROTEIN P21; PROTEIN TYROSINE PHOSPHATASE SHP 1; RGEL TOXIN; STAT3 PROTEIN; UNCLASSIFIED DRUG; DNA; GEL PROTEIN, GELONIUM MULTIFLORUM; HYBRID PROTEIN; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; RIBOSOME INACTIVATING PROTEIN 1; SIGNAL PEPTIDE; STAT3 PROTEIN, HUMAN;

ARTICLE; CELL CYCLE G1 PHASE; CELL GROWTH; CONTROLLED STUDY; DNA BINDING; DOWN REGULATION; DRUG TARGETING; GERMINAL CENTER; HUMAN; HUMAN CELL; LARGE CELL LYMPHOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; APOPTOSIS; DRUG EFFECTS; LYMPHOMA, LARGE B-CELL, DIFFUSE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

APOPTOSIS; B-CELL ACTIVATING FACTOR; CELL LINE, TUMOR; DNA; DOWN-REGULATION; G1 PHASE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOMA, LARGE B-CELL, DIFFUSE; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, INTERLEUKIN-6; RECOMBINANT FUSION PROTEINS; RIBOSOME INACTIVATING PROTEINS, TYPE 1; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 77956651261     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.07.017     Document Type: Article

References (44)

1. Vose J.M. Current approaches to the management of non-Hodgkin's lymphoma. Semin Oncol 1998, 25:483-491.
2. Rosenwald A., Wright G., Chan W.C., Connors J.M., Campo E., Fisher R.I. The use of molecular profiling to predict survival after chemotherapy for diffuse large B-cell lymphoma. N Engl J Med 2002, 346:1937-1947.
3. Wright G., Tan B., Rosenwald A., Hurt E.H., Wiestner A., Staudt L.M. A gene expression-based method to diagnose clinically distinct subgroups of diffuse large B cell lymphoma. Proc Natl Acad Sci USA 2003, 100:9991-9996.
4. Ihle J.N. STATs: signal transducers and activators of transcription. Cell 1996, 84:331-334.
5. Darnell J.E. Transcription factors as targets for cancer therapy. Nat Rev Cancer 2002, 2:740-749.
6. Buettner R., Mora L.B., Jove R. Activated STAT signaling in human tumors provides novel molecular targets for therapeutic intervention. Clin Cancer Res 2002, 8:945-954.
7. Bharti A.C., Donato N., Aggarwal B.B. Curcumin (diferuloylmethane) inhibits constitutive and IL-6-inducible STAT3 phosphorylation in human multiple myeloma cells. J Immunol 2003, 171:3863-3871.
8. Bowman T., Garcia R., Turkson J., Jove R. STATs in oncogenesis. Oncogene 2000, 19:2474-2488.
9. Sinibaldi D., Wharton W., Turkson J., Bowman T., Pledger W.J., Jove R. Induction of p21WAF1/CIP1 and cyclin D1 expression by the Src oncoprotein in mouse fibroblasts: role of activated STAT3 signaling. Oncogene 2000, 19:5419-5427.
10. Bowman T., Broome M.A., Sinibaldi D., Wharton W., Pledger W.J., Sedivy J.M. Stat3-mediated Myc expression is required for Src transformation and PDGF-induced mitogenesis. Proc Natl Acad Sci USA 2001, 98:7319-7324.
11. Epling-Burnette P.K., Liu J.H., Catlett-Falcone R., Turkson J., Oshiro M., Kothapalli R. Inhibition of STAT3 signaling leads to apoptosis of leukemic large granular lymphocytes and decreased Mcl-1 expression. J Clin Invest 2001, 107:351-362.
12. Opfeman J.T., Letal A., Beard C., Sorcinelli M.D., Ong C.C., Korsmeyer S.J. Development and maintenance of B and T lymphocytes requires anti-apoptotic Mcl-1. Nature 2003, 426:671-676.
13. Kitada S., Anderson J., Akar S., Zapata J.M., Takayama S., Krajewski S. Expression of apoptosis-regulating proteins in chronic lymphocytic leukemia: correlation with in vitro and in vivo chemoresponses. Blood 1998, 91:3379-3389.
14. Ding B.B., Yu J.J., Yu R.Y., Mendez L.M., Shaknovich R., Zhang Y. Constitutively activated STAT3 promotes cell proliferation and survival in the activated B-cell subtype of diffuse large B-cell lymphomas. Blood 2008, 111:1515-1523.
15. Lam L.T., Wright G., Davis R.E., Wright G., Lenz G., Farinha P. Cooperative signaling through the signal transducer and activator of transcription 3 and nuclear factor-κB pathways in subtypes of diffuse large B-cell lymphoma. Blood 2008, 111:3701-3713.
16. Lyu M.-A., Cheung L.H., Hittelman W.N., Marks J.W., Aguiar R.C., Rosenblum M.G. The rGel/BLyS fusion toxin specifically targets malignant B cells expressing the BLyS receptors BAFF-R, TACI, and BCMA. Mol Cancer Ther 2007, 6:460-470.
17. Nimmanapalli R., Lyu M.-A., Du M., Keating M.J., Rosenblum M.G., Gandhi V. The growth factor fusion construct containing B-lymphocyte stimulator (BLyS) and the toxin rGel induces apoptosis specifically in BAFF-R-positive CLL cells. Blood 2007, 109:2557-2564.
18. Alizadeh A.A., Eisen M.B., Davis R.E., Ma C., Lossos I.S., Rosenwald A., et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 2000, 403:503-511.
19. Davis R.E., Brown K.D., Siebenlist U., Staudt L.M. Constitutive nuclear factor kappa activity is required for survival of activated B cell-like diffuse large B cell lymphoma cells. J Exp Med 2001, 194:1861-1874.
20. Rai D., Karanti S., Jung I., Dahia P.L., Aguiar R.C. Coordinated expression of microRNA-155 and predicted target genes in diffuse large B-cell lymphoma. Cancer Genet Cytogenet 2008, 181:8-15.
21. Yu H., Jove R. The STATs of cancer: new molecular targets come of age. Nat Rev Cancer 2004, 4:97-105.
22. Laâbi Y., Gras M.P., Carbonnel F., Brouet J.C., Berger R., Larsen C.J. A new gene, BCM, on chromosome 16 is fused to the interleukin 2 gene by a t(4;16)(q26;p13) translocation in a malignant T cell lymphoma. EMBO J 1992, 11:3897-3904.
23. von Bulow G.U., Bram R.J. NFAT activation induced by a CAML-interacting member of the tumor necrosis factor receptor superfamily. Science 1997, 278:138-141.
24. Thompson J.S., Bixler S.A., Qian F., Vora K., Scott M.L., Cachero T.G. BAFF-R, a newly identified TNF receptor that specifically interacts with BAFF. Science 2001, 293:2108-2111.
25. Yu C.L., Meyer D.J., Campbell G.S., Larner A.C., Carter-Su C., Schwartz J. Enhanced DNA-binding activity of a Stat3-related protein in cells transformed by the Src oncoprotein. Science 1995, 269:81-83.
26. Oka T., Ouchida M., Koyama M., Ogama Y., Takada S., Nakatani Y. Gene silencing of the tyrosine phosphatase SHP1 gene by aberrant methylation in leukemias/lymphomas. Cancer Res 2002, 62:6390-6394.
27. Kim S.-W., Rai D., McKeller M.R., Aguiar R.C. Rational combined targeting of phosphodiesterase 4B and SYK in DLBCL. Blood 2009, 113:6153-6160.
28. Uckun F.M., Qazi S., Ma H., Tuei-Ahlgren L., Ozar Z. STAT3 is a substrate of SYK tyrosine kinase in B-lineage leukemia/lymphoma cells exposed to oxidative stress. Proc Natl Acad Sci USA 2010, 107:2902-2907.
29. Yee C., Biondi A., Wang X.H., Iscove N.N., de Sousa J., Aarden L.A. A possible autocrine role for interleukin-6 in two lymphoma cell lines. Blood 1989, 74:798-804.
30. Ludwig H., Nachbaur D.M., Fritz E., Krainer M., Huber H. Interleukin-6 is a prognostic factor in multiple myeloma. Blood 1991, 77:2794-2795.
31. Voorzanger N., Touitou R., Garcia E., Delecluse H.J., Rousset F., Joab I. Interleukin (IL)-10 and IL-6 are produced in vivo by non-Hodgkin's lymphoma cells and act as cooperative growth factors. Cancer Res 1996, 56:5499-5505.
32. Seymour J.F., Talpaz M., Cabanillas F., Wetzler M., Kurzrock R. Serum interleukin-6 levels correlated with prognosis in diffuse large-cell lymphoma. J Clin Oncol 1995, 13:575-582.
33. Zushi S., Shinomura Y., Kiyohara T., Miyazaki Y., Kondo S., Sugimachi M. STAT3 mediates the survival signal in oncogenic ras-transfected intestinal epithelial cells. Int J Cancer 1998, 78:326-330.
34. Kiuchi N., Nakajima K., Ichiba M. STAT3 is required for the gp130-mediated full activation of the c-myc gene. J Exp Med 1999, 189:63-73.
35. Puthier D., Bataille R., Amiot M. IL-6 up-regulates mcl-1 in human myeloma cells through JAK/STAT rather than ras/MAP kinase pathway. Eur J Immunol 1999, 29:33945-33950.
36. Sellers L.A., Feniuk W., Humphrey P.P., Lauder H. Activated G protein-coupled receptor induces tyrosine phosphorylation of STA3 and agonist-selective serine phosphorylation via sustained stimulation of mitogen-activated protein kinase. Resultant effects on cell proliferation. J Biol Chem 1999, 274:16423-16430.
37. Sriuranpong V., Park J.I., Amornphimoltham P., Patel V., Nelkin B.D., Gutkind J.S. Epidermal growth factor receptor-independent constitutive activation of STAT3 in head and neck squamous cell carcinoma is mediated by the autocrine/paracrine stimulation of the interleukin 6/gp130 cytokine system. Cancer Res 2003, 63:2948-2956.
38. Shinriki S., Jono H., Ota K., Ueda M., Kudo M., Ota T. Humanized anti-interleukin-6 receptor antibody suppresses tumor angiogenesis and in vivo growth of human oral squamous cell carcinoma. Clin Cancer Res 2009, 15:5426-5434.
39. Bromberg J.F., Wrzesczynska M.H., Devgan G., Zhao Y., Pestell R.G., Albanese C. Stat3 as an oncogene. Cell 1999, 99:295-303.
40. Catlett-Falcone R., Landowski T.H., Oshiro M.M., Turkson J., Levitzki A., Savino R. Constitutive activation of STAT3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 1999, 10:105-115.
41. Rinaldi A., Kwee I., Taborelli M., Largo C., Uccella S., Martin V., et al. Genomic and expression profiling identifies the B-cell associated tyrosine kinase Syk as a possible therapeutic target in mantle cell lymphoma. Br J Haematol 2006, 132:303-316.
42. Chen L., Monti S., Juszczynski P., Daley J., Chen W., Witzig T.E., et al. Syk-dependent tonic B-cell receptor signaling is a rational treatment target in diffuse large B-cell lymphoma. Blood 2008, 111:2230-2237.
43. Yu Z., Zhang W., Kone B.C. Signal transducers and activation of transcription3 (STAT3) inhibits transcription of the inducible nitric oxide synthase gene by interacting with nuclear factor κB. Biochem J 2002, 367:97-105.
44. Digicaylioglu M., Lipton S.A. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-κB signaling cascades. Nature 2001, 412:641-647.