Interleukin-6 and JAK2/STAT3 signaling mediate the reversion of dexamethasone resistance after dexamethasone withdrawal in 7TD1 multiple myeloma cells

Leukemia Research

Volumn 37, Issue 10, 2013, Pages 1322-1328

  Liu, Tuoen ^a   Fei, Zhiqiang ^b   Gangavarapu, Kalyan J ^c   Agbenowu, Senyo ^c   Bhushan, Alok ^c   Lai, James C K ^c   Daniels, Christopher K ^c   Cao, Shousong ^d  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Shenzhen Second Hospital   (China)

^c IDAHO STATE UNIVERSITY   (United States)

^d ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

AG490; Dexamethasone resistance; Dexamethasone withdrawal; Interleukin 6; JAK2 STAT3 signaling pathway; Multiple myeloma

Indexed keywords

DEXAMETHASONE; ETOPOSIDE; INTERLEUKIN 6; INTERLEUKIN 6 ANTIBODY; JANUS KINASE 2; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; STAT3 PROTEIN;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER RESISTANCE; CELL PROLIFERATION; CELL STRAIN 7TD1; CONTROLLED STUDY; CYTOTOXICITY; MOUSE; MULTIPLE MYELOMA; MYELOMA CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

AG490; DEXAMETHASONE RESISTANCE; DEXAMETHASONE WITHDRAWAL; INTERLEUKIN-6; JAK2/STAT3 SIGNALING PATHWAY; MULTIPLE MYELOMA;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; DEXAMETHASONE; DRUG RESISTANCE, NEOPLASM; INTERLEUKIN-6; JANUS KINASE 2; MICE; MULTIPLE MYELOMA; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TYRPHOSTINS;

EID: 84883558293     PISSN: 01452126     EISSN: 18735835     Source Type: Journal    
DOI: 10.1016/j.leukres.2013.06.026     Document Type: Article

References (50)

1. Zaidi A.A., Vesole D.H. Multiple myeloma: an old disease with new hope for the future. CA Cancer J Clin 2001, 51:273-285.
2. Siegel R., Naishadham D., Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012, 62:10-29.
3. Gadóa K., Domjána G., Hegyesib H., Falus A. Role of interleukin-6 in the pathogenesis of multiple myeloma. Cell Biol Int 2000, 24:195-209.
4. Kyle R.A., Rajkumar S.V. Multiple myeloma. Blood 2008, 111:2962-2972.
5. Barlogie B., Shaughnessy J., Tricot G., Jacobson J., Zangari M., Anaissie E., et al. Treatment of multiple myeloma. Blood 2004, 103:20-32.
6. Bruno B., Giaccone L., Rotta M., Anderson K., Boccadoro M. Novel targeted drugs for the treatment of multiple myeloma: from bench to bedside. Leukemia 2005, 19:1729-1738.
7. Rousseau G.G., Baxter J.D., Tomkins G.M. Glucocorticoid receptors: relations between steroid binding and biological effects. J Mol Biol 1972, 67:99-115.
8. Okret S., Poellinger L., Dong Y., Gustafsson J.A. Down-regulation of glucocorticoid receptor mRNA by glucocorticoid hormones and recognition by the receptor of a specific binding sequence within a receptor cDNA clone. Proc Natl Acad Sci USA 1986, 83:5899-5903.
9. Rogatsky I., Trowbridge J.M., Garabedian M.J. Glucocorticoid receptor-mediated cell cycle arrest is achieved through distinct cell-specific transcriptional regulatory mechanisms. Mol Cell Biol 1997, 17:3181-3193.
10. Kip1 and enhances dexamethasone-induced G1 arrest and apoptosis in human T lymphoblastic leukemia cells. Leuk Res 2000, 24:119-127.
11. Nuutinen U., Suoranta S., Eeva J., Eray M., Pellinen R., Wahlfors J., et al. Dexamethasone-induced apoptosis and up-regulation of Bim is dependent on glycogen synthase kinase-3. Leuk Res 2009, 33:1714-1717.
12. Marchetti M.C., Marco B.D., Cifone G., Migliorati G., Riccardi C. Dexamethasone-induced apoptosis of thymocytes: role of glucocorticoid receptor-associated Src kinase and caspase-8 activation. Blood 2003, 101:585-593.
13. Chua C.C., Chua B.H.L., Chen Z., Cathy L., Hamdy R.C. Dexamethasone induces caspase activation in murine osteoblastic MC3T3-E1 cells. Biochim Biophys Acta 2003, 1642:79-85.
14. Abrams M.T., Robertson N.M., Yoon K., Wickstrom E. Inhibition of glucocorticoid-induced apoptosis by targeting the major splice variants of BIM mRNA with small interfering RNA and short hairpin RNA. J Biol Chem 2004, 279:55809-55817.
15. Chrysis D., Zaman F., Chagin A.S., Takigawa M., Sävendahl L. Dexamethasone induces apoptosis in proliferative chondrocytes through activation of caspases and suppression of the Akt-phosphatidylinositol 3'-kinase signaling pathway. Endocrinology 2005, 146:1391-1397.
16. Sharma S., Lichtenstein A. Dexamethasone-induced apoptotic mechanisms in myeloma cells investigated by analysis of mutant glucocorticoid receptors. Blood 2008, 112:1338-1345.
17. Schmidt S., Rainer J., Ploner C., Presul E., Riml S., Kofler R. Glucocorticoid-induced apoptosis and glucocorticoid resistance: molecular mechanisms and clinical relevance. Cell Death Differ 2004, 11:S45-S55.
18. Marchetti M.C., Marco B.D., Santini M.C., Bartoli A., Delfino D.V., Riccardi C. Dexamethasone-induced thymocytes apoptosis requires glucocorticoid receptor nuclear translocation but not mitochondrial membrane potential transition. Toxicol Lett 2003, 139:175-180.
19. Bachmann P.S., Gorman R., MacKenzie K.L., Lutze-Mann L., Lock R.B. Dexamethasone resistance in B-cell precursor childhood acute lymphoblastic leukemia occurs downstream of ligand-induced nuclear translocation of the glucocorticoid receptor. Blood 2005, 105:2519-2526.
20. Gazitt Y., Fey V., Thomas C., Alvarez R. Bcl-2 overexpression is associated with resistance to dexamethasone, but not melphalan, in multiple myeloma cells. Int J Oncol 1998, 13:397-405.
21. Kerr R., Stirling D., Ludlam C.A. Interleukin 6 and haemostasis. Br J Haematol 2001, 115:3-12.
22. Heinrich P.C., Behrmann I., Haan S., Hermanns H.M., Müller-Newen G., Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 2003, 374:1-20.
23. Simpson R.J., Hammacher A., Smith D.K., Matthews J.M., Ward L.D. Interleukin-6: structure-function relationships. Protein Sci 1997, 6:929-955.
24. Mitsiades C.S., McMillin D.W., Klippel S., Hideshima T., Chauhan D., Richardson P.G., et al. The role of the bone marrow microenvironment in the pathophysiology of myeloma and its significance in the development of more effective therapies. Hematol Oncol Clin North Am 2007, 21:1007-1034.
25. Chatterjee M., Hönemann D., Lentzsch S., Bommert K., Sers C., Herrmann P., et al. In the presence of bone marrow stromal cells human multiple myeloma cells become independent of the IL-6/gp130/STAT3 pathway. Blood 2002, 100:3311-3318.
26. Chauhan D., Pandey P., Hideshima T., Treon S., Raje N., Davies F.E., et al. SHP2 mediates the protective effect of interleukin-6 against dexamethasone-induced apoptosis in multiple myeloma cells. J Biol Chem 2000, 275:27845-27850.
27. Urashima M., Teoh G., Chauhan D., Hoshi Y., Ogata A., Treon S.P., et al. Interleukin-6 overcomes p21WAF1 upregulation and G1 growth arrest induced by dexamethasone and interferon-gamma in multiple myeloma cells. Blood 1997, 90:279-289.
28. Xu F.H., Sharma S., Gardner A., Tu Y., Raitano A., Sawyers C., et al. Interleukin-6-induced inhibition of multiple myeloma cell apoptosis: support for the hypothesis that protection is mediated via inhibition of the JNK/SAPK pathway. Blood 1998, 92:241-251.
29. Bosscher K.D., Berghe W.V., Vermeulen L., Plaisance S., Boone E., Haegeman G. Glucocorticoids repress NF-αB-driven genes by disturbing the interaction of p65 with the basal transcription machinery, irrespective of coactivator levels in the cell. Proc Natl Acad Sci USA 2000, 97:3919-3924.
30. Ray A., Prefontaine K.E. Physical association and functional antagonism between the p65 subunit of transcription factor NF-αB and the glucocorticoid receptor. Proc Natl Acad Sci USA 1994, 91:752-756.
31. D'Acquisto F., May M.J., Ghosh S. Inhibition of nuclear factor kappa B (NF-αB): an emerging theme in anti-inflammatory therapies. Mol Interv 2002, 2:22-35.
32. Boumpas D. A novel action of glucocorticoids-NF-kappa B inhibition. Br J Rheumatol 1996, 35:709-710.
33. Bruno B., Rotta M., Giaccone L., Massaia M., Bertola A., Palumbo A., et al. New drugs for treatment of multiple myeloma. Lancet Oncol 2004, 5:430-442.
34. Greenstein S., Krett N.L., Kurosawa Y., Ma C., Chauhan D., Hideshima T., et al. Characterization of the MM.1 human multiple myeloma (MM) cell lines: a model system to elucidate the characteristics, behavior, and signaling of steroid-sensitive and -resistant MM cells. Exp Hematol 2003, 31:271-282.
35. Frassanito M.A., Cusmai A., Iodice G., Dammacco F. Autocrine interleukin-6 production and highly malignant multiple myeloma: relation with resistance to drug-induced apoptosis. Blood 2001, 97:483-489.
36. Boulanger M.J., Chow D.C., Brevnova E.E., Garcia K.C. Hexameric structure and assembly of the interleukin-6/IL-6α-receptor/gp130 complex. Science 2003, 300:2101-2104.
37. Hibi M., Murakami M., Saito M., Hirano T., Taga T., Kishimoto T. Molecular cloning and expression of an IL-6 signal transducer, gp130. Cell 1990, 63:1149-1157.
38. Sandur S.K., Pandey M.K., Sung B., Aggarwal B.B. 5-hydroxy-2-methyl-1,4-naphthoquinone, a vitamin K3 analogue, suppresses STAT3 activation pathway through induction of protein tyrosine phosphatase, SHP-1: potential role in chemosensitization. Mol Cancer Res 2010, 8:107-118.
39. Wegenka U.M., Lutticken C., Jan B., Yuan J., Lottspeich F., Mueller-Esterl W., et al. The interleukin-6-activated acute-phase response factor is antigenically and functionally related to members of the signal transducer and activator of transcription (STAT) family. Mol Cell Biol 1994, 14:3186-3196.
40. Heinrich P.C., Behrmann I., MÜller-Newen G., Schaper F., Graeve L. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem J 1998, 334:297-314.
41. Lentzsch S., Chatterjee M., Gries M., Bommert K., Gollasch H., Doerken B., et al. PI3-K/AKT/FKHR and MAPK signaling cascades are redundantly stimulated by a variety of cytokines and contribute independently to proliferation and survival of multiple myeloma cells. Leukemia 2004, 18:1883-1890.
42. Ogata A., Chauhan D., Teoh G., Treon S.P., Urashima M., Schlossman R.L., et al. IL-6 triggers cell growth via the Ras-dependent mitogen-activated protein kinase cascade. J Immunol 1997, 159:2212-2221.
43. Irvina B.J., Hansona C.L., Smithb L.H., Daniels C.K. Cyclic AMP- and IL6-signaling cross talk: comodulation of proliferation and apoptosis in the 7TD1 B cell hybridoma. Exp Cell Res 2001, 265:73-79.
44. Gangavarapu K.J., Olbertz J.L., Bhushan A., Lai J.C.K., Daniels C.K. Apoptotic resistance exhibited by dexamethasone-resistant murine 7TD1 cells is controlled independently of interleukin-6 triggered signaling. Apoptosis 2008, 13:1394-1400.
45. Wang L.H., Kirken R.A., Erwin R.A., Yu C.R., Farrar W.L. JAK3, STAT, and MAPK signaling pathways as novel molecular targets for the tyrphostin AG-490 regulation of IL-2-mediated T cell response. J Immunol 1999, 162:3897-3904.
46. Raeve H.R.D., Vanderkerke K. The role of the bone marrow microenvironment in multiple myeloma. Histol Histopathol 2005, 20:1227-1250.
47. Meydan N., Grunberger T., Dadi H., Shahar M., Arpaia E., Lapidot Z., et al. Inhibition of acute lymphoblastic leukaemia by a Jak-2 inhibitor. Nature 1996, 379:645-648.
48. James S.E., Burden H., Burgess R., Xie Y., Yang T., Massa S.M., et al. Anti-cancer drug Induced neurotoxicity and identification of Rho pathway signaling modulators as potential neuroprotectants. Neurotoxicology 2008, 29:605-612.
49. Wang L., Kitaichi K., Hui C.S., Takagi K., Takagi K., Sakai M., et al. Reversal of anticancer drug resistance by macrolide antibiotics in vitro and in vivo. Clin Exp Pharmacol Physiol 2000, 27:587-593.
50. Dudakov J.A., Goldberg G.L., Reiseger J.J., Chidgey A.P., Boyd R.L. Withdrawal of sex steroids reverses age- and chemotherapy-related defects in bone marrow lymphopoiesis. J Immunol 2009, 182:6247-6260.