Transcriptional Repression of Bim by a Novel YY1-RelA Complex Is Essential for the Survival and Growth of Multiple Myeloma

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Potluri, Veena ^a   Noothi, Sunil K ^a   Vallabhapurapu, Subrahmanya D ^a   Yoon, Sang Oh ^a   Driscoll, James J ^a   Lawrie, Charles H ^b,c   Vallabhapurapu, Sivakumar ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b BIODONOSTIA HEALTH RESEARCH INSTITUTE   (Spain)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR YY1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CARCINOGENESIS; CELL NUCLEUS; CELL SURVIVAL; COLONY FORMATION; CONTROLLED STUDY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MOUSE; MULTIPLE MYELOMA; NONHUMAN; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; TRANSCRIPTION REGULATION; TUMOR XENOGRAFT;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; CELL PROLIFERATION; CELL SURVIVAL; HEK293 CELLS; HUMANS; MEMBRANE PROTEINS; MICE; MICE, NUDE; MULTIPLE MYELOMA; MULTIPROTEIN COMPLEXES; PROTO-ONCOGENE PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION, GENETIC; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS; YY1 TRANSCRIPTION FACTOR;

EID: 84880011606     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066121     Document Type: Article

References (45)

1. Kuehl WM, Bergsagel PL, (2002) Multiple myeloma: evolving genetic events and host interactions. Nat Rev Cancer 2: 175-187.
2. Chng WJ, Glebov O, Bergsagel PL, Kuehl WM, (2007) Genetic events in the pathogenesis of multiple myeloma. Best Pract Res Clin Haematol 20: 571-596.
3. Kuehl WM, Bergsagel PL (2005) Early genetic events provide the basis for a clinical classification of multiple myeloma. Hematology Am Soc Hematol Educ Program: 346-352.
4. Fonseca R, Bergsagel PL, Drach J, Shaughnessy J, Gutierrez N, et al. (2009) International Myeloma Working Group molecular classification of multiple myeloma: spotlight review. Leukemia 23: 2210-2221.
5. Chng WJ, Kuehl WM, Bergsagel PL, Fonseca R, (2008) Translocation t(4;14) retains prognostic significance even in the setting of high-risk molecular signature. Leukemia 22: 459-461.
6. Kuehl WM, Bergsagel PL, (2012) Molecular pathogenesis of multiple myeloma and its premalignant precursor. J Clin Invest 122: 3456-3463.
7. Zhan F, Huang Y, Colla S, Stewart JP, Hanamura I, et al. (2006) The molecular classification of multiple myeloma. Blood 108: 2020-2028.
8. Vallabhapurapu S, Karin M, (2009) Regulation and function of NF-kappaB transcription factors in the immune system. Annu Rev Immunol 27: 693-733.
9. Hayden MS, Ghosh S, (2008) Shared principles in NF-kappaB signaling. Cell 132: 344-362.
10. Naugler WE, Karin M, (2008) NF-kappaB and cancer-identifying targets and mechanisms. Curr Opin Genet Dev 18: 19-26.
11. Ben-Neriah Y, Karin M, (2011) Inflammation meets cancer, with NF-kappaB as the matchmaker. Nat Immunol 12: 715-723.
12. Keats JJ, Fonseca R, Chesi M, Schop R, Baker A, et al. (2007) Promiscuous mutations activate the noncanonical NF-kappaB pathway in multiple myeloma. Cancer Cell 12: 131-144.
13. Annunziata CM, Davis RE, Demchenko Y, Bellamy W, Gabrea A, et al. (2007) Frequent engagement of the classical and alternative NF-kappaB pathways by diverse genetic abnormalities in multiple myeloma. Cancer Cell 12: 115-130.
14. Wang H, Hertlein E, Bakkar N, Sun H, Acharyya S, et al. (2007) NF-kappaB regulation of YY1 inhibits skeletal myogenesis through transcriptional silencing of myofibrillar genes. Mol Cell Biol 27: 4374-4387.
15. Castellano G, Torrisi E, Ligresti G, Malaponte G, Militello L, et al. (2009) The involvement of the transcription factor Yin Yang 1 in cancer development and progression. Cell Cycle 8: 1367-1372.
16. Gordon S, Akopyan G, Garban H, Bonavida B, (2006) Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene 25: 1125-1142.
17. Shi Y, Lee JS, Galvin KM, (1997) Everything you have ever wanted to know about Yin Yang 1. Biochim Biophys Acta 1332: F49-66.
18. Galvin KM, Shi Y, (1997) Multiple mechanisms of transcriptional repression by YY1. Mol Cell Biol 17: 3723-3732.
19. Ficzycz A, Eskiw C, Meyer D, Marley KE, Hurt M, et al. (2001) Expression, activity, and subcellular localization of the Yin Yang 1 transcription factor in Xenopus oocytes and embryos. J Biol Chem 276: 22819-22825.
20. Palko L, Bass HW, Beyrouthy MJ, Hurt MM, (2004) The Yin Yang-1 (YY1) protein undergoes a DNA-replication-associated switch in localization from the cytoplasm to the nucleus at the onset of S phase. J Cell Sci 117: 465-476.
21. Rizkallah R, Hurt MM, (2009) Regulation of the transcription factor YY1 in mitosis through phosphorylation of its DNA-binding domain. Mol Biol Cell 20: 4766-4776.
22. Ficzycz A, Ovsenek N, (2002) The Yin Yang 1 transcription factor associates with ribonucleoprotein (mRNP) complexes in the cytoplasm of Xenopus oocytes. J Biol Chem 277: 8382-8387.
23. Strasser A, Puthalakath H, Bouillet P, Huang DC, O'Connor L, et al. (2000) The role of bim, a proapoptotic BH3-only member of the Bcl-2 family in cell-death control. Ann N Y Acad Sci 917: 541-548.
24. Gillings AS, Balmanno K, Wiggins CM, Johnson M, Cook SJ, (2009) Apoptosis and autophagy: BIM as a mediator of tumour cell death in response to oncogene-targeted therapeutics. FEBS J 276: 6050-6062.
25. Bergsagel PL, Chesi M, Nardini E, Brents LA, Kirby SL, et al. (1996) Promiscuous translocations into immunoglobulin heavy chain switch regions in multiple myeloma. Proc Natl Acad Sci U S A 93: 13931-13936.
26. Tan BT, Park CY, Ailles LE, Weissman IL, (2006) The cancer stem cell hypothesis: a work in progress. Lab Invest 86: 1203-1207.
27. Takebe N, Harris PJ, Warren RQ, Ivy SP, (2011) Targeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathways. Nat Rev Clin Oncol 8: 97-106.
28. Mertins SD, Scudiero DA, Hollingshead MG, Divelbiss RD Jr, Alley MC, et al. (2013) A small molecule (pluripotin) as a tool for studying cancer stem cell biology: proof of concept. PLoS One 8: e57099.
29. Matsui W, Wang Q, Barber JP, Brennan S, Smith BD, et al. (2008) Clonogenic multiple myeloma progenitors, stem cell properties, and drug resistance. Cancer Res 68: 190-197.
30. Jakubikova J, Adamia S, Kost-Alimova M, Klippel S, Cervi D, et al. (2011) Lenalidomide targets clonogenic side population in multiple myeloma: pathophysiologic and clinical implications. Blood 117: 4409-4419.
31. Matsui W, Huff CA, Wang Q, Malehorn MT, Barber J, et al. (2004) Characterization of clonogenic multiple myeloma cells. Blood 103: 2332-2336.
32. Yang H, Robinson SN, Nieto Y, Jones RJ, Gocke CD, et al. (2011) Ex vivo graft purging and expansion of autologous blood progenitor cell products from patients with multiple myeloma. Cancer Res 71: 5040-5049.
33. Ley R, Ewings KE, Hadfield K, Cook SJ, (2005) Regulatory phosphorylation of Bim: sorting out the ERK from the JNK. Cell Death Differ 12: 1008-1014.
34. Jiang CC, Lai F, Tay KH, Croft A, Rizos H, et al. (2010) Apoptosis of human melanoma cells induced by inhibition of B-RAFV600E involves preferential splicing of bimS. Cell Death Dis 1: e69.
35. Inta I, Paxian S, Maegele I, Zhang W, Pizzi M, et al. (2006) Bim and Noxa are candidates to mediate the deleterious effect of the NF-kappa B subunit RelA in cerebral ischemia. J Neurosci 26: 12896-12903.
36. Laubach JP, Mitsiades CS, Roccaro AM, Ghobrial IM, Anderson KC, et al. (2009) Clinical challenges associated with bortezomib therapy in multiple myeloma and Waldenstroms Macroglobulinemia. Leuk Lymphoma 50: 694-702.
37. Lopez-Royuela N, Balsas P, Galan-Malo P, Anel A, Marzo I, et al. (2010) Bim is the key mediator of glucocorticoid-induced apoptosis and of its potentiation by rapamycin in human myeloma cells. Biochim Biophys Acta 1803: 311-322.
38. Romagnoli M, Seveno C, Wuilleme-Toumi S, Amiot M, Bataille R, et al. (2009) The imbalance between Survivin and Bim mediates tumour growth and correlates with poor survival in patients with multiple myeloma. Br J Haematol 145: 180-189.
39. Namba M, Ohtsuki T, Mori M, Togawa A, Wada H, et al. (1989) Establishment of five human myeloma cell lines. In Vitro Cell Dev Biol 25: 723-729.
40. Jackson N, Lowe J, Ball J, Bromidge E, Ling NR, et al. (1989) Two new IgA1-kappa plasma cell leukaemia cell lines (JJN-1 & JJN-2) which proliferate in response to B cell stimulatory factor 2. Clin Exp Immunol 75: 93-99.
41. Hitzler JK, Martinez-Valdez H, Bergsagel DB, Minden MD, Messner HA, (1991) Role of interleukin-6 in the proliferation of human multiple myeloma cell lines OCI-My 1 to 7 established from patients with advanced stage of the disease. Blood 78: 1996-2004.
42. Cook G, Campbell JD, Carr CE, Boyd KS, Franklin IM, (1999) Transforming growth factor beta from multiple myeloma cells inhibits proliferation and IL-2 responsiveness in T lymphocytes. J Leukoc Biol 66: 981-988.
43. Vallabhapurapu S, Matsuzawa A, Zhang W, Tseng PH, Keats JJ, et al. (2008) Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-kappaB signaling. Nat Immunol 9: 1364-1370.
44. Jensen MM, Jorgensen JT, Binderup T, Kjaer A, (2008) Tumor volume in subcutaneous mouse xenografts measured by microCT is more accurate and reproducible than determined by 18F-FDG-microPET or external caliper. BMC Med Imaging 8: 16.
45. Sivakumar V, Hammond KJ, Howells N, Pfeffer K, Weih F, (2003) Differential requirement for Rel/nuclear factor kappa B family members in natural killer T cell development. J Exp Med 197: 1613-1621.