The biphasic role of NF-κB in progression and chemoresistance of ovarian cancer

Clinical Cancer Research

Volumn 17, Issue 8, 2011, Pages 2181-2194

  Yang, Gong ^a,d   Xiao, Xue ^c,d   Rosen, Daniel G ^d   Cheng, Xi ^a   Wu, Xiaohua ^a   Chang, Bin ^d   Liu, Guangzhi ^d   Xue, Fengxia ^d   Mercado Uribe, Imelda ^d   Chiao, Paul ^d   Du, Xiang ^a,b   Liu, Jinsong ^d  

^a FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

^b FUDAN UNIVERSITY   (China)

^c SICHUAN UNIVERSITY   (China)

^d UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOPLATIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PACLITAXEL; STRESS ACTIVATED PROTEIN KINASE 1; SYNAPTOTAGMIN I; TRANSCRIPTION FACTOR RELA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL; CANCER RESISTANCE; CANCER SURVIVAL; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GROWTH INHIBITION; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; ONCOGENE; OVARY CANCER; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGNOSIS; PROTEIN PHOSPHORYLATION; SURVIVAL TIME; TUMOR SUPPRESSOR GENE;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; CARBOPLATIN; CELL LINE, TUMOR; CELL NUCLEUS; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; EPITHELIAL CELLS; FEMALE; HUMANS; I-KAPPA B PROTEINS; KAPLAN-MEIER ESTIMATE; MICE; MICE, INBRED BALB C; MICE, NUDE; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; OVARIAN NEOPLASMS; PACLITAXEL; PHOSPHORYLATION; RNA INTERFERENCE; TRANSCRIPTION FACTOR RELA; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 79954612742     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-10-3265     Document Type: Article

References (50)

1. Dixit V, Mak TW. NF-kappaB signaling. Many roads lead to Madrid. Cell 2002;111:615-9. (Pubitemid 35441244)
2. Vallabhapurapu S, Karin M. Regulation and function of NF-kappaB transcription factors in the immune system. Annu Rev Immunol 2009;27:693-733.
3. Aggarwal BB. Nuclear factor-kappaB: the enemy within. Cancer Cell 2004;6:203-8.
4. Biswas DK, Shi Q, Baily S, Strickland I, Ghosh S, Pardee AB, et al. NFkappa B activation in human breast cancer specimens and its role in cell proliferation and apoptosis. Proc Natl Acad Sci U S A 2004;101:10137-42. (Pubitemid 38891208)
5. Scherer DC, Brockman JA, Chen Z, Maniatis T, Ballard DW. Signalinduced degradation of I kappa B alpha requires site-specific ubiquitination. Proc Natl Acad Sci U S A 1995;92:11259-63. (Pubitemid 3015352)
6. Brown K, Gerstberger S, Carlson L, Franzoso G, Siebenlist U. Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation. Science 1995;267:1485-8.
7. Brockman JA, Scherer DC, McKinsey TA, Hall SM, Qi X, Lee WY, et al. Coupling of a signal response domain in I kappa B alpha to multiple pathways for NF-kappa B activation. Mol Cell Biol 1995;15:2809-18.
8. Dajee M, Lazarov M, Zhang JY, Cai T, Green CL, Russell AJ, et al. NFkappaB blockade and oncogenic Ras trigger invasive human epidermal neoplasia. Nature 2003;421:639-43. (Pubitemid 36227672)
9. Meylan E, Dooley AL, Feldser DM, Shen L, Turk E, Ouyang C, et al. Requirement for NF-kappaB signalling in a mouse model of lung adenocarcinoma. Nature 2009;462:104-7.
10. Regnier CH, Song HY, Gao X, Goeddel DV, Cao Z, Rothe M. Identification and characterization of an IkappaB kinase. Cell 1997;90:373-83.
11. Wang CY, Mayo MW, Baldwin AS. Jr. TNF-and cancer therapyinduced apoptosis: potentiation by inhibition of NF-kappaB. Science 1996;274:784-7. (Pubitemid 26398259)
12. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature 2006;441:431-6. (Pubitemid 44050137)
13. Luo JL, Maeda S, Hsu LC, Yagita H, Karin M. Inhibition of NF-kappaB in cancer cells converts inflammation-induced tumor growth mediated by TNFalpha to TRAIL-mediated tumor regression. Cancer Cell 2004;6:297-305. (Pubitemid 39222042)
14. Barkett M, Gilmore TD. Control of apoptosis by Rel/NF-kappaB transcription factors. Oncogene 1999;18:6910-24.
15. Perkins ND, Gilmore TD. Good cop, bad cop: the different faces of NFkappaB. Cell Death Differ 2006;13:759-72.
16. Ryan KM, Ernst MK, Rice NR, Vousden KH. Role of NF-kappaB in p53-mediated programmed cell death. Nature 2000;404:892-7. (Pubitemid 30230343)
17. Lee BL, Lee HS, Jung J, Cho SJ, Chung HY, Kim WH, et al. Nuclear factor-kappaB activation correlates with better prognosis and Akt activation in human gastric cancer. Clin Cancer Res 2005;11:2518-25. (Pubitemid 40569448)
18. van Hogerlinden M, Rozell BL, Ahrlund-Richter L, Toftgard R. Squamous cell carcinomas and increased apoptosis in skin with inhibited Rel/nuclear factor-kappaB signaling. Cancer Res 1999;59:3299-303. (Pubitemid 29334479)
19. Zhang JY, Green CL, Tao S, Khavari PA. NF-kappaB RelA opposes epidermal proliferation driven by TNFR1 and JNK. Genes Dev 2004;18:17-22. (Pubitemid 38090684)
20. Lazarov M, Kubo Y, Cai T, Dajee M, Tarutani M, Lin Q, et al. CDK4 coexpression with Ras generates malignant human epidermal tumorigenesis. Nat Med 2002;8:1105-14. (Pubitemid 35175965)
21. Liu J, Yang D, Minemoto Y, Leitges M, Rosner MR, Lin A. NF-kappaB is required for UV-induced JNK activation via induction of PKCdelta. Mol Cell 2006;21:467-80. (Pubitemid 43228003)
22. Campbell KJ, Rocha S, Perkins ND. Active repression of antiapoptotic gene expression by RelA (p65) NF-kappa B. Mol Cell 2004;13:853-65. (Pubitemid 38438480)
23. Bratasz A, Weir NM, Parinandi NL, Zweier JL, Sridhar R, Ignarro LJ, et al. Reversal to cisplatin sensitivity in recurrent human ovarian cancer cells by NCX-4016, a nitro derivative of aspirin. Proc Natl Acad Sci U S A 2006;103:3914-9. (Pubitemid 43376655)
24. Rocconi RP, Case AS, Straughn JM. Jr, Estes JM, Partridge EE. Role of chemotherapy for patients with recurrent platinum-resistant advanced epithelial ovarian cancer: a cost-effectiveness analysis. Cancer 2006;107:536-43. (Pubitemid 44107214)
25. Kleinberg L, Dong HP, Holth A, Risberg B, Trope' CG, Nesland JM, et al. Cleaved caspase-3 and nuclear factor-kappaB p65 are prognostic factors in metastatic serous ovarian carcinoma. Hum Pathol 2009;40:795-806.
26. Annunziata CM, Stavnes HT, Kleinberg L, Berner A, Hernandez LF, Birrer MJ, et al. Nuclear factor kappaB transcription factors are coexpressed and convey a poor outcome in ovarian cancer. Cancer 2010;116:3276-84.
27. Mabuchi S, Ohmichi M, Nishio Y, Hayasaka T, Kimura A, Ohta T, et al. Inhibition of NFkappaB increases the efficacy of cisplatin in in vitro and in vivo ovarian cancer models. J Biol Chem 2004;279:23477-85. (Pubitemid 38685659)
28. Hernandez L, Hsu SC, Davidson B, Birrer MJ, Kohn EC, Annunziata CM. Activation of NF-kappaB signaling by inhibitor of NF-kappaB kinase beta increases aggressiveness of ovarian cancer. Cancer Res 2010;70:4005-14.
29. Jinawath N, Vasoontara C, Jinawath A, Fang X, Zhao K, Yap KL, et al. Oncoproteomic analysis reveals co-upregulation of RELA and STAT5 in carboplatin resistant ovarian carcinoma. PLoS One 2010;5:e11198.
30. Huang S, Robinson JB, Deguzman A, Bucana CD, Fidler IJ. Blockade of nuclear factor-kappaB signaling inhibits angiogenesis and tumorigenicity of human ovarian cancer cells by suppressing expression of vascular endothelial growth factor and interleukin 8. Cancer Res 2000;60:5334-9.
31. Mabuchi S, Ohmichi M, Nishio Y, Hayasaka T, Kimura A, Ohta T, et al. Inhibition of inhibitor of nuclear factor-kappaB phosphorylation increases the efficacy of paclitaxel in in vitro and in vivo ovarian cancer models. Clin Cancer Res 2004;10:7645-54. (Pubitemid 39557528)
32. Huang Y, Fan W. IkappaB kinase activation is involved in regulation of paclitaxel-induced apoptosis in human tumor cell lines. Mol Pharmacol 2002;61:105-13. (Pubitemid 34049517)
33. Aghajanian C, Dizon DS, Sabbatini P, Raizer JJ, Dupont J, Spriggs DR. Phase I trial of bortezomib and carboplatin in recurrent ovarian or primary peritoneal cancer. J Clin Oncol 2005;23:5943-9.
34. Konstantinopoulos PA, Fountzilas E, Pillay K, Zerbini LF, Libermann TA, Cannistra SA, et al. Carboplatin-induced gene expression changes in vitro are prognostic of survival in epithelial ovarian cancer. BMC Med Genomics 2008;1:59.
35. Munshi A, Kurland JF, Nishikawa T, Chiao PJ, Andreeff M, Meyn RE. Inhibition of constitutively activated nuclear factor-kappaB radiosensitizes human melanoma cells. Mol Cancer Ther 2004;3:985-92. (Pubitemid 39199593)
36. Yang G, Rosen DG, Zhang Z, Bast RC, Mills GB, Colacino JA, et al. The chemokine growth-regulated oncogene 1 (Gro-1) links RAS signaling to the senescence of stromal fibroblasts and ovarian tumorigenesis. Proc Natl Acad Sci U S A 2006;103:16472-7. (Pubitemid 44715220)
37. Yang G, Rosen DG, Liu G, Yang F, Guo X, Xiao X, et al. CXCR2 promotes ovarian cancer growth through dysregulated cell cycle, diminished apoptosis, and enhanced angiogenesis. Clin Cancer Res 2010;16:3875-86.
38. Camp RL, Dolled-Filhart M, Rimm DL. X-tile: a new bio-informatics tool for biomarker assessment and outcome-based cut-point optimization. Clin Cancer Res 2004;10:7252-9. (Pubitemid 39487712)
39. Chung H, Wu D, Han SN, Gay R, Goldin B, Bronson RE, et al. Vitamin E supplementation does not alter azoxymethane-induced colonic aberrant crypt foci formation in young or old mice. J Nutr 2003;133:528-32. (Pubitemid 36172911)
40. Yu D, Wolf JK, Scanlon M, Price JE, Hung MC. Enhanced c-erbB-2/neu expression in human ovarian cancer cells correlates with more severe malignancy that can be suppressed by E1A. Cancer Res 1993;53:891-8. (Pubitemid 23077880)
41. Ahluwalia A, Hurteau JA, Bigsby RM, Nephew KP. DNA methylation in ovarian cancer. II. Expression of DNA methyltransferases in ovarian cancer cell lines and normal ovarian epithelial cells. Gynecol Oncol 2001;82:299-304. (Pubitemid 32730607)
42. Moore DH, Allison B, Look KY, Sutton GP, Bigsby RM. Collagenase expression in ovarian cancer cell lines. Gynecol Oncol 1997;65:78-82. (Pubitemid 27171556)
43. Bednarski BK, Baldwin AS. Jr, Kim HJ. Addressing reported proapoptotic functions of NF-kappaB: targeted inhibition of canonical NF-kappaB enhances the apoptotic effects of doxorubicin. PLoS One 2009;4:e6992.
44. Huang Y, Johnson KR, Norris JS, Fan W. Nuclear factor-kappaB/IkappaB signaling pathway may contribute to the mediation of paclitaxel induced apoptosis in solid tumor cells. Cancer Res 2000;60:4426-32. (Pubitemid 32103621)
45. Monick MM, Powers LS, Gross TJ, Flaherty DM, Barrett CW, Hunninghake GW. Active ERK contributes to protein translation by preventing JNK-dependent inhibition of protein phosphatase 1. J Immunol 2006;177:1636-45. (Pubitemid 44092499)
46. van Hogerlinden M, Auer G, Toftgard R. Inhibition of Rel/nuclear factor-kappaB signaling in skin results in defective DNA damageinduced cell cycle arrest and Ha-ras-and p53-independent tumor development. Oncogene 2002;21:4969-77.
47. Jin F, Liu X, Zhou Z, Yue P, Lotan R, Khuri FR, et al. Activation of nuclear factor-kappaB contributes to induction of death receptors and apoptosis by the synthetic retinoid CD437 in DU145 human prostate cancer cells. Cancer Res 2005;65:6354-63. (Pubitemid 40994422)
48. Rocha S, Campbell KJ, Perkins ND. p53-and Mdm2-independent repression of NF-kappa B transactivation by the ARF tumor suppressor. Mol Cell 2003;12:15-25. (Pubitemid 36945034)
49. Rocha S, Perkins ND. ARF the integrator: linking NF-kappaB, p53 and checkpoint kinases. Cell Cycle 2005;4:756-9. (Pubitemid 41353824)
50. Stark LA, Dunlop MG. Nucleolar sequestration of RelA (p65) regulates NF-kappaB-driven transcription and apoptosis. Mol Cell Biol 2005;25:5985-6004. (Pubitemid 40946553)