The activated NF-κB-snail-RKIP circuitry in cancer regulates both the metastatic cascade and resistance to apoptosis by cytotoxic drugs

Critical Reviews in Immunology

Volumn 29, Issue 3, 2009, Pages 241-254

  Wu, Katherine ^a   Bonavida, Benjamin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Immunotherapy; Raf 1 MEK ERK1 2; Sensitization; Synergy; Therapy

Indexed keywords

1 [2 (2 AMINOETHYL) N (2 AMMONIOETHYL)AMINODIAZEN 1 IUM 1, 2 DIOLATE; ANTINEOPLASTIC AGENT; BORTEZOMIB; CETUXIMAB; CISPLATIN; CYTOTOXIC AGENT; DEHYDROXYMETHYL EPOXYQUINOMICIN; DOCETAXEL; DOXORUBICIN; ETOPOSIDE; FLUOROURACIL; GENE PRODUCT; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IRINOTECAN; MELPHALAN; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; RITUXIMAB; RUBITECAN; SALINOSPORAMIDE A; TRANSCRIPTION FACTOR SNAIL; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; PEBP1 PROTEIN, HUMAN; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

APOPTOSIS; BREAST CANCER; CANCER CELL; CANCER INHIBITION; CANCER RELAPSE; CANCER RESISTANCE; CANCER SURVIVAL; CARCINOMA; CELL SURVIVAL; CYTOTOXICITY; DISEASE COURSE; DISTANT METASTASIS; DOWN REGULATION; DRUG EFFICACY; DRUG SENSITIVITY; ENZYME ACTIVATION; ENZYME REGULATION; FIBROBLAST; HUMAN; IMMUNOTHERAPY; LIVER CELL CARCINOMA; LUNG CANCER; LYMPHOMA; MACROPHAGE; METASTASIS; MULTIPLE MYELOMA; NECK CANCER; NEOPLASM; NONHODGKIN LYMPHOMA; NONHUMAN; OVARY CANCER; OVERALL SURVIVAL; PANCREAS CANCER; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REVIEW; SURVIVAL RATE; TREATMENT RESPONSE; ANIMAL; CANCER INVASION; CELL DIFFERENTIATION; DRUG EFFECT; DRUG RESISTANCE; EPITHELIUM CELL; GENE EXPRESSION REGULATION; MESODERM; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL DIFFERENTIATION; DRUG RESISTANCE, NEOPLASM; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MESODERM; NEOPLASM INVASIVENESS; NEOPLASMS; NF-KAPPA B; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 67650305927     PISSN: 10408401     EISSN: None     Source Type: Journal    
DOI: 10.1615/critrevimmunol.v29.i3.40     Document Type: Review

References (99)

1. Yokota J. Tumor progression and metastasis. Carcinogenesis. 2000 Mar; 21(3):497-503.
2. Welch DR, Rinker-Schaeffer CW. What defines a useful marker of metastasis in human cancer? J Natl Cancer Inst. 1999 Aug 18;91(16):1351-3.
3. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ. Cancer statistics, 2008. CA Cancer J Clin. 2008 Mar-Apr;58(2):71-96.
4. Sabbah M, Emami S, Redeuilh G, Julien S, Prevost G, Zimber A, Ouelaa R, Bracke M, De Wever O, Gespach C. Molecular signature and therapeutic perspective of the epithelial-to-mesenchymal transitions in epithelial cancers. Drug Resist Updat. 2008 Aug-Oct;11(4-5):123-51.
5. Th iery JP. Epithelial-mesenchymal transitions in development and pathologies. Curr Opin Cell Biol. 2003 Dec; 15(6):740-6.
6. McCubrey JA, Steelman LS, Abrams SL, Lee JT, Chang F, Bertrand FE, Navolanic PM, Terrian DM, Franklin RA, D'Assoro AB, Salisbury JL, Mazzarino MC, Stivala F, Libra M. Roles of the RAF/MEK/ERK and PI3K/PTEN/AKT pathways in malignant transformation and drug resistance. Adv Enzyme Regul. 2006;46:249-79.
7. Inoue J, Gohda J, Akiyama T, Semba K. NF-kappaB activation in development and progression of cancer. Cancer Sci. 2007 Mar; 98(3):268-74.
8. McCubrey JA, Steelman LS, Chappell WH, Abrams SL, Wong EW, Chang F, Lehmann B, Terrian DM, Milella M, Tafuri A, Stivala F, Libra M, Basecke J, Evangelisti C, Martelli AM, Franklin RA. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta. 2007 Aug; 1773(8):1263-84.
9. Bonavida B, Baritaki S, Huerta-Yepez S, Vega MI, Chatterjee D, Yeung K. Novel therapeutic applications of nitric oxide donors in cancer: roles in chemo- and immunosensitization to apoptosis and inhibition of metastases. Nitric Oxide. 2008 Sep; 19(2):152-7.
10. May MJ, Ghosh S. Rel/NF-kappa B and I kappa B proteins: an overview. Semin Cancer Biol. 1997 Apr; 8(2):63-73.
11. Lenardo MJ, Baltimore D. NF-kappa B: a pleiotropic mediator of inducible and tissue-specific gene control. Cell. 1989 Jul 28;58(2):227-9.
12. Bonizzi G, Bebien M, Otero DC, Johnson-Vroom KE, Cao Y, Vu D, Jegga AG, Aronow BJ, Ghosh G, Rickert RC, Karin M. Activation of IKKalpha target genes depends on recognition of specific kappaB binding sites by RelB:p52 dimers. EMBO J. 2004 Oct 27;23(21):4202-10.
13. Beg AA, Baltimore D. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science. 1996 Nov 1;274 (5288):782-4.
14. Grilli M, Pizzi M, Memo M, Spano P. Neuroprotection by aspirin and sodium salicylate through blockade of NF-kappaB activation. Science. 1996 Nov 22; 274 (5291):1383-5.
15. Lin KI, Lee SH, Narayanan R, Baraban JM, Hardwick JM, Ratan RR. Th iol agents and Bcl-2 identify an alphavirus-induced apoptotic pathway that requires activation of the transcription factor NF-kappa B. J Cell Biol. 1995 Dec; 131(5):1149-61.
16. Katsman A, Umezawa K, Bonavida B. Reversal of resistance to cytotoxic cancer therapies: DHMEQ as a chemo-sensitizing and immuno-sensitizing agent. Drug Resist Updat. 2007 Feb-Apr;10(1-2):1-12.
17. Li Y, Ahmed F, Ali S, Philip PA, Kucuk O, Sarkar FH. Inactivation of nuclear factor kappaB by soy isoflavone genistein contributes to increased apoptosis induced by chemotherapeutic agents in human cancer cells. Cancer Res. 2005 Aug 1;65(15):6934-42.
18. Li Y, Sarkar FH. Inhibition of nuclear factor kappaB activation in PC3 cells by genistein is mediated via Akt signaling pathway. Clin Cancer Res. 2002 Jul; 8(7):2369-77.
19. Lin ZP, Boller YC, Amer SM, Russell RL, Pacelli KA, Patierno SR, Kennedy KA. Prevention of brefeldin A-induced resistance to teniposide by the proteasome inhibitor MG-132: involvement of NF-kappaB activation in drug resistance. Cancer Res. 1998 Jul 15;58(14):3059-65.
20. Shah SA, Potter MW, McDade TP, Ricciardi R, Perugini RA, Elliott PJ, Adams J, Callery MP. 26S proteasome inhibition induces apoptosis and limits growth of human pancreatic cancer. J Cell Biochem. 2001 Apr 2-27;82(1):110-22.
21. Mitsiades N, Mitsiades CS, Richardson PG, Poulaki V, Tai YT, Chauhan D, Fanourakis G, Gu X, Bailey C, Joseph M, Libermann TA, Schlossman R, Munshi NC, Hideshima T, Anderson KC. Th e proteasome inhibitor PS-341 potentiates sensitivity of multiple myeloma cells to conventional chemotherapeutic agents: therapeutic applications. Blood. 2003 Mar 15;101(6):2377-80.
22. Camp ER, Li J, Minnich DJ, Brank A, Moldawer LL, MacKay SL, Hochwald SN. Inducible nuclear factor-kappaB activation contributes to chemotherapy resistance in gastric cancer. J Am Coll Surg. 2004 Aug; 199(2):249-58.
23. Mitsiades CS, Mitsiades N, Poulaki V, Schlossman R, Akiyama M, Chauhan D, Hideshima T, Treon SP, Munshi NC, Richardson PG, Anderson KC. Activation of NF-kappaB and upregulation of intra cellular antiapoptotic proteins via the IGF-1/Akt signaling in human multiple myeloma cells: therapeutic implications. Oncogene. 2002 Aug 22;21(37):5673-83.
24. Jazirehi AR, Vega MI, Bonavida B. Development of rituximab-resistant lymphoma clones with altered cell signaling and cross-resistance to chemotherapy. Cancer Res. 2007 Feb 1;67(3):1270-81.
25. Scartozzi M, Bearzi I, Pierantoni C, Mandolesi A, Loupakis F, Zaniboni A, Catalano V, Quadri A, Zorzi F, Berardi R, Biscotti T, Labianca R, Falcone A, Cascinu S. Nuclear factor-kB tumor expression predicts response and survival in irinotecan-refractory metastatic colorectal cancer treated with cetuximab-irinotecan therapy. J Clin Oncol. 2007 Sep 1;25(25):3930-5.
26. Shao R, Karunagaran D, Zhou BP, Li K, Lo SS, Deng J, Chiao P, Hung MC. Inhibition of nuclear factor-kappaB activity is involved in E1A-mediated sensitization of radiation-induced apoptosis. J Biol Chem. 1997 Dec 26;272(52):32739-42.
27. Russo SM, Tepper JE, Baldwin AS Jr, Liu R, Adams J, Elliott P, Cusack JC. Enhancement of radiosensitivity by proteasome inhibition: implications for a role of NF-kappaB. Int J Radiat Oncol Biol Phys. 2001 May 1;50(1):183-93.
28. Xu Y, Fang F, St Clair DK, Sompol P, Josson S, St Clair WH. SN52, a novel nuclear factor-kappaB inhibitor, blocks nuclear import of RelB:p52 dimer and sensitizes prostate cancer cells to ionizing radiation. Mol Cancer Ther. 2008 Aug; 7(8):2367-76.
29. Gasparian AV, Yao YJ, Kowalczyk D, Lyakh LA, Karseladze A, Slaga TJ, Budunova IV. The role of IKK in constitutive activation of NF-kappaB transcription factor in prostate carcinoma cells. J Cell Sci. 2002 Jan 1;115(Pt 1):141-51.
30. Zhang L, Chen W, Li X. A novel anticancer effect of butein: inhibition of invasion through the ERK1/2 and NF-kappa B signaling pathways in bladder cancer cells. FEBS Lett. 2008 Jun 11;582(13):1821-8.
31. Huber MA, Azoitei N, Baumann B, Grunert S, Sommer A, Pehamberger H, Kraut N, Beug H, Wirth T. NF-kappaB is essential for epithelial-mesenchymal transition and metastasis in a model of breast cancer progression. J Clin Invest. 2004 Aug; 114(4):569-81.
32. Shin SR, Sanchez-Velar N, Sherr DH, Sonenshein GE. 7, 12-dimethylbenz(a)anthracene treatment of a c-rel mouse mammary tumor cell line induces epithelial to mesenchymal transition via activation of nuclear factor-kappa B. Cancer Res. 2006 Mar 1;66(5):2570-5.
33. Cox G, O'Byrne KJ. Matrix metalloproteinases and cancer. Anticancer Res. 2001 Nov-Dec;21(6B): 4207-19.
34. Liu J, Zhan M, Hannay JA, Das P, Bolshakov SV, Kotilingam D, Yu D, Lazar AF, Pollock RE, Lev D. Wild-type p53 inhibits nuclear factor-kappaB-induced matrix metalloproteinase-9 promoter activation: implications for soft tissue sarcoma growth and metastasis. Mol Cancer Res. 2006 Nov; 4(11):803-10.
35. Kim JH, Choi C, Benveniste EN, Kwon D. TRAIL induces MMP-9 expression via ERK activation in human astrocytoma cells. Biochem Biophys Res Commun. 2008 Dec 5;377(1):195-9.
36. Lilienbaum A, Paulin D. Activation of the human vimentin gene by the Tax human T-cell leukemia virus. I. Mechanisms of regulation by the NF-kappa B transcription factor. J Biol Chem. 1993 Jan 25;268(3): 2180-8.
37. Wang X, Belguise K, Kersual N, Kirsch KH, Mineva ND, Galtier F, Chalbos D, Sonenshein GE. Oestrogen signalling inhibits invasive phenotype by repressing RelB and its target BCL2. Nat Cell Biol. 2007 Apr; 9(4):470-8.
38. Barbera MJ, Puig I, Dominguez D, Julien-Grille S, Guaita-Esteruelas S, Peiro S, Baulida J, Franci C, Dedhar S, Larue L, Garcia de Herreros A. Regulation of Snail transcription during epithelial to mesenchymal transition of tumor cells. Oncogene. 2004 Sep 23;23(44):7345-54.
39. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J, Garcia De Herreros A. Th e transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol. 2000 Feb; 2(2):84-9.
40. Kim HJ, Litzenburger BC, Cui X, Delgado DA, Grabiner BC, Lin X, Lewis MT, Gottardis MM, Wong TW, Attar RM, Carboni JM, Lee AV. Constitutively active type I insulin-like growth factor receptor causes transformation and xenograft growth of immortalized mammary epithelial cells and is accompanied by an epithelial-to-mesenchymal transition mediated by NF-kappaB and snail. Mol Cell Biol. 2007 Apr; 27(9):31365-75.
41. Simpson P. Maternal-zygotic gene interactions during formation of the dorsoventral pattern in Drosophila embryos. Genetics. 1983 Nov; 105(3):615-32.
42. Nieto MA. The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol. 2002 Mar; 3(3):155-66.
43. Ko H, Kim HS, Kim NH, Lee SH, Kim KH, Hong SH, Yook JI. Nuclear localization signals of the E-cadherin transcriptional repressor Snail. Cells Tissues Organs. 2007;185(1-3):66-72.
44. Peiró S, Escriva M, Puig I, Barbera MJ, Dave N, Herranz N, Larriba MJ, Takkunen M, Franci C, Munoz A, Virtanen I, Baulida J, Garcia de Herreros A. Snail1 transcriptional repressor binds to its own promoter and controls its expression. Nucleic Acids Res. 2006;34(7):2077-84.
45. Yook JI, Li XY, Ota I, Fearon ER, Weiss SJ. Wnt-dependent regulation of the E-cadherin repressor snail. J Biol Chem. 2005 Mar 25;280(12):11740-8.
46. Miyoshi A, Kitajima Y, Kido S, Shimonishi T, Matsuyama S, Kitahara K, Miyazaki K. Snail accelerates cancer invasion by upregulating MMP expression and is associated with poor prognosis of hepatocellular carcinoma. Br J Cancer. 2005 Jan 31;92(2):252-8.
47. Toyama T, Zhang Z, Iwase H, Yamashita H, Ando Y, Hamaguchi M, Mizutani M, Kondo N, Fujita T, Fujii Y, Iwata H. Low expression of the snail gene is a good prognostic factor in node-negative invasive ductal carcinomas. Jpn J Clin Oncol. 2006 Jun; 36(6):357-63.
48. Yang MH, Chang SY, Chiou SH, Liu CJ, Chi CW, Chen PM, Teng SC, Wu KJ. Overexpression of NBS1 induces epithelial-mesenchymal transition and co-expression of NBS1 and Snail predicts metastasis of head and neck cancer. Oncogene. 2007 Mar 1;26(10):1459-67.
49. Blechschmidt K, Sassen S, Schmalfeldt B, Schuster T, Hofler H, Becker KF. The E-cadherin repressor Snail is associated with lower overall survival of ovarian cancer patients. Br J Cancer. 2008 Jan 29;98(2):489-95.
50. Burdsal CA, Damsky CH, Pedersen RA. The role of E-cadherin and integrins in mesoderm differentiation and migration at the mammalian primitive streak. Development. 1993 Jul; 118(3):829-44.
51. Howard EW, Camm KD, Wong YC, Wang XH. E-cadherin upregulation as a therapeutic goal in cancer treatment. Mini Rev Med Chem. 2008 May; 8(5):496-518.
52. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA. Th e transcription factor snail controls epithelialmesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol. 2000 Feb; 2(2):76-83.
53. Olmeda D, Jorda M, Peinado H, Fabra A, Cano A. Snail silencing effectively suppresses tumour growth and invasiveness. Oncogene. 2007 Mar 22;26(13): 1862-74.
54. Zha YH, He JF, Mei YW, Yin T, Mao L. Zinc-finger transcription factor snail accelerates survival, migration and expression of matrix metalloproteinase-2 in human bone mesenchymal stem cells. Cell Biol Int. 2007 Oct; 31(10):1089-96.
55. Ohkubo T, Ozawa M. The transcription factor Snail downregulates the tight junction components independently of E-cadherin downregulation. J Cell Sci. 2004 Apr 1;117(Pt 9):1675-85.
56. Ikenouchi J, Matsuda M, Furuse M, Tsukita S. Regulation of tight junctions during the epitheliummesenchyme transition: direct repression of the gene expression of claudins/occludin by Snail. J Cell Sci. 2003 May 15;116(Pt 10):1959-67.
57. Yokoyama K, Kamata N, Fujimoto R, Tsutsumi S, Tomonari M, Taki M, Hosokawa H, Nagayama M. Increased invasion and matrix metalloproteinase-2 expression by Snail-induced mesenchymal transition in squamous cell carcinomas. Int J Oncol. 2003 Apr; 22(4):891-8.
58. Miyoshi A, Kitajima Y, Sumi K, Sato K, Hagiwara A, Koga Y, Miyazaki K. Snail and SIP1 increase cancer invasion by upregulating MMP family in hepatocellular carcinoma cells. Br J Cancer. 2004 Mar 22;90(6):1265-73.
59. Maatta M, Soini Y, Liakka A, Autio-Harmainen H. Differential expression of matrix metalloproteinase (MMP)-2, MMP-9, and membrane type 1-MMP in hepatocellular and pancreatic adenocarcinoma: implications for tumor progression and clinical prognosis. Clin Cancer Res. 2000 Jul; 6(7):2726-34.
60. Li Y, Ma J, Guo Q, Duan F, Tang F, Zheng P, Zhao Z, Lu G. Overexpression of MMP-2 and MMP-9 in esophageal squamous cell carcinoma. Dis Esophagus. 2009 Jan 23. [Epub ahead of print]
61. Sen T, Moulik S, Dutta A, Choudhury PR, Banerji A, Das S, Roy M, Chatterjee A. Multifunctional effect of epigallocatechin-3-gallate (EGCG) in downregulation of gelatinase-A (MMP-2) in human breast cancer cell line MCF-7. Life Sci. 2009 Feb 13;84(7-8):194-204.
62. Liu M, Sun YN, Jiao H, Tian LL, Guo YL. [Role of siRNA mediated matrix metalloproteinase-2 gene silencing in the inhibition of invasion and growth of laryngeal cancer cells]. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi. 2008 Aug; 43(8):612-6.
63. Haraguchi M, Okubo T, Miyashita Y, Miyamoto Y, Hayashi M, Crotti TN, McHugh KP, Ozawa M. Snail regulates cell-matrix adhesion by regulation of the expression of integrins and basement membrane proteins. J Biol Chem. 2008 Aug 29;283(35):23514-23.
64. Vega S, Morales AV, Ocana OH, Valdes F, Fabregat I, Nieto MA. Snail blocks the cell cycle and confers resistance to cell death. Genes Dev. 2004 May 15;18(10):1131-43.
65. Kajita M, McClinic KN, Wade PA. Aberrant expression of the transcription factors snail and slug alters the response to genotoxic stress. Mol Cell Biol. 2004 Sep; 24(17):7559-66.
66. Zhuo W, Wang Y, Zhuo X, Zhang Y, Ao X, Chen Z. Knockdown of Snail, a novel zinc finger transcription factor, via RNA interference increases A549 cell sensitivity to cisplatin via JNK/mitochondrial pathway. Lung Cancer. 2008 Oct; 62(1):8-14.
67. Escriva M, Peiro S, Herranz N, Villagrasa P, Dave N, Montserrat-Sentis B, Murray SA, Franci C, Gridley T, Virtanen I, Garcia de Herreros A. Repression of PTEN phosphatase by Snail1 transcriptional factor during gamma radiation-induced apoptosis. Mol Cell Biol. 2008 Mar; 28(5):1528-40.
68. Beach S, Tang H, Park S, Dhillon AS, Keller ET, Kolch W, Yeung KC. Snail is a repressor of RKIP transcription in metastatic prostate cancer cells. Oncogene. 2008 Apr 3;27(15):2243-8.
69. Baritaki S, Chapman A, Yeung K, Spandidos D, Palladino M, Bonavida B. Inhibition of epithelial to mesenchymal transition (EMT) in metastatic prostate cancer cells by the novel proteasome inhibitor, NPI-0052: Pivotal roles of Snail repression and RKIP induction. Oncogene. In press 2009.
70. Yeung K, Seitz T, Li S, Janosch P, McFerran B, Kaiser C, Fee F, Katsanakis KD, Rose DW, Mischak H, Sedivy JM, Kolch W. Suppression of Raf-1 kinase activity and MAP kinase signalling by RKIP. Nature. 1999 Sep 9;401 (6749):173-7.
71. Fu Z, Kitagawa Y, Shen R, Shah R, Mehra R, Rhodes D, Keller PJ, Mizokami A, Dunn R, Chinnaiyan AM, Yao Z, Keller ET. Metastasis suppressor gene Raf kinase inhibitor protein (RKIP) is a novel prognostic marker in prostate cancer. Prostate. 2006 Feb 15;66(3):248-56.
72. Al-Mulla F, Hagan S, Behbehani AI, Bitar MS, George SS, Going JJ, Garcia JJ, Scott L, Fyfe N, Murray GI, Kolch W. Raf kinase inhibitor protein expression in a survival analysis of colorectal cancer patients. J Clin Oncol. 2006 Dec 20;24(36):5672-9.
73. Minoo P, Zlobec I, Baker K, Tornillo L, Terracciano L, Jass JR, Lugli A. Loss of raf-1 kinase inhibitor protein expression is associated with tumor progression and metastasis in colorectal cancer. Am J Clin Pathol. 2007 May; 127(5):820-7.
74. Hagan S, Al-Mulla F, Mallon E, Oien K, Ferrier R, Gusterson B, Garcia JJ, Kolch W. Reduction of Raf-1 kinase inhibitor protein expression correlates with breast cancer metastasis. Clin Cancer Res. 2005 Oct 15;11(20):7392-7.
75. Schuierer MM, Bataille F, Hagan S, Kolch W, Bosserhoff AK. Reduction in Raf kinase inhibitor protein expression is associated with increased Ras-extracellular signal-regulated kinase signaling in melanoma cell lines. Cancer Res. 2004 Aug 1; 64(15):5186-92.
76. Fu Z, Smith PC, Zhang L, Rubin MA, Dunn RL, Yao Z, Keller ET. Effects of raf kinase inhibitor protein expression on suppression of prostate cancer metastasis. J Natl Cancer Inst. 2003 Jun 18;95(12):878-89.
77. Li HZ, Wang Y, Gao Y, Shao J, Zhao XL, Deng WM, Liu YX, Yang J, Yao Z. Effects of raf kinase inhibitor protein expression on metastasis and progression of human epithelial ovarian cancer. Mol Cancer Res. 2008 Jun; 6(6):917-28.
78. Dangi-Garimella S, Yun J, Eves EM, Newman M, Erkeland SJ, Hammond SM, Minn AJ, Rosner MR. Raf kinase inhibitory protein suppresses a metastasis signalling cascade involving LIN28 and let-7. EMBO J. 2009 Feb 18;28(4):347-58.
79. Chatterjee D, Bai Y, Wang Z, Beach S, Mott S, Roy R, Braastad C, Sun Y, Mukhopadhyay A, Aggarwal BB, Darnowski J, Pantazis P, Wyche J, Fu Z, Kitagwa Y, Keller ET, Sedivy JM, Yeung KC. RKIP sensitizes prostate and breast cancer cells to drug-induced apoptosis. J Biol Chem. 2004 Apr 23;279(17):17515-23.
80. Jazirehi AR, Vega MI, Chatterjee D, Goodglick L, Bonavida B. Inhibition of the Raf-MEK1/2-ERK1/2 signaling pathway, Bcl-xL down-regulation, and chemosensitization of non-Hodgkin's lymphoma B cells by Rituximab. Cancer Res. 2004 Oct 1;64(19):7117-26.
81. Baritaki S, Katsman A, Chatterjee D, Yeung KC, Spandidos DA, Bonavida B. Regulation of tumor cell sensitivity to TRAIL-induced apoptosis by the metastatic suppressor Raf kinase inhibitor protein via Yin Yang 1 inhibition and death receptor 5 up-regulation. J Immunol. 2007 Oct 15;179(8):5441-53.
82. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, Garnett MJ, Bottomley W, Davis N, Dicks E, Ewing R, Floyd Y, Gray K, Hall S, Hawes R, Hughes J, Kosmidou V, Menzies A, Mould C, Parker A, Stevens C, Watt S, Hooper S, Wilson R, Jayatilake H, Gusterson BA, Cooper C, Shipley J, Hargrave D, Pritchard-Jones K, Maitland N, Chenevix-Trench G, Riggins GJ, Bigner DD, Palmieri G, Cossu A, Flanagan A, Nicholson A, Ho JW, Leung SY, Yuen ST, Weber BL, Seigler HF, Darrow TL, Paterson H, Marais R, Marshall CJ, Wooster R, Stratton MR, Futreal PA. Mutations of the BRAF gene in human cancer. Nature. 2002 Jun 27;417 (6892):949-54.
83. Webb CP, Van Aelst L, Wigler MH, Woude GF. Signaling pathways in Ras-mediated tumorigenicity and metastasis. Proc Natl Acad Sci U S A. 1998 Jul 21; 95(15):8773-8.
84. Treisman R. Regulation of transcription by MAP kinase cascades. Curr Opin Cell Biol. 1996 Apr; 8(2):205-15.
85. Yeung K, Janosch P, McFerran B, Rose DW, Mischak H, Sedivy JM, Kolch W. Mechanism of suppression of the Raf/MEK/extracellular signal-regulated kinase pathway by the raf kinase inhibitor protein. Mol Cell Biol. 2000 May; 20(9):3079-85.
86. Corbit KC, Trakul N, Eves EM, Diaz B, Marshall M, Rosner MR. Activation of Raf-1 signaling by protein kinase C through a mechanism involving Raf kinase inhibitory protein. J Biol Chem. 2003 Apr 11;278(15):13061-8.
87. Lorenz K, Lohse MJ, Quitterer U. Protein kinase C switches the Raf kinase inhibitor from Raf-1 to GRK-2. Nature. 2003 Dec 4;426 (6966):574-9.
88. Ribas C, Penela P, Murga C, Salcedo A, Garcia-Hoz C, Jurado-Pueyo M, Aymerich I, Mayor F. Th e G protein-coupled receptor kinase (GRK) interactome: role of GRKs in GPCR regulation and signaling. Biochim Biophys Acta. 2007 Apr; 1768(4):913-22.
89. Eves EM, Shapiro P, Naik K, Klein UR, Trakul N, Rosner MR. Raf kinase inhibitory protein regulates aurora B kinase and the spindle checkpoint. Mol Cell. 2006 Aug; 23(4):561-74.
90. Vagnarelli P, Earnshaw WC. Chromosomal passengers: the four-dimensional regulation of mitotic events. Chromosoma. 2004 Nov; 113(5):211-22.
91. Yeung KC, Rose DW, Dhillon AS, Yaros D, Gustafsson M, Chatterjee D, McFerran B, Wyche J, Kolch W, Sedivy JM. Raf kinase inhibitor protein interacts with NF-kappaB-inducing kinase and TAK1 and inhibits NF-kappaB activation. Mol Cell Biol. 2001 Nov; 21(21):7207-17.
92. Shukla S, MacLennan GT, Fu P, Patel J, Marengo SR, Resnick MI, Gupta S. Nuclear factor-kappaB/p65 (Rel A) is constitutively activated in human prostate adenocarcinoma and correlates with disease progression. Neoplasia. 2004 Jul-Aug;6(4):390-400.
93. Baritaki S, Suzuki E, Umezawa K, Spandidos DA, Berenson J, Daniels TR, Penichet ML, Jazirehi AR, Palladino M, Bonavida B. Inhibition of Yin Yang 1-dependent repressor activity of DR5 transcription and expression by the novel proteasome inhibitor NPI-0052 contributes to its TRAIL-enhanced apoptosis in cancer cells. J Immunol. 2008 May 1;180(9):6199-210.
94. Huerta-Yepez S, Vega M, Jazirehi A, Garban H, Hongo F, Cheng G, Bonavida B. Nitric oxide sensitizes prostate carcinoma cell lines to TRAIL-mediated apoptosis via inactivation of NF-kappa B and inhibition of Bcl-xl expression. Oncogene. 2004 Jun 24;23(29):4993-5003.
95. Vega MI, Martinez-Paniagua M, Jazirehi AR, Huerta-Yepez S, Umezawa K, Martinez-Maza O, Bonavida B. The NF-kappaB inhibitors (bortezomib and DHMEQ) sensitise rituximab-resistant AIDS- B-non-Hodgkin lymphoma to apoptosis by various chemotherapeutic drugs. Leuk Lymphoma. 2008 Oct; 49(10):1982-94.
96. Horiuchi K, Morioka H, Nishimoto K, Suzuki Y, Susa M, Nakayama R, Kawai A, Sonobe H, Takaishi H, Ozaki T, Yabe H, Umezawa K, Toyama Y. Growth suppression and apoptosis induction in synovial sarcoma cell lines by a novel NF-kappaB inhibitor, dehydroxymethylepoxyquinomicin (DHMEQ). Cancer Lett. 2008 Dec 18;272(2):336-44.
97. Chauhan D, Hideshima T, Anderson KC. A novel proteasome inhibitor NPI-0052 as an anticancer therapy. Br J Cancer. 2006 Oct 23;95(8):961-5.
98. Huerta S, Baay-Guzman G, Gonzalez-Bonilla CR, Livingston EH, Huerta-Yepez S, Bonavida B. In vitro and in vivo sensitization of SW620 metastatic colon cancer cells to CDDP-induced apoptosis by the nitric oxide donor DETANONOate: involvement of AIF. 2009 May; 20(3):182-94.
99. Ohno O, Shima Y, Ikeda Y, Sakurai K, Watanabe K, Kawai Y, Umezawa K. Inhibition of cellular adhesion in human umbilical vein endothelial cells by NF-kappaB inhibitor DHMEQ under flow. Oncol Res. 2005;15(4):189-97.