Nuclear factor kappa B subunit p50 promotes melanoma angiogenesis by upregulating interleukin-6 expression

International Journal of Cancer

Volumn 124, Issue 2, 2009, Pages 494-501

  Karst, Alison M ^a   Gao, Kai ^a   Nelson, Colleen C ^a   Li, Gang ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b JACK BELL RESEARCH CENTRE   (Canada)

Author keywords

Angiogenesis; ATF3; IL 6; Melanoma; NF B p50

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; COMPLEMENTARY DNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MATRIGEL; NUCLEAR FACTOR KAPPA B SUBUNIT P50; UNCLASSIFIED DRUG; ATF3 PROTEIN, HUMAN; COLLAGEN; LAMININ; PROTEOGLYCAN;

ARTICLE; CANCER GROWTH; CONTROLLED STUDY; DNA MICROARRAY; ENDOTHELIUM CELL; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MELANOMA CELL; MOLECULAR CLONING; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA TRANSLATION; SKIN CARCINOGENESIS; UPREGULATION; ANIMAL; BIOSYNTHESIS; CANCER TRANSPLANTATION; CELL PROLIFERATION; CHEMISTRY; DRUG COMBINATION; GENE EXPRESSION REGULATION; MALE; METABOLISM; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NUDE MOUSE; PHYSIOLOGY; TUMOR CELL LINE;

ACTIVATING TRANSCRIPTION FACTOR 3; ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; COLLAGEN; DRUG COMBINATIONS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTERLEUKIN-6; LAMININ; MALE; MICE; MICE, NUDE; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; NF-KAPPA B P50 SUBUNIT; PROTEOGLYCANS; UP-REGULATION;

EID: 58249089041     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.23973     Document Type: Article

References (51)

1. Kumar A, Takada Y, Boriek AM, Aggarwal BB. Nuclear factor-κB: its role in health and disease. J Mol Med 2004;82:434-48.
2. Yamamoto Y, Gaynor RB. Role of the NF-κB pathway in the pathogenesis of human disease states. Curr Mol Med 2001;1:287-96.
3. Gilmore TD. NF-κB, κBF1, dorsal, and related matters. Cell 1990;62:841-3.
4. Ghosh S, Karin M. Missing pieces in the NF-κB puzzle. Cell 2002;109(Suppl):S81-S96.
5. Gilmore TD. Introduction to NF-κB: players, pathways, perspectives. Oncogene 2006;25:6680-4.
6. Scheidereit C. IκB kinase complexes: gateways to NF-κB activation and transcription. Oncogene 2006;25:6685-705.
7. Sovak MA, Bellas RE, Kim DW, Zanieski GJ, Rogers AE, Traish AM, Sonenshein GE. Aberrant nuclear factor-κB/Rel expression and the pathogenesis of breast cancer. J Clin Invest 1997;100:2952-60.
8. Sweeney C, Li L, Shanmugam R, Bhat-Nakshatri P, Jayaprakasan V, Baldridge LA, Gardner T, Smith M, Nakshatri H, Cheng L. Nuclear factor-κB is constitutively activated in prostate cancer in vitro and is overexpressed in prostatic intraepithelial neoplasia and adenocarcinoma of the prostate. Clin Cancer Res 2004;10:5501-7.
9. Kojima M, Morisaki T, Sasaki N, Nakano K, Mibu R, Tanaka M, Katano M. Increased nuclear factor-κB activation in human colorectal carcinoma and its correlation with tumor progression. Anticancer Res 2004;24:675-81.
10. Wang W, Abbruzzese JL, Evans DB, Larry L, Cleary KR, Chiao PJ. The nuclear factor-κB RelA transcription factor is constitutively activated in human pancreatic adenocarcinoma cells. Clin Cancer Res 1999;5:119-27.
11. Huang S, Robinson JB, Deguzman A, Bucana CD, Fidler IJ. Blockade of nuclear factor-κB 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.
12. McNulty SE, del Rosario R, Cen D, Meyskens FL Jr, Yang S. Comparative expression of NFκB proteins in melanocytes of normal skin vs. benign intradermal naevus and human metastatic melanoma biopsies. Pigment Cell Res 2004;17:173-80.
13. McNulty SE, Tohidian NB, Meyskens FL Jr. RelA, p50 and inhibitor of κB & alpha; are elevated in human metastatic melanoma cells and respond aberrantly to ultraviolet light B. Pigment Cell Res 2001;14:456-65.
14. Yang J, Richmond A. Constitutive IκB kinase activity correlates with nuclear factor-κB activation in human melanoma cells. Cancer Res 2001;61:4901-9.
15. Shattuck-Brandt RL, Richmond A. Enhanced degradation of I-κB a contributes to endogenous activation of NF-κB in Hs294T melanoma cells. Cancer Res 1997;57:3032-9.
16. Dhawan P, Richmond A. A novel NF-κB-inducing kinase-MAPK signaling pathway up-regulates NF-κB activity in melanoma cells. J Biol Chem 2002;277:7920-8.
17. Huang S, DeGuzman A, Bucana CD, Fidler IJ. Nuclear factor-κB activity correlates with growth, angiogenesis, and metastasis of human melanoma cells in nude mice. Clin Cancer Res 2000;6: 2573-81.
18. Huang S, DeGuzman A, Bucana CD, Fidler IJ. Level of interleukin-8 expression by metastatic human melanoma cells directly correlates with constitutive NF-κB activity. Cytokines Cell Mol Ther 2000;69-17 .
19. Prusty BK, Husain SA, Das BC. Constitutive activation of nuclear factor-κB: preferential homodimerization of p50 subunits in cervical carcinoma. Front Biosci 2005;10:1510-1 9.
20. Mishra A, Bharti AC, Varghese P, Saluja D, Das BC. Differential expression and activation of NF-κB family proteins during oral carcinogenesis: role of high risk human papillomavirus infection. Int J Cancer 2006;119:2840-50.
21. Budunova IV, Perez P, Vaden VR, Spiegelman VS, Slaga TJ, Jorcano JL. Increased expression of p50-NF-κB and constitutive activation of NF-κB transcription factors during mouse skin carcinogenesis. Oncogene 1999;9:7423-31.
22. Thornburg NJ, Pathmanathan R, Raab-Traub N. Activation of nuclear factor-κB p50 homodimer/Bcl-3 complexes in nasopharyngeal carcinoma. Cancer Res 2003;63:8293-301.
23. Mukhopadhyay T, Roth JA, Maxwell SA. Altered expression of the p50 subunit of the NF-κB transcription factor complex in non-small cell lung carcinoma. Oncogene 1995;11:999-1003.
24. Kurland JF, Kodym R, Story MD, Spurgers κB, McDonnell TJ, Meyn RE. NF-κB1 (p50) homodimers contribute to transcription of the bcl-2 oncogene. J Biol Chem 2001;276:45380-6.
25. Mathas S, Jöhrens K, Joos S, Lietz A, Hummel F, Janz M, Jundt F, Anagnostopoulos I, Bommert K, Lichter P, Stein H, Scheidereit C, et al. Elevated NF-κB p50 complex formation and Bcl-3 expression in classical Hodgkin, anaplastic large-cell, and other peripheral T-cell lymphomas. Blood 2005;106:4287-93.
26. Gao K, Dai DL, Martinka M, Li G. Prognostic significance of nuclear factor-κB p105/p50 in human melanoma and its role in cell migration. Cancer Res 2006;66:8382-8.
27. Sehgal PB, Wang L, Rayanade R, Pan H, Margulies L. Interleukin-6-type cytokines. Ann N Y Acad Sci 1995;762:1-14.
28. Komyod W, Böhm M, Metze D, Heinrich PC, Behrmann I. Constitutive suppressor of cytokine signaling 3 expression confers a growth advantage to a human melanoma cell line. Mol Cancer Res 2007;5: 271-81.
29. Lu C, Kerbel RS. Interleukin-6 undergoes transition from paracrine growth inhibitor to autocrine stimulator during human melanoma progression. J Cell Biol 1993;120:1281-8.
30. Sun WH, Kreisle RA, Phillips AW, Ershler WB. In vivo and in vitro characteristics of interleukin 6-transfected B16 melanoma cells. Cancer Res 1992;52:5412-15.
31. Wang Y, Li G. ING3 promotes UV-induced apoptosis via Fas/cas-pase-8 pathway in melanoma cells. J Biol Chem 2006;281:11887-93.
32. Gilchrist M, Thorsson V, Li B, Rust AG, Korb M, Kennedy K, Hai T, Bolouri H, Aderem A. Systems biology approaches identify ATF3 as a negative regulator of Toll-like receptor 4. Nature 2006;441:173-8.
33. Cohen T, Nahari D, Cerem LW, Neufeld G, Levi BZ. Interleukin 6 induces the expression of vascular endothelial growth factor. J Biol Chem 1996;271:736-41.
34. Molnár EL, Hegyesi H, Tóth S, Darvas Z, László V, Szalai C, Falus A. Biosynthesis of interleukin-6, an autocrine growth factor for melanoma, is regulated by melanoma-derived histamine. Semin Cancer Biol 2000;10:25-8.
35. Mouawad R, Benhammouda A, Rixe O, Antoine EC, Borel C, Weil M, Khayat D, Soubrane C. Endogenous interleukin 6 levels in patients with metastatic malignant melanoma: correlation with tumour burden. Clin Cancer Res 1996;2:1405-9.
36. Soubrane C, Rixe O, Meric JB, Khayat D, Mouawad R. Pretreatment serum interleukin-6 concentration as a prognostic factor of overall survival in metastatic malignant melanoma patients treated with bio-chemotherapy: a retrospective study. Melanoma Res 2005;15:199-204.
37. Mouawad R, Rixe O, Meric JB, Khayat D, Soubrane C. Serum inter-leukin-6 concentrations as predictive factor of time to progression in metastatic malignant melanoma patients treated by biochemotherapy: a retrospective study. Cytokines Cell Mol Ther 2002;7:151-6.
38. Tas F, Oguz H, Argon A, Duranyildiz D, Camlica H, Yasasever V, Topuz E. The value of serum levels of IL-6. TNF-α, and erythropoie-tin in metastatic malignant melanoma: serum. IL-6 level is a valuable prognostic factor at least as serum. LDH in advanced melanoma. Med Oncol 2005;22:241-6.
39. Fujita T, Nolan GP, Liou HC, Scott ML, Baltimore D. The candidate proto-oncogene bcl-3 encodes a transcriptional coactivator that activates through NF-κB p50 homodimers. Genes Dev 1993;7:1354-63.
40. Bours V, Franzoso G, Azarenko V, Park S, Kanno T, Brown K, Sie-benlist U. The oncoprotein Bcl-3 directly transactivates through κB motifs via association with DNA-binding p50B homodimers. Cell 1993;72:729-39.
41. Watanabe N, Iwamura T, Shinoda T, Fujita T. Regulation of NFκB1 proteins by the candidate oncoprotein BCL-3: generation of NF-κB homodimers from the cytoplasmic pool of p50-p105 and nuclear translocation. EMBO J 1997;16:3609-20.
42. Cogswell PC, Guttridge DC, Funkhouser WK, Baldwin AS Jr. Selective activation of NF-κB subunits in human breast cancer: potential roles for NF-κB2/p52 and for Bcl-3. Oncogene 2000;19:1123-31.
43. Deng WG, Wu WK. Regulation of inducible nitric oxide synthase expression by p300 and p50 acetylation. J Immunol 2003;171: 6581-8.
44. Cao S, Zhang X, Edwards JP, Mosser DM. NF-κB1 (p50) homo-dimers differentially regulate pro- and anti-inflammatory cytokines in macrophages. J Biol Chem 2006;281:26041-50.
45. Hai T, Wolfgang CD, Marsee DK, Allen AE, Sivaprasad U. ATF3 and stress responses. Gene Expr 1999;7:321-35.
46. Kishimoto T, Akira S, Narazaki M, Taga T. Interleukin-6 family of cytokines and gp130. Blood 1995;86:1243-54.
47. Nilsson MB, Langley RR, Fidler IJ. Interleukin-6, secreted by human ovarian carcinoma cells, is a potent proangiogenic cytokine. Cancer Res 2005;65:10794-800.
48. Huang SP, Wu MS, Shun CT, Wang HP, Lin MT, Kuo ML, Lin JT. Interleukin-6 increases vascular endothelial growth factor and angio-genesis in gastric carcinoma. J Biomed Sci 2004;11:517-27.
49. Koong AC, Chen EY, Giaccia AJ. Hypoxia causes the activation of nuclear factor κB through the phosphorylation of I κB α on tyrosine residues. Cancer Res 1994;54:1425-30.
50. Huang S, DeGuzman A, Bucana CD, Fidler IJ. Nuclear factor-κB activity correlates with growth, angiogenesis, and metastasis of human melanoma cells in nude mice. Clin Cancer Res 2000;6:2573-81.
51. Lázár-Molnár E, Hegyesi H, Tóth S, Falus A. Autocrine and paracrine regulation by cytokines and growth factors in melanoma. Cytokine 2000;12:547-54.