Aberrant nuclear factor-κb/Rel expression and the pathogenesis of breast cancer

Journal of Clinical Investigation

Volumn 100, Issue 12, 1997, Pages 2952-2960

  Sovak, Mika A ^a   Bellas, Robert E ^a   Kim, Dong W ^a   Zanieski, Gregory J ^a   Rogers, Adrianne E ^a   Traish, Abdulmaged M ^a   Sonenshein, Gail E ^a,b  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON UNIVERSITY   (United States)

Author keywords

7,12 dimethylbeaz( )anthracene; Apoptosis; Aromatic hydrocarbons; Rat model; Transcription factors

Indexed keywords

DIMETHYLBENZ[A]ANTHRACENE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CARCINOGENESIS; HUMAN; PRIORITY JOURNAL;

EID: 0031440245     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119848     Document Type: Article

References (70)

1. Harris, J.R., M.E. Lippman, U. Veronesi, and W. Willett. 1992. Breast cancer (1). N. Engl. J. Med. 327:319-328.
2. DiAugustine, R., and D.L. Davis. 1993. A holistic approach to breast cancer. Environ. Health Perspect. 101:116-120.
3. Falck, F., Jr., A. Ricci, Jr., M.S. Wolff, J. Godbold, and P. Deckers. 1992. Pesticides and polychlorinated biphenyl residues in human breast lipids and their relation to breast cancer. Arch. Environ. Health. 47:143-146.
4. Morris, J.J., and E. Seifter. 1992. The role of aromatic hydrocarbons in the genesis of breast cancer. Med. Hypotheses. 38:177-184.
5. Wolff, M.S., P.G. Toniolo, E.W. Lee, M. Rivera, and N. Dubin. 1993. Blood levels of organochlorine residues and risk of breast cancer. J. Natl. Cancer Inst. 85:648-652.
6. Burbach, K.M., A. Poland, and C.A. Bradfield. 1992. Cloning of the Ahreceptor cDNA reveals a distinctive ligand-activated transcription factor. Proc. Natl. Acad. Sci. USA. 89:8185-8189.
7. Ema, M., K. Sogawa, N. Watanabe, Y. Chujoh, N. Matsushita, O. Gotoh, Y. Funae, and Y. Fujii-Kuriyama. 1992. cDNA cloning and structure of mouse putative Ah receptor. Biochem. Biophys. Res. Commun. 184:246-253.
8. Safe, S. 1984. Polychlorinated biphenyls (PCBs) and polybrominated biphenyls (PBBs): biochemistry, toxicology, and mechanism of action. Crit. Rev. Toxicol. 13:319-395.
9. Buening, M.K., R.L. Chang, M.T. Huang, J.G. Fortner, A.W. Wood, and A.H. Conney. 1981. Activation and inhibition of benzo(a)pyrene and aflatoxin B1 metabolism in human liver microsomes by naturally occurring flavonoids. Cancer Res. 41:67-72.
10. Le Bon, A.M., M.H. Siess, and M. Suschetet. 1992. Inhibition of microsome-mediated binding of benzo[a]pyrene to DNA by flavonoids either in vitro or after dietary administration to rats. Chem. Bio. Interact. 83:65-71.
11. Nebert, D.W., and F.J. Gonzalez. 1987. P450 genes: structure, evolution, and regulation. Annu. Rev. Biochem. 56:945-993.
12. Nebert, D.W., D.D. Petersen, and A.J. Fornace, Jr. 1990. Cellular responses to oxidative stress: the [Ah] gene battery as a paradigm. Environ. Health Perspect. 88:13-25.
13. Ghosh, S., A.M. Gifford, L.R. Riviere, P. Tempst, G.P. Nolan, and D. Baltimore. 1990. Cloning of the p50 DNA binding subunit of NF-κB: homology to rel and dorsal. Cell. 62:1019-1029.
14. Kieran, M., V. Blank, F. Logeat, J. Vandekerckhove, F. Lottspeich, O. Le Bail, M.B. Urban, P. Kourilsky, P.A. Baeuerle, and A. Israel. 1990. The DNA binding subunit of NF-κB is identical to factor KBF1 and homologous to the rel oncogene product. Cell. 62:1007-1018.
15. Ruben, S.M., P.J. Dillon, R. Schreck, T. Henkel, C.H. Chen, M. Maher, P.A. Baeuerle, and C.A. Rosen. 1991. Isolation of a rel-related human cDNA that potentially encodes the 65-kD subunit of NF-κB. Science. 251:1490-1493.
16. Grilli, M., J.J. Chiu, and M.J. Lenardo. 1993. NF-κB and Rel: participants in a multiform transcriptional regulatory system. Int. Rev. Cytol. 143:1-62.
17. Gilmore, T.D. 1991. Malignant transformation by mutant Rel proteins. Trends Genet. 7:318-322.
18. Schmid, R.M., N.D. Perkins, C.S. Duckett, P.C. Andrews, and G.J. Nabel. 1991. Cloning of an NF-κB subunit which stimulates HIV transcription in synergy with p65. Nature. 352:733-736.
19. Ryseck, R.P., P. Bull, M. Takamiya, V. Bours, U. Siebenlist, P, Dobrzanski, and R. Bravo. 1992. RelB, a new Rel family transcription activator that can interact with p50-NF-κB. Mol. Cell. Biol. 12:674-684.
20. Baeuerle, P.A. 1991. The inducible transcription activator NF-κB: regulation by distinct protein subunits. Biochem. Biophvs. Acta. 1072:63-80.
21. Blank, V., P. Kourilsky, and A. Israel. 1992. NF-κB and related proteins: Rel/dorsal homologies meet ankyrin-like repeats. Trends Biochem. Sci. 17:135-140.
22. Verma, I.M., J.K. Stevenson, E.M. Schwarz, D. Van Antwerp, and S. Miyamoto. 1995. Rel/NF-κB/IκB family: intimate tales of association and dissociation. Genes Dev. 9:2723-2735.
23. Baeuerle, P.A., and T. Henkel. 1994. Function and activation of NF-κB in the immune system. Annu. Rev. Immunol. 12:141-179.
24. Wu, M., H. Lee, R.E. Bellas, S.L. Schauer, M. Arsura, D. Katz. M.J. FitzGerald, T.L. Rothstein, D.H. Sherr, and G.E. Sonenshein. 1996. Inhibition of NF-κB/Rel induces apoptosis of murine B cells. EMBO J. 15:4682-4690.
25. Arsura, M., M. Wu, and G.E, Sonenshein. 1996. TGF-β1 inhibits NF-κB/Rel activity inducing apoptosis of B cells: transcriptional activation of IκB-α. Immunity. 5:31-40.
26. Arsura, M., M.J. FitzGerald, N. Fausto, and G.E. Sonenshein. 1997. NF-κB/Rel blocks transforming growth factor-β1-induced apoptosis of murine hepatocyte cell lines. Cell Growth & Differ. 8:1049-1059.
27. Bellas, R.E., M.J. FitzGerald, N. Fausto, and G.E. Sonenshein. 1997. Inhibition of NF-κB activity induces apoptosis in murine hepatocytes. Am. J. Pathol. 151:891-896.
28. Wang, C.Y., M.W. Mayo, and A.S. Baldwin, Jr. 1996. TNF-α and cancer therapy-induced apoptosis: potentiation by inhibition of NF-κB. Science. 274: 784-787.
29. Van Antwerp, D.J., S.J. Martin, T. Kafri, D.R. Green, and I.M. Verma. 1996. Suppression of TNF-α-induced apoptosis by NF-κB. Science. 274:787-789.
30. Liu, Z.G., H. Hsu, D.V. Goeddel, and M. Karin. 1996. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-κB activation prevents cell death. Cell. 87:565-576.
31. Beg, A.A., and D. Baltimore. 1996. An essential role for NF-κB in preventing TNF-α-induced cell death. Science. 274:782-784.
32. Soule, H.D., J. Vazguez, A. Long, S. Albert, and M. Brennan. 1973. A human cell line from a pleural effusion derived from a breast carcinoma. J. Natl. Cancer Inst. 51:1409-1416.
33. Hackett, A.J., H.S. Smith, E.L. Springer, R.B. Owens, W.A. NelsonRees, J.L. Riggs, and M.B. Gardner. 1977. Two syngeneic cell lines from human breast tissue: the aneuploid mammary epithelial (Hs578T) and the diploid myoepithelial (Hs578Bst) cell lines. J. Natl. Cancer Inst. 58:1795-1806.
34. Calaf, G., and J. Russo. 1993. Transformation of human breast epithelial cells by chemical carcinogens. Carcinogenesis. 14:483-492.
35. Soule, H.D., T.M. Maloney, S.R. Wolman, W.D. Peterson, Jr., R. Brenz, C.M. McGrath, J. Russo, R.J. Pauley, R.F. Jones, and S.C. Brooks. 1990. Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res. 50:6075-6086.
36. Dignam, J.D., R.M. Lebovitz, and R.G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
37. Duyao, M.P., A.J. Buckler, and G.E. Sonenshein. 1990. Interaction of an NF-κB-like factor with a site upstream of the c-myc promoter. Proc. Natl. Acad. Sci. USA. 87:4727-4731.
38. Bellas, R.E., J.S. Lee, and G.E. Sonenshein. 1995. Expression of a constitutive NF-κB-like activity is essential for proliferation of cultured bovine vascular smooth muscle cells. J. Clin. Invest. 96:2521-2527.
39. Sen, R., and D. Baltimore. 1986. Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell. 46:705-716.
40. Chen, C., and H. Okayama. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:2745-2752.
41. Lawrence, R., L.J. Chang, U. Siebenlist, P. Bressler, and G.E. Sonenshein. 1994. Vascular smooth muscle cells express a constitutive NF-κB-like activity. J. Biol. Chem. 269:28913-28918.
42. La Rosa, F.A., J.W. Pierce, and G.E. Sonenshein. 1994. Differential regulation of the c-myc oncogene promoter by the NF-κB rel family of transcription factors. Mol. Cell. Biol. 14:1039-1044.
43. Kunsch, C., S.M. Ruben, and C.A. Rosen. 1992. Selection of optimal κB/Rel DNA-binding motifs: interaction of both subunits of NF-κB with DNA is required for transcriptional activation. Mol. Cell. Biol. 12:4412-4421.
44. Lee, H., M. Arsura, M. Wu, M. Duyao, A.J. Buckler, and G.E. Sonenshein. 1995. Role of Rel-related factors in control of c-myc gene transcription in receptor-mediated apoptosis of the murine B cell WEHI 231 line. J. Exp. Med. 181:1169-1177.
45. Brown, K., S. Gerstberger, L. Carlson, G. Franzoso, and U. Siebenlist. 1995. Control of IκB-α proteolysis by site-specific, signal-induced phosphorylation. Science. 267:1485-1488.
46. Duyao, M.P., D.J. Kessler, D.B. Spicer, C. Bartholomew, J.L. Cleveland, M. Siekevitz, and G.E. Sonenshein. 1992. Transactivation of the c-myc promoter by human T cell leukemia virus type 1 tax is mediated by NF-κB. J. Biol. Chem. 267:16288-16291.
47. Simon, M.C., M. Olson, E. Scott, A. Hack, G. Su, and H. Singh. 1996. Terminal myeloid gene expression and differentiation requires the transcription factor PU.1. Curr. Top. Microbiol. Immunol. 211:113-119.
48. Moreau-Gachelin, F. 1994. Spi-1/PU.1: an oncogene of the Ets family. Biochem. Biophys. Acta. 1198:149-163.
49. Buras, J.A., W.R. Reenstra, and M.J. Fenton. 1995. NF-βA, a factor required for maximal interleukin-1β gene expression is identical to the ets family member PU.1. Evidence for structural alteration following LPS activation. Mol. Immunol. 32:541-554.
50. Michaelson, J.S., M. Singh, C.M. Snapper, W.C. Sha, D. Baltimore, and B.K. Birshtein. 1996. Regulation of 3′ IgH enhancers by a common set of factors, including κB-binding proteins. J. Immunol. 156:2828-2839.
51. Lamb, N.J., A. Fernandez, N. Tourkine, P. Jeanteur, and J.M. Blanchard. 1990. Demonstration in living cells of an intragenic negative regulatory element within the rodent c-fos gene. Cell 61:485-496.
52. Gilman, M.Z., L.A. Berkowitz, J.R. Feramisco, B.R. Franza, Jr., R.M. Graham, K.T. Riabowol, and W.A. Ryan, Jr. 1988. Intracellular mediators of c-fos induction. Cold Spring Harbor Symp. Quant. Biol. 53:761-767.
53. Rogers, A.E., and B.H. Conner. 1990. Dimethylbenzanthracene-induced mammary tumorigenesis in ethanol-fed rats. Nutr. Res. 10:915-928.
54. Rice, N.R., and M.K. Ernst. 1993. In vivo control of NF-κB activation by IκB-α. EMBO J. 12:4685-4695.
55. Biswas, D.K., B.J. Dezube, C.M. Ahlers, and A.B. Pardee. 1993. Pentoxifylline inhibits HIV-1 LTR-driven gene expression by blocking NF-κB action. J. AIDS. 6:778-786.
56. Staal, F.J., M. Roederer, and L.A. Herzenberg. 1990. Intracellular thiols regulate activation of NF-κB and transcription of human immunodeficiency virus. Proc. Natl. Acad. Sci. USA. 87:9943-9947.
57. Manz, A., J. Berger, J.H. Dwyer, D. Flesch-Janys, S. Nagel, and H. Waltsgott. 1991. Cancer mortality among workers in chemical plant contaminated with dioxin. Lancet. 338:959-964.
58. Willett, W. 1989. The search for the causes of breast and colon cancer. Nature. 338:389-394.
59. Conney, A. H. 1982. Induction of microsomal enzymes by foreign chemicals and carcinogenesis by polycyclic aromatic hydrocarbons: G.H.A. Clowes memorial lecture. Cancer Res. 42:4875-4917.
60. Wu, M., M. Arsura, R.E. Bellas, M.J. Fitzgerald, H. Lee, S.L. Schauer, D.H. Sherr, and G.E. Sonenshein. 1996. Inhibition of c-myc expression induces apoptosis of WEHI 231 murine B cells. Mol. Cell. Biol. 16:5015-5025.
61. Roux-Dosseto, M., S. Romain, N. Dussault, C. Desideri, L. Piana, P. Bonnier, N. Tubiana, and P.M. Martin. 1992. c-myc gene amplification in selected node-negative breast cancer patients correlates with high rate of early relapse. Eur. J. Cancer. 28A:1600-1604.
62. Berns, E.M., J.G. Klijn, W.L. van Putten, I.L. van Staveren, H. Portengen, and J.A. Foekens. 1992. c-myc amplification is a better prognostic factor than Her2/neu amplification in primary breast cancer. Cancer Res. 52:1107-1113.
63. Bonilla, M., M. Ramirez, J. Lopez-Cueto, and P. Gariglio. 1988. In vivo amplification and rearrangement of c-myc oncogene in human breast tumors. J. Natl. Cancer Inst. 80:665-671.
64. Leder, A., P.K. Pattengale, A. Kuo, T.A. Stewart, and P. Leder. 1986. Consequences of widespread deregulation of the c-myc gene in transgenic mice: multiple neoplasms and normal development. Cell. 45:485-495.
65. Pavelic, Z.P., P. Steele, and H.D. Preisler. 1991. Evaluation of c-myc proto-oncogene in primary human breast carcinomas. Anticancer Res. 11:1421-1427.
66. Schoenenberger, C.A., A.C. Andres, B. Groner, M. van der Valk, M. LeMeur, and P. Gerlinger. 1988. Targeted c-myc gene expression in mammary glands of transgenic mice induces mammary tumours with constitutive milk protein gene transcription. EMBO J. 7:169-175.
67. Borg, A., B. Baldetorp, M. Ferno, H. Olsson, and H. Sigurdsson. 1992. c-myc amplification is an independent prognostic factor in postmenopausal breast cancer. Int. J. Cancer. 51:687-691.
68. Pertschuk, L.P., J.G. Feldman, D.S. Kim, K. Nayeri, K.B. Eisenberg, A.C. Carter, W.T. Thelmo, Z.T. Rhong, P. Benn, and A. Grossman. 1993. Steroid hormone receptor immunohistochemistry and amplification of c-myc protooncogene. Relationship to disease-free survival in breast cancer. Cancer. 71: 162-171.
69. Dupont, W.D., and D.L. Page. 1985. Risk factors for breast cancer in women with proliferative breast disease. N. Engl. J. Med. 312:146-151.
70. Cai, Z., M. Korner, N. Tarantino, and S. Chouaib. 1997. IκB-α overexpression in human breast carcinoma MCF7 cells inhibits nuclear factor-κB activation but not tumor necrosis factor-α-induced apoptosis. J. Biol. Chem. 272: 96-101.