Mullerian-inhibiting substance induces Gro-β expression in breast cancer cells through a nuclear factor-κB-dependent and Smad1-dependent mechanism

Cancer Research

Volumn 67, Issue 6, 2007, Pages 2747-2756

  Gupta, Vandana ^a   Yeo, Giminna ^a   Kawakubo, Hirofumi ^a   Rangnekar, Vivek ^b   Ramaswamy, Preethi ^a   Hayashida, Tetsu ^a   MacLaughlin, David T ^c   Donahoe, Patricia K ^c   Maheswaran, Shyamala ^a,d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CHEMOKINE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 1; MUELLERIAN INHIBITING FACTOR; PROTEIN GRO BETA; SMAD1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; BREAST EPITHELIUM; BTG2 GENE; CANCER CELL; CANCER GROWTH; CHROMATIN IMMUNOPRECIPITATION; CLONAL VARIATION; CONTROLLED STUDY; DRUG MECHANISM; GENE; GENE EXPRESSION; GENE TRANSLOCATION; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION;

BREAST NEOPLASMS; CELL LINE, TUMOR; CELL NUCLEUS; CHEMOKINES, CXC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; GLYCOPROTEINS; HUMANS; IMMEDIATE-EARLY PROTEINS; INTERFERON REGULATORY FACTOR-1; NF-KAPPA B; PHOSPHORYLATION; PROMOTER REGIONS (GENETICS); RECOMBINANT PROTEINS; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SMAD1 PROTEIN; TESTICULAR HORMONES; TRANSCRIPTION FACTOR RELA;

EID: 34047274468     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-06-2312     Document Type: Article

References (52)

1. Teixeira J, Donahoe PK. Molecular biology of MIS and its receptors. J Androl 1996;7:336-41.
2. Segev DL, Ha TU, Tran TT, et al. Mullerian inhibiting substance inhibits breast cancer cell growth through an NFκB-mediated pathway [In Process Citation]. J Biol Chem 2000;275:28371-9.
3. Segev DL, Hoshiya Y, Hoshiya M, et al. Mullerian-inhibiting substance regulates NF-κB signaling in the prostate in vitro and in vivo. Proc Natl Acad Sci U S A 2000;99:239-44.
4. Aggarwal BB. Nuclear factor-κB: the enemy within. Cancer Cell 2004;6:203-8.
5. Hayden MS, Ghosh S. Signaling to NF-κB. Genes Dev 2004;18:2195-224.
6. Verma IM. Nuclear factor (NF)-κB proteins: therapeutic targets. Ann Bheum Dis 2004;63 Suppl 2:ii57-61.
7. Karin M, Yamamoto Y, Wang QM. The IKK NF-κB system: a treasure trove for drug development. Nat Rev Drug Discov 2004;3:17-26.
8. Hacker H, Karin M. Regulation and function of IKK and IKK-related kinases. Sci STKE 2006;357:rel3.
9. Kovalenko A, Wallach D. If the prophet does not come to the mountain: dynamics of signaling complexes in NF-κB activation. Mol Cell 2006;22:433-6.
10. Ghosh S, May MJ, Kopp EB. NF-κB and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 1998;16:225-60.
11. Leung TH, Hoffmann A, Baltimore D. One nucleotide in a κB site can determine cofactor specificity for NF-κB dimers. Cell 2004;118:453-64.
12. Thanos D, Maniatis T. The high mobility group protein HMG I(Y) is required for NF-κB-dependent virus induction of the human IFN-β gene. Cell 1992;71:777-89.
13. Escalante CR, Shen L, Thanos D, Aggarwal AK. Structure of NF-κB p50/p65 heterodimer bound to the PRDII DNA element from the interferon-β promoter. Structure 2002;10:383-91.
14. Berkowitz B, Huang DB, Chen-Park FE, Sigler PB, Ghosh G. The X-ray crystal structure of the NF-κB p50.p65 heterodimer bound to the interferon β-κB site. J Biol Chem 2002;277:24694-700.
15. Benezra M, Chevallier N, Morrison DJ, MacLachlan TK, El-Deiry WS, Licht JD. BRCA1 augments transcription by the NF-κB transcription factor by binding to the Rel domain of the p65/RelA subunit. J Biol Chem 2003; 278:26333-41.
16. Falvo JV, Thanos D, Maniatis T. Reversal of intrinsic DNA bends in the IFNβ gene enhancer by transcription factors and the architectural protein HMG I(Y). Cell 1995;83:1101-11.
17. Gouedard L, Chen YG, Thevenet L, et al. Engagement of bone morphogenetic protein type IB receptor and Smad1 signaling by anti-Mullerian hormone and its type II receptor. J Biol Chem 2000;275:27973-8.
18. Bitzer M, von Gersdorff G, Liang D, et al. A mechanism of suppression of TGF-β/SMAD signaling by NF-κB/RelA Genes Dev 2000;14:187-97.
19. Chen S, Guttridge DC, Tang E, Shi S, Guan K, Wang CY. Suppression of tumor necrosis factor-mediated apoptosis by nuclear factor κB-independent bone morphogenetic protein/Smad signaling. J Biol Chem 2001;276:39259-63.
20. Lopez-Rovira T, Chalaux E, Rosa JL, Bartrons R, Ventura F. Interaction and functional cooperation of NF-κB with Smads. Transcriptional regulation of the junB promoter. J Biol Chem 2000;275:28937-46.
21. Oquendo P, Alberta J, Wen DZ, Graycar JL, Derynck R, Stiles CD. The platelet-derived growth factor-inducible KC gene encodes a secretory protein related to platelet α-granule proteins. J Biol Chem 1989;264:4133-7.
22. Haskill S, Peace A, Morris J, et al. Identification of three related human GRO genes encoding cytokine functions. Proc Natl Acad Sci U S A 1990;87:7732-6.
23. Baggiolini M, Dewald B, Moser B. Human chemokines: an update. Annu Rev Immunol 1997;15:675-705.
24. Anisowicz A, Zajchowski D, Stenman G, Sager R. Functional diversity of gro gene expression in human fibroblasts and mammary epithelial cells. Proc Natl Acad Sci U S A 1988;85:9645-9.
25. Pulai JI, Chen H, Im HJ, et al. NF-κB mediates the stimulation of cytokine and chemokine expression by human articular chondrocytes in response to fibronectin fragments. J Immunol 2005;174:5781-8.
26. Joshi-Barve SS, Rangnekar W, Sells SF, Rangnekar VM. Interleukin-1- inducible expression of gro-β via NF-κB activation is dependent upon tyrosine kinase signaling. J Biol Chem 1993;268:18018-29.
27. Tian B, Nowak DE, Jamaluddin M, Wang S, Brasier AR. Identification of direct genomic targets downstream of the nuclear factor-κB transcription factor mediating tumor necrosis factor signaling. J Biol Chem 2005;280: 17435-48.
28. Segev DL, Hoshiya Y, Stephen AE, et al. Mullerian inhibiting substance regulates NFκB signaling and growth of mammary epithelial cells in vivo. J Biol Chem 2001;276:26799-806.
29. Ragin RC, Donahoe PK, Kenneally MK, Ahmad MF, MacLaughlin DT. Human mullerian inhibiting substance: enhanced purification imparts biochemical stability and restores antiproliferative effects. Protein Expr Purif 1992;3:236-45.
30. Hoshiya Y, Gupta V, Kawakubo H, et al. Mullerian inhibiting substance promotes interferon γ-induced gene expression and apoptosis in breast cancer cells. J Biol Chem 2003;278:51703-12.
31. Tran TT, Segev DL, Gupta V, et al. Mullerian inhibiting substance regulates androgen-induced gene expression and growth in prostate cancer cells through a nuclear factor-κB-dependent Smad-independent mechanism. Mol Endocrinol 2006;20:2382-91.
32. Ha TU, Segev DL, Barbie D, et al. Mullerian inhibiting substance inhibits ovarian cell growth through an Rb-independent mechanism. J Biol Chem 2000;275:37101-9.
33. Kawakubo H, Carey JL, Brachtel E, et al. Expression of the NF-κB-responsive gene BTG2 is aberrantly regulated in breast cancer. Oncogene 2004;23:8310-9.
34. Meluh PB, Broach JR. Immunological analysis of yeast chromatin. Methods Enzymol 1999;304:414-30.
35. Porter DA, Krop IE, Nasser S. A SAGE (serial analysis of gene expression) view of breast tumor progression. Cancer Res 2001;61:5697-702.
36. Kehlen A, Thiele K, Riemann D, Langner J. Expression, modulation, and signalling of IL-17 receptor in fibroblast-like synoviocytes of patients with rheumatoid arthritis. Clin Exp Immunol 2002;127:539-46.
37. Anisowicz A, Messineo M, Lee SW, Sager R. An NF-κB-like transcription factor mediates IL-1/TNF-α induction of gro in human fibroblasts. J Immunol 1991;147:520-7.
38. Zhang Y, Feng XH, Derynck R. Smad3 and Smad4 cooperate with c-Jun/c-Fos to mediate TGF-β-induced transcription. Nature 1998;394:909-13.
39. Nakashima K, Yanagisawa M, Arakawa H, et al. Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 1999;284:479-82.
40. Lin R, Gewert D, Hiscott J. Differential transcriptional activation in vitro by NF-κB/Rel proteins. J Biol Chem 1995;270:3123-31.
41. Anrather J, Racchumi G, Iadecola C. cis-Acting, element-specific transcriptional activity of differentially phosphorylated nuclear factor-κB. J Biol Chem 2005;280: 244-52.
42. Yamit-Hezi A, Nir S, Wolstein O, Dikstein R. Interaction of TAFII105 with selected p65/RelA dimers is associated with activation of subset of NF-κB genes. J Biol Chem 2000;275:18180-7.
43. He B, Weber GF. Phosphorylation of NF-κB proteins by cyclic GMP-dependent kinase. A noncanonical pathway to NF-κB activation. Eur J Biochem 2003;270: 2174-85.
44. Eroshkin A, Mushegian A. Conserved transactivation domain shared by interferon regulatory factors and Smad morphogens. J Mol Med 1999;77:403-5.
45. Takahasi K, Suzuki NN, Horiuchi M, et al. X-ray crystal structure of IRF-3 and its functional implications. Nat Struct Biol 2003;10:922-7.
46. Cao Y, Chen C, Weatherbee JA, Tsang M, Folkman J. gro-β, a -C-X-C- chemokine, is an angiogenesis inhibitor that suppresses the growth of Lewis lung carcinoma in mice. J Exp Med 1995;182:2069-77.
47. Owen JD, Strieter R, Burdick M, et al. Enhanced tumor-forming capacity for immortalized melanocytes expressing melanoma growth stimulatory activity/ growth-regulated cytokine β and γ proteins. Int J Cancer 1997;73:94-103.
48. Wang D, Yang W, Du J, et al. MGSA/GRO-mediated melanocyte transformation involves induction of Ras expression. Oncogene 2000;19:4647-59.
49. Nakshatri H, Bhat-Nakshatri P, Martin DA, Goulet RJ, Jr., Sledge GW, Jr. Constitutive activation of NF-κB during progression of breast cancer to hormone-independent growth. Mol Cell Biol 1997;17:3629-39.
50. Sovak MA, Bellas RE, Kim D, et al. Aberrant nuclear factor-κB/Rel expression and the pathogenesis of breast cancer. J Clin Invest 1997;100:2952-60.
51. Ryan KM, Ernst MK, Rice NR, Vousden KH. Role of NF-κB in p53-mediated programmed cell death. Nature 2000;404:892-7.
52. Gapuzan ME, Schmah O, Pollock AD, Hoffmann A, Gilmore TD. Immortalized fibroblasts from NF-κB RelA knockout mice show phenotypic heterogeneity and maintain increased sensitivity to tumor necrosis factor α after transformation by v-Ras. Oncogene 2005;24: 6574-83.