Aberrant activation of NF-κB signaling in mammary epithelium leads to abnormal growth and ductal carcinoma in situ

BMC Cancer

Volumn 15, Issue 1, 2015, Pages

  Barham, Whitney ^a   Chen, Lianyi ^a   Tikhomirov, Oleg ^a   Onishko, Halina ^a   Gleaves, Linda ^b   Stricker, Thomas P ^b   Blackwell, Timothy S ^b,c   Yull, Fiona E ^a,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c VANDERBILT INGRAM CANCER CENTER   (United States)

Author keywords

Ductal carcinoma in situ; Hyperplasia; Inflammation; Mammary; Mucin 1; Nuclear factor kappa B

Indexed keywords

CXCL1 CHEMOKINE; CYCLOOXYGENASE 2; ESTROGEN RECEPTOR ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; MUCIN 1; PROGESTERONE RECEPTOR; PROLACTIN RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; BIOLOGICAL MARKER; I KAPPA B KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOGENESIS; BREAST EPITHELIUM; BREAST HYPERPLASIA; CONTROLLED STUDY; DOWN REGULATION; FEMALE; INFLAMMATION; INTRADUCTAL CARCINOMA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TRANSGENIC MOUSE; UPREGULATION; ANIMAL; ANTIBODY SPECIFICITY; BREAST TUMOR; CANCER GRADING; CARCINOMA IN SITU; CELL PROLIFERATION; CELL TRANSFORMATION; DISEASE MODEL; ENZYME ACTIVATION; EPITHELIUM; GENE EXPRESSION; GENETICS; HUMAN; HYPERPLASIA; METABOLISM; PAGET NIPPLE DISEASE; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BIOMARKERS; BREAST NEOPLASMS; CARCINOMA IN SITU; CARCINOMA, DUCTAL, BREAST; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; EPITHELIUM; FEMALE; GENE EXPRESSION; HUMANS; HYPERPLASIA; I-KAPPA B KINASE; INFLAMMATION MEDIATORS; MICE; MICE, TRANSGENIC; NEOPLASM GRADING; NF-KAPPA B; ORGAN SPECIFICITY; SIGNAL TRANSDUCTION;

EID: 84942608135     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/s12885-015-1652-8     Document Type: Article

References (51)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646-74.
2. Hinck L, Näthke I. Changes in cell and tissue organization in cancer of the breast and colon. Curr Opin Cell Biol. 2014;26:87-95.
3. Ernster V, Barclay J, Kerlikowske K, Grady D, Henderson C. Incidence of and Treatment for Ductal Carcinoma In Situ of the Breast. JAMA. 1996;275:913-8.
4. American Cancer Society: Breast Cancer Facts and Figures 2011-2012. American Cancer Society Inc. Atlanta, GA; 2012
5. Wells CJ, O'Donoghue C, Ojeda-Fournier H, Retallack HEG, Esserman LJ. Evolving paradigm for imaging, diagnosis, and management of DCIS. J Am Coll Radiol. 2013;10:918-23.
6. Erbas B, Provenzano E, Armes J, Gertig D. The natural history of ductal carcinoma in situ of the breast: a review. Breast Cancer Res Treat. 2006;97:135-44.
7. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420:860-7.
8. Baeuerle P, Baltimore D. I kappa B: a specific inhibitor of the NF-kappa B transcription factor. Science (80-). 1988;242:540-6.
9. Hayden MS, Ghosh S. Shared principles in NF-kappaB signaling. Cell. 2008;132:344-62.
10. Vallabhapurapu S, Karin M. Regulation and function of NF-kappaB transcription factors in the immune system. Annu Rev Immunol. 2009;27:693-733.
11. Zheng C, Yin Q, Wu H. Structural studies of NF-κB signaling. Cell Res. 2011;21:183-95.
12. Connelly L, Barham W, Pigg R, Saint-Jean L, Sherrill T, Cheng D-S, et al. Activation of nuclear factor kappa B in mammary epithelium promotes milk loss during mammary development and infection. J Cell Physiol. 2010;222:73-81.
13. Howe LR, Subbaramaiah K, Hudis CA, Dannenberg AJ. Molecular pathways: adipose inflammation as a mediator of obesity-associated cancer. Clin Cancer Res. 2013;19:6074-83.
14. McGregor BA, Antoni MH. Psychological intervention and health outcomes among women treated for breast cancer: a review of stress pathways and biological mediators. Brain Behav Immun. 2009;23:159-66.
15. Brantley DM, Chen CL, Muraoka RS, Bushdid PB, Bradberry JL, Kittrell F, et al. Nuclear factor-kappaB (NF-kappaB) regulates proliferation and branching in mouse mammary epithelium. Mol Biol Cell. 2001;12:1445-55.
16. Connelly L, Barham W, Onishko HM, Sherrill T, Chodosh LA, Blackwell TS, et al. Inhibition of NF-kappa B activity in mammary epithelium increases tumor latency and decreases tumor burden. Oncogene. 2011;30:1402-12.
17. Pratt M, Tibbo E, Robertson SJ, Jansson D, Hurst K, Perez-Iratxeta C, et al. The canonical NF-kappaB pathway is required for formation of luminal mammary neoplasias and is activated in the mammary progenitor population. Oncogene. 2009;28:2710-22.
18. Liu M, Sakamaki T, Casimiro MC, Willmarth NE, Quong AA, Ju X, et al. The canonical NF-kappaB pathway governs mammary tumorigenesis in transgenic mice and tumor stem cell expansion. Cancer Res. 2010;70:10464-73.
19. Gonzalez-Suarez E, Jacob AP, Jones J, Miller R, Roudier-Meyer MP, Erwert R, et al. RANK ligand mediates progestin-induced mammary epithelial proliferation and carcinogenesis. Nature. 2010;468:103-7.
20. Cheng DS, Han W, Chen SM, Sherrill TP, Chont M, Park G-Y, et al. Airway Epithelium Controls Lung Inflammation and Injury through the NF-kappaB Pathway. J Immunol. 2007;178:6504-13.
21. Gunther E, Belka G, Wertheim G, Wang J, Hartman J, Boxer R, et al. A novel doxycycline-inducible system for the transgenic analysis of mammary gland biology. FASEB J. 2002;16:283-92.
22. Connelly L, Robinson-Benion C, Chont M, Saint-Jean L, Li H, Polosukhin VV, et al. A transgenic model reveals important roles for the NF-kappa B alternative pathway (p100/p52) in mammary development and links to tumorigenesis. J Biol Chem. 2007;282:10028-35.
23. Dunphy KA, Tao L, Jerry DJ: Mammary epithelial transplant procedure. J Vis Exp 2010, doi: 10.3791/1849
24. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402-8.
25. Chen C-L, Singh N, Yull FE, Strayhorn D, Van Kaer L, Kerr LD. Lymphocytes Lacking I kappaB-alpha Develop Normally, But Have Selective Defects in Proliferation and Function. J Immunol. 2000;165:5418-27.
26. Reginato MJ, Muthuswamy SK. Illuminating the center: mechanisms regulating lumen formation and maintenance in mammary morphogenesis. J Mammary Gland Biol Neoplasia. 2006;11:205-11.
27. Kawamoto H, Koizumi H, Uchikoshi T. Expression of the G2-M Checkpoint Regulators Cyclin B1 and cdc2 in Nonmalignant and Malignant Human Breast Lesions. Am J Pathol. 1997;150:15-23.
28. Pei X, Bai F, Smith M, Usary J, Fan C, Pai S, et al. CDK Inhibitor p18 INK4c Is a Downstream Target of GATA3 and Restrains Mammary Luminal Progenitor Cell Proliferation and Tumorigenesis. Cancer Cell. 2009;15:389-401.
29. Reed JR, Leon RP, Hall MK, Schwertfeger KL. Interleukin-1beta and fibroblast growth factor receptor 1 cooperate to induce cyclooxygenase-2 during early mammary tumourigenesis. Breast Cancer Res. 2009;11:R21.
30. Montesano R, Soulié P, Eble JA, Carrozzino F. Tumour necrosis factor alpha confers an invasive, transformed phenotype on mammary epithelial cells. J Cell Sci. 2005;118(Pt 15):3487-500.
31. Liu CH, Chang SH, Narko K, Trifan OC, Wu MT, Smith E, et al. Overexpression of cyclooxygenase-2 is sufficient to induce tumorigenesis in transgenic mice. J Biol Chem. 2001;276:18563-9.
32. Choi YS, Chakrabarti R, Escamilla-Hernandez R, Sinha S. Elf5 conditional knockout mice reveal its role as a master regulator in mammary alveolar development: failure of Stat5 activation and functional differentiation in the absence of Elf5. Dev Biol. 2009;329:227-41.
33. Kufe DW. MUC1-C oncoprotein as a target in breast cancer: activation of signaling pathways and therapeutic approaches. Oncogene. 2013;32:1073-81.
34. Mommers EC, Leonhart AM, von Mensdorff-Pouilly S, Schol DJ, Hilgers J, Meijer CJ, et al. Aberrant expression of MUC1 mucin in ductal hyperplasia and ductal carcinoma In situ of the breast. Int J Cancer. 1999;84:466-9.
35. Lu P, Weaver VM, Werb Z. The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol. 2012;196:395-406.
36. Holloway RW, Bogachev O, Bharadwaj AG, McCluskey GD, Majdalawieh AF, Zhang L, et al. Stromal adipocyte enhancer-binding protein (AEBP1) promotes mammary epithelial cell hyperplasia via proinflammatory and hedgehog signaling. J Biol Chem. 2012;287:39171-81.
37. Welm BE, Freeman KW, Chen M, Contreras A, Spencer DM, Rosen JM. Inducible dimerization of FGFR1: development of a mouse model to analyze progressive transformation of the mammary gland. J Cell Biol. 2002;157:703-14.
38. Witzel I-I, Koh LF, Perkins ND. Regulation of cyclin D1 gene expression. Biochem Soc Trans. 2010;38(Pt 1):217-22.
39. Antonaki A, Demetriades C, Polyzos A, Banos A, Vatsellas G, Lavigne MD, et al. Genomic analysis reveals a novel nuclear factor-κB (NF-κB)-binding site in Alu-repetitive elements. J Biol Chem. 2011;286:38768-82.
40. Pellegrini P, Pasquale P, Cordero A, Alex C, Gallego MI, Marta Ines G, et al. Constitutive activation of RANK disrupts mammary cell fate leading to tumorigenesis. Stem Cells. 2013;31:1954-65.
41. Chua HL, Bhat-Nakshatri P, Clare SE, Morimiya A, Badve S, Nakshatri H. NF-kappaB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2. Oncogene. 2007;26:711-24.
42. Ueno T, Toi M, Saji H. Significance of Macrophage Chemoattractant Protein-1 in Macrophage Recruitment, Angiogenesis, and Survival in Human Breast Cancer. Clin Cancer Res. 2000;6:3282-9.
43. Valković T, Lucin K, Krstulja M, Dobi-Babić R, Jonjić N. Expression of monocyte chemotactic protein-1 in human invasive ductal breast cancer. Pathol Res Pract. 1998;194:335-40.
44. Li H, Chen K, Su F, Song E, Gong C. Preoperative CA 15-3 levels predict the prognosis of nonmetastatic luminal A breast cancer. J Surg Res. 2014;189:48-56.
45. Li Y, Yi H, Yao Y, Liao X, Xie Y, Yang J, et al. The cytoplasmic domain of MUC1 induces hyperplasia in the mammary gland and correlates with nuclear accumulation of β-catenin. PLoS One. 2011;6:e19102.
46. Bitler BG, Goverdhan A, Schroeder J. MUC1 regulates nuclear localization and function of the epidermal growth factor receptor. J Cell Sci. 2010;123(Pt 10):1716-23.
47. Raina D, Ahmad R, Joshi MD, Yin L, Wu Z, Kawano T, et al. Direct targeting of the mucin 1 oncoprotein blocks survival and tumorigenicity of human breast carcinoma cells. Cancer Res. 2009;69:5133-41.
48. Uchida Y, Raina D, Kharbanda S, Kufe D. Inhibition of the MUC1-C oncoprotein is synergistic with cytotoxic agents in the treatment of breast cancer cells. Cancer Biol Ther. 2013;14:127-34.
49. Bane A. Ductal Carcinoma In Situ : What the Pathologist Needs to Know and Why. Int J Breast Cancer. 2013;2013:914053.
50. Welch H, Black W. Using Autopsy Series To Estimate the Disease "Reservoir" for Ductal Carcinoma in Situ of the Breast: How Much More Breast Cancer Can We Find? Ann Intern Med. 1997;127:1023-8.
51. Page D, Dupont W, Rogers L, Landenberger M. Intraductal carcinoma of the breast: follow-up after biopsy only. Cancer. 1982;49:751-8.