β1-integrin via NF-κB signaling is essential for acquisition of invasiveness in a model of radiation treated in situ breast cancer

Breast Cancer Research

Volumn 15, Issue 4, 2013, Pages

  Nam, Jin Min ^a   Ahmed, Kazi M ^b   Costes, Sylvain ^b   Zhang, Hui ^b   Onodera, Yasuhito ^a   Olshen, Adam B ^c   Hatanaka, Kanako C ^d   Kinoshita, Rumiko ^a   Ishikawa, Masayori ^a   Sabe, Hisataka ^a   Shirato, Hiroki ^a   Park, Catherine C ^b,e  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d HOKKAIDO UNIVERSITY HOSPITAL   (Japan)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

DCIS; Ductal carcinoma in situ; Integrin; Ionizing radiation

Indexed keywords

BETA1 INTEGRIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN KINASE B;

ANIMAL; APOPTOSIS; BREAST NEOPLASMS; CARCINOMA, INTRADUCTAL, NONINFILTRATING; DISEASE MODEL; ENZYME ACTIVATION; FEMALE; GENETICS; HUMAN; IONIZING RADIATION; METABOLISM; MOUSE; MULTICELLULAR SPHEROID; PATHOLOGY; PHOSPHORYLATION; RADIATION RESPONSE; SIGNAL TRANSDUCTION; TUMOR CELL CULTURE; TUMOR CELL LINE; TUMOR INVASION; TUMOR RECURRENCE; UPREGULATION; XENOGRAFT;

ANIMALS; ANTIGENS, CD29; APOPTOSIS; BREAST NEOPLASMS; CARCINOMA, INTRADUCTAL, NONINFILTRATING; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; FEMALE; HETEROGRAFTS; HUMANS; MICE; NEOPLASM INVASIVENESS; NEOPLASM RECURRENCE, LOCAL; NF-KAPPA B; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RADIATION, IONIZING; SIGNAL TRANSDUCTION; SPHEROIDS, CELLULAR; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 84880957117     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr3454     Document Type: Article

References (39)

1. Polyak K, Kalluri R. The role of the microenvironment in mammary gland development and cancer. Cold Spring Harb Perspect Biol 2010, 2:a003244. 2964182, 20591988.
2. Solin LJ. The impact of adding radiation treatment after breast conservation surgery for ductal carcinoma in situ of the breast. J Natl Cancer Inst Monogr 2010, 2010:187-192. 10.1093/jncimonographs/lgq020, 20956827.
3. Fisher B, Costantino J, Redmond C, Fisher E, Margolese R, Dimitrov N, Wolmark N, Wickerham DL, Deutsch M, Ore L, Mamounas E, Poller W, Kavanah M. Lumpectomy compared with lumpectomy and radiation therapy for the treatment of intraductal breast cancer. N Engl J Med 1993, 328:1581-1586. 10.1056/NEJM199306033282201, 8292119.
4. Brown LF, Guidi AJ, Schnitt SJ, Van De Water L, Iruela-Arispe ML, Yeo TK, Tognazzi K, Dvorak HF. Vascular stroma formation in carcinoma in situ, invasive carcinoma, and metastatic carcinoma of the breast. Clin Cancer Res 1999, 5:1041-1056.
5. Orimo A, Weinberg RA. Stromal fibroblasts in cancer: a novel tumor-promoting cell type. Cell Cycle 2006, 5:1597-1601. 10.4161/cc.5.15.3112, 16880743.
6. Pavlakis K, Messini I, Vrekoussis T, Yiannou P, Keramopoullos D, Louvrou N, Liakakos T, Stathopoulos EN. The assessment of angiogenesis and fibroblastic stromagenesis in hyperplastic and pre-invasive breast lesions. BMC Cancer 2008, 8:88. 10.1186/1471-2407-8-88, 2323394, 18384688.
7. Desgrosellier JS, Cheresh DA. Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 2010, 10:9-22. 10.1038/nrc2748, 20029421.
8. Cordes N, Blaese MA, Meineke V, Van Beuningen D. Ionizing radiation induces up-regulation of functional beta1-integrin in human lung tumour cell lines in vitro. Int J Radiat Biol 2002, 78:347-357. 10.1080/09553000110117340, 12020426.
9. Park CC, Zhang H, Pallavicini M, Gray JW, Baehner F, Park CJ, Bissell MJ. Beta1 integrin inhibitory antibody induces apoptosis of breast cancer cells, inhibits growth, and distinguishes malignant from normal phenotype in three dimensional cultures and in vivo. Cancer Res 2006, 66:1526-1535. 10.1158/0008-5472.CAN-05-3071, 2933188, 16452209.
10. Nam JM, Onodera Y, Bissell MJ, Park CC. Breast cancer cells in three-dimensional culture display an enhanced radioresponse after coordinate targeting of integrin alpha5beta1 and fibronectin. Cancer Res 2010, 70:5238-5248. 10.1158/0008-5472.CAN-09-2319, 2933183, 20516121.
11. Ahmed KM, Dong S, Fan M, Li JJ. Nuclear factor-kappaB p65 inhibits mitogen-activated protein kinase signaling pathway in radioresistant breast cancer cells. Mol Cancer Res 2006, 4:945-955. 10.1158/1541-7786.MCR-06-0291, 17189385.
12. Cao N, Li S, Wang Z, Ahmed KM, Degnan ME, Fan M, Dynlacht JR, Li JJ. NF-kappaB-mediated HER2 overexpression in radiation-adaptive resistance. Radiat Res 2009, 171:9-21. 10.1667/RR1472.1, 2659759, 19138055.
13. Brach MA, Hass R, Sherman ML, Gunji H, Weichselbaum R, Kufe D. Ionizing radiation induces expression and binding activity of the nuclear factor kappa B. J Clin Invest 1991, 88:691-695. 10.1172/JCI115354, 295415, 1864978.
14. Bhoopathi P, Chetty C, Kunigal S, Vanamala SK, Rao JS, Lakka SS. Blockade of tumor growth due to matrix metalloproteinase-9 inhibition is mediated by sequential activation of beta1-integrin, ERK, and NF-kappaB. J Biol Chem 2008, 283:1545-1552. 2206181, 17991734.
15. Holmes KM, Annala M, Chua CY, Dunlap SM, Liu Y, Hugen N, Moore LM, Cogdell D, Hu L, Nykter M, Hess K, Fuller GN, Zhang W. Insulin-like growth factor-binding protein 2-driven glioma progression is prevented by blocking a clinically significant integrin, integrin-linked kinase, and NF-kappaB network. Proc Natl Acad Sci USA 2012, 109:3475-3480. 10.1073/pnas.1120375109, 3295320, 22345562.
16. Sil H, Sen T, Chatterjee A. Fibronectin-integrin (alpha5beta1) modulates migration and invasion of murine melanoma cell line B16F10 by involving MMP-9. Oncol Res 2011, 19:335-348. 10.3727/096504011X13079697132925, 21936403.
17. Ahmed KM, Zhang H, Park CC. NF-kappaB regulates radioresistance mediated by beta1-integrin in three-dimensional culture of breast cancer cells. Cancer Res 2013, 73:3737-3748. 10.1158/0008-5472.CAN-12-3537, 23576567.
18. Debnath J, Walker SJ, Brugge JS. Akt activation disrupts mammary acinar architecture and enhances proliferation in an mTOR-dependent manner. J Cell Biol 2003, 163:315-326. 10.1083/jcb.200304159, 2173511, 14568991.
19. Behbod F, Kittrell FS, LaMarca H, Edwards D, Kerbawy S, Heestand JC, Young E, Mukhopadhyay P, Yeh HW, Allred DC, Hu M, Polyak K, Rosen JM, Medina D. An intraductal human-in-mouse transplantation model mimics the subtypes of ductal carcinoma in situ. Breast Cancer Res 2009, 11:R66. 10.1186/bcr2358, 2790841, 19735549.
20. Debnath J, Muthuswamy SK, Brugge JS. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 2003, 30:256-268. 10.1016/S1046-2023(03)00032-X, 12798140.
21. Lee GY, Kenny PA, Lee EH, Bissell MJ. Three-dimensional culture models of normal and malignant breast epithelial cells. Nat Methods 2007, 4:359-365. 10.1038/nmeth1015, 2933182, 17396127.
22. Nam JM, Onodera Y, Mazaki Y, Miyoshi H, Hashimoto S, Sabe H. CIN85, a Cbl-interacting protein, is a component of AMAP1-mediated breast cancer invasion machinery. EMBO J 2007, 26:647-656. 10.1038/sj.emboj.7601534, 1794391, 17255943.
23. Park CC, Georgescu W, Polyzos A, Pham C, Ahmed KM, Zhang H, Costes SV. Rapid and automated multidimensional fluorescence microscopy profiling of 3D human breast cultures. Integr Biol 2013, 5:681-691.
24. Bose S, Chandran S, Mirocha JM, Bose N. The Akt pathway in human breast cancer: a tissue-array-based analysis. Mod Pathol 2006, 19:238-245. 10.1038/modpathol.3800525, 16341149.
25. Yao ES, Zhang H, Chen YY, Lee B, Chew K, Moore D, Park C. Increased beta1 integrin is associated with decreased survival in invasive breast cancer. Cancer Res 2007, 67:659-664. 10.1158/0008-5472.CAN-06-2768, 17234776.
26. Maity G, Choudhury PR, Sen T, Ganguly KK, Sil H, Chatterjee A. Culture of human breast cancer cell line (MDA-MB-231) on fibronectin-coated surface induces pro-matrix metalloproteinase-9 expression and activity. Tumour Biol 2011, 32:129-138. 10.1007/s13277-010-0106-9, 20821288.
27. Meineke V, Gilbertz KP, Schilperoort K, Cordes N, Sendler A, Moede T, van Beuningen D. Ionizing radiation modulates cell surface integrin expression and adhesion of COLO-320 cells to collagen and fibronectin in vitro. Strahlenther Onkol 2002, 178:709-714. 10.1007/s00066-002-0993-9, 12491059.
28. Cordes N, Seidler J, Durzok R, Geinitz H, Brakebusch C. beta1-integrin-mediated signaling essentially contributes to cell survival after radiation-induced genotoxic injury. Oncogene 2006, 25:1378-1390. 10.1038/sj.onc.1209164, 16247454.
29. Cordes N, Blaese MA, Plasswilm L, Rodemann HP, Van Beuningen D. Fibronectin and laminin increase resistance to ionizing radiation and the cytotoxic drug Ukrain in human tumour and normal cells in vitro. Int J Radiat Biol 2003, 79:709-720. 10.1080/09553000310001610240, 14703944.
30. Nam JM, Chung Y, Hsu HC, Park CC. beta1 integrin targeting to enhance radiation therapy. Int J Radiat Biol 2009, 85:923-928. 10.3109/09553000903232876, 19895268.
31. Park CC, Zhang HJ, Yao ES, Park CJ, Bissell MJ. Beta1 integrin inhibition dramatically enhances radiotherapy efficacy in human breast cancer xenografts. Cancer Res 2008, 68:4398-4405. 10.1158/0008-5472.CAN-07-6390, 3719863, 18519702.
32. Sen T, Dutta A, Maity G, Chatterjee A. Fibronectin induces matrix metalloproteinase-9 (MMP-9) in human laryngeal carcinoma cells by involving multiple signaling pathways. Biochimie 2010, 92:1422-1434. 10.1016/j.biochi.2010.07.005, 20638438.
33. Deryugina EI, Quigley JP. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev 2006, 25:9-34. 10.1007/s10555-006-7886-9, 16680569.
34. Stetler-Stevenson WG. Matrix metalloproteinases in angiogenesis: a moving target for therapeutic intervention. J Clin Invest 1999, 103:1237-1241. 10.1172/JCI6870, 408361, 10225966.
35. Sun Y, Lu N, Ling Y, Gao Y, Chen Y, Wang L, Hu R, Qi Q, Liu W, Yang Y, You Q, Guo Q. Oroxylin A suppresses invasion through down-regulating the expression of matrix metalloproteinase-2/9 in MDA-MB-435 human breast cancer cells. Eur J Pharmacol 2009, 603:22-28. 10.1016/j.ejphar.2008.12.008, 19100732.
36. Kim ES, Kim JS, Kim SG, Hwang S, Lee CH, Moon A. Sphingosine 1-phosphate regulates matrix metalloproteinase-9 expression and breast cell invasion through S1P3-Galphaq coupling. J Cell Sci 2011, 124:2220-2230. 10.1242/jcs.076794, 21652634.
37. Biswas DK, Iglehart JD. Linkage between EGFR family receptors and nuclear factor kappaB (NF-kappaB) signaling in breast cancer. J Cell Physiol 2006, 209:645-652. 10.1002/jcp.20785, 17001676.
38. Sovak MA, Bellas RE, Kim DW, Zanieski GJ, Rogers AE, Traish AM, Sonenshein GE. Aberrant nuclear factor-kappaB/Rel expression and the pathogenesis of breast cancer. J Clin Invest 1997, 100:2952-2960. 10.1172/JCI119848, 508506, 9399940.
39. Wu JT, Kral JG. The NF-kappaB/IkappaB signaling system: a molecular target in breast cancer therapy. J Surg Res 2005, 123:158-169. 10.1016/j.jss.2004.06.006, 15652965.