Loss of BRCA1 leads to an increase in epidermal growth factor receptor expression in mammary epithelial cells, and epidermal growth factor receptor inhibition prevents estrogen receptor-negative cancers in BRCA1-mutant mice

Breast Cancer Research

Volumn 13, Issue 2, 2011, Pages

  Burga, Laura N ^a   Hu, Hai ^a   Juvekar, Ashish ^a   Tung, Nadine M ^a   Troyan, Susan L ^b   Hofstatter, Erin W ^a   Wulf, Gerburg M ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; ESTROGEN RECEPTOR; ALDEHYDE DEHYDROGENASE ISOENZYME 1; BRCA1 PROTEIN; EPIDERMAL GROWTH FACTOR; ISOENZYME; PROTEIN KINASE INHIBITOR; QUINAZOLINE DERIVATIVE; RETINAL DEHYDROGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER SURVIVAL; CONTROLLED STUDY; DISEASE FREE SURVIVAL; FEMALE; GENE REPRESSION; MOUSE; NONHUMAN; ONCOGENE; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; BREAST; C57BL MOUSE; CELL CULTURE; CELL TRANSFORMATION; CYTOLOGY; DRUG ANTAGONISM; EPITHELIUM CELL; EXPERIMENTAL NEOPLASM; GENETICS; HUMAN; METABOLISM; MOUSE MAMMARY TUMOR ONCOVIRUS; MOUSE MUTANT; RNA INTERFERENCE; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE; UDDER;

ANIMALS; BRCA1 PROTEIN; BREAST; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; EPIDERMAL GROWTH FACTOR; EPITHELIAL CELLS; FEMALE; GENES, BRCA1; GENES, P53; HUMANS; ISOENZYMES; MAMMARY GLANDS, ANIMAL; MAMMARY NEOPLASMS, EXPERIMENTAL; MAMMARY TUMOR VIRUS, MOUSE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, ESTROGEN; RETINAL DEHYDROGENASE; RNA INTERFERENCE;

EID: 84860390160     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr2850     Document Type: Article

References (60)

1. Fisher B, Costantino JP, Wickerham DL, Cecchini RS, Cronin WM, Robidoux A, Bevers TB, Kavanah MT, Atkins JN, Margolese RG, et al. Tamoxifen for the prevention of breast cancer: current status of the National Surgical Adjuvant Breast and Bowel Project P-1 study. J Natl Cancer Inst 2005, 97:1652-1662. 10.1093/jnci/dji372, 16288118.
2. Cleator S, Heller W, Coombes RC. Triple-negative breast cancer: therapeutic options. Lancet Oncol 2007, 8:235-244. 10.1016/S1470-2045(07)70074-8, 17329194.
3. Trivers KF, Lund MJ, Porter PL, Liff JM, Flagg EW, Coates RJ, Eley JW. The epidemiology of triple-negative breast cancer, including race. Cancer Causes Control 2009, 20:1071-1082. 10.1007/s10552-009-9331-1, 19343511.
4. Foulkes WD. Clinically relevant biology of hereditary breast cancer. Semin Oncol 2007, 34:379-383. 10.1053/j.seminoncol.2007.07.010, 17920891.
5. Collins LC, Martyniak AJ, Kandel MJ, Stadler ZK, Masciari S, Miron A, Richardson AL, Schnitt SJ, Garber JE. Basal Cytokeratin and Epidermal Growth Factor Receptor Expression Are Not Predictive of BRCA1 Mutation Status in Women With Triple-negative Breast Cancers. Am J Surg Pathol 2009, 33:1093-1097. 10.1097/PAS.0b013e3181b7cb7a, 19390427.
6. van der Groep P, Bouter A, van der Zanden R, Siccama I, Menko FH, Gille JJ, van Kalken C, van der Wall E, Verheijen RH, van Diest PJ. Distinction between hereditary and sporadic breast cancer on the basis of clinicopathological data. J Clin Pathol 2006, 59:611-617. 10.1136/jcp.2005.032151, 1860390, 16603649.
7. Birgisdottir V, Stefansson OA, Bodvarsdottir SK, Hilmarsdottir H, Jonasson JG, Eyfjord JE. Epigenetic silencing and deletion of the BRCA1 gene in sporadic breast cancer. Breast Cancer Res 2006, 8:R38. 10.1186/bcr1522, 1779478, 16846527.
8. Burga LNTN, Troyan SE, Bostina M, Miron A, Konstantinopoulos P, Fountzilas H, Spentzos D, Lee B, Wulf GM. Altered Differentiation and Proliferation Properties of Primary Mammary Epithelial Cells (PMECs) from BRCA1 mutation Carriers. Cancer Res 2009, 69:1273-1278. 10.1158/0008-5472.CAN-08-2954, 19190334.
9. Nishi H, Senoo M, Nishi KH, Murphy B, Rikiyama T, Matsumura Y, Habu S, Johnson AC. p53 Homologue p63 represses epidermal growth factor receptor expression. J Biol Chem 2001, 276:41717-41724. 10.1074/jbc.M101241200, 11546792.
10. Ben-Dor I, Itsykson P, Goldenberg D, Galun E, Reubinoff BE. Lentiviral vectors harboring a dual-gene system allow high and homogeneous transgene expression in selected polyclonal human embryonic stem cells. Mol Ther 2006, 14:255-267. 10.1016/j.ymthe.2006.02.010, 16632408.
11. Burga LN, Tung NM, Troyan SL, Bostina M, Konstantinopoulos PA, Fountzilas H, Spentzos D, Miron A, Yassin YA, Lee BT, Wulf GM. Altered proliferation and differentiation properties of primary mammary epithelial cells from BRCA1 mutation carriers. Cancer Res 2009, 69:1273-1278. 10.1158/0008-5472.CAN-08-2954, 3041511, 19190334.
12. Chen JZ, Grigorieff N. SIGNATURE: a single-particle selection system for molecular electron microscopy. J Struct Biol 2007, 157:168-173. 10.1016/j.jsb.2006.06.001, 16870473.
13. Carraway KL, Cerione RA. Fluorescent-labeled growth factor molecules serve as probes for receptor binding and endocytosis. Biochemistry 1993, 32:12039-12045. 10.1021/bi00096a014, 8218281.
14. Schmitz G, Wulf G, Bruning T, Assmann G. Flow-cytometric determination of high-density-lipoprotein binding sites on human leukocytes. Clin Chem 1987, 33:2195-2203.
15. Xu X, Wagner KU, Larson D, Weaver Z, Li C, Ried T, Hennighausen L, Wynshaw-Boris A, Deng CX. Conditional mutation of Brca1 in mammary epithelial cells results in blunted ductal morphogenesis and tumour formation. Nat Genet 1999, 22:37-43. 10.1038/8743, 10319859.
16. Wagner KU, Wall RJ, St-Onge L, Gruss P, Wynshaw-Boris A, Garrett L, Li M, Furth PA, Hennighausen L. Cre-mediated gene deletion in the mammary gland. Nucleic Acids Res 1997, 25:4323-4330. 10.1093/nar/25.21.4323, 147032, 9336464.
17. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA, Butel JS, Bradley A. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 1992, 356:215-221. 10.1038/356215a0, 1552940.
18. Miller FR, Soule HD, Tait L, Pauley RJ, Wolman SR, Dawson PJ, Heppner GH. Xenograft model of progressive human proliferative breast disease. J Natl Cancer Inst 1993, 85:1725-1732. 10.1093/jnci/85.21.1725, 8411256.
19. Elenbaas B, Spirio L, Koerner F, Fleming MD, Zimonjic DB, Donaher JL, Popescu NC, Hahn WC, Weinberg RA. Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev 2001, 15:50-65. 10.1101/gad.828901, 312602, 11156605.
20. Abramovitch S, Glaser T, Ouchi T, Werner H. BRCA1-Sp1 interactions in transcriptional regulation of the IGF-IR gene. FEBS Lett 2003, 541:149-154. 10.1016/S0014-5793(03)00315-6, 12706836.
21. Maor SB, Abramovitch S, Erdos MR, Brody LC, Werner H. BRCA1 suppresses insulin-like growth factor-I receptor promoter activity: potential interaction between BRCA1 and Sp1. Mol Genet Metab 2000, 69:130-136. 10.1006/mgme.1999.2958, 10720440.
22. Parvin JD. The BRCA1-dependent ubiquitin ligase, gamma-tubulin, and centrosomes. Environ Mol Mutagen 2009, 50:649-653. 10.1002/em.20475, 19274767.
23. Ma Y, Fan S, Hu C, Meng Q, Fuqua SA, Pestell RG, Tomita YA, Rosen EM. BRCA1 regulates acetylation and ubiquitination of estrogen receptor-alpha. Mol Endocrinol 24:76-90. 10.1210/me.2009-0218, 2802901, 19887647.
24. Xiang T, Ohashi A, Huang Y, Pandita TK, Ludwig T, Powell SN, Yang Q. Negative Regulation of AKT Activation by BRCA1. Cancer Res 2008, 68:10040-10044. 10.1158/0008-5472.CAN-08-3009, 2605656, 19074868.
25. Asselin-Labat ML, Shackleton M, Stingl J, Vaillant F, Forrest NC, Eaves CJ, Visvader JE, Lindeman GJ. Steroid hormone receptor status of mouse mammary stem cells. J Natl Cancer Inst 2006, 98:1011-1014. 10.1093/jnci/djj267, 16849684.
26. Burke PM, Wiley HS. Human mammary epithelial cells rapidly exchange empty EGFR between surface and intracellular pools. J Cell Physiol 1999, 180:448-460. 10.1002/(SICI)1097-4652(199909)180:3<448::AID-JCP16>3.0.CO;2-8, 10430185.
27. Agelopoulos K, Greve B, Schmidt H, Pospisil H, Kurtz S, Bartkowiak K, Andreas A, Wieczorek M, Korsching E, Buerger H, Brandt B. Selective regain of egfr gene copies in CD44+/CD24-/low breast cancer cellular model MDA-MB-468. BMC Cancer 10:78. 10.1186/1471-2407-10-78, 2841141, 20199686.
28. Wright MH, Calcagno AM, Salcido CD, Carlson MD, Ambudkar SV, Varticovski L. Brca1 breast tumors contain distinct CD44+/CD24- and CD133+ cells with cancer stem cell characteristics. Breast Cancer Res 2008, 10:R10. 10.1186/bcr1855, 2374965, 18241344.
29. Liu S, Ginestier C, Charafe-Jauffret E, Foco H, Kleer CG, Merajver SD, Dontu G, Wicha MS. BRCA1 regulates human mammary stem/progenitor cell fate. Proc Natl Acad Sci USA 2008, 105:1680-1685. 10.1073/pnas.0711613105, 2234204, 18230721.
30. Schmidt-Glenewinkel H, Reinz E, Eils R, Brady NR. Systems biological analysis of epidermal growth factor receptor internalization dynamics for altered receptor levels. J Biol Chem 2009, 284:17243-17252. 10.1074/jbc.M809586200, 2719361, 19297331.
31. Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH, Asselin-Labat ML, Gyorki DE, Ward T, Partanen A, et al. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med 2009, 15:907-913. 10.1038/nm.2000, 19648928.
32. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007, 1:555-567. 10.1016/j.stem.2007.08.014, 2423808, 18371393.
33. Pannu KK, Joe ET, Iyer SB. Performance evaluation of QuantiBRITE phycoerythrin beads. Cytometry 2001, 45:250-258. 10.1002/1097-0320(20011201)45:4<250::AID-CYTO10021>3.0.CO;2-T, 11746094.
34. Brodie SG, Xu X, Qiao W, Li WM, Cao L, Deng CX. Multiple genetic changes are associated with mammary tumorigenesis in Brca1 conditional knockout mice. Oncogene 2001, 20:7514-7523. 10.1038/sj.onc.1204929, 11709723.
35. Higgins B, Kolinsky K, Smith M, Beck G, Rashed M, Adames V, Linn M, Wheeldon E, Gand L, Birnboeck H, Hoffmann G. Antitumor activity of erlotinib (OSI-774, Tarceva) alone or in combination in human non-small cell lung cancer tumor xenograft models. Anticancer Drugs 2004, 15:503-512. 10.1097/01.cad.0000127664.66472.60, 15166626.
36. Ludwig T, Fisher P, Ganesan S, Efstratiadis A. Tumorigenesis in mice carrying a truncating Brca1 mutation. Genes Dev 2001, 15:1188-1193. 10.1101/gad.879201, 313794, 11358863.
37. Shah C, Miller TW, Wyatt SK, McKinley ET, Olivares MG, Sanchez V, Nolting DD, Buck JR, Zhao P, Ansari MS, et al. Imaging biomarkers predict response to anti-HER2 (ErbB2) therapy in preclinical models of breast cancer. Clin Cancer Res 2009, 15:4712-4721. 10.1158/1078-0432.CCR-08-2635, 2819132, 19584166.
38. Furuta S, Jiang X, Gu B, Cheng E, Chen PL, Lee WH. Depletion of BRCA1 impairs differentiation but enhances proliferation of mammary epithelial cells. Proc Natl Acad Sci USA 2005, 102:9176-9181. 10.1073/pnas.0503793102, 1166629, 15967981.
39. Shukla V, Coumoul X, Cao L, Wang RH, Xiao C, Xu X, Ando S, Yakar S, Leroith D, Deng C. Absence of the full-length breast cancer-associated gene-1 leads to increased expression of insulin-like growth factor signaling axis members. Cancer Res 2006, 66:7151-7157. 10.1158/0008-5472.CAN-05-4570, 16849561.
40. Xu J, Thompson KL, Shephard LB, Hudson LG, Gill GN. T3 receptor suppression of Sp1-dependent transcription from the epidermal growth factor receptor promoter via overlapping DNA-binding sites. J Biol Chem 1993, 268:16065-16073.
41. Chen Y, Farmer AA, Chen CF, Jones DC, Chen PL, Lee WH. BRCA1 is a 220-kDa nuclear phosphoprotein that is expressed and phosphorylated in a cell cycle-dependent manner. Cancer Res 1996, 56:3168-3172.
42. Kiyokawa N, Lee EK, Karunagaran D, Lin SY, Hung MC. Mitosis-specific negative regulation of epidermal growth factor receptor, triggered by a decrease in ligand binding and dimerization, can be overcome by overexpression of receptor. J Biol Chem 1997, 272:18656-18665. 10.1074/jbc.272.30.18656, 9228035.
43. Maor S, Yosepovich A, Papa MZ, Yarden RI, Mayer D, Friedman E, Werner H. Elevated insulin-like growth factor-I receptor (IGF-IR) levels in primary breast tumors associated with BRCA1 mutations. Cancer Lett 2007, 257:236-243. 10.1016/j.canlet.2007.07.019, 17766039.
44. Razandi M, Pedram A, Rosen EM, Levin ER. BRCA1 inhibits membrane estrogen and growth factor receptor signaling to cell proliferation in breast cancer. Mol Cell Biol 2004, 24:5900-5913. 10.1128/MCB.24.13.5900-5913.2004, 480898, 15199145.
45. Yan Y, Haas JP, Kim M, Sgagias MK, Cowan KH. BRCA1-induced apoptosis involves inactivation of ERK1/2 activities. J Biol Chem 2002, 277:33422-33430. 10.1074/jbc.M201147200, 12082091.
46. Kauff ND, Brogi E, Scheuer L, Pathak DR, Borgen PI, Hudis CA, Offit K, Robson ME. Epithelial lesions in prophylactic mastectomy specimens from women with BRCA mutations. Cancer 2003, 97:1601-1608. 10.1002/cncr.11225, 12655515.
47. van der Groep P, van Diest PJ, Menko FH, Bart J, de Vries EG, van der Wall E. Molecular profile of ductal carcinoma in situ of the breast in BRCA1 and BRCA2 germline mutation carriers. J Clin Pathol 2009, 62:926-930. 10.1136/jcp.2009.065524, 19541683.
48. Klijn JG, Berns PM, Schmitz PI, Foekens JA. The clinical significance of epidermal growth factor receptor (EGF-R) in human breast cancer: a review on 5232 patients. Endocr Rev 1992, 13:3-17.
49. Fox SB, Harris AL. The epidermal growth factor receptor in breast cancer. J Mammary Gland Biol Neoplasia 1997, 2:131-141. 10.1023/A:1026399613946, 10882299.
50. Rampaul RS, Pinder SE, Nicholson RI, Gullick WJ, Robertson JF, Ellis IO. Clinical value of epidermal growth factor receptor expression in primary breast cancer. Adv Anat Pathol 2005, 12:271-273. 10.1097/01.pap.0000184178.43048.80, 16210923.
51. Gee JM, Hutcheson IR. Understanding endocrine resistance: the critical need for sequential samples from clinical breast cancer and novel in vitro models. Breast Cancer Res 2005, 7:187-189. 10.1186/bcr1289, 1242147, 16168136.
52. Dickler MN, Cobleigh MA, Miller KD, Klein PM, Winer EP. Efficacy and safety of erlotinib in patients with locally advanced or metastatic breast cancer. Breast Cancer Res Treat 2009, 115:115-121. 10.1007/s10549-008-0055-9, 18496750.
53. Guix M, Granja Nde M, Meszoely I, Adkins TB, Wieman BM, Frierson KE, Sanchez V, Sanders ME, Grau AM, Mayer IA, et al. Short preoperative treatment with erlotinib inhibits tumor cell proliferation in hormone receptor-positive breast cancers. J Clin Oncol 2008, 26:897-906. 10.1200/JCO.2007.13.5939, 18180460.
54. Lu C, Speers C, Zhang Y, Xu X, Hill J, Steinbis E, Celestino J, Shen Q, Kim H, Hilsenbeck S, et al. Effect of epidermal growth factor receptor inhibitor on development of estrogen receptor-negative mammary tumors. J Natl Cancer Inst 2003, 95:1825-1833.
55. Li Y, Brown PH. Prevention of ER-negative breast cancer. Recent Results Cancer Res 2009, 181:121-134. full_text, 19213564.
56. Strecker TE, Shen Q, Zhang Y, Hill JL, Li Y, Wang C, Kim HT, Gilmer TM, Sexton KR, Hilsenbeck SG, et al. Effect of lapatinib on the development of estrogen receptor-negative mammary tumors in mice. J Natl Cancer Inst 2009, 101:107-113. 10.1093/jnci/djn436, 2639315, 19141783.
57. Lenferink AE, Simpson JF, Shawver LK, Coffey RJ, Forbes JT, Arteaga CL. Blockade of the epidermal growth factor receptor tyrosine kinase suppresses tumorigenesis in MMTV/Neu + MMTV/TGF-alpha bigenic mice. Proc Natl Acad Sci USA 2000, 97:9609-9614. 10.1073/pnas.160564197, 16912, 10931950.
58. Rhee J, Oishi K, Garey J, Kim E. Management of rash and other toxicities in patients treated with epidermal growth factor receptor-targeted agents. Clin Colorectal Cancer 2005, 5(Suppl 2):S101-106. 10.3816/CCC.2005.s.014, 16336749.
59. Afaq F, Zaman N, Khan N, Syed DN, Sarfaraz S, Zaid MA, Mukhtar H. Inhibition of epidermal growth factor receptor signaling pathway by delphinidin, an anthocyanidin in pigmented fruits and vegetables. Int J Cancer 2008, 123:1508-1515. 10.1002/ijc.23675, 18623129.
60. Zhang Y, Vareed SK, Nair MG. Human tumor cell growth inhibition by nontoxic anthocyanidins, the pigments in fruits and vegetables. Life Sci 2005, 76:1465-1472. 10.1016/j.lfs.2004.08.025, 15680311.