The functional role of notch signaling in triple-negative breast cancer

Vitamins and Hormones

Volumn 93, Issue , 2013, Pages 277-306

  Speiser, Jodi J ^a   Erşahin, Çaǧatay ^a   Osipo, Clodia ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

Breast cancer; Gamma secretase inhibitor; Notch 1; Notch 4; Triple negative

Indexed keywords

EID: 84880274930     PISSN: 00836729     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-416673-8.00013-7     Document Type: Chapter

References (158)

1. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proceedings of the National Academy of Sciences of the United States of America 2003, 100(7):3983-3988. 10.1073/pnas.0530291100.
2. Alimirah F., Panchanathan R., Davis F.J., Chen J., Choubey D. Restoration of p53 expression in human cancer cell lines upregulates the expression of Notch1: Implications for cancer cell fate determination after genotoxic stress. Neoplasia 2007, 9(5):427-434.
3. Allred D.C., Harvey J.M., Berardo M., Clark G.M. Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Modern Pathology: An Official Journal of the United States and Canadian Academy of Pathology, Inc. 1998, 11(2):155-168.
4. Angel P., Karin M. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochimica et Biophysica Acta 1991, 1072(2-3):129-157.
5. Bauer K.R., Brown M., Cress R.D., Parise C.A., Caggiano V. Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple negative phenotype. Cancer 2007, 109(9):1721-1728.
6. Benbow U., Brinckerhoff C.E. The AP-1 site and MMP gene regulation: What is all the fuss about?. Matrix Biology: Journal of the International Society for Matrix Biology 1997, 15(8-9):519-526.
7. Berrada N., Delaloge S., Andre F. Treatment of triple-negative metastatic breast cancer: Toward individualized targeted treatments or chemosensitization?. Annals of Oncology: Official Journal of the European Society for Medical Oncology/ESMO 2010, 21(Suppl. 7):vii30-vii35. (Review). 10.1093/annonc/mdq279.
8. Beverly L.J., Felsher D.W., Capobianco A.J. Suppression of p53 by Notch in lymphomagenesis: Implications for initiation and regression. Cancer Research 2005, 65(16):7159-7168. 10.1158/0008-5472.CAN-05-1664.
9. Bieche I., Tozlu S., Girault I., Onody P., Driouch K., Vidaud M., et al. Expression of PEA3/E1AF/ETV4, an Ets-related transcription factor, in breast tumors: Positive links to MMP2, NRG1 and CGB expression. Carcinogenesis 2004, 25(3):405-411. 10.1093/carcin/bgh024.
10. Blaumueller C.M., Artiavanis-Tsakonas S. Comparative aspects of Notch signaling in lower and higher eukaryotes. Perspectives on Developmental Neurobiology 1997, 4:325-343.
11. Bojovic B.B., Hassell J.A. The transactivation function of the Pea3 subfamily Ets transcription factors is regulated by sumoylation. DNA and Cell Biology 2008, 27(6):289-305. 10.1089/dna.2007.0680.
12. Bolton J.L., Thatcher G.R. Potential mechanisms of estrogen quinone carcinogenesis. Chemical Research in Toxicology 2008, 21(1):93-101. 10.1021/tx700191p.
13. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nature Medicine 1997, 3(7):730-737.
14. Brennan K., Brown A.M. Is there a role for Notch signalling in human breast cancer?. Breast Cancer Research: BCR 2003, 5(2):69-75.
15. Brou C., Logeat F., Gupta N., Bessia C., LeBail O., Doedens J.R., et al. A novel proteolytic cleavage involved in Notch signaling: The role of the disintegrin-metalloprotease TACE. Molecular Cell 2000, 5(2):207-216.
16. Callahan R., Raafat A. Notch signaling in mammary gland tumorigenesis. Journal of Mammary Gland Biology and Neoplasia 2001, 6(1):23-36. (Review).
17. Chang E.C., Frasor J., Komm B., Katzenellenbogen B.S. Impact of estrogen receptor beta on gene networks regulated by estrogen receptor alpha in breast cancer cells. Endocrinology 2006, 147(10):4831-4842. 10.1210/en.2006-0563.
18. Chang J., Landis M., Schott A., Pavlick A., Dobrolecki L., Korkaya H., et al. Targeting intrinsically-resistant breast cancer stem cells with gamma-secretase inhibitors. Cancer Research 2009, 69(24). Suppliment 3.
19. Cheang M.C., Voduc D., Bajdik C., Leung S., McKinney S., Chia S.K., et al. Basal-like breast cancer defined by five biomarkers has superior prognostic value than triple-negative phenotype. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2008, 14(5):1368-1376. 10.1158/1078-0432.CCR-07-1658.
20. Chen Y., Fischer W.H., Gill G.N. Regulation of the ERBB-2 promoter by RBPJkappa and NOTCH. The Journal of Biological Chemistry 1997, 272(22):14110-14114.
21. Chen J.Q., Russo J. ERalpha-negative and triple negative breast cancer: Molecular features and potential therapeutic approaches. Biochimica et Biophysica Acta 2009, 1796(2):162-175. 10.1016/j.bbcan.2009.06.003.
22. Clementz A.G., Rogowski A., Pandya K., Miele L., Osipo C. NOTCH-1 and NOTCH-4 are novel gene targets of PEA3 in breast cancer: Novel therapeutic implications. Breast Cancer Research: BCR 2011, 13(3):R63. 10.1186/bcr2900.
23. Colditz G.A., Rosner B. Cumulative risk of breast cancer to age 70 years according to risk factor status: Data from the Nurses' Health Study. American Journal of Epidemiology 2000, 152(10):950-964.
24. Conforti R., Boulet T., Tomasic G., Taranchon E., Arriagada R., Spielmann M., et al. Breast cancer molecular subclassification and estrogen receptor expression to predict efficacy of adjuvant anthracyclines-based chemotherapy: A biomarker study from two randomized trials. Annals of Oncology: Official Journal of the European Society for Medical Oncology/ESMO 2007, 18(9):1477-1483. 10.1093/annonc/mdm209.
25. Curran T., Franza B.R. Fos and Jun: The AP-1 connection. Cell 1988, 55(3):395-397. (Review).
26. Davidson B., Goldberg I., Tell L., Vigdorchik S., Baekelandt M., Berner A., et al. The clinical role of the PEA3 transcription factor in ovarian and breast carcinoma in effusions. Clinical & Experimental Metastasis 2004, 21(3):191-199.
27. Dent R., Trudeau M., Pritchard K.I., Hanna W.M., Kahn H.K., Sawka C.A., et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clinical Cancer Research 2007, 13:4429-4434.
28. Diaz L.K., Cryns V.L., Symmans W.F., Sneige N. Triple negative breast carcinoma and the basal phenotype: From expression profiling to clinical practice. Advances in Anatomic Pathology 2007, 14(6):419-430. 10.1097/PAP.0b013e3181594733.
29. Dickson B.C., Mulligan A.M., Zhang H., Lockwood G., O'Malley F.P., Egan S.E., et al. High-level JAG1 mRNA and protein predict poor outcome in breast cancer. Modern Pathology: An Official Journal of the United States and Canadian Academy of Pathology, Inc. 2007, 20(6):685-693. 10.1038/modpathol.3800785.
30. Discenza M.T., Vaz D., Hassell J.A., Pelletier J. Activation of the WT1 tumor suppressor gene promoter by Pea3. FEBS Letters 2004, 560(1-3):183-191. 10.1016/S0014-5793(04)00104-8.
31. Dotzlaw H., Leygue E., Watson P.H., Murphy L.C. Estrogen receptor-beta messenger RNA expression in human breast tumor biopsies: Relationship to steroid receptor status and regulation by progestins. Cancer Research 1999, 59(3):529-532.
32. Dunnwald L.K., Rossing M.A., Li C.I. Hormone receptor status, tumor characteristics, and prognosis: A prospective cohort of breast cancer patients. Breast Cancer Research: BCR 2007, 9(1):R6. 10.1186/bcr1639.
33. Dunwoodie S.L., Henrique D., Harrison S.M., Beddington R.S. Mouse Dll3: a novel divergent Delta gene which may compliment the function of other Delta homologues during early pattern formation in the mouse embryo. Development 1997, 124:3065-3076.
34. Elbashir S.M., Harborth J., Lendeckel W., Yalcin A., Weber K., Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001, 411(6836):494-498. 10.1038/35078107.
35. Evans C.P., Stapp E.C., Dall'Era M.A., Juarez J., Yang J.C. Regulation of u-PA gene expression in human prostate cancer. International Journal of Cancer. Journal International Du Cancer 2001, 94(3):390-395.
36. Farnie G., Clarke R.B. Mammary stem cells and breast cancer-Role of Notch signalling. Stem Cell Reviews 2007, 3(2):169-175. (Review).
37. Fasano J., Muggia F. Breast cancer arising in a BRCA-mutated background: therapeutic implications from an animal model and drug development. Annals of Oncology 2009, 20:609-614.
38. Firlej V., Ladam F., Brysbaert G., Dumont P., Fuks F., de Launoit Y., et al. Reduced tumorigenesis in mouse mammary cancer cells following inhibition of Pea3- or Erm-dependent transcription. Journal of Cell Science 2008, 121(Pt 20):3393-3402. 10.1242/jcs.027201.
39. Fortini M.E. Notch and presenilin: A proteolytic mechanism emerges. Current Opinion in Cell Biology 2001, 13(5):627-634.
40. Fujita T., Kobayashi Y., Wada O., Tateishi Y., Kitada L., Yamamoto Y., et al. Full activation of estrogen receptor alpha activation function-1 induces proliferation of breast cancer cells. The Journal of Biological Chemistry 2003, 278(29):26704-26714. 10.1074/jbc.M301031200.
41. Fuqua S.A., Schiff R., Parra I., Moore J.T., Mohsin S.K., Osborne C.K., et al. Estrogen receptor beta protein in human breast cancer: Correlation with clinical tumor parameters. Cancer Research 2003, 63(10):2434-2439.
42. Graham J.D., Mote P.A., Salagame U., van Dijk J.H., Balleine R.L., Huschtscha L.I., et al. DNA replication licensing and progenitor numbers are increased by progesterone in normal human breast. Endocrinology 2009, 150(7):3318-3326. 10.1210/en.2008-1630.
43. Graves B.J., Petersen J.M. Specificity within the ets family of transcription factors. Advances in Cancer Research 1998, 75:1-55.
44. Hall J.M., Couse J.F., Korach K.S. The multifaceted mechanisms of estradiol and estrogen receptor signaling. The Journal of Biological Chemistry 2001, 276(40):36869-36872. (Review). 10.1074/jbc.R100029200.
45. Hammond M.E., Hayes D.F., Dowsett M., Allred D.C., Hagerty K.L., Badve S., et al. American society of clinical oncology/College Of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. Journal of Clinical Oncology: Official Journal of the American Society of Clinical Oncology 2010, 28(16):2784-2795. (Review). 10.1200/JCO.2009.25.6529.
46. Han J., Ma I., Hendzel M.J., Allalunis-Turner J. The cytotoxicity of gamma-secretase inhibitor I to breast cancer cells is mediated by proteasome inhibition, not by gamma-secretase inhibition. Breast Cancer Research: BCR 2009, 11(4):R57. 10.1186/bcr2347.
47. Harrison H., Farnie G., Howell S.J., Rock R.E., Stylianou S., Brennan K.R., et al. Regulation of breast cancer stem cell activity by signaling through the Notch4 receptor. Cancer Research 2010, 70(2):709-718. 10.1158/0008-5472.CAN-09-1681.
48. Harvey J.M., Clark G.M., Osborne C.K., Allred D.C. Estrogen receptor status by immunohistochemistry is superior to the ligand-binding assay for predicting response to adjuvant endocrine therapy in breast cancer. Journal of Clinical Oncology: Official Journal of the American Society of Clinical Oncology 1999, 17(5):1474-1481.
49. Haughian J.M., Pinto M.P., Harrell J.C., Bliesner B.S., Joensuu K.M., Dye W.W., et al. Maintenance of hormone responsiveness in luminal breast cancers by suppression of Notch. Proceedings of the National Academy of Sciences of the United States of America 2012, 109(8):2742-2747. 10.1073/pnas.1106509108.
50. Helguero L.A., Faulds M.H., Gustafsson J.A., Haldosen L.A. Estrogen receptors alfa (ERalpha) and beta (ERbeta) differentially regulate proliferation and apoptosis of the normal murine mammary epithelial cell line HC11. Oncogene 2005, 24(44):6605-6616. 10.1038/sj.onc.1208807.
51. Herynk M.H., Fuqua S.A. Estrogen receptor mutations in human disease. Endocrine Reviews 2004, 25(6):869-898. 10.1210/er.2003-0010.
52. Hesselbrock D.R., Kurpios N., Hassell J.A., Watson M.A., Fleming T.P. PEA3, AP-1, and a unique repetitive sequence all are involved in transcriptional regulation of the breast cancer-associated gene, mammaglobin. Breast Cancer Research and Treatment 2005, 89(3):289-296. 10.1007/s10549-004-2622-z.
53. Hida K., Shindoh M., Yasuda M., Hanzawa M., Funaoka K., Kohgo T., et al. Antisense E1AF transfection restrains oral cancer invasion by reducing matrix metalloproteinase activities. The American Journal of Pathology 1997, 150(6):2125-2132.
54. Hoey T., Yen W.C., Axelrod F., Basi J., Donigian L., Dylla S., et al. DLL4 blockade inhibits tumor growth and reduces tumor-initiating cell frequency. Cell Stem Cell 2009, 5(2):168-177. 10.1016/j.stem.2009.05.019.
55. Hopp T.A., Weiss H.L., Hilsenbeck S.G., Cui Y., Allred D.C., Horwitz K.B., et al. Breast cancer patients with progesterone receptor PR-A-rich tumors have poorer disease-free survival rates. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2004, 10(8):2751-2760.
56. Horwitz K.B., Dye W.W., Harrell J.C., Kabos P., Sartorius C.A. Rare steroid receptor-negative basal-like tumorigenic cells in luminal subtype human breast cancer xenografts. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(15):5774-5779. 10.1073/pnas.0706216105.
57. Hsieh J.J., Zhou S., Chen L., Young D.B., Hayward S.D. CIR, a corepressor linking the DNA binding factor CBF1 to the histone deacetylase complex. Proceedings of the National Academy of Sciences of the United States of America 1999, 96(1):23-28.
58. Hu C., Dievart A., Lupien M., Calvo E., Tremblay G., Jolicoeur P. Overexpression of activated murine Notch1 and Notch3 in transgenic mice blocks mammary gland development and induces mammary tumors. The American Journal of Pathology 2006, 168(3):973-990. 10.2353/ajpath.2006.050416.
59. Iguchi A., Kitajima I., Yamakuchi M., Ueno S., Aikou T., Kubo T., et al. PEA3 and AP-1 are required for constitutive IL-8 gene expression in hepatoma cells. Biochemical and Biophysical Research Communications 2000, 279(1):166-171. 10.1006/bbrc.2000.3925.
60. Iwao K., Miyoshi Y., Egawa C., Ikeda N., Noguchi S. Quantitative analysis of estrogen receptor-beta mRNA and its variants in human breast cancers. International Journal of Cancer. Journal International Du Cancer 2000, 88(5):733-736.
61. Iwao K., Miyoshi Y., Egawa C., Ikeda N., Tsukamoto F., Noguchi S. Quantitative analysis of estrogen receptor-alpha and -beta messenger RNA expression in breast carcinoma by real-time polymerase chain reaction. Cancer 2000, 89(8):1732-1738. 10.1002/1097-0142(20001015)89:8<1732::AID-CNCR13>3.0.CO;2-2.
62. Jarvinen T.A., Pelto-Huikko M., Holli K., Isola J. Estrogen receptor beta is coexpressed with ERalpha and PR and associated with nodal status, grade, and proliferation rate in breast cancer. The American Journal of Pathology 2000, 156(1):29-35.
63. Jensen E.V., Cheng G., Palmieri C., Saji S., Makela S., Van Noorden S., et al. Estrogen receptors and proliferation markers in primary and recurrent breast cancer. Proceedings of the National Academy of Sciences of the United States of America 2001, 98(26):15197-15202. 10.1073/pnas.211556298.
64. Jubb A.M., Soilleux E.J., Turley H., Steers G., Parker A., Low I., et al. Expression of vascular notch ligand delta-like 4 and inflammatory markers in breast cancer. The American Journal of Pathology 2010, 176(4):2019-2028. 10.2353/ajpath.2010.090908.
65. Kabos P., Haughian J.M., Wang X., Dye W.W., Finlayson C., Elias A., et al. Cytokeratin 5 positive cells represent a steroid receptor negative and therapy resistant subpopulation in luminal breast cancers. Breast Cancer Research and Treatment 2011, 128(1):45-55. 10.1007/s10549-010-1078-6.
66. Kalen M., Heikura T., Karvinen H., Nitzsche A., Weber H., Esser N., et al. Gamma-secretase inhibitor treatment promotes VEGF-A-driven blood vessel growth and vascular leakage but disrupts neovascular perfusion. PLoS One 2011, 6(4):e18709. 10.1371/journal.pone.0018709.
67. Kapila S., Xie Y., Wang W. Induction of MMP-1 (collagenase-1) by relaxin in fibrocartilaginous cells requires both the AP-1 and PEA-3 promoter sites. Orthodontics & Craniofacial Research 2009, 12(3):178-186. 10.1111/j.1601-6343.2009.01451.x.
68. Keith B., Simon M.C. Hypoxia-inducible factors, stem cells, and cancer. Cell 2007, 129(3):465-472. 10.1016/j.cell.2007.04.019.
69. Key T., Appleby P., Barnes I., Reeves G. Endogenous sex hormones and breast cancer in postmenopausal women: Reanalysis of nine prospective studies. Journal of the National Cancer Institute 2002, 94(8):606-616.
70. Kim S.H., Yin Y.I., Li Y.M., Sisodia S.S. Evidence that assembly of an active gamma-secretase complex occurs in the early compartments of the secretory pathway. The Journal of Biological Chemistry 2004, 279(47):48615-48619. 10.1074/jbc.C400396200.
71. Kinoshita J., Kitamura K., Tanaka S., Sugimachi K., Ishida M., Saeki H. Clinical significance of PEA3 in human breast cancer. Surgery 2002, 131(Suppl. 1):S222-S225.
72. Khalifeh I.M., Albarracin C., Diaz L.K., Symmans F.W., Edgerton M.E., Hwang R.F., et al. Clinical, histopatholigic, and immunohistochemical features of microglandular adenosis and transition into in situ and invasive carcinoma. The American Journal of Surgical Pathology 2008, 32:544-552.
73. Knowlden J.M., Gee J.M., Robertson J.F., Ellis I.O., Nicholson R.I. A possible divergent role for the oestrogen receptor alpha and beta subtypes in clinical breast cancer. International Journal of Cancer. Journal International Du Cancer 2000, 89(2):209-212.
74. Kondratyev M., Kreso A., Hallett R.M., Girgis-Gabardo A., Barcelon M.E., Ilieva D., et al. Gamma-secretase inhibitors target tumor-initiating cells in a mouse model of ERBB2 breast cancer. Oncogene 2012, 31(1):93-103. 10.1038/onc.2011.212.
75. Korkaya H., Paulson A., Iovino F., Wicha M.S. HER2 regulates the mammary stem/progenitor cell population driving tumorigenesis and invasion. Oncogene 2008, 27(47):6120-6130. 10.1038/onc.2008.207.
76. Korkaya H., Wicha M.S. Selective targeting of cancer stem cells: A new concept in cancer therapeutics. BioDrugs: Clinical Immunotherapeutics, Biopharmaceuticals and Gene Therapy 2007, 21(5):299-310.
77. Korkaya H., Wicha M.S. HER-2, notch, and breast cancer stem cells: Targeting an axis of evil. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2009, 15(6):1845-1847. 10.1158/1078-0432.CCR-08-3087.
78. Lange C.A., Yee D. Progesterone and breast cancer. Women's Health 2008, 4(2):151-162. (Review). 10.2217/17455057.4.2.151.
79. Lindsell C.E., Shawber C.J., Boulter J., Weinmaster G. Jagged: a mammalian ligand that activates Notch1. Cell 1995, 80:909-917.
80. Lee C.W., Raskett C.M., Prudovsky I., Altieri D.C. Molecular dependence of estrogen receptor-negative breast cancer on a notch-survivin signaling axis. Cancer Research 2008, 68(13):5273-5281. 10.1158/0008-5472.CAN-07-6673.
81. Lee C.W., Simin K., Liu Q., Plescia J., Guha M., Khan A., et al. A functional Notch-survivin gene signature in basal breast cancer. Breast Cancer Research: BCR 2008, 10(6):R97. 10.1186/bcr2200.
82. Lehmann B.D., Bauer J.A., Chen X., Sanders M.E., Chakravarthy A.B., Shyr Y., et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. Journal of Clinical Investigation 2011, 121(7):2750-2767.
83. Leygue E., Dotzlaw H., Watson P.H., Murphy L.C. Altered estrogen receptor alpha and beta messenger RNA expression during human breast tumorigenesis. Cancer Research 1998, 58(15):3197-3201.
84. Liedtke C., Mazouni C., Hess K.R., Andre F., Tordai A., Mejia J.A., et al. Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer. Journal of Clinical Oncology: Official Journal of the American Society of Clinical Oncology 2008, 26(8):1275-1281. 10.1200/JCO.2007.14.4147.
85. Lydon J.P., DeMayo F.J., Funk C.R., Mani S.K., Hughes A.R., Montgomery C.A., et al. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes & Development 1995, 9(18):2266-2278.
86. Lydon J.P., Edwards D.P. Finally! A model for progesterone receptor action in normal human breast. Endocrinology 2009, 150(7):2988-2990. 10.1210/en.2009-0383.
87. Magnifico A., Albano L., Campaner S., Delia D., Castiglioni F., Gasparini P., et al. Tumor-initiating cells of HER2-positive carcinoma cell lines express the highest oncoprotein levels and are sensitive to trastuzumab. Clinical Cancer Research: An official Journal of the American Association for Cancer Research 2009, 15(6):2010-2021. 10.1158/1078-0432.CCR-08-1327.
88. Maier M.M., Gessler M. Comparative analysis of the human and mouse Hey1 promoter: Hey genes are new Notch target genes. Biochemical and Biophysical Research Communications 2000, 275(2):652-660. 10.1006/bbrc.2000.3354.
89. Mann S., Laucirica R., Carlson N., Younes P.S., Ali N., Younes A., et al. Estrogen receptor beta expression in invasive breast cancer. Human Pathology 2001, 32(1):113-118. 10.1053/hupa.2001.21506.
90. Matsui K., Sugimori K., Motomura H., Ejiri N., Tsukada K., Kitajima I. PEA3 cooperates with c-Jun in regulation of HER2/neu transcription. Oncology Reports 2006, 16(1):153-158.
91. Matthews C.P., Colburn N.H., Young M.R. AP-1 a target for cancer prevention. Current Cancer Drug Targets 2007, 7(4):317-324.
92. Miele L. Rational targeting of Notch signaling in breast cancer. Expert Review of Anticancer Therapy 2008, 8(8):1197-1202. 10.1586/14737140.8.8.1197.
93. Miele L., Miao H., Nickoloff B.J. NOTCH signaling as a novel cancer therapeutic target. Current Cancer Drug Targets 2006, 6:313-323.
94. Miyoshi Y., Taguchi T., Gustafsson J.A., Noguchi S. Clinicopathological characteristics of estrogen receptor-beta-positive human breast cancers. Japanese Journal of Cancer Research: Gann 2001, 92(10):1057-1061.
95. Mote P.A., Bartow S., Tran N., Clarke C.L. Loss of co-ordinate expression of progesterone receptors A and B is an early event in breast carcinogenesis. Breast Cancer Research and Treatment 2002, 72(2):163-172.
96. Mote P.A., Graham J.D., Clarke C.L. Progesterone receptor isoforms in normal and malignant breast. Ernst Schering Foundation Symposium Proceedings 2007, 2007(1):77-107. (Review).
97. Nakamura T., Tsuchiya K., Watanabe M. Crosstalk between Wnt and Notch signaling in intestinal epithelial cell fate decision. Journal of Gastroenterology 2007, 42(9):705-710. 10.1007/s00535-007-2087-z.
98. Oikawa T., Yamada T. Molecular biology of the Ets family of transcription factors. Gene 2003, 303:11-34.
99. Okamoto R., Tsuchiya K., Watanabe M. Regulation of epithelial cell differentiation and regeneration in IBD. Nihon Shokakibyo Gakkai zasshi-The Japanese Journal of Gastro-Enterology 2007, 104(8):1165-1171.
100. Omoto Y., Inoue S., Ogawa S., Toyama T., Yamashita H., Muramatsu M., et al. Clinical value of the wild-type estrogen receptor beta expression in breast cancer. Cancer Letters 2001, 163(2):207-212.
101. Omoto Y., Kobayashi S., Inoue S., Ogawa S., Toyama T., Yamashita H., et al. Evaluation of oestrogen receptor beta wild-type and variant protein expression, and relationship with clinicopathological factors in breast cancers. European Journal of Cancer 2002, 38(3):380-386.
102. O'Neill C.F., Urs S., Cinelli C., Lincoln A., Nadeau R.J., Leon R., et al. Notch2 signaling induces apoptosis and inhibits human MDA-MB-231 xenograft growth. The American Journal of Pathology 2007, 171(3):1023-1036. 10.2353/ajpath.2007.061029.
103. Osborne, B. (2000). Role of Notch in regulating apoptosis in the mammary gland. Taken from Annual Grant Report DAMD17-98-1-8314, U.S. Army Medical Research and Materiel Command, Fort Detrick, Maryland.
104. Osipo C., Patel P., Rizzo P., Clementz A.G., Hao L., Golde T.E., et al. ErbB-2 inhibition activates Notch-1 and sensitizes breast cancer cells to a gamma-secretase inhibitor. Oncogene 2008, 27(37):5019-5032. 10.1038/onc.2008.149.
105. Park S.Y., Gonen M., Kim H.J., Michor F., Polyak K. Cellular and genetic diversity in the progression of in situ human breast carcinomas to an invasive phenotype. The Journal of Clinical Investigation 2010, 120(2):636-644. 10.1172/JCI40724.
106. Paruthiyil S., Parmar H., Kerekatte V., Cunha G.R., Firestone G.L., Leitman D.C. Estrogen receptor beta inhibits human breast cancer cell proliferation and tumor formation by causing a G2 cell cycle arrest. Cancer Research 2004, 64(1):423-428.
107. Perou C.M., Sorlie T., Eisen M.B., van de Rijn M., Jeffrey S.S., Rees C.A., et al. Molecular portraits of human breast tumours. Nature 2000, 406(6797):747-752. 10.1038/35021093.
108. Prat A., Parker J.S., Karginova O., Fan C., Livasy C., Herschkowitz J.I., et al. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Research: BCR 2010, 12(5):R68. 10.1186/bcr2635.
109. Rakha E.A., Elsheikh S.E., Aleskandarany M.A., Habashi H.O., Green A.R., Powe D.G., et al. Triple-negative breast cancer: Distinguishing between basal and nonbasal subtypes. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2009, 15(7):2302-2310. 10.1158/1078-0432.CCR-08-2132.
110. Rakha E.A., Reis-Filho J.S., Ellis I.O. Basal-like breast cancer: A critical review. Journal of Clinical Oncology: Official Journal of the American Society of Clinical Oncology 2008, 26(15):2568-2581. (Review). 10.1200/JCO.2007.13.1748.
111. Raouf A., Zhao Y., To K., Stingl J., Delaney A., Barbara M., et al. Transcriptome analysis of the normal human mammary cell commitment and differentiation process. Cell Stem Cell 2008, 3(1):109-118. 10.1016/j.stem.2008.05.018.
112. Reedijk M., Odorcic S., Chang L., Zhang H., Miller N., McCready D.R., et al. High-level coexpression of JAG1 and NOTCH1 is observed in human breast cancer and is associated with poor overall survival. Cancer Research 2005, 65(18):8530-8537. 10.1158/0008-5472.CAN-05-1069.
113. Reedijk M., Pinnaduwage D., Dickson B.C., Mulligan A.M., Zhang H., Bull S.B., et al. JAG1 expression is associated with a basal phenotype and recurrence in lymph node-negative breast cancer. Breast Cancer Research and Treatment 2008, 111(3):439-448. 10.1007/s10549-007-9805-3.
114. Reis-Filho J.S., Tutt A.N. Triple negative tumors: a critical review. Histopathology 2008, 52:108-118.
115. Ridgway J., Zhang G., Wu Y., Stawicki S., Liang W.C., Chanthery Y., et al. Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 2006, 444(7122):1083-1087. 10.1038/nature05313.
116. Rizzo P., Miao H., D'Souza G., Osipo C., Song L.L., Yun J., et al. Cross-talk between notch and the estrogen receptor in breast cancer suggests novel therapeutic approaches. Cancer Research 2008, 68(13):5226-5235. 10.1158/0008-5472.CAN-07-5744.
117. Roger P., Sahla M.E., Makela S., Gustafsson J.A., Baldet P., Rochefort H. Decreased expression of estrogen receptor beta protein in proliferative preinvasive mammary tumors. Cancer Research 2001, 61(6):2537-2541.
118. Ronchini C., Capobianco A.J. Induction of cyclin D1 transcription and CDK2 activity by Notch(ic): Implication for cell cycle disruption in transformation by Notch(ic). Molecular and Cellular Biology 2001, 21(17):5925-5934.
119. Ross R.K., Paganini-Hill A., Wan P.C., Pike M.C. Effect of hormone replacement therapy on breast cancer risk: Estrogen versus estrogen plus progestin. Journal of the National Cancer Institute 2000, 92(4):328-332.
120. Rouzier R., Perou C.M., Symmans W.F., Ibrahim N., Cristofanilli M., Anderson K., et al. Breast cancer molecular subtypes respond differently to preoperative chemotherapy. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2005, 11(16):5678-5685. 10.1158/1078-0432.CCR-04-2421.
121. Saxena M.T., Schroeter E.H., Mumm J.S., Kopan R. Murine notch homologs (N1-4) undergo presenilin-dependent proteolysis. The Journal of Biological Chemistry 2001, 276(43):40268-40273. 10.1074/jbc.M107234200.
122. Scarpin K.M., Graham J.D., Mote P.A., Clarke C.L. Progesterone action in human tissues: Regulation by progesterone receptor (PR) isoform expression, nuclear positioning and coregulator expression. Nuclear Receptor Signaling 2009, 7:e009. (Review). 10.1621/nrs.07009.
123. Schroeter E.H., Kisslinger J.A., Kopan R. Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 1998, 393(6683):382-386. 10.1038/30756.
124. Sharma V.M., Calvo J.A., Draheim K.M., Cunningham L.A., Hermance N., Beverly L., et al. Notch1 contributes to mouse T-cell leukemia by directly inducing the expression of c-myc. Molecular and Cellular Biology 2006, 26(21):8022-8031. 10.1128/MCB.01091-06.
125. Sharma A., Paranjape A.N., Rangarajan A., Dighe R.R. A monoclonal antibody against human Notch1 ligand-binding domain depletes subpopulation of putative breast cancer stem-like cells. Molecular Cancer Therapeutics 2012, 11(1):77-86. 10.1158/1535-7163.MCT-11-0508.
126. Sharrocks A.D. The ETS-domain transcription factor family. Nature Reviews. Molecular Cell Biology 2001, 2(11):827-837. 10.1038/35099076.
127. Shawber C., Boulter J., Lindsell C.E., Weinmaster G. Jagged2: A serrate-like gene expressed during rat embryogenesis. Developmental Biology 1996, 180(1):370-376. 10.1006/dbio.1996.0310.
128. Shepherd T.G., Kockeritz L., Szrajber M.R., Muller W.J., Hassell J.A. The pea3 subfamily ets genes are required for HER2/Neu-mediated mammary oncogenesis. Current Biology 2001, 11(22):1739-1748.
129. Skliris G.P., Carder P.J., Lansdown M.R., Speirs V. Immunohistochemical detection of ERbeta in breast cancer: Towards more detailed receptor profiling?. British Journal of Cancer 2001, 84(8):1095-1098. 10.1054/bjoc.2001.1721.
130. Skliris G.P., Leygue E., Watson P.H., Murphy L.C. Estrogen receptor alpha negative breast cancer patients: Estrogen receptor beta as a therapeutic target. The Journal of Steroid Biochemistry and Molecular Biology 2008, 109(1-2):1-10. 10.1016/j.jsbmb.2007.12.010.
131. Skliris G.P., Munot K., Bell S.M., Carder P.J., Lane S., Horgan K., et al. Reduced expression of oestrogen receptor beta in invasive breast cancer and its re-expression using DNA methyl transferase inhibitors in a cell line model. The Journal of Pathology 2003, 201(2):213-220. 10.1002/path.1436.
132. Slamon D.J., Godolphin W., Jones L.A., Holt J.A., Wong S.G., Keith D.E., et al. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 1989, 244(4905):707-712.
133. Soares R., Balogh G., Guo S., Gartner F., Russo J., Schmitt F. Evidence for the notch signaling pathway on the role of estrogen in angiogenesis. Molecular Endocrinology 2004, 18(9):2333-2343. 10.1210/me.2003-0362.
134. Soares R., Guo S., Gartner F., Schmitt F.C., Russo J. 17 beta -estradiol-mediated vessel assembly and stabilization in tumor angiogenesis requires TGF beta and EGFR crosstalk. Angiogenesis 2003, 6(4):271-281. 10.1023/B:AGEN.0000029413.32882.dd.
135. Sotiriou C., Neo S.Y., McShane L.M., Korn E.L., Long P.M., Jazaeri A., et al. Breast cancer classification and prognosis based on gene expression profiles from a population-based study. Proceedings of the National Academy of Sciences of the United States of America 2003, 100(18):10393-10398. 10.1073/pnas.1732912100.
136. Sotiriou C., Pusztai L. Gene-expression signatures in breast cancer. The New England Journal of Medicine 2009, 360(8):790-800. 10.1056/NEJMra0801289.
137. Speirs V., Parkes A.T., Kerin M.J., Walton D.S., Carleton P.J., Fox J.N., et al. Coexpression of estrogen receptor alpha and beta: Poor prognostic factors in human breast cancer?. Cancer Research 1999, 59(3):525-528.
138. Speiser J., Foreman K., Drinka E., Godellas C., Perez C., Salhadar A., et al. Notch-1 and Notch-4 biomarker expression in triple-negative breast cancer. International Journal of Surgical Pathology 2012, 20(2):139-145. 10.1177/1066896911427035.
139. Strom A., Hartman J., Foster J.S., Kietz S., Wimalasena J., Gustafsson J.A. Estrogen receptor beta inhibits 17beta-estradiol-stimulated proliferation of the breast cancer cell line T47D. Proceedings of the National Academy of Sciences of the United States of America 2004, 101(6):1566-1571. 10.1073/pnas.0308319100.
140. Subbaramaiah K., Norton L., Gerald W., Dannenberg A.J. Cyclooxygenase-2 is overexpressed in HER-2/neu-positive breast cancer: Evidence for involvement of AP-1 and PEA3. The Journal of Biological Chemistry 2002, 277(21):18649-18657. 10.1074/jbc.M111415200.
141. Takahashi A., Higashino F., Aoyagi M., Yoshida K., Itoh M., Kobayashi M., et al. E1AF degradation by a ubiquitin-proteasome pathway. Biochemical and Biophysical Research Communications 2005, 327(2):575-580. 10.1016/j.bbrc.2004.12.045.
142. Tan A.R., Swain S.M. Therapeutic strategies for triple-negative breast cancer. Cancer Journal 2008, 14(6):343-351. (Review). 10.1097/PPO.0b013e31818d839b.
143. Tower G.B., Coon C.I., Belguise K., Chalbos D., Brinckerhoff C.E. Fra-1 targets the AP-1 site/2G single nucleotide polymorphism (ETS site) in the MMP-1 promoter. European Journal of Biochemistry 2003, 270(20):4216-4225.
144. Trimble M.S., Xin J.H., Guy C.T., Muller W.J., Hassell J.A. PEA3 is overexpressed in mouse metastatic mammary adenocarcinomas. Oncogene 1993, 8(11):3037-3042.
145. van Es J.H., van Gijn M.E., Riccio O., van den Born M., Vooijs M., Begthel H., et al. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 2005, 435(7044):959-963. 10.1038/nature03659.
146. Vona-Davis L., Rose D.P., Hazard H., Howard-McNatt M., Adkins F., Partin J., et al. Triple negative breast cancer and obesity in a rural Appalachian population. Cancer Epidemiology, Biomarkers & Prevention 2008, 17:3319-3324.
147. Wasylyk B., Hagman J., Gutierrez-Hartmann A. Ets transcription factors: Nuclear effectors of the Ras-MAP-kinase signaling pathway. Trends in Biochemical Sciences 1998, 23(6):213-216.
148. Weigelt B., Baehner F.L., Reis-Filho J.S. The contribution of gene expression profiling to breast cancer classification, prognostication, and prediction: a retrospective of the last decade. The Journal of Pathology 2010, 220:263-280.
149. Weijzen S., Rizzo P., Braid M., Vaishnav R., Jonkheer S.M., Zlobin A., et al. Activation of Notch-1 signaling maintains the neoplastic phenotype in human Ras-transformed cells. Nature Medicine 2002, 8(9):979-986. 10.1038/nm754.
150. Weng A.P., Millholland J.M., Yashiro-Ohtani Y., Arcangeli M.L., Lau A., Wai C., et al. c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia/lymphoma. Genes & Development 2006, 20(15):2096-2109. 10.1101/gad.1450406.
151. Wu L., Aster J.C., Blacklow S.C., Lake R., Artavanis-Tsakonas S., Griffin J.D. MAML1, a human homologue of Drosophila mastermind, is a transcriptional co-activator for NOTCH receptors. Nature Genetics 2000, 26(4):484-489. 10.1038/82644.
152. Wu J., Iwata F., Grass J.A., Osborne C.S., Elnitski L., Fraser P., et al. Molecular determinants of NOTCH4 transcription in vascular endothelium. Molecular and Cellular Biology 2005, 25(4):1458-1474. 10.1128/MCB.25.4.1458-1474.2005.
153. Xia W.Y., Lien H.C., Wang S.C., Pan Y., Sahin A., Kuo Y.H., et al. Expression of PEA3 and lack of correlation between PEA3 and HER-2/neu expression in breast cancer. Breast Cancer Research and Treatment 2006, 98(3):295-301. 10.1007/s10549-006-9162-7.
154. Yamaguchi N., Oyama T., Ito E., Satoh H., Azuma S., Hayashi M., et al. NOTCH3 signaling pathway plays crucial roles in the proliferation of ErbB2-negative human breast cancer cells. Cancer Research 2008, 68(6):1881-1888. 10.1158/0008-5472.CAN-07-1597.
155. Yao K., Rizzo P., Rajan P., Albain K., Rychlik K., Shah S., et al. Notch-1 and notch-4 receptors as prognostic markers in breast cancer. International Journal of Surgical Pathology 2011, 19(5):607-613. 10.1177/1066896910362080.
156. Yong S.R., Pilarski R.T., Donenberg T., Shapiro C., Hammond L.S., Miller J., et al. The prevalence of BRCA-1 mutations among young women with triple -negative breast cancer. BMC Cancer 2009, 9:86.
157. Yen W., Fischer M., Lewicki J., Gurney A., Hoey T. Targeting cancer stem cells and vasculature by a novel anti-delta-like 4 ligand (DLL4) antibody for treatment of triple negative breast cancer. Cancer Research 2009, 69(24). Supplement 3.
158. Zang S., Chen F., Dai J., Guo D., Tse W., Qu X., et al. RNAi-mediated knockdown of Notch-1 leads to cell growth inhibition and enhanced chemosensitivity in human breast cancer. Oncology Reports 2010, 23(4):893-899.