Degree of Early Estrogen Response Predict Survival after Endocrine Therapy in Primary and Metastatic ER-Positive Breast Cancer
Abstract
:Simple Summary
Abstract
1. Introduction
2. Results
2.1. Estrogen Response Early Score Was Significantly Higher in the Estrogen Receptor (ER)-Positive Breast Cancer Compared with the Other Subtype, and Correlated with ESR1 but Not with ESR2 Expressions
2.2. High Estrogen Response Early Score Was Significantly Associated with Less Tumor Aggressiveness and Better Survival in ER-Positive/HER2-Negative Breast Cancer
2.3. Allograft Rejection Was the Only Gene Set that Enriched to Low Estrogen Response Early Score Breast Cancer in METABRIC and GSE96058 Cohorts
2.4. Low Estrogen Response Early Score Was Associated with High Infiltration of Both Anti- and Pro- Cancer Immune Cells as Well as B Cells in ER-Positive/HER2-Negative Breast Cancer
2.5. High Estrogen Response Early Score Was Significantly Associated with Better Response to Endocrine Therapy in ER-Positive Breast Cancer More Strongly than ESR1 Expression
2.6. High Estrogen Response Early Score Metastatic Tumors Were Significantly Associated with Better Survival in Metastatic Breast Cancer More Strongly than ESR1 Expression
3. Discussion
4. Materials and Methods
4.1. Clinical and Transcriptomic Data Collection for Breast Cancer Patients
4.2. Estimate the Estrogen Response Early Score
4.3. Gene Set Enrichment Analysis
4.4. Tumor Immune Microenvironment Analysis
4.5. Other Statistical Analyses
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
Abbreviations
References
- Spring, L.M.; Gupta, A.; Reynolds, K.L.; Gadd, M.A.; Ellisen, L.W.; Isakoff, S.J.; Moy, B.; Bardia, A. Neoadjuvant Endocrine Therapy for Estrogen Receptor-Positive Breast Cancer: A Systematic Review and Meta-analysis. JAMA Oncol. 2016, 2, 1477–1486. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Early Breast Cancer Trialists’ Collaborative Group (EBCTCG). Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: An overview of the randomised trials. Lancet 2005, 365, 1687–1717. [Google Scholar] [CrossRef]
- Hagen, K.B.; Aas, T.; Kvaløy, J.T.; Søiland, H.; Lind, R. Adherence to adjuvant endocrine therapy in postmenopausal breast cancer patients: A 5-year prospective study. Breast 2019, 44, 52–58. [Google Scholar] [CrossRef] [PubMed]
- Walsh, E.M.; Smith, K.L.; Stearns, V. Management of hormone receptor-positive, HER2-negative early breast cancer. Semin. Oncol. 2020, 47, 187–200. [Google Scholar] [CrossRef] [PubMed]
- Huiart, L.; Ferdynus, C.; Giorgi, R. A meta-regression analysis of the available data on adherence to adjuvant hormonal therapy in breast cancer: Summarizing the data for clinicians. Breast Cancer Res. Treat. 2013, 138, 325–328. [Google Scholar] [CrossRef]
- Wang, X.; Sun, Z.; Zimmermann, M.T.; Bugrim, A.; Kocher, J.P. Predict drug sensitivity of cancer cells with pathway activity inference. BMC Med Genom. 2019, 12, 15. [Google Scholar] [CrossRef] [Green Version]
- Shi, W.; Jiang, T.; Nuciforo, P.; Hatzis, C.; Holmes, E.; Harbeck, N.; Sotiriou, C.; Peña, L.; Loi, S.; Rosa, D.D.; et al. Pathway level alterations rather than mutations in single genes predict response to HER2-targeted therapies in the neo-ALTTO trial. Ann. Oncol. 2019, 30, 1018. [Google Scholar] [CrossRef]
- Tokumaru, Y.; Oshi, M.; Katsuta, E.; Yan, L.; Satyananda, V.; Matsuhashi, N.; Futamura, M.; Akao, Y.; Yoshida, K.; Takabe, K. KRAS signaling enriched triple negative breast cancer is associated with favorable tumor immune microenvironment and better survival. Am. J. Cancer Res. 2020, 10, 897–907. [Google Scholar]
- Oshi, M.; Takahashi, H.; Tokumaru, Y.; Yan, L.; Rashid, O.M.; Matsuyama, R.; Endo, I.; Takabe, K. G2M Cell Cycle Pathway Score as a Prognostic Biomarker of Metastasis in Estrogen Receptor (ER)-Positive Breast Cancer. Int. J. Mol. Sci. 2020, 21, 2921. [Google Scholar] [CrossRef] [Green Version]
- Oshi, M.; Takahashi, H.; Tokumaru, Y.; Yan, L.; Rashid, O.M.; Nagahashi, M.; Matsuyama, R.; Endo, I.; Takabe, K. The E2F Pathway Score as a Predictive Biomarker of Response to Neoadjuvant Therapy in ER+/HER2- Breast Cancer. Cells 2020, 9, 1643. [Google Scholar] [CrossRef]
- Oshi, M.; Newman, S.; Tokumaru, Y.; Yan, L.; Matsuyama, R.; Endo, I.; Nagahashi, M.; Takabe, K. Intra-Tumoral Angiogenesis Is Associated with Inflammation, Immune Reaction and Metastatic Recurrence in Breast Cancer. Int. J. Mol. Sci. 2020, 21, 6708. [Google Scholar] [CrossRef] [PubMed]
- Hänzelmann, S.; Castelo, R.; Guinney, J. GSVA: Gene set variation analysis for microarray and RNA-seq data. BMC Bioinform. 2013, 14, 7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Subramanian, A.; Tamayo, P.; Mootha, V.K.; Mukherjee, S.; Ebert, B.L.; Gillette, M.A.; Paulovich, A.; Pomeroy, S.L.; Golub, T.R.; Lander, E.S.; et al. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 2005, 102, 15545–15550. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Putnik, M.; Zhao, C.; Gustafsson, J.; Dahlman-Wright, K. Global identification of genes regulated by estrogen signaling and demethylation in MCF-7 breast cancer cells. Biochem. Biophys. Res. Commun. 2012, 426, 26–32. [Google Scholar] [CrossRef] [PubMed]
- Madak-Erdogan, Z.; Kieser, K.J.; Kim, S.H.; Komm, B.; Katzenellenbogen, J.A.; Katzenellenbogen, B.S. Nuclear and extranuclear pathway inputs in the regulation of global gene expression by estrogen receptors. Mol. Endocrinol. 2008, 22, 2116–2127. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chang, E.C.; Charn, T.H.; Park, S.H.; Helferich, W.G.; Komm, B.; Katzenellenbogen, J.A.; Katzenellenbogen, B.S. Estrogen Receptors alpha and beta as determinants of gene expression: Influence of ligand, dose, and chromatin binding. Mol. Endocrinol. 2008, 22, 1032–1043. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Musgrove, E.A.; Sergio, C.M.; Loi, S.; Inman, C.K.; Anderson, L.R.; Alles, M.C.; Pinese, M.; Caldon, C.E.; Schütte, J.; Gardiner-Garden, M.; et al. Identification of functional networks of estrogen- and c-Myc-responsive genes and their relationship to response to tamoxifen therapy in breast cancer. PLoS ONE 2008, 3, e2987. [Google Scholar] [CrossRef] [Green Version]
- Peto, R.; Davies, C.; Godwin, J.; Gray, R.; Pan, H.C.; Clarke, M.; Cutter, D.; Darby, S.; McGale, P.; Taylor, C.; et al. Comparisons between different polychemotherapy regimens for early breast cancer: Meta-analyses of long-term outcome among 100,000 women in 123 randomised trials. Lancet 2012, 379, 432–444. [Google Scholar] [CrossRef] [Green Version]
- Paik, S.; Tang, G.; Shak, S.; Kim, C.; Baker, J.; Kim, W.; Cronin, M.; Baehner, F.L.; Watson, D.; Bryant, J.; et al. Gene expression and benefit of chemotherapy in women with node-negative, estrogen receptor-positive breast cancer. J. Clin. Oncol. 2006, 24, 3726–3734. [Google Scholar] [CrossRef]
- Tang, G.; Shak, S.; Paik, S.; Anderson, S.J.; Costantino, J.P.; Geyer, C.E., Jr.; Mamounas, E.P.; Wickerham, D.L.; Wolmark, N. Comparison of the prognostic and predictive utilities of the 21-gene Recurrence Score assay and Adjuvant! for women with node-negative, ER-positive breast cancer: Results from NSABP B-14 and NSABP B-20. Breast Cancer Res. Treat. 2011, 127, 133–142. [Google Scholar] [CrossRef] [Green Version]
- AlOmeir, O.; Patel, N.; Donyai, P. Adherence to adjuvant endocrine therapy among breast cancer survivors: A systematic review and meta-synthesis of the qualitative literature using grounded theory. Support. Care Cancer 2020, 28, 5075–5084. [Google Scholar] [CrossRef] [PubMed]
- Mercatali, L.; Spadazzi, C.; Miserocchi, G.; Liverani, C.; De Vita, A.; Bongiovanni, A.; Recine, F.; Amadori, D.; Ibrahim, T. The Effect of Everolimus in an In Vitro Model of Triple Negative Breast Cancer and Osteoclasts. Int. J. Mol. Sci. 2016, 17, 1827. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rashid, O.M.; Nagahashi, M.; Ramachandran, S.; Dumur, C.; Schaum, J.; Yamada, A.; Terracina, K.P.; Milstien, S.; Spiegel, S.; Takabe, K. An improved syngeneic orthotopic murine model of human breast cancer progression. Breast Cancer Res. Treat. 2014, 147, 501–512. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nagahashi, M.; Ramachandran, S.; Kim, E.Y.; Allegood, J.C.; Rashid, O.M.; Yamada, A.; Zhao, R.; Milstien, S.; Zhou, H.; Spiegel, S.; et al. Sphingosine-1-phosphate produced by sphingosine kinase 1 promotes breast cancer progression by stimulating angiogenesis and lymphangiogenesis. Cancer Res. 2012, 72, 726–735. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rashid, O.M.; Takabe, K. Animal models for exploring the pharmacokinetics of breast cancer therapies. Expert Opin. Drug Metab. Toxicol. 2015, 11, 221–230. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Katsuta, E.; Oshi, M.; Rashid, O.M.; Takabe, K. Generating a Murine Orthotopic Metastatic Breast Cancer Model and Performing Murine Radical Mastectomy. J. Vis. Exp. JoVE 2018, 29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Katsuta, E.; DeMasi, S.C.; Terracina, K.P.; Spiegel, S.; Phan, G.Q.; Bear, H.D.; Takabe, K. Modified breast cancer model for preclinical immunotherapy studies. J. Surg. Res. 2016, 204, 467–474. [Google Scholar] [CrossRef] [Green Version]
- Berners-Price, S.J.; Gorle, A.K.; Haselhorst, T.; Katner, S.J.; Everest-Dass, A.V.; Hampton, J.D.; Peterson, E.J.; Koblinski, J.E.; Katsuta, E.; Takabe, K.; et al. Conformational Modulation of Iduronic Acid-Containing Sulfated Glycosaminoglycans by a Polynuclear Platinum Compound. Implications for Development of Antimetastatic Platinum Drugs. Angew. Chem. 2020. [Google Scholar] [CrossRef]
- Katsuta, E.; Yan, L.; Nagahashi, M.; Raza, A.; Sturgill, J.L.; Lyon, D.E.; Rashid, O.M.; Hait, N.C.; Takabe, K. Doxorubicin effect is enhanced by sphingosine-1-phosphate signaling antagonist in breast cancer. J. Surg. Res. 2017, 219, 202–213. [Google Scholar] [CrossRef]
- Rashid, O.M.; Nagahashi, M.; Ramachandran, S.; Dumur, C.I.; Schaum, J.C.; Yamada, A.; Aoyagi, T.; Milstien, S.; Spiegel, S.; Takabe, K. Is tail vein injection a relevant breast cancer lung metastasis model? J. Thorac. Dis. 2013, 5, 385–392. [Google Scholar] [CrossRef]
- Rashid, O.M.; Nagahashi, M.; Ramachandran, S.; Graham, L.; Yamada, A.; Spiegel, S.; Bear, H.D.; Takabe, K. Resection of the primary tumor improves survival in metastatic breast cancer by reducing overall tumor burden. Surgery 2013, 153, 771–778. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Katsuta, E.; Rashid, O.M.; Takabe, K. Murine breast cancer mastectomy model that predicts patient outcomes for drug development. J. Surg. Res. 2017, 219, 310–318. [Google Scholar] [CrossRef] [PubMed]
- Nagahashi, M.; Yamada, A.; Katsuta, E.; Aoyagi, T.; Huang, W.C.; Terracina, K.P.; Hait, N.C.; Allegood, J.C.; Tsuchida, J.; Yuza, K.; et al. Targeting the SphK1/S1P/S1PR1 Axis That Links Obesity, Chronic Inflammation, and Breast Cancer Metastasis. Cancer Res. 2018, 78, 1713–1725. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kawaguchi, T.; Foster, B.A.; Young, J.; Takabe, K. Current Update of Patient-Derived Xenograft Model for Translational Breast Cancer Research. J. Mammary Gland Biol. Neoplasia 2017, 22, 131–139. [Google Scholar] [CrossRef] [PubMed]
- Okano, M.; Oshi, M.; Butash, A.; Okano, I.; Saito, K.; Kawaguchi, T.; Nagahashi, M.; Kono, K.; Ohtake, T.; Takabe, K. Orthotopic Implantation Achieves Better Engraftment and Faster Growth Than Subcutaneous Implantation in Breast Cancer Patient-Derived Xenografts. J. Mammary Gland Biol. Neoplasia 2020, 25, 27–36. [Google Scholar] [CrossRef] [PubMed]
- Oshi, M.; Okano, M.; Maiti, A.; Rashid, O.M.; Saito, K.; Kono, K.; Matsuyama, R.; Endo, I.; Takabe, K. Novel Breast Cancer Brain Metastasis Patient-Derived Orthotopic Xenograft Model for Preclinical Studies. Cancers 2020, 12, 444. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gandhi, S.; Elkhanany, A.; Oshi, M.; Dai, T.; Opyrchal, M.; Mohammadpour, H.; Repasky, E.A.; Takabe, K. Contribution of Immune Cells to Glucocorticoid Receptor Expression in Breast Cancer. Int. J. Mol. Sci. 2020, 21, 4635. [Google Scholar] [CrossRef]
- Oshi, M.; Katsuta, E.; Yan, L.; Ebos, J.M.L.; Rashid, O.M.; Matsuyama, R.; Endo, I.; Takabe, K. A Novel 4-Gene Score to Predict Survival, Distant Metastasis and Response to Neoadjuvant Therapy in Breast Cancer. Cancers 2020, 12, 1148. [Google Scholar] [CrossRef]
- Oshi, M.; Newman, S.; Murthy, V.; Tokumaru, Y.; Yan, L.; Matsuyama, R.; Endo, I.; Takabe, K. ITPKC as a Prognostic and Predictive Biomarker of Neoadjuvant Chemotherapy for Triple Negative Breast Cancer. Cancers 2020, 12, 2758. [Google Scholar] [CrossRef]
- Oshi, M.; Tokumaru, Y.; Asaoka, M.; Yan, L.; Satyananda, V.; Matsuyama, R.; Matsuhashi, N.; Futamura, M.; Ishikawa, T.; Yoshida, K.; et al. M1 Macrophage and M1/M2 ratio defined by transcriptomic signatures resemble only part of their conventional clinical characteristics in breast cancer. Sci. Rep. 2020, 10, 16554. [Google Scholar] [CrossRef]
- Oshi, M.; Asaoka, M.; Tokumaru, Y.; Angarita, F.A.; Yan, L.; Matsuyama, R.; Zsiros, E.; Ishikawa, T.; Endo, I.; Takabe, K. Abundance of Regulatory T Cell (Treg) as a Predictive Biomarker for Neoadjuvant Chemotherapy in Triple-Negative Breast Cancer. Cancers 2020, 12, 3038. [Google Scholar] [CrossRef] [PubMed]
- Oshi, M.; Asaoka, M.; Tokumaru, Y.; Yan, L.; Matsuyama, R.; Ishikawa, T.; Endo, I.; Takabe, K. CD8 T Cell Score as a Prognostic Biomarker for Triple Negative Breast Cancer. Int. J. Mol. Sci. 2020, 21, 6968. [Google Scholar] [CrossRef]
- Katsuta, E.; Rashid, O.M.; Takabe, K. Fibroblasts as a Biological Marker for Curative Resection in Pancreatic Ductal Adenocarcinoma. Int. J. Mol. Sci. 2020, 21, 3890. [Google Scholar] [CrossRef] [PubMed]
- Tokumaru, Y.; Oshi, M.; Katsuta, E.; Yan, L.; Huang, J.L.; Nagahashi, M.; Matsuhashi, N.; Futamura, M.; Yoshida, K.; Takabe, K. Intratumoral Adipocyte-High Breast Cancer Enrich for Metastatic and Inflammation-Related Pathways but Associated with Less Cancer Cell Proliferation. Int. J. Mol. Sci. 2020, 21, 5744. [Google Scholar] [CrossRef] [PubMed]
- Schulze, A.; Oshi, M.; Endo, I.; Takabe, K. MYC Targets Scores Are Associated with Cancer Aggressiveness and Poor Survival in ER-Positive Primary and Metastatic Breast Cancer. Int. J. Mol. Sci. 2020, 21, 8127. [Google Scholar] [CrossRef]
- Oshi, M.; Newman, S.; Tokumaru, Y.; Yan, L.; Matsuyama, R.; Endo, I.; Katz, M.H.G.; Takabe, K. High G2M Pathway Score Pancreatic Cancer is Associated with Worse Survival, Particularly after Margin-Positive (R1 or R2) Resection. Cancers 2020, 12, 2871. [Google Scholar] [CrossRef]
- Liu, J.; Lichtenberg, T.; Hoadley, K.A.; Poisson, L.M.; Lazar, A.J.; Cherniack, A.D.; Kovatich, A.J.; Benz, C.C.; Levine, D.A.; Lee, A.V.; et al. An Integrated TCGA Pan-Cancer Clinical Data Resource to Drive High-Quality Survival Outcome Analytics. Cell 2018, 173, 400–416.e411. [Google Scholar] [CrossRef] [Green Version]
- Rueda, O.M.; Sammut, S.J.; Seoane, J.A.; Chin, S.F.; Caswell-Jin, J.L.; Callari, M.; Batra, R.; Pereira, B.; Bruna, A.; Ali, H.R.; et al. Dynamics of breast-cancer relapse reveal late-recurring ER-positive genomic subgroups. Nature 2019, 567, 399–404. [Google Scholar] [CrossRef]
- Curtis, C.; Shah, S.P.; Chin, S.F.; Turashvili, G.; Rueda, O.M.; Dunning, M.J.; Speed, D.; Lynch, A.G.; Samarajiwa, S.; Yuan, Y.; et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 2012, 486, 346–352. [Google Scholar] [CrossRef]
- Cerami, E.; Gao, J.; Dogrusoz, U.; Gross, B.E.; Sumer, S.O.; Aksoy, B.A.; Jacobsen, A.; Byrne, C.J.; Heuer, M.L.; Larsson, E.; et al. The cBio cancer genomics portal: An open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012, 2, 401–404. [Google Scholar] [CrossRef] [Green Version]
- Miller, W.R.; Larionov, A. Changes in expression of oestrogen regulated and proliferation genes with neoadjuvant treatment highlight heterogeneity of clinical resistance to the aromatase inhibitor, letrozole. Breast Cancer Res. BCR 2010, 12, R52. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Massarweh, S.; Tham, Y.L.; Huang, J.; Sexton, K.; Weiss, H.; Tsimelzon, A.; Beyer, A.; Rimawi, M.; Cai, W.Y.; Hilsenbeck, S.; et al. A phase II neoadjuvant trial of anastrozole, fulvestrant, and gefitinib in patients with newly diagnosed estrogen receptor positive breast cancer. Breast Cancer Res. Treat. 2011, 129, 819–827. [Google Scholar] [CrossRef] [Green Version]
- Sinn, B.V.; Fu, C.; Lau, R.; Litton, J.; Tsai, T.H.; Murthy, R.; Tam, A.; Andreopoulou, E.; Gong, Y.; Murthy, R.; et al. SET(ER/PR): A robust 18-gene predictor for sensitivity to endocrine therapy for metastatic breast cancer. NPJ Breast Cancer 2019, 5, 16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brueffer, C.; Vallon-Christersson, J.; Grabau†, D.; Ehinger, A.; Häkkinen, J.; Hegardt, C.; Malina, J.; Chen, Y.; Bendahl, P.-O.; Manjer, J.; et al. Clinical Value of RNA Sequencing-Based Classifiers for Prediction of the Five Conventional Breast Cancer Biomarkers: A Report From the Population-Based Multicenter Sweden Cancerome Analysis Network—Breast Initiative. JCO Precis. Oncol. 2018, 2, 1–18. [Google Scholar] [CrossRef] [PubMed]
- Liberzon, A.; Birger, C.; Thorvaldsdóttir, H.; Ghandi, M.; Mesirov, J.P.; Tamayo, P. The Molecular Signatures Database (MSigDB) hallmark gene set collection. Cell Syst. 2015, 1, 417–425. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Okano, M.; Oshi, M.; Butash, A.L.; Asaoka, M.; Katsuta, E.; Peng, X.; Qi, Q.; Yan, L.; Takabe, K. Estrogen Receptor Positive Breast Cancer with High Expression of Androgen Receptor has Less Cytolytic Activity and Worse Response to Neoadjuvant Chemotherapy but Better Survival. Int. J. Mol. Sci. 2019, 20, 2655. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Okano, M.; Oshi, M.; Butash, A.L.; Katsuta, E.; Tachibana, K.; Saito, K.; Okayama, H.; Peng, X.; Yan, L.; Kono, K.; et al. Triple-Negative Breast Cancer with High Levels of Annexin A1 Expression Is Associated with Mast Cell Infiltration, Inflammation, and Angiogenesis. Int. J. Mol. Sci. 2019, 20, 4197. [Google Scholar] [CrossRef] [Green Version]
- Takahashi, H.; Asaoka, M.; Yan, L.; Rashid, O.M.; Oshi, M.; Ishikawa, T.; Nagahashi, M.; Takabe, K. Biologically Aggressive Phenotype and Anti-cancer Immunity Counterbalance in Breast Cancer with High Mutation Rate. Sci. Rep. 2020, 10, 1852. [Google Scholar] [CrossRef] [Green Version]
- Aran, D.; Hu, Z.; Butte, A.J. xCell: Digitally portraying the tissue cellular heterogeneity landscape. Genome Biol. 2017, 18, 220. [Google Scholar] [CrossRef] [Green Version]
- Tokumaru, Y.; Katsuta, E.; Oshi, M.; Sporn, J.C.; Yan, L.; Le, L.; Matsuhashi, N.; Futamura, M.; Akao, Y.; Yoshida, K.; et al. High Expression of miR-34a Associated with Less Aggressive Cancer Biology but Not with Survival in Breast Cancer. Int. J. Mol. Sci. 2020, 21, 3045. [Google Scholar] [CrossRef]
- Tokumaru, Y.; Asaoka, M.; Oshi, M.; Katsuta, E.; Yan, L.; Narayanan, S.; Sugito, N.; Matsuhashi, N.; Futamura, M.; Akao, Y.; et al. High Expression of microRNA-143 is Associated with Favorable Tumor Immune Microenvironment and Better Survival in Estrogen Receptor Positive Breast Cancer. Int. J. Mol. Sci. 2020, 21, 3213. [Google Scholar] [CrossRef] [PubMed]
- Takahashi, H.; Oshi, M.; Asaoka, M.; Yan, L.; Endo, I.; Takabe, K. Molecular Biological Features of Nottingham Histological Grade 3 Breast Cancers. Ann. Surg. Oncol. 2020, 27, 4475–4485. [Google Scholar] [CrossRef] [PubMed]
- Smith, I.E.; Dowsett, M.; Ebbs, S.R.; Dixon, J.M.; Skene, A.; Blohmer, J.U.; Ashley, S.E.; Francis, S.; Boeddinghaus, I.; Walsh, G. Neoadjuvant treatment of postmenopausal breast cancer with anastrozole, tamoxifen, or both in combination: The Immediate Preoperative Anastrozole, Tamoxifen, or Combined with Tamoxifen (IMPACT) multicenter double-blind randomized trial. J. Clin. Oncol. 2005, 23, 5108–5116. [Google Scholar] [CrossRef] [PubMed]
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Oshi, M.; Tokumaru, Y.; Angarita, F.A.; Yan, L.; Matsuyama, R.; Endo, I.; Takabe, K. Degree of Early Estrogen Response Predict Survival after Endocrine Therapy in Primary and Metastatic ER-Positive Breast Cancer. Cancers 2020, 12, 3557. https://doi.org/10.3390/cancers12123557
Oshi M, Tokumaru Y, Angarita FA, Yan L, Matsuyama R, Endo I, Takabe K. Degree of Early Estrogen Response Predict Survival after Endocrine Therapy in Primary and Metastatic ER-Positive Breast Cancer. Cancers. 2020; 12(12):3557. https://doi.org/10.3390/cancers12123557
Chicago/Turabian StyleOshi, Masanori, Yoshihisa Tokumaru, Fernando A. Angarita, Li Yan, Ryusei Matsuyama, Itaru Endo, and Kazuaki Takabe. 2020. "Degree of Early Estrogen Response Predict Survival after Endocrine Therapy in Primary and Metastatic ER-Positive Breast Cancer" Cancers 12, no. 12: 3557. https://doi.org/10.3390/cancers12123557