Molecular Biomarkers Predict Pathological Complete Response of Neoadjuvant Chemotherapy in Breast Cancer Patients: Review
Abstract
:Simple Summary
Abstract
1. Introduction
2. Genomic: DNA as Biomarkers of NAC Response in BC Patients
2.1. DNA Mutation
2.2. DNA Methylation
2.3. Circulating Tumor DNA
3. Transcriptomic: mRNA and miRNAs as Biomarkers of NAC Response in BC Patients
3.1. Gene Expression Panels
3.2. Differentially Expressed miRNA
4. Proteomic: Proteins as Biomarkers of NAC Response in BC Patients
5. Final Considerations
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global Cancer Statistics 2018: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J. Clin. 2018, 68, 394–424. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Harbeck, N.; Penault-Llorca, F.; Cortes, J.; Gnant, M.; Houssami, N.; Poortmans, P.; Ruddy, K.; Tsang, J.; Cardoso, F. Breast Cancer. Nat. Rev. Dis. Primers 2019, 5, 66. [Google Scholar] [CrossRef] [PubMed]
- Li, C.I.; Uribe, D.J.; Daling, J.R. Clinical Characteristics of Different Histologic Types of Breast Cancer. Br. J. Cancer 2005, 93, 1046–1052. [Google Scholar] [CrossRef]
- Prat, A.; Perou, C.M. Deconstructing the Molecular Portraits of Breast Cancer. Mol. Oncol. 2011, 5, 5–23. [Google Scholar] [CrossRef]
- Early Breast Cancer Trialists’ Collaborative Group (EBCTCG). Long-Term Outcomes for Neoadjuvant versus Adjuvant Chemotherapy in Early Breast Cancer: Meta-Analysis of Individual Patient Data from Ten Randomised Trials. Lancet Oncol. 2018, 19, 27–39. [Google Scholar] [CrossRef] [Green Version]
- Kong, X.; Moran, M.S.; Zhang, N.; Haffty, B.; Yang, Q. Meta-Analysis Confirms Achieving Pathological Complete Response after Neoadjuvant Chemotherapy Predicts Favourable Prognosis for Breast Cancer Patients. Eur. J. Cancer 2011, 47, 2084–2090. [Google Scholar] [CrossRef]
- I-SPY2 Trial Consortium. Association of Event-Free and Distant Recurrence—Free Survival with Individual-Level Pathologic Complete Response in Neoadjuvant Treatment of Stages 2 and 3 Breast Cancer: Three-Year Follow-up Analysis for the I-SPY2 Adaptively Randomized Clinical Trial. JAMA Oncol. 2020, 6, 1355–1362. [Google Scholar] [CrossRef]
- Von Minckwitz, G.; Untch, M.; Blohmer, J.-U.; Costa, S.D.; Eidtmann, H.; Fasching, P.A.; Gerber, B.; Eiermann, W.; Hilfrich, J.; Huober, J.; et al. Definition and Impact of Pathologic Complete Response on Prognosis After Neoadjuvant Chemotherapy in Various Intrinsic Breast Cancer Subtypes. J. Clin. Oncol. 2012, 30, 1796–1804. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Asaoka, M.; Narui, K.; Suganuma, N.; Chishima, T.; Yamada, A.; Sugae, S.; Kawai, S.; Uenaka, N.; Teraoka, S.; Miyahara, K.; et al. Clinical and Pathological Predictors of Recurrence in Breast Cancer Patients Achieving Pathological Complete Response to Neoadjuvant Chemotherapy. Eur. J. Surg. Oncol. 2019, 45, 2289–2294. [Google Scholar] [CrossRef] [PubMed]
- Bossuyt, V.; Provenzano, E.; Symmans, W.F.; Boughey, J.C.; Coles, C.; Curigliano, G.; Dixon, J.M.; Esserman, L.J.; Fastner, G.; Kuehn, T.; et al. Recommendations for Standardized Pathological Characterization of Residual Disease for Neoadjuvant Clinical Trials of Breast Cancer by the BIG-NABCG Collaboration. Ann. Oncol. 2015, 26, 1280–1291. [Google Scholar] [CrossRef]
- Symmans, W.F.; Peintinger, F.; Hatzis, C.; Rajan, R.; Kuerer, H.; Valero, V.; Assad, L.; Poniecka, A.; Hennessy, B.; Green, M.; et al. Measurement of Residual Breast Cancer Burden to Predict Survival after Neoadjuvant Chemotherapy. J. Clin. Oncol. 2007, 25, 4414–4422. [Google Scholar] [CrossRef]
- McDonald, B.R.; Contente-Cuomo, T.; Sammut, S.-J.; Odenheimer-Bergman, A.; Ernst, B.; Perdigones, N.; Chin, S.-F.; Farooq, M.; Mejia, R.; Cronin, P.A.; et al. Personalized Circulating Tumor DNA Analysis to Detect Residual Disease after Neoadjuvant Therapy in Breast Cancer. Sci. Transl. Med. 2019, 11, eaax7392. [Google Scholar] [CrossRef]
- Guan, G.; Wang, Y.; Sun, Q.; Wang, L.; Xie, F.; Yan, J.; Huang, H.; Liu, H. Utility of Urinary CtDNA to Monitoring Minimal Residual Disease in Early Breast Cancer Patients. Cancer Biomark. 2020, 28, 111–119. [Google Scholar] [CrossRef] [PubMed]
- Katayama, A.; Miligy, I.M.; Shiino, S.; Toss, M.S.; Eldib, K.; Kurozumi, S.; Quinn, C.M.; Badr, N.; Murray, C.; Provenzano, E.; et al. Predictors of Pathological Complete Response to Neoadjuvant Treatment and Changes to Post-Neoadjuvant HER2 Status in HER2-Positive Invasive Breast Cancer. Mod. Pathol. 2021, 34, 1271–1281. [Google Scholar] [CrossRef]
- Rouzier, R.; Perou, C.M.; Symmans, W.F.; Ibrahim, N.; Cristofanilli, M.; Anderson, K.; Hess, K.R.; Stec, J.; Ayers, M.; Wagner, P.; et al. Breast Cancer Molecular Subtypes Respond Differently to Preoperative Chemotherapy. Clin. Cancer Res. 2005, 11, 5678–5685. [Google Scholar] [CrossRef] [Green Version]
- Edenberg, E.R.; Downey, M.; Toczyski, D. Polymerase Stalling during Replication, Transcription and Translation. Curr. Biol. 2014, 24, R445–R452. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Banys-Paluchowski, M.; Krawczyk, N.; Fehm, T. Liquid Biopsy in Breast Cancer. Geburtshilfe Frauenheilkd 2020, 80, 1093–1104. [Google Scholar] [CrossRef] [PubMed]
- McCartney, A.; Vignoli, A.; Biganzoli, L.; Love, R.; Tenori, L.; Luchinat, C.; Leo, A.D. Metabolomics in Breast Cancer: A Decade in Review. Cancer Treat. Rev. 2018, 67, 88–96. [Google Scholar] [CrossRef]
- Wood, S.L.; Westbrook, J.A.; Brown, J.E. Omic-Profiling in Breast Cancer Metastasis to Bone: Implications for Mechanisms, Biomarkers and Treatment. Cancer Treat. Rev. 2014, 40, 139–152. [Google Scholar] [CrossRef]
- Ma, J.; Setton, J.; Lee, N.Y.; Riaz, N.; Powell, S.N. The Therapeutic Significance of Mutational Signatures from DNA Repair Deficiency in Cancer. Nat. Commun. 2018, 9, 3292. [Google Scholar] [CrossRef]
- Fasching, P.A.; Loibl, S.; Hu, C.; Hart, S.N.; Shimelis, H.; Moore, R.; Schem, C.; Tesch, H.; Untch, M.; Hilfrich, J.; et al. BRCA1/2 Mutations and Bevacizumab in the Neoadjuvant Treatment of Breast Cancer: Response and Prognosis Results in Patients With Triple-Negative Breast Cancer From the GeparQuinto Study. J. Clin. Oncol. 2018, 36, 2281–2287. [Google Scholar] [CrossRef]
- Guo, S.; Loibl, S.; von Minckwitz, G.; Darb-Esfahani, S.; Lederer, B.; Denkert, C. PIK3CA H1047R Mutation Associated with a Lower Pathological Complete Response Rate in Triple-Negative Breast Cancer Patients Treated with Anthracycline-Taxane–Based Neoadjuvant Chemotherapy. Cancer Res. Treat. 2020, 52, 689–696. [Google Scholar] [CrossRef] [PubMed] [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. 2017, 28, 128–135. [Google Scholar] [CrossRef] [PubMed]
- Glück, S.; Ross, J.S.; Royce, M.; McKenna, E.F.; Perou, C.M.; Avisar, E.; Wu, L. TP53 Genomics Predict Higher Clinical and Pathologic Tumor Response in Operable Early-Stage Breast Cancer Treated with Docetaxel-Capecitabine ± Trastuzumab. Breast Cancer Res. Treat. 2012, 132, 781–791. [Google Scholar] [CrossRef] [PubMed]
- Desmedt, C.; Di Leo, A.; de Azambuja, E.; Larsimont, D.; Haibe-Kains, B.; Selleslags, J.; Delaloge, S.; Duhem, C.; Kains, J.-P.; Carly, B.; et al. Multifactorial Approach to Predicting Resistance to Anthracyclines. J. Clin. Oncol. 2011. [Google Scholar] [CrossRef]
- Tibau, A.; López-Vilaró, L.; Pérez-Olabarria, M.; Vázquez, T.; Pons, C.; Gich, I.; Alonso, C.; Ojeda, B.; Ramón y Cajal, T.; Lerma, E.; et al. Chromosome 17 Centromere Duplication and Responsiveness to Anthracycline-Based Neoadjuvant Chemotherapy in Breast Cancer. Neoplasia 2014, 16, 861–867. [Google Scholar] [CrossRef] [Green Version]
- Kaklamani, V.G.; Jeruss, J.S.; Hughes, E.; Siziopikou, K.; Timms, K.M.; Gutin, A.; Abkevich, V.; Sangale, Z.; Solimeno, C.; Brown, K.L.; et al. Phase II Neoadjuvant Clinical Trial of Carboplatin and Eribulin in Women with Triple Negative Early-Stage Breast Cancer (NCT01372579). Breast Cancer Res. Treat. 2015, 151, 629–638. [Google Scholar] [CrossRef]
- Rodríguez-Paredes, M.; Esteller, M. Cancer Epigenetics Reaches Mainstream Oncology. Nat. Med. 2011, 17, 330–339. [Google Scholar] [CrossRef] [PubMed]
- De Almeida, B.P.; Apolónio, J.D.; Binnie, A.; Castelo-Branco, P. Roadmap of DNA Methylation in Breast Cancer Identifies Novel Prognostic Biomarkers. BMC Cancer 2019, 19, 219. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fujii, S.; Yamashita, S.; Yamaguchi, T.; Takahashi, M.; Hozumi, Y.; Ushijima, T.; Mukai, H. Pathological Complete Response of HER2-Positive Breast Cancer to Trastuzumab and Chemotherapy Can Be Predicted by HSD17B4 Methylation. Oncotarget 2017, 8, 19039–19048. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Connolly, R.M.; Fackler, M.J.; Zhang, Z.; Zhou, X.C.; Goetz, M.P.; Boughey, J.C.; Walsh, B.; Carpenter, J.T.; Storniolo, A.M.; Watkins, S.P.; et al. Tumor and Serum DNA Methylation in Women Receiving Preoperative Chemotherapy with or without Vorinostat in TBCRC008. Breast Cancer Res. Treat. 2018, 167, 107–116. [Google Scholar] [CrossRef]
- Fackler, M.J.; Umbricht, C.; Williams, D.; Argani, P.; Cruz, L.-A.; Merino, V.F.; Teo, W.W.; Zhang, Z.; Huang, P.; Visvananthan, K.; et al. Genome-Wide Methylation Analysis Identifies Genes Specific to Breast Cancer Hormone Receptor Status and Risk of Recurrence. Cancer Res. 2011, 71, 6195–6207. [Google Scholar] [CrossRef] [Green Version]
- Fackler, M.J.; Bujanda, Z.L.; Umbricht, C.; Teo, W.W.; Cho, S.; Zhang, Z.; Visvanathan, K.; Jeter, S.; Argani, P.; Wang, C.; et al. Novel Methylated Biomarkers and a Robust Assay to Detect Circulating Tumor DNA in Metastatic Breast Cancer. Cancer Res. 2014, 74, 2160–2170. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huang, Z.H.; Li, L.H.; Hua, D. Quantitative Analysis of Plasma Circulating DNA at Diagnosis and during Follow-up of Breast Cancer Patients. Cancer Lett. 2006, 243, 64–70. [Google Scholar] [CrossRef]
- Rohanizadegan, M. Analysis of Circulating Tumor DNA in Breast Cancer as a Diagnostic and Prognostic Biomarker. Cancer Genet. 2018, 228–229, 159–168. [Google Scholar] [CrossRef] [PubMed]
- Magbanua, M.J.M.; Swigart, L.B.; Wu, H.-T.; Hirst, G.L.; Yau, C.; Wolf, D.M.; Tin, A.; Salari, R.; Shchegrova, S.; Pawar, H.; et al. Circulating Tumor DNA in Neoadjuvant-Treated Breast Cancer Reflects Response and Survival. Ann. Oncol. 2021, 32, 229–239. [Google Scholar] [CrossRef] [PubMed]
- Perou, C.M.; Sørlie, T.; Eisen, M.B.; van de Rijn, M.; Jeffrey, S.S.; Rees, C.A.; Pollack, J.R.; Ross, D.T.; Johnsen, H.; Akslen, L.A.; et al. Molecular Portraits of Human Breast Tumours. Nature 2000, 406, 747–752. [Google Scholar] [CrossRef] [PubMed]
- Chang, J.C.; Hilsenbeck, S.G.; Fuqua, S.A. The Promise of Microarrays in the Management and Treatment of Breast Cancer. Breast Cancer Res. 2005, 7, 100–104. [Google Scholar] [CrossRef] [Green Version]
- Cobleigh, M.A.; Tabesh, B.; Bitterman, P.; Baker, J.; Cronin, M.; Liu, M.-L.; Borchik, R.; Mosquera, J.-M.; Walker, M.G.; Shak, S. Tumor Gene Expression and Prognosis in Breast Cancer Patients with 10 or More Positive Lymph Nodes. Clin. Cancer Res. 2005, 11, 8623–8631. [Google Scholar] [CrossRef] [Green Version]
- Cardoso, F.; van’t Veer, L.J.; Bogaerts, J.; Slaets, L.; Viale, G.; Delaloge, S.; Pierga, J.-Y.; Brain, E.; Causeret, S.; DeLorenzi, M.; et al. 70-Gene Signature as an Aid to Treatment Decisions in Early-Stage Breast Cancer. N. Engl. J. Med. 2016, 375, 717–729. [Google Scholar] [CrossRef] [Green Version]
- Filipits, M.; Rudas, M.; Jakesz, R.; Dubsky, P.; Fitzal, F.; Singer, C.F.; Dietze, O.; Greil, R.; Jelen, A.; Sevelda, P.; et al. A New Molecular Predictor of Distant Recurrence in ER-Positive, HER2-Negative Breast Cancer Adds Independent Information to Conventional Clinical Risk Factors. Clin. Cancer Res. 2011, 17, 6012–6020. [Google Scholar] [CrossRef] [Green Version]
- Nielsen, T.O.; Parker, J.S.; Leung, S.; Voduc, D.; Ebbert, M.; Vickery, T.; Davies, S.R.; Snider, J.; Stijleman, I.J.; Reed, J.; et al. A Comparison of PAM50 Intrinsic Subtyping with Immunohistochemistry and Clinical Prognostic Factors in Tamoxifen-Treated Estrogen Receptor–Positive Breast Cancer. Clin. Cancer Res. 2010, 16, 5222–5232. [Google Scholar] [CrossRef] [Green Version]
- Jerevall, P.-L.; Ma, X.-J.; Li, H.; Salunga, R.; Kesty, N.C.; Erlander, M.G.; Sgroi, D.C.; Holmlund, B.; Skoog, L.; Fornander, T.; et al. Prognostic Utility of HOXB13:IL17BR and Molecular Grade Index in Early-Stage Breast Cancer Patients from the Stockholm Trial. Br. J. Cancer 2011, 104, 1762–1769. [Google Scholar] [CrossRef]
- Yamashita, T.; Honda, M.; Kaneko, S. Application of Serial Analysis of Gene Expression in Cancer Research. Curr. Pharm. Biotechnol. 2008, 9, 375–382. [Google Scholar] [CrossRef]
- Mazo, C.; Barron, S.; Mooney, C.; Gallagher, W.M. Multi-Gene Prognostic Signatures and Prediction of Pathological Complete Response to Neoadjuvant Chemotherapy in ER-Positive, HER2-Negative Breast Cancer Patients. Cancers 2020, 12, 1133. [Google Scholar] [CrossRef] [PubMed]
- Pease, A.M.; Riba, L.A.; Gruner, R.A.; Tung, N.M.; James, T.A. Oncotype DX® Recurrence Score as a Predictor of Response to Neoadjuvant Chemotherapy. Ann. Surg. Oncol. 2019, 26, 366–371. [Google Scholar] [CrossRef]
- Iorio, M.V.; Ferracin, M.; Liu, C.-G.; Veronese, A.; Spizzo, R.; Sabbioni, S.; Magri, E.; Pedriali, M.; Fabbri, M.; Campiglio, M.; et al. MicroRNA Gene Expression Deregulation in Human Breast Cancer. Cancer Res. 2005, 65, 7065–7070. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Casey, M.; Sweeney, K.J.; Brown, J.A.L.; Kerin, M.J. Exploring Circulating Micro-RNA in the Neoadjuvant Treatment of Breast Cancer. Int. J. Cancer 2016, 139, 12–22. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Di Cosimo, S.; Appierto, V.; Pizzamiglio, S.; Silvestri, M.; Baselga, J.; Piccart, M.; Huober, J.; Izquierdo, M.; de la Pena, L.; Hilbers, F.S.; et al. Early Modulation of Circulating MicroRNAs Levels in HER2-Positive Breast Cancer Patients Treated with Trastuzumab-Based Neoadjuvant Therapy. Int. J. Mol. Sci. 2020, 21, 1386. [Google Scholar] [CrossRef] [Green Version]
- Liu, B.; Su, F.; Lv, X.; Zhang, W.; Shang, X.; Zhang, Y.; Zhang, J. Serum MicroRNA-21 Predicted Treatment Outcome and Survival in HER2-Positive Breast Cancer Patients Receiving Neoadjuvant Chemotherapy Combined with Trastuzumab. Cancer Chemother. Pharmacol. 2019, 84, 1039–1049. [Google Scholar] [CrossRef] [PubMed]
- Stevic, I.; Müller, V.; Weber, K.; Fasching, P.A.; Karn, T.; Marmé, F.; Schem, C.; Stickeler, E.; Denkert, C.; van Mackelenbergh, M.; et al. Specific MicroRNA Signatures in Exosomes of Triple-Negative and HER2-Positive Breast Cancer Patients Undergoing Neoadjuvant Therapy within the GeparSixto Trial. BMC Med. 2018, 16, 179. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cosimo, S.D.; Appierto, V.; Pizzamiglio, S.; Tiberio, P.; Iorio, M.V.; Hilbers, F.; de Azambuja, E.; de la Peña, L.; Izquierdo, M.; Huober, J.; et al. Plasma MiRNA Levels for Predicting Therapeutic Response to Neoadjuvant Treatment in HER2-Positive Breast Cancer: Results from the NeoALTTO Trial. Clin. Cancer Res. 2019, 25, 3887–3895. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- García-García, F.; Salinas-Vera, Y.M.; García-Vázquez, R.; Marchat, L.A.; Rodríguez-Cuevas, S.; López-González, J.S.; Carlos-Reyes, Á.; Ramos-Payán, R.; Aguilar-Medina, M.; Pérez-Plasencia, C.; et al. MiR-145-5p Is Associated with Pathological Complete Response to Neoadjuvant Chemotherapy and Impairs Cell Proliferation by Targeting TGFβR2 in Breast Cancer. Oncol. Rep. 2019, 41, 3527–3534. [Google Scholar] [CrossRef]
- Raychaudhuri, M.; Bronger, H.; Buchner, T.; Kiechle, M.; Weichert, W.; Avril, S. MicroRNAs MiR-7 and MiR-340 Predict Response to Neoadjuvant Chemotherapy in Breast Cancer. Breast Cancer Res. Treat. 2017, 162, 511–521. [Google Scholar] [CrossRef] [Green Version]
- Müller, V.; Gade, S.; Steinbach, B.; Loibl, S.; von Minckwitz, G.; Untch, M.; Schwedler, K.; Lübbe, K.; Schem, C.; Fasching, P.A.; et al. Changes in Serum Levels of MiR-21, MiR-210, and MiR-373 in HER2-Positive Breast Cancer Patients Undergoing Neoadjuvant Therapy: A Translational Research Project within the Geparquinto Trial. Breast Cancer Res. Treat. 2014, 147, 61–68. [Google Scholar] [CrossRef] [PubMed]
- Gasparello, J.; Allegretti, M.; Tremante, E.; Fabbri, E.; Amoreo, C.A.; Romania, P.; Melucci, E.; Messana, K.; Borgatti, M.; Giacomini, P.; et al. Liquid Biopsy in Mice Bearing Colorectal Carcinoma Xenografts: Gateways Regulating the Levels of Circulating Tumor DNA (CtDNA) and MiRNA (CtmiRNA). J. Exp. Clin. Cancer Res. 2018, 37, 124. [Google Scholar] [CrossRef] [Green Version]
- Souza, K.C.B.; Evangelista, A.F.; Leal, L.F.; Souza, C.P.; Vieira, R.A.; Causin, R.L.; Neuber, A.C.; Pessoa, D.P.; Passos, G.A.S.; Reis, R.M.V.; et al. Identification of Cell-Free Circulating MicroRNAs for the Detection of Early Breast Cancer and Molecular Subtyping. J. Oncol. 2019, 2019, 8393769. [Google Scholar] [CrossRef] [Green Version]
- Alix-Panabières, C.; Pantel, K. Clinical Applications of Circulating Tumor Cells and Circulating Tumor DNA as Liquid Biopsy. Cancer Discov. 2016, 6, 479–491. [Google Scholar] [CrossRef] [Green Version]
- Openshaw, M.R.; Page, K.; Fernandez-Garcia, D.; Guttery, D.; Shaw, J.A. The Role of CtDNA Detection and the Potential of the Liquid Biopsy for Breast Cancer Monitoring. Expert Rev. Mol. Diagn. 2016, 16, 751–755. [Google Scholar] [CrossRef]
- Denkert, C.; Liedtke, C.; Tutt, A.; von Minckwitz, G. Molecular Alterations in Triple-Negative Breast Cancer—the Road to New Treatment Strategies. Lancet 2017, 389, 2430–2442. [Google Scholar] [CrossRef] [Green Version]
- Geiger, T.; Madden, S.F.; Gallagher, W.M.; Cox, J.; Mann, M. Proteomic Portrait of Human Breast Cancer Progression Identifies Novel Prognostic Markers. Cancer Res. 2012, 72, 2428–2439. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yanovich, G.; Agmon, H.; Harel, M.; Sonnenblick, A.; Peretz, T.; Geiger, T. Clinical Proteomics of Breast Cancer Reveals a Novel Layer of Breast Cancer Classification. Cancer Res. 2018, 78, 6001–6010. [Google Scholar] [CrossRef] [Green Version]
- Mueller, C.; Haymond, A.; Davis, J.B.; Williams, A.; Espina, V. Protein Biomarkers for Subtyping Breast Cancer and Implications for Future Research. Expert Rev. Proteom. 2018, 15, 131–152. [Google Scholar] [CrossRef]
- Allred, D.C.; Harvey, J.M.; Berardo, M.; Clark, G.M. Prognostic and Predictive Factors in Breast Cancer by Immunohistochemical Analysis. Mod. Pathol. 1998, 11, 155–168. [Google Scholar] [PubMed]
- Yoshioka, T.; Hosoda, M.; Yamamoto, M.; Taguchi, K.; Hatanaka, K.C.; Takakuwa, E.; Hatanaka, Y.; Matsuno, Y.; Yamashita, H. Prognostic Significance of Pathologic Complete Response and Ki67 Expression after Neoadjuvant Chemotherapy in Breast Cancer. Breast Cancer 2015, 22, 185–191. [Google Scholar] [CrossRef] [PubMed]
- Alves, W.E.F.M.; Bonatelli, M.; Dufloth, R.; Kerr, L.M.; Carrara, G.F.A.; da Costa, R.F.A.; Scapulatempo-Neto, C.; Tiezzi, D.; da Costa Vieira, R.A.; Pinheiro, C. CAIX Is a Predictor of Pathological Complete Response and Is Associated with Higher Survival in Locally Advanced Breast Cancer Submitted to Neoadjuvant Chemotherapy. BMC Cancer 2019, 19, 1173. [Google Scholar] [CrossRef] [Green Version]
- Cerbelli, B.; Pernazza, A.; Botticelli, A.; Fortunato, L.; Monti, M.; Sciattella, P.; Campagna, D.; Mazzuca, F.; Mauri, M.; Naso, G.; et al. PD-L1 Expression in TNBC: A Predictive Biomarker of Response to Neoadjuvant Chemotherapy? BioMed Res. Int. 2017, 2017, e1750925. [Google Scholar] [CrossRef]
- Xing, M.; Wang, J.; Yang, Q.; Wang, Y.; Li, J.; Xiong, J.; Zhou, S. FKBP12 Is a Predictive Biomarker for Efficacy of Anthracycline-Based Chemotherapy in Breast Cancer. Cancer Chemother. Pharmacol. 2019, 84, 861–872. [Google Scholar] [CrossRef] [Green Version]
- Nakai, K.; Mitomi, H.; Alkam, Y.; Arakawa, A.; Yao, T.; Tokuda, E.; Saito, M.; Kasumi, F. Predictive Value of MGMT, HMLH1, HMSH2 and BRCA1 Protein Expression for Pathological Complete Response to Neoadjuvant Chemotherapy in Basal-like Breast Cancer Patients. Cancer Chemother. Pharmacol. 2012, 69, 923–930. [Google Scholar] [CrossRef]
- Chuthapisith, S.; Bean, B.E.; Cowley, G.; Eremin, J.M.; Samphao, S.; Layfield, R.; Kerr, I.D.; Wiseman, J.; El-Sheemy, M.; Sreenivasan, T.; et al. Annexins in Human Breast Cancer: Possible Predictors of Pathological Response to Neoadjuvant Chemotherapy. Eur. J. Cancer 2009, 45, 1274–1281. [Google Scholar] [CrossRef]
- Yerushalmi, R.; Woods, R.; Ravdin, P.M.; Hayes, M.M.; Gelmon, K.A. Ki67 in Breast Cancer: Prognostic and Predictive Potential. Lancet Oncol. 2010, 11, 174–183. [Google Scholar] [CrossRef]
- Dowsett, M.; Nielsen, T.O.; A’Hern, R.; Bartlett, J.; Coombes, R.C.; Cuzick, J.; Ellis, M.; Henry, N.L.; Hugh, J.C.; Lively, T.; et al. Assessment of Ki67 in Breast Cancer: Recommendations from the International Ki67 in Breast Cancer Working Group. J. Natl. Cancer Inst. 2011, 103, 1656–1664. [Google Scholar] [CrossRef] [Green Version]
- Faneyte, I.F.; Schrama, J.G.; Peterse, J.L.; Remijnse, P.L.; Rodenhuis, S.; van de Vijver, M.J. Breast Cancer Response to Neoadjuvant Chemotherapy: Predictive Markers and Relation with Outcome. Br. J. Cancer 2003, 88, 406–412. [Google Scholar] [CrossRef] [Green Version]
- Lee, H.; Ko, H.; Seol, H.; Noh, D.-Y.; Han, W.; Kim, T.-Y.; Im, S.-A.; Park, I.A. Expression of Immunohistochemical Markers before and after Neoadjuvant Chemotherapy in Breast Carcinoma, and Their Use as Predictors of Response. J. Breast Cancer 2013, 16, 395–403. [Google Scholar] [CrossRef] [Green Version]
- Botti, G.; Collina, F.; Scognamiglio, G.; Rao, F.; Peluso, V.; De Cecio, R.; Piezzo, M.; Landi, G.; De Laurentiis, M.; Cantile, M.; et al. Programmed Death Ligand 1 (PD-L1) Tumor Expression Is Associated with a Better Prognosis and Diabetic Disease in Triple Negative Breast Cancer Patients. Int. J. Mol. Sci. 2017, 18, 459. [Google Scholar] [CrossRef]
- Harding, M.W.; Galat, A.; Uehling, D.E.; Schreiber, S.L. A Receptor for the Immuno-Suppressant FK506 Is a Cis–Trans Peptidyl-Prolyl Isomerase. Nature 1989, 341, 758–760. [Google Scholar] [CrossRef]
- Schaff, L.R.; Yan, D.; Thyparambil, S.; Tian, Y.; Cecchi, F.; Rosenblum, M.; Reiner, A.S.; Panageas, K.S.; Hembrough, T.; Lin, A.L. Characterization of MGMT and EGFR Protein Expression in Glioblastoma and Association with Survival. J. Neurooncol. 2020, 146, 163–170. [Google Scholar] [CrossRef]
- Moss, S.E.; Morgan, R.O. The Annexins. Genome Biol. 2004, 5, 219. [Google Scholar] [CrossRef] [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] [PubMed] [Green Version]
- Lokman, N.A.; Ween, M.P.; Oehler, M.K.; Ricciardelli, C. The Role of Annexin A2 in Tumorigenesis and Cancer Progression. Cancer Microenviron. 2011, 4, 199–208. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Beyene, D.A.; Kanarek, N.F.; Naab, T.J.; Ricks-Santi, L.L.; Hudson, T.S. Annexin 2 Protein Expression Is Associated with Breast Cancer Subtypes in African American Women. Heliyon 2020, 6, e03241. [Google Scholar] [CrossRef]
- Cortazar, P.; Zhang, L.; Untch, M.; Mehta, K.; Costantino, J.P.; Wolmark, N.; Bonnefoi, H.; Cameron, D.; Gianni, L.; Valagussa, P.; et al. Pathological Complete Response and Long-Term Clinical Benefit in Breast Cancer: The CTNeoBC Pooled Analysis. Lancet 2014, 384, 164–172. [Google Scholar] [CrossRef] [Green Version]
- Chica-Parrado, M.R.; Godoy-Ortiz, A.; Jiménez, B.; Ribelles, N.; Barragan, I.; Alba, E. Resistance to Neoadjuvant Treatment in Breast Cancer: Clinicopathological and Molecular Predictors. Cancers 2020, 12, 2012. [Google Scholar] [CrossRef] [PubMed]
- Bianchini, G.; Kiermaier, A.; Bianchi, G.V.; Im, Y.-H.; Pienkowski, T.; Liu, M.-C.; Tseng, L.-M.; Dowsett, M.; Zabaglo, L.; Kirk, S.; et al. Biomarker Analysis of the NeoSphere Study: Pertuzumab, Trastuzumab, and Docetaxel versus Trastuzumab plus Docetaxel, Pertuzumab plus Trastuzumab, or Pertuzumab plus Docetaxel for the Neoadjuvant Treatment of HER2-Positive Breast Cancer. Breast Cancer Res. 2017, 19, 16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Harris, L.N.; Ismaila, N.; McShane, L.M.; Andre, F.; Collyar, D.E.; Gonzalez-Angulo, A.M.; Hammond, E.H.; Kuderer, N.M.; Liu, M.C.; Mennel, R.G.; et al. Use of Biomarkers to Guide Decisions on Adjuvant Systemic Therapy for Women With Early-Stage Invasive Breast Cancer: American Society of Clinical Oncology Clinical Practice Guideline. J. Clin. Oncol. 2016, 34, 1134–1150. [Google Scholar] [CrossRef] [Green Version]
- Shamai, G.; Binenbaum, Y.; Slossberg, R.; Duek, I.; Gil, Z.; Kimmel, R. Artificial Intelligence Algorithms to Assess Hormonal Status From Tissue Microarrays in Patients With Breast Cancer. JAMA Netw. Open 2019, 2, e197700. [Google Scholar] [CrossRef] [PubMed]
- Liefaard, M.C.; Lips, E.H.; Wesseling, J.; Hylton, N.M.; Lou, B.; Mansi, T.; Pusztai, L. The Way of the Future: Personalizing Treatment Plans Through Technology. Am. Soc. Clin. Oncol. Educ. Book 2021, 41, 12–23. [Google Scholar] [CrossRef] [PubMed]
- Haque, W.; Verma, V.; Hatch, S.; Suzanne Klimberg, V.; Brian Butler, E.; Teh, B.S. Response Rates and Pathologic Complete Response by Breast Cancer Molecular Subtype Following Neoadjuvant Chemotherapy. Breast Cancer Res. Treat. 2018, 170, 559–567. [Google Scholar] [CrossRef]
- Wu, H.-J.; Chu, P.-Y. Recent Discoveries of Macromolecule- and Cell-Based Biomarkers and Therapeutic Implications in Breast Cancer. Int. J. Mol. Sci. 2021, 22, 636. [Google Scholar] [CrossRef]
- Goossens, N.; Nakagawa, S.; Sun, X.; Hoshida, Y. Cancer Biomarker Discovery and Validation. Transl. Cancer Res. 2015, 4, 256–269. [Google Scholar] [CrossRef]
Author, Year | Specimens | DNA Mutation Biomarkers | NAC | IHC Subtypes (n) | Outcome | Ref. |
---|---|---|---|---|---|---|
Fasching et al., 2018 | Plasma | BRCA1/2 | Epirubicin Cyclophosphamide Docetaxel Bevacizumab | TNBC (n = 493) | pCR | [21] |
Guo et al., 2020 | FFPE | PIK3CA H1047R | Paclitaxel Doxorubicin Bevacizumab Carboplatin | TNBC (n = 92) | non-pCR | [22] |
Shi et al., 2017 | Frozen tissue | PIK3CA | Lapatinibe Trastuzumab | HER2+ (n = 207) | non-pCR | [23] |
Gluck et al., 2011 | Frozen tissue | TP53 | Capecitabine Docetaxel Trastuzumab | HER2− (n = 99) HER2+ (n = 38) | pCR | [24] |
Desmedt et al., 2011 | FFPE Frozen tissue | TOP2A | Anthracycline Epirubicin Taxanes | ER− HER2+ (n = 106) | pCR | [25] |
Tibau et al., 2014 | FFPE | TOP2A CEP17 | Fluorouracil Epirubicin Cyclophosphamide Doxorubicin Docetaxel | Non-classification (n = 140) | pCR | [26] |
Author, Year | Specimens | DNA Methylation Biomarkers | NAC | IHC Subtypes | Outcome | Ref. |
---|---|---|---|---|---|---|
Fujii et al., 2017 | FFPE | HSD17B4 | Trastuzumab Paclitaxel Anthracycline | HER2+ (n = 67) | pCR | [30] |
Connolly et al., 2018 | FFPE Serum | HIST1H3C AKR1B1 GPX7 HOXB4 TMEFF2 RASGRF2 COL6A2 ARHGEF7 TM6SF1 RASSF1A | Carboplatin Nab-paclitaxel Vorinostat | HER2− (n = 61) | non-pCR | [31] |
Panel | Techonology | Genes |
---|---|---|
Oncotype DX | RT-qPCR | ACTB; BAG1; BCL2; BIRC5; CCNB1; CD68; CTSL2; ESR1; GAPDH; GRB7; GSTM1; GUS; HER2; Ki-67; MMP11; MYBL2; PGR; RPLPO; SCUBE2; STK15; TRFC |
Mammaprint | NGS | AA555029_RC; ALDH4A1; AP2B1; AYTL2; BBC3; C16orf61; C20orf46; C9orf30; CCNE2; CDC42BPA; CDCA7; CENPA; COL4A2; DCK; DIAPH3; DTL; EBF4; ECT2; EGLN1; ESM1; EXT1; FGF18; FLT1; GMPS; GNAZ; GPR126; GPR180; GSTM3; HRASLS; IGFBP5; JHDM1D; KNTC2; LGP2; LIN9; LOC100131053; LOC100288906; LOC730018; MCM6; MELK; MMP9; MS4A7; MTDH; NMU; NUSAP1; ORC6L; OXCT1; PALM2; PECI; PITRM1; PRC1; QSCN6L1; RAB6B; RASSF7; RECQL5; RFC4; RTN4RL1; RUNDC1; SCUBE2; SERF1A; SLC2A3; STK32B; TGFB3; TSPYL5; UCHL5; WISP1; ZNF533 |
Prosigna/ PAM50 | Nanostring | ACTR3B; ANLN; BAG1; BCL2; BIRC5; BLVRA; CCNB1; CCNE1; CDC20; CDC6; CDCA1; CDH3; CENPF; CEP55; CXXC5; EGFR; ERBB2; ESR1; EXO1; FGFR4; FOXA1; FOXC1; GPR160; GRB7; KIF2C; KNTC2; KRT14; KRT17; KRT5; MAPT; MDM2; MELK; MIA; MKI-67; MLPH; MMP11; MYBL2; MYC; NAT1; ORC6L; PGR; PHGDH; PTTG1; RRM2; SFRP1; SLC39A6; TMEM45B; TYMS; UBE2C; UBE2T |
EndoPredict | RT-qPCR | AZGP1; BIRC5; CALM2; DHCR7; HBB; IL6ST; MGP; OAZ1; RBBP8; RPL37A; STC2; UBE2C |
BCI | RT-qPCR | BUB1B; CENPA; HOXB13; IL17BR; NEK2; RACGAP1; RRM2 |
Author, Year | Specimens | miRNA Biomarkers | NAC | IHC Subtypes (n) | Outcome | Ref. |
---|---|---|---|---|---|---|
Cosimo et al., 2020 | Plasma | ct-miR-148a-3p | Lapatinib Trastuzumab Paclitaxel | HER2+ (n = 52) | pCR | [49] |
ct-miR-374a-5p | ||||||
Liu et al., 2019 | Serum | ct-miR-21 | Taxotere Paraplatin Trastuzumab | HER2+ (n = 83) | non-pCR | [50] |
Stevic et al., 2018 | Plasma (exosomes) | 18 exosomal miRNAs | Paclitaxel Doxorubicin Carboplatin | HER2+ (n = 211) TNBC (n = 224) | pCR | [51] |
Cosimo et al., 2019 | Plasma | ct-miR-140-5p | Lapatinib Trastuzumab Paclitaxel | HER2+ (n = 429) | non-pCR | [52] |
García-García et al., 2019 | FFPE | miR-145-5p | Cisplatin Doxorubicin | TNBC (n = 32) | pCR | [53] |
Raychaudhuri et al., 2017 | FFPE | miR-7 | Epirrubicin Paclitaxel Cyclophosphamide Docetaxel | ER+ (n = 41) PR+ (n = 37) HER2+ (n = 36) | pCR | [54] |
miR-340 | ||||||
Müller et al., 2014 | Serum | ct-miR-21 | Lapatinib Trastuzumab | HR+ (n = 71) HER2+ (n = 127) | non-pCR | [55] |
ct-miR-210 | ||||||
ct-miR-373 |
Author, Year | Specimens | Protein Biomarkers | NAC | IHC Subtypes (n) | Outcome | Ref. |
---|---|---|---|---|---|---|
Yoshioka et al., 2015 | FFPE | Ki-67 | Anthracycline Taxane-based | Luminal A (n = 8) Luminal B (n = 22) ER+ HER2+ (n = 11) ER− HER2+ (n = 12) TNBC (n = 11) | pCR | [65] |
Alves et al., 2019 | FFPE | CAIX | Doxorubicin Cyclophosphamide Paclitaxel | Luminal A (n = 22) Luminal B (n = 77) Luminal B HER2+ (n = 46) HER2 (n = 20) TNBC (n = 31) | pCR | [66] |
Cerbelli et al., 2017 | FFPE | PDL-1 | Doxorubicin Cyclophosphamide Paclitaxel | TNBC (n = 54) | pCR | [67] |
Xing et al., 2019 | FFPE | FKBP12 | 5-florouracil Epirubicin Cyclophosphamide | Luminal HER2− (n = 334) HER2+ (n = 102) TNBC (n = 88) | pCR | [68] |
Nakai et al., 2012 | FFPE | MGMT | Anthracycline Taxane | TNBC (n = 32) | pCR | [69] |
Chuthapisith et al., 2009 | FFPE | ANXA1 | Adriamycin Cyclophosphamid Docetaxel | Non-classification (n = 40) | non-pCR | [70] |
ANXA2 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Freitas, A.J.A.d.; Causin, R.L.; Varuzza, M.B.; Hidalgo Filho, C.M.T.; Silva, V.D.d.; Souza, C.d.P.; Marques, M.M.C. Molecular Biomarkers Predict Pathological Complete Response of Neoadjuvant Chemotherapy in Breast Cancer Patients: Review. Cancers 2021, 13, 5477. https://doi.org/10.3390/cancers13215477
Freitas AJAd, Causin RL, Varuzza MB, Hidalgo Filho CMT, Silva VDd, Souza CdP, Marques MMC. Molecular Biomarkers Predict Pathological Complete Response of Neoadjuvant Chemotherapy in Breast Cancer Patients: Review. Cancers. 2021; 13(21):5477. https://doi.org/10.3390/cancers13215477
Chicago/Turabian StyleFreitas, Ana Julia Aguiar de, Rhafaela Lima Causin, Muriele Bertagna Varuzza, Cassio Murilo Trovo Hidalgo Filho, Vinicius Duval da Silva, Cristiano de Pádua Souza, and Márcia Maria Chiquitelli Marques. 2021. "Molecular Biomarkers Predict Pathological Complete Response of Neoadjuvant Chemotherapy in Breast Cancer Patients: Review" Cancers 13, no. 21: 5477. https://doi.org/10.3390/cancers13215477