Anti-Tumor Immunity to Patient-Derived Breast Cancer Cells by Vaccination with Interferon-Alpha-Conditioned Dendritic Cells (IFN-DC)
Abstract
:1. Introduction
2. Materials and Methods
2.1. Patients and Samples
2.2. Statistical Analysis
2.3. Cell Lines
2.4. Cell Preparation
2.5. Isolation of Patient-Derived BC Organoids (PDBCOs) from Primary Tumors
2.6. Isolation of Patient-Derived Metastatic (PDM) Cells from Ascitic Fluid or Pleural Effusion
2.7. Confocal Laser Scanning Microscopy (CLSM)
2.8. Flow Cytometry
2.9. Immunohistochemistry
2.10. Lysate Tumor Cell and PBL/DC Cocultures
2.11. Therapeutic Vaccination of Tumor-Bearing Hu-PBL-NSG Mice
2.12. Cytokine Assay
2.13. Cytotoxicity Assay
3. Results
3.1. In Vitro Induction of Immune Responses to MCF-7 Breast Tumor Cells
3.2. In Vivo Efficacy of Therapeutic Vaccination with IFN-DC Loaded with HOCl-Oxidized Tumor Cell Lysate
3.3. Patient-Specific BC Organoids Allow an Efficient Expansion of BC Cells and a Faithful Reconstruction of Parental Tumors Maintaining Antigenic Profiles
3.4. In Vitro Evaluation of the IFN-DC-Based Vaccine in a Selected Group of Breast Cancer Patients
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA. Cancer J. Clin. 2021, 71, 209–249. [Google Scholar] [CrossRef]
- Moo, T.A.; Sanford, R.; Dang, C.; Morrow, M. Overview of Breast Cancer Therapy. PET Clin. 2018, 13, 339–354. [Google Scholar] [PubMed]
- Yang, J.; Ju, J.; Guo, L.; Ji, B.; Shi, S.; Yang, Z.; Gao, S.; Yuan, X.; Tian, G.; Liang, Y.; et al. Prediction of HER2-positive breast cancer recurrence and metastasis risk from histopathological images and clinical information via multimodal deep learning. Comput. Struct. Biotechnol. J. 2022, 20, 333–342. [Google Scholar] [CrossRef] [PubMed]
- Locy, H.; Verhulst, S.; Cools, W.; Waelput, W.; Brock, S.; Cras, L.; Schiettecatte, A.; Jonckheere, J.; van Grunsven, L.A.; Vanhoeij, M.; et al. Assessing Tumor-Infiltrating Lymphocytes in Breast Cancer: A Proposal for Combining Immunohistochemistry and Gene Expression Analysis to Refine Scoring. Front. Immunol. 2022, 13, 794175. [Google Scholar] [CrossRef]
- Garaud, S.; Buisseret, L.; Solinas, C.; Gu-Trantien, C.; De Wind, A.; Van Den Eynden, G.; Naveaux, C.; Lodewyckx, J.N.; Boisson, A.; Duvillier, H.; et al. Tumor-infiltrating B cells signal functional humoral immune responses in breast cancer. JCI Insight 2019, 4, e129641. [Google Scholar] [CrossRef]
- Lee, K.H.; Kim, E.Y.; Yun, J.S.; Park, Y.L.; Do, S.I.; Chae, S.W.; Park, C.H. The prognostic and predictive value of tumor-infiltrating lymphocytes and hematologic parameters in patients with breast cancer. BMC Cancer 2018, 18, 938. [Google Scholar] [CrossRef]
- Morales, M.A.G.; Rodríguez, R.B.; Cruz, J.R.S.; Teran, L.M. Overview of new treatments with immunotherapy for breast cancer and a proposal of a combination therapy. Molecules 2020, 25, 5686. [Google Scholar] [CrossRef] [PubMed]
- Sivaganesh, V.; Promi, N.; Maher, S.; Peethambaran, B. Emerging immunotherapies against novel molecular targets in breast cancer. Int. J. Mol. Sci. 2021, 22, 2433. [Google Scholar] [CrossRef]
- Li, X.; Bu, X. Progress in vaccine therapies for breast cancer. In Advances in Experimental Medicine and Biology; Springer: New York, NY, USA, 2017; Volume 1026, pp. 315–330. [Google Scholar]
- Prokopowicz, Z.M.; Arce, F.; Biedron, R.; Chiang, C.L.-L.; Ciszek, M.; Katz, D.R.; Nowakowska, M.; Zapotoczny, S.; Marcinkiewicz, J.; Chain, B.M. Hypochlorous Acid: A Natural Adjuvant That Facilitates Antigen Processing, Cross-Priming, and the Induction of Adaptive Immunity. J. Immunol. 2010, 184, 824–835. [Google Scholar] [CrossRef]
- Santini, S.M.; Lapenta, C.; Logozzi, M.; Parlato, S.; Spada, M.; Di Pucchio, T.; Belardelli, F. Type I interferon as a powerful adjuvant for monocyte-derived dendritic cell development and activity in vitro and in Hu-PBL-SCID mice. J. Exp. Med. 2000, 191, 1777–1788. [Google Scholar] [CrossRef]
- Lapenta, C.; Gabriele, L.; Santini, S.M. IFN-alpha-mediated differentiation of dendritic cells for cancer immunotherapy: Advances and perspectives. Vaccines 2020, 8, 617. [Google Scholar] [CrossRef] [PubMed]
- Lapenta, C.; Santini, S.M.; Spada, M.; Donati, S.; Urbani, F.; Accapezzato, D.; Franceschini, D.; Andreotti, M.; Barnaba, V.; Belardelli, F. IFN-alpha-conditioned dendritic cells are highly efficient in inducing cross-priming CD8(+) T cells against exogenous viral antigens. Eur. J. Immunol. 2006, 36, 2046–2060. [Google Scholar] [CrossRef] [PubMed]
- Bartucci, M.; Dattilo, R.; Moriconi, C.; Pagliuca, A.; Mottolese, M.; Federici, G.; Di Benedetto, A.; Todaro, M.; Stassi, G.; Sperati, F.; et al. TAZ is required for metastatic activity and chemoresistance of breast cancer stem cells. Oncogene 2015, 34, 681–690. [Google Scholar] [CrossRef]
- Sachs, N.; de Ligt, J.; Kopper, O.; Gogola, E.; Bounova, G.; Weeber, F.; Balgobind, A.V.; Wind, K.; Gracanin, A.; Begthel, H.; et al. A Living Biobank of Breast Cancer Organoids Captures Disease Heterogeneity. Cell 2018, 172, 373–386.e10. [Google Scholar] [CrossRef] [PubMed]
- Tandon, N.; Thakkar, K.; LaGory, E.; Liu, Y.; Giaccia, A. Generation of Stable Expression Mammalian Cell Lines Using Lentivirus. Bio-Protoc. 2018, 8, e3073. [Google Scholar] [CrossRef]
- Lapenta, C.; Donati, S.; Spadaro, F.; Castaldo, P.; Belardelli, F.; Cox, M.C.; Santini, S.M. NK Cell Activation in the Antitumor Response Induced by IFN-α Dendritic Cells Loaded with Apoptotic Cells from Follicular Lymphoma Patients. J. Immunol. 2016, 197, 795–806. [Google Scholar] [CrossRef]
- Riedl, A.; Schlederer, M.; Pudelko, K.; Stadler, M.; Walter, S.; Unterleuthner, D.; Unger, C.; Kramer, N.; Hengstschläger, M.; Kenner, L.; et al. Comparison of cancer cells in 2D vs 3D culture reveals differences in AKT-mTOR-S6K signaling and drug responses. J. Cell Sci. 2017, 130, 203–218. [Google Scholar] [CrossRef]
- Dai, X.; Cheng, H.; Bai, Z.; Li, J. Breast cancer cell line classification and Its relevance with breast tumor subtyping. J. Cancer 2017, 8, 3131–3141. [Google Scholar]
- Grimm, S.L.; Hartig, S.M.; Edwards, D.P. Progesterone Receptor Signaling Mechanisms. J. Mol. Biol. 2016, 428, 3831–3849. [Google Scholar]
- Zattarin, E.; Leporati, R.; Ligorio, F.; Lobefaro, R.; Vingiani, A.; Pruneri, G.; Vernieri, C. Hormone Receptor Loss in Breast Cancer: Molecular Mechanisms, Clinical Settings, and Therapeutic Implications. Cells 2020, 9, 2644. [Google Scholar] [CrossRef]
- Cartaxo, A.L.; Estrada, M.F.; Domenici, G.; Roque, R.; Silva, F.; Gualda, E.J.; Loza-Alvarez, P.; Sflomos, G.; Brisken, C.; Alves, P.M.; et al. A novel culture method that sustains ERα signaling in human breast cancer tissue microstructures. J. Exp. Clin. Cancer Res. 2020, 39, 161. [Google Scholar] [CrossRef] [PubMed]
- Ponti, D.; Costa, A.; Zaffaroni, N.; Pratesi, G.; Petrangolini, G.; Coradini, D.; Pilotti, S.; Pierotti, M.A.; Daidone, M.G. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 2005, 65, 5506–5511. [Google Scholar] [CrossRef]
- Cordenonsi, M.; Zanconato, F.; Azzolin, L.; Forcato, M.; Rosato, A.; Frasson, C.; Inui, M.; Montagner, M.; Parenti, A.R.; Poletti, A.; et al. The hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell 2011, 147, 759–772. [Google Scholar] [CrossRef] [PubMed]
- Gilles, C.; Polette, M.; Zahm, J.M.; Tournier, J.M.; Volders, L.; Foidart, J.M.; Birembaut, P. Vimentin contributes to human mammary epithelial cell migration. J. Cell Sci. 1999, 112, 4615–4625. [Google Scholar] [CrossRef]
- Gilles, C.; Polette, M.; Mestdagt, M.; Nawrocki-Raby, B.; Ruggeri, P.; Birembaut, P.; Foidart, J.M. Transactivation of vimentin by β-catenin in human breast cancer cells. Cancer Res. 2003, 63, 2658–2664. [Google Scholar] [CrossRef] [PubMed]
- Péchoux, C.; Gudjonsson, T.; Rønnov-Jessen, L.; Bissell, M.J.; Petersen, O.W. Human mammary luminal epithelial cells contain progenitors to myoepithelial cells. Dev. Biol. 1999, 206, 88–99. [Google Scholar] [CrossRef]
- Böcker, W.; Moll, R.; Poremba, C.; Holland, R.; Van Diest, P.J.; Dervan, P.; Bürger, H.; Wai, D.; Diallo, R.I.; Brandt, B.; et al. Common adult stem cells in the human breast give rise to glandular and myoepithelial cell lineages: A new cell biological concept. Lab. Investig. 2002, 82, 737–745. [Google Scholar] [CrossRef] [PubMed]
- Kakarala, M.; Wicha, M.S. Implications of the cancer stem-cell hypothesis for breast cancer prevention and therapy. J. Clin. Oncol. 2008, 26, 2813–2820. [Google Scholar]
- Sarrió, D.; Rodriguez-Pinilla, S.M.; Hardisson, D.; Cano, A.; Moreno-Bueno, G.; Palacios, J. Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res. 2008, 68, 989–997. [Google Scholar] [CrossRef]
- Artibani, M.; Sims, A.H.; Slight, J.; Aitken, S.; Thornburn, A.; Muir, M.; Brunton, V.G.; Del-Pozo, J.; Morrison, L.R.; Katz, E.; et al. WT1 expression in breast cancer disrupts the epithelial/mesenchymal balance of tumour cells and correlates with the metabolic response to docetaxel. Sci. Rep. 2017, 7, 45255. [Google Scholar] [CrossRef]
- Ahn, H.K.; Sim, S.H.; Suh, K.J.; Kim, M.H.; Jeong, J.H.; Kim, J.Y.; Lee, D.W.; Ahn, J.H.; Chae, H.; Lee, K.H.; et al. Response Rate and Safety of a Neoadjuvant Pertuzumab, Atezolizumab, Docetaxel, and Trastuzumab Regimen for Patients with ERBB2-Positive Stage II/III Breast Cancer: The Neo-PATH Phase 2 Nonrandomized Clinical Trial. JAMA Oncol. 2022, 8, 1271–1277. [Google Scholar] [CrossRef] [PubMed]
- Waks, A.G.; Keenan, T.E.; Li, T.; Tayob, N.; Wulf, G.M.; Richardson, E.T.; Attaya, V.; Anderson, L.; Mittendorf, E.A.; Overmoyer, B.; et al. Phase Ib study of pembrolizumab in combination with trastuzumab emtansine for metastatic HER2-positive breast cancer. J. Immunother. Cancer 2022, 10, e005119. [Google Scholar] [CrossRef] [PubMed]
- Santisteban, M.; Solans, B.P.; Hato, L.; Urrizola, A.; Mejías, L.D.; Salgado, E.; Sánchez-Bayona, R.; Toledo, E.; Rodríguez-Spiteri, N.; Olartecoechea, B.; et al. Final results regarding the addition of dendritic cell vaccines to neoadjuvant chemotherapy in early HER2-negative breast cancer patients: Clinical and translational analysis. Ther. Adv. Med. Oncol. 2021, 13, 17588359211064653. [Google Scholar] [CrossRef] [PubMed]
- Solans, B.P.; López-Díaz de Cerio, A.; Elizalde, A.; Pina, L.J.; Inogés, S.; Espinós, J.; Salgado, E.; Mejías, L.D.; Trocóniz, I.F.; Santisteban, M. Assessing the impact of the addition of dendritic cell vaccination to neoadjuvant chemotherapy in breast cancer patients: A model-based characterization approach. Br. J. Clin. Pharmacol. 2019, 85, 1670–1683. [Google Scholar] [CrossRef] [PubMed]
- Maeng, H.M.; Moore, B.N.; Bagheri, H.; Steinberg, S.M.; Inglefield, J.; Dunham, K.; Wei, W.Z.; Morris, J.C.; Terabe, M.; England, L.C.; et al. Phase I Clinical Trial of an Autologous Dendritic Cell Vaccine Against HER2 Shows Safety and Preliminary Clinical Efficacy. Front. Oncol. 2021, 11, 789078. [Google Scholar] [CrossRef]
- Lowenfeld, L.; Mick, R.; Datta, J.; Xu, S.; Fitzpatrick, E.; Fisher, C.S.; Fox, K.R.; Demichele, A.; Zhang, P.J.; Weinstein, S.P.; et al. Dendritic cell vaccination enhances immune responses and induces regression of HER2pos DCIS independent of route: Results of randomized selection design trial. Clin. Cancer Res. 2017, 23, 2961–2971. [Google Scholar] [CrossRef]
- Bergh, J.; Hall, P.; Östman, A.; Toftgård, R. Breast cancer biology and the future of tailored therapies. J. Intern. Med. 2013, 274, 102–104. [Google Scholar] [CrossRef]
- Onkar, S.S.; Carleton, N.M.; Lucas, P.C.; Bruno, T.C.; Lee, A.V.; Vignali, D.A.A.; Oesterreich, S. The Great Immune Escape: Understanding the Divergent Immune Response in Breast Cancer Subtypes. Cancer Discov. 2023, 13, 23–40. [Google Scholar] [PubMed]
- Hayes, D.F.; Paoletti, C. Circulating tumour cells: Insights into tumour heterogeneity. J. Intern. Med. 2013, 274, 137–143. [Google Scholar] [CrossRef]
- Schönharting, W.; Roehnisch, T.; Manoochehri, M.; Christoph, J.; Sieger, M.; Nogueira, M.; Martos-Contreras, M.C.; Kunz, M. Improved Survival of a HER2-Positive Metastatic Breast Cancer Patient Following a Personalized Peptide Immunization. Vaccines 2023, 11, 1023. [Google Scholar] [CrossRef]
- Burkholz, S.R.; Herst, C.V.; Carback, R.T.; Harris, P.E.; Rubsamen, R.M. Survivin (BIRC5) Peptide Vaccine in the 4T1 Murine Mammary Tumor Model: A Potential Neoadjuvant T Cell Immunotherapy for Triple Negative Breast Cancer: A Preliminary Study. Vaccines 2023, 11, 644. [Google Scholar] [CrossRef] [PubMed]
- Tomasicchio, M.; Semple, L.; Esmail, A.; Meldau, R.; Randall, P.; Pooran, A.; Davids, M.; Cairncross, L.; Anderson, D.; Downs, J.; et al. An autologous dendritic cell vaccine polarizes a Th-1 response which is tumoricidal to patient-derived breast cancer cells. Cancer Immunol. Immunother. 2019, 68, 71–83. [Google Scholar] [CrossRef] [PubMed]
- Montico, B.; Lapenta, C.; Ravo, M.; Martorelli, D.; Muraro, E.; Zeng, B.; Comaro, E.; Spada, M.; Donati, S.; Santini, S.M.; et al. Exploiting a new strategy to induce immunogenic cell death to improve dendritic cell-based vaccines for lymphoma immunotherapy. Oncoimmunology 2017, 6, e1356964. [Google Scholar] [CrossRef] [PubMed]
- Lapenta, C.; Donati, S.; Spadaro, F.; Lattanzi, L.; Urbani, F.; Macchia, I.; Sestili, P.; Spada, M.; Cox, M.C.; Belardelli, F.; et al. Lenalidomide improves the therapeutic effect of an interferon-α-dendritic cell-based lymphoma vaccine. Cancer Immunol. Immunother. 2019, 68, 1791–1804. [Google Scholar] [CrossRef]
- Bandola-Simon, J.; Roche, P.A. Dysfunction of antigen processing and presentation by dendritic cells in cancer. Mol. Immunol. 2019, 113, 31–37. [Google Scholar] [CrossRef] [PubMed]
- Van Willigen, W.W.; Bloemendal, M.; Gerritsen, W.R.; Schreibelt, G.; De Vries, I.J.M.; Bol, K.F. Dendritic Cell Cancer Therapy: Vaccinating the Right Patient at the Right Time. Front. Immunol. 2018, 9, 2265. [Google Scholar] [CrossRef]
- Ock, C.Y.; Keam, B.; Kim, S.; Lee, J.S.; Kim, M.; Kim, T.M.; Jeon, Y.K.; Kim, D.W.; Chung, D.H.; Heo, D.S. Pan-Cancer Immunogenomic Perspective on the Tumor Microenvironment Based on PD-L1 and CD8 T-Cell Infiltration. Clin. Cancer Res. 2016, 22, 2261–2270. [Google Scholar] [CrossRef]
- Gajewski, T.F. Failure at the effector phase: Immune barriers at the level of the melanoma tumor microenvironment. Clin. Cancer Res. 2007, 13, 5256–5261. [Google Scholar]
- Spranger, S.; Spaapen, R.M.; Zha, Y.; Williams, J.; Meng, Y.; Ha, T.T.; Gajewski, T.F. Up-regulation of PD-L1, IDO, and Tregs in the melanoma tumor microenvironment is driven by CD8+ T cells. Sci. Transl. Med. 2013, 5, 200ra116. [Google Scholar]
- Sun, Z.; Fourcade, J.; Pagliano, O.; Chauvin, J.M.; Sander, C.; Kirkwood, J.M.; Zarour, H.M. IL10 and PD-1 cooperate to limit the activity of tumor-specific CD8+ T cells. Cancer Res. 2015, 75, 1635–1644. [Google Scholar] [CrossRef]
(a) | |||||||||
Patient No. | Age | Menopausal Status | Histology | Pathology, Tumor Size (pT) | Lymph Node Status (pN) | Grade | ER/PgR/HER2 2 Status (%) | Ki67 (%) | Neo-Adjuvant Treatment and Response |
1 | 37 | Pre | IDC nos 1 | T2 | SN neg | 3 | -/-/- | 70 | NA 3 |
2 | 69 | Post | ILC | T1b(m) | N2a | X 4 | 95/1/- | 5 | Ctx-Epi + Txl(RP) |
3 | 46 | Pre | NET | T2 | N1(sn) | 3 | 80/80/- | 70 | NA |
4 | 34 | Pre | IDC | T2ypM1(L) | N1a | 3 | -/-/- | 60 | Beva + Txl (RP-Li; PD-T) |
5 | 52 | Post | IDC | T2 | N1(mi) | 2 | 90/2/- | 30 | NA |
6 | 73 | Post | IDC | T2 | N0(sn) | 2 | 90/3/- | 25 | NA |
7 | 75 | post | IDC nos | T1c | N1mi(sn) | 2 | 95/95/- | 20 | NA |
8 | 82 | Post | IDC | T3 | N0(sn) | 2 | 95/95/- | 20 | NA |
9 | 49 | Pre | R 5:IDC | T2 | N0(sn) | 2 | 95/95/- | 30 | NA |
L: ILC | T2m | N1(sn) | 2 | 95/95/- | 15 | ||||
10 | 62 | Post | IDC | T1c | N1mi(sn) | 2 | 95/95/- | 20 | NA |
11 | 43 | Pre | IDC | T1c | N1a | 2 | 95/95/- | 20 | NA |
12 | 46 | Pre | IDC nos | T2 | N0(sn) | 2 | 95/95/- | 20 | NA |
13 | 49 | Pre | IDC nos | T1c | N1a | 2 | 90/90/- | 10 | NA |
14 | 51 | Pre | Ca papillary + NET | T2 | N1(sn) | 2 | 95/85/- | 20 | NA |
15 | 66 | Post | IDC | T2 | N0(sn) | 3 | 10/-/- | 50 | NA |
16 | 50 | Pre | ILC + NET | T3 | N1a | 3 | 90/90/- | 50 | NA |
17 | 32 | Pre | IDC apocrine | T2(m) | N1a | 3 | 80/-/- | 30 | NA |
18 | 76 | Post | IDC | T1c(m) | N3a | 3 | -/-/- | 25 | NA |
19 | 41 | Pre | IDC | T2 | N0 | 3 | -/-/- | 80 | Epi + Taxol(PD) |
20 | 78 | Post | IDC nos | T2 | N1mi(sn) | 2 | 95/70/- | 15 | NA |
21 | 79 | Post | IDC nos | T2(m) | N1a | 2 | 95/-/- | 22 | NA |
22 | 77 | Post | ILC | T2 | N1a | 2 | 90/40/- | 25 | NA |
1 IDC, infiltrating ductal carcinoma; DCIS, ductal carcinoma in situ; ILC, invasive lobular carcinoma; ILCI, lobular carcinoma in situ, Neuroendocrine tumor (NET); sn (sentinel lymph node); mi (micrometastasis); 2 ER, estrogen receptor; PgR, progesterone receptor, expressed in percentage; HER2status + positive or—negative; 3 NA, not applicable; Ctx: cyclophosphamide; Epi, epirubicin; Beva, bevacizumab; Txl: taxol; FEC, 5-fluorouracil, Epi, epirubicin, Ctx, cyclophoasphamide; 4 X, undetermined; 5 R: right side; L: left side. | |||||||||
(b) | |||||||||
Patient No. | Age | Source of Cells | Histology on Original T | Pathology, pTNM Original T | Grade | ER/PgR/HER2 2 Status of the Original T (%) | ER/PgR/HER2 Status of M Disease | Previous Treatments | |
1 | 50 | Ascites | ILC 1 | NA 3 | NA | 95/95/+ | -/-/- | 5 CMF, Herc, Tam, AI, Pertuzumab, Dxt, CDDP, Gem | |
2 | 59 | Ascites | DCIS+ comedoCa | pT1mN0 (m) | 3 | 70/60/- | -/-/- | Fulvestrant, Everolimus, Exem; Txl | |
3 | 67 | PE 6 | IDC | T3N+ | 3 | 95/30/- | -/-/- | NA (met at the diagnosis) | |
4 | 43 | PE | IDC | pT1cN1a | 2 | 80/50/+ | -/-/- | FEC, Herc, Cape, Lapatinb, Txl, CBDCA, CMF | |
1 IDC, infiltrating ductal carcinoma; DCIS, ductal carcinoma in situ; ILC, invasive lobular carcinoma; ILCI, lobular carcinoma in situ comedoca, comedocarcinoma; Neuroendocrine tumor (NET); sn (sentinel lymph node); mi (micrometastasis); 2 ER, estrogen receptor; PgR, progesterone receptor, expressed in percentage; HER2status + positive or—negative; 3 NA, not applicable; Ctx: cyclophosphamide; Epi, epirubicin; Beva, bevacizumab; Txl: taxol; FEC, 5-fluorouracil, Epi, epirubicin, Ctx, cyclophoasphamide; 4 X, undetermined; 5 R: right side; L: left side1 5 CMF, cyclophosphamide, methotrexate, 5-fluorouracil; Herc, Herceptin; Tam, Tamoxifen; A.I.: aromatase inhibitors; Exeme, exemestane; Dxt, Docetaxel; CDDP, Cisplatino; GEM, gemcitabine; Txl, Taxol; Cape: capecitabina; CBDCA: carboplatino; 6 PE: pleural effusion. |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 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
Lapenta, C.; Santini, S.M.; Antonacci, C.; Donati, S.; Cecchetti, S.; Frittelli, P.; Catalano, P.; Urbani, F.; Macchia, I.; Spada, M.; et al. Anti-Tumor Immunity to Patient-Derived Breast Cancer Cells by Vaccination with Interferon-Alpha-Conditioned Dendritic Cells (IFN-DC). Vaccines 2024, 12, 1058. https://doi.org/10.3390/vaccines12091058
Lapenta C, Santini SM, Antonacci C, Donati S, Cecchetti S, Frittelli P, Catalano P, Urbani F, Macchia I, Spada M, et al. Anti-Tumor Immunity to Patient-Derived Breast Cancer Cells by Vaccination with Interferon-Alpha-Conditioned Dendritic Cells (IFN-DC). Vaccines. 2024; 12(9):1058. https://doi.org/10.3390/vaccines12091058
Chicago/Turabian StyleLapenta, Caterina, Stefano Maria Santini, Celeste Antonacci, Simona Donati, Serena Cecchetti, Patrizia Frittelli, Piera Catalano, Francesca Urbani, Iole Macchia, Massimo Spada, and et al. 2024. "Anti-Tumor Immunity to Patient-Derived Breast Cancer Cells by Vaccination with Interferon-Alpha-Conditioned Dendritic Cells (IFN-DC)" Vaccines 12, no. 9: 1058. https://doi.org/10.3390/vaccines12091058