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Research Article

Interleukin-3 production by basal-like breast cancer cells is associated with poor prognosis

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Received 28 Jun 2023, Accepted 07 Dec 2023, Published online: 01 Feb 2024

References

  • Bulaeva, E., D. Pellacani, N. Nakamichi, C. A. Hammond, P. A. Beer, A. Lorzadeh, M. Moksa, et al. 2020. “MYC-Induced Human Acute Myeloid Leukemia Requires a Continuing IL-3/GM-CSF Costimulus.” Blood 136 (24): 2764–2773. https://doi.org/10.1182/blood.2020006374
  • Cancer Genome Atlas, Network. 2012. “Comprehensive Molecular Portraits of Human Breast Tumours.” Nature 490 (7418): 61–70. https://doi.org/10.1038/nature11412
  • Casasent, A. K., M. Edgerton, and N. E. Navin. 2017. “Genome Evolution in Ductal Carcinoma in Situ: invasion of the Clones.” The Journal of Pathology 241 (2): 208–218. https://doi.org/10.1002/path.4840
  • Cortes, J., D. W. Cescon, H. S. Rugo, Z. Nowecki, S. A. Im, M. M. Yusof, C. Gallardo, et al. 2020. “Pembrolizumab plus Chemotherapy versus Placebo plus Chemotherapy for Previously Untreated Locally Recurrent Inoperable or Metastatic Triple-Negative Breast Cancer (KEYNOTE-355): a Randomised, Placebo-Controlled, Double-Blind, Phase 3 Clinical Trial.” Lancet 396 (10265): 1817–1828. and https://doi.org/10.1016/S0140-6736(20)32531-9
  • Dentelli, P., L. Del Sorbo, A. Rosso, A. Molinar, G. Garbarino, G. Camussi, L. Pegoraro, and M. F. Brizzi. 1999. “Human IL-3 Stimulates Endothelial Cell Motility and Promotes in Vivo New Vessel Formation.” The Journal of Immunology 163 (4): 2151–2159. 10.4049/jimmunol.163.4.2151
  • Dentelli, P., A. Rosso, C. Calvi, B. Ghiringhello, G. Garbarino, G. Camussi, L. Pegoraro, and M. F. Brizzi. 2004. “IL-3 Affects Endothelial Cell-Mediated Smooth Muscle Cell Recruitment by Increasing TGF Beta Activity: potential Role in Tumor Vessel Stabilization.” Oncogene 23 (9): 1681–1692. https://doi.org/10.1038/sj.onc.1207290
  • Dentelli, P., A. Rosso, G. Garbarino, C. Calvi, E. Lombard, P. Di Stefano, P. Defilippi, L. Pegoraro, and M. F. Brizzi. 2005. “The Interaction between KDR and Interleukin-3 Receptor (IL-3R) Beta Common Modulates Tumor Neovascularization.” Oncogene 24 (42): 6394–6405. https://doi.org/10.1038/sj.onc.1208786
  • Dentelli, P., A. Rosso, C. Olgasi, G. Camussi, and M. F. Brizzi. 2011. “IL-3 is a Novel Target to Interfere with Tumor Vasculature.” Oncogene 30 (50): 4930–4940. https://doi.org/10.1038/onc.2011.204
  • Frankel, A. E., J. H. Woo, C. Ahn, N. Pemmaraju, B. C. Medeiros, H. E. Carraway, O. Frankfurt, et al. 2014. “Activity of SL-401, a Targeted Therapy Directed to Interleukin-3 Receptor, in Blastic Plasmacytoid Dendritic Cell Neoplasm Patients.” Blood 124 (3): 385–392. https://doi.org/10.1182/blood-2014-04-566737
  • He, S. Z., S. Busfield, D. S. Ritchie, M. S. Hertzberg, S. Durrant, I. D. Lewis, P. Marlton, et al. 2015. “A Phase 1 Study of the Safety, Pharmacokinetics and anti-Leukemic Activity of the anti-CD123 Monoclonal Antibody CSL360 in Relapsed, Refractory or High-Risk Acute Myeloid Leukemia.” Leukemia & Lymphoma 56 (5): 1406–1415. https://doi.org/10.3109/10428194.2014.956316
  • Hercus, T. R., W. L. T. Kan, S. E. Broughton, D. Tvorogov, H. S. Ramshaw, J. J. Sandow, T. L. Nero, et al. 2017. “Role of the Beta Common (Betac) Family of Cytokines in Health and Disease.” Cold Spring Harbor Perspectives in Biology 10 (6): 1–26. https://doi.org/10.1101/cshperspect.a028514
  • Jin, L., E. M. Lee, H. S. Ramshaw, S. J. Busfield, A. G. Peoppl, L. Wilkinson, M. A. Guthridge, et al. 2009. “Monoclonal Antibody-Mediated Targeting of CD123, IL-3 Receptor Alpha Chain, Eliminates Human Acute Myeloid Leukemic Stem Cells.” Cell Stem Cell 5 (1): 31–42. https://doi.org/10.1016/j.stem.2009.04.018
  • Johnson, S. F., C. Cruz, A. K. Greifenberg, S. Dust, D. G. Stover, D. Chi, B. Primack, et al. 2016. “CDK12 Inhibition Reverses De Novo and Acquired PARP Inhibitor Resistance in BRCA Wild-Type and Mutated Models of Triple-Negative Breast Cancer.” Cell Reports 17 (9): 2367–2381. https://doi.org/10.1016/j.celrep.2016.10.077
  • Jordan, C. T., D. Upchurch, S. J. Szilvassy, M. L. Guzman, D. S. Howard, A. L. Pettigrew, T. Meyerrose, et al. 2000. “The Interleukin-3 Receptor Alpha Chain is a Unique Marker for Human Acute Myelogenous Leukemia Stem Cells.” Leukemia 14 (10): 1777–1784. https://doi.org/10.1038/sj.leu.2401903
  • Koni, M., I. Castellano, E. Venturelli, A. Sarcinella, T. Lopatina, C. Grange, M. Cedrino, et al. 2022. “Interleukin-3-Receptor-Alpha in Triple-Negative Breast Cancer (TNBC): An Additional Novel Biomarker of TNBC Aggressiveness and a Therapeutic Target.” Cancers 14 (16): 3918. https://doi.org/10.3390/cancers14163918
  • Korpelainen, E. I., J. R. Gamble, W. B. Smith, G. J. Goodall, S. Qiyu, J. M. Woodcock, M. Dottore, M. A. Vadas, and A. F. Lopez. 1993. “The Receptor for Interleukin 3 is Selectively Induced in Human Endothelial Cells by Tumor Necrosis Factor Alpha and Potentiates Interleukin 8 Secretion and Neutrophil Transmigration.” Proceedings of the National Academy of Sciences of the United States of America 90 (23): 11137–11141. https://doi.org/10.1073/pnas.90.23.11137
  • Korpelainen, E. I., J. R. Gamble, M. A. Vadas, and A. F. Lopez. 1996. “IL-3 Receptor Expression, Regulation and Function in Cells of the Vasculature.” Immunology and Cell Biology 74 (1): 1–7. https://doi.org/10.1038/icb.1996.1
  • Laszlo, G. S., J. J. Orozco, A. R. Kehret, M. C. Lunn, J. Huo, D. K. Hamlin, D. Scott Wilbur, et al. 2022. “Development of [(211)at]Astatine-Based anti-CD123 Radioimmunotherapy for Acute Leukemias and Other CD123+ Malignancies.” Leukemia 36 (6): 1485–1491. https://doi.org/10.1038/s41375-022-01580-7
  • Lehmann, B. D., J. A. Bauer, X. Chen, M. E. Sanders, A. B. Chakravarthy, Y. Shyr, and J. A. Pietenpol. 2011. “Identification of Human Triple-Negative Breast Cancer Subtypes and Preclinical Models for Selection of Targeted Therapies.” The Journal of Clinical Investigation 121 (7): 2750–2767. https://doi.org/10.1172/JCI45014
  • Liedtke, Cornelia, Chafika Mazouni, Kenneth R. Hess, Fabrice André, Attila Tordai, Jaime A. Mejia, W. Fraser Symmans, et al. 2008. “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 26 (8): 1275–1281. https://doi.org/10.1200/JCO.2007.14.4147
  • Lombardo, G., M. Gili, C. Grange, C. Cavallari, P. Dentelli, G. Togliatto, D. Taverna, G. Camussi, and M. F. Brizzi. 2018. “IL-3R-Alpha Blockade Inhibits Tumor Endothelial Cell-Derived Extracellular Vesicle (EV)-Mediated Vessel Formation by Targeting the Beta-Catenin Pathway.” Oncogene 37 (9): 1175–1191. https://doi.org/10.1038/s41388-017-0034-x
  • Lopatina, T., C. Grange, C. Cavallari, V. Navarro-Tableros, G. Lombardo, A. Rosso, M. Cedrino, et al. 2020. “Targeting IL-3Ralpha on Tumor-Derived Endothelial Cells Blunts Metastatic Spread of Triple-Negative Breast Cancer via Extracellular Vesicle Reprogramming.” Oncogenesis 9 (10): 90. https://doi.org/10.1038/s41389-020-00274-y
  • Lopatina, Tatiana, Malvina Koni, Cristina Grange, Massimo Cedrino, Saveria Femminò, Giusy Lombardo, Enrica Favaro, and Maria Felice Brizzi. 2022. “IL-3 Signalling in the Tumour Microenvironment Shapes the Immune Response via Tumour Endothelial Cell-Derived Extracellular Vesicles.” Pharmacological Research 179: 106206. https://doi.org/10.1016/j.phrs.2022.106206
  • Madden, S. F., C. Clarke, P. Gaule, S. T. Aherne, N. O”Donovan, M. Clynes, J. Crown, and W. M. Gallagher. 2013. “BreastMark: An Integrated Approach to Mining Publicly Available Transcriptomic Datasets Relating to Breast Cancer Outcome.” Breast Cancer Research: BCR 15 (4): R52. https://doi.org/10.1186/bcr3444
  • Mahara, S., P. L. Lee, M. Feng, V. Tergaonkar, W. J. Chng, and Q. Yu. 2016. “HIFI-Alpha Activation Underlies a Functional Switch in the Paradoxical Role of Ezh2/PRC2 in Breast Cancer.” Proceedings of the National Academy of Sciences of the United States of America 113 (26): E3735–44. https://doi.org/10.1073/pnas.1602079113
  • Manz, M. G. 2007. “Human-Hemato-Lymphoid-System Mice: Opportunities and Challenges.” Immunity 26 (5): 537–541. https://doi.org/10.1016/j.immuni.2007.05.001
  • Moldenhauer, L. M., M. P. Cockshell, L. Frost, K. A. Parham, D. Tvorogov, L. Y. Tan, L. M. Ebert, et al. 2015. “Interleukin-3 Greatly Expands Non-Adherent Endothelial Forming Cells with Pro-Angiogenic Properties.” Stem Cell Research 14 (3): 380–395. https://doi.org/10.1016/j.scr.2015.04.002
  • Montesinos, P., G. J. Roboz, C. E. Bulabois, M. Subklewe, U. Platzbecker, Y. Ofran, C. Papayannidis, et al. 2021. “Safety and Efficacy of Talacotuzumab plus Decitabine or Decitabine Alone in Patients with Acute Myeloid Leukemia Not Eligible for Chemotherapy: results from a Multicenter, Randomized, Phase 2/3 Study.” Leukemia 35 (1): 62–74. https://doi.org/10.1038/s41375-020-0773-5
  • Morigi, C. 2017. “Highlights from the 15th St Gallen International Breast Cancer Conference 15–18 March, 2017, Vienna: tailored Treatments for Patients with Early Breast Cancer.” Ecancermedicalscience 11: 732. https://doi.org/10.3332/ecancer.2017.732
  • Pasha, N., and N. C. Turner. 2021. “Understanding and Overcoming Tumor Heterogeneity in Metastatic Breast Cancer Treatment.” Nature Cancer 2 (7): 680–692. https://doi.org/10.1038/s43018-021-00229-1
  • Pemmaraju, N., A. A. Lane, K. L. Sweet, A. S. Stein, S. Vasu, W. Blum, D. A. Rizzieri, et al. 2019. “Tagraxofusp in Blastic Plasmacytoid Dendritic-Cell Neoplasm.” The New England Journal of Medicine 380 (17): 1628–1637. https://doi.org/10.1056/NEJMoa1815105
  • Perou, C. M., T. Sørlie, M. B. Eisen, M. van de Rijn, S. S. Jeffrey, C. A. Rees, J. R. Pollack, et al. 2000. “Molecular Portraits of Human Breast Tumours.” Nature 406 (6797): 747–752. https://doi.org/10.1038/35021093
  • Savas, P., B. Virassamy, C. Ye, A. Salim, C. P. Mintoff, F. Caramia, R. Salgado,., et al. 2018. “Single-Cell Profiling of Breast Cancer T Cells Reveals a Tissue-Resident Memory Subset Associated with Improved Prognosis.” Nature Medicine 24 (7): 986–993. https://doi.org/10.1038/s41591-018-0078-7
  • Schmid, Peter, Sylvia Adams, Hope S. Rugo, Andreas Schneeweiss, Carlos H. Barrios, Hiroji Iwata, Véronique Diéras, et al. 2018. “Atezolizumab and Nab-Paclitaxel in Advanced Triple-Negative Breast Cancer.” The New England Journal of Medicine 379 (22): 2108–2121. https://doi.org/10.1056/NEJMoa1809615
  • Sharma, M., M. Das, E. Stephen-Victor, C. Galeotti, A. Karnam, M. S. Maddur, P. Bruneval, S. V. Kaveri, and J. Bayry. 2018. “Regulatory T Cells Induce Activation Rather than Suppression of Human Basophils.” Science Immunology 3 (23): 1–14. https://doi.org/10.1126/sciimmunol.aan0829
  • Sørlie, T., C. M. Perou, R. Tibshirani, T. Aas, S. Geisler, H. Johnsen, T. Hastie, et al. 2001. “Gene Expression Patterns of Breast Carcinomas Distinguish Tumor Subclasses with Clinical Implications.” Proceedings of the National Academy of Sciences of the United States of America 98 (19): 10869–10874. https://doi.org/10.1073/pnas.191367098
  • Sung, H., J. Ferlay, R. L. Siegel, M. Laversanne, I. Soerjomataram, A. Jemal, and F. Bray. 2021. “Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries.” CA: a Cancer Journal for Clinicians 71 (3): 209–249. https://doi.org/10.3322/caac.21660
  • Syed, Y. Y. 2019. “Tagraxofusp: First Global Approval.” Drugs 79 (5): 579–583. https://doi.org/10.1007/s40265-019-01087-z
  • Tan, L. Y., M. P. Cockshell, E. Moore, K. K. Myo Min, M. Ortiz, M. Z. Johan, B. Ebert, et al. 2022. “Vasculogenic Mimicry Structures in Melanoma Support the Recruitment of Monocytes.” Oncoimmunology 11 (1): 2043673. https://doi.org/10.1080/2162402X.2022.2043673
  • Tan, L. Y., C. Mintoff, M. Z. Johan, B. W. Ebert, C. Fedele, Y. F. Zhang, P. Szeto, et al. 2016. “Desmoglein 2 Promotes Vasculogenic Mimicry in Melanoma and is Associated with Poor Clinical Outcome.” Oncotarget 7 (29): 46492–46508. https://doi.org/10.18632/oncotarget.10216
  • Testa, U., R. Riccioni, S. Militi, E. Coccia, E. Stellacci, P. Samoggia, R. Latagliata, et al. 2002. “Elevated Expression of IL-3Ralpha in Acute Myelogenous Leukemia is Associated with Enhanced Blast Proliferation, Increased Cellularity, and Poor Prognosis.” Blood 100 (8): 2980–2988. https://doi.org/10.1182/blood-2002-03-0852
  • Varricchi, G., R. Poto, G. Marone, and J. T. Schroeder. 2021. “IL-3 in the Development and Function of Basophils.” Seminars in Immunology 54: 101510. https://doi.org/10.1016/j.smim.2021.101510
  • Vellenga, E., D. Ostapovicz, B. O”Rourke, and J. D. Griffin. 1987. “Effects of Recombinant IL-3, GM-CSF, and G-CSF on Proliferation of Leukemic Clonogenic Cells in Short-Term and Long-Term Cultures.” Leukemia 1 (8): 584–589.
  • Warso, M. A., A. J. Maniotis, X. Chen, D. Majumdar, M. K. Patel, A. Shilkaitis, T. K. Gupta, and R. Folberg. 2001. “Prognostic Significance of Periodic acid-Schiff-Positive Patterns in Primary Cutaneous Melanoma.” Clin Cancer Res 7 (3): 473–477.
  • Yu, D., Y. Zhong, X. Li, Y. Li, X. Li, J. Cao, H. Fan, et al. 2015. “ILs-3, 6 and 11 Increase, but ILs-10 and 24 Decrease Stemness of Human Prostate Cancer Cells in Vitro.” Oncotarget 6 (40): 42687–42703. https://doi.org/10.18632/oncotarget.5883