Metastatic Heterogeneity of Breast Cancer: Companion and Theranostic Approach in Nuclear Medicine
Abstract
:1. Introduction
2. Metastatic Dissemination of Breast Cancer
2.1. Generalities
2.2. Metastatic Dissemination Pattern of Breast Cancer
2.3. The Metastatic Dissemination as an Early Event of Tumor Progression
2.4. Metastatic Dormancy
3. Heterogeneity of Breast Cancer Metastases
4. Nuclear Medicine: Companion Marker and Theranostic Approach
4.1. Companion Approach
4.2. Therapies and the Era of Theranostics
5. Validated and Future Imaging Agents for Metastatic Breast Cancer
5.1. HER-2 Targeting Imaging Agents
5.2. Estrogen-Receptor Targeting Imaging Agents
5.3. Other Imaging Agents Currently in Development
6. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Ferlay, J.; Steliarova-Foucher, E.; Lortet-Tieulent, J.; Rosso, S.; Coebergh, J.W.; Comber, H.; Forman, D.; Bray, F. Cancer incidence and mortality patterns in Europe: Estimates for 40 countries in 2012. Eur. J. Cancer 2013, 49, 1374–1403. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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]
- Sorlie, T.; Tibshirani, R.; Parker, J.; Hastie, T.; Marron, J.S.; Nobel, A.; Deng, S.; Johnsen, H.; Pesich, R.; Geisler, S.; et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc. Natl. Acad. Sci. USA 2003, 100, 8418–8423. [Google Scholar] [PubMed] [Green Version]
- 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]
- Anders, C.K.; Carey, L.A. Biology, metastatic patterns, and treatment of patients with triple-negative breast cancer. Clin. Breast Cancer 2009, 9, S73–S81. [Google Scholar] [CrossRef]
- Jemal, A.; Ward, E.M.; Johnson, C.J.; Cronin, K.A.; Ma, J.; Ryerson, B.; Mariotto, A.; Lake, A.J.; Wilson, R.; Sherman, R.L.; et al. Annual Report to the Nation on the Status of Cancer, 1975–2014, Featuring Survival. J. Natl. Cancer Inst. 2017, 109, djx030. [Google Scholar] [CrossRef]
- 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 Lond. Engl. 2005, 365, 1687–1717. [Google Scholar] [CrossRef]
- Lindström, L.S.; Karlsson, E.; Wilking, U.M.; Johansson, U.; Hartman, J.; Lidbrink, E.K.; Hatschek, T.; Skoog, L.; Bergh, J. Clinically used breast cancer markers such as estrogen receptor, progesterone receptor, and human epidermal growth factor receptor 2 are unstable throughout tumor progression. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2012, 30, 2601–2608. [Google Scholar] [CrossRef]
- Yordanova, A.; Eppard, E.; Kürpig, S.; Bundschuch, R.A.; Schonberger, S.; Gonzalez-Carmona, M.; Feldmann, G.; Ahmadzadehfar, H.; Essler, M. Theranostics in nuclear medicine practice. OncoTargets Ther. 2017, 10, 4821–4828. [Google Scholar]
- Seyfried, T.N.; Huysentruyt, L.C. On the Origin of Cancer Metastasis. Crit. Rev. Oncog. 2013, 18, 43–73. [Google Scholar]
- Jin, X.; Mu, P. Targeting Breast Cancer Metastasis. Breast Cancer Basic Clin. Res. 2015, 9, 23–34. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hoeferlin, L.A.; Chalfant, C.E.; Park, M.A. Challenges in the Treatment of Triple Negative and HER2-Overexpressing Breast Cancer. J. Surg. Sci. 2013, 1, 3–7. [Google Scholar] [PubMed]
- Largillier, R.; Ferrero, J.-M.; Doyen, J.; Barriere, J.; Namer, M.; Mari, V.; Courdi, A.; Hannon-Levi, J.M.; Ettore, F.; Birtwisle-Peyrottes, I.; et al. Prognostic factors in 1,038 women with metastatic breast cancer. Ann. Oncol. Off. J. Eur. Soc. Med. Oncol. 2008, 19, 2012–2019. [Google Scholar] [CrossRef] [PubMed]
- Wu, Q.; Li, J.; Zhu, S.; Wu, J.; Chen, C.; Liu, Q.; Wei, W.; Zhang, Y.; Sun, S. Breast cancer subtypes predict the preferential site of distant metastases: A SEER based study. Oncotarget 2017, 8, 27990–27996. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tham, Y.-L.; Sexton, K.; Kramer, R.; Hilsenbeck, S.; Elledge, R. Primary breast cancer phenotypes associated with propensity for central nervous system metastases. Cancer 2006, 107, 696–704. [Google Scholar] [CrossRef] [PubMed]
- Smid, M.; Wang, Y.; Zhang, Y.; Sieuwerts, A.M.; Klijn, J.G.; Foekens, J.A.; Martens, J.W. Subtypes of breast cancer show preferential site of relapse. Cancer Res. 2008, 68, 3108–3114. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Witzel, I.; Oliveira-Ferrer, L.; Pantel, K.; Müller, V.; Wikman, H. Breast cancer brain metastases: Biology and new clinical perspectives. Breast Cancer Res. 2016, 18, 8. [Google Scholar] [CrossRef] [Green Version]
- van Maaren, M.C.; de Munck, L.; Strobbe, L.J.A.; Sonke, G.S.; Westenend, P.J.; Smidt, M.L.; Poortmans, P.M.P.; Siesling, S. Ten-year recurrence rates for breast cancer subtypes in the Netherlands: A large population-based study. Int. J. Cancer 2019, 144, 263–272. [Google Scholar] [CrossRef] [Green Version]
- Minicozzi, P.; Bella, F.; Toss, A.; Giacomin, A.; Fusco, M.; Zarcone, M.; Tumino, R.; Falcini, F.; Cesaraccio, R.; Candela, G.; et al. Relative and disease-free survival for breast cancer in relation to subtype: A population-based study. J. Cancer Res. Clin. Oncol. 2013, 139, 1569–1577. [Google Scholar] [CrossRef]
- Klein, C.A.; Blankenstein, T.J.F.; Schmidt-Kittler, O.; Petronio, M.; Polzer, B.; Stoecklein, N.H.; Riethmüller, G. Genetic heterogeneity of single disseminated tumour cells in minimal residual cancer. Lancet Lond. Engl. 2002, 360, 683–689. [Google Scholar] [CrossRef]
- Schmidt-Kittler, O.; Ragg, T.; Daskalakis, A.; Granzow, M.; Ahr, A.; Blankenstein, T.J.; Kaufmann, M.; Diebold, J.; Arnholdt, H.; Muller, P.; et al. From latent disseminated cells to overt metastasis: Genetic analysis of systemic breast cancer progression. Proc. Natl. Acad. Sci. USA 2003, 100, 7737–7742. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Braun, S.; Pantel, K.; Müller, P.; Janni, W.; Hepp, F.; Kentenich, C.R.; Gastroph, S.; Wischnik, A.; Dimpfl, T.; Kindermann, G.; et al. Cytokeratin-positive cells in the bone marrow and survival of patients with stage I, II, or III breast cancer. N. Engl. J. Med. 2000, 342, 525–533. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hüsemann, Y.; Geigl, J.B.; Schubert, F.; Musiani, P.; Meyer, M.; Burghart, E.; Forni, G.; Eils, R.; Fehm, T.; Riethmüller, G.; et al. Systemic spread is an early step in breast cancer. Cancer Cell 2008, 13, 58–68. [Google Scholar]
- Eyles, J.; Puaux, A.-L.; Wang, X.; Toh, B.; Prakash, C.; Hong, M.; Tan, T.G.; Zheng, L.; Ong, L.C.; Jin, Y.; et al. Tumor cells disseminate early, but immunosurveillance limits metastatic outgrowth, in a mouse model of melanoma. J. Clin. Investig. 2010, 120, 2030–2039. [Google Scholar] [CrossRef]
- Rhim, A.D.; Mirek, E.T.; Aiello, N.M.; Maitra, A.; Bailey, J.M.; McAllister, F.; Reichert, M.; Beatty, G.L.; Rustgi, A.K.; Vonderheide, R.H.; et al. EMT and dissemination precede pancreatic tumor formation. Cell 2012, 148, 349–361. [Google Scholar] [CrossRef] [Green Version]
- Sänger, N.; Effenberger, K.E.; Riethdorf, S.; Van Haasteren, V.; Gauwerky, J.; Wiegratz, I.; Strebhardt, K.; Kaufmann, M.; Pantel, K. Disseminated tumor cells in the bone marrow of patients with ductal carcinoma in situ. Int. J. Cancer 2011, 129, 2522–2526. [Google Scholar] [CrossRef]
- Banys, M.; Gruber, I.; Krawczyk, N.; Becker, S.; Kurth, R.; Wallwiener, D.; Jakubowska, J.; Hoffmann, J.; Rothmund, R.; Staebler, A.; et al. Hematogenous and lymphatic tumor cell dissemination may be detected in patients diagnosed with ductal carcinoma in situ of the breast. Breast Cancer Res. Treat. 2012, 131, 801–808. [Google Scholar] [CrossRef]
- Wikman, H.; Vessella, R.; Pantel, K. Cancer micrometastasis and tumour dormancy. Acta. Pathol. Microbiol. Immunol. Scand. 2008, 116, 754–770. [Google Scholar] [CrossRef]
- Gomis, R.R.; Gawrzak, S. Tumor cell dormancy. Mol. Oncol. 2017, 11, 62–78. [Google Scholar] [CrossRef] [Green Version]
- Almog, N. Molecular mechanisms underlying tumor dormancy. Cancer Lett. 2010, 294, 139–146. [Google Scholar] [CrossRef]
- Pantel, K.; Brakenhoff, R.H.; Brandt, B. Detection, clinical relevance and specific biological properties of disseminating tumour cells. Nat. Rev. Cancer 2008, 8, 329–340. [Google Scholar] [CrossRef] [PubMed]
- Aguirre-Ghiso, J.A. Models, mechanisms and clinical evidence for cancer dormancy. Nat. Rev. Cancer 2007, 7, 834–846. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grabinski, N.; Bartkowiak, K.; Grupp, K.; Brandt, B.; Pantel, K.; Jücker, M. Distinct functional roles of Akt isoforms for proliferation, survival, migration and EGF-mediated signalling in lung cancer derived disseminated tumor cells. Cell Signal. 2011, 23, 1952–1960. [Google Scholar] [CrossRef] [PubMed]
- Koebel, C.M.; Vermi, W.; Swann, J.B.; Zerafa, N.; Rodig, S.J.; Old, L.J.; Smyth, M.J.; Schreiber, R.D. Adaptive immunity maintains occult cancer in an equilibrium state. Nature 2007, 450, 903–907. [Google Scholar] [CrossRef]
- Pagani, O.; Senkus, E.; Wood, W.; Colleoni, M.; Cufer, T.; Kyriakides, S.; Costa, A.; Winer, E.P.; Cardoso, F. International Guidelines for Management of Metastatic Breast Cancer: Can Metastatic Breast Cancer Be Cured? J. Natl. Cancer Inst. 2010, 102, 456–463. [Google Scholar] [CrossRef] [Green Version]
- Gavilá, J.; Lopez-Tarruella, S.; Saura, C.; Munoz, M.; Oliveira, M.; De la Cruz-Merino, L.; Morales, S.; Alvarez, I.; Virizuela, J.A.; Martin, M. SEOM clinical guidelines in metastatic breast cancer 2015. Clin. Transl. Oncol. 2015, 17, 946–955. [Google Scholar] [CrossRef] [Green Version]
- Roulot, A.; Héquet, D.; Guinebretière, J.-M.; Vincent-Salomon, A.; Lerebours, F.; Dubot, C.; Rouzier, R. Tumoral heterogeneity of breast cancer. Ann. Biol. Clin. 2016, 74, 653–660. [Google Scholar] [CrossRef]
- Santinelli, A.; Pisa, E.; Stramazzotti, D.; Fabris, G. HER-2 status discrepancy between primary breast cancer and metastatic sites. Impact on target therapy. Int. J. Cancer 2007, 122, 999–1004. [Google Scholar] [CrossRef]
- Karagöz Özen, D.S.; Ozturk, M.A.; Aydin, Ö.; Turna, Z.H.; Ilvan, S.; Özgüroglu, M. Receptor expression discrepancy between primary and metastatic breast cancer lesions. Oncol. Res. Treat. 2014, 37, 622–626. [Google Scholar] [CrossRef]
- Rosen, P.P.; Menendez-Botet, C.J.; Urban, J.A.; Fracchia, A.; Schwartz, M.K. Estrogen receptor protein (ERP) in multiple tumor specimens from individual patients with breast cancer. Cancer 1977, 39, 2194–2200. [Google Scholar] [CrossRef]
- Webster, D.J.; Bronn, D.G.; Minton, J.P. Estrogen receptor levels in multiple biopsies from patients with breast cancer. Am. J. Surg. 1978, 136, 337–338. [Google Scholar] [CrossRef]
- Holdaway, I.M.; Bowditch, J.V. Variation in receptor status between primary and metastatic breast cancer. Cancer 1983, 52, 479–485. [Google Scholar] [CrossRef]
- Foukakis, T.; Åström, G.; Lindström, L.; Hatschek, T.; Bergh, J. When to order a biopsy to characterise a metastatic relapse in breast cancer. Ann. Oncol. Off. J. Eur. Soc. Med. Oncol. 2012, 23, x349–x353. [Google Scholar] [CrossRef] [PubMed]
- Guarneri, V.; Giovannelli, S.; Ficarra, G.; Bettelli, S.; Maiorana, A.; Piacentini, F.; Barbieri, E.; Vittoria Dieci, M.; D’Amico, R.; Jovic, G.; et al. Comparison of HER-2 and hormone receptor expression in primary breast cancers and asynchronous paired metastases: Impact on patient management. Oncologist 2008, 13, 838–844. [Google Scholar] [CrossRef]
- Koren, S.; Bentires-Alj, M. Breast Tumor Heterogeneity: Source of Fitness, Hurdle for Therapy. Mol. Cell 2015, 60, 537–546. [Google Scholar] [CrossRef]
- Billaud, M. L’hétérogénéité intratumorale—Un obstacle darwinien à la médecine personnalisée? Médecine/Sciences 2012, 28, 1116–1119. [Google Scholar] [CrossRef] [Green Version]
- Vaupel, P. Hypoxia and aggressive tumor phenotype: Implications for therapy and prognosis. Oncologist 2008, 13, 21–26. [Google Scholar] [CrossRef] [Green Version]
- Dagogo-Jack, I.; Shaw, A.T. Tumour heterogeneity and resistance to cancer therapies. Nat. Rev. Clin. Oncol. 2018, 15, 81–94. [Google Scholar] [CrossRef]
- Jin, G.; Han, Y.; Liu, C.; Chen, L.; Ding, B.; Xuan, S.; Liu, X.; Ma, G.; Gao, J.; Tian, X. Evaluation of biomarker changes after administration of various neoadjuvant chemotherapies in breast cancer. Int. J. Clin. Exp. Pathol. 2015, 8, 914–921. [Google Scholar]
- Yang, Y.-F.; Liao, Y.-Y.; Li, L.-Q.; Xie, S.-R.; Xie, Y.-F.; Peng, N.-F. Changes in ER, PR and HER2 receptors status after neoadjuvant chemotherapy in breast cancer. Pathol. Res. Pract. 2013, 209, 797–802. [Google Scholar] [CrossRef]
- Yoshida, A.; Hayashi, N.; Suzuki, K.; Takimoto, M.; Nakamura, S.; Yamauchi, H. Change in HER2 status after neoadjuvant chemotherapy and the prognostic impact in patients with primary breast cancer. J. Surg. Oncol. 2017, 116, 1021–1028. [Google Scholar] [CrossRef] [PubMed]
- Botteri, E.; Disalvatore, D.; Curigliano, G.; Brollo, J.; Bagnardi, V.; Viale, G.; Orsi, F.; Goldhirsch, A.; Rotmensz, N. Biopsy of liver metastasis for women with breast cancer: Impact on survival. Breast Edinb. Scotl. 2012, 21, 284–288. [Google Scholar] [CrossRef] [PubMed]
- Van Heertum, R.L.; Scarimbolo, R.; Ford, R.; Berdougo, E.; O’Neal, M. Companion diagnostics and molecular imaging-enhanced approaches for oncology clinical trials. Drug Des. Devel. Ther. 2015, 9, 5215–5223. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sörensen, J.; Velikyan, I.; Sandberg, D.; Wennborg, A.; Feldwisch, J.; Tolmachev, V.; Orlova, A.; Sandström, M.; Lubberink, M.; Olofsson, H.; et al. Measuring HER2-Receptor Expression In Metastatic Breast Cancer Using [68 Ga] ABY-025 Affibody PET/CT. Theranostics 2016, 6, 262–271. [Google Scholar]
- Ulaner, G.A.; Hyman, D.M.; Ross, D.S.; Corben, A.; Chandarlapaty, S.; Goldfarb, S.; McArthur, H.; Erinjeri, J.P.; Solomon, S.B.; Kolb, H.; et al. Detection of HER2-Positive Metastases in Patients with HER2-Negative Primary Breast Cancer Using 89Zr-Trastuzumab PET/CT. J. Nucl. Med. Off. Publ. Soc. Nucl. Med. 2016, 57, 1523–1528. [Google Scholar] [CrossRef] [Green Version]
- Mariotto, A.B.; Etzioni, R.; Hurlbert, M.; Penberthy, L.; Mayer, M. Estimation of the Number of Women Living with Metastatic Breast Cancer in the United States. Cancer Epidemiol. Prev. Biomark. 2017, 26, 809–815. [Google Scholar] [CrossRef] [Green Version]
- Daly, M.J. Death by protein damage in irradiated cells. DNA Repair. 2012, 11, 12–21. [Google Scholar] [CrossRef] [Green Version]
- Baskar, R.; Dai, J.; Wenlong, N.; Yeo, R.; Yeoh, K.-W. Biological response of cancer cells to radiation treatment. Front. Mol. Biosci. 2014, 1, 24. [Google Scholar] [CrossRef] [Green Version]
- Prise, K.M.; Schettino, G.; Folkard, M.; Held, K.D. New insights on cell death from radiation exposure. Lancet Oncol. 2005, 6, 520–528. [Google Scholar] [CrossRef]
- Maier, P.; Hartmann, L.; Wenz, F.; Herskind, C. Cellular Pathways in Response to Ionizing Radiation and Their Targetability for Tumor Radiosensitization. Int. J. Mol. Sci. 2016, 17, 102. [Google Scholar] [CrossRef] [Green Version]
- Blower, P.J. A nuclear chocolate box: The periodic table of nuclear medicine. Dalton. Trans. Camb. Engl. 2015, 44, 4819–4844. [Google Scholar] [CrossRef] [PubMed]
- Brady, D.; O’Sullivan, J.M.; Prise, K.M. What is the Role of the Bystander Response in Radionuclide Therapies? Front. Oncol. 2013, 3, 215. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sathekge, M.; Bruchertseifer, F.; Knoesen, O.; Reyneke, F.; Lawal, I.; Lengana, T.; Davis, C.; Mahapane, J.; Corbett, C.; Vorster, M.; et al. 225Ac-PSMA-617 in chemotherapy-naive patients with advanced prostate cancer: A pilot study. Eur. J. Nucl. Med. Mol. Imaging 2019, 46, 129–138. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kratochwil, C.; Bruchertseifer, F.; Rathke, H.; Bronzel, M.; Apostolidis, C.; Weichert, W.; Haberkorn, U.; Giesel, F.L.; Morgenstern, A. Targeted α-Therapy of Metastatic Castration-Resistant Prostate Cancer with 225Ac-PSMA-617: Swimmer-Plot Analysis Suggests Efficacy Regarding Duration of Tumor Control. J. Nucl. Med. Off. Publ. Soc. Nucl. Med. 2018, 59, 795–802. [Google Scholar] [CrossRef] [Green Version]
- Kratochwil, C.; Bruchertseifer, F.; Rathke, H.; Bronzel, M.; Apostolidis, C.; Weichert, W.; Haberkorn, U.; Giesel, F.L.; Morgenstern, A. Targeted α-Therapy of Metastatic Castration-Resistant Prostate Cancer with 225Ac-PSMA-617: Dosimetry Estimate and Empiric Dose Finding. J. Nucl. Med. Off. Publ. Soc. Nucl. Med. 2017, 58, 1624–1631. [Google Scholar]
- Liu, F.; Zhu, H.; Yu, J.; Han, X.; Xie, Q.; Liu, T.; Xia, C.; Li, N.; Yang, Z. 68Ga/177Lu-labeled DOTA-TATE shows similar imaging and biodistribution in neuroendocrine tumor model. Tumour. Biol. J. Int. Soc. Oncodev. Biol. Med. 2017, 39, 1010428317705519. [Google Scholar] [CrossRef] [Green Version]
- Maffey-Steffan, J.; Scarpa, L.; Svirydenka, A.; Fink, K.; Bektic, J.; Gruber, L.; Decristoforo, C.; Uprimny, C.; Lukas, P.; Horninger, W.; et al. The 68Ga/177Lu-theragnostic concept in PSMA-targeting of metastatic castration-resistant prostate cancer: Impact of post-therapeutic whole-body scintigraphy in the follow-up. Eur. J. Nucl. Med. Mol. Imaging 2020, 47, 695–712. [Google Scholar] [CrossRef] [Green Version]
- Dalm, S.U.; Bakker, I.L.; de Blois, E.; Doeswijk, G.N.; Konijnenberg, M.W.; Orlandi, F.; Barbato, D.; Tedesco, M.; Maina, T.; Nock, B.A.; et al. 68Ga/177Lu-NeoBOMB1, a Novel Radiolabeled GRPR Antagonist for Theranostic Use in Oncology. J. Nucl. Med. Off. Publ. Soc. Nucl. Med. 2017, 58, 293–299. [Google Scholar]
- Strosberg, J.; El-Haddad, G.; Wolin, E.; Hendifar, A.; Yao, J.; Chasen, B.; Mittra, E.; Kunz, P.L.; Kulke, M.H.; Jacene, H.; et al. Phase 3 Trial of 177Lu-Dotatate for Midgut Neuroendocrine Tumors. N. Engl. J. Med. 2017, 376, 125–135. [Google Scholar] [CrossRef]
- Kabasakal, L.; Toklu, T.; Yeyin, N.; Demirci, E.; Abuqbeitah, M.; Ocak, M.; Aygün, A.; Karayel, E.; Pehlivanoğlu, H.; Alan Selçuk, N. Lu-177-PSMA-617 Prostate-Specific Membrane Antigen Inhibitor Therapy in Patients with Castration-Resistant Prostate Cancer: Stability, Bio-distribution and Dosimetry. Mol. Imaging Radionucl. Ther. 2017, 26, 62–68. [Google Scholar] [CrossRef]
- Han, S.; Woo, S.; Kim, Y.J.; Suh, C.H. Impact of 68Ga-PSMA PET on the Management of Patients with Prostate Cancer: A Systematic Review and Meta-analysis. Eur. Urol. 2018, 74, 179–190. [Google Scholar] [CrossRef] [PubMed]
- Marcu, L.; Bezak, E.; Allen, B.J. Global comparison of targeted alpha vs targeted beta therapy for cancer: In vitro, in vivo and clinical trials. Crit. Rev. Oncol. Hematol. 2018, 123, 7–20. [Google Scholar] [CrossRef] [PubMed]
- Tamura, K.; Kurihara, H.; Yonemori, K.; Tsuda, H.; Suzuki, J.; Kono, Y.; Honda, N.; Kodaira, M.; Yamamoto, H.; Yunokawa, M.; et al. 64Cu-DOTA-trastuzumab PET imaging in patients with HER2-positive breast cancer. J. Nucl. Med. Off. Publ. Soc. Nucl. Med. 2013, 54, 1869–1875. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dijkers, E.C.F.; Kosterink, J.G.W.; Rademaker, A.P.; Perk, L.R.; van Dongen, G.A.; Bart, J.; de Jong, J.R.; de Vries, E.G.; Lub-de Hooge, M.N. Development and characterization of clinical-grade 89Zr-trastuzumab for HER2/neu immunoPET imaging. J. Nucl. Med. Off. Publ. Soc. Nucl. Med. 2009, 50, 974–981. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vaneycken, I.; Devoogdt, N.; Van Gassen, N.; Vincke, C.; Xavier, C.; Wernery, U.; Muyldermans, S.; Lahoutte, T.; Caveliers, V. Preclinical screening of anti-HER2 nanobodies for molecular imaging of breast cancer. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2011, 25, 2433–2446. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xavier, C.; Vaneycken, I.; D’huyvetter, M.; Heemskerk, J.; Keyaerts, M.; Vincke, C.; Devoogdt, N.; Muyldermans, S.; Lahoutte, T.; Caveliers, V. Synthesis, preclinical validation, dosimetry, and toxicity of 68Ga-NOTA-anti-HER2 Nanobodies for iPET imaging of HER2 receptor expression in cancer. J. Nucl. Med. Off. Publ. Soc. Nucl. Med. 2013, 54, 776–784. [Google Scholar] [CrossRef] [Green Version]
- D’Huyvetter, M.; Vincke, C.; Xavier, C.; Aerts, A.; Impens, N.; Baatout, S.; De Raeve, H.; Muyldermans, S.; Caveliers, V.; Devoogdt, N.; et al. Targeted radionuclide therapy with A 177Lu-labeled anti-HER2 nanobody. Theranostics 2014, 4, 708–720. [Google Scholar] [CrossRef] [Green Version]
- Keyaerts, M.; Xavier, C.; Heemskerk, J.; Devoogdt, N.; Everaert, H.; Ackaert, C.; Vanhoeij, M.; Duhoux, F.P.; Gevaert, T.; Simon, P.; et al. Phase I Study of 68Ga-HER2-Nanobody for PET/CT Assessment of HER2 Expression in Breast Carcinoma. J. Nucl. Med. Off. Publ. Soc. Nucl. Med. 2016, 57, 27–33. [Google Scholar] [CrossRef] [Green Version]
- McGuire, A.H.; Dehdashti, F.; Siegel, B.A.; Lyss, A.P.; Brodack, J.W.; Mathias, C.J.; Mintun, M.A.; Katzenellenbogen, J.A.; Welch, M.J. Positron Tomographic Assessment of 16a-[18F] Fluoro-17/3-Estradiol Uptake in Metastatic Breast Carcinoma. J. Nucl. Med. 1991, 32, 1526–1531. [Google Scholar]
- Evangelista, L.; Guarneri, V.; Conte, P.F. 18F-Fluoroestradiol Positron Emission Tomography in Breast Cancer Patients: Systematic Review of the Literature & Meta-Analysis. Curr. Radiopharm. 2016, 9, 244–257. [Google Scholar]
- Koleva-Kolarova, R.G.; Greuter, M.J.W.; van Kruchten, M.; Vermeulen, K.M.; Feenstra, T.; Buskens, E.; Glaudemans, A.W.J.M.; de Vries, E.F.J.; de Vries, E.G.E.; Hospers, G.A.P.; et al. The value of PET/CT with FES or FDG tracers in metastatic breast cancer: A computer simulation study in ER-positive patients. Br. J. Cancer 2015, 112, 1617–1625. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mortimer, J.E.; Dehdashti, F.; Siegel, B.A.; Trinkaus, K.; Katzenellenbogen, J.A.; Welch, M.J. Metabolic Flare: Indicator of Hormone Responsiveness in Advanced Breast Cancer. J. Clin. Oncol. 2001, 19, 2797–2803. [Google Scholar] [CrossRef] [PubMed]
- Chae, S.Y.; Ahn, S.H.; Kim, S.-B.; Han, S.; Lee, S.H.; Oh, S.J.; Lee, S.J.; Kim, H.J.; Ko, B.S.; Lee, J.W.; et al. Diagnostic accuracy and safety of 16α-[18F]fluoro-17β-oestradiol PET-CT for the assessment of oestrogen receptor status in recurrent or metastatic lesions in patients with breast cancer: A prospective cohort study. Lancet Oncol. 2019, 20, 546–555. [Google Scholar] [CrossRef]
- Edmonds, C.E.; Makvandi, M.; Lieberman, B.P.; Xu, K.; Zeng, C.; Li, S.; Hou, C.; Lee, H.; Greenberg, R.A.; Mankoff, D.A.; et al. [18F]FluorThanatrace uptake as a marker of PARP1 expression and activity in breast cancer. Am. J. Nucl. Med. Mol. Imaging 2016, 6, 94–101. [Google Scholar]
- Rahbar, K.; Schmidt, M.; Heinzel, A.; Eppard, E.; Bode, A.; Yordanova, A.; Claesener, M.; Ahmadzadehfar, H. Response and Tolerability of a Single Dose of 177Lu-PSMA-617 in Patients with Metastatic Castration-Resistant Prostate Cancer: A Multicenter Retrospective Analysis. J. Nucl. Med. Off. Publ. Soc. Nucl. Med. 2016, 57, 1334–1338. [Google Scholar] [CrossRef] [Green Version]
- Hofman, M.S.; Violet, J.; Hicks, R.J.; Ferdinandus, J.; Thang, S.P.; Akhurst, T.; Iravani, A.; Kong, G.; Ravi Kumar, A.; Murphy, D.G.; et al. [177Lu]-PSMA-617 radionuclide treatment in patients with metastatic castration-resistant prostate cancer (LuPSMA trial): A single-centre, single-arm, phase 2 study. Lancet Oncol. 2018, 19, 825–833. [Google Scholar] [CrossRef]
- Broos, K.; Lecocq, Q.; Raes, G.; Devoogdt, N.; Keyaerts, M.; Breckpot, K. Noninvasive imaging of the PD-1:PD-L1 immune checkpoint: Embracing nuclear medicine for the benefit of personalized immunotherapy. Theranostics 2018, 8, 3559–3570. [Google Scholar] [CrossRef]
- Vag, T.; Steiger, K.; Rossmann, A.; Keller, U.; Noske, A.; Herhaus, P.; Ettl, J.; Niemeyer, M.; Wester, H.-J.; Schwaiger, M. PET imaging of chemokine receptor CXCR4 in patients with primary and recurrent breast carcinoma. EJNMMI Res. 2018, 8, 90. [Google Scholar] [CrossRef]
- Kobayashi, K.; Sasaki, T.; Takenaka, F.; Yakushiji, H.; Fujii, Y.; Kishi, Y.; Kita, S.; Shen, L.; Kumon, H.; Matsuura, E. A novel PET imaging using 64Cu-labeled monoclonal antibody against mesothelin commonly expressed on cancer cells. J. Immunol. Res. 2015, 2015, 268172. [Google Scholar] [CrossRef] [Green Version]
- ter Weele, E.J.; Terwisscha van Scheltinga, A.G.T.; Kosterink, J.G.W.; Pot, L.; Vedelaar, S.R.; Lamberts, L.E.; Williams, S.P.; Lub-de Hooge, M.N.; de Vries, E.G. Imaging the distribution of an antibody-drug conjugate constituent targeting mesothelin with 89Zr and IRDye 800CW in mice bearing human pancreatic tumor xenografts. Oncotarget 2015, 6, 42081–42090. [Google Scholar] [CrossRef] [Green Version]
- Montemagno, C.; Bacot, S.; Ahmadi, M.; Kerfelec, B.; Baty, D.; Debiossat, M.; Soubies, A.; Perret, P.; Riou, L.; Fagret, D.; et al. Preclinical Evaluation of Mesothelin-Specific Ligands for SPECT Imaging of Triple-Negative Breast Cancer. J. Nucl. Med. Off. Publ. Soc. Nucl. Med. 2018, 59, 1056–1062. [Google Scholar] [CrossRef] [PubMed]
- Morgat, C.; MacGrogan, G.; Brouste, V.; Vélasco, V.; Sévenet, N.; Bonnefoi, H.; Fernandez, P.; Debled, M.; Hindié, E. Expression of Gastrin-Releasing Peptide Receptor in Breast Cancer and Its Association with Pathologic, Biologic, and Clinical Parameters: A Study of 1,432 Primary Tumors. J. Nucl. Med. 2017, 58, 1401–1407. [Google Scholar] [CrossRef] [PubMed]
- Reubi, J.C.; Wenger, S.; Schmuckli-Maurer, J.; Schaer, J.-C.; Gugger, M. Bombesin receptor subtypes in human cancers: Detection with the universal radioligand (125) I-[D-TYR(6), beta-ALA(11), PHE(13), NLE(14)] bombesin(6-14). Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2002, 8, 1139–1146. [Google Scholar]
- Jiang, X.; Li, W.; Li, X.; Bai, H.; Zhang, Z. Current status and future prospects of PARP inhibitor clinical trials in ovarian cancer. Cancer Manag. Res. 2019, 11, 4371–4390. [Google Scholar] [CrossRef] [Green Version]
- Zhou, D.; Chu, W.; Xu, J.; Jones, L.A.; Peng, X.; Li, S.; Chen, D.L.; Mach, R.H. Synthesis, [18F] radiolabeling, and evaluation of poly (ADP-ribose) polymerase-1 (PARP-1) inhibitors for in vivo imaging of PARP-1 using positron emission tomography. Bioorg. Med. Chem. 2014, 22, 1700–1707. [Google Scholar] [CrossRef] [Green Version]
- Hassan, R.; Thomas, A.; Alewine, C.; Le, D.T.; Jaffee, E.M.; Pastan, I. Mesothelin Immunotherapy for Cancer: Ready for Prime Time? J. Clin. Oncol. 2016, 34, 4171–4179. [Google Scholar] [CrossRef] [Green Version]
- Pastan, I.; Hassan, R. Discovery of mesothelin and exploiting it as a target for immunotherapy. Cancer Res. 2014, 74, 2907–2912. [Google Scholar] [CrossRef] [Green Version]
- Singh, D.; Attri, B.K.; Gill, R.K.; Bariwal, J. Review on EGFR Inhibitors: Critical Updates. Mini Rev. Med. Chem. 2016, 16, 1134–1166. [Google Scholar] [CrossRef]
- Chen, W.; Shen, B.; Sun, X. Analysis of Progress and Challenges of EGFR-Targeted Molecular Imaging in Cancer with a Focus on Affibody Molecules. Mol. Imaging 2019, 18. [Google Scholar] [CrossRef] [Green Version]
- Santos do Carmo, F.; Ricci-Junior, E.; Cerqueira-Coutinho, C.; Albernaz, M.; Bernardes, E.S.; Missailidis, S.; Santos-Oliveira, R. Anti-MUC1 nano-aptamers for triple-negative breast cancer imaging by single-photon emission computed tomography in inducted animals: Initial considerations. Int. J. Nanomed. 2016, 12, 53–60. [Google Scholar] [CrossRef] [Green Version]
Molecular Target | Expression in Breast Cancer (%) | Theranostic Molecule | Clinical Trial | References |
---|---|---|---|---|
PARP | 45% | 18F-fluorthanatrace | Yes | [84] |
Gastrin-Releasing | 75.8% | 68Ga-NeoBOMB1 | Yes | [68] |
Peptide Receptor | 177Lu-NeoBOMB1 | Yes | ||
PSMA | 60% | 68Ga-PSMA-617 | Yes | [71,85,86] |
177Lu-PSMA-617 | Yes | |||
PD-1/PD-L1 | 29% to 50% | 89Zr-Pembrolizumab | Yes (Phase II) | [87] |
89Zr-Atezolizumab | Yes (Phase I) | |||
18F or 89Zr-Adnectin | Yes (Feasibility) | |||
99mTc-Nb | Yes (Phase I) | |||
CXCR-4 | 56% | 68Ga-Pentixafor | Yes | [88] |
Mesothelin | 30% | 89Zr-mAb (MM0T0530A) | Phase I | [89,90,91] |
111In-Amatuximab | Phase I | |||
99mTc-A1 | No |
© 2020 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 (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Montemagno, C.; Pagès, G. Metastatic Heterogeneity of Breast Cancer: Companion and Theranostic Approach in Nuclear Medicine. Cancers 2020, 12, 821. https://doi.org/10.3390/cancers12040821
Montemagno C, Pagès G. Metastatic Heterogeneity of Breast Cancer: Companion and Theranostic Approach in Nuclear Medicine. Cancers. 2020; 12(4):821. https://doi.org/10.3390/cancers12040821
Chicago/Turabian StyleMontemagno, Christopher, and Gilles Pagès. 2020. "Metastatic Heterogeneity of Breast Cancer: Companion and Theranostic Approach in Nuclear Medicine" Cancers 12, no. 4: 821. https://doi.org/10.3390/cancers12040821