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Current Topics in Medicinal Chemistry


ISSN (Print): 1568-0266
ISSN (Online): 1873-4294

Review Article

Peptide Receptor Radionuclide Therapy: Looking Back, Looking Forward

Author(s): Danny Feijtel, Marion de Jong and Julie Nonnekens*

Volume 20, Issue 32, 2020

Page: [2959 - 2969] Pages: 11

DOI: 10.2174/1568026620666200226104652

open access plus


Peptide receptor radionuclide therapy (PRRT) is a highly effective anti-cancer treatment modality for patients with non-resectable, metastasized neuroendocrine tumors (NETs). During PRRT, specific receptors that are overexpressed on the cancer cells are targeted with a peptide labeled with a DNA-damaging radionuclide. Even though PRRT is a powerful treatment for metastasized NET patients, the majority still cannot be cured at this stage of the disease. Hence, many investigators focus on improving the therapeutic efficacy of this therapy. Improving PRRT can, for example, be achieved by using other radionuclides with different physical properties, by combining PRRT with radiosensitizing agents or by radiolabeling peptides with different characteristics. However, due to lack of extensive knowledge of radiobiological responses of cancer cells to PRRT, biological parameters that influence absorbed dose or that might even elicit insensitivity to therapy remain elusive and the context in which these improvements will be successful warrants further investigation. In this review, we will discuss the development of PRRT, its clinical merits in current treatment and future perspectives. We will highlight different radionuclides and their benefits and pitfalls, as well as different peptide-conjugates that hold these radionuclides. We will zoom in on the latest developments regarding combinatorial treatments and how investigators from different disciplines such as dosimetry and radiobiology are now joining forces to improve PRRT for NETs.

Keywords: Peptide receptor radionuclide therapy (PRRT), Combination therapy, Neuroendocrine tumors (NET), Radiopharmaceuticals, Radiobiology, Therapeutic effects.

Graphical Abstract
Riihimäki, M.; Hemminki, A.; Sundquist, K.; Sundquist, J.; Hemminki, K. The epidemiology of metastases in neuroendocrine tumors. Int. J. Cancer, 2016, 139(12), 2679-2686.
[] [PMID: 27553864]
Kim, J.Y.; Hong, S.M.; Ro, J.Y. Recent updates on grading and classification of neuroendocrine tumors. Ann. Diagn. Pathol., 2017, 29, 11-16.
[] [PMID: 28807335]
Barakat, M.T.; Meeran, K.; Bloom, S.R. Neuroendocrine tumours. Endocr. Relat. Cancer, 2004, 11(1), 1-18.
[] [PMID: 15027882]
Hofving, T.; Arvidsson, Y.; Almobarak, B.; Inge, L.; Pfragner, R.; Persson, M.; Stenman, G.; Kristiansson, E.; Johanson, V.; Nilsson, O. The neuroendocrine phenotype, genomic profile and therapeutic sensitivity of GEPNET cell lines. Endocr. Relat. Cancer, 2018, 25(3), 367-380.
[] [PMID: 29444910]
Modlin, I.M.; Gustafsson, B.I.; Moss, S.F.; Pavel, M.; Tsolakis, A.V.; Kidd, M.; Chromogranin, A. Chromogranin A--biological function and clinical utility in neuro endocrine tumor disease. Ann. Surg. Oncol., 2010, 17(9), 2427-2443.
[] [PMID: 20217257]
Gould, V.E.; Lee, I.; Wiedenmann, B.; Moll, R.; Chejfec, G.; Franke, W.W. Synaptophysin: a novel marker for neurons, certain neuroendocrine cells, and their neoplasms. Hum. Pathol., 1986, 17(10), 979-983.
[] [PMID: 3093369]
Kulaksiz, H.; Eissele, R.; Rössler, D.; Schulz, S.; Höllt, V.; Cetin, Y.; Arnold, R. Identification of somatostatin receptor subtypes 1, 2A, 3, and 5 in neuroendocrine tumours with subtype specific antibodies. Gut, 2002, 50(1), 52-60.
[] [PMID: 11772967]
Wolin, E.M. The expanding role of somatostatin analogs in the management of neuroendocrine tumors. Gastrointest. Cancer Res., 2012, 5(5), 161-168.
[PMID: 23112884]
Krenning, E.P.; Bakker, W.H.; Breeman, W.A.; Koper, J.W.; Kooij, P.P.; Ausema, L.; Lameris, J.S.; Reubi, J.C.; Lamberts, S.W. Localisation of endocrine-related tumours with radioiodinated analogue of somatostatin. Lancet, 1989, 1(8632), 242-244.
[] [PMID: 2563413]
Krenning, E.P.; Kwekkeboom, D.J.; Bakker, W.H.; Breeman, W.A.; Kooij, P.P.; Oei, H.Y.; van Hagen, M.; Postema, P.T.; de Jong, M.; Reubi, J.C. Somatostatin receptor scintigraphy with [111In-DTPA-D-Phe1]- and [123I-Tyr3]-octreotide: the Rotterdam experience with more than 1000 patients. Eur. J. Nucl. Med., 1993, 20(8), 716-731.
[] [PMID: 8404961]
Baum, R.P.; Kulkarni, H.R. THERANOSTICS: From molecular imaging using Ga-68 labeled tracers and PET/CT to personalized radionuclide therapy - The bad berka experience. Theranostics, 2012, 2(5), 437-447.
[] [PMID: 22768024]
Krenning, E.P.; Kooij, P.P.; Bakker, W.H.; Breeman, W.A.; Postema, P.T.; Kwekkeboom, D.J.; Oei, H.Y.; de Jong, M.; Visser, T.J.; Reijs, A.E. Radiotherapy with a radiolabeled somatostatin analogue, [111In-DTPA-D-Phe1]-octreotide. A case history. Ann. N. Y. Acad. Sci., 1994, 733, 496-506.
[] [PMID: 7978900]
Fjälling, M.; Andersson, P.; Forssell-Aronsson, E.; Grétarsdóttir, J.; Johansson, V.; Tisell, L.E.; Wängberg, B.; Nilsson, O.; Berg, G.; Michanek, A.; Lindstedt, G.; Ahlman, H. Systemic radionuclide therapy using indium-111-DTPA-D-Phe1-octreotide in midgut carcinoid syndrome. J. Nucl. Med., 1996, 37(9), 1519-1521.
[PMID: 8790206]
Bomanji, J. B.; Papathanasiou, N. D. (1)(1)(1)In-DTPA(0)- octreotide (Octreoscan), (1)(3)(1)I-MIBG and other agents for radionuclide therapy of NETs. Eur. J. Nucl. Med. Mol. Imaging, 2012, 39(Suppl. 1)(1), S113-25.
Levine, R.; Krenning, E.P. Clinical history of the theranostic radionuclide approach to neuroendocrine tumors and other types of cancer: Historical review based on an interview of Eric P. Krenning by Rachel Levine. J. Nucl. Med., 2017, 58(Suppl. 2), 3S-9S.
[] [PMID: 28864612]
Strosberg, J.; El-Haddad, G.; Wolin, E.; Hendifar, A.; Yao, J.; Chasen, B.; Mittra, E.; Kunz, P.L.; Kulke, M.H.; Jacene, H.; Bushnell, D.; O’Dorisio, T.M.; Baum, R.P.; Kulkarni, H.R.; Caplin, M.; Lebtahi, R.; Hobday, T.; Delpassand, E.; Van Cutsem, E.; Benson, A.; Srirajaskanthan, R.; Pavel, M.; Mora, J.; Berlin, J.; Grande, E.; Reed, N.; Seregni, E.; Öberg, K.; Lopera Sierra, M.; Santoro, P.; Thevenet, T.; Erion, J.L.; Ruszniewski, P.; Kwekkeboom, D.; Krenning, E. Phase 3 trial of 177Lu-dotatate for midgut neuroendocrine tumors. N. Engl. J. Med., 2017, 376(2), 125-135.
[] [PMID: 28076709]
Choppin, G.R.; Liljenzin, J-O.; Rydberg, J.A.N. CHAPTER 7 - Radiation Effects on Matter**This chapter has been revised by Prof. T. Eriksen, Royal Institute of Technology, Stockholm. In: Radiochemistry and Nuclear Chemistry (Third Edition); Choppin, G.R.; Liljenzin, J-O.; Rydberg, J.A.N., Eds.; Butterworth- Heinemann: Woburn , 2002; pp. 166-191.
Kassis, A.I. The amazing world of auger electrons. Int. J. Radiat. Biol., 2004, 80(11-12), 789-803.
[] [PMID: 15764386]
Kassis, A.I. Therapeutic radionuclides: biophysical and radiobiologic principles. Semin. Nucl. Med., 2008, 38(5), 358-366.
[] [PMID: 18662557]
Kondev, F.G. Nuclear Data Sheets for A = 177. Nucl. Data Sheets (N.Y. N.Y.), 2003, 98(4), 801-1095.
Schötzig, U.; Schrader, H.; Schönfeld, E.; Günther, E.; Klein, R. Standardisation and decay data of 177Lu and 188Re. Appl. Radiat. Isot., 2001, 55(1), 89-96.
[] [PMID: 11339536]
Bodei, L.; Mueller-Brand, J.; Baum, R.P.; Pavel, M.E.; Hörsch, D.; O’Dorisio, M.S.; O’Dorisio, T.M.; Howe, J.R.; Cremonesi, M.; Kwekkeboom, D.J.; Zaknun, J.J. The joint IAEA, EANM, and SNMMI practical guidance on peptide receptor radionuclide therapy (PRRNT) in neuroendocrine tumours. Eur. J. Nucl. Med. Mol. Imaging, 2013, 40(5), 800-816.
[] [PMID: 23389427]
Valkema, R.; Pauwels, S.; Kvols, L.K.; Barone, R.; Jamar, F.; Bakker, W.H.; Kwekkeboom, D.J.; Bouterfa, H.; Krenning, E.P. Survival and response after peptide receptor radionuclide therapy with [90Y-DOTA0,Tyr3]octreotide in patients with advanced gastroenteropancreatic neuroendocrine tumors. Semin. Nucl. Med., 2006, 36(2), 147-156.
[] [PMID: 16517236]
Miller, W.H.; Hartmann-Siantar, C.; Fisher, D.; Descalle, M.A.; Daly, T.; Lehmann, J.; Lewis, M.R.; Hoffman, T.; Smith, J.; Situ, P.D.; Volkert, W.A. Evaluation of beta-absorbed fractions in a mouse model for 90Y, 188Re, 166Ho, 149Pm, 64Cu, and 177Lu radionuclides. Cancer Biother. Radiopharm., 2005, 20(4), 436-449.
[] [PMID: 16114992]
Gudkov, S.V.; Shilyagina, N.Y.; Vodeneev, V.A.; Zvyagin, A.V. Targeted radionuclide therapy of human tumors. Int. J. Mol. Sci., 2015, 17(1), 33.
[] [PMID: 26729091]
Capello, A.; Krenning, E.P.; Breeman, W.A.; Bernard, B.F.; Konijnenberg, M.W.; de Jong, M. Tyr3-octreotide and Tyr3-octreotate radiolabeled with 177Lu or 90Y: peptide receptor radionuclide therapy results in vitro. Cancer Biother. Radiopharm., 2003, 18(5), 761-768.
[] [PMID: 14629824]
Vinjamuri, S.; Gilbert, T.M.; Banks, M.; McKane, G.; Maltby, P.; Poston, G.; Weissman, H.; Palmer, D.H.; Vora, J.; Pritchard, D.M.; Cuthbertson, D.J. Peptide receptor radionuclide therapy with (90)Y-DOTATATE/(90)Y-DOTATOC in patients with progressive metastatic neuroendocrine tumours: assessment of response, survival and toxicity. Br. J. Cancer, 2013, 108(7), 1440-1448.
[] [PMID: 23492685]
Wu, T-J.; Chiu, H-Y.; Yu, J.; Cautela, M.P.; Sarmento, B. Chapter 1 Nanotechnologies for early diagnosis, in situ disease monitoring, and prevention.Nanotechnologies in Preventive and Regenerative Medicine; Uskoković, V.; Uskoković, D.P., Eds.; Elsevier: Amsterdam, 2018, pp. 1-92.
Chinol, M.; Franceschini, R.; Paganelli, G.; Pecorale, A.; Paiano, A. Simple production of Yttrium-90 in a chemical form suitable to clinical grade radioconjugates. Proceedings of the 22nd International Badgastein Symposium, 1997, pp. 327-332.
Kunikowska, J.; Królicki, L.; Hubalewska-Dydejczyk, A.; Mikołajczak, R.; Sowa-Staszczak, A.; Pawlak, D. Clinical results of radionuclide therapy of neuroendocrine tumours with 90Y-DOTATATE and tandem 90Y/177Lu-DOTATATE: which is a better therapy option? Eur. J. Nucl. Med. Mol. Imaging, 2011, 38(10), 1788-1797.
[] [PMID: 21553086]
Valkema, R.; Pauwels, S.A.; Kvols, L.K.; Kwekkeboom, D.J.; Jamar, F.; de Jong, M.; Barone, R.; Walrand, S.; Kooij, P.P.; Bakker, W.H.; Lasher, J.; Krenning, E.P. Long-term follow-up of renal function after peptide receptor radiation therapy with (90)Y-DOTA(0),Tyr(3)-octreotide and (177)Lu-DOTA(0), Tyr(3)-octreotate. J. Nucl. Med., 2005, 46(Suppl. 1), 83S-91S.
[PMID: 15653656]
Cremonesi, M.; Ferrari, M.E.; Bodei, L.; Chiesa, C.; Sarnelli, A.; Garibaldi, C.; Pacilio, M.; Strigari, L.; Summers, P.E.; Orecchia, R.; Grana, C.M.; Botta, F. Correlation of dose with toxicity and tumour response to 90Y- and 177Lu-PRRT provides the basis for optimization through individualized treatment planning. Eur. J. Nucl. Med. Mol. Imaging, 2018, 45(13), 2426-2441.
[] [PMID: 29785514]
Rolleman, E.J.; Valkema, R.; de Jong, M.; Kooij, P.P.; Krenning, E.P. Safe and effective inhibition of renal uptake of radiolabelled octreotide by a combination of lysine and arginine. Eur. J. Nucl. Med. Mol. Imaging, 2003, 30(1), 9-15.
[] [PMID: 12483404]
Lenain, R.; Hamroun, A.; Lion, G.; Chamley, P.; Bui, L.; Lionet, A.; Hazzan, M.; Provôt, F. Description of a transient proximal tubulopathy induced by amino acids perfusion in peptide receptor radionuclide therapy: A case report. Medicine (Baltimore), 2019, 98(52)e18478
[] [PMID: 31876733]
Todorović-Tirnanić, M.; Kaemmerer, D.; Prasad, V.; Hommann, M.; Baum, R.P. Intraoperative somatostatin receptor detection after peptide receptor radionuclide therapy with (177)Lu- and (90)Y-DOTATOC (tandem PRRNT) in a patient with a metastatic neuroendocrine tumor. Recent Results Cancer Res., 2013, 194, 487-496.
[] [PMID: 22918778]
Baum, R.P.; Kulkarni, H.R.; Singh, A.; Kaemmerer, D.; Mueller, D.; Prasad, V.; Hommann, M.; Robiller, F.C.; Niepsch, K.; Franz, H.; Jochems, A.; Lambin, P.; Hörsch, D. Results and adverse events of personalized peptide receptor radionuclide therapy with 90Yttrium and 177Lutetium in 1048 patients with neuroendocrine neoplasms. Oncotarget, 2018, 9(24), 16932-16950.
[] [PMID: 29682195]
Seregni, E.; Maccauro, M.; Chiesa, C.; Mariani, L.; Pascali, C.; Mazzaferro, V.; De Braud, F.; Buzzoni, R.; Milione, M.; Lorenzoni, A.; Bogni, A.; Coliva, A.; Lo Vullo, S.; Bombardieri, E. Treatment with tandem [90Y]DOTA-TATE and [177Lu]DOTA-TATE of neuroendocrine tumours refractory to conventional therapy. Eur. J. Nucl. Med. Mol. Imaging, 2014, 41(2), 223-230.
[] [PMID: 24233003]
Hörsch, D.; Ezziddin, S.; Haug, A.; Gratz, K.F.; Dunkelmann, S.; Miederer, M.; Schreckenberger, M.; Krause, B.J.; Bengel, F.M.; Bartenstein, P.; Biersack, H.J.; Pöpperl, G.; Baum, R.P. Effectiveness and side-effects of peptide receptor radionuclide therapy for neuroendocrine neoplasms in Germany: A multi-institutional registry study with prospective follow-up. Eur. J. Cancer, 2016, 58, 41-51.
[] [PMID: 26943056]
Navalkissoor, S.; Grossman, A. Targeted alpha particle therapy for neuroendocrine tumours: The next generation of peptide receptor radionuclide therapy. Neuroendocrinology, 2019, 108(3), 256-264.
[PMID: 30352433]
Chan, H.S.; de Blois, E.; Morgenstern, A.; Bruchertseifer, F.; de Jong, M.; Breeman, W.; Konijnenberg, M. In Vitro comparison of 213Bi- and 177Lu-radiation for peptide receptor radionuclide therapy. PLoS One, 2017, 12(7)e0181473
[] [PMID: 28732021]
Nayak, T.K.; Norenberg, J.P.; Anderson, T.L.; Prossnitz, E.R.; Stabin, M.G.; Atcher, R.W. Somatostatin-receptor-targeted alpha-emitting 213Bi is therapeutically more effective than beta(-)-emitting 177Lu in human pancreatic adenocarcinoma cells. Nucl. Med. Biol., 2007, 34(2), 185-193.
[] [PMID: 17307126]
Chan, H.S.; Konijnenberg, M.W.; de Blois, E.; Koelewijn, S.; Baum, R.P.; Morgenstern, A.; Bruchertseifer, F.; Breeman, W.A.; de Jong, M. Influence of tumour size on the efficacy of targeted alpha therapy with (213)Bi-[DOTA(0),Tyr(3)]-octreotate. EJNMMI Res., 2016, 6(1), 6.
[] [PMID: 26791386]
Miederer, M.; Scheinberg, D.A.; McDevitt, M.R. Realizing the potential of the Actinium-225 radionuclide generator in targeted alpha particle therapy applications. Adv. Drug Deliv. Rev., 2008, 60(12), 1371-1382.
[] [PMID: 18514364]
Scheinberg, D.A.; McDevitt, M.R. Actinium-225 in targeted alpha-particle therapeutic applications. Curr. Radiopharm., 2011, 4(4), 306-320.
[] [PMID: 22202153]
Miederer, M.; Henriksen, G.; Alke, A.; Mossbrugger, I.; Quintanilla-Martinez, L.; Senekowitsch-Schmidtke, R.; Essler, M. Preclinical evaluation of the alpha-particle generator nuclide 225Ac for somatostatin receptor radiotherapy of neuroendocrine tumors. Clin. Cancer Res., 2008, 14(11), 3555-3561.
[] [PMID: 18519789]
Ballal, S.; Yadav, M.; Bal, C.; Tripathi, M.; Sahoo, R. Early results of 225Ac-DOTATATE targeted alpha therapy in metastatic gastroenteropancreatic neuroendocrine tumors: First clinical experience on safety and efficacy. J. Nucl. Med., 2019, •••, 60.
Kratochwil, C.; Giesel, F.L.; Bruchertseifer, F.; Mier, W.; Apostolidis, C.; Boll, R.; Murphy, K.; Haberkorn, U.; Morgenstern, A. (2)(1)(3)Bi-DOTATOC receptor-targeted alpha-radionuclide therapy induces remission in neuroendocrine tumours refractory to beta radiation: a first-in-human experience. Eur. J. Nucl. Med. Mol. Imaging, 2014, 41(11), 2106-2119.
[] [PMID: 25070685]
Sathekge, M.; Bruchertseifer, F.; Knoesen, O.; Reyneke, F.; Lawal, I.; Lengana, T.; Davis, C.; Mahapane, J.; Corbett, C.; Vorster, M.; Morgenstern, A. 225Ac-PSMA-617 in chemotherapy-naive patients with advanced prostate cancer: a pilot study. Eur. J. Nucl. Med. Mol. Imaging, 2019, 46(1), 129-138.
[] [PMID: 30232539]
Jurcic, J.G. Clinical studies with bismuth-213 and actinium-225 for hematologic malignancies. Curr. Radiopharm., 2018, 11(3), 192-199.
[] [PMID: 29793418]
Delpassand, E.; Tworowska, I.; Shanoon, F.; Nunez, R.; Flores Ii, L.; Muzammil, A.; Stallons, T.; Saidi, A.; Torgue, J. First clinical experience using targeted alpha-emitter therapy with 212Pb-DOTAMTATE (AlphaMedixTM) in patients with SSTR(+) neuroendocrine tumors. J. Nucl. Med., 2019, 60(Suppl. 1), 559-559.
Langbein, T.; Chaussé, G.; Baum, R.P. Salivary gland toxicity of PSMA radioligand therapy: Relevance and preventive strategies. J. Nucl. Med., 2018, 59(8), 1172-1173.
[] [PMID: 29903929]
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., 2017, 58(10), 1624-1631.
[] [PMID: 28408529]
Kruijff, R.M.; Raavé, R.; Kip, A.; Molkenboer-Kuenen, J.; Morgenstern, A.; Bruchertseifer, F.; Heskamp, S.; Denkova, A.G. The in vivo fate of 225Ac daughter nuclides using polymersomes as a model carrier. Sci. Rep., 2019, 9(1), 11671.
[] [PMID: 31406320]
Price, E.W.; Orvig, C. Matching chelators to radiometals for radiopharmaceuticals. Chem. Soc. Rev., 2014, 43(1), 260-290.
[] [PMID: 24173525]
De León-Rodríguez, L.M.; Kovacs, Z. The synthesis and chelation chemistry of DOTA-peptide conjugates. Bioconjug. Chem., 2008, 19(2), 391-402.
[] [PMID: 18072717]
Ferreira, C.L.; Yapp, D.T.; Lamsa, E.; Gleave, M.; Bensimon, C.; Jurek, P.; Kiefer, G.E. Evaluation of novel bifunctional chelates for the development of Cu-64-based radiopharmaceuticals. Nucl. Med. Biol., 2008, 35(8), 875-882.
[] [PMID: 19026949]
Esser, J.P.; Krenning, E.P.; Teunissen, J.J.; Kooij, P.P.; van Gameren, A.L.; Bakker, W.H.; Kwekkeboom, D.J. Comparison of [(177)Lu-DOTA(0),Tyr(3)]octreotate and [(177)Lu-DOTA(0), Tyr(3)]octreotide: which peptide is preferable for PRRT? Eur. J. Nucl. Med. Mol. Imaging, 2006, 33(11), 1346-1351.
[] [PMID: 16847654]
de Jong, M.; Breeman, W.A.; Bakker, W.H.; Kooij, P.P.; Bernard, B.F.; Hofland, L.J.; Visser, T.J.; Srinivasan, A.; Schmidt, M.A.; Erion, J.L.; Bugaj, J.E.; Mäcke, H.R.; Krenning, E.P. Comparison of (111)In-labeled somatostatin analogues for tumor scintigraphy and radionuclide therapy. Cancer Res., 1998, 58(3), 437-441.
[PMID: 9458086]
Reubi, J.C.; Schär, J.C.; Waser, B.; Wenger, S.; Heppeler, A.; Schmitt, J.S.; Mäcke, H.R. Affinity profiles for human somatostatin receptor subtypes SST1-SST5 of somatostatin radiotracers selected for scintigraphic and radiotherapeutic use. Eur. J. Nucl. Med., 2000, 27(3), 273-282.
[] [PMID: 10774879]
Fani, M.; Braun, F.; Waser, B.; Beetschen, K.; Cescato, R.; Erchegyi, J.; Rivier, J.E.; Weber, W.A.; Maecke, H.R.; Reubi, J.C. Unexpected sensitivity of sst2 antagonists to N-terminal radiometal modifications. J. Nucl. Med., 2012, 53(9), 1481-1489.
[] [PMID: 22851637]
Dalm, S.U.; Nonnekens, J.; Doeswijk, G.N.; de Blois, E.; van Gent, D.C.; Konijnenberg, M.W.; de Jong, M. Comparison of the therapeutic response to treatment with a 177Lu-labeled somatostatin receptor agonist and antagonist in preclinical models. J. Nucl. Med., 2016, 57(2), 260-265.
[] [PMID: 26514177]
Wild, D.; Fani, M.; Fischer, R.; Del Pozzo, L.; Kaul, F.; Krebs, S.; Fischer, R.; Rivier, J.E.; Reubi, J.C.; Maecke, H.R.; Weber, W.A. Comparison of somatostatin receptor agonist and antagonist for peptide receptor radionuclide therapy: a pilot study. J. Nucl. Med., 2014, 55(8), 1248-1252.
[] [PMID: 24963127]
Adant, S.; Shah, G.M.; Beauregard, J.M. Combination treatments to enhance peptide receptor radionuclide therapy of neuroendocrine tumours. Eur. J. Nucl. Med. Mol. Imaging, 2019, 41, 907-921.
[] [PMID: 31492995]
Nonnekens, J.; van Kranenburg, M.; Beerens, C.E.; Suker, M.; Doukas, M.; van Eijck, C.H.; de Jong, M.; van Gent, D.C. Potentiation of peptide receptor radionuclide therapy by the PARP inhibitor olaparib. Theranostics, 2016, 6(11), 1821-1832.
[] [PMID: 27570553]
Purohit, N.K.; Shah, R.G.; Adant, S.; Hoepfner, M.; Shah, G.M.; Beauregard, J.M. Potentiation of 177Lu-octreotate peptide receptor radionuclide therapy of human neuroendocrine tumor cells by PARP inhibitor. Oncotarget, 2018, 9(37), 24693-24706.
[] [PMID: 29872498]
Nickoloff, J.A.; Boss, M.K.; Allen, C.P.; LaRue, S.M. Translational research in radiation-induced DNA damage signaling and repair. Transl. Cancer Res., 2017, 6(Suppl. 5), S875-S891.
[] [PMID: 30574452]
Bison, S.M.; Haeck, J.C.; Bol, K.; Koelewijn, S.J.; Groen, H.C.; Melis, M.; Veenland, J.F.; Bernsen, M.R.; de Jong, M. Optimization of combined temozolomide and peptide receptor radionuclide therapy (PRRT) in mice after multimodality molecular imaging studies. EJNMMI Res., 2015, 5(1), 62.
[] [PMID: 26553049]
Lewin, J.; Cullinane, C.; Akhurst, T.; Waldeck, K.; Watkins, D.N.; Rao, A.; Eu, P.; Mileshkin, L.; Hicks, R.J. Peptide receptor chemoradionuclide therapy in small cell carcinoma: from bench to bedside. Eur. J. Nucl. Med. Mol. Imaging, 2015, 42(1), 25-32.
[] [PMID: 25125202]
Claringbold, P.G.; Price, R.A.; Turner, J.H. Phase I-II study of radiopeptide 177Lu-octreotate in combination with capecitabine and temozolomide in advanced low-grade neuroendocrine tumors. Cancer Biother. Radiopharm., 2012, 27(9), 561-569.
[] [PMID: 23078020]
Claringbold, P.G.; Brayshaw, P.A.; Price, R.A.; Turner, J.H. Phase II study of radiopeptide 177Lu-octreotate and capecitabine therapy of progressive disseminated neuroendocrine tumours. Eur. J. Nucl. Med. Mol. Imaging, 2011, 38(2), 302-311.
[] [PMID: 21052661]
Yadav, M.P.; Ballal, S.; Bal, C. Concomitant 177Lu-DOTATATE and capecitabine therapy in malignant paragangliomas. EJNMMI Res., 2019, 9(1), 13.
[] [PMID: 30725219]
Hofving, T.; Sandblom, V.; Arvidsson, Y.; Shubbar, E.; Altiparmak, G.; Swanpalmer, J.; Almobarak, B.; Elf, A.K.; Johanson, V.; Elias, E.; Kristiansson, E.; Forssell-Aronsson, E.; Nilsson, O. 177Lu-octreotate therapy for neuroendocrine tumours is enhanced by Hsp90 inhibition. Endocr. Relat. Cancer, 2019, 26(4), 437-449.
[] [PMID: 30730850]
Lundsten, S.; Spiegelberg, D.; Stenerlöw, B.; Nestor, M. The HSP90 inhibitor onalespib potentiates 177Lu DOTATATE therapy in neuroendocrine tumor cells. Int. J. Oncol., 2019, 55(6), 1287-1295.
[] [PMID: 31638190]
Zhao, Y.; Butler, E.B.; Tan, M. Targeting cellular metabolism to improve cancer therapeutics. Cell Death Dis., 2013, 4(3)e532
[] [PMID: 23470539]
Elf, A.K.; Bernhardt, P.; Hofving, T.; Arvidsson, Y.; Forssell-Aronsson, E.; Wängberg, B.; Nilsson, O.; Johanson, V. NAMPT inhibitor GMX1778 enhances the efficacy of 177Lu-DOTATATE treatment of neuroendocrine tumors. J. Nucl. Med., 2017, 58(2), 288-292.
[] [PMID: 27688470]
Taelman, V.F.; Radojewski, P.; Marincek, N.; Ben-Shlomo, A.; Grotzky, A.; Olariu, C.I.; Perren, A.; Stettler, C.; Krause, T.; Meier, L.P.; Cescato, R.; Walter, M.A. Upregulation of key molecules for targeted imaging and therapy. J. Nucl. Med., 2016, 57(11), 1805-1810.
[] [PMID: 27363833]
Veenstra, M.J.; van Koetsveld, P.M.; Dogan, F.; Farrell, W.E.; Feelders, R.A.; Lamberts, S.W.J.; de Herder, W.W.; Vitale, G.; Hofland, L.J. Epidrug-induced upregulation of functional somatostatin type 2 receptors in human pancreatic neuroendocrine tumor cells. Oncotarget, 2016, 9(19), 14791-14802.
[PMID: 29599907]
Pool, S.E.; Bison, S.; Koelewijn, S.J.; van der Graaf, L.M.; Melis, M.; Krenning, E.P.; de Jong, M. mTOR inhibitor RAD001 promotes metastasis in a rat model of pancreatic neuroendocrine cancer. Cancer Res., 2013, 73(1), 12-18.
[] [PMID: 23149918]
Bison, S.M.; Pool, S.E.; Koelewijn, S.J.; van der Graaf, L.M.; Groen, H.C.; Melis, M.; de Jong, M. Peptide receptor radionuclide therapy (PRRT) with [(177)Lu-DOTA(0),Tyr(3)]octreotate in combination with RAD001 treatment: further investigations on tumor metastasis and response in the rat pancreatic CA20948 tumor model. EJNMMI Res., 2014, 4, 21.
[] [PMID: 24995150]
Claringbold, P.G.; Turner, J.H. NeuroEndocrine tumor therapy with lutetium-177-octreotate and everolimus (NETTLE): A phase I study. Cancer Biother. Radiopharm., 2015, 30(6), 261-269.
[] [PMID: 26181854]
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.
[] [PMID: 25988165]
Nuñez-Valdovinos, B.; Carmona-Bayonas, A.; Jimenez-Fonseca, P.; Capdevila, J.; Castaño-Pascual, Á.; Benavent, M.; Pi Barrio, J.J.; Teule, A.; Alonso, V.; Custodio, A.; Marazuela, M.; Segura, Á.; Beguiristain, A.; Llanos, M.; Martinez Del Prado, M.P.; Diaz-Perez, J.A.; Castellano, D.; Sevilla, I.; Lopez, C.; Alonso, T.; Garcia-Carbonero, R. Neuroendocrine tumor heterogeneity adds uncertainty to the world health organization 2010 classification: Real-World data from the spanish tumor registry (R-GETNE). Oncologist, 2018, 23(4), 422-432.
[] [PMID: 29330208]
Terry, S.Y.A.; Nonnekens, J.; Aerts, A.; Baatout, S.; de Jong, M.; Cornelissen, B.; Pouget, J.P. Call to arms: need for radiobiology in molecular radionuclide therapy. Eur. J. Nucl. Med. Mol. Imaging, 2019, 46(8), 1588-1590.
[] [PMID: 31069454]
Montelius, M.; Spetz, J.; Jalnefjord, O.; Berger, E.; Nilsson, O.; Ljungberg, M.; Forssell-Aronsson, E. Identification of potential MR-derived biomarkers for tumor tissue response to 177Lu-octreotate therapy in an animal model of small intestine neuroendocrine tumor. Transl. Oncol., 2018, 11(2), 193-204.
[] [PMID: 29331677]
Bodei, L.; Kidd, M.; Modlin, I.M.; Severi, S.; Drozdov, I.; Nicolini, S.; Kwekkeboom, D.J.; Krenning, E.P.; Baum, R.P.; Paganelli, G. Measurement of circulating transcripts and gene cluster analysis predicts and defines therapeutic efficacy of peptide receptor radionuclide therapy (PRRT) in neuroendocrine tumors. Eur. J. Nucl. Med. Mol. Imaging, 2016, 43(5), 839-851.
[] [PMID: 26596723]
Kumar, C.; Jayakumar, S.; Pandey, B.N.; Samuel, G.; Venkatesh, M. Cellular and molecular effects of beta radiation from I-131 on human tumor cells: a comparison with gamma radiation. Curr. Radiopharm., 2014, 7(2), 138-143.
[] [PMID: 25030623]
Ricciotti, E.; Sarantopoulou, D.; Grant, G.R.; Sanzari, J.K.; Krigsfeld, G.S.; Kiliti, A.J.; Kennedy, A.R.; Grosser, T. Distinct vascular genomic response of proton and gamma radiation-A pilot investigation. PLoS One, 2019, 14(2)e0207503
[] [PMID: 30742630]
Dikomey, E.; Franzke, J. DNA repair kinetics after exposure to X-irradiation and to internal beta-rays in CHO cells. Radiat. Environ. Biophys., 1986, 25(3), 189-194.
[] [PMID: 3797626]
Murland, S.L. Tumour oxygenation: The importance of hypoxia, anemia, and angiogenesis in radiation therapy. Can. J. Med. Radiat. Technol., 2005, 36(1), 21-33.
Sun, Y. Tumor microenvironment and cancer therapy resistance. Cancer Lett., 2016, 380(1), 205-215.
[] [PMID: 26272180]
Lee, D.; Li, M.; Bednarz, B.; Schultz, M.K. Modeling cell and tumor-metastasis dosimetry with the particle and heavy ion transport code system (PHITS) software for targeted alpha-particle radionuclide therapy. Radiat. Res., 2018, 190(3), 236-247.
[] [PMID: 29944461]
Yu, B.; Wei, H.; He, Q.; Ferreira, C.A.; Kutyreff, C.J.; Ni, D.; Rosenkrans, Z.T.; Cheng, L.; Yu, F.; Engle, J.W.; Lan, X.; Cai, W. Efficient uptake of 177 Lu-Porphyrin-PEG nanocomplexes by tumor mitochondria for multimodal-imaging-guided combination therapy. Angew. Chem. Int. Ed. Engl., 2018, 57(1), 218-222.
[] [PMID: 29092090]
Tamborino, G. Cellular dosimetry of [177Lu]Lu-DOTATATE radionuclide therapy: the impact of modelling assumptions on the correlations with in vitro cytotoxicity. EJNMMI Phys., 2019, 7(1)
Pool, S.E.; Kam, B.L.; Koning, G.A.; Konijnenberg, M.; Ten Hagen, T.L.; Breeman, W.A.; Krenning, E.P.; de Jong, M.; van Eijck, C.H. [(111)In-DTPA]octreotide tumor uptake in GEPNET liver metastases after intra-arterial administration: an overview of preclinical and clinical observations and implications for tumor radiation dose after peptide radionuclide therapy. Cancer Biother. Radiopharm., 2014, 29(4), 179-187.
[] [PMID: 24820805]
Braat, A.J.A.T.; Snijders, T.J.; Seute, T.; Vonken, E.P.A. Will 177Lu-DOTATATE treatment become more effective in salvage meningioma patients, when boosting somatostatin receptor saturation? A promising case on intra-arterial administration. Cardiovasc. Intervent. Radiol., 2019, 42(11), 1649-1652.
[] [PMID: 31187231]
Ilan, E.; Sandström, M.; Wassberg, C.; Sundin, A.; Garske-Román, U.; Eriksson, B.; Granberg, D.; Lubberink, M. Dose response of pancreatic neuroendocrine tumors treated with peptide receptor radionuclide therapy using 177Lu-DOTATATE. J. Nucl. Med., 2015, 56(2), 177-182.
[] [PMID: 25593115]
Pauwels, S.; Barone, R.; Walrand, S.; Borson-Chazot, F.; Valkema, R.; Kvols, L.K.; Krenning, E.P.; Jamar, F. Practical dosimetry of peptide receptor radionuclide therapy with (90)Y-labeled somatostatin analogs. J. Nucl. Med., 2005, 46(Suppl. 1), 92S-98S.
[PMID: 15653657]

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