Toward the Discovery and Development of PSMA Targeted Inhibitors for Nuclear Medicine Applications

Author(s): Sara Pastorino, Mattia Riondato, Licia Uccelli, Giampiero Giovacchini, Elisabetta Giovannini, Valerio Duce, Andrea Ciarmiello*.

Journal Name: Current Radiopharmaceuticals

Volume 13 , Issue 1 , 2020

DOI : 10.2174/1874471012666190729151540

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Abstract:

Background: The rising incidence rate of prostate cancer (PCa) has promoted the development of new diagnostic and therapeutic radiopharmaceuticals during the last decades. Promising improvements have been achieved in clinical practice using prostate specific membrane antigen (PSMA) labeled agents, including specific antibodies and small molecular weight inhibitors. Focusing on molecular docking studies, this review aims to highlight the progress in the design of PSMA targeted agents for a potential use in nuclear medicine.

Results: Although the first development of radiopharmaceuticals able to specifically recognize PSMA was exclusively oriented to macromolecule protein structure such as radiolabeled monoclonal antibodies and derivatives, the isolation of the crystal structure of PSMA served as the trigger for the synthesis and the further evaluation of a variety of low molecular weight inhibitors. Among the nuclear imaging probes and radiotherapeutics that have been developed and tested till today, labeled Glutamate-ureido inhibitors are the most prevalent PSMA-targeting agents for nuclear medicine applications.

Conclusion: PSMA represents for researchers the most attractive target for the detection and treatment of patients affected by PCa using nuclear medicine modalities. [99mTc]MIP-1404 is considered the tracer of choice for SPECT imaging and [68Ga]PSMA-11 is the leading diagnostic for PET imaging by general consensus. [18F]DCFPyL and [18F]PSMA-1007 are clearly the emerging PET PSMA candidates for their great potential for a widespread commercial distribution. After paving the way with new imaging tools, academic and industrial R&Ds are now focusing on the development of PSMA inhibitors labeled with alpha or beta minus emitters for a theragnostic application.

Keywords: Prostate cancer, PSMA, molecular docking, PET, SPECT, imaging, radionuclide therapy.

[1]
International Agency for Research on Cancer. World Health Organization.Global cancer observatory: Cancer Today. https://gco.iarc.fr/today/data/factsheets/populations/900-world-fact-sheets.pdf [Accessed April 08, 2019].
[2]
Babich, J.W.; Joyal, J.L.; Coleman, R.E. Targeting prostate cancer with small molecule inhibitors of prostate -specific membrane antigen In: Targeted Molecular Imaging;; Welch , M. J.; Eckelman, W. C., Eds.; Taylor & Francis Group, LLC: Lenexa,. , 2012; pp. 161-174.
[3]
Spratt, D.E.; McHugh, D.J.; Morris, M.J.; Morgans, A.K. Management of Biochemically Recurrent Prostate Cancer: Ensuring the Right Treatment of the Right Patient at the Right Time. Am. Soc. Clin. Oncol. Educ. Book, 2018, 38, 355-362.
[http://dx.doi.org/10.1200/EDBK_200319] [PMID: 30231323]
[4]
Ilic, D.; Djulbegovic, M.; Jung, J.H.; Hwang, E.C.; Zhou, Q.; Cleves, A.; Agoritsas, T.; Dahm, P. Prostate cancer screening with prostate-specific antigen (PSA) test: a systematic review and meta-analysis. BMJ, 2018, 362, k3519.
[http://dx.doi.org/10.1136/bmj.k3519] [PMID: 30185521]
[5]
Eastham, J. Prostate cancer screening. Investig. Clin. Urol., 2017, 58(4), 217-219.
[http://dx.doi.org/10.4111/icu.2017.58.4.217] [PMID: 28681029]
[6]
Kiess, A.P.; Banerjee, S.R.; Mease, R.C.; Rowe, S.P.; Rao, A.; Foss, C.A.; Chen, Y.; Yang, X.; Cho, S.Y.; Nimmagadda, S.; Pomper, M.G. Prostate-specific membrane antigen as a target for cancer imaging and therapy. Q. J. Nucl. Med. Mol. Imaging, 2015, 59(3), 241-268.
[PMID: 26213140]
[7]
Chen, Y.; Foss, C.A.; Byun, Y.; Nimmagadda, S.; Pullambhatla, M.; Fox, J.J.; Castanares, M.; Lupold, S.E.; Babich, J.W.; Mease, R.C.; Pomper, M.G. Radiohalogenated prostate-specific membrane antigen (PSMA)-based ureas as imaging agents for prostate cancer. J. Med. Chem., 2008, 51(24), 7933-7943.
[http://dx.doi.org/10.1021/jm801055h] [PMID: 19053825]
[8]
Mease, R.C.; Foss, C.A.; Pomper, M.G. PET imaging in prostate cancer: focus on prostate-specific membrane antigen. Curr. Top. Med. Chem., 2013, 13(8), 951-962.
[http://dx.doi.org/10.2174/1568026611313080008] [PMID: 23590171]
[9]
Cuccurullo, V.; Di Stasio, G.D.; Mansi, L. Nuclear Medicine in Prostate Cancer: A New Era for Radiotracers. World J. Nucl. Med., 2018, 17(2), 70-78.
[PMID: 29719480]
[10]
Foss, C.A.; Mease, R.C.; Cho, S.Y.; Kim, H.J.; Pomper, M.G. GCPII imaging and cancer. Curr. Med. Chem., 2012, 19(9), 1346-1359.
[http://dx.doi.org/10.2174/092986712799462612] [PMID: 22304713]
[11]
Schuster, D.M.; Nanni, C.; Fanti, S. Evaluation of Prostate Cancer with Radiolabeled Amino Acid Analogs. J. Nucl. Med., 2016, 57(Suppl. 3), 61S-66S.
[http://dx.doi.org/10.2967/jnumed.115.170209] [PMID: 27694174]
[12]
Afshar-Oromieh, A.; Babich, J.W.; Kratochwil, C.; Giesel, F.L.; Eisenhut, M.; Kopka, K.; Haberkorn, U. The Rise of PSMA Ligands for Diagnosis and Therapy of Prostate Cancer. J. Nucl. Med., 2016, 57(Suppl. 3), 79S-89S.
[http://dx.doi.org/10.2967/jnumed.115.170720] [PMID: 27694178]
[13]
Bařinka, C.; Rojas, C.; Slusher, B.; Pomper, M. Glutamate carboxypeptidase II in diagnosis and treatment of neurologic disorders and prostate cancer. Curr. Med. Chem., 2012, 19(6), 856-870.
[http://dx.doi.org/10.2174/092986712799034888] [PMID: 22214450]
[14]
Tykvart, J.; Schimer, J.; Bařinková, J.; Pachl, P.; Poštová-Slavětínská, L.; Majer, P.; Konvalinka, J.; Šácha, P. Rational design of urea-based glutamate carboxypeptidase II (GCPII) inhibitors as versatile tools for specific drug targeting and delivery. Bioorg. Med. Chem., 2014, 22(15), 4099-4108.
[http://dx.doi.org/10.1016/j.bmc.2014.05.061] [PMID: 24954515]
[15]
Mesters, J.R.; Barinka, C.; Li, W.; Tsukamoto, T.; Majer, P.; Slusher, B.S.; Konvalinka, J.; Hilgenfeld, R. Structure of glutamate carboxypeptidase II, a drug target in neuronal damage and prostate cancer. EMBO J., 2006, 25(6), 1375-1384.
[http://dx.doi.org/10.1038/sj.emboj.7600969] [PMID: 16467855]
[16]
Ghosh, A.; Heston, W.D. Tumor target prostate specific membrane antigen (PSMA) and its regulation in prostate cancer. J. Cell. Biochem., 2004, 91(3), 528-539.
[http://dx.doi.org/10.1002/jcb.10661] [PMID: 14755683]
[17]
Gourni, E.; Henriksen, G. Metal-Based PSMA Radioligands. Molecules, 2017, 22(4)E523
[http://dx.doi.org/10.3390/molecules22040523] [PMID: 28338640]
[18]
Davis, M.I.; Bennett, M.J.; Thomas, L.M.; Bjorkman, P.J. Crystal structure of prostate-specific membrane antigen, a tumor marker and peptidase. Proc. Natl. Acad. Sci. USA, 2005, 102(17), 5981-5986.
[http://dx.doi.org/10.1073/pnas.0502101102] [PMID: 15837926]
[19]
Horoszewicz, J.S.; Kawinski, E.; Murphy, G.P. Monoclonal antibodies to a new antigenic marker in epithelial prostatic cells and serum of prostatic cancer patients. Anticancer Res., 1987, 7(5B), 927-935.
[PMID: 2449118]
[20]
Murphy, G.P. Radioscintiscanning of Prostate Cancer. Cancer, 1995, 75(S7), 1819-1822.
[http://dx.doi.org/10.1002/1097-0142(19950401)75:7+<1819:AID-CNCR2820751611>3.0.CO;2-U]
[21]
Bander, N.H.; Trabulsi, E.J.; Kostakoglu, L.; Yao, D.; Vallabhajosula, S.; Smith-Jones, P.; Joyce, M.A.; Milowsky, M.; Nanus, D.M.; Goldsmith, S.J. Targeting metastatic prostate cancer with radiolabeled monoclonal antibody J591 to the extracellular domain of prostate specific membrane antigen. J. Urol., 2003, 170(5), 1717-1721.
[http://dx.doi.org/10.1097/01.ju.0000091655.77601.0c] [PMID: 14532761]
[22]
Milowsky, M.I.; Nanus, D.M.; Kostakoglu, L.; Vallabhajosula, S.; Goldsmith, S.J.; Bander, N.H. Phase I trial of yttrium-90-labeled anti-prostate-specific membrane antigen monoclonal antibody J591 for androgen-independent prostate cancer. J. Clin. Oncol., 2004, 22(13), 2522-2531.
[http://dx.doi.org/10.1200/JCO.2004.09.154] [PMID: 15173215]
[23]
Tagawa, S.T.; Vallabhajosula, S.; Jhanwar, Y.; Ballman, K.V.; Hackett, A.; Emmerich, L.; Babich, J.; Sartor, A.O.; Harshman, L.C.; Beltran, H.; Molina, A.M.; Nanus, D.M.; Bander, N.H. Phase I dose-escalation study of 225Ac-J591 for progressive metastatic castration resistant prostate cancer (mCRPC). J. Clin. Oncol., 2018, 36(Suppl. 6), TPS399-TPS399.
[http://dx.doi.org/10.1200/JCO.2018.36.6_suppl.TPS399]
[24]
Vallabhajosula, S.; Kuji, I.; Hamacher, K.A.; Konishi, S.; Kostakoglu, L.; Kothari, P.A.; Milowski, M.I.; Nanus, D.M.; Bander, N.H.; Goldsmith, S.J. Pharmacokinetics and biodistribution of 111In- and 177Lu-labeled J591 antibody specific for prostate-specific membrane antigen: prediction of 90Y-J591 radiation dosimetry based on 111In or 177Lu? J. Nucl. Med., 2005, 46(4), 634-641.
[PMID: 15809486]
[25]
Foss, C.A.; Mease, R.C.; Fan, H.; Wang, Y.; Ravert, H.T.; Dannals, R.F.; Olszewski, R.T.; Heston, W.D.; Kozikowski, A.P.; Pomper, M.G. Radiolabeled small-molecule ligands for prostate-specific membrane antigen: in vivo imaging in experimental models of prostate cancer. Clin. Cancer Res., 2005, 11(11), 4022-4028.
[http://dx.doi.org/10.1158/1078-0432.CCR-04-2690] [PMID: 15930336]
[26]
Kularatne, S.A.; Zhou, Z.; Yang, J.; Post, C.B.; Low, P.S. Design, synthesis, and preclinical evaluation of prostate-specific membrane antigen targeted (99m)Tc-radioimaging agents. Mol. Pharm., 2009, 6(3), 790-800.
[http://dx.doi.org/10.1021/mp9000712] [PMID: 19361232]
[27]
Cimadamore, A.; Cheng, M.; Santoni, M.; Lopez-Beltran, A.; Battelli, N.; Massari, F.; Galosi, A.B.; Scarpelli, M.; Montironi, R. New Prostate Cancer Targets for Diagnosis, Imaging, and Therapy: Focus on Prostate-Specific Membrane Antigen. Front. Oncol., 2018, 8, 653.
[http://dx.doi.org/10.3389/fonc.2018.00653] [PMID: 30622933]
[28]
Pandit-Taskar, N.; O’Donoghue, J.A.; Ruan, S.; Lyashchenko, S.K.; Carrasquillo, J.A.; Heller, G.; Martinez, D.F.; Cheal, S.M.; Lewis, J.S.; Fleisher, M.; Keppler, J.S.; Reiter, R.E.; Wu, A.M.; Weber, W.A.; Scher, H.I.; Larson, S.M.; Morris, M.J. First-in-Human Imaging with 89Zr-Df-IAB2M Anti-PSMA Minibody in Patients with Metastatic Prostate Cancer: Pharmacokinetics, Biodistribution, Dosimetry, and Lesion Uptake. J. Nucl. Med., 2016, 57(12), 1858-1864.
[http://dx.doi.org/10.2967/jnumed.116.176206] [PMID: 27516450]
[29]
Evazalipour, M.; D’Huyvetter, M.; Tehrani, B.S.; Abolhassani, M.; Omidfar, K.; Abdoli, S.; Arezumand, R.; Morovvati, H.; Lahoutte, T.; Muyldermans, S.; Devoogdt, N. Generation and characterization of nanobodies targeting PSMA for molecular imaging of prostate cancer. Contrast Media Mol. Imaging, 2014, 9(3), 211-220.
[http://dx.doi.org/10.1002/cmmi.1558] [PMID: 24700748]
[30]
Lakhin, A.V.; Tarantul, V.Z.; Gening, L.V. Aptamers: problems, solutions and prospects. Acta Naturae, 2013, 5(4), 34-43.
[PMID: 24455181]
[31]
Hicke, B.J.; Stephens, A.W.; Gould, T.; Chang, Y.F.; Lynott, C.K.; Heil, J.; Borkowski, S.; Hilger, C.S.; Cook, G.; Warren, S.; Schmidt, P.G. Tumor targeting by an aptamer. J. Nucl. Med., 2006, 47(4), 668-678.
[PMID: 16595502]
[32]
Lupold, S.E.; Hicke, B.J.; Lin, Y.; Coffey, D.S. Identification and characterization of nuclease-stabilized RNA molecules that bind human prostate cancer cells via the prostate-specific membrane antigen. Cancer Res., 2002, 62(14), 4029-4033.
[PMID: 12124337]
[33]
Pavlícek, J.; Ptácek, J.; Barinka, C. Glutamate carboxypeptidase II: an overview of structural studies and their importance for structure-based drug design and deciphering the reaction mechanism of the enzyme. Curr. Med. Chem., 2012, 19(9), 1300-1309.
[http://dx.doi.org/10.2174/092986712799462667] [PMID: 22304708]
[34]
Barinka, C.; Byun, Y.; Dusich, C.L.; Banerjee, S.R.; Chen, Y.; Castanares, M.; Kozikowski, A.P.; Mease, R.C.; Pomper, M.G.; Lubkowski, J. Interactions between human glutamate carboxypeptidase II and urea-based inhibitors: structural characterization. J. Med. Chem., 2008, 51(24), 7737-7743.
[http://dx.doi.org/10.1021/jm800765e] [PMID: 19053759]
[35]
Novakova, Z.; Cerny, J.; Choy, C.J.; Nedrow, J.R.; Choi, J.K.; Lubkowski, J.; Berkman, C.E.; Barinka, C. Design of composite inhibitors targeting glutamate carboxypeptidase II: the importance of effector functionalities. FEBS J., 2016, 283(1), 130-143.
[http://dx.doi.org/10.1111/febs.13557] [PMID: 26460595]
[36]
Kopka, K.; Benešová, M.; Bařinka, C.; Haberkorn, U.; Babich, J. Glu-Ureido-Based Inhibitors of Prostate-Specific Membrane Antigen: Lessons Learned During the Development of a Novel Class of Low-Molecular-Weight Theranostic Radiotracers. J. Nucl. Med., 2017, 58(Suppl. 2), 17S-26S.
[http://dx.doi.org/10.2967/jnumed.116.186775] [PMID: 28864607]
[37]
Jackson, P.F.; Cole, D.C.; Slusher, B.S.; Stetz, S.L.; Ross, L.E.; Donzanti, B.A.; Trainor, D.A. Design, synthesis, and biological activity of a potent inhibitor of the neuropeptidase N-acetylated alpha-linked acidic dipeptidase. J. Med. Chem., 1996, 39(2), 619-622.
[http://dx.doi.org/10.1021/jm950801q] [PMID: 8558536]
[38]
Majer, P.; Jackson, P.F.; Delahanty, G.; Grella, B.S.; Ko, Y.S.; Li, W.; Liu, Q.; Maclin, K.M.; Poláková, J.; Shaffer, K.A.; Stoermer, D.; Vitharana, D.; Wang, E.Y.; Zakrzewski, A.; Rojas, C.; Slusher, B.S.; Wozniak, K.M.; Burak, E.; Limsakun, T.; Tsukamoto, T. Synthesis and biological evaluation of thiol-based inhibitors of glutamate carboxypeptidase II: discovery of an orally active GCP II inhibitor. J. Med. Chem., 2003, 46(10), 1989-1996.
[http://dx.doi.org/10.1021/jm020515w] [PMID: 12723961]
[39]
Jackson, P.F.; Tays, K.L.; Maclin, K.M.; Ko, Y.S.; Li, W.; Vitharana, D.; Tsukamoto, T.; Stoermer, D.; Lu, X.C.; Wozniak, K.; Slusher, B.S. Design and pharmacological activity of phosphinic acid based NAALADase inhibitors. J. Med. Chem., 2001, 44(24), 4170-4175.
[http://dx.doi.org/10.1021/jm0001774] [PMID: 11708918]
[40]
Wu, L.Y.; Anderson, M.O.; Toriyabe, Y.; Maung, J.; Campbell, T.Y.; Tajon, C.; Kazak, M.; Moser, J.; Berkman, C.E. The molecular pruning of a phosphoramidate peptidomimetic inhibitor of prostate-specific membrane antigen. Bioorg. Med. Chem., 2007, 15(23), 7434-7443.
[http://dx.doi.org/10.1016/j.bmc.2007.07.028] [PMID: 17869524]
[41]
Liu, T.; Toriyabe, Y.; Kazak, M.; Berkman, C.E. Pseudoirreversible inhibition of prostate-specific membrane antigen by phosphoramidate peptidomimetics. Biochemistry, 2008, 47(48), 12658-12660.
[http://dx.doi.org/10.1021/bi801883v] [PMID: 18983168]
[42]
Ganguly, T.; Dannoon, S.; Hopkins, M.R.; Murphy, S.; Cahaya, H.; Blecha, J.E.; Jivan, S.; Drake, C.R.; Barinka, C.; Jones, E.F.; VanBrocklin, H.F.; Berkman, C.E. A high-affinity [(18)F]-labeled phosphoramidate peptidomimetic PSMA-targeted inhibitor for PET imaging of prostate cancer. Nucl. Med. Biol., 2015, 42(10), 780-787.
[http://dx.doi.org/10.1016/j.nucmedbio.2015.06.003] [PMID: 26169882]
[43]
Dannoon, S.; Ganguly, T.; Cahaya, H.; Geruntho, J.J.; Galliher, M.S.; Beyer, S.K.; Choy, C.J.; Hopkins, M.R.; Regan, M.; Blecha, J.E.; Skultetyova, L.; Drake, C.R.; Jivan, S.; Barinka, C.; Jones, E.F.; Berkman, C.E.; VanBrocklin, H.F. Structure-Activity Relationship of (18)F-Labeled Phosphoramidate Peptidomimetic Prostate-Specific Membrane Antigen (PSMA)-Targeted Inhibitor Analogues for PET Imaging of Prostate Cancer. J. Med. Chem., 2016, 59(12), 5684-5694.
[http://dx.doi.org/10.1021/acs.jmedchem.5b01850] [PMID: 27228467]
[44]
Lapi, S.E.; Wahnishe, H.; Pham, D.; Wu, L.Y.; Nedrow-Byers, J.R.; Liu, T.; Vejdani, K.; VanBrocklin, H.F.; Berkman, C.E.; Jones, E.F. Assessment of an 18F-labeled phosphoramidate peptidomimetic as a new prostate-specific membrane antigen-targeted imaging agent for prostate cancer. J. Nucl. Med., 2009, 50(12), 2042-2048.
[http://dx.doi.org/10.2967/jnumed.109.066589] [PMID: 19910433]
[45]
Nedrow-Byers, J.R.; Jabbes, M.; Jewett, C.; Ganguly, T.; He, H.; Liu, T.; Benny, P.; Bryan, J.N.; Berkman, C.E. A phosphoramidate-based prostate-specific membrane antigen-targeted SPECT agent. Prostate, 2012, 72(8), 904-912.
[http://dx.doi.org/10.1002/pros.21493] [PMID: 22670265]
[46]
Behr, S.C.; Aggarwal, R.; Van Brocklin, H.F.; Flavell, R.R.; Geo, K.; Small, E.J.; Blecha, J.; Jivan, S.; Hope, T.A.; Simko, J.P. Kurhanewicz, J.; Noworolski, S. M.; Korn, N. J.; De Los Santos, R.; Cooperberg, M. R.; Carroll, P. R.; Nguyen, H.; Greene, K. L.; Langton-Webster, B.; Berkman, C. E.; Seo, Y. First-in-human phase 1 PET study of CTT1057, a novel 18F-labeled imaging agent targeting prostate specific membrane antigen (PSMA) in prostate cancer. J. Clin. Oncol., 2017, 35(15)
[47]
Kozikowski, A.P.; Nan, F.; Conti, P.; Zhang, J.; Ramadan, E.; Bzdega, T.; Wroblewska, B.; Neale, J.H.; Pshenichkin, S.; Wroblewski, J.T. Design of remarkably simple, yet potent urea-based inhibitors of glutamate carboxypeptidase II (NAALADase). J. Med. Chem., 2001, 44(3), 298-301.
[http://dx.doi.org/10.1021/jm000406m] [PMID: 11462970]
[48]
Maresca, K.P.; Hillier, S.M.; Femia, F.J.; Keith, D.; Barone, C.; Joyal, J.L.; Zimmerman, C.N.; Kozikowski, A.P.; Barrett, J.A.; Eckelman, W.C.; Babich, J.W. A series of halogenated heterodimeric inhibitors of prostate specific membrane antigen (PSMA) as radiolabeled probes for targeting prostate cancer. J. Med. Chem., 2009, 52(2), 347-357.
[http://dx.doi.org/10.1021/jm800994j] [PMID: 19111054]
[49]
Rowe, S.P.; Gage, K.L.; Faraj, S.F.; Macura, K.J.; Cornish, T.C.; Gonzalez-Roibon, N.; Guner, G.; Munari, E.; Partin, A.W.; Pavlovich, C.P.; Han, M.; Carter, H.B.; Bivalacqua, T.J.; Blackford, A.; Holt, D.; Dannals, R.F.; Netto, G.J.; Lodge, M.A.; Mease, R.C.; Pomper, M.G.; Cho, S.Y. 18F-DCFBC PET/CT for PSMA-Based Detection and Characterization of Primary Prostate Cancer. J. Nucl. Med., 2015, 56(7), 1003-1010.
[http://dx.doi.org/10.2967/jnumed.115.154336] [PMID: 26069305]
[50]
Chen, Y.; Pullambhatla, M.; Foss, C.A.; Byun, Y.; Nimmagadda, S.; Senthamizhchelvan, S.; Sgouros, G.; Mease, R.C.; Pomper, M.G. 2-(3-1-Carboxy-5-[(6-[18F]fluoro-pyridine-3-carbonyl)-amino]-pentyl-ureido)-pentanedioic acid, [18F]DCFPyL, a PSMA-based PET imaging agent for prostate cancer. Clin. Cancer Res., 2011, 17(24), 7645-7653.
[http://dx.doi.org/10.1158/1078-0432.CCR-11-1357] [PMID: 22042970]
[51]
Szabo, Z.; Mena, E.; Rowe, S.P.; Plyku, D.; Nidal, R.; Eisenberger, M.A.; Antonarakis, E.S.; Fan, H.; Dannals, R.F.; Chen, Y.; Mease, R.C.; Vranesic, M.; Bhatnagar, A.; Sgouros, G.; Cho, S.Y.; Pomper, M.G. Initial Evaluation of [(18)F]DCFPyL for Prostate-Specific Membrane Antigen (PSMA)-Targeted PET Imaging of Prostate Cancer. Mol. Imaging Biol., 2015, 17(4), 565-574.
[http://dx.doi.org/10.1007/s11307-015-0850-8] [PMID: 25896814]
[52]
Cho, S.Y.; Gage, K.L.; Mease, R.C.; Senthamizhchelvan, S.; Holt, D.P.; Jeffrey-Kwanisai, A.; Endres, C.J.; Dannals, R.F.; Sgouros, G.; Lodge, M.; Eisenberger, M.A.; Rodriguez, R.; Carducci, M.A.; Rojas, C.; Slusher, B.S.; Kozikowski, A.P.; Pomper, M.G. Biodistribution, tumor detection, and radiation dosimetry of 18F-DCFBC, a low-molecular-weight inhibitor of prostate-specific membrane antigen, in patients with metastatic prostate cancer. J. Nucl. Med., 2012, 53(12), 1883-1891.
[http://dx.doi.org/10.2967/jnumed.112.104661] [PMID: 23203246]
[53]
Rowe, S.P.; Macura, K.J.; Ciarallo, A.; Mena, E.; Blackford, A.; Nadal, R.; Antonarakis, E.S.; Eisenberger, M.A.; Carducci, M.A.; Ross, A.E.; Kantoff, P.W.; Holt, D.P.; Dannals, R.F.; Mease, R.C.; Pomper, M.G.; Cho, S.Y. Comparison of Prostate-Specific Membrane Antigen-Based 18F-DCFBC PET/CT to Conventional Imaging Modalities for Detection of Hormone-Naïve and Castration-Resistant Metastatic Prostate Cancer. J. Nucl. Med., 2016, 57(1), 46-53.
[http://dx.doi.org/10.2967/jnumed.115.163782] [PMID: 26493203]
[54]
Giesel, F.L.; Cardinale, J.; Schäfer, M.; Neels, O.; Benešová, M.; Mier, W.; Haberkorn, U.; Kopka, K.; Kratochwil, C. (18)F-Labelled PSMA-1007 shows similarity in structure, biodistribution and tumour uptake to the theragnostic compound PSMA-617. Eur. J. Nucl. Med. Mol. Imaging, 2016, 43(10), 1929-1930.
[http://dx.doi.org/10.1007/s00259-016-3447-9] [PMID: 27342416]
[55]
Cardinale, J.; Schäfer, M.; Benešová, M.; Bauder-Wüst, U.; Leotta, K.; Eder, M.; Neels, O.C.; Haberkorn, U.; Giesel, F.L.; Kopka, K. Preclinical Evaluation of 18F-PSMA-1007, a New Prostate-Specific Membrane Antigen Ligand for Prostate Cancer Imaging. J. Nucl. Med., 2017, 58(3), 425-431.
[http://dx.doi.org/10.2967/jnumed.116.181768] [PMID: 27789722]
[56]
Giesel, F.L.; Hadaschik, B.; Cardinale, J.; Radtke, J.; Vinsensia, M.; Lehnert, W.; Kesch, C.; Tolstov, Y.; Singer, S.; Grabe, N.; Duensing, S.; Schäfer, M.; Neels, O.C.; Mier, W.; Haberkorn, U.; Kopka, K.; Kratochwil, C. F-18 labelled PSMA-1007: biodistribution, radiation dosimetry and histopathological validation of tumor lesions in prostate cancer patients. Eur. J. Nucl. Med. Mol. Imaging, 2017, 44(4), 678-688.
[http://dx.doi.org/10.1007/s00259-016-3573-4] [PMID: 27889802]
[57]
Rahbar, K.; Weckesser, M.; Ahmadzadehfar, H.; Schäfers, M.; Stegger, L.; Bögemann, M. Advantage of 18F-PSMA-1007 over 68Ga-PSMA-11 PET imaging for differentiation of local recurrence vs. urinary tracer excretion. Eur. J. Nucl. Med. Mol. Imaging, 2018, 45(6), 1076-1077.
[http://dx.doi.org/10.1007/s00259-018-3952-0] [PMID: 29445927]
[58]
Giesel, F.L.; Will, L.; Kesch, C.; Freitag, M.; Kremer, C.; Merkle, J.; Neels, O.C.; Cardinale, J.; Hadaschik, B.; Hohenfellner, M.; Kopka, K.; Haberkorn, U.; Kratochwil, C. Biochemical Recurrence of Prostate Cancer: Initial Results with [18F]PSMA-1007 PET/CT. J. Nucl. Med., 2018, 59(4), 632-635.
[http://dx.doi.org/10.2967/jnumed.117.196329] [PMID: 29419475]
[59]
Rahbar, K.; Afshar-Oromieh, A.; Seifert, R.; Wagner, S.; Schäfers, M.; Bögemann, M.; Weckesser, M. Diagnostic performance of 18F-PSMA-1007 PET/CT in patients with biochemical recurrent prostate cancer. Eur. J. Nucl. Med. Mol. Imaging, 2018, 45(12), 2055-2061.
[http://dx.doi.org/10.1007/s00259-018-4089-x] [PMID: 30027419]
[60]
Barrett, J.A.; Coleman, R.E.; Goldsmith, S.J.; Vallabhajosula, S.; Petry, N.A.; Cho, S.; Armor, T.; Stubbs, J.B.; Maresca, K.P.; Stabin, M.G.; Joyal, J.L.; Eckelman, W.C.; Babich, J.W. First-in-man evaluation of 2 high-affinity PSMA-avid small molecules for imaging prostate cancer. J. Nucl. Med., 2013, 54(3), 380-387.
[http://dx.doi.org/10.2967/jnumed.112.111203] [PMID: 23303962]
[61]
Banerjee, S.R.; Foss, C.A.; Castanares, M.; Mease, R.C.; Byun, Y.; Fox, J.J.; Hilton, J.; Lupold, S.E.; Kozikowski, A.P.; Pomper, M.G. Synthesis and evaluation of technetium-99m- and rhenium-labeled inhibitors of the prostate-specific membrane antigen (PSMA). J. Med. Chem., 2008, 51(15), 4504-4517.
[http://dx.doi.org/10.1021/jm800111u] [PMID: 18637669]
[62]
Banerjee, S.R.; Maresca, K.P.; Francesconi, L.; Valliant, J.; Babich, J.W.; Zubieta, J. New directions in the coordination chemistry of 99mTc: a reflection on technetium core structures and a strategy for new chelate design. Nucl. Med. Biol., 2005, 32(1), 1-20.
[http://dx.doi.org/10.1016/j.nucmedbio.2004.09.001] [PMID: 15691657]
[63]
Ray Banerjee, S.; Pullambhatla, M.; Foss, C.A.; Falk, A.; Byun, Y.; Nimmagadda, S.; Mease, R.C.; Pomper, M.G. Effect of chelators on the pharmacokinetics of (99m)Tc-labeled imaging agents for the prostate-specific membrane antigen (PSMA). J. Med. Chem., 2013, 56(15), 6108-6121.
[http://dx.doi.org/10.1021/jm400823w] [PMID: 23799782]
[64]
Hillier, S.M.; Maresca, K.P.; Lu, G.; Merkin, R.D.; Marquis, J.C.; Zimmerman, C.N.; Eckelman, W.C.; Joyal, J.L.; Babich, J.W. 99mTc-labeled small-molecule inhibitors of prostate-specific membrane antigen for molecular imaging of prostate cancer. J. Nucl. Med., 2013, 54(8), 1369-1376.
[http://dx.doi.org/10.2967/jnumed.112.116624] [PMID: 23733925]
[65]
Banerjee, S.R.; Pullambhatla, M.; Byun, Y.; Nimmagadda, S.; Green, G.; Fox, J.J.; Horti, A.; Mease, R.C.; Pomper, M.G. 68Ga-labeled inhibitors of prostate-specific membrane antigen (PSMA) for imaging prostate cancer. J. Med. Chem., 2010, 53(14), 5333-5341.
[http://dx.doi.org/10.1021/jm100623e] [PMID: 20568777]
[66]
Kilian, K. 68Ga-DOTA and analogs: Current status and future perspectives. Rep. Pract. Oncol. Radiother., 2014, 19(Suppl.), S13-S21.
[http://dx.doi.org/10.1016/j.rpor.2014.04.016] [PMID: 28443194]
[67]
Eder, M.; Schäfer, M.; Bauder-Wüst, U.; Hull, W.E.; Wängler, C.; Mier, W.; Haberkorn, U.; Eisenhut, M. 68Ga-complex lipophilicity and the targeting property of a urea-based PSMA inhibitor for PET imaging. Bioconjug. Chem., 2012, 23(4), 688-697.
[http://dx.doi.org/10.1021/bc200279b] [PMID: 22369515]
[68]
Benešová, M.; Schäfer, M.; Bauder-Wüst, U.; Afshar-Oromieh, A.; Kratochwil, C.; Mier, W.; Haberkorn, U.; Kopka, K.; Eder, M. Preclinical Evaluation of a Tailor-Made DOTA-Conjugated PSMA Inhibitor with Optimized Linker Moiety for Imaging and Endoradiotherapy of Prostate Cancer. J. Nucl. Med., 2015, 56(6), 914-920.
[http://dx.doi.org/10.2967/jnumed.114.147413] [PMID: 25883127]
[69]
Ahmadzadehfar, H.; Rahbar, K.; Kürpig, S.; Bögemann, M.; Claesener, M.; Eppard, E.; Gärtner, F.; Rogenhofer, S.; Schäfers, M.; Essler, M. Early side effects and first results of radioligand therapy with (177)Lu-DKFZ-617 PSMA of castrate-resistant metastatic prostate cancer: a two-centre study. EJNMMI Res., 2015, 5(1), 114.
[http://dx.doi.org/10.1186/s13550-015-0114-2] [PMID: 26099227]
[70]
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., 2016, 57(9), 1334-1338.
[http://dx.doi.org/10.2967/jnumed.116.173757] [PMID: 27056618]
[71]
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.; Eu, P.; Jackson, P.; Scalzo, M.; Williams, S.G.; Sandhu, S. [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(6), 825-833.
[http://dx.doi.org/10.1016/S1470-2045(18)30198-0] [PMID: 29752180]
[72]
Rahbar, K.; Ahmadzadehfar, H.; Kratochwil, C.; Haberkorn, U.; Schäfers, M.; Essler, M.; Baum, R.P.; Kulkarni, H.R.; Schmidt, M.; Drzezga, A.; Bartenstein, P.; Pfestroff, A.; Luster, M.; Lützen, U.; Marx, M.; Prasad, V.; Brenner, W.; Heinzel, A.; Mottaghy, F.M.; Ruf, J.; Meyer, P.T.; Heuschkel, M.; Eveslage, M.; Bögemann, M.; Fendler, W.P.; Krause, B.J. German Multicenter Study Investigating 177Lu-PSMA-617 Radioligand Therapy in Advanced Prostate Cancer Patients. J. Nucl. Med., 2017, 58(1), 85-90.
[http://dx.doi.org/10.2967/jnumed.116.183194] [PMID: 27765862]
[73]
Weineisen, M.; Simecek, J.; Schottelius, M.; Schwaiger, M.; Wester, H.J. Synthesis and preclinical evaluation of DOTAGA-conjugated PSMA ligands for functional imaging and endoradiotherapy of prostate cancer. EJNMMI Res., 2014, 4(1), 63.
[http://dx.doi.org/10.1186/s13550-014-0063-1] [PMID: 26116124]
[74]
Weineisen, M.; Schottelius, M.; Simecek, J.; Baum, R.P.; Yildiz, A.; Beykan, S.; Kulkarni, H.R.; Lassmann, M.; Klette, I.; Eiber, M.; Schwaiger, M.; Wester, H.J. 68Ga- and 177Lu-Labeled PSMA I&T: Optimization of a PSMA-Targeted Theranostic Concept and First Proof-of-Concept Human Studies. J. Nucl. Med., 2015, 56(8), 1169-1176.
[http://dx.doi.org/10.2967/jnumed.115.158550] [PMID: 26089548]
[75]
McCarthy, M.; Langton, T.; Kumar, D.; Campbell, A. Comparison of PSMA-HBED and PSMA-I&T as diagnostic agents in prostate carcinoma. Eur. J. Nucl. Med. Mol. Imaging, 2017, 44(9), 1455-1462.
[http://dx.doi.org/10.1007/s00259-017-3699-z] [PMID: 28474140]
[76]
Schmuck, S.; Mamach, M.; Wilke, F.; von Klot, C.A.; Henkenberens, C.; Thackeray, J.T.; Sohns, J.M.; Geworski, L.; Ross, T.L.; Wester, H.J.; Christiansen, H.; Bengel, F.M.; Derlin, T. Multiple Time-Point 68Ga-PSMA I&T PET/CT for Characterization of Primary Prostate Cancer: Value of Early Dynamic and Delayed Imaging. Clin. Nucl. Med., 2017, 42(6), e286-e293.
[http://dx.doi.org/10.1097/RLU.0000000000001589] [PMID: 28221194]
[77]
Schmuck, S.; Nordlohne, S.; von Klot, C.A.; Henkenberens, C.; Sohns, J.M.; Christiansen, H.; Wester, H.J.; Ross, T.L.; Bengel, F.M.; Derlin, T. Comparison of standard and delayed imaging to improve the detection rate of [68Ga]PSMA I&T PET/CT in patients with biochemical recurrence or prostate-specific antigen persistence after primary therapy for prostate cancer. Eur. J. Nucl. Med. Mol. Imaging, 2017, 44(6), 960-968.
[http://dx.doi.org/10.1007/s00259-017-3669-5] [PMID: 28280856]
[78]
Berliner, C.; Tienken, M.; Frenzel, T.; Kobayashi, Y.; Helberg, A.; Kirchner, U.; Klutmann, S.; Beyersdorff, D.; Budäus, L.; Wester, H.J.; Mester, J.; Bannas, P. Detection rate of PET/CT in patients with biochemical relapse of prostate cancer using [68Ga]PSMA I&T and comparison with published data of [68Ga]PSMA HBED-CC. Eur. J. Nucl. Med. Mol. Imaging, 2017, 44(4), 670-677.
[http://dx.doi.org/10.1007/s00259-016-3572-5] [PMID: 27896369]


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VOLUME: 13
ISSUE: 1
Year: 2020
Page: [63 - 79]
Pages: 17
DOI: 10.2174/1874471012666190729151540

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