Synthesis and preclinical evaluation of DOTAGA-conjugated PSMA ligands for functional imaging and endoradiotherapy of prostate cancer

Mesters JR, Barinka C, Li W, Tsukamoto T, Majer P, Slusher BS, Konvalinka J, Hilgenfeld R: Structure of glutamate carboxypeptidase II, a drug target in neuronal damage and prostate cancer. EMBO J 2006, 25: 1375–1384. 10.1038/sj.emboj.7600969

Ghosh A, Heston WD: Tumor target prostate specific membrane antigen (PSMA) and its regulation in prostate cancer. J Cell Biochem 2004, 91: 528–539. 10.1002/jcb.10661

Silver DA, Pellicer I, Fair WR, Heston WD, Cordon-Cardo C: Prostate-specific membrane antigen expression in normal and malignant human tissues. Clin Cancer Res 1997, 3: 81–85.

Pinto JT, Suffoletto BP, Berzin TM, Qiao CH, Lin S, Tong WP, May F, Mukherjee B, Heston WDW: Prostate-specific membrane antigen: a novel folate hydrolase in human prostatic carcinoma cells. Clin Cancer Res 1996, 2: 1445–1451.

Carter RE, Feldman AR, Coyle JT: Prostate-specific membrane antigen is a hydrolase with substrate and pharmacologic characteristics of a neuropeptidase. Proc Natl Acad Sci USA 1996, 93: 749–753. 10.1073/pnas.93.2.749

Schulke N, Varlamova OA, Donovan GP, Ma D, Gardner JP, Morrissey DM, Arrigale RR, Zhan C, Chodera AJ, Surowitz KG, Maddon PJ, Heston WD, Olson WC: The homodimer of prostate-specific membrane antigen is a functional target for cancer therapy. Proc Natl Acad Sci USA 2003, 100: 12590–12595. 10.1073/pnas.1735443100

Kozikowski AP, Nan F, Conti P, Zhang J, Ramadan E, Bzdega T, Wroblewska B, Neale JH, Pshenichkin S, Wroblewski JT: Design of remarkably simple, yet potent urea-based inhibitors of glutamate carboxypeptidase II (NAALADase). J Med Chem 2001, 44: 298–301. 10.1021/jm000406m

Pomper MG, Musachio JL, Zhang J, Scheffel U, Zhou Y, Hilton J, Maini A, Dannals RF, Wong DF, Kozikowski AP: 11C-MCG: synthesis, uptake selectivity, and primate PET of a probe for glutamate carboxypeptidase II (NAALADase). Mol Imaging 2002, 1: 96–101. 10.1162/153535002320162750

Foss CA, Mease RC, Fan H, Wang Y, Ravert HT, Dannals RF, Olszewski RT, Heston WD, Kozikowski AP, Pomper MG: Radiolabeled small-molecule ligands for prostate-specific membrane antigen: in vivo imaging in experimental models of prostate cancer. Clin Cancer Res 2005, 11: 4022–4028. 10.1158/1078-0432.CCR-04-2690

Chen Y, Foss CA, Byun Y, Nimmagadda S, Pullambhatla M, Fox JJ, Castanares M, Lupold SE, Babich JW, Mease RC, Pomper MG: Radiohalogenated prostate-specific membrane antigen (PSMA)-based ureas as imaging agents for prostate cancer. J Med Chem 2008, 51: 7933–7943. 10.1021/jm801055h

Mease RC, Dusich CL, Foss CA, Ravert HT, Dannals RF, Seidel J, Prideaux A, Fox JJ, Sgouros G, Kozikowski AP, Pomper MG: N -[ N -[(S)-1,3-Dicarboxypropyl]carbamoyl]-4-[18F]fluorobenzyl- L-cysteine, [18F]DCFBC: a new imaging probe for prostate cancer. Clin Cancer Res 2008, 14: 3036–3043. 10.1158/1078-0432.CCR-07-1517

Maresca KP, Hillier SM, Femia FJ, Keith D, Barone C, Joyal JL, Zimmerman CN, Kozikowski AP, Barrett JA, Eckelman WC, Babich JW: A series of halogenated heterodimeric inhibitors of prostate specific membrane antigen (PSMA) as radiolabeled probes for targeting prostate cancer. J Med Chem 2009, 52: 347–357. 10.1021/jm800994j

Hillier SM, Maresca KP, Femia FJ, Marquis JC, Foss CA, Nguyen N, Zimmerman CN, Barrett JA, Eckelman WC, Pomper MG, Joyal JL, Babich JW: Preclinical evaluation of novel glutamate-urea-lysine analogues that target prostate-specific membrane antigen as molecular imaging pharmaceuticals for prostate cancer. Cancer Res 2009, 69: 6932–6940. 10.1158/0008-5472.CAN-09-1682

Banerjee SR, Foss CA, Castanares M, Mease RC, Byun Y, Fox JJ, Hilton J, Lupold SE, Kozikowski AP, Pomper MG: Synthesis and evaluation of 99mTc and Re-labeled inhibitors of the prostate-specific membrane antigen (PSMA). J Med Chem 2008, 51: 4504–4517. 10.1021/jm800111u

Kularatne SA, Zhou Z, Yang J, Post CB, Low PS: Design, synthesis, and preclinical evaluation of prostate-specific membrane antigen targeted 99mTc-radioimaging agents. Mol Pharm 2009, 6: 790–800. 10.1021/mp9000712

Zhang AX, Murelli RP, Barinka C, Michel J, Cocleaza A, Jorgensen WL, Lubkowski J, Spiegel DA: A remote arene-binding site on prostate specific membrane antigen revealed by antibody-recruiting small molecules. J Am Chem Soc 2010, 132: 12711–12716. 10.1021/ja104591m

Banerjee SR, Pullambhatla M, Byun Y, Nimmagadda S, Green G, Fox JJ, Horti A, Mease RC, Pomper MG: 68Ga-labeled inhibitors of prostate-specific membrane antigen (PSMA) for imaging prostate cancer. J Med Chem 2010, 53: 5333–5341. 10.1021/jm100623e

Eder M, Schafer M, Bauder-Wust U, Hull WE, Wangler C, Mier W, Haberkorn U, Eisenhut M: 68Ga-complex lipophilicity and the targeting property of a urea-based PSMA inhibitor for PET imaging. Bioconj Chem 2012, 23: 688–697. 10.1021/bc200279b

Akhtar NH, Pail O, Saran A, Tyrell L, Tagawa ST: Prostate-specific membrane antigen-based therapeutics. Adv Urol 2012, 2012: 973820. 10.1155/2012/973820

Milowsky MI, Nanus DM, Kostakoglu L, Sheehan CE, Vallabhajosula S, Goldsmith SJ, Ross JS, Bander NH: Vascular targeted therapy with anti-prostate-specific membrane antigen monoclonal antibody J591 in advanced solid tumors. J Clin Oncol 2007, 25: 540–547. 10.1200/JCO.2006.07.8097

Tagawa ST, Milowsky MI, Morris MJ, Vallabhajosula S, Christos PJ, Akhtar NH, Goldsmith SJ, Osborne J, Larson SM, Pandit-Taskar N, Scher HI, Bander NH, Nanus DM: Phase II study of Lutetium-177-labeled anti-prostate-specific membrane antigen (PSMA) monoclonal antibody J591 for metastatic castration-resistant prostate cancer. Clin Cancer Res 2013, 19: 5182–5191. 10.1158/1078-0432.CCR-13-0231

Milowsky MI, Nanus DM, Kostakoglu L, Vallabhajosula S, Goldsmith SJ, Bander NH: 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: 2522–2531. 10.1200/JCO.2004.09.154

Hillier S, Merkin R, Maresca K, Zimmerman C, Barrett J, Tesson M, Eckelman W, Mairs R, Joyal J, Babich J: [131I]MIP-1375, a small molecule prostate-specific membrane antigen (PSMA) inhibitor for targeted therapy of prostate cancer (PCa). J Nucl Med 2011, 52(Supplement 1):361.

Hillier S, Rubino K, Maresca K, Marquis J, Tesson M, Zimmerman C, Eckelman W, Mairs R, Joyal J, Babich J: [131I]MIP-1466, a small molecule prostate-specific membrane antigen (PSMA) inhibitor for targeted radiotherapy of prostate cancer (PCa). J Nucl Med 2012, 53(Supplement 1):170.

Zechmann CM, Afshar-Oromieh A, Armor T, Stubbs JB, Mier W, Hadaschik B, Joyal J, Kopka K, Debus J, Babich JW, Haberkorn U: Radiation dosimetry and first therapy results with a 124I/131I-labelled small molecule (MIP-1095) targeting PSMA for prostate cancer therapy. Eur J Nucl Med Mol Imaging 2014, 41: 1280–1292. 10.1007/s00259-014-2713-y

Bernhard C, Moreau M, Lhenry D, Goze C, Boschetti F, Rousselin Y, Brunotte F, Denat F: DOTAGA-anhydride: a valuable building block for the preparation of DOTA-like chelating agents. Chemistry 2012, 18: 7834–7841. 10.1002/chem.201200132

Eisenwiener KP, Powell P, Macke HR: A convenient synthesis of novel bifunctional prochelators for coupling to bioactive peptides for radiometal labelling. Bioorg Med Chem Lett 2000, 10: 2133–2135. 10.1016/S0960-894X(00)00413-3

Heppeler A, Froidevaux S, Macke HR, Jermann E, Behe M, Powell P, Hennig M: Radiometal-labelled macrocyclic chelator-derivatized somatostatin analogue with superb tumour-targeting properties and potential for receptor-mediated internal radiotherapy. Chemistry 1999, 5: 1974–1981. 10.1002/(SICI)1521-3765(19990702)5:7<1974::AID-CHEM1974>3.0.CO;2-X

Simecek J, Zemek O, Hermann P, Wester HJ, Notni J: A monoreactive bifunctional triazacyclononane phosphinate chelator with high selectivity for 68Ga. Chem Med Chem 2012, 7: 1375–1378. 10.1002/cmdc.201200261

Schottelius M, Reubi JC, Eltschinger V, Schwaiger M, Wester HJ: N-terminal sugar conjugation and C-terminal Thr-for-Thr(ol) exchange in radioiodinated Tyr3-octreotide: effect on cellular ligand trafficking in vitro and tumor accumulation in vivo. J Med Chem 2005, 48: 2778–2789. 10.1021/jm040794i

Dekker B, Keen H, Shaw D, Disley L, Hastings D, Hadfield J, Reader A, Allan D, Julyan P, Watson A, Zweit J: Functional comparison of annexin V analogues labelled indirectly and directly with iodine-124. Nucl Med Biol 2005, 32: 403–413. 10.1016/j.nucmedbio.2005.02.002

Vaidyanathan G, Zalutsky MR: Preparation of N-succinimidyl 3-[*I]iodobenzoate: an agent for the indirect radioiodination of proteins. Nat Protoc 2006, 1: 707–713. 10.1038/nprot.2006.99

Martin R, Juttler S, Muller M, Wester HJ: Cationic eluate pretreatment for automated synthesis of [68Ga]CPCR4.2. Nucl Med Biol 2014, 41: 84–89. 10.1016/j.nucmedbio.2013.09.002

Mueller D, Klette I, Baum RP, Gottschaldt M, Schultz MK, Breeman WA: Simplified NaCl based 68Ga concentration and labeling procedure for rapid synthesis of 68Ga radiopharmaceuticals in high radiochemical purity. Bioconj Chem 2012, 23: 1712–1717. 10.1021/bc300103t

Notni J, Simecek J, Hermann P, Wester HJ: TRAP, a powerful and versatile framework for 68Ga radiopharmaceuticals. Chemistry 2011, 17: 14718–14722. 10.1002/chem.201103503

Afshar-Oromieh A, Malcher A, Eder M, Eisenhut M, Linhart HG, Hadaschik BA, Holland-Letz T, Giesel FL, Kratochwil C, Haufe S, Haberkorn U, Zechmann CM: PET imaging with a 68Ga-labelled PSMA ligand for the diagnosis of prostate cancer: biodistribution in humans and first evaluation of tumour lesions. Eur J Nucl Med Mol Imaging 2013, 40: 486–495. 10.1007/s00259-012-2298-2

Cho SY, Gage KL, Mease RC, Senthamizhchelvan S, Holt DP, Jeffrey-Kwanisai A, Endres CJ, Dannals RF, Sgouros G, Lodge M, Eisenberger MA, Rodriguez R, Carducci MA, Rojas C, Slusher BS, Kozikowski AP, Pomper MG: 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(Supplement 1):1883–1891. 10.2967/jnumed.112.104661

Baur B, Solbach C, Andreolli E, Winter G, Machulla HJ, Reske SN: Synthesis, radiolabelling and in vitro characterization of the 68Ga, 90Y and 177Lu-labelled PSMA ligand, CHX-A''-DTPA-DUPA-Pep. Pharmaceuticals (Basel) 2014, 7: 517–529. 10.3390/ph7050517

Winter G, Zlatopolskiy B, Kull T, Bertram J, Genze F, Cudek G, Machulla H-J, Reske S: 68Ga-DOTA-DUPA-Pep as a new peptide conjugate for molecular imaging of prostate carcinoma. J Nucl Med 2011, 52: 1597.

Benesova M, Schaefer M, Bauder-Wuest U, Mier W, Haberkorn U, Eder M, Kopka K: Preclinical evaluation of a naphthyl-containing DOTA-conjugated PSMA inhibitor with improved targeting and pharmacokinetic properties. Eur J Nucl Med Mol Imaging 2014, 2(Supplement):438.