Small-molecule PSMA ligands. Current state, SAR and perspectives

References

• Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin 2014;64:9–29.
   PubMed Web of Science ®Google Scholar
• Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012;62:10–29.
   PubMed Web of Science ®Google Scholar
• Hudson DL. Epithelial stem cells in human prostate growth and disease. Prostate Cancer Prostatic Dis 2004;7:188–94.
   PubMed Web of Science ®Google Scholar
• Ghosh A, Heston WD. Tumor target prostate specific membrane antigen (PSMA) and its regulation in prostate cancer. J Cell Biochem 2004;91:528–39.
   PubMed Web of Science ®Google Scholar
• Schmittgen TD, Teske S, Vessella RL, et al. Expression of prostate specific membrane antigen and three alternatively spliced variants of PSMA in prostate cancer patients. Int J Cancer 2003;107:323–9.
   PubMed Web of Science ®Google Scholar
• Sweat SD, Pacelli A, Murphy GP, Bostwick DG. Prostate-specific membrane antigen expression is greatest in prostate adenocarcinoma and lymph node metastases. Urology 1998;52:637–40.
   PubMed Web of Science ®Google Scholar
• Silver DA, Pellicer I, Fair WR, et al. Prostate-specific membrane antigen expression in normal and malignant human tissues. Clin Cancer Res 1997;3:81–5.
   PubMed Web of Science ®Google Scholar
• Sharifi N, Gulley JL, Dahut WL. Androgen deprivation therapy for prostate cancer. JAMA 2005;294:238–44.
   PubMed Web of Science ®Google Scholar
• Dassie JP, Hernandez LI, Thomas1 GS, et al. Targeted inhibition of prostate cancer metastases with an RNA aptamer to prostate-specific membrane antigen. Mol Ther 2014;22:1910–22.
   PubMed Web of Science ®Google Scholar
• Taneja SS. ProstaScint® scan: contemporary use in clinical practice. Rev Urol 2004;6:19–28.
   PubMedGoogle Scholar
• Vallabhajosula S, Goldsmith SJ, Hamacher KA, et al. Prediction of myelotoxicity based on bone marrow radiation-absorbed dose: radioimmunotherapy studies using 90Y- and 177Lu-labeled J591 antibodies specific for prostate-specific membrane antigen. J Nucl Med 2005;46:850–8.
   PubMed Web of Science ®Google Scholar
• Smith-Jones PM, Vallabhajosula S, Navarro V, et al. Radiolabeled monoclonal antibodies specific to the extracellular domain of prostate-specific membrane antigen: preclinical studies in nude mice bearing LNCaP human prostate tumor. J Nucl Med 2003;44:610–17.
   PubMed Web of Science ®Google Scholar
• Tagawa ST, Milowsky MI, Morris M, et al. Phase II study of Lutetium-177-labeled anti-prostate specific membrane antigen monoclonal antibody J591 for metastatic castration-resistant prostate cancer. Clin Cancer Res 2013;19:5182–91.
   PubMed Web of Science ®Google Scholar
• Hillier SM, Maresca KP, Femia FJ, et al. Preclinical evaluation of novel glutamate-urea-lysine analogues that target prostate-specific membrane antigen as molecular imaging pharmaceuticals for prostate cancer. Cancer Res 2009;69:6932–40.
   PubMed Web of Science ®Google Scholar
• Hillier SM, Maresca KP, Lu G, et al. 99mTc-labeled small-molecule inhibitors of prostate-specific membrane antigen for molecular imaging of prostate cancer. J Nucl Med 2013;54:1369–76.
   PubMed Web of Science ®Google Scholar
• Eder M, Schafer M, Bauder-Wust U, et al. 68Ga-complex lipophilicity and the targeting property of a urea-based PSMA inhibitor for PET imaging. Bioconjug Chem 2012;23:688–97.
   PubMed Web of Science ®Google Scholar
• Pinto JT, Suffoletto BP, Bergin TM. Prostate-specific membrane antigen: a novel folate hydrolase in human prostatic carcinoma cells. Clin Cancer Res 1996;2:1445–51.
   PubMed Web of Science ®Google Scholar
• Smith-Jones PM, Vallabahajosula S, Goldsmith SJ, et al. In vitro characterization of radiolabeled monoclonal antibodies specific for the extracellular domain of prostate-specific membrane antigen. Cancer Res 2000;60:5237–43.
   PubMed Web of Science ®Google Scholar
• Kantoff PW, Schuetz TJ, Blumenstein BA, et al. Overall survival analysis of a phase II randomized controlled trial of a Poxviral-based PSA-targeted immunotherapy in metastatic castration resistant prostate cancer. J Clin Oncol 2010;28:1099–105.
   PubMed Web of Science ®Google Scholar
• Kübler H, Scheel B, Gnad-Vogt U, et al. Self-adjuvanted mRNA vaccination in advanced prostate cancer patients: a first-in-man phase I/IIa study. J Immunother Cancer 2015;3:26.
   PubMed Web of Science ®Google Scholar
• Davis MI, Bennett MJ, Thomas LM, Bjorkman PJ. Crystal structure of prostate-specific membrane antigen, a tumor marker and peptidase. Proc Natl Acad Sci USA 2005;102:5981–6.
   PubMed Web of Science ®Google Scholar
• Serval V, Galli T, Cheramy A, et al. In vitro and in vivo inhibition of N-acetyl-L-aspartyl-L-glutamate catabolism by N-acylated L-glutamate analogs. J Pharmacol Exp Ther 1992;260:1093–100.
   PubMed Web of Science ®Google Scholar
• Subasinghe N, Schulte M, Chan MY, et al. Synthesis of acyclic and dehydroaspartic acid analogues of Ac-Asp-Glu-OH and their inhibition of rat brain N-acetylated alpha-linked acidic dipeptidase (NAALA dipeptidase). J Med Chem 1990;33:2734–44.
   PubMed Web of Science ®Google Scholar
• Maresca KP, Hillier SM, Femia FJ, et al. A series of halogenated heterodimeric inhibitors of prostate specific membrane antigen (PSMA) as radiolabeled probes for targeting prostate cancer. J Med Chem 2009;52:347–57.
   PubMed Web of Science ®Google Scholar
• Barinka C, Rovenská M, Mlcochová P, et al. Structural insight into the pharmacophore pocket of human glutamate carboxypeptidase II. J Med Chem 2007;50:3267–73.
   PubMed Web of Science ®Google Scholar
• Jackson PF, Cole DC, Slusher BS, et al. Design, synthesis, and biological activity of a potent inhibitor of the neuropeptidase N-acetylated alphalinked acidic dipeptidase. J Med Chem 1996;39:619–22.
   PubMed Web of Science ®Google Scholar
• Vitharana D, France JE, Scarpetti D, et al. Synthesis and biological evaluation of (R)- and (S)-2-(phosphonomethyl)pentanedioic acids as inhibitors of glutamate carboxypeptidase II. Tetrahedron: Asymm 2002;13:1609–14.
   Web of Science ®Google Scholar
• Jackson PF, Tays KL, Maclin KM, et al. Design and pharmacological activity of phosphinic acid based NAALADase inhibitors. J Med Chem 2001;44:4170–5.
   PubMed Web of Science ®Google Scholar
• Tsukamoto T, Flanary JM, Rojas C, et al. Phosphonate and phosphinate analogues of N-acylated gamma-glutamylglutamate. potent inhibitors of glutamate carboxypeptidase II. Bioorg Med Chem Lett 2002;12:2189–92.
   PubMed Web of Science ®Google Scholar
• Williams AJ, Lu XM, Slusher B, Tortella FC. Electroencephalogram analysis and neuroprotective profile of the N-acetylated-alpha-linked acidic dipeptidase inhibitor, GPI5232, in normal and brain-injured rats. J Pharmacol Exp Ther 2001;299:48–57.
   PubMed Web of Science ®Google Scholar
• Nan F, Bzdega T, Pshenichkin S, et al. Dual function glutamate-related ligands: discovery of a novel, potent inhibitor of glutamate carboxypeptidase II possessing mGluR3 agonist activity. J Med Chem 2000;43:772–4.
   PubMed Web of Science ®Google Scholar
• Barinka C, Hlouchova K, Rovenska M, et al. Structural basis of interactions between human glutamate carboxypeptidase II and its substrate analogs. J Mol Biol 2008;376:1438–50.
   PubMed Web of Science ®Google Scholar
• Graham K, Lesche R, Gromov AV, et al. Radiofluorinated derivatives of 2-(phosphonomethyl)pentanedioic acid as inhibitors of prostate specific membrane antigen (PSMA) for the imaging of prostate cancer. J Med Chem 2012;55:9510–20.
   PubMed Web of Science ®Google Scholar
• Beheshti M, Kunit T, Haim S, et al. BAY 1075553 PET-CT for staging and restaging prostate cancer patients: comparison with [18F] fluorocholine PET-CT (Phase I Study). Mol Imaging Biol 2014;17:424–33.
   Web of Science ®Google Scholar
• Lesche R, Kettschau G, Gromov AV, et al. Preclinical evaluation of BAY 1075553, a novel (18)F-labelled inhibitor of prostate-specific membrane antigen for PET imaging of prostate cancer. Eur J Nucl Med Mol Imaging 2014;41:89–101.
   PubMed Web of Science ®Google Scholar
• Vallabhajosula S, Nikolopoulou A, Babich JW, et al. 99mTc-labeled small-molecule inhibitors of prostate-specific membrane antigen: pharmacokinetics and biodistribution studies in healthy subjects and patients with metastatic prostate cancer. J Nucl Med 2014;55:1791–8.
   PubMed Web of Science ®Google Scholar
• Lapi SE, Wahnishe H, Pham D, et al. Assessment of an 18F-labeled phosphoramidate peptidomimetic as a new prostate-specific membrane antigen-targeted imaging agent for prostate cancer. J Nucl Med 2009;50:2042–8.
   PubMed Web of Science ®Google Scholar
• Liu T, Toriyabe Y, Kazak M, Berkman CE. Pseudoirreversible inhibition of prostate-specific membrane antigen by phosphoramidate peptidomimetics. Biochemistry 2008;47:12658–60.
   PubMed Web of Science ®Google Scholar
• Ganguly T, Dannoon S, Hopkins MR, et al. A high-affinity [(18)F]-labeled phosphoramidate peptidomimetic PSMA-targeted inhibitor for PET imaging of prostate cancer. Nucl Med Biol 2015;42:780–7.
   PubMed Web of Science ®Google Scholar
• Majer P, Jackson PF, Delahanty G, et al. Synthesis and biological evaluation of thiol-based inhibitors of glutamate carboxypeptidase II: discovery of an orally active GCP II inhibitor. J Med Chem 2003;46:1989–96.
   PubMed Web of Science ®Google Scholar
• vanderPost de Visser SJ, de Kam ML, Woefler M, et al. The central nervous system effects, pharmacokinetics and safety of the NAALADase-inhibitor GPI 5693. Br J Clin Pharmacol 2005;60:128–36.
   PubMed Web of Science ®Google Scholar
• Cushman DW, Cheung HS, Sabo EF, Ondetti MA. Design of potent competitive inhibitors of angiotensin-converting enzyme. Carboxyalkanoyl and mercaptoalkanoyl amino acids. Biochemistry 1977;16:5484–91.
   PubMed Web of Science ®Google Scholar
• Ondetti MA, Condon ME, Reid J, et al. Design of potent and specific inhibitors of carboxypeptidases A and B. Biochemistry 1979;18:1427–30.
   PubMed Web of Science ®Google Scholar
• Majer P, Hin B, Stoermer D, et al. Structural optimization of thiol-based inhibitors of glutamate carboxypeptidase II by modification of the P1' side chain. J Med Chem 2006;49:2876–85.
   PubMed Web of Science ®Google Scholar
• Stoermer D, Vitharana D, Hin N, et al. Design, synthesis, and pharmacological evaluation of glutamate carboxypeptidase II (GCPII) inhibitors based on thioalkylbenzoic acid scaffolds. J Med Chem 2012;55:5922–32.
   PubMed Web of Science ®Google Scholar
• Ferraris DV, Majer P, Ni C, et al. δ-Thiolactones as prodrugs of thiol-based glutamate carboxypeptidase II (GCPII) inhibitors. J Med Chem 2014;57:243–7.
   PubMed Web of Science ®Google Scholar
• Dansette PM, Libraire J, Bertho G, Mansuy D. Metabolic oxidative cleavage of thioesters: evidence for the formation of sulfenic acid intermediates in the bioactivation of the antithrombotic prodrugs ticlopidine and clopidogrel. Chem Res Toxicol 2009;22:369–73.
   PubMed Web of Science ®Google Scholar
• Kozikowski AP, Nan F, Conti P, et al. Design of remarkably simple, yet potent urea-based inhibitors of glutamate carboxypeptidase II (NAALADase). J Med Chem 2001;44:298–301.
   PubMed Web of Science ®Google Scholar
• Pomper MG, Musachio JL, Zhang J, et al. 11C-MCG: synthesis, uptake selectivity, and primate PET of a probe for glutamate carboxypeptidase II (NAALADase). Mol Imaging 2002;1:96–101.
   PubMed Web of Science ®Google Scholar
• Foss CA, Mease RC, Fan H, et al. Radiolabeled small-molecule ligands for prostate-specific membrane antigen: in vivo imaging in experimental models of prostate cancer. Clin Cancer Res 2005;11:4022–8.
   PubMed Web of Science ®Google Scholar
• Barinka C, Byun Y, Dusich CL, et al. Interactions between human glutamate carboxypeptidase II and urea-based inhibitors: structural characterization. J Med Chem 2008;51:7737–43.
   PubMed Web of Science ®Google Scholar
• Cho SY, Gage KL, Mease RC, et al. 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;53:1883–91.
   PubMed Web of Science ®Google Scholar
• Rowe SP, Gage KL, Faraj SF, et al. 18F-DCFBC PET/CT for PSMA-based detection and characterization of primary prostate cancer. J Nucl Med 2015;56:1003–10.
   PubMed Web of Science ®Google Scholar
• Srinivasarao M, Galliford CV, Low PS. Principles in the design of ligand-targeted cancer therapeutics and imaging agents. Nat Rev Drug Discov 2015;14:203–19.
   PubMed Web of Science ®Google Scholar
• Szabo Z, Mena E, Rowe SP, et al. Initial evaluation of [(18)F]DCFPyL for prostate-specific membrane antigen (PSMA)-targeted PET imaging of prostate cancer. Mol Imaging Biol 2015;17:565–74.
   PubMed Web of Science ®Google Scholar
• Hrkach J, Hoff DV, Ali MM, et al. Preclinical development and clinical translation of a PSMA-targeted docetaxel nanoparticle with a differentiated pharmacological profile. Sci Transl Med 2012;4:128–39.
   Web of Science ®Google Scholar
• Wang H, Byun Y, Barinka C, et al. Bioisosterism of urea-based GCPII inhibitors: synthesis and structure–activity relationship studies. Bioorg Med Chem Lett 2010;20:392–7.
   PubMed Web of Science ®Google Scholar
• Tykvart J, Schimer J, Bařinková J, et al. Rational design of urea-based glutamate carboxypeptidase II (GCPII) inhibitors as versatile tools for specific drug targeting and delivery. Bioorg Med Chem 2014;22:4099–108.
   PubMed Web of Science ®Google Scholar
• Tykvart J, Schimer J, Jančařík A, et al. Design of highly potent urea-based, exosite-binding inhibitors selective for glutamate carboxypeptidase II. J Med Chem 2015;58:4357–63.
   PubMed Web of Science ®Google Scholar
• Olszewski RT, Bukhari N, Zhou J, et al. NAAG peptidase inhibition reduces locomotor activity and some stereotypes in the PCP model of schizophrenia via group II mGluR. J Neurochem 2004;89:876–85.
   PubMed Web of Science ®Google Scholar
• Yamamoto T, Saito O, Aoe T, et al. Local administration of N-acetylaspartylglutamate (NAAG) peptidase inhibitors is analgesic in peripheral pain in rats. Eur J Neurosci 2007;25:147–58.
   PubMed Web of Science ®Google Scholar
• Zhong C, Zhao X, Sarva J, et al. NAAG peptidase inhibitor reduces acute neuronal degeneration and astrocyte damage following lateral fluid percussion TBI in rats. J Neurotrauma 2005;22:266–76.
   PubMed Web of Science ®Google Scholar
• Kozikowski AP, Zhang J, Nan FJ, et al. Synthesis of urea-based inhibitors as active site probes of glutamate carboxypeptidase II: efficacy as analgesic agents. J Med Chem 2004;47:1729–38.
   PubMed Web of Science ®Google Scholar
• Kularatne SA, Zhou Z, Yang J, et al. Design, synthesis, and preclinical evaluation of prostate-specific membrane antigen targeted 99mTc-radioimaging agents. Mol Pharm 2009;6:790–800.
   PubMed Web of Science ®Google Scholar
• Kularatne SA, Wang K, Santhapuram HK, Low PS. Prostate-specific membrane antigen targeted imaging and therapy of prostate cancer using a PSMA inhibitor as a homing ligand. Mol Pharm 2009;6:780–9.
   PubMed Web of Science ®Google Scholar
• Roy J, Nguyen TX, Kanduluru AK, et al. DUPA conjugation of a cytotoxic indenoisoquinoline topoisomerase I inhibitor for selective prostate cancer cell targeting. J Med Chem 2015;58:3094–103.
   PubMed Web of Science ®Google Scholar
• Barrett JA, Coleman RE, Goldsmith SJ, et al. First-in-man evaluation of 2 high-affinity PSMA-avid small molecules for imaging prostate cancer. J Nucl Med 2013;54:380–7.
   PubMed Web of Science ®Google Scholar
• Linn MM, Ball RA, Maradiegue A. Prostate-specific antigen screening: friend or foe? Urol Nurs 2007;27:481–9.
   PubMedGoogle Scholar
• Benešová M, Schäfer M, Bauder-Wüst U, et al. 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;56:914–20.
   PubMed Web of Science ®Google Scholar
• Afshar-Oromieh A, Hetzheim H, Kratochwil C, et al. The theranostic PSMA ligand PSMA-617 in the diagnosis of prostate cancer by PET/CT: biodistribution in humans, radiation dosimetry, and first evaluation of tumor lesions. J Nucl Med 2015;56:1697–705.
   PubMed Web of Science ®Google Scholar