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

Journal of Drug Targeting

Volumn 24, Issue 8, 2016, Pages 679-693

  Machulkin, Alexey E ^a,b   Ivanenkov, Yan A ^a,b,c   Aladinskaya, Anastasia V ^c   Veselov, Mark S ^c   Aladinskiy, Vladimir A ^c   Beloglazkina, Elena K ^a   Koteliansky, Victor E ^a,d   Shakhbazyan, Artem G ^c   Sandulenko, Yuri B ^c   Majouga, Alexander G ^a,b  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b NATIONAL UNIVERSITY OF SCIENCE AND TECHNOLOGY MISIS   (Russian Federation)

^c MOSCOW INSTITUTE OF PHYSICS AND TECHNOLOGY   (Russian Federation)

^d SKOLKOVO INSTITUTE OF SCIENCE AND TECHNOLOGY   (Russian Federation)

Author keywords

Drug delivery; Glutamate carboxypeptidase II; Inhibitors; Prostate cancer

Indexed keywords

ANTIBODY; APTAMER; GLUTAMATE CARBOXYPEPTIDASE II; GLUTAMATE CARBOXYPEPTIDASE II INHIBITOR; PHOSPHORUS; PROSTATE SPECIFIC MEMBRANE ANTIGEN; THIOL; UREA; DRUG CARRIER; GLUTAMATE CARBOXYPEPTIDASE II, HUMAN; LIGAND; MEMBRANE ANTIGEN; PROTEIN BINDING;

BINDING AFFINITY; BIOAVAILABILITY; BIOLOGICAL ACTIVITY; DRUG DELIVERY SYSTEM; DRUG TARGETING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE PERMEABILITY; MOLECULAR DIAGNOSIS; NONHUMAN; PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROSTATE CANCER; REVIEW; STRUCTURE ACTIVITY RELATION; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; MALE; METABOLISM; MOLECULAR LIBRARY; MOLECULARLY TARGETED THERAPY; PHARMACOKINETICS; PROSTATE TUMOR;

ANTIGENS, SURFACE; BINDING SITES; DRUG CARRIERS; GLUTAMATE CARBOXYPEPTIDASE II; HUMANS; LIGANDS; MALE; MOLECULAR STRUCTURE; MOLECULAR TARGETED THERAPY; PROSTATIC NEOPLASMS; PROTEIN BINDING; SMALL MOLECULE LIBRARIES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84961206198     PISSN: 1061186X     EISSN: 10292330     Source Type: Journal    
DOI: 10.3109/1061186X.2016.1154564     Document Type: Review

References (70)

1. R.Siegel, J.Ma, Z.Zou, A.Jemal Cancer statistics, 2014. CA Cancer J Clin 2014;64:9–29.
2. R.Siegel, D.Naishadham, A.Jemal Cancer statistics, 2012. CA Cancer J Clin 2012;62:10–29.
3. D.L.Hudson Epithelial stem cells in human prostate growth and disease. Prostate Cancer Prostatic Dis 2004;7:188–94.
4. A.Ghosh, W.D.Heston Tumor target prostate specific membrane antigen (PSMA) and its regulation in prostate cancer. J Cell Biochem 2004;91:528–39.
5. T.D.Schmittgen, S.Teske, R.L.Vessella,. Expression of prostate specific membrane antigen and three alternatively spliced variants of PSMA in prostate cancer patients. Int J Cancer 2003;107:323–9.
6. S.D.Sweat, A.Pacelli, G.P.Murphy, D.G.Bostwick Prostate-specific membrane antigen expression is greatest in prostate adenocarcinoma and lymph node metastases. Urology 1998;52:637–40.
7. D.A.Silver, I.Pellicer, W.R.Fair,. Prostate-specific membrane antigen expression in normal and malignant human tissues. Clin Cancer Res 1997;3:81–5.
8. N.Sharifi, J.L.Gulley, W.L.Dahut Androgen deprivation therapy for prostate cancer. JAMA 2005;294:238–44.
9. J.P.Dassie, L.I.Hernandez, G.S.Thomas1,. Targeted inhibition of prostate cancer metastases with an RNA aptamer to prostate-specific membrane antigen. Mol Ther 2014;22:1910–22.
10. S.S.Taneja ProstaScint® scan: contemporary use in clinical practice. Rev Urol 2004;6:19–28.
11. S.Vallabhajosula, S.J.Goldsmith, K.A.Hamacher,. 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.
12. P.M.Smith-Jones, S.Vallabhajosula, V.Navarro,. 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.
13. S.T.Tagawa, M.I.Milowsky, M.Morris,. 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.
14. S.M.Hillier, K.P.Maresca, F.J.Femia,. 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.
15. 99mTc-labeled small-molecule inhibitors of prostate-specific membrane antigen for molecular imaging of prostate cancer. J Nucl Med 2013;54:1369–76.
16. M.Eder, M.Schafer, U.Bauder-Wust,. 68Ga-complex lipophilicity and the targeting property of a urea-based PSMA inhibitor for PET imaging. Bioconjug Chem 2012;23:688–97.
17. J.T.Pinto, B.P.Suffoletto, T.M.Bergin Prostate-specific membrane antigen: a novel folate hydrolase in human prostatic carcinoma cells. Clin Cancer Res 1996;2:1445–51.
18. P.M.Smith-Jones, S.Vallabahajosula, S.J.Goldsmith,. In vitro characterization of radiolabeled monoclonal antibodies specific for the extracellular domain of prostate-specific membrane antigen. Cancer Res 2000;60:5237–43.
19. P.W.Kantoff, T.J.Schuetz, B.A.Blumenstein,. 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.
20. H.Kübler, B.Scheel, U.Gnad-Vogt,. Self-adjuvanted mRNA vaccination in advanced prostate cancer patients: a first-in-man phase I/IIa study. J Immunother Cancer 2015;3:26.
21. M.I.Davis, M.J.Bennett, L.M.Thomas, P.J.Bjorkman Crystal structure of prostate-specific membrane antigen, a tumor marker and peptidase. Proc Natl Acad Sci USA 2005;102:5981–6.
22. V.Serval, T.Galli, A.Cheramy,. 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.
23. N.Subasinghe, M.Schulte, M.Y.Chan,. 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.
24. K.P.Maresca, S.M.Hillier, F.J.Femia,. 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.
25. C.Barinka, M.Rovenská, P.Mlcochová,. Structural insight into the pharmacophore pocket of human glutamate carboxypeptidase II. J Med Chem 2007;50:3267–73.
26. P.F.Jackson, D.C.Cole, B.S.Slusher,. Design, synthesis, and biological activity of a potent inhibitor of the neuropeptidase N-acetylated alphalinked acidic dipeptidase. J Med Chem 1996;39:619–22.
27. D.Vitharana, J.E.France, D.Scarpetti,. Synthesis and biological evaluation of (R)- and (S)-2-(phosphonomethyl)pentanedioic acids as inhibitors of glutamate carboxypeptidase II. Tetrahedron: Asymm 2002;13:1609–14.
28. P.F.Jackson, K.L.Tays, K.M.Maclin,. Design and pharmacological activity of phosphinic acid based NAALADase inhibitors. J Med Chem 2001;44:4170–5.
29. T.Tsukamoto, J.M.Flanary, C.Rojas,. Phosphonate and phosphinate analogues of N-acylated gamma-glutamylglutamate. potent inhibitors of glutamate carboxypeptidase II. Bioorg Med Chem Lett 2002;12:2189–92.
30. A.J.Williams, X.M.Lu, B.Slusher, F.C.Tortella 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.
31. F.Nan, T.Bzdega, S.Pshenichkin,. 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.
32. C.Barinka, K.Hlouchova, M.Rovenska,. Structural basis of interactions between human glutamate carboxypeptidase II and its substrate analogs. J Mol Biol 2008;376:1438–50.
33. K.Graham, R.Lesche, A.V.Gromov,. 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.
34. M.Beheshti, T.Kunit, S.Haim,. 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.
35. R.Lesche, G.Kettschau, A.V.Gromov,. 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.
36. S.Vallabhajosula, A.Nikolopoulou, J.W.Babich,. 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.
37. S.E.Lapi, H.Wahnishe, D.Pham,. 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.
38. T.Liu, Y.Toriyabe, M.Kazak, C.E.Berkman Pseudoirreversible inhibition of prostate-specific membrane antigen by phosphoramidate peptidomimetics. Biochemistry 2008;47:12658–60.
39. T.Ganguly, S.Dannoon, M.R.Hopkins,. A high-affinity [(18)F]-labeled phosphoramidate peptidomimetic PSMA-targeted inhibitor for PET imaging of prostate cancer. Nucl Med Biol 2015;42:780–7.
40. P.Majer, P.F.Jackson, G.Delahanty,. 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.
41. S.J.vanderPost de Visser, M.L.de Kam, M.Woefler,. The central nervous system effects, pharmacokinetics and safety of the NAALADase-inhibitor GPI 5693. Br J Clin Pharmacol 2005;60:128–36.
42. D.W.Cushman, H.S.Cheung, E.F.Sabo, M.A.Ondetti Design of potent competitive inhibitors of angiotensin-converting enzyme. Carboxyalkanoyl and mercaptoalkanoyl amino acids. Biochemistry 1977;16:5484–91.
43. M.A.Ondetti, M.E.Condon, J.Reid,. Design of potent and specific inhibitors of carboxypeptidases A and B. Biochemistry 1979;18:1427–30.
44. P.Majer, B.Hin, D.Stoermer,. Structural optimization of thiol-based inhibitors of glutamate carboxypeptidase II by modification of the P1' side chain. J Med Chem 2006;49:2876–85.
45. D.Stoermer, D.Vitharana, N.Hin,. Design, synthesis, and pharmacological evaluation of glutamate carboxypeptidase II (GCPII) inhibitors based on thioalkylbenzoic acid scaffolds. J Med Chem 2012;55:5922–32.
46. D.V.Ferraris, P.Majer, C.Ni,. δ-Thiolactones as prodrugs of thiol-based glutamate carboxypeptidase II (GCPII) inhibitors. J Med Chem 2014;57:243–7.
47. P.M.Dansette, J.Libraire, G.Bertho, D.Mansuy 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.
48. A.P.Kozikowski, F.Nan, P.Conti,. Design of remarkably simple, yet potent urea-based inhibitors of glutamate carboxypeptidase II (NAALADase). J Med Chem 2001;44:298–301.
49. M.G.Pomper, J.L.Musachio, J.Zhang,. 11C-MCG: synthesis, uptake selectivity, and primate PET of a probe for glutamate carboxypeptidase II (NAALADase). Mol Imaging 2002;1:96–101.
50. C.A.Foss, R.C.Mease, H.Fan,. 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.
51. C.Barinka, Y.Byun, C.L.Dusich,. Interactions between human glutamate carboxypeptidase II and urea-based inhibitors: structural characterization. J Med Chem 2008;51:7737–43.
52. S.Y.Cho, K.L.Gage, R.C.Mease,. 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.
53. 18F-DCFBC PET/CT for PSMA-based detection and characterization of primary prostate cancer. J Nucl Med 2015;56:1003–10.
54. M.Srinivasarao, C.V.Galliford, P.S.Low Principles in the design of ligand-targeted cancer therapeutics and imaging agents. Nat Rev Drug Discov 2015;14:203–19.
55. Z.Szabo, E.Mena, S.P.Rowe,. 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.
56. J.Hrkach, D.V.Hoff, M.M.Ali,. Preclinical development and clinical translation of a PSMA-targeted docetaxel nanoparticle with a differentiated pharmacological profile. Sci Transl Med 2012;4:128–39.
57. H.Wang, Y.Byun, C.Barinka,. Bioisosterism of urea-based GCPII inhibitors: synthesis and structure–activity relationship studies. Bioorg Med Chem Lett 2010;20:392–7.
58. J.Tykvart, J.Schimer, J.Bařinková,. 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.
59. J.Tykvart, J.Schimer, A.Jančařík,. Design of highly potent urea-based, exosite-binding inhibitors selective for glutamate carboxypeptidase II. J Med Chem 2015;58:4357–63.
60. R.T.Olszewski, N.Bukhari, J.Zhou,. 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.
61. T.Yamamoto, O.Saito, T.Aoe,. Local administration of N-acetylaspartylglutamate (NAAG) peptidase inhibitors is analgesic in peripheral pain in rats. Eur J Neurosci 2007;25:147–58.
62. C.Zhong, X.Zhao, J.Sarva,. NAAG peptidase inhibitor reduces acute neuronal degeneration and astrocyte damage following lateral fluid percussion TBI in rats. J Neurotrauma 2005;22:266–76.
63. A.P.Kozikowski, J.Zhang, F.J.Nan,. Synthesis of urea-based inhibitors as active site probes of glutamate carboxypeptidase II: efficacy as analgesic agents. J Med Chem 2004;47:1729–38.
64. S.A.Kularatne, Z.Zhou, J.Yang,. Design, synthesis, and preclinical evaluation of prostate-specific membrane antigen targeted 99mTc-radioimaging agents. Mol Pharm 2009;6:790–800.
65. S.A.Kularatne, K.Wang, H.K.Santhapuram, P.S.Low 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.
66. J.Roy, T.X.Nguyen, A.K.Kanduluru,. DUPA conjugation of a cytotoxic indenoisoquinoline topoisomerase I inhibitor for selective prostate cancer cell targeting. J Med Chem 2015;58:3094–103.
67. J.A.Barrett, R.E.Coleman, S.J.Goldsmith,. First-in-man evaluation of 2 high-affinity PSMA-avid small molecules for imaging prostate cancer. J Nucl Med 2013;54:380–7.
68. M.M.Linn, R.A.Ball, A.Maradiegue Prostate-specific antigen screening: friend or foe? Urol Nurs 2007;27:481–9.
69. M.Benešová, M.Schäfer, U.Bauder-Wüst,. 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.
70. A.Afshar-Oromieh, H.Hetzheim, C.Kratochwil,. 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.