Current Status of Prostate-Specific Membrane Antigen Targeting in Nuclear Medicine: Clinical Translation of Chelator Containing Prostate-Specific Membrane Antigen Ligands Into Diagnostics and Therapy for Prostate Cancer

Seminars in Nuclear Medicine

Volumn 46, Issue 5, 2016, Pages 405-418

  Kratochwil, Clemens ^a   Afshar Oromieh, Ali ^a,b   Kopka, Klaus ^b   Haberkorn, Uwe ^a,b   Giesel, Frederik L ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PROSTATE SPECIFIC MEMBRANE ANTIGEN; PROSTATE SPECIFIC MEMBRANE ANTIGEN 11 GA 68; RADIOPHARMACEUTICAL AGENT; TETRAXETAN; UNCLASSIFIED DRUG; CHELATING AGENT; GLUTAMATE CARBOXYPEPTIDASE II; GLUTAMATE CARBOXYPEPTIDASE II, HUMAN; MEMBRANE ANTIGEN;

CANCER RADIOTHERAPY; CANCER RECURRENCE; CANCER STAGING; CANCER SURGERY; CASTRATION RESISTANT PROSTATE CANCER; COMPUTER ASSISTED EMISSION TOMOGRAPHY; HUMAN; MALE; METASTASIS; NUCLEAR MEDICINE; PROSTATE CANCER; REVIEW; TUMOR RECURRENCE; CHEMISTRY; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PROCEDURES; PROSTATIC NEOPLASMS;

ANTIGENS, SURFACE; CHELATING AGENTS; GLUTAMATE CARBOXYPEPTIDASE II; HUMANS; MALE; MOLECULAR TARGETED THERAPY; NUCLEAR MEDICINE; PROSTATIC NEOPLASMS; RADIOPHARMACEUTICALS;

EID: 84983048032     PISSN: 00012998     EISSN: 15584623     Source Type: Journal    
DOI: 10.1053/j.semnuclmed.2016.04.004     Document Type: Review

References (107)

1. 1 Howlader, N., Noone, A.M., Krapcho, M., et al. SEER Cancer Statistics Review, 1975-2009 (Vintage 2009 Populations), 2012, National Cancer Institute, Bethesda, MD.
2. 2 Ferlay, J., Steliarova-Foucher, E., Lortet-Tieulent, J., et al. Cancer incidence and mortality patterns in Europe: Estimates for 40 countries in 2012. Eur J Cancer 49:6 (2013), 1374–1403.
3. 3 Lozano, R., Naghavi, M., Foreman, K., et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: A systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:9859 (2012), 2095–2128.
4. 4 Turkbey, B., Brown, A.M., Sankineni, S., et al. Multiparametric prostate magnetic resonance imaging in the evaluation of prostate cancer. CA Cancer J Clin, 2015 [Epub ahead of print].
5. 5 Bouchelouche, K., Tagawa, S.T., Goldsmith, S.J., et al. PET/CT imaging and radioimmunotherapy of prostate cancer. Semin Nucl Med 41:1 (2011), 29–44.
6. 6 Bjurlin, M.A., Rosenkrantz, A.B., Beltran, L.S., et al. Imaging and evaluation of patients with high-risk prostate cancer. Nat Rev Urol 12:11 (2015), 617–628.
7. 18F-fluorodeoxyglucose PET/CT: Utility and limitations. Eur J Nucl Med Mol Imaging 40 (2013), S5–S10 (suppl 1).
8. 18F]Fluoro-2-deoxyglucose positron emission tomography for the detection of disease in patients with prostate-specific antigen relapse after radical prostatectomy. Clin Cancer Res, 11, 2005, 4761.
9. 18F-fluorocyclobutane-1-carboxylic acid PET/CT in the diagnosis of recurrent prostate carcinoma: A meta-analysis. Acta Radiol 57:4 (2016), 487–493.
10. 11C-choline for evaluation of prostate cancer patients with biochemical recurrence: Meta-analysis and critical review of available data. Eur J Nucl Med Mol Imaging 43:1 (2016), 55–69.
11. 11 Rajasekaran, S.A., Anilkumar, G., Oshima, E., et al. A novel cytoplasmic tail MXXXL motif mediates the internalization of prostate-specific membrane antigen. Mol Biol Cell 14 (2003), 4835–4845.
12. 12 Silver, D.A., Pellicer, I., Fair, W.R., et al. Prostate-specific membrane antigen expression in normal and malignant human tissues. Clin Cancer Res 3 (1997), 81–85.
13. 13 Bostwick, D.G., Pacelli, A., Blute, M., et al. Prostate specific membrane antigen expression in prostatic intraepithelial neoplasia and adenocarcinoma: A study of 184 cases. Cancer 82 (1998), 2256–2261.
14. 14 Perner, S., Hofer, M.D., Kim, R., et al. Prostate-specific membrane antigen expression as a predictor of prostate cancer progression. Hum Pathol 38 (2007), 696–701.
15. 15 Chang, S.S., Overview of prostate-specific membrane antigen. Rev Urol 6 (2004), S13–S18 (suppl 10).
16. 16 Tykvart, J., Navrátil, V., Sedlák, F., et al. Comparative analysis of monoclonal antibodies against prostate-specific membrane antigen (PSMA). Prostate 74 (2014), 1674–1690.
17. 89Zr J591 immuno-PET imaging in patients with advanced metastatic prostate cancer. Eur J Nucl Med Mol Imaging 41 (2014), 2093–2105.
18. 18 Kasten, B.B., Liu, T., Nedrow-Byers, J.R., et al. Targeting prostate cancer cells with PSMA inhibitor-guided gold nanoparticles. Bioorg Med Chem Lett 23 (2013), 565–568.
19. 19 Mukherjee, A., Darlington, T., Holz, R., et al. Development and screening of a series of antibody-conjugated and silica-coated iron oxide nanoparticles for targeting the prostate-specific membrane antigen. Chem Med Chem 9 (2014), 1356–1360.
20. 20 Chu, T.C., Marks, J.W., Lavery, L.A., et al. Aptamer: Toxin conjugates that specifically target prostate tumor cells. Cancer Res 66 (2006), 5989–5992.
21. 21 Baek, S.E., Lee, K.H., Park, Y.S., et al. RNA aptamer-conjugated liposome as an efficient anticancer drug delivery vehicle targeting cancer cells in vivo. J Control Release 196 (2014), 234–242.
22. 22 Eder, M., Eisenhut, M., Babich, J., et al. PSMA as a target for radiolabelled small molecules. Eur J Nucl Med Mol Imaging 40 (2013), 819–823.
23. 23 Maresca, K.P., Hillier, S.M., Lu, G., et al. Small molecule inhibitors of PSMA incorporating technetium-99m for imaging prostate cancer: Effects of chelate design on pharmacokinetics. Inorg Chim Acta 389 (2012), 168–175.
24. 24 Banerjee, S.R., Foss, C.A., Castanares, M., et al. Synthesis and evaluation of technetium-99m- and rhenium-labeled inhibitors of the prostate-specific membrane antigen (PSMA). J Med Chem 51 (2008), 4504–4517.
25. ® scan: Contemporary use in clinical practice. Rev Urol 6 (2004), 19–28.
26. 26 Bander, N.H., Technology insight: Monoclonal antibody imaging of prostate cancer. Nat Clin Pract Urol 3 (2006), 216–225.
27. 27 Morris, M.J., Divgi, C.R., Pandit-Taskar, N., et al. Pilot trial of unlabeled and indium-111-labeled anti-prostate-specific membrane antigen antibody J591 for castrate metastatic prostate cancer. Clin Cancer Res 11 (2005), 7454–7461.
28. 89Zr-DFO-J591 for immunoPET of prostate-specific membrane antigen expression in vivo. J Nucl Med 51 (2010), 1293–1300.
29. 29 Jackson, P.F., Slusher, B.S., Design of NAALADase inhibitors: A novel neuroprotective strategy. Curr Med Chem 8 (2001), 949–957.
30. 30 Kozikowski, A.P., Zhang, J., Nan, F., et al. Synthesis of urea-based inhibitors as active site probes of glutamate carboxypeptidase II: Efficacy as analgesic agents. J Med Chem 47 (2004), 1729–1738.
31. 31 Tiffany, C.W., Lapidus, R.G., Merion, A., et al. Characterization of the enzymatic activity of PSM: Comparison with brain NAALADase. Prostate 39 (1999), 28–35.
32. 32 Mesters, J.R., Barinka, C., Li, W., et al. Structure of glutamate carboxypeptidase II, a drug target in neuronal damage and prostate cancer. EMBO J 25 (2006), 1375–1384.
33. 33 Maresca, K.P., Hillier, S.M., Femia, F.J., et al. A series of halogenated heterodimeric inhibitors of prostate specific membrane antigen (PSMA) as radiolabeled probes for targeting prostate cancer. J Med Chem 52 (2009), 347–357.
34. 34 Hillier, S.M., Maresca, K.P., Femia, F.J., 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 69 (2009), 6932–6940.
35. 99mTc-labeled small-molecule inhibitors of prostate-specific membrane antigen for molecular imaging of prostate cancer. J Nucl Med 54 (2013), 1369–1376.
36. mTc/Re-labeled small molecule prostate specific membrane antigen inhibitors with novel polar chelates. Bioorg Med Chem Lett 23 (2013), 1557–1563.
37. 68Ga-complex lipophilicity and the targeting property of a urea-based PSMA inhibitor for PET imaging. Bioconjugate Chem 23 (2012), 688–697.
38. 38 Barrett, J.A., Coleman, R.E., Goldsmith, S.J., et al. First-in-man evaluation of two high-affinity PSMA-avid small molecules for imaging prostate cancer. J Nucl Med 54 (2013), 380–387.
39. 68Ga]Ga-PSMA-HBED-CC: A new PET tracer for imaging of prostate cancer. Pharmaceuticals (Basel) 2014;, 7: 2014, 779–796.
40. 40 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 56 (2015), 914–920.
41. 18F]DCFPyL, a PSMA-based PET imaging agent for prostate cancer. Clin Cancer Res 17 (2011), 7645–7653.
42. 42 Lecornet, E., Ahmed, H.U., Hu, Y., et al. The accuracy of different biopsy strategies for the detection of clinically important prostate cancer: A computer simulation. J Urol 188:3 (2012), 974–980.
43. 43 Kelloff, G.J., Choyke, P., Coffey, D.S., Challenges in clinical prostate cancer: Role of imaging. AJR Am J Roentgenol, 192, 2009, 1455.
44. 44 Rajinikanth, A., Manoharan, M., Soloway, C.T., et al. Trends in Gleason score: Concordance between biopsy and prostatectomy over 15 years. Urology, 72, 2008, 177.
45. 45 Rahbar, K., Weckesser, M., Huss, S., et al. Correlation of intraprostatic tumor extent with 68-Ga-PSMA distribution in patients with prostate cancer. J Nucl Med 57:4 (2016), 563–567.
46. 68Ga-PSMA11-PET/CT and multi-parametric MR for imaging of primary rostate cancer. Eur J Nucl Med Mol Imaging, 2016 [Epub ahead of print].
47. 99mTc-trofolastat (MIP-1404) SPECT/CT to identify and localize prostate cancer in high-risk patients undergoing radical prostatectomy (RP) and extended pelvic lymph node dissection (EPLND) compared to histopathology: An interim analysis. J Clin Oncol, 32, 2014 [suppl 4; abstr 94].
48. 48 D'Amico, Anthony V., Whittington, Richard, Malkowicz, S. Bruce, et al. Biochemical outcome after radical prostatectomy, external beam radiation therapy, or interstitial radiation therapy for clinically localized prostate cancer. J Am Med Assoc 280:11 (1998), 969–974.
49. 49 Roach, M. III, Marquez, C., Yuo, H.S., et al. Predicting the risk of lymph node involvement using the pre-treatment prostate specific antigen and Gleason score in men with clinically localized prostate cancer. Int J Radiat Oncol Biol Phys 28:1 (1994), 33–37.
50. 50 Yu, J.B., Makarov, D.V., Gross, C., A new formula for prostate cancer lymph node risk. Int J Radiat Oncol Biol Phys 80:1 (2011), 69–75.
51. 68Ga-PSMA-11 PET/CT: A new technique with high potential for the radiotherapeutic management of prostate cancer patients. Eur J Nucl Med Mol Imaging 43:1 (2016), 34–41.
52. 52 Shakespeare, T.P., Effect of prostate-specific membrane antigen positron emission tomography on the decision-making of radiation oncologists. Radiat Oncol, 10, 2015, 233.
53. 68Ga-Prostate-specific membrane antigen has a high detection rate of prostate cancer recurrence outside the prostatic fossa in patients being considered for salvage radiation treatment. BJU Int 117:5 (2016), 732–739.
54. 54 Heidenreich, A., Ohlmann, C.H., Polyakov, S., Anatomical extent of pelvic lymphadenectomy in patients undergoing radical prostatectomy. Eur Urol 52:1 (2007), 29–37.
55. 55 Weckermann, D., Dorn, R., Trefz, M., et al. Sentinel lymph node dissection for prostate cancer: Experience with more than 1,000 patients. J Urol 177:3 (2007), 916–920.
56. 56 Van den Bergh, L., Joniau, S., Haustermans, K., et al. Reliability of sentinel node procedure for lymph node staging in prostate cancer patients at high risk for lymph node involvement. Acta Oncol 54:6 (2015), 896–902.
57. 57 Hövels, A.M., Heesakkersb, R.A., Adang, E.M., et al. The diagnostic accuracy of CT and MRI in the staging of pelvic lymph nodes in patients withprostate cancer: A meta-analysis. Clin Radiol 63 (2008), 387–395.
58. 58 Giesel, F.L., Fiedler, H., Stefanova, M., et al. PSMA PET/CT with Glu-urea-Lys-(Ahx)-[Ga(HBED-CC)] versus 3D CT volumetric lymph node assessment in recurrent prostate cancer. Eur J Nucl Med Mol Imaging 42:12 (2015), 1794–1800.
59. 59 Hijazi, S., Meller, B., Leitsmann, C., et al. See the unseen: Mesorectal lymph node metastases in prostate cancer. Prostate 76:8 (2016), 776–780.
60. 68Ga-PSMA positron emission tomography/computed tomography provides accurate staging of lymph node regions prior to lymph node dissection in patients with prostate cancer. Eur Urol, 2016 [Epub ahead of print].
61. 68Ga-PSMA-positron emission tomography/computerized tomography. Prostate 75:16 (2015), 1934–1940.
62. 111In]PSMA-I&T: Expanding the spectrum of PSMA-I&T applications towards SPECT and radioguided surgery. EJNMMI Res, 5(1), 2015, 68.
63. 68Ga-labelled PSMA ligand HBED-CC in the diagnosis of recurrent prostate cancer. Eur J Nucl Med Mol Imaging 42:2 (2015), 197–209.
64. 64 Eiber, M., Maurer, T., Souvatzoglou, M., et al. Evaluation of hybrid Ga-PSMA ligand PET/CT in 248 patients with biochemical recurrence after radical prostatectomy. J Nucl Med 56:5 (2015), 668–674.
65. 68Ga-PSMA PET/CT for restaging recurrent prostate cancer: Which factors are associated with PET/CT detection rate?. Eur J Nucl Med Mol Imaging 42:8 (2015), 1284–1294.
66. 68Ga-PSMA PET/CT in prostate cancer patients who have rising PSA after curative treatment and are being considered for targeted therapy. J Nucl Med 56:8 (2015), 1185–1190.
67. 18F-choline-based PET/CT for the diagnosis of recurrent prostate cancer. Eur J Nucl Med Mol Imaging 41:1 (2014), 11–20.
68. 68 Heidenreich, A., Bastian, P.J., Bellmunt, J., et al. EAU guidelines on prostate cancer. Part II: Treatment of advanced, relapsing, and castration-resistant prostate cancer. Eur Urol 65 (2014), 467–479.
69. 18F-choline-PET/CT. Clin Nucl Med, 2016, 11.
70. 68Ga]-labeled bombesin analog BAY86-7548. Clin Cancer Res 19:19 (2013), 5434–5443.
71. 18F-radiolabeled bombesin analogue BAY 864367 in patients with prostate cancer. J Nucl Med 56:3 (2015), 372–378.
72. 68Ga-PSMA PET in patients with biochemically recurrent prostate cancer. J Nucl Med 57 (2016), 557–562.
73. 73 Liolios, C., Schäfer, M., Haberkorn, U., et al. Novel bispecific PSMA/GRPr targeting radioligands with optimized pharmacokinetics for improved PET imaging of prostate cancer. Bioconjug Chem, 2016 [Epub ahead of print].
74. 18F-fluoride PET/CT. J Nucl Med 47:2 (2006), 287–297.
75. 75 Dehdashti, F., Picus, J., Michalski, J.M., et al. Positron tomographic assessment of androgen receptors in prostatic carcinoma. Eur J Nucl Med Mol Imaging 32:3 (2005), 344–350.
76. 76 Olbert, P.J., Hegele, A., Kraeuter, P., et al. Clinical significance of a prostate-specific antigen flare phenomenon in patients with hormone-refractory prostate cancer receiving docetaxel. Anticancer Drugs 17 (2006), 993–996.
77. 77 Kuroda, K., Liu, H., Kim, S., et al. Docetaxel down-regulates the expression of androgen receptor and prostate-specific antigen but not prostate-specific membrane antigen in prostate cancer cell lines: Implications for PSA surrogacy. Prostate 69:14 (2009), 1579–1585.
78. 78 Nossa, Kenneth R., Wolfe, Steven A., Grimes, Sidney R., Upregulation of prostate specific membrane antigen/folate hydrolase transcription by an enhancer. Gene 285:1-2 (2002), 247–256.
79. 79 Wright, G.L. Jr., Grob, B.M., Haley, C., et al. Upregulation of prostate-specific membrane antigen after androgen-deprivation therapy. Urology 48 (1996), 326–334.
80. 80 Liu, T., Wu, L.Y., Fulton, M.D., et al. Prolonged androgen deprivation leads to downregulation of androgen receptor and prostate-specific membrane antigen in prostate cancer cells. Int J Oncol 41:6 (2012), 2087–2092.
81. 81 Meller, B., Bremmer, F., Sahlmann, C.O., et al. Alterations in androgen deprivation enhanced prostate-specific membrane antigen (PSMA) expression in prostate cancer cells as a target for diagnostics and therapy. EJNMMI Res, 5(1), 2015, 66.
82. 82 Murphy, G., Ragde, H., Kenny, G., et al. Comparison of prostate specific membrane antigen, and prostate specific antigen levels in prostatic cancer patients. Anticancer Res 15:4 (1995), 1473–1479.
83. 83 Evans, M.J., Smith-Jones, P.M., Wongvipat, J., et al. Noninvasive measurement of androgen receptor signaling with a positron-emitting radiopharmaceutical that targets prostate-specific membrane antigen. Proc Natl Acad Sci U S A 108:23 (2011), 9578–9582.
84. 223Ra therapy in a prostate cancer patient. Eur J Nucl Med Mol Imaging 42:2 (2015), 362–363.
85. 85 Kratochwil, C., Giesel, F.L., Stefanova, M., et al. PSMA-targeted radionuclide therapy of metastatic castration-resistant prostate cancer with Lu-177 labeled PSMA-617. J Nucl Med, 2016 [Epub ahead of print].
86. 86 Crawford, E.D., Higano, C.S., Shore, N.D., et al. Treating patients with metastatic castration resistant prostate cancer: A comprehensive review of available therapies. J Urol 194 (2015), 1537–1547.
87. 87 van Soest, R.J., van Royen, M.E., de Morrée, E.S., et al. Cross-resistance between taxanes and new hormonal agents abiraterone and enzalutamide may affect drug sequence choices in metastatic castration-resistant prostate cancer. Eur J Cancer 49 (2013), 3821–3830.
88. 88 Ma, D., Hopf, C.E., Malewicz, A.D., et al. Potent antitumor activity of an auristatin-conjugated, fully human monoclonal antibody to prostate-specific membrane antigen. Clin Cancer Res 12 (2006), 2591–2596.
89. 89 Rose, J.N., Crook, J.M., The role of radiation therapy in the treatment of metastatic castrate-resistant prostate cancer. Ther Adv Urol 7 (2015), 135–145.
90. 177Lu-DOTAhuJ591 anti prostate specific membrane antigen specific monoclonal antibody. Curr Radiopharm 9:1 (2016), 44–53.
91. 131I-labeled small molecule (MIP-1095) targeting PSMA for prostate cancer therapy. Eur J Nucl Med Mol Imaging 41:7 (2014), 1280–1292.
92. 92 Baum, R.P., Kulkarni, H.R., Schuchardt, C., et al. Lutetium-177 PSMA radioligand therapy of metastatic castration-resistant prostate cancer: Safety and efficacy. J Nucl Med, 2016 [Epub ahead of print].
93. 93 Barinka, C., Byun, Y., Dusich, C.L., et al. Interactions between human glutamate carboxypeptidase II and urea-based inhibitors: Structural characterization. J Med Chem 51 (2008), 7737–7743.
94. 94 Gourni, E., Canovas, C., Goncalves, V., et al. (R)-NODAGA-PSMA: A versatile precursor for radiometal labeling and nuclear imaging of PSMA-positive tumors. PLoS One, 10, 2015, e0145755.
95. 95 Benešová, M., Bauder-Wüst, U., Schäfer, M., et al. Linker modification strategies to control the prostate-specific membrane antigen (PSMA)-targeting and pharmacokinetic properties of DOTA-conjugated PSMA inhibitors. J Med Chem 59:5 (2016), 1761–1775.
96. 177Lu-PSMA-617 prostate-specific membrane antigen (PSMA) inhibitor in patients with castration-resistant prostate cancer. Eur J Nucl Med Mol Imaging 42:13 (2015), 1976–1983.
97. 177Lu-DKFZ-PSMA-617: A new radiopharmaceutical for the treatment of metastatic prostate cancer. Eur J Nucl Med Mol Imaging 43:1 (2016), 42–51.
98. 177Lu]DKFZ-PSMA-617. Mol Imaging Biol, 18, 2016.
99. 177Lu]Lutetium-labelled PSMA ligand-induced remission in a patient with metastatic prostate cancer. Eur J Nucl Med Mol Imaging 42:6 (2015), 987–988.
100. 177Lu prostate-specific membrane antigen treatment in patient with metastatic prostate cancer. Clin Nucl Med 41:2 (2016), 159–160.
101. 177Lu PSMA-617 therapy on bone marrow depression caused by metastatic prostate cancer. Clin Nucl Med, 41, 2016.
102. 177Lu-PSMA-DKFZ-617 of castrate-resistant metastatic prostate cancer. Oncotarget, 2016 [Epub ahead of print].
103. 177Lu-PSMA-I&T in patients with metastatic castration-resistant prostate cancer. J Urol, 2016 [Epub ahead of print].
104. 104 Kratochwil, C., Giesel, F.L., Bruchertseifer, F., et al. 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 41 (2014), 2106–2119.
105. 105 Kratochwil, C., Bruchertseifer, F., Giesel, F.L., et al. Ac-225-PSMA617 PSMA-gerichtete Alpha-Strahler-Therapie des metastasierten Prostatakarzinoms. Nuklearmedizin 54 (2016), A26–V68.
106. 106 Milowsky, M.I., Nanus, D.M., Kostakoglu, L., et al. Vascular targeted therapy with anti-prostate-specific membrane antigen monoclonal antibody J591 in advanced solid tumors. J Clin Oncol 25:5 (2007), 540–547.
107. 68Ga-DKFZ-PSMA-11 and its performance in prostate cancer patients. Molecules 20:8 (2015), 14860–14878.