Recent progress of positron radionuclide labeled small molecule inhibitors of prostate specific membrane antigen for PET/CT imaging of prostate cancer_Journal of Biomedical Engineering

Authors：

PAN Lili , WU Xiaoai , DIAO Wei ,  LI Lin

Department of Nuclear Medicine, Laboratory of Clinical Nuclear Medicine, West China Hospital, Sichuan University, Chengdu 610041, P.R.China;

Corresponding author：

LI Lin, Email: lilinhuaxi@sina.com

Keywords：

prostate cancer; prostate-specific membrane antigen; radiopharmaceuticals; positron emission tomography/computed tomography

DOI：

10.7507/1001-5515.201911073

Video：

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Abstract Full text Figures/Tables Video References Cited by

Prostate cancer is the most common tumor of the urinary system, and its mortality rate is second only to lung cancer. With the specific and high expression on the surface of prostate cancer cells, prostate-specific membrane antigen (PSMA) has been an ideal theranostic target of prostate cancer with great clinical significance and research value. Positron emission tomography/computed tomography (PET/CT), a new modality of molecular imaging combining functional metabolic information and anatomical structure, provides high diagnostic performance for cancer detection. This paper mainly reviewed recent progress of PSMA inhibitors labeled by positron-emitting radionuclides for early diagnosis, preoperative staging, response assessment, restaging and metastasis detection of prostate cancer.

Citation： PAN Lili, WU Xiaoai, DIAO Wei, LI Lin. Recent progress of positron radionuclide labeled small molecule inhibitors of prostate specific membrane antigen for PET/CT imaging of prostate cancer. Journal of Biomedical Engineering, 2020, 37(2): 219-224. doi: 10.7507/1001-5515.201911073 Copy

1.	Siegel R L, Miller K D, Jemal A. Cancer statistics, 2018. CA Cancer J Clin, 2018, 68(1): 7-30.
2.	Chen Wanqing, Zheng Rongshou, Baade P D, et al. Cancer statistics in China, 2015. CA Cancer J Clin, 2016, 66(2): 115-132.
3.	韩苏军, 张思维, 陈万青, 等. 中国前列腺癌发病现状和流行趋势分析. 临床肿瘤学杂志, 2013, 18(4): 330-334.
4.	朱刚, 刘明, 万奔. 早期前列腺癌的诊断与治疗. 中华男科学杂志, 2005, 11(9): 693-696, 712.
5.	Perner S, Hofer M D, Kim R, et al. Prostate-specific membrane antigen expression as a predictor of prostate cancer progression. Hum Pathol, 2007, 38(5): 696-701.
6.	O’Keefe D S, Su S L, Bacich D J, et al. Mapping, genomic organization and promoter analysis of the human prostate-specific membrane antigen gene. Biochim Biophys Acta, 1998, 1443(1/2): 113-127.
7.	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.
8.	Robinson M B, Blakely R D, Couto R, et al. Hydrolysis of the brain dipeptide N-acetyl-L-aspartyl-L-glutamate. Identification and characterization of a novel N-acetylated alpha-linked acidic dipeptidase activity from rat brain. J Biol Chem, 1987, 262(30): 14498-14506.
9.	Carter R E, Feldman A R, Coyle J T. Prostate-specific membrane antigen is a hydrolase with substrate and pharmacologic characteristics of a neuropeptidase. Proc Natl Acad Sci U S A, 1996, 93(2): 749-753.
10.	Barrio M, Fendler W P, Czernin J A. Prostate specific membrane antigen (PSMA) ligands for diagnosis and therapy of prostate cancer. Expert Rev Mol Diagn, 2016, 16(11): 1177-1188.
11.	Huang E, Teh B S, Mody D R, et al. Prostate adenocarcinoma presenting with inguinal lymphadenopathy. Urology, 2003, 61(2): 463.
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, 1997, 3(1): 81-85.
13.	Tsukamoto T, Wozniak K M, Slusher B S. Progress in the discovery and development of glutamate carboxypeptidase II inhibitors. Drug Discov Today, 2007, 12(17/18): 767-776.
14.	Majer P, Jackson P F, 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(10): 1989-1996.
15.	Eder M, Schäfer M, Bauder-Wüst U, et al. 68Ga-complex lipophilicity and the targeting property of a urea-based PSMA inhibitor for PET imaging. Bioconjug Chem, 2012, 23(4): 688-697.
16.	Liu Tiancheng, Wu L Y, Kazak M, et al. Cell-surface labeling and internalization by a fluorescent inhibitor of prostate-specific membrane antigen. Prostate, 2008, 68(9): 955-964.
17.	Lapi S E, 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(12): 2042-2048.
18.	Ganguly T, Dannoon S, Hopkins M R, et al. A high-affinity[¹⁸F]-labeled phosphoramidate peptidomimetic PSMA-targeted inhibitor for PET imaging of prostate cancer. Nucl Med Biol, 2015, 42(10): 780-787.
19.	Hao Guiyang, Kumar A, Dobin T, et al. A multivalent approach of imaging probe design to overcome an endogenous anion binding competition for noninvasive assessment of prostate specific membrane antigen. Mol Pharm, 2013, 10(8): 2975-2985.
20.	Pomper M G, Musachio J L, Zhang Jiazhong, et al. ¹¹C-MCG: synthesis, uptake selectivity, and primate PET of a probe for glutamate carboxypeptidase II (NAALADase). Mol Imaging, 2002, 1(2): 96-101.
21.	Mease R C, Dusich C L, Foss C A, et al. 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(10): 3036-3043.
22.	Cho S Y, Gage K L, Mease R C, 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(12): 1883-1891.
23.	Rowe S P, Macura K J, Ciarallo A, et al. 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.
24.	Harmon S A, Bergvall E, Mena E, et al. A prospective comparison of ¹⁸F-sodium fluoride PET/CT and PSMA-targeted ¹⁸F-DCFBC PET/CT in metastatic prostate cancer. J Nucl Med, 2018, 59(11): 1665-1671.
25.	Chen Y, Pullambhatla M, Foss C A, et al. 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.
26.	Szabo Z, Mena E, Rowe S P, et al. Initial evaluation of[¹⁸F]DCFPyL for prostate-specific membrane antigen (PSMA)-targeted PET imaging of prostate cancer. Mol Imaging Biol, 2015, 17(4): 565-574.
27.	Rowe S P, Macura K J, Mena E, et al. PSMA-based[¹⁸F]DCFPyL PET/CT is superior to conventional imaging for lesion detection in patients with metastatic prostate cancer. Mol Imaging Biol, 2016, 18(3): 411-419.
28.	Chen Ying, Lisok A, Chatterjee S, et al. [¹⁸F]fluoroethyl triazole substituted PSMA inhibitor exhibiting rapid normal organ clearance. Bioconjug Chem, 2016, 27(7): 1655-1662.
29.	Cardinale J, Schäfer M, Benešová M, et al. 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.
30.	Giesel F L, Will L, Lawal I, et al. Intraindividual comparison of ¹⁸F-PSMA-1007 and ¹⁸F-DCFPyL PET/CT in the prospective evaluation of patients with newly diagnosed prostate carcinoma: a pilot study. J Nucl Med, 2018, 59(7): 1076-1080.
31.	Giesel F L, Hadaschik B, Cardinale J, et al. 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.
32.	Afshar-Oromieh A, Malcher A, Eder M, et al. PET imaging with a[⁶⁸Ga]gallium-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(4): 486-495.
33.	Pfister D, Porres D, Heidenreich A, et al. Detection of recurrent prostate cancer lesions before salvage lymphadenectomy is more accurate with ⁶⁸Ga-PSMA-HBED-CC than with ¹⁸F-Fluoroethylcholine PET/CT. Eur J Nucl Med Mol Imaging, 2016, 43(8): 1410-1417.
34.	Afshar-Oromieh A, Holland-Letz T, Giesel F L, et al. Diagnostic performance of ⁶⁸Ga-PSMA-11(HBED-CC) PET/CT in patients with recurrent prostate cancer: evaluation in 1007 patients. Eur J Nucl Med Mol Imaging, 2017, 44(8): 1258-1268.

1. Siegel R L, Miller K D, Jemal A. Cancer statistics, 2018. CA Cancer J Clin, 2018, 68(1): 7-30.
2. Chen Wanqing, Zheng Rongshou, Baade P D, et al. Cancer statistics in China, 2015. CA Cancer J Clin, 2016, 66(2): 115-132.
3. 韩苏军, 张思维, 陈万青, 等. 中国前列腺癌发病现状和流行趋势分析. 临床肿瘤学杂志, 2013, 18(4): 330-334.
4. 朱刚, 刘明, 万奔. 早期前列腺癌的诊断与治疗. 中华男科学杂志, 2005, 11(9): 693-696, 712.
5. Perner S, Hofer M D, Kim R, et al. Prostate-specific membrane antigen expression as a predictor of prostate cancer progression. Hum Pathol, 2007, 38(5): 696-701.
6. O’Keefe D S, Su S L, Bacich D J, et al. Mapping, genomic organization and promoter analysis of the human prostate-specific membrane antigen gene. Biochim Biophys Acta, 1998, 1443(1/2): 113-127.
7. 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.
8. Robinson M B, Blakely R D, Couto R, et al. Hydrolysis of the brain dipeptide N-acetyl-L-aspartyl-L-glutamate. Identification and characterization of a novel N-acetylated alpha-linked acidic dipeptidase activity from rat brain. J Biol Chem, 1987, 262(30): 14498-14506.
9. Carter R E, Feldman A R, Coyle J T. Prostate-specific membrane antigen is a hydrolase with substrate and pharmacologic characteristics of a neuropeptidase. Proc Natl Acad Sci U S A, 1996, 93(2): 749-753.
10. Barrio M, Fendler W P, Czernin J A. Prostate specific membrane antigen (PSMA) ligands for diagnosis and therapy of prostate cancer. Expert Rev Mol Diagn, 2016, 16(11): 1177-1188.
11. Huang E, Teh B S, Mody D R, et al. Prostate adenocarcinoma presenting with inguinal lymphadenopathy. Urology, 2003, 61(2): 463.
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, 1997, 3(1): 81-85.
13. Tsukamoto T, Wozniak K M, Slusher B S. Progress in the discovery and development of glutamate carboxypeptidase II inhibitors. Drug Discov Today, 2007, 12(17/18): 767-776.
14. Majer P, Jackson P F, 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(10): 1989-1996.
15. Eder M, Schäfer M, Bauder-Wüst U, et al. 68Ga-complex lipophilicity and the targeting property of a urea-based PSMA inhibitor for PET imaging. Bioconjug Chem, 2012, 23(4): 688-697.
16. Liu Tiancheng, Wu L Y, Kazak M, et al. Cell-surface labeling and internalization by a fluorescent inhibitor of prostate-specific membrane antigen. Prostate, 2008, 68(9): 955-964.
17. Lapi S E, 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(12): 2042-2048.
18. Ganguly T, Dannoon S, Hopkins M R, et al. A high-affinity[¹⁸F]-labeled phosphoramidate peptidomimetic PSMA-targeted inhibitor for PET imaging of prostate cancer. Nucl Med Biol, 2015, 42(10): 780-787.
19. Hao Guiyang, Kumar A, Dobin T, et al. A multivalent approach of imaging probe design to overcome an endogenous anion binding competition for noninvasive assessment of prostate specific membrane antigen. Mol Pharm, 2013, 10(8): 2975-2985.
20. Pomper M G, Musachio J L, Zhang Jiazhong, et al. ¹¹C-MCG: synthesis, uptake selectivity, and primate PET of a probe for glutamate carboxypeptidase II (NAALADase). Mol Imaging, 2002, 1(2): 96-101.
21. Mease R C, Dusich C L, Foss C A, et al. 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(10): 3036-3043.
22. Cho S Y, Gage K L, Mease R C, 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(12): 1883-1891.
23. Rowe S P, Macura K J, Ciarallo A, et al. 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.
24. Harmon S A, Bergvall E, Mena E, et al. A prospective comparison of ¹⁸F-sodium fluoride PET/CT and PSMA-targeted ¹⁸F-DCFBC PET/CT in metastatic prostate cancer. J Nucl Med, 2018, 59(11): 1665-1671.
25. Chen Y, Pullambhatla M, Foss C A, et al. 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.
26. Szabo Z, Mena E, Rowe S P, et al. Initial evaluation of[¹⁸F]DCFPyL for prostate-specific membrane antigen (PSMA)-targeted PET imaging of prostate cancer. Mol Imaging Biol, 2015, 17(4): 565-574.
27. Rowe S P, Macura K J, Mena E, et al. PSMA-based[¹⁸F]DCFPyL PET/CT is superior to conventional imaging for lesion detection in patients with metastatic prostate cancer. Mol Imaging Biol, 2016, 18(3): 411-419.
28. Chen Ying, Lisok A, Chatterjee S, et al. [¹⁸F]fluoroethyl triazole substituted PSMA inhibitor exhibiting rapid normal organ clearance. Bioconjug Chem, 2016, 27(7): 1655-1662.
29. Cardinale J, Schäfer M, Benešová M, et al. 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.
30. Giesel F L, Will L, Lawal I, et al. Intraindividual comparison of ¹⁸F-PSMA-1007 and ¹⁸F-DCFPyL PET/CT in the prospective evaluation of patients with newly diagnosed prostate carcinoma: a pilot study. J Nucl Med, 2018, 59(7): 1076-1080.
31. Giesel F L, Hadaschik B, Cardinale J, et al. 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.
32. Afshar-Oromieh A, Malcher A, Eder M, et al. PET imaging with a[⁶⁸Ga]gallium-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(4): 486-495.
33. Pfister D, Porres D, Heidenreich A, et al. Detection of recurrent prostate cancer lesions before salvage lymphadenectomy is more accurate with ⁶⁸Ga-PSMA-HBED-CC than with ¹⁸F-Fluoroethylcholine PET/CT. Eur J Nucl Med Mol Imaging, 2016, 43(8): 1410-1417.
34. Afshar-Oromieh A, Holland-Letz T, Giesel F L, et al. Diagnostic performance of ⁶⁸Ga-PSMA-11(HBED-CC) PET/CT in patients with recurrent prostate cancer: evaluation in 1007 patients. Eur J Nucl Med Mol Imaging, 2017, 44(8): 1258-1268.

Journal of Biomedical Engineering

Recent progress of positron radionuclide labeled small molecule inhibitors of prostate specific membrane antigen for PET/CT imaging of prostate cancer

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