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Current Medicinal Chemistry

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ISSN (Online): 1875-533X

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Review Article

Radiolabeled GRPR Antagonists for Imaging of Disseminated Prostate Cancer - Influence of Labeling Chemistry on Targeting Properties

Author(s): Bogdan Mitran, Vladimir Tolmachev * and Anna Orlova

Volume 27, Issue 41, 2020

Page: [7090 - 7111] Pages: 22

DOI: 10.2174/0929867327666200312114902

Price: $65

Abstract

Background: Radionuclide molecular imaging of Gastrin-Releasing Peptide Receptor (GRPR) expression promises unparalleled opportunities for visualizing subtle prostate tumors, which due to small size, adjacent benign tissue, or a challenging location would otherwise remain undetected by conventional imaging. Achieving high imaging contrast is essential for this purpose and the molecular design of any probe for molecular imaging of prostate cancer should be aimed at obtaining as high tumor-to-organ ratios as possible.

Objective: This short review summarizes the key imaging modalities currently used in prostate cancer, with a special focus on radionuclide molecular imaging. Emphasis is laid mainly on the issue of radiometals labeling chemistry and its influence on the targeting properties and biodistribution of radiolabeled GRPR antagonists for imaging of disseminated prostate cancer.

Methods: A comprehensive literature search of the PubMed/MEDLINE, and Scopus library databases was conducted to find relevant articles.

Results: The combination of radionuclide, chelator and required labeling chemistry was shown to have a significant influence on the stability, binding affinity and internalization rate, off-target interaction with normal tissues and blood proteins, interaction with enzymes, activity uptake and retention in excretory organs and activity uptake in tumors of radiolabeled bombesin antagonistic analogues.

Conclusion: Labeling chemistry has a very strong impact on the biodistribution profile of GRPRtargeting peptide based imaging probes and needs to be considered when designing a targeting probe for high contrast molecular imaging. Taking into account the complexity of in vivo interactions, it is not currently possible to accurately predict the optimal labeling approach. Therefore, a detailed in vivo characterization and optimization is essential for the rational design of imaging agents.

Keywords: Prostate cancer, molecular imaging, gastrin-releasing peptide receptor, GRPR antagonist, radiolabeling, radionuclide molecular imaging.

« Previous Next »
[1]
Kelloff, G.J.; Choyke, P.; Coffey, D.S. Prostate cancer imaging working group. Challenges in clinical prostate cancer: role of imaging. AJR Am. J. Roentgenol., 2009, 192(6), 1455-1470.
[http://dx.doi.org/10.2214/AJR.09.2579] [PMID: 19457806]
[2]
Sarkar, S.; Das, S. A review of imaging methods for prostate cancer detection. Biomed. Eng. Comput. Biol., 2016, 7(Suppl. 1), 1-15.
[http://dx.doi.org/10.4137/BECB.S34255] [PMID: 26966397]
[3]
Turkbey, B.; Pinto, P.A.; Choyke, P.L. Imaging techniques for prostate cancer: implications for focal therapy. Nat. Rev. Urol., 2009, 6(4), 191-203.
[http://dx.doi.org/10.1038/nrurol.2009.27] [PMID: 19352394]
[4]
Hricak, H.; Choyke, P.L.; Eberhardt, S.C.; Leibel, S.A.; Scardino, P.T. Imaging prostate cancer: a multidisciplinary perspective. Radiology, 2007, 243(1), 28-53.
[http://dx.doi.org/10.1148/radiol.2431030580] [PMID: 17392247]
[5]
Woo, S.; Suh, C.H.; Kim, S.Y.; Cho, J.Y.; Kim, S.H. Shear-wave elastography for detection of prostate cancer: a systematic review and diagnostic meta-analysis. AJR Am. J. Roentgenol., 2017, 209(4), 806-814.
[http://dx.doi.org/10.2214/AJR.17.18056] [PMID: 28796546]
[6]
Nelson, E.D.; Slotoroff, C.B.; Gomella, L.G.; Halpern, E.J. Targeted biopsy of the prostate: the impact of color Doppler imaging and elastography on prostate cancer detection and Gleason score. Urology, 2007, 70(6), 1136-1140.
[http://dx.doi.org/10.1016/j.urology.2007.07.067] [PMID: 18158034]
[7]
Seitz, M.; Gratzke, C.; Schlenker, B.; Buchner, A.; Karl, A.; Roosen, A.; Singer, B.B.; Bastian, P.J.; Ergün, S.; Stief, C.G.; Reich, O.; Tilki, D. Contrast-enhanced transrectal ultrasound (CE-TRUS) with cadence-contrast pulse sequence (CPS) technology for the identi-fication of prostate cancer. Urol. Oncol., 2011, 29(3), 295-301.
[http://dx.doi.org/10.1016/j.urolonc.2009.03.032] [PMID: 19523857]
[8]
Smith, C.P.; Laucis, A.; Harmon, S.; Mena, E.; Lindenberg, L.; Choyke, P.L.; Turkbey, B. Novel imaging in detection of metastatic prostate cancer. Curr. Oncol. Rep., 2019, 21(4), 31.
[http://dx.doi.org/10.1007/s11912-019-0780-8] [PMID: 30834999]
[9]
Ahmed, H.U.; El-Shater Bosaily, A.; Brown, L.C.; Gabe, R.; Kaplan, R.; Parmar, M.K.; Collaco-Moraes, Y.; Ward, K.; Hindley, R.G.; Freeman, A.; Kirkham, A.P.; Oldroyd, R.; Parker, C.; Emberton, M. PROMIS study group. Diagnostic accuracy of multi-parametric MRI and TRUS biopsy in prostate cancer (PROMIS): a paired validating confirmatory study. Lancet, 2017, 389(10071), 815-822.
[http://dx.doi.org/10.1016/S0140-6736(16)32401-1] [PMID: 28110982]
[10]
Hövels, A.M.; Heesakkers, R.A.; Adang, E.M.; Jager, G.J.; Strum, S.; Hoogeveen, Y.L.; Severens, J.L.; Barentsz, J.O. The diagnostic accuracy of CT and MRI in the staging of pelvic lymph nodes in patients with prostate cancer: a meta-analysis. Clin. Radiol., 2008, 63(4), 387-395.
[http://dx.doi.org/10.1016/j.crad.2007.05.022] [PMID: 18325358]
[11]
Schwarzenboeck, S.M.; Rauscher, I.; Bluemel, C.; Fendler, W.P.; Rowe, S.P.; Pomper, M.G.; Afshar-Oromieh, A.; Herrmann, K.; Eiber, M. PSMA ligands for PET imaging of prostate cancer. J. Nucl. Med., 2017, 58(10), 1545-1552.
[http://dx.doi.org/10.2967/jnumed.117.191031] [PMID: 28687599]
[12]
Bubendorf, L.; Schöpfer, A.; Wagner, U.; Sauter, G.; Moch, H.; Willi, N.; Gasser, T.C.; Mihatsch, M.J. Metastatic patterns of prostate cancer: an autopsy study of 1,589 patients. Hum. Pathol., 2000, 31(5), 578-583.
[http://dx.doi.org/10.1053/hp.2000.6698] [PMID: 10836297]
[13]
Messiou, C.; Cook, G.; deSouza, N.M. Imaging metastatic bone disease from carcinoma of the prostate. Br. J. Cancer, 2009, 101(8), 1225-1232.
[http://dx.doi.org/10.1038/sj.bjc.6605334] [PMID: 19789531]
[14]
Kulshrestha, R.K.; Vinjamuri, S.; England, A.; Nightingale, J.; Hogg, P. The role of 18F-sodium fluoride PET/CT bone scans in the diagnosis of metastatic bone disease from breast and prostate cancer. J. Nucl. Med. Technol., 2016, 44(4), 217-222.
[http://dx.doi.org/10.2967/jnmt.116.176859] [PMID: 27634981]
[15]
Bastawrous, S.; Bhargava, P.; Behnia, F.; Djang, D.S.; Haseley, D.R. Newer PET application with an old tracer: role of 18F-NaF skel-etal PET/CT in oncologic practice. Radiographics, 2014, 34(5), 1295-1316.
[http://dx.doi.org/10.1148/rg.345130061] [PMID: 25208282]
[16]
Jadvar, H. Is there use for FDG-PET in prostate cancer? Semin. Nucl. Med., 2016, 46(6), 502-506.
[http://dx.doi.org/10.1053/j.semnuclmed.2016.07.004] [PMID: 27825430]
[17]
Ramírez de Molina, A.; Gutiérrez, R.; Ramos, M.A.; Silva, J.M.; Silva, J.; Bonilla, F.; Sánchez, J.J.; Lacal, J.C. Increased choline kinase activity in human breast carcinomas: clinical evidence for a potential novel antitumor strategy. Oncogene, 2002, 21(27), 4317-4322.
[http://dx.doi.org/10.1038/sj.onc.1205556] [PMID: 12082619]
[18]
Sathianathen, N.J.; Butaney, M.; Konety, B.R. The utility of PET-based imaging for prostate cancer biochemical recurrence: a systematic review and meta-analysis. World J. Urol., 2019, 37(7), 1239-1249.
[http://dx.doi.org/10.1007/s00345-018-2403-7] [PMID: 30003375]
[19]
Beheshti, M.; Imamovic, L.; Broinger, G.; Vali, R.; Waldenberger, P.; Stoiber, F.; Nader, M.; Gruy, B.; Janetschek, G.; Langsteger, W. 18F choline PET/CT in the preoperative staging of prostate cancer in patients with intermediate or high risk of extracapsular disease: a prospective study of 130 patients. Radiology, 2010, 254(3), 925-933.
[http://dx.doi.org/10.1148/radiol.09090413] [PMID: 20177103]
[20]
Sandblom, G.; Sörensen, J.; Lundin, N.; Häggman, M.; Malmström, P.U. Positron emission tomography with C11-acetate for tumor detection and localization in patients with prostate-specific antigen relapse after radical prostatectomy. Urology, 2006, 67(5), 996-1000.
[http://dx.doi.org/10.1016/j.urology.2005.11.044] [PMID: 16698359]
[21]
Oyama, N.; Akino, H.; Kanamaru, H.; Suzuki, Y.; Muramoto, S.; Yonekura, Y.; Sadato, N.; Yamamoto, K.; Okada, K. 11C-acetate PET imaging of prostate cancer. J. Nucl. Med., 2002, 43(2), 181-186.
[PMID: 11850482]
[22]
Kato, T.; Tsukamoto, E.; Kuge, Y.; Takei, T.; Shiga, T.; Shinohara, N.; Katoh, C.; Nakada, K.; Tamaki, N. Accumulation of [11C]acetate in normal prostate and benign prostatic hyperplasia: comparison with prostate cancer. Eur. J. Nucl. Med. Mol. Imaging, 2002, 29(11), 1492-1495.
[http://dx.doi.org/10.1007/s00259-002-0885-3] [PMID: 12397469]
[23]
Ross, J.S.; Sheehan, C.E.; Fisher, H.A.; Kaufman, R.P. Jr.; Kaur, P.; Gray, K.; Webb, I.; Gray, G.S.; Mosher, R.; Kallakury, B.V. Cor-relation of primary tumor prostate-specific membrane antigen expression with disease recurrence in prostate cancer. Clin. Cancer Res., 2003, 9(17), 6357-6362.
[PMID: 14695135]
[24]
Troyer, J.K.; Beckett, M.L.; Wright, G.L. Jr. Location of prostate-specific membrane antigen in the LNCaP prostate carcinoma cell line. Prostate, 1997, 30(4), 232-242.
[http://dx.doi.org/10.1002/(SICI)1097-0045(19970301)30:4<232:AID-PROS2>3.0.CO;2-N] [PMID: 9111600]
[25]
Osborne, J.R.; Green, D.A.; Spratt, D.E.; Lyashchenko, S.; Fareedy, S.B.; Robinson, B.D.; Beattie, B.J.; Jain, M.; Lewis, J.S.; Christos, P.; Larson, S.M.; Bander, N.H.; Scherr, D.S. A prospective pilot study of (89)Zr-J591/prostate specific membrane antigen positron emission tomography in men with localized prostate cancer undergoing radical prostatectomy. J. Urol., 2014, 191(5), 1439-1445.
[http://dx.doi.org/10.1016/j.juro.2013.10.041] [PMID: 24135437]
[26]
Afshar-Oromieh, A.; Haberkorn, U.; Eder, M.; Eisenhut, M.; Zechmann, C.M. [68Ga]Gallium-labelled PSMA ligand as superior PET tracer for the diagnosis of prostate cancer: comparison with 18F-FECH. Eur. J. Nucl. Med. Mol. Imaging, 2012, 39(6), 1085-1086.
[http://dx.doi.org/10.1007/s00259-012-2069-0] [PMID: 22310854]
[27]
Afshar-Oromieh, A.; Hetzheim, H.; Kratochwil, C.; Benesova, M.; Eder, M.; Neels, O.C.; Eisenhut, M.; Kübler, W.; Holland-Letz, T.; Giesel, F.L.; Mier, W.; Kopka, K.; Haberkorn, U. 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(11), 1697-1705.
[http://dx.doi.org/10.2967/jnumed.115.161299] [PMID: 26294298]
[28]
Szabo, Z.; Mena, E.; Rowe, S.P.; Plyku, D.; Nidal, R.; Eisenberger, M.A.; Antonarakis, E.S.; Fan, H.; Dannals, R.F.; Chen, Y.; Mease, R.C.; Vranesic, M.; Bhatnagar, A.; Sgouros, G.; Cho, S.Y.; Pomper, M.G. Initial evaluation of [(18)F]DCFPyL for prostate-specific membrane antigen (PSMA)-targeted pet imaging of prostate cancer. Mol. Imaging Biol., 2015, 17(4), 565-574.
[http://dx.doi.org/10.1007/s11307-015-0850-8] [PMID: 25896814]
[29]
Zechmann, C.M.; Afshar-Oromieh, A.; Armor, T.; Stubbs, J.B.; Mier, W.; Hadaschik, B.; Joyal, J.; Kopka, K.; Debus, J.; Babich, J.W.; Haberkorn, U. Radiation dosimetry and first therapy results with a (124)I/(131)I-labeled small molecule (MIP-1095) targeting PSMA for prostate cancer therapy. Eur. J. Nucl. Med. Mol. Imaging, 2014, 41(7), 1280-1292.
[http://dx.doi.org/10.1007/s00259-014-2713-y] [PMID: 24577951]
[30]
Giesel, F.L.; Cardinale, J.; Schäfer, M.; Neels, O.; Benešová, M.; Mier, W.; Haberkorn, U.; Kopka, K.; Kratochwil, C. (18)F-Labelled PSMA-1007 shows similarity in structure, biodistribution and tumour uptake to the theragnostic compound PSMA-617. Eur. J. Nucl. Med. Mol. Imaging, 2016, 43(10), 1929-1930.
[http://dx.doi.org/10.1007/s00259-016-3447-9] [PMID: 27342416]
[31]
Krohn, T.; Verburg, F.A.; Pufe, T.; Neuhuber, W.; Vogg, A.; Heinzel, A.; Mottaghy, F.M.; Behrendt, F.F. [68Ga]PSMA-HBED uptake mimicking lymph node metastasis in coeliac ganglia: an important pitfall in clinical practice. Eur. J. Nucl. Med. Mol. Imaging, 2015, 42(2), 210-214.
[http://dx.doi.org/10.1007/s00259-014-2915-3] [PMID: 25248644]
[32]
Thang, S.P.; Violet, J.; Sandhu, S.; Iravani, A.; Akhurst, T.; Kong, G.; Ravi Kumar, A.; Murphy, D.G.; Williams, S.G.; Hicks, R.J.; Hofman, M.S. Poor outcomes for patients with metastatic castration-resistant prostate cancer with low prostate-specific membrane antigen (PSMA) expression deemed ineligible for 177Lu-labelled PSMA radioligand therapy. Eur. Urol. Oncol., 2018.
[http://dx.doi.org/10.1016/j.euo.2018.11.007]
[33]
Ramos-Álvarez, I.; Moreno, P.; Mantey, S.A.; Nakamura, T.; Nuche-Berenguer, B.; Moody, T.W.; Coy, D.H.; Jensen, R.T. Insights into bombesin receptors and ligands: Highlighting recent advances. Peptides, 2015, 72, 128-144.
[http://dx.doi.org/10.1016/j.peptides.2015.04.026] [PMID: 25976083]
[34]
Moreno, P.; Ramos-Álvarez, I.; Moody, T.W.; Jensen, R.T. Bombesin related peptides/receptors and their promising therapeutic roles in cancer imaging, targeting and treatment. Expert Opin. Ther. Targets, 2016, 20(9), 1055-1073.
[http://dx.doi.org/10.1517/14728222.2016.1164694] [PMID: 26981612]
[35]
Gugger, M.; Reubi, J.C. Gastrin-releasing peptide receptors in non-neoplastic and neoplastic human breast. Am. J. Pathol., 1999, 155(6), 2067-2076.
[http://dx.doi.org/10.1016/S0002-9440(10)65525-3] [PMID: 10595936]
[36]
Markwalder, R.; Reubi, J.C. Gastrin-releasing peptide receptors in the human prostate: relation to neoplastic transformation. Cancer Res., 1999, 59(5), 1152-1159.
[PMID: 10070977]
[37]
Ananias, H.J.; van den Heuvel, M.C.; Helfrich, W.; de Jong, I.J. Expression of the gastrin-releasing peptide receptor, the prostate stem cell antigen and the prostate-specific membrane antigen in lymph node and bone metastases of prostate cancer. Prostate, 2009, 69(10), 1101-1108.
[http://dx.doi.org/10.1002/pros.20957] [PMID: 19343734]
[38]
Körner, M.; Waser, B.; Rehmann, R.; Reubi, J.C. Early over-expression of GRP receptors in prostatic carcinogenesis. Prostate, 2014, 74(2), 217-224.
[http://dx.doi.org/10.1002/pros.22743] [PMID: 24150752]
[39]
Beer, M.; Montani, M.; Gerhardt, J.; Wild, P.J.; Hany, T.F.; Hermanns, T.; Müntener, M.; Kristiansen, G. Profiling gastrin-releasing peptide receptor in prostate tissues: clinical implications and molecular correlates. Prostate, 2012, 72(3), 318-325.
[http://dx.doi.org/10.1002/pros.21434] [PMID: 21739464]
[40]
Schollhammer, R.; De Clermont Gallerande, H.; Yacoub, M.; Quintyn Ranty, M.L.; Barthe, N.; Vimont, D.; Hindié, E.; Fernandez, P.; Morgat, C. Comparison of the radiolabeled PSMA-inhibitor 111In-PSMA-617 and the radiolabeled GRP-R antagonist 111In-RM2 in primary prostate cancer samples. EJNMMI Res., 2019, 9(1), 52.
[http://dx.doi.org/10.1186/s13550-019-0517-6] [PMID: 31161459]
[41]
Schroeder, R.P.; de Visser, M.; van Weerden, W.M.; de Ridder, C.M.; Reneman, S.; Melis, M.; Breeman, W.A.; Krenning, E.P.; de Jong, M. Androgen-regulated gastrin-releasing peptide receptor expression in androgen-dependent human prostate tumor xenografts. Int. J. Cancer, 2010, 126(12), 2826-2834.
[http://dx.doi.org/10.1002/ijc.25000] [PMID: 19876914]
[42]
Minamimoto, R.; Sonni, I.; Hancock, S.; Vasanawala, S.; Loening, A.; Gambhir, S.S.; Iagaru, A. prospective evaluation of 68ga-rm2 pet/mri in patients with biochemical recurrence of prostate cancer and negative findings on conventional imaging. J. Nucl. Med., 2018, 59(5), 803-808.
[http://dx.doi.org/10.2967/jnumed.117.197624] [PMID: 29084827]
[43]
Spindel, E.R. Bombesin peptides in: Handbook of Biologically Active Peptides, 2nd ed; Kastin, A., Ed.; Academic Press, 2013, pp. 326-330.
[http://dx.doi.org/10.1016/B978-0-12-385095-9.00046-4]
[44]
Nagalla, S.R.; Barry, B.J.; Falick, A.M.; Gibson, B.W.; Taylor, J.E.; Dong, J.Z.; Spindel, E.R. There are three distinct forms of bombesin. Identification of [Leu13]bombesin, [Phe13]bombesin, and Ser3,Arg10,Phe13]bombesin in the frog Bombina orientalis. J. Biol. Chem., 1996, 271(13), 7731-7737.
[http://dx.doi.org/10.1074/jbc.271.13.7731] [PMID: 8631814]
[45]
Schottelius, M.; Wester, H.J. Molecular imaging targeting peptide receptors. Methods, 2009, 48(2), 161-177.
[http://dx.doi.org/10.1016/j.ymeth.2009.03.012] [PMID: 19324088]
[46]
Rodriguez, M.; Dubreuil, P.; Bali, J.P.; Martinez, J.; Martinez, J. Synthesis and biological activity of partially modified retro-inverso pseudopeptide derivatives of the C-terminal tetrapeptide of gastrin. J. Med. Chem., 1987, 30(5), 758-763.
[http://dx.doi.org/10.1021/jm00388a002] [PMID: 3572963]
[47]
Coy, D.H.; Heinz-Erian, P.; Jiang, N.Y.; Sasaki, Y.; Taylor, J.; Moreau, J.P.; Wolfrey, W.T.; Gardner, J.D.; Jensen, R.T. Probing pep-tide backbone function in bombesin. A reduced peptide bond analogue with potent and specific receptor antagonist activity. J. Biol. Chem., 1988, 263(11), 5056-5060.
[PMID: 2451661]
[48]
Martinez, J.; Bali, J.P.; Rodriguez, M.; Castro, B.; Magous, R.; Laur, J.; Lignon, M.F. Synthesis and biological activities of some pseudo-peptide analogues of tetragastrin: the importance of the peptide backbone. J. Med. Chem., 1985, 28(12), 1874-1879.
[http://dx.doi.org/10.1021/jm00150a020] [PMID: 2999406]
[49]
Laur, J.; Rodriguez, M.; Aumelas, A.; Bali, J.P.; Martinez, J. Synthesis of analogues of the Des-Phe-NH2 C-terminal hexapeptide of cholecystokinin showing gastrin antagonist activity. Int. J. Pept. Protein Res., 1986, 27(4), 386-393.
[http://dx.doi.org/10.1111/j.1399-3011.1986.tb01032.x] [PMID: 3710694]
[50]
Reubi, J.C. Peptide receptors as molecular targets for cancer diagnosis and therapy. Endocr. Rev., 2003, 24(4), 389-427.
[http://dx.doi.org/10.1210/er.2002-0007] [PMID: 12920149]
[51]
Van de Wiele, C.; Dumont, F.; van Belle, S.; Slegers, G.; Peers, S.H.; Dierckx, R.A. Is there a role for agonist gastrin-releasing peptide receptor radioligands in tumour imaging? Nucl. Med. Commun., 2001, 22(1), 5-15.
[http://dx.doi.org/10.1097/00006231-200101000-00002] [PMID: 11233552]
[52]
Smith, C.J.; Volkert, W.A.; Hoffman, T.J. Radiolabeled peptide conjugates for targeting of the bombesin receptor superfamily subtypes. Nucl. Med. Biol., 2005, 32(7), 733-740.
[http://dx.doi.org/10.1016/j.nucmedbio.2005.05.005] [PMID: 16243649]
[53]
Maina, T.; Nock, B.; Mather, S. Targeting prostate cancer with radiolabelled bombesins. Cancer Imaging, 2006, 6, 153-157.
[http://dx.doi.org/10.1102/1470-7330.2006.0025] [PMID: 17098646]
[54]
Panigone, S.; Nunn, A.D. Lutetium-177-labeled gastrin releasing peptide receptor binding analogs: a novel approach to radionuclide therapy. Q. J. Nucl. Med. Mol. Imaging, 2006, 50(4), 310-321.
[PMID: 17043628]
[55]
Ginj, M.; Zhang, H.; Waser, B.; Cescato, R.; Wild, D.; Wang, X.; Erchegyi, J.; Rivier, J.; Mäcke, H.R.; Reubi, J.C. Radiolabeled so-matostatin receptor antagonists are preferable to agonists for in vivo peptide receptor targeting of tumors. Proc. Natl. Acad. Sci. USA, 2006, 103(44), 16436-16441.
[http://dx.doi.org/10.1073/pnas.0607761103] [PMID: 17056720]
[56]
Cescato, R.; Maina, T.; Nock, B.; Nikolopoulou, A.; Charalambidis, D.; Piccand, V.; Reubi, J.C. Bombesin receptor antagonists may be preferable to agonists for tumor targeting. J. Nucl. Med., 2008, 49(2), 318-326.
[http://dx.doi.org/10.2967/jnumed.107.045054] [PMID: 18199616]
[57]
Nock, B.; Nikolopoulou, A.; Chiotellis, E.; Loudos, G.; Maintas, D.; Reubi, J.C.; Maina, T. [99mTc]Demobesin 1, a novel potent bombesin analogue for GRP receptor-targeted tumour imaging. Eur. J. Nucl. Med. Mol. Imaging, 2003, 30(2), 247-258.
[http://dx.doi.org/10.1007/s00259-002-1040-x] [PMID: 12552343]
[58]
Nock, B.A.; Nikolopoulou, A.; Galanis, A.; Cordopatis, P.; Waser, B.; Reubi, J.C.; Maina, T. Potent bombesin-like peptides for GRP-receptor targeting of tumors with 99mTc: a preclinical study. J. Med. Chem., 2005, 48(1), 100-110.
[http://dx.doi.org/10.1021/jm049437y] [PMID: 15634004]
[59]
Mansi, R.; Wang, X.; Forrer, F.; Kneifel, S.; Tamma, M.L.; Waser, B.; Cescato, R.; Reubi, J.C.; Maecke, H.R. Evaluation of a 1,4,7,10-tetraazacyclododecane-1,4,7,10-tetraacetic acid-conjugated bombesin-based radioantagonist for the labeling with single-photon emission computed tomography, positron emission tomography, and therapeutic radionuclides. Clin. Cancer Res., 2009, 15(16), 5240-5249.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-3145] [PMID: 19671861]
[60]
Llinares, M.; Devin, C.; Chaloin, O.; Azay, J.; Noel-Artis, A.M.; Bernad, N.; Fehrentz, J.A.; Martinez, J. Syntheses and biological activities of potent bombesin receptor antagonists. J. Pept. Res., 1999, 53(3), 275-283.
[http://dx.doi.org/10.1034/j.1399-3011.1999.00028.x] [PMID: 10231715]
[61]
Kurth, J.; Krause, B.J.; Schwarzenböck, S.M.; Bergner, C.; Hakenberg, O.W.; Heuschkel, M. First-in-human dosimetry of gastrin-releasing peptide receptor antagonist [177Lu]Lu-RM2: a radiopharmaceutical for the treatment of metastatic castration-resistant prostate cancer. Eur. J. Nucl. Med. Mol. Imaging, 2020, 47(1), 123-135.
[http://dx.doi.org/10.1007/s00259-019-04504-3] [PMID: 31482426]
[62]
Kenakin, T. New concepts in drug discovery: collateral efficacy and permissive antagonism. Nat. Rev. Drug Discov., 2005, 4(11), 919-927.
[http://dx.doi.org/10.1038/nrd1875] [PMID: 16264435]
[63]
Millar, J.B.; Rozengurt, E. Chronic desensitization to bombesin by progressive down-regulation of bombesin receptors in Swiss 3T3 cells. Distinction from acute desensitization. J. Biol. Chem., 1990, 265(20), 12052-12058.
[PMID: 2164025]
[64]
Zhang, J.; Niu, G.; Fan, X.; Lang, L.; Hou, G.; Chen, L.; Wu, H.; Zhu, Z.; Li, F.; Chen, X. PET using a GRPR antagonist 68Ga-RM26 in healthy volunteers and prostate cancer patients. J. Nucl. Med., 2018, 59(6), 922-928.
[http://dx.doi.org/10.2967/jnumed.117.198929] [PMID: 29123014]
[65]
Bodei, L.; Ferrari, M.; Nunn, A.; Llull, J.; Cremonesi, M.; Martano, L.; Laurora, G.; Scardino, E.; Tiberini, S.; Bufi, G.; Eato de Cobelli, O.; Paganelli, G. 177Lu-AMBA bombesin analogue in hormone refractory prostate cancer patients: a phase I escalation study with single-cycle administrations. Eur. J. Nucl. Med. Mol. Imaging, 2007, 34(Suppl. 2), S221.
[66]
Bertaccini, G.; Impicciatore, M. Action of bombesin on the motility of the stomach. Naunyn Schmiedebergs Arch. Pharmacol., 1975, 289(2), 149-156.
[http://dx.doi.org/10.1007/BF00501302] [PMID: 1165792]
[67]
Maina, T.; Bergsma, H.; Kulkarni, H.R.; Mueller, D.; Charalambidis, D.; Krenning, E.P.; Nock, B.A.; de Jong, M.; Baum, R.P. Pre-clinical and first clinical experience with the gastrin-releasing peptide receptor-antagonist [68Ga]SB3 and PET/CT. Eur. J. Nucl. Med. Mol. Imaging, 2016, 43(5), 964-973.
[http://dx.doi.org/10.1007/s00259-015-3232-1] [PMID: 26631238]
[68]
Zang, J.; Mao, F.; Wang, H.; Zhang, J.; Liu, Q.; Peng, L.; Li, F.; Lang, L.; Chen, X.; Zhu, Z. 68Ga-NOTA-RM26 PET/CT in the eval-uation of breast cancer: a pilot prospective study. Clin. Nucl. Med., 2018, 43(9), 663-669.
[http://dx.doi.org/10.1097/RLU.0000000000002209] [PMID: 30036253]
[69]
Casanueva, F.F.; Perez, F.R.; Casabiell, X.; Camiña, J.P.; Cai, R.Z.; Schally, A.V. Correlation between the effects of bombesin antag-onists on cell proliferation and intracellular calcium concentration in Swiss 3T3 and HT-29 cell lines. Proc. Natl. Acad. Sci. USA, 1996, 93(4), 1406-1411.
[http://dx.doi.org/10.1073/pnas.93.4.1406] [PMID: 8643644]
[70]
Raylman, R.R.; Kison, P.V.; Wahl, R.L. Capabilities of two- and three-dimensional FDG-PET for detecting small lesions and lymph nodes in the upper torso: a dynamic phantom study. Eur. J. Nucl. Med., 1999, 26(1), 39-45.
[http://dx.doi.org/10.1007/s002590050357] [PMID: 9933660]
[71]
Tolmachev, V.; Orlova, A. Influence of labelling methods on biodistribution and imaging properties of radiolabelled peptides for visu-alisation of molecular therapeutic targets. Curr. Med. Chem., 2010, 17(24), 2636-2655.
[http://dx.doi.org/10.2174/092986710791859397] [PMID: 20491631]
[72]
Maina, T.; Kaloudi, A.; Valverde, I.E.; Mindt, T.L.; Nock, B.A. Amide-to-triazole switch vs. in vivo NEP-inhibition approaches to promote radiopeptide targeting of GRPR-positive tumors. Nucl. Med. Biol., 2017, 52, 57-62.
[http://dx.doi.org/10.1016/j.nucmedbio.2017.06.001] [PMID: 28636973]
[73]
Lymperis, E.; Kaloudi, A.; Kanellopoulos, P.; de Jong, M.; Krenning, E.P.; Nock, B.A.; Maina, T. Comparing Gly11/dAla11-Replacement vs. the in-situ neprilysin-inhibition approach on the tumor-targeting efficacy of the 111In-SB3/111In-SB4 radiotracer pair. Molecules, 2019, 24(6)E1015
[http://dx.doi.org/10.3390/molecules24061015] [PMID: 30871262]
[74]
Lymperis, E.; Kaloudi, A.; Kanellopoulos, P.; Krenning, E.P.; de Jong, M.; Maina, T.; Nock, B.A. Comparative evaluation of the new GRPR-antagonist 111 In-SB9 and 111 In-AMBA in prostate cancer models: implications of in vivo stability. J. Labelled Comp. Radiopharm., 2019, 62(10), 646-655.
[http://dx.doi.org/10.1002/jlcr.3733] [PMID: 30963606]
[75]
Marsouvanidis, P.J.; Melis, M.; de Blois, E.; Breeman, W.A.; Krenning, E.P.; Maina, T.; Nock, B.A.; de Jong, M. In vivo enzyme inhibition improves the targeting of [177Lu]DOTA-GRP(13-27) in GRPR-positive tumors in mice. Cancer Biother. Radiopharm., 2014, 29(9), 359-367.
[http://dx.doi.org/10.1089/cbr.2014.1706] [PMID: 25286347]
[76]
Abiraj, K.; Mansi, R.; Tamma, M.L.; Fani, M.; Forrer, F.; Nicolas, G.; Cescato, R.; Reubi, J.C.; Maecke, H.R. Bombesin antagonist-based radioligands for translational nuclear imaging of gastrin-releasing peptide receptor-positive tumors. J. Nucl. Med., 2011, 52(12), 1970-1978.
[http://dx.doi.org/10.2967/jnumed.111.094375] [PMID: 22080443]
[77]
Zhang, H. Design, synthesis, and preclinical evaluation of radiolabelled bombesin analogues for the diagnosis and targeted radiotherapy of bombesinreceptor expressing tumors.. PhD thesis Faculty of Science, University of Basel: Basel, 2007.
[http://dx.doi.org/10.5451/unibas-004208085]
[78]
Mansi, R.; Wang, X.; Forrer, F.; Waser, B.; Cescato, R.; Graham, K.; Borkowski, S.; Reubi, J.C.; Maecke, H.R. Development of a potent DOTA-conjugated bombesin antagonist for targeting GRPr-positive tumours. Eur. J. Nucl. Med. Mol. Imaging, 2011, 38(1), 97-107.
[http://dx.doi.org/10.1007/s00259-010-1596-9] [PMID: 20717822]
[79]
Varasteh, Z.; Velikyan, I.; Lindeberg, G.; Sörensen, J.; Larhed, M.; Sandström, M.; Selvaraju, R.K.; Malmberg, J.; Tolmachev, V.; Orlova, A. Synthesis and characterization of a high-affinity NOTA-conjugated bombesin antagonist for GRPR-targeted tumor imaging. Bioconjug. Chem., 2013, 24(7), 1144-1153.
[http://dx.doi.org/10.1021/bc300659k] [PMID: 23763444]
[80]
McBride, W.J.; Sharkey, R.M.; Karacay, H.; D’Souza, C.A.; Rossi, E.A.; Laverman, P.; Chang, C.H.; Boerman, O.C.; Goldenberg, D.M. A novel method of 18F radiolabeling for PET. J. Nucl. Med., 2009, 50(6), 991-998.
[http://dx.doi.org/10.2967/jnumed.108.060418] [PMID: 19443594]
[81]
Varasteh, Z.; Aberg, O.; Velikyan, I.; Lindeberg, G.; Sörensen, J.; Larhed, M.; Antoni, G.; Sandström, M.; Tolmachev, V.; Orlova, A. In vitro and in vivo evaluation of a (18)F-labeled high affinity NOTA conjugated bombesin antagonist as a PET ligand for GRPR-targeted tumor imaging. PLoS One, 2013, 8(12)e81932
[http://dx.doi.org/10.1371/journal.pone.0081932] [PMID: 24312607]
[82]
Liu, Y.; Hu, X.; Liu, H.; Bu, L.; Ma, X.; Cheng, K.; Li, J.; Tian, M.; Zhang, H.; Cheng, Z. A comparative study of radiolabeled bombesin analogs for the PET imaging of prostate cancer. J. Nucl. Med., 2013, 54(12), 2132-2138.
[http://dx.doi.org/10.2967/jnumed.113.121533] [PMID: 24198391]
[83]
Fersing, C.; Bouhlel, A.; Cantelli, C.; Garrigue, P.; Lisowski, V.; Guillet, B. A Comprehensive review of non-covalent radiofluorination approaches using aluminum [18F]fluoride: will [18F]AlF replace 68Ga for metal chelate labeling? Molecules, 2019, 24(16)E2866
[http://dx.doi.org/10.3390/molecules24162866] [PMID: 31394799]
[84]
Lymperis, E.; Kaloudi, A.; Sallegger, W.; Bakker, I.L.; Krenning, E.P.; de Jong, M.; Maina, T.; Nock, B.A. Radiometal-dependent biological profile of the radiolabeled gastrin-releasing peptide receptor antagonist SB3 in cancer theranostics: metabolic and biodistri-bution patterns defined by neprilysin. Bioconjug. Chem., 2018, 29(5), 1774-1784.
[http://dx.doi.org/10.1021/acs.bioconjchem.8b00225] [PMID: 29664606]
[85]
Nock, B.A.; Kaloudi, A.; Lymperis, E.; Giarika, A.; Kulkarni, H.R.; Klette, I.; Singh, A.; Krenning, E.P.; de Jong, M.; Maina, T.; Baum, R.P. Theranostic perspectives in prostate cancer with the gastrin-releasing peptide receptor antagonist NeoBOMB1: preclinical and first clinical results. J. Nucl. Med., 2017, 58(1), 75-80.
[http://dx.doi.org/10.2967/jnumed.116.178889] [PMID: 27493272]
[86]
Breeman, W.A.; Hofland, L.J.; de Jong, M.; Bernard, B.F.; Srinivasan, A.; Kwekkeboom, D.J.; Visser, T.J.; Krenning, E.P. Evaluation of radiolabelled bombesin analogues for receptor-targeted scintigraphy and radiotherapy. Int. J. Cancer, 1999, 81(4), 658-665.
[http://dx.doi.org/10.1002/(SICI)1097-0215(19990517)81:4<658:AID-IJC24>3.0.CO;2-P] [PMID: 10225459]
[87]
Hoffman, T.J.; Gali, H.; Smith, C.J.; Sieckman, G.L.; Hayes, D.L.; Owen, N.K.; Volkert, W.A. Novel series of 111In-labeled bombesin analogs as potential radiopharmaceuticals for specific targeting of gastrin-releasing peptide receptors expressed on human prostate cancer cells. J. Nucl. Med., 2003, 44(5), 823-831.
[PMID: 12732685]
[88]
García Garayoa, E.; Schweinsberg, C.; Maes, V.; Brans, L.; Bläuenstein, P.; Tourwe, D.A.; Schibli, R.; Schubiger, P.A. Influence of the molecular charge on the biodistribution of bombesin analogues labeled with the [99mTc(CO)3]-core. Bioconjug. Chem., 2008, 19(12), 2409-2416.
[http://dx.doi.org/10.1021/bc800262m] [PMID: 18998719]
[89]
Schweinsberg, C. Maes. V.; Brans, L.; Bläuenstein, P.; Tourwé, D.A.; Schubiger, P.A.; Schibli, R.; García Garayoa, E. Novel glycated [99mTc(CO)3]-labelled bombesin analogues for improved targeting of gastrin-releasing peptide receptor-positive tumors. Bioconjug. Chem., 2008, 19(12), 2432-2439.
[http://dx.doi.org/10.1021/bc800319g] [PMID: 19053304]
[90]
Varasteh, Z.; Rosenström, U.; Velikyan, I.; Mitran, B.; Altai, M.; Honarvar, H.; Rosestedt, M.; Lindeberg, G.; Sörensen, J.; Larhed, M.; Tolmachev, V.; Orlova, A. The effect of mini-PEG-based spacer length on binding and pharmacokinetic properties of a 68Ga-labeled NOTA-conjugated antagonistic analog of bombesin. Molecules, 2014, 19(7), 10455-10472.
[http://dx.doi.org/10.3390/molecules190710455] [PMID: 25036155]
[91]
Cheng, S.; Lang, L.; Wang, Z.; Jacobson, O.; Yung, B.; Zhu, G.; Gu, D.; Ma, Y.; Zhu, X.; Niu, G.; Chen, X. Positron emission tomog-raphy imaging of prostate cancer with Ga-68-labeled gastrin-releasing peptide receptor agonist BBN7-14 and antagonist RM26. Bioconjug. Chem., 2018, 29(2), 410-419.
[http://dx.doi.org/10.1021/acs.bioconjchem.7b00726] [PMID: 29254329]
[92]
Gourni, E.; Mansi, R.; Jamous, M.; Waser, B.; Smerling, C.; Burian, A.; Buchegger, F.; Reubi, J.C.; Maecke, H.R. N-terminal modifi-cations improve the receptor affinity and pharmacokinetics of radiolabeled peptidic gastrin-releasing peptide receptor antagonists: ex-amples of 68Ga- and 64Cu-labeled peptides for PET imaging. J. Nucl. Med., 2014, 55(10), 1719-1725.
[http://dx.doi.org/10.2967/jnumed.114.141242] [PMID: 25146125]
[93]
Chatalic, K.L.; Franssen, G.M.; van Weerden, W.M.; McBride, W.J.; Laverman, P.; de Blois, E.; Hajjaj, B.; Brunel, L.; Goldenberg, D.M.; Fehrentz, J.A.; Martinez, J.; Boerman, O.C.; de Jong, M. Preclinical comparison of Al18F- and 68Ga-labeled gastrin-releasing peptide receptor antagonists for PET imaging of prostate cancer. J. Nucl. Med., 2014, 55(12), 2050-2056.
[http://dx.doi.org/10.2967/jnumed.114.141143] [PMID: 25413139]
[94]
Varasteh, Z.; Mitran, B.; Rosenström, U.; Velikyan, I.; Rosestedt, M.; Lindeberg, G.; Sörensen, J.; Larhed, M.; Tolmachev, V.; Orlova, A. The effect of macrocyclic chelators on the targeting properties of the 68Ga-labeled gastrin releasing peptide receptor antagonist PEG2-RM26. Nucl. Med. Biol., 2015, 42(5), 446-454.
[http://dx.doi.org/10.1016/j.nucmedbio.2014.12.009] [PMID: 25684649]
[95]
Mitran, B.; Varasteh, Z.; Selvaraju, R.K.; Lindeberg, G.; Sörensen, J.; Larhed, M.; Tolmachev, V.; Rosenström, U.; Orlova, A. Selection of optimal chelator improves the contrast of GRPR imaging using bombesin analogue RM26. Int. J. Oncol., 2016, 48(5), 2124-2134.
[http://dx.doi.org/10.3892/ijo.2016.3429] [PMID: 26983776]
[96]
Mitran, B.; Thisgaard, H.; Rinne, S.; Dam, J.H.; Azami, F.; Tolmachev, V.; Orlova, A.; Rosenström, U. Selection of an optimal mac-rocyclic chelator improves the imaging of prostate cancer using cobalt-labeled GRPR antagonist RM26. Sci. Rep., 2019, 9(1), 17086.
[http://dx.doi.org/10.1038/s41598-019-52914-y] [PMID: 31745219]
[97]
Lindbo, S.; Garousi, J.; Mitran, B.; Altai, M.; Buijs, J.; Orlova, A.; Hober, S.; Tolmachev, V. Radionuclide tumor targeting using ADAPT scaffold proteins: aspects of label positioning and residualizing properties of the label. J. Nucl. Med., 2018, 59(1), 93-99.
[http://dx.doi.org/10.2967/jnumed.117.197202] [PMID: 28864631]
[98]
Deyev, S.; Vorobyeva, A.; Schulga, A.; Proshkina, G.; Güler, R.; Löfblom, J.; Mitran, B.; Garousi, J.; Altai, M.; Buijs, J.; Chernov, V.; Orlova, A.; Tolmachev, V. Comparative evaluation of two DARPin variants: effect of affinity, size and label on tumor targeting properties. Mol. Pharm., 2019, 16(3), 995-1008.
[http://dx.doi.org/10.1021/acs.molpharmaceut.8b00922] [PMID: 30608701]
[99]
Oroujeni, M.; Abouzayed, A.; Lundmark, F.; Mitran, B.; Orlova, A.; Tolmachev, V.; Rosenström, U. Evaluation of tumor-targeting properties of an antagonistic bombesin analogue RM26 conjugated with a non-residualizing radioiodine label comparison with a radi-ometal-labelled counterpart. Pharmaceutics, 2019, 11(8)E380
[http://dx.doi.org/10.3390/pharmaceutics11080380] [PMID: 31382362]
[100]
Reubi, J.C.; Erchegyi, J.; Cescato, R.; Waser, B.; Rivier, J.E. Switch from antagonist to agonist after addition of a DOTA chelator to a somatostatin analog. Eur. J. Nucl. Med. Mol. Imaging, 2010, 37(8), 1551-1558.
[http://dx.doi.org/10.1007/s00259-010-1445-x] [PMID: 20396884]
[101]
Stoykow, C.; Erbes, T.; Maecke, H.R.; Bulla, S.; Bartholomä, M.; Mayer, S.; Drendel, V.; Bronsert, P.; Werner, M.; Gitsch, G.; Weber, W.A.; Stickeler, E.; Meyer, P.T. Gastrin-releasing peptide receptor imaging in breast cancer using the receptor antagonist (68)Ga-RM2 And PET. Theranostics, 2016, 6(10), 1641-1650.
[http://dx.doi.org/10.7150/thno.14958] [PMID: 27446498]

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