Login Register Cart 0
Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe Translate in Chinese
Mini-Review Article

Cholecystokinin-2 Receptor Targeting with Radiolabeled Peptides: Current Status and Future Directions

Author(s): Maximilian Klingler, Anton Amadeus Hörmann and Elisabeth Von Guggenberg*

Volume 27, Issue 41, 2020

Page: [7112 - 7132] Pages: 21

DOI: 10.2174/0929867327666200625143035

Price: $65

Abstract

A wide variety of radiolabeled peptide analogs for specific targeting of cholecystokinin- 2 receptors (CCK2R) has been developed in the last decades. Peptide probes based on the natural ligands Minigastrin (MG) and Cholecystokinin (CCK) have a high potential for molecular imaging and targeted radiotherapy of different human tumors, such as Medullary Thyroid Carcinoma (MTC) and Small Cell Lung Cancer (SCLC). MG analogs with high persistent uptake in CCK2R expressing tumors have been preferably used for the development of radiolabeled peptide analogs. The clinical translation of CCK2R targeting has been prevented due to high kidney uptake or low metabolic stability of the different radiopeptides developed. Great efforts in radiopharmaceutical development have been undertaken to overcome these limitations. Various modifications in the linear peptide sequence of MG have been introduced mainly with the aim to reduce kidney retention. Furthermore, improved tumor uptake could be obtained by in situ stabilization of the radiopeptide against enzymatic degradation through coinjection of peptidase inhibitors. Recent developments focusing on the stabilization of the Cterminal receptor binding sequence (Trp-Met-Asp-Phe-NH2) have led to new radiolabeled MG analogs with highly improved tumor uptake and tumor-to-kidney ratio. In this review, all the different aspects in the radiopharmaceutical development of CCK2R targeting peptide probes are covered, giving also an overview on the clinical investigations performed so far. The recent development of radiolabeled MG analogs, which are highly stabilized against enzymatic degradation in vivo, promises to have a high impact on the clinical management of patients with CCK2R expressing tumors in the near future.

Keywords: Cholecystokinin-2 receptor, molecular imaging, targeted radiotherapy, gastrin, cholecystokinin, radiometals.

« Previous
[1]
van der Meel, R.; Gallagher, W.M.; Oliveira, S.; O’Connor, A.E.; Schiffelers, R.M.; Byrne, A.T. Recent advances in molecular imaging biomarkers in cancer: application of bench to bedside technologies. Drug Discov. Today, 2010, 15(3-4), 102-114.
[http://dx.doi.org/10.1016/j.drudis.2009.12.003] [PMID: 20035896]
[2]
Moody, T.W.; Ramos-Alvarez, I.; Jensen, R.T. Neuropeptide G protein-coupled receptors as oncotargets. Front. Endocrinol. (Lausanne), 2018, 9, 345.
[http://dx.doi.org/10.3389/fendo.2018.00345] [PMID: 30008698]
[3]
Karpuz, M.; Silindir-Gunay, M.; Ozer, A.Y. Current and future approaches for effective cancer imaging and treatment. Cancer Biother. Radiopharm., 2018, 33(2), 39-51.
[http://dx.doi.org/10.1089/cbr.2017.2378] [PMID: 29634415]
[4]
Reubi, J.C.; Waser, B. Concomitant expression of several peptide receptors in neuroendocrine tumours: molecular basis for in vivo multireceptor tumour targeting. Eur. J. Nucl. Med. Mol. Imaging, 2003, 30(5), 781-793.
[http://dx.doi.org/10.1007/s00259-003-1184-3] [PMID: 12707737]
[5]
Fani, M.; Peitl, P.K.; Velikyan, I. Current status of radiopharmaceuticals for the theranostics of neuroendocrine neoplasms. Pharmaceuticals (Basel), 2017, 10(1), 1-22.
[http://dx.doi.org/10.3390/ph10010030] [PMID: 28295000]
[6]
Fani, M.; Braun, F.; Waser, B.; Beetschen, K.; Cescato, R.; Erchegyi, J.; Rivier, J.E.; Weber, W.A.; Maecke, H.R.; Reubi, J.C. Unex-pected sensitivity of sst2 antagonists to N-terminal radiometal modifications. J. Nucl. Med., 2012, 53(9), 1481-1489.
[http://dx.doi.org/10.2967/jnumed.112.102764] [PMID: 22851637]
[7]
Dash, A.; Chakraborty, S.; Pillai, M.R.A.; Knapp, F.F. Jr. Peptide receptor radionuclide therapy: an overview. Cancer Biother. Radiopharm., 2015, 30(2), 47-71.
[http://dx.doi.org/10.1089/cbr.2014.1741] [PMID: 25710506]
[8]
Nicolas, G.P.; Morgenstern, A.; Schottelius, M.; Fani, M. New developments in peptide receptor radionuclide therapy. J. Nucl. Med., 2018, 60(2), 167-171.
[http://dx.doi.org/10.2967/jnumed.118.213496] [PMID: 30573642]
[9]
Krenning, E.P.; Bakker, W.H.; Breeman, W.A.; Koper, J.W.; Kooij, P.P.; Ausema, L.; Lameris, J.S.; Reubi, J.C.; Lamberts, S.W. Localisation of endocrine-related tumours with radioiodinated analogue of somatostatin. Lancet, 1989, 1(8632), 242-244.
[http://dx.doi.org/10.1016/S0140-6736(89)91258-0] [PMID: 2563413]
[10]
Lamberts, S.W.J.; Reubi, J.C.; Krenning, E.P. Validation of somatostatin receptor scintigraphy in the localization of neuroendocrine tumors. Acta Oncol., 1993, 32(2), 167-170.
[http://dx.doi.org/10.3109/02841869309083907] [PMID: 8391830]
[11]
Fani, M.; Maecke, H.R. Radiopharmaceutical development of radiolabelled peptides. Eur. J. Nucl. Med. Mol. Imaging, 2012, 39(Suppl. 1), S11-S30.
[http://dx.doi.org/10.1007/s00259-011-2001-z] [PMID: 22388624]
[12]
Turner, J.H. An introduction to the clinical practice of theranostics in oncology. Br. J. Radiol., 2018, 91(1091)20180440
[http://dx.doi.org/10.1259/bjr.20180440] [PMID: 30179054]
[13]
Kjaer, A.; Knigge, U. Use of radioactive substances in diagnosis and treatment of neuroendocrine tumors. Scand. J. Gastroenterol., 2015, 50(6), 740-747.
[http://dx.doi.org/10.3109/00365521.2015.1033454] [PMID: 25959100]
[14]
Gabriel, M.; Decristoforo, C.; Kendler, D.; Dobrozemsky, G.; Heute, D.; Uprimny, C.; Kovacs, P.; Von Guggenberg, E.; Bale, R.; Virgolini, I.J. 68Ga-DOTA-Tyr3-octreotide PET in neuroendocrine tumors: comparison with somatostatin receptor scintigraphy and CT. J. Nucl. Med., 2007, 48(4), 508-518.
[http://dx.doi.org/10.2967/jnumed.106.035667] [PMID: 17401086]
[15]
Strosberg, J.; El-Haddad, G.; Wolin, E.; Hendifar, A.; Yao, J.; Chasen, B.; Mittra, E.; Kunz, P.L.; Kulke, M.H.; Jacene, H.; Bushnell, D.; O’Dorisio, T.M.; Baum, R.P.; Kulkarni, H.R.; Caplin, M.; Lebtahi, R.; Hobday, T.; Delpassand, E.; Van Cutsem, E.; Benson, A.; Srirajaskanthan, R.; Pavel, M.; Mora, J.; Berlin, J.; Grande, E.; Reed, N.; Seregni, E.; Öberg, K.; Lopera Sierra, M.; Santoro, P.; Thevenet, T.; Erion, J.L.; Ruszniewski, P.; Kwekkeboom, D.; Krenning, E. NETTER-1 trial investigators. Phase 3 trial of 177Lu-DOTAPPtate for midgut neuroendocrine tumors. N. Engl. J. Med., 2017, 376(2), 125-135.
[http://dx.doi.org/10.1056/NEJMoa1607427] [PMID: 28076709]
[16]
Reubi, J.C. Targeting CCK receptors in human cancers. Curr. Top. Med. Chem., 2007, 7(12), 1239-1242.
[http://dx.doi.org/10.2174/156802607780960546] [PMID: 17584145]
[17]
Sanchez, C.; Escrieut, C.; Clerc, P.; Gigoux, V.; Waser, B.; Reubi, J.C.; Fourmy, D. Characterization of a novel five-transmembrane domain cholecystokinin-2 receptor splice variant identified in human tumors. Mol. Cell. Endocrinol., 2012, 349(2), 170-179.
[http://dx.doi.org/10.1016/j.mce.2011.10.010] [PMID: 22040601]
[18]
Reubi, J.C.; Schaer, J.C.; Waser, B. Cholecystokinin (CCK)-A and CCK-B/gastrin receptors in human tumors. Cancer Res., 1997, 57(7), 1377-1386.
[PMID: 9102227]
[19]
Liu, H.; Wang, X.; Yang, R.; Zeng, W.; Peng, D.; Li, J.; Wang, H. Recent development of nuclear molecular imaging in thyroid cancer. BioMed Res. Int., 2018, 20182149532
[http://dx.doi.org/10.1155/2018/2149532] [PMID: 29951528]
[20]
Ganeshan, D.; Paulson, E.; Duran, C.; Cabanillas, M.E.; Busaidy, N.L.; Charnsangavej, C. Current update on medullary thyroid carci-noma. AJR Am. J. Roentgenol., 2013, 201(6), W867-W876.
[http://dx.doi.org/10.2214/AJR.12.10370] [PMID: 24261394]
[21]
Viola, D.; Elisei, R. Management of medullary thyroid cancer. Endocrinol. Metab. Clin. North Am., 2019, 48(1), 285-301.
[http://dx.doi.org/10.1016/j.ecl.2018.11.006] [PMID: 30717909]
[22]
Machens, A.; Dralle, H. Biomarker-based risk stratification for previously untreated medullary thyroid cancer. J. Clin. Endocrinol. Metab., 2010, 95(6), 2655-2663.
[http://dx.doi.org/10.1210/jc.2009-2368] [PMID: 20339026]
[23]
Maia, A.L.; Wajner, S.M.; Vargas, C.V. Advances and controversies in the management of medullary thyroid carcinoma. Curr. Opin. Oncol., 2017, 29(1), 25-32.
[http://dx.doi.org/10.1097/CCO.0000000000000340] [PMID: 27792051]
[24]
Treglia, G.; Castaldi, P.; Villani, M.F.; Perotti, G.; de Waure, C.; Filice, A.; Ambrosini, V.; Cremonini, N.; Santimaria, M.; Versari, A.; Fanti, S.; Giordano, A.; Rufini, V. Comparison of 18F-DOPA, 18F-FDG and 68Ga-somatostatin analogue PET/CT in patients with recurrent medullary thyroid carcinoma. Eur. J. Nucl. Med. Mol. Imaging, 2012, 39(4), 569-580.
[http://dx.doi.org/10.1007/s00259-011-2031-6] [PMID: 22223169]
[25]
Magnan, R.; Masri, B.; Escrieut, C.; Foucaud, M.; Cordelier, P.; Fourmy, D. Regulation of membrane cholecystokinin-2 receptor by agonists enables classification of partial agonists as biased agonists. J. Biol. Chem., 2011, 286(8), 6707-6719.
[http://dx.doi.org/10.1074/jbc.M110.196048] [PMID: 21156802]
[26]
Rehfeld, J.F.; Friis-Hansen, L.; Goetze, J.P.; Hansen, T.V.O. The biology of cholecystokinin and gastrin peptides. Curr. Top. Med. Chem., 2007, 7(12), 1154-1165.
[http://dx.doi.org/10.2174/156802607780960483] [PMID: 17584137]
[27]
Smeets, R.L.; Fouraux, M.A.; van Emst-de Vries, S.E.; De Pont, J.J.; Willems, P.H. Protein kinase C-mediated inhibition of trans-membrane signalling through CCK(A) and CCK(B) receptors. Br. J. Pharmacol., 1998, 123(6), 1189-1197.
[http://dx.doi.org/10.1038/sj.bjp.0701713] [PMID: 9559904]
[28]
Dufresne, M.; Seva, C.; Fourmy, D. Cholecystokinin and gastrin receptors. Physiol. Rev., 2006, 86(3), 805-847.
[http://dx.doi.org/10.1152/physrev.00014.2005] [PMID: 16816139]
[29]
Noble, F.; Wank, S.A.; Crawley, J.N.; Bradwejn, J.; Seroogy, K.B.; Hamon, M.; Roques, B.P. International Union of Pharmacology. XXI. Structure, distribution and functions of cholecystokinin receptors. Pharmacol. Rev., 1999, 51(4), 745-781.
[PMID: 10581329]
[30]
Fani, M.; Maecke, H.R.; Okarvi, S.M. Radiolabeled peptides: valuable tools for the detection and treatment of cancer. Theranostics, 2012, 2(5), 481-501.
[http://dx.doi.org/10.7150/thno.4024] [PMID: 22737187]
[31]
Roosenburg, S.; Laverman, P.; van Delft, F.L.; Boerman, O.C. Radiolabeled CCK/gastrin peptides for imaging and therapy of CCK2 receptor-expressing tumors. Amino Acids, 2011, 41(5), 1049-1058.
[http://dx.doi.org/10.1007/s00726-010-0501-y] [PMID: 20198494]
[32]
Kaloudi, A.; Nock, B.A.; Krenning, E.P.; Maina, T.; De Jong, M. Radiolabeled gastrin/CCK analogs in tumor diagnosis: towards higher stability and improved tumor targeting. Q. J. Nucl. Med. Mol. Imaging, 2015, 59(3), 287-302.
[PMID: 26158215]
[33]
Aloj, L.; Panico, M.R.; Caracó, C.; Zannetti, A.; Del Vecchio, S.; Di Nuzzo, C.; Arra, C.; Morelli, G.; Tesauro, D.; De Luca, S.; Pedone, C.; Salvatore, M. Radiolabeling approaches for cholecystokinin B receptor imaging. Biopolymers, 2002, 66(6), 370-380.
[http://dx.doi.org/10.1002/bip.10347] [PMID: 12658724]
[34]
Behr, T.M.; Jenner, N.; Radetzky, S.; Béhe, M.; Gratz, S.; Yücekent, S.; Raue, F.; Becker, W. Targeting of cholecystokinin-B/gastrin receptors in vivo: preclinical and initial clinical evaluation of the diagnostic and therapeutic potential of radiolabelled gastrin. Eur. J. Nucl. Med., 1998, 25(4), 424-430.
[http://dx.doi.org/10.1007/s002590050241] [PMID: 9553173]
[35]
Behr, T.M.; Béhé, M.; Angerstein, C.; Gratz, S.; Mach, R.; Hagemann, L.; Jenner, N.; Stiehler, M.; Frank-Raue, K.; Raue, F.; Becker, W. Cholecystokinin-B/gastrin receptor binding peptides: preclinical development and evaluation of their diagnostic and therapeutic potential. Clin. Cancer Res., 1999, 5(Suppl. 10), 3124s-3138s.
[PMID: 10541353]
[36]
von Guggenberg, E.; Behe, M.; Behr, T.M.; Saurer, M.; Seppi, T.; Decristoforo, C. 99mTc-labeling and in vitro and in vivo evaluation of HYNIC- and (Nalpha-His)acetic acid-modified [D-Glu1]-minigastrin. Bioconjug. Chem., 2004, 15(4), 864-871.
[http://dx.doi.org/10.1021/bc0300807] [PMID: 15264875]
[37]
de Jong, M.; Bakker, W.H.; Bernard, B.F.; Valkema, R.; Kwekkeboom, D.J.; Reubi, J.C.; Srinivasan, A.; Schmidt, M.; Krenning, E.P. Preclinical and initial clinical evaluation of 111In-labeled nonsulfated CCK8 analog: a peptide for CCK-B receptor-targeted scintigraphy and radionuclide therapy. J. Nucl. Med., 1999, 40(12), 2081-2087.
[PMID: 10616889]
[38]
Laverman, P.; Roosenburg, S.; Gotthardt, M.; Park, J.; Oyen, W.J.G.; de Jong, M.; Hellmich, M.R.; Rutjes, F.P.J.T.; van Delft, F.L.; Boerman, O.C. Targeting of a CCK(2) receptor splice variant with (111)In-labelled cholecystokinin-8 (CCK8) and (111)In-labelled minigastrin. Eur. J. Nucl. Med. Mol. Imaging, 2008, 35(2), 386-392.
[http://dx.doi.org/10.1007/s00259-007-0604-1] [PMID: 17934729]
[39]
Laverman, P.; Béhé, M.; Oyen, W.J.G.; Willems, P.H.G.M.; Corstens, F.H.M.; Behr, T.M.; Boerman, O.C. Two technetium-99m-labeled cholecystokinin-8 (CCK8) peptides for scintigraphic imaging of CCK receptors. Bioconjug. Chem., 2004, 15(3), 561-568.
[http://dx.doi.org/10.1021/bc034208w] [PMID: 15149184]
[40]
Aloj, L.; Caracò, C.; Panico, M.; Zannetti, A.; Del Vecchio, S.; Tesauro, D.; De Luca, S.; Arra, C.; Pedone, C.; Morelli, G.; Salvatore, M. In vitro and in vivo evaluation of 111In-DTPAGlu-G-CCK8 for cholecystokinin-B receptor imaging. J. Nucl. Med., 2004, 45(3), 485-494.
[PMID: 15001692]
[41]
Aloj, L.; Aurilio, M.; Rinaldi, V.; D’ambrosio, L.; Tesauro, D.; Peitl, P.K.; Maina, T.; Mansi, R.; von Guggenberg, E.; Joosten, L.; Sosabowski, J.K.; Breeman, W.A.P.; De Blois, E.; Koelewijn, S.; Melis, M.; Waser, B.; Beetschen, K.; Reubi, J.C.; de Jong, M. Comparison of the binding and internalization properties of 12 DOTA-coupled and 111In-labelled CCK2/gastrin receptor binding pep-tides: a collaborative project under COST Action BM0607. Eur. J. Nucl. Med. Mol. Imaging, 2011, 38(8), 1417-1425.
[http://dx.doi.org/10.1007/s00259-011-1816-y] [PMID: 21523391]
[42]
Sauter, A.W.; Mansi, R.; Hassiepen, U.; Muller, L.; Panigada, T.; Wiehr, S.; Wild, A-M.; Geistlich, S.; Béhé, M.; Rottenburger, C.; Wild, D.; Fani, M. Targeting of the cholecystokinin-2 receptor with the minigastrin analog 177Lu-DOTAPP-PP-F11N: does the use of protease inhibitors further improve in vivo distribution? J. Nucl. Med., 2019, 60(3), 393-399.
[http://dx.doi.org/10.2967/jnumed.118.207845] [PMID: 30002107]
[43]
Behr, T.M.; Jenner, N.; Béhé, M.; Angerstein, C.; Gratz, S.; Raue, F.; Becker, W. Radiolabeled peptides for targeting cholecystokinin-B/gastrin receptor-expressing tumors. J. Nucl. Med., 1999, 40(6), 1029-1044.
[PMID: 10452322]
[44]
Béhé, M.; Becker, W.; Gotthardt, M.; Angerstein, C.; Behr, T.M. Improved kinetic stability of DTPA- dGlu as compared with con-ventional monofunctional DTPA in chelating indium and yttrium: preclinical and initial clinical evaluation of radiometal labelled minigastrin derivatives. Eur. J. Nucl. Med. Mol. Imaging, 2003, 30(8), 1140-1146.
[http://dx.doi.org/10.1007/s00259-003-1178-1] [PMID: 12768330]
[45]
Béhé, M.; Kluge, G.; Becker, W.; Gotthardt, M.; Behr, T.M. Use of polyglutamic acids to reduce uptake of radiometal-labeled minigastrin in the kidneys. J. Nucl. Med., 2005, 46(6), 1012-1015.
[PMID: 15937313]
[46]
Gotthardt, M.; van Eerd-Vismale, J.; Oyen, W.J.; de Jong, M.; Zhang, H.; Rolleman, E.; Maecke, H.R.; Béhé, M.; Boerman, O. Indi-cation for different mechanisms of kidney uptake of radiolabeled peptides. J. Nucl. Med., 2007, 48(4), 596-601.
[http://dx.doi.org/10.2967/jnumed.106.036020] [PMID: 17401097]
[47]
Good, S.; Walter, M.A.; Waser, B.; Wang, X.; Müller-Brand, J.; Béhé, M.P.; Reubi, J.C.; Maecke, H.R. Macrocyclic chelator-coupled gastrin-based radiopharmaceuticals for targeting of gastrin receptor-expressing tumours. Eur. J. Nucl. Med. Mol. Imaging, 2008, 35(10), 1868-1877.
[http://dx.doi.org/10.1007/s00259-008-0803-4] [PMID: 18509636]
[48]
Aloj, L.; Panico, M.; Caraco, C.; Del Vecchio, S.; Arra, C.; Affuso, A.; Accardo, A.; Mansi, R.; Tesauro, D.; De Luca, S.; Pedone, C.; Visentin, R.; Mazzi, U.; Morelli, G.; Salvatore, M. In vitro and in vivo characterization of Indium-111 and Technetium-99m labeled CCK-8 derivatives for CCK-B receptor imaging. Cancer Biother. Radiopharm., 2004, 19(1), 93-98.
[http://dx.doi.org/10.1089/108497804773391739] [PMID: 15068617]
[49]
von Guggenberg, E.; Dietrich, H.; Skvortsova, I.; Gabriel, M.; Virgolini, I.J.; Decristoforo, C. 99mTc-labelled HYNIC-minigastrin with reduced kidney uptake for targeting of CCK-2 receptor-positive tumours. Eur. J. Nucl. Med. Mol. Imaging, 2007, 34(8), 1209-1218.
[http://dx.doi.org/10.1007/s00259-006-0348-3] [PMID: 17308920]
[50]
D’Andrea, L.D.; Testa, I.; Panico, M.; Di Stasi, R.; Caracò, C.; Tarallo, L.; Arra, C.; Barbieri, A.; Romanelli, A.; Aloj, L. In vivo and in vitro characterization of CCK8 bearing a histidine-based chelator labeled with 99mTc-tricarbonyl. Biopolymers, 2008, 90(5), 707-712.
[http://dx.doi.org/10.1002/bip.21041] [PMID: 18615495]
[51]
Kaloudi, A.; Nock, B.A.; Lymperis, E.; Krenning, E.P.; de Jong, M.; Maina, T. (99m)Tc-labeled gastrins of varying peptide chain length: Distinct impact of NEP/ACE-inhibition on stability and tumor uptake in mice. Nucl. Med. Biol., 2016, 43(6), 347-354.
[http://dx.doi.org/10.1016/j.nucmedbio.2016.03.003] [PMID: 27260775]
[52]
Nock, B.A.; Maina, T.; Béhé, M.; Nikolopoulou, A.; Gotthardt, M.; Schmitt, J.S.; Behr, T.M.; Mäcke, H.R. CCK-2/gastrin receptor-targeted tumor imaging with (99m)Tc-labeled minigastrin analogs. J. Nucl. Med., 2005, 46(10), 1727-1736.
[PMID: 16204724]
[53]
Sosabowski, J.K.; Matzow, T.; Foster, J.M.; Finucane, C.; Ellison, D.; Watson, S.A.; Mather, S.J. Targeting of CCK-2 receptor-expressing tumors using a radiolabeled divalent gastrin peptide. J. Nucl. Med., 2009, 50(12), 2082-2089.
[http://dx.doi.org/10.2967/jnumed.109.064808] [PMID: 19910426]
[54]
Summer, D.; Kroess, A.; Woerndle, R.; Rangger, C.; Klingler, M.; Haas, H.; Kremser, L.; Lindner, H.H.; von Guggenberg, E.; De-cristoforo, C. Multimerization results in formation of re-bindable metabolites: a proof of concept study with FSC-based minigastrin imaging probes targeting CCK2R expression. PLoS One, 2018, 13(7)e0201224
[http://dx.doi.org/10.1371/journal.pone.0201224] [PMID: 30059514]
[55]
Summer, D.; Rangger, C.; Klingler, M.; Laverman, P.; Franssen, G.M.; Lechner, B.E.; Orasch, T.; Haas, H.; von Guggenberg, E.; Decristoforo, C. Exploiting the concept of multivalency with 68Ga- and 89Zr-labelled fusarinine C-minigastrin bioconjugates for targeting CCK2R expression. Contrast Media Mol. Imaging, 2018, 20183171794
[http://dx.doi.org/10.1155/2018/3171794] [PMID: 29849512]
[56]
von Guggenberg, E.; Sallegger, W.; Helbok, A.; Ocak, M.; King, R.; Mather, S.J.; Decristoforo, C. Cyclic minigastrin analogues for gastrin receptor scintigraphy with technetium-99m: preclinical evaluation. J. Med. Chem., 2009, 52(15), 4786-4793.
[http://dx.doi.org/10.1021/jm900400w] [PMID: 19591486]
[57]
von Guggenberg, E.; Rangger, C.; Sosabowski, J.; Laverman, P.; Reubi, J.C.; Virgolini, I.J.; Decristoforo, C. Preclinical evaluation of radiolabeled DOTA-derivatized cyclic minigastrin analogs for targeting cholecystokinin receptor expressing malignancies. Mol. Imaging Biol., 2012, 14(3), 366-375.
[http://dx.doi.org/10.1007/s11307-011-0506-2] [PMID: 21732165]
[58]
Kolenc-Peitl, P.; Mansi, R.; Tamma, M.; Gmeiner-Stopar, T.; Sollner-Dolenc, M.; Waser, B.; Baum, R.P.; Reubi, J.C.; Maecke, H.R. Highly improved metabolic stability and pharmacokinetics of indium-111-DOTA-gastrin conjugates for targeting of the gastrin receptor. J. Med. Chem., 2011, 54(8), 2602-2609.
[http://dx.doi.org/10.1021/jm101279a] [PMID: 21456601]
[59]
Ocak, M.; Helbok, A.; Rangger, C.; Peitl, P.K.; Nock, B.A.; Morelli, G.; Eek, A.; Sosabowski, J.K.; Breeman, W.A.P.; Reubi, J.C.; Decristoforo, C. Comparison of biological stability and metabolism of CCK2 receptor targeting peptides, a collaborative project under COST BM0607. Eur. J. Nucl. Med. Mol. Imaging, 2011, 38(8), 1426-1435.
[http://dx.doi.org/10.1007/s00259-011-1818-9] [PMID: 21528387]
[60]
Laverman, P.; Joosten, L.; Eek, A.; Roosenburg, S.; Peitl, P.K.; Maina, T.; Mäcke, H.; Aloj, L.; von Guggenberg, E.; Sosabowski, J.K.; de Jong, M.; Reubi, J.C.; Oyen, W.J.G.; Boerman, O.C. Comparative biodistribution of 12 111In-labelled gastrin/CCK2 receptor-targeting peptides. Eur. J. Nucl. Med. Mol. Imaging, 2011, 38(8), 1410-1416.
[http://dx.doi.org/10.1007/s00259-011-1806-0] [PMID: 21461732]
[61]
Mather, S.J.; McKenzie, A.J.; Sosabowski, J.K.; Morris, T.M.; Ellison, D.; Watson, S.A. Selection of radiolabeled gastrin analogs for peptide receptor-targeted radionuclide therapy. J. Nucl. Med., 2007, 48(4), 615-622.
[http://dx.doi.org/10.2967/jnumed.106.037085] [PMID: 17401100]
[62]
Roosenburg, S.; Laverman, P.; Joosten, L.; Eek, A.; Oyen, W.J.G.; de Jong, M.; Rutjes, F.P.J.T.; van Delft, F.L.; Boerman, O.C. Sta-bilized (111)in-labeled sCCK8 analogues for targeting CCK2-receptor positive tumors: synthesis and evaluation. Bioconjug. Chem., 2010, 21(4), 663-670.
[http://dx.doi.org/10.1021/bc900465y] [PMID: 20302291]
[63]
Roosenburg, S.; Laverman, P.; Joosten, L.; Eek, A.; Rutjes, F.P.J.T.; van Delft, F.L.; Boerman, O.C. In vitro and in vivo characterization of three 68Ga- and 111In-labeled peptides for cholecystokinin receptor imaging. Mol. Imaging, 2012, 11(5), 401-407.
[http://dx.doi.org/10.2310/7290.2012.00001] [PMID: 22954184]
[64]
Grob, N.M.; Behe, M.; von Guggenberg, E.; Schibli, R.; Mindt, T.L. Methoxinine - an alternative stable amino acid substitute for oxidation-sensitive methionine in radiolabelled peptide conjugates. J. Pept. Sci., 2017, 23(1), 38-44.
[http://dx.doi.org/10.1002/psc.2948] [PMID: 28054429]
[65]
Helbok, A.; Decristoforo, C.; Behe, M.; Rangger, C.; Guggenberg, E. Preclinical evaluation of In-111 and Ga-68 labelled minigastrin analogues for CCK-2 receptor imaging. Curr. Radiopharm., 2009, 2(4), 304-310.
[http://dx.doi.org/10.2174/1874471010902040304]
[66]
Pawlak, D.; Rangger, C.; Kolenc Peitl, P.; Garnuszek, P.; Maurin, M.; Ihli, L.; Kroselj, M.; Maina, T.; Maecke, H.; Erba, P.; Kremser, L.; Hubalewska-Dydejczyk, A.; Mikołajczak, R.; Decristoforo, C. From preclinical development to clinical application: kit formulation for radiolabelling the minigastrin analogue CP04 with In-111 for a first-in-human clinical trial. Eur. J. Pharm. Sci., 2016, 85, 1-9.
[http://dx.doi.org/10.1016/j.ejps.2016.01.023] [PMID: 26826279]
[67]
Maina, T.; Konijnenberg, M.W. KolencPeitl, P.; Garnuszek, P.; Nock, B.A.; Kaloudi, A.; Kroselj, M.; Zaletel, K.; Maecke, H.; Mansi, R.; Erba, P.; von Guggenberg, E.; Hubalewska-Dydejczyk, A.; Mikolajczak, R.; Decristoforo, C. Preclinical pharmacokinetics, bi-odistribution, radiation dosimetry and toxicity studies required for regulatory approval of a phase I clinical trial with (111)In-CP04 in medullary thyroid carcinoma patients. Eur. J. Pharm. Sci., 2016, 91, 236-242.
[http://dx.doi.org/10.1016/j.ejps.2016.05.011] [PMID: 27185299]
[68]
Kolenc Peitl, P.; Tamma, M.; Kroselj, M.; Braun, F.; Waser, B.; Reubi, J.C.; Sollner Dolenc, M.; Maecke, H.R.; Mansi, R. Stereo-chemistry of amino acid spacers determines the pharmacokinetics of (111)In-DOTA-minigastrin analogues for targeting the CCK2/gastrin receptor. Bioconjug. Chem., 2015, 26(6), 1113-1119.
[http://dx.doi.org/10.1021/acs.bioconjchem.5b00187] [PMID: 25971921]
[69]
Konijnenberg, M.W.; Breeman, W.A.P.; de Blois, E.; Chan, H.S.; Boerman, O.C.; Laverman, P.; Kolenc-Peitl, P.; Melis, M.; de Jong, M. Therapeutic application of CCK2R-targeting PP-F11: influence of particle range, activity and peptide amount. EJNMMI Res., 2014, 4(1), 47.
[http://dx.doi.org/10.1186/s13550-014-0047-1] [PMID: 26116111]
[70]
Rangger, C.; Klingler, M.; Balogh, L.; Pöstényi, Z.; Polyak, A.; Pawlak, D.; Mikołajczak, R.; von Guggenberg, E. 177Lu labeled cyclic minigastrin analogues with therapeutic activity in CCK2R expressing tumors: preclinical evaluation of a kit formulation. Mol. Pharm., 2017, 14(9), 3045-3058.
[http://dx.doi.org/10.1021/acs.molpharmaceut.7b00241] [PMID: 28728415]
[71]
Melis, M.; Vegt, E.; Konijnenberg, M.W.; de Visser, M.; Bijster, M.; Vermeij, M.; Krenning, E.P.; Boerman, O.C.; de Jong, M. Ne-phrotoxicity in mice after repeated imaging using 111In-labeled peptides. J. Nucl. Med., 2010, 51(6), 973-977.
[http://dx.doi.org/10.2967/jnumed.109.074310] [PMID: 20484435]
[72]
Roosenburg, S.; Laverman, P.; Joosten, L.; Cooper, M.S.; Kolenc-Peitl, P.K.; Foster, J.M.; Hudson, C.; Leyton, J.; Burnet, J.; Oyen, W.J.G.; Blower, P.J.; Mather, S.J.; Boerman, O.C.; Sosabowski, J.K. PET and SPECT imaging of a radiolabeled minigastrin analogue conjugated with DOTA, NOTA, and NODAGA and labeled with (64)Cu, (68)Ga, and (111). Mol. Pharm., 2014, 11(11), 3930-3937.
[http://dx.doi.org/10.1021/mp500283k] [PMID: 24992368]
[73]
Maurin, M.; Garnuszek, P.; Baran, P.; Pawlak, D.; Mikołajczak, R. The radiometal makes a difference. Synthesis and preliminary characterisation of DOTA-minigastrin analogue complexes with Ga, Lu and Y. Nucl. Med. Rev. Cent. East. Eur., 2015, 18(2), 51-55.
[http://dx.doi.org/10.5603/NMR.2015.0014] [PMID: 26315862]
[74]
Breeman, W.A.P.; Fröberg, A.C.; de Blois, E.; van Gameren, A.; Melis, M.; de Jong, M.; Maina, T.; Nock, B.A.; Erion, J.L.; Mäcke, H.R.; Krenning, E.P. Optimised labeling, preclinical and initial clinical aspects of CCK-2 receptor-targeting with 3 radiolabeled peptides. Nucl. Med. Biol., 2008, 35(8), 839-849.
[http://dx.doi.org/10.1016/j.nucmedbio.2008.09.006] [PMID: 19026945]
[75]
Behr, T.M.; Béhé, M.; Becker, W. Diagnostic applications of radiolabeled peptides in nuclear endocrinology. Q. J. Nucl. Med., 1999, 43(3), 268-280.
[PMID: 10568142]
[76]
Kwekkeboom, D.J.; Bakker, W.H.; Kooij, P.P.M.; Erion, J.; Srinivasan, A.; de Jong, M.; Reubi, J.C.; Krenning, E.P. Cholecystokinin receptor imaging using an octapeptide DTPA-CCK analogue in patients with medullary thyroid carcinoma. Eur. J. Nucl. Med., 2000, 27(9), 1312-1317.
[http://dx.doi.org/10.1007/s002590000296] [PMID: 11007512]
[77]
Béhé, M.; Behr, T.M. Cholecystokinin-B (CCK-B)/gastrin receptor targeting peptides for staging and therapy of medullary thyroid cancer and other CCK-B receptor expressing malignancies. Biopolymers, 2002, 66(6), 399-418.
[http://dx.doi.org/10.1002/bip.10356] [PMID: 12658727]
[78]
Behr, T.M.; Béhé, M.P. Cholecystokinin-B/Gastrin receptor-targeting peptides for staging and therapy of medullary thyroid cancer and other cholecystokinin-B receptor-expressing malignancies. Semin. Nucl. Med., 2002, 32(2), 97-109.
[http://dx.doi.org/10.1053/snuc.2002.31028] [PMID: 11965605]
[79]
Gotthardt, M.; Béhé, M.P.; Beuter, D.; Battmann, A.; Bauhofer, A.; Schurrat, T.; Schipper, M.; Pollum, H.; Oyen, W.J.G.; Behr, T.M. Improved tumour detection by gastrin receptor scintigraphy in patients with metastasised medullary thyroid carcinoma. Eur. J. Nucl. Med. Mol. Imaging, 2006, 33(11), 1273-1279.
[http://dx.doi.org/10.1007/s00259-006-0157-8] [PMID: 16832634]
[80]
Gotthardt, M.; Béhé, M.P.; Grass, J.; Bauhofer, A.; Rinke, A.; Schipper, M.L.; Kalinowski, M.; Arnold, R.; Oyen, W.J.G.; Behr, T.M. Added value of gastrin receptor scintigraphy in comparison to somatostatin receptor scintigraphy in patients with carcinoids and other neuroendocrine tumours. Endocr. Relat. Cancer, 2006, 13(4), 1203-1211.
[http://dx.doi.org/10.1677/erc.1.01245] [PMID: 17158765]
[81]
Behr, T.; Behe, M.; Gotthardt, M.; Angerstein, C.; Heufelder, C.; Becker, W. Cholecystokinin(CCK(-B)/Gastrin-Receptor bining peptides for diagnosis and therapy of metastatic medullary thyroid cancer. Eur. J. Nucl. Med., 2001, 28(8), 1023.
[82]
Fröberg, A.C.; de Jong, M.; Nock, B.A.; Breeman, W.A.P.; Erion, J.L.; Maina, T.; Verdijsseldonck, M.; de Herder, W.W.; van der Lugt, A.; Kooij, P.P.M.; Krenning, E.P. Comparison of three radiolabelled peptide analogues for CCK-2 receptor scintigraphy in me-dullary thyroid carcinoma. Eur. J. Nucl. Med. Mol. Imaging, 2009, 36(8), 1265-1272.
[http://dx.doi.org/10.1007/s00259-009-1098-9] [PMID: 19266197]
[83]
Kosowicz, J.; Czepczyński, R.; Ziemnicka, K.; Gryczyńska, M.; Sowiński, J. The use of a new analogue DGlu-Octagastrin in scintig-raphy of medullary thyroid carcinoma Endokrynol. Pol., 2006, 57(4), 427-430.
[PMID: 17006848]
[84]
Kosowicz, J.; Mikołajczak, R.; Czepczyński, R.; Ziemnicka, K.; Gryczyńska, M.; Sowiński, J. Two peptide receptor ligands (99m)Tc-EDDA/HYNIC-Tyr(3)-octreotide and (99m)Tc-EDDA/HYNIC-(D)Glu-octagastrin for scintigraphy of medullary thyroid carcinoma. Cancer Biother. Radiopharm., 2007, 22(5), 613-628.
[http://dx.doi.org/10.1089/cbr.2006.368] [PMID: 17979564]
[85]
Kunikowska, J.; Ziemnicka, K.; Pawlak, D.; Ruchała, M.; Kolasa, A.; Janicka-Jedyńska, M.; Woźniak, A.; Mikołajczak, R.; Królicki, L. Medullary thyroid carcinoma - PET/CT imaging with 68Ga-labelled gastrin and somatostatin analogues. Endokrynol. Pol., 2016, 67(1), 68-71.
[http://dx.doi.org/10.5603/EP.2016.0010] [PMID: 26884118]
[86]
Hubalewska-Dydejczyk, A.; Mikolajczak, R.; Decristoforo, C.; Kolenc-Peitl, P.; Erba, P.A.; Zaletel, K.; Maecke, H.; Maina, T.; Konijnenberg, M.; Garnuszek, P.; Trofimiuk-Müldner, M.; Przybylik-Mazurek, E.; Virgolini, I.; de Jong, M.; Froberg, A.C.; Rangger, C.; Goebel, G.; Scarpa, L.; Glowa, B.; Skórkiewicz, K.; Lezaic, L.; Solnica, B.; Fedak, D.; Gawęda, P.; Sowa-Staszczak, A.; Nock, B.A.; Bergant, D.; Rep, S.; Lenda-Tracz, V.; Phase, I. Clinical trial using a novel CCK2 receptor-localizing radiolabelled peptide probe for personalized diagnosis and therapy of patients with progressive or metastatic medullary thyroid carcinoma - final results. Eur. J. Nucl. Med. Mol. Imaging, 2019, 46(Suppl. 1), S339.
[87]
Rottenburger, C.; Nicolas, G.P.; McDougall, L.; Kaul, F.; Cachovan, M.; Vija, A.H.; Schibli, R.; Geistlich, S.; Schumann, A.; Rau, T.; Glatz, K.; Behe, M.; Christ, E.R.; Wild, D. Cholecystokinin-2 receptor agonist 177Lu-PP-F11N for radionuclide therapy of medullary thyroid carcinoma - results of the lumed phase 0a study. J. Nucl. Med., 2019.
[http://dx.doi.org/10.2967/jnumed.119.233031 ] [PMID: 31519804]
[88]
Erba, P.A.; Maecke, H.; Mikolajczak, R.; Decristoforo, C.; Zaletel, K.; Maina-Nock, T.; Peitl, P.K.; Garnuszek, P.; Froberg, A.; Goebel, G.; de Jong, M.; Jabrocka-Hybel, A.; Konijnenberg, M.; Virgolini, I.; Nock, B.; Lenda-Tracz, W.; Pawlak, D.; Rangger, C.; Trofimiuk-Müldner, M.; Sowa-Staszczak, A.; Tomaszuk, M.; von Guggenberg, E.; Scarpa, L.; Hubalewska-Dydejczyk, A. A novel CCK2/gastrin receptor-localizing radiolabeled peptide probe for personalized diagnosis and therapy of patients with progressive or metastatic medullary thyroid carcinoma: a multicenter phase I GRAN-T-MTC study. Polish Arch. Intern. Med., 2018, 128(12), 791-795.
[http://dx.doi.org/10.20452/pamw.4387] [PMID: 30516761]
[89]
Bozkurt, M.F.; Virgolini, I.; Balogova, S.; Beheshti, M.; Rubello, D.; Decristoforo, C.; Ambrosini, V.; Kjaer, A.; Delgado-Bolton, R.; Kunikowska, J.; Oyen, W.J.G.; Chiti, A.; Giammarile, F.; Sundin, A.; Fanti, S. Guideline for PET/CT imaging of neuroendocrine ne-oplasms with 68Ga-DOTA-conjugated somatostatin receptor targeting peptides and 18F-DOPA. Eur. J. Nucl. Med. Mol. Imaging, 2017, 44(9), 1588-1601.
[http://dx.doi.org/10.1007/s00259-017-3728-y] [PMID: 28547177]
[90]
Wild, D.; Fani, M.; Fischer, R.; Del Pozzo, L.; Kaul, F.; Krebs, S.; Fischer, R.; Rivier, J.E.F.; Reubi, J.C.; Maecke, H.R.; Weber, W.A. Comparison of somatostatin receptor agonist and antagonist for peptide receptor radionuclide therapy: a pilot study. J. Nucl. Med., 2014, 55(8), 1248-1252.
[http://dx.doi.org/10.2967/jnumed.114.138834] [PMID: 24963127]
[91]
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]
[92]
Pauwels, E.; Cleeren, F.; Bormans, G.; Deroose, C.M. Somatostatin receptor PET ligands - the next generation for clinical practice. Am. J. Nucl. Med. Mol. Imaging, 2018, 8(5), 311-331.
[PMID: 30510849]
[93]
Bison, S.M.; Konijnenberg, M.W.; Melis, M.; Pool, S.E.; Bernsen, M.R.; Teunissen, J.J.M.; Kwekkeboom, D.J.; de Jong, M. Peptide receptor radionuclide therapy using radiolabeled somatostatin analogs: focus on future developments. Clin. Transl. Imaging, 2014, 2(1), 55-66.
[http://dx.doi.org/10.1007/s40336-014-0054-2] [PMID: 24765618]
[94]
Fani, M.; Nicolas, G.P.; Wild, D. Somatostatin receptor antagonists for imaging and therapy. J. Nucl. Med., 2017, 58(Suppl. 2), 61S-66S.
[http://dx.doi.org/10.2967/jnumed.116.186783] [PMID: 28864614]
[95]
Akgün, E.; Körner, M.; Gao, F.; Harikumar, K.G.; Waser, B.; Reubi, J.C.; Portoghese, P.S.; Miller, L.J. Synthesis and in vitro charac-terization of radioiodinatable benzodiazepines selective for type 1 and type 2 cholecystokinin receptors. J. Med. Chem., 2009, 52(7), 2138-2147.
[http://dx.doi.org/10.1021/jm801439x] [PMID: 19271701]
[96]
Wayua, C.; Low, P.S. Evaluation of a nonpeptidic ligand for imaging of cholecystokinin 2 receptor-expressing cancers. J. Nucl. Med., 2015, 56(1), 113-119.
[http://dx.doi.org/10.2967/jnumed.114.144998] [PMID: 25500824]
[97]
Nock, B.A.; Maina, T.; Krenning, E.P.; de Jong, M. “To serve and protect”: enzyme inhibitors as radiopeptide escorts promote tumor targeting. J. Nucl. Med., 2014, 55(1), 121-127.
[http://dx.doi.org/10.2967/jnumed.113.129411] [PMID: 24287321]
[98]
Dubreuil, P.; Fulcrand, P.; Rodriguez, M.; Fulcrand, H.; Laur, J.; Martinez, J. Novel activity of angiotensin-converting enzyme. Hy-drolysis of cholecystokinin and gastrin analogues with release of the amidated C-terminal dipeptide. Biochem. J., 1989, 262(1), 125-130.
[http://dx.doi.org/10.1042/bj2620125] [PMID: 2554881]
[99]
Migaud, M.; Durieux, C.; Viereck, J.; Soroca-Lucas, E.; Fournié-Zaluski, M.C.; Roques, B.P. The in vivo metabolism of cholecysto-kinin (CCK-8) is essentially ensured by aminopeptidase A. Peptides, 1996, 17(4), 601-607.
[http://dx.doi.org/10.1016/0196-9781(96)00036-8] [PMID: 8804068]
[100]
Kaloudi, A.; Nock, B.A.; Lymperis, E.; Krenning, E.P.; de Jong, M.; Maina, T. Improving the in vivo profile of minigastrin radiotracers: a comparative study involving the neutral endopeptidase inhibitor phosphoramidon. Cancer Biother. Radiopharm., 2016, 31(1), 20-28.
[http://dx.doi.org/10.1089/cbr.2015.1935] [PMID: 26844849]
[101]
Kaloudi, A.; Nock, B.A.; Lymperis, E.; Valkema, R.; Krenning, E.P.; de Jong, M.; Maina, T. Impact of clinically tested NEP/ACE inhibitors on tumor uptake of [111In-DOTA]MG11-first estimates for clinical translation. EJNMMI Res., 2016, 6(1), 15.
[http://dx.doi.org/10.1186/s13550-015-0158-3] [PMID: 26882895]
[102]
Valverde, I.E.; Bauman, A.; Kluba, C.A.; Vomstein, S.; Walter, M.A.; Mindt, T.L. 1,2,3-Triazoles as amide bond mimics: triazole scan yields protease-resistant peptidomimetics for tumor targeting. Angew. Chem. Int. Ed. Engl., 2013, 52(34), 8957-8960.
[http://dx.doi.org/10.1002/anie.201303108] [PMID: 23832715]
[103]
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]
[104]
Grob, N.; Béhé, M.; Schibli, R.; Mindt, T.P.C. #50 -177Lu-labelled peptidomimetics: novel minigastrin analogues for improved tumour targeting. Nucl. Med. Biol., 2019, 72-73, S20.
[http://dx.doi.org/10.1016/S0969-8051(19)30243-4]
[105]
Corringer, P.J.; Weng, J.H.; Ducos, B.; Durieux, C.; Boudeau, P.; Bohme, A.; Roques, B.P. CCK-B agonist or antagonist activities of structurally hindered and peptidase-resistant Boc-CCK4 derivatives. J. Med. Chem., 1993, 36(1), 166-172.
[http://dx.doi.org/10.1021/jm00053a022] [PMID: 8421283]
[106]
Klingler, M.; Decristoforo, C.; Rangger, C.; Summer, D.; Foster, J.; Sosabowski, J.K.; von Guggenberg, E. Site-specific stabilization of minigastrin analogs against enzymatic degradation for enhanced cholecystokinin-2 receptor targeting. Theranostics, 2018, 8(11), 2896-2908.
[http://dx.doi.org/10.7150/thno.24378] [PMID: 29896292]
[107]
Klingler, M.; Summer, D.; Rangger, C.; Haubner, R.; Foster, J.; Sosabowski, J.; Decristoforo, C.; Virgolini, I.; von Guggenberg, E. DOTA-MGS5, a new cholecystokinin-2 receptor-targeting peptide analog with an optimized targeting profile for theranostic use. J. Nucl. Med., 2019, 60(7), 1010-1016.
[http://dx.doi.org/10.2967/jnumed.118.221283] [PMID: 30530828]
[108]
Klingler, M.; Rangger, C.; Summer, D.; Kaeopookum, P.; Decristoforo, C.; von Guggenberg, E. Cholecystokinin-2 receptor targeting with novel C-terminally stabilized HYNIC-minigastrin analogs radiolabeled with technetium-99m. Pharmaceuticals (Basel), 2019, 12(1)E13
[http://dx.doi.org/10.3390/ph12010013] [PMID: 30650563]
[109]
von Guggenberg, E.; Klingler, M.; Garnuszek, P.; Mikolajczak, R.; Janota, B.; Hubalewska-Dydejczyk, A.; Kiec-Klimczak, M.; Przybylik-Mazurek, E.; Virgolini, I. Gallium-68 labelled minigastrin analogue for high sensitivity PET imaging of cholecystokinin-2 receptor expressing tumours, Proceedings of annual congress of the European Association of Nuclear MedicineOctober 12-16Barcelona, Spain 2019, S268

Rights & Permissions Print Cite
Article Metrics
19
© 2024 Bentham Science Publishers | Privacy Policy